The chain of infection transmission in the home and

The chain of infection transmission in the home and

The chain of infection transmission in the home and
everyday life settings, and the role of hygiene in
reducing the risk of infection
July 2012
Professor Sally F. Bloomfield1, Professor Martin Exner2, Professor Carlo Signorelli3,
Professor Kumar Jyoti Nath4, Dr Elizabeth A Scott5,
1
Honorary Professor, London School of Hygiene and Tropical Medicine, London, UK.
Direktor, Hygiene-Institut, Rheinische Friedrich-Wilhelms-Universität, Bonn, Germany.
3
Direttore Scuola di Specalizzazione in Igiene e medicina preventive. Department of Public
Health, University of Parma, Italy.
4
Chairman, Sulabh International Social Service Organization, Calcutta, India.
5
Assistant Professor in the Department of Biology, Director Of Undergraduate Program in
Public Health, Co-director Simmons Center for Hygiene and Health in Home and
Community, Simmons College, Boston, MA USA.
2
1
This review was drafted by IFH Chairman and Scientific Advisory Board Member Professor
Sally F Bloomfield. It was then submitted to the other members of the IFH Scientific Advisory
Board to discuss and develop the review and agree on final content.
We would like to thank Dr Jon Otter, Dr Stephanie Dancer, Dr Ben Tanner and Dr Cristobel
Chaidez and Professor Joan Rose for valuable comments and contributions to this review
Other data, more recently published, on the chain of infection transmission in the domestic
home and everyday life settings, and the role of hygiene in reducing the risk of infection can
be found in the IFH Library of Recent Publications, Topic 2 Infection transmission. This
library is updated every 6 months with new publications related to home hygiene. These
papers can be found at:
http://www.ifhhomehygiene.org/IntegratedCRD.nsf/IFH_Topic_Infection_Transmission?OpenForm
Details for citation of the paper: Bloomfield SF, Exner M, Carlo Signorelli C, Nath KJ, Scott
EA. (2012) The chain of infection transmission in the home and everyday life settings, and
the role of hygiene in reducing the risk of infection. http://www.ifhhomehygiene.org/IntegratedCRD.nsf/111e68ea0824afe1802575070003f039/9df1597d9058
89868025729700617093?OpenDocument
Copyright © International Scientific Forum on Home Hygiene, 2012
2
CONTENTS
SECTION 1. INTRODUCTION – AIMS AND OBJECTIVES OF THE REVIEW
6
SECTION 2. INTRODUCTION – THE IFH TARGETED APPROACH TO HOME HYGIENE
8
2.1 A RISK-BASED APPROACH TO HOME AND EVERYDAY LIFE HYGIENE – BASIC PRINCIPLES
2.2. DEVELOPING THE IFH TARGETED APPROACH TO HOME HYGIENE
8
11
SECTION 3. ASSESSMENT OF THE CAUSAL LINK BETWEEN HYGIENE PRACTICE AND
INFECTIOUS DISEASE TRANSMISSION
3.1. SOURCES OF PATHOGENS IN HOME AND EVERYDAY LIFE SETTINGS
15
15
3.2. ASSESSING THE CAUSAL LINK BETWEEN HYGIENE AND INFECTIOUS DISEASE USING
MICROBIOLOGICAL DATA
15
3.3 ASSESSING THE LINK BETWEEN HYGIENE AND INFECTIOUS DISEASE USING INTERVENTION
STUDIES
19
3.4 ASSESSING THE LINK BETWEEN HYGIENE AND INFECTIOUS DISEASE FROM OBSERVATION
STUDIES
20
SECTION 4. DISCUSSION – REVIEWING THE IFH RISK-BASED APPROACH TO HOME HYGIENE
22
4.1 USING DATA FROM ALL SOURCES TO ASSESS HYGIENE RISKS AND DEVELOP CODES OF
HYGIENE PRACTICE
23
SECTION 5. IMPLICATIONS FOR FURTHER DEVELOPMENT OF TARGETED HYGIENE, AND FOR
DEVELOPMENT OF HYGIENE PROMOTION PROGRAMMES BASED ON TARGETED HYGIENE
26
5.1 DEVELOPING AND PROMOTING HYGIENE CODES – A SINGLE OR MULTI-BARRIER
APPROACH?
26
5.2 BRINGING ABOUT BEHAVIOUR CHANGE
27
5.3 DEVELOPED COUNTRIES – PROMOTING MULTI-BARRIER APPROACHES AND ACHIEVING
BEHAVIOUR CHANGE
30
5.4 DEVELOPING COUNTRIES – PROMOTING SINGLE AND MULTI-BARRIER APPROACHES AND
ACHIEVING BEHAVIOUR CHANGE
31
5.5 IFH – DEVELOPING CODES OF HYGIENE PRACTICE FOR DEVELOPED AND DEVELOPING
COUNTRY SITUATIONS
SECTION 6. CONCLUSIONS AND RECOMMENDATIONS
33
33
3
APPENDICES
36
1. MICROBIOLOGICAL ASSESSMENT OF THE SOURCES, DISPERSAL, PERSISTENCE AND
SPREAD OF MICROBES IN THE DOMESTIC ENVIRONMENT
1.1 CHAIN OF TRANSMISSION OF INFECTIOUS GASTROINTESTINAL DISEASE
36
36
1.1.1. Sources of enteric pathogens in the home
36
1.1.2 Survival and spread of gastrointestinal pathogens in the home
42
1.1.3 Risks from exposure to gastrointestinal pathogens in the home
52
1.2 CHAIN OF TRANSMISSION OF RESPIRATORY TRACT INFECTIONS
53
1.2.1 Sources and spread of cold and flu pathogens
54
1.2.2 Infection risks from exposure to cold and flu pathogens
57
1.2.3 Lower respiratory tract infections
58
1.2.4 Other respiratory pathogens
59
1.3 CHAIN OF TRANSMISSION OF SKIN AND WOUND INFECTIONS
61
1.3.1 Staphylococcus aureus and methicillin resistant Staphylococcus aureus (MRSA)
62
1.3.2 Other skin and wound pathogens
1.4 CHAIN OF TRANSMISSION OF EYE AND EAR INFECTIONS
68
69
2. CLOTHING AND HOUSEHOLD LINENS AS VECTORS FOR TRANSMISSION OF INFECTION
70
3. AUDITS OF MICROBIAL CONTAMINATION IN THE DOMESTIC ENVIRONMENT
70
3.1 AUDIT STUDIES OF CONTAMINATION OF ENVIRONMENTAL SITES AND SURFACES IN THE
HOME
70
3.2 AUDIT STUDIES OF CONTAMINATION OF MOBILE PHONES, COMPUTER KEYBOARDS ETC
73
3.3 AUDIT STUDIES OF CHILDREN’S TOYS
74
3.4 STUDIES IN DEVELOPING COUNTRY SITUATIONS
75
3.5 AUDIT STUDIES OF HAND CONTAMINATION NORMAL DAILY LIVING
78
4. AIR AS A SOURCE OF FUNGAL PATHOGEN AND BACTERIAL ENDOTOXIN EXPOSURE IN THE
HOME
78
5. ASSESSMENT OF THE CAUSAL LINK BETWEEN HYGIENE AND INFECTIOUS DISEASES USING
DATA FROM INTERVENTION AND OBSERVATIONAL STUDIES
80
5.1 OBSERVATIONAL STUDIES OF THE IMPACT OF HYGIENE ON INFECTIOUS DISEASES
81
4
5.1.1 Hygiene and infectious intestinal diseases
81
5.1.2 Hygiene and respiratory tract infections
89
5.1.3 Hygiene and skin and wound infections
90
5.1.4 Hygiene and fungal infections
91
5.1.5 Home hygiene and overall rate of infection
92
5.2. ASSESSMENTS OF THE CAUSAL LINK BETWEEN HYGIENE AND INFECTIOUS DISEASES USING
DATA FROM INTERVENTION STUDIES
92
5.2.1 Intervention studies assessing the impact of hand hygiene on gastrointestinal,
respiratory tract and skin and wound infection
92
5.2.2 Impact of safe faeces disposal, and household water treatment and safe storage
on diarrhoeal disease
95
5.2.3 Impact of environmental/surface hygiene procedures applied to hand-contact,
food-contact and other critical contact surfaces
96
6. USE OF QUANTITATIVE MICROBIAL RISK ASSESSMENT (QMRA) TO EVALUATE THE
HEALTH IMPACT OF HYGIENE
101
REFERENCES
103
5
SECTION 1. INTRODUCTION – AIMS AND OBJECTIVES OF THE REVIEW
The evidence presented in the 2009 IFH review on the global burden of hygiene-related
diseases 1 shows that infection outbreaks in the domestic home and everyday life settings,
particularly gastrointestinal (GI) infections (also called infectious intestinal disease (IID)),
respiratory infections (RT), and skin, wound and eye infections, continue to exact a heavy
toll on the health and prosperity of the global community. The evidence indicates that a
significant proportion of these infections are preventable by getting people to practice better
hygiene in their own homes and in everyday life. This includes food and respiratory hygiene,
and better hand, surface and laundry hygiene practices coupled with other practices such as
safe disposal of refuse and wastewater. In communities that lack access to adequate
sanitation and clean water, this may also involve ensuring water treatment and safe storage
and the safe disposal of faeces.
As reported in the 2009 IFH Review1 in recent years a number of events or trends have
prompted a need for greater investment in hygiene promotion:
• Food-related, waterborne, and non food-related infectious intestinal diseases (e.g.
many norovirus infections) remain at unacceptably high levels, much of this infection
occurring in or being related to practices in people’s homes).
• Evidence now suggests that respiratory hygiene plays a significant part in limiting the
spread of respiratory infections such as cold and influenza.
• New pathogens (including antimicrobial resistant strains) are continually emerging. In
the event of a pandemic, hygiene is seen as an important first line of defence.
• Alongside prudent antibiotic prescribing, hygiene is now seen as a key strategy for
reducing the impact of antibiotic resistance. Resistant strains traditionally regarded as
causing Healthcare–Associated infections are emerging in the community such as CAMRSA, and ESBL and NDM-1-producing gram negative strains. As persistent nasal or
bowel carriage of these strains in the healthy population increases, this increases the
risk of infection with these strains in both hospitals and the community. Hygiene
provides a means to reduce this “silent epidemic”.
• In developing countries, there is increasing realisation that integrating hygiene
education and hygiene promotion into water and sanitation programmes is key to
reducing the burden of diarrhoeal diseases.
At the same time:
• Social and demographic changes mean that people who have more or less reduced
immunity to infection make up an increasing proportion of the population (currently up
to 20%). The largest proportion is the elderly. It also includes the very young, patients
discharged from hospital, or home-based patients taking immuno-suppressive drugs or
using invasive systems, etc.
• Infectious diseases can act as co-factors in other diseases that manifest at a later
date, such as cancer and chronic degenerative diseases, or as triggers for allergic
diseases such as asthma.
• Globally, there is an inequitable distribution of disease. Populations with a low
education level, income level or occupational class are at a higher risk of infection.
This initiates a “vicious cycle” of infection predisposing to malnutrition and growth
faltering, which in turn leads to increased risk for further infection.
These changes demand new containment strategies, increasingly involving the community
as a whole. A number of interrelated factors should be considered:
• Although it is often assumed that respiratory and foodborne infections are a minor
concern, the burden in terms of absence from work and school is considerable.
6
• Community and hospital care for at-risk groups who become seriously ill, or develop
ongoing sequelae are further adding to the healthcare costs.
• Technological and policy changes (for example, use of less water and lower
temperatures for laundering) are being introduced in order to reduce costs and/or
environmental/ecological impacts without regard to the importance of a balanced
approach in which the need to reduce disease risks is also considered.
Governments, under pressure to fund the level of healthcare that people expect, are looking
at prevention strategies as a means to reduce health spending. Hygiene is recognised as a
cost effective means to reduce the infectious disease burden. Increased homecare is one
approach to reducing health spending, but gains are likely to be undermined by inadequate
infection control at home.
Although hygiene practice is now acknowledged universally as a cost effective means to
reduce the burden of infectious diseases, in developing countries, the overriding priority for
most governments is still the provision of clean drinking water, safe sanitation (excreta
disposal) and environmental issues (control of waste water, disposal of refuse etc).
According to a 2012 report by UNICEF and WHO, 2 in the developing countries, 2.5 billion
still lack access to sanitation services. Even though 1.8 billion people have gained access to
improved sanitation since 1990, the world remains off track for the Millenium Development
Goals sanitation target. Since 1990, although more than 2 billion people have gained access
to improved drinking water sources, there are still 780 million people without access to an
improved drinking water source. If we take into account the problems of chemical/microbial
quality, and those associated with collection/storage/handling of water in the home, the
figure would be much higher. As such any discussion on prevention of infection in homes of
the developing countries must be contextual to these realities. According to a World Bank
report, 3 inadequate water, sanitation and hygiene account for a large part of the burden of
illnesses (4 billion cases of diarrhea including 2.2 million deaths and 62.5 million DALYS
(Disability-adjusted life years), intestinal worms infect 10% of the developing country
population, 6 million people are blind from Trachoma, 300 million suffer from malaria, 200
million people are infected with schistomiosis). It is pertinent to note that, of the total number
of deaths globally attributable to poor water supply, sanitation and hygiene, 99.9% occurs in
developing countries. For total DALYS, the corresponding percentage is 99.8.
The International Scientific Forum on Home Hygiene (IFH) is a global, professional, nongovernment organisation which was established in 1997 to meet a growing need to develop
and promote an effective approach to home hygiene based on sound scientific principles. To
achieve this, IFH has drawn on the expanding volume of scientific data, to formulate a riskbased approach to home hygiene. Applied to the home, it has come to be known as
“targeted hygiene”.
The aim of targeted hygiene is to maximise protection against infectious diseases by
breaking the chain of infection transmission at critical points before infectious agents can
spread further.
The principles of targeted hygiene are reviewed in Section 2. The major objectives of this
report are:
• To assess the strength of the causal link between hygiene practice and infectious
disease (see section 3).
• To review the validity and applicability of the IFH risk-based approach to hygiene in
home and everyday life settings (see section 4).
• To review the key factors to be considered in applying targeted hygiene as part of
hygiene promotion programmes (see section 5).
7
These aspects are discussed in the following sections. The database of scientific material
used for developing the concepts outlined in Sections 3-5 is detailed in the appendices to
this review. This includes microbiological studies (laboratory and field-based), data on how
and to what extent pathogenic organisms enter the home and how they survive and are
spread around the home environment. This is reviewed together with data on the extent to
which we are exposed to these agents in our daily lives, and what is known about their
infectivity (infectious doses). Data from epidemiological (intervention and observational
studies) and data generated by quantitative microbial risk assessment is also reviewed.
This review is based on a previous review, prepared by the IFH in 2002, which has been
updated to contain material from the peer-reviewed literature accumulated by IFH since
2002 (the “new” material can be found in the reading rooms of the IFH website Library of
Recent Publications), together with contributions (published scientific literature) from the
knowledge base of the authors. These data are also addressed in some of our other IFH
reviews on specific issues including hand hygiene, 4 household water treatment and safe
storage, 5 viral 6 and fungal 7 infections, and on MRSA, Clostridium difficile and ESBLproducing Escherichia coli. 8 Evidence assessing the role and effectiveness of hygiene
procedures in breaking the chain of infection is reviewed in detail in another IFH review
“Hygiene procedures in the home and their effectiveness: a review of the evidence base”. 9
The focus of this review is infection prevention in the home and in everyday life, including
that part of primary healthcare which occurs in the home. It is not intended to cover other
primary care settings including residential facilities, although much of the data is also
relevant to these settings.
We anticipate that readers will sometimes use this review as a reference source for
individual issues. For this reason, we have tried to make sections as internally
comprehensive as possible; thus readers may find some repetition in the material presented.
SECTION 2. INTRODUCTION – THE IFH TARGETED APPROACH TO HOME HYGIENE
2.1 A RISK-BASED APPROACH TO HOME AND EVERYDAY LIFE HYGIENE – BASIC PRINCIPLES
The aim of using a risk-based (targeted) approach to hygiene is to maximise protection
especially against infectious diseases by breaking the chain of infection transmission and
addressing other risk factors. As specified by Aiello and Larson, 10 although a single factor (or
control point) such as the hands may be a “sufficient cause” of infection transmission, spread
of infection frequently involves a number of interdependent “component causes” which act
together or independently to determine the overall risk. The interdependent roles of the
hands and environmental sites and surfaces etc in the chain of infection transmission can be
understood by mapping the potential routes of spread of GI, RT and skin infections in the
home as shown in Figure 1. This suggests that, for all 3 groups, the hands are probably the
single most important transmission route because, in all cases they come into direct contact
with the known portals of entry for pathogens (the mouth, nose and conjunctiva of the eyes),
and are thus the key last line of defence. Figure 1 shows that, although, in some cases, the
hands alone may be “sufficient cause” for transmission of an infection (e.g., from an MRSA
carrier, to hands, to the wound of a recipient), in other cases transmission involves a number
of component causes (e.g., from contaminated food, to a food contact surface, to hands, to
the mouth of a recipient).
8
Figure 1 – Routes of transmission of infection in the home
There is considerable debate regarding the extent to which respiratory viruses such as cold
and flu viruses, and enteric viruses such as norovirus are transmitted via surfaces as
opposed to via aerosols droplets. The data on this aspect is reviewed in appendix 1.2. It is
also noted that, although people and domestic animals are the primary reservoirs of GI
infections, in situations where sanitation is inadequate, faeces are a key vehicle for
transmission of pathogens to hands and surfaces.
The criteria (and methodology) for assessing causal inference of a link between hygiene
practices and infectious disease risk reduction have been reviewed by Aiello, Larson and coworkers. 11,12 They postulate that establishing the health impact of a hygiene intervention
requires evaluation of a range of criteria including the strength, consistency, specificity and
temporality (cause and effect) of the association, together with data on plausibility
(microbiological or behavioural). Other factors include time dependency (did the outcome
occur after the cause?), biological gradient (is there a relationship between the number of
infectious agents to which the population is exposed and occurrence of infection?) and
consistency of the association (has the same association between a hygiene practice and a
health-related outcome, been shown among different populations, at different times and in
different geographical locations?).
9
One of the problems in making the case for hygiene as a cost-effective means to reduce the
burden of infectious disease has always been the lack of quantitative data (intervention
studies, randomized controlled trials etc.) indicating the extent to which infections result from
poor hygiene relative to other causes. Although epidemiological studies have been used to
assess the impact of hand hygiene, household water treatment and safe disposal of faeces,
relatively few studies have directly assessed the health impact of procedures such as
surface hygiene, cleaning cloth hygiene or laundry hygiene. Even for hand hygiene, where
intervention or case-control studies have been performed, most of these have involved
settings such as schools or day-care centres rather than the home and everyday life
settings.
Assessing the health impact of practices, such as surface and cleaning cloth hygiene, either
in combination with or separate from that of practices such as hand hygiene or household
water treatment, is particularly difficult because of the multiplicity and close interdependence
of the routes of infection transmission which make it difficult to determine the separate
effects of different interventions, and the difficulties in controlling variables. It also stems
from the large population sizes required to produce a significant result which makes the cost
of such studies prohibitive. The impact may also vary from one community or even one
household to another, according to a range of factors such as the types of pathogens
prevalent within that community, their modes of transmission and the social conditions and
domestic habits of the study population. In developing codes of hygiene practice for the
home, this makes it difficult to assign values to the relative importance of different
procedures e.g., hand hygiene relative to surface hygiene.
Relative to intervention and observational study data, there is now a large body of
microbiological data which shows the extent to which infectious disease agents enter the
home, how they survive and are spread, the extent to which we are exposed to these agents
in our daily lives, and what is known about their infectivity. A limiting factor is that the
majority of these data come from homes in developed countries, with advanced systems of
water and sanitation. Although laboratory tests and field data can be used to quantify the
impact of hygiene procedures on transmission of infectious agents, they give no assessment
of how microbiological contamination reduction correlates with reduction in disease burden.
Risk modelling techniques now offer the possibility to perform such assessments but this
approach is also open to challenge.
Currently, there is still a tendency to demand that data from intervention studies should take
precedence over data from other sources in formulating public health policy. Although there
are those who still adhere to this, it is increasingly accepted that, since transmission of
pathogens is so complex, infection control policies and guidelines must be based on the
totality of evidence including microbiological as well as epidemiological data. This is
particularly important for home hygiene, for which little or no intervention data is available
and where it is virtually impossible to isolate the effects of specific hygiene procedures
(handwashing, surface hygiene, laundry, washing and bathing etc.). This shift of opinion is
reflected in a 2005 document produced by the UK Health Development Agency 13 which
concluded that “Although the randomised controlled trial (RCT) has the highest internal
validity and, where feasible, is the research design of choice when evaluating effectiveness,
however, many commentators felt the RCT may be too restrictive for some public health
interventions, particularly community-based programmes. In addition, supplementing data
from quantitative studies with the results of qualitative research is regarded as key to the
successful replication and ultimate effectiveness of interventions”.
In the following section, the IFH targeted approach to home hygiene is outlined. The
development of this approach has been based on a consideration of the totality of data
10
which ranges from microbiological studies (laboratory and field-based), to investigations of
outbreaks, data from intervention and observational, and data generated by quantitative
microbial risk assessment. These data are summarised in Appendices 1-6.
2.2. DEVELOPING THE IFH TARGETED APPROACH TO HOME HYGIENE
As outlined in the introduction, in devising a strategy for home hygiene and producing
hygiene practice advice, the IFH has developed an approach based on risk management
which involves identifying the “critical control points” for preventing the spread of
infectious disease. Risk management is now the standard approach for controlling microbial
risks in food and other manufacturing environments, and is becoming accepted as the
optimum means to prevent such risks in home and healthcare settings.11,14,15
The key feature of the IFH approach is that it recognises the need to look at hygiene from the
point of view of the family and the total range of problems that they faces in order to reduce
infectious disease risks. This includes risks related to poor food and water hygiene, poor
personal hygiene (particularly hand hygiene), hygiene related to clothing and household
linens, and hygiene related to the general environment (toilets, baths, hand basins, surfaces
etc.), to domestic animals, and to family members at increased risk of infection. Other factors
include unsafe disposal of faeces and refuse. Adopting a holistic approach makes sense,
since all these issues are interdependent and based on the same underlying microbiological
principles. A risk assessment approach also forms the basis for developing an approach to
home hygiene which can be adapted to meet differing needs in differing communities across
the world. Indeed, it is only by adopting such a holistic approach that the causal link between
hands and infection transmission in the home can be addressed properly, since hand
hygiene is a central component to all of these issues.
The IFH risk approach starts from the principle that pathogens are introduced continually into
the home, by people (who may be ill or infected even without apparent symptoms), food and
domestic animals, but also sometimes in water, via insects, or via the air. People, food,
water, animals etc. as sources of infection in the home are reviewed in Appendices 1.1.1,
1.2.1 and 1.3.1. Household pets as a source of infection has also recently been reviewed by
Chomel and Sun (2011). 16 Additionally, sites where stagnant water accumulates such as
sinks, toilets, waste pipes, or items such as cleaning or face cloths readily support microbial
growth and can become primary reservoirs of infection; although species are mostly those
which represent a risk to vulnerable groups, primary pathogens can also be present. Damp
conditions such as the tiling and other surfaces in kitchens and bathrooms readily support the
growth of fungi, but sites of fungal growth also include carpets and soft furnishings. 17 Fungi
found on these surfaces are mostly opportunistic species that cause infection in the immunocompromised community living at home.
As long as there are people, animals and food in the home, there will always be a risk of
exposure to pathogens. In many homes, there will also be at least one family member who is
more susceptible to infection for one reason or another.
Reducing the spread of infection in homes and everyday life is achieved in 2 ways:
• To some extent we can control the spread of infection by controlling potential infection
sources/reservoirs e.g. preventing the growth of mould and fungi, safe storage of food
etc.
• By controlling the vectors (e.g. insects) and vehicles (e.g. hands and surfaces) which
serve as transmitters of pathogens.
11
Within the home (as in other environments) there is a chain of events, as described in Figure
2 that results in transmission of an infection from its original source to a new recipient such
that when circumstances combine, people become infected.
Figure 2 – The chain of infection transmission in the home
The risk-based approach to home hygiene has previously been outlined in a number of IFH
publications. 18,19 To carry out a risk assessment, sites and surfaces in the home are
categorised into six groups: reservoir sites, reservoir/disseminators, hands, hand and food
contact surfaces, clothing and household linens, and other surfaces. Risk assessment is
based on assessing the frequency of occurrence of pathogenic contamination at that site,
together with the probability of transfer from that site such that family members may be
exposed. This means that, even if a particular environmental site is highly likely to be
contaminated, unless there is a probability of transfer from that site, the risk of infection
transmission is low. From this, the “critical control points” for preventing spread of infection
can be determined.
The development of this risk-based approach has been based largely on consideration of the
available microbiological data as detailed in the Appendices, including assessments of:
• frequency of occurrence of sources of pathogens in the home;
• rate of “shed” from an infected source into the environment;
• rate of die away on hands and surfaces etc.;
• rate of transfer via the hands to the mouth, nose, conjunctiva etc. or to ready-to-eat
foods;
• the infectious dose. A key factor which determines the infection risk is the number of
particles to which the recipient is exposed, their immune status and the route by which
they are infected. The “infectious dose” varies for different pathogens and is usually
lower for people who are immuno-compromised than for healthy household members.
Overall these data suggest that:
• For reservoir sites such as the sink, waste pipes or toilets, although the probability of
significant contamination (i.e., with potentially pathogenic bacteria, fungior viruses) is
high, the risk of transfer is relatively limited, unless there is a particular risk situation
(e.g., a family member with enteric infection and fluid diarrhoea, when toilet flushing
can produce splashing or aerosol formation that can be inhaled or come into contact
with the eyes or nose, or can settle on contact surfaces around the toilet).
12
• For reservoir sites such as wet cleaning cloths, not only is there a high probability of
significant contamination, but, by the very nature of their usage, they carry a high risk
of disseminating contamination to other surfaces and to the hands.
• For hands, and hand contact and food preparation surfaces, although the probability of
significant contamination is, in relative terms, less, it is still significant, for example,
particularly following contact with contaminated food, people, pets or other
contaminated surfaces such as door, tap (faucet) and toilet-flush handles. Since there
is a constant risk of spread from these surfaces, hygiene measures are important for
these surfaces.
• For clothing and household linens, although the probability of significant contamination
is less than for hands, hand and food contact surfaces and cleaning utensils, the
microbiological data suggests it is still significant, particularly following contact with an
infected source (people, raw contaminated food, domestic animals). Since there is a
risk of spread from these surfaces, it is important that, for items that come into direct
contact with body surfaces, laundry processes should be used which eliminate
contamination.
• For other surfaces (floors, walls, furniture etc.), risks are mainly due to pathogens such
as S. aureus and C. difficile that survive dry conditions. Because the risks of transfer
and exposure are relatively low, these surfaces are considered low risk, but where
there is known contamination, (e.g., floors soiled by pets) crawling infants may be at
risk. Cleaning can also re-circulate dust-borne pathogens onto hand and food contact
surfaces. However, damp surfaces e.g. tiled bathroom or shower surfaces can support
the growth of fungi/moulds which can be spread by hand, feet or body contact or by
airborne dispersal of spores
Overall, this approach allows us to rank sites and surfaces (Figure 3) according to the level
of risk. This indicates that the “critical control points” or “component causes” of infection
transmission in the home are the hands, together with hand and food contact surfaces and
cleaning cloths. Although, in some cases, the hands alone may be “sufficient cause” for
transmission of an infection (e.g., from an MRSA carrier, to hands, to the wound of a
recipient), in other cases, transmission involves a combination of control points, hand and
food contact surfaces, cleaning cloths and other cleaning utensils. Transmission via the
hands in itself also depends on the extent to which these surfaces become contaminated
with pathogens during normal daily activities, i.e., the risk of hand-to-mouth transfer will be
increased if extensive transfer from raw food to food preparation surfaces also occurs. Other
control points include clothing and household linens, together with other surfaces which
come into contact with the body such as baths and hand basins.
Figure 3 – Ranking of sites and surfaces based on risk of transmission of infections
13
Although Figure 3 gives a useful “rule of thumb” ranking, it is not a constant. Risks can
increase substantially where a family member is infected Risks are also increased in
situations where there are family members living at home who have reduced immunity to
infection.
Whereas Figure 3 is constructed mainly in relation to westernized home where there is
adequate access to clean water and a means of safe faeces disposal, it must be recognised
that the priorities of home hygiene practices vary substantively between developing and
developed countries. In developing countries the home is the vital interface between
personal and domestic hygiene and environmental/community hygiene. Given that the level
of environmental and community hygiene particularly in respect of safe water and sanitation
are often extremely poor, particularly in low income communities, Figure 4 gives a more
realistic basis for prioritising hygiene interventions in the homes of developing countries,
where safe disposal of faeces, adequate and safe water, and hand washing are regarded as
the basic “pillars” for building effective hygiene practice
Figure 4 – Ranking of sites and surfaces based on risk of transmission of infections
For example:
• For rural and urban unserved communities, the priority is to educate and empower
people on how to achieve safe disposal of faeces, ensure a sufficient supply of clean
water for drinking and how to develop a culture in which handwashing at critical times
is an accepted norm
• For other communities, the extent to which the community needs to take responsibility
for activities in stage 1 and 2 will vary according to prevailing conditions i.e. the
availability of water, sanitation, municipal waste collection and wastewater drainage
• For urban middle class served communities, although basic amenities of sanitation,
water and refuse collection may be available, promotion of handwashing at critical
times and safe refuse disposal are still a major priority. If municipal water quality is
poor, promoting “water at point of use”, hygiene must also be included as a priority.
For these communities it should be possible to build stage 2 and 3 interventions into
hygiene promotion programmes
This approach is described in more detail in the IFH home hygiene training resource for
developing country situations. 20 The IFH Home Hygiene guidelines contain the results of a
review by Feacham in which he rates the importance of different interventions in relation to
different types of infections e.g. diarrhoea, helminth, skin, eye etc. 21
14
SECTION 3. ASSESSMENT
OF THE CAUSAL LINK BETWEEN HYGIENE PRACTICE AND
INFECTIOUS DISEASE TRANSMISSION
In this section the data from microbiological, observational and intervention studies, and
studies involving Quantitative Microbial Risk Assessment (QMRA), as documented in the
Appendices, are integrated and compared in order to draw conclusions about the routes of
infection transmission, the strength of the causal link between hygiene and infectious
disease, and the relative impact of different hygiene interventions on infectious disease rates
in home and everyday life settings.
3.1. SOURCES OF PATHOGENS IN HOME AND EVERYDAY LIFE SETTINGS
Appendices 1-4 show that the main sources of pathogens in home and everyday life settings
are people or animals that are infected (or are carriers), and contaminated food and water.
Surveillance data suggest that these pathogen sources are constantly present in our homes
and elsewhere. An interesting finding of this 2011 review is the extent to which the data (not
only microbiological, but also observation study data) implicate domestic animals as a source
of GI infections in the home. Case-control studies, as cited in Appendix 5.1, identified pets
and domestic animals as significant risk factors for campylobacter infection in 3/5 studies,
whilst pets and reptiles were identified as risk factors for Salmonella in 6/9 studies. In one of
these studies, the authors concluded that environmental sources, infected family members
and pets were more significant risk factors for salmonellosis in children than contaminated
foods. The data also suggest that dogs and cats can act as a source and/or vector of MRSA
in the home. Although the public are traditionally most concerned about the risks associated
with the “germs” that can form permanent resident populations in their home environment
(e.g. in the toilet or sink waste trap), the data (as reviewed in appendix 3) suggest that these
are mostly (although not always) potential or conditional pathogens which represent a risk
mainly to those who are immuno-compromised.
3.2. ASSESSING THE CAUSAL LINK BETWEEN HYGIENE AND INFECTIOUS DISEASE USING
MICROBIOLOGICAL DATA
Microbiological data from field studies and laboratory models (Appendices 1.1.1, 1.2.1 and
1.3.1.1) show that pathogens are constantly being shed or spread (often in high numbers)
from human, animal and food sources in home and everyday life settings, and are
transmitted via environmental sites and surfaces such that people become exposed. The
IFH targeted approach to hygiene focuses on breaking the chain of infection transmission by
intervening at “critical points” in the chain. The key principle of this approach is that, in order
to identify critical points, it is necessary to assess not only the likelihood that pathogens may
be present, but equally, whether they are likely to be transferred around the environment
such that we are exposed to them.
Microbiological data showing shedding of pathogens from an infected person, contaminated
food, domestic animals etc., is consistent with data (Appendix 1.1.2, 1.2.1, 1.2.4, 1.3.1.2,
1.3.2, 2 and 4) showing that these agents can be isolated from hands, hand contact
surfaces, food contact surfaces and cleaning utensils in the home and elsewhere. The
data suggest that the greatest risks occur immediately after contact with, or shedding from
an infected source. During the 1980s, infection risks associated with environmental sites and
surfaces were largely assessed from audit studies which involved microbiological sampling
of sites and surfaces in homes sampled at random. These studies, as reviewed in Appendix
3, showed that, although pathogenic species are present, detection is relatively infrequent in
15
homes sampled at random, even in studies involving up to 200 or more homes. These data
tended to foster a view that infection transmission risks via hands and environmental sites
and surfaces in the home are relatively low. Since around 1990, studies now tend to focus
on looking at the extent of shedding, persistence and spread of organisms via hands and
surfaces from a known infected source such as contaminated food or an infected person.
This report contains the significant amount of data, published since the 2002 IFH review (see
Appendix 1.1) which confirms that, following handling of contaminated food, or where there
is an infected person present, enteric pathogens such as Salmonella or Campylobacter are
frequently isolated from hand and food contact surfaces. Of particular interest is the range of
new studies, which support earlier data (Appendix 1.2) showing the extent to which, not only
enteric viruses such as norovirus, but also respiratory viruses such as rhinovirus, influenza
and parainfluenza viruses, can be found on “critical point” surfaces, in situations where there
is known to be, or is likely to be, an infected person. Data in Appendix 1.3 show the extent to
which S. aureus (including MRSA) can persist and be transferred via hands and
environmental surfaces where there is a known infected person. Most surprising perhaps, (in
contrast to the audit studies as mentioned above) is the 2010 study of Boone and Gerba 22
where parainfluenza virus was isolated from 37% of surfaces in office buildings sampled at
random. Appendix 1.1.2 also contains 3 examples from studies reported in 2010 and 2011
where norovirus was detected on environmental surfaces in the absence of an identified
infected source. 23,24,25 Another new study 26 shows that, not only S. aureus but also MRSA,
can be found on environmental surfaces in homes sampled at random (i.e., not selected on
the basis that there was an identified carrier). Although the hands are assumed to be the
main vehicle for transmission of infection in the home there is surprisingly little data on the
nature and extent of hand contamination, both during normal daily activities or associated
with exposure to an infected source, but some studies e.g. studies involving handling of
contaminated poultry or contaminated cloths confirm this.
From the data which shows the high levels of pathogens (up to 104-1011/g for enteric
pathogens, 107/ml for influenza virus) found in very small volumes of faeces, vomit, food
particles, skin scales etc., and the amounts of material which are shed or spread, it must be
assumed that the numbers of organisms deposited within a relatively small area of these
surfaces can be well in excess of 103 to 104 or more cells or particles. Importantly, although
there is an amount of data, showing the frequency with which pathogens shed from an
infected source can be found on surfaces, there is currently little data on the numbers of
cells or particles which can be recovered from these surfaces over extended time periods
following contamination. One example is the studies of Cogan et al. 27,28 which showed that,
following preparation of Salmonella and Campylobacter-contaminated chickens as an
infection risk in domestic kitchens, these species could be isolated from 17.3% of hands, and
hand and food contact surfaces. Although 18.3% of sites recorded Salmonella counts of
<10, on 22 (18.3%) and 2 (1.7%) of occasions, counts were >10 and >1000, respectively.
For Campylobacter, 20% of sites recorded counts of >1000. Sampling of surfaces 3 hours
later27 showed that 7% of surfaces were still contaminated with either Salmonella or
Campylobacter.
Although there is relatively little data available, it would be expected that children’s toys are
an important hand (or mouth) contact site for transmission of enteric and respiratory
pathogens, particularly as these items frequently come into contact with children’s mouths.
The available data are reviewed in Appendix 3. Most studies review data for toys sampled at
random rather than in situations where there is a known infected source.
A key factor which determines the risks associated with hands and surfaces is the extent to
which infectious agents can survive outside a human or animal host and retain their
infectivity. The data (Appendices 1.1.2, 1.2.1, 1.3.1.2, 1.3.2, 2) indicate that the numbers of
viable units decline at a more or less rapid rate, depending on the species and other factors
16
such as surface type and RH. The data indicate that Gram positive spp. such as S. aureus,
C. difficile, and fungal spp. can survive long periods (several days to months) on hands and
non-porous surfaces. Although Gram negative species such as E. coli and P. aeruginosa are
generally more sensitive to drying, survival times of the order of up to 4 or more hours are
recorded. In one study, survival of E. coli O157 for up to 60 days on stainless steel and 10
days on a chopping board was reported. Reported survival times for viruses on non-porous
surfaces vary significantly; some data suggest that both enveloped and non-enveloped
viruses can survive for up to 3-4 hours, whilst other investigators suggest survival times of
days and weeks, particularly for non-enveloped viruses. Survival times for the enveloped
influenza and PIV viruses are relatively less than for non-enveloped rhinovirus and
Respiratory syncitial virus (RSV), particularly on hands where parainfluenza virus (PIV) and
influenza virus appear to survive relatively short periods (measured in minutes). This may be
due to the presence of fatty acids on the skin which exert a virucidal effect via the lipid virus
envelope. This may have a significant impact in reducing the transmissibility of the
enveloped influenza viruses via hands, relative to the non-enveloped rhinoviruses and RSV.
A further determinant of the infection risk is the extent to which these agents are transmitted
around the environment such that we become exposed either by direct hand to mouth or to
the nasal mucosa etc., or indirectly by transfer to food which is then consumed. Laboratory
models (Appendices 1.3.1.2, 1.3.1.3, 1.2.1, 1.2.2, 1.3.1.2, 1.3.1.3, 2) suggest that transfer
rates for enteric pathogens from contaminated surfaces to hands and from contaminated
hands to surfaces are of the order of 10-60%, but could be as little as 1% or as high as
100%. The data also show significant transfer from contaminated hands to the mouth or
other foods, or to the nasal mucosa.
Taken together, the total data indicate that significant numbers of bacterial, viral and fungal
pathogens are constantly circulating in the environment such that we are regularly exposed
to potentially infectious doses. The data (Appendices 1.1.3, 1.2.2, 1.3.1.3) show that
infectious doses for bacteria such as Campylobacter and E. coli O157 may be as little as
100-500 cells whilst for some viruses, 1-10 particles may be sufficient. For the most part, the
body defences are able to deal with this challenge, but in some cases infection results. This
is increasingly important for the increasing numbers of people particularly for those with
lowered immunity to infection who are now living in the home and community.
Risk assessment shows that clothing and household linens are also potential vehicles for
infection transmission. In view of the large amount of data on this subject it was decided to
address this issue in a separate IFH report. 29 The data in this report show that fabrics can
become contaminated with bacterial, viral and fungal pathogens. The main contaminants are
organisms such as S. aureus shed from the skin surface and other pathogens from the body
flora such as dermatophytic fungi and enteric pathogens. The data suggest that the greatest
risks occur immediately after contact with, or shedding from, an infected (or carrier) source,
but pathogens can survive on, and be transferred from, fabrics for significant periods of time.
The microbiological data suggests however that risks associated with clothing and linens
(particularly when dry) are somewhat less than those associated with the hands, hand and
food contact surfaces, and cleaning cloths. This is because survival of pathogens on porous
surfaces such as fabrics is significantly less than that on non-porous surfaces, and the
transfer rates for bacteria and viruses from fabrics to hands are much lower. Opportunities
for infection via clothing etc. are also less frequent; whereas there are constant opportunities
for person to person transfer through mutual touching of e.g. door or tap handles, we do not
deliberately touch other people’s clothing. Whereas the small area of a door or tap handle
means that it is highly likely that people will touch the same area, the large area offered by
clothing makes this less likely. Although the data suggest that laundry handling represents a
risk, the risk is specific to the person handling the laundry. A separate concern is that, where
laundry processes are insufficient to eliminate pathogens, these can be transferred to other
17
clothing. This is a current concern in relation to the trend towards using low temperature
laundry cycles. There is little data on the extent to which microbes can be shed onto
environmental surfaces from clothing and household linens, but the IFH report29 contains
some data on shedding of S.aureus from bed linens during changing of bedding
The major threat posed by antibiotic resistance means that greater emphasis must now be
placed on preventive strategies rather than relying on antibiotic therapy. By preventing
spread through better hygiene, we also reduce the reservoir of antibiotic resistant strains
circulating in the community. An example of this is the community MRSA strains (CA-MRSA)
which are just as likely to affect young active people as the elderly or infirm. The findings of
the IFH report29 suggest that transmission via clothing etc. is (alongside transfer via hands
and surfaces etc.) a risk factor for spread of S. aureus (including MRSA), and that the
hygienic effectiveness of laundry processes is important in defining their rate of spread in the
community. Over the period since 2002, CA-MRSA strains have become a major problem in
the US, but are still relatively uncommon in Europe and elsewhere, and there is still an
opportunity to avoid the problem escalating to a similar scale. We need to assess the impact
of hygiene, not only on MRSA infections, but also on colonisation rates in households and
communities. Data assessing the infection risks associated with S. aureus (including MRSA)
and the impact of hygiene are reviewed in Appendices 1.3,2, 5.1.3 and 5.2.3.Risk
assessment suggests that contact surfaces of baths, kitchen and bathroom wash basins,
draining boards etc. also have the potential to act as vehicles for transmission of infection.
Data from “audit” studies where homes were sampled at random (Appendix 2, Section 3)
(i.e., not selected on the basis that there was an identified carrier) indicate that these wet or
damp surfaces are commonly associated with high total counts and the presence of E. coli
and coliforms (isolation rates were mostly of the order of 10-20%, but up to 60% isolation
rates were recorded for coliforms on kitchen sink surfaces) and S. aureus (including MRSA)
(isolation rates for S. aureus ranged from 0.5 to 20%). A number of these studies showed
the presence of Salmonella, Listeria and P. aeruginosa on kitchen sink surfaces, whilst P.
aeruginosa was also isolated from baths and wash basin surfaces and Listeria spp from
toothbrushes in the bathroom. The data suggest that the stagnant water which builds up in
sink waste traps can act as semi-permanent sources or reservoirs of organisms (sometimes
as biofilms) such as E. coli and Salmonella and that these free-living populations can
transfer back into the basin due to splashing and aerosols.
This report (Appendix 1.1.2) contains new data assessing the potential risk from splashing
and aerosols generated by flushing of toilets. Although there is an assumption that infection
risks from properly functioning toilets are relatively low, the data suggest that dissemination
of pathogens by splashing and aerosol formation during toilet flushing, particularly where
someone is vomiting into the toilet, or has fluid diarrhoea e.g., where there is a norovirus
outbreak or salmonella infection can cause infection. It must be borne in mind that, in the
home, there is also risk of direct contact with toilet surfaces, by small children who see this
as just another play area to be explored. An issue which has been receiving recent attention
is the potential risks associated with aerosols generated by shower heads. Recent data as
reviewed in Appendix 1.2.4 report isolation of species such as Mycobacterium avium and
Legionella pneumophila from showerheads in homes and apartments, and in some
instances this has been linked to outbreaks of Legionella. In general, it is concluded that the
risks are low, and that preventive action is only/mainly required in homes where there are
people who are immuno-compromised.
Microbiological data indicate that infection transfer risks via floors, walls and furnishings
are relatively low except under certain specific conditions. The report contains data indicating
that dry surfaces such as floors and furnishings play a part in the spread of desiccationresistant organisms such as S. aureus (including MRSA), C. difficile and fungal spores. This
report contains some of the increasing number of studies showing that environmental
18
cleaning contributes to reducing hospital infection risks from MRSA and C. difficile, but more
data are needed to show the extent to which transmission via floors and furnishings (relative
to hand contact surfaces etc.) represent a risk in the home. It is interesting to note that,
alongside the observation studies suggesting that domestic animals can be a source of
Salmonella infection, microbiological data in Appendix 1.1.2 suggest that Salmonella can
survive in house dust on floors and furnishings, and can represent an infection risk. However,
data reviewed in Appendix 4 shows that damp surfaces, particularly e.g. tiled bathroom or
shower surfaces but also other surfaces can support the growth of fungi/moulds which can
be spread by hand, feet or body contact or by airborne dispersal of spores
3.3 ASSESSING THE LINK BETWEEN HYGIENE AND INFECTIOUS DISEASE USING INTERVENTION
STUDIES
Appendix 5.2 of this report reviews the growing amount of intervention study data which
provides consistent evidence of a strong causal link between poor hygiene and the spread of
infections in home and everyday life settings. The majority of studies, as reviewed in
Appendix 5.2.1 address the impact of hand hygiene, either alone or in combination with
environmental hygiene. Only a few studies have evaluated the impact of environmental
hygiene in isolation, and none compared the impact of environmental hygiene relative to
hand hygiene.
For studies where hand hygiene (either handwashing or using an alcohol hand gel) was
assessed as the sole intervention, the microbiological data are well supported by data from
intervention studies. These data (summarised in Table 4) suggest that the hands are the
“sufficient”, or a “component” cause of spread of infection, for up to 59 and 79% of GI
illnesses for developed and developing country situations, respectively. This fits with the
microbiological and observation data which suggest that, although there is a tendency, in
developed country situations, to assume that GI infections are mostly food-borne and result
from inadequate cooking and inadequate storage of food, in reality, many or most GI
infections (particularly in low income communities in developing countries) result from
person-to-person (faecal:oral) spread, involving hand to mouth transfer or transfer from
hands to food which is then eaten. For RT infection, the data (summarised in Table 4)
suggest that transmission via hands could be a sufficient or component cause of up to 53%
of illnesses; whereas there has been a tendency to assume that the impact of hand hygiene
on RT infections is lower than for GI infections because spread of RT pathogens is mainly
airborne, the microbiological data (both laboratory and field data as reviewed in Appendix
3.2.1) suggest that, for RT infections such as rhinovirus and RSV, the hands are the major
route of spread. Only 3 studies are reported in which the impact of hand hygiene on skin and
eye infections was studied; studies by Luby et al. 30 carried out in Pakistan showed a 25-34%
reduction in rates of impetigo in children whilst Nicholson et al. 31 in Mumbai demonstrated a
46% reduction in eye infections in children aged approximately 5 years old.
Intervention study data presented in this review (Appendix 5.2.2) indicate that unsafe
disposal of faeces and household handling and storage of water can be a sufficient or
component cause of GI infection. In the most recent reviews Waddington et al. 32 estimated
that, water quality interventions and safe excreta disposal interventions on average effect
respectively a 42% and 37% relative reduction in child diarrhoea morbidity, whilst Cairncross
et al. propose a diarrhoea risk reduction of 17 and 36%, associated respectively, with
improved water quality and excreta disposal. 33 However they concluded that most of the
evidence is of poor quality and more trials are needed.
19
Intervention studies where hand hygiene was combined with cleaning and/or
disinfection of environmental surfaces (Appendix 5.2.3) also consistently indicate a
positive impact on disease rates. The report includes 5 studies 34,35,36,37,38 which demonstrate
the positive impact of combined hand and environmental hygiene in reducing GI (including 1
norovirus study), RT and skin infections, together with absenteeism. Only 1 of these studies
was carried out in the home. In this 2007 study of 685 households in South Africa, Cole et
al.36 demonstrated that intensive hand and environmental hygiene education alone and in
combination with use of hygiene products (soap, surface cleaner/disinfectant, antiseptic)
could produce a significant reduction in GI infections (65-78%), RT (20-75%) and skin (2677%) infections. Some of the most compelling data demonstrating the impact of hygiene on
surface to hand to mouth/eye/nose transfer of GI and RT viruses come from the studies
carried out during the 1980s showed that surface hygiene could prevent experimental
rhinovirus infections caused by touching contaminated surfaces 39 and the studies of Ward et
al.(1991) which showed that, of 13 out of 14 individuals who touched rotavirus-contaminated
plates with their fingers and put the fingers to their mouths, about half became infected. 40
Only a few studies have been reported on the impact of environmental cleaning and/or
disinfection in isolation. Although these studies consistently indicate a positive impact on
disease rates, there was no attempt to assess the separate effects of one type of
intervention (e.g., touch surfaces, food contact surfaces, laundry etc) relative to another and
thereby rank their importance. The most compelling data showing a positive impact of
environmental cleaning relate to MRSA, 41 C. difficile and norovirus infections. 42,43 This is
perhaps unsurprising in view of the microbiological data which demonstrate the ability of
these species to survive and retain their infectivity on environmental surfaces. Data showing
a positive impact on combined RT and GI infection rates also come from a 2008 school
intervention study by Bright et al.(2009) in Seattle, US.23 This study measured the impact of
cleaning surfaces daily with disinfectant wipes before arrival of students on GI and RT illness
leading to absenteeism. Despite no significant reduction in bacterial counts on surfaces,
children in control classrooms were 2.32 times more likely to become ill than children in
intervention classrooms. Studies showing how enhanced cleaning/disinfection can reduce
transmission of infection in hospitals is reviewed by Otter et al. 2011. 44
Although these data come from studies in hospitals41,43, and public settings,23,42 they indicate
the potential for transmission in the home where good hygiene practice is not observed.
Data specific to the impact of environmental cleaning on the spread of MRSA in homes
come from 3 studies 45,46,47 where MRSA-colonised healthcare workers (HCWs) were treated
to produce eradication, but subsequently became re-colonised. In each case, MRSA was
isolated from environmental surfaces (pillows, bed linen, brushes, cosmetics, hand contact
surfaces and household dust) in their home, and the problem was only terminated after
thorough cleaning of the home environment.
3.4 ASSESSING THE LINK BETWEEN HYGIENE AND INFECTIOUS DISEASE FROM OBSERVATION
STUDIES
Appendix 5.1 reviews the growing amount of observational data assessing the link between
hygiene and infection. Most, but not all of the data is consistent with the data from
microbiological and intervention studies.
For RT infections (Appendix 5.1.2), new data on the impact of interventions such as
handwashing, wearing face masks etc. comes from case-control studies prompted by the
2003 SARS outbreak. From a 2003 review of 6 studies relating to this outbreak, Jefferson et
al. 48 concluded that handwashing was an effective measure in reducing spread. This report
20
also contains 2 case-control studies (one related to SARS) which also addressed
environmental cleaning, both of which recorded hand and environmental cleaning as risk
factors.
For skin infections (Appendix 5.1.3), the only case-control study data relates to MRSA. In
addition to reviewing US population-based data citing skin-to-skin contact and indirect
contact with contaminated objects such as towels as risk factors, Appendix 5.1.3 reviews 10
studies involving the home environment. Five of these studies involved healthcare workers
at home for whom the environment was cited as a causative factor in recolonisation following
treatment to eradicate MRSA, whilst 7 reported transmission to other family members.
For GI infections, Appendix 5.1.1 reviews 25 outbreak studies where hands, hand and food
contact surfaces, clothing and linen, toilets and other surfaces were implicated as a, or the,
route of transmission, including outbreaks associated with Salmonella (6 studies), E. coli (2),
Campylobacter (2), Listeria (1), Helicobacter pylori (2), norovirus (9), rotavirus (3) and
hepatitis A (3). Some of the data from case-control studies however, tend to conflict with
these findings, and with the microbiological data. This IFH report reviews a number of
relatively large scale case-control studies, and systematic reviews of these studies, which
investigated the links between foodborne infection and food handling behaviour (food
preparation, temperature control, and opportunities for cross contamination) in domestic
kitchens. In their systematic review Stenberg et al. 49 in general found no differences
between cases and controls. Contrary to the microbiological and other data, their reanalysis
of the UK IID study showed no difference between numbers of cases and controls which
reported not using a separate chopping board for raw and cooked foods, not cleaning the
chopping board between raw and cooked food, and using the same cloth for wiping all
kitchen surfaces. Since there was no possibility to identify and exclude non-foodborne cases
from the data, it is perhaps unsurprising that the studies failed to identify food handling
activities as significant risk factors for GI infection. These studies show the difficulties of
making accurate assessments about hygiene risk factors for GI disease from studies which
use pooled data involving a range of different pathogens with different transfer properties
and interdependent routes of transfer. Stenberg et al.49 conclude “It is doubtful that the
impact of domestic kitchen hygiene can be resolved based on case-control studies. There is
a need for properly conducted intervention studies to really investigate the contribution which
particular domestic kitchen hygiene practices may or may not have on the risk of diarrhoeal
disease”. These would only have relevance if it is possible to exclude GI infections outcomes
which are non-foodborne.
Although the epidemiological data shed little light on the relative risks associated with
different environmental “control points”, one factor which was identified as significant in
several case-control and other studies was the laundering of clothing and household linens.
These data are reviewed in a separate 2011 IFH report.29 Of particular relevance is the 2001
correlational prevalence study of Larson and Duarte 50 which examined the relationship
between specific hygiene practices and prevalence of GI, RT and skin infectious disease
symptoms in household members in a city population in New York. In general, the study
showed no association between a range of hygiene practices (frequency of personal bathing
or showering, cleaning of kitchens, bathrooms and toilets, changing of dish-sponges, or
use/non-use of antimicrobial cleaning products) and infection risk. However 2 activities,
using a communal laundry and not using bleach in communal laundering were found to be
predictive of increased risk of infection (although duration of bathroom towel use was not
significant). Again the results are unsurprising since, apart from laundry, the “hygiene”
practices investigated were mostly non-targeted daily or weekly routine cleaning activities
which are unlikely on their own to have a measurable impact on breaking the chain of
infection.
21
SECTION 4. DISCUSSION – REVIEWING THE IFH RISK-BASED APPROACH TO HOME HYGIENE
In this section the data from microbiological, observational and intervention studies is
considered in relation to the validity and development of the IFH targeted approach to home
hygiene as outlined in Section 2. The “targeted” approach to hygiene in home and everyday
life settings was developed by IFH during 1997 to 2000 using the microbiological evidence
available at the time. This approach is outlined in Section 2. In general, the totality of data as
detailed in this review continues to fit well with the IFH targeted approach.
Overall, the intervention study data, as reviewed in this report, consistently demonstrate the
positive impact of hand hygiene, safe collection, storage, handling and point of use treatment
of household water, safe disposal of faeces and environmental hygiene (either alone or in
combination with hand hygiene) on infectious disease rates, thereby establishing the critical
nature of these interventions, or groups of interventions, as “control points” for breaking the
chain of infection. As far as environmental hygiene (surface hygiene, laundry hygiene etc.) is
concerned however, there has been little or no attempt in any of these studies to separately
assess the impact of individual environmental interventions such as surface, cleaning cloth
or laundry hygiene on disease rates. This makes it very difficult to assess their relative
importance i.e. their relative contribution to reducing infectious disease rates in the home.
To an extent, the lack of intervention study data can be overcome, by using the
microbiological data together with observation studies of people’s behaviour in the home
(such as the studies of Griffiths et al. as described in section 4.1) to assess the risks
associated with different routes of infection transmission (surfaces, cleaning cloths, airborne
etc.) relative to those associated with the hands, for which quantitative estimates of the
impact of hygiene measures on GI, RT and skin infection diseases rates provide a
benchmark. In general, the microbiological data continue to fit well with the ranking hierarchy
of risks as shown in Figure 3. The data indicate that, overall, the hands are the single most
important transmission route since they come into direct contact with the mouth, nose and
conjunctiva of the eyes. Comparison of the microbiological data and observation data for
contact surfaces against data for hands indicates that these are also important risk factors or
control points. The data suggest that the most important are surfaces which come into
contact with our hands and body surfaces, and with food and water These include hand and
food contact surfaces (including children’s toys), cleaning cloths and other cleaning utensils.
This conclusion is inferred, not only from the microbiological data which shows that
pathogens are readily transferred to these surfaces from contaminated sources during daily
life activities, but also the fact that daily life activity and conditions offer constant opportunity
for contact with, or onward transmission from, these vehicles. As far as clothing and
household linens are concerned, the microbiological data suggest that, although these are
important risk factors, the risks are probably somewhat less than those associated with
surfaces such as the hands, hand and food contact surfaces, and cleaning cloths. The data
in Appendix 1 suggest that surfaces which come into contact with the body such as baths
and hand basins can also sometimes act as vehicles of infection, as can surfaces associated
with the toilet.
The relative contribution to household illness from transmission of RT and GI infections via
aerosol particles, as compared with hand and surface transmission, is not well understood.
For colds and flu, based on the available evidence as reviewed in Appendix 1.2 and 5.2.1,
opinion as to the importance of the hands and surfaces relative to the airborne route is
divided. Some investigators maintain that, for cold viruses such as rhinovirus and RSV,
contamination of the hands followed by inoculation of the eyes or nose is of paramount
importance whilst others maintain that the evidence favours droplet and droplet nuclei
transmission as the most important mode of spread, particularly for influenza virus. Although
there is data which shows that wearing of masks can contribute to reducing risk of spread of
22
RT infections such as SARS and influenza, there is no data on the impact of basic
respiratory hygiene (e.g. covering the nose and mouth during coughing and sneezing) on RT
infection rates. In section 5.1.1 data supporting aerosol transmission of norovirus is
reviewed, but again there is no data to show the importance of this route relative to
transmission via hands and surfaces.
As stated in Section 2.2, although this gives us an assessment of the “daily life” risks
associated with these various sites and surfaces and the activities associated with them, it is
important, in developing hygiene practice codes, to recognise that these risks are not
constant, and can increase significantly under certain conditions. For example, although
risks from toilets, sinks, floors etc., relate mainly to the relatively low risk of transfer from
these sites to hands, hand and food contact surfaces and cloths, this risk can increase
substantially where an infected family member has diarrhoea, or where a floor surface is
contaminated with vomit or faeces. Similarly, the risks of transmission via clothing and
household linens will increase where one family member has a skin or wound infection.
Risks are also increased where there are family members living at home who have reduced
immunity to infection and may require special care to protect them from infection.
Some quantitative estimation of the health impact (i.e., the infectious disease reduction), and
relative impact, of individual hygiene practices, can be achieved using Quantitative Microbial
Risk Assessment (QMRA) which, as outlined in Appendix 6, involves using published data
on each stage of the transmission cycle to calculate a quantitative estimate of the impact of
a specific hygiene intervention on infection rates. Although risk modelling is a promising
approach, it has limitations because of the multi-factorial nature of infection transmission and
paucity of data to specify model parameters. What QMRA-generated data do illustrate
however is how even a relatively small quantifiable increase in the log reduction (e.g., using
a process which produces a 3 rather than a 2 log reduction on hands) can translate into a
significant decrease in the risk of infection transmission within a national population.
In developing appropriate hygiene practice codes, a particular concern is the fact that the
majority of the available microbiological data come from studies in developed countries and
from homes with access to “high quality” water and sanitation. Of interest are new studies
which are now being carried out in developing countries, as reported in Appendix 3.3, which
allow us to begin to assess the risks from environmental contamination in situations where
many of the amenities which are standard in westernised homes, are lacking. The recent
studies carried out in 8 homes in Cambodia by Sinclair and Gerba 51 are thus of particular
interest. The data suggest that levels of faecal and faecal indicator bacteria were up to 2
logs higher than in equivalent situations (sites and surfaces) in homes in the US and Japan,
despite the fact that the Cambodian homes had a pour-flush latrine for disposal of faeces.
The extent of the differences in environmental contamination levels suggest that more
extensive studies of these environments should be carried out to better inform decisions
about hygiene promotion in developing country settings in relation to their access to
adequate water, sanitation and other amenities.
4.1 USING DATA FROM ALL SOURCES TO ASSESS HYGIENE RISKS AND DEVELOP CODES OF
HYGIENE PRACTICE
This report is unique, because it brings together data from various experimental approaches
to provide clearer insights into the causal link between hygiene and infectious disease rates.
One of the things which clearly emerges from this exercise is the need to always consider
data from microbiological as well as from epidemiological studies in making risks
assessment and informing decisions about codes of hygiene practice. In the past, as
23
discussed in Section 2, there has been a tendency to demand that a specific intervention
should only be recommended on the basis of intervention study data which shows a clear
health benefit. New thinking on infection prevention is now challenging the assumption that
decisions regarding which interventions should be considered as critical control points and
which should be excluded, should only be made on the basis of clinical evidence of health
benefit. It is now being argued that not only is this not achievable, where routes of transfer
are closely inter-dependent, but is also not the most effective or practical approach. This
report shows that reliance on intervention study data alone can be misleading and that
predictive tools such as models to assess transmission risk must be used in conjunction with
interventions studies to structure decision when formulating hygiene codes. Since there is
little epidemiological data available on the impact of environmental interventions, IFH has
relied almost entirely on microbiological data coupled with known modes of infection
transmission to formulate hygiene codes for home and everyday life settings.
This report shows that using pooled data from intervention studies from different
communities to estimate disease reductions rates, can also be misleading. Hand hygiene
intervention data, as summarised in Table 4, for example, indicate that disease reduction
rates can vary significantly e.g., they suggest that the impact on GI diseases in developing
country situations may be as little as 26% up to as much as 79%. This could be due to
different methodologies and methodological issues, but could just as well be due to real
difference in the level of impact within and between study communities. Microbiological data
suggest that differences in outcome may relate to differences in the range of pathogens with
differing modes of spread prevalent in different study groups, which means that hand
hygiene has greater impact in some intervention groups than others. As stated by Eisenberg
et al. 2007 52 “the efficacy of any hygiene intervention strategy depends on the level of
pathogen exposure through other pathways. This may explain why some household water
quality interventions have shown disease reductions as high as 85% whilst others have
shown none”. For practices such as hand hygiene, it may also reflect differing levels of hand
hygiene compliance; the quality of the hygiene education, the approach to hygiene
promotion, and the enthusiasm with which it was received, may have given some
intervention groups a better understanding of what was required, with the result that they
were more likely to apply it at critical times or use better hand hygiene technique. As
discussed in Appendix 6, QMRA illustrates how, even a relatively modest increase in log
reduction on hands within a population, could produce a significant increase in the health
impact of a hygiene promotion campaign.
The microbiological data also shows that, although intervention studies assessing the impact
of hygiene measures on “pooled” GI or RT infection rates determined on the basis of nonspecific symptoms rather than identification of the causative agent may be the most cost
effective approach, results must be extrapolated with care. Microbiological data in Section
1.2.1 show, for example, that survival of influenza on hands is less than for rhinovirus and
RSV, which means that assessments of the impact of hygiene on RT infections, measured
on the basis of respiratory symptoms alone may not reflect the impact on spread of
influenza. The review of case-control studies as described in Appendix 5.1.1 suggests that,
to get any meaningful assessment of the impact of food hygiene practices in the kitchen,
data from food-borne infections must be separated from data on GI infections transmitted via
the faecal:oral route.
Viewed from another perspective, this review suggests that the quality of data obtained from
intervention and case-control studies could be significantly improved by taking account of
microbiological data in designing such studies. Preliminary data on the types of GI
pathogens circulating in the study community, for example, could give significant insights
into potential sources and routes of spread which could inform better design of the
intervention. This is particularly important in meeting the differing hygiene needs of low
24
income compared with high income communities, and developed compared with developing
country situations. Most of the microbiological data in this report come from studies in higher
income homes in developed countries. Microbiological data from settings in developing
country situations could, at relatively low cost compared with intervention studies, enable us
to better understand the similarities and difference between hygiene needs in these
situations. It should be noted that, on one hand, the largest amount of data on the efficacy of
handwashing comes from studies in developing countries, whilst the majority of
microbiological data comes from homes in developed countries. In recent intervention
studies of Sandora et al. 200837 and Bright et al. 2009,23 microbiological sampling during the
intervention, enabled the investigators to examine the relationship between diseases rates
and isolation of norovirus and influenza virus.
Other valuable sources of information about hygiene, which are sometimes overlooked, are
studies which examine the interaction between human behaviour and the behaviour of
pathogens. Over the past 20 years Griffiths and co-workers have carried out studies to
evaluate consumer behaviour during preparation of food in a domestic kitchen to identify
opportunities for cross contamination which can lead to infection. In a study reported in
2004 53 they used observational data indicating cross contamination behaviours in
conjunction with microbial sampling of surfaces and prepared foods in a domestic kitchen to
gain a better understanding of microbial risks associated with food-handling malpractices.
Thirty participants were asked to prepare a chicken salad meal using chicken pieces, 80% of
which were subsequently found to be contaminated with either Campylobacter or
Salmonella. Food safety behaviours were observed using CCTV and behavioural
malpractices were scored using a risk-based scoring system. The kitchen was sampled
immediately after participants had completed individual food preparation sessions. Most
samples were taken from pre-determined locations e.g., work surfaces and tap handles.
Other sampled locations were variables depending on observed behaviours during individual
food preparation sessions, for example, the number and types of chopping boards used or
hob controls/door handles touched after handling raw chicken. Observations enabled
identification of surfaces and/or materials that may have been directly contaminated from
raw chicken/raw chicken packaging or indirectly contaminated by hands that had been in
direct contact with raw chicken. Cumulatively, positive Campylobacter isolations were made
from 3 end-products, 3 surface wipers (a scourer and 2 dishcloths), a T-towel, a hand towel
and a Formica kitchen work surface. Using observational data, suspected routes of cross
contamination from positive raw chicken pieces were identified for each of the
Campylobacter positive sites. The presence of Campylobacter in 3 end-products was traced
back to hygiene errors. During preparation of salads, participants handled ready to eat (RTE)
ingredients or the assembled salad with potentially contaminated hands and also used the
same, inadequately decontaminated chopping board and/or knife for preparation of raw
chicken and then RTE salad ingredients. Fifty-six per cent of Campylobacter positive
samples taken after food preparation were dishcloths, T-towels and hand towels. These
materials were all placed on, or used to wipe surfaces in the model kitchen. A hand towel
and T-towel also became contaminated with Campylobacter after being used to dry
inadequately washed and unwashed hands. One dishcloth may also have been
contaminated with Campylobacter due to direct contact with a piece of raw chicken.
In a 2012 study Kennedy et al., 54 adopted the concept of the IFH targeted approach in order
to carry out a study to identify and prioritise critical points (CPs) in the home kitchen
environment during food preparation in order to inform food safety campaigns. The aim of
the study was to link observed consumer food safety practices in the home to food safety
knowledge, attitudes, perceptions, psychosocial and demographic factors to identify these
CPs. The study involved filming participants (n = 60) while they prepared a meal according
to a specified recipe (30 beef/salad burgers and 30 chicken salads), microbiological
sampling of key potential contamination sites in the participant’s kitchen, sampling the meat
25
and salad components of the meal for microbiological testing, visual inspection and
temperature check of the meat after cooking, and administering a survey of knowledge,
attitudes and demographic factors. The study confirmed the critical points (CPs) during
domestic food preparation as: CP1: correct cooking practices; CP2: prevention of crosscontamination; and CP3: correct food storage practices. Importantly statistically significant
links were found between food safety knowledge and behaviour as well as between food
safety attitudes and demographic factors.
SECTION 5. IMPLICATIONS
FOR FURTHER DEVELOPMENT OF TARGETED HYGIENE, AND FOR
DEVELOPMENT OF HYGIENE PROMOTION PROGRAMMES BASED ON TARGETED HYGIENE
In this section the data from microbiological, observational and intervention studies are
considered in relation to the future development of the IFH targeted approach to home
hygiene and its promotion as a means to reduce the impact of infectious disease.
In Sections 2-4, the IFH targeted approach to home hygiene is outlined and assessed. The
microbiological data in Appendices 1-4, however, show significant differences in the nature
of the infection risk within and between communities which means that what are considered
the “most risky practices” are likely to vary quite considerably from one region or one
community to another demanding different codes of hygiene practice according to the types
of pathogens prevalent in the community, access to adequate water and sanitation, climatic
conditions, social conditions and so on. Translating the concept of a risk management
approach into identifying priorities and developing codes of hygiene practice which meet the
needs of specific communities and deliver maximum heath benefit, requires consideration of
a number of factors as outlined in the following section. This relates not only to identifying
what are the most risky practices in that community, but equally importantly to how we best
get the community to change their behaviour and adopt new practices.
5.1 DEVELOPING AND PROMOTING HYGIENE CODES – A SINGLE OR MULTI-BARRIER APPROACH?
The adoption of risk management approaches dates from the mid-1900s when scientists in
the food, pharmaceutical and other industries recognised the need for a new approach to
controlling microbial contamination in products. They came to recognise that, because
pathogens are transmitted through a complex system of interdependent pathways, it was not
sufficient to implement processes such as handwashing or manufacturing plant cleaning as
single/isolated interventions. What was needed was an integrated system, in which the
major transmission routes, and the interactions between them, were identified – and an
integrated system of controls put in place to ensure that all major routes for transfer of
microbes into their products were controlled. This scientifically-validated system has now
become standard practice in a range of manufacturing settings.
More recently the US Institute for Healthcare Improvement (IHI) and other groups have
begun to adopt this type of approach by using “care bundles” as the optimum means to
reduce Healthcare Associated Infections (HAI). 55,56 These are defined by IHI as “bundles of
scientifically grounded elements (usually 3-5 practices) essential to improving clinical
outcome”. The concept is that several effective practices are used in combination in order to
have a greater impact on HAI rates compared to their individual use. Aboelela55 et al. argue
that “while the traditional view of causality dictates that a single cause leads to a single
effect, because of the multi-factorial nature of interventions to prevent HAI, the definition of a
‘single cause’ should be expanded to include a ‘set of interventions’ ”.
26
The debate about promoting hand hygiene, not in isolation but as part of a multi-barrier
approach in healthcare settings is reflected in a recent paper entitled “Control of
Transmission of Infection in Hospitals Requires More than Clean Hands” by Dr Stephanie
Dancer. She argues “Unfortunately, people do not always clean their hands when they
should, and even if they do, there are other factors that contribute to the acquisition of
infection”. 57 She concludes “Hand hygiene needs to be part of an integrated approach to
infection control. Given the costs, work required and time taken to increase compliance with
hand hygiene, it is arguable that other control interventions are easier to implement and to
maintain, and they produce equally good or better results more quickly. Because people will
not - or cannot - always clean their hands, let us engage managerial support for space, time,
isolation capacity, staffing, and sufficient cleaning of all hand-touch surfaces.”
The same arguments apply to home and everyday life settings, where focusing on single
interventions such as hand hygiene, respiratory hygiene, laundry hygiene etc. means that
the impact on disease rates depends on the level of compliance. In reality, the risk of
transmission via the hands, depends on the extent to which they become contaminated with
pathogens during normal daily activities which must increase as the extent of the
contamination of hand contact surfaces increases, which in turn depends on other factors.
Intuitively, although there is no supporting evidence, it would be expected that combined
hand and environmental hygiene will have a greater health impact than hand hygiene alone,
since hand hygiene compliance is always likely to be less than 100%. Taking the “care
bundles” approach, it could be concluded that the top 5 groups of environmental hand, food
and body contact surfaces, clothing etc., and baths, basins etc. identified in Figure 3 should
be regarded as a “set of integrated interventions” for the purpose of developing a code of
hygiene practice.
As far as food or respiratory or other hygiene practices areas concerned, it is well accepted
that this must involve a multi-barrier approach. Good food hygiene needs to be an integrated
set of actions related to safe cooking and safe storage of food, combined with prevention of
cross contamination either directly or via hands and surfaces, whilst respiratory hygiene
requires blocking coughs and sneezes, disposing of tissues/ handkerchiefs safely and
washing hands.
In all parts of the world, not only in healthcare but most particularly in public health, hand
hygiene is, for the most part, still promoted as a separate issue from other environmental
interventions such as food hygiene, surface hygiene, laundry hygiene etc., rather than as an
integral part of a multi-barrier approach. In some/many settings, as discussed below, this
focus on hand hygiene is justified. Public health planners, particularly in developing countries
where resources are limited, have to make difficult choices about which specific hygiene
practices to promote and logically, these should reflect the particular practices that are
putting health most at risk. This argument does not necessarily extend into other, more
prosperous regions of the world. Making choices about hygiene promotion programme
development must also take account of issues such as the educational and social status of
the community. Although the scientific data suggests that multi-barrier approaches are the
optimum way to reduce infectious disease, experience in the developing world, as outlined
below, suggests that behaviour change interventions work best when they focus on a single
or small number of hygiene behaviours.
5.2 BRINGING ABOUT BEHAVIOUR CHANGE
As stated above, the health impact from increased investment in hygiene promotion not only
requires the development of effective codes of hygiene practice based on sound scientific
27
principles, it is equally and critically dependent on persuading people to change their
behaviour and to sustain that behaviour change.
In comparison with trained industrial or healthcare personnel, where sanctions can be
applied for non-compliance, getting the general public to change their hygiene behaviour is
extremely difficult. In recent years, a significant amount of research has been done to
identify effective strategies for changing hygiene behaviour. The standard approach to
hygiene promotion in developing countries, whether through schools, clinics, or health
outreach programmes, has, until recently, been educational. Whereas those who manage
hygiene improvements still often choose to promote hygiene by educating people on the
links between hygiene and better health, one of the lessons that has been learnt, is that
traditional (cognitive) approaches can raise awareness, but do not necessarily achieve the
desired effects. This applies to both developed and developing countries.
A considerable amount of work is being carried out to evaluate the impact of different
approaches to achieving and sustaining behaviour change and is reviewed
elsewhere. 58,59,60,61,62,63,64,65 The various approaches that have been developed and are
being tested in developing countries are reviewed by Curtis et al. 66 These workers conclude
that “Though changing behaviour is difficult, we know a lot more about hygiene behaviour
than we did 10 years ago and promising approaches to changing hygiene on a large scale
are emerging”.
In developing countries, approaches which are being tested in low income communities
range from the use of social marketing techniques to promote “single” rule-based hygiene
messages on practices such as hand hygiene or respiratory hygiene, to community
mobilisation approaches based on engaging community participation and developing an
understanding of the need for and the principles of hygiene.
Community mobilisation, demand led, approaches:
In the past 2 decades an approach known as PHAST (participatory hygiene and sanitation
transformation) or the CHC (community health club) approach has become a predominant
model among non-government organisations. 67,68 The aim is to involve communities in
solving their own hygiene problems. This is mostly an educational approach and is heavily
reliant on the skills of trained facilitators, making it more difficult and costly to implement on a
large scale. Community mobilisation i.e., training community members in the technology and
reasons for use of HHWTSS methods, means involving the community so that they develop
a sense of commitment to, and ownership of, the project.
CLTS (Community led Total Sanitation) is another demand led approach, but is concerned
solely with the achievement of open defecation-free (ODF) communities and the practice of
handwashing with soap. 69 CLTS is essentially a “vertical” approach whereas the CHC
approach is “horizontal”, seeing the problem as a social issue. Unlike CLTS, the CHC
approach addresses a raft of health issues, from HIV/AIDS and malaria to pit latrines,
handwashing and refuse pits. The other difference is that, for CLTS, behaviour change is
brought about by using tried and tested techniques to elicit emotions such as shame,
embarrassment and disgust from villagers as they realise that by practising OD they are in
essence eating each other’s faeces. This realisation is designed to bring about a
transformation in the community who vow to come up with a plan to stop OD, usually
involving the construction of toilets from locally available resources.
In 2011, Whalley and Webster reported a study of the effectiveness and sustainability of the
two approaches in Zimbabwe. 70 Results showed that, despite little resistance to the idea, a
household’s ability to own a latrine depends heavily on affordability. Whilst both approaches
effectively encouraged measures that combat open defecation, only CHC’s witnessed a
28
significant increase in handwashing. However, CLTS proved more effective in promoting
latrine construction, suggesting that the emphasis the CHCs place on hygiene practices
such as handwashing needs to be coupled with the greater focus on the issue of sanitation
brought by CLTS.
Social marketing approaches
Research in low income communities by Curtis and co-workers63,66,71 has demonstrated the
effectiveness of hygiene interventions which focus on as few interventions as possible, with
simple rule-based messages. Key to this approach is communicating with the target
audience in a way that will motivate behaviour change. This involves techniques such as
social marketing – the use of marketing techniques to promote altered behaviours through
generation of demand. A review of 11 studies in Africa, Asia, and Latin America66 concluded
that, although there are local differences, common patterns exist. Three kinds of hygiene
behaviour were identified: habitual, motivated, and planned. Hygiene habits were learnt at an
early age, but soap use was rarely taught by parents or schools. Key motivations for
handwashing were disgust of contamination on hands and to do what everyone else was
perceived to be doing (social norms). Other motivations included comfort and nurturance
(the desire to care for one’s children). Planned handwashing, with the aim of preventing
disease, took place rarely. Mothers did not find the threat of diarrhoeal disease particularly
relevant and found the connection between handwashing and diarrhoea in children tenuous.
In 2010, a study was carried out by Sulabh International Academy of Environmental
Sanitation in collaboration with IFH South East Asia Office in order to better understand the
impact of perceptions and practices of hygiene in the home on reduction of disease burden
in respect of cholera, typhoid/enteric fever, diarrhea, hepatitis, worm infection, malaria/
dengue 72. The study was carried out in 5 Indian states namely Assam, Bihar and Jharkhand
& Orissa & West Bengal. The study showed that the level of awareness and perception of
public health and hygiene issues is a determining factor for hygiene behaviour and practice
in the community and that perception and practice of hygiene plays a role in reducing the
burden of communicable diseases. In addition it was shown that, when executed with an
awareness campaign on public health and, hygiene, provision of household toilets for safe
and sanitary disposal of human excreta, had a strong negative correlation with the burden of
communicable disease,
In developed countries, the factors which drive the development of hygiene promotion
programmes are very different from those in low income communities in developing
countries. One of the key factors in developing countries is the very high levels of endemic
diarrhoeal and helminth infection due to inadequate water, sanitation and environmental
conditions as well as hygiene. Clearly there is no clear demarcation between “developed”
and “developing” country conditions. The infection risks and hygiene needs for middle and
upper socio-economic groups in developing countries who have access to adequate water
and sanitation can be quite similar to those in developed countries, although the fact that
these communities can still have a higher level of endemic diarrhoeal disease needs to be
taken into account. This can result from exposure to faecal contamination of public water
supply systems, the overall soil and water pollution, and extremely low level of
environmental hygiene in the community. This means that hygiene promotion programmes
must be tailored to individual circumstances and factors such as access to clean water and
sanitation, and should be based on assessment of the local situation in relation to the type of
disease being targeted (diarrhoeal, respiratory, eye, skin etc.), the types of pathogens
prevalent in the community, climatic conditions, social conditions and so on.
However, some generalisations can be made as discussed in the following 2 sections.
29
5.3 DEVELOPED COUNTRIES – PROMOTING MULTI-BARRIER APPROACHES AND ACHIEVING
BEHAVIOUR CHANGE
The multi-barrier risk-based approach as outlined and assessed in Sections 2-4 has been
developed mainly on the basis of microbiological data generated in developed countries in
Europe and the US. As discussed in Section 4, the data indicate that, overall, the hands are
the single most important transmission route. A comparison of the microbiological data for
contact surfaces against the data for hands indicates that surfaces which come into contact
with our hands and body surfaces, and with food and water are also important risk factors or
control points. Clothing and household linens are also important risk factors, although the
risks are probably somewhat less than those associated with other contact surfaces.
Surfaces which come into contact with the body such as baths and hand basins can also
sometimes act as vehicles of infection, as can surfaces associated with the toilet.
In developing hygiene promotion programmes, the key question is – how big is the risk for
each of these “control points”? Or put another way, what is the health benefit from promotion
of any given hygiene practice. As discussed in Section 4, although we can make some
assessment using microbiological data to compare risks relative to hand hygiene as a
benchmark, there is no quantitative intervention data to allow us to determine which risks are
significant and should be included and which are insignificant and should be excluded.
Hygiene codes of practice must also, as discussed in Section 4, take account of the fact that,
although the microbiological data give us an assessment of the “daily life” risks associated
with these various sites and surfaces and the activities associated with them, they also show
that the risks are not constant, and can increase significantly under certain conditions. For
example, although risks from toilets, sinks, floors etc, relate mainly to the relatively low risk
of transfer from these sites to hands, hand and food contact surfaces and cloths, this risk
can increase substantially where an infected family member has fluid diarrhoea, or where a
floor surface is contaminated with vomit or faeces. Similarly, the risks of transmission via
clothing and household linens will increase where one family member has a skin or wound
infection. Risks are also increased in situations where there are family members living at
home who have reduced immunity to infection and may require special care to protect them
from infection.
Governments, under pressure to fund the level of healthcare that people expect, are looking
at disease prevention strategies as a means to reduce health spending. Increased homecare
is one approach to reducing health spending, but gains are likely to be undermined by
inadequate infection control at home. Healthcare workers are now increasingly looking for
support in developing and promoting codes of hygiene for the care of infected and
vulnerable groups in the home. Much of the care of risk groups in the home is done by family
members who thus require a good understanding of hygiene. The principles of hygiene for
protection of vulnerable groups or to prevent spread of infection from an index infected
person in the home, are no different from those of everyday hygiene. The major difference is
that if good hygiene practices are not followed the risk of infection is higher. One of the
reasons for this is that the infectious dose i.e., the number of bacterial or viral particles
needed to cause infection may be lower for those with reduced immunity to infection.
In developed countries, which enjoy access to adequate safe water and an effective means
of faeces disposal, infectious disease prevention priorities are very different from those in
low income communities where the overwhelming need is to focus on preventing diarrhoeal,
respiratory and trachoma infections. In recent years, developed countries have faced a
diverse range of issues which range from reducing the burden of foodborne infection through
control from “farm to fork”, to promoting respiratory hygiene as the means to reduce the
spread of pandemic respiratory viruses, to preventing cross infection from MRSA or C
30
difficile, to caring for vulnerable/at-risk groups in the home and community from infection. All
of these issues place a significant additional burden on the already overstretched health
budgets of developed nations, which could be reduced through adoption of better hygiene in
home and everyday life settings.
In the last 20 years we have seen significant investment across Europe in reducing the
burden of infectious diseases, not only with the establishment of ECDC, but also through
national hygiene promotion programmes. In the UK, for example, there has been extensive
investment in programmes to promote food hygiene at home. In 2009 we saw investment in
promotion of hand hygiene as a means to mitigate the spread of the pandemic H1N1
influenza strain. Although current thinking might suggest that the most effective way to
change hygiene behaviour is through single rule-based messages, the data in this review
suggest that, in developed countries, the complexity and shifting nature of the infectious
disease threat is such that a rule-based approach to hygiene is inadequate to meet current
public health needs. IFH also believes that the impact of hygiene promotion programmes on
the public is being weakened by the fact that the different aspects of hygiene are dealt with
by separate agencies which means that the information that the family receives is also
fragmented. If things are to improve we need a family centred (rather than an agency
oriented) i.e. an approach which looks at hygiene from the point of view of the family and the
range of problems they face in order to reduce infection risks, and provides them with an
integrated approach to home hygiene. This includes risks related to poor food and water
hygiene, poor personal hygiene (particularly hand hygiene), respiratory hygiene, hygiene
related to clothing and household linens, and hygiene related to the general environment
(toilets, baths, hand basins, surfaces etc.). It also includes hygiene related to care of
domestic animals, and to family members at increased risk of infection. It also includes risks
associated with unsafe disposal of faeces and refuse.
The need is for an approach founded on awareness of the chain of infection transmission
and how it differs for different groups of infections. Hygiene education needs to be
consistently incorporated as part of hand hygiene promotion programmes, if people are to
properly understand the risks, and adapt their behaviour accordingly. At the very least we
must ensure that the principles of infectious disease transmission and hygiene are part of
the school curriculum. In line with this, the EU-funded e-Bug project (http://www.e-bug.eu/) is
working to roll out education on antibiotic resistance and hygiene at primary and secondary
school level across Europe.65,73
5.4 DEVELOPING COUNTRIES – PROMOTING SINGLE AND MULTI-BARRIER APPROACHES AND
ACHIEVING BEHAVIOUR CHANGE
In developing countries, the issue of single versus multi-barrier approaches to infectious
disease prevention is a matter for considerable debate – at 2 levels
Firstly in relation to whether, and to what extent, programmes to improve water in the
absence of programmes to improve sanitation are effective in reducing diarrhoeal disease.
On one hand, using modelling approaches, Eisenberg and co-workers 200752 argue that,
when sanitation conditions are poor, water quality improvements are likely to have minimal
impact regardless of amount of water contamination. They conclude that, if each
transmission pathway alone is sufficient to maintain diarrhoeal disease, single-pathway
interventions will have minimal benefit, and ultimately an intervention will be successful only
if all sufficient pathways are eliminated. On the basis of a Cochrane review of 38 trials of
water quality interventions for preventing diarrhoea involving more than 53,000 persons from
19 countries over 20 years, Clasen, Cairncross and co-workers however concluded that
31
“pooled estimates of effect showed that water quality interventions were effective in settings
without “improved” sanitation. 74
Secondly, in the past 10 years or so, significant investment has been made to integrate
“hygiene promotion” into programmes aimed at providing improved water and a means of
safe faeces disposal to low income communities in developing countries. In these situations,
the focus of hygiene promotion has been on the promotion of hand hygiene on the basis that
this is the single most important intervention which, based on intervention study data, can
produce up to 50% or more decrease in diarrhoeal disease rates and up to 23% reduction in
respiratory infections. The extent of the emphasis on hand hygiene means that in some
circles, hygiene is considered as synonymous with handwashing.
In developing countries, where investment in hygiene promotion is now recognised as a vital
component, alongside provision of adequate water and sanitation, hand hygiene is being
promoted as a single issue, rather than as an integral part of a multi-barrier approach to
infection prevention i.e. an approach which also involves food hygiene, respiratory hygiene
etc. To an extent, as discussed above, this focus on hand hygiene is justified; public health
planners, particularly in developing countries where resources are limited, have to make
hard choices about which specific hygiene practices to promote and logically, these should
reflect the particular practices that are putting health most at risk.
Until recently there has been little or no data to suggest whether the risks associated with
other interventions such as surface hygiene, laundry hygiene and so on, relative to those
associated with the hands are the same or different from those in developed countries. Until
recently the microbiological data has come almost exclusively from developed countries,
most particularly the US and Europe. New data is now emerging which suggests that this
may not be the case. Thus, for example, recent data such as that produced by Sinclair and
Gerba51 suggest that surfaces may be more important than in developed countries even in
homes where there is access to improved water and sanitation. In their 2010 study of
environmental contamination in homes in Cambodia, Sinclair and Gerba showed that levels
of faecal and faecal indicator bacteria were up to 2 logs higher than in equivalent situations
(sites and surfaces) in homes in the US and Japan, despite the fact that the Cambodian
homes had a pour-flush latrine for disposal of faeces. From this, they concluded that “these
results indicate that a latrine barrier alone is only partially effective for household sanitation.
For complete sanitation, multiple environmental barriers may be necessary”. When
compared to homes in Cambodia, homes in industrialised countries have a range of
additional environmental barriers that may control surface contamination including
chlorinated water distribution systems, solid waste disposal systems, more elaborate home
construction with easily washable surfaces, and cleaning product availability. Homes in
these countries also have indoor climate control systems and lower relative humidity than
tropical Cambodia. Sinclair and Gerba propose that efforts should be made to include as
many pathogen control points as possible in hygiene and sanitation improvement
programmes.
At the very least, these data indicate that more studies should be carried out to better
understand the role of the environment most particularly in situations where faecal
contamination of the environment is likely to be higher due to higher incidence of diarrhoeal
disease and lower standards of sanitation, and how this may contribute to transmission via
the faecal:oral route or via food.
To explore these issues further, Eisenberg and co-workers 75 have developed a model which
uses microbiological data to evaluate the health impact of not only single but also multiple
environmental hygiene interventions to prevent person-to-person transmission. The model
describes the dynamics of human interaction with pathogens in the environment in relation to
32
factors such as physical proximity, microbe pick-up rate, pathogen elimination rate,
deposition rate and social encounters. These insights provide theoretical contexts which
could be used to examine the role of the environment in pathogen transmission and a
framework to interpret environmental data in order to inform hygiene interventions.
5.5 IFH – DEVELOPING CODES OF HYGIENE PRACTICE FOR DEVELOPED AND DEVELOPING
COUNTRY SITUATIONS
Over the past 10 years, IFH has used the targeted approach to produce a code of hygiene
practice for the home, and to produce a series of guidelines and training resources for use
by community healthcare workers in both developed and developing countries (see Table 1).
The IFH “Guidelines for Home Hygiene” are based on a multi-barrier approach and give
detailed guidance on all aspects of home hygiene including food hygiene, general hygiene,
personal hygiene, care of pets, care of vulnerable groups and those who pose an infection
risk to others. In turn, using the guidelines and recommendations as the basis, IFH (in
collaboration with the UK Infection Prevention Society and the Water Supply and Sanitation
Collaborative Council) has also produced teaching resources on home hygiene (2 editions
are available one of which focuses on the developed world, the other on issues in
developing countries) which present home hygiene theory and practice in simple practical
language which can be understood by community workers with relatively little infection
control background. All of these materials are downloadable from the IFH website.
The primary aim of these materials is to give healthcare workers a basic understanding of
how infections are transmitted in the home, and the principles of a multi-barrier approach to
breaking the chain of infection transmission through good hygiene practice. The training
resource for use in developing country situations also addresses the problem of adapting
hygiene promotion programmes in order to meet local needs and constraints.
Table 1 – IFH guidelines, recommendations and training resources on home hygiene
Guidelines on home
Guidelines for prevention of infection and cross infection in the
hygiene
domestic environment. 76
Guidelines for prevention of infection and cross infection in the
domestic environment: focus on issues in developing countries.21
Recommendations for Recommendations for selection of suitable hygiene procedures
selection of hygiene
for use in the domestic environment. 77
procedures
Teaching/self-learning Home Hygiene – prevention of infection at home: a training
resources
resource for carers and their trainers. 78
Home Hygiene in Developing Countries: prevention of infection
in the home and peridomestic setting. A training resource for
teachers and community health professionals in developing
countries.20
SECTION 6. CONCLUSIONS AND RECOMMENDATIONS
Microbiological and other data reviewed in this report show that pathogens are constantly
being shed or spread from human, animal, food and water sources in home and everyday
life settings, and are transmitted via the hands and via environmental sites and surfaces etc.
such that people become exposed and infected. It is now well accepted that reducing the
infection risk is not achieved by trying to eliminate infectious agents from our environment.
33
Not only is this unachievable, it is also undesirable. The optimum approach is to focus on
breaking the chain of infection transmission by intervening at “critical points” in the chain.
This maximises protection against infection exposure whilst disturbing our human and
natural environment to the least extent. This is the basis of the “targeted” approach to home
hygiene developed by IFH during 1997 to 2000 using the microbiological evidence available
at the time.
IFH – Advocating increased investment in hygiene promotion
Governments worldwide are under considerable pressure to fund the level of healthcare that
people expect, and are more and more looking to disease prevention strategies, including
the promotion of hygiene, as a means to reduce health spending. This is particularly so in
developing countries, where there is growing awareness of the need for more investment in
hygiene promotion alongside programmes to provide improved water and sanitation in order
to reduce the unacceptable burden of diarrhoeal disease. Hygiene is now recognised as a
means to reduce the spread of respiratory diseases, and is a component part of pandemic
influenza preparedness plans. It is also recognised as a key strategy for reducing the impact
of antibiotic resistance. Healthcare workers now accept that reducing the burden of infection
in healthcare settings cannot be achieved without also reducing the circulation of pathogens
such as norovirus and MRSA in the community. For the Transatlantic Task Force on
Antimicrobial resistance (TATFAR) one of the 3 component strategies for tackling antibiotic
resistance is “Prevention of both healthcare- and community-associated drug-resistant
infections“. 79 Hygiene provides a means to reduce the “silent epidemic”, which is the spread
of MRSA, and ESBL and NDM-1-producing gram negative strains in the community. As
persistent nasal or bowel carriage of these strains in the healthy population increases, this
increases the risk of infection with these strains in both hospitals and the community.8,80, 81
Milstone et al. 2012, 82 for example, have shown that MRSA colonization is a risk factor for
subsequent MRSA infection. Admission prevalence of MRSA colonization among 3140
children admitted to a paediatric care unit was 4.9%. Nearly 10% of children with MRSA
colonization or infection on admission to the intensive care unit developed a later MRSA
infection, most often after hospital discharge. Cotter et al. 2012 83 demonstrated the potential
for acquisition of antibiotic resistant strains in healthcare workers and ongoing possibility of
cross-transmission to household contacts. The report describes a case of ESBL-producing
E. coli bloodstream infection in a healthcare worker associated with subsequent isolation of
an indistinguishable strain from one causing a urinary tract infection in his spouse.
What is needed, however, is translation of awareness into action. To achieve this, a number
of issues need to be addressed:
• If we are to sustain high level protection against infectious disease, in the face of
changing demographics and microbial evolution, we must recognise that the
responsibility for hygiene must be shared by the public. To achieve this, we need an
integrated family-centred approach to hygiene promotion, co-ordinated by a single
agency. In most countries worldwide, public health is currently structured such that the
separate aspects of home and everyday life hygiene – food hygiene, personal hygiene,
handwashing, safe water, pandemic flu preparedness, patient empowerment etc. – are
dealt with by separate agencies. There is a need for the various agencies to work in
partnership in order to promote an approach to hygiene which is family-centred rather
than issue-oriented.
• If things are to change we must recognise that fragmented, rule-based knowledge is
not enough to meet the challenges we face. Hand hygiene, for example is a central
component of all hygiene issues and it is only by adopting a holistic, integrated
approach that the causal link between e.g. hands and infection transmission in the
home can be properly addressed. Where resources and socio-economic conditions
allow, at the very least we need to ensure that the principles of infectious disease
34
transmission and the role of hygiene are part of the school curriculum. What works
best is likely to depend on a whole range of factors including socio-economic and
educational status, and the resources available. This is particularly so in developing
countries.
• If hygiene promotion is to attract public and private investment, there is a need for
more data to enable health agencies to assess the health gains from investment in
hygiene promotion relative to other preventive measures (e.g., immunisation
programmes). A key driver to the successful establishment of the Global Public Private
Partnership on Handwashing was the quantitative data showing the health gains from
promotion of handwashing with soap in low income communities. In order to argue the
case for an integrated approach to hygiene promotion, there is a particular need for
intervention study data assessing the health impact (and health cost savings) of an
integrated set of interventions based on targeted hygiene over and above that
achieved by handwashing alone. Although it is probably not possible to measure the
impact of handwashing and environmental hygiene separately (i.e., an intervention
promoting environmental cleaning without hand hygiene would not be feasible or
ethical), the 2002 US home study (238 households, 48 weeks) by Larson et al..50 and
the 2007 household study in South Africa by Cole et al.36 (685 households, 6 months)
demonstrate the feasibility (i.e., sufficient statistical power to yield meaningful results)
of doing a comparative intervention study measuring the impact of hand hygiene, and
the incremental effect of targeted environmental hygiene over that achieved by
handwashing alone.
• If the health benefits from hygiene promotion are to be realised, one of the key aspects
is persuading people to change their behaviour.
In developing and promoting hygiene practice, the issue of sustainability must also be
addressed. A 2010 IFH report 84 shows that the IFH targeted hygiene approach provides a
framework for building sustainability into hygiene because it minimises the life-cycle impacts
of hygiene processes, maximises safety margins against any hazards of their use, and
minimises any risks of the development antibiotic resistance from exposure to biocides. It
also looks to sustain “normal” interaction with the microbial flora of our environment.
35
APPENDICES
1. MICROBIOLOGICAL
ASSESSMENT OF THE SOURCES, DISPERSAL, PERSISTENCE AND
SPREAD OF MICROBES IN THE DOMESTIC ENVIRONMENT
1.1 CHAIN OF TRANSMISSION OF INFECTIOUS GASTROINTESTINAL DISEASE
Within the home, the primary sources by which enteric pathogens are introduced into this
setting are people, food and water, pets and to a certain extent (particularly in tropical
countries) insects. Additionally, sites where stagnant water accumulates, such as sinks, Ubends, toilets and cleaning cloths, can support microbial growth and become a primary
reservoir of infectious agents. Gl infections can occur by eating contaminated food that has
not been properly cooked, or has been incorrectly stored, or by drinking contaminated water.
Food and water can be contaminated at source outside the home, but can also become
contaminated in the home, either by contact (handling) with contaminated hands or by
contact with contaminated surfaces.
Alternatively, GI infections can occur by direct hand to mouth transfer of infectious agents
that are transmitted via hands or environmental surfaces. For some infections e.g. norovirus
infection can occur by inhalation of particles of infected vomit.
Infectious agents spread via these routes include bacterial strains such as Salmonella,
Shigella, Campylobacter, E. coli (including E. coli O157 and E. coli O104) and Helicobacter
pylori, viral strains such as norovirus, rotavirus, adenovirus and astrovirus, and
Cryptosporidium. Although Cryptosporidium infections are generally assumed to be
waterborne, there is evidence of person-to-person transmission in household settings. 85 The
risk of exposure to enteric pathogens in home and everyday life settings, as illustrated in
Figure 1, depends on the extent to which these pathogens are brought into the home and
the extent to which they are spread via hands and other sites and surfaces, and by airborne
transmission.
Data showing the extent to which enteric pathogens are introduced into the home, remain
viable and infective, and circulate around the home comes from various sources and is
summarised below. Taken together, it suggests that exposure to enteric pathogens via the
hands, surfaces and food is a frequent occurrence during normal daily activities, and that the
numbers of organisms transferred by hand-to-mouth contact (or into ready-to eat foods or
water) can be well within the numbers required to cause infection.
1.1.1. Sources of enteric pathogens in the home
Food as a source of enteric pathogen in the home
Pathogenic micro-organisms are ubiquitous throughout nature and are frequently found on or
in raw foods. Pathogens brought into the home on raw or processed food include Salmonella,
Campylobacter, Listeria and E. coli O157. A variety of foods can act as a source of these
organisms including meat, fish and poultry products, dairy products, fruits and vegetables.
Using data from 18 OECD countries, a 2003 World Health Organization (WHO) report
concluded that about 31% of reported food-borne outbreaks occur in private homes. 86 The
potential for food poisoning at home is indicated by the prevalence of food-related pathogens
in products purchased from retail premises:
36
• The 2010 EFSA report based on data reported back from EU countries in 2008 87
indicates that Campylobacter is mostly found in raw poultry meat with a reported
average of 30.1% of samples showing contamination. The highest proportion of
Salmonella-positive units was reported for fresh broiler meat, turkey meat and pig
meat, on average at levels of 5.1%, 5.6% and 0.7%, respectively. A prevalence study
conducted among broilers in Malaysia indicated that 35.5% of broiler carcasses
obtained from wet-markets and 50.0% from processing plants were contaminated with
Salmonella. 88 High rates of Salmonella spp. contamination were detected in fresh
samples of chicken carcasses from butcheries, while increased Campylobacter spp.
levels were detected in fresh supermarket samples in another study by Van Nierop et
al. in South Africa. 89 A 2000-2005 United States (US) survey on Salmonella enterica
serotype Enteritidis in broiler chicken carcasses showed that the annual number of
isolates have increased by more than 4-fold and the proportion of establishments with
Salmonella enteritidis-positive samples has increased by nearly 3-fold. Case control
studies from the US and England identify consumption of chicken as a risk factor for
sporadic human Salmonella enteritidis infection. 90
• Luber et al.(2007) analysed 100 retail chicken breast fillets for surface contamination
and 55 fillets for internal contamination. Prevalence was 87% on the surface and 20%
in the deep tissue. The mean number of Campylobacter on the surface was 1903
colony forming units (CFU) (median 537cfu, maximum 38,905cfu). Internal counts
were <1 cfu/gram meat. Given the high numbers of the pathogen on the chicken
surface, they concluded that cross-contamination during preparation of contaminated
chicken is a more important pathway for exposure to Campylobacter than eating
undercooked meat. 91
• A 2005 UK study of 3,662 prepackaged raw meat samples from retail premises showed
that the external packaging of raw meats is also a vehicle for potential crosscontamination by Campylobacter, Salmonella and E. coli. These could potentially cross
contaminate ready-to-eat foods during and after purchase in consumers’ homes. 92
• Chapman et al. showed that 0.4-0.8% of meat products purchased from butchers in
the United Kingdom (UK) were positive for Escherichia coli O157. 93
• E. coli O157:H7 was recovered from 2.8% samples of minced beef and beef burgers
from butcher shops and supermarkets in the Republic of Ireland. Fresh packaged
burgers from supermarkets had the highest prevalence of 4.5%, while fresh
unpackaged mince had the lowest prevalence of 2%. 94
• In a 2007 study in Canada, C. difficile was isolated from 20% of 60 samples of retail
ground meat purchased over a 10-month period, and 11 of the isolates were
toxigenic. 95
• A 2010 study by Weese et al. conducted across Ontario, Canada, was the first to
report C. difficile contamination in retail chicken meat. All isolates of C. difficile (26 of
203 chicken samples) were ribotype 078, a strain that has been associated with food,
animals and potentially community-associated disease in humans. 96
• The food chain can also be a route for transmission of noroviruses. GIII (bovine), GII.18
(swine), and GII.4 (human) norovirus sequences have been isolated from animal faecal
samples demonstrating that GII.4 –like strains can be present in livestock. 97
• Van loo et al. 98 identified 36 S. aureus strains in 79 meat samples. Two meat samples
(2.5%) contained MRSA. S. aureus is found regularly in low amounts in meat sold to
the consumers. This study demonstrates that MRSA has entered the food chain.
Persoons et al. in a 2009 study also confirmed the presence of MRSA in broiler
chickens in Belgium. The number of positive samples varied between 20% and 100%.
Interestingly, from the 1 MRSA-positive farms that was sampled twice, MRSA was
isolated on both occasions. This indicates that MRSA may persist on a farm and
colonize future flocks. 99 Van Loo et al. concluded that, as the amounts of MRSA
isolated were low, it is not likely to cause disease, but contamination of food products
37
may be a potential threat for the acquisition of MRSA by those who handle the food.
Despite this, an outbreak of community-acquired foodborne illness caused by MRSA
has been reported. This report by Jones et al. showed that a food handler in a
delicatessen, an asymptomatic carrier of the same strain of MRSA, probably
contaminated the food. The person may have acquired the MRSA strain during visits
to a nursing home prior to the outbreak, demonstrating the spread of MRSA into the
community. 100
Water as a source of bacterial infections in the home
In developing countries, lack of access to clean water is still a significant problem. In 2008,
WHO/UNICEF 101,102 reported that, in the last few years, the situation has significantly
improved and that for the first time since data were first compiled in 1990, the number of
people globally who lack access to an improved drinking water source has fallen below 1
billion. The WHO/UNICEF joint monitoring group101,102 assess that the percentage of people
served with an “improved water supply” worldwide has now reached 87%. Overall, 54% of
the world’s population now has piped water on the premises (piped household connection
located inside the users dwelling, plot or yard). The WHO/UNICEF report, however,
highlights large disparities within national borders, particularly between rural and urban
dwellers. Water supply quality depends on factors such as the quality of the raw water
source, the extent and type of treatment used, the integrity of the distribution system and the
maintenance of positive pressure within the network.
In general, it is assumed that community water supplies in developed countries are safe.
This is not necessarily the case, 103 particularly in regions of Europe where political and
economic upheaval have led to infrastructure deterioration. Additionally, whereas towns and
cities of Europe are generally well supplied, many rural populations still rely on small private
supplies, where contamination risks are higher. In situations where water quality is
consistently poor, or in emergency situations (e.g., where outbreaks of Cryptosporidium
occur as a result of breakdowns in the water treatment or distribution system), point-of-use
water treatment within the home is necessary if GI infections are to be prevented.
Contamination of domestic water supplies and the burden of waterborne disease is reviewed
in more detail in a 2005 IFH report.5
In addition to risks from consumption of contaminated water, waterborne pathogens can be
transmitted in the home. Water can easily become contaminated by unsafe consumer
storage and handling practices at home. This can happen when water has to be collected
from a communal source. This water is stored in containers of various designs and often, is
not protected from subsequent contamination during use, and/or water storage containers
are not cleaned before refilling. 104,105,106 The extent and causes of contamination of
household drinking water are reviewed by Sobsey 107 and Wright et al. 108
Humans as a source of pathogens in the home
Household members who are, or have been recently infected, or who are persistent carriers,
are a primary source of GI infection in the home. Enteric pathogens which can be carried
persistently by otherwise healthy people include Salmonella and C. difficile. Other enteric
pathogens which are spread in the home from infected people include E. coli O157 and
O104, Campylobacter, norovirus, rotavirus etc. Studies carried out in Germany and France
in 2011 report on secondary transmission of E. coli O104 within the family. 109, 110 People that
carry enteric pathogens shed large numbers of organisms in their faeces, or when they
vomit:
• A single vomiting incident following norovirus infection may produce 30 million viral
particles, 111 whilst, at the peak of a rotavirus infection >1011 virions may be excreted
per gram faeces. 112 Atmar et al. evaluated the magnitude and duration of shedding in
38
faeces of persons experimentally infected with norovirus. Shedding was detected 18
hours after infection and lasted a median of 28 days. The median peak shedding was
95 x 109 (range 0.5-1, 640 x 109) genomic copies/gram faeces. 113 Aoki et al. in a 2010
study suggested that precautions should be taken for at least 14 days after onset of
symptoms. 114
• Gibson et al. 115 review data which suggests that the number of particles of adenovirus,
rotavirus and hepatitis A virus shed per gram of faeces is approx. 1010-1011 cfu/g,
whilst for Shigella, the number of organisms shed reportedly ranges from 105-109 cfu/g
of faeces. If infection is asymptomatic, the average number is typically between 102
and 106 cfu/g. Although the average duration of Shigella infection is a week, one study
suggests that 7% of infected persons may shed the organism for more than 1 year. 116
As discussed below, surfaces in the home may become contaminated by enteric organisms
such as norovirus that are aerosolized during vomiting or by transfer of vomitus and fecal
matter from hands to surfaces. Viruses aerosolized from flushing the toilet can remain
airborne long enough to contaminate bathroom surfaces. 117
Although there is a tendency to assume that GI infections are the result of eating
contaminated food or drinking contaminated water, it is increasingly recognised that a
substantial proportion of the total GI infection burden in the community is due to person-toperson spread within households, particularly for viral infections such as norovirus. Personto-person transmission in the home can occur by direct hand-to-mouth transfer, via food
prepared by an infected person, or by transmission due to aerosolised particles resulting
from vomiting or fluid diarrhoea. Evans et al.(1998) 118 reported that, whereas 174 out of 233
outbreaks of infection in the UK attributed to Salmonella were “mainly foodborne” and 15
regarded as “mainly person-to-person”, for 680 reported outbreaks of norovirus infection,
607 were attributed to person-to-person transfer and only 21 were reported as foodborne. In
a more recent study of data from 4083 outbreaks, Le Baigue et al.(2000) 119 suggested that
19% of Salmonella outbreaks were transmitted by other means and fewer than half of E. coli
O157 outbreaks were foodborne. Friedich (2011) reviews data which shows the potential for
transmission of Enterohaemorrhagic Escherichia coli (both O104 and O157) arising from
household transmission. 120
The risk of exposure to GI pathogens from a human source depends on the extent to which
they are circulating in the community. Surveillance data gives some indication of incidence
and prevalence, but it is well accepted that GI diseases are under-reported. National
surveillance systems mostly focus on foodborne disease which means that non-foodborne
infections circulating in the community are under-reported. The prevalence of GI infections
circulating in the community is illustrated by two large community studies in the UK 121 and
The Netherlands. 122 The UK study, carried out between 1993 and 1996, estimated that only
1 in 136 cases of GI illness is detected by surveillance and that, for every one reported case
of Campylobacter, Salmonella, rotavirus and norovirus, another 7.6, 3.2, 35 and 1,562
cases, respectively, occur in the community. The UK study indicated that up to 1 in 5 people
in the UK population develop IID each year (an estimated 9.4 million cases) of which about
50% is non-foodborne.121,123 Although it is not possible to obtain proof since the sources of
these cases was not investigated, the most obvious conclusions are that a significant
proportion relate to community settings including the home. The Netherlands122 study
estimated that about 1 in 3.5 people experience a bout of GI infection each year. A 2007
report of food and non-foodborne outbreaks in Germany 124 suggested that the most common
settings for outbreaks are households (53%); of 14,566 outbreaks, 5,400 were attributed to
person-to person spread, 1637 to food, and 85 to water.
39
Indications are that norovirus is now the most significant cause of GI infection in the
developed world. 125 Rotavirus is the leading cause of gastroenteritis in children under 5
years of age. 126 Parashar et al. 127 estimate that, globally, each year, rotavirus causes
approx. 111 million episodes of gastroenteritis in children less than 5 years of age. Hepatitis
A virus is common worldwide, 128 whilst adenovirus is also a frequent cause of gastroenteritis.
C. difficile-associated intestinal disease occurs with increasing frequency in the community,
where it mostly affects home-based patients, but occasionally affects healthy individuals.8
Over 80% of cases are in the over-65 age group. Carriage rates in healthy people in the
community may be around 3 up to 5%. 129,130,131 Although there are no data to indicate what
proportion are carriers of toxin-producing strains, indications are that the numbers which are
toxin producers has increased. 132,133 Release of spores is easily accomplished as C. difficile
causes explosive diarrhoea; it is estimated that infected patients excrete over 100 C. difficile
per gram of faeces. 134
Pets, domestic animals etc as a source of GI pathogens in the home
More than 50% of homes in the English-speaking world have cats and dogs. Chomel et al.
201116 review data which shows that in the US, >60% of households have pets; pet
ownership increased from 56% in 1988 to 62% in 2008. In the UK, an estimated 6.5 million
dogs live in ≈25% of households. In the Netherlands, the pet population is ≈2 million dogs
and 3 million cats, the percentage of households with pets increased from 50% in 1999 to
55% in 2005. In France, the estimated pet population is ≈8.1 million dogs in 25% of
households and ≈9 million cats in 26% of households, with the number of dogs increased
from ≈4 million in the late 1950s to its current 8.1 million.
In the US, up to 39% of dogs may carry Campylobacter, and 10-27% may carry
Salmonella; 135 cats are also carriers of these organisms. Carriage of C. difficile in household
pets is common; 136 up to 23% of household pets are affected, although carriage appears to
be transient and not associated with IID. The extent of the problem is shown by a number of
recent studies:
• Fredriksson-Ahomaa et al.(2001) demonstrated that raw pork can be a source of
Yersinia enterocolitica: 3 infections in dogs and cats. Pathogenic isolates can cause
enteritis in dogs and cats, but pets can also shed this organism in the faeces for
several weeks after infection. Carrier animals may be a source of infection, especially
for young children, due to their close contact with humans. 137
• Transmission of cryptosporidium from pets has been recorded. 138 A study in
Indonesia showed that 13 (2.4%) of 532 cats passed C. parvum oocysts. 139
• Lefebvrea et al.(2006) 140 evaluated the prevalence of zoonotic agents in a group of 102
dogs from a variety of sources across Ontario, Canada, and zoonotic agents were
isolated from 80 of 102 (80%) animals. The primary pathogen was C. difficile, which
was isolated from 58 (58%) faecal specimens; 71% (41/58) of these isolates were
toxigenic. The authors also reviewed reports from the US and Australia indicating
asymptomatic carriage in the canine population between 0-37%.
• People in close contact with farm animals are at risk of animal-to-human transmission
of Salmonella Typhimurium DT104A variant. Salmonella enterica serovar Typhimurium
was isolated from a pig, a calf, and a child on a farm in The Netherlands. The isolates
were indistinguishable by phenotyping and genotyping methods, which suggested nonfoodborne animal-to-animal and animal-to-human transmission. 141
• Feeding raw meat to dogs may have an impact on the faecal prevalence of several
enteric bacterial zoonotic pathogens. Lenz et al. isolated Campylobacter jejuni from
2.6% of raw meat-fed dogs and Salmonella enterica from 14% of raw meat-fed dog
faeces. Salmonella enterica was recovered more frequently in the vacuum cleaner
waste samples from households with raw meat fed dogs than from those where raw
meat was not fed to dogs (10.5% versus 4.5%). 142
40
• Jhung et al. 2008 observed that there has been a rise in toxinotype V strains of C.
difficile from <0.02% before 2001 to 1.3% in 2006. Community-associated CDAD was
identified in 46.2% case-patients. Molecular characterization showed a high degree of
similarity between human and animal toxinotype V isolates. 143
• A review by Tsiodrasa et al. shows that human pathogens can be associated with wild
and migratory birds. Indirect transmission to humans has been reported for some of
these such as E. coli and Salmonella spp. The authors conclude however that the
available evidence suggests wild birds play a limited role in human infectious diseases.
Direct transmission of an infectious agent from wild birds to humans is rarely
identified. 144
• Fielder (2010) reviews the infection risks related to touching animals during visits to
open farms zoos etc. 145
• Behravesh et al. 2010 146 investigated an outbreak of Salmonella Schwarzengrund,
primarily affecting young children, in which 79 case-patients in 21 US states were
identified; 48% were children aged 2 years or younger. Case-households were
significantly more likely than control households to report dog contact and to have
recently purchased manufacturer X brands of dry pet food. Illness among infant casepatients was significantly associated with feeding pets in the kitchen. The outbreak
strain was isolated from opened bags of dry dog food produced at plant X, fecal
specimens from dogs that ate manufacturer X dry dog food, and an environmental
sample and unopened bags of dog and cat foods from plant X.
The increasing popularity of exotic pets also increases the risk of humans acquiring zoonotic
infections. 147 Human salmonellosis associate with exposure to exotic pets is reviewed by
Woodward et al. 1997. 148 From a review of the period from 1993 to 1995, they estimated that
3-5% of 20,000 laboratory-confirmed human cases of salmonellosis in Canada were
associated with exposure to exotic pets. Case:control studies assessing the Salmonella
infection risks associated with turtles, reptiles, ducklings etc. are reviewed in section 5.1.1.
Although there is significant evidence that domestic pets have the potential to act as a
source of infection in the home, there is little data indicating the extent to which this may or
may not occur.49,149 In their 2011 review Chomel et al. 201116 report that in the US, 56% of
dog owners sleep with their dog next to them. They also review a study in the Netherlands
showing that among 159 households with pets, 50% of pet owners interviewed allowed the
pet to lick their face; 60% of pets visited the bedroom; 45% of dogs and 62% of cats were
allowed on the bed; and 18% and 30% of the dogs and cats, respectively, were allowed to
sleep with the owner in bed. A study in France reported that ≈45% of cat owners and ≈30%
of dog owners slept with their pet.
In a 2008 UK study, Westgarth et al. investigated the dog-human and dog-dog interactions
among 260 dog-owning households. It was found that contacts were highly variable and
were affected by the size, sex and age of the dog, individual dog behaviours, human
behaviours and human preferences in the management of the dog. The authors identified a
number of situations that may be important in relation to zoonoses such as sleeping areas,
playing and greeting behaviours, food sources, walking, disposal of faeces, veterinary
preventive treatment and general hygiene. 150
Insects as a source of pathogen in the home
Domestic flies are accepted vectors of diarrhoea-causing pathogens. Several studies have
examined the impact of fly control on the incidence of diarrhoea. Cohen et al.(1991) 151, in a
study carried out at a military base in Israel, demonstrated that houseflies can transmit
Shigella diarrhoeal infections by acting as a mechanical vector. Shigella was isolated from a
proportion of flies. After implementation of fly control measures, the prevalence of houseflies
41
was greatly reduced. Soldiers at bases where fly control measures were implemented had
significantly less diarrhoeal disease and shigellosis.
In Gambian villages, the control of muscid flies resulted in 75% fewer new cases of
trachoma in intervention villages than in control villages. In the villages with fly control, there
was also 22% less childhood diarrhoea in the wet season and 26% less in the dry season
than in the control villages. 152 In a study in Pakistan, the incidence of diarrhoea was lower
(23% reduction) in villages sprayed with insecticide than in unsprayed villages. 153
1.1.2 Survival and spread of gastrointestinal pathogens in the home
The potential for exposure to GI pathogen shed or spread into the home or other
environments from a human, animal, food or other source is shown by a whole range of
laboratory and field studies which demonstrate the extent to which environmental
persistence and spread of enteric bacteria and viruses can occur during preparation of food
in the domestic kitchen and during other normal daily activities.
Although drying of inanimate surfaces has a microbicidal effect, there is a significant amount
of data from laboratory studies, as reviewed by Kramer et al., 154 and Rzezutka and Cook 155
(see in Table 1) showing that enteric pathogens can survive in significant numbers for
several hours, and in some cases, days and weeks, particularly on moist, but also on dry
surfaces. In a separate study, Cryptosporidium oocysts have been shown to survive on
soiled environmental surfaces for at least 2 days. 156
Table 1 – Persistence of gastrointestinal pathogens on dry inanimate surfaces154
Type of bacteria
Duration of persistence (range)
Campylobacter jejuni
Up to 6 days
C. difficile (spores)
5 months
Escherichia coli
1.5 h to 16 months
Klebsiella spp.
<90mins
Helicobacter pylori
less than 90 min
Listeria spp.
1 day to months
Salmonella spp.
1 day
Shigella spp.
2 days to 5 months
Adenovirus
7day – 3 months
Norovirus and feline calicivirus
8 h to 7 days
Rotavirus
6-60 days
Hepatitis A
2h - 60 days
A number of lab-based studies are reported on the survival of enteric pathogens on hands
and surfaces:
• Hutchinson (1956) reported that Shigella sonnei can remain viable on hands for more
than 3 hours. 157
• Pether and Gilbert (1971) 158 reported survival of E. coli and Salmonella spp. at 1 hour
after inoculation onto the hands (inoculum size 103-106 per fingertip) although the
extent of survival varied significantly between replicate tests.
• Scott and Bloomfield (1990) 159 studied the survival of small numbers (100-500 cells) of
environmental isolates and laboratory strains of E. coli, Klebsiella and Salmonella
inoculated onto laminate surfaces. To simulate clean and dirty conditions, cells were
suspended in either distilled water of nutrient broth. Under clean conditions, between 1
and 50% of the inoculum could be recovered at 1 hour, but after 4 hours and 24 hours,
the numbers recovered were very small (1-10 cfu) or undetectable. Under soiled
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conditions, up to 10% of the inoculum was recovered at 4 hours, but the numbers
recovered at 24h were very small (1-10 cfu) or undetectable.
Maule 160 evaluated the survival of E. coli O157 inoculated in high numbers onto
surfaces and held at 18°C. Survival times were up to 60 days on stainless steel and 10
days on a chopping board.
Ansari et al.(1988) 161 report 43% and 7% survival of rotavirus on hands at 1 and 4 h
respectively.
Sattar et al. 162 report that hepatitis A can remain viable on the surfaces of vegetables
for several days.
Abad et al.(2001) 163 reported that human astroviruses showed considerable
persistence when dried onto porous and nonporous material. On china, it survived for
60 days at 4ºC and 7 days at 20ºC. On paper at 4ºC, astrovirus infectivity was
detected after 90 days, and for up to 60 days at 20ºC.
Sattar et al.(2002) 164 compared survival of bacterial and also viral pathogens on
fingerpads of human volunteers. Survival after 1 hour ranged from 4% for E. coli to up
to 25% for adenovirus, 45% for rotavirus and 63% for hepatitis A virus. They also
reported that adenovirus can persist on hands for many hours.
Studies of the survival of bacteria and viruses on fabrics are reviewed separately in the 2010
report on the infection potential associated with clothing and household linens.29
Comparative studies suggest that survival on porous surfaces is relatively less than that on
non-porous surfaces, but enteric bacteria and viruses can survive for several hours to up to
days and weeks on fabrics. For contaminated kitchen cleaning cloths,28,165 not only survival,
but also re-growth of Gram-negative species readily occurs at ambient temperatures,
particularly where cloths remain in a damp condition. Growth of bacteria in samples of toilet
water has also been demonstrated. 166
These laboratory studies are supported by an ever increasing range of field studies, as
summarised below, showing not only survival but also spread of enteric pathogens via the
hands and other surfaces during food preparation and other normal daily activities. These
and other studies are also reviewed elsewhere.4, 6,12,167,168,169,170,171,
Salmonella, Campylobacter and E. coli
The spread of bacterial enteric pathogens such as Salmonella and Campylobacter from a
contaminated food source to hands and surfaces during handling and preparation for eating
is demonstrated by a range of studies:
• De Wit et al.(1979) 172 demonstrated cross-contamination of foodborne pathogens via
inanimate surfaces in the domestic environment during preparation of raw chickens.
• Dawkins et al.(1984) 173 demonstrated that when fresh or frozen chickens contaminated
with Campylobacter are introduced into a kitchen preparation area, the surrounding
work surfaces are very likely to become contaminated.
• Borneff et al.(1988) 174 showed that during preparation of a dinner, micro-organisms in
contaminated chopped meat were spread over all the utensils and working surfaces
used, thus contaminating ready-prepared food.
• Cross-contamination experiments by De Boer and Hahne (1990) 175 showed that
Campylobacter jejuni and Salmonella are easily transferred from raw chicken products
to chopping boards, plates and hands.
• Scott and Bloomfield (1993) 176 evaluated the relationship between bacterial
contamination of food preparation surfaces and cleaning cloths during morning food
preparation activities in a college kitchen. Cloths used became heavily contaminated
during food preparation and the post preparation cleaning process. An increase in the
contamination of surfaces after cleaning compared with after food preparation was
also observed indicating transfer of contamination from cloths to surfaces during the
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clean-up process.
• Humphrey et al.(1994) 177 found that, following preparation of egg dishes using eggs
artificially contaminated with Salmonella enteritidis PT4, the strain was recovered from
fingers and utensils, sometimes even after washing. The organisms could be
recovered from dry films of either batter or eggs on work surfaces for up to 24 hours.
• McDermid and Lever (1996) 178 showed that Salmonella enteritidis PT4 could remain
viable in aerosols for up to 2 hours.
• Using a laboratory model, Zhao et al.(1998) 179 showed that bacteria can be readily
transferred to chopping boards after cutting and handling contaminated raw poultry.
They showed that large numbers of bacteria can survive on chopping boards for at
least 4 hours and can cross-contaminate fresh vegetables if the boards are not cleaned
or disinfected.
• Cogan et al.(1999,2003) demonstrated that, following preparation of Salmonella and
campylobacter-contaminated chickens in domestic kitchens, these species were
isolated from 17.3% of hands, and hand and food contact surfaces. Isolation rates were
highest for hands, chopping boards and cleaning cloths (25, 35 and 60%, respectively,
of surfaces sampled).27,180 Results suggested that not only hands but also cloths were
responsible for dissemination. After preparation of the chickens, participants were
asked to clean up the kitchen using their normal cleaning routine. Sampling of surfaces
3 hours later showed that 7% of surfaces were still contaminated with either Salmonella
or Campylobacter.
• In a further study (Cogan et al. 2002)28, involving a limited number of sites (hands,
cloths, chopping board, utensils, tap handles), the number of bacteria disseminated
was evaluated. For Salmonella-contaminated surfaces although counts of <10 were
recorded on 18.3% of occasions, on 22 (18.3%) and 2 (1.7%) of occasions (a board
and a cloth) counts were >10 and >1000, respectively. For Campylobactercontaminated surfaces, high counts were isolated more frequently with 20% of sites
recording counts of >1000. High counts of both species occurred on chopping boards
despite the fact that participants were asked to clean the boards between preparing
the chicken and the vegetables. In this latter study, 3 cloth samples showed an
increase in Salmonella count from 102 to 103 during overnight storage, suggesting
growth of Salmonella in the soiled cloth. For 3 other cloths, a 1-2 log reduction in count
occurred during overnight storage.
• Gorman et al.(2002) investigated cross-contamination in the domestic kitchen during
preparation of a roast chicken lunch. The chickens were found to be contaminated with
Salmonella, Campylobacter, S. aureus or E. coli, which were subsequently found on
hand and food contact surfaces after food preparation. 181
• Hilton and Austin 182 evaluated transfer of contamination from un-rinsed and rinsed
cloths and sponges taken from domestic homes and inoculated with 108 E. coli. Rinsing
of clothes and sponges produced a significant reduction (1 and 2 logs for cloths and
sponges, respectively) in the numbers of organisms transferred to a chopping board
surface, but even where rinsed cloths were used, significant numbers of organisms
(104-105) were still recovered from surfaces after wiping.
• Meredith et al.(2001) 183 demonstrated that during the preparation of a chicken meal,
artificially seeded bioluminescent E. coli was widely disseminated throughout the
kitchen and equipment used, especially to hand contact surfaces. All but 2/35 hand and
food contact surfaces were contaminated.
• Mattick et al.(2003) determined the temperature of washing-up water and bacterial
quality of the water, dishcloths, tea towels and other surfaces following meal
preparation by people without food safety training in their own kitchen or by trained
staff in a commercial kitchen. Campylobacter and Salmonella, respectively, were found
in 96% and 13% of the raw chickens used in the meal preparation. In domestic
kitchens, 2 of 45 sponges/dishcloths/scourers and 1 of 32 hand/tea-towels were
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contaminated with Campylobacter after washing-up and cleaning. Campylobacter was
detected in 1 of 10 washing-up water samples from the commercial kitchen. 184 In
another study by Mattick and co-workers, in a typical UK washing-up process
simulation, bacterially contaminated soiled dishes were washed in warm water
containing detergent and the risk of bacterial transfer to other dishes and sponges,
kitchen surfaces or food was assessed. Some dishes remained contaminated with
bacteria after washing-up and water hardness did not appear to affect survival. E. coli
and Salmonella survived towel or air-drying on dishes and after towel-drying, the cloth
became contaminated on every occasion. Some sterile dishes washed after
contaminated dishes also became contaminated. Washing-up sponges frequently
became contaminated with bacteria. 185
Studies evaluating cross contamination in the kitchen are reported by van Asselt et
al.(2008) 186 and de Jong et al.(2008). 187 Van Asselt et al. estimated transfer rates for
Campylobacter jejuni and Lactobacillus casei as a tracer organism. Transfer for both
micro-organisms were comparable when washing regimes and transfer via items
(cutting board, hands and knives) were compared. They concluded however that the
use of separate rates for transfer from chicken to items and from items to salad may
lead to an overestimation of campylobacteriosis risk and that applying good hygiene
practices resulted in residual levels of bacteria in the salad below the detection limit.
The study of de Jong et al. re-enforced the fact that cross-contamination plays an
important role in the transmission of food-borne illness, especially for C. Jejuni. This
study demonstrated that dish-washing does not sufficiently prevent crosscontamination.
In a study by Bergen et al.(2009), surface were contaminated with bacteria (4
cfu/bacteria/cm2), and cleaned with premoistened microfiber clothes. After cleaning,
surface imprints of cloths showed a median of 45.5 cfu/plate for E. faecalis and 2.5
cfu/plate for B. cereus. From cloth sides 2-16, the median values from imprints were 1
and 12 cfu/plate for E. faecalis and 0 cfu/plate for B. cereus. Samples of contaminated
surfaces gave a median of 45.5 cfu/plate for E. faecalis, giving a reduction of 5.6-fold.
Surface numbers 2-16 had median values between 0.5 and 7.5 for E. faecalis, which
was spread to 11-15 of the 15 sterile surfaces. B. cereus was found in 6 out of 180
imprints on surfaces 2-16, all with 1 cfu/plate. 188
Jimenez et al.(2009) investigated the effect of refrigeration time and temperature on
Salmonella on inoculated chicken carcasses and their transfer to a plastic cutting
board. It was found that all of the carcasses remained contaminated even after 9 days
of refrigeration. On carcasses untreated with a decontaminating acetic acid solution,
Salmonella numbers increased almost 1.5 log at 80C, while numbers decreased about
1 log at 2 and 60C. On acid-treated samples, cell numbers slightly decreased at all of
the temperatures studied. Temperature did not affect salmonellae transfer to the
cutting board, but time did. Acid decontamination increased cell numbers transferred to
the cutting board compared with untreated samples. 189
Tang et al.(2011) found that the mean transfer of Campylobacter jejuni from scored
rubberwood (RW) and polyethylene cutting boards contaminated by contact with
naturally contaminated chickens to cooked chicken was 44.9 and 40.3%, respectively.
Whilst unscored PE and RW boards were not significantly different in regards to the
mean transfer, transfer of C. jejuni from scored RW was significantly higher than from
scored PE. 190
Soares (2012) 191 evaluated transfer of S. Enteritidis from contaminated poultry skin (5
log cfu/g) to different cutting boards (wood, triclosan-treated, plastic glass and
stainless steel) and then to tomatoes. The pathogen was recovered from all surfaces
with counts ranging from 1.90-2.80 log as well as from the tomatoes handled on it.
A 2011 study by Kennedy et al.54 involved filming 60 participants while they prepared a
meal according to a specified recipe (30 beef/salad burgers and 30 chicken salads)
45
and swabbing key potential contamination sites in the participant’s kitchen. Sites
sampled included the sink drainer, taps, work top, refrigerator handle, chopping board
and knife blade. Results showed that C. jejuni was not detected at all. S. aureus was
detected on between 26 and 63 % of sites sampled, and more likely to be found and
more prevalent than E. coli which was found on between 0 and 10% of sites sampled.
S aureus was found on 78% of hands after food preparation and on between 26 and
66 of the items prepared. E. coli was found on 3.3% of hands after food preparation,
but was not isolated from any food samples
• The occurrence and numbers of Salmonella was studied in 60 homes in Culican,
Mexico, over a six week period in which half disinfected kitchen cleaning clothes with a
sodium hypochlorite based disinfectant (Chaidez et al., unpublished- in press). A total
of 360 samples were taken from both home groups (disinfectant using and control
groups). Overall, Salmonella was present in 1.11% and 3.89% of the cleaning cloths
from test group and control group households, respectively.
The potential for spread of enteric bacterial pathogens such as Salmonella, Campylobacter
and also C. difficile, from a human source via the toilet and other environmental surfaces is
also demonstrated by a range of studies.
• Gerba et al.(1975)117 assessed hazards of household toilets as a source and vector for
cross infection in the home. Large numbers of bacteria and viruses were seeded into
the household toilet. Detection of these organisms on bathroom surfaces showed that
the organisms remain airborne and viable long enough to settle on surfaces.
• Van Schothurst et al.(1978) 192 demonstrated that, in 73 homes where a case of
salmonellosis had occurred, in over half of these homes, the same serotypes were
recovered from environmental sites, including worktops, sinks and towels, etc.
• Following the investigation of 9 cases of infant salmonellosis, Haddock (1986) isolated
Salmonella from the contents of 4 of 9 vacuum cleaners. Three of the four isolates
were of the same serogroup as the infant case. 193
• A 1994 study by Haddock et al. carried out on the island of Guam reported isolation of
various spp. of Salmonella (S. java, S. houten) from 4/68 (6.9%) soles of shoes taken
from a variety of settings 194
• In a study in Mexico City, 195 where water and soil are thought to be contaminated with
human waste, because of inadequate disposal services, dust samples from indoor and
outdoor environments, collected using a vacuum cleaner, were found to contain E. coli.
• Barker and Bloomfield (2000) 196 demonstrated that in 4 out of 6 homes where there
was a Salmonella case, the causative species was isolated from faecal soiling under
the flushing rim of the toilet and scale material in the toilet bowl, despite the fact that
the samples were taken 3 weeks or more following notification of the infection. Toilet seeding experiments were set up using Salmonella enteritidis PT4 to mimic
environmental conditions associated with acute diarrhoea. Flushing the toilet resulted
in contamination of the toilet seat and the toilet seat lid. In 1/3 seedings, Salmonella
was also isolated from an air sample taken immediately after flushing, indicating that
airborne spread of the organism could contaminate surfaces in the bathroom. In
seeded toilets, Salmonella was isolated from the biofilm in the toilet bowl below the
waterline for up to 50 days after seeding and also on one occasion from the bowl
water. Although the risk of exposure to pathogens from the toilet is relatively low under
normal conditions, these studies suggest that during diarrhoeal illness, there is
considerable risk of spread of Salmonella infection via the environment, including
contaminated surfaces in the toilet area.
• Schutze et al.(1999) 197 studied environmental contamination in 50 homes where
children under 4 years were known to be infected with Salmonella spp. In 34% of
homes there was also illness in other family members. The authors concluded that
environmental sources, infected family members and pets, appeared to be more
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significant risk factors for development of salmonellosis in these children than
contaminated foods. Cultures were obtained from foods, persons residing in the home,
animals/pets/insects, and environmental sources. Isolates with a serotype identical to
those in the index patient were found in 16 homes, 3 of which included an isolate of a
second serotype. A different serotype was recovered in 3 homes. Serotypes from the
subjects and their environment were indistinguishable in all but 2 patients. The
identical serotype was found in multiple locations (4), dirt surrounding front doors (4),
household members (3), vacuum cleaner (1), animals/pets/insects (1), and a
refrigerator shelf (1).
Barker et al.(2005) evaluated the spread of infection by aerosol contamination of
surfaces after flushing a domestic toilet. This study showed that although a single flush
reduced the level of micro-organisms in the toilet bowl water, when contaminated at
concentrations reflecting pathogen shedding, large numbers of micro-organisms
persisted on the toilet bowl surface and in the bowl water which were disseminated
into the air by further flushes. 198
A range of studies are reported showing extensive contamination with C. difficile of
hands and environmental surfaces in settings where there is an infected person or a
carrier. These are reviewed in more detail in the 2006 IFH report on C.difficile. More
recent studies are reviewed by Dubberke et al. 199, Mutters et al. 200, Otter et al.44 ,
Webber and Rutala. 201 The majority of studies were carried out in hospitals, nursing
homes, extended care facilities, and nurseries, but Kim et al.(1981) 202 found that
12.2% of environmental surfaces were positive for C. difficile in the home of an
infected infant recently discharged from hospital. Surfaces found to be contaminated
included floors and furniture. In contrast, in a control home where none of the family
members were carriers, none of the 84 environment samples were positive for C.
difficile.
Best et al. 2012 performed in-situ testing, using faecal suspensions to measure C.
difficile measure aerosolisation and splashing from toilets 203. C. difficile was
recoverable from air sampled at heights up to 25 cm above the toilet seat. The highest
numbers of C. difficile were recovered from air sampled immediately following flushing,
and then declined 8-fold after 60 min and a further 3-fold after 90 min. Surface
contamination with C. difficile occurred within 90 min after flushing, demonstrating that
relatively large droplets are released which then contaminate the immediate
environment. The mean numbers of droplets emitted upon flushing by the lidless toilets
in clinical areas were 15-47, depending on design. C. difficile aerosolisation and
surrounding environmental contamination occur when a lidless toilet is flushed.
Gerhardts et al. 2012 204 reported studies carried out to simulate the chain of infection
from a pathogen source (i.e. stool). Transmission of E. coli, Bacillus atrophaeus
spores, Candida albicans and bacteriophage MS2 from hands to surfaces was
examined in a transmission model, that is toilet brush and door handle to water tap.
Although the load of viable pathogens was significantly reduced during sequential
transfer from hands to objects, nevertheless, it was shown that pathogens were
successfully transferred to other people in contagious doses by contact with
contaminated surfaces.
Norovirus, rotavirus and other viral enteric pathogens
Bellamy et al.(1998) 205 investigated the domestic environment for the presence of viruses
and body fluids that may contain viruses. Haemoglobin was found on 2% of surfaces (taps,
washbasins, toilet bowls and seats) indicating the presence of blood. Amylase (an indicator
of saliva, sweat and urine) was found on 29% of surfaces, which were frequently handled or
in contact with urine. These data highlight that surfaces may remain soiled for some time,
and that cleaning procedures may not be effective. Enteroviral RNA was detected in 3 out of
448 samples tested (tap handle, telephone handpiece and toilet bowl).
47
Virus transmission in a childcare centre was studied by using modified cauliflower virus DNA
as an environmental marker. 206 The DNA markers were introduced into the environment
through treated toy balls. The marker treated objects were removed after one day, but the
markers continued circulating in the settings for up to 2 weeks. Hand contact with
contaminated surfaces played an important part in the transmission of the markers. After
introduction into the child-care centre, the markers were detected in the children’s homes, on
toys and environmental surfaces, and from the hands of family members.
In homes where there was an infant recently vaccinated for polio (during which time
shedding occurs in faeces), using polio vaccine virus as an indicator of viral contamination
from faeces, Curtis et al.(2001) 207 carried out a study of the hygiene practices of mothers
with young children in England. A total of 234 surface samples were taken from 10
households and tested for poliovirus. Of these samples, 13% were positive: 15% of
bathroom sites were positive, 12% of living room sites and 10% of kitchen sites. Most
frequently contaminated were hand contact sites, such as bathroom taps, door handles,
toilet flushes, liquid soap dispensers, nappy changing equipment and potties.
Transmission of viruses in a household setting was studied, using bacteriophage X174 as a
model virus with resistance properties similar to polio-or parvoviruses. 208 Contaminated door
handles and skin surfaces were found to be efficient vectors of contamination. At least 14
persons could be contaminated one after another by touching a contaminated door handle.
Successive transmission from one person to another could be followed up to the sixth
contact person. Transfer from contaminated door handles to other surfaces was also
confirmed under everyday life conditions in a flat shared by four students.
The potential for environmental spread of enteric viruses was demonstrated in a 2008 study
by Gallimore et al. 209 in 2 UK hospital paediatric wards over a winter season. Environmental
swabs were collected weekly from 11 sites in both wards and examined for the presence of
norovirus, astrovirus, and rotavirus by reverse transcriptase PCR. Viruses were detected in
17% and 19% of swabs from both wards. Surfaces sampled included tap and door handles,
telephones, televisions and light switches.
Norovirus
As mentioned earlier, projectile vomiting associated with norovirus infection represents the
major route of cross infection and it is estimated that 3 x 107 particles may be distributed as
an aerosol into the environment during a vomiting attack. 210 The potential for person to
person transmission in home and everyday life settings is shown by a whole range of
microbiological studies:
• Studies by Cheesbrough et al. 211 showed the extent to which airborne contamination
and contamination of environmental sites and surfaces can occur during outbreaks in
hospital and hotel settings. The authors found that during and after an outbreak of
norovirus-associated gastroenteritis in a hotel, 42% of environmental samples were
positive for norovirus nucleic acid. All positive samples were from sites likely to have
been directly contaminated (i.e., known recent vomit) e.g. carpets, toilet rims or seats.
Positive samples were just as likely to be collected from a high horizontal surface, very
unlikely to have been touched, as they were from items to be handled such as
telephones and door knobs. Contact with contaminated fomites appears to have
played an important role in maintaining the outbreak over several months. The
prolonged nature of the outbreak indicates the ability of the virus to survive and be
transferred in an infective form.
• Barker et al.(2004) showed that, where fingers come into contact with noroviruscontaminated faecal material, the virus is consistently transferred via the fingers to
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surfaces and from there to hand contact surfaces, such as taps, door handles and
telephone receivers. Contaminated fingers sequentially transferred the virus to up to
seven clean surfaces.180
A 2006 study 212 with feline calicivirus (FCV) showed survival for up to 3 days on
telephone buttons and receivers, for 1 or 2 days on computer mouse, and for 8-12
hours on keyboard keys, and brass disks representing faucets and door handles. The
time for 90% virus reduction was <4 hours on computer keys, mouse and brass disks;
4-8 hours on telephone receivers; and 12-24 hours on telephone buttons.
During a 2005 outbreak in a long-term care facility, norovirus RNA was identified on 5
of 10 environmental sites collected after disinfection, suggesting widespread persistent
contamination. Positive sites included an elevator call button used only by staff. The
outbreak resolved following a second, more thorough facility-wide disinfection. 213
Jones et al. (2007) 214 reported an outbreak which affected 74% of guests on 3
consecutive houseboat trips. An environmental investigation identified norovirus RNA
on 71% of surfaces in bathrooms, kitchens, and door handles.
Norovirus strains were detected in 2 patients and in environmental swabs from a
paediatric immunodeficiency unit in London, UK, during an infection control incident in
2007. 215 Detailed genetic analysis demonstrated that the majority of the strains were
not related to the patients and that the environmental contamination was most likely
due to secondary transfer by the hands of staff or visitors.
Bright et al.(2009)23 carried out a 6 week intervention study of the impact of hygiene in
6 (3 intervention, 3 control, 148 students) classrooms in a school in Seattle, US.
Surfaces were sampled in the afternoon on 4 study days. Norovirus was detected on
surfaces in two of three control classrooms sampled. The virus was found on 16.4% (9
of 55) of surfaces tested including student desktops (6 of 27), a paper towel dispenser
(1 of 4), a sink faucet handle (1 of 7), and a water fountain toggle (1 of 7) but was not
detected on the soap dispenser or the entrance doorknob in any of the classrooms.
The potential for contamination of environmental surfaces in situations where there is
an infected person is demonstrated in a 2011 hospital study24 where norovirus strains
were collected over a four-month period from hospitalised patients with symptoms of
gastroenteritis. These were characterised in order to estimate how many strains were
introduced into the hospital from the community. A total of eight distinct genetic
clusters of the GII-4 genotype were identified, with some wards experiencing multiple
outbreaks with different GII-4 strains during the season. Norovirus was detected from
31.4% of environmental swabs including surfaces of trolleys, computer keyboards,
soap and alcohol dispensers together with surfaces around the bedside environment,
and furniture, fixtures and fittings associated with toilets and shower rooms.
In a 2011 study,25 the prevalence of norovirus in catering companies without recently
reported outbreaks of gastroenteritis was investigated and compared to prevalence in
catering companies with recently reported outbreaks. Swab samples were collected
from surfaces in the kitchens and (staff) bathrooms in 832 randomly chosen companies
and analyzed for the presence of norovirus RNA. In total, 1.7% of 2,496 environmental
swabs from 35 (4.2%) catering companies tested positive compared with 39.7% of the
370 samples for 44 (61.1%) of the 72 establishments associated with gastroenteritis
outbreaks. Sequence analysis showed that environmental strains were interspersed
with strains found in outbreaks of illness in humans suggesting that presence of
norovirus was associated with presence in the population.
In a UK hospital, norovirus strains were collected over a four-month period during
2009-2010 from hospitalised patients with symptoms of gastroenteritis. 216 These were
characterised in order to estimate how many strains were introduced into the hospital
from the community. A total of eight distinct genetic clusters of norovirus GII-4
genotype were identified during the four-month period, with some wards experiencing
multiple outbreaks with different GII-4 strains during the season. Norovirus was
49
detected from 31.4% of environmental swabs. Contaminated sites suggested
transmission via hand contact, and hot spots were identified as patient monitoring
equipment, computers and notes trolleys at the nurses’ stations, soap and alcohol
dispensers, hand and grab rails within toilets and the bedside environment.
Rotavirus
• Studies in child day-care centers have shown that rotavirus is widely disseminated
when outbreaks occur. In one centre, faecal contamination of hands and the
environment was demonstrated during an outbreak of rotavirus diarrhea. 217 Other
studies in day-care centers have shown that 16–30% of surfaces sampled can be
contaminated with rotavirus; in particular, hand contact surfaces (e.g. refrigerator
handle, toilet handles, telephone receivers, and toys) and moist surfaces, such as
sinks, water fountains and water-play tables were contaminated.217,218,219
• Akhter et al.(1995) 220 and Soule et al.(1999) 221 found that increases in the number of
children suffering from rotavirus gastroenteritis in hospital paediatric units were
correlated with an increase in the number of environmental surfaces contaminated with
rotavirus. Soule et al.(1999) detected rotavirus in 63% of samples from surfaces in
direct contact with children (thermometers, play mats, toys) compared with 36% of
surfaces without direct contact with children (telephones, door handles, washbasins).
Akhter et al. also showed frequent detection of rotavirus on surfaces such as toilet
handles, televisions and toys, i.e., objects handled by humans.
• In a treatment centre in Bangladesh, hand washings from 78% of the attendants of
patients with diarrhoea (children under 5 years) were positive for rotavirus antigens. 222
Rotavirus was also found in hand washings of 19% of attendants of patients with nonrotavirus diarrhoea, indicating that they may have come into contact with other
attendants and patients in adjacent beds.
• Sattar et al.(1986) 223 and Ansari et al.(1988)161 demonstrated survival of rotavirus on
human hands, and transfer of infectious virus to animate and non-porous inanimate
surfaces.
• Ward et al.(1991)40 examined the transfer of rotavirus from contaminated surfaces to
the mouth and from surfaces to hands to the mouth. All the volunteers who licked
rotavirus contaminated plates became infected. Of those individuals who touched the
virus-contaminated plates with their fingers and put the fingers to their mouths, about
half became infected. Ward et al.(1991) demonstrated that 13 out of 14 adult subjects
who consumed rotavirus (103 focus forming units) became infected.
• Rogers et al.(2000) reported an outbreak of rotavirus in a paediatric unit. Rotavirus
transmission continued for more than a month even after applying aggressive infection
control measures. An examination of the outbreak revealed that communal toys had
not been cleaned for several months, in line with the weekly protocol. The authors
believe that improperly cleaned toys may have served as fomites in the transmission of
rotavirus and contributed to the outbreak. 224
Hepatitis A Virus
It is generally agreed that hepatitis A virus (HAV) is most commonly spread via water, food
and by person-to-person transmission. However, from an assessment of data showing the
occurrence of HAV in secretions, such as saliva, and its ability to survive on dry surfaces,
Hadler (1991) 225 and Cliver (1983) 226 concluded that fomites are potential risk factors in the
spread of the virus, especially in hospital wards, day-care centres or restaurants. A review
by Sattar et al. 2000162 summarises the findings of studies showing how transfer of HAV can
occur from contaminated fingers to surfaces and objects during casual contact.
50
Infection risks associated with spread of Salmonella, Campylobacter, norovirus, rotavirus
etc. via hands and surfaces depend on the number of infectious agents transferred via
hands and surface etc. by contact between surface, hands, food etc.:
• Scott and Bloomfield (1990)159 studied the transfer of small numbers (200-600 cells) of
environmental and laboratory strains of E. coli and Salmonella from laminate surfaces
to fingertips and to a stainless steel bowl surface. To simulate dirty conditions, cells
were suspended in nutrient broth for inoculation onto surfaces. Immediately after
inoculation and after 1 hour drying, transfer rates of around 10-40% were recorded. At
2 hours, transfer rates were lower, ranging from no detectable transfer of salmonella
from laminate surface to bowl, up to 30% transfer of E.coli from laminate surface to
fingertips.
• Chen et al. 2001 investigated the transfer of bacteria between hands and other kitchen
surfaces during food preparation using Enterobacter aerogenes as a model. Transfer
of bacteria was studied when handling a chicken, lettuce and a tap with results
showing significant variation but quite a high rate of transfer (as high as 100%) in all of
these situations. 227 Chen and co-workers found that transfer rates are highly variable
but can range as high as 100% and as low as less than 1%.
• Rusin et al.(2002) 228 determined that transfer from surfaces to hands (using Serratia
rudidea, Micrococcus luteus and bacteriophage PRD-1) was highest from non-porous
surfaces, such as faucets, with a 48.7% transfer efficiency and much lower from other
surfaces such as carrots (<1%) and sponges and dishrags (<1%). Even so, up to 1
million bacteria and viruses were transferred to the hands after wringing out a seeded
sponge or dishrag. Rusin et al. sampled volunteer’s hands after touching surfaces
contaminated with M. luteus, S. rubidea and phage PRD-1. Activities included wringing
out a dishcloth/sponge, turning off a faucet, cutting up a carrot, making hamburger
patties, holding a phone receiver, and removing laundry from the washing machine.
Transfer efficiencies for the phone receiver and faucet were 38-65% and 27-40%,
respectively.
• Paulson 229 showed that when gloved hands were contacted for 5-10 seconds with
surfaces such as cutting boards and door knobs contaminated with FCV (log 5.9
particles), the log number of particles recovered from the gloved hands was 4.7-5.4.
• Kusumaningrum et al.(2003) 230 quantified survival of Salmonella enteritidis, S. aureus
and Campylobacter jejuni at room temperature on stainless steel surfaces. Transfer
from kitchen sponges to surfaces and from surfaces to foods was also investigated.
Bacterial levels decreased rapidly, particularly when initial levels were low. S. aureus
was recovered from surfaces for at least 96 hours when the inoculum level was high
(105 cfu/cm2) or moderate (103 cfu/cm2). At low levels (10 cfu/cm2), numbers
decreased below the detection limit (4 cfu/100cm2) within 2 days. All bacteria were
readily transferred from wet sponges to surfaces and then to food (transfer rates
between 20-100%).
• By contrast, Montville et al. showed that the effect of inoculum size on transfer rates
was highly statistically significant. With higher inoculum sizes, transfer rates were
lower, and where inoculum size was less, transfer rates were higher. The negative
linear trend has serious implications for research, seeking to determine bacterial cross
contamination rates, since transfer efficiencies previously shown to be associated with
certain activities may actually be the result of differing inoculum levels. 231
• Julian et al. 2010 232 reported a study modelling transfer rates for bacteriophage
between fingerpads and surfaces. Aggregating 656 transfer events, they reported that
the mean fraction of virus transferred between finger pad and glass was 0.23 +/- 0.22.
Transfer rates were significantly affected by virus species and time since last hand
washing.
51
1.1.3 Risks from exposure to gastrointestinal pathogens in the home
As shown in Figure 1, exposure to enteric pathogens can occur either by direct hand-tomouth contact, or by the consumption of contaminated food or water. The infection risk from
oral consumption of GI pathogens depends upon the number of bacterial cells or viral
particles which are consumed. For many common GI pathogens, the oral infectious dose is
relatively small. Infection risk also depends on the immune status of the recipient and is
generally lower for someone with lowered immunity to infection. Table 2 shows examples of
infectious doses as estimated for some pathogens, although they should not be regarded as
comparative since many are not estimated as ID-50 values. Data on the minimum infective
dose for enteric viruses transmitted through food and the environment is summarized in a
2011 review by Yezli and Otter 233 a 2011 EFA report. 234 ID-50 values for enteric pathogens
can also be obtained from the Quantitative Microbial Risk Assessment Wiki site (QMRAwiki)
at: http://wiki.camra.msu.edu/index.php?title=Table_of_Recommended_Best-Fit_Parameters
Table 2 – Infectious doses for gastrointestinal pathogens
Organism
Infectious dose
Salmonella spp.
Up to 106, but could be as low as 10-100 cells. 235 Contamination
may be amplified by transfer to foods which are then stored
incorrectly.
Campylobacter spp. 500 organisms can result in human illness. 236
E. coli 0157
Oral dose for E. coli 0157 may be as little as 10-100 cells. 237,238,239
Norovirus
10-100 units or even as little as 1 unit.210,240 According to Yezli et
al., recent work suggests that the HID50 of the virus is 18
particles.233
Rotavirus
May be as few as 10 particles.40 Ward et al. showed that 13/14
adults became infected after consuming rotavirus (103 particles)
picked up from a contaminated surface via the hands.40 Yezli et
al.233 report that low doses of rotavirus were shown to cause
infection with less than 1 focus forming unit of strain CJN causing
infection in adult volunteers
Hepatitis A
According to Yezli et al.233, there is little quantitative data on the
MID in humans; a 0.5 ml stool suspension containing 3.0 9 105
RNA copies/ml of the HAV strain HAF-203 administered orally or
intravenously to animals caused infection.
C. difficile
Consumption of one to two spores may be sufficient to establish
colonisation and CDAD in clindamycin-treated mice. 241 Less than 1
CFU/cm2 was sufficient to cause C. difficile disease in mice 242
Cryptosporidium parvum and C. hominis, are responsible for most human cases of
cryptosporidiosis. 243 Dupont et al.(1995) estimated the median infective dose of C. parvum in
healthy adults as132 oocysts. 244 Chappell et al. demonstrated that C. hominis is infectious
for healthy adults (ID50=10 oocysts) and is clinically similar to C. parvum-induced illness.243
Hand-to-mouth contact is a frequent occurrence, particularly among children; a study of
mouthing behaviour in 72 young children showed that children <24 months exhibit the
highest frequency, with 81 events/hour; for children >24 months this was reduced, but was
still of the order of 42 events/hour. 245
The potential for transmission of pathogens from hands to ready-to-eat foods, or from hands
and surfaces directly to the mouth is supported by a number of studies:
• In a model domestic kitchen, 29% of food preparation sessions using campylobactercontaminated chicken resulted in positive campylobacter isolations from prepared
salads, cleaning materials and food contact surfaces. 246
52
• Bidawid et al. 247,248 showed that touching lettuce with fingers contaminated with HAV
and feline calicivirus (used as surrogate for norovirus) for 10 seconds resulted in
transfer of 9.2 and 18%, respectively, of the virus. Based on the known load in faeces
(106 to 109 viral particles/g), an estimated 1,300 HIV particles were transferred to the
lettuce.
• Rusin et al. showed that when volunteers’ fingertips were inoculated with a pooled
suspension of Micrococcus luteus (M. luteus), Serratia rubidea (S. rubidea) and
bacteriophage PRD-1 and held to the lip area, transfer rates were 40.99, 33.97 and
33.90%, respectively.228
• Lingaas et al.(2009) indicated low transfer of bacteria during short contact with dry
hands of healthcare workers to a recipient wearing sterile gloves. A smaller proportion
of E. coli was recovered from skin compared with glove surfaces, indicating reduced
survival of bacteria in contact with skin. 249
1.2 CHAIN OF TRANSMISSION OF RESPIRATORY TRACT INFECTIONS
Within the home, the primary source by which respiratory pathogens are introduced into this
setting is via people who are infected. Infections can spread by transmission of infected
particles of mucous generated by coughing and sneezing which remain airborne, or settle on
surfaces, including those which are frequently touched (door handles, tap handles etc).
Infectious material can also be deposited directly on hands and tissues during sneezing and
blowing the nose. Contamination of hands can occur by handshaking or touching
contaminated surfaces. Pathogens shed into the environment can survive for significant
periods, and are readily spread around the home, to and from the hands, and via surfaces
such as handkerchiefs and tissues, tap and door handles, telephones and other hand
contact surfaces. Infection occurs by inhaling airborne particles of infected mucous
generated by coughing and sneezing. It also occurs by direct transfer of infectious agents
from the hands to the eyes, nose or mouth.
Respiratory infectious agents thought to be spread via these routes include rhinovirus,
respiratory syncitial virus (RSV), adenovirus, parainfluenza (PIV) and influenza virus. The
last 2 years have seen an unprecedented global focus on developing strategies for
preventing transmission of influenza. The WHO 250 has taken the lead on pharmaceutical
interventions such as vaccines and antivirals, but has also made recommendations for other
interventions 251 which include highlighting the importance of good respiratory hygiene in
minimizing spread in the home and community.
In addition, there is evidence that Legionella infection can occur in the home as a result of
inhalation of contaminated water sprays or mists which occur in association with showers,
spas and hot tubs, whilst P. aeruginosa and Stenotrophomonas maltophilia represents a risk
to patients with increased susceptibility to infection who are cared for at home. To determine
the composition of showerhead biofilms and waters, Feazel et al.(2009) 252 analysed rRNA
gene sequences from 45 showerhead sites around the US. They found that microbial
assemblages containing sequences representative of non-tuberculous mycobacteria (such
as M. avium and M. gordonae) and other opportunistic human pathogens are enriched to
high levels in many showerhead biofilms, >100-fold above background water contents. Other
species identified in showerheads included Pseudomonas spp. (3.8% of total clones),
Staphylococcus spp. (2%), Streptococcus spp. (1%), Legionella spp. (0.1%) and Escherichia
spp. (6%).
The risk of exposure to respiratory pathogens, as illustrated in Figure 1, depends on the
extent to which these pathogens are brought into the home and the extent to which they are
53
spread via hands and other sites and surfaces, and by airborne transmission. Data on the
survival and spread of respiratory pathogens in homes and other settings comes from
various sources and is summarised below. Taken together, it suggests that exposure to
respiratory pathogens by direct inhalation or via the hands and surfaces is a frequent
occurrence during normal daily activities, and that the numbers of organisms transferred via
the hands to the eyes, nose and mouth can be well within the numbers required to cause
infection.
1.2.1 Sources and spread of cold and flu pathogens
The potential for exposure to respiratory pathogens shed or spread from a human, animal,
food or other source is shown by a whole range of laboratory and field studies, as
summarised below. These studies are also reviewed elsewhere.4,6,22,12,169,253
Rhinovirus
The common cold is reported to be the most frequent, acute infectious illness to humans. 254
Estimates suggest that adults suffer 2 to 5 colds per year and infants have about 4 to 8 colds
per year. 255 People infected with cold viruses shed large quantities of virus-laden mucus.
Droplets of nasal secretions generated by coughing, sneezing and talking can travel over a
distance >3 m to contaminate surrounding surfaces. 251, 256,257,258,259
The mean duration of a cold is 7.5 days. Viral shedding may occur 24-48 hours before
illness onset, but mostly at lower titers than during the symptomatic phase. Titers generally
peak during the first 24-72 hours of illness, and decline within several days, with low or
undetectable titres by day five. Children can shed virus for longer periods (up to 3 weeks),
whilst immuno-compromised people may continue to shed virus for weeks to months.251
The potential for spread of rhinovirus from infected people during normal daily life activities is
demonstrated by a range of studies:
• Hendley et al.(1973) 260, Reed (1975) 261 and Kramer et al.(2006)154 review data
showing that rhinovirus can survive for significant periods (2 hours to 7 days) on dry
surfaces, and for at least 2 hours on human skin.
• Hendley et al.(1973)260 found that 2 of 25 persons infected with rhinovirus colds
expelled virus in a cough or sneeze and 4 of 10 had virus on their hands. Dried
rhinovirus could be picked up by the fingers from skin or environmental surfaces.
• Reed (1975)261 recovered rhinovirus from the fingers of 16 of 38 volunteers, who were
swabbed during the acute stages of infection. Very low titres of virus were also
recovered from 6 of 40 objects recently handled by infected volunteers, but not from
the fingers of 18 non-infected subjects whose flat-mates were shedding virus. When
rhinovirus from nasal secretions was dried on skin or other surfaces, approximately 4099% of infectivity was lost. Virus could be transferred from surface to surface by
rubbing, transfer being more efficient if the inoculum was still damp.
• Gwaltney, Moskalski and Hendley (1978) 262 showed that hand transfer of rhinovirus
from experimentally infected volunteers to susceptible recipients was very efficient. As
much as 70% of infectious rhinovirus has been shown to transfer to a recipient’s
fingers after contact for 10 seconds.
• Gwaltney and Hendley (1982) 263 demonstrated that most subjects with experimental
colds had rhinovirus on their hands, and that rhinovirus could be recovered from 43%
of plastic tiles they touched. For people with natural rhinovirus colds, virus was found
on 39% of hands and 6% of objects in their immediate environment.
• Ansari et al.(1991) 264 determined the survival of mucin-suspended rhinovirus 14 (RV14) and the transfer to and from the fingers of adult volunteers. When each finger pad
54
was contaminated with 10ul of RV-14 (2.1 x 10' to 1.1 x 10 PFU), 37.8% of RV-14
remained viable after 1 h. After 3 hours, nearly 16% of RV-14 could still be detected.
Tests on the spread of viruses from contaminated hands or surfaces were conducted
20 min after contamination of the donor surface by pressing together donor and
recipient surfaces for 5s. Irrespective of type of donor or recipient surface, 0.7-0.9% of
RV-14 was transferred.
• Pancic et al.(1980) estimated recovery rates from 3-1,800 plaque forming units of
rhinovirus from fingers of volunteers who handled contaminated door knobs or
faucets,. 265
• In a 2006 study, Winther et al.(2007) 266 recruited volunteers with rhinovirus colds to
stay overnight in hotel rooms. After checkout, before room cleaning, 10 frequently
touched surfaces were sampled for residual rhinovirus. Rhinovirus was found on 35%
of objects, including door handles, light switches, pens, faucet and toilet handles, and
television remote controls. Some people contaminated none or few sites, most
contaminated several, and some contaminated almost all (up to eight) sites. In a
second study where the same subjects stayed overnight in a hotel room where hand
contact surfaces (light switch phone button and handset) had been contaminated with
rhinovirus-contaminated mucus, 60% of subjects became contaminated with
rhinovirus.
Based on the available evidence, opinion as to the importance of the hands relative to the
airborne route for transmission of rhinovirus colds is divided. Some investigators 267, 268, 269
maintain that contamination of the hands followed by inoculation of the eyes or nose is of
paramount importance; in fact, Gwaltney and co-workers found that it was exceedingly
difficult to transmit virus orally or by kissing, and found little evidence of droplet or droplet
nuclei transmission.260,262 Others maintain that the evidence favours droplet and droplet
nuclei transmission as the most important mode of spread. 270
Respiratory syncytial virus (RSV)
For RSV, there is general agreement that hands are the primary route for spread of
infection.253,271,272,273 Infants with RSV excrete prodigious amounts of virus in their nasal
secretions for a number of days. 274,271 RSV has been shown to survive well on inanimate
objects – more than 5 hours on impervious surfaces such as countertops.
• Kramer et al.154 review evidence showing that RSV can survive for significant periods (up
to 6 hours) on dry surfaces.
Parainfluenza virus (PIV)
• Brady et al.(1990) 275 studied survival of PIV on nonabsorptive (stainless steel,
laminated plastic, skin) and absorptive (hospital gown and laboratory coat) surfaces, at
room temperature. The inoculum size was approx. 103 per 2 sq cm. Persistence on
stainless steel was greater than on fabrics, but all 3 strains of PIV survived for up to 4
h on fabrics, and up to 10 h on non porous surfaces. PIV virus survived on skin for a
minimum of 1 h.
• Ansari et al.(1991)264 determined the survival of mucin-suspended human
parainfluenza virus 3 (HPIV-3) and the transfer of the viruses to and from the fingers of
adult volunteers. When each finger pad was contaminated with 10ul of HPIV-3 (1.3 x
105 to 5.5 x 105 PFU), <1.0% of HPIV-3 was recovered after 1 h. After 3 hours HPIV-3
became undetectable. Tests on the potential spread of viruses from contaminated
hands or surfaces were conducted 20 min after contamination of the donor surface by
pressing together donor and recipient surfaces for 5 s. Transfer of HPIV-3 from finger
to finger, or finger to a metal disk could not be detected, but 1.5% of infectious HPIV-3
was transferred from disk to finger. The authors concluded that the relatively rapid loss
55
of HPIV-3 infectivity on hands suggests that their role in the direct spread of
parainfluenza viruses is limited.
• Sattar et al.(2002) compared survival of viral pathogens on fingerpads of human
volunteers.164 Survival after 1 hour was only 1% for PIV3 compared with 25% for
adenovirus, 45% for rotavirus, 63% for hepatitis A and 35% for rhinovirus.
• Aitken et al.(2001) reported that PIV environmental stability is greatest at 4°C with viral
survival decreasing significantly at 37°C and low humidity. Recovery was enhanced by
increasing the inoculum size. 276
• Boone and Gerba (2010)22 reported a study evaluating the potential role of fomites in
human parainfluenza virus 1 transmission in an adult setting (office). A total of 328
surfaces from 12 office buildings in 5 US cities were evaluated including 76 telephone
receivers, 62 computer mouse, 51 office and cubical desktops, 26 conference room
table tops, 50 chair arms, 42 door knobs or door handles, 21 light switches. HPIV1
was detected on 37% of all office surfaces. It was detected more often on the desktops
(47%), the computer mouse (46%), and the phone (45%). Viruses were isolated least
often on door handles (26%) and light switch (19%). The quantity of positive surfaces
varied within object category from 20% (New York phone) to 66% (Atlanta phone).
Influenza virus
The data suggest that up to 107 infectious influenza particles per ml may be found in nasal
secretions. 277 Survival and transfer via hands and environmental surfaces is reported in 2
studies as follows:
• Bean et al.(1982) 278 showed that influenza viruses could survive up to 24-48 hours on
non-porous surfaces, and up to 8-12 hours on cloth, paper, and tissues. By contrast,
viruses could be recovered from hands for only 5 minutes, and then only if the hands
were contaminated with high viral titers. Virus could be transferred from non-porous
surfaces to hands for 24 hours and from tissues to hands for 15 minutes. Higher RH
shortened virus survival. Virus on nonporous surfaces could be transferred to hands
24 hours after surfaces were contaminated, while tissues could transfer virus to hands
for 15 minutes after tissues were contaminated. On hands, virus concentration fell by
100 to 1,000-fold within 5 minutes after transfer.
• In a two and a half year study of US day care centers and domestic homes by Gerba
et al. 279, influenza A virus was detected on 23% of day care center surfaces sampled
during the fall of 2003 and 53% of surfaces sampled during the spring. Whilst no
influenza was detected on home surfaces during the summer, influenza was detected
on 59% of surfaces sampled during March in five homes where there was an
influenza-infected child. No virus was recovered from three other homes where all
household members were healthy. Influenza virus was recovered most frequently from
telephone receivers (80%) and least frequently from computer keyboards (40%). Other
surfaces found to be contaminated included refrigerators, kitchen faucets, light
switches, microwaves, TV remote controls, door knobs, bath and faucet and toilet
handles. Virus was recovered from 69% of day care center diaper changing areas
indicating presence of virus in infant faeces.
For influenza, although more data is needed, it is increasingly accepted that, not only
airborne (both true airborne transmission involving droplet nuclei (<5 µm in diameter), and
“droplet transmission” involving droplets >10 µm which deposit onto surfaces quite rapidly),
but also surface (including hand) transmission can come into play.251,280,281 The relative
contribution of each mode of transmission is unknown, but appears to vary depending on the
circumstances, symptoms, respiratory tract loads and the viral strain. 282 Data from animal
studies and influenza outbreaks suggest that droplets generated from infected person’s
cough or sneeze are the predominant mechanism of airborne transmission,256 although data
supporting droplet nuclei spread (especially in unventilated conditions) is also
56
available. 283,284,285,286 It is possible however that influenza is less transmissible via hands and
surfaces compared with rhinovirus etc., because of its lower ability to survive outside a
human or animal host. Data suggest that, to some extent, airborne droplets and droplet
nuclei can cause infection as a result of settling on hand contact surfaces. In 2009,
Mubareka et al. 287 reported a study using a guinea pig model, demonstrating that
transmission of influenza A virus through the air is efficient, compared to spread through
environmental surfaces. The data provide new insights into the modes of influenza virus
spread and strain-specific differences in the efficiency of transmission. Frequent occurrence
of diarrhoea and the detection of viral RNA in faecal samples tested suggest that the H5N1
influenza virus may replicate in the human gut and could be a source of transmission via
hands and surfaces. 288 At present, however, it is thought that this is unlikely.
1.2.2 Infection risks from exposure to cold and flu pathogens
As shown in Figure 1, exposure to RT viruses occurs either by inhalation of infected mucous
or inoculation of the nasal mucosa or eyes with virus-contaminated hands, which then cause
infection via the mucous membranes and upper RT. Rhinovirus and RSV are deposited into
the front of the nose or into the eye (where they pass down the lachrymal duct).268 A feature
of rhinovirus is the susceptibility of the nose to the virus. Rubbing the eyes and nose with the
fingertips is a common occurrence; Hendley et al. found that one in 2.7 attendees of hospital
rounds rubbed their eyes, and 33% picked their nose, within a 1-hour observation period.260
A review of the data by Boone and Gerba (2007)171171 (Table 3) suggests that the infectious
dose for respiratory viruses is relatively small. Alford et al. suggest that aerosolised doses of
as little as one TCID50 of influenza virus could infect volunteers.283
Table 3 – Infectious doses for viruses that cause respiratory diseases171
Virus
Minimal infectious dose associated with
intranasal inoculation
Respiratory syncytial virus
100-640 TCID50
Rhinovirus
0.032-0.4 TCID50
also cited as 1-10 TCID50
Influenza
2-790 TCID50
Parainfluenza
1.5-80 TCID50
The most recent data on the minimum infective dose for respiratory viruses has been
reviewed in a 2011 report by Yezli and Otter.233 They report an HID50 for influenza A (H2N2)
of 0.6-3.0 TCID50 when administered in small particle aerosols to serum antibody-free
volunteers. They concluded that the nasal infectious dose of influenza virus A is several
orders of magnitude higher than that of airborne infection. They also concluded that
Rhinovirus 15 has a greater infectivity in man than in culture, with a HID50 of 0.032 TCID50
and that it is more infectious when given as nasal droplets than as an aerosol spray and has
a lower infectious dose in the nose compared to other sites of inoculation such as the mouth.
They report that a dose of 30–40 TCID50 of ts-1 mutant RSV vaccine caused infection in an
infant. However, because infection studies rely on the use of attenuated vaccine strains,
passaged in tissue culture, the MID of wild RSV is probably less. ID-50 values for enteric
pathogens can also be obtained from the Quantitative Microbial Risk Assessment Wiki site
(QMRAwiki) at: http://wiki.camra.msu.edu/index.php?title=Table_of_Recommended_BestFit_Parameters
Evidence for transmission of rhinovirus and RSV infections via contaminated hands to the
eye or nose comes from a number of studies. A number of these investigations have
57
demonstrated that self-inoculation by the rubbing of the nasal mucosa or conjunctivae with
rhinovirus-contaminated fingers can lead to infection:
• Hendley et al.(1973)260, found that dried rhinovirus could be picked up by the fingers
from skin or environmental surfaces contaminated by shedding from subjects with
rhinovirus colds. Four of 11 volunteers became infected after touching their nasal or
conjunctival mucosa with fingers previously contaminated by rubbing a dried drop of
rhinovirus.
• Reed (1975)261 recovered rhinovirus from the fingers of 16 of 38 volunteers swabbed
during the acute stages of infection. Volunteers could infect themselves if a moderately
heavy dose (88 TCD50) of virus was inoculated on the finger and then rubbed into the
conjunctiva or nostril, especially if the inoculum was still damp. From estimates of virus
titres in nasal washings and on fingers, and of amounts transferred by rubbing, it was
concluded that spread of colds is unlikely to occur via objects contaminated by the
hands of the virus-shedder, but recipients might pick up enough virus by direct hand
contact with heavily infected skin or secretions to constitute a risk of self-inoculation
via the conjunctiva or nostril.
• Gwaltney, Moskalski and Hendley (1978)262 showed that hand transfer of rhinovirus
from experimentally infected volunteers to susceptible recipients was very efficient: 11
of 15 hand-contact exposures initiated infection, compared with one of 12 largeparticle (P < 0.005) and none of 10 small-particle (P < 0.005) exposures.
• Gwaltney and Hendley (1982)263 examined transfer of experimental rhinovirus infection
by an intermediary environmental in healthy young adults by having recipients handle
surfaces previously contaminated by infected donors and then touching their nasal and
conjunctival mucosa. Five (50%) of 10 recipients developed infection after exposure to
virus-contaminated coffee cup handles and 9 (56%) of 18 became infected after
exposure to contaminated plastic tiles. Fifty-six per cent (9/16) of recipients exposed to
untreated tiles became infected.
• In 1992, Gwaltney and Hayden269 reported that, over a period of 10 years they
performed intranasal challenges on 343 healthy young adults who had no antibody to
the challenge, and infected 321 (95%).
• Hall et al.(1978) found that volunteers touching contaminated objects and, or the
fingers, of symptomatic individuals had a higher attack rate of colds if they touched
their eyes or nose.271 In another study they showed that close contact with
symptomatic infants infected with RSV, who were producing abundant secretions, or
their immediate environment, was necessary for infection.272
1.2.3 Lower respiratory tract infections
Globally, acute lower respiratory infections (ALRIs) such as pneumonia and bronchitis cause
up to 4 million deaths annually, mostly of children, the major burden of disease falling in
developing countries. There is little data showing whether hygiene plays any significant role
in the spread of ALRIs. However, in 2005, Luby et al. reported a study of the impact of
handwashing on pneumonia in children under 5, in squatter settlements in Karachi,
Pakistan. 289 Results indicated a 50% reduction in pneumonia in the intervention compared
with the control group. Luby et al. assess that a link between hand washing and the
prevention of pneumonia in developing countries is plausible on the basis that, in developing
countries, viruses commonly cause pneumonias. It is also known that some viruses that
infect the respiratory tract are readily transmitted from person to person via hands. Viruses
that cause RT infections can predispose children to bacterial pneumonia.
58
1.2.4 Other respiratory pathogens
Legionnaires’ disease
Legionnaires’ disease is believed to occur worldwide, but the incidence varies widely. 290 The
majority of reported cases are either community-acquired (in public settings), nosocomial
(acquired in healthcare settings) or travel-associated, but some cases are thought to be
domestically acquired. In Germany, 49% of notified Legionella infections are estimated to be
acquired at home. 291 Legionella pneumophila and other Legionella species are found
naturally in the environment and thrive in warm water and warm damp places. 292
Investigations have shown that shower heads and hot water taps can produce aerosols
containing low numbers of L. pneumophila during routine use. 293 The aerosol particle size
generated would be small enough to penetrate the lower human respiratory system.
Infection results from inhalation of contaminated water sprays or mists which can occur in
the home in association with showers, spas and hot tubs. An infected source can
disseminate sprays or droplets of water containing Legionellae. When this occurs, most or all
of the water in the droplet evaporates quickly, leaving airborne particulate matter that is
small enough to be inhaled. Particles of less than 5 μm in diameter can be deeply inhaled,
and enter the respiratory airways to cause legionellosis. Risk factors for community or
domestic-acquired legionellosis include: age over 40 years, smoking, immune-suppression,
and chronic debilitating illnesses. There is no evidence of person-to-person transmission.
Legionella infections have also been reported among previously healthy people, including
young people without underlying disease, and those without other known risk factors. 294
Examples illustrating the potential for infection transmission in the home via domestic
shower units, hot tubs etc. is as follows:
• L. pneumophila was isolated from 30% of hot water distribution systems in apartment
buildings in Finland, the highest concentration being in the shower water. 295
• Pedro-Botet et al. 296 evaluated 4 surveys (US, Canada and Germany) where
Legionella was isolated from 6-32% of environmental samples taken from homes.
They also reviewed 9 anecdotal cases of Legionnaires’ disease linked to homes or
apartments colonised by Legionella pneumophila, and 4 prospective studies of
community-acquired Legionnaires’ disease linked to homes. Overall they concluded
that the risk for individuals residing in homes colonised with Legionella pneumophila
appears to be low.
• During August 2006, there was an increase in non-travel related Legionella cases in
England and in The Netherlands, possibly associated with fluctuating weather
conditions in July. In August and September, 8 cases were reported but no common
source could be established. Legionella was isolated from the homes of 2 patients (2
showerheads in one home and a hot tub in the other) but unfortunately clinical isolates
were not available for genetic typing. The incident team concluded that multiple
sources (both domestic and environmental) may have caused the cluster. 297
• In Italian houses, Legionella contamination of domestic hot water ranges from 22.6%
of 146 samples from a multi-centre investigation around the country 298 to 41.9% of
samples obtained from 59 apartments in Bologna. 299
• Legionella pneumophila is responsible for 6-11% of community-acquired pneumonias.
While association with contaminated cold and hot water supplies, condensers, spa
pools, thermal springs or respiratory therapy equipment has been documented, garden
hoses have not yet been linked to Legionnaires’ disease. 300
• Wallensten et al.(2010) reported a newly identified risk factor for Legionnaires'
disease. The researchers found that professional drivers are five times more
commonly represented among community acquired sporadic cases in England and
Wales than expected. An increased risk of Legionnaires’ disease is associated with
59
driving through industrial areas and driving or being a passenger in a vehicle with
windscreen wiper fluid not containing added screen wash. 301
Mycobacterium avium
Two studies suggest that showers may be a source of infection by waterborne M. avium:
• Falkinham et al.(2008) report that Mycobacterium avium was isolated from hot and
cold water samples and from sediment (biofilm) collected from the showerhead in the
home of a woman with M. avium pulmonary disease lacking known M. avium risk
factors 302. DNA fingerprinting demonstrated that M. avium isolates from the hot and
cold water and showerhead sediment demonstrated clonal similarity with the patient's
M. avium isolate.
• Feazel et al.252 analysed rRNA gene sequences from 45 showerhead sites (including
apartment blocks) around the US. They found that complex microbial assemblages
occur inside showerheads. They reported that sequences representative of nontuberculous mycobacteria (NTM) and other opportunistic pathogens are enriched to
high levels in showerhead biofilms. Mycobacterium avium was found in 20% of
showerhead samples and accounted for an average of 32% of the microbes found.
The organisms were not however found in the aerosols produced by the shower. The
authors concluded that this may be because the mycobacteria are released at the start
of the shower and then diluted as the shower progressed.
Pseudomonas aeruginosa and Stenotrophomonas maltophilia
P. aeruginosa and Stenotrophomonas maltophilia are opportunist pathogens that are a risk
to patients with increased susceptibility to infection including those who are cared for at
home. 303 P. aeruginosa is widespread in the environment and is isolated from soil, water,
plants and some vegetables:
• Studies have shown that wet sites such as sinks, tap water outlets and toilets in
hospitals are often colonised with P. aeruginosa and may be a source of infection in
ICUs. 304
• An investigation in German hospitals showed a correlation between strains of P.
aeruginosa isolated from patients with cystic fibrosis (for whom P. aeruginosa is a high
risk) and from environmental sites, such as sink U-tubes, toilets, cloths and other
sites. 305,306,307,308
• Doring et al.(1991) 309 demonstrated transfer of P. aeruginosa from contaminated
hospital sinks to the hands during hand-washing.
• Studies by Scott and Bloomfield (1985) 310 suggest that in hospitals, where P.
aeruginosa is prevalent, it can become established as a secondary source/permanent
reservoir in toilets, and are spread to surrounding sites in aerosol particles generated
by toilet flushing. It was found that, whereas P. aeruginosa was isolated from toilet
surround surfaces (toilet seat, flush handle, and floor) in 8 out of 144 samples taken
from toilets cleaned daily but not disinfected (where sampling of the toilet itself
indicated the presence of residual persistent contamination with P. aeruginosa in 58
samples), no samples positive for P. aeruginosa were obtained from surfaces
associated with toilets where a continuous release disinfectant was installed (where
only 8 samples from the toilet were positive for P. aeruginosa).
• Piper et al.(1997) 311 and Ferroni et al.(1998) 312 also report hospital infection outbreaks
traced to specific reservoirs, such as sinks and also tap water.
• A 2009 review by Kerr et al. shows that environmental reservoirs of P. aeruginosa are
readily identifiable, and reviews outbreaks attributed to environmental sources. 313
• A study in a UK cystic fibrosis (CF) centre 314 evaluated samples from staff, patients
and the environment (drains, bath tubs, showers). P. aeruginosa was isolated not only
from patients' hands, clothes and bed linen, but was also detected in the majority of air
60
samples from inside the patients' rooms, the ward corridor and outpatient clinic,
suggesting that airborne dissemination plays a role in the spread.
• The Burkholderia cepacia complex (Bcc) is a multispecies complex of bacteria that
commonly cause respiratory infections in persons with cystic fibrosis (CF). Lucero et
al.(2011) investigated a cluster of Burkholderia cepacia complex colonization in
ventilated pediatric patients in hospitals. 315 Isolates from 15 patients, 2 sink drains, and
several ventilator components were found to belong to a single B. cenocepacia clone.
Hospital tap water used during oral and tracheostomy care was identified as the most
likely mechanism for transmission.
However, whereas this organism is quite frequently found in hospitals, indications are that, in
the absence of a known source, it is not commonly found in the home, although audit studies
of the home, as reviewed in section 4 show that the organism is sometimes found. The
infection risk for cystic fibrosis patients in the home is illustrated by 2 studies:
• Schelstraete reported a study of 50 newly infected patients attending a cystic fibrosis
centre. 316 P. aeruginosa could be cultured from 5.9% of the environmental samples
(mainly in the bathroom), corresponding to 18 patients. For nine of these, the
genotype of the isolate was identical to the patient's isolate.
• Denton, et al. 317 studied homes and hospital environments associated with 41
children with cystic fibrosis, a proportion of whom were colonised with
Stenotrophomonas maltophilia, an organism which commonly infects such children.
They reported widespread contamination with this organism in 36% of homes of
colonised children and 42% of homes of non-colonised children, from sites which
included dishcloths and sponges, washing up bowls, washing machines and a
kitchen work surface.
Streptococcus pneumoniae
Kellner et al. 318 describe outbreaks of multidrug resistant S. pneumoniae in 3 married
couples in Calgary. While S. pneumoniae outbreaks have been reported from a variety of
community settings, cases within households have rarely been reported. Outbreaks of the
disease generally occur in institutions with crowding, poor air quality, or increased host
susceptibility, but these factors can also exist within households.
1.3 CHAIN OF TRANSMISSION OF SKIN AND WOUND INFECTIONS
Skin and wound infections are common in the home and community. Within the home, the
primary source by which skin and wound pathogens are introduced into this setting is via
people who are infected – and possibly also via domestic animals. Fungal skin pathogens
can enter the home via the airborne route or via dust particles.
Van loo et al.98 found 36 S. aureus strains in 79 meat samples (including 2 samples
containing MRSA). Furthermore, low amounts of S. aureus are regularly found in meat sold
to consumers demonstrating that MRSA has entered the food chain. Persoons et al. in 2009
confirmed the presence of MRSA in broiler chickens indicating that MRSA may persist in
farm environments.99 Van Loo et al. concluded that the contamination of food products may
be a potential threat for the acquisition of MRSA by those who handle the food.
Skin and wound pathogens shed into the environment from human and animal can survive
for significant periods, and are readily spread around the home, to and from the hands and
via surfaces such as tap and door handles, telephones or other hand contact surfaces.
Infections can also be transmitted via clothing and household linens such as towels and bed
linen which come into direct contact with the skin. Contamination of the hands can occur by
61
handshaking or touching contaminated surfaces. Exposure of the skin to these agents may
produce colonisation and/or infection which usually occur where there are cuts, abrasions or
other conditions that damage the integrity of the skin. Some organisms, such as fungi which
cause superficial fungal infections, can invade and infect the intact skin.
Infectious agents which spread via these routes include bacteria such as S. aureus and
Streptococcus pyogenes, and viruses such as herpes simplex virus (cold sore lesions) and
varicella-zoster virus (chicken pox and shingles). Typical fungal infections are ringworm
(caused by Tinea capitis) and athletes foot (caused by Tinea pedis).
The risk of exposure to skin and wound pathogens in home and everyday life settings, as
illustrated in Figure 1, depends on the extent to which these pathogens are brought into the
home and the extent to which they are spread via hands and other sites and surfaces, and
by airborne transmission. Data on the survival and spread of skin and wound pathogens via
hands and surfaces in the home are summarised below (data on survival and spread via
clothing and household linens is reviewed in a separate IFH report). Taken together, it
suggests that exposure to skin and wound pathogens via the hands, clothing and linens, and
environmental surfaces etc is a frequent occurrence during normal daily activities, and that
the numbers of organisms transferred can be well within the numbers required to initiate
infection in a susceptible recipient.
1.3.1 Staphylococcus aureus and methicillin resistant Staphylococcus aureus (MRSA)
S. aureus is the most common cause of skin and soft tissue infections, which are mostly selflimiting, but a small proportion of cases, lead to severe invasive bacteremia or pneumonia. 319
A UK study 320 indicates a major increase in pathogenic community-onset staphylococcal
disease over the past 15 years. It was found that hospital admission rates for staphylococcal
septicemia, pneumonia, impetigo etc increased >5-fold. It was postulated that this trend may
be partly due to changes in hygiene behaviour.
MRSA in the home and community was reviewed in the 2006 and 2009 IFH reports1,8 which
show that MRSA is no means confined to the hospital setting. Infected patients discharged
from hospitals may continue to carry MRSA, even after their infection has healed, and pass it
on to healthy family members who become colonised, thereby spreading the organism into
the community and then back into hospitals. 321 Healthcare workers caring for MRSA-infected
hospital patients may also bring MRSA back into the home on their hands or uniforms etc.
MRSA has the same potential to infect the elderly and immuno-compromised in a home
setting, whilst family members who are MRSA carriers risk self-infection, following hospital
admission or outpatient treatments.
A new concern, as also reviewed in the 2006 IFH report on MRSA8 is the emergence of new
“community” strains of MRSA (community-acquired MRSA or CA-MRSA). Whereas
healthcare associated (HCA) MRSA strains are mainly a risk to vulnerable people, for CAMRSA any family member is at risk, although US experience suggests that CA-MRSA strains
present a threat mainly to those engaging in activities involving close skin contact and
abrasion such as sports clubs and schools. Some S. aureus strains circulating in the
community (both CA-MRSA and methicillin sensitive S. aureus strains (MSSA)) strains have
also acquired the ability to produce Panton-Valentine Leukocidin (PVL) toxin. These can
cause severe invasive infections such as bacteraemia, or necrotising pneumonia that kills
more than 40% of patients.
62
1.3.1.1 Sources of S. aureus in the home
Humans as sources of S aureus in the home
Household members who are, or have been recently infected, or who are carriers, are the
primary source of S. aureus infection in the home. People who carry S. aureus can shed the
organism in large numbers most usually associated with skin scales. 322,323 It is estimated that
between 30 and 60% of the general population 324 carry S. aureus as part of their normal
body flora. 325 People who carry S. aureus can shed the organism in large numbers into the
air and onto clothing in contact with the skin, most usually associated with skin scales.322 It is
estimated that around 106 skin squames containing viable organisms are shed daily from
normal skin 326 Solberg (2000)322 reported that whereas some people are extensive
shedders, others are not. Shedding also varies over time, and may increase when the carrier
has a cold or is under antibiotic therapy. Solberg presented the results of 157 patients with
persistent MRSA carriage and 18 patients with MRSA lesions in a medical department in
Bergen, Sweden. The numbers of organisms recovered from the hands of nasal carriers
varied widely, from 10 to 2 x 106 cfu. They also found correlation between the numbers
found on hands and the numbers liberated into air.
Establishing the prevalence of MRSA circulating in the general community is difficult and can
vary significantly from one area to another. 327 In the US, although it is concluded that MRSA
colonisation rates in the community are still low, it is thought to be increasing. 328,329 Graham
et al.325 reported an analysis of 2001-2002 data from the National Health and Nutrition
Examination Survey (NHANES) documenting colonisation with S. aureus in a noninstitutionalized US population. From a total of 9622 participants, it was found that 31.6%
were colonised with S. aureus, of which 2.5% were colonised with MRSA. Of persons with
MRSA, half were identified as strains containing the SCCmec type IV gene (most usually
associated with CA-MRSA), whilst the other half were strains containing the SCCmec type II
gene (most usually associated with HCA-MRSA). Other US studies suggest sporadic
distribution of CA-MRSA, with carriage rates ranging from 8-20% in Baltimore, Atlanta and
Minnesota, and up to 28-35% for an apparently healthy population in New York. 330
In the UK, indications are that the proportion of the general population carrying antibiotic
resistant strains of S. aureus is somewhere between 0.5-1.5%, the majority being carriers of
HCA-MRSA who are >65 years of age and/or have had recent association with a healthcare
setting. 331 Although cases of CA-MRSA and PVL-producing MRSA have been reported,
indications are that the prevalence of MRSA and PVL-producing strains circulating in the
community is small. 332 Although CA-MRSA strains are now a major problem in the US, 333
they are still relatively uncommon in Europe, and there is thus still an opportunity to avoid
the problem escalating to a similar same scale. CA-MRSA strains are reported not only in
UK, France, Switzerland, Germany, Greece, Ireland, Nordic countries, Netherlands and
Latvia. 334 The burden of MRSA infections across Europe is reviewed in a 2010 survey by
Kock et al. 335 who estimate that the proportion of CA-MRSA with respect to total MRSA
ranges between 1% and 2% in Spain and Germany and 29–56% in Denmark and Sweden.
Among outpatients with S. aureus infections, MRSA accounted for 6% in the Ligurian region
in Italy, 14% in Germany, 18% in France and 30% in Greece.
The potential for spread of MRSA to family members from healthcare workers in the home
was shown by Albrich et al.(2008), Ben-David et al.(2008), Zafar et al.(2007) and Aiello et
al.(2003). Albrich et al.(2008) evaluated data from 27 mostly high income countries. In 127
investigations, the average MRSA carriage rate among 33,318 screened health-care
workers was 4.6%, while 5.1% had clinical infections. Risk factors included chronic skin
diseases, poor hygiene practices, and having worked in countries with endemic MRSA. 336
According to Ben-David et al., transmission of MRSA in an ICU was observed despite
infection control precautions. Identifying and treating colonised healthcare workers (HCWs)
63
was followed by a significant reduction in the incidence of MRSA. Unrecognized MRSAcolonised HCWs may be an important source of MRSA in the home. 337 The report by Zafar
et al.(2007) suggested that the frequency of CA-MRSA colonisation among household
members of patients with CA-MRSA infections is higher than among the general population.
Among colonised household members, only half of MRSA strains were related to the
patients' infective isolate. Within the same household, multiple strains of CA-MRSA may be
present. 338 Aiello et al. in a 2003 study found that the mean total log counts of bacteria were
5.73 and 5.24 for the homemakers and nurse hands, respectively. There were a higher
proportion of antibiotic resistant bacteria on the hands of the nurses. This study
demonstrates differences in prevalence, bacterial composition and antimicrobial resistance
of hand flora of hospital personnel compared with homemakers. 339
Domestic animals as sources of S. aureus exposure in the home
Indications are that staphylococci are commonly carried by animals, but tend to be hostadapted varieties. S. intermedius is the most common isolate from dogs. Domestic pets can
also be a source of S. aureus, including MRSA and PVL-producing strains. Although little
information is available on the prevalence of MRSA in the domestic animals, isolation from
household pets has been documented:
• Cefai et al.(1994) 340 reported persistent carriage of MRSA in a health-care worker
where the source or colonisation (or recolonisation) was identified as a domestic dog.
• Manian et al.(2003) 341 described two dog owners suffering from persistent MRSA
infection, who suffered from relapses whenever they returned home from the hospital.
Further investigation revealed that their dog was carrying the same strain of MRSA.
• van Duijkeren et al.(2004) 342 isolated MRSA from the nose of a healthy dog, the owner
of which worked in a Dutch nursing home and was colonised with MRSA. Typing of the
staphylococcal chromosome showed that the MRSA strains were identical.
• Rankin et al.(2005) 343 carried out a study to determine the presence of S. aureus PVL
toxin genes in MRSA strains isolated from companion animals. Eleven MRSA isolates
from 23 animals were found to be positive for the PVL toxin genes as well as for
methicillin resistance (mecA) genes.
• Enoch et al.(2005) 344 reported a pet therapy dog that acquired MRSA in a UK district
general hospital after visiting care-of-the-elderly wards. The dog and owner were
asymptomatic and had no observable source of MRSA. Two other pet therapy dogs,
screened before visiting the hospital, were found to be MRSA negative. Further
investigations suggested that the dog was colonised by contact with a human carrier.
• A colonisation prevalence of study in clinically normal dogs by Vengust et al. in 2006 in
Ontario, Canada reported that at present Methicillin-resistant Staphylococcus
intermedius (MRSI) is not considered to be a significant zoonotic concern; however, it
may become an important pathogen in dogs. Although Methicillin-resistant coagulase
negative staphylococci mostly cause disease in compromised human or animal hosts,
these bacteria can serve as reservoirs of resistance determinants in the community,
which could lead to the emergence of novel MRSA strains. 345
• Sing et al.(2008) reported transmission of PVL-positive MRSA between a symptomatic
woman and both her asymptomatic family and their healthy pet cat. This case
illustrates that MRSA transmission also occurs between humans and cats and that
pets should be considered as possible household reservoirs of MRSA that can cause
infection or reinfection in humans. 346
Transmission of S. aureus (including MRSA) between humans and cats and dogs is further
reviewed by Oehler et al.(2009). 347 Several workers have noted that MRSA in pets is closely
linked to MRSA in humans and concluded that that the source of MRSA in pets or other
animals may often be colonised or infected humans, although this is by no means proven. 348
64
A one day survey conducted at a veterinary hospital in February 2004 by Loeffler et al.
2005 349 identified MRSA carriage in 17.9% of veterinary staff, 9% of dogs, and 10% of
environmental sites. CA-MRSA has also been identified in livestock animals (particularly
pigs), veterinarians, and animal farm workers. Angelo et al.(2009) reported a case of
infection in a pig-farm worker in an animal farming area in Italy. The infection was caused by
MRSA of swine origin, ST398. 350 Veterinary staff and owners of MRSA-infected pets are
high risk groups for MRSA carriage despite not having direct hospital links. As part of a UKwide case-control study investigating risk factors for MRSA infection in dogs and cats
between 2005 and 2008, 608 veterinary staff and pet owners in contact with 106 MRSA and
91 methicillin-susceptible S. aureus (MSSA)-infected pets were screened for S. aureus nasal
carriage. This study indicated for the first time an occupational risk for MRSA carriage in
small animal general practitioners. 351
In a 2011 review, Kassem conclude that, besides humans, perhaps the most important
community reservoirs of staphylococci are pets and livestock. 352. He cites evidence showing
that MRSA has been isolated from pigs, horses, dogs, cats, cattle, sheep, chinchillas, and
parrots. Targeted sampling suggests that up to 8% of dogs, 12% of horses, 15% of lactating
cows, 14.3% of broiler farms, and 68% of fattening pig farms were potentially positive for
MRSA. In many cases, MRSA clones from animals were shared by their owners and/or
handlers, suggesting the possibility for MRSA transmission between animals and humans
1.3.1.2 Survival and spread of S. aureus in the home
The potential for exposure to S. aureus (including MRSA) following shedding from a human,
animal, or other source depends on the extent to which dispersal and persistence of S.
aureus can occur during normal daily activities. Although S. aureus cannot multiply outside a
human or animal host, it is particularly resistant to dessication and can survive in the
environment for significant periods of time. Survival and transfer of S. aureus via hands and
surfaces is shown by a range of laboratory and field studies as follows. Survival and transfer
of S. aureus via clothing and household linens is reviewed in a separate IFH report29:
• Kramer et al.154 review data showing that S. aureus (including MRSA) can survive on
dry surfaces for periods from 7 days up to 7 months.
• Wagenvoort et al. 2000353 studied long term survival suspensions of 2 outbreak and 3
sporadic MRSA strains, with and without added hospital dust. A gradual decline was
noted for all strains. All survived longer than six months, but the two outbreak strains
survived significantly better and for 1–3 months longer. Survival patterns of the MRSA
strains with and without added dust were similar.
• Makison et al. in a 2006 study measured the effect of different humidities potentially
achievable on a hospital ward on survival of MRSA on hard surfaces. Surface type had
a greater effect on the rate of reduction of MRSA than humidity. 354
• Scott and Bloomfield 1990159 showed that when S. aureus was inoculated onto clean
cloths and surfaces (200-300 cfu/sq cm) and allowed to dry, the organism could be
isolated from surfaces for up to four hours, and on soiled surfaces for up to 24 hours.
During a 4-hour drying period, up to 50% of S. aureus inoculated onto laminate could
be transferred to fingertips by contact. Transfer to fingertips also occurred cloths
contaminated with S. aureus were used to wipe clean surfaces.
• A study by Desai et al.(2009) showed MRSA may persist on contaminated surfaces for
>5 weeks. The study also determined that 3 s of skin contact with a MRSAcontaminated surface or object was all that was required to transfer MRSA to the skin
under laboratory conditions. 355
Studies on the survival and transfer of S. aureus in healthcare settings, are reviewed in the
2006 IFH report on MRSA8 and elsewhere. 356,357 The IFH report summarises results of 11
65
studies which show that, where there is an infected or carrier individual, MRSA can be
isolated from hands, environmental surfaces and cleaning utensils, including surfaces
frequently touched by hands such as computer keyboards, pens, television sets, etc and
also from clothing, mattresses, pillows, beds and chairs, and door handles. Although these
investigations were largely carried out in hospitals, they show the potential for contamination
of the home environment, where there is a family member carrying and shedding MRSA.
Other studies not included in the 2006 IFH report are as follows:
• Data reporting isolation of MRSA from the hands of patients or caregivers in settings
where there is an MRSA carrier are reviewed by Pittet et al.(2006)14
• Colbeck et al. 358 studied patients suffering from S. aureus infections in a Canadian
hospital. S. aureus was isolated on a number of occasions from baths and wash
basins.
• Oie et al.(1996) 359 report survival of MRSA on dry mops. Exner et al.(2004) 360 carried
out tests in which the first (field 1) of 4 flooring pieces was inoculated with S. aureus.
After drying, a mop was wetted with cleaning product, and swept over the
contaminated field followed by the other 4 fields and then back to field 1. Under these
conditions, water and surfactants did not achieve complete reduction of S. aureus in
Field 1 and the contamination was disseminated from Field 1 to other fields.
• Davies et al. 361 sampled 34 toys from 19 infants in an ICU in an Australian hospital.
MRSA was isolated from the toys of 6 infants, and from 1 of those infants.
• Bures et al. 2002 found that computer keyboards were uniformly contaminated by
MRSA throughout the ICU regardless of their proximity to patients or geographic
location. 362
• A 2006 study by Hardy et al. showed that MRSA was isolated from the environment at
every environmental screening, when both small and large numbers of patients were
colonised. Evidence strongly suggested that patients who acquired MRSA while in the
intensive care unit acquired MRSA from the environment. 363
• Wilson et al. in 2007 showed that 34 out of 52 colonised patients had a similar strain
found subsequently in their environment. Thus, it was interpreted that although MRSAcolonised patients frequently contaminates their environment, transmission from the
environment to the patient was relatively uncommon. 364
• In a culture survey by Trillis et al. in 2008, it was found that 42% of hospital privacy
curtains were contaminated with vancomycin-resistant enterococci (VRE), 22% with
MRSA, and 4% with C. difficile. Hand imprint cultures demonstrated that these
pathogens were easily acquired on hands. 365
• Giannini et al. studied contamination of toilet seats in a children's cancer hospital to
validate a policy requesting that immune-compromised children should use alcohol
wipes on the seats prior to use of the toilets. MRSA was recovered from 3.3% of
hospital toilets when wipes were not in use. Use of wipes resulted in a 50-fold
reduction in mean daily bacterial counts and eliminated MRSA. 366
• A 2006 study in an Indian hospital indicated that soap may act as a vector for spread
of S. aureus. 367
• A 2011 study of 40 MRSA carriers showed that hand contamination was equally likely
after contact with commonly examined skin sites and commonly touched
environmental surfaces in patient rooms (40% vs 45%). These findings suggest that
contaminated surfaces may be an important source of MRSA transmission. 368
There is evidence suggesting that airborne transmission may also be important for
transmission of S. aureus. 369 For example, an MRSA outbreak originating from the exhaust
ducting of an adjacent isolation room ventilation system was terminated once the ventilation
system was repaired and an opening in a window sealed. In a 2011 study evaluating the
potential for aerosol dispersal, Thompson et al. 370 evaluated survival of Staphylococcus
66
epidermidis, as surrogate for S. aureus, in aerosols at RH of <20%, 40-60%, 70-80% and
>90%. At all relative humidities, 13% of the initial aerosol was recovered after 5 h. RH did
not have a significant effect on the survival in aerosol form. Additional experiments indicated
that S. epidermidis was recoverable after five days at 76% humidity.
In recent years, a wide range of laboratory and field studies have been carried out that
focussed specifically on the spread of pathogens in a domestic setting. These studies show
that, in situations where good hygiene practice is not observed, S. aureus are readily
transferred in the home during normal daily activities via hands, cleaning cloths, hand
contact surfaces, clothing, linens and sometimes also via the airborne route such that family
members are regularly exposed:
• In studies of HCWs colonised with MRSA,340,45,46,371,372 the HCW was treated to
eradicate the organism, but subsequently became recolonised. In each case, MRSA
was isolated from environmental surfaces in the home of the HCW, including door
handles, a computer desk shelf and computer joystick, linens, furniture, and in some
cases also from other family members45,371,372 and family pets. Also, HCWs may
become a source of MRSA infection for their own families as well as for patients. 373
• A number of cases are reported where family members in the home of an infected
person have become colonized. 374,375,376,377 Hollis et al.374 found that transmission of
the MRSA strain from an index case to two siblings and the mother occurred at least
three times, and one family member was colonised for up to 7 months or more.
• Lis et al.(2009) evaluated the airborne Staphylococcus genus features in homes in
which inhabitants have had contact with the hospital environment and found a higher
prevalence of methicillin-resistant (MR) strains among the species isolated (40% of S.
epidermidis, 40% of S. hominis, and 60% of S. cohnii spp cohnii) was found in homes
of persons who had contact with a hospital environment compared with the reference
homes (only 12% of S. hominis). 378
• A sample of 35 homes of healthcare and non–healthcare workers, each with a child in
diapers and a cat or dog, was recruited from the Boston area between January and
April 2006. In each home, 32 surfaces were sampled in kitchens, bathrooms, and living
areas. S. aureus was found in 34 of the 35 homes (97%) and was isolated from all
surfaces in 1 or more homes, with the exception of the kitchen chopping board and the
child training potty. MRSA was isolated from 9 of 35 homes (26%) and was found on
kitchen and bathroom sinks, countertops, kitchen faucet handle, kitchen drain, dish
sponge/cloth, dish towel, tub, infant high chair tray, and pet food dish. A positive
correlation was indicated for the presence of a cat and the isolation of MRSA from
surfaces. 379
• Roberts et al.(2011) 380 studied the presence of MRSA on 509 frequently touched
nonhospital environmental surfaces at university, student homes and local community
sites. Twenty-four isolates from 21 (4.1%, n = 509) surfaces were MRSA positive and
included ten (11.8%, n = 85) student house samples, eight (2.7%, n = 294) university
samples and three (2.3%, n = 130) community samples. MRSA-positive university
samples were isolated from the bathroom, floors, ATM keypads, elevator buttons,
locker handles, but not computer keyboards. Two university ATM keypads were
sampled nine times over a 6-month time period. During that time, one keypad was
positive 3 (33%, n = 9) times for S. aureus including twice for MRSA and MSSA, while
the other was positive 4 (44%, n = 9) for S. aureus including once with MRSA and
three times with MSSA.
• Uhlemman et al. 2011 381 carried out a community-based, study of 95 case and 95
control patients. Case patients presented with CA-MRSA infections to a New York
hospital. During a home visit, nasal swabs were collected from index respondents and
household members and environmental surfaces were swabbed. Among case
households, 53 (56%) were environmentally contaminated with S. aureus, compared
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to 36 (38%) control households (p = .02), MRSA was detected on fomites in 30 (32%)
case households and 5 (5%; p = .001) control households. More case patients, 20
(21%) were nasally colonized with MRSA. In a subgroup analysis, the clinical isolate
(predominantly USA300), was more commonly detected on environmental surfaces in
case households with recurrent MRSA infections (16/36, 44%) than those without
(14/58, 24%, p = .04).
S. aureus in public places
Boost et al.(2008) examined levels of contamination of common-access environmental
surfaces over a 5-week period. 100 samples were collected from a range of publicly
accessed surfaces in a densely populated area of Hong Kong, with each of the 25 sites
being sampled 4 times daily. Of 500 samples, 11.2% yielded S. aureus. Frequently
contaminated sites were ATM machines (11.9%), drink vending machines (15%), ticket
vending machines (15%), escalator belts (10%), game center consoles (10%), public toilet
door plates (11.7%), elevator buttons (8.3%), travel card add-value machines (10%) and
door access keypads (13.3%). 382
1.3.1.3 Risks from exposure to S. aureus
Exposure to S. aureus can produce colonisation and/or infection which usually occur where
there are cuts, abrasions or other conditions that damage the integrity of the skin. Where
there are pre-disposing factors, the numbers of organisms required to produce infection may
be relatively small. Foster et al. estimated that less than 15 S. aureuscells were sufficient to
cause infection in experimental lesions. 383 Marples 384 showed that up to 106 cells may be
required to produce pus in healthy skin, but as little as 102 may be sufficient where the skin
is occluded or traumatised. Shinefield et al.(1963) 385 showed that it was possible to establish
set up a S. aureus carriage rate in the nose of 50% of newborn infants by the inoculation of
between 200 and 400 cocci. In experimental colonisation of burns on rabbits, an inoculum of
104 to 105 cfu. S. aureus was necessary for 100 % colonisation. 386 Foster and Hutt (1960)
reported that less than 15 S. aureus cells were sufficient to cause infection in experimental
lesions.383 Experimental models of staphylococcal disease, however, may bear little
resemblance to the natural disease in man. The risks associated with exposure to HCAMRSA and CA-MRSA are significantly different. HCA-MRSA usually affects the elderly and
those who are immuno-compromised, particularly those with surgical or other wounds or
who have indwelling catheters. For CA-MRSA, those at particular risk appear to be younger,
generally healthy people who practice contact sports or other activities that put them at
higher risk of acquiring skin cuts and abrasions.328 US experience suggests that CA-MRSA
may be more virulent than other strains and is easily transmissible within households and
community settings (e.g., schools, day care centers, sport teams) where skin-to-skin contact
or sharing of contaminated towels and sport equipment are vehicles for person-to-person
transmission. 387
The extent to which people may be exposed to pathogens through frequent close contact
with domestic pets is reviewed in section 1.1.1.
1.3.2 Other skin and wound pathogens
P. aeruginosa
Some skin infections attributable to P. aeruginosa are more likely to be encountered in
community settings. These include folliculitis and the green nail syndromes following
recreational exposure to water sources such as hot tubs, Jacuzzis and swimming pools, and
septic arthritis in injecting drug users.313 Zichichi et al. 388 reported 14 cases of P. aeruginosa
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folliculitis after shower/bath exposure. In all cases, P. aeruginosa was isolated from lesional
skin. In 3 families, P. aeruginosa was isolated in the well water. In further 3 families, P.
aeruginosa was isolated from bathroom and kitchen components.
Herpes simplex virus
Humans are the only known reservoir of herpes simplex virus 1 (HSV). It is most commonly
spread by oral secretions, and can be shed by persons with or without symptoms. HSV can
be recovered from the skin for up to 2 hours after inoculating the hands with the virus. 389 It
was found that the virus is more readily transmitted from moist drops than from drops which
had been allowed to dry, although touching dried virus-containing droplets on the skin with
moistened fingers results in transmission. Infectious HSV has been recovered from
environmental surfaces, such as doorknobs and toilet seats, but virus detection rapidly
decreases with drying. 390,391,392 Turner et al. 393 examined 9 adults with virus-positive herpes
labialis. The virus was detected in the anterior oral pool of seven (78%) and on the hands of
six (67%); HSV isolated from patients with oral lesions were found to survive for up to 3
hours on cloth as well as 2 hours on skin, and 4 hours on plastic. Nerurker et al. also found
that HSV survived for up to 4 hours on plastic surfaces. 394
Varicella-zoster virus
A recent study demonstrated the rapid and broad contamination of the environment with
varicella-zoster virus (VZV) when a family member acquired the disease. 395 Eight days after
onset of the index case VZV DNA was detected in both samples from the patient and on the
surfaces of an air-conditioning filter, a table, television channel push-buttons and a door
handle. The virus was also detected on the hands of the parents and the children. Two
siblings developed the disease 18 days after onset of the index case.
Another study by Yoshikawa et al.(2001) showed that rapid and widespread VZV DNA
contamination may occur with a patient with zoster (shingles). Positive surfaces for VZV DNA
from the room environment of a patient with zoster included the back of a chair, table, doorknob and the air conditioner filter. 396
1.4 CHAIN OF TRANSMISSION OF EYE AND EAR INFECTIONS
Conjunctivitis is a very common eye condition in the community, and is an inflammation of
the conjunctivae, the mucous membranes covering the white of the eyes and the inner side
of the eyelids. Bacterial conjunctivitis is caused by strains of staphylococci, streptococci or
haemophilus which may come from the patient’s own skin or upper respiratory tract or from
another infected person. Viral conjunctivitis is often associated with the common cold and
may be caused by adenoviruses. Viral conjunctivitis can spread rapidly from person-toperson, between people and may cause an epidemic of conjunctivitis. Chlamydia
trachomatis may also be a cause of conjunctivitis. Babies and small children are particularly
susceptible to infective conjunctivitis and can develop severe forms of the condition. One of
the most important pathogens in kerato-konjunvctivitis associated with contact lenses is P.
aeruginosa where unhygienic behaviour is a risk factor. 397,398
A number of studies carried out in ophthalmology clinics have demonstrated the role of hand
hygiene in preventing the transmission of adenoviral keratoconjunctivitis. 399,400 Jernigan et
al. 401 showed that the hands of physician and patients remained culture-positive for the
incriminated adenovirus even after washing hands with soap and water and drying them with
a paper towel. Azar et al. 402 recovered infectious adenoviruses from the hands of 46%
(12/26) of the patients with epidemic keratoconjunctivitis indicating the potential for virus
transfer to hospital personnel through casual hand contact.
69
Otitis externa attributable to P. aeruginosa is more likely to be encountered in community
settings. It can manifest as severe, potentially life-threatening malignant otitis externa in
patients with diabetes and immune-compromised individuals.297
Tjen et al.(2007) reviewed Pasteurella multocida meningitis and otitis media infections
transmitted by contact with household pets. 403 Tjen reports that animal exposure is reported
in 89% of cases of P. multocida meningitis, the majority without known bites or scratches,
whilst Otitis media has been documented or strongly suspected in 24% of cases.
2. CLOTHING AND HOUSEHOLD LINENS AS VECTORS FOR TRANSMISSION OF INFECTION
Recently, there has been renewed interest in the role of clothing and household linens in
spread of infectious disease in the home, particularly in relation to their potential role in
transmission of MRSA and Clostridium difficile, but also because of concerns about the
increasing numbers of people in the general community who are more susceptible to
infection. There is also concern regarding the availability of detergents active at ambient
water temperatures and about how well washing techniques at lower temperatures reduce or
eliminate pathogens. There is evidence to show that transfer of pathogens can occur
between contaminated and clean laundry during the washing cycle. The infection
transmission risks associated with clothing and household linens are assessed in a separate
IFH report.29
3. AUDITS OF MICROBIAL CONTAMINATION IN THE DOMESTIC ENVIRONMENT
Over the last 30 years a whole range of studies have been carried out to evaluate the
distribution of micro-organisms in the domestic environment (Finch et al.(1978), 404 Scott et
al.(1982) 405, Speirs et al.(1995), 406 Josephson et al.(1997), 407, Rusin et al.(1998), 408, Tierney
et al.(2002), 409 Ojima et al.(2002), 410 Toshima et al.(2002), 411, Sharp et al.(2003), 412 Rice et
al.(2003), 413 Haysom et al.(2005), 414 Scott et al.(2009)26). The majority of these audit studies
have been carried out in developed country situations including UK, Japan and the US, but
recently studies have begun to appear which look at contamination in homes in developing
country situations such as Mexico and Cambodia (Chaidez and Gerba (2000) 415, Carasco et
al.(2008), 416 Medrano-Felix et al. (2010), 417 Sinclair and Gerba (2010) 418). These studies
differ from those described earlier in this review, in that there was no attempt to recruit
homes where there was a known infected person.
The studies looked for a range of organisms including pathogens such as Salmonella,
Campylobacter and norovirus, and potential pathogens such as P. aeruginosa and S. aureus
(including MRSA). In many or most studies, the presence of E. coli, coliforms and/or
Enterococcus faecalis was evaluated as an indicator of residual faecal contamination from
humans or animals, or from raw foods such as meat or poultry. Although many/most species
of E. coli are not normally pathogenic to the healthy adult, they are regarded as indicators of
poor hygiene.
Suprisingly, given their importance, relatively few studies looked at contamination of hands
during normal daily activities, most studies focussed on contamination of environmental
sites.
3.1 AUDIT STUDIES OF CONTAMINATION OF ENVIRONMENTAL SITES AND SURFACES IN THE HOME
The studies, as summarised below, indicate that wet sites such as kitchen sink areas
(particularly sink surfaces, draining board, U-tubes), toilets and nappy buckets are most
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commonly associated with heavy contamination and the occurrence of E. coli and coliforms.
Almost universally, dishcloths and other wet cleaning utensils were also found to be
frequently and heavily contaminated. For these “reservoir” sites, typically, from 10% up to as
much as 30% of samples were contaminated with these species. Counts varied significantly,
but in some cases, particularly for dishcloths and dish sponges, counts up to 107 cfu per
sample were obtained. These results suggest that, in the kitchen, wet areas such sinks,
waste traps cleaning cloths etc can act as semi-permanent sources or reservoirs which
harbour and encourage the establishment of free-living bacterial populations. Similarly, in the
bathroom or toilet, although enteric bacteria probably originate from the toilet or directly from
humans, baths, basins, cleaning cloths and face cloths may form semi-permanent reservoirs
of bacteria. These conclusions are supported by laboratory studies146,152,153 which
demonstrate the ability of Gram-negative species such as E.coli, Klebsiella spp. and
Pseudomonas to grow to substantial numbers in samples of sink U-tube and toilet water, and
in wet cloths. Additionally, although less frequently, potentially harmful organisms are quite
often isolated from hand and food contact surfaces in the bathroom and toilet as well as the
kitchen, although the numbers are usually relatively small.
Haysom and Sharp studied changes in contamination levels at five key sites in 10 UK
domestic kitchens during a period of 24 hours414. Colony counts and Enterobacteriacae
counts varied during the day, peaking after meal preparation and generally falling overnight.
Contamination levels were lower in vegetarian than in non-vegetarian households.
Enterobacteriacae spp. isolated in the 1982 study of 200 UK homes by Scott et al. included
Klebsiella, Enterobacter, Citrobacter, Proteus and E. coli. Salmonella and Campylobacter
were not isolated.405 A similar pattern was also reported by Finch et al.(1978)404 and Speirs
et al.(1995).406 In Josephson’s study,407 of 10 US homes sampled over a period of 19
months, Salmonella was isolated once (from a sponge) and Campylobacter twice (from
sinks). Tierney et al.(2002)409 sampled the sink, draining board and tap surfaces in 35
kitchens in Ireland; both E. coli and Salmonella were isolated; isolation rates ranged from 1250% for E. coli and 8-30% for salmonella. By contrast, in a study of 100 dishcloths and
sponges from domestic kitchens, Hilton and Austin (2000)182 did not detect the presence of
Salmonella or Campylobacter in any samples. The fact that in many of the audit studies,
primary pathogens such as Salmonella and Campylobacter were not isolated, should not be
taken as an indication that these organisms do not occur in the home; it must be borne in
mind that the number of homes surveyed was relatively small in global terms, and the homes
were evaluated at random under "normal" conditions. From an investigation of 140 sponges,
and from 56 dishcloths from US homes, Enriquez et al. 419 however reported that, although
the most common bacteria were Enterobacteriacae and Pseudomonas spp., Salmonella spp.
was identified in 15% of sponges and 14% of dishcloths. Rice et al.413 also reported frequent
isolations of Salmonella from the contents of household vacuum cleaner bags. A total of 16
bags from 79 bags were found to be positive for S. enterica. Contamination however was
associated with occupational exposure to Salmonella, such as cattle farms with known
salmonellosis. None of the 12 out of 79 of the samples which were taken from homes where
occupants had no exposure to livestock or exposure to S. enterica in the workplace were
found to be positive for S. enterica. Chaidez and Gerba also reported that the most
frequently occurring enterobacteria in a survey of 50 cleaning tools from Mexican domestic
kitchens was Salmonella and Klebsiella pneumoniae, isolated from 9.8% and 4.9% of
sponges respectively.415 In a 2009 study of 32 surfaces in kitchens, bathrooms, and living
areas in 35 homes of healthcare and non–healthcare workers in Boston USA, Scott et al.
obtained 2 isolates of Salmonella spp., one from the toilet bowl and one from the bathroom
tub. Shigella spp. was isolated on 1 occasion from the kitchen counter top, but Escherichia
spp. was rarely isolated.26
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In a survey of 213 homes, Listeria spp. were found in about 47.4% of homes and were
recovered from wet sites such as kitchen sinks, dishcloths and washing up brushes, the
refrigerator and the toothbrush. 420 Spiers et al.(1995)406 isolated Listeria monocytogenes
from fridge surfaces in 2.2% of homes. Yersinia enterocolitica was also isolated from the
sink area in 4.2% of homes, and Bacillus cereus from 10.9% of homes. A UK study also
found 84% of dishcloth samples contaminated with Listeria spp. 421 A study in Portugal 422
showed that Listeria mononcytogenes was present in 3/68 domestic refrigerators. L. grayi
and L. inoccua were isolated from four and one refrigerators, respectively.
In their study of 86 Tokyo Metropolitan households involving around 100 sites in each home,
Ojima et al.410 found S. aureus at most sites in 1 or more homes. Highest isolation rates were
from sinks, drains, floors showerheads, futons and pillows where isolation rates of 10% or
more were recorded. Maximum counts were mostly of the order of around 100 cfu per
sample. S. aureus was detected on the arms of 5.4% of housewives and 4.0% of children. It
was detected on items in households with carriers and households without carriers at
statistically different rates of 10.7% and 3.5% respectively. Enriquez et al.(1997)419 recorded
the presence of S. aureus in 20% of household sponges and 19% of dishcloths. Hilton and
Austin (2000)182 sampled 100 dishcloths and sponges from domestic kitchens and isolated S.
aureus from 4% of sponge-type cloths, ranging from 102 to 4 x 104 cfu/ml. The total viable
count from all cloth types ranged from 20 to 6 x 108 cfu/ml. Scott et al. sampled a total of 32
surfaces in kitchens, bathrooms, and living areas in 35 homes of healthcare and non–
healthcare workers in Boston USA, each with a child in diapers and either a cat or dog in the
home. S. aureus was found in 34 of the 35 homes (97%) and was isolated from all surfaces
in 1 or more homes, with the exception of the kitchen chopping board and the child training
potty. MRSA was isolated from 9 of 35 homes (26%) and was found on kitchen and
bathroom sinks, countertops, kitchen faucet handle, kitchen drain, dish sponge/cloth, dish
towel, tub, infant high chair tray, and pet food dish. 423
In their study of homes in the Boston area, Scott et al.423 also found P. aeruginosa in 4% of
35 homes where it was isolated from wet sites such as sinks and dishcloths but also from dry
sites such as a worktop and chopping board. Ojima et al.410 reported that detection rates for
P. aeruginosa were on the whole, low, but this spp. was found on items where coliforms
were detected, such as kitchen drains, dishwashing tubs, dishwashing sponges, sinks and
cleaning sponges and floors. Counts were generally less than 100 cfu per sample.
In a 2010 study Egert et al. 424 reported an evaluation of the microbial composition of biofilms
in domestic toilets by molecular means. Only 15 genera (representing 121 sequences
affiliated with Acidobacteria, Actinobacteria, Bacteroidetes, Planctomycetes and
Proteobacteria) occurred in at least half of the samples or contributed at least 10% of the
sequences in a single biofilm. They concluded that virtually all ‘typical’ clones were closely
related to bacteria or to sequences obtained from environmental sources, implicating that the
flushing water is the main source of recruitment.
In June 2011, a new study was published that investigated the rubber sealing on the doors
of domestic dishwashers. 425 The study found Exophiala dermatitidis and Exophiala
phaeomuriformisin in around 30% of 189 domestic dishwashers sampled in multiple
locations across the world. The authors verbally reported that they had also found the
organism on plates and cutlery taken from the dishwashers. Although the organism is known
to be an opportunist pathogen (can cause systemic disease in humans and frequently
colonises the lungs of patients with cystic fibrosis) no incidents of infection from dishwashers
were reported. Exophiala is a fungus widely distributed in soil, plants, water and decaying
wood material. The somewhat odd spectrum of main sources of isolation (fruit surfaces,
steam baths, faeces and human tissue) suggests that a hitherto unknown, quite specific
natural niche must be concerned. Consistent occurrence in steam rooms of public bathing
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facilities suggests that the artificial environment of the steam bath provides a novel
environmental opportunity for this fungus.
A recent study sampled 118 hand-touched surfaces in buses, trains, stations, hotels and
public areas of hospital in central London and cultured MSSA from 8% of the sites but did
not find MRSA (Otter and French 2009). 426
Over the period 1999–2003 Reynolds et al. 427 carried out an evaluation of “public” surfaces.
They evaluated 1,061 environmental surfaces from shopping, day-care, and office
environments, personal items, and miscellaneous activities (i.e., gymnasiums, airports,
movie theatres, restaurants, etc.), in four US cities. Samples were analysed for faecal and
total coliform bacteria, and biochemical markers. Biochemical markers, i.e., haemoglobin
(blood marker), amylase (mucus, saliva, sweat, and urine marker), and urea (urine and
sweat marker) were detected on 3%, 15% and 6% of the surfaces, respectively. Protein
(general hygiene marker) was present on 26% of surfaces. Surfaces from children's
playground equipment and day-care centers were the most frequently contaminated. Half
and one-third of the sites positive for biochemical markers were also positive for total and
faecal coliforms, respectively. Artificial contamination of public surfaces with an invisible
fluorescent tracer showed that contamination from outside surfaces was transferred to 86%
of exposed individual's hands and 82% later tracked the tracer to their home or personal
belongings.
3.2 AUDIT STUDIES OF CONTAMINATION OF MOBILE PHONES, COMPUTER KEYBOARDS ETC
A number of investigations have been carried out to evaluate the potential for transmission
of infection via mobile phones. The majority of these were mobile phones of healthcare
workers (HCWs) working in hospitals. The studies were conducted in the US and Israel, 428
UK 429, Saudi Arabia 430 and India. 431 Isolates from mobile phones of HCW included S. aureus
(both MRSA and MSSA), E. coli, Klebsiella pneumoniae, P. aeruginosa and E. faecalis.
Goldblatt et al.428 reported that one-fifth of cellular telephones examined were found to
harbor pathogenic microorganisms, whilst Sadat-Ali et al.430 reported that (43.6%) HCWs
carried infective organisms on their cell phones. O’Connor et al. 432 studied 100 municipal
public telephones cited in Belfast, Ireland during the summer of 2006. Phones were sampled
for the presence of MRSA, but no isolates were obtained.
Anderson et al. 433 investigated the keyboards of multiple-user (student) and single-user
(staff) computers located on a university campus. Contamination levels on multiple-user
computer keyboards was significantly greater than on single-user keyboards, and the
number of keyboards harbouring potential pathogens was also greater for multiple-user
computers. Overall, a greater number of different types of microorganisms were detected on
the keyboards of the multiple-user computers. Forty-seven percent of multiple-user
keyboards were found to be contaminated with S. aureus, compared to only 20% of the
single-user keyboards. In one multiple-user laboratory, 60% of keyboards contained either S.
aureus, E. coli and/or E. faecalis. Investigation of microbial contamination of computer
keyboards in hospital settings is also reviewed by Lu et al.(2009). 434
Kassem et al.(2007) 435 found 8% of the 24 university computer keyboards were MRSA
positive although they did not characterize the isolates. In contrast, in a second university
study, no MRSA were identified from 70 frequently used environmental surfaces, although
MSSA was isolated in computer keyboards, telephone mouthpieces and an elevator button
of a large Midwestern United States urban university (Brook et al. 2009) 436. Brook et
al.(2009) examined 70 frequently used environmental surfaces in a university of 25 000
individuals for contamination of S. aureus and MRSA from 420 samples taken from student
73
desktops, computer keyboards, telephone mouthpieces, water fountains, photocopy
keypads, vending machines and elevators buttons over a 3-week period in 2007.
Staphylococcus aureus was isolated from computer keyboards, telephones and elevator
buttons; however, no MRSA strains were isolated
Tekerekoglu report a 2011 cross-sectional study of the bacterial colonization on the mobile
phones (MPs) used by patients, patients’ companions, visitors, and healthcare workers
(HCWs). Significantly higher rates of pathogens (39.6% vs 20.6%, respectively) were found
in MPs of patients’ versus the HCWs’. There were also more multidrug pathogens in the
patents’ MPs including MRSA, extended-spectrum b-lactamase-producing E. coli, and
Klebsiella spp. 437
In a study of 60 rented DVDs obtained from 5 local DVD rental shops in Tripoli city, 438 S.
aureus was detected on 35 (58.3%), S epidermidis on 20 (33.3%) and P. aeruginosa on 3.
Messina et al. conducted a study to assess keyboard contamination, comparing results from
15 shared keyboards and 15 nonshared keyboards of 30 computers in use at the University
of Siena. 439 Microbes were recovered from all keyboards, with counts ranging from 6 cfu/key
to 430 cfu/key. Mould was not found on 8 keyboards, but was detected on all other
keyboards up to a maximum of 120 cfu/key. Yeast was found on 17 keyboards up to a
maximum of 420 cfu/key. Staphylococci were found on all keyboards but one at counts up to
120 cfu/key. Typing revealed S. aureus, S epidermidis, and Micrococcus spp. Enterococcus
was found on only 7 keys, including 6 shared keyboards, and was typed as E avium (1-31
cfu/key) (possibly related to presence of pigeons on windowsills). Pseudomonas was not
detected on any keyboard. S aureus was significantly more common on shared keyboards
than on nonshared keyboards (P= .03). Greater growth of Staphylococcus was found on
keyboards of users who ate at their desks
3.3 AUDIT STUDIES OF CHILDREN’S TOYS
Considering the potential infection risks from contaminated children’s toys, which are not
only frequent hand contact surfaces, but also carry the risk that they may come into contact
with children’s mouths, relatively few studies have been carried out to determine the levels of
contamination which can be found on these items:
• Hughes et al.(1986) 440 described a prospective study of 39 sterilized teddy bears. The
bears all became colonized with bacteria, fungi, or both within 1 week of being given to
children in the hospital
• Studies by Van et al.(1991) 441 and Pickering et al.(1986) 442 demonstrated
contamination of hands, toys, and other classroom objects with faecal coliforms in a
day-care setting. It was found that contamination increased during outbreaks of
diarrhoea.
• In 2000 Davies et al.361 carried out a survey of toys in the cots of infants in a neonatal
intensive care unit in a hospital in Melbourne, Australia over a 4-week period (86
cultures from 34 toys of 19 infants). Bacteria were grown from 84/86 samples (98%):
13 of the cultures grew MRSA, 4 group B streptococcus, 3 S aureus, 3 nonhemolytic
streptococci, 3 group D streptococci, 4 a-hemolytic streptococci, and 2 coliforms. None
grew fungi. Colonization rates did not differ with cot type, presence of humidity, toy
size or fiber length, or the fluffiness score. Eight (42%) of infants had positive blood
cultures and 5/8 of the isolates (63%) were of the same type as that colonizing their
toy.
• In a 2002 study in New Zealand of hard toys (Merriman et al.) 443 from general
practitioners’ waiting rooms relatively low levels of contamination were found, with only
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13.5% of 30 toys showing any coliform counts. There were no hard toys with heavy
contamination by coliforms or other bacteria (1 toy only had a coliform count >103). Soft
toys were far more likely to be contaminated, with 20% of toys showing moderate to
heavy coliform contamination (>103 per toy) and 90% showing moderate to heavy
bacterial contamination (103 – 105 per toy).
• Hanrahan et al.(2004) 444 found that eliminating toys in the neonatal intensive care unit
decreased the rates of nosocomial infections from 4.6 to 1.99 per 1000 patient-days
over a six-month evaluation period.
• In 2004, Avila-Aguero et al. 445 reported a study to determine whether toys were
contaminated with potentially pathogenic bacteria when they arrived in the hospital,
and whether they were contaminated in the hospital. After a first culture, toys were
cleaned with 4% chlorhexidine and water and were immediately re-cultured. Following
cultures were collected on days 5 to 7, 10 to 15, and every week until the ownerpatient was discharged. All first cultures were positive for at least 1 pathogen: 55
(78%) coagulase-negative Staphylococcus (CNS); 26 (37%) Bacillus spp; 13 (18%) S.
aureus; 8 (11%) alpha-hemolytic Streptococcus; 5 (9%), Pseudomonas spp; 2 (3%)
Stenotrophomonas maltophilia, and 6 (11%) other gram-negative organisms. After toys
were cleaned, subsequent cultures showed significant decreases in bacterial growth
rates. Because some patients were discharged, additional cultures were obtained for
only 31 toys.
• In a 2007/8 study by Naesens et al. 446 of 57 toys of 57 infants from two neonatal
intensive care units in a hospital in Belgium were analysed for their microbial load.
Before washing, 13/57 toys (23%) were positive for potential pathogens (8 for S.
aureus, 3 Enterococcus spp., 1 Klebsiella pneumoniae and 1 P. aeruginosa).
Postwashing cultures resulted in 5/57 (9%) positive cultures (4 revealed Enterococcus
spp., 1 S. aureus), which was a significant decrease compared with the pre-wash
cultures.
Other studies of contamination of toys are reported by Van et al. 1991 447, Suviste et al.
1996 448 and McKay et al. 2000. 449
In 2011 Chaidez et al. reported studies of contamination of children’s toys during play. In a
pilot study involving 12 children who had played in parks, sidewalks etc., the presence of
faecal coliforms was detected on hands and toys together with hepatitis A virus and Giardia
lamblia. 450 In an intervention study with 40 children, faecal coliforms were found on toys and
hands. S aureus and K. pneumoniae was found on hands at concentrations up to 2.4x104
and 1x104 per toy. On toys, E. coli and K. pneumoniae was found at concentrations up to
2.4x102 and 2.7x104 per toy. Salmonella spp. were also present on toys, whilst G lamblia
was found on toys and hands.
3.4 STUDIES IN DEVELOPING COUNTRY SITUATIONS
As stated above, a number of studies are now being published to examine households in
developing country situations, and to determine whether, and to what extent levels and types
of contamination are different.
Carrasco et al.416 studied 135 households in Ciudad Juarez, Mexico, and El Paso, Texas.
Five different kitchen surfaces and head of households’ hands were sampled. Sponge⁄
dishcloth samples were the most commonly contaminated, followed by countertops and
cutting boards. Isolation rates for wet sponges and sink faucet handles were 51% and 27%,
respectively for households in Mexico compared with 25% and 14% for households in
Texas, but these differences were not deemed statistically significant. Faecal coliforms were
75
recovered respectively from 13% and 5% of child care givers hands. This indicator was
moderately associated with self-reported failure to wash hands after visiting the toilet.
Medrano-Felix et al. 2010417 carried out a study to identify and quantify the presence of E.
coli, S. aureus, Salmonella, hepatitis A and norovirus in households in the city of Culiacan,
Mexico. Eleven sites in kitchen, bathroom, pet and children’s areas of two groups of 30
homes were sampled weekly for 6 weeks. One group (controls) were asked to continue their
normal cleaning and disinfection routine, whilst the other (intervention) group were given
specific training about cleaning and disinfection procedures. E. coli and S. aureus were
detected in both groups of homes. The frequency of isolation of these species was not
recorded, but the authors reported that the occurrence and concentration of bacteria in the
intervention households was less than in the control households. For E. coli, mean cfu log
counts per 900cm2 ranged from 0.5 to 4.0, with maximum counts between 7.0 and 10.0
being recorded. For S. aureus mean cfu log counts per 900cm2 ranged from 0.2 to 1.0, with
maximum counts between 6.0 and 8.0 being recorded. A total of 720 samples (360 kitchen
sponges and 360 dishcloths) from test and control group homes were tested for the
presence of Salmonella, hepatitis A and norovirus. Salmonella was present in 5 (1.38%) and
8 (2.22%) of the sponges and dishcloths analysed from both disinfection and control group
households, ranging from 300 to 110 000 MPN as minimum and maximum values. Several
of the isolated serotypes have been associated with foodborne outbreaks. Two samples
were positive for HAV, but norovirus was never detected.
In a paper published in 2010, Sinclair and Gerba51 set out to establish whether households
that have met the MDG metrics in a developing country by having an improved latrine, have
different concentrations of microbes than households in industrialized countries. To this end
they monitored faecal coliforms, total coliforms, E. coli and heterotrophic plate count bacteria
on household surfaces in 8 homes that possess improved latrines (i.e a pour-flush latrine) in
a rural village of Cambodia, and compared the results with similar data from homes in the
US408 and Japan.410 Surfaces which were sampled included the dipping ladle for sink water,
the table or counter for food preparation, the floor surface near kitchen sink, the cutting
board, the handle of the ladle for anal cleansing, the top of toilet (squat style) and the floor
surface around the base of the toilet. Faecal coliform levels in Cambodia were highest on
moist locations such as the plastic ladle used for sink water, the toilet seat surface and the
cutting board surface. For E. coli mean log cfu per 4 cm2 ranged from 0.5 to 4.0 with highest
counts of up to 4 logs found on the top of the squat toilet, the wash basin and the floor
around the toilet and the well. Faecal coliform levels were 100-fold higher than that for
equivalent surfaces in the US and Japanese studies. They found that the top of the squatstyle toilet was highly contaminated with faecal coliforms. These ceramic pour-flush bowls
have two positions on either side of the toilet bowl for the user’s feet. Although made from
the same smooth ceramic material as the bowl, the tread positions have grooves where
water can pool allowing the area to be moister than the surrounding floor.
On the basis of the evidence which suggests that surfaces can have a significant role in
transmission of infections, the authors conclude that their results indicate that a latrine
barrier alone is only partially effective for household sanitation. For complete sanitation,
multiple environmental barriers may be necessary. When compared to homes in Cambodia,
homes in industrialized countries (US and Japan) have additional environmental barriers that
may control surface contamination including the chlorinated water distribution system, a solid
waste disposal system, a more elaborate home construction with easily washable surfaces
and cleaning product availability. Homes in these countries also have indoor climate control
systems and lower relative humidity than tropical Cambodia. The authors suggest that efforts
should be made to include as many pathogen control points as possible in hygiene and
sanitation improvement programmes.
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All eight houses sampled have similar stilt-house construction with elevated living and
sleeping quarters. Five of the eight houses had a kitchen attached to the upper level, while
the remaining houses had their kitchen area in an improvised zone under the house. Houses
were constructed with wooden walls and tile or corrugated metal roofs. These latrines were
built with a cement septic tank and PVC plumbing. Latrines and bathrooms were kept
relatively clean, but no soap or other cleaning material was seen with the exception of
powdered laundry detergent at one house. Dishes are washed with plastic scrub brush in
large plastic basins with water, which was obtained from the onsite well. The dishes are then
air-dried on a rack and sometimes wiped with a rag designated for the kitchen. There was a
plastic ladle cup, which is used to transfer water to the dish washing basins. Although no
pets were reported, many pigs, chickens, stray dogs and cats were seen in the all of the
house yards. Escherichia coli and enterococci on hands can be significantly increased by
various household activities, including those involving the use of soap and water
In order to study mechanisms of hand contamination with faecal indicator bacteria on
mothers’ hands, Pickering et al. carried out a household observational study combined with
repeated microbiological hand rinse sampling among 119 mothers in Dar es Salaam,
Tanzania. 451 Hand rinse samples were analysed for enterococci and Escherichia coli, and
selected samples were analysed for genetic markers of Bacteroidales, enterovirus and
pathogenic E. coli. Using the toilet, cleaning up a child’s faeces, sweeping, cleaning dishes,
preparing food and bathing all increased faecal indicator bacterial levels on hands.
Geometric mean increases in cfu per two hands ranged from 50 (cleaning dishes) to 6310
(food preparation). Multivariate modelling of faecal indicator bacteria as a function of
activities recently performed shows that food handling, exiting the household premises and
longer time since last handwashing with soap were positively associated with bacterial levels
on hands, while bathing was negatively associated. Genetic markers of Bacteroidales,
enterovirus and pathogenic E. coli were each detected on a subset of mothers’ hands.
Pickering et al. also studied the association between hand contamination and stored water
quality within households. 452 This study measured levels of E. coli, fecal streptococci, and
occurrence of the general Bacteroidales faecal DNA marker in source water, in stored water,
and on hands in 334 households among communities in Dar es Salaam, where residents
use non-networked water sources. Faecal contamination levels on hands of mothers and
children were positively correlated to fecal contamination in stored drinking water within
households. Household characteristics associated with hand contamination included
mother’s educational attainment, use of an improved toilet, an infant in the household, and
dissatisfaction with the quantity of water available for hygiene. In addition, fecal
contamination on hands was associated with the prevalence of gastrointestinal and
respiratory symptoms within a household.
In a study in developing country situations Luby et al. 453 studied 30 housing compounds: 10
received handwashing promotion with free soap, 10 received handwashing promotion with
free waterless hand sanitizer and 10 were non-intervention controls. Fieldworkers assessed
handwashing behaviour by structured observation but also collected hand rinse specimens.
Hand rinse samples were tested for thermotolerant coliforms and faecal streptococci and
Clostridium perfringens. The authors reasoned that the high variability of hand microbiology
assessments involving the most common indicator organisms, thermotolerant coliforms, E.
coli, and faecal streptococci have limited usefulness in evaluating handwashing interventions
By contrast C. perfringens is a potential alternative biomarker of faecal contamination
because it persists in the environment longer than E. coli and so may provide a more stable
indicator of faecal contamination. Although the data indicate that coliforms, faecal
streptococci and C. perfringens were isolated from hands in significant numbers (from 10 to
104) cfu, unfortunately the data was not presented in a manner which allowed assessment of
the frequency occurrence and concentrations of these organisms relative to hand sampling
carried out in developed country situations.
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3.5 AUDIT STUDIES OF HAND CONTAMINATION NORMAL DAILY LIVING
Considering the central role of hand hygiene, it is perhaps surprising that relatively few
studies have been carried out to audit hand contamination during normal daily activities. In
2003, Aiello et al.339 reported a prevalence study comparing the types of bacterial flora on the
hands of individuals in the community. Hand cultures were obtained from 204 homemakers
(defined as the person (usually the mother) who is the primary person responsible for
arranging childcare, cooking, cleaning etc] during a home visit. There 32 homemakers with
S. aureus on their hands. The five most prevalent species of bacteria found on the hands of
the 204 homemakers were: Pseudomonas fluorescens/putida (59), Staphylococcus warneri
(56), Klebseilla pneumoniae (44), S. aureus (32), and Enterobacter cloacae (26), E. faecalis
(20%). P. aeruginosa was not found on any hands.
In 2010, Judah et al. analysed swabs taken from the hands of 409 commuters at train
stations across the UK. Most common were Enterococcus in 22% of samples, followed by E.
coli in 9%, Klebsiella 2.5, Enterobacter 0.3%. 454 In another study 455 20 volunteers were taken
to a large, frequently visited British museum, or asked to travel on a bus or the underground.
They were asked to deliberately wipe their hands over hand contact surfaces such as
handrails, door handles and seats with the aim of contaminating their hands with whatever
bacteria were present. Out of 160 samples taken, sampling of hands showed that the
frequency of occurrence of different species was Enterococcus spp. (29%), Enterobacter
amnigenus 14%, Enterobacter cloacae 13%, Shigella 1% Klebsiella spp. 3%.
Staphylococcus spp. were not isolated. E. coli was isolated once from 160 samples taken
from a repeat experiment in which volunteers washed their hands before sampling.
Hand contamination studies in developing countries are described in the previous section
3.4.
4. AIR AS A SOURCE OF FUNGAL PATHOGEN AND BACTERIAL ENDOTOXIN EXPOSURE IN THE
HOME
Fungi (moulds) in indoor environments are a potential problem. They can be responsible for
infections, cause allergic responses, deteriorate/damage surfaces and cause unpleasant
odours. Moulds produce millions of spores, which, due to their small size (average size 1–5
µm) easily stay air-borne and may be breathed deep into the airways. Air-borne fungi are
usually associated with damp conditions, poor ventilation or closed air systems. Primary
sites of fungal growth are inanimate surfaces, including carpets and soft furnishings.17
The home provides reservoirs for opportunistic fungi that mostly cause infection in the
immuno-compromised community living at home. Infections caused by common indoor
moulds, such as Aspergillus, Penicillium, Fusarium, Rhizopus and Alternaria, are increasing
in HIV-infected and other immunodeficient patients.456 Some fungi are pathogenic to healthy
humans, causing superficial infections (mycoses), where the fungus grows on body surfaces
such as the feet, skin, hair and nails, as well as the oral or vaginal mucosa. They are spread
by direct contact and are highly contagious and easily spread to other individuals. Infections
within the body (deep mycoses) are rare in healthy humans but people with impaired
immune functions (e.g. cancer patients receiving chemotherapy or people with AIDS) are at
significant risk. They can be acquired by inhalation of spores or by entry through
wounds. 456,457
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There have been a number of studies investigating fungal species which can be found in the
home. In one study, spores of Penicillium spp. and Cladosporium spp. were isolated on
every occasion from at least one room in all homes. 458 Aspergillus spp. and other fungi as
well as yeasts were also isolated. Total airborne mould counts ranged from 0–41000 cfu/m3
but were usually in the range 50–1500 cfu/m3.
Visible mould was found in 46% of households in a cross-sectional study in Glasgow,
Edinburgh and London. 459 In a survey in central Scotland, the main fungus isolated from the
indoor air was Penicillium spp., with Cladosporium spp. being the next common. Pink and
cream yeasts were also isolated from the air in >90% of houses, with Rhodotorula and
Sporobolomyces being the main ones. 460 Higher airborne mould counts (1000–2000 cfu/m3)
were found in homes with visible mould. The fungi isolated from the air were similar to
homes surveyed in Europe 461, North America 462, Taiwan 463 and Canada 464 in which
Penicillium, Cladosporium and Aspergillus also predominated. A study of homes in Berlin
showed 63% having large amounts of viable fungal propagules and/or visible fungal
growth. 465 Penicillium, Cladosporium, Aspergillus, Mycelia sterilia and yeasts were
prominent. In one study in Australia, visible mould growth was present in every house at
some time during the study. 466
Aspergillus niger can grow in the topsoil of houseplants. In hospitals and homes, the soil
from a wide range of potted plants was found to be a major source of A. fumigatus, as well
as A. niger and A. flavus. 467 Bacteria, moulds and mildews may be found in air conditioning
equipment, humidifier reservoirs, dehumidifier drip pans and shower heads.
Fungal contamination of soft furnishings in the home has been documented in publications
by Cole and co-workers.17 Levels of fungal contamination in carpets and upholstery have
been shown to approach or exceed 100,000 cfu/gram and consist of potential aeroallergens,
such as Cladosporium, Alternaria and Penicillium. The predominating fungal contaminants
recovered from upholstered furniture include Cladosporium, Alternaria, Penicillium,
Aureobasidium and cream yeast. Other fungi recovered include Aspergillus versicolor,
Rhodotorula, Aspergillus fumigatus, Aspergillus flavus, Paecilomyces, Trichoderma,
Phialophora, Rhizopus, Ulocladium, Fusarium and Stachtbotrys. 468
Studies over the last decade have focused on the link between airborne bacteria and fungi,
associated with poor housing, and the incidence of respiratory allergies, such as asthma. 469
Fungal infections in the home and the role of hygiene in preventing fungal infections are
reviewed in more detail in a 2004 IFH review.7 Some further examples are as follows:
• In an Australian study of houses with visible mould growth at some time during the
study, asthma, atopy and respiratory symptoms in children were significantly
associated with indoor exposure in winter to fungal spores. Penicillium exposure was a
risk factor for asthma, while Aspergillus exposure was a risk factor for atopy.466
• An analysis of data collected in the winter of 1993-1994 in the framework of the
PEACE study (Pollution Effects on Asthmatic Children in Europe) showed that peak
flow variability was positively related to self reported moulds in homes of European
children with chronic respiratory symptoms. 470
• A high rate of morbidity related primarily to the upper airways, skin and mucous
membranes was found in children who had been living in indoor environments with
high levels of fungi. Also, the results of a sentinel case investigation of a family living in
an apartment with widespread visible fungal growth (predominantly Cladosporium and
toxigenic Stachybotrys chartarum) showed a marked improvement in their health after
exposure to the fungi ceased. 471
• Participants of an international Workshop held at Alexandria, Virginia, April 1998
concluded that exposure to moulds may constitute a health threat resulting in
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respiratory symptoms, increased incidence of infections, skin symptoms or allergy.
They advise that paediatricians and allergists should obtain information about mould
and dampness in the home environment when examining children with chronic
respiratory symptoms, recurrent infections or persistent fatigue and headache. 472
Kilpeläinena et al.(2001) in a study involving 10,667 Finnish students aged 18-25
years, found that living in traditional student homes with mouldy and damp walls not
only increased the risk of asthma, but students had a greater chance of repeated
colds. The strongest statistical association was found between exposure to visible
mould and asthma and common colds. 473
Zureik et al.(2002) studied over 1100 adults to see if severity of asthma is increased
due to airborne moulds present on walls of their homes. Three out of four people were
sensitive to at least one allergen. Two out of three people were sensitive to 2 or more
allergens. Almost 1 in 5 was allergic to Alternaria alternata or Cladosporium herbarum.
Hence, it was concluded that people sensitive to mould were more likely to have a
severe form of asthma. This may be because mould spores can reach the lower
airways. 474
Surveillance data from 8 European cities showed that dampness and mould were
associated with depression, independent of individual and housing characteristics.
This association was independently mediated by perception of control over one’s
home and by physical health. 475
There is also an increasing risk in normal subjects dwelling in such homes which can
contribute to the risk of developing asthma and chronic obstructive lung diseases due
to the potential inhalation risk of airborne endotoxin particularly during the winter and
summer seasons. 476
Mobin et al.(2011) carried out a study to determine the fungal species in toothbrushes
of residents of a neighbourhood on the east side of Pittsburgh, USA. 477 Fifty
toothbrushes were divided into two groups: group A comprised 30 toothbrushes used
by the residents and group B (control group) 20 new toothbrushes. Seventeen fungal
species were identified in group A, all of which were considered opportunistic and may
cause health problems mainly in immunocompromised patients. The species most
frequently found were: Candida albicans, Aspergillus niger, Penicillium citrinum,
Geotrichum candidum, Aspergillus fumigatus and Cladosporium oxysporum.
In 2011 Tischer et al. reported a systematic review of studies of children from eight
European birth cohorts which suggested that a mouldy home environment in early life
is associated with an increased risk of asthma particularly in young children and
allergic rhinitis symptoms in school-age children. 478 They analysed data from 31,742
children from eight ongoing European birth cohorts. Results showed that exposure to
visible mould and/or dampness during first 2 years of life was associated with an
increased risk of developing asthma: there was a significant association with early
asthma symptoms in meta-analyses of four cohorts [0–2 years: adjusted odds ratios
(aOR), 1.39 (95%CI, 1.05–1.84)] and with asthma later in childhood in six cohorts [6–
8 years: aOR, 1.09(95%CI, 0.90–1.32) and 3–10 years: aOR, 1.10 (95%CI, 0.90–
1.34)]. A statistically significant association was observed in six cohorts with symptoms
of allergic rhinitis at school age [6–8 years: aOR, 1.12 (1.02–1.23)] and at any time
point between 3 and 10 years [aOR, 1.18 (1.09–1.28)].
5. ASSESSMENT OF THE CAUSAL LINK BETWEEN HYGIENE AND INFECTIOUS DISEASES USING
DATA FROM INTERVENTION AND OBSERVATIONAL STUDIES
Significant insights into the sources and routes of spread of infectious diseases in the home
come from epidemiological studies. These include intervention studies in which the impact of
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different hygiene measures on disease incidence within a population is evaluated. It also
includes observational studies in which case and control populations are investigated in
relation to disease rates (self-reported or assessed according to criteria such as
absenteeism) and questioned about hygiene practices. The data is then used to identify risk
factors. Although surveillance provides information on modes of transmission, it is biased
towards investigation of outbreaks and gives only a limited picture of how sporadic personto-person transmission occurs in community and home environments.
5.1 OBSERVATIONAL STUDIES OF THE IMPACT OF HYGIENE ON INFECTIOUS DISEASES
In the following section, observational studies assessing the causal link between hygiene
and infection are categorized according to whether they looked at overall rates of infection,
groups of infections e.g., GI or RT, or specific pathogens e.g., salmonella.
5.1.1 Hygiene and infectious intestinal diseases
Food borne infection in the home results from one, or a combination of the following factors:
inadequate cooking, inadequate storage of food, or cross contamination during handling of
contaminated food. One of the difficulties in developing good kitchen hygiene practice is
understanding the relative extent of the risk from each of these components. From a 1990
study, Roberts (1990) 479 concluded that, although most food-borne outbreaks result from
poor temperature control of raw and cooked foods, many are associated with cross
contamination. This review suggested that cross contamination is implicated in about 6% of
outbreaks and poor hand hygiene in about 4% of outbreaks. Another report (Roberts
1986) 480 suggests that cross-contamination is a contributory factor in up to 14% of outbreaks
of Salmonella. Ryan et al.(1996) 481 estimated that poor hygiene involving hands and other
surfaces is a contributory factor in up to 39% of domestic food poisoning outbreaks. In an
evaluation of reported outbreaks linked to UK households for 1992-1999, Gillespie et al. 482
estimated that, of the 85% of outbreaks designated as foodborne, cross contamination was
implicated in 20% of outbreaks compared with 30 and 31% for outbreaks where inadequate
storage and cooking were thought to be the cause. Gillespie et al. expressed concern that
most of the reported outbreaks were linked to home catering, thus not necessarily
representative of normal daily routine.
A number of early surveys of the day-care centre environment demonstrate increased risk of
diarrhoea associated with faecal contamination levels of hands and environmental
surfaces. 483,484,485,486,487,488 Researchers were able to demonstrate that toys had the highest
coliform levels, and that hand contamination of children and adults strongly affected
diarrhoea incidence. Laborde et al.(1993)488 also demonstrated a correlation between
contamination levels and increased risk of disease.
Salmonella
A number of investigations of salmonella outbreaks are reported which showed that spread
via hands, environmental surfaces, cleaning cloths and household linens was a, or the,
causative factor:
• In 1981, Palmer et al. 489 reported an outbreak of Salmonella typhimurium infection
among healthy students in a university hall of residence. The first phase of the
outbreak was due to food contamination, while the second phase was best explained
by person-to-person spread. In 13 out of 18 residential blocks there was only one
toilet. Soiling of the toilet environment must have occurred. All 12 students ill during
the second phase of the outbreak had used the toilet in a block where students ill in
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the first phase were also living. The last case in the outbreak did not eat any
contaminated food or use the residence hall but had emptied a commode used by a
severely affected student and disposed of soiled sheets, indicating that infection was
via an environmental source.
After a hospital outbreak of S. typhimurium, organisms were isolated from ward dust
and from sputum of patients, indicating that aerial spread can occur. 490 Several laundry
workers and domestic staff became infected when their only contact was with
contaminated bed linen.
Sanborn (1963) 491 described several outbreaks of gastroenteritis in which
contaminated surfaces were involved. In one outbreak at a naval station, S.
typhimurium was isolated from patients and from a cutting board on which turkey had
been carved. The majority of patients had eaten turkey. The organism was isolated
from the chopping board 12 days after the turkey had been carved, despite being
cleaned following use. Another outbreak aboard a ship, due to Salmonella chester,
occurred in 2 phases. Roast pork was the suspect vehicle in phase 1, while turkey
sandwiches were the suspect vehicle in phase 2. Both foods had been carved on a
cutting board placed on a table used to thaw frozen turkeys. The juices from the
thawing turkeys apparently contaminated the cutting board.
Following an outbreak of food poisoning in a public house, Salmonella enteritidis was
isolated from environmental sites in the kitchen, including a cleaning cloth. 492 Surfaces
were cleaned using a reusable cleaning cloth. Pre-cooked foods, which were possible
vehicles of infection, were thought to have been contaminated after being brought into
the kitchen, suggesting cross contamination may have played a part. Several sites
were contaminated with Salmonella 9 days after the outbreak, suggesting cleaning had
not been done properly. After thorough cleaning repeat sampling was negative, but 1
of the 2 joints between work surfaces was still positive.
An investigation of an outbreak of diarrhoea due to Salmonella berta linked it to
unpasteurised cheese produced on a farm. 493 Cases increased weekly following
weekends when the cheese was sold at markets. A review of the cheese-making
process at the farm showed several opportunities for contamination. The cheese was
made by ripening curds in buckets for a few days. Chicken carcasses had also been
soaked in 2 buckets overnight, with 1 bucket then used for ripening curds without
being adequately disinfected. S. berta was isolated from faecal specimens, cheese
from case homes and a curd sample from the farm. One chicken carcass also yielded
S. berta.
Schutze et al.(1999)197 studied 50 homes where children under 4 years were infected
with Salmonella spp. The study was carried out in Aransas, USA where case rates for
salmonella were higher than the national average. In 34% of homes there was also
illness in other family members. The data indicate that environmental sources, infected
family members and pets, appeared to be much more significant risk factors for
development of salmonellosis in these children than contaminated foods.
The literature also reports a number of case-control studies in which transmission via hands
and surfaces were identified as risk factors. It is interesting that, in 6 of the following 9
reports, contact with animals was identified as the likely source:
• Following a 1998 outbreak of diarrhoea in children attending a Komodo dragon exhibit
at a zoo, caused by Salmonella enteritidis, a case-control study was conducted with 39
confirmed and 26 suspected cases. No patients and 2 controls reported touching a
dragon; however, 83% of patients but only 52% of controls touched the barrier
surrounding the dragon pen (odds ratio = 4.0). Washing hands after the visit was
highly protective (OR = 0.14). Cultures from patients, a dragon, and the exhibit barriers
yielded Salmonella enteritidis. 494
• Parry et al.(2002) 495 sampled kitchen dishcloths and refrigerators for Salmonella spp.,
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total Enterobacteriaceae and total aerobic colony counts in homes of subjects who had
suffered sporadic Salmonella infection (cases) as compared with control domestic
kitchens. Salmonella spp. were isolated from 12/125 (10%) case dishcloths and 4/81
(5%) control dishcloths, but the result was not statistically different. All 4 controls with
positive cloths had handled chicken in the previous weeks and 3 had handled eggs. In
6/12 case households with a Salmonella positive dishcloth, the strain was the same
phage type as the clinical isolate; in 4 a different strain was isolated. Salmonella was
isolated from 1 out of 137 (0.7%) case refrigerators compared to 3 out of 96 (3%)
control refrigerators. It was concluded that the presence of Salmonella in the domestic
kitchen is necessary, but not sufficient, to result in transmission of foodborne illness,
and there are further risk factors not identified by a study of this type which increase
transmission risks.
In previous study, Parry et al.(2002)495 found no evidence of differences in food
consumption and food handling practices, opportunities for cross contamination and
refrigerator temperature control in 99 households in Wales in 1997/8 with a case of
Salmonella food poisoning, against control households. Cases were more likely to
have purchased free-range eggs in the preceding week and handled frozen chicken.
Kohl et al.(2002) 496 report that, in the US, about 90% of Salmonella infections are
sporadic. They studied the risk for sporadic salmonellosis among 115 persons aged
>15 years reported in Louisiana, USA, compared with 115 age-matched controls.
Although consumption of food items likely to contain Salmonella was not associated
with illness, inconsistent handwashing between preparation of meat and non-meat
items was associated with illness (aOR 8.3).
Marcus et al.(2007) 497 conducted a case-control study (218 cases and 742 controls) of
sporadic Salmonella enteritidis infection in 5 US Foodborne Diseases Active
Surveillance Network (FoodNet) sites. Eating chicken prepared outside the home and
undercooked eggs inside the home, and contact with birds and reptiles were
associated with infection.
Centers for Disease Control and Prevention (CDC) reported cases of Salmonellosis in
the US associated with a range of animals including pet turtles, 498 reptiles 499 and
chicks. 500
During 1996-7, Mermin et al. 501 estimated the burden of reptile- and amphibianassociated Salmonella infections in Minnesota, Oregon California, Connecticut, and
Georgia (501 cases, 9047 controls). Reptile and amphibian contact was associated
with infection with serogroup B or D Salmonella (multivariable odds ratio 1.6; P< .009)
and infection with non–serogroup B or D Salmonella (OR, 4.2; P<.001). The population
attributable fraction for reptile or amphibian contact was 6% for sporadic Salmonella
infections and 11% for persons >21 years old. They estimated that reptile and
amphibian exposure is associated with apprx 4,000 Salmonella infections annually in
the US.
A large case-case study in England between 2004 and 2007 indicated that reptile
exposure is a rare but significant risk factor for Salmonella infection, with higher risk in
children <5 years old. Among the Salmonella serotypes found in people exposed to
reptiles, several non-Enteritidis, non-Typhimurium serotypes were identified. 502
Campylobacter
A number of outbreaks of Campylobacter are reported, where studies suggested that spread
via hands, environmental surfaces and cleaning cloths was a, or the, causative factor:
• Cross-contamination of food with Campylobacter jejuni from raw chicken was cited as
the cause of an outbreak of enteritis from eating at a restaurant. 503 Inspection of the
kitchen showed the food preparation area to be too small to separate raw poultry and
other foods adequately during preparation. The cook had cut up raw chicken before
preparing salads and lasagne (which were statistically associated with illness). The
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lettuce or lasagne was probably contaminated with C. jejuni from raw chicken through
unwashed or inadequately washed hands, cooking utensils or the countertop.
• A review by Pebody et al.(1997) 504 reported general outbreaks of Campylobacter
infection in England and Wales indicating that some foodborne outbreaks were related
to the handling and consumption of poultry and cross contamination from other foods.
The literature also reports a number of case-control studies in which transmission via hands
and surfaces were identified as risk factors. Again in 4 (but not in 2) of these 6 reports,
contact with animals was identified as the likely source:
• Neimann et al.(2003) 505 did a case control study (282 cases and 319 controls) in
Denmark during 1996–7. Consumption of undercooked poultry (OR 4.5; 8.2), red meat
at a barbecue, or grapes (OR 1.6; 2.8), and drinking unpasteurized milk (OR 2.3; 11.8)
were identified as risk factors for sporadic Campylobacter infection. Frequent
consumption of pork chops (OR 4.4) and daily contact with domestic animals and pets
were identified as risk factors in one of the two models only.
• A 2001 case-control study in children aged 0-35 months (81 cases, 144 controls) in
Australia showed that ownership of pet puppies (adjusted OR16.58) and pet chickens
(OR 11.80), and consumption of mayonnaise (OR 4.13) were risk factors for
infection. 506
• By contrast, in a UK case-control study aimed at identifying risk factors for intestinal
infection with Campylobacter jejuni 507 involving subjects with diarrhoea occurring in
community cohorts or presenting to General Practitioners with Campylobacter jejuni in
stools, there was no significant risk associated with consumption of chicken other than
in restaurants, nor with reported domestic kitchen hygiene practices. Pets or other
animals were not identified as risk factors and most cases remained unexplained.
They suggested that infection with low numbers of micro-organisms, and individual
susceptibility may play a greater role in causation of Campylobacter infection than
previously thought. They also concluded that, in mild, sporadic cases, infection may
result from cross contamination from kitchen hygiene practices usually regarded as
acceptable and that chicken may be a less important vehicle of infection for sporadic
cases than for outbreaks.
• In 1989 and 1990, Kapperud et al. 508 performed a case-control study designed to
identify risk factors for sporadic Campylobacter infections in Norway. Risk factors
found to be associated with illness included consumption of sausages at a barbecue
(OR 7.64; P = 0.005), daily contact with a dog (OR =4.26; P = 0.024), and eating of
poultry brought into the house raw (frozen or refrigerated) (OR =3.20; P = 0.024).
• In contrast, a case-control study by Danis et al. 509 conducted in Ireland showed that
although factors such as eating chicken were risk factors for sporadic Campylobacter
infections, contact with pet cats, dogs and other was not.
Norovirus
A number of norovirus outbreaks have been reported for which person to person
transmission via the environment (both via hands and surfaces and also by aerosol
transmission) or via food was implicated as the route of transmission:
• Following a wedding reception, an outbreak of norovirus gastroenteritis affected 50%
of guests. 510 The previous day, a kitchen assistant had vomited in a sink that was
subsequently used for preparing vegetables eaten by the wedding guests.
• The causal agent of recurrent outbreaks of gastroenteritis on a cruise ship was found
to be norovirus. 511 There had been at least 10 outbreaks of gastroenteritis aboard the
ship in the previous 2 years. Thorough inspections and cleaning of the ship between
cruises were not sufficient to stop the outbreaks. The likely modes of transmission
were person-to-person contact or surface contamination by aerosol droplets from
infectious stool or vomitus in the communal bathrooms.
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• Although direct evidence is lacking, this and other outbreaks reported in cruise ships in
which recurrent waves of infection occurred in successive cohorts of guests strongly
suggests transmission of norovirus via environmental sites and surfaces. 512,513
• An outbreak of norovirus gastroenteritis in an elderly care unit of a hospital spread
rapidly within and between wards, affecting both patients and staff. Analysis of risk
exposure showed areas where patients had vomited to be the most significant factor
for the spread of norovirus to staff. 514
• Cheesbrough et al. 1997 515 reported that 2 carpet fitters became ill after removing a
carpet from a hospital ward 13 days after the last case in rotavirus outbreak. Routine
daily vacuuming since the outbreak had not removed the virus.
• During a norovirus outbreak in a long stay ward for the mentally ill, 36 environmental
samples were collected on the affected ward of which 11 (30%) were positive by RTPCR. Positive swabs were from lockers, curtains and commodes and were confined to
the immediate environment of the affected patients. 516
• The potential for environmental spread of norovirus was demonstrated in a prolonged
hotel outbreak in successive cohorts of guests.211 Environmental sampling
demonstrated widespread dissemination of the virus on hand contact and other
surfaces. From the patterns of infection, it was concluded that although infectious
aerosols were probably the main route of dissemination of infection within a particular
cohort of guests, contact with contaminated fomites was the most likely factor
responsible for maintaining the outbreak by forming the link between successive
cohorts.
• Evans et al. 517 investigated a 1999 outbreak of norovirus which affected more than
3000 people who attended a UK concert hall over a 5 day period. The index case was
a concert attendee who vomited in the auditorium and in an adjacent toilet. Illness
occurred among 8/15 school parties who attended the following day. Illness affected
257/1229 (20.9%) of the children, but attack rate by school was 0.6 to 75%. Children
who sat on the same auditorium level as the index case were more likely to be ill than
those seated elsewhere (RR 7.1, p=<0.001).
• Data from 2 norovirus outbreaks in 2000 and 2003 indicate how infection can result
from direct inhalation of infected particles of vomit by people immediately adjacent to
the person who vomits. The potential for airborne transmission was demonstrated in
studies in a restaurant and a primary school, where close proximity to infected persons
in the immediate aftermath of a vomiting attack was found to be a risk factor. 518,519
• Investigation of a 2008 norovirus outbreak in the US identified insufficiently cleaned
computer keyboards as a probable risk factor for a school-based outbreak. 520
• In a case-control study carried out in the Netherlands, De Wit et al. identified risk
factors, modes of transmission, and opportunities for prevention gastroenteritis due to
norovirus, Sapporo-like virus (SLV), and rotavirus. The main risk factor for viral
gastroenteritis was contact with other persons with gastroenteritis, supporting the
hypothesis that these viruses are mainly transmitted from person to person. However,
for NV gastroenteritis, foodborne transmission also seems to play an important role. 521
• Jones et al. (2007)214 reported an outbreak which affected 74% of guests on 3
consecutive houseboat trips. An environmental investigation identified norovirus RNA
on 71% of surfaces in bathrooms, kitchens, and door handles.
• During an outbreak in a long-term care facility, norovirus RNA was identified on 5 of 10
environmental sites collected after disinfection, suggesting widespread persistent
contamination. Positive sites included an elevator call button used only by staff. The
outbreak resolved following a second, more thorough facilitywide disinfection.213
• Nicolay et al. 2011 investigated a cluster of 4 gastroenteritis cases among people who
attended a family lunch in a Dublin hotel in 2009. 522 Consumption of egg mayonnaise,
turkey with stuffing or chicken sandwiches were each associated with increased risk of
gastroenteritis: (risk ratio (RR): 2.3; 95% CI: 1.4–3.9), (RR: 1.9; 95% CI: 1.2–3.2), (RR:
85
1.9; 95% CI: 1.1–3.1). Further investigations suggested that the ready to eat
sandwiches had most likely been contaminated during preparation, by three
asymptomatic kitchen food handlers who had used the same toilets. All eight cases
and three asymptomatic food handlers on duty at the lunch tested positive for
norovirus.
Although the data suggest that both aerosol, and hand and surface transmission contribute
to spread of norovirus infection, there are no data to indicate the relative importance of these
two routes.
Rotavirus
Outside the hospital environment, rotavirus outbreaks are most usually reported for young
children in day-care centers. Ekanem et al.(1983)483 concluded that contamination of hands
and classroom objects plays a role in transmission in day-care centers. Astroviruses and
enteric adenoviruses have been associated with gastroenteritis outbreaks in schools,
paediatric hospital wards and nursing homes. 523 Rotavirus shows a distinct winter peak. Low
humidity and crowding indoors associated with winter may be factors in the spread of this
virus. 524 One-third of parents whose children are infected with rotavirus become ill indicating
that transmission takes place in the home between family members.
In the Netherlands case-control study by De Wit et al., as described above, the main risk
factor for rotavirus as well as norovirus gastroenteritis was contact with other persons with
gastroenteritis, supporting the hypothesis that these viruses are mainly transmitted from
person to person.521
A number of investigations are reported for which cross-contamination from person to
person was implicated as the route of transmission of rotavirus:
• A US study revealed that rotaviruses infected one or more members in 51% of
families, including 28% of children and 13% of adults. 525 Some adults acquired
rotavirus infections a few days after their children’s illnesses, suggesting that children
rather than the parents brought infection into the home.
• Rodriguez et al.(1979) 526 found rotavirus infection in 55% of adult family contacts of
children hospitalised with gastroenteritis.
• In a community study in New Zealand, in families with an index case of rotavirus
infection, children were more frequently infected than adults. Once a family member
became infected, probability of cross infection was high. 527
Escherichia coli
A number of E. coli outbreaks have been reported for which cross-contamination was
implicated as the route of transmission:
• Linton et al.(1977) 528 demonstrated that E. coli strains from chicken carcasses became
part of the majority coliform flora of one volunteer who had handled, cooked and eaten
the chickens at home. None of the strains had been detected in the faecal flora prior to
handling the chicken. The strains were isolated from faecal specimens taken the day
after the chicken was handled, prepared and cooked, but before it was eaten. This
indicates that it was handling of the uncooked chicken that provided the opportunity for
transmission of E. coli rather than the eating of the cooked chicken. The strains of E.
coli from the chicken also remained in the faecal flora for about 10 days.
• Mead et al.(1997) 529 conducted a case-control study to identify sources of infection
and contributing practices to sporadic outbreaks of E. coli O157:H7. Illness was
strongly associated with having consumed a hamburger in the previous week, with
80% of hamburgers being prepared at home. Case households were more likely to
report not washing their hands or work surfaces being in contact with raw beef, and
86
•
•
•
•
•
were more likely to report placing cooked hamburgers back onto unwashed plates
previously in contact with raw beef. Transmission was believed to have occur more
often when the hands of food preparers were allowed to cross-contaminate other food
and utensils. The authors concluded that 34% of infections could have been avoided
by adequate hand hygiene.
Varma et al. 530 carried out a case control study to determine the risk factors for E coli
O157 infection during an outbreak at a county fair in Ohio, in August 2001. Casepatients were more likely than controls to have visited building A (a multipurpose
community facility on the fairgrounds). Among visitors to building A, illness was
independently associated with attending a dance in the building, handling sawdust
from the floor, or eating and/or drinking in the building. Twenty-four (44%) of 54
specimens from building A 6 weeks after the fair grew Shiga toxin-producing E coli
O157. Isolates from sawdust, rafters, and other surfaces were identical by molecular
fingerprinting to patient isolates. Sawdust specimens collected 42 weeks after the fair
also grew the same E coli O157 strain.
Rangel et al. 531 reviewed E. coli O157 outbreaks in the US from 1982–2002
Outbreak settings included 40 (80%) child daycare centers;5 (10%) individual
residences; 3 (6%) communities 1 (2%) school, and 1 (2%) residential facility.
Transmission route for 183 (52%) was foodborne, 74 (21%) unknown, 50 (14%)
person-to-person, 31 (9%) waterborne, 11 (3%) animal contact, and 1 (0.3%)
laboratory-related.
In a study of sporadic E. coli O157 infections in Wales, Parry and Salmon (1998) 532
calculated that the household transmission rate from an index case to be 4–14%,
although many of the secondary cases were asymptomatic.
In a 2011 report, Friedrich review cases of E. coli O104 in Germany Netherland and
France which were due to secondary person-to person transmission within households
or associated with an infected food handler.120
Investigations involving other bacterial and viral enteric pathogens are as follows:
Listeria
• Listeria monocytogenes was the causal agent of an outbreak of gastroenteritis among
supper guests at a private home. The rice salad was deemed the most likely vehicle
since the attack rate was 90% for those who ate rice salad. The salad had been
prepared 24 hours in advance and stored at room temperature. Listeria
monocytogenes was also isolated from other foods left over from the supper, and from
the blender and the freezer in the home of the cook indicating that cross-contamination
from kitchen surfaces or utensils may have played a role in this outbreak. 533
Helicobacter pylori
• A Japanese study examined the relationship between persistent Helicobacter pylori
infection, and factors such as sanitary conditions or home environment during
childhood. Almost 6000 participants completed a questionnaire and H. pylori antibody
test. The authors concluded that drinking water, type of toilet, residential area, number
of people in the house and birth order showed significant correlation with H. pylori
infection. 534
• Perry et al.(2006) examined household members in California, USA for H. pylori
infection. Among 1,752 person considered uninfected at baseline, 30 new infections
occurred. The risk for definite or probable new infection increased by 4.8-fold upon
exposure to an infected household member. Of probable/definite new infections, 75%
were attributable to exposure to an infected person. The authors suggest that personto-person transmission of H. pylori is most commonly implicated with faecal/oral,
87
oral/oral, or gastric/oral pathways; infection is associated with conditions of crowding
and poor hygiene and intrafamilial clustering. 535
Hepatitis A
• Rajaratnam et al. 536 describe an outbreak of hepatitis A (HAV) associated with a
Middle school involved 23 cases. The probable source was a male pupil infected by a
sibling who had contracted hepatitis A while abroad on holiday. A questionnaire survey
and salivary IgG and IgM anti-HAV testing of the pupils demonstrated a statistically
significant association between infection and the use of a changing room toilet for
defecation. An inspection of the school showed that toilets lacked toilet paper, soap
and hand towels.
• An outbreak of HAV was associated with a public house whose barman had chronic
diarrhoea and had served drinks while incubating HAV himself. 537 Fomite transmission
by contamination of glasses was the likely route of spread.
• Investigation of community outbreaks of HAV show that people involved in nappychanging in day-care centers often handle food. 538 HAV may be acquired from children
who are excreting HAV, the majority of whom are asymptomatic. 539 A significant
percentage (23–52%) of household contacts of index cases with HAV infection, are at
risk of acquiring infection. 540 Higher rates of infection in children (71–80%) compared
with parents (29%) suggest that child play activity is a risk factor for transmission in
homes.
Shigella sonnei dysentery
Poor surface hygiene has been implicated in the spread of Shigella infection. In 1992 there
was an epidemic outbreak of dysentery caused by Shigella sonnei. Some 17,000 cases of
dysentery were reported for England and Wales in 1992 compared with 2313 in 1990. 541
Transmission of Shigella is via the faecal–oral route and it is recognised that prevention
requires careful attention to hand hygiene and cleaning of washbasins, toilets and
surrounding areas. 542 Outbreaks are often centered on nursery schools, etc., but there is
also substantial evidence for spread within the home. The infectious dose is very small and
young children are implicated in the spread of shigellosis to their families.
Cryptosporidium
Cryptosporidium,a common cause of diarrhea, has been associated with sporadic and
epidemic diarrhoea in child-care settings with evidence for secondary transmission to
household and other close contacts 543 Transmission from pets has also been recorded.138
Gastrointestinal infections linked to petting farms
Gormley et al. 2011 544 reviewed 55 outbreaks of infectious intestinal disease associated with
petting farms in England and Wales as reported to the UK Health Protection Agency during
1992–2009. Verocytotoxin-producing Escherichia coli O157 (VTEC O157) caused 30 (55%)
of these outbreaks (244 persons were affected [range 2–93, mean 8 persons] and 84 were
hospitalized); Salmonella enterica serovar Typhimurium definitive phage type 104 caused 2
(3%) of the outbreaks. A total of 23 (42%) petting farm outbreaks were caused by
Cryptosporidium spp. (1,078 persons were affected [range 2–541, mean 45 persons] and 29
were hospitalized). Contributory factors reported in the cryptosporidiosis outbreaks included
direct contact with preweaned lambs, calves, kids, or animal faeces (e.g., diarrhea in lambs,
a recognized risk factor for cryptosporidiosis; 11/23 [48%]) and inadequate hand washing
facilities (7/23 [30%]). Of outbreaks in which hand washing facilities were inadequate, thumb
sucking by children was also noted in 1; in another, alcohol-based hand gels and sanitizers,
which are ineffective against Cryptosporidium spp., were used.
88
With overall regard to infectious intestinal diseases, the difficulties of drawing general
conclusions from case-control studies about the role of environmental hygiene in preventing
GI infections involving several pathogens is illustrated by the study of Stenberg et al.49 The
study evaluated 14 published studies (11 case-control studies, 2 cross-sectional surveys,
and 1 randomised control trial (some described in more detail above)) in order to assess
whether household kitchen practices contribute to development of diarrhoea. Exposures
identified were related to kitchen hygiene and cleanliness or food preparation and storage
practices. Outcomes studied were self-reported diarrhoea with no identified pathogen, or
diarrhoea involving a known pathogen. The study also included reanalysis of the UK IID
study investigating associations between self-reported diarrhoea and poor domestic kitchen
hygiene.121 Overall, the authors concluded that the data does not support the hypothesis that
poor environmental hygiene in the domestic kitchen is a risk factor for Salmonella,
Campylobacter or self-reported diarrhoea although there is evidence that poor kitchen
hygiene may be a risk factor for Enterohemorrhagic E. coli. Although some variables in the
reanalysis of the UK IID study were statistically significant, no obvious trend was seen.
Importantly, the study which did not distinguish between the various infectious agents
(Salmonella, Campylobacter, norovirus and rotavirus) for which the sources and routes of
transmission are likely to be quite different. The study also looked mostly at kitchen hygiene
practices, whereas a large proportion of disease may have resulted from person-to-person
transmission outside the kitchen, not involving food handling; most diarrhoeal diseases in
developed nations are probably due to viruses which are largely transmitted from person-toperson. The authors also concurred that they did not list all potential risk factors, which may
have caused under-ascertainment of negative relative to positive outcomes. Overall, the
authors concluded that no unequivocal conclusions about the impact of kitchen hygiene on
diarrhoeal disease could be drawn from their study.
Similarly, Mitakakis et al. 545 studied 600 families (cases and controls) to identify whether
dietary intake and food-handling and storage practices in the home were risk factors for
gastroenteritis. No association with food-handling and storage practices was detected.
However cases were more likely to have a baby in nappies in the house.
5.1.2 Hygiene and respiratory tract infections
A number of case-control studies are reported which assess the impact of hygiene measures
in preventing the spread of viral RT infections:
• St. Sauver et al.(1998) 546 studied prevalence of respiratory illness in children attending
daycare homes. Never or rarely washing hands by both children and carers, using
shared cloth towels rather than disposable paper towels and washing of sleeping mats
less than once a week were associated with higher frequency of respiratory infection.
• Jefferson et al.(2009)48 assessed 6 case-control studies which assessed the impact of
public health measures to curb the spread of severe acute respiratory syndrome
(SARS) during February to June 2003 in China, Singapore, and Vietnam. Studies
reported that disinfection of living quarters was highly effective in preventing the
spread of severe acute respiratory syndrome (odds ratio 0.30, 95% confidence interval
0.23 to 0.39, one study); handwashing for a minimum of 11 times daily prevented most
cases (0.45, 0.36 to 0.57; all six studies), wearing simple masks was highly effective
(0.32, 0.25 to 0.40; five studies), wearing N95 masks was even more effective (0.09,
0.03 to 0.30; two studies), wearing gloves was effective (0.43, 0.29 to 0.65; three
studies), wearing gowns was also effective (0.23, 0.14 to 0.37; four studies). All
approaches combined achieved high effectiveness (0.09, 0.02 to 0.35; two studies).
• In one of the case-control studies included above, Lau et al. 547 analysed data from
1,192 patients with probable SARS reported in Hong Kong. Multivariate analysis
89
showed that having visited mainland China, hospitals, or the Amoy Gardens were risk
factors (OR 1.95 to 7.63). Mask use in public venues (OR 0.36), frequent hand
washing (OR 0.58), and disinfecting the living quarters (OR 0.41) were also significant
protective factors.
5.1.3 Hygiene and skin and wound infections
S. aureus and MRSA
A range of MRSA outbreaks related to the home and community have been evaluated where
transmission via hands and environmental surfaces has been identified as a likely cause of
transmission. These are also reviewed elsewhere.8,548,549 In addition, a small number of
instances are recorded where the home environment was cited as a causative factor:
• In studies of HCWs colonised with MRSA,45,46,47,340,371 the HCW was treated to
eradicate the organism, but subsequently became recolonised. In each case, MRSA
was isolated from environmental surfaces in the home of the HCW, including door
handles, a computer desk shelf and computer joystick, linens, furniture, and in some
cases also from other family members45,46,47,371 and family pets.340
• A number of cases are reported where family members in the home of an infected
person have become colonised.374,375,376,377 Hollis et al.374 found that transmission of the
MRSA strain from an index case to two siblings and the mother occurred at least three
times, and one family member was colonised for up to 7 months or more.
• The potential for HCWs acquiring PVL-MRSA in the community with onward
transmission to patients or fellow HCWs was demonstrated during investigation of a
fatal PVL-MRSA infection in a Filipino healthcare worker (HCW, case 1) in the UK. 550
Both household members (partner and child) were identified as asymptomatic carriers
(cases 2 and 3). From analysis of blood cultures from 5 patients on the ward where
case 1 had worked, one patient with an MRSA strain indistinguishable from the
outbreak clone was identified (case 4). Screening of HCWs who worked on the ward
with case 1 and where case 4 had been admitted revealed the outbreak clone in
another HCW (case 5). Cases 1 and 5 had previously shared accommodation and had
cared for case 4. Case 5 lived in a household with partner and child. Both were
identified as carriers (cases 6 and 7). Case 6 was a HCW who worked on a different
ward. Overall, representatives of the same lineage were identified in 16 individuals in
community and hospital. Infections likely to be caused by PVL-MRSA had occurred in
12 cases of which 9 worked as nursing staff in the hospital. Eight of these were linked
socially.
In 2006, Turabelidze et al. 551 reported a case-control study, involving 55 culture-confirmed
cases of MRSA in a US prison examining risk factors for MRSA infection with a focus on
personal hygiene. It was found that the risk for MRSA infection increased with lower
frequency of hand washing per day and showers per week. Patients were also less likely
than controls to wash personal items (80.0% vs. 88.8%) or bed linens (26.7% vs. 52.5%)
themselves instead of using the prison laundry. When personal hygiene factors were
examined for cases and controls, patients were more likely than controls to share personal
products (e.g. cosmetic items, lotion, bedding, toothpaste, headphones), especially nail
clippers (26.7% vs. 10%) and shampoo (13.3% vs. 1.3%), with other inmates. To evaluate
an overall effect of personal hygiene practice on MRSA infection, a composite hygiene score
was created on the basis of the sum of scores of 3 hygiene practices, including frequency of
hand washing per day, frequency of showering per week, and sharing personal items shared
with other inmates. A significantly higher proportion of case-patients than controls had lower
90
hygiene scores (<6) (46.7% vs. 20.0%). Sharing of towels and soap was also identified as
significant risk factors in recurrent outbreaks of CA-MRSA in a US football team. 552
Experience in the US, suggests that CA-MRSA is easily transmissible not only within families
but also on a larger scale in community settings such as prisons, schools and sports teams.
For CA-MRSA, those at particular risk appear to be younger, generally healthy people who
practice contact sports or other activities that put them at higher risk of acquiring skin cuts
and abrasions.328 Skin-to-skin contact (including intact skin) and indirect contact with
contaminated objects such as towels, sheets and sport equipment are seen as the primary
vehicles of transmission; Johnson387 cites risk factors for spread of CA-MRSA as close skinto-skin contact, cuts and abrasions, shared contaminated items or surfaces, poor hygiene
and crowded living conditions. A 2008 study by Archibald et al. 553 investigated a cluster of
MRSA infections in college football players. Risk factors included a history of recurrent skin
infections and contact with the skin lesions of persons outside college.
Uhlemman et al. 2011381 carried out a community-based study (95 case and 95 controls)
which indicated that environmental colonization may contribute to the community spread of
epidemic strains such as USA300. Case patients presented with CA-MRSA infections to a
New York hospital. Age-matched controls without infections were randomly selected. During
a home visit, case and control subjects completed a questionnaire, nasal swabs were
collected from index respondents and household members and standardized environmental
surfaces were swabbed. Among case households, 53 (56%) were environmentally
contaminated with S. aureus, compared to 36 (38%) control households (p = .02). MRSA
was detected on fomites in 30 (32%) case households and 5 (5%; p,.001) control
households. More case patients, 20 (21%) were nasally colonized with MRSA. In a subgroup
analysis, the clinical isolate (predominantly USA300), was more commonly detected on
environmental surfaces in case households with recurrent MRSA infections (16/36, 44%)
than those without (14/58, 24%, p = .04).
Mycobacteria
Infections with Mycobacterium avium and M. fortuitum have been linked to inadequately
sanitised domestic hot tubs in both healthy and immune-compromised individuals. 554,555 A
community-based outbreak of infection with M. fortuitum was associated with contamination
of a foot-bath at a nail salon. 556
Streptococcus
Clusters of Group A streptococcal infections in family, hospital and nursing home settings
have been reported by Schwartz et al.(1992). 557 A report 558 of a nursing home outbreak of
Group A streptococcal infection involved infected skin lesions among residents. One of 3
throat swabs from staff members complaining of a sore throat yielded the same organism.
As some infected lesions followed falls on the nursing home carpet, samples were taken
which indicated widespread occurrence of the outbreak strain on carpets and furnishings. In
comparison there was no evidence of environmental contamination in a “control” nursing
home which was also sampled. Repeat environmental sampling after cleaning measures
had been implemented showed decreased streptococcal contamination and no further cases
of infection were reported among staff and residents.
5.1.4 Hygiene and fungal infections
Fungal contamination in homes and hospitals has been implicated as the cause of infection
or increased prevalence of infection:
• The presence of the fungus Stachybotrys atra in a house in Chicago was implicated in
an outbreak of illness among the occupants. 559 The symptoms of the illness only
91
ceased following the removal of the fungus.
• Mould growth on a floor and underside of linoleum was the cause of more severe
respiratory symptoms in patients returning home from hospital and they only recovered
after treatment of the mouldy area. 560
• In Finland, visible mould was reported in 3.7% of homes, and 5.5% reported mould
odour. 561 Increased prevalence of respiratory infections and respiratory symptoms was
recorded in homes reporting dampness or mould.
5.1.5 Home hygiene and overall rate of infection
Larson and Duarte50 examined the relationship between prevalence of non-specific
infections and home hygiene practices amongst household members. The study involved
398 households in New York. Infections investigated were defined as 2 or more members of
the same household with the same symptoms that included fever, cough, cold, diarrhoea,
vomiting, sore throat, skin infection or other infection. Only 2 specific “targeted” practices,
using a communal laundry and not using bleach in communal laundering, were predictive of
increased risk of infection. For the remaining practices there was no evidence of an
association with infection risk. Other hygiene practices studied were mostly cleaning
practices such as daily personal bathing or showering, daily cleaning of bathrooms and
toilets, frequent changing of dish-sponges, or use/non use of antimicrobial cleaning products
for these activities.
5.2. ASSESSMENTS OF THE CAUSAL LINK BETWEEN HYGIENE AND INFECTIOUS DISEASES USING
DATA FROM INTERVENTION STUDIES
One of the most important aspects of intervention studies is that they give a quantitative
estimate of the extent to which hygiene measures can reduce infection rates. However, apart
from hand hygiene and household water treatment, very few intervention studies have been
carried out to assess the impact of procedures such as surface hygiene, cleaning cloth
hygiene or laundry hygiene, as used in the home. Even for hand hygiene, most studies have
involved settings such as schools or day-care centres rather than the home.
5.2.1 Intervention studies assessing the impact of hand hygiene on gastrointestinal,
respiratory tract and skin and wound infection
Impact of hand hygiene on gastrointestinal disease
From a systematic review of hand washing intervention studies carried out in 2007 (Table 4),
Bloomfield, Aiello et al.4 estimated that the range of reduction in the incidence of infectious
intestinal diseases was between -13% to 79% for developing countries and between -10%
and 57% for developed countries. Of the studies that were statistically significant (7/11 and
3/5), reductions in GI infection ranged from 26–79% and 48–57% for developing and
developed countries, respectively. In the same review it was estimated that the range of
reduction in the incidence of infectious intestinal diseases by use of an alcohol hand
sanitizer was between 0 and 59%for developed countries. Of the studies that were
statistically significant (3/4), reductions in GI infection ranged from 20–50%.
92
Table 4 – Data from intervention studies on the impact of hand hygiene on respiratory and
gastrointestinal infections
Type of
Area of study Risk reduction from
infection
hand washing with soap
Use of alcohol hand
sanitizer
Range
No. of
Range
No. of
statistically
statistically
significant
significant
studies
studies
(range)
(range)
GastroDeveloped
-10 to 57%
3/5 studies (48 0 to 59%
3/4 studies
intestinal
to 57%)
(20-50%)
Developing
-13% to 79% 7/11 (26% to
79%)
Respiratory Developed and 5% to 53%
2/6 studies
-6 to 26%
2/4 studies
developing
(20%-51%)
(13–26%)
In a 2009 study by Nicholson et al., a 10 month study was carried out to evaluate the impact
of handwashing with soap on the incidence of diarrhoea, acute respiratory infections (ARIs),
and eye infections.31 The study involved 1,656 families across 70 communities in Mumbai,
India. Half of the families were provided with soap along with education about the
importance of handwashing at 5 key occasions: before eating meals, when bathing and after
using the toilet. At the end of the trial, children aged approximately 5 years old in the
intervention group had 25% fewer episodes of diarrhoea than those in the control group, with
similar reductions in children in other age groups and adults, ranging from 21.4% to 24.7%.
Furthermore, due to the reduction in the number of episodes of disease there was a 40%
increase in school attendance during the trial.
The strong causal relationship between hand hygiene and GI disease risk has been
demonstrated by a range of systematic evaluations of data from intervention studies 562, 563,564
These studies were carried out using data from both developed and developing countries.
Individual studies on the impact of hand hygiene on GI infections are described in more
detail in IFH review papers on the effectiveness of hygiene procedures.4,9 In most cases,
these studies assessed the overall impact on diarrhoea, but in some cases the impact of
hand hygiene on specific infections such as Shigella, rotavirus or norovirus was investigated.
Some of these studies looked at the impact of handwashing, whilst others evaluated use of
alcohol hand sanitizers.
In the most recent reviews Waddington et al. 200932 concluded that handwashing with soap
lead to an estimated 31% reduction in child diarrhoea morbidity. Analysis by sub-group
suggested that provision of soap is more effective in reducing diarrhoea morbidity than
education campaigns alone. In a 2010 review, Cairncross et al. proposed a diarrhoea risk
reduction of 48% associated with handwashing with soap.33 However they concluded that
most of the evidence is of poor quality and more trials are needed, although they
commented on the consistency of the results across various study designs and pathogens.
Impact of hand hygiene on respiratory disease
A range of intervention studies have been carried out which indicate a significant link
between hand hygiene and spread of RT infections. Individual studies on the impact of hand
hygiene on RT infections are described in more detail in the IFH review paper on the
effectiveness of hygiene procedures.4,9 Some of these studies evaluate the impact of
handwashing, whilst other studied use of alcohol hand sanitizers.
93
Some of the earlier studies evaluated the impact of hygiene in interrupting the transmission
of “experimental” rhinovirus colds:
• Gwaltney et al.(1980)39 showed that aqueous iodine (2%) applied to fingers was
effective in blocking hand transmission of experimental rhinovirus infection. None of
the 8 volunteers became infected when exposed to rhinovirus immediately after
treatment of fingers with iodine whilst all of 7 subjects treated with a placebo
preparation became infected. One of 10 volunteers became infected when exposed 2
hour after treatment of fingers with iodine, compared with 6 of 10 who became infected
in the control group. Virus was recovered from three (11%) of 27 hand rinses from
volunteers using iodine and from 11 (41%) of 27 hand rinses from volunteers using the
placebo preparation.
• In a 4-year trial, Hendley and Gwaltney (1988)268 studied the impact of prophylactic
treatment of mothers’ fingers with iodine on RT infections. When illness occurred in the
family, mothers were instructed to dip their fingers in iodine first thing in the morning,
then every 3-4 hours or after activities that washed the iodine from the skin. Secondary
attack rates in mothers were 7% in the iodine group and 20% in placebo families. No
infections occurred in mothers after 11 exposures to an index case with infection in the
iodine group, compared with 5 infections after 16 exposures in the placebo group.
In 2007, Aiello et al. carried out a systematic review of hand hygiene intervention studies
carried out to assess the impact on RT infections.4 Based on these studies, Table 4
summarises the results of community-based interventions (i.e. excluding healthcare-related
and military settings). Most studies were conducted in economically developed countries
(83%, 5/6). Reduction in illness due to handwashing ranged from 5–53%, but only 33% (2/6)
of studies were statistically significant. In the same review it was estimated that the range of
reduction in the incidence of respiratory infections by use of an alcohol hand sanitizer was
between -6 and 26%. Of the studies that were statistically significant (3/4), reductions in GI
infection ranged from 13-26%. Rabie and Curtis in 2006 also published a review of hand
hygiene studies involving RT infections. 565 They reported that hand hygiene (hand washing,
education, and waterless hand sanitizers) can reduce the risk of respiratory infection by 16%
(95% CI: 11-21%). These investigators have now updated their estimate with two further,
more recent, studies which, when all studies are taken together, give a pooled impact on
respiratory infection of 23%. 566 In a more recent 2008 study, Aiello et al., estimated that the
reduction in respiratory illness associated with the pooled effects of hand hygiene (hand
washing with soap, use of alcohol handrubs) was 21%.564
In the 2009 study by Nicholson et al.31 of the impact of handwashing with soap on diarrhoea,
acute respiratory infections (ARIs), and eye infections in 1,656 families in Mumbai, India
(described in more detail above), a 15% reduction in the number of episodes of ARI was
observed in children aged approximately 5 years in the intervention group.
In 2009, Jefferson et al.48 reported a systematic review of 58 intervention and observational
studies on the impact of physical interventions to interrupt the spread of viral respiratory tract
infections. The authors concluded that “hygiene and physical measures, such as
handwashing, wearing masks and isolating potentially infected patients, are highly effective
in preventing the spread of viral infections. The results show that regular handwashing (more
than 10 times a day) and wearing masks, gloves and gowns were effective individually
against all forms of acute infectious respiratory disease, and were even more effective when
combined. The highest quality trials suggested that spread of respiratory viruses can best be
prevented by hygienic measures in younger children and within households. They also
concluded that “the incremental effect of adding virucidals or antiseptics to normal
handwashing to reduce respiratory disease remains uncertain”.
94
Impact of hand hygiene on skin, wound and eye infections
Although skin, wound and eye infections are common in the home and community, and are
transmitted from person-to-person, other than for S. aureus infections, there is little
intervention study data on the impact of hand hygiene.
Perhaps the most convincing evidence for hand transmission of S. aureus comes from a US
controlled trial in 1962 comparing the effect of no handwashing with antiseptic handwashing
on the acquisition of S. aureus in infants in a hospital nursery. Infants cared for by nurses
who did not wash their hands after handling an index infant colonised with S. aureus
acquired the organism significantly (p<0.05) more often and more rapidly than infants cared
for by nurses who used hexachlorophene to cleanse their hands between infant contacts. 567
In two studies carried out in Pakistan, Luby et al.30, 289 studied the impact of hand washing
with soap on impetigo. Impetigo is a skin infection caused by S. aureus which is frequently
found as part of the normal body flora. In the 2002 study30 involving 162 households, it was
found that, children had a 25% lower incidence of impetigo (-52% to -16%) compared with
controls (no hand washing promotion). In the 2005289 study involving 600 households, it was
found that, compared with controls, children younger than 15 years in households with plain
soap had a 34% lower incidence of impetigo (-52% to -16%).
In a more recent study by Nicholson et al.31 on the impact of handwashing with soap on
diarrhoea, acute respiratory infections (ARIs), and eye infections in families across Mumbai,
India (described in more detail above), a 46% reduction in the number of episodes of eye
infections was observed in children aged approximately 5 years old.
5.2.2 Impact of safe faeces disposal, and household water treatment and safe storage
on diarrhoeal disease
In a 1991 review Esrey et al. examined a total of 144 studies to examine the impact of
improved water supply and sanitation facilities on ascariasis, diarrhea, dracunculiasis, hook
worm, schistomiosis and trachoma. 568 The median reduction in morbidity for diarrhea,
trachoma and ascariasis induced by water supply and/or sanitation was 26%, 27% and 29%
respectively. The same for schistomiosis was 77%.
A 2005 systematic review by Fewtrell et al.563 concluded that diarrhoeal episodes can be
reduced by 39% via household water treatment and safe storage. The link between
household water storage, handling and point-of-use treatment and its effectiveness in
reducing the burden of diarrhoeal diseases is also reviewed in a 2006 IFH report.5 The
results of intervention studies showing that safe excreta disposal and improved water supply
are effective in preventing diarrhoeal diseases are more recently reviewed in a 2008 WHO
report, 569 and two Cochrane reviews, a 2009 review on water supply 570 and a 2010 review
on improved sanitation. 571 One of the key findings of the Cochrane review on water is that
the effectiveness of household interventions is significantly greater than those at the source.
In the most recent reviews, Waddington et al.32 found results that were generally consistent
with previous reviews, suggesting that, water quality interventions and safe excreta disposal
interventions on average effect respectively a 42% and 37% relative reduction in child
diarrhoea morbidity. The pooled meta-analysis suggested that sanitation and/or hygiene do
exert additional impact on diarrhoea morbidity when combined with either water supply or
water quality interventions. In a 2010 review, Cairncross et al. propose a diarrhoea risk
reduction of 17 and 36%, associated respectively, with improved water quality and excreta
disposal.33 However they concluded that most of the evidence is of poor quality and more
95
trials are needed, although they commented on the consistency of the results across various
study designs and pathogens.
5.2.3 Impact of environmental/surface hygiene procedures applied to hand-contact,
food-contact and other critical contact surfaces
Although most of the interventions studies summarised above, measured only the impact of
hand hygiene, in some studies hand hygiene was combined with other measures. In some
studies, hand hygiene promotion was combined with hygiene education, whilst in a few
others hand hygiene was combined with cleaning and/or disinfection of environmental
surfaces. In these studies however, no attempt was made to assess the separate effects of
one intervention relative to another, and thereby rank their importance. In some studies, the
impact of hygiene on groups of infections (e.g., respiratory tract infection), whilst in others
the impact on specific infections (e.g. norovirus, C. difficile, MRSA) was assessed:
• Krilov et al.(1996)34 reported an intervention study in a preschool daycare centre for
children with Down syndrome enrolled in a school-based early intervention program.
Through a series of questionnaires, the number and types of infections in the children
were chronicled for a year before and a year after the implementation of an
intervention program. Intervention measures included reinforcing handwashing
procedures and education of staff and families on issues of infection control including
surface cleaning and disinfection and disinfection of toys. Compliance with these
measures was monitored. During the interventional year the median number of
illnesses/ child/month decreased significantly from the baseline year (0.70 vs 0.53 P <
0.05), with a trend toward a decrease in the number of respiratory illnesses (0.67 vs
0.42, P < 0.07). Significant decreases were also seen in the median number of
physician visits (0.50 vs 0.33, P < 0.05), courses of antibiotics administered (0.33 vs
0.28, P < 0.05), and days of school missed as a result of RT illness (0.75 vs 0.40, P <
0.05).
• Uhari and Mottonen (1999)35 reported a 15 month randomised controlled trial to
evaluate a programme for reducing infection transmission in 20 US child daycare
centres. Most of the infections that did occur were viral. The programme included
increased handwashing, cleaning of the daycare centers and regular washing of toys.
Both the children and the personnel in the program centers had significantly fewer
infections than those in control centers, the reduction being 9% (P < 0.002) among 3year-old children and 8% (P = 0.049) among older children. The children at the
program centers received 24% fewer prescriptions of antimicrobials (P < 0.001).
Likewise, there were 2.5 man-year fewer absences from work on the part of parents
because of a child's illness during 1 year in the program centers, a 24% difference (P <
0.001).
Since 2007, 3 new intervention studies (one in the home and two in schools) have been
reported, which assessed the effect of promotion of environmental cleaning with or without
hand hygiene, on rates of GI, RT, and skin and eye infections:
• In a household study carried out in South Africa in 2007 by Cole et al.,36 the effects of
intensive hand and environmental hygiene education alone and in combination with
use of hygiene products (soap, surface cleaner/disinfectant, and antiseptic) were
assessed. Four communities (685 households) participated: two of government (RDP)
housing (indoor tap/flush toilet) and two of informal (INF) housing (communal
tap/latrines). Illness symptoms were monitored weekly and reinforced diseaseprevention behaviours established through participatory learning focusing on
handwashing/bathing with soap, cleaning toilet and food surfaces, and treating skin
problems with antiseptic. RDP and INF communities were located in 2 areas, with one
96
area receiving education and products (intervention), and the other receiving education
only. Illness data were gathered from Jun-Nov 2006 (baseline), and for the same 2007
period following education and product introduction and the percentage reduction in
illness calculated.
Table 5 – Incidence and reduction in gastrointestinal, respiratory and skin disease in
hygiene intervention and control households in government and informal housing
communities
Incidence and reduction in gastrointestinal, respiratory and skin
disease
Gastrointestinal
Respiratory
Skin
Reduction Reduction Reduction Reduction Reduction Reduction
%
difference %
difference %
difference
Formal housing
Education +
78.6%
14.0%
74.2%
24.6%
65.5%
39.1%
products
Education only 64.6%
49.6%
26.4%
Informal housing
Education +
77.4%
11.3%
57.4%
37.8%
74.6%
-2.5%
products
Education only 66.1%
19.6%
77.1%
Table 5 indicates that hygiene promotion produced a significant reduction in rates of
infection. Calculation of hazard ratios (HR) using proportional hazard models indicated that
RDP controls were more likely to experience GI (HR=1.27, CI: 1.10-1.46), RT (1.25, CI 1.081.43) and skin (HR=1.26, CI: 1.10-1.44) illnesses than intervention counterparts. INF
controls were more likely to experience GI (HR=1.43, CI: 1.26-1.62), RT (HR=1.26, CI: 1.111.44) and skin (HR=1.46, CI: 1.29-1.66) infections than intervention counterparts.
• In 2008, Sandora et al.37 reported a cluster-randomised, controlled trial at an
elementary school in the USA. Intervention classrooms (285 students) received
alcohol hand sanitizer and quaternary ammonium wipes to disinfect classroom
surfaces daily for 8 weeks; control classrooms followed usual hand-washing and
cleaning practices. Absenteeism rates for GI illness were significantly lower in the
intervention-group; 24% of students in the control group missed ≥1 day because of GI
illness, compared with 16% of students in the intervention group. Absenteeism rates
for respiratory illness were not significantly different between groups. After adjusting
for race, health status, family size, and current hand-sanitizer use in the home, the
absenteeism rate for GI was significantly lower in the intervention group compared with
the control group [rate ratio: 0.91 (P < 0.01)]. The adjusted absenteeism rate ratio for
respiratory illness was 1.10 (P < 0.12). Of interest is the fact that swabs of
environmental surfaces were also taken which showed that norovirus was present on
29% of surfaces evaluated in control classrooms. In the intervention classrooms this
was reduced to 9%.
• Bright et al.(2009)23 carried out a 6 week intervention study of the impact of hygiene in
6 (3 intervention, 3 control, 148 students) classrooms in a school in Seattle, USA. For
the intervention group, test surfaces were cleaned with a disinfectant wipe each
morning before arrival of students. Surfaces were sampled in the afternoon on 4 study
days, and mean heterotrophic bacterial counts determined. Teachers collected
information on the incidence of GI and RT illnesses (self-reported coughing, sneezing,
fever, headache, sinus problems, sore throat, vomiting, abdominal pain, diarrhoea)
leading to absenteeism. Although there was a reduction in the bacterial counts in
intervention classrooms, the results were not statistically significant. Water fountain
toggles, pencil sharpeners, computer keyboards, and faucet handles were the most
97
bacterially contaminated. Influenza A virus and norovirus was also detected on 24%
(13 of 54) and 16.4% (9 of 55) of control classroom surfaces, respectively. During 2
weeks prior to the viral sampling date, from 3 to 6 children had been absent from
control classrooms due to illness. Despite no significant reduction in bacterial counts
on surfaces, children in control classrooms were 2.32 times more likely to become ill
than children in intervention classrooms (p=.026, 95% CI 1.03–5.28). In control
classrooms, 26 of 74 children (35.1%) became ill (either GI or RT symptoms) with a
total of 57 days absent, whilst 14 of 74 children (18.9%) became ill in the intervention
classrooms with 22 days absence.
Impact of hygiene measures on gastrointestinal diseases
In the section above, 3 intervention studies (one in the home and two in schools) are
reported, which assessed the effect of promotion of environmental cleaning with or without
hand hygiene, on rates of GI infections:
• The South Africa household study by Cole et al.36 (Table 5) showed that hand and
environmental hygiene education alone or combined with use of hygiene products
could produce, respectively, up to 64.6% and 78.6% reduction in the incidence of GI
infection.
• The US study of Sandora et al.37 in elementary school settings showed that
absenteeism rates for GI illnesses were significantly lower in classrooms where
students used alcohol hand santizers and surface disinfectants compared with control
classrooms that followed usual hand-washing and cleaning practices. Adjusted and
unadjusted absenteeism rate ratios were 0.91 and 0.86 respectively for intervention
compared with the control groups.
• The US classroom study of Bright et al.23 showed that children in control classrooms
were 2.32 times more likely to become ill than children in intervention classrooms (P
=0.026, 95% CI 1.03–5.28) where surfaces were cleaned with a disinfectant wipe each
morning before arrival of students. In control classrooms, 35.1% of children became ill
(either GI or RT symptoms) with a total of 57 days absent, whilst 18.9% became ill in
the intervention classrooms with 22 days absence. There was no attempt to distinguish
the impact on respiratory compared with GI infections
Three further studies indicate that surface hygiene (in one study this was combined with
handwashing promotion) has a significant impact in reducing spread of norovirus infection:
• Following recurrent and consecutive norovirus outbreaks on a cruise ship, the ship was
cleaned and disinfected at the end of the fourth cruise.513 Fewer than 10 cases
presented on subsequent cruises compared to195 cases during the fourth cruise.
Control measures included cleaning and disinfection of cabins, crew and staff quarters
and communal bathrooms and steam cleaning of soft furnishings.
• During a hospital outbreak of norovirus, the attack rate among patients decreased in
several wards following implementation of environmental hygiene procedures.42
Infection control measures included cleaning and hypochlorite disinfection (ward floors,
toilet areas, toilet seats, taps and spillages of vomit and faeces) to reduce
environmental contamination. Disinfection was applied to places contaminated with
vomit or faeces and for general disinfection of ward floors and toilets areas.
• Heijne et al. analysed norovirus outbreaks in 7 camps at an international scouting
jamboree in the Netherlands. Implementation of hygiene measures such as washing
hands, thoroughly cleaning contaminated surfaces, avoiding contact between sick and
healthy persons, and requesting caretakers and cleaning staff to wear gloves and
aprons coincided with an 84.8% reduction in the reproduction number. 572
The potential for transfer of rotavirus infections via surfaces and hands is shown in an
intervention study by Ward et al.(1991).40 These workers examined transfer of rotavirus from
98
contaminated surfaces to the mouth and from surfaces to hands to the mouth. All volunteers
who licked rotavirus contaminated plates became infected. Of those individuals who touched
the virus-contaminated plates with their fingers and put the fingers to their mouths, about half
became infected. It was found that 13 out of 14 adult subjects who consumed rotavirus (103
focus forming units) became infected.
The 2006 IFH review8 summarises the results of 6 intervention studies indicating the positive
impact of environmental cleaning and hygiene on infection risks associated with C. difficile.
In more recent hospital intervention studies by Hacek et al. 573 and Abderrahmane et al. 574
report reduction in nosocomial rates of C difficile infection associated with targeted cleaning
of the environment using hypochlorite disinfectant. Salgado et al.(2009) 575 also report control
of an outbreak without a change in antibiotic policy as a result of enhanced cleaning with
bleach, and soap and water hand hygiene when caring for patients. Although these studies
were carried out in hospitals they indicate the potential for transmission in the home where
good hygiene practice is not observed.
Impact on respiratory tract infections
Gwaltney and Hendley (1982)263 examined the impact of surface disinfection on transfer of
experimental rhinovirus infection in 4 studies by having recipients handle surfaces previously
contaminated by infected donors and then touch their nasal and conjunctival mucosa. Five
(50%) of 10 recipients developed infection after exposure to virus-contaminated coffee cup
handles and 9 (56%) of 18 became infected after exposure to contaminated plastic tiles.
Spraying contaminated tiles with disinfectant reduced recovery of virus from the tiles from
42% (20/47) to 8% (2/26) and the rate of detection of virus on fingers touching the tiles was
reduced from 61% (28/46) with unsprayed tiles to 21% (11/53) with sprayed tiles. Fitly-six
percent (9/16) of recipients exposed to untreated tiles became infected while 35% (7/20)
touching only sprayed tiles became infected with rhinovirus.
Three more recent intervention studies (one in the home and two in schools), as described
above, are reported, which assessed the effect of promotion of environmental cleaning with
or without hand hygiene, on rates of RT infections:
• The South Africa study in household settings by Cole et al.36 (Table 5), showed that
hand and environmental hygiene education, alone or combined with use of hygiene
products, produced, respectively, up to 26.4% and 65.5% reduction in incidence of RT
infections.
• The US study of Sandora et al.37 in elementary school settings showed that
absenteeism rates for RT illnesses were not significantly lower in classrooms where
students used alcohol hand santisers and surface disinfectants compared with control
classrooms that followed usual hand-washing and cleaning practices. Adjusted and
unadjusted absenteeism rate ratios were 1.10 and 1.07 respectively for intervention
compared with the control groups.
• The US classroom study of Bright et al.23 showed that children in control classrooms
were 2.32 times more likely to become ill than children in intervention classrooms (P =
0.026, 95% CI 1.03–5.28) where surfaces were cleaned with a disinfectant wipe each
morning before arrival of students. In control classrooms, 35.1% of children became ill
(either GI or RT symptoms) with a total of 57 days absent, whilst 18.9% became ill in
the intervention classrooms with 22 days absence. There was no attempt to distinguish
the impact on respiratory compared with GI infections.
In 2009, Jefferson et al.48 reported a systematic review of 58 epidemiological studies on the
impact of physical interventions to interrupt the spread of viral respiratory tract infections.
None of the intervention studies assessed the impact of surface hygiene.
99
Impact on skin infection
In the South Africa study in household settings by Cole et al.36 (Table 5 ), it was found that
that intensive hygiene education alone (participatory learning focusing on
handwashing/bathing with soap, cleaning toilet and food surfaces, and treating skin
problems with antiseptic) and in combination with use of hygiene products could produce,
respectively, up to 26.4% and 65.5% reduction in the incidence of skin infection.
In studies45,46,47 in the homes of healthcare workers (HCWs) colonised with MRSA, the HCW
was treated to eradicate the organism, but subsequently became re-colonised. In each case,
MRSA was isolated from environmental surfaces (pillows, bed linen, brushes, cosmetics and
hand contact surfaces and household dust) in the home. In each case, the problem was
finally terminated only after thorough cleaning of the home environment.
A hospital intervention study by Dancer et al.41 indicates that enhanced hygiene of near
patient hand contact surfaces can reduce transmission of MRSA. In this study, an additional
cleaner was introduced into 2 wards, with each ward receiving enhanced cleaning for 6
months. Enhanced cleaning was associated with a 32.5% reduction in microbial
contamination rates at handtouch sites. Near-patient sites (lockers, overbed tables and
beds) were more frequently contaminated with MRSA/S. aureus than sites further from the
patient. Genotyping identified indistinguishable strains from handtouch sites and patients,
supporting the possibility that patients acquired MRSA from environmental sources. There
was a 26.6% reduction in new MRSA infections on wards receiving extra cleaning, despite
higher MRSA patient-days and bed occupancy rates during enhanced cleaning periods.
Adjusting for MRSA patient-days and based on 9 new MRSA infections seen during routine
cleaning, they expected 13 new infections during enhanced cleaning periods rather than the
4 that actually occurred. Clusters of new MRSA infections were identified 2 to 4 weeks after
the cleaner left both wards.
This is one of a number of studies which indicate the impact of environmental cleaning and
hygiene on infection risks associated with MRSA. 576,577,578 Although these studies were
carried out in hospitals they indicate the potential for transmission of MRSA in the home in
situations where good surface hygiene practice is not observed.
Elias et al.96 describe a community-based intervention to manage an outbreak of communityassociated MRSA skin infections in a US Midwestern county jail. A systematic investigation
conducted by a family medicine residency program identified 64 total cases and 19 MRSA
cases between January 1 and December 31, 2007. Even though they could not separate the
effect of individual interventions, based on the data, factors identified as contributing to
MRSA transmission included inadequate surveillance, lack of antibacterial soap, and a
defective laundry process.
Higashyami et al. (2011) investigated dissemination of community-associated MRSA (CAMRSA) strains among healthy students in a Japanese boarding school, which frequently
caused skin infection. 579 Of 21 patients with skin disease, in whom MRSA strains were
isolated, MRSA colonization rates in 3 selected groups ranged from 7.6% to 36.6%. Genetic
analysis revealed dissemination of a PVL-positive SCCmec IVc clone (41/47 isolates in
total). Risk factors for CA-MRSA infection included skin damage, frequent-contact sports,
inadequate hygiene, sharing of equipment or clothing, scratching insect bites, hot and humid
weather, and crowded dormitory rooms containing 6-10 students. Among the 50 contact
points, one PVL-positive MRSA strain was isolated from a toilet seat. MSSA strains were
also isolated from tatami mats in the judo facility, mats from the wrestling club, and a
strength-training machine. Based on these risk factors, students were educated about SSTIs
and hygiene practices and alcohol-based handrub dispensers were installed. Rates of skin
disease and MRSA carriage decreased significantly after infection controls were introduced.
100
Some of the best evidence that contaminated surfaces are involved in transmission of
infection in hospitals, comes from relatively recent findings that admission to a room when
the prior room occupant was infected or colonised with a pathogen increases their risk of
acquisition. These data are review by Otter et al. 2011 and include studies involving MRSA,
C.difficile and P aeruginosa.44
6. USE
OF
QUANTITATIVE MICROBIAL RISK ASSESSMENT (QMRA)
TO EVALUATE THE
HEALTH IMPACT OF HYGIENE
Although intervention studies yield quantitative data on health impact, the reliability of
estimates is difficult to confirm. On the other hand, data from in vivo and in vitro tests can be
used to quantify the impact of hygiene procedures on transmission of infectious agents, but
give no assessment of how contamination reduction on hands correlates with health impact.
In an attempt to overcome this problem, Haas et al. have applied techniques of Quantitative
Microbial Risk Assessment (QMRA) to estimate the relative health benefits resulting from the
use of hygiene procedures with different efficacies. 580 This involves using microbiological
data from the published literature, related to each stage of the infection transmission cycle to
calculate infection risk. The investigators used this approach to compare the impact of
different hand hygiene procedures in preventing transference of E. coli and E. coli O157:H7
from hand-to-mouth following hand contact with ground beef during food preparation. 581 Data
on the density of pathogens in ground beef, transference from beef to hands, removal by
handwashing or alcohol hand sanitiser (AHS), rate of transfer from hand-to-mouth and
infectivity of ingested pathogens were obtained from the literature, and, after screening for
data quality, used to develop probability distributions. With some plausible assumptions, it
was assessed that, assuming that there are 100 million individuals in the United States each
of whom handles ground beef once per month, this results in 1.2 x 109 contacts per year.
Assuming that 10% of these individuals contact hand-to-mouth after handling ground beef,
this amounts to 1.2 x 108 incidents per year. For E. coli O157:H7, it was assessed (Table 6)
that if no handwashing is done this would result in 0.7 infections per year. By contrast, if all
individuals washed their hands with soap following contact with ground beef, producing a 0.3
log reduction on hands, this would result in an estimated 0.014 infections per year, equating
to a 98% median risk reduction compared with no handwashing. If all individuals used a
hand hygiene process, following contact with ground beef, producing a 4.3 log reduction on
hands (i.e. they used an AHS), this would then result in an estimated 0.00005 infections per
year, equating to a 99.9996% median risk reduction for use of the AHS compared with
handwashing.
Table 6 – Risk of infection from handling raw beef contaminated with E. coli O157, and
subsequent hand-to-mouth contact with or without hand hygiene intervention581
No handwashing
Handwashing
Use of alcohol hand
rub
Log reduction on hands
0.7
4.3
Mean
1.39 x 10-2
1.25 x 10-2
1.15 x 10-2
-9
-10
Median
5.98 x 10
1.18 x 10
3.71 x 10-13
-2
-2
Standard deviation
7.79 x 10
7.52 x 10
7.26 x 10-2
This follows on from an earlier study by Haas et al. 582 to calculate ID risks associated with
hand-to-mouth transfer after diaper changing of a baby infected with Shigella. Based on this
model, it was calculated that the probability of acquiring infection was between 24/100 and
91/100 for those who used handwashing with soap after changing diapers. This was based
on panel test data indicating that the mean log reduction of S. marcescens on hands due to
101
handwashing is 2.56. The authors calculated that, by using a hand hygiene formulation
which increased the log reduction in release of bacteria from hands to 2.91, the infection risk
would be reduced to between 15/100 and 90/100.
In another study, Gibson et al.115 applied QMRA to estimate the relative infection risks
associated with fabrics laundered with detergent alone or with detergent plus bleach. The
study modelled transference of Shigella from hand-to-mouth following hand contact with
laundered clothing. Rose and Haas 583 have also applied QMRA as a means to assess the
potential impact of antibacterial soap use on skin infection with S. aureus.
Risk modelling is a promising approach, but has limitations because of the multifactorial
nature of infection transmission and paucity of data to specify model parameters. What the
data does illustrate however is how a quantifiable increase in the log reduction, for example,
an increase from a 2.5 to a 3.5 log reduction on hands can translate into a significant
decrease in the risk of infection transmission within a national population. More information
and data on QMRA can be found on the Quantitative Microbial Risk Assessment Wiki site
(QMRAwiki) at: http://wiki.camra.msu.edu/index.php?title=Table_of_Recommended_BestFit_Parameters. QMRAwiki is the QMRA community's portal for current quantitative
information and knowledge developed for the Quantitative Microbial Risk Assessment
(QMRA) field. It is an evolving repository for QMRA knowledge and data available to the risk
analysis community.
To study the potential effectiveness of a targeted disinfection program for food preparation in
household kitchens, Duff et al. 584 developed a computer-based model in which published
literature and expert opinion for US, Canada and UK was used to estimate the cost of the
program, the number of cases of Salmonella, Campylobacter, and E. coli O157 infections
prevented. The model estimated that approximately 80,000 infections could be prevented
annually in US homes, resulting in $138 million in direct medical cost savings, 15,845
quality-adjusted life-years (QALYs) gained, as against $788 million in programme costs.
Results were similar for households in Canada and the UK. Evaluating the program for
households with high-risk members showed a more favourable cost-effectiveness.
102
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