Risk assessment and new developing strategies to reduce

Transcription

Science against microbial pathogens: communicating current research and technological advances
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A. Méndez-Vilas (Ed.)
Risk assessment and new developing strategies to reduce prevalence of
campylobacter spp. In broiler chicken meat
Djamel Djenane1 and Pedro Roncalés2
1
Department of Microbiology and Biochemistry. Faculty of Biological and Agricultural Sciences. University Mouloud
Mammeri, BP 17. 15000. Tizi-Ouzou, Algeria
2
Department of Animal Production and Food Science. University of Zaragoza. C/ Miguel Servet, 177-50013. Zaragoza.
Spain
1. Introduction
Over the last two decades, Campylobacter has emerged as the most commonly reported cause of bacterial enteritis in
humans in the UE and most other developed countries. Campylobacter spp. contamination of chicken carcasses is
common, and poultry is generally recognised to play a significant role in human Campylobacter spp. infection.
Campylobacteriosis remains the most frequently reported zoonotic disease in humans in the EU with an incidence rate
of approximately 50 confirmed cases per 100,000 population in over 17 countries. It is estimated that there are
approximately nine million cases of human campylobacteriosis per year in the EU27 (EFSA, 2010, 2011).
Campylobacter are ubiquitous bacteria, frequently found in the alimentary tracts of animals, especially birds, and
commonly contaminate the environment, including water. Campylobacteriosis in humans is caused by emerged
thermotolerant Campylobacter spp. Campylobacter jejuni (C. jejuni) has recently overtaken Salmonella spp. as the
major reported source of food-borne bacterial diseases within the European Union. C. jejuni has been found associated
with biofilms of other bacterial species. Biofilm formation may play a role in the epidemiology of C. jejuni infections
(Gunther and Chen, 2009). Although it is generally recognized that there are many sources of Campylobacter,
Campylobacteriosis is predominantly believed to be associated with the consumption of poultry meat, especially fresh
broiler meat. Over the past decade, Risk Analysis—a process consisting of risk assessment, risk management and risk
communication—has emerged as a structured model for improving food control systems, with the objectives of
producing safer food and reducing the numbers of foodborne illnesses. Therefore, control of Campylobacter spp.
commonly focuses on reducing its occurrence in broiler meat. In recent years, several quantitative risk assessments for
Campylobacter spp. in broiler meat have been developed to support risk managers in controlling this pathogen. The risk
assessments are not only used to assess the human incidence of campylobacteriosis due to contaminated broiler meat,
but more importantly for analyses of the effects of control measures at different stages in the broiler meat production
chain. Microbiological risk assessment can be considered as a tool that can be used in the management of the risks
posed by foodborne pathogens and in the elaboration of standards for food in international trade.
Given the public health and economic problem represented by Campylobacter spp., it is important to take measures
in order to reduce its prevalence throughout the poultry production chain leading to a reduced incidence of the human
illness. Several strategies have been applied to reduce Campylobacter spp. counts on chicken meat, including attempts
to elimination from the farms by increasing biosecurity and the separation of contaminated flocks, and by improving
hygiene during the process of slaughtering. In addition, several experimental approaches like the reduction of
colonization by competitive exclusion, antibacterial agents, or phage therapy are being investigated for their efficacy.
The combination of prebiotics and probiotics to reduce Campylobacter spp. are known as symbiotic, and may have
antimicrobial activity. It is generally acknowledged that Campylobacter spp. is sensitive to acid conditions. Several
strategies developed to reduce Campylobacter spp. populations are based on the acidification of the pathogen
environment or by acidification of drinking water and feed. Although these measures undoubtedly will help to control
shedding of Campylobacter by the animals and may reduce the number of positive flocks, vaccination of poultry against
Campylobacter will probably be most effective and remains a major goal. However, several studies have actually
pointed out partial association between the veterinary use of antibiotics and the emergence of resistant strains of
Campylobacter spp. related to human enteritis. In recent years, there has been increased research interest in the use of
nonthermal alternative methods for microbial inactivation, such as high hydrostatic pressure or pulsed electric fields
(Sagarzazu et al., 2010). The attraction of these technologies lies in the production of microbiologically safe foods with
minimal changes in their sensory and nutritional attributes. Consumers demand high quality, natural, nutritious, fresh
appearance and convenient meat products with natural flavour and taste and an extended shelf-life. One area of research
is the development of new and improved methods of meat preservation. Due to negative consumer perceptions of
artificial preservatives, attention is shifting towards alternatives that the consumers perceive as natural and in particular,
biopreservation and plant extracts, including their essential oils (EOs) and essences (Djenane et al., 2011a,b). It is well
established that these natural compounds have antimicrobial properties against C. jejuni. This chapter presents a short
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review of recent works on the strategies application to prevent or reduce Campylobacter spp. contamination in broiler
meat.
2. Chicken meat production and the implications for Campylobacter
2.1 Primary production
The public health benefits of controlling Campylobacter spp. in primary broiler production are expected to be greater
than control later in the chain as the bacteria may also spread from farms to humans by other pathways than broiler
meat. Workman et al. (2008) indicate that Campylobacter spp. horizontal transmission is the most significant mode of
broiler flock colonization. It is widely assumed that farm workers constitute risk factors for colonization of the flock,
and that human traffic is an important vehicle for Campylobacter being introduced into the poultry house from the
external environment. Water in drinkers can also be contaminated and act as a rapid vector of Campylobacter
spp.within the flock. Once a bird is colonized with Campylobacter spp., it will excrete large numbers of the organism in
its faeces. Contact with the faeces of such a bird is one mechanism by which the organisms spread throughout a flock.
However, the second consequence of this excretion of organisms is the contamination of the exterior of the birds. This
external contamination may occur while the birds are on the farm or during transportation to the slaughter facility. It has
been shown that Campylobacter strains can survive overnight in slaughterhouses surfaces after a cleaning and
disinfection procedure and highlight a new putative source of carcass contamination during processing (Peyrat et al.,
2008).
Table 1. Prevalence of Campylobacter-contaminated broiler batches, by country and in the EU.
Country
Netherlands
Sweden
Iceland
Denmark
Austria
Denmark
Japan
France
USA
Canada
Belgium
France
Spain
Finland
Broiler batches
661
287
71
125
398
8911
212
75
32
93
446
422
389
411
Prevalence (%)
32
27
25
50.4
56.8
42.5
32.1
42.7
87.5
60
86.8%
67.1
88
3.9
References
Jacobs-Reitsma et al., 1995
Berndtson et al., 1996
Birgisdottir et al., 2001
Dang et al., 2001
Ursinitsch et al., 2001
Wedderkopp et al., 2001
Chuma et al., 2001
Refregier-Petton et al., 2001
Stern et al., 2001
Nadeau et al., 2002
Ghafir et al., 2007
EFSA, 2010
EFSA, 2010
EFSA, 2010
2.2. The slaughter and processing of chicken
The prevalence of flock positivity is directly related to slaughter age. In Sweden, Berndtson et al. (1996) found that
where the majority of flocks are harvested at 33-35 days of age; increasing the age of slaughter to 42-44 days increased
the flock positivity by about two-fold and to 48-61 days by about four-fold. Campylobacter spp. can be expected to
contaminate the chicken meat during slaughter and processing of chicken as a result of faecal contamination. The
process operations that have been found to cause the greatest changes in the contamination are: scalding, de-feathering,
evisceration, washing and chilling (Rosenquist et al., 2006). The stunning process has few microbiological implications,
although birds may sometimes inhale contaminated water, which can reach internal tissues (Gregory and Whittington,
1992). Although immersion scalding results in a net reduction in carcass contamination, the highly contaminated state
of the water offers ample opportunity for microbial transmission between carcasses. The principal microbiological
problem with de-feathering is cross-contamination of carcasses associated with the mechanical action of the machines,
and the tendency to disperse microbial contaminants in all directions via aerosols. Evisceration is a critical stage where
bacteria can be spread in poultry processing (Perko-Mäkelä et al., 2009). In most cases, the levels and numbers of
carcasses contaminated can significantly increase (ICMSF, 1980). Of major importance is the need to minimize rupture
of the exposed intestines and prevent the spread of faecal Campylobacter, which is present in relatively high numbers in
the intestines of positive birds. Washing has been found to produce a ten-fold reduction in Campylobacter (Cudjoe et
al., 1991), but it would be expected to have little effect on cells attached to carcass surfaces. C. jejuni has been found to
form and attach onto biofilm in the poultry industry (Nguyen et al., 2011) thus being an important source of
contamination of final products. Biofilms may provide the ideal niche for C. jejuni survival, as there are
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microenvironments in the biofilm that are believed to provide ideal conditions for development. A reduction in the
Campylobacter spp. concentration on chicken carcasses may also be obtained by interventions aimed at reducing the
concentration of Campylobacter spp. in the intestines of the living birds (Rosenquist et al., 2006).
Table 2. Prevalence of Campylobacter-contaminated broiler carcasses, by country and in the EU, 2008 (EFSA, Journal,
2010).
Country
Austria
Denmark
Estonia
Germany
Luxembourg
Portugal
Spain
Sweden
United Kingdom
Broiler
batches
408
396
102
432
13
421
389
410
401
% Prevalence
80.6
31.4
4.9
60.8
100
70.2
92.6
14.6
86.3
2.3 Distribution, retail, consumer handling and preparation
Many papers have reported on the level of contamination with Campylobacter spp. in retail poultry meats and/or byproducts. For example, the prevalence of Campylobacter spp. was reported to be 32.0–43.0% in Germany (Adam et al.,
2006), 50.5–73.5% in the UK (Meldrum et al., 2006), 79.0% in the USA (Nannapaneni et al., 2005), and 62.4% in
Canada (Valdivieso-Garcia et al., 2007).
The majority of Campylobacter infections are acquired via the oral route after handling raw poultry or consuming
undercooked poultry. Seasonality has been found to influence the Campylobacter prevalence in retail chicken meat
(Boysen et al., 2011). Contaminated chickens are most abundant during summer and early autumn. At home, during
meal preparation, individuals can be exposed to Campylobacter from fresh chicken through a large number of
pathways. These pathways include: direct contamination from the chicken to any food commodities not undergoing a
subsequent cooking step before ingestion; indirect contamination of surfaces upon which cooked products or ready-toeat food are placed; contamination directly onto hands and subsequent ingestion; insufficient cooking; and a wide
variety of other potential contamination events. Transfer can be facilitated by liquid carried on hands, utensils and
cutting boards. Unsafe food handling procedures in private kitchens are assumed to be responsible for a large number of
cases of food-borne diseases in most countries (Zhao et al., 1998).
3. Campylobacter risk assessments and hazard identification
The pathogenesis of Campylobacter has been reviewed (Wooldridge and Ketley, 1997). Motility, chemotaxis and the
flagella are known to be important factors in the virulence as they are required for attachment and colonization of the
intestinal epithelium (Ketley, 1997). Once colonization has occurred, Campylobacter may perturb the normal absorptive
capacity of the intestine by damaging epithelial cell function either directly, by cell invasion and/or production of
toxin(s), or indirectly, following the initiation of an inflammatory response (Wooldridge and Ketley, 1997). The
exposure assessment initially evaluates the frequency and levels of Campylobacter on the farm, estimating the
probability that a random flock is Campylobacter-positive, the within-flock prevalence and the levels of colonization
and contamination of the broilers. Subsequently, the stages of transport, processing, storage and preparation by the
consumer are explored, and combined to predict the overall impact that these stages will have upon the contaminating
Campylobacter load on a random chicken carcass or product, and to determine the final exposure level. Hazard
characterization describes the adverse health effects of organism. This component of the risk assessment usually
includes a dose-response relationship. This is represented as a probability that a random member of the population will
become infected or ill after exposure to a specific number of Campylobacter organisms. The types of data that can be
used to establish dose-response relationships include animal and human feeding studies, and epidemiological data, such
as data from outbreak investigations. Populations at risk with respect to infectious diseases often include the elderly,
children and individuals suffering from illnesses that compromise their immune systems (e.g. AIDS and cancer
patients). As birds are prepared, caught, loaded, transported to processing plants and finally slaughtered, they undergo
stresses that may affect not only broiler meat quality, but also its microbiological status (EFSA, 2011). The normal,
balanced gut microflora in animals provides reasonable protection against colonization with pathogens. Stress in
animals can disturb this status, weaken the immune responsiveness, and cause an increase in shedding of pathogens.
Hence, stress management is a relevant aspect of pathogen control. During transportation to the slaughterhouse, and
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while waiting to be slaughtered, the stress of crowding birds in close proximity in crates is likely to further disseminate
Campylobacter contamination present in faeces, and on the skin and feathers or released from the gastrointestinal tract.
Spreading untreated farm wastes containing enteric pathogens as fertilizers on pasture or agricultural land for crop
production can mediate further infections or re-infections of animals with pathogens through contaminated grazing,
harvested feed or water supply (Hutchison et al., 2004).
Table 3. Growth characteristics of thermophilic Campylobacter species (ICMSF, 1996).
Temperature
pH
O2
CO2
Water activity
Na Cl
Optimum
40–42°C
6.5–7.5
3 – 5%
10%
0.997
0.5%
Inhibition
< 30°C – > 45°C
< 4.9 – > 9.0
0 – 15 to 19%
< 0.987
>2%
3.1. Antibiotic-resistant
The use of antimicrobial agents in food animals has resulted in the emergence and dissemination of antimicrobialresistant bacteria, including antimicrobial-resistant Campylobacter (Helms et al., 2005), which has potentially serious
impact on food safety in both veterinary and human health. The antimicrobial resistance, especially to fluoroquinolone,
ciprofloxacin, increased in many Campylobacter species. This is particularly seen as a risk for fluoroquinolone resistant
Campylobacter (Geenen et al., 2010), and the use of antimicrobials to control Campylobacter in broilers is strongly
discouraged. Andersen et al. (2006) found that raw food samples from the retail level represent an important sampling
point, which reflects the consumer exposure to resistant C. jejuni originating from raw poultry.
3.2 Disease description
The most common pathogenic species for humans are C. jejuni and C. coli. Motility by the flagellum is required for
efficient colonisation of intestinal cells. Cell invasion is a major pathogenic mechanism of Campylobacter infection.
Campylobacters have been shown to produce cytotoxic proteins that may play a role in clinical courses of the disease.
Apart from causing diarrhoea, Campylobacters can cause neurological complications such as Guillain-Barré syndrome
(GBS) and the Miller Fisher Syndrome. Evidence suggests an association between Campylobacter illness and a rare but
serious paralytic condition, GBS, a demyelinating disorder of the peripheral nervous system resulting in weakness,
usually symmetrical, of the limbs, weakness of the respiratory muscles and loss of reflexes. Early symptoms of GBS
include burning sensations and numbness that can progress to flaccid paralysis (Yan et al., 2005). GBS has been
estimated to occur about once in every 1000 cases of campylobacteriosis (Allos, 1997). The syndrome is correlated with
prior infection by C. jejuni in up to 40% of cases (Nachamkin et al., 2000). It has been shown that GBS arises as a
result of autoimmune attack due to molecular mimicry that exists between certain lipopolysaccharide (LPS) molecules
of C. jejuni strains and human nerve tissue gangliosides. Furthermore, some serotypes of C. jejuni are associated with
GBS. Reactive arthritis (incomplete Reiters Syndrome) has been estimated to occur in approximately 1% of patients
with campylobacteriosis. The symptoms occur seven to ten days after onset of diarrhoea (Peterson, 1994).
3.3 Sources of illness and risk factors
A recent study showed that the number of food-borne gastrointestinal infections in humans associated with pathogens
has increased worldwide in recent years. Although salmonelloses still are the most common pathogens in most
industrialized countries, campylobacterioses are continuously increasing and have already overtaken the salmonelloses
in the EU (EFSA, 2010). The probability of illness is dependent on the occurrence of three conditional probabilities: the
probability that the organism is ingested; the probability that the organism is able to survive and infect the host once it is
ingested; and the probability of the host becoming ill once infected. The environment, the pathogen and the host are all
variables that play an important role in the probability of illness. Environmental factors include the food vehicle and the
stability of the gastrointestinal tract ecosystem. Pathogen factors include the dose, virulence, and the colonization
potential in the host gastrointestinal tract. Host factors include immune status, age and stomach contents (Coleman and
Marks, 1998). The primary risk in developed countries is considered to be the food related risk factors. There is no
doubt that poultry is a major source of Campylobacter spp. and there is scope for cross-contamination of other foods if
contaminated poultry is introduced into the kitchen. Chicken meat preparations of minced meat, marinated or seasoned
wings or filets… are a new food type introduced in the UE market and gaining growing popularity by consumers. They
may contain skin due to their nature or because of sensory characteristics (Uyttendaele et al., 2006). All of these items
have in common that they have been manipulated extensively during processing and as such also have a potential for
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Campylobacter contamination levels not only on the surface of the meat but also interior to the meat preparation. Harris
et al. (1986) observed an association between infection and not washing the kitchen cutting board with soap. Other
food-related risk factors that have repeatedly been identified include consumption of other meat types, undercooked or
barbecued meat, raw seafood, drinking untreated surface water, or unpasteurized milk or dairy products (El-Sharoud,
2009). Eating meat cooked outside the home has also been identified as a risk factor. Other food items that have been
related to sporadic cases of human campylobacteriosis are contaminated shellfish (Harris et al., 1986). Simulation
showed that eating raw chicken meat products can give rise to exposures that are 1010 times higher than when the
product is heated, indicating that campaigns are important to inform consumers about the necessity of an appropriate
heat treatment of these types of food products (Uyttendaele et al., 2006).
The importance of poultry as a risk factor for human cases has been demonstrated in countries where interventions
have been implemented in the broiler production chain or where poultry has been withdrawn from the market, and
where a decline in human cases has followed. For example, in Belgium, due to the dioxin crisis in 1999, where all
poultry meat and eggs were withdrawn from the market, the estimated reduction of campylobacteriosis cases following
this event was 40% within the crisis period (Vellinga and Van Lock, 2002). Different studies have shown associations
between sporadic human cases and animal sources, suggesting that these sources would be the most important risk
factors for sporadic human infections. Seasonal variation in Campylobacter prevalence in broilers, with a peak in the
summer has been previously reported from several countries in northern Europe (Hofshagen and Kruse, 2003). The
reason for the association of higher Campylobacter prevalence and season is not known, but appears to be temperaturerelated. During summer, ventilation and water consumption also increase because of the higher temperatures. Human
infections show similar seasonality in many European countries. There is strong evidence for frequent cross
contamination during slaughtering and product processing.
Water
Milk/meat
Chicken
Illness Campylobacter spp. sources and risk factors
4. Usual prevention methods
The poultry industry should be receptive to new interventions that could be applied at different stages during
processing. Many poultry processors have increased the use of chlorine and water and have incorporated intervention
strategies to reduce Escherichia coli and Salmonella spp. on carcasses to comply with the pathogen reduction and
HACCP regulations. However, these strategies may have little impact on the reduction of Campylobacter populations.
Strict implementation of biosecurity in primary production and Good Manufactured Practices/Hazard Analysis Critical
Control Points (HACCP) during slaughter may reduce colonization of broilers with Campylobacter.
Prevention of horizontal transmission on-farm. This control measure is generally known by the term “biosecurity”
and is concerned with protecting birds from infection from outside sources. This is a very important control measure;
because once Campylobacter enter a poultry flock the spread can be rapid and currently impossible to control. Practical
biosecurity measures at the farm level have been determined as the primary strategy to prevent colonisation of housed
broiler flocks with Campylobacter entering the processing plant and hence the food chain. Campylobacter enters the
broiler house from the exterior environment, and the most important control measure is to prevent or, more realistically,
to limit this entry (Hermans et al., 2011). The limited action of hygiene procedures is based on the fact that in
conditions where broilers are confronted with environmental factors that are scarcely controllable, biosecurity is
difficult to apply. In these production systems, Rivoal et al. (2005) have shown that, even if strict hygiene measures
allow broiler flocks to be Campylobacter-negative during the first weeks of age, birds are almost always colonized at
slaughter, after the access of birds to the open-air range. Another factor linked to biosecurity is the quality of the
drinking water. Several studies have found that drinking water of poor quality is related to an increased risk of a flock
being positive for Campylobacter (Sparks, 2009).
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Vaccination. Vaccination of animals, particularly when combined with other measures implemented further along the
food chain, can be an efficient strategy for pathogen reduction. Assuming that biosecurity can never be fully effective,
the vaccination of poultry to reduce susceptibility to Campylobacter could be used to support biosecurity measures (De
Zoete et al., 2007). Vaccination might reduce or even prevent colonization and in both cases would affect the numbers
of organisms entering the food chain and the environment. It is also important to ensure that the vaccine delivery is cost
effective (Humphrey et al., 2007).
Antibiotic use. The use of antibiotics in modern intensive animal production as growth-promoters and for therapy and
prevention of diseases could not be a rational solution to reduce Campylobacter incidence. Several studies have actually
pointed out the partial association between the veterinary use of antibiotics and the emergence of resistant strains of
Campylobacter related to human enteritis (Luangtongkum et al., 2006).
Competitive exclusion. These products consist of bacterial collections from the microbiota of adult chickens and are
given to young chicks to prevent colonization by Campylobacter species. Competitive exclusion concept can be
applied, primarily in monogastric animals. This involves feeding with complex mixtures of bacteria that reduce
attachment of pathogens to the gut mucosa. Competitive exclusion flora is a concept taking advantage of bacterial
antagonism to reduce animal intestinal colonization by pathogenic microorganisms (Schneitz, 2005). Commensal gut
flora may be manipulated by changing the diet of the animal and some research has shown that chickens given certain
diets are more prone to resist challenge with campylobacters.
Bacteriophage therapy. Bacteriophage therapy is one possible means by which Campylobacter colonization might be
controlled, thus limiting the entry of Campylobacter into the human food chain (Carrillo et al., 2011). Similarly,
experiments suggest that treating live birds with specific bacteriophages shortly prior to slaughter may be an effective
control measure (Havelaar et al., 2007). Recently, there has been a renewed interest in the use of bacteriophages as
‘therapeutic’ agents; a prerequisite for their use in such therapies is a thorough understanding of their genetic
complement, genome stability and their ecology to avoid the dissemination or mobilisation of phage or bacterial
virulence and toxin genes (Timms et al., 2010).
Bacteriocins. Other method to reduce the Campylobacter spp. load in poultry is the use of bacteriocins as a therapeutic
treatment for chickens colonized by Campylobacter (Svetoch et al., 2003). By feeding the animals therapeutic feed at
the appropriate moment in the cycle, levels and frequency of colonization can be reduced, which may be effective in
lowering the human health risk imposed by Campylobacter. Lin (2009) has reviewed anti-Campylobacter bacteriocins
for potential use in reducing the numbers of Campylobacter (jejuni as well as coli) in poultry. Stern et al. (2006) found
that control chickens (standard feed) were colonized in the caecum with 6.6–8.3 log10 CFU of Campylobacter per g,
while all treated chickens (feed modified with purified bacteriocin) contained undetectable numbers (< 2 log10 CFU/g).
Svetoch et al. (2005) administered bacteriocin E 50–52 to young chicks. High levels of C. jejuni were found in the
control chicks (8.40 log10 CFU/g of caecal contents), while no Campylobacter was detected in the treated group. Thus,
it seems that bacteriocins, administered just before slaughter, can reduce Campylobacter colonization in the chicken
caecum to undetectable levels.
Probiotic. To decrease the risk of human infection, Campylobacter should be controlled at farm levels. Orally given
probiotic bacteria could prevent colonisation of chicken with pathogenic Campylobacter (Morishita et al., 1997).
Chaveerach et al. (2004) found that Lactobacillus (P93) strain isolated from conventional chicken had potential
inhibitory activities against all tested Campylobacter. Probiotics can be incorporated in the diet. This is based on
feeding with viable microorganisms antagonistic toward pathogens via either modifying environmental factors in the
gut or producing antimicrobial compounds (Morishita et al., 1997).
Prebiotics and synbiotics. Combinations of prebiotics and probiotics are known as synbiotics, and may have
antimicrobial activity (Klewicki and Klewicka, 2004). Fooks and Gibson (2002) have yet recorded a C. jejuni inhibition
in vitro, with a population reduction below detectable level after 24 h culture, with a Lactobacillus plantarum or
Bifidobacterium bifidum, when combined with oligofructose or an oligosaccharide.
Litter acidification. Acidification of poultry litter has also been suggested as a method to limit pathogen proliferation
in breeding flocks (Line, 2002). Campylobacter was not detected in unused litter (Jacobs-Reitsma et al., 1995) probably
because the lack of moisture renders it a very hostile environment for the organism. Thus fresh litter is an unlikely
source of contamination in the house.
Freezing. Freezing of chicken products during post-processing has been shown to reduce the level of carcass
contamination and is used as part of the control strategy in some countries (Sampers et al., 2010). Rapid freezing of
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chicken carcasses may also offer additional control measures (Sandberg et al., 2005). Freezing is already used to treat
carcasses from Campylobacter colonized flocks, and reduces numbers by about 1 to 3 log10 cycles (Rosenquist et al.,
2006; Georgsson et al., 2006) with minimal impact on the appearance and quality of the meat, although using this
technique would require expanded cold storage facilities, and the increased cost of frozen storage (EFSA, 2011).
Irradiation. Chun et al. (2010) investigated the applicability of UV-C irradiation (wavelengths of 220–300 nm) on the
inactivation of C. jejuni in ready-to-eat meat and poultry meat respectively, The results have clearly indicate that UV-C
irradiation effectively decreased C. jejuni inoculated on meat during storage. Irradiation of food materials, using
electron beams (from electron accelerators) or high-energy electromagnetic radiation (gamma-rays from 60Co or Xrays), is permitted in some European countries and will inactivate campylobacters and other infectious bacteria
(Humphrey et al., 2007). The application of irradiation in poultry at doses of 1-10 kGy eliminates pathogenic bacteria
(Lacroix and Ouattara, 2000). However, irradiation might have some effects on the organoleptical quality of meat
products. The threshold dose above which off-flavors are detected in irradiated meats was reported to be 2.5 kGy for
poultry (Hanis et al., 1989). Natural antioxidants from spices could be employed to stabilize fats and control oxidative
deterioration of foods during irradiation. The effect of the combination of irradiation and marinating with rosemary and
thyme extract on the sensitivity of pathogen and sensory characteristics of poultry has also been investigated. A dose of
2-3 kGy would be sufficient to decontaminate meat from campylobacters (Ingram and Farkas, 1977; Monk et al., 1995).
However, application of this technology has been very limited. A disadvantage in the European Union is that at present
the use of gamma-irradiation for meat is strongly discouraged. Its limited use appears to be due to distrust by the public
of any process which depends on the nuclear industry as well as lack of knowledge by the public in general concerning
food borne infections and the effectiveness of irradiation. A preferred option might be to use electron accelerators
which require no isotope. These are used, particularly in UE, to decontaminate raw chicken portions (Carry et al.,
1995). Kampelmacher, (1984) showed that a dose as low as 1 kGy was effective in reducing C. jejuni by more than 4
log-cycles with this dose. The directive 1999/3/EC contains a list of foodstuffs authorized for irradiation treatment and
the doses allowed. So far, only dried aromatic herbs, spices and vegetable seasonings are included in the list. However,
irradiation of other foodstuffs including poultry is temporarily permitted in some Member States. In the United States,
FDA and USDA have approved irradiation of poultry meat at a maximum dose of 3 kGy to control foodborne
pathogens such as Campylobacter (Keener et al., 2004).
Chemical treatments. It is generally acknowledged that Campylobacter is sensitive to acid conditions. Several
strategies developed to reduce Campylobacter populations are based on the acidification of the pathogen environment.
Application of organic acids via drinking water has produced various results. Byrd et al. (2001) found that the
prevalence of Campylobacter spp. in broiler crops was reduced from 85% to 62% by application of lactic acid in
drinking water during the ten-hour feed withdrawal. Animal health and welfare were not affected by the acid
application. A pH of around 4.0 proved to be most effective against Campylobacter when formic, acetic, propionic, and
hydrochloric acids were tested in vitro as additives to a mixture of water and feed, alone or in combination (Chaveerach
et al., 2002). Skanseng et al. (2010) found that a combination of 1.5% formic acid and 0.1% sorbate reduced the
colonization of C. jejuni significantly, while a concentration of 2.0% formic acid in combination with 0.1% sorbate
prevented C. jejuni colonization in chickens. Acidifying bacteria, particularly lactic acid bacteria (LAB) may also
contribute to preserve food. Nevertheless, their antimicrobial properties are not limited to the food industry field.
Several in vitro and in vivo studies have investigated the bacterial antagonistic activities against Campylobacter
(Chaveerach et al., 2004; Svetoch et al., 2005). The authors have suggested that the inhibitory effect of Lactobacillus
(P93) on Campylobacter growth could be explained mainly by organic acids production, resulting in pH reduction.
Then, several studies have pointed out the bactericidal activity of hydrogen peroxide (H2O2) produced by LAB in the
presence of oxygen (Strus et al., 2006). Besides organic acids and H2O2, bacteriocins are the third kind of compounds
that may help to inhibit Campylobacter growth, as shown by Stern et al. (2006) for a bacteriocin produced by a
Lactobacillus salivarius strain. The antimicrobial activity of organic acids is based on the ability of their undissociated
form to penetrate through the cell membrane and to dissociate inside the cell, decreasing the intracellular pH value, thus
disrupting homeostasis which is essential for the control of ATP synthesis, RNA and protein synthesis, DNA replication
and cell growth (Hirshfield et al., 2003). Riedel et al. (2009) used formic and lactic acids to inactivate C. jejuni
inoculated on chicken skin. Riedel et al. (2009) dipped inoculated pieces of skin into 10% trisodium phosphate for 15
sec and found that numbers were reduced by about 1 log10 cycle compared to dipping in water. Arritt et al. (2002) found
that the commercial use of an effective antimicrobial chemical spray may help to reduce the level of Campylobacter on
raw poultry carcasses and reduce the volume of rinse water applied for carcass washing. Chlorine dioxide (ClO2) is a
powerful oxidising and sanitizing agent, with a broad biocidal activity against bacteria, yeasts, viruses, fungi and
protozoa (Gomez-Lopez et al., 2009). When 100 ppm ClO2 was used on chicken carcasses for 10 min, C. jejuni was
reduced by 0.9–1.2 log cycles (Hong et al., 2007). Doyle and Waldroup (1996) found that ClO2 added to chill water in
two commercial broiler processing plants reduced Campylobacter spp. concentrations by 90%. The effectiveness of
electrolyzed water for killing C. jejuni on poultry was also evaluated. Complete inactivation of C. jejuni occurred within
10 s after exposure to electrolyzed water or chlorinated water, both of which contained 50 mg/l of residual chlorine.
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Results demonstrated that electrolyzed water was very effective not only in reducing the populations of C. jejuni on
chicken, but also could prevent cross-contamination of processing environments (Park et al., 2002). Hot water treatment
of broiler carcasses may result in reductions in Campylobacter counts varying from 0.27 and 1.5 log10 units (EFSA,
2011). Most of these chemicals have been investigated in laboratory studies by inoculating samples of skin, meat or
whole carcasses, and then dipping them into solutions of the chemicals (Riedel et al., 2009). Immersion is a very
effective method of ensuring full coverage of a product (Hong et al., 2007). In some countries, chlorine, as
hypochlorite, has traditionally been used at levels of 50 ppm and higher in the water used during poultry processing,
including in the water for immersion chilling (EFSA, 2011). Automatic spraying is the alternative method of applying
chemicals to chicken carcasses.
5. New developing strategies against Campylobacter in food
Campylobacter jejuni
(Log10 cfu/g)
Essential oils. Increased consumer demand for all natural food products has put pressure on industry and regulatory
agencies to closely examine the potential for use of natural antimicrobials that prevent or control the growth of
foodborne pathogens and spoilage microorganisms. Although many studies have indicated that EOs have the potential
to be used as a natural antimicrobial preservative in the food industry (Djenane et al., 2011a,b), the success in simple
agar diffusion systems has not been seen in foods because the antimicrobial activity of EO is reduced in the presence of
fat and protein (Burt, 2004). It is generally supposed that the high levels of fat and/or protein in foodstuffs protect the
bacteria from the action of the EO in some way (Tassou et al., 1995). In one of such studies, an increase in
concentration of 10-fold when used in pork sausages, 50- fold when used in soup and 25 to 100-fold when used in soft
cheese, 2-fold when used in minced beef and chicken was required to produce a similar effect to that reported in vitro
(Djenane et al., 2011c,d). Also the oils may have been less effective on the chicken skin because of the rough surface of
the skin, which allowed greater adhesion by the bacteria (Fisher and Philips, 2006). EOs, as antimicrobial agents present
two main characteristics: first is their natural origin, which means more safety for consumers, and second is that they
are considered to be of low risk for resistance development by pathogenic microorganisms.
Storage time (days)
Fig.1. Inhibition growth of C. jejuni by I. graveolens, L. nobilis, P. lentiscus and S. montana EOs at 2 fold MICs values in chicken
meat stored under microaerobic conditions: (◊) control; () S. montana; (▲) P. lentiscus; (■) I. graveolens; (●) L. nobilis. The error
bars represent standard deviation (Djenane et al., 2011d).
Coriander EO was tested in vitro for antimicrobial activities against Campylobacter jejuni using disk diffusion and
minimal inhibitory concentration determination assays. It was found that the oil at concentration of 0.5% v/w killed all
of the bacteria on the meat, while 0.1% and 0.25% v/w oils reduced the bacterial cell loads on the meat from 5 log
cfu/ml to 3 and 1 log CFU/ml respectively (Rattanachaikunsopon and Phumkhachorn, 2010). Antimicrobial activities of
the EOs of various herbs were investigated by Abdollah et al. (2010) against C. jejuni and C. coli isolated from chicken
meat. The results indicated that the EOs of these plants exerted remarkable activity against C. jejuni and C. coli and,
therefore, they could be used as natural anti-Campylobacter additives in meat. Several recent studies described in detail
the antimicrobial properties of some EOs against C. jejuni, which may be envisaged as natural alternatives to chemicalbased antibacterial for food safety and preservation (Nannapaneni et al., 2009; Djenane et al., 2011d). Despite the
potential of many common plants and EOs is considerable, knowledge of this area and studies on their biological
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activities remain scarce. Most of the data published on the antimicrobial properties of plant EOs are fragmented and
employ only basic screening techniques. Moreover, most studies on the antimicrobial action of plant extracts have been
conducted in vitro, so that little information exists regarding the antimicrobial activity of EOs in food systems (Burt,
2004). Tested EOs showed promising antibacterial activity against target bacteria. Djenane et al. (2011d) support the
possible use of Inula graveolens, Laurus nobilis, Pistacia lentiscus and Satureja montana EOs, particularly that from I.
graveolens, for the preservation of chicken meat. By using this method, chicken meat can be stored in a modified
atmosphere assuring a low risk associated to Campylobacter, at the same time that lipid oxidation is inhibited, giving
rise to a higher sensory quality. The ability of I. graveolens to inhibit C. jejuni, which are gram-negative bacteria,
makes it more interesting for use to prevent food-related illness caused by C. jejuni and other gram-negative bacteria.
Aslim and Yucel (2008) found that the EO obtained from Origanum minutiflorum showed strong antimicrobial activity
against all of the tested ciprofloxacin-resistance Campylobacter spp. The same suggest that the essential oil of O.
minutiflorum may be used as a natural preservative in food against food-born campylobacteriosis. Many studies have
demonstrated that higher concentrations of EOs are required in food systems than in in vitro investigations (Djenane et
al., 2011a).The use of EO vapours may be a potential way of combating the organoleptic effect brought about by direct
contact between the food and EO. However, longer exposure to the vapour is required to produce a similar inhibitory
effect (18 h as against 60 s) which has cost implications for the food industry (Fisher and Philips, 2006).
Wine. Isohanni et al. (2010) suggest that wines could be used as antimicrobial ingredients together with the addition of
further antimicrobial agents in meat marinades to reduce the numbers of Campylobacter in naturally contaminated
poultry products, thus lowering the risk of Campylobacter cross-contamination and transmission through food.
According to Gañan et al. (2009), wine constitutes an adverse environment for the survival of C. jejuni. Furthermore, it
would be interesting to study the possible use of phenolic compounds in wine as an alternative to the use of
antimicrobial growth promoters against these bacteria in broilers.
Nonthermal methods. In recent years, there has been increased research interest in the use of nonthermal alternative
methods for microbial inactivation, such as, high hydrostatic pressure or pulsed electric fields. The attraction of these
technologies lies in the production of microbiologically safe foods with minimal changes in their sensory and nutritional
attributes. Sagarzazu et al. (2010) shown that incubation of heat-treated cells in the presence of sodium pyruvate highly
improved the survival ability of C. jejuni; on the contrary, it did not enhance survival ability of this microorganism after
exposure to pulsed electric fields treatments.
Active packaging. Interest in the use of active packaging systems for meat and meat products has increased in recent
years (Kerry et al., 2006). Changes in consumer preferences have led to innovations and developments in new
packaging technologies. Active packaging is useful for extending the shelf life of fresh, cooked and other meat
products. Forms of active packaging relevant to muscle foods include; O2 scavengers, CO2 scavengers and emitters, drip
absorbent sheets, antioxidant and antimicrobial packaging (Camo et al., 2011). Recently, Sánchez-González et al.
(2011) found that antimicrobial films were prepared by incorporating different concentrations of various EOs, into
chitosan and hydroxypropylmethylcellulose films. Their antibacterial effectiveness against pathogens bacteria was
studied at 10 °C during a storage period of 12 days. Hydroxypropylmethylcellulose-EO and chitosan-EO composite
films present a significant antimicrobial activity against the pathogens considered.
Combined methods. Study of Smigic et al. (2010) highlighted the importance of combining decontamination
technologies with subsequent storage under O2-rich atmosphere, at low pH and low temperature to the control survival
and growth of C. jejuni. The combination of heat and acid pH was one of the first combined processes used by the food
industry, with the objective of reducing the intensity of heat treatments. This practise has the advantage of decreasing
heat resistance of C. jejuni, but also of preventing the growth of survivors (Palop et al., 1999). Gálvez et al. (2010)
found that Application of natural antimicrobial substances (such as bacteriocins) combined with novel technologies
provides new opportunities for the control of pathogenic bacteria, improving food safety and quality. Bacteriocinactivated films and/or in combination with food processing technologies (high-hydrostatic pressure, high-pressure
homogenization, in-package pasteurization, food irradiation, pulsed electric fields, or pulsed light) may increase
microbial inactivation and avoid food cross-contamination. Piskernik et al. (2011) found the synergistic effect of
freezing and rosemary extract antimicrobial activity. As the combination of pre-freezing and plant extract treatment
reduced the C. jejuni cell number by more than 2.0 log reduction.
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