Occurrence and prevalence of intestinal protozoan parasites in male

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Occurrence and prevalence of intestinal protozoan parasites in male
47
Occurrence and prevalence of intestinal protozoan
parasites in male and female Libyan nationals residing
in Benghazi, Libya.
EI-Ammari, N. E. & Nair, G.A.
Department of Zoology. Faculty of Science. University of Garyounis. Benghazi, LIBYA
Received: 01.07.02
Accepted: 10.12.03
Abstract: Examination of the stool of 1452 Libyan nationals (852 men and 606 women) residing in Benghazi, Libya, during
September, 1998- August, 1999, revealed that 18.3% men and 14.2 % women had the cysts andl or trophozoites of seven intestinal
protozoan parasites in them . These were the pathogenic Entamoeba histolytiea, Giardia lamblia and the non- pathogenie
Entamoeba dispar, Entamoeba eoli, Endolimax nana, Chilomastix mesnili and Blastoeystis hominis. Higher overall and group-wise
percentages of both sex had the cysts of E. histolytiea/ E. dispar, followed by the cysts and/or trophozoites of G lamblia in their
stoo1s. Nearly 50% ofthe positive cases ofboth men and women had single infection of E. histolytiea/ E. dispar. Regarding mixed
infection, 11.6% men and 12% women contained the cysts of E. histolytiea/ E. dispar + E. eoli in their stools. Prevalence of the
cysts of E. histolytiea/ E. dispar reached its peak in 21-30, and the cysts and/or trophozoites of G lamblia in 5-10 age groups with
a de crease thereafter. Significant difference existed (F= 4.99; p< 0.005) in the parasitic infections between different age groups.
Keywords: Intestinal protozoa, cysts, trophozoites, age-sex distribution, human, Libya.
Resumen: El examen coprológico de 1452 personas de nacionalidad Libia (852 hombres y 606 mujeres) residentes en Benghazi,
Libia, desde Septiembre de 1998 a Agosto de 1999, reveló que el 18.3% de los hombres y el 14.2 % de las mujeres tenían quistes
y/o trofozoitos de siete protozoos intestinales. Estos fueron los patógenos Entamoeba histolytiea, Giardia lamblia, y los no
patógenos Entamoeba dispar, Entamoeba eoli, Endolimax nana, Chilomastix mesnili y Blastoeystis hominis. En ambos sexos el
hallazgo más frecuente fue la presencia de quistes de E. histolytiea/ E. dispar, seguido de la presencia de quistes y/o trofozoitos de
G lamblia en sus heces. En ambos sexos cerca del 50% de los casos positivos padecían una infección simple de E. histolytiea/ E.
dispar. En cuanto a las infecciones mixtas, el 11.6% de los hombres y 12% de las mujeres tenían quistes de E. histolytiea/ E. dispar
+ E. eoli en sus heces. La prevalencia de quistes de E. histolytiea/ E. dispar alcanzó un máximo en el grupo de edad de 21-30 años,
y los quistes y/o trofozoitos de G lamblia en el grupo de 5-10 años, con un descenso posterior, siendo las diferencias entre grupos
de edad estadísticamente significativas (F= 4.99; p< 0.005).
Palabras clave: protozoos intestinales, quistes, trofozoitos, edad, sexo, humanos, Libia.
1. Introduction
Increased awareness emerged that parasites
were becoming a problem and were responsible for
infection, infestation and diseases and effective
means of healing infected persons became a priority
(Zeilbig, 1997). Even though treatment, prevention
and control measures are available, parasitic
infections still occur worldwide, and increased
population density, poor sanitation, marginal water
Corresponding author:
Prof. Dr. G. A. Nair
Oepartment of Zoology. Faculty of Science. University of Garyounis
Post Box: 9480 Benghazi. UBYA
e-mail: [email protected]; [email protected]
Revista Ibérica de Parasitología (2003),63 (3-4), 47-54
resources and environmental change account for the
prevalence of parasites (WHO, 1987). In a rapidly
developing country like Libya, the epidemiological
parterns of parasitic diseases are further complicated
by the arrival of large numbers of migrant workers
leading to destabilizing effects on the normal pattern
of disease transmissions. The present study conducted
during the period September, 1998 - August, 1999,
investigated the occurrence and prevalence of
intestinal protozoan parasites among the randomly
selected men and women Libyan nationals residing in
Benghazi, Libya. Earlier studies on the subject were
confined on the school children of Benghazi, (Dar et
al. , 1979; EI-Boulaqi et al., 1980; EI-Buni and Khan,
© 2003 Sociedad Española de Parasitología (SEP)
48
El-Ammari, N. E. & Nair, G.A., Intestinal protozoan parasites in Libyans.
1998) and the present investigation is the first of its
kind undertaken on different age-groups of male and
females Libyan nationals. The objectives ofthe study
were to find out 1) the occurrence ofthe cysts and/or
trophozoites of different species of intestinal
protozoan parasites in the stools of men and women
Libyans, 2) the total , overall and group-wise
percentages of both sex having the cysts and/or
trophozoites of intestinal protozoan parasites, and 3)
the percentages of positive cases and of different age
groups having single or mixed parasite infections.
The study gives an insight on the intestinal protozoan
parasitic prevalence in these nationals and the
importance of taking preventive and precautionary
measures to control them.
2. Materials and Methods
2. 1 Number of Libyan nationals examined
The stools of 1458 Libyan nationals
permanently settled in Benghazi, Libya, were
examined during September, 1998 - August 1999, for
the cysts and/or trophozoites of intestinal protozoan
parasites in them. Out ofthese, 852 were men and 606
were women, and they belonged to different ages
from 5 to 60 years. The stools of these people were
procured from the Central Medical Laboratory,
Benghazi, and they gave their stools as part of routine
check-ups, and thus cannot be considered as sick
persons. The stools of referred sick cases from
different health centers of Benghazi to the Central
Medical Laboratory, were not included in the study.
2.2 Parasitological examination.
Fresh stools (color: brown, blackish brown,
black, green or yellow) were collected thrice a week
in clean, numbered plastic containers. Personal details
including name, age and sex were recorded for each
sample. The consistency of the sample was checked,
and observations were made on the presence of
mucus or blood in the stools. They were later
homogeneously mixed and directly examined, on the
same day of collection, for cysts and/or trophozoites
ofprotozoan parasites employing the techniques of 1)
direct smear examination by the use of both normal
saline solution, and Lugol's iodine solution (Markell
et al., 1999), and 2) Zinc sulphate centrifuged
floatation technique (Zeilbig, 1997).
The cysts and/or trophozoites of protozoans
found in the stools were identified using the keys and
description given by Neva and Brown (1994). The
lengths and widths of the same were measured with
the aid of a calibrated ocular micrometer microscope.
2.3 Analysis of the data
Stools without any cysts and/or trophozoites of
protozoan parasites were categorized as negative, and
those that contained the same, as positive. The
positive cases were further sub-divided into a) single,
or b) mixed prevalence, depending on the number of
cysts and/or trophozoites of these parasites and their
combinations, present in the stools.
The data were subjected to relevant statistical
analysis (Grimm, 1993).
3. Results
3.1 Occurrence and identification of intestinal protozoan parasites
The stools of 242 mal e and female Libyan
nationals (16.6%), out ofthe total 1458 examined were
found to have the cysts andlor trophozoites of intestinal
protozoan parasites in them. Sex-wise examination of
the same revealed that 18.31 % males (156 out of the
total 852 males) and 14.19 % females (86 out ofthe
total 606 females) showed positive on the occurrence
of the cysts andlor trophozoites of these parasites in
their stools. The percentage of positive cases in males
was higher when compared with those of females.
However, normal tests comparing the proportions of
positive cases between male and female Libyan
nationals did not reveal any significant difference
between them (d=O.04; the critical value of d is ± 1.96;
sample value falls within the acceptance region).
The examination of stools of mal e and female
nationals showed the occurrence of seven intestinal
protozoan parasites in them. These were 1)
Entamoeba histolytica (cysts) 2) Entamoeba dispar
(cysts) 3) Giardia lamblia (cysts and lor trophozoites),
4) Entamoeba coZ¡ (cysts), 5) Endolimax nana (cysts),
49
EI-Ammari, N. E. & Nair, G.A., Intestinal protozoan parasites in Libyans.
6) Chilomastix mesnili (trophozoites), and 7)
Blastocystis hominis (cysts). Entamoeba histolytica is
pathogenic causing intestinal amebiasis, whereas
Entamoeba dispar is non-pathogenic. The cysts of the
former and the latter were clubbed together as
Entamoeba histolytica/ Entamoeba dispar in the
present study, since it was not possible to differentiate
morphologically the cysts of both these parasites.
Giardia lamblia was the other pathogenic protozoan
parasites causing intestinal giardiosis in human
beings. Regarding Blastocystis hominis, whether this
parasite is a pathogen or a commensal is still not clear.
All the remaining parasites were non-pathogenics.
3.2 Overall and group-wise percentages
Table 1 shows the overall and group-wise
percentages of male and female nationals having the
cysts and/or trophozoites of intestinal protozoan
parasites in their stools. Higher percentages (both overall
and group-wise) of men and women Libyan nationals
had the cysts of E. histolytica/ E. dispar in their stools
when compared with the occurrence of the cysts and/or
trophozoites of other parasites. This was followed by the
next higher percentages of both males and females
recording the cysts and/or trophozoites of the pathogenic
protozoan Giardia lamblia in their stools. Low to
moderate overall and group-wise percentages of men
and women recorded the cysts of E. coli, E. nana and B.
hominis in their stools. The trophozoites of C. mesnili
were detected in the stools of men only.
Parasites
Entamoeba histolytica
/ E. dispar
Giardia lamblia
Entamoeba coli
Endolimax nana
Chilomastix mesnili
Blastocystis hominis
Overall percentage in
Male Female
6.17
2.1 3
1.30
0.62
0.14
0.34
3.16
1.30
0.89
0.41
0.00
0.14
Group-wise percentage in
Male
Female
10.56
3.64
2.23
1.06
0.24
0.59
7.59
3.14
2.15
0.99
0.00
0.33
Table 1. Overall (n=1458) and group-wise (male; n=852; female:
n=606) Percentages of male and female Libyan nationals having
the cysts and/or trophozoites of intestinal protozoan parasites in
their stools.
A significant different did not exist m the
overall (F= 0.67; p> 0.05) and group-wise (F=0.12;
p> 0.05) percentages of men and women Libyan
nationals having the cysts and/or trophozoites ofthese
parasites in their stools.
3.3 Single or mixed parasitic infection
The percentages of positive cases of mal e and
female Libyan nationals having the single or mixed
infections, as was evident from the occurrence of
cysts and/or trophozoites of intestinal protozoan
parasites in their stools, are presented in Table 2.
Regarding single infection, nearly 50% of the
positive cases of both sexes had the cysts of E.
histolytica/E. dispar in their stools, AIso, the stools of
19.38% males and 24% females were found to contain
the cysts and/or trophozoites of G lamblia. The cysts of
the non-pathogenic forms were found in comparatively
lower percentages of male and female Libyan nationals
and their ranges were limited between 1 to 6 % only.
Among the mixed infection, 11.63% males and
12.00% females contained the combination of the
cysts of E. histolytica/E. dispar + E. coli in their
stools. The stools of 4.65% males had the
combination ofthe cysts ofE. histolytica/E. dispar +
the cysts and/or trophozoites of G. lamblia. The
different other double combinations of these parasites
were found in comparatively lesser percentage of
males and females. The stools of a male contained the
combination of the cysts of 3 parasitic protozoans viz
Parasites
Percentages
Male
Female
Single infection
Entamoeba histolytica/ Entamoeba dispar
Giardia lamblia
Entamoeba coli
Endolimax nana
Chilomastix mesnili
Blastocystis hominis
49.61
19.38
2.33
5.42
1.55
1.55
48.00
24.00
5.34
5.34
0.00
1.33
Mixed infectioll
E. histolytica/ E. dispar + E. coli
E. histolylica/ E. dispar + G lamblia
E. histolytica/ E. dispar + E. nana
G lamblia + E. nana
E. coli + E. nana
E. histolytica/ E. dispar + B. hominis
E. histolytica/ E. dispar + B. hominis + E. coli
11.63
4.65
1.55
0.00
0.00
1.55
0.78
12.00
0.00
0.00
1.33
1.33
1.33
0.00
Table 2: Percentages of the positive cases of ma1e and female
Libyan nationals having the single or mixed infection of intestinal protozoan parasites.
50
El-Ammari, N. E. & Nair, G.A., Intestinal protozoan parasites in Libyans.
E. histolytica/E. dispar + E. coZ¡ + B. hominis.
A significant different existed (F= 4.59; p< 0.05)
between the single or mixed parasitic infection (Factor
A) among the male and female Libyan nationals,
whereas such a difference was not discernible in the
parasitic infection between males and females (Factor
B) (F=0.65; p>0.05) or on their interactions (Factors A
X B) (F= 0.21; p> 0.05) (Table 2).
3.4
Single or mixed parasitic infection in different age-groups
The percentages of positive cases of male and
female Libyan nationals in different age groups of 5-1 O,
11-20, 21-30,31-40,41-50, and 51-60 years, having the
cysts and/or trophozoites of single or mixed infections
of protozoan parasites in their stools are presented in
Table 3.
Regarding single infection, the cysts of E.
histolytica/E. dispar in the stools began to increase from
5 to 10 age group onwards reaching their peaks in 21 to
30 age group ofboth sex, with a slow decrease thereafter.
On the other hand, higher percentages of 5 to 10 year
males and females were found to contain the cysts and/or
trophozoites of G lamblia in their stools which showed
a declining trend as the age groups advanced. The cysts
and/or trophozoites of the non-pathogenic protozoan
parasites were mainly detected among the males and
females whose age-groups ranged from 11 to 30, with
the exception of E. nana, whose cysts were detected also
in the older age-groups of more than 51 years.
An almost uniform occurrence of the
combination ofthe cysts ofE. histolytica/E. dispar +
E. coZ¡ were discernible among all age-groups of mal e
and female Libyan nationals, whereas the occurrence
of different other combinations of the cysts and/or
trophozoites of protozoan parasites were patchy
among the males and females belonging to different
age-groups.
A significant difference existed in the parasitic
infection between different age-groups of mal e and
female Libyan nationals combined together (Factor
A) (F= 4.99; p> 0.05). Such a difference, however,
was not evident between the single or mixed parasitic
infection among the different age-group (Factor B)
(F= 1.89; p>0.05) or on their interactions (Factors A X
B) (F= 0.58 ; p>0.05).
Table 3: Percentages of the positive cases of different age-groups of male and female Libyan nationals having the single or mixed
infection of intestinal protozoan parasites
Age groups
Parasites
OS-ocl
nov-20
M
F
Enlamoeba histolytica/ E. dispar
3.43
Giardia lamblia
4.90
Entamoeba coli
21-30
31-40
F
41-50
51-60
M
F
M
2.45
4.41
2.45
10JO
6J8
5.40
4.90
5.89 0.98
1.996 0.49
2.94
4.43
1.96
3.43
2.45
0.49
0.49
0.00 0.49
0.00
0.49
0.00
0.49
0.49
0.49
0.49
0.98
0.49
0.00
0.00 0.00
0.00
0.00
Endolimax nana
0.00
0.00
0.00
0.00
0.98
1.47
1.47
0.00
0.00 0.00
0.98
0.49
Chilomastix mesnili
Blastocystis hominis
0.00
0.00
0.49
0.00
0.00
0.00
0.00
0.00
0.49 0.00
0.00
0.00
0.00
0.00
0.49
0.00
0.49
0.49
0.00
0.00
0.00 0.00
0.00
0.00
E. histolytica/ E. dispar +E. coli
0.98
0.98
0.98
0.49
0.98
2.45
1.47
0.49
1.96 0.00
0.98
0.00
M
F
M
F
M
F
Single infeelion
Mixed infeelion
E. histolytica/ E. dispar + G lamblia
0.49
0.00
0.49
0.00
1.47
0.00
0.00
0.00
0.00 0.00
0.49
0.00
E. histolytica/ E. dispar +E. nana
0.00
0.00
0.98
0.00
0.00
0.00
0.00
0.00
0.00 0.00
0.00
0.00
G lamblia +E. nana
0.00
0.49
0.00
0.00
0.00
0.00
0.00
0.00
0.00 0.00
0.00
0.00
E. coli +E. nana
E. histolytica/ E. dispar +B. hominis
0.00
0.49
0.00
0.00
0.00
0.00
0.00
0.00
0.00 0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.49
0.49
0.00
0.00
0.49 0.00
0.00
0.00
E. histolytica/ E. dispar +B. hominis +E. colí
0.49
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00 0.00
0.00
0.00
EI-Ammari, N. E. & Nair, G.A., Intestinal protozoan parasites in Libyans.
4. Discussion
Examination of the stools of male and female
Libyan nationals residing in Benghazi, Libya,
revealed the presence of seven protozoan parasites,
out of which two (E. histolytiealE. dispar and G
lamblia) were pathogenic and the remaining five were
either commensals or non-pathogenics. The
percentages of males found infected with these
parasites were higher when compared with the same
of females, even though the difference was found to
be insignificant. AIso, higher overall and group-wise
percentages of male and female Libyan nationals had
the cysts and/or trophozoites of E. histolytiealE.
dispar and G lamblia in their stools when compared
with the occurrence of other parasites. Moderate
percentage of mal e Libyans had the combination of
the cysts of E. histolytiealE. dispar + the cysts and/or
trophozoites of G lamblia in their stools. Specific
prevalence was quite different for the parasites E.
histolytiealE. dispar and G lamblia. For the former,
rates rose progressively with age to reach peak
prevalence in males and females of age-group 21 to
30, whereas in G lamblia infections peaked in
younger age groups of 5 to 10 in both sex and
progressively declined in adults, indicated that
effective immunity towards this parasitic might have
acquired.
Intestinal protozoans are the etiological agents
of several widespread parasitic diseases, the most
common of which are caused by Entamoeba
histolytica and G lamblia. E. histolytiea the causative
parasite of the disease amebiasis, can invade
intestinal mucosa and can spread to other organs as
well, mainly the liver. E. dispar, on the other hand,
colonizes the human gut with no invasive potential
(Clark, 1998). Amebiasis is a cosmopolitan infection
transmitted by the fecal- oral route, food and drink
and its greatest impact is in Africa and in Asia. In
Africa, Egypt, Morocco and countries located
between 10° N and 10° S are severely affected (WHO,
1981). This categorization includes Libya also.
Moderate to high prevalence of this parasite in
population residing sub-Saharan and Arabian
countries are also reported (Gatti et al., 1998; Shubair
et al., 2000).
51
The pathogenic G lamblia is worldwide
distribution, apparently more prevalent in children
than in adults, and more common in warm climates
than in cool ones (Meyer and Jarroll, 1980). Dar et al
(1979) reported high incidence of giardiosis among
the school children of Benghazi. These authors
observed that most children harboring this parasite
complained of abdominal pain and diarrhea, and that
infection rates in children from different school of
Benghazi are closely associated with the standards of
cleanliness of the schools and the socio-economic
status of the neighborhood.
Transmission of this parasite may be direct by
ingestion of feces or indirect through ingestion of
contaminated water or food (Neva and Brown, 1994).
G lamblia may cause acute 01' chronic diarrhea,
steatorrhoea, loose stools, malabsorption of fat
(Benenson, 1990), growth retardation and malnutrition
in children (Farthing et al., 1986) It is also a cause of
morbidity in adults (Farthing, 1993). With the advent
of AIDS, there was speculation that G lamblia may be
an important pathogen in this group, but clinical
findings to data do not seem to confirm this possibility
(Meyer, 1990). Giardiosis was also reported among
Jordanian (Morsy and EI-Maridi, 1978), Egyptian
(Hammouda et al., 1986) and PaJestinian (Shubair et
al., 2000) populations, but is less severe in sub-Saharan
African countries (Annan et al., 1986).
Regarding non-pathogenic intestinal protozoan
parasites, the stools of 10w to moderate percentages of
both male and female Libyan nationals contained the
cysts of E. eoli, E. nana and B. hominis and moderately
higher percentage of both sexes recorded the
combination of the cysts of E. eoli + E. histolytiea/ E.
dispar. E. eoli is a parasite of the large intestine and is
of medical importance only, because it may be mistaken
for E. histolytiea (Neva and Brown, 1994). Higher
prevalence of E. coZ¡ was reported earlier among the
school children in Benghazi (EI-Boulaqi et al., 1980)
and in the neighboring Egyptian (Hammouda et al.,
1986). The cysts of C. mesnili, another non-pathogenic
protozoan, were detected in the stools of male Libyans
only.
The most critical question concerning
Blastocystis hominis today is whether it is a pathogen
52
EI-Ammari, N. E. & Nair, G.A., Intestinal protozoan parasites in Libyans.
or a commensal. Garcia (2001) made a current
revision ofthe paper on Blastocystis and recognizes it
as a pathogen. This parasite is a common inhabitant of
the human bowel and is increasingly recognized as a
potential cause of diarrhea (Telalabasic et al., 1991).
The disease in humans caused by B. hominis has been
called Zierdt-Garavelli disease (Garavelli, 1992).
This was not approved by Borcham and Stenzel
(1993), who proposes that such a designation seems
premature until it is proved that B. hominis actually
causes the disease, and the term blastocystosis seems
more appropriate. However, the same authors
suggested that even if B. hominis proves to be
primarily a commensal, it can be pathogenic under
specific conditions such as immunosuppression, poor
nutrition or concurrent infections. There were also
reports (Henny et al., 1986; Garavell i and Seaglione,
1990; Vallano et al., 1991) that B. hominis may be an
opportunistic infection in immunosuppressed patients
with AIDS, but whether as a commensal or as a
pathogen remains to be determined.
The recogmtlOn of the non-pathogenic
intestinal parasites is generally accepted as an useful
epidemiological indication of the level of fecal
contamination (Hammouda et al., 1986). The nonpathogenic forms recorded in the present study are
cosmopolitan in distribution and are reported
harrnless (except perhaps B. hominis?) in humans
other than creating intestinal disturbances, if found in
large numbers.
In conclusion, a moderate to high prevalence of
E. histolytica/ E. dispar and G lamblia and their
combinations, and the low prevalence of B. hominis and
its combination with E. histolytica/E. dispar in male
and female Libyan nationals, are matters of concem,
suggesting the urgency and priority for implementing
the preventive and precautionary measures to check the
spreading of these and other parasites. These inc1ude
effective environmental sanitation to prevent water and
food contamination, proper sewage, adequate handling
and treatment of water supplies and food, and health
education. The gravity of the situation increases further
after recent findings that G lamblia and B. hominis are
important and opportunistic parasites related with
AIDS. Our studies (unpublished data) on the prevalence
of intestinal protozoan and helminth parasites among
the non-Libyan populations residing in Benghazi,
revealed the occurrence of many pathogenic forms in
them, which, if adequate precautions are not taken
immediately, can also be transmitted to the indigenous
populations, in due course of time.
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