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: gachuthannair@yahoo.com; gachu@wmcmail.com

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),

EI-Ammari, N. E. & Nair, G.A., Intestinal protozoan parasites in Libyans. 49

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.

Overall percentage in Group-wise percentage in Parasites Male Female Male Female

Entamoeba histolytica / E. dispar 6.17 3.16 10.56 7.59 Giardia lamblia 2.1 3 1.30 3.64 3.14 Entamoeba coli 1.30 0.89 2.23 2.15 Endolimax nana 0.62 0.41 1.06 0.99 Chilomastix mesnili 0.14 0.00 0.24 0.00 Blastocystis hominis 0.34 0.14 0.59 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

Percentages Parasites Male Female

Single infection Entamoeba histolytica/ Entamoeba dispar 49.61 48.00 Giardia lamblia 19.38 24.00 Entamoeba coli 2.33 5.34 Endolimax nana 5.42 5.34 Chilomastix mesnili 1.55 0.00 Blastocystis hominis 1.55 1.33

Mixed infectioll E. histolytica/ E. dispar + E. coli 11.63 12.00 E. histolylica/ E. dispar + G lamblia 4.65 0.00 E. histolytica/ E. dispar + E. nana 1.55 0.00 G lamblia + E. nana 0.00 1.33 E. coli + E. nana 0.00 1.33 E. histolytica/ E. dispar + B. hominis 1.55 1.33 E. histolytica/ E. dispar + B. hominis + E. coli 0.78 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 diffe-rent 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 21-30 31-40 41-50 51-60

M F M F M F M F M F M F

Single infeelion

Enlamoeba histolytica/ E. dispar 3.43 2.45 4.41 2.45 10JO 6J8 5.40 4.90 5.89 0.98 1.996 0.49

Giardia lamblia 4.90 2.94 4.43 1.96 3.43 2.45 0.49 0.49 0.00 0.49 0.00 0.49

Entamoeba coli 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 0.00 0.00 0.49 0.00 0.00 0.00 0.00 0.00 0.49 0.00 0.00 0.00

Blastocystis hominis 0.00 0.00 0.49 0.00 0.49 0.49 0.00 0.00 0.00 0.00 0.00 0.00

Mixed infeelion

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

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 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. histolytica/ E. dispar + B. hominis 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. 51

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).

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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