A.T. Al-Saeed1 and S.H. Issa1
ABSTRACT Out of 1261 stool specimens collected from children in Dohuk city, northern Iraq, the prevalence of Giardia lamblia infection was 38.5%. The highest rate of infection was in orphan care centres (48.1%) and the lowest in the paediatric hospital (31.3%). The age group 10–12 years had the highest rate (81.2%) and 7–9 years the lowest (22.9%); boys had a higher rate than girls. Some infected samples (70/486) showed double or triple infections and G. lamblia was combined with Hymenolepis nana, Blastocystis hominis, Entamoeba histolytica and Iodamoeba buetschlii.
Fréquence de Giardia lamblia chez des enfants à Dohuk (Iraq septentrional)
RÉSUMÉ Dans les 1261 échantillons de selles prélevés chez des enfants de la ville de Dohuk (Iraq septentrional), la prévalence de l’infection à Giardia lamblia était de 38,5 %. Le taux d’infection le plus élevé se trouvait dans les centres d’accueil pour orphelins (48,1 %) et le plus faible à l’hôpital pédiatrique (31,3 %). Le groupe d’âge des 10-12 ans avait le taux le plus élevé (81,2 %) et celui des 7-9 ans le plus faible (22,9 %) ; le taux était plus élevé chez les garçons que chez les filles. Certains échantillons infectés (70/486) présentaient une double ou une triple infection et G. lamblia était associé à Hymenolepis nana, Blastocystis hominis, Entamoeba histolytica et Iodamoeba buetschlii.
1Department of Microbiology, College of Medicine, University of Dohuk, Dohuk, Iraq (Correspondence to A.T. Al-Saeed:
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Received: 13/04/03; accepted: 24/08/04
EMHJ, 2006, 12(5): 555-561
Introduction
Giardia lamblia is a protozoan parasite which has worldwide distribution and is common in warm and moist climates throughout the world. Giardiasis is an important unresolved health problem in developing countries, as it is related to poor sanitation and management of supplied water, a problem that is exacerbated by the absence of a simple reliable diagnostic test [1]. The prevalence of G. lamblia ranges from 2%–7% in industrialized countries and 20%–60% in developing countries [2]. The majority of infections are probably asymptomatic but some are associated with subacute or chronic diarrhoea and intestinal irritation [3], which contribute to malabsorption and nutritional deficiency especially in children [4,5].
Giardiasis is transmitted by the faecal–oral route and direct person-to-person spread. In most cases it is associated with contaminated drinking water but also occasionally by recreational activity in still water [6,7]. G. lamblia is more common in children but all age groups are affected in epidemic areas [8]. Infants under 1 year old are less likely to be infected than the older children [9]. It is particularly common in children’s institutions such as day care centres, primary schools and big families [10,11].
Several surveys of intestinal parasitosis in Iraq have shown a high incidence of giardiasis among children [12,13]. The present study was conducted because little information is available about G. lamblia infection among children in northern Iraq.
The aim of this study in Dohuk city was directed to determine the frequency of G. lamblia in different age groups of children, the incidence of G. lamblia throughout the year and the association of G. lamblia with other intestinal parasites.
Methods
This study was conducted from 1 October 2001 to 31 July 2002 on children living in Dohuk city.
Sample
Stool samples were collected from boys and girls aged 3 months to 12 years attending day care centres, kindergartens, primary schools and the local paediatric hospital. With the assistance of the children’s parents and supervisors of centres, a fresh stool specimen was collected from each child into a disposable plastic container. The stool samples were taken immediately to the laboratory of the Microbiology Department at the University of Dohuk College of Medicine for examination. Those with negative results had 2 other samples taken at different times for examination.
Laboratory methods
The stool samples were examined with the naked eye for colour, consistency and the presence of any adult helminths. They were then examined microscopically by direct and concentration methods for presence of Giardia trophozoite and cyst stages and for detection of other parasites stages. The concentration method used in this study was the zinc sulphate floatation method [14].Two types of direct wet film preparation were done for each sample at the same time, 1 slide by using normal saline 0.85% for detecting the motility of trophozoites and Lugol’s iodine 5% slide for demonstrating structures [14].
Data about age, sex and residence were recorded for each child on a special form, together with the stool examination results (type of stool, direct and concentration test results), stage of Giardia lamblia and associated parasites.
The results were analysed statistically using the F-test.
Results
A total of 1261 stool samples were collected and examined: 833 samples were from children in schools and care centres (451 attending primary schools, 261 attending kindergartens, 94 day attending care centres and 27 attending orphan care centres) and 428 samples were from children presenting at the paediatric hospital with a complaint of gastroenteritis.
The total infection rate with G. lamblia among the examined samples was 38.5% (standard error range 38.49%–38.51%).
The distribution of G. lamblia according to the children’s institute and schools is summarized in Table 1. The highest rates of giardiasis were from the orphan care centres (48.1%) and kindergartens (45.6%), whereas the rates were lower in the primary schools, day care centres and the paediatric hospital) (41.2%, 36.2% and 31.3% respectively). The statistical analysis revealed a highly significant difference in infection rate between primary schools and other children’s institutes (P < 0.01).
The rate of infection varied across different age groups of children (Table 2). The age group 10–12 years showed the highest rate of infection (81.1%), and the lowest rate was in children 7–9 years (22.9%). There was a highly significant difference among different age groups (P < 0.01). The infection rate was higher among boys (41.6%) than girls (35.6%).
The distribution of G. lamblia according to the months of the year is shown in Table 3. Although more samples were collected in the summer months, the rate of G. lamblia infection as a proportion of the number of stools examined was lowest in June (28.4%). Fewer sample were collected in the colder months but the highest infection rate of samples was in December (49.2%) followed by November (44.8%), April (43.5%) and May (43.4%). The difference in the rates of infection during the months was significant (P < 0.05).
Overall, 70 out of 486 infected samples showed double and triple infections with other intestinal parasites combined with G. lamblia (Table 4). G. lamblia was combined with Hymenolepis nana (46.4%), with Blastocystis hominis (39.4%) and each of Entamoeba histolytica and Iodamoeba buetschlii (7.1%). These results indicated that the infection with G. lamblia was usually more associated with the intestinal cestode H. nana. As triple infections, G. lamblia was combined with H. nana and B. hominis in 61.9% of samples, and combined with H. nana and Ent. coli in 38.1%.
Discussion
The infection rate with G. lamblia in stool samples from children in Dohuk city was very high (38.5%). The narrow standard error range in the samples is due to the large number of samples analysed.
The rate of infection in the present study is similar to other studies in Iraq [12,15–17]. The results are also in agreement with studies in other parts of the world [4,18,19]. This high rate of infection among children could be related to a number of factors such as poor health hygiene and toilet training, overcrowding, low education of children, low socioeconomic status and climatic conditions [20]. Giardia lamblia was isolated from stool samples of children in all primary schools but the highest rate of infection was reported from children in a primary school which is located in a low socioeconomic area (Serheldan region).
Another important factor which affects the rate of giardiasis is the presence of asymptomatic patients in the community who can be considered as the main source of infection through continuously excreting the cysts stages with their stools [21]. Most of the cases in this study were infected with cysts. Regarding the life-cycle of these parasites, those carrier patients act as a source of infection by continuously excreting the cyst stage with their stool [22]. Although carrier persons are asymptomatic, the infection may be converted to acute infection through excystation of cysts inside the intestine resulting in the main complaints of giardiasis such as abdominal pain, steatorrhoea and loss of weight [23].
The higher rate of infection with G. lamblia among children in orphan care centres, kindergartens and primary schools might be related to bad personal hygiene or overcrowding. On the other hand, the lower rate of infection among children in day care centres and the hospital might be an indication of good care taken by the supervisors of these centres [24].
Regarding the results of G. lamblia infection among different age groups, the < 1 year old group had a low rate of infection, perhaps because parents are responsible for their hygiene [25]. The infection rate was highest in the age group 10–12 years. This may be because this group of children are fully independent in toilet use and are more involved in outdoor activities which might lead to Giardia transmission [26]. The present results are similar to studies of intestinal parasitosis in Saudi Arabia and Senegal [27,28].
Higher numbers of samples were collected during the summer months when the maximum temperature in Dohuk is about 40–45 ºC. Cold weather kills the infective cysts [29,30]. The unfavourable temperature of G. lamblia cyst is less than 5 ºC and the cysts usually die at more than 62 ºC [31]. In Dohuk city the temperature in winter is 0 ºC or less to 5 ºC [32]. Other behavioural factors could be involved, for example there is greater consumption of drinks and food, e.g. ice cream, in summer which may be sources of infection [33].
The present study revealed that the intestinal cestode H. nana was the most common intestinal parasite associated with G. lamblia infection. Although other studies have demonstrated the same results [34], there was no clear reason for this association. However, it may be related to the infective stage of both parasites being resistant to various environmental conditions and remaining viable for a long time [35]. The other important pathogenic intestinal parasites recorded were B. hominis and Ent. histolytica.
References
- Addiss DG et al. Evaluation of a commercially available enzyme-linked immunosorbent assay for Giardia lamblia antigen in stool. Journal of clinical microbiology, 1991, 29(6):1137–42.
- Thompson RCA et al. Genetic variation in Giardia, Kunstler 1882: taxonomic and epidemiological significance. Protozoology abstracts, 1990, 14:1–28.
- Reitmeyer M, Robertson S. Giardiasis. Chief Medical Resident’s Clinical Medicine Conferences 1996–97. Charlottesville, Virginia, University of Virginia, 1997.
- Brown HW, Neva FA. Basic clinical parasitology, 5th ed. Appleton Century Croft, New York, 1983:43–6.
- Dubey R et al. Intestinal giardiasis: an unusual cause for hypoproteinemia. Indian journal of gastroenterology, 2000, 19(1):365–73.
- Gillin FD, Reiner DS. Cell biology of the primitive eukaryote Giardia lamblia. Annual review of microbiology, 1996, 50:679–705.
- Thompson RCA. The future impact of societal and cultural factors on parasitic disease—some emerging issues. International journal for parasitology, 2001, 31:949–59.
- Norhayati M et al. Prevalence and risk factors of Giardia duodenalis infection in a rural community. Southeast Asian journal of tropical medicine and public health, 1998, 29(4):735–8.
- Thompson RCA. Giardia as a re-emerging infection disease and its zoonotic potential. International journal for parasitology, 2000, 30:1259–67.
- Yaeger GR. Protozoa: structure, classification, growth and development. In: Baron S, ed. Medical microbiology, 4th ed. Galveston, Texas, University of Texas Medical Branch, 1996.
- Beaver PC, Jung RC, eds. Animal agent and vectors of human diseases, 5th ed. Philadelphia, Leaf and Febiger, 1985:13–4.
- Al-Dabagh MA et al. Giardiasis in a group of preschool age children in Iraq. Journal of the Faculty of Medicine Baghdad, 1967, 9:73–83.
- Al-Jeboori T, Shafiq MA. Intestinal parasites in Baghdad: a survey in two districts. Journal of the Faculty of Medicine Baghdad, 1976, 18:161–70.
- Cheesbrough M, ed. District laboratory practice in tropical countries. Part 1. Cambridge, Cambridge University Press, 1998:192–205.
- Mahdi NK, Jassim AH. Intestinal parasitic infections of primary school children in three regions of southern Iraq. Medical journal of Basra University, 1987, 6:55–61.
- Al-Rahaley IMK. Some aspects of enteropathogenic Escherichia coli from diarrheic children in hospitals and normal children in nurseries [MSc thesis]. Mosul, Iraq, University of Mosul, 1988.
- Molan AL, Farag AM. Prevalence of intestinal parasites in school children of Erbil, Northern Iraq. Saudi medical journal, 1989, 10:107–10.
- Gharbi T et al. Etude de l’anémie au cours de la giardiase chez des enfants Tunisiens d’âge préscolaire [Study of anemia in giardiasis intestinalis in Tunisian preschool children]. La Tunisie medicale, 1999, 77(11):558–61.
- Boia MN et al. Cross sectional study of intestinal parasites and chaga’s disease in the municipality of Nova Airao, State of Amazonaz, Brazil. Cadernos de saúde pública, 1999, 15(3):497–504.
- Hellard ME et al. Prevalence of enteric pathogens among community based asymptomatic individuals. Journal of gastroenterology and hepatology, 2000, 15(3):290–3.
- Al-Sa’eed ATM, Saeed AY, Mohammed JB. Prevalence of gastrointestinal parasites among the population in Dohuk–Kurdistan region Iraq. Zanco—journal for medical sciences (special issue), 2001, 5:14–9.
- Swadi AA. Epidemiological study on giardiasis in dogs in Baghdad province [MSc Thesis]. Baghdad, Iraq, Veterinary Medicine College University of Baghdad, 2000.
- Farag AM. Intestinal infection with Entamoeba histolytica and Giardia lamblia regular patients to Yafrin general hospital, Libya. Journal of Dohuk University, 1999, 2(2):407–13.
- Markell EK, John DT, Krotoski WA, eds. Markell and Voge’s medical parasitology, 8th ed. Philadelphia, Saunders, 1999, 55–62.
- Yassin MM et al. Prevalence of intestinal parasites among school children in Gaza City, Gaza strip. Journal of the Egyptian Society of Parasitology, 1999, 29(2):365–73.
- Mercado R, Otto JP, Perez M. Variacion estacional de las infecciones por protozoos intestinales en pacientes ambulatorios del sector norte de Santiago, Chile, 1995-1996 [Seasonal variation of intestinal protozoa infection in outpatients of the north section of Santiago, Chile, 1995–1996]. Boletin chileno de parasitologia, 1999, 54(1–2):41–4.
- Bolbol AH, Mahmoud AA. Laboratory and clinical study of intestinal pathogenic parasites among the Riyadh population. Saudi medical journal, 1984, 5:159–66.
- Dieng Y et al. Les parasitoses intestinales chez des habitants d’une zone peri-urbaine a nappe phreatique polluee par les nitrates d’origine fecale (Yeumbeul, Senegal) [Intestinal parasitosis in the inhabitants of a suburban zone in which the groundwater is polluted by nitrates of fecal origin (Yeumbeul, Senegal)]. Sante, 1999, 9(6):351–6.
- Belding DL. Textbook of parasitology, 3rd ed. New York, Appleton Century Crofts, 1965:123–6.
- Faust EC, Beaver PC, Jung RC, eds. Animal agents and vectors of human disease, 4th ed. Philadelphia, Lea and Febiger, 1978:25–7.
- Meyer EA, Radulescu S. Giardia and giardiasis. Advances in parasitology, 1979, 17:1–47.
- Agro-Meteorological Sub-Sector. Monthly bulletins (October 2001–July 2002). Duhok, Food and Agriculture Organization Coordination Office for Northern Iraq, 2001/2.
- Al-Barzanjy RKA. Epidemiological study of Giardia spp. in Erbil Governorate [MSc thesis]. Erbil, Iraq, College of Science, University of Salahaddin, 1992.
- Craun GF. Waterborne giardiasis in the United States: a review. American journal of public health, 1979, 69:817–9.
- Farthing MJ. Giardiasis as a disease. In: Thompson RCA, Reynoldson JA, Lymbery AJ, eds. Giardia: from molecules to disease and beyond. Wallingford, CAB International, 1994:15–57.