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Table of Contents
Year : 2019  |  Volume : 10  |  Issue : 2  |  Page : 89-94

Prevalence of intestinal parasites and risk factors with emphasis on Enterobius vermicularis in children of daycares and preparatory schools of the city of Khodabandeh, Northwestern Iran

1 Department of Medical Parasitology and Mycology, School of Medicine, Qazvin University of Medical Sciences, Qazvin, Iran
2 Department of Social Medicine, Faculty of Medicine, Qazvin University of Medical Sciences, Qazvin, Iran
3 Department of Medical Parasitology and Mycology, School of Medicine; Cellular and Molecular Research Center, Qazvin University of Medical Sciences, Qazvin, Iran

Date of Submission16-Mar-2019
Date of Decision14-Apr-2019
Date of Acceptance16-Apr-2019
Date of Web Publication24-May-2019

Correspondence Address:
Dr. Mehrzad Saraei
Department of Medical Parasitology and Mycology, School of Medicine, Qazvin University of Medical Sciences, Qazvin
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/INJMS.INJMS_22_19

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Introduction: Intestinal parasitic infections (IPIs) are considered as a common cause of morbidity and mortality in children in the developing countries. The present study was aimed at examining the status of IPIs in the children of daycares and preparatory schools in the city of Khodabandeh located at Northwestern Iran. Materials and Methods: A total of 520 daycare and preprimary school-age children in the northwest of Iran were tested for the presence of intestinal parasites using direct smear and the standard formalin-ethyl acetate sedimentation techniques. Furthermore, the specific “scotch tape” test was used to identify the eggs of pinworm Enterobius vermicularis. Results: Of total 520 children, 55 cases (10.6%) were infected to intestinal parasites, including 9.2% monoparasitism and 1.4% double-parasitism. The prevalence rate for protozoan infections was 7.3% and 3.65% for helminths. Giardia lamblia infection was shown to have the highest prevalence rate among intestinal protozoa by 3.26%. The prevalence rate for E. vermicularis was 3.5% using “scotch tape” test and stool examination. There was a significant correlation between infection with intestinal parasites and daycares (P = 0.004). A significant inverse correlation was established between anal itching (as a sign of E. vermicularis infections) and hand-washing in children using soap or hand-washing liquid (P = 0.004). Conclusions: Infection with intestinal parasites in children of nursery schools and preschools of the study region, compared to the previous situation, is considerably decreased.

Keywords: Children, daycare, Iran, parasites, prevalence

How to cite this article:
Salahi K, Javadi A, Saraei M. Prevalence of intestinal parasites and risk factors with emphasis on Enterobius vermicularis in children of daycares and preparatory schools of the city of Khodabandeh, Northwestern Iran. Indian J Med Spec 2019;10:89-94

How to cite this URL:
Salahi K, Javadi A, Saraei M. Prevalence of intestinal parasites and risk factors with emphasis on Enterobius vermicularis in children of daycares and preparatory schools of the city of Khodabandeh, Northwestern Iran. Indian J Med Spec [serial online] 2019 [cited 2023 Feb 3];10:89-94. Available from: http://www.ijms.in/text.asp?2019/10/2/89/258984

  Introduction Top

Intestinal parasitic infections (IPIs) are considered as one of the common causes of morbidity and mortality in the developing countries. An estimate by the WHO indicates that approximately 1.5 billion of the world populations are infected with soil-transmitted helminths. The IPIs are mostly present in the tropical and subtropical regions, particularly within Sub-Saharan areas in Africa, Latin America, China, and East Asia. These regions have a climate quite susceptible for the transmission and further dissemination of intestinal parasites.[1]

Pathogenesis and clinical manifestations of the intestinal parasites depend on host's factors such as species of parasite, intensity of infection, nutritional condition, and immune system status. In general, mild infections are asymptomatic or with minor signs while heavy infections are with serious outcomes and even fatal. Disturbance in immune system function has no apparent effect on the degree of pathogenesis of some intestinal parasites; however, in case of parasites such as Strongyloides stercoralis, it could turn a mild asymptomatic infection into a severe and fatal infection.[2]

The clinical manifestations of IPIs are indeed nonspecific; however, some signs such as anal itching are to some extent pathognomonic for enterobiasis. Furthermore, iron deficiency anemia caused by hookworm infections, dysentery by amoebiasis, and malabsorption and steatorrhea by chronic giardiasis are among the most well-known complications produced by these parasites.

Although a considerable decrease in the prevalence rate of IPIs has occurred in some developing countries within the last decades, yet the high prevalence rate of such infections is still reported from a number of countries such as Peru,[3] south of Ethiopia,[4] Cambodia,[5] Burkina Faso,[6] Tajikistan,[7] and Nigeria.[8]

Iran is one of the developing countries located in Western Asia and the Middle East with different geographical climates. In the central regions with warm and dry climate, the prevalence of intestinal parasites is more limited, compared to the northern areas (the south of Caspian Sea) with a temperate climate and high humidity, which makes the region susceptible to the transmission of intestinal parasites. In the past up to four decades ago, infections with these parasites were considered as one of the most important public health challenges in the majority of regions in Iran, particularly those located in north, northwest, and west of the country as it was reported that at least 50% of the population, especially those living in villages, was infected with intestinal parasites.[9],[10],[11],[12],[13] In recent years, the prevalence rate of intestinal parasites has remarkably decreased in many regions of Iran; however, considering the population and the study area, significant differences may be observed; for instance, 3.73% of food handler in Tabriz,[14] 10.4% of food distributors in Shiraz,[15] 11.7% of individuals with immunodeficiency in Kashan and Qom,[16] and 32.7% of the residents of the city of Roudehen[17] (northeast of Tehran) were reported to be infected with these parasites.

School-age children and preprimary school kids are among the most important populations subject to the risk of IPIs. This group of children is more susceptible to acquire IPIs due to failure to follow the principles of personal hygiene while they are more sensitive and vulnerable to the occurrence of clinical signs and symptoms of parasitic diseases. Daryani et al. in their systematic review and meta-analysis reported that the prevalence rate of IPIs has largely reduced in preschool- and school-age children in some regions of Iran.[18] The present study was attempted to show, for the first time, the current state of IPIs in children of primary schools and kindergartens in the city of Khodabandeh, situated within Zanjan Province, Iran.

  Materials and Methods Top

Study area

The city of Khodabandeh is located in Zanjan Province which is among the northwestern provinces of Iran [Figure 1]. The land area of the city is up to 5151 km2 with a longitude and latitude of 48° 57'–47° 51' E and 35° 33'–36° 25' N, respectively. The city is a mountainous region with a temperate climate and based on the formal information published in 2015, with average maximum temperatures of 32.5° in July and 32.7° in August and average minimum temperatures of −5.3° in January and −5° in February. The average annual rainfall was 392.4 mm (maximum: 83.7 mm in April; minimum: 0 mm in August). In addition, the maximum weather humidity was reported to be around 71% in November and 72% in December with an average frosty days of 98 days/year and a total population of 52,572 in 2015.[19]
Figure 1: The study area. Khodabandeh is located in Zanjan Province of Northwestern Iran (http://www.miras-zanjan.ir)

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Study population

The individuals included in the study were the children of all day cares and preprimary schools (16 cases) of the city of Khodabandeh located in Zanjan Province (Iran) in 2016. The total number of children was 730, of whom 520 kids were included in the study.

Ethical considerations and data collection

This study was done in Compliance with Ethical Standard. Initially, the methodology and the ethical principles to be followed in the current study project were approved by the Ethical Committee of Research Department of Qazvin University of Medical Sciences (IR. QUMS.1395.125). Before sampling, coordination with all daycares and preprimary schools was made through a letter of introduction written by the Research Department of the university. To attract the agreement of parents, all parents were invited to attend in one of the nurseries at a fixed time. All necessary information regarding the different aspects of the research such as the objectives, sampling method, assay procedure, and free laboratory testing was fully explained. Later, the notice letters and agreement forms were delivered to all parents. A contact phone number to respond to parents' questions was also included in the notice letter. Data were recorded through an in-person interview with parents using a questionnaire. The data regarding the children were several items including age, gender, the number of family members, washing habit using hand-wash liquid or soap, nail biting or nail chewing, and finger sucking habits and clinical signs and symptoms, while the items considered for mothers were only profession and the education level.

Parasitological examinations

Primarily, all fecal specimens collected from the children were macroscopically examined for the presence of adult worms and Taenia saginata proglottid. Stool samples were tested by two methods; wet mount and formalin-ethyl acetate sedimentation concentration methods. Samples suspected of being positive for intestinal amoebas and flagellated protozoa by wet mount or formalin-ethyl acetate were permanently stained with trichrome solution and those suspected of having Cryptosporidium parasite were examined following Ziehl–Neelsen staining procedure. Furthermore, the specific “scotch tape” test was used to detect the infection caused by Enterobius vermicularis. All experiments were performed at Parasitology Department of Qazvin Medical School affiliated to Qazvin University of Medical Sciences, Qazvin, Iran. Those samples positive for intestinal parasites by at least one laboratory method were considered as positive.

Statistical analysis

Data were analyzed by SPSS version 19 (SPSS Inc, Chicago, Illinois, USA) using Chi-square test and Fischer's exact test to determine the possible correlation between IPI and associated risk factors. A P< 0.05 was considered statistically significant.

  Results Top

In general, of 520 children under the study, 55 cases (10.6%) were infected with intestinal parasites with 48 individuals (9.2%) infected only with one parasite (monoparasitism) and 7 persons (1.4%) with two parasites (double-parasitism). The prevalence rate for intestinal protozoa was 7.3% (38 cases) and for intestinal helminths was 3.65% (19 persons) with Giardia lamblia as the most common intestinal pathogenic protozoa with prevalence rate of 3.26% [Table 1]. There was no significant correlation between the infection caused by intestinal parasites and the study variables including age, gender, hand-washing habit using soap, raw vegetables consumption, the number of family, and mothers' education level, and occupation; however, a significant correlation was found when the results were compared between the daycares (P = 0.004) [Table 2]. The prevalence rate for E. vermicularis was 3.5%. Of 18 children infected by E. vermicularis, 16 cases were detected by “scotch tape” method alone, one by “scotch tape” test plus observation of adult worm on the surface of stool, and the last case only by observing the adult worm. Of those with enterobiasis, 72.2% had clinical symptoms with anal itching as the most common sign with a frequency of 61.1%. A significant inverse correlation between this parasitic infection and anal itching (P = 0.004) and hand-washing with soap (P = 0.022) was found. No significant correlation with other variables was demonstrated [Table 3].
Table 1: Prevalence of intestinal parasites in 520 children of day cares and preschools of the city of Khoda-bendeh in Zanjan province in northwest of Iran (2016)

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Table 2: Prevalence of intestinal parasites in 520 children of day cares and preschools of the city of Khoda-bendeh according to the demographic factors (2016)

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Table 3: Prevalence of infection with E. vermicularis in 520 children of day cares and preschools of the city of Khoda-bendeh according to the demographic factors (2016)

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  Discussion Top

In the present study, the prevalence of infection with intestinal parasites in the children of kindergartens and preprimary schools of the city of Khodabandeh showed a reduction, compared to the majority of studies reported from different parts of Iran within the last decade. This study showed that 10.6% of children were infected by intestinal parasites whereas others found higher prevalence rate for parasitic infection in the children of nurseries and primary schools of Iran including 16.3%,[20] 34.34%,[21] 22.2%,[22] 16.7%,[23] 12.9%,[24] 11.99%,[25] 28.5%,[26] and 15.5%.[27] These differences could be associated with a number of factors such as economic, social, and health care system conditions as well as the study populations. While the prevalence rate of intestinal parasites has significantly decreased in Iran, compared to the past years, yet it is still quite high in some developing countries such as Peru, 100%;[3] south of Ethiopia, 80%;[4] Cambodia, 56.2%;[5] Burkina Faso, 84.7%;[6] Tajikistan, 32% with helminths and 47.1% with protozoa;[7] and Nigeria, 51%;[8] United Arab Emirates, 96.5%;[28] Argentina, 71.5%;[29] Ethiopia, 48.2%;[30] Brazil, 61.6%;[31] and West Africa, 64.7%,[32] indicating that the regional control and prevention measures on intestinal parasites in the study area have been more successful than many other parts of Iran. In addition, the implementation of such control and prevention strategies in Iran has achieved more fruitful outcomes, compared to other developing countries.

Based on the present study, the diversity of intestinal parasites, in particular, that of intestinal helminths, showed a reduction when compared to previous years so that even one case of infection by soil-transmitted helminths was not observed. In our study, four species of protozoa and two species of helminths were found. Several studies have reported the number of parasite species isolated in their studies including Norouzi et al.,[20] 9 species (7 protozoa and 2 helminths); Bahmani et al.,[21] 10 species (6 protozoa and 4 helminths); Rahimi et al.,[22] 4 species (3 protozoa and one helminth); Haji Aliani et al.,[23] 6 species (5 protozoa and 1 helminth); Anvari Tafti et al.,[24] 5 species (all protozoa); Iranikhah et al.,[25] 5 species (3 protozoa and 2 helminths); Ghahramanloo et al.,[26] 7 species (3 protozoa and 4 helminths); and Rafiei et al.,[27] 4 species (1 protozoon and 3 helminths). In addition, a reduction in the diversity of intestinal parasites has occurred in some developing countries reflected in the studies by Choi and Kim[3] from Peru (5 species of parasites; 4 protozoa and 1 helminth); Abossie and Seid[4] from Ethiopia (4 species; 2 protozoa and 2 helminths); and Matthys et al.[7] from Tajikistan (6 species; 2 protozoa and 4 helminths).

In the present study, similar to most studies reported from Iran in the recent years, G. lamblia was the most common intestinal protozoa although the prevalence rate of this parasite has shown considerable differences in various studies. The prevalence rate of G. lamblia in our study was 3.26%. There are many studies on the prevalence of G. lamblia by other authors such as those reported by Norouzi et al., 2.34%;[20] Rahimi et al., 7.4%;[22] Haji Aliani et al., 6.5%;[23] Anvari Tafti et al., 2.8%;[24] Iranikhah et al., 6.23%;[25] Ghahramanloo et al., 21.4%;[26] and Rafiei et al., 14.11%.[27] Higher prevalence rate of giardiasis in children may be due to possible zoonotic transmission of this parasite.

Generally, in most studies reported from Iran within recent years, the major human infections have been limited to intestinal protozoa and infection by intestinal helminths has significantly decreased during these years.[18],[23],[33] In the far distant past, different types of intestinal helminths, especially Ascaris, Trichuris trichiura, hookworms, Trichostrongylus, T. saginata, and Hymenolepis nana were reported at different frequencies from various parts of Iran.[9],[10],[11],[12],[13] For example, 87%–95% of residents of six villages in Isfahan, located in central regions of Iran, were infected by Ascaris lumbricoides.[9] In the present study, no case of infection by soil-transmitted nematodes was observed. It seems that at present, these parasitic infections need to be on the verge of local transmission cessation in the study area.

In our study, only one case of infection with T. saginata was identified, a finding comparable with those of other studies showing low prevalence of this parasitic infection in Iran.[18],[20],[23] Beef as the main source of animal protein is often consumed completely cooked among Iranian. Therefore, this food habit can be a major factor for low prevalence rate of this helminthic infection in the past and the present time of the country.

The data of the current study showed that 3.5% of children were infected with E. vermicularis, a figure much lower than the prevalence rate found in the majority of the studies carried out in various parts of Iran within the last decade including those from Babol, located in the north of Iran (22.2% of primary school-age children);[34] Khaash located in the southeast of Iran (24.1% of primary school-age children);[35] Shahroud located in the northeast of Iran (22.2% of nurseries children);[27] Kuhdasht in Lorestan, located in the southwest of Iran (33.8% of primary school-age children);[36] and Oraman region in Marivan located in the west of Iran (41.1% of nurseries children).[37] Reduced prevalence rate for enterobiasis found in our study, compared with those reported from other regions of Iran, may be associated with differences in the local health care services and health awareness of the families and nurseries teachers. Decrease in the prevalence of enterobiasis, in comparison with the soil-transmitted helminths, has been extremely noticeable in Iran, a documented fact which could possibly be related to the difference in the life cycle and the transmission route of this parasite. E. vermicularis is the only intestinal worm, for which the major transmission route is direct person-to-person contact. Moreover, in the life cycle of this pinworm, external autoinfection could easily and frequently happen, leading to continuation and progression of this parasitic infection.

Altogether, the studies on the intestinal parasites carried out in different parts of Iran have demonstrated a significant decrease in the prevalence of these parasites. It seems that a chain of factors, in a synergistic manner, have played a role in the reduction of IPIs. These factors include development and expansion of primary healthcare services offered in nurseries, increased education level and health awareness of both parents and nurseries teachers, reduced number of family members, easy access to broad-spectrum antiparasitic agents, widespread use of hygienic drinking water by establishing water treatment plants and water distribution systems, and decreased environmental contamination through installation of sanitation system, which lead to reduced contaminating foci in particular for vegetables. One of other factors that may specifically play a role in reducing the number of parasitic infections in children of nurseries is the need for mandatory tests on intestinal parasites for children to be admitted. In the present study, no significant correlation between IPI and the study variables including children's age, sex, hand-washing habit using soap, and raw vegetable consumption, as well as mothers' education level and occupation, was observed; nevertheless, a significant correlation was only demonstrated when a comparison was made between the study nurseries. In this respect, in a number of nurseries, no case of IPIs was found. This discrepancy in the prevalence of intestinal parasites between nurseries could possibly be associated with the difference in health care services offered to children in nurseries, health awareness of nursery teachers as well as parents. In the present study, it was shown that the prevalence rate of enterobiasis among the kids with hand-washing habit using soap was lower than those lacking this habit, a finding in agreement with a previous study.[38]

  Conclusions Top

Based on our results, it could be concluded that the prevalence rate for infection with E. vermicularis and other intestinal parasites in the children of nurseries and preschools has reduced in the study area, compared to the figures published in the previous years, confirming the promotion of hygiene and health care services. Furthermore, a lack of infection by some intestinal parasites such as A. lumbricoides and T. trichiura indicates that these parasites are in the stage of transmission chain cessation in this study area of Iran.


This study was part of an MSc thesis in Qazvin University of Medical Sciences, Qazvin, Iran. The project was financially supported by the Deputy for Research and Technology of Qazvin University of Medical Sciences.

Financial support and sponsorship

Qazvin University of Medical Sciences supported the study.

Conflicts of interest

There are no conflicts of interest.

  References Top

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  [Table 1], [Table 2], [Table 3]

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