Intestinal Parasitic Infection among School Children in Golestan Province, Iran

INTRODUCTION

Infections by intestinal parasites are a major public health problem worldwide, especially among children in developing countries. WHO estimated that approximately 3.5 billion people are infected by intestinal parasites and about 450 million children are ill due to these infections WHO, 2000: Warunee et al., 2007). Infections with intestinal parasites may have important health consequences and cause iron deficiency anemia, growth retardation in children and other physical problems” (Scolari et al., 2000; Nasiri et al., 2009). The type of infection is much different depending on the behavioral factors and the geographical regions.

It is necessary to conduct periodic studies for information of intestinal parasitic infections in the general population. There are previous studies that has reported different prevalence rates of parasitic infection in various areas of Islamic Republic of Iran (Sayyari et al., 2005). Although, there have been a few reports of infection rates of intestinal parasites in some local areas of Golestan province (Saebi, 1998), no extensive epidemiological survey in the area has been conducted. The objective of this investigation was to study intestinal parasitic infections in primary school children living in Gorgan to estimate their prevalence, their association with socio-economic characteristics and the influence of simple and primary hygienic measures in reducing their frequency.

MATERIALS AND METHODS

Study group: A cross-sectional survey was conducted in 18 primary schools of Gorgan city, capital of Golestan province, located in the north of Iran. This survey was performed between October 2010 and March 2011. The sample size was calculated according to the prevalence of 27%, based on the results of previous studies Daryani and Ettehad, 2005, at precision of 0.07 and at 0.05 significant levels. 800 school children from both boys and girls ranging from 8 to 12 years old were conducted to this study.

Study design: Parents of the participating children filled out a questionnaire on common risk factors for parasite infections, as described in literature questions on environmental risk factors were related to living background; those on sanitary risk factors to water supply (piped water); those on socioeconomic risk factor to household income (6 000 000 Rial/month or less) (Ostan et al., 2007) and education level of the parents (less than 12 grades or higher). Behavioral factors were eating with unwashed hands (yes or no), eating unwashed/raw vegetables (yes or no), eating unpeeled/unwashed fruit (yes or no), biting fingernails/sucking thumb (yes or no) (Herrstrom et al., 1997; Rai et al., 2005; Asaolu et al., 2002).

Intestinal parasitic examinations: An oral description and specific instructions for handling and contamination avoidance of the stool specimen were given to all the children. All stool specimens were preserved in 10% formalin before examination at the department of Parasitology, Faculty of Medicine, Golestan University of Medical Sciences. In the Parasitology lab, stool samples were examined macroscopically for visible proglottides or adult helminths. Then each sample concentrated using formalin-ether sedimentation technique for microscopic examination. Protozoan parasites were examined by staining with logul’s iodine solution using light microscopy at high (400 X) magnification. Ova of helminth parasites were examined by direct wet-mount observation at low (100 X) magnification.

Ethical considerations: The present study was approved by the Ethics Committee of the Faculty of Medicine at Golestan University of Medical Sciences and all students and their parents were aware from the study objective and were content to participate in this survey.

Statistical analysis: For statistical computations, SPSS (Chicago, IL, USA) program for Windows, version 16 were used. Statistical differences of the data were analyzed by Chi-square tests or Fisher’s Exact test where appropriated at 0.05 significant level. Consent forms were signed by the parents of participating schoolchildren.

RESULTS AND DISCUSSION

A total of 800 schoolchildren were screened. The participating children were 482 (60.25%) boys and 318 (39.75%) girls. The mean age of the participants was 8.5 years. The response rate to the questionnaires was 100%. The overall prevalence of parasite infection among the participants was 28.8% (230/800). Giardia intestinalis and Hymenolepis nana were the most common protozoa and helminth infections, respectively.

No statistically significant difference was observed between the prevalence rate of intestinal infection across gender (p = 0.22) and age (grade of education) (p = 0.80). Prevalence was highest in the 8-11 years age group (34.1-32.1%) children, respectively.

The prevalence of parasitic infection increased by family size including 39.1% (27/69), among the families having ≥3 children (p<0.05). There was no significant relation between prevalence of parasitic infection and parent's education level (Table 2). The prevalence rate of infection was lower in those students (28.2%) whose fathers were employer (673/190) and more among those students (31.4%) whose fathers were not employer (127/40).

The most common intestinal pathogenic and nonpathogenic parasite were Giardia intestinalis (9.9%; 79/800) and Blastocystis sp. (15.2%; 122/800), respectively. The rate of contamination with protozoa was 26.1 and 3.6% for intestinal helminthes. The prevalence rates of Hymenolepis nana, Ascaris lumbricoides, Enterobius vermicularis, Entamoeba histolytica/dispar and hook worms among participants were 1.5, 0.5, 1.2, 1 and 0.4, respectively. 10.5% of boys and 8.8% of girls were infected to intestinal parasites.

The frequency distribution and Prevalence of intestinal parasites infection among the schoolchildren are indicated in Table 1. Table 2 describes the distribution of environmental, socioeconomic, sanitary and behavioral risk factors among the children in the respective areas and municipalities. Significant associations were found between infections and take care of animals in house as well as brother, sister number (p-value<0.05) (Table 2). No statistically significant relationship found between rate of intestinal parasite infection and education levels of parents, household income, using pipe water, biting fingernails/sucking thumb, eating unpeeled/unwashed fruit/vegetables and washing hands before eating or after toilets

Nearly one third of students (28.8%) aged 8- 12 years in North of Iran, Golestan Province were infected with intestinal parasites. Recent reports in Iran, showed a prevalence rate of intestinal parasites ranging from 18.4 to 29.75% in general populations (Nematian et al., 2008; Sayyari et al., 2005). There are many epidemiological studies of intestinal parasites throughout the Iran, reported similar results including 30% in Kerman in 1991 (Valian and Sharifi, 1993); 37.3% in Islamshahr in 1992 (Godarzi, 1993); 59.4% in Tehran in 1994 (Rohanni, 1994); 30.5% in Zabol in 1997 (Baraoe and Sharifi, 1996); 48.2% in Isfahan in 1998 (Baghaie et al., 1999); 56.6% in Qazvin in 2000 (Mahyar et al., 2000); 39.4% in Mashhad in 2001 (Salehabadi, 1990); 28.5% in Babol in 2001 (Ghahramanloo et al., 2001); 49.6% in Robatkarim in 2005 (Soheil Azad et al., 2005); 13.7% in school children in Semnan Province in 2005 (Atashnafas et al., 2006); 13.7% in Jahroom in 2007 (Davami et al., 2008).

Table 1:	Frequency distribution and prevalence of intestinal parasites in school children of Gorgan city according to gender

OR: Odd ratio, CI: Confidence interval

Table 2:	Distribution of environmental, socioeconomic, sanitary and behavioural risk factors among the school children of Gorgan city

*Statistically significant differences, OR: Odd ratio, CI: Confidence interval

However, there are national Study in Islamic Republic of Iran that reported the prevalence of parasite infection 19.3% in general population and 25.5% in the children aged less than 15 years (Taheri et al., 2011). The results of the present study revealed that the prevalence of intestinal infection was higher than that reported in comparison.

Giardia intestinalis and Blastocystis hominis, the first and second most common protozoa in the present study, both can be transmitted orally through drinking water. Concerning polyparasitism, our results are comparable to those of Keiser et al., (2002) obtained in western Cote d’Ivoire. The observed multiple infections could be explained by the facts that many species of protozoa have the same mode of transmission and that hygiene is poor in these areas. Blastocystiss sp. and G. lamblia were found in samples from all the localities studied.

Because there are no reports of parasites from Gorgan so we could not compare our results with previous data. It should be mention that in most of the surveys performed in Iran and in other countries, G. intestinalis was the most common intestinal protozoa among the residents of rehabilitation centers as well as normal populations, that are in concordance with the present study. For example The prevalence rate of G. intestinalis was 37.4% in students of southwest of Tehran in 1985 (Garoz, 1985); 25.3% in Kerman's students in 1991 (Valian and Sharifi, 1993); 19% in children of north of Tehran in 1992 (Nazari, 1992);14.2% in Islamshahr in 1992 (Godarzi, 1993); 17.2% in Lahijan in 1997 (Saraei and Rezaian, 1997); 40% in elementary school of Yazd in 1998 (Saebi, 1998); 29.8% in Mobarakeh in 2001 (Atashnafas et al., 2006); 24.1% in primary school students of Babol in 2001 (Ghahramanloo et al., 2001); 38.1% in Birjand in 2002 (Taheri et al., 2004); 18.5% in Robat karim in 2005 (Soheil Azad et al., 2005); 8.4% in Semnan in 2005 (Atashnafas et al., 2006); 8.1% in Jahrom in 2007 (Davami et al., 2008); 18.5% in Gorgan in 2008 (Touhidi and Mostafa, 2009); and 28.7% in South Khorasan Province in 2011 (Taheri et al., 2011).

One of the important risk factor for the parasite infection is water supply. Giardiasis outbreaks have occurred from the contamination of drinking water supplies (Wilson, 1998). Giardia spp. as a cause of water-borne disease of human has been increasingly recognized over the past 10 years (Zuckerman et al., 1999). Also In water supplies of different parts from the world the cyst of Giardia spp. have been isolated (Okyay et al., 2004).

In our findings, the prevalence of H. nana was 1.5%. H. nana has detected from many part of Iran especially in western areas. The prevalence of this parasite was reported 20% in Bandar Abbas and Minab (Saebi, 1998), 14.7% in Zahedan (Fazaeli et al., 1997), 13% in Khozestan and Gonbad Kavous (Saebi, 1998), 3.9% in Kerman (Ziya Ali and Masuod, 1997), 3.8% in children of Birjand (Taheri et al., 2004).

In previous studies (Sayyari et al., 2005), ascariasis was high prevalency in most area of Iran for example 83% in Khozestan; 81% in Tabriz; 78% in Kermanshah; 72-97% in Isfahan; and 14-60% in Mazandaran; but 1-4% in Sistan and Bandar Abbas. According to the results of this study, the prevalence of ascariasis was 0.55% such as the results of mentioned study in various parts of Iran (Sayyari et al., 2005; Valian and Sharifi, 1993; Godarzi, 1993; Soheil Azad et al., 2005; Taheri et al., 2011). These data declare that prevalence of ascariasis has been decreased a lot between the last 10-15 years. It means that the public health knowledge about the ascariasis disease has increased in different populations.

In this study The prevalence of E. vermicularis was 1.2%. In other studies that use non specific stool examination method for E. vermicularis detection, the prevalence of this parasite was 0.2% in Kerman (Nasiri et al., 2009), 0.4% in Jahrom (Davami et al., 2008), 0.7% in Zabol (Baraoe and Sharifi, 1996) and 2.9% in Islamshahr (Valian and Sharifi, 1993). In other studies with specific examination method (Scoth test), E. vermicularis was prevalent. For example the prevalence was 22.1% in Birjand in 2002, 54.1% in Ramsar in 1990, respectively (Sayyari et al., 2005).

Many studies on the prevalence of intestinal parasitic infections have been performed in developing countries, due to their wide diffusion in this continent, reported the same results. In most of these areas, G. lamblia was the most dominant infection. The prevalence rate of the intestinal parasitic infections in mentally retarded individuals in the world, were 76.67% in Egypt (Mohamed et al., 1991), 66.4% in northeastern part of Nepal (Sharma et al., 2004); and 54.2% in Combodia of Korea (Lee et al., 2002); 46.7% in Srinaga of India (Wani et al., 2007); 31.8% in Aydinca, west of Turkey (Okyay et al., 2004); 30% in Abha, Saudi Arabia (Omar et al., 1991), 14.6% in Tripoli of Libya (Ben Musa et al., 2007).

We did the study among schoolchildren because they were one of age groups the most exposed to intestinal parasites and were generally accessible.

The data of the study showed no significant difference between sex of children and intestinal parasitic infection Even though gender was not a significant risk factor for the prevalence of intestinal parasitic infections, males were more likely to be infected (10.5%) than females (8.8%) in the present study, which is consistent with other reports (Kim et al., 2003; Noor Azian et al., 2007; Arani et al., 2008). Children living in crowded family (≥3) were more susceptible to infection. The data also showed that take care of animals in house helps to transmission of parasite infections as there was a significant association between that and rates of parasite infections (p-value<0.05).

The correlation between children health status and parents’ education is well known (Zuckerman et al., 1999). However in this study, the degree of parents’ education was not significantly associated to rates of infection, as were other factors such as hand washing and washing vegetables and fruits.

In conclusion, the study showed that intestinal parasites are remarkable among school children in Gorgan, thus, intervention programs including health education and environmental sanitation are required.

ACKNOWLEDGMENTS

We gratefully acknowledge the students, parents and school staff who participated in this study. This project was financially supported by Golestan University of Medical Science, project No. G/P/35/2073.