Introduction

Intestinal helminth infections are highly prevalent among school-age children both in schools and communities of developing countries (Poudyal et al. 2006). Many helminth parasites remain major contributors to morbidity in developing countries. Among the effects associated with these parasites are growth retardation, intestinal obstruction, hepatic and biliary diseases, impaired cognitive development, and nutritional effects such as iron deficiency anemia (Ramdath et al. 1995). Intestinal parasites are transmitted through the contamination of water, soil, and food by feces, a direct consequence of poor hygienic and living conditions (Gamboa et al. 1998). According to WHO, the level of helminth infection can be viewed as an index of a community’s progress towards a desirable level of sanitation (WHO 1981). There are a few studies on the prevalence of intestinal helminths in other parts of Kashmir Valley (Wani et al. 2007a, b, c), but there is no record in literature regarding the status of helminth infections and their associated risk factors in district Shopian of Kashmir Valley. Therefore, present study was undertaken to determine the prevalence of intestinal helminths and related factors among children of Shopian district in the Kashmir Valley, India.

Materials and methods

Study area

Shopian town-the district headquarter is situated at a distance of 51 kms from Srinagar & 20 kms from Pulwama district and 2146 m above the sea level. It has decades of old road connectivity with Anantnag district as well as Kulgam district. Presently district Shopian having two assembly constituencies consists of one Tehsil, one CD block, one municipal Committee with 13 Wards, 43 Patwar Halqas & 231 inhabited villages. As per census of 2011, total population of the district is 2.66 lacs including 15 % of ST population. About 95 % of the population lives in its rural areas (http://www.shopian.nic.in/index.html).

This study was carried out between May 2013 and November 2013 in all the study sites of district Shopian. Official meetings with the personnel from health services, city councils, and schools, as well as with parents and school children from study sites were conducted in order to explain the protocol of study. In total, 352 children including 228 males and 124 females between the ages of 4-15 year (X ± SD = 9.2 ± 2.3) participated in the study (these children had no apparent disabilities and were not receiving drug therapy for parasitic infections). Written consents were required from both parents in order for the children to participate. Children requiring medical assistance were properly treated or referred for medical attention. The children’s ages were obtained through school records.

Collection of socio-economic characteristics of the children’s families was under taken with a structured questionnaire. Interviews were administered face to face with mothers in children’s schools. The level of education of mothers, sanitation facilities, type of drinking water (tap, well, or stream/pond water) and defecation site (open or modern sanitary latrine) were collected as proxy variables of socio-economic conditions. Five grams of fresh morning stool samples were collected in nylon containers containing 10 ml of 10 % formaldehyde. The containers were labeled, and immediately transported to the parasitological laboratoryfor further processing. Stool specimens were examined using direct smear and zinc sulphate concentration techniques. A computer program (SPSS10.05 for windows) was used for data analysis. Descriptive data was given as a mean ± standard deviation (SD). Student’s t test was used for the analytic assessment. The differences were considered to be significant when the P-value obtained was less than 0.05. Following the WHO ethical guidelines of ‘no survey with out service’, all children enrolled in the survey received 1 tablet of 400 mg albendazole as a treatment protocol for STH.

Results

Among 352 children subjected to stool examination, data reveal that 265 (75.28 %) cases were positive for intestinal helminths. Ascaris lumbricoides was the most prevalent helminth parasite (71.87 %) followed by Trichuris trichiura (26.42 %), Enterobius vermicularis (13.92 %) and Taenia saginata (5.39 %). Single type infection was seen in 38.63 % of the infected children, where as 38.64 % were infected with multiple type of helminth parasites. Prevalence of infection peaked in the age group of 12–15 years (84.91 %) followed by the age group of 8–11 years (81.70 %) and age group of 4–7 years (50.54 %) (P < 0.05). The study reveals that, age group, water source, condition of water, defecation site, personal hygiene, and maternal education were significantly associated with the prevalence of intestinal infections (Table 1) (P < 0.05), whereas residence and sex were not significantly associated with it (P > 0.05).

Table 1 Risk factors in district Shopian
Full size table

Discussion

Results of the present study indicate a prevalence of 75.28 % (265 positive cases out of the total of 352 children screened). These figures when compared with studies conducted in other parts of the Kashmir Valley and world show that district Shopian is endemic for intestinal helminthiasis. For example Studies conducted in the Kupwara district of Kashmir Valley (Wani et al. 2007a), Srinagar city of Kashmir Valley (Wani et al. 2007b) and Budgam district of Kashmir Valley (Wani et al. 2007c) show that intestinal helminths are endemic in these areas with Ascaris lumbricoides the most prevalent helminth parasite. Studies conducted on the frequency distribution of gastrointestinal helminths by Bundy et al. (1988) showed a high overall prevalence of 62 % among the urban slum children of Malaysia. Rodriguez et al. (2000) reported a high prevalence of 72 % among the school children studying in a public institution in Maracaibo, Venezuela. High prevalence of intestinal helminth infections is probably a consequence of a low standard of living, poor sanitation, lack of personal hygiene, traditional methods of agriculture, indiscriminate defecation, the use of night soil as fertilizers and other occupational work. (Wani et al. 2007b). In the present study not a single case of Hookworm infection was observed. The reason for the absence of Hookworm infection is that climatic factors are not favorable for the survival of hookworm eggs and larvae in the soil as the temperatures remain mostly cool in Kashmir Valley.

Age specific prevalence data shows a relationship between age and prevalence of parasites. Highest infection, i.e., 84.91 % was seen in the 12–15 age group (P < 0.05), followed by 81.7 % in the 8–11 age group, and 50.5 % in the 4–7 year age group. Similar age related prevalence variations have been reported by other investigators among school children. For example, Ibrahim (2002) in Gaza, Palestine, showed that most of the positive cases were clustered in the age groups of 9–14 years. The reason for this type of distribution is that children in the lower age groups mostly remain indoors and are not exposed to infections. As the age advances, children start to play and so get exposed to infections.

Even though gender was not a significant risk factor for prevalence of intestinal parasitic infections, males were more likely to be infected (78.0 %) than females (70.1 %). This finding could be partially explained by the difference in gender roles. Males in their early age are likely to adopt work responsibilities in outdoor environments and girls are likely to commence duties in indoors because of social and religious restrictions. The outdoor environments, in farm lands, or in playing fields, are a common place of defecation for males during working or playing hours and, therefore, contamination of soil in these areas would constitute a significant risk for parasite transmission. Singh et al. (1984) reported similar results in their study on rural community of Varanasi, India, where in males exhibited a higher prevalence of intestinal parasitism than females. A study conducted by Ibrahim (2002) on the prevalence of parasites among school children in Gaza, Palestine, likewise showed a significantly higher prevalence of infection among males compared to females.

Children that sourced drinking water from rivers or streams and wells were found to harbor a greater prevalence of infection than those who had access to tap water. This pattern of infection has been confirmed in the studies of Norhayati et al. (Norhayati et al. 1998) and Narain et al. (2000). Curtis et al. (1995) demonstrated that mothers from poor community in Burkina-faso, Africa, with access to tap water in the yard, were more likely to use safe hygiene practices than mothers using wells in the yard. It is possible that poor hygiene practices associated with access to water is a more probable risk factor for increased parasitic infection among children. Also children drinking boiled water were found contracting less infection than those who drank unboiled water from any source. This fact has been confirmed in the study conducted in Srinagar city of Kashmir Valley (Wani et al. 2007b).

Even though, it is argued that in highly contaminated environments, faecal transmission in defecation ground may not be a single most important site for geohelminth infection (Feachem et al. 1983), it was found to be a significant univariate risk factor for infection with intestinal helminthiasis, where in a high prevalence was seen in children defecating in open fields, compared to low prevalence among children who defecate in modern septic latrines. In Shopian district children are at particular risk with nearly 70 % of children less than the age of 15 years, defecating outdoors in either the open latrines or nearby fields. More over, at this age non supervised children may be more prone to defecating in sites that are already polluted by faeces and therefore be exposed to more frequent and heavy infections than adults (Hominick et al. 1987). Most of the government schools in both rural and urban areas in Shopian district are with out modern septic lavatory facilities, so regardless of defecation practices, while at home, children have no option but discretely defecate openly. So, the school environment becomes the transmission ground of intestinal helminthiasis and constitutes a significant source of infection.

It is also evident from the present study that children with better personal hygiene had a lower prevalence of intestinal parasitic infections than those living in less hygienic conditions (P < 0.05). In our study, it was also found that maternal education was a significant risk factor for the prevalence of infection; apparently, this factor extensively contributes to controlling risk factors for intestinal infections. Maternal education has been found to be the most important risk factor for parasitism in other studies as well (Toma et al. 1999; Phiri et al. 2000).

The present study reveals that intestinal helminths are highly abundant among children of Shopian district. This situation strongly calls for the institution of control measures, including treatment of infected individuals, improvement of sanitation practices, and provision of clean water. The impact of each measure would be maximized through a health education program directed at children and their mothers in particular, and to communities in general.