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Soil-transmitted helminths (STHs) infect over a billion individuals worldwide. In India, 241 million children are estimated to need deworming to avert the negative consequences STH infections can have on child health and development. In February-April 2011, 17 million children in Bihar State were dewormed during a government-led school-based deworming campaign. Prior to programme implementation, a study was conducted to assess STH prevalence in the school-age population to direct the programme. The study also investigated risk factors for STH infections, including caste, literacy, and defecation and hygiene practices, in order to inform the development of complementary interventions. A cross-sectional survey was conducted among children in 20 schools in Bihar. In addition to providing stool samples for identification of STH infections, children completed a short questionnaire detailing their usual defecation and hand-hygiene practices. Risk factors for STH infections were explored. In January-February 2011, 1279 school children aged four to seventeen provided stool samples and 1157 children also completed the questionnaire. Overall, 68% of children (10-86% across schools) were infected with one or more soil-transmitted helminth species. The prevalence of ascariasis, hookworm and trichuriasis was 52%, 42% and 5% respectively. The majority of children (95%) practiced open defecation and reported most frequently cleansing hands with soil (61%). Increasing age, lack of maternal literacy and certain castes were independently associated with hookworm infection. Absence of a hand-washing station at the schools was also independently associated with A. lumbricoides infection. STH prevalence in Bihar is high, and justifies mass deworming in school-aged children. Open defecation is common-place and hands are often cleansed using soil. The findings reported here can be used to help direct messaging appropriate to mothers with low levels of literacy and emphasise the importance of water and sanitation in the control of helminths and other diseases.
Bihar state is land-locked, bordered to the north by Nepal and split by the river Ganges which flows from west to east through the state. Located far from the sea and influenced by the Himalayas, the state has a continental monsoon climate, typical of most of Northern India. The survey conducted in Bihar State was a school-based, cross-sectional survey. Data on Bihar is scarce; according to recent reports, Bihar still has high levels of poverty and low levels of basic sanitation: 33% of the population falls into the lowest wealth quartile in India, only 17% of households have access to a toilet facility and 12% of children report having had diarrhoea in the last week [15]. Bihar is composed of thirty-eight administrative districts, four of which were selected for the survey: Araria, Aurangabad, Muzaffarpur and Gopalganj. These districts were selected to complement the existing survey data in Bihar which was collected in Supaul and Patna in 2010 (not reported here). Primary school children were surveyed using a two-stage cluster sampling scheme: five primary schools were randomly selected in each district, within which sixty-five children were selected using a table of random numbers and the school’s list of registered children (in attendance) as the sampling frame. The children were selected class by class, spread equally between year groups and half male and half female. Any children younger than four were excluded even if they were enrolled at the school. A different random number table was provided for each school, class and for males and females. Children in a class were asked to stand and then counted out to the specifications of the random number table. The selection procedure took non-compliance into account and aimed to ensure that a minimum of fifty children were sampled per school. This sample size and sampling methodology is deemed sufficient for determining prevalence in a district, taking into account the design effect and misclassification errors [16, 17]. All laboratory technicians underwent a three-day training to ensure study methodologies were consistent. They were divided into two teams, and employed to collect the data over a period of three weeks completing one district each week. Prior to the study, an information letter was sent by the state health department inviting the school to participate. Data were collected from each school over the course of two days. On day one, the team spoke with teachers and parents, ensured receipt of the letter, answered questions and took informed consent from the head teacher of each school. Children were selected for the study, provided with a small screw capped plastic container, other sample collection materials and a local language flyer explaining the study verbally and pictorially. School coordinates were recorded using a hand held Global Positioning System Monitor (GPS). Students collected their samples at home the next morning and brought them to a collection point that day. Samples were discarded if the ID labels did not match the child’s name on the registration list. Participants also provided basic demographic data including age, sex, caste and class. In collecting information on caste local terms and broad classifications were pre agreed and used as follows: General Caste; Backward Caste One; Backward Caste Two; Extremely Backward Caste; Scheduled Caste) and Scheduled Tribes [18]. Muslim children were not classified by caste as it was difficult to establish standard classifications that would be reliable and universally applicable—the caste system is mainly associated with Hinduism. Each child was interviewed in the local language by a trained community volunteer using a short questionnaire which included additional socio-demographic questions and inquired into defecation and hygiene practices. Survey teams also recorded information on the presence of water on tap, hand-washing stations and toilets on the school premises and documented any known recent deworming activities including the State community based Lymphatic Filariasis mass drug administration (MDA) which included Albendazole. All stool samples were processed within a few hours of collection using the modified Kato-Katz technique (kits supplied by Vestergaard-Frandsen) recommended by WHO for use in field settings [19]. Screening of infection for STH was based on a double Kato-Katz smear of 41.7 mg prepared from fresh stool samples. Samples were left to clear for a minimum of 20 minutes and examined within one hour of preparation since hookworm eggs would be cleared thereafter. The mean total number of eggs was expressed as eggs per gram (EPG) of faeces. Senior parasitologists carried out quality control on every negative slide and confirmed the first egg identification on each slide under the microscope. Egg counts were multiplied by 24 to adjust them to eggs per gram and classified as ‘light’, ‘medium’ or ‘heavy’ intensity infections according to WHO guidelines [16]. Prevalence statistics were used to produce maps in Arc Map 9.3 (ERSI, Redlands, CA, USA). Questionnaire data were double entered into MS Excel, and any missing or unclear data were clarified with the child during sample collection. The data were cleaned and transported to Stata 12 for analysis (StataCorp, 2011). Variables detailing the frequency (always, sometimes or never) of use of different defecation sites (open field, jungle, river or latrine) were recoded to create one variable for defecation practice. One variable for hand-hygiene practices was similarly created from questions on whether ash, soil, water only, or soap are ever used to wash hands after defecation. Due to data recording issues, analysis of defecation practices was restricted to Aurangabad and Gopalganj districts only. Castes are described in the categories outlined in Table 1 (Castes 1 to 6). As only twelve children from Caste 6 were included in the survey, they were combined with children from Caste 5 to allow for stratification by caste in further analysis. The relationship between STH infection and demographic and socio—economic variables (household assets), maternal education (proxy based on maternal literacy), caste, defecation practice, hand-hygiene practice, and school-level variables was explored in univariate analysis, taking into account the cluster effect of school. A log binomial model (family: binomial, link: log) was developed to allow for and to explore between-school variance in infection levels, assuming a fixed effect of individual and school level variables and using generalised estimating equations to account for school-level clustering. Explanatory variables significant at P < 0.2 level in univariate analysis were included in the model, which looked for associations significant at P < 0.05. The study was carried out by the State Government of Bihar in order to inform a public health programme. Data for the risk factor analysis was released by the Government and has been analysed and published only with their permission. Ethical consent was sought from Imperial College Ethical Review Board for the publishing of the data (June 2011); the board returned that no ethical approval was required as the data collection was not primarily research but for a public health programme, and the government had authorised publication of its public health information. Consent procedures were in line with those laid out by the government of Bihar. Letters were sent in advance to schools to allow them sufficient time to liaise with parents and decline consent. On the survey day, as many parents as possible were invited to the schools on survey day to observe the distribution of sample pots. No samples were requested from children on the day, but they were sent home each with the required materials and a flyer explaining the survey and instructions for collecting the sample. Children who presented with a sample the next morning were assumed to have parental consent to participate in the study. No information was retained or utilized for any child who did not return a sample. Informed consent was taken from each head teacher on behalf of the parents before the materials were distributed to children, and the school head teachers signed a consent form as a written record of informed consent. Verbal assent was taken from every child. Schools were provided with the results of the survey the next day, which were delivered and explained by a member of the survey team. All schools in Bihar were provided with deworming medication as well as two trained teachers during state deworming.
