January 2013

January 2013Soil-transmitted Helminths, Deworming, and Reinfection in Chinas Guizhou Province

Linxiu Zhang, Yingping Cai, Xiaobing Wang, Xiaochen Ma, Alexis Medina, D. Scott Smith*Soil-transmitted Helminths, Deworming and Reinfections in Chinas

Guizhou Province

AbstractThere is little hard data on STH infections in China. To examine this issue in a more systematic way, we conducted a survey of 1,724 children, aged 3-5 and aged 8-10, in 6 counties in poor, impoverished and minority areas of Guizhou province in Southwest China. Anthropometric, demographic, parasitological and hygiene data were collected to better understand the prevalence of STH infections and the effectiveness of deworming in rural China. We find that 37.5% of the sample children were infected with one or more of the three types of STH tested for in this study. However, only 50.4% of them reported having taken deworming medicine during the 18 month period prior to the survey. Of those who reported being dewormed, 34.6% tested positive for STH infections. We find that poverty and the number of siblings are significantly and positively correlated with infections and reinfections, and parental education is significantly and negatively correlated with infections and reinfections. We find no statistically significant evidence linking ethnicity with infection rate, decision to deworm, or reinfection status.

Key Words: intestinal roundworms, soil-transmitted helminths (STH), children, poor,

rural, China, deworming; reinfectionsJEL Codes: I14, I15, I18, O10, O53

Soil-transmitted Helminths, Deworming, and Reinfection in Chinas Guizhou Province1. Introduction

Infections with soil-transmitted helminths (STH)including the roundworm (Ascaris lumbricoides), two types of hookworm (Ancylostoma duodenale and Necator americanus), and the whipworm (Trichuris trichiura)are amongst the most common infections worldwide. More than 130 countries/territories are endemic with STHs (World Health Organization, 2008). Children are disproportionately vulnerable to STH infections. Globally, there are around 800 million children infected with STH, and most them live in developing countries (Chan, 2011).

There is a well-established linkage between STH infection and anemia, malnutrition and other adverse health and nutrition outcomes (Adams et al., 1994; Corbett et al., 1992; Hotez and Pritchard, 1995; Pollitt, 1990). These findings point to the importance of deworming programs; indeed, researchers have even shown a positive educational impact of deworming in rural schools (Miguel and Kremer, 2004). Thus, more effort in recent years has focused on deworming programs in the developing world (see, for example, the Children Without Worms project).

Despite academic consensus in the international literature of the adverse consequences of STH infections and the importance of deworming, as well as a growing worldwide awareness about STHs, high infection rates continue to be observed in China. While Chinas health officials were concerned with STH infections throughout the 1960s and 1970s, and even had a comprehensive national deworming program admired by many development practitioners (Wagstaff et al., 2009a), attention to the disease and its treatment seems to have declined over the past two decades since then. This trend began in the 1980s when public funding for rural health declined precipitously (Wagstaff et al., 2009b). At the same time, rural Chinas barefoot doctor systemwhich effectively offered free treatment of common diseases, including STH infectionscollapsed, leaving rural residents to fend for themselves and forcing them to seek care from private providers with little or no help from a national insurance system. A number of diseases that had been well-controlled have re-emerged in rural China in recent years. STHsperhaps due to their nearly invisible nature and prevalence that is highest in remote, rural areasare now re-emerging (Wang et al., forthcoming).

The literature in Chinathough it is mostly anecdotal or focused on a single regionseems to support the claim that there is a resurgence of STH infections in China. High STH prevalence has been observed in various regions of the country from Yunnan (Steinmann et al., 2008) to Fujian (Xu et al., 2000) to Hunan (Zhou et al., 2007), though nearly all of these studies were small, limited to a single township or village. A parasitological survey of 274 school children, aged 10-12 years, in five villages in Hunan Province showed STH infection rates to be 37.3% in girls and 33.3% in boys (Zhou et al., 2007). The prevalence of the three main STHs (Ascaris, hookworm, and Trichuris) in 215 individuals in one village in the southern part of Yunnan Province was above 85%.

Within our study areas, the national Ministry of Health (MOH) survey of helminth prevalence from 2001-2004 included 356,629 individuals across China, and encompassed several studies by local Centers for Disease Control and Prevention (CDC), including in Guizhou Province (Coordinating Office of the National Survey on the Important Human Parasitic Diseases, 2005). The Guizhou Provincial CDC found an STH prevalence of 53.8% among 4091 primary and middle school students, 48.3% among 1748 children of preschool age (Wang et al., 2008). A more localized study in Guizhou found similar rates of 50.0% in 2007 among children aged 2-12 years in a rural, mountainous county in western Guizhou (Chen and Xia, 2010). These rates suggest that STH infections persist at high levels among the rural population in Guizhou Province.

If there is little research on the prevalence of STH infections in China, there is even less about recent efforts to control them. Ziegelbauer et al. (2010) looked at two schools in Yunnan Province: one underwent annual deworming treatment for several years, the other had no deworming treatment. They found a significant difference in the prevalence and intensity of infections between the two schools, but no significant difference in the self-rated quality of life or end-of-term grades among students with infections compared to students without infections. They did find that students infected with Ascaris had significantly lower measures of self-rated health. Besides the small sample size, one of the main drawbacks of the study was that the two sample schools were quite different. The school undergoing deworming was larger and located on the outskirts of a large city, while the other school was a small boarding school located in a remote rural area. These differences could lead to problems in identifying causality.

To our knowledge, there are no large statistical studies that have measured the correlates of the decision to seek deworming treatment.

The overall goals of this paper are to report on the relationship between deworming treatment and STH infection in rural China and to identify the individual and household characteristics correlated with the decision to deworm. To achieve these goals, we adopt a two-prong approach. First, we measure STH infection rates among school-aged children in rural Guizhou, measure reinfection rates among children who have been dewormed in the past, and analyze the effect of past deworming on current infection status. Next, we identify the factors associated with STH infection, reinfection, and participation in deworming activities, and compare the prevalence of STH infection rates and effectiveness of deworming activities between Han Chinese and ethnic minorities.

The rest of the paper is organized as follows. Section 2 describes the data and methodology. Section 3 documents the prevalence and intensity of STH infections, the deworming efforts and the subsequent reinfection status in rural Guizhou. Using multivariate analysis, we shed light on the effectiveness of deworming efforts, who chooses to deworm and what other factors are associated with infection and reinfection status. We also describe how the prevalence of STH infections, deworming, and reinfection rates differ between communities of Han Chinese and communities of ethnic minorities. Section 4 concludes.2. Data and Methods

2.1 Study Setting

This survey of impoverished children in rural settings was carried out in June and September of 2010 in Guizhou Province, located in Chinas Southwest region. Here, high rates of poverty and the humid climate are conducive to STH infection. Guizhou is demographically one of the most ethnically diverse provinces in China, with minority groups representing 35.7% of the total population (National Bureau of Statistics of China, 2012).

Six rural counties were randomly selected from the bottom quartile of counties based on average net per capita incomes (National Bureau of Statistics of China, 2010). The average net per capita income in the study areas is 433 US$/year.

2.2 Study Population, Sample Size and Sampling Strategy

We studied two groups of children, aged 3-5 years old and 8-10 years old. Each group differed with respect to socialization and exposure to school environments.

In each of the six selected counties, we ranked all towns according to net income per capita, and then randomly chose four towns: two with income per capita above the mean for the county and two with income per capita below the mean for the county. For each of the four chosen towns, two sample schools were chosen: the central primary school (which also serves as the local Bureau of Educations administrative representative for all educational affairs in the town) and a randomly selected primary school.

For each school, we obtained a list of all local villages that feed into the school. We ranked this list of villages by the number of 8-10 year old students (henceforth called school-aged children) enrolled at the school. We randomly selected two villages from the list (henceforth called sample villages) that had 16 or more students enrolled at the school. We then randomly chose 11 enrolled students from each sample village. In each sample school, a total of 22 students were surveyed.

Next, we went to the sample villages to conduct the sampling of the 3-5 year old children. We obtained a list of all the 3-5 year old children in each sample village from the Registry of Child Immunization (which is recorded and stored in the towns health center) and randomly chose 11 children from each of the sample villages (henceforth called preschool-aged children).

Our power calculations indicated that for our primary variable of interest, roundworm infection status, to estimate a 95% confidence interval with precision of 0.05 around a population prevalence of 40% and assuming a village-level intra-cluster correlation (ICC) of 0.15, we required 8 children in each age group per village. We increased this to 11 children to account for attrition.

In each sample village we randomly sampled 11 preschool-aged children and 11 school-aged children. This led to a total sample size of 844 pre-school aged children and 880 school-aged children (Table 1), for a total of 1,724 students in 48 schools and 94 villages. Because fecal samples were unattainable for some children, some sample villages had fewer than 22 observations with fecal samples. In no case were there fewer than 8 pre-school aged children and 8 school-aged children who provided samples. On average, there were 9.36 school-aged children per sample village and 8.98 preschool-aged children per sample village. This level of attrition is considered to be low in the existing literature (Steinmann et al., 2008; Xu et al., 2000; Zhou et al., 2004).

2.3 Data Collection and Survey

The primary variable of interest was stool parasite status of the selected child, whether positive or negative for any of three types of STH, as determined by a single stool sample. In addition, the intensity of every infection by egg density per gram was measured using WHO standard protocol (Montresor et al., 2002). Other variables and characteristics, such as household eating habits and sanitation information, were collected using a socio-economic survey instrument. The survey contained questions about age, gender, parental levels of education, health and sanitation behavior, household characteristics, and whether the child had taken anti-helminthic medication within the 18 month period prior to the survey. The school-aged children completed the survey themselves under the direct supervision of trained enumerators from the Chinese Academy of Sciences. The preschool-aged childrens data was obtained by trained enumerators who interviewed the childrens parents or caregivers.

Body height and weight were measured and recorded by trained nurses from Xian Jiaotong University according to WHO recommendations (de Onis et al., 2004). The children were measured in light clothing without shoes. Weight was measured with a calibrated electronic scale recommended by the medical department at Xian Jiaotong University. Body height was measured using a standard tape measure. The nursing team was trained to make sure the weighing station was set up on level ground to ensure accuracy of the equipment. Two nurses manned each measurement station, with one responsible for preparing subjects for measurement (removing shoes, offering instruction, reassuring parents, positioning children, etc.) and the other responsible for conducting and recording the actual measurements.

2.4 Stool Sample Collection and Laboratory Testing

Stool samples of each of the children included in the study were collected once and sent to the local county Center for Disease Control & Prevention (CDC). There was one lab per county, for a total of six labs. The majority of the samples were tested the same day that they were collected. Due to time and labor constraints, a small fraction of samples were tested the day after collection. These samples were stored overnight in the CDC laboratory refrigerator, which is kept at a constant 4 C. The Kato-Katz smear method was used for species-specific identification of parasite eggs: Ascaris, hookworm, and Trichuris. A single smear test was performed on each sample. Samples found to be positive for any of these three parasites underwent egg burden counts to determine eggs per gram (epg) of feces using standard WHO protocol. CDC employees at the county level examined the samples and performed the tests. As a quality control, ten percent of samples were also checked by a parasite expert from the National Institute for Parasitic Disease to verify the initial diagnosis.2.5 Ethical Considerations

This study was approved by the Stanford University Institutional Review Board (IRB) on May 18, 2010 and was assigned study protocol number 18780. The legal guardians (either parents or school principals) of all subjects provided informed oral consent and the children themselves provided oral assent. The IRB approves the use of oral consents in rural China to clarify understanding because many rural villagers are illiterate and it is culturally unusual to sign in writing. Our study enumerators recorded the consents on a list of names that is stored in a locked filing cabinet at the study center in Beijing, China.

Stool sampling falls within the regular purview of the Chinese Center for Disease Control & Prevention (CDC). CDC employees are professionally trained and perform routine stool sampling in the study areas as part of their national responsibilities. The stool sampling conducted as part of this study was approved and sanctioned by the national Chinese CDC as well as the regional and local CDCs in the sample province.

2.6 Data Management and Statistical Analysis

In order to better understand the relationship between deworming treatment and STH infection in rural China, we conduct a number of multivariate regression analyses. First, using a probit estimator (since our dependent variable is binary in natureinfected with STHs or not), we regress deworming history; household wealth measured by an asset index (following Wang et al., 2012); individual and household characteristics; and self-reported health and sanitation behavior on STH infection. The results of this analysis will help shed light on understanding whether deworming is effective for reducing STH infections among school-aged children in rural China, as well as what other factors are most strongly associated with STH infection.

Second, we focus on the subsample of children who have undergone deworming treatment in the past, and regress poverty level, individual and household characteristics, and health and sanitation behavior on reinfection with STHs. We define reinfection to include anyone who reported taking deworming medicine within the 18 month period prior to the survey and who tested positive for STH infection. The results of this regression will help us understand those behaviors and characteristics that are correlated with reinfection.

Finally, we regress poverty level, individual and household characteristics, and health and sanitation behavior on deworming history in order to identify factors associated with the household / individual decision to undergo deworming treatment.

3. Results

3.1 Summary Statistics

We collected data on a variety of individual and household characteristics, including age, gender, number of siblings, and parental education. In our sample, 45.1% of children were female and 54.9% were male, a ratio typical in most poor areas in China (National Bureau of Statistics of China, 2010). The average number of siblings is 1.6, which means that, on average, each family has two or three children. Only 31.8% of mothers and 48.7% of fathers have 9 years of education or more.

Health and sanitation habits include whether the children wash their hands before eating; whether the children wash their hands after using the toilet; whether the children consume undercooked or raw meat or vegetables; and whether the children drink un-boiled water. The results are discouraging. Only 54.4% of children reported that they wash their hands before eating, while just under half (49.3%) reported that they wash their hands after using the toilet. Although we do not have data on why hand washing behavior is so infrequent, our field visits and interviews suggest that one possible reason may be a lack of water near the toilet and cooking facilities; indeed, many families in our sample only have a single faucet in the courtyard of their homes, and no indoor plumbing. Our data also show that 20.3% of children reported consuming uncooked meat, while the rates for consumption of uncooked vegetables and un-boiled drinking water were as high as 75.0% and 85.3%.

Infection rates in the study sites are high. Overall, 37.5% of the sampled children were infected with one or more of the three types of STHs (Table 2). Infection rates with Ascaris were the highest and infection with hookworm was the lowest. Infection rates were higher in school-aged children (42.3%), and lower in preschool-aged children (32.6%), and these differences were statistically significant (p