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