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      Soil-Transmitted Helminths in Southwestern China: A Cross-Sectional Study of Links to Cognitive Ability, Nutrition, and School Performance among Children

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          Abstract

          Background

          Empirical evidence suggests that the prevalence of soil-transmitted helminth (STH) infections in remote and poor rural areas is still high among children, the most vulnerable to infection. There is concern that STH infections may detrimentally affect children’s healthy development, including their cognitive ability, nutritional status, and school performance. Medical studies have not yet identified the exact nature of the impact STH infections have on children. The objective of this study is to examine the relationship between STH infections and developmental outcomes among a primary school-aged population in rural China.

          Methodology/Principal Findings

          We conducted a large-scale survey in Guizhou province in southwest China in May 2013. A total of 2,179 children aged 9-11 years living in seven nationally-designated poverty counties in rural China served as our study sample. Overall, 42 percent of the sample’s elementary school-aged children were infected with one or more of the three types of STH— Ascaris lumbricoides (ascaris), Trichuris trichuria (whipworm) and the hookworms Ancylostoma duodenale or Necator americanus. After controlling for socioeconomic status, we observed that infection with one or more STHs is associated with worse cognitive ability, worse nutritional status, and worse school performance than no infection. This study also presents evidence that children with Trichuris infection, either infection with Trichuris only or co-infected with Trichuris and Ascaris, experience worse cognitive, nutritional and schooling outcomes than their uninfected peers or children infected with only Ascaris.

          Conclusions/Significance

          We find that STH infection still poses a significant health challenge among children living in poor, rural, ethnic areas of southwest China. Given the important linkages we find between STH infection and a number of important child health and educational outcomes, we believe that our results will contribute positively to the debate surrounding the recent Cochrane report.

          Author Summary

          Empirical evidence suggests that the prevalence of soil-transmitted helminth (STH) infections in remote and poor rural areas is still high among children, the most vulnerable to infection. There is concern that STH infections may detrimentally affect children’s healthy development, including their cognitive ability, nutritional status, and school performance. Medical studies have not yet identified the exact nature of the impact STH infections have on children. The objective of this study is to examine the relationship between STH infections and developmental outcomes among a primary school-aged population in rural China. We conducted a large-scale survey in Guizhou province in southwest China in May, 2013. Overall, 42 percent of elementary school-aged children were infected with one or more of the three types of STH— Ascaris lumbricoides (ascaris), Trichuris trichuria (whipworm) and the hookworms Ancylostoma duodenale or Necator americanus. After controlling for socioeconomic status, we observed that children infected with one or more STHs have worse cognitive ability, worse nutritional status, and worse school performance than their uninfected peers. While not causal, this study also presents evidence that children with Trichuris infection, either infection with Trichuris only or co-infected with Trichuris and Ascaris, have worse cognitive, nutritional and schooling outcomes than their uninfected peers or children infected with only Ascaris. Given these important linkages, we hope that our results will contribute positively to the debate surrounding the recent Cochrane report.

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          Most cited references9

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          Evidence for an association between hookworm infection and cognitive function in Indonesian school children.

          The association between helminth infection and cognitive and motor function was investigated in school-age children in Java, Indonesia. 432 children from 42 primary schools participated in the study. Children were stratified by age and sex into two age groups, 8-9 years and 11-13 years. Children infected with hookworm performed significantly worse than children without hookworm infection in 6 of the 14 cognitive or motor tests. After controlling for school (as a random effect) plus age, socio-economic status and parental education, sex, stunting (height-for-age 0.05). Tests associated with helminths represented various functions of working memory. No significant associations between helminth infection and motor function were observed that could not be explained by chance. The results suggest that hookworm infection can have a significant adverse effect on children's working memory which may have consequences for a child's reasoning ability and reading comprehension. Although the results are only associational, the fact that differences in cognition were observed at baseline imply that preventing infection with helminths in school-age children could be of benefit.
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            Hookworm, Ascaris lumbricoides infection and polyparasitism associated with poor cognitive performance in Brazilian schoolchildren.

            To investigate the relationship between hookworm and Ascaris lumbricoides infection and performance on three subsets of the Wechsler Intelligence Scale for Children - third edition (WISC-III) (Digit Span, Arithmetic and Coding) and Raven Colored Progressive Matrices. Cross-sectional study of 210 children between the ages of 6 and 11 years in Americaninhas, Minas Gerais, Brazil. Separate proportional odds models were used to measure the association between the intensity of helminth infections and poor performance on each of the four cognitive tests. After adjusting for sex, age, socioeconomic status and other helminth infections, moderate-to-high-intensity hookworm infection was associated with poor performance on the WISC-III Coding subtest [OR = 3.20; 95% confidence interval (CI) = 1.43-7.17], low intensity of hookworm infection was associated with poor performance on the WISC-III Coding subtest [odds ratio (OR) = 3.71; 95% CI = 1.80-7.66] and moderate-to-high-intensity A. lumbricoides infection was associated with poor performance on the Raven test (OR = 2.03; 95% CI = 1.04-3.99), all in comparison with uninfected children. Children co-infected with A. lumbricoides infection and hookworm infection had greater odds of poor performance on some WISC-III subtests than children with only A. lumbricoides infection. These findings suggest that hookworm infection may be associated with poorer concentration and information processing skills, as measured on the WISC-III Coding subtest, and that A. lumbricoides infection may be associated with poorer general intelligence, as measured through the Raven Colored Progressive Matrices. This study also presents evidence that polyparasitized children experience worse cognitive outcomes than children with only one helminth infection.
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              Parasite risk factors for stunting in grade 5 students in a community of extreme poverty in Peru.

              Malnutrition in school-age children is common in developing countries and includes both stunting and underweight. Stunting, which represents a chronic state of nutritional stress, leads to adverse health, educational and cognitive effects. Although much research is focused on preschool-age children, recent studies show both the high prevalence of stunting and the effectiveness of interventions in school-age children. The objectives of the current study were to determine the risk factors for stunting only, and stunting and underweight. A survey was conducted in 1074 grade 5 children (mean age 10 years) from 17 schools in Belen, Peru, a community of extreme poverty. Prevalence of underweight and stunting were 10.5 and 34.5%, respectively, co-prevalence was 9.3%. Based on multivariable logistic regression analyses, significant independent risk factors (odds ratio: OR) for stunting and underweight were: age (per 1 year increment) (OR=1.55; 95% confidence interval (CI): 1.33, 1.81); diarrhoea in the last week (OR=1.96; 95% CI: 1.17, 3.29) and hookworm infection (OR=1.74; 95% CI: 1.05, 2.86). Significant independent risk factors for stunting only were: age (per 1 year increment) (OR=1.51; 95% CI: 1.35, 1.70); anaemia (OR=1.98; 95% CI: 1.26, 3.11); and moderate and heavy Trichuris and Ascaris co-infection (OR=1.95; 95% CI: 1.35, 2.82). Our results indicate a high prevalence of stunting, in addition to other adverse health indicators, in the study population. Due to the interrelation between many of these health and nutrition problems, interventions at both the school and community levels, including de-worming, feeding programs and health and hygiene education, are needed to reduce malnutrition in this and other similar populations living in conditions of extreme poverty.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                PLoS Negl Trop Dis
                plos
                plosntds
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, CA USA )
                1935-2727
                1935-2735
                25 June 2015
                June 2015
                : 9
                : 6
                : e0003877
                Affiliations
                [1 ]Center for Chinese Agricultural Policy, Institute of Geographical Sciences and Natural Resource Research, Chinese Academy of Sciences, Beijing, China
                [2 ]University of Chinese Academy of Sciences, Beijing, China
                [3 ]Freeman Spogli Institute, Stanford University, Stanford, California, United States of America
                [4 ]Stanford University School of Medicine, Stanford, California, United States of America
                [5 ]National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, Shanghai, China
                Australian National University, AUSTRALIA
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: CL RL HY LZ AM SR. Performed the experiments: CL RL HY LZ SL YB GW JW. Analyzed the data: CL RL AM LZ SR SS. Contributed reagents/materials/analysis tools: CL RL GW JW SR LZ. Wrote the paper: CL AM SR SS LZ RL GW.

                Article
                PNTD-D-14-01401
                10.1371/journal.pntd.0003877
                4481344
                26110518
                7b2b37d3-f15c-440c-a278-e361f4af51f0
                Copyright @ 2015

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited

                History
                : 14 August 2014
                : 5 June 2015
                Page count
                Figures: 2, Tables: 3, Pages: 16
                Funding
                The authors acknowledge financial support from the National Natural Science Foundation of China (grant numbers 71473240, 71333012, 71103171 and 71473239), the International Initiative for Impact Evaluation (3IE, grant number PW2.04.02.02), the UBS Optimus Foundation, and the Stanford University Global Underdevelopment Action Fund. We also thank Eric Hemel, Barbara Morgen, and Karen Eggleston for their continued support. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Custom metadata
                Public availability of data would compromise patient privacy. Data are available to researchers who meet the criteria for access to confidential data from the ethics committees of the Institutional Review Board at Stanford University in Stanford, California as well as the Institutional Review Board at Sichuan University in Chengdu, China. Contact of the IRB committee at Stanford University: Elizabeth Sze, esze@ 123456stanford.edu . Contact of the IRB committee at Sichuan University: Liu Min, scdxyxll@ 123456163.com .

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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