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      The Synergistic Effect of Concomitant Schistosomiasis, Hookworm, and Trichuris Infections on Children's Anemia Burden

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          Abstract

          Objective

          To estimate the degree of synergism between helminth species in their combined effects on anemia.

          Methods

          Quantitative egg counts using the Kato–Katz method were determined for Ascaris lumbricoides, hookworm, Trichuris trichiura, and Schistosoma japonicum in 507 school-age children from helminth-endemic villages in The Philippines. Infection intensity was defined in three categories: uninfected, low, or moderate/high (M+). Anemia was defined as hemoglobin <11 g/dL. Logistic regression models were used to estimate odds ratios (OR), 95% confidence intervals (CI), and synergy index for pairs of concurrent infections.

          Results

          M+ co-infection of hookworm and S. japonicum (OR = 13.2, 95% CI: 3.82–45.5) and of hookworm and T. trichiura (OR = 5.34, 95% CI: 1.76–16.2) were associated with higher odds of anemia relative to children without respective M+ co-infections. For co-infections of hookworm and S. japonicum and of T. trichiura and hookworm, the estimated indices of synergy were 2.9 (95% CI: 1.1–4.6) and 1.4 (95% CI: 0.9–2.0), respectively.

          Conclusion

          Co-infections of hookworm and either S. japonicum or T. trichiura were associated with higher levels of anemia than would be expected if the effects of these species had only independent effects on anemia. This suggests that integrated anti-helminthic treatment programs with simultaneous deworming for S. japonicum and some geohelminths could yield a greater than additive benefit for reducing anemia in helminth-endemic regions.

          Author Summary

          Polyparasitic infections have been recognized as the norm in many tropical developing countries, but the significance of this phenomenon for helminth-associated morbidities is largely unexplored. Earlier studies have suggested that multi-species, low-intensity parasitic infections were associated with higher odds of anemia among school-age children relative to their uninfected counterparts or those with one low-intensity infection. However, specific studies of the nature of interactions between helminth species in the mediation of helminth-associated morbidities are lacking. This study quantifies the extent to which polyparasitic infections have more than the sum of adverse effects associated with individual infections in the context of childhood anemia. This study found that the risk of anemia is amplified beyond the sum of risks for individual infections in children simultaneously exposed to 1) hookworm and schistosomiasis, and 2) hookworm and trichuris, and suggests that combined treatment for some geohelminth species and schistosomiasis could yield greater than additive benefits for the reduction of childhood anemia in helminth-endemic areas. However, more studies to understand the full range of interactions between parasitic species in their joint effects on helminth-associated morbidities will be necessary to better predict the impact of any future public health intervention.

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          Most cited references98

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          Estimating wealth effects without expenditure data--or tears: an application to educational enrollments in states of India.

          Using data from India, we estimate the relationship between household wealth and children's school enrollment. We proxy wealth by constructing a linear index from asset ownership indicators, using principal-components analysis to derive weights. In Indian data this index is robust to the assets included, and produces internally coherent results. State-level results correspond well to independent data on per capita output and poverty. To validate the method and to show that the asset index predicts enrollments as accurately as expenditures, or more so, we use data sets from Indonesia, Pakistan, and Nepal that contain information on both expenditures and assets. The results show large, variable wealth gaps in children's enrollment across Indian states. On average a "rich" child is 31 percentage points more likely to be enrolled than a "poor" child, but this gap varies from only 4.6 percentage points in Kerala to 38.2 in Uttar Pradesh and 42.6 in Bihar.
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            Modern epidemiology

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              Modern Epidemiology

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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                plos
                plosntds
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, USA )
                1935-2727
                1935-2735
                June 2008
                4 June 2008
                : 2
                : 6
                : e245
                Affiliations
                [1 ]Department of Community Health and International Health Institute, Brown University Providence, Rhode Island, United States of America
                [2 ]Health Effects Institute, Boston, Massachusetts, United States of America
                [3 ]Department of Immunology, Research Institute of Tropical Medicine, Manila, The Philippines
                [4 ]Department of Community Health, Brown University, Providence, Rhode Island, United States of America
                [5 ]Department of Pathogenic Biology, Nanjing Medical University, Nanjing, Jiangsu, China
                [6 ]Center for International Health Research, Rhode Island Hospital, Providence, Rhode Island, United States of America
                [7 ]Department of Pathology and Laboratory Medicine, Brown University Medical School, Providence, Rhode Island, United States of America
                [8 ]Department of Pediatrics, Brown University, Providence, Rhode Island, United States of America
                London School of Hygiene & Tropical Medicine, United Kingdom
                Author notes

                Conceived and designed the experiments: AE DM HW JK JF. Performed the experiments: AE DM HW JF. Analyzed the data: AE. Contributed reagents/materials/analysis tools: AE SM JK VM JF. Wrote the paper: AE SM LA SZ JK VM RO JF. Critiqued drafts of the manuscript: DM RO. Provided substantive contribution regarding the definition of interaction terms, and reviewed, refined, and approved manuscript drafts: SZ.

                Article
                07-PNTD-RA-0011R3s
                10.1371/journal.pntd.0000245
                2390851
                18523547
                ade982f8-57c9-4017-b548-b1cec5799b6b
                Ezeamama et al. 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
                : 6 February 2007
                : 8 May 2008
                Page count
                Pages: 9
                Categories
                Research Article
                Public Health and Epidemiology
                Public Health and Epidemiology/Environmental Health
                Public Health and Epidemiology/Global Health
                Public Health and Epidemiology/Infectious Diseases

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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