Research Article: The Synergistic Effect of Concomitant Schistosomiasis, Hookworm, and Trichuris Infections on Children’s Anemia Burden

Date Published: June 4, 2008

Publisher: Public Library of Science

Author(s): Amara E. Ezeamama, Stephen T. McGarvey, Luz P. Acosta, Sally Zierler, Daria L. Manalo, Hai-Wei Wu, Jonathan D. Kurtis, Vincent Mor, Remigio M. Olveda, Jennifer F. Friedman, Simon Brooker

Abstract: ObjectiveTo estimate the degree of synergism between helminth species in their combined effects on anemia.MethodsQuantitative 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.ResultsM+ 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.ConclusionCo-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.

Partial Text: The high prevalence of polyparasitic infections of geohelminth and schistosomiasis infections has received considerable attention in epidemiologic literature [1],[2],[3],[4],[5],[6],[7]. This profile of infection is now recognized to be the norm for many residents of parasite endemic regions [3],[5],[6],[7],[8],[9]. There are few human studies of the morbidity implications of polyparasitism, which may elicit a range of biologic interactions between the host’s immune system and the invading parasites [10]. One possible form of interaction is synergism, which implies that the adverse health effect associated with multiple species infection is greater than the sum of adverse effects for individual species. This has been observed in mice co-infected with Trichinella spiralis and Heligmosomoides polygyrus[11]. The generalizability of observations from murine systems to human populations is unknown. Understanding the morbidity implications of polyparasitism, including any evidence of synergism between helminths in their cumulative health impacts, could provide valuable information for healthcare providers in many developing countries who must decide how aggressively to screen and treat children for polyparasitism in their resource limited settings.

Prevalent malnutrition and anemia in the study sample were 87.1% and 19.9% respectively. The prevalence of infection by individual helminth species in this sample ranged from a low of 55% for hookworm to a high of 93% for trichuris. Only 0.7% of the sample was free of infection by all four parasitic species. 7.4% and 14.3% of children were infected by only one and two helminth species respectively while the majority of the sample (77.6%) were infected by 3 or 4 parasites concurrently (data not shown). Only seven children were simultaneously uninfected by hookworm, S. japonicum and trichuris in the analytic sample; all seven children were free of anemia. Among the subset of children uninfected by S. japonicum and who were either free, or at most had a low infection, of both hookworm and trichuris (N = 50), the prevalence of anemia was 8% (data not shown). Relative to the reference in each exposure category, anemia was higher among children concurrently infected by any two species regardless of whether co-infection occurred at low or M+ intensity (Table 1). Anemia was highest among children with M+ intensity hookworm or S. japonicum infection, especially when these infections were contemporaneous with one another or trichuris. These trends are reinforced in bivariate analyses.

Despite the reported high prevalence of polyparasitic helminth infections [3],[5],[6],[7],[8],[9], little is known about how these contemporaneous infections interact biologically and influence morbidity. We have examined interactions, at moderate or high intensity, for concomitant infections of three pairs of helminth infections: hookworm and S. japonicum, hookworm and trichuris, S. japonicum and trichuris. Our results suggest the presence of synergistic interactions for the following pairs of helminths: 1) hookworm and S. japonicum, and 2) hookworm and trichuris. Among children co-infected with hookworm and S. japonicum, an estimated 60% of the anemia is attributable to the biologic interaction between them. Similarly, with M+ co-infection of hookworm and trichuris, an estimated 22% of the observed odds of anemia were attributable to the synergistic interaction between these species. We found no evidence of departure from additive risk model additivity for co-infection of trichuris and S. japonicum. Also found, though not expected, was the protective association between M+ ascaris infection and anemia.



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