Research Article: Multi-Host Transmission Dynamics of Schistosoma japonicum in Samar Province, the Philippines

Date Published: January 22, 2008

Publisher: Public Library of Science

Author(s): Steven Riley, Hélène Carabin, Patrick Bélisle, Lawrence Joseph, Veronica Tallo, Ernesto Balolong, A. Lee Willingham, Tomas J Fernandez, Ryan O’Neal Gonzales, Remigio Olveda, Stephen T McGarvey, Charles H King

Abstract: BackgroundAmong the 6.7 million people living in areas of the Philippines where infection with Schistosoma japonicum is considered endemic, even within small geographical areas levels of infection vary considerably. In general, the ecological drivers of this variability are not well described. Unlike other schistosomes, S. japonicum is known to infect several mammalian hosts. However, the relative contribution of different hosts to the transmission cycle is not well understood. Here, we characterize the transmission dynamics of S. japonicum using data from an extensive field study and a mathematical transmission model.Methods and FindingsIn this study, stool samples were obtained from 5,623 humans and 5,899 potential nonhuman mammalian hosts in 50 villages in the Province of Samar, the Philippines. These data, with variable numbers of samples per individual, were adjusted for known specificities and sensitivities of the measurement techniques before being used to estimate the parameters of a mathematical transmission model, under the assumption that the dynamic transmission processes of infection and recovery were in a steady state in each village. The model was structured to allow variable rates of transmission from different mammals (humans, dogs, cats, pigs, domesticated water buffalo, and rats) to snails and from snails to mammals. First, we held transmission parameters constant for all villages and found that no combination of mammalian population size and prevalence of infectivity could explain the observed variability in prevalence of infection between villages. We then allowed either the underlying rate of transmission (a) from snails to mammals or (b) from mammals to snails to vary by village. Our data provided substantially more support for model structure (a) than for model structure (b). Fitted values for the village-level transmission intensity from snails to mammals appeared to be strongly spatially correlated, which is consistent with results from descriptive hierarchical analyses.ConclusionsOur results suggest that the process of acquiring mammalian S. japonicum infection is more important in explaining differences in prevalence of infection between villages than the process of snails becoming infected. Also, the contribution from water buffaloes to human S. japonicum infection in the Philippines is less important than has been recently observed for bovines in China. These findings have implications for the prioritization of mitigating interventions against S. japonicum transmission.

Partial Text: Modern, inexpensive pharmaceuticals are dramatically reducing the burden of disease caused by schistosomes and other waterborne macroparasites in resource-poor settings [1,2]. Many of the national programs delivering these anthelmintics are motivated and funded by large international aid initiatives. Given the high efficacy of the drugs and the increasingly recognized burden of morbidity and mortality imposed by these infections on the affected populations, such initiatives can be expected to represent good use of the large funds currently being made available by charities and governments for the control of neglected tropical diseases. However, even though some drugs such as praziquantel and albendazole are currently free or nearly free up to the point of importation into countries of use, their continued widespread distribution cannot be considered sustainable until such programs are independently prioritized by the health care systems of the populations that require them [3]. In addition, the mass delivery of such treatments is sometimes difficult. For example, during our project in 2004 in Samar province, the Philippines, only 49% of the population presented themselves for treatment with praziquantel, despite the treatment being provided free of charge. Given numerous competing local development objectives, it may be many years until countries such as the Philippines choose to prioritize the procurement and distribution of praziquantel in order to reduce the morbidity and mortality associated with Schistosoma japonicum infection.

Initially, we assumed that there was no difference between the underlying transmission parameters in each village, i.e., for hypothesis H0 (Table 1), βMS(j) = βMS(k) and βSM(j) = βSM(k) for j,k ∈ 1…49. Therefore, the only source of variation in transmission was the different numbers of hosts of each species in each village. This model variant was not flexible enough to reproduce the observed variation in the data adjusted for measurement error (Figure 2). For each village, for a given class of infection prevalence, the values were very similar. This result suggests that it is not the distribution of potential mammalian reservoir and humans hosts in each village that drives the village-to-village variation in transmission. For example, there is no strong trend of increased infection in humans in those villages with a greater number of water buffaloes: this result is consistent with previous analyses based on a nonmechanistic model of these data [8].

We have used a simple transmission model to show that it is unlikely that variation in numbers of mammalian hosts is the main cause of variation in human S. japonicum infection in Samar, the Philippines. Inference using two slightly more complex model structures supports the hypothesis that site-specific variation in the underlying rate of transmission from snails to mammals is more important than site-specific variation in the underlying rate of transmission from mammals to snails. This result confirms and extends results from similar studies in China [18] in that a village-specific index of transmission seems likely to be driven more by one side of the parasite life cycle (the transmission from snails to mammals) than the other (the transmission from mammals to snails). Also, variation in the estimated rate of transmission from snails to mammals appears to be geographically clustered. Our results suggest that neither water buffaloes nor dogs contribute substantially to variation in infection rates, but that rats may be important.



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