Among 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 Findings
In 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.
Our 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.
Obtaining schistosome infection data from thousands of humans and mammalian hosts in the Philippines, Steven Riley and colleagues find that mammalian acquisition, rather than transmission to snails, drives prevalence.
Parasitic worms called schistosomes infect about 200 million people worldwide. Different schistosome species are common in different parts of the world. Schistosoma japonicum, for example, is restricted to the Pacific region. In the Philippines, 6.7 million people live in areas where this parasite is endemic (constantly present). S. japonicum has a complex life cycle that starts with the parasite reproducing in freshwater snails. Free-swimming infectious parasites emerge from the snails and which burrow into the skin of people and other mammals (most schistosome species infect only people) when they swim in infected water. The parasites migrate to the veins draining the gut, where they mature into adult worms, mate, and lay eggs, some of which pass into the feces and back into the water where they hatch and infect fresh snails. Infection with S. japonicum does not kill many people but it causes serious health problems, including liver, lung, and gut damage.
Why Was This Study Done?
Schistosome infections can be cured with inexpensive drugs, but people living in endemic countries usually become reinfected. The only way to avoid this problem is to eliminate the parasite in the environment, but to do so the relative contributions of snails, people, and other mammals to the transmission cycle need to be understood. Villages in the Philippines have very different levels of infection with S. japonicum. This variation suggests that the location of snail colonies and water courses and the behavior of the parasite's mammalian hosts (for example, their contact with water and their sanitary habits) affect the efficiency of S. japonicum transmission. Knowing which of these factors are the most important would help public-health officials instigate effective interventions to reduce infection rates. In this study, the researchers devise a mathematical model of S. japonicum transmission and use information on the number of people and other mammals infected in several villages in the Philippines to find out what drives inter-village variability in infection.
What Did the Researchers Do and Find?
The researchers counted schistosome eggs in human and nonhuman mammalian feces collected in 50 villages in the Philippines (about 11,500 samples in total) and used these counts to estimate the parameters (values such as the rate of transmission from snails to people) for an S. japonicum transmission model. They then asked whether the proportion of the human population infected with S. japonicum predicted by the model matched actual data on infection levels in the villages. When they assumed that the transmission parameters were the same in all the villages, the variation in the number of mammalian hosts in each village could not explain the observed variation among villages in human infection levels. The researchers, therefore, tested two slightly more complex models in which the underlying rate of transmission from snails to mammals or from mammals to snails varied between villages to reflect different environmental conditions in each village. The first of these models fitted the available data best and also showed that cats, dogs, pigs, and water buffalo were less susceptible to infection with S. japonicum than people but that rats were more susceptible.
What Do These Findings Mean?
These findings suggest that the snail-to-mammal side of the S. japonicum life cycle affects the inter-village variability in human schistosome infection more than the mammal-to-snail side. The findings also indicate that the contribution of water buffaloes to human S. japonicum infection in the Philippines is not particularly important. This contrasts with a recent study that identified water buffaloes as the major mammalian reservoir for S. japonicum in China. As with all mathematical models, the findings of this one depend on the assumptions made to build the model. Nevertheless, they suggest that interventions to reduce the size of the snail population and the exposure of mammals to parasite-containing water might reduce human infection levels more effectively than interventions that interrupt other parts of the parasite's life cycle. These results also suggest that further studies of the transmission of S. japonicum by water buffalo are needed before efforts are dedicated to treat or vaccinate water buffalo as a control measure against human S. japonicum infection.
Please access these Web sites via the online version of this summary at http://dx.doi.org/10.1371/journal.pmed.0050018.
The MedlinePlus encyclopedia has a page on schistosomiasis (in English and Spanish)
The US Centers for Disease Control and Prevention provides information for the public and professionals on schistosomiasis
The World Health Organization provides information on schistosomiasis and research into its control