Identifying host species driving transmission of schistosomiasis japonica, a multihost parasite system, in China

Abstract

Understanding disease transmission dynamics in multihost parasite systems is a research priority for control and potential elimination of many infectious diseases. In China, despite decades of multifaceted control efforts against schistosomiasis, the indirectly transmitted helminth Schistosoma japonicum remains endemic, partly because of the presence of zoonotic reservoirs. We used mathematical modeling and conceptual frameworks of multihost transmission ecology to assess the relative importance of various definitive host species for S. japonicum transmission in contrasting hilly and marshland areas of China. We examine whether directing control interventions against zoonotic reservoirs could further reduce incidence of infection in humans or even eliminate transmission. Results suggest that, under current control programs, infections in humans result from spillover of transmission among zoonotic reservoirs. Estimates of the basic reproduction number within each species suggest that bovines (water buffalo and cattle) maintained transmission in the marshland area and that the recent removal of bovines from this area could achieve local elimination of transmission. However, the sole use of antifecundity S. japonicum vaccines for bovines, at least at current efficacies, may not achieve elimination in areas of comparable endemicity where removal of bovines is not a feasible option. The results also suggest that rodents drive transmission in the hilly area. Therefore, although targeting bovines could further reduce and potentially interrupt transmission in marshland regions of China, elimination of S. japonicum could prove more challenging in areas where rodents might maintain transmission. In conclusion, we show how mathematical modeling can give important insights into multihost transmission of indirectly transmitted pathogens.

Why infectious disease research needs community ecology

“…For example, Rudge et al . (10) quantified host species contributions to the number of cases generated ( R 0 ) of S. japonicum in China, for which more than 120 host species have been identified. They showed that bovids maintain infection in marshlands, whereas rodents are the main source of transmission in hilly areas, which suggests that different control strategies are needed in the two habitats.…”

“…1), such that treating animals to reduce their worm burdens improves individual survival but, by enabling infected hosts to live longer, is predicted to increase population-level spread of bTB (63). Reciprocally, variation in host community composition within a region can affect infection risk and spread at the individual and population levels (10, 55). For vector-borne infections such as Lyme disease, wildlife species vary considerably in their tendency to amplify the bacterium responsible and transmit it to suitable tick vectors, such that regional variation in host species diversity is hypothesized to be a major determinant of local infection risk for humans (65) (Box 1).…”

“…Simple extensions of basic disease ecology theory can determine the conditions under which one host species amplifies or dilutes infection risk for other species in the community. For directly transmitted parasites, or even those transmitted via infective stages in the environment, theory shows that the parasite's overall basic reproductive number among the available host community ( R 0,TOT ) can simply be proportional to the sum of the R 0 for each host species alone, provided there is equal mixing within and between host species (although other relationships between the individual-level and community-level R 0 values may occur if mixing is not equal) (10, 102). Hence, there is a clear connection between this more complex scenario and the classical single-host theory.…”

“…1). The use of multiple hosts by parasites complicates control efforts that target particular hosts for management; for example, Schistosoma japonicum , the primary cause of human schistosomiasis in Asia, can infect 120 different species of mammals (10). Similarly, more than 20 species of triatomine bugs can transmit Trypanosoma cruzi , which causes Chagas disease in South America, such that efforts to control the dominant vector species alone may be inadequate to achieve elimination (11).…”

Who acquires infection from whom and how? Disentangling multi-host and multi-mode transmission dynamics in the ‘elimination’ era

“…vaccine stockpiling.[113]molecular techniques such as whole genome sequencing can for some diseases be used to trace transmission events.[114]7. which transmission pathway or group is driving transmission, and therefore where should interventions be targeted?mathematical models of disease dynamics, informed by many of the above forms of study, can be used to identify key and maintenance hosts, and also to predict the impact of interventions.[6,10,115–117]…”