Research Article: Population Genetics of Schistosoma japonicum within the Philippines Suggest High Levels of Transmission between Humans and Dogs

Date Published: November 25, 2008

Publisher: Public Library of Science

Author(s): James W. Rudge, Hélène Carabin, Ernesto Balolong, Veronica Tallo, Jaya Shrivastava, Da-Bing Lu, María-Gloria Basáñez, Remigio Olveda, Stephen T. McGarvey, Joanne P. Webster, Matty Knight

Abstract: BackgroundSchistosoma japonicum, which remains a major public health problem in the Philippines and mainland China, is the only schistosome species for which zoonotic transmission is considered important. While bovines are suspected as the main zoonotic reservoir in parts of China, the relative contributions of various non-human mammals to S. japonicum transmission in the Philippines remain to be determined. We examined the population genetics of S. japonicum in the Philippines in order to elucidate transmission patterns across host species and geographic areas.Methodology/Principal FindingsS. japonicum miracidia (hatched from eggs within fecal samples) from humans, dogs, pigs and rats, and cercariae shed from snail-intermediate hosts, were collected across two geographic areas of Samar Province. Individual isolates were then genotyped using seven multiplexed microsatellite loci. Wright’s FST values and phylogenetic trees calculated for parasite populations suggest a high frequency of parasite gene-flow across definitive host species, particularly between dogs and humans. Parasite genetic differentiation between areas was not evident at the definitive host level, possibly suggesting frequent import and export of infections between villages, although there was some evidence of geographic structuring at the snail–intermediate host level.Conclusions/SignificanceThese results suggest very high levels of transmission across host species, and indicate that the role of dogs should be considered when planning control programs. Furthermore, a regional approach to treatment programs is recommended where human migration is extensive.

Partial Text: Infection by the Asian blood fluke Schistosoma japonicum remains an important public health burden in the Philippines, China and parts of Indonesia, despite continued efforts of ongoing control programs [1]. In the Philippines alone, it has been estimated that approximately 6.7 million people live in areas endemic for S. japonicum[2]. S. japonicum is unique among the species of schistosomes infecting humans, in that it can infect more than 40 other species of mammalian hosts and is the only species for which zoonotic transmission is considered important [3]. Recent studies by our group in Samar, the Philippines, found high prevalence and intensities of S. japonicum infection in dogs and rodents [4], with intensities of infections in dogs at the village level found to be associated with the intensity of human infection [5]. Conversely, the same data used in a transmission dynamics model suggest that rats may play some role in human infection [6]. However, from such parasitological data alone it remains unclear which, if any, of these animals are most important as zoonotic reservoirs for human infection.

To our knowledge this work represents the first study of the population genetic structure of S. japonicum across host species and geographic areas within the Philippines. The lack of genetic differentiation observed between parasite isolates from different definitive host species suggests high levels of parasite gene-flow between host species, and thus also a high frequency of S. japonicum transmission across species, particularly between dogs and humans. Dogs could thus potentially be a very important zoonotic reservoir of S. japonicum in the province of Samar, Philippines, in contrast to marshland regions of China where parasite genotypes from humans have been demonstrated to cluster with bovines and away from other domesticated animals such as dogs, cats, pigs and goats [16].



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