Biology ETDs

Publication Date

7-1-2015

Abstract

Globally, digenetic trematodes called schistosomes (Family Schistosomatidae) have enormous public and veterinary health significance because they cause debilitating and chronic infections collectively called schistosomiasis. Schistosomes have a life cycle featuring a bird or mammal definitive host in which adult worms are found, and freshwater snail intermediate hosts in which larval stages are found and free-swimming cercariae are produced which infect the definitive host. Although schistosomes are known to be common in tropical and subtropical Asia, their presence in Nepal, a small south Asian country situated between India and China, was almost completely unknown at the beginning of this study. Consequently, from 2007-2014, we investigated the presence of schistosomes in and around Chitwan National Park (CNP) in the Terai and hilly regions of Nepal. We sampled both the dung of selected mammals for schistosome eggs, and screened 19,360 freshwater snails for cercariae of schistososmes. As reported in Chapter 2 and published in the Journal of Helminthology, because elephants are known hosts for schistosomes elsewhere, dung samples from both domestic and wild Indian elephants (Elephus maximus) were examined, and were found to be positive for eggs of the elephant schistosome Bivitellobilharzia nairi. Surprisingly, we also found similar eggs in dung samples of the endangered Asian or greater one-horned rhinoceros (Rhinoceros unicornis) from CNP. Subsequent study of cox1 and 28S DNA sequences obtained from eggs from both host species confirmed them to be those of B. nairi. This represents the first sequence-verified identification of an elephant schistosome from another mammal, the first sequence-verified report of a schistosome from any rhinoceros, and the only report indicating elephants and rhinos, even though unrelated, both transmit the same parasite in and around CNP in Nepal. Regarding the snails collected during our study, as reported in Chapter 3 and published in Parasitology International, only two snails were found to harbor avian schistosome cercariae. Phylogenetic analyses of both 28S rDNA and cox1 sequences showed that the cercaria recovered from the snail Radix luteola grouped in a distinctive and previously unknown lineage within Trichobilharzia, a genus well-known for causing dermatitis outbreaks elsewhere. The second schistosome cercaria recovered from the snail Indoplanorbis exustus clustered most closely with Macrobilharzia macrobilharzia, a schistosome with unknown snail host, although the Nepalese specimens seem to represent a distinct lineage. This is the first sequence-verified documentation of an avian schistosome reported from I. exustus, and the first report of any sequence-verified avian schistosomes from south Asia. Chapter 4 (accepted for publication in The International Journal for Parasitology) provides the first molecular evidence for the presence of the Schistosoma indicum species group in Nepal. Schistosomes of this group are of considerable veterinary importance and cause dermatitis or potentially even more advanced infections in people. Based on analysis of cox1, 12S, 16S and 28S genes, two recognizable lineages were found, S. spindale and S. nasale. Unexpectedly, we also found a third distinct lineage that was not S. indicum as predicted, but rather one that was previously uncharacterized and that failed to group with any known members of S. indicum group. This suggests the presence of a new species of the S. indicum group in Nepal. Analysis of cox1, 16S and ITS1 sequences for the snail host I. exustus was also surprising in revealing the presence of four genetically distinct clades of this snail in Nepal, providing further evidence that I. exustus is actually a complex of related species. This finding will stimulate a general reevaluation of the role of this snail species complex in disease transmission. In chapter 5 (in preparation for submission) we report that 16 of 2,588 specimens of Radix luteola from 4 different Nepalese habitats were found to be shedding mammalian schistosome cercariae. Based on 28S, cox1, 16S and 12S sequences analysis, these cercariae were found to be very similar to one another and to cluster with Schistosoma turkestanicum, although they were clearly genetically distinct from it. This study provides sequence-verification for a third lymnaeid-transmitted Schistosoma lineage in Asia, validates the existence of the S. turkestanicum species group, and reveals the presence of a distinct but unknown species of that group within Nepal. This study concludes that schistosomes, and by extension schistosomiasis, are common in Nepal: the Terai region of Nepal alone harbors at least five distinct species of mammalian schistosomes and two distinct species of avian schistosomes. Our study was limited to a small portion of Nepal so we recommend more extensive sampling from different areas of the country, which may yield even more surprising results. Further study is also required to examine the adult stages of Nepalese schistosomes though cultural and religious practices there make it difficult to get access to adult worms. These results also highlight that the Indian subcontinent in general needs much more additional study with respect to schistosome diversity and that our current knowledge of the schistosomes in this area is very poor. We need to remain mindful of the possibility that some of the schistosomes present may be able to infect humans in some locations.

Language

English

Keywords

Elephant schistosomes, Bivitellobilharzia nairi, schistosomiasis, avian schistosomes, hostΓÇôparasite relationships, cercarial dermatitis, Nepal, Schistosoma indicum group, Indoplanorbis exustus, host switch, mammalian schistosomes, Schistosoma dattai, Schistosoma bomfordi, Radix luteola

Document Type

Dissertation

Degree Name

Biology

Level of Degree

Doctoral

Department Name

UNM Biology Department

First Advisor

Loker, Eric

First Committee Member (Chair)

Brant, Sara

Second Committee Member

Adema, Coenraad

Third Committee Member

Snell, Howard

Fourth Committee Member

DeJong, Randall

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