Plagiorchis sp. in small mammals of Senegal and the potential emergence of a zoonotic trematodiasis.

Stefano Catalano,Simon L Priestnall,Mariama Sène,Cheikh B Fall,Khalilou Bâ,Joanne P Webster,Nicolas D Diouf,Steven A Nadler,Kirsty J Marsh,Elsa Léger,Chelsea L Wood

doi:10.1016/j.ijppaw.2019.02.003

Abstract

Trematodes of the genus Plagiorchis have a wide geographical distribution and can exploit a variety of hosts. The occurrence and zoonotic potential of Plagiorchis spp. have been characterised across several countries in Asia; in contrast, information on Plagiorchis parasites in Africa remains anecdotal. We isolated a previously undescribed Plagiorchis species from the biliary tract and small intestine of 201 out of 427 small mammals collected in the region of Lake Guiers, Senegal, with local prevalence ranging from 38.6% to 77.0%. Conversely, Plagiorchis isolates were not observed in the 244 small mammals sampled in and around the town of Richard Toll, Senegal. Molecular phylogenetics of the internal transcribed spacer region, nuclear ribosomal DNA, and of the cytochrome c oxidase subunit 1 gene, mitochondrial DNA, supported the monophyly and multi-host spectrum of this newly discovered West African Plagiorchis species. Sequencing of individual cercariae shed by Radix natalensis (Gastropoda: Lymnaeidae) suggested that these freshwater snails may act as suitable first intermediate hosts. Phylogenetic analysis yielded a highly resolved topology indicating two different clades, one composed by Plagiorchis spp. infecting rodents, insectivores, and birds, while the other included parasites of bats. Our findings showed the low host specificity and high prevalence of the isolated Plagiorchis sp. in the Lake Guiers region, with Hubert's multimammate mice (Mastomys huberti) appearing to play a primary role in the epidemiology of this parasite. The results raise concern about the zoonotic potential of Plagiorchis sp. in local communities of the Lake Guiers region, and highlight food-borne trematodiases and their link to land-use change as a neglected public health issue in regions of West Africa.

Highlights

Trematodes of the genus Plagiorchis have a heteroxenous life cycle involving freshwater pulmonate gastropods of the family Lymnaeidae as first intermediate hosts and mosquito and chironomid larvae, insect naiads, freshwater fish, and crustaceans as second intermediate hosts (Guk et al, 2007; Boyce et al, 2014; Soldánová et al, 2017)
We conducted our study in and around the town of Richard Toll and on the shores of Lake Guiers, Senegal. This region has experienced major infrastructure development and land-use change that have generated a rapid agroindustrial growth while dramatically altering the ecology of the territory (Uhlir, 2003). These anthropogenic changes have been associated with outbreaks of schistosomiasis disease, which is currently endemic in the Senegal River Basin and for which wild rodents may act as local reservoirs (Duplantier and Sène, 2000; Catalano et al, 2018)
Sequencing of the internal transcribed spacer (ITS) region proved to be useful for characterising Plagiorchis spp. (Tkach et al, 2000; Boyce et al, 2014), while the simultaneous examination of ribosomal DNA (rDNA) and mitochondrial DNA (mtDNA) loci is suitable for molecular prospecting and further hypothesis testing on species delimitation (Nadler and Pérez-Ponce de León, 2011)

Summary

Introduction

Trematodes of the genus Plagiorchis have a heteroxenous life cycle involving freshwater pulmonate gastropods of the family Lymnaeidae as first intermediate hosts and mosquito and chironomid larvae, insect naiads, freshwater fish, and crustaceans as second intermediate hosts (Guk et al, 2007; Boyce et al, 2014; Soldánová et al, 2017). Plagiorchis spp. are cosmopolitan, their vast distribution spanning from boreal to tropical zones around the globe. Their wide geographic range may be a consequence of their relatively low host specificity, with records of adult parasites of the genus Plagiorchis from the small intestine of a variety of definitive hosts, including reptiles, birds, and mammals (Guk et al, 2007; Boyce et al, 2014). Further findings of P. harinasutai, P. philippinensis, and P. javensis seem sporadic and localised in the same countries where these Plagiorchis spp. were first described, with few human cases and one report on P. harinasutai infecting rodents in the Republic of the Philippines (Radomyos et al, 1998; Eduardo and Lee, 2006). The taxonomic validity of these records may be questionable since the identification of Plagiorchis isolates was based solely on morphological traits, which lack diagnostic accuracy due to their high intra-specific variability (e.g., Brendow, 1970; Tkach et al, 2000; Boyce et al, 2014; Zikmundová et al, 2014)

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