Versteria mustelae (Gmelin, 1790)

Deplazes, Peter, Eichenberger, Ramon M. & Grimm, Felix, 2019, Wildlife-transmitted Taenia and Versteria cysticercosis and coenurosis in humans and other primates, International Journal for Parasitology: Parasites and Wildlife 9, pp. 342-358 : 348-349

2.2. Versteria mustelae and Versteria sp. cysticercosis

Versteria mustelae (new genus created by Nakao et al., 2013; syn. Taenia mustelae ) is an up to 10cm long tapeworm of mustelids with a wide range of rodents as intermediate hosts, bearing in the liver the rather small, ovoid, 0.4–2.0mm large cysticerci containing many calcerous bodies ( Freeman, 1956; Slais, 1973). In Europe, weasel ( Mustela sp. ), stone marten ( Martes foina ) and pine marten ( M. martes ), and in the USA American pine marten ( Martes americana ), ermine ( Mustela ermine ) and mink ( Neovison vison ) have been described as definitive hosts ( Lee et al., 2016, Hoberg et al., 1990). Between 1981 and 1987, V. mustelae was identified in 2.9% of 272 Martes zibellina in Southwestern Yakutia (Sibiria) (Sedalischev and Odnokurtsev, 2011).

A variety of rodents have been identified as intermediate hosts of V. mustelae in Europe and Asia. In eastern Switzerland, V. mustelae was fond in very low prevalences in 0.1% of 1276 A. sylvaticus , in 0.1% of 1211 M. glareolus , in 0.3% of 347 M. arvalis and in 0.4% of 250 M. agrestis, but neither in 411 A. flavicollis nor in 894 A. terrestris ( Schaerer, 1987) . In Zealand ( Denmark), 14 of 46 M. glareolus were infected with V. mustelae ( Tenora et al., 1991) , and this species was found in 9.3% of 172 M. glareolus trapped in rural forest habitats and in 0.4% of 231 animals from urban forests and parks but not in 41 and 129 A. flavicollis , respectively ( Al-Sabi et al., 2015). In this study, prevalences were determined by molecular analyses with considerably higher sensitivities as compared to morphological identification. Interestingly, the authors stated that “several poorly developed cysts without specific morphology were observed”. In Sweden, V. mustelae was diagnosed by PCR in 13% of 56 A. amphibius and in 14% of 187 M. agrestis from field habitats, and in 8.4% of 655 M. glareolus, but not in 79 A. flavicollis and 206 A. sylvaticus from forest habitats ( Miller et al., 2017). In Finland M. glareolus , M. rutilius , M. rufocanus , M. agrestis , M. oeconomus and A. flavicollis have been identified as intermediate hosts of V. mustelae (syn. Taenia tenuicollis ) ( Tenora et al., 1983). In South-Central Finland, cysts of V. mustelae were detected in 9% of 34 M. agrestis and in 27% of 117 C. glareolus in the liver in a habitat with Mustela nivalis and M. erminea as main definitive hosts ( Soveri et al., 2000).

In France (Jura), V. mustelae was more frequently observed in M. glareolus (24% of 349) than in Pitymys subterraneus (5% of 75), M. agrestis (9% of 47), M. arvalis (1% of 2520) and Apodemus sp. (1% of 230) ( Le Pesteur et al., 1992). In Spain, V. mustelae was reported in P. duodecimcostatus , P. lusitanicus , P. pyrenaicus , M. agrestis , M. arvalis , M. cabrerae and M. glareolus ( Feliu et al., 1997) . Ribas et al. (2009) documented the occurrence of T. tenuicollis (former syn. of V. mustelae , not to be confused with Cysticercus tenuicollis of T. hydatigena ) in 6.7–12.6% of 376 M. glareolus caught in northern Spain.

Genetic investigations revealed that a complex of species, genotypes and genetic lineages exist within the genus Versteria in North America ( Lee et al., 2016). The authors suggested the occurrence of a “western lineage” (present in Colorado, Oregon, and Idaho, and the Nordwest Territories (NWT) of Canada) and a “northern continental lineage” (presentin Wisconsin and the NWT), with sympatry in the NWT. This northern continental lineage clusters with V. mustelae from Eurasia ( Finland and Siberia). The western lineage responsible for fatal infections of an orangutan and a human patient (Case 2, Table 2) also infects muskrats ( Ondatra zibethicus ) in Idaho, USA, and the NWT.

So far, V. mustelae genetically related to the European isolates, have not been found in primates, including humans all over the northern hemisphere. On the other hand, in North America, a “zoonotic” lineage named Versteria sp. responsible for a fatal infection of an orangutan (Table 5) and in 2018 of infections in two human patients ( Table 3) seems to be genetically closely related, but distinct from V. mustelae . In this review we refer to this genotype as Versteria sp. or North American zoonotic V. mustelae variant as used by Goldberg et al., 2014; Lee et al., 2016. Furthermore, based on the description of a patient from Pennsylvania ( USA) with Hodgkin disease and an undefined helminthic infection ( Connor et al., 1976), Olson et al. (2003) published a 18S sequence (GenBank: AY193876) without significant homology to other sequences in the database at the time of publication. We reanalysed this sequence in 2019 and identified a homology of 95% with V. mustelae (GenBank: AB731633) of European origin. Moreover, we recently sequenced the corresponding 18S region obtained by molecular analysis of clinical material of a female patient from Atlantic Canada with a Versteria sp. infection (published by Barkati et al., 2018, Table 3), and detected a homology of 99.7% with the GenBank entry (AY193876) of the Pennsylvanian patient mentioned above. Therefore, we conclude that the patient originating from Pennsylvania ( USA) ( Connor et al., 1976) represents the first documented case of human Vesteria sp. cysticercosis (patient 1, Table 3).

Interestingly, North American V. mustelae isolates from Minnesota ( USA) and from Algonquin Park ( Canada) are capable of asexual multiplication in the intermediate host ( Freeman, 1956), however it is unclear whether V. mustelae or the zoonotic Versteria sp. have been investigated. This phenomenon is distinct from the budding multiplication of T. crassiceps , and could be responsible for the systemic and invasive infections in heavily immunocompromised human patients. However, further investigations with genetically defined isolates are needed to elucidate the fascinating biology of Versteria spp. Furthermore, based on the small, not fully developed Versteria sp. cysticerci in the liver in immunocompromised patients, this infection must be considered in the differential diagnosis of alveolar echinococcosis as proposed by Barkati et al. (2018).