Versteria mustelae (Gmelin, 1790)
publication ID |
https://doi.org/ 10.1016/j.ijppaw.2019.03.013 |
persistent identifier |
https://treatment.plazi.org/id/03BD87BA-FFBA-FFA7-4112-413DFE37ED80 |
treatment provided by |
Felipe (2024-08-02 16:44:13, last updated 2024-08-03 07:17:26) |
scientific name |
Versteria mustelae |
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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 View in CoL ) and pine marten ( M. martes View in CoL ), and in the USA American pine marten ( Martes americana View in CoL ), ermine ( Mustela ermine ) and mink ( Neovison vison View in CoL ) 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 View in CoL 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 View in CoL , in 0.1% of 1211 M. glareolus , in 0.3% of 347 M. View in CoL arvalis and in 0.4% of 250 M. View in CoL agrestis, but neither in 411 A. flavicollis View in CoL nor in 894 A. terrestris ( Schaerer, 1987) View in CoL . 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 View in CoL , 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. View in CoL agrestis from field habitats, and in 8.4% of 655 M. glareolus, but not in 79 A. flavicollis View in CoL and 206 A. sylvaticus View in CoL from forest habitats ( Miller et al., 2017). In Finland M. glareolus , M. rutilius , M. rufocanus , M. agrestis View in CoL , M. oeconomus and A. flavicollis View in CoL 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. View in CoL agrestis and in 27% of 117 C. glareolus in the liver in a habitat with Mustela nivalis View in CoL and M. erminea View in CoL 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).
Al-Sabi, M. N. S., Jensen, P. M., Christensen, M. U., Kapel, C. M. O., 2015. Morphological and molecular analyses of larval taeniid species in small mammals from contrasting habitats in Denmark. J. Helminthol. 89, 112 - 117.
Barkati, S., Gottstein, B., Muller, N., Sheitoyan-Pesant, C., Metrakos, P., Chen, T., Garceau, R., Libman, M. D., Ndao, M., Yansouni, C. P., 2018. First human case of metacestode infection caused by Versteria sp. in a kidney transplant recipient. Clin. Infect. Dis. 68, 680 - 683.
Connor, D. H., Sparks, A. K., Strano, A. J., Neafie, R. C., Juvelier, B., 1976. Disseminated parasitosis in an immunosuppressed patient: possibly a mutated sparganum. Arch. Pathol. Lab Med. 100, 65 - 68.
Feliu, C., Renaud, F., Catzeflis, F., Hugot, J. - P., Durand, P., Morand, S., 1997. A comparative analysis of parasite species richness of Iberian rodents. Parasitology 115, 453 - 466.
Freeman, R. S., 1956. Life history studies on Taenia mustelae Gmelin, 1790, and the taxonomy of certain taenioid cestodes from mustelidae. Can. J. Zool. 34, 219 - 242.
Goldberg, T. L., Gendron-Fitzpatrick, A., Deering, K. M., Wallace, R. S., Clyde, V. L., Lauck, M., 2014. Fatal metacestode infection in Bornean orangutan caused by unknown Versteria species. Emerg. Infect. Dis. 20, 109 - 113.
Le Pesteur, M. H., Giraudoux, P., Delattre, P., Damange, J. P., Quere, J. P., 1992. Spatiotemporal distribution of four species of cestodes in a landscape of mid-altitude mountains (Jura, France). Ann. Parasitol. Hum. Comp. 67, 155 - 160.
Lee, L. M., Wallace, R. S., Clyde, V. L., Gendron-Fitzpatrick, A., Sibley, S. D., Stuchin, M., Lauck, M., O'Connor, D. H., Nakao, M., Lavikainen, A., Hoberg, E. P., Goldberg, T. L., 2016. Definitive hosts of Versteria tapeworms (Cestoda: Taeniidae) causing fatal infection in North America. Emerg. Infect. Dis. 22, 707 - 710.
Miller, A. L., Olsson, G. E., Sollenberg, S., Walburg, M. R., Skarin, M., Hoglund, J., 2017. Transmission ecology of taeniid larval cestodes in rodents in Sweden, a low endemic area for Echinococcus multilocularis. Parasitology 144, 1041 - 1051.
Nakao, M., Lavikainen, A., Iwaki, T., Haukisalmi, V., Konyaev, S., Oku, Y., 2013. Molecular phylogeny of the genus Taenia (Cestoda: Taeniidae): proposals for the resurrection of Hydatigera Lamarck, 1816 and the creation of a new genus Versteria. Int. J. Parasitol. 43, 427 - 437.
Odnokurtsev, V. A., Sedalischev, V. T., 2011. Helminthes fauna of sable (Martes zibellina Linnaeus, 1758) in Yakutia. Tomsk State Univ. J. Biol. 2, 22 - 34.
Olson, P. D., Yoder, K., Fajardo, L. - G. L. F., Marty, A. M., van de Pas, S., Olivier, C., Relman, D. A., 2003. Lethal invasive cestodiasis in immunosuppressed patients. J. Infect. Dis. 187, 1962 - 1966.
Ribas, A., Torre, I., Feliu, C., Arrizabalaga, A., Casanova, J. C., 2009. Helminth communities of the bank vole Myodes glareolus in two populations: Montsenyu natural park (NE Spain) and Pi Natural reserve (French Pyrenees). Rev. Ibero-Latinoam. Parasitol. Int. 1, 73 - 89.
Schaerer, O., 1987. Die Metacestoden der Kleinsauger (Insectivora und Rodentia) und ihre Wirtsarten, Verbreitung und Haufigkeit im Kanton Thurgau (Schweiz). Dissertation. University of Zurich, Zurich, Switzerland.
Slais, J., 1973. Functional morphology of cestode larvae. Adv. Parasitol. 11, 395 - 480.
Soveri, T., Henttonen, H., Rudback, E., Schildt, R., Tanskanen, R., Husu-Kallio, J., Haukisalmi, V., Sukura, A., Laakkonen, J., 2000. Disease patterns in field and bank vole populations during a cyclicdecline in central Finland. Comp. Immunol. Microbiol. Infect. Dis. 23, 73 - 89.
Tenora, F., Henttonen, H., Haukisalmi, V., 1983. On helminths of rodents in Finland. Ann. Zool. Fenn. 20, 37 - 45.
Tenora, F., Andreassen, J., Hindsbo, O., Lodal, J., 1991. Helminths of small rodents in Denmark. Helminthologia 28, 151 - 154.
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Genus |
Versteria mustelae
Deplazes, Peter, Eichenberger, Ramon M. & Grimm, Felix 2019 |
Taenia tenuicollis
Rudolphi 1819 |
Mustela nivalis
Linnaeus 1766 |
Mustela ermine
Linnaeus 1758 |
M. erminea
Linnaeus 1758 |