Abstract
Hantaviruses (genus Orthohantavirus, family Hantaviridae) have been identified worldwide and cause two kinds of human disease. In recent years, genetic evidence of pathogenicity for humans has been demonstrated for Tula virus, circulating in Europe among common voles (Microtus arvalis). The goal of the study consisted in detection of natural foci of hantavirus infection among voles in Siberia and genetic identification of vole-borne hantaviruses. A total of 254 rodents of the Arvicolinae subfamily were captured in West and East Siberia and tested for hantavirus-specific antibodies by immunofluorescent assay and for hantavirus RNA using reverse transcription polymerase chain reaction. results. Hantavirus antibody-positive rodents were found in Altai and Krasnoyarsk krai, Tomsk, Novosibirsk oblast, and the Republic of Altai among root voles (Alexandromys oeconomus), field voles (Microtus agrestis), narrow-headed voles (Lasiopodomys gregalis), and steppe lemmings (Lagurus lagurus). Viral RNA was detected and identified as Tula virus in two species of seropositive animals. Phylogenetic analysis showed that Siberian strains of Tula virus represent distinct genetic variants, Russia II and Russia III, associated with narrow-headed voles and steppe lemmings, respectively. Our data demonstrated that Tula virus is present from Altai krai, Tomsk, Novosibirsk oblast in West Siberia up to East Siberia (Krasnoyarsk krai) in Asian Russia.
REFERENCES
Jonsson, C.B., Figueiredo, L.T., and Vapalahti, O., A global perspective on hantavirus ecology, epidemiology, and disease, Clin. Microbiol. Rev., 2010, vol. 23, no. 2, pp. 412–441. https://doi.org/10.1128/CMR.00062-09
Avšič-Županc, T., Saksida, A., and Korva, M., Hantavirus infections, Clin. Microbiol. Infect., 2019, vol. 21, pp. 6–16. https://doi.org/10.1111/1469-0691.12291
Clement, J., Maes, P., Lagrou, K., Van Ranst, M., and Lameire, N., A unifying hypothesis and a single name for a complex globally emerging infection: Hantavirus disease, Eur. J. Clin. Microbiol. Infect. Dis., 2012, vol. 31, no. 1, pp. 1–5. https://doi.org/10.1007/s10096-011-1456-y
Tkachenko, E.A., Dzagurova, T.K., and Tkachenko, P.E., Hantaviruses: Ecology, molecular biology, morphology, pathogenesis and diagnostics of hantaviral infections, Mol. Med. (Moscow), 2009, vol. 5, pp. 36–41.
Hofmann, M.M., Petraityte-Burneikiene, R., Ziller, M., Sanauskas, K., Friedrich, R., Neiderstrasser, O., et al., Seroprevalence study in forestry workers of a non-endemic region in eastern Germany reveals infection by Tula and Dobrava-Belgrade hantaviruses, Med. Microbiol. Immunol., 2011, vol. 200, no. 4, pp. 263–268. https://doi.org/10.1007/s00430-011-0203-4
Zelena, H., Mrazek, J., and Kuhn, T., Tula hantavirus in immunocompromised host, Czech Republic, Emerging Infect. Dis., 2013, vol. 19, pp. 1873–1876. https://doi.org/10.3201/eid1911.130421
Reynes, J.M., Carli, D., Boukezia, N., Debruyne, M., and Herti, S., Tula hantavirus infection in a hospitalised patient, France, June, 2015, Eurosurveillance, 2015, vol. 20, no. 50, p. 30095. https://doi.org/10.2807/1560-7917.ES.2015.20.50.30095
Hofmann, J., Kramer, S., Herrlinger, K.R., Jeske, K., Kuhns, M., Weiss, S., et al., Tula virus as causative agent of hantavirus disease in immunocompetent person, Germany, Emerging Infect. Dis., 2021, vol. 27, no. 4, pp. 1234–1237. https://doi.org/10.3201/eid2704.203996
Kruger, D.H., Figueiredo, L.T., Song, J.W., and Klempa, B., Hantaviruses—globally emerging pathogens, J. Clin. Virol., 2015, vol. 64, pp. 128–136. https://doi.org/10.1016/j.jcv.2014.08.033
Plyusnin, A., Vapalahti, O., Lankinen, H., Lehvaslaiho, H., Apekina, N., Myasnikov, Y., et al., Tula virus: a newly detected hantavirus carried by European common voles, J. Virol., 1994, vol. 68, pp. 7833–7839.
Schmidt-Chanasit, J., Essbauer, S., Petraityte, R., Yoshimatsu, K., Tackmann, K., Conraths, F.J., et al., Extensive host sharing of central European Tula virus, J. Virol., 2010, vol. 84, pp. 459–474. https://doi.org/10.1128/JVI.01226-09
Chen, J.T., Qin, J., Li, K., Xu, Q.Y., Wang, X.P., Plyusnin, A., et al., Identification and characterization of a novel subtype of Tula virus in Microtus arvalis obscurus voles sampled from Xinjiang, China, Infect., Genet. Evol., 2019, vol. 75, p. 104012. https://doi.org/10.1016/j.meegid.2019.104012
Polat, C., Ergünay, K., Irmak, S., Erdin, M., Brinkmann, A., Çetintaş, O., et al., A novel genetic lineage of Tula orthohantavirus in Altai voles (Microtus obscurus) from Turkey, Infect., Genet. Evol., 2019, vol. 67, pp. 150–158. https://doi.org/10.1016/j.meegid.2018.11.015
Plyusnina, A., Laakkonen, J., Niemimaa, J., Henttonen, H., and Plyusnin, A., New genetic lineage of tula hantavirus in Microtus arvalis obscurus in Eastern Kazakhstan, Open Virol. J., 2008, vol. 2, pp. 32–36. https://doi.org/10.2174/1874357900802010032
Tkachenko, E.A., Witkowski, P.T., Radosa, L., Dzagurova, T.K., Okulova, N.M., Yunicheva, Y.V., et al., Adler hantavirus, a new genetic variant of Tula virus. identified in Major’s pine voles (Microtus majori) sampled in southern European Russia, Infect., Genet. Evol., 2015, vol. 29, pp. 156–163. https://doi.org/10.1016/j.meegid.2014.11.018
Yakimenko, V.V., Garanina, S.B., Mal’kova, M.G., Valitskaya, A.V., Konstantinova, G.A., Tantsev, A.K., et al., Results of hantavirus investigation in Western Siberia, Tikhookean. Med. Zh., 2008, vol. 2, pp. 20–26.
Yashina, L.N., Zaykovskaya, A.V., Protopopova, E.V., Babkin, I.V., Malyshev, B.S., Tovpinets, N.N., and Evstafiev, I.L., Tula hantavirus in Crimea, Mol. Genet., Microbiol. Virol., 2015, vol. 30, no. 4, pp. 201–205.
Gromov, I.M. and Erbaeva, M.A., Mlekopitayushchie fauny Rossii i sopredel’nykh territorii. Zaitseobraznye i gryzuny (Mammals of the Fauna of Russia and Adjacent Territories. Lagomorphs and Rodents), St. Petersburg: Zoological Institute Russ. Acad. Sci., 1995.
Mlekopitayushchie Rossii: sistematiko-geograficheskii spravochnik (Mammals of Russia: Systematic and Geographical Handbook), Pavlinov, I.Ya. and Lisovskii, A.A., Eds., Moscow: KMK, 2012.
Klempa, B., Fichet-Calvet, E., Lecompte, E., Auste, B., Aniskin, V., Meisel, H., et al., Hantavirus in African wood mouse, Guinea, Emerging Infect. Dis., 2006, vol. 12, pp. 838–840. https://doi.org/10.3201/eid1205.051487
Kumar, S., Stecher, G., Li, M., Knyaz, C., and Tamura, K., MEGA X: Molecular evolutionary genetics analysis across computing platforms, Mol. Biol. Evol., 2018, vol. 35, no. 6, pp. 1547–1549. https://doi.org/10.1093/molbev/msy096
Yashina, L.N., Abramov, S.A., Dupal, T.A., Danchinova, G.A., Malyshev, B.S., Hay, J., et al., Hokkaido genotype of Puumala virus in the grey red-backed vole (Myodes rufocanus) and northern red-backed vole (Myodes rutilus) in Siberia, Infect., Genet. Evol., 2015, vol. 33, pp. 304–313. https://doi.org/10.1016/j.meegid.2015.05.021
Klingström, J., Heyman, P., Escutenaire, S., Sjölander, K.B., De Jaegere, F., Henttonen, H., et al., Rodent host specificity of European hantaviruses: evidence of Puumala virus interspecific spillover, J. Med. Virol., 2002, vol. 68, no. 4, pp. 581–588. https://doi.org/10.1002/jmv.10232
Jeske, K., Hiltbrunner, M., Drewes, S., Ryll, R., Wenk, M., Špakova, A., et al., Field vole-associated Traemmersee hantavirus from Germany represents a novel hantavirus species, Virus Genes, 2019, vol. 55, no. 6, pp. 848–853. https://doi.org/10.1007/s11262-019-01706-7
Drewes, S., Jeske, K., Straková, P., Balčiauskas, L., Ryll, R., Balčiauskienė, L., et al., Identification of a novel hantavirus strain in the root vole (Microtus oeconomus) in Lithuania, Eastern Europe, Infect., Genet. Evol., 2021, vol. 90, p. 104520. https://doi.org/10.1016/j.meegid.2020.104520
Thomason, A.G., Begon, M., Bradley, J.E., Paterson, S., and Jackson, J.A., Endemic hantavirus in field voles, Northern England, Emerging Infect. Dis., 2017, vol. 23, no. 6, pp. 1033–1035. https://doi.org/10.3201/eid2306.161607
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This study was supported by the state budget and partially supported by Fundamental Scientific Research Program FWGS-2021-0002.
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This study was carried out in accordance with the Rules for conducting work using experimental animals (order of the Ministry of Higher and Secondary Education no. 742 dated November 13, 1984), as well as the European Convention for the Protection of Vertebrate Animals Used for Experimental and Other Scientific Purposes (ETS no. 123 dated March 18, 1986). The study did not use endangered or protected species.
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Translated by V. Mittova
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Yashina, L.N., Abramov, S.A., Smetannikova, N.A. et al. Hantaviruses in Populations of Voles in Siberia. Mol. Genet. Microbiol. Virol. 38, 101–108 (2023). https://doi.org/10.3103/S0891416823020106
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DOI: https://doi.org/10.3103/S0891416823020106