Rabies re-emergence after long-term disease freedom (Amur Oblast, Russia)
https://doi.org/10.29326/2304-196X-2022-11-4-309-318
Abstract
Retrospective descriptive epizootological study was conducted in the Amur Oblast (Russian Far East), where a rabies outbreak was reported in 2018. The aim of the study was to analyze probable routes of rabies introduction and features of its spatial and temporal spread in the territory that remained free from this infection from 1972 to 2018. In 2018–2021, altogether 1,416 animals were examined for the infection with the rabies virus. Forty-seven animal rabies cases were confirmed; the proportion of wild animals (Vulpes vulpes, Nyctereutes procyonoides, Canis lupus) amounted to 66%. The first cases were detected within 30 km from the state border with China. Nucleotide sequences of the nucleoprotein gene of three rabies virus isolates were determined and their belonging to the Arctic-like-2 genetic lineage was established. Genetically closest rabies virus isolates have been found in Heilongjiang Province (China, 2011, 2018) and Jewish Autonomous Oblast (Russia, 1980). GIS and open Earth remote sensing data were used to map the rabies cases. After 2018, the epizootic spread within the forest-steppe landscapes of the Zeya-Bureya Plain, where human and animal rabies cases had been earlier reported (until 1972). The front of the epizootic spread in a north-eastern direction at an average speed of 59 (16–302) km during one epizootic cycle. The introduction of the rabies virus was most likely along the Amur River valley from downstream regions of Russia and China that are rabies infected.
Keywords
About the Authors
A. D. BotvinkinRussian Federation
Aleksandr D. Botvinkin, Doctor of Science (Medicine), Professor, Head of Department of Epidemiology
Irkutsk
I. D. Zarva
Russian Federation
Ivan D. Zarva, Candidate of Science (Medicine), Assistant of the Department of Epidemiology
Irkutsk
I. V. Meltsоv
Russian Federation
Ivan V. Meltsov, Candidate of Science (Veterinary Medicine), Associate Professor, Chair of Special Veterinary Disciplines
Irkutsk
S. A. Chupin
Russian Federation
Sergei A. Chupin, Candidate of Science (Biology), Leading Researcher, Reference Laboratory for Rabies and BSE
Vladimir
E. M. Poleshchuk
Russian Federation
Еlena M. Poleshchuk, Candidate of Science (Biology), Head of the Laboratory, Leading Researcher of the Laboratory of Ecology and Epidemiology of Rabies
Omsk
N. G. Zinyakov
Russian Federation
Nikolay G. Zinyakov, Candidate of Science (Biology), Senior Researcher, Reference Laboratory for Avian Viral Diseases
Vladimir
S. V. Samokhvalov
Russian Federation
Sergey V. Samokhvalov, Head
Blagoveshchensk
I. V. Solovey
Russian Federation
Irina V. Solovey, Deputy Head of the Unit for Anti-Epizootic Measures
Blagoveshchensk
N. V. Yakovleva
Russian Federation
Natalya V. Yakovleva, Director
Blagoveshchensk
G. N. Sidorov
Russian Federation
Gennady N. Sidorov, Doctor of Science (Biology), Professor of the Department of Biology and Biological Education; Chief Researcher, Laboratory of Ecology and Epidemiology of Rabies
Omsk
I. A. Boyko
Russian Federation
Irina A. Boyko, Zoologist
Blagoveshchensk
V. G. Yudin
Russian Federation
Viktor G. Yudin, Candidate of Science (Biology), Senior Researcher, Laboratory of Theriology
Vladivostok
E. I. Andaev
Russian Federation
Evgeny I. Andaev, Doctor of Science (Medicine), Deputy Director
Irkutsk
A. Ye. Metlin
Austria
Artem Ye. Metlin, Doctor of Science (Veterinary Medicine), Animal Production and Health Section
Vienna
References
1. Shulpin M. I., Nazarov N. A., Chupin S. A., Korennoy F. I., Metlin A. Ye., Mischenko A. V. Rabies surveillance in the Russian Federation. Rev. Sci. Tech. 2018; 37 (2): 483–495. DOI: 10.20506/rst.37.2.2817.
2. Poleshchuk E. M., Sidorov G. N. Comparative analysis of features of epizootiological and epidemic situation and risk of rabies infection in the Russian Federation in early XXI century. Problems of Particularly Dangerous Infections. 2020; (4): 16–25. DOI: 10/21055/0370-1069-2020-4-16-25. (in Russ.)
3. Poleshchuk E. M., Sidorov G. N., Nashatyreva D. N., Gradoboyeva Ye. A., Pakskina N. D., Popova I. V. Rabies in the Russian Federation: research and information newsletter. Omsk: Izdatel’skii tsentr KAN; 2019. 110 p. eLIBRARY ID: 41024936. (in Russ.)
4. Poleshchuk E. M., Sidorov G. N., Berezina E. S. Rabies in the Russian Federation: research and information newsletter. Omsk: Poligraficheskii tsentr KAN; 2018: 65 р. eLIBRARY ID: 25563479. (in Russ.)
5. Botvinkin A. D., Sidorov G. N., Poleshchuk E. M., Zarva I. D., Nashatyreva D. N., Yakovchits N. V., et.al. Retrospective evaluation of implementation of long-term forecast on spatial spread of rabies in the Asian part of Russia. Problems of Particularly Dangerous Infections. 2020; (2): 13–21. DOI: 10.21055/0370-1069-2-13-21. (in Russ.)
6. Miao F., Li N., Yang J., Chen T., Liu Y., Zhang S., Hu R. Neglected challenges in the control of animal rabies in China. One Health. 2021; 12:100212. DOI: 10.1016/j.onehlt.2021.100212.
7. Yao H.-W., Yang Y., Liu K., Li X.-L., Zuo S.-Q., Sun R.-X., Fang L. Q., Cao W. C. The spatiotemporal expansion of human rabies and its probable explanation in Mainland China, 2004–2013. PLoS Negl. Trop. Dis. 2015; 9 (2):e0003502. DOI: 10.1371/journal.pntd.0003502.
8. Minghui R., Stone M., Semedo M. H., Nel L. New global strategic plan to eliminate dog-mediated rabies by 2030. Lancet Glob. Health. 2018; 6 (8): e828–e829. DOI: 10.1016/S2214-109X(18)30302-4.
9. Savitskiy V. P., Botvinkin A. D., Belko V. I., Mayorov S. P., Sidel’nikova N. F., Gorkovenko L. Ye. Epidemiologicheskie osobennosti beshenstva na Dal’nem Vostoke = Rabies epidemiological features in Far East. Modern methods of studying natural focal diseases: conference proceedings (September 18–20, 1979). Omsk; 1980; 31–41. (in Russ.)
10. Vedernikov V. A., Zemlyanova V. E., Makhashov E., Anderson Z. E., Zhukov I. V., Zhanuzakov N. Zh. Razrabotka kratkosrochnykh prognozov epizooticheskoi obstanovkii = Development of epizootic short-term forecasts. Proceedings of the All-Russian Institute of Experimental Veterinary Medicine. Moscow: 1982; 55: 21–26. (in Russ.)
11. Adelshin R. V., Melnikova O. V., Trushina Y. N., Botvinkin A. D., Borisova T. I., Andaev E. I., et al. A new outbreak of fox rabies at the Russian-Mongolian border. Virol. Sin. 2015; 30 (4): 313–315. DOI: 10.1007/s12250-015-3609-0.
12. Kumar S., Stecher G., Li M., Knyaz C., Tamura K. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 2018; 35 (6): 1547–1549. DOI: 10.1093/molbev/msy096.
13. Department of Regulation, Protection, and Use Control of Fauna Objects and Their Habitat in the Amur Region. Available at: https://amurohota.amurobl.ru (date of access: 28.03.2022). (in Russ.)
14. Senchik А. V., Toushkin А. А. State and economic use of wild animal population in the Amur Region. Far East Agrarian Herald. 2019; 4 (52): 86–93. DOI: 10.24411/1999-6837-2019-14058. (in Russ.)
15. Lomanova N. V., Borisov B. P., Volodina O. A., Gubar Yu. P., Lyapina M. G., Komissarov M. A., et al. Sostoyanie okhotnich’ikh resursov v Rossiiskoi Federatsii v 2008–2010 gg. = Condition hunting resources in the Russian Federation in 2008–2010: information and analytical materials. Hunting animals of Russia (biology, protection, resource studies, rational use). Moscow: Fizicheskaya kul’tura; 2011, Issue 9. 219 p. (in Russ.)
16. Deviatkin A. A., Lukashev A. N., Poleshchuk E. M., Dedkov V. G., Tkachev S. E., Sidorov G. N., et al. The phylodynamics of the rabies virus in the Russian Federation. PLoS One. 2017; 12 (2):e0171855. DOI: 10.1371/journal.pone.0171855.
17. Chupin S. A., Chernyshova E. V., Metlin A. E. Genetic characterization of the rabies virus field isolates detected in Russian Federation within the period 2008–2011. Problems of Virology. 2013. 4: 44–49. eLIBRARY ID: 20502319. (in Russ.)
18. Yudin V. G. Fox of USSR Far East. Vladivostok: Far East Research of USSR AoS; 1986. 284 p. (in Russ.)
19. Yudin V. G. Primorye and Amur raccoon dog. Moscow: Nauka; 1977. 162 p. (in Russ.)
20. Gribanova L. Ya., Malkov G. B., Savitsky V. P., Sidorov G. N., Botvinkin A. D., Pochekunin D. I., et al. Results of a study of natural foci of rabies and evaluation of the risk of hydrophobia in new construction areas of Eastern Siberia and the Far East. Zhurnal mikrobiologii, epidemiologii, immunobiologii. 1980; 57 (7): 86–90. PMID: 7435025. (in Russ.)
21. Botvinkin A. D., Zarva I. D., Yakovchits N. V., Adelshin R. V., Melnikova O. V., Andaev E. I., et al. Epidemiological analysis оf rabies outbreaks in the Trans-Baikal region after transboundary drift of infection. Epidemiologiya i infektsionnyye bolezni. Aktual’nyye voprosy. 2019; 9 (3): 15–24. DOI: 10.18656/epidem.2019.9.3.15-24. (in Russ.)
22. Yanovich V. A. Rabies epidemiology, epizootology and prevention in Jewish Autonomous Oblast: author’s thesis of Candidate of Science (Medicine). Vladivostok; 2004: 28 p. eLIBRARY ID: 15791073. (in Russ.)
23. Liu Y., Zhang S., Zhao J., Zhang F., Li N., Lian H., Wurengege, Guo S., Hu R. Fox- and raccoon-dog-associated rabies outbreaks in northern China. Virol. Sin. 2014; 29 (5): 308–310. DOI: 10.1007/s12250-014-3484-0.
24. Tao X. Y., Guo Z. Y., Li H., Jiao W. T., Shen X. X., Zhu W. Y., Rayner S., Tang Q. Rabies cases in the West of China have two distinct origins. PLoS Negl. Trop. Dis. 2015; 9 (10):e0004140. DOI: 10.1371/journal.pntd.0004140.
25. Shao X. Q., Yan X. J., Luo G. L., Zhang H. L., Chai X. L., Wang F. X., Yang F. H. Genetic evidence for domestic raccoon dog rabies caused by Arctic-like rabies virus in Inner Mongolia, China. Epidemiol. Infect. 2011; 139 (4): 629–635. DOI: 10.1017/S0950268810001263.
26. Botvinkin A. D., Gribanova L. Ya., Nikiforova T. A. Experimental rabies in the raccoon dog. Zhurnal mikrobiologii, epidemiologii, immunobiologii. 1983; 60 (12): 37–40. PMID: 6666446. (in Russ.)
27. Sidorov G. N., Savitskiy V. P., Botvinkin A. D. Landshaftnoe raspredelenie khishchnykh mlekopitayushchikh semeistva sobach’ikh (Canidae) kak faktor formirovaniya areala virusa beshenstva na yugo-vostoke SSSR = Landscape distribution of carnivorous mammals of Canidae family as a factor for rabies virus range in the south-east USSR. Zoologicheskii Zhurnal. 1983; 62 (5): 761–770. eLIBRARY ID: 28786114. (in Russ.)
Review
For citations:
Botvinkin A.D., Zarva I.D., Meltsоv I.V., Chupin S.A., Poleshchuk E.M., Zinyakov N.G., Samokhvalov S.V., Solovey I.V., Yakovleva N.V., Sidorov G.N., Boyko I.A., Yudin V.G., Andaev E.I., Metlin A.Ye. Rabies re-emergence after long-term disease freedom (Amur Oblast, Russia). Veterinary Science Today. 2022;11(4):309-318. https://doi.org/10.29326/2304-196X-2022-11-4-309-318