Retrospective Evaluation of Implementation of Long-Term Forecast on Spatial Spread of Rabies in the Asian Part of Russia

Objective: To evaluate the historical long-term forecast of the spatial spread of rabies in Siberia and Far East and to characterize modern approaches to spatial forecasting. The concept of spatial spread of rabies in the Asian part of Russia, developed in the 80s of the twentieth century, is subjected to critical analysis based on information on rabies registration for 1881–1980 and zoogeographic data. At that time, 5 rabies enzootic regions were identified, and the most probable directions of further exportation of infection suggested. At first, a review of published data on human and animal rabies cases for the period of 1985–2019 was undertaken (including reference publications). Data on cases of rabies among humans and animals were selected for which geographical coordinates could be determined. Mapping was performed using GIS (QGIS 3.12.0 software and “Natural Earth” and “OpenStreetMap” electronic maps). Comparison of maps for different time periods demonstrated that rabies incidence was recorded mainly within the previously identified risk areas. However, the occurrence of human disease in different regions did not always correspond to the intensity of epizootics and the predicted risk. Next, in an attempt to correct the prognosis of the spatiotemporal rabies spread, we reviewed publications that incorporated virus genetic data along with GIS technology and modeling application. The distribution of the three major rabies virus lineages (“steppe”, “Arctiс-like”, “Arctic”) corresponded to the regions that were previously identified. The spread of fox rabies (the “steppe” rabies virus lineage) in the north-east direction was described. In several instances, rabies outbreaks in southern Siberia and Far East were associated with cross-border movement of the virus from Kazakhstan, Mongolia and China. Data on the speed of the epizootic waves, pathways, and natural barriers for virus spread are discussed. The correction of the forecast for rabies virus circulation and spread is important for the development of control strategies in the region, including oral vaccination of wildlife virus reservoirs.

1. Popov N.V., Kouklev E.V., Kutyrev V.V. [Relevant issues of geo-informational support to provide for monitoring and prognosti- cation of epizootic activity in natural foci of plague and other zoonot- ic infections in the territory of the Russian Federation]. Problemy Osobo Opasnykh Infektsii [Problems of Particularly Dangerous Infections]. 2006; 2:28–30.

2. Sidorov G.N., Sidorova D.G., Kolychev N.M., Poleshchuk E.M. [On the question of predicting the epizootic process for rabies in Russia]. Veterinarnaya Patologiya [Veterinary pathology]. 2007; 3:17–23.

3. Hanlon C.F. Rabies in terrestrial animals. In: Jackson A.C., editors. Rabies Scientific Basis of the Disease and its Management. Oxford: Academic Press; 2013. P. 179–214.

4. Belchikhina A.V., Karaulov A.K. [A retrospective analysis of the epizootic situation on rabies in the territory of the Russian Federation]. Veterinariya Segodnya [Veterinary Medicine Today]. 2016; 1:64–70.

5. Sidorov G.N., Poleshchuk E.M., Sidorova D.G. [Changes in the role of mammals in human rabies infection in Russia for a historically graspable period of the 16th to 21st centuries] Zoologicheskii Zhurnal [Zoological Journal]. 2019; 98(4):437–52 DOI: 10.1134/S0044513419040159

6. Shabejkin A. A., Gulyukin A. M., Zajkova O. N. [Overview of the epizootic situation on rabies for 2015 in the Russian Federation]. Veterinariya Kubani [Veterinary of Kuban]. 2016; (4):4–6.

7. Shulpin M.I., Nazarov N.A., Chupin S.A., Korennoy F.I., Metlin A.E., Mischenko A.V. Rabies surveillance in the Russian Federation. Rev. Sci. Tech. 2018; 37(2):483–95. DOI: 10.20506/rst.37.2.2817.

8. Mal’kov G.B. [The concept of population-biological aspects of the natural foci of rabies]. In: [Natural Focal Human Diseases (Epidemiology and Prevention)]. Omsk; 1981. P. 105–14.

9. Sidorov G.N., Savitsky V.P., Botvinkin A.D. [Landscape distribution of carnivorous canine mammals (Canidae) as a factor in the formation of rabies nosoareal in the southeast of the USSR]. Zoologicheskii Zhurnal [Zoological Journal]. 1983; 62 (5):761–70.

10. Savitsky V.P., Botvinkin A.D. [Epidemiological zoning and long-term prognosis of rabies incidence in Eastern Siberia and Far East]. In: [Modern Methods of Studying Natural-Focal Infections]. Leningrad; 1980. P. 41–52.

11. Deviatkin A.A., Lukashev N.L., Poleshchuk E.M., Dedkov V.G, Tkachev S.E., Sidorov G.N., Karganova G.G., Galkina I.V., Shchelkanov M.Yu., Shipulin G.A. The phylodynamics of the rabies virus in the Russian Federation. PLoS One. 2017; 12(2):e0171855. DOI: 10.1371/journal.pone.0171855.

12. Kuzmin I.V., Botvinkin A.D., McElhinney L.M., Smith J.S., Orciari L.A., Hughes G.J., Fooks A.R., Rupprecht C.E. Molecular epidemiology of terrestrial rabies in the former Soviet Union. J. Wildl. Dis. 2004; 40(4):17–631. DOI: 10.7589/0090-3558-40.4.617.

13. Koneva I.V., Batuev A.R., Lopatkin D.A. [The map «Nozoecosystems of the Asian Russia»]. Izvestiya Irkutskogo Gosudarstvennogo Universiteta [News of Irkutsk State University]. 2011; 4 (1):119–34.

14. Zarva I.D., Botvinkin A.D., Goryaev D.V., Demchin P.M., Dmitrieva G.M., Zaykova T.A., Lutsenko G.V., Romanova T.G., Rusin M.V., Sorokina O.V., Suturina Yu.E., Shalginova E.Yu., Shmatova L.V. [Geographic information system analysis of rabies spread in island forest-steppe of East Siberia]. Fundamental'naya i Klinicheskaya Meditsina [Fundamental and Clinical Medicine]. 2019; 4 (2):48–57. DOI: 10.23946/2500-0764-2019-4-2-48-57.

15. Yakovchits N.V., Bondaryuk A.N., Adel’shin R.V., Noskov A.K., Andaev E.I., Botvinkin A.D. Rabies virus in the Krasnoyarsk Territory: two independent phylogroups. Dal'nevostochnyj Zhurnal Infektsionnoy Patologii [Far Eastern Journal of Infectious Pathology]. 2019; (37):38–9.

16. Metlin A.E., Rybakov S.S., Mikhalishin V.V., Muller Th. [Oral vaccination of wild carnivores against rabies]. Veterinariya [Veterinary Medicine]. 2009; 8:18–25.

17. Slivko I.A., Safonov G.A., Khripunov E.M., Gogin A.E., Zhesterev V.I., Ban’kovsky D.O. [Probable causes of failure of oral anti-rabies immunization of wild carnivores in the Russian Federation]. Veterinariya [Veterinary Medicine]. 2013; 10:27–31.

18. Freuling C.M., Hampson K., Selhorst T., Schröder R., Meslin F.X., Mettenleiter T.C., Müller Т. The elimination of fox ra- bies from Europe: determinants of success and lessons for the future. Philos. Trans. R. Soc. Lond. B. Biol Sci. 2013; 368(1623):20120142. DOI: 10.1098/rstb.2012.0142.

19. Müller T.F., Freuling C.M. Rabies control in Europe: an overview of past, urgent and future strategies. Rev. Sci. Tech. 2018, 37(2):409–419. DOI: 10.20506/rst.37.2.2811.

20. Karpov V.S., Chernyavsky V.F., Karataeva T.D. The Main Zooanthroponoses in Yakutia (Epizootology and epidemiology). Yakutsk; 1997. 154 p.

21. Nesterova Yu.V., Devyatilova S.V., Homichuk T.F., Semeykina L.M. Rabies as a relevant problem of the Primorsky Territory of Russia. Zdorov’e. Meditsinskaya Ekologiya. Nauka [Health. Medical Ecology. Science]. 2016; 3(66):112–5. DOI: 10.18411/hmes.d-2016-124

22. Yanovich V.A. [The epidemiological and epizootiological situation on rabies in the Jewish Autonomous Region]. Zhurnal Mikrobiologii, Epidemiologii i Immunobiologii [Journal of Microbiology, Epidemiology and Immunobiology]. 1999; (4):119–20.

23. Adelshin R.V., Melnikova O.V., Trushina Y.N., Botvinkin A.D., Borisova T.I., Andaev E.I., Verzhutsky D.B., Khangazhinov A.S., Balakhonov S.V. A new outbreak of fox rabies at the RussianMongolian border. Virologica Sinica. 2015; 30(4):313–5. DOI: 10.1007/s12250-015-3609-0.

24. Kuzmin I.V. An arctic fox rabies virus strain as a cause of human rabies in Russian Siberia. Arch. Virol. 1999; 144:627–9. DOI: 10.1007/s007050050531.

25. Rabies in the Russian Federation. Information and Analytical Bulletin. Compiled by: Poleshchuk E.M., Sidorov G.N., Berezina E.S.. Omsk: KAN Publishing House; 2009. 65 p.

26. Rabies in the Russian Federation. Information and ana- lytical bulletin. Compiled by: E.M.Poleshchuk, G.N.Sidorov, D.G.Sidorova, N.M.Kolychev. Omsk: KAN Publishing House, 2019. 49 p. (Cited 12 Mar 2019). [Internet]. Available from: http://oniipi.org/author/admin.

27. Rabies in the Russian Federation. Information and ana- lytical bulletin. Compiled by: E.M. Poleshchuk, G.N.Sidorov, D.N.Nashatyreva, E.A.Gradoboeva, N.D.Pakskina, I.V.Popova. Omsk: KAN Publishing House, 2019. 110 p. (Cited 12 Mar 2019). [Internet]. Available from: http://oniipi.org/author/admin.

28. Prevention of rabies in the conditions of cattle-breeding (by the example of the Republic of Tuva): Methodological recommenda- tions. Compiled by: E.M.Poleshchuk, G.N.Sidorov, L.K.Saryglar, et al. Omsk, 2016. 99 p. (Cited 12 Mar 2019). [Internet] Available from: https://search.rsl.ru/ru/record/01008950007.

29. Rabies Bulletin Europe. (Cited 12 Mar 2019). [Internet] Available from: https://rbe.fli.de/resource/journal.

30. Giannakopoulos A., Valiakos G., Papaspyropoulos K., Dougas G., Korou L.M., Tasioudi K.E., Fthenakis G.C., Hutchings M.R., Kaimaras D., Tsokana C.N., Iliadou P., Spyrou V., Tzani M., Birtsas P., Kostoglou P., Sokos C., Doudounakis S., Yon L., Hannant D., Artois M., Tsiodras S., Hadjichristodoulou C., Billinis C. Rabies outbreak in Greece during 2012–2014: use of geographical informa- tion system for analysis, risk assessment and control. Epidemiol. Infect. 2016; 144(14):3068–79. DOI: 10.1017/S0950268816001527.

31. Boldbaatar B., Inoue S., Tuya N., Dulam P., Batchuluun D., Sugiura N., Okutani A., Kaku Y., Noguchi A., Kotaki A., Yamada A. Molecular epidemiology of rabies virus in Mongolia, 2005–2008. Jpn. J. Infect. Dis. 2010; 63(5):358–63. PMID: 20859006.

32. Feng Y., Wang W., Guo J., Alatengheli, Li Y., Yang G., Su N., Zhang L., Xu W., Sheng Z., Ma L., Gui J., Dejide, Lin H., Tu C. Disease outbreaks caused by steppe-type rabies viruses in China. Epidemiol. Infect. 2015; 143(6):1287–91. DOI: 10.1017/S0950268814001952.

33. 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 ra- bies and its probable explanation in mainland China, 2004–2013. PLoS Negl. Trop. Dis. 2015; 9(2):e0003502. DOI: 10.1371/journal.pntd.0003502.

34. Pant G.R., Lavenir R., Wong F.Y.K., Certoma A., Larrous F., Bhatta D.R., Bourhy H., Stevens V., Dacheux L. Recent emer- gence and spread of an Arctic-related phylogenetic lineage of ra- bies virus in Nepal. PLoS Negl. Trop. Dis. 2013; 7(11):e2560. DOI: 10.1371/journal.pntd.0002560.

35. Zhu H., Chen X., Shao X., Ba H., Wang F., Wang H., Yang Y., Sun N., Ren J., Cheng S., Wen Y. Characterization of a virulent dog-originated rabies virus affecting more than twenty fallow deer(Dama dama) in Inner Mongolia, China. Infect. Genet. Evol. 2015; 31:127–34. DOI: 10.1016/j.meegid.2014.12.024.

36. Hanke D., Freuling C.M., Fischer S., Hueffer K., Hundertmark K., Nadin-Davis S., Marston D., Fooks A.R., Bøtner A., Mettenleiter T.C., Beer M., Rasmussen T.B., Müller T.F., Höper D. Spatio-temporal аnalysis of the genetic diversity of arctic rabies viruses and their reservoir hosts in Greenland. PLoS Negl. Trop. Dis. 2016. 10(7):e0004779. DOI: 10.1371/journal.pntd.0004779.

37. Huefferand K., Murphy M. Rabies in Alaska, from the past to an uncertain future. Int. J. Circumpolar Health. 2018; 77(1):1475185. DOI: 10.1080/22423982.2018.1475185.

38. Biek R., Henderson J.C., Waller L.A., Rupprecht C.E., Real L.A. A high-resolution genetic signature of demographic and spatial expansion in epizootic rabies virus. Proc. Natl. Acad. Sci. USA. 2007; 104(19):7993–8. DOI: 10.1073/pnas.0700741104.

39. Kuzmina N.A., Lemey P., Kuzmin I.V., Mayes B.C., Ellison J.A, Orciari L.A., Hightower D., Taylor S.T., Rupprecht C.E. The phylogeography and spatiotemporal spread of south-central skunk rabies virus. PLoS ONE. 2013; 8(12):e82348. DOI: 10.1371/journal.pone.0082348.

40. Ruan S. Modeling the transmission dynamics and control of rabies in China. Math. Biosci. 2017; 286:65–93. DOI: 10.1016/j.mbs.2017.02.005.

41. Tyul’ko Zh.S., Kuzmin I.V. [Modeling of rabies epizootics in fox populations with limited ecological capacity of biotopes]. Ekologiya [Ecology]. 2002; (5): 351-357.

42. Sultanov A.A., Abdrakhmanov S.K., Abdybekova A.M., Karatayev B.S., Torgerson P.R. Rabies in Kazakhstan. PLoS Negl. Trop. Dis. 2016; 10(8):e0004889. DOI: 10.1371/journal.pntd.0004889.