Epidemiological Situation on Crimean-Congo Hemorrhagic Fever in the Russian Federation in 2019 and Forecast for 2020

The review presents an analysis of epidemic and epizootic situation of Crimean-Congo hemorrhagic fever in the Russian Federation in 2010–2019, summarizes the results of epizootiological monitoring of the CCHF natural focus territory in the south of European part of Russia. An unfavorable epidemiological situation regarding CCHF is maintained in the Russian Federation. In 2010–2019, 999 CCHF cases were registered in nine regions of Southern and North-Caucasian Federal Districts. In 2019, an increase in the CCHF incidence level in the entities of the SFD and NCFD was observed as compared to 2017–2018. The expansion of the territory with registered epidemic manifestations of CCHF continues. In 2010–2019, the number of imago and pre-imaginal phases of Hyalomma marginatum – the main vector of the CCHF virus in Russia, remained consistently high. High numbers of H. marginatum ticks and their CCHFV infection rates can contribute to the development of an unfavorable epidemiological situation in the south of the Russian Federation with a possible increase in the CCHF incidence in 2020.

Crimean-Congo hemorrhagic fever, epidemic situation, epidemiological monitoring, morbidity, forecast

1. Bente D.A., Forrester N.L., Watts D.M., McAuley A.J., Whitehouse C.A., Bray M. Crimean-Congo hemorrhagic fever: his- tory, epidemiology, pathogenesis, clinical syndrome and genetic diversity. Antiviral Res. 2013; 100(1):159–89. DOI: 10.1016/j.antiviral.2013.07.006.

2. Esser H.J., Mogling R., Cleton N.B., van der Jeugd H., Sprong H., Stroo A., Koopmans M.P.G., de Boer W.F., Reusken C.B.E.M. Risk factors associated with sustained circulation of six zoonotic arboviruses: a systematic review for selection of surveil- lance sites in non-endemic areas. Parasit. Vectors. 2019; 12:265. DOI: 10.1186/s13071-019-3515-7.

3. Fillatre P., Revest M., Tattevin P. Crimean-Congo hemor- rhagic fever: An update. Med. Mal. Infect. 2019; 49(8):574–585. DOI: 10.1016/j.medmal.2019.09.005.

4. Papa A., Mirazimi A., Köksal I., Estrada-Pena A., Feldmann H. Recent advances in research on Crimean-Congo hemorrhagic fever. J. Clin. Virol. 2015; 64:137–43. DOI: 10.1016/j.jcv.2014.08.029.

5. Papa A., Weber F., Hewson R., Weidmann M., Köksal I., Korukluoglu G., Mirazimi A. Meeting report: First International Conference on Crimean-Congo hemorrhagic fever. Antiviral Res. 2015; 120:57–65. DOI: 10.1016/j.antiviral.2015.05.005.

6. Wahid B., Altaf S., Naeem N., Ilyas N., Idrees M. Scoping Review of Crimean-Congo Hemorrhagic Fever (CCHF) Literature and Implications of Future Research. J. Coll. Physicians Surg. Pak. 2019; 29(6):563–73. DOI: 10.29271/jcpsp.2019.06.563.

7. ICTV. Virus Taxonomy 2016. (Cited 31 Jan 2020). [Internet]. Available from: https://talk.ictvonline.org/ictv-reports/ictv_online_report/.

8. Kulichenko A.N., Maletskaya O.V., Vasilenko N.F., Beyer A.P., Sannikova I.V., Pasechnikov V.D., Kovalchuk I.V., Ermakov A.V., Butayev T.M., Smirnova S.E., Karan L.S., Maleev V.V., Platonov A.E. Crimean-Congo hemorrhagic fever in Eurasia in the 21st century: Epidemiological aspects. Epidemiologiya i Infektsionnye Bolezni. Aktualnie Voprosy [Epidemiology and Infectious Diseases Current Items]. 2012; 3:42–53

9. Butenko A.M., Trusova I.N. Morbidity of the Crimean hemorrhagic fever in the countries of Europe, Africa and Asia (1943– 2012). Epidemiologiya i Infektsionnye Bolezni [Epidemiology and Infectious Diseases]. 2013; 5:46–8.

10. Zakham F., Alaloui A., Levanov L., Vapalahti O. Viral haemorrhagic fevers in the Middle East. Rev. Sci. Tech. 2019; 38(1):185– 98. DOI: 10.20506/rst.38.1.2952.

11. Nasirian H. New aspects about Crimean-Congo hemorrhagic fever (CCHF) cases and associated fatality trends: A global systematic review and meta-analysis. Comp. Immunol. Microbiol. Infect Dis. 2020; 69:101429. DOI: 10.1016/j.cimid.2020.101429.

12. Chinikar S., Bouzari S., Shokrgozar M.A., Mostafavi E., Jalali T., Khakifirouz S., Nowotny N., Fooks A.R., Shah-Hosseini N. Genetic diversity of Crimean Congo hemorrhagic fever virus strains from Iran. J. Arthropod. Borne Dis. 2016; 10(2):127–40. PMID: 27308271. PMCID: PMC4906752.

13. Farhadpour F., Telmadarraiy Z., Chinikar S., Akbarzadeh K., Moemenbellah-Fard M.D., Faghihi F., Fakoorziba M.R., Jalali T., Mostafavi E., Shahhosseini N., Mohammadian M. Molecular detection of Crimean-Congo haemorrhagic fever virus in ticks collected from infested livestock populations in a New Endemic Area, South of Iran. Trop. Med. Int. Health. 2016; 21(3):340–7. DOI: 10.1111/ tmi.12667.

14. Saghafipour A., Mousazadeh-Mojarrad A., Arzamani N., Telmadarraiy Z., Rajabzadeh R., Arzamani K. Molecular and seroep- idemiological survey on Crimean-Congo Hemorrhagic Fever virus in Northeast of Iran. Med. J. Islam Repub. Iran. 2019; 33:41. DOI: 10.34171/mjiri.33.41.

15. Shahbazi N., Firouz S.K., Karimi M., Mostafavi E. Seroepidemiological survey of Crimean-Congo haemorrhagic fe- ver among high-risk groups in the west of Iran. J. Vector Borne Dis. 2019; 56(2):174–7. DOI: 10.4103/0972-9062.263720.

16. Abdiyeva K., Turebekov N., Dmitrovsky A., Tukhanova N., Shin A., Yeraliyeva L., Heinrich N., Hoelscher M., Yegemberdiyeva R., Shapiyeva Z., Kachiyeva Z., Zhalmagambetova A., Montag J., Dobler G., Zinner J., Wagner E., Frey S., Essbauer S. Seroepidemiological and molecular investigations of infections with Crimean-Congo haemorrhagic fever virus in Kazakhstan. Int. J. Infect. Dis. 2019; 78:121–7. DOI: 10.1016/j.ijid.2018.10.015.

17. Ahmeti S., Berisha L., Halili B., Ahmeti F., von Possel R., Thomé-Bolduan C., Michel A., Priesnitz S., Reisinger E.C., Günther S., Krüger A., Sherifi K., Jakupi X., Hemmer C.J., Emmerich P. Crimean-Congo Hemorrhagic Fever, Kosovo, 2013–2016. Emerg. Infect. Dis. 2019; 25(2):321–4. DOI: 10.3201/eid2502.171999.

18. Al-Abri S.S., Hewson R., Al-Kindi H., Al-Abaidani I., AlJardani A., Al-Maani A., Almahrouqi S., Atkinson B., Al-Wahaibi A., Al-Rawahi B., Bawikar S., Beeching N.J. Clinical and molecu- lar epidemiology of Crimean-Congo hemorrhagic fever in Oman. PLoS Negl. Trop. Dis. 2019; 13(4):e0007100. DOI: 10.1371/journal.pntd.0007100.

19. Camp J.V., Ahmed D., Osman B.M., Shah M.S., Howarth B., Khafaga T., Weidinger P., Karuvantevida N., Kolodziejek J., Mazrooei H., Wolf N., Loney T., Nowotny N. Crimean-Congo Hemorrhagic Fever Virus Endemicity in United Arab Emirates, 2019. Emerg. Infect. Dis. 2020; 26(5). DOI: 10.3201/eid2605.191414.

20. Elata AT, Karsany MS, Elageb RM, Hussain MA, Eltom KH, Elbashir MI, Aradaib IE. A nosocomial transmission of Crimean-Congo hemorrhagic fever to an attending physician in North Kordufan, Sudan. Virol. J. 2011; 8:303. DOI: 10.1186/1743-422X-8-303.

21. Khurshid A., Hassan M., Alam M.M., Aamir U.B., Rehman L., Sharif S., Shaukat S., Rana M.S., Angez M., Zaidi S.S.Z. CCHF virus variants in Pakistan and Afghanistan: Emerging diversity and epidemiology. J. Clin. Virol. 2015; 67:25–30. DOI: 10.1016/j.jcv.2015.03.021.

22. Nurmakhanov T., Sansyzbaev Y., Atshabar B., Deryabin P., Kazakov S., Zholshorinov A., Matzhanova A., Sadvakassova A., Saylaubekuly R., Kyraubaev K., Hay J., Atkinson B., Hewson R. Crimean-Congo haemorrhagic fever virus in Kazakhstan (1948–2013). Int. J. Infect. Dis. 2015; 38:19–23. DOI: 10.1016/j.ijid.2015.07.007.

23. Papa A., Pappa S., Panayotova E., Papadopoulou E., Christova I. Molecular epidemiology of Crimean-Congo hemorrhag- ic fever in Bulgaria – An update. J. Med. Virol. 2016; 88(5):769–73. DOI: 10.1002/jmv.24400.

24. Sahak M.N., Arifi F., Saeedzai S.A. Descriptive epidemiology of Crimean-Congo Hemorrhagic Fever (CCHF) in Afghanistan: Reported cases to National Surveillance System, 2016–2018. Int. J. Infect. Dis. 2019; 88:135–40. DOI: 10.1016/j.ijid.2019.08.016.

25. Vawda S., Goedhals D., Bester P.A., Burt F. Seroepidemiologic Survey of Crimean-Congo Hemorrhagic Fever Virus in Selected Risk Groups, South Africa. Emerg. Infect. Dis. 2018; 24(7):1360–3. DOI: 10.3201/eid2407.172096.

26. Yadav P.D., Cherian S.S., Zawar D., Kokate P., Gunjikar R., Jadhav S., Mishra A.C., Mourya D.T. Genetic characterization and molecular clock analyses of the Crimean-Congo hemorrhagic fever virus from human and ticks in India, 2010–2011. Infect. Genet. Evol. 2013; 14:223–31. DOI: 10.1016/j.meegid.2012.10.005.

27. Yaqub T., Oneeb M., Mukhtar N., Tahir Z., Shahid F., Subhan S., Salman M. Crimean-Congo Haemorrhagic Fever: Case study analysis of a sporadic outbreak from Chakwal, Pakistan. Zoonoses Public Health. 2019; 66(7):871–3. DOI: 10.1111/zph.12623.

28. Atkinson B., Latham J., Chamberlain J., Logue C., O’Donoghue L., Osborne J., Carson G., Brooks T., Carroll M., Jacobs M., Hopkins S., Hewson R. Sequencing and phylogenetic characterization of a fatal Crimean-Congo haemorrhagic fever case imported into the United Kingdom, 2012. Euro Surveill. 2012; 17(48):pii=20327. DOI: 10.2807/ese.17.48.20327-en.

29. Chamberlain J., Atkinson B., Logue C.H., Latham J., Newman E.N.C., Hewson R. Genome Sequence of Ex-Afghanistan Crimean-Congo Hemorrhagic Fever Virus SCT Strain, from an Imported United Kingdom Case in October 2012. Genome Announc. 2013; 1(3):e00161-13. DOI: 10.1128/genomeA.00161-13.

30. Lumley S., Atkinson B., Dowall S., Pitman J., Staplehurst S., Busuttil J., Simpson A., Aarons E., Petridou C., Nijjar M., Glover S., Brooks T., Hewson R. Non-fatal case of Crimean-Congo haemorrhagic fever imported into the United Kingdom (ex Bulgaria), June 2014. Euro Surveill. 2014; 19(30):pii=20864. DOI: 10.2807/1560- 7917.es2014.19.30.20864.

31. Papa A., Markatou F., Maltezou H.C., Papadopoulou E., Terzi E., Ventouri S., Pervanidou D., Tsiodras S., Maltezos E. Crimean-Congo haemorrhagic fever in a Greek worker returning from Bulgaria, June 2018. Euro Surveill. 2018; 23(35):pii=1800432. DOI: 10.2807/1560-7917.ES.2018.23.35.1800432.

32. Gismeteo. Weather in Neftekumsk for the next month. (Cited 18 Mar 2020). [Internet]. Available from: https://www.gismeteo.ru/weather-neftekumsk-5231/month/.