Crimean-Congo hemorrhagic fever (CCHF) is a widely distributed, tick-borne viral disease. Humans are the only species known to develop illness after CCHF virus (CCHFV) infection, characterized by a nonspecific febrile illness that can progress to severe, often fatal, hemorrhagic disease. A variety of animals may serve as asymptomatic reservoirs of CCHFV in an endemic cycle of transmission. Seroepidemiological studies have been instrumental in elucidating CCHFV reservoirs and in determining endemic foci of viral transmission. Herein, we review over 50 years of CCHFV seroepidemiological studies in domestic and wild animals. This review highlights the role of livestock in the maintenance and transmission of CCHFV, and provides a detailed summary of seroepidemiological studies of wild animal species, reflecting their relative roles in CCHFV ecology.
References
[1]
Bente DA, Forrester NL, Watts DM, McAuley AJ, Whitehouse CA, Bray M. Crimean-Congo hemorrhagic fever: history, epidemiology, pathogenesis, clinical syndrome and genetic diversity. Antiviral Res. 2013;100: 159–89. doi: 10.1016/j.antiviral.2013.07.006. pmid:23906741
[2]
Ergonul O. Crimean-Congo hemorrhagic fever virus: new outbreaks, new discoveries. Curr Opin Virol. Elsevier B.V.; 2012;2: 215–20. doi: 10.1016/j.coviro.2012.03.001. pmid:22482717
[3]
Ceylan B, Calica A, Ak O, Akkoyunlu Y, Turhan V. Ribavirin is not effective against Crimean-Congo hemorrhagic fever: Observations from the Turkish experience. Int J Infect Dis. International Society for Infectious Diseases; 2013;17: e799–e801. doi: 10.1016/j.ijid.2013.02.030. pmid:23773242
[4]
Arda B, Aciduman A, Johnston JC. A randomised controlled trial of ribavirin in Crimean Congo haemorrhagic fever: ethical considerations. J Med Ethics. 2012;38: 117–120. doi: 10.1136/medethics-2011-100107. pmid:21994465
[5]
Nalca A, Whitehouse CA. Crimean-Congo hemorrhagic fever virus infection among animals. In: Ergonul O, Whitehouse C, editors. Crimean–Congo Hemorrhagic Fever: A Global Perspective. Dordrecht, Netherlands: Springer; 2007. pp. 155–165.
[6]
Hoogstraal H. The epidemiology of tick-borne Crimean-Congo hemorrhagic fever in Asia, Europe, and Africa. J Med Entomol. 1979;15: 307–417. pmid:113533 doi: 10.1093/jmedent/15.4.307
Saidi S, Casals J, Faghih MA, Faghih AA. Crimean hemorrhagic fever-Congo (CHF-C) virus antibodies in man, and in domestic and small mammals, in Iran. Am J Trop Med Hyg. 1975;24: 353–357. pmid:164135
[10]
Tuncer P, Yesilbag K, Alpay G, Dincer E, Girisgin AO, Aydin L, et al. Crimean-Congo Hemorrhagic Fever infection in domestic animals in Marmara region, Western Turkey. Ankara Univ Vet Fak Derg. 2014;61: 49–53. doi: 10.1501/vetfak_0000002604
[11]
Gaidamovich S, Klisenko G, Shanoyan N, Obukhova V, Melnikova E. Indirect hemagglutination for diagnosis of Crimean hemorrhagic fever. Intervirology. 1974;2: 181–185. doi: 10.1159/000149421
[12]
Swanepoel R, Struthers JK, McGillivray GM. Reversed passive hemagglutination and inhibition with Rift Valley fever and Crimean-Congo hemorrhagic fever viruses. Am J Trop Med Hyg. 1983;32: 610–617. pmid:6407347
[13]
Shepherd AJ, Swanepoel R, Shepherd SP, McGillivray GM, Searle LA. Antibody to Crimean-Congo hemorrhagic fever virus in wild mammals from southern Africa. Am J Trop Med Hyg. 1987;36: 133–42. pmid:3101526
[14]
Chumakov M, Butenko A, Zavodona T, Tkachenko E, Rubin S, Smirnova S. Antigenic relationships between Crimean hemorrhagic fever virus strains isolated from different geographical regions (NAMRU-T853). Mater 16 Nauch Sess Inst Polio Virus Entsef. 1969; 151–152.
[15]
Shanmugam J, Smirova S, Chumakov M. Detection of antibodies to CHF-Congo viruses in human and dometic animal blood sera in India. Tr Inst Polio Virus Entsef. 1973;21: 149–152.
[16]
Berezin V, Chumakov M, Reshetnikov I, Zgurskaya G. Study of the role of birds in the ecology of Crimean hemorrhagic fever virus. 1971; 94–95.
[17]
Shepherd A, Swanepoel R, Leman P, Shepherd SP. Field and laboratory investigation of Crimean-Congo haemorrhagic fever virus (Nairovirus, family Bunyaviridae) infection in birds. Trans R Soc Trop Med Hyg. 1987;81: 1004–1007. pmid:3140434 doi: 10.1016/0035-9203(87)90379-8
[18]
Shanmugam J, Smirnova S, Chamakov M. Presence of Antibody to Arboviruses of the Crimean Haemorrhagic Fever-Congo (CHF-Congo) Group in Human Beings and Domestic Animals in India. Indian J Med Res. 1976;64: 1403–1413. pmid:828146
[19]
Saluzzo JF, Digoutte JP, Camicas JL, Chauvancy G. Crimean-Congo haemorrhagic fever and Rift Valley fever in south-eastern Mauritania. Lancet. 1985;1: 116. pmid:2857020
[20]
Morrill JC, Soliman AK, Imam IZ, Botros BA, Moussa MI, Watts DM. Serological evidence of Crimean-Congo haemorrhagic fever viral infection among camels imported into Egypt. J Trop Med Hyg. 1990;93: 201–204. pmid:2112203
[21]
Mariner JC, Morrill J, Ksiazek TG. Antibodies to hemorrhagic fever viruses in domestic livestock in Niger: Rift Valley fever and Crimean-Congo hemorrhagic fever. Am J Trop Med Hyg. 1995;53: 217–21. pmid:7573699
[22]
Gergova I, Kamarinchev B. Comparison of the prevalence of Crimean-Congo hemorrhagic fever virus in endemic and non-endemic Bulgarian locations. J Vector Borne Dis. 2013;50: 265–70. pmid:24499848
[23]
Németh V, Oldal M, Egyed L, Gyuranecz M, Erdélyi K, Kvell K, et al. Serologic evidence of Crimean-Congo hemorrhagic fever virus infection in Hungary. Vector Borne Zoonotic Dis. 2013;13: 270–2. doi: 10.1089/vbz.2012.1011. pmid:23421895
[24]
Mertens M, Vatansever Z, Mrenoshki S, Krstevski K, Stefanovska J, Djadjovski I, et al. Circulation of Crimean-Congo Hemorrhagic Fever Virus in the Former Yugoslav Republic of Macedonia Revealed by Screening of Cattle Sera Using a Novel Enzyme-linked Immunosorbent Assay. PLoS Negl Trop Dis. 2015;9: e0003519. doi: 10.1371/journal.pntd.0003519. pmid:25742017
[25]
Guilherme JM, Gonella-Legall C, Legall F, Nakoume E, Vincent J. Seroprevalence of five arboviruses in Zebu cattle in the Central African Republic. Trans R Soc Trop Med Hyg. 1996;90: 31–33. doi: 10.1016/S0035-9203(96)90468-X. pmid:8730305
[26]
Ibrahim AM, Adam I a., Osman BT, Aradaib IE. Epidemiological survey of Crimean Congo hemorrhagic fever virus in cattle in East Darfur State, Sudan. Ticks Tick Borne Dis. Elsevier GmbH.; 2015;6: 439–444. doi: 10.1016/j.ttbdis.2015.03.002.
[27]
Barthel R, Mohareb E, Younan R, Gladnishka T, Kalvatchev N, Moemen A, et al. Seroprevalance of Crimean–Congo haemorrhagic fever in Bulgarian livestock. Biotechnol Biotechnol Equip. Taylor & Francis; 2014;28: 540–542. doi: 10.1080/13102818.2014.931685. pmid:26019541
[28]
Burt FJ, Swanepoel R, Braack LE. Enzyme-linked immunosorbent assays for the detection of antibody to Crimean-Congo haemorrhagic fever virus in the sera of livestock and wild vertebrates. Epidemiol Infect. 1993;111: 547–557. doi: 10.1017/S0950268800057277. pmid:8270014
[29]
Palomar AM, Portillo A, Santibanez P, Mazuelas D, Arizaga J, Crespo A, et al. Crimean-Congo Hemorrhagic Fever Virus in Ticks from Migratory Birds, Morocco. Emerg Infect Dis. 2013;19: 260–263. doi: http://dx.doi.org/10.3201/eid1902.121193. pmid:23347801
[30]
Lindeborg M, Barboutis C, Ehrenborg C, Fransson T, Jaenson TGT, Lindgren P- E, et al. Migratory Birds, Ticks, and Crimean-Congo Hemorrhagic Fever Virus. Emerg Infect Dis. 2012;18. doi: 10.3201/eid1812.120718.
[31]
Estrada-Pe？a A, Palomar A, Santibá？ez P, Sánchez N, Habela M, Portillo A, et al. Crimean-Congo Hemorrhagic Fever Virus in Ticks, Southwestern Europe, 2010. Emerg Infect Dis. 2012;18: 179–180. doi: 10.3201/eid1801.111040. pmid:22261502
[32]
Smirnova SE, Nepesova NM, Tachmuradov G, Kir’Yanova AM, Chumakov MP. Data on studying Crimean hemorrhagic fever in Turkmen SSR. NAMRU-T804. Tr Inst Polio Virus Entsef Akad Med Nauk SSSR. 1971;19: 86–91.
[33]
Ceianu CS, Panculescu-Gatej RI, Coudrier D, Bouloy M. First Serologic Evidence for the Circulation of Crimean-Congo Hemorrhagic Fever Virus in Romania. Vector-Borne Zoonotic Dis. 2012;12: 718–721. doi: 10.1089/vbz.2011.0768. pmid:22897346
[34]
Mustafa ML, Ayazi E, Mohareb E, Yingst S, Zayed A, Rossi C, et al. Crimean-Congo haemorrhagic fever, Afghanistan, 2009. Emerg Infect Dis. 2011;17: 1940–1941. doi: 10.3201/eid1710.110061. pmid:22000377
[35]
Tantawi H, Shony M, Al-Tikriti SK. Antibodies to Crimean-Congo haemorrhagic fever virus in domestic animals in Iraq: a seroepidemiological survey. Int J Zoon. 1981;8: 115–120.
[36]
Pak TP. Epidemiology of Crimean hemorrhagic fever in Tadzhik SSR. NAMRU-T1188. Inst Polio Virus Entsef, Akad Med Nauk SSSR Moskva. 1970. p. 26.
[37]
Swanepoel R, Shepherd AJ, Leman P, Shepherd SP, Mcgillivray M, Erasmus MJ, et al. Epidemiologic and clinical features of Crimean-Congo hemorrhagic fever in Southern Africa. Amercian J Top Med Hygeine. 1987;36: 120–132.
[38]
Darwish M, Imam I, Omar F, Hoogstraal H. Results of a preliminary seroepidemiological survey for Crimean-Congo hemorrhagic fever virus in Egypt. Acta virol. 1978;22: 77. pmid:25013
[39]
Horton KC, Wasfy M, Samaha H, Abdel-Rahman B, Safwat S, Abdel Fadeel M, et al. Serosurvey for zoonotic viral and bacterial pathogens among slaughtered livestock in egypt. Vector Borne Zoonotic Dis. 2014;14: 633–9. doi: 10.1089/vbz.2013.1525. pmid:25198525
[40]
Rodrigues FM, Padbidri VS, Ghalsasi GR, Gupta NP, Mandke VB, Pinto BD, et al. Prevalence of Crimean haemorrhagic fever-Congo virus in Jammu & Kashmir State. Indian J Med Res. 1986; 134–138. pmid:3093378
[41]
Yadav PD, Gurav YK, Mistry M, Shete AM, Sarkale P, Deoshatwar AR, et al. Emergence of Crimean-Congo hemorrhagic fever in Amreli District of Gujarat State, India, June to July 2013. Int J Infect Dis. 2014;18: 97–100. doi: 10.1016/j.ijid.2013.09.019. pmid:24211848
[42]
Mourya DT, Yadav PD, Shete AM, Gurav YK, Raut CG, Jadi RS, et al. Detection, isolation and confirmation of Crimean-Congo hemorrhagic fever virus in human, ticks and animals in Ahmadabad, India, 2010–2011. PLoS Negl Trop Dis. 2012;6: e1653. doi: 10.1371/journal.pntd.0001653. pmid:22616022
[43]
Darwish MA, Hoogstraal H, Roberts TJ, Ghazi R, Amer T. A sero-epidemiological survey for Bunyaviridae and certain other arboviruses in Pakistan. Trans R Soc Trop Med Hyg. 1983;77: 446–450. doi: 10.1016/0035-9203(83)90108-6. pmid:6415873
[44]
Sun S, Dai X, Aishan M, Wang X, Meng W, Feng C, et al. Epidemiology and phylogenetic analysis of Crimean-Congo hemorrhagic fever viruses in Xinjiang, China. J Clin Microbiol. 2009;47: 2536–2543. doi: 10.1128/JCM.00265-09. pmid:19553586
[45]
Chumakov M, Smirnova S. Detection of antibodies to CHF in wild and domestic animal blood sera from Iran and Africa. NAMRU T1072. Tezisy 17 Nauch Sees Inst Posvyashch Aktual Probl Virus Profil Virus Zabolev. 1972; 367–368.
[46]
Williams RJ, Al-Busaidy S, Mehta FR, Maupin GO, Wagoner KD, Al-Awaidy S, et al. Crimean-congo haemorrhagic fever: a seroepidemiological and tick survey in the Sultanate of Oman. Trop Med Int Health. 2000;5: 99–106. doi: 10.1046/j.1365-3156.2000.00524.x. pmid:10747269
[47]
Khan AS, Maupin GO, Rollin PE, Noor AM, Shurie HH, Shalabi AG, et al. An outbreak of Crimean-Congo hemorrhagic fever in the United Arab Emirates, 1994–1995. Am J Trop Med Hyg. 1997;57: 519–525. pmid:9392589
[48]
Berezin V V., Chumakov MP, Stolbov DN, Butenko AM. On the problem of natural hosts of Crimean hemorrhagic fever virus in Astrakhan region. (In Russian). (In English: NAMRU3-T912). Tr Inst Polio Virusn Entsefalitov Akad Med Nauk SSSR. 1971;19: 210–216.
[49]
Chumakov M. Contribution to 30 years of investigation of Crimean hemorrhagic fever. NAMRU-T950. Tr Inst Polio Virus Entsef Akad Med Naul USSR. 1974;22: 5–18.
[50]
Papa A, Velo E, Papadimitriou E, Cahani G, Kota M, Bino S. Ecology of the Crimean-Congo hemorrhagic fever endemic area in Albania. Vector Borne Zoonotic Dis. 2009;9: 713–716. doi: 10.1089/vbz.2008.0141. pmid:19402760
[51]
Lugaj A, B？rxhol K. Serological Survey of CCHFV in Cattle in 10 Regions of Albania. IMPACT Int J Res Applied, Nat Soc Sci (IMPACT IJRANSS). 2014;2: 55–60.
[52]
Lugaj A, Koni M, Mertens M, Groschup MH, Berxholi K. Serological survey of Crimean-Congo hemorrhagic fever virus in cattle in Berat and Kolonje, Albania. Albanian j agric sci. 2014; 325–328.
[53]
Lugaj A, B？rxholi K. Serological survey of Crimean-Congo hemorrhagic fever virus CCHFV in cattle in Kukes Rreshen, and Gjirokastra regions of Albania. 2nd International conference on Research and Education (ICRAE), ISSN: 2308-0825. Shkodra, Albania; 2014.
[54]
Matevosyan KS, Semashko I, Rubin S, Chumakov M. Antibodies to CHF virus in human and cattle blood sera from Armenia SSR (NAMRU-T939). Tr Inst Polio Virus Entsef Akad Med Nauk SSSR. 1974;22: 173–175.
[55]
Chumakov MP, Ismailova S, Rubin S, Smirnova S, Zgurskaya G, Khankishiev AS, et al. Detection of crimean hemorrhagic fever foci in Azerbaijan SSR from results of serological investigations of domestic animals (NAMRU-T941). Tr Inst Polio Virus Entsef Akad Med Nauk SSSR. 1970;18: 120–122.
[56]
Vasilenko S, Katsarov G, Mikhailov A, Teckharova M, Levi V, Levi S, et al. Crimean hemorrhagic fever (CHF) in Bulgaria. Tr Inst Polio Virus Entsef. 1971;19: 100–111.
[57]
Hassanein K, El-Azazy O, Yousef H. Detection of Crimean-Congo haemorrhagic fever virus antibodies in humans and imported livestock in Saudi Arabia. Trans R Soc Trop Med Hyg. 1997;91: 536–537. pmid:9463660 doi: 10.1016/s0035-9203(97)90014-6
[58]
Horvath L. Incidence of antibodies to Crimean hemorrhagic fever virus in animals. Acta Microbiol Acad Sci Hung. 1975;22: 61–66. pmid:803341
[59]
Horvath LB. Precipitating antibodies to Crimean haemorrhagic fever virus in human sera collected in Hungary. Acta Microbiol Acad Sci Hung. 1976;23: 331–335. pmid:829015
[60]
Mourya DT, Yadav PD, Shete A, Majumdar TD, Kanani A, Kapadia D, et al. Serosurvey of Crimean-Congo hemorrhagic Fever virus in domestic animals, Gujarat, India, 2013. Vector Borne Zoonotic Dis. 2014;14: 690–2. doi: 10.1089/vbz.2014.1586. pmid:25229708
[61]
Lotfollahzadeh S, Nikbakht Boroujeni GR, Mokhber Dezfouli MR, Bokaei S. A serosurvey of Crimean-Congo haemorrhagic fever virus in dairy cattle in Iran. Zoonoses Public Health. 2011;58: 54–9. doi: 10.1111/j.1863-2378.2009.01269.x. pmid:19912604
[62]
Telmadarraiy Z, Ghiasi SM, Moradi M, Vatandoost H, Eshraghian MR, Faghihi F, et al. A survey of Crimean-Congo haemorrhagic fever in livestock and ticks in Ardabil Province, Iran during 2004–2005. Scand J Infect Dis. 2010;42: 137–41. doi: 10.3109/00365540903362501. pmid:19958240
[63]
Chinikar S, Ghiasi SM, Naddaf S, Piazak N, Moradi M, Razavi MR, et al. Serological Evaluation of Crimean-Congo Hemorrhagic Fever in Humans with High-Risk Professions Living in Enzootic Regions of Isfahan Province of Iran and Genetic Analysis of Circulating Strains. Vector-Borne Zoonotic Dis. 2012;12: 733–738. doi: 10.1089/vbz.2011.0634. pmid:22217167
[64]
Mostafavi E, Haghdoost A, Khakifirouz S, Chinikar S. Spatial Analysis of Crimean Congo Hemorrhagic Fever in Iran. Am J Trop Med Hyg. 2013; doi: 10.4269/ajtmh.12-0509.
[65]
Al-Yabis AS, Al-Thamery AAK, Hasony HJ. Seroepidemiology of Crimean-Congo haemorrhagic fever in rural community of Basrah. Med J Basrah Univ. 2005;23: 30–35.
[66]
Semashko I, Dobritsa P, Bashkirtsev V, Chumakov M. Results from investigating blood sera from healthy persons, animals, and birds collected in southern Kazakhstan for antibodies to CHF-Congo virus. NAMRU-T1128. Mater 9 Simp Ekol Virus. 1975; 43–44.
[67]
Fajs L, Humolli I, Saksida A, Knap N, Jelov？ek M, Korva M, et al. Prevalence of Crimean-Congo Hemorrhagic Fever Virus in Healthy Population, Livestock and Ticks in Kosovo. PLoS ONE. 2014;9: e110982. doi: 10.1371/journal.pone.0110982. pmid:25393542
[68]
Umoh J, Ezeokoli C, Ogwu D. Prevalence of antibodies to Crimean-haemorrhagic fever-Congo virus in cattle in northern Nigeria. Int J Zoonoses. 1983;10: 151–4. pmid:6427128
[69]
Berezin V, Chumakov M, Rubin S, Stolbov D, Butenko A, Bashkirtsev V. Contribution to the ecology of Crimean hemorrhagic fever virus in the lower Volga River (NAMRU-T836). Arboviruses. 1969;2: 120–122.
[70]
Badalov M, Butenko A, Karinskaya G, Leshchinskaya E, Rubin S, Tkachenko E, et al. Results of serological investigation of the rural population and domestic animals in Rostov Oblast in connection with the problem of prevention (NAMRU-T834). Mater 16 Nauch Sess Inst Polio Virus Entsef. 1969;2: 117–118.
[71]
Karinskaya G, Chumakov M, Butenko A, Badalow M, Rubin S. Investigation of Antibodies to Crimean Hemorrhagic Fever Virus in Animal Blood Samples from Rostov Oblast. A Transl Crime Hemorrhagic fever Misc Publ Entomol Soc Am. 1974; 147–149.
[72]
Kuchin V, Yanovich T, Butenko A, Kirsanova K. Serological Examination for Antibodies to CHF Virus in Domestic Animals of Rostov Oblast. A Transl Crime Hemorrhagic fever Misc Publ Entomol Soc Am. 1974; 149–150.
[73]
Chunikhin SP, Chumakov MP, Butenko A, Smirnova SE, Taufflieb R, Camicas JL, et al. Results investigating human and domestic and wild animal blood sera in the Senegalese Republic (Western Africa) for antibodies to Crimean hemorrhagic fever virus. (In Russian). (In English: NAMRU-3, T810). Mater 16 Nauch Sess Inst Polio Virus Entsef. Moscow, October 21–23; 1969;2: 158–160.
[74]
Swanepoel R, Shepherd a J, Leman P a, Shepherd SP. Investigations following initial recognition of Crimean-Congo haemorrhagic fever in South Africa and the diagnosis of 2 further cases. S Afr Med J. 1985;68: 638–641. pmid:3933132
[75]
Adam I a, Mahmoud MA, Aradaib IE. A seroepidemiological survey of Crimean Congo hemorrhagic fever among Cattle in North Kordufan State, Sudan. Virol J. Virology Journal; 2013;10: 178. doi: 10.1186/1743-422X-10-178. pmid:23738961
[76]
Smirnova SE, Daniyarov OA, Zgurskaya GN, Kasymov KT, Pavlovich AN, Pak TP, et al. Serological investigation of humans and animals in Tadzhik SSR for antibodies to Crimean hemorrhagic fever virus (from the 1968 data). NAMRU-T964. Tr Inst Polio Virus Entsef Akad Med Nauk SSSR. 1971;19: 66–71.
[77]
Kirya B, Semenov B, Tretiyakov A, Gromashevsky V, Madzhomba E. Preliminary report on investigating animal sera from East Africa for antibodies to Congo virus by the agar gel diffusion and precipitation method. NAMRU-T1073. Tezisy 17 Nauch Sees Inst Posvyashch Aktual Probl Virus Profil Virus Zabolev. 1972; 368–9.
[78]
Nabeth P, Cheikh DO, Lo B, Faye O, Vall IOM, Niang M, et al. Crimean-Congo Hemorrhagic Fever, Mauritania. Emerg Infect Dis. 2004;10: 2143–2149. pmid:15663851 doi: 10.3201/eid1012.040535
[79]
Humolli I, Dedushaj I, Zupanac TA, Mu？aj S. Epidemiological, serological and herd immunity of Crimean-Congo haemorrhagic fever in Kosovo. Med Arh. 2010;64: 91–93. pmid:20514773
[80]
Mostafavi E, Chinikar S, Moradi M, Bayat N, Meshkat M, Fard MK, et al. A case report of Crimean Congo hemorrhagic Fever in ostriches in Iran. Open Virol J. 2013;7: 81–3. doi: 10.2174/1874357901307010081. pmid:24015162
[81]
Papa A, Chaligiannis I, Kontana N, Sourba T, Tsioka K, Tsatsaris A, et al. A novel AP92-like Crimean-Congo hemorrhagic fever virus strain, Greece. Ticks Tick Borne Dis. 2014;5: 590–3. doi: 10.1016/j.ttbdis.2014.04.008. pmid:24953797
[82]
Mostafavi E, Chinikar S, Esmaeili S, Amiri FB, Tabrizi AMA, KhakiFirouz S. Seroepidemiological Survey of Crimean-Congo Hemorrhagic Fever Among Sheep in Mazandaran Province, Northern Iran. Vector-Borne Zoonotic Dis. 2012;12: 739–742. doi: 10.1089/vbz.2011.0958. pmid:22917135
[83]
Wilson ML, Leguenno B, Guillaud M. Distribution of Crimean-Congo hemorrhagic viral antibody in Senegal: environmental and vectorial correlates. Am J Trop Med Hyg. 1990;43: 557–566. pmid:2122750
[84]
Papa A, Sidira P, Kallia S, Ntouska M, Zotos N, Doumbali E, et al. Factors associated with IgG positivity to Crimean-Congo hemorrhagic fever virus in the area with the highest seroprevalence in Greece. Ticks Tick Borne Dis. Elsevier GmbH.; 2013;4: 417–420. doi: 10.1016/j.ttbdis.2013.04.003. pmid:23831367
[85]
Yu-Chen Y, Ling-Xiong K, Ling L, Yu-Qin Z, Feng L, Bao-Jian C, et al. Characteristics of Crimean-Congo hemorrhagic fever virus (Xinjiang strain) in China. Am J Trop Med Hyg. 1985;34: 1179–1182. pmid:2422968
[86]
Chumakov M, Vafakulov BK, Zavodova T, Karmysheva VY, Maksumov S, Mart’Yanova LI, et al. Cases of Crimean hemorrhagic fever transmission in Uzbekistan through contacts with the blood of a sick cow and a patient and also by tickbites (NAMRU-T1111). Tr Inst Polio Virus Entsef Akad Med Nauk SSSR. 1974;22: 29–34.
[87]
Chinikar S, Ghiasi SM, Moradi M, Goya MM, Shirzadi MR, Zeinali M, et al. Geographical distribution and surveillance of Crimean-Congo hemorrhagic fever in Iran. Vector Borne Zoonotic Dis. 2010;10: 705–8. doi: 10.1089/vbz.2009.0247. pmid:20854025
[88]
Kadanali A, Erol S, Ozkurt Z, Ozden K. Epidemiological risk factors for Crimean-Congo hemorrhagic fever patients. Turk J Med Sci. 2009;39: 829–832. doi: 10.3906/sag-0904-49.
[89]
Sargianou M, Panos G, Tsatsaris A, Gogos C, Papa A. Crimean-Congo hemorrhagic fever: seroprevalence and risk factors among humans in Achaia, western Greece. Int J Infect Dis. International Society for Infectious Diseases; 2013;17: e1160–e1165. doi: 10.1016/j.ijid.2013.07.015. pmid:24084247
[90]
Christova I, Gladnishka T, Taseva E, Kalvatchev N, Tsergouli K, Papa A. Seroprevalence of Crimean-Congo Hemorrhagic Fever Virus, Bulgaria. Emerg Infect Dis. 2013;19: 177–179. doi: 10.3201/eid1901.120299. pmid:23260369
[91]
Lwande OW, Irura Z, Tigoi C, Chepkorir E, Orindi B, Musila L, et al. Seroprevalence of Crimean Congo Hemorrhagic Fever Virus in Ijara District, Kenya. Vector-Borne Zoonotic Dis. 2012;12: 727–732. doi: 10.1089/vbz.2011.0914. pmid:22925021
[92]
Sharifi-Mood B, Metanat M, Alavi-Naini R. Prevalence of crimean-congo hemorrhagic Fever among high risk human groups. Int J high risk Behav Addict. 2014;3: e11520. doi: 10.5812/ijhrba.11520. pmid:24971294
[93]
Camicas JL, Wilson ML, Cornet J, Digoutte J, Calvo M, Adam F, et al. Ecology of ticks as potential vectors of Crimean-Congo hemorrhagic fever virus in Senegal: epidemiological implications. Arch Virol. 1990;1: 303–322. doi: 10.1007/978-3-7091-9091-3_34
[94]
Fakoorziba MR, Golmohammadi P, Moradzadeh R, Moemenbellah-Fard MD, Azizi K, Davari B, et al. Reverse Transcription PCR-Based Detection of Crimean-Congo Hemorrhagic Fever Virus Isolated from Ticks of Domestic Ruminants in Kurdistan Province of Iran. Vector-Borne Zoonotic Dis. 2012;12: 794–799. doi: 10.1089/vbz.2011.0743. pmid:22651389
[95]
Zeller HG, Cornet JP, Diop a, Camicas JL. Crimean-Congo hemorrhagic fever in ticks (Acari: Ixodidae) and ruminants: field observations of an epizootic in Bandia, Senegal (1989–1992). J Med Entomol. 1997;34: 511–516. pmid:9379454
[96]
Watts DM, Ksiasek T, Unthicum K, Hoogstraal H. Crimean-Congo hemorrhagic fever. The arboviruses epidemiology and ecology, vol 2 CRC. Mona T. P. Boca Raton, FL; 1988. pp. 177–260.
[97]
Gunes T, Poyraz O, Vatansever Z. Crimean-Congo Hemorrhagic Fever Virus in Ticks Collected from Humans, Livestock, and Picnic Sites in the Hyperendemic Region of Turkey. Vector-Borne Zoonotic Dis. 2011;11: 1411–1416. doi: 10.1089/vbz.2011.0651. pmid:21736490
[98]
Papadopoulos O, Koptopoulos G. Isolation of Crimean-Congo hemorrhagic fever (CCHF) virus from Rhipicephalus bursa ticks in Greece. Acta Microbiol Hell. 1978;23: 20–28.
[99]
Keshtkar-Jahromi M, Sajadi MM, Ansari H, Mardani M, Holakouie-Naieni K. Crimean-Congo hemorrhagic fever in Iran. Antiviral Res. 2013;100: 20–8. doi: 10.1016/j.antiviral.2013.07.007. pmid:23872313
[100]
Berezin V V., Povalishina TP, Ermakova RM, Stolbov DN. On the role of birds in feeding immature stages of Hyalomma plumbeum plumbeum ticks-vectors of hemorrhagic fever of the Crimean type in foci of the Volga Delta. (In Russian). (In English, NAMRU3- Tl98). Tr Inst Polio Virusn Entsefalitov Akad Med Nauk SSSR. 1965;7: 296–303.
[101]
Blagoveshchenskaya N, Donets M, Zaruna L, Kondratenko VF, Kuchin V. Study of susceptibility to Crimean hemorrhagic fever (CHF) virus in European and long-eared hedgehogs (In Russian). (In English: NAMRU-T985). Tezisy Konf Vop Med Virus. 1975; 269–270.
[102]
Zarubinsky VY, Klisenko GA, Kuchin V V., Timchenko V V., Shanoyan NK. Application of the indirect hemagglutination inhibition test for serological investigation of Crimean hemorrhagic fever focus in Rostov Oblast. (In Russian). (In English, NAMRU3-T1145). Sb Tr Inst Virus Im D I Ivanov Akad Med Nauk SSSR. 1975;2: 73–77.
[103]
Smirnova SE, Zgurskaya GN, Nepesova NM, Pak TP, Chumakov MP, Chunikhin SP. Examination of animal blood samples in Central Asia for antibodies to Crimean hemorrhagic fever virus (CHF). (In Russian). (In English, NAMRU3-T820). Mater 16 Nauch Sess Inst Polio Virus Entsef. Moscow, October; 1969;2: 146–47.
[104]
Tkachenko E, Khanun K, Berezin V. Serological investigation of human and animal sera in agar gel diffusion and precipitation (AGDP) test for the presence of antibodies of Crimean hemorrhagic fever and Grand Arbaud viruses. (In Russian). (In English, NAMRU3-T620). Mater 16 Nauch Sess Inst Polio Virus Entsef. Moscow, October; 1969;2: 265.
[105]
Chunikhin SP, Chumakov MP, Smirnova SE, Pak TP, Pavlovich AN, Kuima AU. Division into biocenotic groups of mammals and ixodid ticks in Crimean hemorrhagic foci of southern Central Asia. (In Russian). (In English, NAMRU3-T821). Mater 16 Nauch Sess Inst Polio Virus Entsef. Moscow, October; 1969. pp. 156–57.
[106]
Arata AA. The importance of small mammals in public health. Int Biol Program. 1975;5: 349–59.
[107]
Dacheux L, Cervantes-Gonzalez M, Guigon G, Thiberge JM, Vandenbogaert M, Maufrais C, et al. A preliminary study of viral metagenomics of french bat species in contact with humans: Identification of new mammalian viruses. PLoS ONE. 2014;9. doi: 10.1371/journal.pone.0087194.
[108]
Ishii A, Ueno K, Orba Y, Sasaki M, Moonga L, Hang BM, et al. A nairovirus isolated from African bats causes haemorrhagic gastroenteritis and severe hepatic disease in mice. Nat commincations. 2014; doi: 10.1038/ncomms6651.
[109]
？iroky P, Bělohlávek T, Papou？ek I, Jandzik D, Mikulí？ek P, Kubelová M, et al. Hidden threat of tortoise ticks: high prevalence of Crimean-Congo haemorrhagic fever virus in ticks Hyalomma aegyptium in the Middle East. Parasit Vectors. 2014;7: 101. doi: 10.1186/1756-3305-7-101. pmid:24618184
[110]
Capek M, Literak I, Kocianova E, Sychra O, Najer T, Trnka A, et al. Ticks of the Hyalomma marginatum complex transported by migratory birds into Central Europe. Ticks Tick Borne Dis. Elsevier GmbH.; 2014;5: 489–493. doi: 10.1016/j.ttbdis.2014.03.002. pmid:24877976
[111]
Jameson LJ, Morgan PJ, Medlock JM, Watola G, Vaux AGC. Importation of Hyalomma marginatum, vector of Crimean-Congo haemorrhagic fever virus, into the United Kingdom by migratory birds. Ticks Tick Borne Dis. Elsevier GmbH.; 2012;3: 95–99. doi: 10.1016/j.ttbdis.2011.12.002. pmid:22300969
[112]
Gale P, Stephenson B, Brouwer a., Martinez M, de la Torre a., Bosch J, et al. Impact of climate change on risk of incursion of Crimean-Congo haemorrhagic fever virus in livestock in Europe through migratory birds. J Appl Microbiol. 2012;112: 246–257. doi: 10.1111/j.1365-2672.2011.05203.x. pmid:22118269
[113]
Berezin V, Stolbov D, Povalishchina T, Zimina Y. On the role of rooks in the epidemiology of Crimean hemorrhagic fever in Astrakhan Oblast (NAMRU-T376). Tr Inst Pollo Virus Entsef Akad Mad Nauk SSSR. 1965;7: 304–311.
[114]
Zeller HG, Cornet JP, Camicas JL. Crimean-Congo haemorrhagic fever virus infection in birds: field investigations in Senegal. Res Virol. 1994;145: 105–9. pmid:8059064
[115]
Zeller HG, Cornet JP, Camicas JL. Experimental transmission of Crimean-Congo hemorrhagic fever virus by West African wild ground-feeding birds to Hyalomma Marginatum Rufipes ticks. Am J Trop Med. 1994;50: 676–681.
[116]
Swanepoel R, Leman PA, Burt FJ, Jardine J, Verwoerd DJ, Capua I, et al. Experimental infection of ostriches with Crimean-Congo haemorrhagic fever virus. Epidemiol Infect. 1998;121: 427–32. pmid:9825796
[117]
Causey OR, Kemp GE, Madbouly MH, David-West TS. Congo virus from domestic livestock, African hedgehog, and arthropods in Nigeria. Am J Trop Med Hyg. 1970;19: 846–850. pmid:5453910
[118]
Rabinovich V, Blagoveshchenskaya N, Butenko A, Zarubina L, Kondratenko VF, Milyutin V. Virological and Serological Examination of Wild Animals and Birds in Rostov Oblast CHF focus (NAMRU-T650). Third Regional Workshop at Rostov-on-Don in May 1970. 1970. pp. 138–139.
[119]
Smirnova SE. A Comparative Study of the Crimean Hemorrhagic Fever-Congo Group of Viruses. Arch Virol. 1979;62: 137–143. pmid:94536 doi: 10.1007/bf01318066
[120]
Shepherd AJ, Swanepoel R, Cornel A, Mathee O. Experimental studies on the replication and transmission of Crimean-Congo hemorrhagic fever virus in some African tick species. Am J Trop Med Hyg. 1989;40: 326–331. pmid:2494900
[121]
Fagbami AH, Tomori O, Fabiyi A, Isoun T. Experimental Congo virus (Ib-AN 7620) infection in primates. Virologie. 1975;26: 33–37. pmid:814708
[122]
Obukhova V, Klisenko G, Lapina T. Indirect hemagglutination inhibition test for serological diagnosis of CHF (. Sborn Tr Inst Virus Im D I Ivanov Akad Med Nauk SSSR. 1978;3: 110–113.
[123]
Swanepoel R, Struthers JK, Erasmus MJ, Shepherd SP, McGillivray GM, Erasmus BJ, et al. Comparison of techniques for demonstrating antibodies to Rift Valley fever virus. J Hyg (Lond). 1986;97: 317–329. doi: 10.1017/S0022172400065414.
[124]
Donets M, Rezapkin G, Ivanov A, Tkachenko E. Immunosorbent Assays for Diagnosis of Crimean-Congo Hemorrhagic Fever (CCHF). Am J Trop Med Hyg. 1982;31: 156–162. pmid:6800272
[125]
Qing T, Saijo M, Lei H, Niikura M, Maeda A, Ikegami T, et al. Detection of immunoglobulin G to Crimean-Congo hemorrhagic fever virus in sheep sera by recombinant nucleoprotein-based enzyme- linked immunosorbent and immunofluorescence assays. J Virol Methods. 2003;108: 111–116. pmid:12565161
[126]
Kagunyu AW, Wanjohi J. Camel rearing replacing cattle production among the Borana community in Isiolo County of Northern Kenya, as climate variability bites. Pastor Res Policy Pract. 2014;4: 13. doi: 10.1186/s13570-014-0013-6.
[127]
Rodriguez LL, Maupin G, Ksiazek TG, Rollin PE, Khan AS, Schwarz TE, et al. Molecular investigation of a multisource outbreak of Crimean-Congo hemorrhagic fever in the United Arab Emirates. Am J Trop Med Hyg. 1997;57: 512–518. pmid:9392588
[128]
Jaureguiberry S, Tattevin P, Tarantola A, Legay F, Tall A, Nabeth P, et al. Imported Crimean-Congo hemorrhagic fever. J Clin Microbiol. 2005;43: 4905–4907. doi: 10.1128/JCM.43.9.4905. pmid:16145173
[129]
Lumley S, Atkinson B, Dowall SD, Pitman JK, Staplehurst S, Busuttil J, et al. Non-fatal case of crimean-congo haemorrhagic fever imported into the United Kingdom (ex Bulgaria), June 2014. Eurosurveillance. 2014;19: 3–5. doi: 10.2807/1560-7917.ES2014.19.30.20864.
