Journals / Iğdır Üniversitesi Fen Bilimleri Enstitüsü Dergisi / 2026 / Cilt: 14 Sayı: 2

Crimean-Congo Haemorrhagic Fever Virus: From Genomic Insights to Control Strategies

Yonca Keşkek Türk(University of Leeds, Faculty of Medicine and Health)0000-0002-7955-086X
Fatma Necmiye Kacı(University of Leeds, Faculty of Medicine and Health)0000-0003-3745-8173
Pages
650–667
Publication Date
2024-06-01
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AI Summary & Key Takeaways

AI Insight
⚡ TL;DR(Too Long; Didn't Read)

This review demonstrates general knowledge of CCHFV, summarising its molecular biology, pathogenesis, diagnosis, epidemiology, sustaining and transmission, treatment and prevention strategies, including vaccine candidates.

📌 3 Key Takeaways

🎯
Objective & Hypothesis:Crimean-Congo hemorrhagic fever virus (CCHFV) is a life-threatening arthropod-borne virus transmitted by tick bites or contact with blood or tissues of viraemic individuals and animals.
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Key Findings & Data:CCHFV continues its existence in a broad region with sporadic cases or outbreaks.
💡
Conclusion & Impact:This review demonstrates general knowledge of CCHFV, summarising its molecular biology, pathogenesis, diagnosis, epidemiology, sustaining and transmission, treatment and prevention strategies, including vaccine candidates.
🔬Design:Review & Systematic Survey
📍Scope:Comprehensive Sample
⚙️Variables:Crimean-Congo haemorrhagic fever (CCHFV) · Viral haemorrhagic fevers · Tick-borne

Abstract

Crimean-Congo hemorrhagic fever virus (CCHFV) is a life-threatening arthropod-borne virus transmitted by tick bites or contact with blood or tissues of viraemic individuals and animals. CCHFV continues its existence in a broad region with sporadic cases or outbreaks. CCHFV infection is observed frequently as an asymptomatic, but sudden severe disease characterised by haemorrhagic can occur. Diagnostic methods employ enzyme-linked immunosorbent assay (ELISA) and real-time reverse transcription-polymerase chain reaction (RT-PCR). Although ribavirin has been recommended in treatment besides supportive therapy approaches, no antiviral or vaccine for CCHF is currently approved. This review demonstrates general knowledge of CCHFV, summarising its molecular biology, pathogenesis, diagnosis, epidemiology, sustaining and transmission, treatment and prevention strategies, including vaccine candidates.

🔖

Cite This Article

Türk, Y. K., Kacı, F. N. (2024). Crimean-Congo Haemorrhagic Fever Virus: From Genomic Insights to Control Strategies. Iğdır Üniversitesi Fen Bilimleri Enstitüsü Dergisi, Cilt: 14 Sayı: 2, 650–667. https://doi.org/10.21597/jist.1412021

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References (130)

  1. Adamu, A. M., Onoja, A. B., Ugbodu, V. E., Bala, R. S., Maina, M., Salisu, U. S., … Adegboye, O. (2024). Investigating Crimean-Congo Haemorrhagic Fever Virus Seropositivity in Camels and Human Behavioural Risks in an Abattoir in Nigeria. Epidemiology and Infection, 1, 1–8. https://doi.org/10.1017/S0950268824000189
  2. Ahata, B., & Akçapınar, G. B. (2023). CCHFV vaccine development, current challenges, limitations, and future directions. Frontiers in Immunology, 14(September), 1–18. https://doi.org/10.3389/fimmu.2023.1238882
  3. Ahmeti, S., Berisha, L., Halili, B., Ahmeti, F., von Possel, R., Thomé-Bolduan, C., … Emmerich, P. (2019). Crimean-congo hemorrhagic fever, Kosovo, 2013–2016. Emerging Infectious Diseases, 25(2), 321–324. https://doi.org/10.3201/eid2502.171999
  4. Akuffo, R., Brandful, J. A. M., Zayed, A., Adjei, A., Watany, N., Fahmy, N. T., … Dueger, E. (2016). Crimean-Congo hemorrhagic fever virus in livestock ticks and animal handler seroprevalence at an abattoir in Ghana. BMC Infectious Diseases, 16(1), 1–5. https://doi.org/10.1186/s12879-016-1660-6
  5. Al-Abri, S. S., Hewson, R., Al-Kindi, H., Al-Abaidani, I., Al-Jardani, A., Al-Maani, A., … Beeching, N. J. (2019). Clinical and molecular epidemiology of Crimean-Congo hemorrhagic fever in Oman. PLoS Neglected Tropical Diseases, 13(4), 1–15. https://doi.org/10.1371/journal.pntd.0007100
  6. Albayrak, H., Ozan, E., & Kurt, M. (2012). Serosurvey and molecular detection of Crimean-Congo hemorrhagic fever virus (CCHFV) in northern Turkey. Tropical Animal Health and Production, 44(7), 1667–1671. https://doi.org/10.1007/s11250-012-0122-4
  7. Antoniadis, A., Alexiou-Daniel, S., Malissiovas, N., Doutsos, J., Polyzoni, T., LeDue, J. W., … Saviolakis, G. (1991). Seroepidemiological survey for antibodies to arboviruses in Greece. Hemorrhagic Fever with Renal Syndrome, Tick-and Mosquito-Borne Viruses, 277–285. Springer.
  8. Arteaga, L. M., Bellido, J. L. M., Lista, M. C. V., Santiago, M. B. V., Soto, P. F., Bas, I., … Muro, A. (2020). Crimean-Congo haemorrhagic fever (CCHF) virusspecific antibody detection in blood donors, Castile-León, Spain, summer 2017 and 2018. Eurosurveillance, 25(10), 1–7. https://doi.org/10.2807/1560-7917.ES.2020.25.10.1900507
  9. Atwan, Z., Alhilfi, R., Mousa, A. K., Rawaf, S., Torre, J. D. L., Hashim, A. R., … Tabche, C. (2024). Alarming update on incidence of Crimean-Congo hemorrhagic fever in Iraq in 2023. IJID Regions, 10(November 2023), 75–79. https://doi.org/10.1016/j.ijregi.2023.11.018
  10. Barnwal, B., Karlberg, H., Mirazimi, A., & Tan, Y. J. (2016). The non-structural protein of Crimean-Congo hemorrhagic fever virus disrupts the mitochondrial membrane potential and induces apoptosis. Journal of Biological Chemistry, 291(2), 582–592. https://doi.org/10.1074/jbc.M115.667436
  11. Bartolini, B., Gruber, C. E. M., Koopmans, M., Avšič, T., Bino, S., Christova, I., … Di Caro, A. (2019). Laboratory management of Crimean-Congo haemorrhagic fever virus infections: Perspectives from two European networks. Eurosurveillance, 24(5), 1–14. https://doi.org/10.2807/1560-7917.ES.2019.24.5.1800093
  12. Bente, D. A., Forrester, N. L., Watts, D. M., McAuley, A. J., Whitehouse, C. A., & Bray, M. (2013). Crimean-Congo hemorrhagic fever: History, epidemiology, pathogenesis, clinical syndrome and genetic diversity. Antiviral Research, 100(1), 159–189. https://doi.org/10.1016/j.antiviral.2013.07.006
  13. Bergeron, É., Albariño, C. G., Khristova, M. L., & Nichol, S. T. (2010). Crimean-Congo Hemorrhagic Fever Virus-Encoded Ovarian Tumor Protease Activity Is Dispensable for Virus RNA Polymerase Function. Journal of Virology, 84(1), 216–226. https://doi.org/10.1128/jvi.01859-09
  14. Bernard, C., Holzmuller, P., Bah, M. T., Bastien, M., Combes, B., Jori, F., … Vial, L. (2022). Systematic Review on Crimean–Congo Hemorrhagic Fever Enzootic Cycle and Factors Favoring Virus Transmission: Special Focus on France, an Apparently Free-Disease Area in Europe. Frontiers in Veterinary Science, 9(July), 1–17. https://doi.org/10.3389/fvets.2022.932304
  15. Bernard, C., Joly Kukla, C., Rakotoarivony, I., Duhayon, M., Stachurski, F., Huber, K., … Vial, L. (2024). Detection of Crimean-Congo haemorrhagic fever virus in Hyalomma marginatum ticks, southern France, May 2022 and April 2023. Euro Surveillance: Bulletin Europeen Sur Les Maladies Transmissibles = European Communicable Disease Bulletin, 29(6), 1–6. https://doi.org/10.2807/1560-7917.ES.2024.29.6.2400023
  16. Bertolotti-Ciarlet, A., Smith, J., Strecker, K., Paragas, J., Altamura, L. A., McFalls, J. M., … Doms, R. W. (2005). Cellular Localization and Antigenic Characterization of Crimean-Congo Hemorrhagic Fever Virus Glycoproteins. Journal of Virology, 79(10), 6152–6161. https://doi.org/10.1128/jvi.79.10.6152-6161.2005
  17. Blair, P. W., Kuhn, J. H., Pecor, D. B., Apanaskevich, D. A., Kortepeter, M. G., Cardile, A. P., … Keshtkar-Jahromi, M. (2019). An emerging biothreat: Crimean-Congo hemorrhagic fever virus in southern and western Asia. American Journal of Tropical Medicine and Hygiene, 100(1), 16–23. https://doi.org/10.4269/ajtmh.18-0553
  18. Bodur, H., Akinci, E., Ascioglu, S., Öngürü, P., & Uyar, Y. (2012). Subclinical infections with Crimean-Congo hemorrhagic fever virus, Turkey. Emerging Infectious Diseases, 18(4), 640–642. https://doi.org/10.3201/eid1804.111374
  19. Body, M. H. H., Abdulmajeed, H. Al., Hammad, M. H., Mohamed, S. A., Saif, S. Alh., Salim, A.-M., … Rajamony, S. (2016). Cross-sectional survey of Crimean-Congo hemorrhagic fever virus in the sultanate of Oman. Journal of Veterinary Medicine and Animal Health, 8(6), 44–49.
  20. Bonnet, S. I., Bertagnoli, S., Falchi, A., Figoni, J., Fite, J., Hoch, T., … Vial, L. (2023). An Update of Evidence for Pathogen Transmission by Ticks of the Genus Hyalomma. Pathogens, 12(4), 1–19. https://doi.org/10.3390/pathogens12040513
  21. Bonnet, S. I., Vourc’h, G., Raffetin, A., Falchi, A., Figoni, J., Fite, J., … Quillery, E. (2022). The control of Hyalomma ticks, vectors of the Crimean–Congo hemorrhagic fever virus: Where are we now and where are we going? PLoS Neglected Tropical Diseases, 16(11), 1–23. https://doi.org/10.1371/journal.pntd.0010846
  22. Bonney, L. C., Watson, R. J., Afrough, B., Mullojonova, M., Dzhuraeva, V., Tishkova, F., & Hewson, R. (2017). A recombinase polymerase amplification assay for rapid detection of Crimean-Congo Haemorrhagic fever Virus infection. PLOS Neglected Tropical Diseases, 11(10), e0006013. https://doi.org/10.1371/journal.pntd.0006013
  23. Bouaicha, F., Eisenbarth, A., Elati, K., Schulz, A., Ben Smida, B., Bouajila, M., … Khamassi Khbou, M. (2021). Epidemiological investigation of Crimean-Congo haemorrhagic fever virus infection among the one-humped camels (Camelus dromedarius) in southern Tunisia. Ticks and Tick-Borne Diseases, 12(1). https://doi.org/10.1016/j.ttbdis.2020.101601
  24. Burney, M. I., Ghafoor, A., Webb, P. A., Saleen, M., & Casals, J. (1980). Nosocomial Outbrak of Viral Hemorrhagic Fever Caused by Crimean Hemorrhagic Fever-Congo Virus in Pakistan, January 1976 *. The American Journal of Tropical Medicine and Hygiene, 29(5), 941–947. https://doi.org/10.4269/ajtmh.1980.29.941
  25. Burt, F. J., Leman, P. A., Smith, J. F., & Swanepoel, R. (1998). The use of a reverse transcription-polymerase chain reaction for the detection of viral nucleic acid in the diagnosis of Crimean-Congo haemorrhagic fever. Journal of Virological Methods, 70(2), 129–137. https://doi.org/10.1016/S0166-0934(97)00182-1
  26. Casals, J. (1969). Antigenic similarity between the virus causing Crimean hemorrhagic fever and Congo virus. Proceedings of the Society for Experimental Biology and Medicine, 131(1), 233–236. https://doi.org/https://doi.org/10.3181/00379727-131-33847
  27. Chinikar, S., Ghiasi, S. M., Naddaf, S., Piazak, N., Moradi, M., Razavi, M. R., … Ataei, B. (2012). 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 and Zoonotic Diseases, 12(9), 733–738.
  28. Chinikar, S., Shayesteh, M., Khakifirouz, S., Jalali, T., Rasi Varaie, F. S., Rafigh, M., … Shah-Hosseini, N. (2013). Nosocomial infection of Crimean-Congo haemorrhagic fever in eastern Iran: Case report. Travel Medicine and Infectious Disease, 11(4), 252–255. https://doi.org/10.1016/j.tmaid.2012.11.009
  29. Conger, N. G., Paolino, K. M., Osborn, E. C., Rusnak, J. M., Günther, S., Pool, J., … Rieger, T. (2015). Health care response to CCHF in US soldier and nosocomial transmission to health care providers, Germany, 2009. Emerging Infectious Diseases, 21(1), 23.
  30. Cooper, R. G., Horbanczuk, J. O., & Fujihara, N. (2004). Viral diseases of the Ostrich (Struthio camelus var. domesticus). Animal Science Journal, 75(2), 89–95. https://doi.org/10.1111/j.1740-0929.2004.00161.x
  31. D’Addiego, J., Elaldi, N., Wand, N., Osman, K., Bagci, B. K., Kennedy, E., … Hewson, R. (2023). Investigating the effect of ribavirin treatment on genetic mutations in Crimean–Congo haemorrhagic fever virus (CCHFV) through next-generation sequencing. Journal of Medical Virology, 95(2). https://doi.org/10.1002/jmv.28548 de la Fuente, J., & Contreras, M. (2022). Additional considerations for anti-tick vaccine research. Expert Review of Vaccines, 21(8), 1019–1021. https://doi.org/10.1080/14760584.2022.2071704
  32. Dowall, S. D., Richards, K. S., Graham, V. A., Chamberlain, J., & Hewson, R. (2012). Development of an indirect ELISA method for the parallel measurement of IgG and IgM antibodies against Crimean-Congo haemorrhagic fever (CCHF) virus using recombinant nucleoprotein as antigen. Journal of Virological Methods, 179(2), 335–341. https://doi.org/10.1016/j.jviromet.2011.11.020
  33. Drosten, C., Göttig, S., Schilling, S., Asper, M., Panning, M., Schmitz, H., & Günther, S. (2002). Rapid detection and quantification of RNA of Ebola and Marburg viruses, Lassa virus, Crimean-Congo hemorrhagic fever virus, Rift Valley fever virus, dengue virus, and yellow fever virus by real-time reverse transcription-PCR. Journal of Clinical Microbiology, 40(7), 2323–2330. https://doi.org/10.1128/JCM.40.7.2323-2330.2002
  34. Drosten, C., Kümmerer, B. M., Schmitz, H., & Günther, S. (2003). Molecular diagnostics of viral hemorrhagic fevers. Antiviral Research, 57(1–2), 61–87. https://doi.org/10.1016/S0166-3542(02)00201-2
  35. Duh, D., Saksida, A., Petrovec, M., Dedushaj, I., & Avšič-ŽUpanc, T. (2006). Novel one-step real-time RT-PCR assay for rapid and specific diagnosis of Crimean-Congo hemorrhagic fever encountered in the Balkans. Journal of Virological Methods, 133(2), 175–179. https://doi.org/10.1016/j.jviromet.2005.11.006
  36. Emmerich, P., Mika, A., von Possel, R., Rackow, A., Liu, Y., Schmitz, H., … Deschermeier, C. (2018). Sensitive and specific detection of Crimean-Congo Hemorrhagic Fever Virus (CCHFV)—Specific IgM and IgG antibodies in human sera using recombinant CCHFV nucleoprotein as antigen in μ-capture and IgG immune complex (IC) ELISA tests. PLoS Neglected Tropical Diseases, 12(3), 1–24. https://doi.org/10.1371/journal.pntd.0006366
  37. Emmerich, P., von Possel, R., Deschermeier, C., Ahmeti, S., Berisha, L., Halili, B., … Borchardt-Lohölter, V. (2021). Comparison of diagnostic performances of ten different immunoassays detecting anti-CCHFVIgM and IgG antibodies from acute to subsided phases of Crimean-Congo hemorrhagic fever. PLoS Neglected Tropical Diseases, 15(3), 1–15. https://doi.org/10.1371/journal.pntd.0009280
  38. Ergönül, Ö. (2006). Crimean-Congo haemorrhagic fever. The Lancet Infectious Diseases, 6(4), 203–214. https://doi.org/10.1016/S1473-3099(06)70435-2
  39. Ergonul, O., Celikbas, A., Baykam, N., Eren, S., & Dokuzoguz, B. (2006). Analysis of risk-factors among patients with Crimean-Congo haemorrhagic fever virus infection: severity criteria revisited. Clinical Microbiology and Infection, 12(6), 551–554. https://doi.org/10.1111/j.1469-0691.2006.01445.x
  40. Ergönül, Ö., Çelikbaş, A., Dokuzoǧuz, B., Eren, Ş., Baykam, N., & Esener, H. (2004). Characteristics of patients with crimean-congo heniorrhagic fever in a recent outbreak in Turkey and impact of oral ribavirin therapy. Clinical Infectious Diseases, 39(2), 284–287. https://doi.org/10.1086/422000
  41. Ergönül, Ö., Keske, Ş., Çeldir, M. G., Kara, İ. A., Pshenichnaya, N., Abuova, G., … Gönen, M. (2018). Systematic review and meta-analysis of postexposure prophylaxis for crimean-congo hemorrhagic fever virus among healthcare workers. Emerging Infectious Diseases, 24(9), 1642–1648. https://doi.org/10.3201/eid2409.171709 Ergonul, Onder. (2008). Treatment of Crimean-Congo hemorrhagic fever. Antiviral Research, 78(1), 125–131. https://doi.org/10.1016/j.antiviral.2007.11.002
  42. Ergonul, Onder. (2012). Crimean-Congo hemorrhagic fever virus: New outbreaks, new discoveries. Current Opinion in Virology, 2(2), 215–220. https://doi.org/10.1016/j.coviro.2012.03.001
  43. Espunyes, J., Cabezón, O., Pailler-García, L., Dias-Alves, A., Lobato-Bailón, L., Marco, I., … Napp, S. (2021). Hotspot of Crimean-congo hemorrhagic fever virus seropositivity in wildlife, northeastern Spain. Emerging Infectious Diseases, 27(9), 2480–2484. https://doi.org/10.3201/eid2709.211105
  44. Estrada-Peña, A., Palomar, A. M., Santibáñez, P., Sánchez, N., Habela, M. A., Portillo, A., … Oteo, J. A. (2012). Crimean-Congo Hemorrhagic Fever Virus in Ticks, Southwestern Europe, 2010. Emerging Infectious Diseases, 18(1), 179–180. https://doi.org/10.3201/eid1801.111040
  45. Estrada, D. F., & De Guzman, R. N. (2011). Structural Characterization of the Crimean-Congo Hemorrhagic Fever Virus Gn Tail Provides Insight into Virus Assembly. Journal of Biological Chemistry, 286(24), 21678–21686. https://doi.org/10.1074/jbc.M110.216515
  46. Febrer-Sendra, B., Fernández-Soto, P., García-Bernalt Diego, J., Crego-Vicente, B., Negredo, A., Muñor-Bellido, J. L., … Muro, A. (2023). A Novel RT-LAMP for the Detection of Different Genotypes of Crimean–Congo Haemorrhagic Fever Virus in Patients from Spain. International Journal of Molecular Sciences, 24(7). https://doi.org/10.3390/ijms24076411
  47. Fels, J. M., Maurer, D. P., Herbert, A. S., Wirchnianski, A. S., Vergnolle, O., Cross, R. W., … Laura, M. (2022). HHS Public Access. 184(13), 3486–3501. https://doi.org/10.1016/j.cell.2021.05.001.Protective
  48. Fillâtre, P., Revest, M., & Tattevin, P. (2019). Crimean-Congo hemorrhagic fever: An update. Medecine et Maladies Infectieuses, 49(8), 574–585. https://doi.org/10.1016/j.medmal.2019.09.005
  49. Fletcher, T. E., Gulzhan, A., Ahmeti, S., Al-Abri, S. S., Asik, Z., Atilla, A., … Leblebicioglu, H. (2017). Infection prevention and control practice for Crimean-Congo hemorrhagic fever - A multi-center cross-sectional survey in Eurasia. PLoS ONE, 12(9), 1–10. https://doi.org/10.1371/journal.pone.0182315
  50. Freitas, N., Enguehard, M., Denolly, S., Levy, C., Neveu, G., Lerolle, S., … Cosset, F. L. (2020). The interplays between crimean-congo hemorrhagic fever virus (cchfv) m segment-encoded accessory proteins and structural proteins promote virus assembly and infectivity. PLoS Pathogens, 16(9), 1–29. https://doi.org/10.1371/journal.ppat.1008850
  51. García Rada, A. (2016). First outbreak of Crimean-Congo haemorrhagic fever in western Europe kills one man in Spain. BMJ, 354(September), i4891. https://doi.org/10.1136/bmj.i4891
  52. Gargili, A., Estrada-Peña, A., Spengler, J. R., Lukashev, A., Nuttall, P. A., & Bente, D. A. (2017). The role of ticks in the maintenance and transmission of Crimean-Congo hemorrhagic fever virus: A review of published field and laboratory studies. Antiviral Research, 144, 93–119. https://doi.org/10.1016/j.antiviral.2017.05.010
  53. Garrison, A. R., Alkhovsky [Альховский Сергей Владимирович], S. V., Avšič-Županc, T., Bente, D. A., Bergeron, É., Burt, F., … Consortium, I. R. (2020). ICTV Virus Taxonomy Profile: Nairoviridae. Journal of General Virology, 101(8), 798–799. https://doi.org/10.1099/jgv.0.001485
  54. Goedhals, D., Paweska, J. T., & Burt, F. J. (2017). Long-lived CD8+ T cell responses following Crimean-Congo haemorrhagic fever virus infection. PLoS Neglected Tropical Diseases, 11(12), 1–12. https://doi.org/10.1371/journal.pntd.0006149
  55. Graci, J. D., & Cameron, C. E. (2006). Mechanisms of action of ribavirin against distinct viruses. Reviews in Medical Virology, 16(1), 37–48. https://doi.org/10.1002/rmv.483
  56. Grandi, G., Chitimia-dobler, L., Choklikitumnuey, P., Strube, C., Springer, A., Albihn, A., … Omazic, A. (2020). First records of adult Hyalomma marginatum and H. rufipes ticks (Acari: Ixodidae) in Sweden. Ticks and Tick-Borne Diseases, 11(3), 101403. https://doi.org/https://doi.org/10.1016/j.ttbdis.2020.101403
  57. Grard, G., Drexler, J. F., Fair, J., Muyembe, J. J., Wolfe, N. D., Drosten, C., & Leroy, E. M. (2011). Re-Emergence of Crimean-Congo hemorrhagic fever virus in central Africa. PLoS Neglected Tropical Diseases, 5(10), 4–6. https://doi.org/10.1371/journal.pntd.0001350
  58. Guglielmone, A. A., Robbins, R. G., Apanaskevich, D. A., Petney, T. N., Estrada Peña, A., Horak, I. G., … Barker, S. C. (2010). The Argasidae, Ixodidae and Nuttalliellidae (Acari: Ixodida) of the world: a list of valid species names.
  59. Hawman, D. W., & Feldmann, H. (2023). Crimean–Congo haemorrhagic fever virus. Nature Reviews Microbiology, 21(7), 463–477. https://doi.org/10.1038/s41579-023-00871-9
  60. Hawman, D. W., Haddock, E., Meade-White, K., Williamson, B., Hanley, P. W., Rosenke, K., … Feldmann, H. (2018). Favipiravir (T-705) but not ribavirin is effective against two distinct strains of Crimean-Congo hemorrhagic fever virus in mice. Antiviral Research, 157(June), 18–26. https://doi.org/10.1016/j.antiviral.2018.06.013
  61. Hema, M., & Konakalla, N. C. (2021). Recent developments in detection and diagnosis of plant viruses. Recent Developments in Applied Microbiology and Biochemistry, 163–180.
  62. Hoogstraal, H. (1979). Review Article: The Epidemiology of Tick-Borne Crimean-Congo Hemorrhagic Fever in Asia, Europe, and Africa. Journal of Medical Entomology, 15(4), 307–417. https://doi.org/10.1093/jmedent/15.4.307
  63. Hulswit, R. J. G., Paesen, G. C., Bowden, T. A., & Shi, X. (2021). Recent advances in bunyavirus glycoprotein research: Precursor processing, receptor binding and structure. Viruses, 13(2), 1–30. https://doi.org/10.3390/v13020353
  64. Ibrahim, A. S., Ibrahim, K. S., Mohammed, M. O., Al-Shaikhani, M. A., Barzanji, A. A., Saeed, S. J., … Bhnam, M. N. (2014). Crimean Congo hemorrhagic fever management in Erbil during 2010-2011. European Scientific Journal, 10(24).
  65. Jalali, T., Salehi-Vaziri, M., Pouriayevali, M. H., & Gargari, S. L. M. (2021). Aptamer based diagnosis of crimean-congo hemorrhagic fever from clinical specimens. Scientific Reports, 11(1), 12639. https://doi.org/10.1038/s41598-021-91826-8
  66. Johnson, S., Henschke, N., Maayan, N., Mills, I., Buckley, B. S., Kakourou, A., & Marshall, R. (2018). Ribavirin for treating Crimean Congo haemorrhagic fever. Cochrane Database of Systematic Reviews, 2018(6). https://doi.org/10.1002/14651858.CD012713.pub2
  67. Kadanali, A., Erol, S., Özkurt, Z., & Özden, K. (2009). Epidemiological risk factors for Crimean-Congo hemorrhagic fever patients. Turkish Journal of Medical Sciences, 39(6), 829–832. https://doi.org/10.3906/sag-0904-49
  68. Kamboj, A., Pateriya, A. K., Mishra, A., Ranaware, P., Kulkarni, D. D., & Raut, A. A. (2014). Novel molecular beacon probe-based real-time RT-PCR assay for diagnosis of Crimean-Congo hemorrhagic fever encountered in India. BioMed Research International, 2014, 5–8. https://doi.org/10.1155/2014/496219
  69. Karti, S. S., Odabasi, Z., Korten, V., Yilmaz, M., Sonmez, M., Caylan, R., … Ksiazek, T. G. (2004). Crimean-Congo hemorrhagic fever in Turkey. Emerging Infectious Diseases, 10(8), 1379–1384. https://doi.org/10.3201/eid1008.030928
  70. Keshtkar-Jahromi, M., Kuhn, J. H., Christova, I., Bradfute, S. B., Jahrling, P. B., & Bavari, S. (2011). Crimean-Congo hemorrhagic fever: Current and future prospects of vaccines and therapies. Antiviral Research, 90(2), 85–92. https://doi.org/10.1016/j.antiviral.2011.02.010
  71. Khan, A. S., Maupin, G. O., Rollin, P. E., Noor, A. M., Shurie, H. H., Shalabi, A. G., … Ijaz, K. (1997). An outbreak of Crimean-Congo hemorrhagic fever in the United Arab Emirates, 1994-1995. The American Journal of Tropical Medicine and Hygiene, 57(5), 519–525.
  72. Komut, S., Çorakyer, N., Kaplan, G., & Baykam, N. (2023). An Evaluation of the Hitit Index in Differential Diagnosis of Crimean-Congo Hemorrhagic Fever in the Emergency Department. Medicina, 59(10), 1796. https://doi.org/10.3390/medicina59101796
  73. Kubar, A., Haciomeroglu, M., Ozkul, A., Bagriacik, U., Akinci, E., Sener, K., & Bodur, H. (2011). Prompt administration of crimean-congo hemorrhagic fever (CCHF) virus hyperimmunoglobulin in patients diagnosed with CCHF and viral load monitorization by reverse transcriptase-PCR. Japanese Journal of Infectious Diseases, 64(5), 439–443. https://doi.org/10.7883/yoken.64.439
  74. Kumar, B., Manjunathachar, H. V., & Ghosh, S. (2020). A review on Hyalomma species infestations on human and animals and progress on management strategies. Heliyon, 6(12), e05675. https://doi.org/10.1016/j.heliyon.2020.e05675
  75. Leblebicioglu, H. (2010). Crimean-Congo haemorrhagic fever in Eurasia. International Journal of Antimicrobial Agents, 36(SUPPL. 1), 43–46. https://doi.org/10.1016/j.ijantimicag.2010.06.020 Leblebicioglu, H., Ozaras, R., Irmak, H., & Sencan, I. (2016). Crimean-Congo hemorrhagic fever in Turkey: Current status and future challenges. Antiviral Research, 126, 21–34. https://doi.org/10.1016/j.antiviral.2015.12.003
  76. Liu, D., Li, Y., Zhao, J., Deng, F., Duan, X., Kou, C., … Sun, S. (2014). Fine Epitope Mapping of the Central Immunodominant Region of Nucleoprotein from Crimean-Congo Hemorrhagic Fever Virus (CCHFV). PLoS ONE, 9(11), e108419. https://doi.org/10.1371/journal.pone.0108419
  77. Maltezou, H. C., Papa, A., Tsiodras, S., Dalla, V., Maltezos, E., & Antoniadis, A. (2009). Crimean-Congo hemorrhagic fever in Greece: a public health perspective. International Journal of Infectious Diseases, 13(6), 713–716. https://doi.org/10.1016/j.ijid.2008.11.011
  78. Mardani, M., Jahromi, M. K., Naieni, K. H., & Zeinali, M. (2003). The Efficacy of Oral Ribavirin in the Treatment of Crimean-Congo Hemorrhagic Fever in Iran. Clinical Infectious Diseases, 36(12), 1613–1618. https://doi.org/10.1086/375058
  79. Messina, J. P., Pigott, D. M., Golding, N., Duda, K. A., Brownstein, J. S., Weiss, D. J., … Hay, S. I. (2015). The global distribution of Crimean-Congo hemorrhagic fever. (July), 503–513. https://doi.org/10.1093/trstmh/trv050
  80. Mofleh, J., & Ahmad, A. Z. (2012). Crimean–Congo haemorrhagic fever outbreak investigation in the Western Region of Afghanistan in 2008. Eastern Mediterranean Health Journal, 18(5), 522–526. https://doi.org/10.26719/2012.18.5.522
  81. Moshref, Z. S., Jalali, T., Rezaei Adriani, R., Soltati, E., & Mousavi Gargari, S. L. (2023). Aptamer-based diagnosis of various SARS-CoV2 strains isolated from clinical specimens. Heliyon, 9(6), e16458. https://doi.org/10.1016/j.heliyon.2023.e16458
  82. Mousavi-Jazi, M., Karlberg, H., Papa, A., Christova, I., & Mirazimi, A. (2012). Healthy individuals’ immune response to the Bulgarian Crimean-Congo hemorrhagic fever virus vaccine. Vaccine, 30(44), 6225–6229. https://doi.org/10.1016/j.vaccine.2012.08.003
  83. Mustafa, M. L., Ayazi, E., Mohareb, E., Yingst, S., Zayed, A., Rossi, C. A., … Leslie, T. (2011). Crimean-Congo Hemorrhagic Fever, Afghanistan, 2009. Emerging Infectious Diseases, 17(10), 1940–1941. https://doi.org/10.3201/eid1710.110061
  84. Negredo, A., de la Calle-Prieto, F., Palencia-Herrejón, E., Mora-Rillo, M., Astray-Mochales, J., Sánchez-Seco, M. P., … Arribas, J. R. (2017). Autochthonous Crimean–Congo Hemorrhagic Fever in Spain. New England Journal of Medicine, 377(2), 154–161. https://doi.org/10.1056/nejmoa1615162
  85. Nekliudov, M. (1952). A case of hemorrhagic fever (Crimean). Savremenna Medicina, 5, 92–95.
  86. Oestereich, L., Rieger, T., Neumann, M., Bernreuther, C., Lehmann, M., Krasemann, S., … Günther, S. (2014). Evaluation of Antiviral Efficacy of Ribavirin, Arbidol, and T-705 (Favipiravir) in a Mouse Model for Crimean-Congo Hemorrhagic Fever. PLoS Neglected Tropical Diseases, 8(5). https://doi.org/10.1371/journal.pntd.0002804
  87. Omoga, D. C. A., Tchouassi, D. P., Venter, M., Ogola, E. O., Osalla, J., Kopp, A., … Sang, R. (2023). Transmission Dynamics of Crimean–Congo Haemorrhagic Fever Virus (CCHFV): Evidence of Circulation in Humans, Livestock, and Rodents in Diverse Ecologies in Kenya. Viruses, 15(9), 1–17. https://doi.org/10.3390/v15091891
  88. Ozdarendeli, A. (2023). Crimean–Congo Hemorrhagic Fever Virus: Progress in Vaccine Development. Diagnostics, 13(16), 1–29. https://doi.org/10.3390/diagnostics13162708
  89. Ozkaya, E., Dincer, E., Carhan, A., Uyar, Y., Ertek, M., Whitehouse, C. A., & Ozkul, A. (2010). Molecular epidemiology of Crimean-Congo hemorrhagic fever virus in Turkey: Occurrence of local topotype. Virus Research, 149(1), 64–70. https://doi.org/10.1016/j.virusres.2009.12.014
  90. Palomar, A. M., Portillo, A., Santibáñez, P., Mazuelas, D., Arizaga, J., Crespo, A., … Oteo, J. A. (2013). Crimean-congo hemorrhagic fever virus in ticks from migratory birds, Morocco. Emerging Infectious Diseases, 19(2), 260–263. https://doi.org/10.3201/eid1902.121193
  91. Papa, Anna, Christova, I., Papadimitriou, E., & Antoniadis, A. (2004). Crimean-Congo hemorrhagic fever in Bulgaria. Emerging Infectious Diseases, 10(8), 1465–1467. https://doi.org/10.3201/eid1008.040162
  92. Papa, Anna, Papadimitriou, E., & Christova, I. (2011). The Bulgarian vaccine Crimean-Congo haemorrhagic fever virus strain. Scandinavian Journal of Infectious Diseases, 43(3), 225–229. https://doi.org/10.3109/00365548.2010.540036
  93. Papa, Anna, Tsergouli, K., Tsioka, K., & Mirazimi, A. (2017). Crimean-Congo hemorrhagic fever: Tick-host-virus interactions. Frontiers in Cellular and Infection Microbiology, 7(MAY), 1–7. https://doi.org/10.3389/fcimb.2017.00213
  94. Papa, Anna, Tzala, E., & Maltezou, H. C. (2011). Crimean-Congo Hemorrhagic Fever Virus, Northeastern Greece. Emerging Infectious Diseases, 17(1), 141–143. https://doi.org/10.3201/eid1701.100073
  95. Papadopoulos, O. t, & Koptopoulos, G. (1980). Crimean-Congo hemorrhagic fever (CCHF) in Greece: isolation of the virus from Rhipicephalus bursa ticks and a preliminary serological survey. Zentbl Bakteriol Hyg Abt, 1(Suppl 9), 189–193.
  96. Pattyn, S. R. (1978). Ebola virus haemorrhagic fever. Proceedings of an International Colloquium on Ebola Virus Infection and Other Haemorrhagic Fevers held in Antwerp, Belgium, 6-8 December, 1977. Ebola Virus Haemorrhagic Fever. Proceedings of an International Colloquium on Ebola Virus Infection and Other Haemorrhagic Fevers Held in Antwerp, Belgium, 6-8 December, 1977. Elsevier/North-Holland Biomedical Press, 335 Jan van Galenstraat, PO Box 211 ….
  97. Rosenke, K., Feldmann, H., Westover, J. B., Hanley, P. W., Martellaro, C., Feldmann, F., … Safronetz, D. (2018). Use of favipiravir to treat lassa virus infection in Macaques. Emerging Infectious Diseases, 24(9), 1696–1699. https://doi.org/10.3201/eid2409.180233
  98. Safronetz, D., Rosenke, K., Westover, J. B., Martellaro, C., Okumura, A., Furuta, Y., … Gowen, B. B. (2015). The broad-spectrum antiviral favipiravir protects Guinea pigs from lethal Lassa virus infection post-disease onset. Scientific Reports, 5(June), 1–11. https://doi.org/10.1038/srep14775
  99. Saijo, M., Tang, Q., Shimayi, B., Han, L., Zhang, Y., Asiguma, M., … Morikawa, S. (2005). Recombinant nucleoprotein-based serological diagnosis of Crimean-Congo hemorrhagic fever virus infections. Journal of Medical Virology, 75(2), 295–299. https://doi.org/10.1002/jmv.20270
  100. Salim Abadi, Y., Telmadarraiy, Z., Vatandoost, H., Chinikar, S., Oshaghi, M. A., Moradi, M., … Nasiri, A. (2010). Hard ticks on domestic ruminants and their seasonal population pynamics in Yazd Province, Iran. Iranian Journal of Arthropod-Borne Diseases, 4(1), 66–71.
  101. Sargianou, M., Panos, G., Tsatsaris, A., Gogos, C., & Papa, A. (2013). Crimean-Congo hemorrhagic fever: Seroprevalence and risk factors among humans in Achaia, western Greece. International Journal of Infectious Diseases, 17(12), e1160–e1165. https://doi.org/10.1016/j.ijid.2013.07.015
  102. Schluederberg, A. N. N. (1965). Immune Globulins in Human Viral Infections. Nature, 205(4977), 1232–1233. https://doi.org/10.1038/2051232a0
  103. Schwarz, T. F., Nsanze, H., Longson, M., Nitschko, H., Gilch, S., Shurie, H., … Jager, G. (1996). Polymerase chain reaction for diagnosis and identification of distinct variants of Crimean-Congo hemorrhagic fever virus in the United Arab Emirates. The American Journal of Tropical Medicine and Hygiene, 55(2), 190—196. https://doi.org/10.4269/ajtmh.1996.55.190
  104. Shahhosseini, N., Wong, G., Babuadze, G., Camp, J. V., Ergonul, O., Kobinger, G. P., … Nowotny, N. (2021). Crimean-congo hemorrhagic fever virus in asia, africa and europe. Microorganisms, 9(9), 1–24. https://doi.org/10.3390/microorganisms9091907
  105. Sharifi-Mood, B., Metanat, M., & Alavi-Naini, R. (2014). Prevalence of Crimean-Congo Hemorrhagic FeverAmong High Risk Human Groups. International Journal of High Risk Behaviors and Addiction, 3(1), 5–8. https://doi.org/10.5812/ijhrba.11520
  106. Simpson, D. I. H., Knight, E. M., Courtois, G. H., Williams, M. C., Weinbren, M. P., & Kibukamusoke, J. W. (1967). Congo virus: a hitherto undescribed virus occurring in Africa. Part 1. Human isolations-clinical notes. East African Medical Journal, 44(2), 87–92.
  107. Spengler, J. R., Bente, D. A., Bray, M., Burt, F., Hewson, R., Korukluoglu, G., … Papa, A. (2018). Second International Conference on Crimean-Congo Hemorrhagic Fever. Antiviral Research, 150(November 2017), 137–147. https://doi.org/10.1016/j.antiviral.2017.11.019
  108. Spengler, J. R., Bergeron, É., & Rollin, P. E. (2016). Seroepidemiological Studies of Crimean-Congo Hemorrhagic Fever Virus in Domestic and Wild Animals. PLoS Neglected Tropical Diseases, 10(1), 1–28. https://doi.org/10.1371/journal.pntd.0004210
  109. Spengler, J. R., Estrada-Peña, A., Garrison, A. R., Schmaljohn, C., Spiropoulou, C. F., Bergeron, É., & Bente, D. A. (2016). A chronological review of experimental infection studies of the role of wild animals and livestock in the maintenance and transmission of Crimean-Congo hemorrhagic fever virus. Antiviral Research, 135, 31–47. https://doi.org/10.1016/j.antiviral.2016.09.013
  110. Spiropoulou, C. F., & Bente, D. A. (2020). Orthohantavirus, orthonairovirus, orthobunyavirus, and phlebovirus. Fields Virology. Philadelphia, Pennsylvania: Wolters Kluwer/Lippincott Williams & Wilkins, 750–783.
  111. Stähelin-Massik, J., Zimmermann, H., & Gnehm, H. E. (2008). Tick-borne encephalitis in swiss children 2000-2004: Five-year nationwide surveillance of epidemiologic characteristics and clinical course. Pediatric Infectious Disease Journal, 27(6), 555–557. https://doi.org/10.1097/INF.0b013e318165c195
  112. Tang, Q., Saijo, M., Zhang, Y., Asiguma, M., Tianshu, D., Han, L., … Morikawa, S. (2003). A patient with Crimean-Congo hemorrhagic fever serologically diagnosed by recombinant nucleoprotein-based antibody detection systems. Clinical and Diagnostic Laboratory Immunology, 10(3), 489–491. https://doi.org/10.1128/CDLI.10.3.489-491.2003
  113. Tchesnokov, E. P., Bailey-Elkin, B. A., Mark, B. L., & Götte, M. (2020). Independent inhibition of the polymerase and deubiquitinase activities of the Crimean-Congo Hemorrhagic Fever Virus full-length L-protein. PLOS Neglected Tropical Diseases, 14(6), e0008283. https://doi.org/10.1371/journal.pntd.0008283
  114. Temur, A. I., Kuhn, J. H., Pecor, D. B., Apanaskevich, D. A., & Keshtkar-Jahromi, M. (2021). Epidemiology of Crimean-Congo Hemorrhagic Fever (CCHF) in Africa—Underestimated for Decades. The American Journal of Tropical Medicine and Hygiene, 104(6), 1978–1990. https://doi.org/10.4269/ajtmh.20-1413
  115. Tezer, H., Sucakli, I. A., Sayli, T. R., Celikel, E., Yakut, I., Kara, A., … Ergonul, O. (2010). Crimean-Congo hemorrhagic fever in children. Journal of Clinical Virology, 48(3), 184–186. https://doi.org/10.1016/j.jcv.2010.04.001
  116. Tignor, G. H., & Hanham, C. A. (1993). Ribavirin efficacy in an in vivo model of Crimean-Congo hemorrhagic fever virus (CCHF) infection. Antiviral Research, 22(4), 309–325.
  117. Tipih, T., & Burt, F. J. (2020). Crimean–Congo hemorrhagic fever virus: advances in vaccine development. BioResearch Open Access, 9(1), 137–150.
  118. Vesenjak-Hirjan, J., Punda-Polić, V., & Dobe, M. (1991). Geographical distribution of arboviruses in Yugoslavia. Journal of Hygiene, Epidemiology, Microbiology, and Immunology, 35(2), 129–140.
  119. Vorou, R., Pierroutsakos, I. N., & Maltezou, H. C. (2007). Crimean-Congo hemorrhagic fever. Current Opinion in Infectious Diseases, 20(5), 495–500. https://doi.org/10.1097/QCO.0b013e3282a56a0a
  120. Wasfi, F., Dowall, S., Ghabbari, T., Bosworth, A., Chakroun, M., Varghese, A., … Letaief, A. (2016). Sero-epidemiological survey of Crimean-Congo hemorrhagic fever virus in Tunisia. Parasite, 23. https://doi.org/10.1051/parasite/2016010
  121. Watts, D. M., Ksiazek, T. G., Linthicum, K. J., & Hoogstraal, H. (2019). Crimean-Congo hemorrhagic fever. The Arboviruses, 177–222.
  122. Watts, D. M., Ussery, M. A., Nash, D., & Peters, C. J. (1989). Inhibition of Crimean-Congo hemorrhagic fever viral infectivity yields in vitro by ribavirin. The American Journal of Tropical Medicine and Hygiene, 41(5), 581–585.
  123. Weidmann, M., Avsic-Zupanc, T., Bino, S., Bouloy, M., Burt, F., Chinikar, S., … Zeller, H. (2016). Biosafety standards for working with crimean-congo hemorrhagic fever virus. Journal of General Virology, 97(11), 2799–2808. https://doi.org/10.1099/jgv.0.000610
  124. Whitehouse, C. A. (2004). Crimean-Congo hemorrhagic fever. Antiviral Research, 64(3), 145–160. https://doi.org/10.1016/j.antiviral.2004.08.001
  125. World Health Organization (WHO). (2018). Roadmap for Research and Product Development against Crimean-Congo Haemorrhagic Fever (CCHF). 1–11. Retrieved from https://www.who.int/blueprint/priority-diseases/key-action/cchf-draft-r-and-d-roadmap.pdf?ua=1
  126. World Health Organization (WHO). (2020). Vector-borne diseases. Retrieved from https://www.who.int/news-room/fact-sheets/detail/vector-borne-diseases
  127. World Health Organization (WHO). (2022a). Crimean-Congo haemorrhagic fever. Retrieved from https://www.who.int/news-room/fact-sheets/detail/crimean-congo-haemorrhagic-fever
  128. World Health Organization (WHO). (2022b). Crimean-Congo haemorrhagic fever. Retrieved from https://www.who.int/health-topics/crimean-congo-haemorrhagic-fever/#tab=tab_1
  129. Zivcec, M., Scholte, F., Spiropoulou, C., Spengler, J., & Bergeron, É. (2016). Molecular Insights into Crimean-Congo Hemorrhagic Fever Virus. Viruses, 8(4), 106. https://doi.org/10.3390/v8040106
  130. Bernard, C., Joly Kukla, C., Rakotoarivony, I., Duhayon, M., Stachurski, F., Huber, K., … Vial, L. (2024). Detection of Crimean-Congo haemorrhagic fever virus in Hyalomma marginatum ticks, southern France, May 2022 and April 2023. Euro Surveillance: Bulletin Europeen Sur Les Maladies Transmissibles = European Communicable Disease Bulletin, 29(6), 1–6. https://doi.org/10.2807/1560-7917.ES.2024.29.6.2400023