Sweileh WM. Global research trends of World Health Organization’s top eight emerging pathogens. Global Health. 2017;13:9–27.
Mehand MS, Millett P, Al-Shorbaji F, Roth C, Kieny MP, Murgue B. World health organization methodology to prioritize emerging infectious diseases in need of research and development. Emerg Infect Dis. 2018;24:e171427.
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.
Fels JM, Maurer DP, Herbert AS, Wirchnianski AS, Vergnolle O, Cross RW, Abelson DM, Moyer CL, Mishra AK, Aguilan JT, et al. Protective neutralizing antibodies from human survivors of Crimean-Congo hemorrhagic fever. Cell. 2021;184:3486-3501 e3421.
Spengler JR, Bente DA, Bray M, Burt F, Hewson R, Korukluoglu G, Mirazimi A, Weber F, Papa A. Second International Conference on Crimean-Congo Hemorrhagic Fever. Antiviral Res. 2018;150:137–47.
Spengler JR, Bergeron E, Spiropoulou CF. Crimean-Congo hemorrhagic fever and expansion from endemic regions. Curr Opin Virol. 2019;34:70–8.
Abudurexiti A, Adkins S, Alioto D, Alkhovsky SV, Avsic-Zupanc T, Ballinger MJ, Bente DA, Beer M, Bergeron E, Blair CD, et al. Taxonomy of the order Bunyavirales: update 2019. Arch Virol. 2019;164:1949–65.
Li H, Bello A, Smith G, Kielich DMS, Strong JE, Pickering BS. Degenerate sequence-based CRISPR diagnostic for Crimean-Congo hemorrhagic fever virus. PLoS Negl Trop Dis. 2022;16:e0010285.
Conger NG, Paolino KM, Osborn EC, Rusnak JM, Gunther S, Pool J, Rollin PE, Allan PF, Schmidt-Chanasit J, Rieger T, Kortepeter MG. Health care response to CCHF in US soldier and nosocomial transmission to health care providers, Germany, 2009. Emerg Infect Dis. 2015;21:23–31.
Mild M, Simon M, Albert J, Mirazimi A. Towards an understanding of the migration of Crimean-Congo hemorrhagic fever virus. J Gen Virol. 2010;91:199–207.
Grandi G, Chitimia-Dobler L, Choklikitumnuey P, Strube C, Springer A, Albihn A, Jaenson TGT, Omazic A. First records of adult Hyalomma marginatum and H. rufipes ticks (Acari: Ixodidae) in Sweden. Ticks Tick Borne Dis. 2020;11:101403.
Andersen LK, Davis MD. Climate change and the epidemiology of selected tick-borne and mosquito-borne diseases: update from the International Society of Dermatology Climate Change Task Force. Int J Dermatol. 2017;56:252–9.
Pavel STI, Yetiskin H, Kalkan A, Ozdarendeli A. Evaluation of the cell culture based and the mouse brain derived inactivated vaccines against Crimean-Congo hemorrhagic fever virus in transiently immune-suppressed (IS) mouse model. PLoS Negl Trop Dis. 2020;14:e0008834.
Berber E, Canakoglu N, Tonbak S, Ozdarendeli A. Development of a protective inactivated vaccine against Crimean-Congo hemorrhagic fever infection. Heliyon. 2021;7:e08161.
Dai S, Wu Q, Wu X, Peng C, Liu J, Tang S, Zhang T, Deng F, Shen S. Differential cell line susceptibility to crimean-congo hemorrhagic fever virus. Front Cell Infect Microbiol. 2021;11:648077.
Appelberg S, John L, Pardi N, Vegvari A, Bereczky S, Ahlen G, Monteil V, Abdurahman S, Mikaeloff F, Beattie M, et al. Nucleoside-modified mRNA vaccines protect IFNAR(-/-) mice against crimean-congo hemorrhagic fever virus infection. J Virol. 2022;96:e0156821.
Golden JW, Zeng X, Cline CR, Smith JM, Daye SP, Carey BD, Blancett CD, Shoemaker CJ, Liu J, Fitzpatrick CJ, et al. The host inflammatory response contributes to disease severity in Crimean-Congo hemorrhagic fever virus infected mice. PLoS Pathog. 2022;18:e1010485.
Hua BL, Scholte FE, Ohlendorf V, Kopp A, Marklewitz M, Drosten C, Nichol ST, Spiropoulou C, Junglen S, Bergeron E. A single mutation in Crimean-Congo hemorrhagic fever virus discovered in ticks impairs infectivity in human cells. Elife. 2020;9:e50999.
Mishra AK, Moyer CL, Abelson DM, Deer DJ, El Omari K, Duman R, Lobel L, Lutwama JJ, Dye JM, Wagner A, et al: Structure and characterization of crimean-congo hemorrhagic fever virus GP38. J Virol 2020, 94.
Smith DR, Shoemaker CJ, Zeng X, Garrison AR, Golden JW, Schellhase CW, Pratt W, Rossi F, Fitzpatrick CJ, Shamblin J, et al. Persistent Crimean-Congo hemorrhagic fever virus infection in the testes and within granulomas of non-human primates with latent tuberculosis. PLoS Pathog. 2019;15:e1008050.
Golden JW, Shoemaker CJ, Lindquist ME, Zeng X, Daye SP, Williams JA, Liu J, Coffin KM, Olschner S, Flusin O, et al. GP38-targeting monoclonal antibodies protect adult mice against lethal Crimean-Congo hemorrhagic fever virus infection. Sci Adv. 2019;5:eaaw9535.
Rodriguez SE, Cross RW, Fenton KA, Bente DA, Mire CE, Geisbert TW. Vesicular stomatitis virus-based vaccine protects mice against Crimean-Congo hemorrhagic fever. Sci Rep. 2019;9:7755.
Cajimat MNB, Rodriguez SE, Schuster IUE, Swetnam DM, Ksiazek TG, Habela MA, Negredo AI, Estrada-Pena A, Barrett ADT, Bente DA. Genomic characterization of Crimean-Congo hemorrhagic fever virus in Hyalomma Tick from Spain, 2014. Vector Borne Zoonotic Dis. 2017;17:714–9.
Spengler JR, Kelly Keating M, McElroy AK, Zivcec M, Coleman-McCray JD, Harmon JR, Bollweg BC, Goldsmith CS, Bergeron E, Keck JG, et al. Crimean-Congo hemorrhagic fever in humanized mice reveals glial cells as primary targets of neurological infection. J Infect Dis. 2017;216:1386–97.
Hinkula J, Devignot S, Akerstrom S, Karlberg H, Wattrang E, Bereczky S, Mousavi-Jazi M, Risinger C, Lindegren G, Vernersson C, et al: Immunization with DNA plasmids coding for Crimean-Congo hemorrhagic fever virus capsid and envelope proteins and/or virus-like particles induces protection and survival in challenged mice. J Virol 2017, 91.
Dowall SD, Graham VA, Rayner E, Hunter L, Watson R, Taylor I, Rule A, Carroll MW, Hewson R. Protective effects of a Modified Vaccinia Ankara-based vaccine candidate against Crimean-Congo Haemorrhagic Fever virus require both cellular and humoral responses. PLoS ONE. 2016;11:e0156637.
Ferraris O, Moroso M, Pernet O, Emonet S, Ferrier Rembert A, Paranhos-Baccala G, Peyrefitte CN. Evaluation of Crimean-Congo hemorrhagic fever virus in vitro inhibition by chloroquine and chlorpromazine, two FDA approved molecules. Antiviral Res. 2015;118:75–81.
Foldes K, Aligholipour Farzani T, Ergunay K, Ozkul A: Differential growth characteristics of Crimean-Congo Hemorrhagic fever virus in kidney cells of human and Bovine Origin. Viruses 2020, 12.
Aligholipour Farzani T, Foldes K, Hanifehnezhad A, Yener Ilce B, Bilge Dagalp S, Amirzadeh Khiabani N, Ergunay K, Alkan F, Karaoglu T, Bodur H, Ozkul A. Bovine Herpesvirus Type 4 (BoHV-4) Vector Delivering Nucleocapsid Protein of Crimean-Congo Hemorrhagic Fever Virus Induces Comparable Protective Immunity against Lethal Challenge in IFNalpha/beta/gammaR-/- Mice Models. Viruses. 2019;11:237.
Hawman DW, Meade-White K, Leventhal S, Appelberg S, Ahlen G, Nikouyan N, Clancy C, Smith B, Hanley P, Lovaglio J, et al: Accelerated DNA vaccine regimen provides protection against Crimean-Congo hemorrhagic fever virus challenge in a macaque model. Mol Ther 2022.
Mears MC, Rodriguez SE, Schmitz KS, Padilla A, Biswas S, Cajimat MNB, Mire CE, Welch SR, Bergeron E, Alabi CA, et al. Design and evaluation of neutralizing and fusion inhibitory peptides to Crimean-Congo hemorrhagic fever virus. Antiviral Res. 2022;207:105401.
Leventhal SS, Meade-White K, Rao D, Haddock E, Leung J, Scott D, Archer J, Randall S, Erasmus JH, Feldmann H, Hawman DW. Replicating RNA vaccination elicits an unexpected immune response that efficiently protects mice against lethal Crimean-Congo hemorrhagic fever virus challenge. EBioMedicine. 2022;82:104188.
Neogi U, Elaldi N, Appelberg S, Ambikan A, Kennedy E, Dowall S, Bagci BK, Gupta S, Rodriguez JE, Svensson-Akusjarvi S, et al: Multi-omics insights into host-viral response and pathogenesis in Crimean-Congo hemorrhagic fever viruses for novel therapeutic target. Elife 2022, 11.
Salvati MV, Salaris C, Monteil V, Del Vecchio C, Palu G, Parolin C, Calistri A, Bell-Sakyi L, Mirazimi A, Salata C. Virus-derived DNA forms mediate the persistent infection of tick cells by Hazara virus and Crimean-Congo Hemorrhagic fever virus. J Virol. 2021;95:e0163821.
Hawman DW, Meade-White K, Leventhal S, Feldmann F, Okumura A, Smith B, Scott D, Feldmann H. Immunocompetent mouse model for Crimean-Congo hemorrhagic fever virus. Elife. 2021;10:e63906.
Hawman DW, Ahlen G, Appelberg KS, Meade-White K, Hanley PW, Scott D, Monteil V, Devignot S, Okumura A, Weber F, et al. A DNA-based vaccine protects against Crimean-Congo haemorrhagic fever virus disease in a Cynomolgus macaque model. Nat Microbiol. 2021;6:187–95.
Cross RW, Prasad AN, Borisevich V, Geisbert JB, Agans KN, Deer DJ, Fenton KA, Geisbert TW. Crimean-Congo hemorrhagic fever virus strains Hoti and Afghanistan cause viremia and mild clinical disease in cynomolgus monkeys. PLoS Negl Trop Dis. 2020;14:e0008637.
Rodriguez SE, McAuley AJ, Gargili A, Bente DA. Interactions of human dermal dendritic cells and langerhans cells treated with Hyalomma tick Saliva with Crimean-Congo Hemorrhagic fever virus. Viruses. 2018;10:381.
Welch SR, Scholte FEM, Flint M, Chatterjee P, Nichol ST, Bergeron E, Spiropoulou CF. Identification of 2’-deoxy-2’-fluorocytidine as a potent inhibitor of Crimean-Congo hemorrhagic fever virus replication using a recombinant fluorescent reporter virus. Antiviral Res. 2017;147:91–9.
Zivcec M, Guerrero LIW, Albarino CG, Bergeron E, Nichol ST, Spiropoulou CF. Identification of broadly neutralizing monoclonal antibodies against Crimean-Congo hemorrhagic fever virus. Antiviral Res. 2017;146:112–20.
Berber E, Canakoglu N, Yoruk MD, Tonbak S, Aktas M, Ertek M, Bolat Y, Kalkan A, Ozdarendeli A. Application of the pseudo-plaque assay for detection and titration of Crimean-Congo hemorrhagic fever virus. J Virol Methods. 2013;187:26–31.
Lombe BP, Miyamoto H, Saito T, Yoshida R, Manzoor R, Kajihara M, Shimojima M, Fukushi S, Morikawa S, Yoshikawa T, et al. Purification of Crimean-Congo hemorrhagic fever virus nucleoprotein and its utility for serological diagnosis. Sci Rep. 2021;11:2324.
Flick R, Flick K, Feldmann H, Elgh F. Reverse genetics for crimean-congo hemorrhagic fever virus. J Virol. 2003;77:5997–6006.
Peyrefitte CN, Perret M, Garcia S, Rodrigues R, Bagnaud A, Lacote S, Crance JM, Vernet G, Garin D, Bouloy M, Paranhos-Baccala G. Differential activation profiles of Crimean-Congo hemorrhagic fever virus- and Dugbe virus-infected antigen-presenting cells. J Gen Virol. 2010;91:189–98.
Rodrigues R, Paranhos-Baccala G, Vernet G, Peyrefitte CN. Crimean-Congo hemorrhagic fever virus-infected hepatocytes induce ER-stress and apoptosis crosstalk. PLoS ONE. 2012;7:e29712.
Connolly-Andersen AM, Moll G, Andersson C, Akerstrom S, Karlberg H, Douagi I, Mirazimi A. Crimean-Congo hemorrhagic fever virus activates endothelial cells. J Virol. 2011;85:7766–74.
Canakoglu N, Berber E, Tonbak S, Ertek M, Sozdutmaz I, Aktas M, Kalkan A, Ozdarendeli A. Immunization of knock-out alpha/beta interferon receptor mice against high lethal dose of Crimean-Congo hemorrhagic fever virus with a cell culture based vaccine. PLoS Negl Trop Dis. 2015;9:e0003579.
Monteil V, Salata C, Appelberg S, Mirazimi A. Hazara virus and Crimean-Congo Hemorrhagic Fever Virus show a different pattern of entry in fully-polarized Caco-2 cell line. PLoS Negl Trop Dis. 2020;14:e0008863.
Zivcec M, Safronetz D, Scott DP, Robertson S, Feldmann H. Nucleocapsid protein-based vaccine provides protection in mice against lethal Crimean-Congo hemorrhagic fever virus challenge. PLoS Negl Trop Dis. 2018;12:e0006628.
Ranadheera C, Valcourt EJ, Warner BM, Poliquin G, Rosenke K, Frost K, Tierney K, Saturday G, Miao J, Westover JB, et al. Characterization of a novel STAT 2 knock-out hamster model of Crimean-Congo hemorrhagic fever virus pathogenesis. Sci Rep. 2020;10:12378.
Haddock E, Feldmann F, Hawman DW, Zivcec M, Hanley PW, Saturday G, Scott DP, Thomas T, Korva M, Avsic-Zupanc T, et al. A cynomolgus macaque model for Crimean-Congo haemorrhagic fever. Nat Microbiol. 2018;3:556–62.
Kozak RA, Fraser RS, Biondi MJ, Majer A, Medina SJ, Griffin BD, Kobasa D, Stapleton PJ, Urfano C, Babuadze G, et al. Dual RNA-Seq characterization of host and pathogen gene expression in liver cells infected with Crimean-Congo Hemorrhagic Fever Virus. PLoS Negl Trop Dis. 2020;14:e0008105.
Bente DA, Alimonti JB, Shieh WJ, Camus G, Stroher U, Zaki S, Jones SM. Pathogenesis and immune response of Crimean-Congo hemorrhagic fever virus in a STAT-1 knockout mouse model. J Virol. 2010;84:11089–100.
Koehler JW, Delp KL, Hall AT, Olschner SP, Kearney BJ, Garrison AR, Altamura LA, Rossi CA, Minogue TD. Sequence optimized real-time reverse transcription polymerase chain reaction assay for detection of Crimean-Congo hemorrhagic fever virus. Am J Trop Med Hyg. 2018;98:211–5.
Li H, Hai Y, Lim SY, Toledo N, Crecente-Campo J, Schalk D, Li L, Omange RW, Dacoba TG, Liu LR, et al. Mucosal antibody responses to vaccines targeting SIV protease cleavage sites or full-length Gag and Env proteins in Mauritian cynomolgus macaques. PLoS ONE. 2018;13:e0202997.
Suschak JJ, Golden JW, Fitzpatrick CJ, Shoemaker CJ, Badger CV, Schmaljohn CS, Garrison AR. A CCHFV DNA vaccine protects against heterologous challenge and establishes GP38 as immunorelevant in mice. NPJ Vac. 2021;6:31.
Welch SR, Scholte FEM, Spengler JR, Ritter JM, Coleman-McCray JD, Harmon JR, Nichol ST, Zaki SR, Spiropoulou CF, Bergeron E. The Crimean-Congo hemorrhagic fever virus NSm protein is dispensable for growth in vitro and disease in Ifnar(-/-) mice. Microorganisms. 2020;8:775.
Welch SR, Ritter JM, McElroy AK, Harmon JR, Coleman-McCray JD, Scholte FEM, Kobinger GP, Bergeron E, Zaki SR, Nichol ST, et al. Fluorescent Crimean-Congo hemorrhagic fever virus illuminates tissue tropism patterns and identifies early mononuclear phagocytic cell targets in Ifnar-/- mice. PLoS Pathog. 2019;15:e1008183.
Spengler JR, Patel JR, Chakrabarti AK, Zivcec M, Garcia-Sastre A, Spiropoulou CF, Bergeron E. RIG-I mediates an antiviral response to Crimean-Congo hemorrhagic fever virus. J Virol. 2015;89:10219–29.
Nakabayashi H, Taketa K, Miyano K, Yamane T, Sato J. Growth of human hepatoma cells lines with differentiated functions in chemically defined medium. Cancer Res. 1982;42:3858–63.
Buchholz UJ, Finke S, Conzelmann KK. Generation of bovine respiratory syncytial virus (BRSV) from cDNA: BRSV NS2 is not essential for virus replication in tissue culture, and the human RSV leader region acts as a functional BRSV genome promoter. J Virol. 1999;73:251–9.
Pickering BS, Smith G, Pinette MM, Embury-Hyatt C, Moffat E, Marszal P, Lewis CE. Susceptibility of domestic swine to experimental infection with severe acute respiratory syndrome coronavirus 2. Emerg Infect Dis. 2021;27:104–12.
Li H, Nykoluk M, Li L, Liu LR, Omange RW, Soule G, Schroeder LT, Toledo N, Kashem MA, Correia-Pinto JF, et al. Natural and cross-inducible anti-SIV antibodies in Mauritian cynomolgus macaques. PLoS ONE. 2017;12:e0186079.
Li H, Omange RW, Liang B, Toledo N, Hai Y, Liu LR, Schalk D, Crecente-Campo J, Dacoba TG, Lambe AB, et al. Vaccine targeting SIVmac251 protease cleavage sites protects macaques against vaginal infection. J Clin Invest. 2020;130:6429–42.
Scholte FEM, Zivcec M, Dzimianski JV, Deaton MK, Spengler JR, Welch SR, Nichol ST, Pegan SD, Spiropoulou CF, Bergeron E. Crimean-Congo hemorrhagic fever virus suppresses innate immune responses via a ubiquitin and ISG15 specific protease. Cell Rep. 2017;20:2396–407.
Paragas J, Whitehouse CA, Endy TP, Bray M. A simple assay for determining antiviral activity against Crimean-Congo hemorrhagic fever virus. Antiviral Res. 2004;62:21–5.
Bergeron E, Zivcec M, Chakrabarti AK, Nichol ST, Albarino CG, Spiropoulou CF. Recovery of recombinant crimean Congo Hemorrhagic fever virus reveals a function for non-structural glycoproteins cleavage by furin. PLoS Pathog. 2015;11:e1004879.
Karlberg H, Tan YJ, Mirazimi A. Induction of caspase activation and cleavage of the viral nucleocapsid protein in different cell types during Crimean-Congo hemorrhagic fever virus infection. J Biol Chem. 2011;286:3227–34.
VERO C1008 [Vero 76, clone E6, Vero E6]. Available from: https://www.atcc.org/products/crl-1586 [Cited 2022 September 24]. American Type Culture Collection 2022.
Dulbecco R, Freeman G. Plaque production by the polyoma virus. Virology. 1959;8:396–7.
DMEM – Dulbecco’s Modified Eagle Medium. Available from: https://www.thermofisher.com/ca/en/home/life-science/cell-culture/mammalian-cell-culture/classical-media/dmem.html [Cited 2022 September 24]. ThermoFisher Scientific 2022.
Classical Media & Buffers. Available from: https://www.sigmaaldrich.com/CA/en/products/cell-culture-and-analysis/cell-culture-media-and-buffers/classical-media-and-buffers [Cited 2022-09-24]. Sigma-Aldrich 2022.
Wu XW, Wang RF, Yuan M, Xu W, Yang XW. Dulbecco’s modified eagle’s medium and minimum essential medium–which one is more preferred for establishment of Caco-2 cell monolayer model used in evaluation of drug absorption? Pharmazie. 2013;68:805–10.
SW-13. Available from: https://www.atcc.org/products/ccl-105 [Cited 2022 September 24]. American Type Culture Collection 2022.
Leibovitz A, McCombs WM, 3rd, Johnston D, McCoy CE, Stinson JC: New human cancer cell culture lines. I. SW-13, small-cell carcinoma of the adrenal cortex. J Natl Cancer Inst 1973, 51:691–697.
Ammerman NC, Beier-Sexton M, Azad AF: Growth and maintenance of Vero cell lines. Curr Protoc Microbiol 2008, Appendix 4:Appendix 4E.
Nahapetian AT, Thomas JN, Thilly WG. Optimization of environment for high density Vero cell culture: effect of dissolved oxygen and nutrient supply on cell growth and changes in metabolites. J Cell Sci. 1986;81:65–103.
JCRB9069 SW-13. Available from: https://cellbank.nibiohn.go.jp/~cellbank/en/search_res_det.cgi?ID=608 [Cited 2022 September 24]. Japanese Collection of Research Bioresources Cell Bank 2022.
Andersson I, Karlberg H, Mousavi-Jazi M, Martinez-Sobrido L, Weber F, Mirazimi A. Crimean-Congo hemorrhagic fever virus delays activation of the innate immune response. J Med Virol. 2008;80:1397–404.
Zivcec M, Safronetz D, Scott D, Robertson S, Ebihara H, Feldmann H. Lethal Crimean-Congo hemorrhagic fever virus infection in interferon alpha/beta receptor knockout mice is associated with high viral loads, proinflammatory responses, and coagulopathy. J Infect Dis. 2013;207:1909–21.
Lindquist ME, Zeng X, Altamura LA, Daye SP, Delp KL, Blancett C, Coffin KM, Koehler JW, Coyne S, Shoemaker CJ, et al. Exploring Crimean-Congo Hemorrhagic fever virus-induced hepatic injury using antibody-mediated Type I interferon blockade in mice. J Virol 2018, 92.
Mo Q, Feng K, Dai S, Wu Q, Zhang Z, Ali A, Deng F, Wang H, Ning YJ. Transcriptome profiling highlights regulated biological processes and type III interferon antiviral responses upon Crimean-Congo hemorrhagic fever virus infection. Virol Sin. 2023;38:34–46.
Li M, Embury-Hyatt C, Weingartl HM. Experimental inoculation study indicates swine as a potential host for Hendra virus. Vet Res. 2010;41:33.
Sanchez AJ, Vincent MJ, Nichol ST. Characterization of the glycoproteins of Crimean-Congo hemorrhagic fever virus. J Virol. 2002;76:7263–75.
Li N, Rao G, Li Z, Yin J, Chong T, Tian K, Fu Y, Cao S. Cryo-EM structure of glycoprotein C from Crimean-Congo hemorrhagic fever virus. Virol Sin. 2022;37:127–37.
Duh D, Nichol ST, Khristova ML, Saksida A, Hafner-Bratkovic I, Petrovec M, Dedushaj I, Ahmeti S, Avsic-Zupanc T. The complete genome sequence of a Crimean-Congo hemorrhagic fever virus isolated from an endemic region in Kosovo. Virol J. 2008;5:7.