Recent advances in understanding crimean-congo hemorrhagic fever virus.

F1000Research

Volumn 7, Issue , 2018, Pages

  Hawman, David W ^a   Feldmann, Heinz ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

Animal models; Antivirals; CCHF disease; CCHFV; Crimean Congo hemorrhagic fever virus; Pathogenesis; Vaccines

Indexed keywords

FAVIPIRAVIR; RIBAVIRIN; VIRUS GLYCOPROTEIN; VIRUS NUCLEOPROTEIN; VIRUS VACCINE;

CRIMEAN CONGO HEMORRHAGIC FEVER; DRUG DESIGN; GENETIC VARIABILITY; GEOGRAPHIC DISTRIBUTION; HUMAN; MORBIDITY; MORTALITY RATE; NONHUMAN; PATHOGENESIS; REVIEW; ANIMAL; CRIMEAN-CONGO HEMORRHAGIC FEVER VIRUS; DISEASE MODEL; GENETICS; IMMUNOLOGY; PATHOGENICITY; VIROLOGY;

ANIMALS; DISEASE MODELS, ANIMAL; HEMORRHAGIC FEVER VIRUS, CRIMEAN-CONGO; HEMORRHAGIC FEVER, CRIMEAN; HOST MICROBIAL INTERACTIONS; HUMANS; VIRAL VACCINES;

EID: 85056313193     PISSN: None     EISSN: 20461402     Source Type: Journal    
DOI: 10.12688/F1000RESEARCH.16189.1     Document Type: Review

References (90)

1. Hoogstraal H: The epidemiology of tick-borne Crimean-Congo hemorrhagic fever in Asia, Europe, and Africa. J Med Entomol. 1979; 15(4): 307-417.
2. Casals J: Antigenic similarity between the virus causing Crimean hemorrhagic fever and Congo virus. Proc Soc Exp Biol Med. 1969; 131(1): 233-6.
3. Bente DA, Forrester NL, Watts DM, et al.: Crimean-Congo hemorrhagic fever: History, epidemiology, pathogenesis, clinical syndrome and genetic diversity. Antiviral Res. 2013; 100(1): 159-89.
4. Gargili A, Estrada-Peña A, Spengler JR, et al.: The role of ticks in the maintenance and transmission of Crimean-Congo hemorrhagic fever virus: A review of published field and laboratory studies. Antiviral Res. 2017; 144: 93-119.
5. Spengler JR, Bergeron É, Rollin PE: Seroepidemiological Studies of Crimean-Congo Hemorrhagic Fever Virus in Domestic and Wild Animals. PLoS Negl Trop Dis. 2016; 10(1): E0004210.
6. Gordon SW, Linthicum KJ, Moulton JR: Transmission of Crimean-Congo hemorrhagic fever virus in two species of Hyalomma ticks from infected adults to cofeeding immature forms. Am J Trop Med Hyg. 1993; 48(4): 576-80.
7. Crimean-Congo haemorrhagic fever. 2017.
8. Ergönül O: Crimean-Congo haemorrhagic fever. Lancet Infect Dis. 2006; 6(4): 203-14.
9. Bodur H, Akinci E, Ascioglu S, et al.: Subclinical infections with Crimean-Congo hemorrhagic fever virus, Turkey. Emerg Infect Dis. 2012; 18(4): 640-2.
10. Hasanoglu I, Guner R, Carhan A, et al.: Crucial parameter of the outcome in Crimean Congo hemorrhagic fever: Viral load. J Clin Virol. 2016; 75: 42-6.
11. Duh D, Saksida A, Petrovec M, et al.: Viral load as predictor of Crimean-Congo hemorrhagic fever outcome. Emerg Infect Dis. 2007; 13(11): 1769-72.
12. Ergonul O, Celikbas A, Baykam N, et al.: Analysis of risk-factors among patients with Crimean-Congo haemorrhagic fever virus infection: Severity criteria revisited. Clin Microbiol Infect. 2006; 12(6): 551-4.
13. Shepherd AJ, Swanepoel R, Leman PA: Antibody response in Crimean-Congo hemorrhagic fever. Rev Infect Dis. 1989; 11 Suppl 4: S801-S806.
14. Swanepoel R, Gill DE, Shepherd AJ, et al.: The clinical pathology of Crimean-Congo hemorrhagic fever. Rev Infect Dis. 1989; 11 Suppl 4: S794-S800.
15. Cevik MA, Erbay A, Bodur H, et al.: Clinical and laboratory features of Crimean-Congo hemorrhagic fever: Predictors of fatality. Int J Infect Dis. 2008; 12(4): 374-9.
16. Ergonul O, Tuncbilek S, Baykam N, et al.: Evaluation of serum levels of interleukin (IL)-6, IL-10, and tumor necrosis factor-alpha in patients with Crimean-Congo hemorrhagic fever. J Infect Dis. 2006; 193(7): 941-4.
17. Papa A, Bino S, Velo E, et al.: Cytokine levels in Crimean-Congo hemorrhagic fever. J Clin Virol. 2006; 36(4): 272-6.
18. Kaya S, Elaldi N, Kubar A, et al.: Sequential determination of serum viral titers, virus-specific IgG antibodies, and TNF-α, IL-6, IL-10, and IFN-γ levels in patients with Crimean-Congo hemorrhagic fever. BMC Infect Dis. 2014; 14: 416.
19. Papa A, Tsergouli K, Çağlayık DY, et al.: Cytokines as biomarkers of Crimean-Congo hemorrhagic fever. J Med Virol. 2016; 88(1): 21-7.
20. Sas MA, Vina-Rodriguez A, Mertens M, et al.: A one-step multiplex real-time RT-PCR for the universal detection of all currently known CCHFV genotypes. J Virol Methods. 2018; 255: 38-43.
21. Atkinson B, Chamberlain J, Logue CH, et al.: Development of a real-time RT-PCR assay for the detection of Crimean-Congo hemorrhagic fever virus. Vector Borne Zoonotic Dis. 2012; 12(9): 786-93.
22. Jääskeläinen AJ, Kallio-Kokko H, Ozkul A, et al.: Development and evaluation of a real-time RT-qPCR for detection of Crimean-Congo hemorrhagic fever virus representing different genotypes. Vector Borne Zoonotic Dis. 2014; 14(12): 870-2.
23. Zivcec M, Safronetz D, Scott D, et al.: Lethal Crimean-Congo hemorrhagic fevervirus infection in interferon α/β receptor knockout mice is associated with high viral loads, proinflammatory responses, and coagulopathy. J Infect Dis. 2013; 207(12): 1909-21.
24. Bereczky S, Lindegren G, Karlberg H, et al.: Crimean-Congo hemorrhagic fever virus infection is lethal for adult type I interferon receptor-knockout mice. J Gen Virol. 2010; 91(Pt 6): 1473-7.
25. Bente DA, Alimonti JB, Shieh WJ, et al.: Pathogenesis and immune response of Crimean-Congo hemorrhagic fever virus in a STAT-1 knockout mouse model. J Virol. 2010; 84(21): 11089-100.
26. Spengler JR, Patel JR, Chakrabarti AK, et al.: RIG-I Mediates an Antiviral Response to Crimean-Congo Hemorrhagic Fever Virus. J Virol. 2015; 89(20): 10219-29.
27. Habjan M, Andersson I, Klingström J, et al.: Processing of genome 5’ termini as a strategy of negative-strand RNA viruses to avoid RIG-I-dependent interferon induction. PLoS One. 2008; 3(4): E2032.
28. Arslan S, Engin A, Özbilüm N, et al.: Toll-like receptor 7 Gln11Leu, c.4-151A/G, and +1817G/T polymorphisms in Crimean Congo hemorrhagic fever. J Med Virol. 2015; 87(7): 1090-5.
29. Engin A, Arslan S, Kizildag S, et al.: Toll-like receptor 8 and 9 polymorphisms in Crimean-Congo hemorrhagic fever. Microbes Infect. 2010; 12(12-13): 1071-8.
30. Kızıldağ S, Arslan S, Özbilüm N, et al.: Effect of TLR10 (2322A/G, 720A/C, and 992T/A) polymorphisms on the pathogenesis of Crimean Congo hemorrhagic fever disease. J Med Virol. 2018; 90(1): 19-25.
31. Arslan S, Engin A: Relationship between NF-κB1 and NF-κBIA genetic polymorphisms and Crimean-Congo hemorrhagic fever. Scand J Infect Dis. 2012; 44(2): 138-43.
32. Barnwal B, Karlberg H, Mirazimi A, et al.: The Non-structural Protein of Crimean-Congo Hemorrhagic Fever Virus Disrupts the Mitochondrial Membrane Potential and Induces Apoptosis. J Biol Chem. 2016; 291(2): 582-92.
33. Rodrigues R, Paranhos-Baccalà G, Vernet G, et al.: Crimean-Congo hemorrhagic fever virus-infected hepatocytes induce ER-stress and apoptosis crosstalk. PLoS One. 2012; 7(1): E29712.
34. 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(5): 3227-34.
35. Wang Y, Dutta S, Karlberg H, et al.: Structure of Crimean-Congo hemorrhagic fever virus nucleoprotein: Superhelical homo-oligomers and the role of caspase-3 cleavage. J Virol. 2012; 86(22): 12294-303.
36. Scholte FEM, Zivcec M, Dzimianski JV, et al.: Crimean-Congo Hemorrhagic Fever Virus Suppresses Innate Immune Responses via a Ubiquitin and ISG15 Specific Protease. Cell Rep. 2017; 20(10): 2396-407.
37. Frias-Staheli N, Giannakopoulos NV, Kikkert M, et al.: Ovarian tumor domaincontaining viral proteases evade ubiquitin-and ISG15-dependent innate immune responses. Cell Host Microbe. 2007; 2(6): 404-16.
38. James TW, Frias-Staheli N, Bacik JP, et al.: Structural basis for the removal of ubiquitin and interferon-stimulated gene 15 by a viral ovarian tumor domaincontaining protease. Proc Natl Acad Sci U S A. 2011; 108(6): 2222-7.
39. Perng YC, Lenschow DJ: ISG15 in antiviral immunity and beyond. Nat Rev Microbiol. 2018; 16(7): 423-39.
40. Capodagli GC, Deaton MK, Baker EA, et al.: Diversity of ubiquitin and ISG15 specificity among nairoviruses’ viral ovarian tumor domain proteases. J Virol. 2013; 87(7): 3815-27.
41. Deaton MK, Dzimianski JV, Daczkowski CM, et al.: Biochemical and Structural Insights into the Preference of Nairoviral DeISGylases for Interferon-Stimulated Gene Product 15 Originating from Certain Species. J Virol. 2016; 90(18): 8314-27.
42. Fritzen A, Risinger C, Korukluoglu G, et al.: Epitope-mapping of the glycoprotein from Crimean-Congo hemorrhagic fever virus using a microarray approach. PLoS Negl Trop Dis. 2018; 12(7): E0006598.
43. Bertolotti-Ciarlet A, Smith J, Strecker K, et al.: Cellular localization and antigenic characterization of crimean-congo hemorrhagic fever virus glycoproteins. J Virol. 2005; 79(10): 6152-61.
44. Buttigieg KR, Dowall SD, Findlay-Wilson S, et al.: A novel vaccine against Crimean-Congo Haemorrhagic Fever protects 100% of animals against lethal challenge in a mouse model. PLoS One. 2014; 9(3): E91516.
45. Dowall SD, Graham VA, Rayner E, et al.: 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(6): E0156637.
46. Akinci E, Yilmaz M, Bodur H, et al.: Analysis of lymphocyte subgroups in Crimean-Congo hemorrhagic fever. Int J Infect Dis. 2009; 13(5): 560-3.
47. Goedhals D, Paweska JT, Burt FJ: Long-lived CD8+ T cell responses following Crimean-Congo haemorrhagic fever virus infection. PLoS Negl Trop Dis. 2017; 11(12): E0006149.
48. Akıncı E, Bodur H, Muşabak U, et al.: The relationship between the human leukocyte antigen system and Crimean-Congo hemorrhagic fever in the Turkish population. Int J Infect Dis. 2013; 17(11): E1038-41.
49. Spengler JR, Kelly Keating M, McElroy AK, et al.: Crimean-Congo Hemorrhagic Fever in Humanized Mice Reveals Glial Cells as Primary Targets of Neurological Infection. J Infect Dis. 2017; 216(11): 1386-97.
50. Lindquist ME, Zeng X, Altamura LA, et al.: Exploring Crimean-Congo Hemorrhagic Fever Virus-Induced Hepatic Injury Using Antibody-Mediated Type I Interferon Blockade in Mice. J Virol. 2018; 92(21): Pii: E01083-18.
51. Haddock E, Feldmann F, Hawman DW, et al.: A cynomolgus macaque model for Crimean-Congo haemorrhagic fever. Nat Microbiol. 2018; 3(5): 556-62.
52. Smirnova SE: A comparative study of the Crimean hemorrhagic fever-Congo group of viruses. Arch Virol. 1979; 62(2): 137-43.
53. Oestereich L, Rieger T, Neumann M, et al.: Evaluation of antiviral efficacy of ribavirin, arbidol, and T-705 (favipiravir) in a mouse model for Crimean-Congo hemorrhagic fever. PLoS Negl Trop Dis. 2014; 8(5): E2804.
54. Hawman DW, Haddock E, Meade-White K, et al.: Favipiravir (T-705) but not ribavirin is effective against two distinct strains of Crimean-Congo hemorrhagic fever virus in mice. Antiviral Res. 2018; 157: 18-26.
55. Canakoglu N, Berber E, Tonbak S, et al.: Immunization of knock-out α/β 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(3): E0003579.
56. Garrison AR, Shoemaker CJ, Golden JW, et al.: A DNA vaccine for Crimean-Congo hemorrhagic fever protects against disease and death in two lethal mouse models. PLoS Negl Trop Dis. 2017; 11(9): E0005908.
57. Papa A, Tsergouli K, Tsioka K, et al.: Crimean-Congo Hemorrhagic Fever: Tick-Host-Virus Interactions. Front Cell Infect Microbiol. 2017; 7: 213.
58. Šimo L, Kazimirova M, Richardson J, et al.: The Essential Role of Tick Salivary Glands and Saliva in Tick Feeding and Pathogen Transmission. Front Cell Infect Microbiol. 2017; 7: 281.
59. Rodriguez SE, McAuley AJ, Gargili A, et al.: Interactions of Human Dermal Dendritic Cells and Langerhans Cells Treated with Hyalomma Tick Saliva with Crimean-Congo Hemorrhagic Fever Virus. Viruses. 2018; 10(7): Pii: E381.
60. Xia H, Beck AS, Gargili A, et al.: Transstadial Transmission and Long-term Association of Crimean-Congo Hemorrhagic Fever Virus in Ticks Shapes Genome Plasticity. Sci Rep. 2016; 6: 35819.
61. Mousavi-Jazi M, Karlberg H, Papa A, et al.: Healthy individuals’ immune response to the Bulgarian Crimean-Congo hemorrhagic fever virus vaccine. Vaccine. 2012; 30(44): 6225-9.
62. Papa A, Papadimitriou E, Christova I: The Bulgarian vaccine Crimean-Congo haemorrhagic fever virus strain. Scand J Infect Dis. 2011; 43(3): 225-9.
63. Hinkula J, Devignot S, Åkerström S, 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(10): Pii: E02076-16. 64.
64. Ghiasi SM, Salmanian AH, Chinikar S, et al.: Mice orally immunized with a transgenic plant expressing the glycoprotein of Crimean-Congo hemorrhagic fever virus. Clin Vaccine Immunol. 2011; 18(12): 2031-7.
65. Kortekaas J, Vloet RP, McAuley AJ, et al.: Crimean-Congo Hemorrhagic Fever Virus Subunit Vaccines Induce High Levels of Neutralizing Antibodies But No Protection in STAT1 Knockout Mice. Vector Borne Zoonotic Dis. 2015; 15(12): 759-64.
66. Rahpeyma M, Samarbaf-Zadeh A, Makvandi M, et al.: Expression and characterization of codon-optimized Crimean-Congo hemorrhagic fever virus Gn glycoprotein in insect cells. Arch Virol. 2017; 162(7): 1951-62.
67. Zivcec M, Safronetz D, Scott DP, et al.: Nucleocapsid protein-based vaccine provides protection in mice against lethal Crimean-Congo hemorrhagic fever virus challenge. PLoS Negl Trop Dis. 2018; 12(7): E0006628.
68. Dowall SD, Buttigieg KR, Findlay-Wilson SJ, et al.: A Crimean-Congo hemorrhagic fever (CCHF) viral vaccine expressing nucleoprotein is immunogenic but fails to confer protection against lethal disease. Hum Vaccin Immunother. 2016; 12(2): 519-27.
69. Soares-Weiser K, Thomas S, Thomson G, et al.: Ribavirin for Crimean-Congo hemorrhagic fever: Systematic review and meta-analysis. BMC Infect Dis. 2010; 10: 207.
70. Ascioglu S, Leblebicioglu H, Vahaboglu H, et al.: Ribavirin for patients with Crimean-Congo haemorrhagic fever: A systematic review and meta-analysis. J Antimicrob Chemother. 2011; 66(6): 1215-22.
71. Johnson S, Henschke N, Maayan N, et al.: Ribavirin for treating Crimean Congo haemorrhagic fever. Cochrane Database Syst Rev. 2018; 6: CD012713.
72. Koksal I, Yilmaz G, Aksoy F, et al.: The efficacy of ribavirin in the treatment of Crimean-Congo hemorrhagic fever in Eastern Black Sea region in Turkey. J Clin Virol. 2010; 47(1): 65-8.
73. Ergönül Ö, Keske Ş, Çeldir MG, et al.: Systematic Review and Meta-analysis of Postexposure Prophylaxis for Crimean-Congo Hemorrhagic Fever Virus among Healthcare Workers. Emerg Infect Dis. 2018; 24(9): 1642-8.
74. Espy N, Pérez-Sautu U, Ramírez de Arellano E, et al.: Ribavirin Had Demonstrable Effects on the Crimean-Congo Hemorrhagic Fever Virus (CCHFV) Population and Load in a Patient With CCHF Infection. J Infect Dis. 2018; 217(12): 1952-6.
75. Negredo A, de la Calle-Prieto F, Palencia-Herrejón E, et al.: Autochthonous Crimean-Congo Hemorrhagic Fever in Spain. N Engl J Med. 2017; 377(2): 154-61.
76. Muller MP, Dresser L, Raboud J, et al.: Adverse events associated with highdose ribavirin: Evidence from the Toronto outbreak of severe acute respiratory syndrome. Pharmacotherapy. 2007; 27(4): 494-503.
77. Devine EB, Kowdley KV, Veenstra DL, et al.: Management strategies for ribavirin-induced hemolytic anemia in the treatment of hepatitis C: Clinical and economic implications. Value Health. 2001; 4(5): 376-84.
78. Ergonul O: Evidence supports ribavirin use in Crimean-Congo hemorrhagic fever. Int J Infect Dis. 2014; 29: 296.
79. Ergonul O: DEBATE (see Elaldi N et al, Efficacy of oral ribavirin treatment in Crimean-Congo haemorrhagic fever: A quasi-experimental study from Turkey. Journal of Infection 2009; 58: 238-244).
80. Ergonul O. Biases and misinterpretation in the assessment of the efficacy of oral ribavirin in the treatment of Crimean-Congo hemorrhagic fever. J Infect. 2009; 59(4): 284-6; author reply 286-9.
81. Ceylan B, Calıca A, Ak O, et al.: Ribavirin is not effective against Crimean-Congo hemorrhagic fever: Observations from the Turkish experience. Int J Infect Dis. 2013; 17(10): E799-801.
82. Ascioglu S, Leblebicioglu H, Elaldi N, et al.: Response to Ergonul: Scientific Evidence Versus Personal Beliefs In Crimean-Congo Haemorrhagic Fever Treatment. J Infect. 2009; 59(4): 286-9.
83. Arda B, Aciduman A, Johnston JC: A randomised controlled trial of ribavirin in Crimean Congo haemorrhagic fever: Ethical considerations. J Med Ethics. 2012; 38(2): 117-20.
84. Furuta Y, Takahashi K, Fukuda Y, et al.: In vitro and in vivo activities of antiinfluenza virus compound T-705. Antimicrob Agents Chemother. 2002; 46(4): 977-81.
85. Oestereich L, Lüdtke A, Wurr S, et al.: Successful treatment of advanced Ebola virus infection with T-705 (favipiravir) in a small animal model. Antiviral Res. 2014; 105: 17-21.
86. Rosenke K, Feldmann H, Westover JB, et al.: Use of Favipiravir to Treat Lassa Virus Infection in Macaques. Emerg. Infect. Dis. 2018; 24(9): 1696-9.
87. Safronetz D, Rosenke K, Westover JB, et al.: The broad-spectrum antiviral favipiravir protects guinea pigs from lethal Lassa virus infection post-disease onset. Sci Rep. 2015; 5: 14775.
88. Raabe VN, Kann G, Ribner BS, et al.: Favipiravir and Ribavirin Treatment of Epidemiologically Linked Cases of Lassa Fever. Clin Infect Dis. 2017; 65(5): 855-9.
89. Welch SR, Scholte FEM, Flint M, et al.: 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.
90. Zivcec M, Guerrero LIW, Albariño CG, et al.: Identification of broadly neutralizing monoclonal antibodies against Crimean-Congo hemorrhagic fever virus. Antiviral Res. 2017; 146: 112-20.