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Crimean-Congo Haemorrhagic Fever Virus, an Emerging and Re-Emerging Pathogen

  • Felicity Jane BurtEmail author
  • Dominique Goedhals
Chapter

Abstract

Crimean-Congo haemorrhagic fever (CCHF) is a tick-borne viral zoonosis distributed in Africa, Asia, eastern Europe and the Balkans. The broad geographic range correlates with that of the principal vector of the virus, ticks belonging to the genus Hyalomma. Humans acquire infection through tick-bite or exposure to infected blood or tissues of animals or humans. Human infection is characterized by febrile illness with headache, myalgia and petechial rash, frequently followed by a hemorrhagic state and in some cases a fatal outcome. The importance of the tick-vertebrate-tick cycle in maintaining virus transmission is well established. Small mammals are considered important amplifying hosts of the virus. Domestic livestock show mild or no clinical signs of illness but develop a short period of viremia, during which the virus can be transmitted to humans, hence there is an occupational risk associated with employment in the livestock industry among farmers, farm workers, abattoir workers and veterinarians. The emergence of CCHF from 2002 in several countries in the Balkans raises concerns that this virus could expand its current geographic distribution and establish new endemic foci. Monitoring and control of the spread will require increased diagnostic capacity as well as surveillance and novel approaches to development of vaccines and drugs and vector control .

Keywords

Reverse Transcription Polymerase Chain Reaction Viral Nucleic Acid Rift Valley Fever Real Time Reverse Transcription Polymerase Chain Reaction Acalculous Cholecystitis 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Aksoy HZ, Yilmaz G, Aksoy F et al (2010) Crimean-Congo haemorrhagic fever presenting as epididymo-orchitis. J Clin Virol 48:282–284PubMedGoogle Scholar
  2. Akyol M, Özçelik S, Engin A et al (2010) Cutaneous manifestations of Crimean-Congo haemorrhagic fever: morbilliform eruptions may reflect a favourable outcome and not low platelet levels. Eur J Dermatol 20:523–524PubMedGoogle Scholar
  3. Al Tikriti SK, Al Ani F, Jurji FJ et al (1981) Congo/Crimean haemorrhagic fever in Iraq. Bull WHO 59:85–90PubMedCentralPubMedGoogle Scholar
  4. Altamura LA, Bertolotti-Ciarlet A, Teogler J (2007) Identification of a novel C-terminal cleavage of Crimean-Congo hemorrhagic fever virus PreGN that leads to generation of an NSM protein. J Virol 81:6632–6642PubMedCentralPubMedGoogle Scholar
  5. Ascioglu S, Leblebicioglu H, Vahaboglu H et al (2011) Ribavirin for patients with Crimean-Congo haemorrhagic fever: a systematic review and meta-analysis. J Antimicrob Chemother 66:1215–1222PubMedGoogle Scholar
  6. Barr JN, Elliott RM, Dunn EF et al (2003) Segment specific terminal sequences of Bunyamwera bunyavirus regulate genome replication. Virology 311:326–338PubMedGoogle Scholar
  7. Begum F, Wisseman CL, Casals J (1970) Tick-borne viruses of West-Pakistan. II Hazara virus, a new agent isolated from Ixides redikorzevi ticks from the Kaghan valley, West Pakistan. Am J Epidemiol 92:192–194PubMedGoogle Scholar
  8. Bente DA, Alimonti JB, Wun-Ju S et al (2010) Pathogenesis and immune response of Crimean-Congo hemorrhagic fever virus in a STAT-1 knockout mouse model. J Virol 84:11089–11100PubMedCentralPubMedGoogle Scholar
  9. Bergeron E, Vincent MJ, Nichol ST (2007) Crimean-Congo hemorrhagic fever virus glycoprotein processing by the endoprotease SKI-1/S1P is critical for virus infectivity. J Virol 81:13271–13276PubMedCentralPubMedGoogle Scholar
  10. Bergeron E, Albarino CG, Khristova ML et al (2010) Crimean-Congo hemorrhagic fever virus-encoded ovarian tumor protease activity is dispensable for virus RNA polymerase function. J Virol 84:216–226PubMedCentralPubMedGoogle Scholar
  11. Bertolotti-Ciarlet A, Smith J, Strecker K et al (2005) Cellular localization and antigenic characterization of Crimean-Congo hemorrhagic fever virus glycoproteins. J Virol 79:6152–6162PubMedCentralPubMedGoogle Scholar
  12. Burney MI, Ghafoor A, Saleen M et al (1980) Nosocomial outbreak of viral hemorrhagic fever caused by Crimean Hemorrhagic fever-Congo virus in Pakistan, January 1976. Am J Trop Med Hyg 29:941–947PubMedGoogle Scholar
  13. Burt FJ, Leman PA, Abbott JC et al (1994) Serodiagnosis of Crimean-Congo haemorrhagic fever. Epidemiol Infect 113:551–562PubMedCentralPubMedGoogle Scholar
  14. Burt FJ, Swanepoel R, Shieh WJ et al (1997) Immunohistochemical and in situ localization of Crimean-Congo hemorrhagic fever (CCHF) virus in human tissues and implications for CCHF pathogenesis. Arch Pathol Lab Med 121:839–846PubMedGoogle Scholar
  15. Burt FJ, Leman PA, Smith JF et al (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. J Virol Methods 70:129–137PubMedGoogle Scholar
  16. Burt FJ, Swanepoel R (2005) Molecular epidemiology of African and Asian Crimean-Congo haemorrhagic fever isolates. Epidemiol Infect 133:659–666PubMedCentralPubMedGoogle Scholar
  17. Burt FJ, Paweska JT, Ashkettle B et al (2009). Genetic relationship among southern African Crimean-Congo haemorrhagic fever virus isolates and evidence for occurrence of reassortment. Epid Infect Sep 137:1302–1308Google Scholar
  18. Burt FJ (2011) Laboratory diagnosis of Crimean-Congo hemorrhagic fever virus infections. Future Virol 6:831–841Google Scholar
  19. Calisher CH, Karabatsos N (1989) Arbovirus serogroups: definition and geographic distribution. In: Monath TP (ed) The arboviruses: epidemiology and ecology, vol 1. CRC Press, Florida, pp 19–57Google Scholar
  20. Calisher CH (1991) Bunyaviridae. In: Rancki RJB, Fauquet CM, Knidson DL, Brown F (eds) Classification of viruses. Fifth report of the international committee on taxonomy of viruses. (Arch Virol 121:S273–S283)Google Scholar
  21. Casals J (1969) Antigenic similarity between the virus causing Crimean hemorrhagic fever and Congo virus. Proc Soc Exp Biol Med 131:233–236PubMedGoogle Scholar
  22. Casals J, Tignor GH (1980) The Nairovirus genus: serological relationships. Intervirology. 14:144–147PubMedGoogle Scholar
  23. Ceianu CS, Panculescu-Gatej RI, Coudrier D et al (2012) First serologic evidence for the circulation of Crimean-Congo hemorrhagic fever virus in Romania. Vector Borne Zoonotic Dis 12:718–721PubMedGoogle Scholar
  24. Cevik MA, Erbay A, Bodur H et al (2007) Viral load as a predictor of outcome in Crimean-Congo hemorrhagic fever. Clin Infect Dis 45:96–100Google Scholar
  25. Chinikar S, Persson SM, Johansson M et al (2004) Genetic analysis of Crimean-Congo hemorrhagic fever virus in Iran. J Med Virol 73:404–411PubMedGoogle Scholar
  26. Chumakov MP, Smirnova SE, Tkachenko EA (1970) Relationship between strains of Crimean haemorrhagic fever and Congo viruses. Acta Virol 14:82–85PubMedGoogle Scholar
  27. Clerx JP, Casals J, Bishop DH (1981) Structural characteristics of nairoviruses (genus Nairovirus, Bunyaviridae). J Gen Virol 55:165–178PubMedGoogle Scholar
  28. Connolly-Andersen AM, Moll G, Andersson C et al (2011) Crimean-Congo hemorrhagic fever virus activates endothelial cells. J Virol 85:7766–7774PubMedCentralPubMedGoogle Scholar
  29. Deyde VM, Khristova ML, Rollin PE et al (2006) Crimean-Congo hemorrhagic fever virus genomics and global diversity. J Virol 80:8834–8842PubMedCentralPubMedGoogle Scholar
  30. Dilber E, Cakir M, Acar EA et al (2009) Crimean-Congo haemorrhagic fever among children in north-eastern Turkey. Ann Trop Paediatr 29:23–28PubMedGoogle Scholar
  31. Donets MA, Chumakov MP, Korolev MB et al (1977) Physicochemical characteristics, morphology and morphogenesis of virions of the causative agent of Crimean hemorrhagic fever. Intervirology 8:294–308PubMedGoogle Scholar
  32. Drosten CS, Gottig S, Schilling M et al (2002) Rapid detection and quantification of RNA of Ebola and Marburg viruses, Lassa virus, dengue virus, and yellow fever virus by real-time reverse transcription-PCR. J Clin Microbiol 40:2323–2330PubMedCentralPubMedGoogle Scholar
  33. Duh D, Saksida A, Petrovec M et al (2006) Novel one-step real-time RT-PCR assay for rapid and specific diagnosis of Crimean-Congo hemorrhagic fever encountered in the Balkans. J Virol Methods 133:175–179PubMedGoogle Scholar
  34. Duh D, Saksida A, Petrovec M et al (2007) Viral load as predictor of Crimean-Congo hemorrhagic fever outcome. Emerg Infect Dis 13:1769–1772PubMedCentralPubMedGoogle Scholar
  35. Dunster L, Dunster M, Ofula V et al (2002) First documentation of human Crimean-Congo hemorrhagic fever, Kenya. Emerg Infect Dis 8:1005–1006PubMedCentralPubMedGoogle Scholar
  36. El Azazy OM, Scrimgeour EM (1997) Crimean-Congo haemorrhagic fever virus infection in the western province of Saudi Arabia. Trans R Soc Trop Med Hyg 91:275–278PubMedGoogle Scholar
  37. Elevli M, Ozkul AA, Civilibal M et al (2010) A newly identified Crimean-Congo hemorrhagic fever virus strain in Turkey. Int J Infect Dis 14:e213–216PubMedGoogle Scholar
  38. Engin A, Erdogan H, Ozec AV et al (2009) Ocular findings in patients with Crimean-Congo hemorrhagic fever. Am J Ophthalmol 147:634–638PubMedGoogle Scholar
  39. Erbay A, Çevik MA, Önguru P et al (2008) Breastfeeding in Crimean-Congo haemorrhagic fever. Scand J Infect Dis 40:186–188PubMedGoogle Scholar
  40. Ergönül O, Çelikbaş A, Dokuzoğuz B et al (2004) Characteristics of patients with Crimean-Congo hemorrhagic fever in a recent outbreak in Turkey and impact of oral ribavirin therapy. Clin Infect Dis 39:284–287PubMedGoogle Scholar
  41. Ergonul O, Celikbas A, Baykam N et al (2006a) Analysis of risk-factors among patients with Crimean-Congo haemorrhagic fever virus infection: severity criteria revisited. Clin Microbiol Infect 12:551–554Google Scholar
  42. Ergonul O, Tuncbilek S, Baykam N et al (2006b) 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 193:941–944Google Scholar
  43. Ergonul O (2006c) Crimean-Congo haemorrhagic fever. Lancet Infect Dis 6:203–214Google Scholar
  44. Ergonul O (2008) Treatment of Crimean-Congo hemorrhagic fever. Antiviral Res 78:125–131PubMedGoogle Scholar
  45. Ergonul O, Celikbas A, Yildrim U et al (2010) Pregnancy and Crimean-Congo haemorrhagic fever. Clin Microbiol Infect 16:647–650PubMedGoogle Scholar
  46. Estrada-Peña A, Palomar AM, Santibáñez P et al (2012). Crimean-Congo hemorrhagic fever virus in ticks, Southwestern Europe, 2010. Emerg Infect Dis 18:179–180PubMedCentralPubMedGoogle Scholar
  47. Fisgin NT, Fisgin T, Tanyel E et al (2008) Crimean-Congo hemorrhagic fever: five patients with hemophagocytic syndrome. Am J Hematol 83:73–76PubMedGoogle Scholar
  48. Fisher-Hoch SP, Khan JA, Rehman S et al (1995) Crimean Congo-haemorrhagic fever treated with oral ribavirin. Lancet 346:472–475PubMedGoogle Scholar
  49. Flick R, Elgh F, Pettersson RF (2002) Mutational analysis of the Uukuniemei virus (Bunyaviridae family) promoter reveals two elements of functional importance. J Virol 76:10849–10860PubMedCentralPubMedGoogle Scholar
  50. Frias-Staheli N, Giannakopoulos NV, Kikkert M et al (2007) Ovarian tumor (OTU)-domain containing viral proteases evade ubiquitin- and ISG15-dependent innate immune responses. Cell Host Microbe 2:404–416PubMedCentralPubMedGoogle Scholar
  51. Garrison AR, Alakbarova S, Kulesh DA et al (2007) Development of a TaqMan minor groove binding protein assay for the detection and quantification of Crimean-Congo hemorrhagic fever virus. Am J Trop Med Hyg 77:514–520PubMedGoogle Scholar
  52. Gear JH, Thomson PD, Hopp M et al (1982) Congo-Crimean haemorrhagic fever in South Africa. Report of a fatal case in the Transvaal. S Afr Med J 62:576–580PubMedGoogle Scholar
  53. Geisbert TW, Jahrling PB (2004) Exotic emerging viral diseases: progress and challenges. Nat Med 10:S110–S121Google Scholar
  54. Gonzalez J-P, Camicas JL, Cornet JP et al (1992) Sexual and transovarian transmission of Crimean-Congo haemorrhagic fever in hyalomma truncatum ticks. Res Virol 142:23–28Google Scholar
  55. Gordon SW, Linthicum KJ, Moulton JR (1993) 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 48:576–580PubMedGoogle Scholar
  56. Gozalan A, Esen B, Fitzner J et al (2007) Crimean-Congo haemorrhagic fever cases in Turkey. Scand J Infect Dis 39:332–336PubMedGoogle Scholar
  57. Gul S, Gul EU, Yesilyurt M et al (2012) Health-related quality of life and the prevalence of post-traumatic stress disorder among Crimean-Congo hemorrhagic fever survivors. Jpn J Infect Dis 65:392–395PubMedGoogle Scholar
  58. Guner R, Hasanoglu I, Yapar D et al (2011) A case of Crimean Congo hemorrhagic fever complicated with acalculous cholecystitis and intraabdominal abscess. J Clin Virol 50:162–163PubMedGoogle Scholar
  59. Hassanein KM, El Azazy OM, Yousef HM (1997) Detection of Crimean-Congo haemorrhagic fever virus antibodies in humans and imported livestock in Saudi Arabia. Trans R Soc Trop Med Hyg 91:536–537PubMedGoogle Scholar
  60. Hewson R, Chamberlain J, Mioulet V et al (2004a) Crimean-Congo haemorrhagic fever virus: sequence analysis of the small RNA segments from a collection of viruses worldwide. Virus Res 102:185–189Google Scholar
  61. Hewson R, Gmyl A, Gmyl L et al (2004b) Evidence of segment reassortment in Crimean-Congo haemorrhagic fever virus. J Gen Virol 85:3059–3070Google Scholar
  62. Hoogstraal H (1979) The epidemiology of tick-borne Crimean-Congo hemorrhagic fever in Asia, Europe, and Africa. J Med Entomol 15:307–417PubMedGoogle Scholar
  63. Honig JE, Osborne JC, Nichol ST et al (2004) Crimean-Congo hemorrhagic fever virus genome L RNA segment and encoded protein. Virology 321:29–35PubMedGoogle Scholar
  64. Jones LD, Davies CR, Steele GM et al (1987) A novel mode of arbovirus transmission involving a nonviremic host. Science 237:775–777PubMedGoogle Scholar
  65. Joubert JR, King JB, Rossouw DJ et al (1985) A nosocomial outbreak of Crimean-Congo haemorrhagic fever at Tygerberg Hospital. Part III. Clinical pathology and pathogenesis. S Afr Med J 68:722–728PubMedGoogle Scholar
  66. Karabatsos N (1985) International Catalogue of Arboviruses (including certain other viruses of vertebrates), 3rd edn. San Antonio. (Am Soc Trop Med Hyg)Google Scholar
  67. Karti SS, Odabasi Z, Korten V et al (2004) Crimean-Congo hemorrhagic fever in Turkey. Emerg Infect Dis 10:1379–1384PubMedCentralPubMedGoogle Scholar
  68. Kaya S, Yilmaz G, Ertunç B et al (2012) Parotitis associated with Crimean Congo hemorrhagic fever virus. J Clin Virol 53:159–161PubMedGoogle Scholar
  69. Keshtkar-Jahromi M, Kuhn JH, Christova I et al (2011) Crimean-Congo hemorrhagic fever: current and future prospects of vaccines and therapies. Antiviral Res 90:85–92PubMedGoogle Scholar
  70. Kinsella E, Martin SG, Grolla A et al (2004) Sequence determination of the Crimean-Congo hemorrhagic fever virus L segment. Virology 321:23–28PubMedGoogle Scholar
  71. Kondiah K, Swanepoel R, Paweska JT et al (2010) A simple-probe real-time PCR assay for genotyping reassorted and non-reassorted isolates of Crimean-Congo hemorrhagic fever virus in southern Africa. J Virol Methods 169:34–38PubMedGoogle Scholar
  72. Korolev MB, Donets MA, Rubin SG et al (1976) Morphology and morphogenesis of Crimean hemorrhagic fever virus. Arch Virol 50:169–172PubMedGoogle Scholar
  73. Logan TM, Linthicun KJ, Bailey CL et al (1989) Experimental transmission of Crimean-Congo hemorrhagic fever by Hyalomma truncatum Koch. Am J Trop Med Hyg 40:207–212PubMedGoogle Scholar
  74. Marriott AC, Nuttall PA (1992) Comparison of the S RNA segments and nucleoprotein sequences of Crimean-Congo hemorrhagic fever, Hazara, and Dugbe viruses. Virology 189:795–799PubMedGoogle Scholar
  75. Maltezou HC, Papa A (2010) Crimean-Congo hemorrhagic fever: risk for emergence of new endemic foci in Europe? Travel Med Infect Dis 8:139–143PubMedGoogle Scholar
  76. Maltezou HC, Andonova L, Andraghetti R et al (2010) Crimean-Congo hemorrhagic fever in Europe: current situation calls for preparedness. Euro Surveill 15:19504–19508PubMedGoogle Scholar
  77. Midilli K, Gargili A, Ergonul O et al (2009) The first clinical case due to AP92 like strain of Crimean-Congo hemorrhagic fever virus and a field survey. BMC Infect Dis 9:90PubMedCentralPubMedGoogle Scholar
  78. Mild M, Simon M, Albert J et al (2010) Towards an understanding of the migration of Crimean-Congo hemorrhagic fever virus. J Gen Virol 91:199–207PubMedGoogle Scholar
  79. Mishra AC, Mehta M, Mourya DT et al (2011) Crimean-Congo haemorrhagic fever in India. Lancet 378:372PubMedGoogle Scholar
  80. Morikawa S, Saijo M, Kurane I (2007) Recent progress in molecular biology of Crimean-Congo hemorrhagic fever. Comp Immunol Microbiol Infect Dis 30:375–389PubMedGoogle Scholar
  81. Ozkurt Z, Kiki I, Erol S et al (2006) Crimean-Congo hemorrhagic fever in Eastern Turkey: clinical features, risk factors and efficacy or ribavirin therapy. J Infect 52:207–215PubMedGoogle Scholar
  82. Palomar AM, Portillo A, Santibanez P et al (2013) Crimean-Congo hemorrhagic fever virus in ticks from migratory birds, Morocco. Emerg Infect Dis 19:260–263PubMedCentralPubMedGoogle Scholar
  83. Papa A, Ma B, Kouidou S et al (2002a) Genetic characterization of the M RNA segment of Crimean Congo hemorrhagic fever virus strains, China. Emerg Infect Dis 8:50–53Google Scholar
  84. Papa A, Bino S, Llagami A et al (2002b) Crimean-Congo hemorrhagic fever in Albania, 2001. Eur J Clin Microbiol Infect Dis 21:603–606Google Scholar
  85. Papa A, Bozovi B, Pavlidou V et al (2002c) Genetic detection and isolation of Crimean-Congo hemorrhagic fever virus, Kosovo, Yugoslavia. Emerg Infect Dis 8:852–854Google Scholar
  86. Papa A, Christova I, Papadimitriou E et al (2004) Crimean-Congo hemorrhagic fever in Bulgaria. Emerg Infect Dis 10:1465–1467PubMedCentralPubMedGoogle Scholar
  87. Papa A, Papadimitriou E, Boźović B et al (2005) Genetic characterization of the M RNA segment of a Balkan Crimean-Congo hemorrhagic fever virus strain. J Med Virol 75:466–469PubMedGoogle Scholar
  88. Papa A, Bino S, Velo E et al (2006) Cytokine levels in Crimean-Congo hemorrhagic fever. J Clin Virol 36:272–276PubMedGoogle Scholar
  89. Papa A, Drosten C, Bino S et al (2007) Viral load and Crimean-Congo hemorrhagic fever. Emerg Infect Dis 13:805–806PubMedCentralPubMedGoogle Scholar
  90. Papa A, Maltezou HC, Tsiodras S et al (2008). A case of Crimean-Congo haemorrhagic fever in Greece, June 2008. Euro Surveill 13:13–14Google Scholar
  91. Papa A, Papadimitriou E, Christova I (2011). The Bulgarian vaccine Crimean-Congo haemorrhagic fever virus strain. Scand J Infect Dis 43:225–229PubMedGoogle Scholar
  92. Randolph SE, Rogers DJ (2007) Ecology of tick-borne disease and the role of climate. In: Ergonul O, Whitehouse CA (eds) Crimean-Congo haemorrhagic fever. A global perspective. Springer, Dordrecht, pp 167–186Google Scholar
  93. Rodriguez LL, Maupin GO, Ksiazek TG et al (1997) Molecular investigation of a multisource outbreak of Crimean-Congo hemorrhagic fever in the United Arab Emirates. Am J Trop Med Hyg 57:512–518PubMedGoogle Scholar
  94. Saijo M, Tang Q, Shimayi B et al (2005a) Antigen-capture enzyme-linked immunosorbent assay for the diagnosis of Crimean-Congo hemorrhagic fever using a novel monoclonal antibody. J Med Virol 77:83–88Google Scholar
  95. Saijo M, Tang Q, Shimayi B et al (2005b) Recombinant nucleoprotein-based serological diagnosis of Crimean-Congo hemorrhagic fever virus infections. J Med Virol 75:295–299Google Scholar
  96. Saksida A, Duh D, Wraber B et al (2010) Interacting roles of immune mechanisms and viral load in the pathogenesis of Crimean-Congo hemorrhagic fever. Clin Vaccine Immunol 17:1086–1093PubMedCentralPubMedGoogle Scholar
  97. Saluzzo JF, Digoutte JP, Cornet M et al (1984) Isolation of Crimean-Congo haemorrhagic fever and Rift Valley fever viruses in Upper Volta. Lancet 1:1179PubMedGoogle Scholar
  98. Saluzzo JF, Aubry P, McCormick J et al (1985) Haemorrhagic fever caused by Crimean Congo haemorrhagic fever virus in Mauritania. Trans R Soc Trop Med Hyg 79:268PubMedGoogle Scholar
  99. Samudzi RR, Leman PA, Paweska JT et al (2012). Bacterial expression of Crimean-Congo hemorrhagic fever virus nucleoprotein and its evaluation as a diagnostic reagent in an indirect ELISA. J Virol Methods 179:70–76PubMedGoogle Scholar
  100. Sanchez AJ, Vincent MJ, Nichol ST (2002) Characterization of the glycoproteins of Crimean-Congo hemorrhagic fever virus. J Virol 76:7263–7275PubMedCentralPubMedGoogle Scholar
  101. Sanchez AJ, Vincent MJ, Ericksen BR et al (2006) Crimean-Congo hemorrhagic fever virus glycoprotein precursor is cleaved by Furin-like and SKI-1 proteases to generate a novel 38-kilodalton glycoprotein. J Virol 80:514–525PubMedCentralPubMedGoogle Scholar
  102. Şensoy G, Çaltepe Dinler G, Kalkan G et al (2011) Crimean-Congo haemorrhagic fever: peritoneal and pleural effusion. Ann Trop Paediatr 31:169–172PubMedGoogle Scholar
  103. Schmaljohn CS, Patterson JL (1990) Bunyaviridae and their replication. Part II: replication of Bunyaviridae. In: Fields BN (ed) Virology, 2nd edn. Raven Press Ltd, New YorkGoogle Scholar
  104. Schwarz TF, Nitschko H, Jager G et al (1995) Crimean-Congo haemorrhagic fever in Oman. Lancet 346:1230PubMedGoogle Scholar
  105. Seregin SV, Samokhvalov EI, Petrova ID et al (2004) Genetic characterization of the M RNA segment of Crimean-Congo hemorrhagic fever virus strains isolated in Russia and Tajikistan. Virus Genes 28:187–193PubMedGoogle Scholar
  106. Shepherd AJ, Swanepoel R, Leman PA et al (1986) Comparison of methods for isolation and titration of Crimean-Congo hemorrhagic fever virus. J Clin Microbiol 24:654–656PubMedCentralPubMedGoogle Scholar
  107. Shepherd AJ, Swanepoel R, Leman PA et al (1987) Field and laboratory investigation of Crimean-Congo haemorrhagic fever virus (Nairovirus, family Bunyaviridae) infection in birds. Trans R Soc Trop Med Hyg 81:1004–1007PubMedGoogle Scholar
  108. Shepherd AJ, Swanepoel R, Gill DE (1988) Evaluation of enzyme-linked immunosorbent assay and reversed passive hemagglutination for detection of Crimean-Congo hemorrhagic fever virus antigen. J Clin Microbiol 26:347–353PubMedCentralPubMedGoogle Scholar
  109. Shepherd AJ, Leman PA, Swanepoel R (1989a) Viremia and antibody response of small Africa and laboratory mammals to Crimean-Congo hemorrhagic fever virus infection. Am J Trop Med Hyg 40:541–547Google Scholar
  110. Shepherd AJ, Swanepoel R, Leman PA (1989b) Antibody response in Crimean-Congo hemorrhagic fever. Rev Infect Dis 11:S801–S806Google Scholar
  111. Shepherd AJ, Swanepoel R, Shepherd SP et al (1991) Viraemic transmission of Crimean-Congo haemorrhagic fever virus to ticks. Epidemiol Infect 106:373–382PubMedCentralPubMedGoogle Scholar
  112. Simpson DI, Knight EM, Courtois GH et al (1967) Congo virus: a hitherto undescribed virus occurring in Africa. Part 1-Human isolations-clinical notes. East Afr Med J 44:86–92Google Scholar
  113. Smirnova SE (1979) A comparative study of the Crimean hemorrhagic fever-Congo group of viruses Arch Virol 62:137–143PubMedGoogle Scholar
  114. Soares-Weiser K, Thomas S, Thomson G et al (2010) Ribavirin for Crimean-Congo hemorrhagic fever: systematic review and meta-analysis. BMC Infect Dis 10:207PubMedCentralPubMedGoogle Scholar
  115. Spik K, Shurtleff A, McElroy AK et al (2006) Immunogenicity of combination DNA vaccines for Rift Valley fever virus, tick-borne encephalitis virus, Hantaan virus and Crimean-Congo hemorrhagic virus. Vaccine 24:4657–4666PubMedGoogle Scholar
  116. Suleiman MN, Muscat-Baron JM, Harries JR et al (1980) Congo/Crimean haemorrhagic fever in Dubai. An outbreak at the Rashid Hospital. Lancet 2:939–941PubMedGoogle Scholar
  117. Swanepoel R, Shepherd AJ, Leman PA et al (1987) Epidemiologic and clinical features of Crimean-Congo hemorrhagic fever in southern Africa. Am J Trop Med Hyg 36:120–132PubMedGoogle Scholar
  118. Swanepoel R, Gill DE, Shepherd AJ et al (1989) The clinical pathology of Crimean-Congo hemorrhagic fever. Rev Infect Dis 11:S794–800Google Scholar
  119. Swanepoel R, Leman PA, Burt FJ et al (1998) Experimental infection of ostriches with Crimean-Congo haemorrhagic fever virus. Epidemiol Infect 121:427–432PubMedCentralPubMedGoogle Scholar
  120. Tang Q, Saijo M, Zhang Y et al (2003) A patient with Crimean-Congo hemorrhagic fever serologically diagnosed by recombinant nucleoprotein-based antibody detection systems. Clin Diagn Lab Immunol 10:489–491PubMedCentralPubMedGoogle Scholar
  121. Tantawi HH, Al-Moslih MI, Al-Janabi NY et al (1980) Crimean-Congo haemorrhagic fever virus in Iraq: isolation, identification and electron microscopy. Acta Virol 24:464–467PubMedGoogle Scholar
  122. Tezer H, Sucakli IA, Sayli TR et al (2010) Crimean-Congo hemorrhagic fever in children. J Clin Virol 48:184–186PubMedGoogle Scholar
  123. Tonbak S, Aktas M, Altay K et al (2006) Crimean-congo hemorrhagic fever virus: genetic analysis and tick survey in Turkey. J Clin Microbiol 44:4120–4124PubMedCentralPubMedGoogle Scholar
  124. van Eeden PJ, Joubert JR, van de Wal BW et al (1985) A nosocomial outbreak of Crimean-Congo haemorrhagic fever at Tygerberg Hospital. Part I. Clinical features. S Afr Med J 68:711–717PubMedGoogle Scholar
  125. Watts DM, Ksiazek TG, Linthicum KJ et al (1989) Crimean-Congo haemorrhagic fever. In: Monath TP (ed) The arboviruses: epidemiology and ecology, vol  II. CRC Press, Inc, Boca Raton.Google Scholar
  126. Wilson ML, Gonzalez J-P, Cornet JP et al (1991) Transmission of Crimean-Congo haemorrhagic fever virus from experimentally infected sheep to Hyalomma truncatum ticks Res Virol 142:395–404PubMedGoogle Scholar
  127. Wolfel R, Paweska JT, Petersen N et al (2007) Virus detection and monitoring of viral load in Crimean-Congo hemorrhagic fever virus patients. Emerg Infect Dis 13:1097–1100PubMedCentralPubMedGoogle Scholar
  128. Wolfel R, Paweska JT, Petersen N et al (2009) Low-density macroarray for rapid detection and identification of Crimean-Congo hemorrhagic fever virus. J Clin Microbiol 47:1025–1030PubMedCentralPubMedGoogle Scholar
  129. Yapar M, Aydogan H, Pahsa A et al (2005) Rapid and quantitative detection of Crimean-Congo hemorrhagic fever virus by one-step real-time reverse transcriptase-PCR. Jpn J Infect Dis 58:358–362PubMedGoogle Scholar
  130. Yashina L, Petrova I, Seregin S (2003) Genetic variability of Crimean-Congo haemorrhagic fever virus in Russia and central Asia. J Gen Virol 84:1199–1206PubMedGoogle Scholar

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© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  1. 1.National Health Laboratory ServicesUniversity of the Free StateBloemfonteinSouth Africa

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