Skip to main content
Log in

Molecular detection of Crimean-Congo hemorrhagic fever virus in ticks, Greece, 2012–2014

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Crimean-Congo hemorrhagic fever virus (CCHFV) is transmitted to humans mainly through the bite of infected ticks. In Greece, only one clinical case has been observed, in 2008, but the seroprevalence in humans is relatively high (4.2%). To have a first insight into the circulation of CCHFV in Greece, 2000 ticks collected from livestock during 2012–2014 were tested. CCHFV was detected in 36 of the 1290 (2.8%) tick pools (1–5 ticks per pool). Two genetic lineages were identified: Europe 1 and Europe 2. Most Europe 1 sequences were obtained from Rhipicephalus sanguineus sensu lato ticks, while most Europe 2 sequences were recovered from Rhipicephalus bursa ticks. The number of collected Hyalomma marginatum ticks (the principal vector of CCHFV) was low (0.5% of ticks) and all were CCHFV negative. Since it is not known how efficient ticks of the Rhipicephalus genus are as vectors of the virus, laboratory studies will be required to explore the role of Rhipicephalus spp. ticks in CCHFV maintenance and transmission.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Antoniadis A, Casals J (1982) Serological evidence of human infection with Congo-Crimean hemorrhagic fever virus in Greece. Am J Trop Med Hyg 31:1066–1067

    Article  CAS  PubMed  Google Scholar 

  • Bente DA, Forrester NL, Watts DM, McAuley AJ, Whitehouse CA, Bray M (2013) Crimean-Congo hemorrhagic fever: history, epidemiology, pathogenesis, clinical syndrome and genetic diversity. Antivir Res 100:159–189

    Article  CAS  PubMed  Google Scholar 

  • Elevli M, Ozkul AA, Civilibal M, Midilli K, Gargili A, Duru NS (2009) A newly identified Crimean-Congo hemorrhagic fever virus strain in Turkey. Int J Infect Dis 14(Suppl 3):e213–e216

    PubMed  Google Scholar 

  • Estrada-Peña A, Bouattour A, Camicas JL, Walker AR (2004) Ticks of domestic animals in the Mediterranean region. A Guide to Identification of Species. University of Zaragoza Press, Zaragoza

  • Gargili A, Estrada-Pena A, Spengler JR, Lukashev A, Nuttall PA, Bente DA (2017) The role of ticks in the maintenance and transmission of Crimean-Congo hemorrhagic fever virus: a review of published field and laboratory studies. Antivir Res 144:93–119

    Article  CAS  PubMed  Google Scholar 

  • Honig JE, Osborne JC, Nichol ST (2004) The high genetic variation of viruses of the genus Nairovirus reflects the diversity of their predominant tick hosts. Virology 318:10–16

    Article  CAS  PubMed  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    Article  CAS  PubMed  Google Scholar 

  • Midilli K, Gargili A, Ergonul O, Elevli M, Ergin S, Turan N, Sengoz G, Ozturk R, Bakar M (2009) The first clinical case due to AP92 like strain of Crimean-Congo hemorrhagic fever virus and a field survey. BMC Infect Dis 9:90

    Article  PubMed  PubMed Central  Google Scholar 

  • OIE Crimean-Congo Haemorrhagic Fever OIE Terrestrial Manual 2014

    Google Scholar 

  • Ozkaya E, Dincer E, Carhan A, Uyar Y, Ertek M, Whitehouse CA, Ozkul A (2010) Molecular epidemiology of Crimean-Congo hemorrhagic fever virus in Turkey: occurrence of local topotype. Virus Res 149:64–70

    Article  CAS  PubMed  Google Scholar 

  • Panayotova E, Papa A, Trifonova I, Christova I (2016) Crimean-Congo hemorrhagic fever virus lineages Europe 1 and Europe 2 in Bulgarian ticks. Ticks Tick Borne Dis 7:1024–1028

    Article  PubMed  Google Scholar 

  • Papa A, Maltezou HC, Tsiodras S, Dalla VG, Papadimitriou T, Pierroutsakos I, Kartalis GN, Antoniadis A (2008) A case of Crimean-Congo haemorrhagic fever in Greece, June 2008. Euro Surveill 13

  • Papa A, Sidira P, Kallia S, Ntouska M, Zotos N, Doumbali E, Maltezou H, Demiris N, Tsatsaris A (2013) Factors associated with IgG positivity to Crimean-Congo hemorrhagic fever virus in the area with the highest seroprevalence in Greece. Ticks Tick Borne Dis 4:417–420

    Article  PubMed  Google Scholar 

  • Papa A, Chaligiannis I, Kontana N, Sourba T, Tsioka K, Tsatsaris A, Sotiraki S (2014) A novel AP92-like Crimean-Congo hemorrhagic fever virus strain, Greece. Ticks Tick Borne Dis 5:590–593

    Article  PubMed  Google Scholar 

  • Papa A, Mirazimi A, Koksal I, Estrada-Pena A, Feldmann H (2015) Recent advances in research on Crimean-Congo hemorrhagic fever. J Clin Virol 64:137–143

    Article  PubMed  Google Scholar 

  • Papa A, Sidira P, Tsatsaris A (2016) Spatial cluster analysis of Crimean-Congo hemorrhagic fever virus seroprevalence in humans, Greece. Parasit Epidemiol Control 1:211–218

    Article  Google Scholar 

  • Papadopoulos O, Koptopoulos G (1978) Isolation of Crimean-Congo hemorrhagic fever (C-CHF) virus from Rhipicephalus bursa ticks in Greece. Acta Hell Microbiol 23:20–28

    Google Scholar 

  • Reeves WC (1957) Arthropods as vectors and reservoirs of animal pathogenic viruses. In: Hallauer C, Meyer KF (eds) Handbuch der Virusforschung. Springer-Verlag, Vienna, pp 177–202

    Google Scholar 

  • Rodriguez LL, Maupin GO, Ksiazek TG, Rollin PE, Khan AS, Schwarz TF, Lofts RS, Smith JF, Noor AM, Peters CJ, Nichol ST (1997) Molecular investigation of a multisource outbreak of Crimean-Congo hemorrhagic fever in the United Arab Emirates. Am J Trop Med Hyg 57:512–518

    Article  CAS  PubMed  Google Scholar 

  • Salehi-Vaziri M, Baniasadi V, Jalali T, Mirghiasi SM, Azad-Manjiri S, Zarandi R, Mohammadi T, Khakifirouz S, Fazlalipour M (2016) The first fatal case of Crimean-Congo hemorrhagic fever caused by the AP92-like strain of the Crimean-Congo hemorrhagic fever virus. Jpn J Infect Dis 69:344–346

    Article  CAS  PubMed  Google Scholar 

  • Schuster I, Mertens M, Mrenoshki S, Staubach C, Mertens C, Bruning F, Wernike K, Hechinger S, Berxholi K, Mitrov D, Groschup MH (2016) Sheep and goats as indicator animals for the circulation of CCHFV in the environment. Exp Appl Acarol 68:337–346

    Article  PubMed  Google Scholar 

  • Shepherd AJ, Swanepoel R, Shepherd SP, Leman PA, Mathee O (1991) Viraemic transmission of Crimean-Congo haemorrhagic fever virus to ticks. Epidemiol Infect 106:373–382

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sherifi K, Cadar D, Muji S, Robaj A, Ahmeti S, Jakupi X, Emmerich P, Kruger A (2014) Crimean-Congo hemorrhagic fever virus clades V and VI (Europe 1 and 2) in ticks in Kosovo, 2012. PLoS Negl Trop Dis 8:e3168

    Article  PubMed  PubMed Central  Google Scholar 

  • Sidira P, Maltezou HC, Haidich AB, Papa A (2012) Seroepidemiological study of Crimean-Congo haemorrhagic fever in Greece, 2009-2010. Clin Microbiol Infect 18:E16–E19

    Article  CAS  PubMed  Google Scholar 

  • Tekin S, Bursali A, Mutluay N, Keskin A, Dundar E (2011) Crimean-Congo hemorrhagic fever virus in various ixodid tick species from a highly endemic area. Vet Parasitol 186:546–552

    Article  PubMed  Google Scholar 

  • Tonbak S, Aktas M, Altay K, Azkur AK, Kalkan A, Bolat Y, Dumanli N, Ozdarendeli A (2006) Crimean-Congo hemorrhagic fever virus: genetic analysis and tick survey in Turkey. J Clin Microbiol 44:4120–4124

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Turell MJ (2007) Role of ticks in the transmission of Crimean-Congo Hemorrhagic fever virus. In: Ergonul O, Whitehouse CA (eds) Crimean-Congo Hemorrhagic Fever. Springer, Dordrecht, pp 143–154

  • Wolfel R, Paweska JT, Petersen N, Grobbelaar AA, Leman PA, Hewson R, Georges-Courbot MC, Papa A, Gunther S, Drosten C (2007) Virus detection and monitoring of viral load in Crimean-Congo hemorrhagic fever virus patients. Emerg Infect Dis 13:1097–1100

    Article  PubMed  PubMed Central  Google Scholar 

  • World Health Organization (2013) Crimean-Congo Haemorrhagic Fever. Fact sheet No. 208 - January 2013. http://www.who.int/mediacentre/factsheets/fs208/en/

Download references

Acknowledgements

The work was supported by ANTIGONE and COMPARE EU projects (grant agreement numbers 278976 and 643476, respectively).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Anna Papa.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Papa, A., Kontana, A., Tsioka, K. et al. Molecular detection of Crimean-Congo hemorrhagic fever virus in ticks, Greece, 2012–2014. Parasitol Res 116, 3057–3063 (2017). https://doi.org/10.1007/s00436-017-5616-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-017-5616-6

Keywords

Navigation