Volume 29, Number 2—February 2023
CME ACTIVITY - Synopsis
Crimean-Congo Hemorrhagic Fever, Spain, 2013–2021
Figure 1

Figure 1. Locations of CCHF cases (A) and phylogenetic tree of CCHFV (B) in Spain, 2013–2021. Dots on the map indicate patients with a CCHF diagnosis in Spain: black dots indicate cases from this study, and colored dots indicate cases previously described. Two cases (patients 8 and 10) were not sequenced. The phylogenetic tree was constructed by the neighbor-joining method based on sequences of the small segment of the virus. The numbers on the right indicate bootstrap values for the groups; values <75 are not shown. Other sequences are listed by GenBank accession number, strain, geographic origin, and sampling year. Genotypes are indicated by Roman numerals according to Carroll et al. (14) with the equivalent clade nomenclature according to Chamberlain et al. (15) in brackets; I, West Africa (Africa 1); III, South and West Africa (Africa 3); IV, Middle East/Asia, divided into 2 groups (Asia 1/Asia 2); V, Europe/Turkey (Europe 1); VI, Greece (Europe 2). New lineage, Africa 4 described by Negredo et al. (12). CCHF, Crimean-Congo hemorrhagic fever; CCHFV, CCHF virus.
References
- Ballinger MJ, Medeiros AS, Qin J, Taylor DJ. Unexpected differences in the population genetics of phasmavirids (Bunyavirales) from subarctic ponds. Virus Evol. 2017;3:
vex015 . DOIPubMedGoogle Scholar - Dai S, Deng F, Wang H, Ning Y. Crimean-Congo hemorrhagic fever virus: current advances and future prospects of antiviral strategies. Viruses. 2021;13:1195. DOIPubMedGoogle Scholar
- Çevik MA, Erbay A, Bodur H, Gülderen E, Baştuğ A, Kubar A, et al. Clinical and laboratory features of Crimean-Congo hemorrhagic fever: predictors of fatality. Int J Infect Dis. 2008;12:374–9. DOIPubMedGoogle Scholar
- Bodur H, Akinci E, Ascioglu S, Öngürü P, Uyar Y. Subclinical infections with Crimean-Congo hemorrhagic fever virus, Turkey. Emerg Infect Dis. 2012;18:640–2. DOIPubMedGoogle Scholar
- Mostafavi E, Pourhossein B, Chinikar S. Clinical symptoms and laboratory findings supporting early diagnosis of Crimean-Congo hemorrhagic fever in Iran. J Med Virol. 2014;86:1188–92. DOIPubMedGoogle Scholar
- 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. DOIPubMedGoogle Scholar
- Spengler JR, Bente DA. Crimean-Congo hemorrhagic fever in Spain—new arrival or silent resident? N Engl J Med. 2017;377:106–8. DOIPubMedGoogle Scholar
- Estrada-Peña A, de la Fuente J. The ecology of ticks and epidemiology of tick-borne viral diseases. Antiviral Res. 2014;108:104–28. DOIPubMedGoogle Scholar
- Monsalve-Arteaga L, Alonso-Sardón M, Muñoz Bellido JL, Vicente Santiago MB, Vieira Lista MC, López Abán J, et al. Seroprevalence of Crimean-Congo hemorrhagic fever in humans in the World Health Organization European region: A systematic review. PLoS Negl Trop Dis. 2020;14:
e0008094 . DOIPubMedGoogle Scholar - Negredo A, de la Calle-Prieto F, Palencia-Herrejón E, Mora-Rillo M, Astray-Mochales J, Sánchez-Seco MP, et al.; Crimean Congo Hemorrhagic Fever@Madrid Working Group. Autochthonous Crimean-Congo Hemorrhagic Fever in Spain. N Engl J Med. 2017;377:154–61. DOIPubMedGoogle Scholar
- Negredo A, Sánchez-Ledesma M, Llorente F, Pérez-Olmeda M, Belhassen-García M, González-Calle D, et al. Retrospective identification of early autochthonous case of Crimean-Congo hemorrhagic fever, Spain, 2013. Emerg Infect Dis. 2021;27:1754–6. DOIPubMedGoogle Scholar
- Negredo A, Sánchez-Arroyo R, Díez-Fuertes F, de Ory F, Budiño MA, Vázquez A, et al. Fatal case of Crimean-Congo hemorrhagic fever caused by reassortant virus, Spain, 2018. Emerg Infect Dis. 2021;27:1211–5. DOIPubMedGoogle Scholar
- Monsalve Arteaga L, Muñoz Bellido JL, Negredo AI, García Criado J, Vieira Lista MC, Sánchez Serrano JÁ, et al. New circulation of genotype V of Crimean-Congo haemorrhagic fever virus in humans from Spain. PLoS Negl Trop Dis. 2021;15:
e0009197 . DOIPubMedGoogle Scholar - Carroll SA, Bird BH, Rollin PE, Nichol ST. Ancient common ancestry of Crimean-Congo hemorrhagic fever virus. Mol Phylogenet Evol. 2010;55:1103–10. DOIPubMedGoogle Scholar
- Chamberlain J, Cook N, Lloyd G, Mioulet V, Tolley H, Hewson R. Co-evolutionary patterns of variation in small and large RNA segments of Crimean-Congo hemorrhagic fever virus. J Gen Virol. 2005;86:3337–41. DOIPubMedGoogle Scholar
- Bakır M, Gözel MG, Köksal I, Aşık Z, Günal Ö, Yılmaz H, et al. Validation of a severity grading score (SGS) system for predicting the course of disease and mortality in patients with Crimean-Congo hemorrhagic fever (CCHF). Eur J Clin Microbiol Infect Dis. 2015;34:325–30. DOIPubMedGoogle Scholar
- Estrada-Peña A, Palomar AM, Santibáñez P, Sánchez N, Habela MA, Portillo A, et al. Crimean-Congo hemorrhagic fever virus in ticks, Southwestern Europe, 2010. Emerg Infect Dis. 2012;18:179–80. DOIPubMedGoogle Scholar
- Monsalve Arteaga L, Muñoz Bellido JL, Vieira Lista MC, Vicente Santiago MB, Fernández Soto P, Bas I, et al. Crimean-Congo haemorrhagic fever (CCHF) virus-specific antibody detection in blood donors, Castile-León, Spain, summer 2017 and 2018. Euro Surveill. 2020;25:
1900507 . DOIPubMedGoogle Scholar - Moraga-Fernández A, Ruiz-Fons F, Habela MA, Royo-Hernández L, Calero-Bernal R, Gortazar C, et al. Detection of new Crimean-Congo haemorrhagic fever virus genotypes in ticks feeding on deer and wild boar, Spain. Transbound Emerg Dis. 2021;68:993–1000. DOIPubMedGoogle Scholar
- Espunyes J, Cabezón O, Pailler-García L, Dias-Alves A, Lobato-Bailón L, Marco I, et al. Hotspot of Crimean-Congo hemorrhagic fever virus seropositivity in wildlife, northeastern Spain. Emerg Infect Dis. 2021;27:2480–4. DOIPubMedGoogle Scholar
- Sánchez-Seco MP, Sierra MJ, Estrada-Peña A, Valcárcel F, Molina R, de Arellano ER, et al.; Group for CCHFv Research. Widespread detection of multiple strains of Crimean-Congo hemorrhagic fever virus in ticks, Spain. Emerg Infect Dis. 2021;28:394–402. DOIPubMedGoogle Scholar
- Negredo A, Habela MÁ, Ramírez de Arellano E, Diez F, Lasala F, López P, et al. Survey of Crimean-Congo hemorrhagic fever enzootic focus, Spain, 2011–2015. Emerg Infect Dis. 2019;25:1177–84. DOIPubMedGoogle Scholar
- Papa A, Sidira P, Larichev V, Gavrilova L, Kuzmina K, Mousavi-Jazi M, et al. Crimean-Congo hemorrhagic fever virus, Greece. Emerg Infect Dis. 2014;20:288–90. DOIPubMedGoogle Scholar
- Ahmeti S, Berisha L, Halili B, Ahmeti F, von Possel R, Thomé-Bolduan C, et al. Crimean-Congo hemorrhagic fever, Kosovo, 2013–2016. Emerg Infect Dis. 2019;25:321–4. DOIPubMedGoogle Scholar
- Yilmaz GR, Buzgan T, Irmak H, Safran A, Uzun R, Cevik MA, et al. The epidemiology of Crimean-Congo hemorrhagic fever in Turkey, 2002-2007. Int J Infect Dis. 2009;13:380–6. DOIPubMedGoogle Scholar
- Aker S, Akıncı H, Kılıçoğlu C, Leblebicioglu H. The geographic distribution of cases of Crimean-Congo hemorrhagic fever: Kastamonu, Turkey. Ticks Tick Borne Dis. 2015;6:730–6. DOIPubMedGoogle Scholar
- Henter JI, Horne A, Aricó M, Egeler RM, Filipovich AH, Imashuku S, et al. HLH-2004: Diagnostic and therapeutic guidelines for hemophagocytic lymphohistiocytosis. Pediatr Blood Cancer. 2007;48:124–31. DOIPubMedGoogle Scholar
- Tasdelen Fisgin N, Fisgin T, Tanyel E, Doganci L, Tulek N, Guler N, et al. Crimean-Congo hemorrhagic fever: five patients with hemophagocytic syndrome. Am J Hematol. 2008;83:73–6. DOIPubMedGoogle Scholar
- Johnson S, Henschke N, Maayan N, Mills I, Buckley BS, Kakourou A, et al. Ribavirin for treating Crimean Congo haemorrhagic fever. Cochrane Database Syst Rev. 2018;6:
CD012713 . DOIPubMedGoogle Scholar - Palomar AM, Portillo A, Santibáñez P, Mazuelas D, Arizaga J, Crespo A, et al. Crimean-Congo hemorrhagic fever virus in ticks from migratory birds, Morocco. Emerg Infect Dis. 2013;19:260–3. DOIPubMedGoogle Scholar
1These authors contributed equally to this article.