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Crimean-Congo hemorrhagic fever virus circulating among sheep of Portugal: a nationwide serosurvey assessment

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Abstract

Crimean-Congo hemorrhagic fever virus (CCHFV) is a widespread zoonotic pathogen that can cause mild to severe hemorrhagic disease in humans. CCHFV may be transmitted through direct contact with tissue or blood of viremic animals; however, the primary transmission route is through infected tick bites. CCHFV RNA has been detected in ticks feeding on domestic and wild animals in western Spain, suggesting an established circulation of CCHFV in Western Europe. Ruminants have been recognized as important CCHFV reservoirs and have been linked to human cases in endemic regions. Given the emergence of CCHF in neighboring Spain, and a report of two CCHFV seropositive humans in southern Portugal in 1985, we investigated the potential circulation of this virus in the country by performing a nationwide anti-CCHFV IgG serosurvey in sentinel sheep of Portugal. Sera (n = 459) randomly selected from widely distributed farms (n = 20) of Portugal were tested using a commercial double-antigen enzyme-linked immunosorbent assay, yielding an overall seroprevalence of 0.4% (95% confidence interval [CI] 0.04–1.56%). Positive sheep were from the southern region of Portugal (Alentejo region), which raise the seroprevalence of this region to 0.74% (95% CI 0.09–2.66%). This is the first study reporting the presence of CCHFV antibodies in sheep of Portugal, thus suggesting a geographical expansion of CCHFV to this country. It seems likely that CCHFV may exist focally in southern Portugal.

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Fig. 1

Data availability

Raw data were generated at Virology Lab of Faculty of Pharmacy of the University of Porto. Derived data supporting the findings of this study are available from the corresponding author [PB] on request.

Code availability

Not applicable.

References

  • Abramson, J.H., 2011. WINPEPI updated: computer programs for epidemiologists, and their teaching potential. Epidemiologic Perspectives and Innovations 8, 1.

    Article  Google Scholar 

  • Barthel, R., Mohareb, E., Younan, R., Gladnishka, T., Kalvatchev, N., Moemen, A., Mansour, S.S., Rossi, C., Schoepp, R., and Christova, I., 2014. Seroprevalance of Crimean-Congo haemorrhagic fever in Bulgarian livestock. Biotechnology, Biotechnological Equipment 28, 540-542.

    Article  Google Scholar 

  • Christova, I., Panayotova, E., Groschup, M.H., Trifonova, I., Tchakarova, S., and Sas, M.A., 2018. High seroprevalence for Crimean-Congo haemorrhagic fever virus in ruminants in the absence of reported human cases in many regions of Bulgaria. Experimental & Applied Acarology 75, 227-234.

    Article  CAS  Google Scholar 

  • Esteves, F., Mesquita, J.R., Vala, H., Abreu-Silva, J., van der Poel, W.H., and Nascimento, M.S., 2016. Serological Evidence for Schmallenberg Virus Infection in Sheep of Portugal, 2014. Vector Borne and Zoonotic Diseases 16, 63-65.

    Article  Google Scholar 

  • Estrada-Peña, A., Palomar, A.M., Santibáñez, P., Sánchez, N., Habela, M.A., Portillo, A., Romero, L., and Oteo, J.A., 2012. Crimean-Congo hemorrhagic fever virus in ticks, Southwestern Europe, 2010. Emerging Infectious Diseases 18, 179-180.

    Article  Google Scholar 

  • Garrison, A.R., Alkhovsky , S.V., Avšič-Županc, T., Bente, D.A., Bergeron, É., Burt, F., Di Paola, N., Ergünay, K., Hewson, R., Kuhn, J.H., Mirazimi, A., Papa , A., Sall, A.A., Spengler, J.R., Palacios, G., and Consortium, I.R., 2020. ICTV Virus Taxonomy Profile: Nairoviridae. Journal of General Virology 101, 798-799.

    Article  CAS  Google Scholar 

  • Pfeiffer D.U., 2002. Veterinary Epidemiology: An Introduction. (Wiley-Blackwell; Oxford, UK).

  • Grech-Angelini, S., Lancelot, R., Ferraris, O., Peyrefitte, C.N., Vachiery, N., Pédarrieu, A., Peyraud, A., Rodrigues, V., Bastron, D., Libeau, G., Fernandez, B., Holzmuller, P., Servan de Almeida, R., Michaud, V., Tordo, N., Comtet, L., Métras, R., Casabianca, F., and Vial, L., 2020. Crimean-Congo Hemorrhagic Fever Virus Antibodies among Livestock on Corsica, France, 2014-2016. Emerging Infectious Diseases 26, 1041-1044.

    Article  CAS  Google Scholar 

  • Hawman, D.W., and Feldmann, H., 2018. Recent advances in understanding Crimean-Congo hemorrhagic fever virus. F1000Research 7, F1000 Faculty Rev-1715.

  • Humolli, I., Dedushaj, I., Zupanac, T.A., and Muçaj, S., 2010. Epidemiological, serological and herd immunity of Crimean-Congo haemorrhagic fever in Kosovo. Medical Arhives 64, 91-93.

    Google Scholar 

  • IFAP, Instituto Financiamento da Agricultura e Pescas 2013. Available at www.ifap.min-agricultura.pt/portal/page/portal/F73E9028F8EB5096E043C0A8C8C55096.

  • Kadriaj, P., Kota, M., Velo, E., Mersini, K., Simaku, A., Berxholi, K., and Bino, S., 2018. Seroepidemiology of CCHF in Domestic Animals in Endemic Areas in Albania. Academic Journal of Interdisciplinary Studies 7, 25-29.

    Article  Google Scholar 

  • Kasi, K.K., Sas, M.A., Sauter-Louis, C., von Arnim, F., Gethmann, J.M., Schulz, A., Wernike, K., Groschup, M.H., and Conraths, F.J., 2020. Epidemiological investigations of Crimean-Congo haemorrhagic fever virus infection in sheep and goats in Balochistan, Pakistan. Ticks and Tick-borne Diseases 11, 101324.

    Article  Google Scholar 

  • Mertens, M., Schuster, I., Sas, M.A., Vatansever, Z., Hubalek, Z., Güven, E., Deniz, A., Georgiev, G., Peshev, R., and Groschup, M.H., 2016. Crimean-Congo Hemorrhagic Fever Virus in Bulgaria and Turkey. Vector Borne and Zoonotic Diseases 16, 619-623.

    Article  Google Scholar 

  • Mustafa, M.L., Ayazi, E., Mohareb, E., Yingst, S., Zayed, A., Rossi, C.A., Schoepp, R.J., Mofleh, J., Fiekert, K., Akhbarian, Z., Sadat, H., and Leslie, T., 2011. Crimean-Congo hemorrhagic fever, Afghanistan, 2009. Emerging Infectious Diseases 17, 1940-1941.

    Article  Google Scholar 

  • Nabeth, P., Cheikh, D.O., Lo, B., Faye, O., Vall, I.O.M., Niang, M., Wague, B., Diop, D., Diallo, M., Diallo, B., Diop, O.M., and Simon, F., 2004. Crimean-Congo hemorrhagic fever, Mauritania. Emerging Infectious Diseases 10, 2143-2149.

    Article  Google Scholar 

  • Negredo, A., de la Calle-Prieto, F., Palencia-Herrejón, E., Mora-Rillo, M., Astray-Mochales, J., Sánchez-Seco, M.P., Bermejo Lopez, E., Menárguez, J., Fernández-Cruz, A., Sánchez-Artola, B., Keough-Delgado, E., Ramírez de Arellano, E., Lasala, F., Milla, J., Fraile, J.L., Ordobás Gavín, M., Martinez de la Gándara, A., López Perez, L., Diaz-Diaz, D., López-García, M.A., Delgado-Jimenez, P., Martín-Quirós, A., Trigo, E., Figueira, J.C., Manzanares, J., Rodriguez-Baena, E., Garcia-Comas, L., Rodríguez-Fraga, O., García-Arenzana, N., Fernández-Díaz, M.V., Cornejo, V.M., Emmerich, P., Schmidt-Chanasit, J., and Arribas, J.R., 2017. Autochthonous Crimean-Congo Hemorrhagic Fever in Spain. New England Journal of Medicine 377, 154-161.

    Article  Google Scholar 

  • Negredo, A., Habela, M.Á., Ramírez de Arellano, E., Diez, F., Lasala, F., López, P., Sarriá, A., Labiod, N., Calero-Bernal, R., Arenas, M., Tenorio, A., Estrada-Peña, A., and Sánchez-Seco, M.P., 2019. Survey of Crimean-Congo Hemorrhagic Fever Enzootic Focus, Spain, 2011–2015. Emerging Infectious Disease Journal 25, 1177.

    Article  Google Scholar 

  • Ozan, E., and Ozkul, A., 2020. Investigation of Crimean-Congo hemorrhagic fever virus in ruminant species slaughtered in several endemic provinces in Turkey. Archives of Virology 165, 1759-1767.

    Article  CAS  Google Scholar 

  • Papa, A., Chaligiannis, I., Kontana, N., Sourba, T., Tsioka, K., Tsatsaris, A., and Sotiraki, S., 2014. A novel AP92-like Crimean-Congo hemorrhagic fever virus strain, Greece. Ticks and Tick-borne Diseases 5, 590-593.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Papa, A., Tsergouli, K., Tsioka, K., and Mirazimi, A., 2017. Crimean-Congo Hemorrhagic Fever: Tick-Host-Virus Interactions. Frontiers in Cellular and Infection Microbiology 7, 213-213.

    Article  Google Scholar 

  • Relatório REVIVE 2020 - Culicídeos e Ixodídeos: Rede de Vigilância de Vetores. http://hdl.handle.net/10400.18/7711 Accessed 01 January, 2020.

  • Sas, M.A., Comtet, L., Donnet, F., Mertens, M., Vatansever, Z., Tordo, N., Pourquier, P., and Groschup, M.H., 2018. A novel double-antigen sandwich ELISA for the species-independent detection of Crimean-Congo hemorrhagic fever virus-specific antibodies. Antiviral Research 151, 24-26.

    Article  CAS  Google Scholar 

  • Schuster, I., Chaintoutis, S.C., Dovas, C.I., Groschup, M.H., and Mertens, M., 2017. Detection of Crimean-Congo hemorrhagic fever virus-specific IgG antibodies in ruminants residing in Central and Western Macedonia, Greece. Ticks and Tick-borne Diseases 8, 494-498

    Article  Google Scholar 

  • Schuster, I., Mertens, M., Mrenoshki, S., Staubach, C., Mertens, C., Brüning, F., Wernike, K., Hechinger, S., Berxholi, K., Mitrov, D., and Groschup, M.H., 2016. Sheep and goats as indicator animals for the circulation of CCHFV in the environment. Experimental & Applied Acarology. 68, 337-346.

    Article  Google Scholar 

  • Spengler, J.R., Bergeron, É., and Rollin, P.E., 2016a. Seroepidemiological Studies of Crimean-Congo Hemorrhagic Fever Virus in Domestic and Wild Animals. PLoS Neglected Tropical Diseases. 10, e0004210-e0004210.

    Article  Google Scholar 

  • Spengler, J.R., Estrada-Peña, A., Garrison, A.R., Schmaljohn, C., Spiropoulou, C.F., Bergeron, É., and Bente, D.A., 2016b. A chronological review of experimental infection studies of the role of wild animals and livestock in the maintenance and transmission of Crimean-Congo hemorrhagic fever virus. Antiviral Research 135, 31-47.

    Article  CAS  Google Scholar 

  • WHO 2018. Annual review of diseases prioritized under the Research and Development Blueprint. https://www.who.int/newsroom/events/detail/2018/02/06/default-calendar/2018-Annual-review-of-diseasesprioritized-under-the-research-and development-blueprint.

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Authors and Affiliations

Authors

Contributions

JRM and PB: Conceptualization; data curation; formal analysis; methodology; resources; writing, original draft; writing, review and editing. RC, FE, CS, CC, ACM, CN, HV: Sampling, writing—review and editing. HP: Methodology. CNP and MSJ: Writing—review and editing.

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Correspondence to Patrícia Ferreira Barradas.

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The authors confirm that the ethical policies of the journal, as noted on the journal’s author guidelines page, have been adhered to. No ethical approval was required as this study was performed with samples obtained from remnants, hence causing no further pain to the animal.

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The authors declare no competing interests.

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Mesquita, J.R., Cruz, R., Esteves, F. et al. Crimean-Congo hemorrhagic fever virus circulating among sheep of Portugal: a nationwide serosurvey assessment. Trop Anim Health Prod 54, 237 (2022). https://doi.org/10.1007/s11250-022-03238-z

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