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Seroepidemiological survey of the Crimean-Congo Hemorrhagic Fever Virus (CCHFV) infection amongst domestic ruminants in Adana province, East Mediterranean, Turkey.

Year 2021, Volume: 6 Issue: 3, 228 - 238, 31.12.2021

Bilge Kaan Tekelioğlu Emre Ozan Armağan Erdem Ütük Ayça Hatice Atlı Harun Albayrak Mabrouk Elsabagh Mahmut Gökçe Nevin Turut Ömer Memduh Esendal Mehmet Çelik

https://doi.org/10.31797/vetbio.997150

Abstract

Crimean-Congo hemorrhagic fever virus (CCHFV) has been observing since 2002 and 2015 in Turkey and Adana, respectively. However, there were no previous seroepidemiological data on CCHFV in Adana. This study, thus, aimed to investigate the seroepidemiological status of Adana province for CCHFV in ruminants, according to species, breed, age, gender and geographical location. The study was carried out in 15 districts from sea level to plateaus (0-1472 m), within a 14,030 km² area. 485 samples were tested with modified anti-CCHFV IgG ELISA. A human-based IgG ELISA was adapted to recognize cattle, sheep and goats IgG antibodies. The conjugation (anti-human IgG peroxidase) was replaced with appropriate conjugate in each species. Statistical analyses indicated a significant relationship between antibody presence and animal age, species, breed and location but there was no relation with animal gender. Out of 485 samples, 154 were seropositive (31.8%). It was determined that the statistical cluster varied between 5.8% and 74.3% according to location and seropositivity. The most important variable associated with antibody presence was geographic location. While high seropositivity is found at altitudes above 555 meters, it is found to be 7% and 3% at sea level. The seropositivity reached 100% in the village where human deaths were seen in 2015, and 74.3% in the Tufanbeyli district where this village is located. The results indicate that Adana is an endemic province for CCHFV infection, especially in high altitude regions.

Keywords

Crimean-Congo Hemorrhagic Fever Virus ELISA seroepidemiology ruminants Adana

Supporting Institution

Çukurova Üniversitesi Bilimsel Araştırma Koordinasyon Birimi tarafından desteklenmiştir

Project Number

TS-7862:

Thanks

This project; TS-7862 was funded by Çukurova University Scientific Research Coordination Department. We would like to thank the animal owners, Adana and Samsun Veterinary Research Institutes, for their kind contribution. During the study, a high standard (best practice) veterinary care and informed customer approval were provided.

References

  • Al-Abri, S. S., Abaidani, I. A., Fazlalipour, M., Mostafavi, E., Leblebicioglu, H., Pshenichnaya, N., Memish, Z. A., Hewson, R., Petersen, E., Mala, P., Nhu Nguyen, T. M., Rahman Malik, M., Formenty, P., &Jeffries, R. (2017). Current status of Crimean-Congo haemorrhagic fever in the World Health Organization Eastern Mediterranean Region: issues, challenges, and future directions. International Journal of Infectious Diseases, 58, 82-89. doi: 10.1016/j.ijid.2017.02.018
  • Albayrak, H., Ozan, E., &Kurt, M. (2010). An antigenic investigation of Crimean-Congo hemorrhagic fever virus (CCHFV) in hard ticks from provinces in Northern Turkey. Tropical Animal Health and Production, 42(7), 1323-1325. doi: 10.1007/s11250-010-9579-1
  • Albayrak, H., Ozan, E., &Kurt, M. (2012). Serosurvey and molecular detection of Crimean-Congo hemorrhagic fever virus (CCHFV) in northern Turkey. Tropical Animal Health and Production, 44(7), 1667-1671. doi: 10.1007/s11250-012-0122-4
  • Appannanavar, S. B., &Mishra, B. (2011). An update on Crimean Congo hemorrhagic fever. Journal of Global Infectious Diseases, 3(3), 285–292. doi: 10.4103/0974-777X.83537
  • Athar, M. N., Khalid, M. A., Ahmad, A. M., Bashir, N., Baqai, H. Z.,Ahmad, M., Balouch, A. H., & Bashir, K.(2005). Crimean-Congo hemorrhagic fever outbreak in Rawalpindi, Pakistan, February 2002: contact tracing and risk assessment. The American Journal of Tropical Medicine and Hygiene, 72(4), 471-473. doi: 10.4269/ajtmh.2005.72.471
  • Aydın, M. F. & Coşkun, A. (2019). İnsanlarda kene ile bulaşan hastalık etkenleri ve Türkiye’deki mevcut durumu. Journal of Advances in VetBio Science and Techniques, 4 (1) , 26-32 . DOI: 10.31797/vetbio.486679
  • Bodur, H., Akinci, E., Ascioglu, S., Öngürü, P., &Uyar, Y. (2012). Subclinical infections with Crimean-Congo hemorrhagic fever virus, Turkey. Emerging Infectious Diseases, 18(4), 640-642. doi: 10.3201/eid1804.111374
  • Commission Decision SANCO/B3/R11. (1999). Scientific Committee on Animal Health and Animal Welfare. Diagnostic tests for Crimean Congo haemorrhagic fever [CCHF] in ratites. European Commission, Health & Consumer Protection Directorate-General, Directorate B-Scientific Health Opinions, Unit B3-Management of Scientific Committees II.
  • Deka, M. A. (2017). Crimean-Congo hemorrhagic fever geographic and environmental risk assessment in the Balkan and Anatolian Peninsulas. Papers in Applied Geography, 4(1), 46-71. doi: 10.1080/23754931.2017.1378122
  • Günaydın, S. N., Aydın, K., Yılmaz, G., Çaylan, R., &Köksal, İ. (2010). Crimean-Congo hemorrhagic fever cases in the eastern Black Sea Region of Turkey: demographic, geographic, climatic, and clinical characteristics. Turkish Journal of Medical Sciences, 40(6), 829-834.
  • Kadanalı, A., Erol, S., Özkurt, Z., &Özden, K. (2009). Epidemiological risk factors for Crimean-Congo hemorrhagic fever patients. Turkish Journal of Medical Sciences, 39(6), 829-832.
  • Karaer, F., &Kılınç, M. (2001). The Flora of Kelkit Valley. Turkish Journal of Botany, 25(4), 195-238.
  • Kasi, K. K., Sas, M. A., Sauter-Louis, C., Gethmann, J. M., Groschup, M. H., &Conraths, F. J.(2019). Risk factors for Crimean-Congo hemorrhagic fever virus infection in Livestock in Pakistan. International Journal of Infectious Diseases, 79(1), 137. doi: 10.1016/j.ijid.2018.11.335
  • Kuşcu, F., Kömür, S., Yağcı Çağlayık, D., Ulu, A., İnal, A. S., Kurtaran, B., Taşova, Y., Aksu, H. S. Z., &Özkul, A.(2017). Is Crimean-Congo hemorrhagic fever virus topotype important in the possibility of nosocomial transmission? Acta Medica Mediterranea, 33(4), 575-580. doi: 10.19193/0393-6384_2017_4_084
  • Leblebicioglu, H., Eroglu, C., Erciyas-Yavuz, K., Hokelek, M., Acici, M., &Yilmaz, H.(2014). Role of migratory birds in spreading Crimean-Congo hemorrhagic fever, Turkey. Emerging Infectious Diseases, 20(8), 1331-1334. doi: 10.3201/eid2008.131547
  • Leblebicioglu, H., Ozaras, R., &Irmak, H. (2016). Crimean-Congo hemorrhagic fever in Turkey: Current status and future challenges. Antiviral Research, 126, 21-34. doi: 10.1016/j.antiviral.2015.12.003
  • Leblebicioglu, H., Sunbul, M., Memish, Z. A., Al-Tawfig, J. A., Bodur, H.,Ozkul, A., Gucukoglu, A., Chinikar, S., & Hasan, Z. (2015). Consensus report: Preventive measures for Crimean-Congo Hemorrhagic Fever during Eid-al-Adha festival. International Journal of Infectious Diseases, 38, 9-15. doi: 10.1016/j.ijid.2015.06.029
  • Leventhal, S. S., Wilson, D., Feldmann, H., & Hawman, D. W. (2021). A Look into Bunyavirales Genomes: Functions of Non-Structural (NS) Proteins. Viruses, 13(2), 314. https://doi.org/10.3390/v13020314
  • Mertens, M., Schmidt, K., Ozkul, A., &Groschup, M. H. (2013). The impact of Crimean-Congo hemorrhagic fever virus on public health. Antiviral Research, 98(2), 248-260. doi: 10.1016/j.antiviral.2013.02.007
  • Mertens, M., Schuster, I., Sas, M. A., Vatansever, Z., Hubalek, Z., Güven, E., Deniz, A., Georgiev, G., Peshev, R., &Groschup, M. H. (2016). Crimean-Congo hemorrhagic fever virus in Bulgaria and Turkey. Vector-Borne and Zoonotic Diseases, 16(9), 619-623. doi: 10.1089/vbz.2016.1944
  • Mertens, M., Vatansever, Z., Mrenoshki, S., Krstevski, K., Stefanovska, J., Djadjovski, I., Cvetkovikj, I., Farkas, R., Schuster, I., Donnet, F., Comtet, L., Tordo, N., Ben Mechlia, M., Balkema-Buschmann, A., Mitrov, D., &Groschup, M. H. (2015). Circulation of Crimean-Congo Hemorrhagic Fever Virus in the former Yugoslav Republic of Macedonia revealed by screening of cattle sera using a novel enzyme-linked immunosorbent assay. PLOS Neglected Tropical Diseases, 9(3), e0003519. doi: 10.1371/journal.pntd.0003519
  • Orkun, Ö.,Karaer, Z., Çakmak, A., &Nalbantoglu, S. (2017). Crimean-Congo hemorrhagic fever virus in ticks in Turkey: A broad range tick surveillance study. Infection, Genetics and Evolution, 52, 59-66. doi: 10.1016/j.meegid.2017.04.017
  • Rencher, A. C. (2002). Multivariate Analysis of Variance. USA: John Wiley & Sons.
  • Rokach, L., &Maimon, O. (2008). Data mining with decision trees theory and applications. Singapore: World Scientific.
  • Schuster, I., Mertens, M., Mrenoshki, S., Staubach, C., Mertens, C., Brüning, F., Wernike, K., Hechinger, S., Berxholi, K., Mitrov, D., & Groschup, M. H.(2016). Sheep and goats as indicator animals for circulation of CCHFV in the environment. Experimental and Applied Acarology, 68(3), 337-346. doi: 10.1007/s10493-015-9996-y
  • Tonbak, S., Aktas, M., Altay, K., Azkur, A. K., Kalkan, A., Bolat, Y., Dumanli, N., &Ozdarendeli, A.(2006). Crimean-Congo hemorrhagic fever virus: genetic analysis and tick survey in Turkey. Journal of Clinical Microbiology, 44(11), 4120–4124. doi: 10.1128/JCM.00644-06
  • Tuncer, P., Yesilbag, K., Alpay, G., Dincer, E., Girisgin, A. O., Aydın, L., Uyar, Y., & Ozkul, A.(2014). Crimean-Congo hemorrhagic fever infection in domestic animals in Marmara region, Western Turkey. Ankara Üniversitesi Veteriner Fakültesi Dergisi, 61, 49-53. doi: 10.1501/Vetfak_0000002604
  • World Health Organization (2013). Crimean-Congo haemorrhagic fever. https://www.who.int/en/news-room/fact-sheets/detail/crimean-congo-haemorrhagic-fever
  • Yilmaz, G. R., Buzgan, T., Irmak, H., Safran, A., Uzun, R., Cevik, M. A., & Torunoglu, M. A. (2009). The epidemiology of Crimean-Congo hemorrhagic fever in Turkey, 2002–2007. International Journal of Infectious Diseases, 13(3), 380-386. doi: 10.1016/j.ijid.2008.07.021

Evcil ruminatlarda Kırım-Kongo Kanamalı Ateşi Virusu (KKKAV) enfeksiyonunun seroepidemiyolojik araştırması, Adana ili, Doğu Akdeniz bölgesi, Türkiye.

Year 2021, Volume: 6 Issue: 3, 228 - 238, 31.12.2021

Bilge Kaan Tekelioğlu Emre Ozan Armağan Erdem Ütük Ayça Hatice Atlı Harun Albayrak Mabrouk Elsabagh Mahmut Gökçe Nevin Turut Ömer Memduh Esendal Mehmet Çelik

https://doi.org/10.31797/vetbio.997150

Abstract

Kırım-Kongo kanamalı ateşi virusu (KKKAV), Türkiye'de 2002 ve 2015'ten beri Adana'da görülmektedir. Ancak Adana'da KKKAV ile ilgili daha önceki dönemlere ait seroepidemiyolojik veri mevcut değildir. Bu çalışmada, Adana ilinin ruminantlarda KKKAV için tür, ırk, yaş, cinsiyet ve coğrafi konuma göre seroepidemiyolojik durumunun araştırılması amaçlanmıştır. Çalışma 14.030 km² alan içerisinde deniz seviyesinden yaylalara (0-1472 m) kadar 15 ilçede gerçekleştirilmiştir. 485 numune, modifiye anti-CCHFV IgG ELISA ile test edilmiştir. İnsan bazlı bir IgG ELISA, sığır, koyun ve keçi IgG antikorlarını tanımak için uyarlanmıştır. Konjugasyon (anti-insan IgG peroksidaz), her türe uygun konjugat ile değiştirilmiştir. İstatistiksel analizler, antikor varlığı ile hayvan yaşı, türü, ırkı ve coğrafi konumu arasında önemli bir ilişki olduğunu gösterirken hayvanların cinsiyeti ile ilişki olmadığını da göstermiştir. 485 örnekten 154'ü seropozitif bulunmuş (%31,8). İstatistiksel kümenin coğrafi konuma ve seropozitifliğe göre %5,8 ile %74,3 arasında değiştiği belirlenmiştir. Antikor varlığı ile ilişkili en önemli değişkenin coğrafi konum olduğu saptanmıştır. 555 metrenin üzerindeki rakımlarda yüksek seropozitiflik bulunurken, deniz seviyesinde %7 ve %3 olarak bulunmuştur. 2015 yılında insan ölümlerinin görüldüğü köyde seropozitifliğin %100'e ulaştığı, bu köyün bulunduğu Tufanbeyli ilçesinde ise %74,3'e ulaştığı saptanmıştır. Sonuçlar, Adana ilinin KKKA enfeksiyonu için özellikle yüksek irtifalı bölgeler açsısından endemik bir il olduğunu göstermektedir.

Project Number

TS-7862:

References

  • Al-Abri, S. S., Abaidani, I. A., Fazlalipour, M., Mostafavi, E., Leblebicioglu, H., Pshenichnaya, N., Memish, Z. A., Hewson, R., Petersen, E., Mala, P., Nhu Nguyen, T. M., Rahman Malik, M., Formenty, P., &Jeffries, R. (2017). Current status of Crimean-Congo haemorrhagic fever in the World Health Organization Eastern Mediterranean Region: issues, challenges, and future directions. International Journal of Infectious Diseases, 58, 82-89. doi: 10.1016/j.ijid.2017.02.018
  • Albayrak, H., Ozan, E., &Kurt, M. (2010). An antigenic investigation of Crimean-Congo hemorrhagic fever virus (CCHFV) in hard ticks from provinces in Northern Turkey. Tropical Animal Health and Production, 42(7), 1323-1325. doi: 10.1007/s11250-010-9579-1
  • Albayrak, H., Ozan, E., &Kurt, M. (2012). Serosurvey and molecular detection of Crimean-Congo hemorrhagic fever virus (CCHFV) in northern Turkey. Tropical Animal Health and Production, 44(7), 1667-1671. doi: 10.1007/s11250-012-0122-4
  • Appannanavar, S. B., &Mishra, B. (2011). An update on Crimean Congo hemorrhagic fever. Journal of Global Infectious Diseases, 3(3), 285–292. doi: 10.4103/0974-777X.83537
  • Athar, M. N., Khalid, M. A., Ahmad, A. M., Bashir, N., Baqai, H. Z.,Ahmad, M., Balouch, A. H., & Bashir, K.(2005). Crimean-Congo hemorrhagic fever outbreak in Rawalpindi, Pakistan, February 2002: contact tracing and risk assessment. The American Journal of Tropical Medicine and Hygiene, 72(4), 471-473. doi: 10.4269/ajtmh.2005.72.471
  • Aydın, M. F. & Coşkun, A. (2019). İnsanlarda kene ile bulaşan hastalık etkenleri ve Türkiye’deki mevcut durumu. Journal of Advances in VetBio Science and Techniques, 4 (1) , 26-32 . DOI: 10.31797/vetbio.486679
  • Bodur, H., Akinci, E., Ascioglu, S., Öngürü, P., &Uyar, Y. (2012). Subclinical infections with Crimean-Congo hemorrhagic fever virus, Turkey. Emerging Infectious Diseases, 18(4), 640-642. doi: 10.3201/eid1804.111374
  • Commission Decision SANCO/B3/R11. (1999). Scientific Committee on Animal Health and Animal Welfare. Diagnostic tests for Crimean Congo haemorrhagic fever [CCHF] in ratites. European Commission, Health & Consumer Protection Directorate-General, Directorate B-Scientific Health Opinions, Unit B3-Management of Scientific Committees II.
  • Deka, M. A. (2017). Crimean-Congo hemorrhagic fever geographic and environmental risk assessment in the Balkan and Anatolian Peninsulas. Papers in Applied Geography, 4(1), 46-71. doi: 10.1080/23754931.2017.1378122
  • Günaydın, S. N., Aydın, K., Yılmaz, G., Çaylan, R., &Köksal, İ. (2010). Crimean-Congo hemorrhagic fever cases in the eastern Black Sea Region of Turkey: demographic, geographic, climatic, and clinical characteristics. Turkish Journal of Medical Sciences, 40(6), 829-834.
  • Kadanalı, A., Erol, S., Özkurt, Z., &Özden, K. (2009). Epidemiological risk factors for Crimean-Congo hemorrhagic fever patients. Turkish Journal of Medical Sciences, 39(6), 829-832.
  • Karaer, F., &Kılınç, M. (2001). The Flora of Kelkit Valley. Turkish Journal of Botany, 25(4), 195-238.
  • Kasi, K. K., Sas, M. A., Sauter-Louis, C., Gethmann, J. M., Groschup, M. H., &Conraths, F. J.(2019). Risk factors for Crimean-Congo hemorrhagic fever virus infection in Livestock in Pakistan. International Journal of Infectious Diseases, 79(1), 137. doi: 10.1016/j.ijid.2018.11.335
  • Kuşcu, F., Kömür, S., Yağcı Çağlayık, D., Ulu, A., İnal, A. S., Kurtaran, B., Taşova, Y., Aksu, H. S. Z., &Özkul, A.(2017). Is Crimean-Congo hemorrhagic fever virus topotype important in the possibility of nosocomial transmission? Acta Medica Mediterranea, 33(4), 575-580. doi: 10.19193/0393-6384_2017_4_084
  • Leblebicioglu, H., Eroglu, C., Erciyas-Yavuz, K., Hokelek, M., Acici, M., &Yilmaz, H.(2014). Role of migratory birds in spreading Crimean-Congo hemorrhagic fever, Turkey. Emerging Infectious Diseases, 20(8), 1331-1334. doi: 10.3201/eid2008.131547
  • Leblebicioglu, H., Ozaras, R., &Irmak, H. (2016). Crimean-Congo hemorrhagic fever in Turkey: Current status and future challenges. Antiviral Research, 126, 21-34. doi: 10.1016/j.antiviral.2015.12.003
  • Leblebicioglu, H., Sunbul, M., Memish, Z. A., Al-Tawfig, J. A., Bodur, H.,Ozkul, A., Gucukoglu, A., Chinikar, S., & Hasan, Z. (2015). Consensus report: Preventive measures for Crimean-Congo Hemorrhagic Fever during Eid-al-Adha festival. International Journal of Infectious Diseases, 38, 9-15. doi: 10.1016/j.ijid.2015.06.029
  • Leventhal, S. S., Wilson, D., Feldmann, H., & Hawman, D. W. (2021). A Look into Bunyavirales Genomes: Functions of Non-Structural (NS) Proteins. Viruses, 13(2), 314. https://doi.org/10.3390/v13020314
  • Mertens, M., Schmidt, K., Ozkul, A., &Groschup, M. H. (2013). The impact of Crimean-Congo hemorrhagic fever virus on public health. Antiviral Research, 98(2), 248-260. doi: 10.1016/j.antiviral.2013.02.007
  • Mertens, M., Schuster, I., Sas, M. A., Vatansever, Z., Hubalek, Z., Güven, E., Deniz, A., Georgiev, G., Peshev, R., &Groschup, M. H. (2016). Crimean-Congo hemorrhagic fever virus in Bulgaria and Turkey. Vector-Borne and Zoonotic Diseases, 16(9), 619-623. doi: 10.1089/vbz.2016.1944
  • Mertens, M., Vatansever, Z., Mrenoshki, S., Krstevski, K., Stefanovska, J., Djadjovski, I., Cvetkovikj, I., Farkas, R., Schuster, I., Donnet, F., Comtet, L., Tordo, N., Ben Mechlia, M., Balkema-Buschmann, A., Mitrov, D., &Groschup, M. H. (2015). Circulation of Crimean-Congo Hemorrhagic Fever Virus in the former Yugoslav Republic of Macedonia revealed by screening of cattle sera using a novel enzyme-linked immunosorbent assay. PLOS Neglected Tropical Diseases, 9(3), e0003519. doi: 10.1371/journal.pntd.0003519
  • Orkun, Ö.,Karaer, Z., Çakmak, A., &Nalbantoglu, S. (2017). Crimean-Congo hemorrhagic fever virus in ticks in Turkey: A broad range tick surveillance study. Infection, Genetics and Evolution, 52, 59-66. doi: 10.1016/j.meegid.2017.04.017
  • Rencher, A. C. (2002). Multivariate Analysis of Variance. USA: John Wiley & Sons.
  • Rokach, L., &Maimon, O. (2008). Data mining with decision trees theory and applications. Singapore: World Scientific.
  • Schuster, I., Mertens, M., Mrenoshki, S., Staubach, C., Mertens, C., Brüning, F., Wernike, K., Hechinger, S., Berxholi, K., Mitrov, D., & Groschup, M. H.(2016). Sheep and goats as indicator animals for circulation of CCHFV in the environment. Experimental and Applied Acarology, 68(3), 337-346. doi: 10.1007/s10493-015-9996-y
  • Tonbak, S., Aktas, M., Altay, K., Azkur, A. K., Kalkan, A., Bolat, Y., Dumanli, N., &Ozdarendeli, A.(2006). Crimean-Congo hemorrhagic fever virus: genetic analysis and tick survey in Turkey. Journal of Clinical Microbiology, 44(11), 4120–4124. doi: 10.1128/JCM.00644-06
  • Tuncer, P., Yesilbag, K., Alpay, G., Dincer, E., Girisgin, A. O., Aydın, L., Uyar, Y., & Ozkul, A.(2014). Crimean-Congo hemorrhagic fever infection in domestic animals in Marmara region, Western Turkey. Ankara Üniversitesi Veteriner Fakültesi Dergisi, 61, 49-53. doi: 10.1501/Vetfak_0000002604
  • World Health Organization (2013). Crimean-Congo haemorrhagic fever. https://www.who.int/en/news-room/fact-sheets/detail/crimean-congo-haemorrhagic-fever
  • Yilmaz, G. R., Buzgan, T., Irmak, H., Safran, A., Uzun, R., Cevik, M. A., & Torunoglu, M. A. (2009). The epidemiology of Crimean-Congo hemorrhagic fever in Turkey, 2002–2007. International Journal of Infectious Diseases, 13(3), 380-386. doi: 10.1016/j.ijid.2008.07.021
There are 29 citations in total.

Details

Primary Language English
Subjects Veterinary Surgery
Journal Section Research Articles
Authors

Bilge Kaan Tekelioğlu 0000-0001-6727-3175

Emre Ozan 0000-0001-9872-8152

Armağan Erdem Ütük 0000-0002-7986-3583

Ayça Hatice Atlı 0000-0002-4375-9733

Harun Albayrak 0000-0002-4468-2790

Mabrouk Elsabagh 0000-0002-0596-6547

Mahmut Gökçe 0000-0002-8716-5996

Nevin Turut 0000-0003-2950-001X

Ömer Memduh Esendal 0000-0002-2700-2634

Mehmet Çelik 0000-0003-4330-2490

Project Number TS-7862:
Publication Date December 31, 2021
Submission Date September 18, 2021
Acceptance Date November 7, 2021
Published in Issue Year 2021 Volume: 6 Issue: 3

Cite

APA Tekelioğlu, B. K., Ozan, E., Ütük, A. E., Atlı, A. H., et al. (2021). Seroepidemiological survey of the Crimean-Congo Hemorrhagic Fever Virus (CCHFV) infection amongst domestic ruminants in Adana province, East Mediterranean, Turkey. Journal of Advances in VetBio Science and Techniques, 6(3), 228-238. https://doi.org/10.31797/vetbio.997150
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