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

Öz:

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. Total of 485 serum samples (165 cattle, 169 sheep and 160 goats) were collected from domestic ruminants. A modified human-based IgG ELISA kit was used for the detection of CCHFV specific antibodies in cattle, sheep and goats. 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 results indicate that Adana province is at risk for CCHFV infection, especially in high altitude regions.

Anahtar Kelime: Crimean-Congo Hemorrhagic Fever Virus ruminants ELISA seroepidemiology Adana Province East Mediterranean

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

Öz:

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.

Anahtar Kelime:

Belge Türü: Makale Makale Türü: Araştırma Makalesi Erişim Türü: Erişime Açık

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
Barthel, R., Mohareb, E., Younan, R., Gladnishka, T., Kalvatchev, N., Moemen, A., Mansour, S.S., Rossi, C., Schoepp, R., Christova, I. (2014). Seroprevalance of Crimean-Congo haemorrhagic fever in Bulgarian livestock. Biotechnol Biotechnol Equip, 28, 540-542.
Blanco-Penedo, I., Obanda, O., Kingori, E., Agwanda, B., Ahlm, C., Lwande, O. W. (2021). Seroepidemiology of Crimean-Congo Hemorrhagic Fever Virus (CCHFV) in cattle across three livestock pastoral regions in Kenya. Dairy, 2, 425–434.
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
Fajs, L., Humolli, I., Saksida, A., Knap, N., Jelovšek, M., Korva, M., Dedushaj, I., Avšič-Županc, T. (2014). Prevalence of Crimean-Congo hemorrhagic fever virus in healthy population, livestock and ticks in Kosovo. PLoS One, 9:e110982.
Gergova, I., Kunchev, M., Kamarinchev, B. (2012). CrimeanCongo hemorrhagic fever virus-tick survey in endemic areas in Bulgaria. J Med Virol, 84, 608-614.
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.
Hoek, M., Fischer, E., Hengel, R. V. D., Backer, J., Koeijer, A. D. (2012). Workshop on a risk assessment of Crimen Congo Hemorrhagic fever in Western Europe. Central Veterinary Institute, Report number 12/CVI0361. Lelystad, The Netherlands.
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
Kırbaş, A. (2009). Elazığ, Samsun, Sivas, Tokat Ve Yozgat İllerindeki Sığır Ve Koyunlarda Kırım Kongo Kanamalı Ateş Virüs Enfeksiyonunun Seroprevalansının Araştırılması (Publication No: 236097) [PhD Thesis, Fırat Üniversitesi] Fırat University Open Access Archive.
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
Özüpak, T. (2017). Kırım kongo kanamalı ateşi virüsü'nün kene ve evcil ruminant (sığır, koyun ve keçi) kan ve sütlerinde varlığının araştırılması / The investigation of presence of crimean-congo hemorrhagic fever virüs (cchfv) in tick and blood and milk of domestic ruminant species (cattle, sheep and goat). (Publication No. 468749) [PhD Thesis, Samsun 19 Mayıs University]. Thesis Center of Turkish Council of Higher Education.
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
Şevik, M. (2018). Epidemiological Investigation of CrimeanCongo Hemorrhagic Fever infection in Cattle in some provinces of Turkey. Etlik Vet Mikrobiyol Derg, 29(1), 24-29.
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
Vatansever, Z. R., Uzun, A., Estrada-Pena, O., Ergonul (2007). Crimean-Congo hemorrhagic fever in Turkey. In Crimean- Congo Hemorrhagic Fever, eds. O. Ergonul and C. Whitehouse, 155–165. Dordrecht, The Netherlands: Springer.
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

APA	Tekelioglu B, Ozan E, UTUK A, Atlı A, ALBAYRAK H, Elsabagh M, GOKCE M, Turut N, Esendal Ö, celik m (2021). Seroepidemiological survey of the Crimean-Congo Hemorrhagic Fever Virus (CCHFV) infection amongst domestic ruminants in Adana province, East Mediterranean, Turkey. , 228 - 238. 10.31797/vetbio.997150
Chicago	Tekelioglu Bilge Kaan,Ozan Emre,UTUK Armagan Erdem,Atlı Ayça Hatice,ALBAYRAK Harun,Elsabagh Mabrouk,GOKCE MAHMUT ALI,Turut Nevin,Esendal Ömer Memduh,celik mehmet Seroepidemiological survey of the Crimean-Congo Hemorrhagic Fever Virus (CCHFV) infection amongst domestic ruminants in Adana province, East Mediterranean, Turkey. (2021): 228 - 238. 10.31797/vetbio.997150
MLA	Tekelioglu Bilge Kaan,Ozan Emre,UTUK Armagan Erdem,Atlı Ayça Hatice,ALBAYRAK Harun,Elsabagh Mabrouk,GOKCE MAHMUT ALI,Turut Nevin,Esendal Ömer Memduh,celik mehmet Seroepidemiological survey of the Crimean-Congo Hemorrhagic Fever Virus (CCHFV) infection amongst domestic ruminants in Adana province, East Mediterranean, Turkey. , 2021, ss.228 - 238. 10.31797/vetbio.997150
AMA	Tekelioglu B,Ozan E,UTUK A,Atlı A,ALBAYRAK H,Elsabagh M,GOKCE M,Turut N,Esendal Ö,celik m Seroepidemiological survey of the Crimean-Congo Hemorrhagic Fever Virus (CCHFV) infection amongst domestic ruminants in Adana province, East Mediterranean, Turkey. . 2021; 228 - 238. 10.31797/vetbio.997150
Vancouver	Tekelioglu B,Ozan E,UTUK A,Atlı A,ALBAYRAK H,Elsabagh M,GOKCE M,Turut N,Esendal Ö,celik m Seroepidemiological survey of the Crimean-Congo Hemorrhagic Fever Virus (CCHFV) infection amongst domestic ruminants in Adana province, East Mediterranean, Turkey. . 2021; 228 - 238. 10.31797/vetbio.997150
IEEE	Tekelioglu B,Ozan E,UTUK A,Atlı A,ALBAYRAK H,Elsabagh M,GOKCE M,Turut N,Esendal Ö,celik m "Seroepidemiological survey of the Crimean-Congo Hemorrhagic Fever Virus (CCHFV) infection amongst domestic ruminants in Adana province, East Mediterranean, Turkey." , ss.228 - 238, 2021. 10.31797/vetbio.997150
ISNAD	Tekelioglu, Bilge Kaan vd. "Seroepidemiological survey of the Crimean-Congo Hemorrhagic Fever Virus (CCHFV) infection amongst domestic ruminants in Adana province, East Mediterranean, Turkey". (2021), 228-238. https://doi.org/10.31797/vetbio.997150

APA	Tekelioglu B, Ozan E, UTUK A, Atlı A, ALBAYRAK H, Elsabagh M, GOKCE M, Turut N, Esendal Ö, celik m (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. 10.31797/vetbio.997150
Chicago	Tekelioglu Bilge Kaan,Ozan Emre,UTUK Armagan Erdem,Atlı Ayça Hatice,ALBAYRAK Harun,Elsabagh Mabrouk,GOKCE MAHMUT ALI,Turut Nevin,Esendal Ömer Memduh,celik mehmet 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, no.3 (2021): 228 - 238. 10.31797/vetbio.997150
MLA	Tekelioglu Bilge Kaan,Ozan Emre,UTUK Armagan Erdem,Atlı Ayça Hatice,ALBAYRAK Harun,Elsabagh Mabrouk,GOKCE MAHMUT ALI,Turut Nevin,Esendal Ömer Memduh,celik mehmet 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, vol.6, no.3, 2021, ss.228 - 238. 10.31797/vetbio.997150
AMA	Tekelioglu B,Ozan E,UTUK A,Atlı A,ALBAYRAK H,Elsabagh M,GOKCE M,Turut N,Esendal Ö,celik m 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. 2021; 6(3): 228 - 238. 10.31797/vetbio.997150
Vancouver	Tekelioglu B,Ozan E,UTUK A,Atlı A,ALBAYRAK H,Elsabagh M,GOKCE M,Turut N,Esendal Ö,celik m 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. 2021; 6(3): 228 - 238. 10.31797/vetbio.997150
IEEE	Tekelioglu B,Ozan E,UTUK A,Atlı A,ALBAYRAK H,Elsabagh M,GOKCE M,Turut N,Esendal Ö,celik m "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, ss.228 - 238, 2021. 10.31797/vetbio.997150
ISNAD	Tekelioglu, Bilge Kaan vd. "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 (2021), 228-238. https://doi.org/10.31797/vetbio.997150