Phylogenetic Analysis and Genetic Characterization of Bovine Respiratory Syncytial Virus G Glycoprotein / Bovine Respiratory Syncytial Virus G Glycoproteininin Filogenetik ve Analizi ve Genetik Karakterizasyonu
Yıl 2024,
Cilt: 3 Sayı: 2, 32 - 39, 23.12.2024
Ali Küçük
,
Özge Sevinç Korkmaz Akar
,
Yakup Yıldırım
,
Kamil Atlı
Öz
This study aimed to molecularly detect Bovine Respiratory Syncytial Virus (BRSV) in cattle with clinical signs of respiratory system infection and to conduct a phylogenetic analysis of the detected strains. To detect the pathogen, nasal swab samples collected from 96 cattle were subjected to Reverse Transcriptase – nested PCR using specific primer sets. As a result of the molecular techniques, viral nucleic acid was detected in 2.08% (2/96) of the samples. Additionally, sequence and phylogenetic analyses of the detected local variant were performed and compared with various BRSV strains identified in different regions of Turkey and around the world. The genetic data obtained revealed that the isolates identified in this study belong to Subgroup III, alongside BRSV strains reported from various regions of Turkey, France, and the USA. Immunologically significant point mutations were detected in the immunodominant G glycoprotein region of the variant (Asn(N)179 → Asp(D) / Ala(A) 205 → Thr (T)). This result indicates that BRSV strains circulating among cattle can escape the host immune system without losing their pathogenicity and is considered to be one of the important factors that can cause respiratory system infection outbreaks in cattle.
Etik Beyan
Approval was obtained from the animal testing local ethics committee of Burdur Mehmet Akif Ersoy University. The procedures used in this study adhere to the tenets of the Declaration of Helsinki (MAKU-HADYEK 1045/2023)
Destekleyen Kurum
The authors did not receive support from any organization for the submitted work.
Kaynakça
- Bertolotti, L., Giammarioli, M., & Rosati, S. (2018). Genetic characterization of bovine respiratory syncytial virus strains isolated in Italy: evidence fort he circulation of new divergent clades. Journal of Veterinary Diagnostic Investigation, 30, 300-304. https://doi.org/ 10.1177/1040638717746202.
- Bidokhti, M.R.M., Traven, M., Ohlson, A., Zarnegar, B., Baule, C., Belak, S., Alenius, S., & Liu, L. (2012). Phylogenetic analysis of bovine respiratory syncytial viruses from recent outbreaks in feedlot and dairy cattle herds. Archive of Virology, 157, 601-607. https://doi.org/ 10.1007/s00705-011-1209-3
- Chang, Y., Yue, H., & Tang, C. (2022). Prevalence and molecular characteristics of bovine respiratory syncytial virus in beef cattle in China. Animals, 12, 3511. https://doi.org/10.3390/ani12243511
- Ellis, J. (2013). Bovine respiratory syncytial virus. In: Munir M. (ed), Mononegaviruses of Veterinary Importance: Pathobiology and Molecular Diagnosis (pp.117-140). CPI Group.
- İnce, Ö.B., Şevik, M., Özgür, E.G., & Sait A. (2022). Risk factors and genetic characterization of bovine respiratory syncytial virus in the inner Aegean Region, Turkey. Tropical Animal Health and Production, 54, 4. https://doi.org/10.1007/s11250-021-03022-5.
- Jia, S., Yao, X., Yang, Y., Niu, C., Zhao, Y., Zhang, X., Pan, R., Jiang, X., Xiaobo, S., Qiao, X., Guan, X., & Xu, Y. (2021). Isolation, identification, and phylogenetic analysis of subgroup III strain of bovine respiratory syncytial virus contributed to outbreak of acute respiratory disease among cattle in Northeast China. Virulence, 12, 404-414. https://doi.org/10.1080/21505594.2021.1872178
- Karayel-Hacıoğlu, I., Coşkun, N., Duran-Yelken, S., Sevinç, S., & Alkan, F. (2019). Phylogenetic analysis of bovine respiratory syncytial virus from calves with respiratory disorders. Kafkas Universitesi Veteriner Fakultesi Dergisi. 25, 251-256. https://doi.org/ 10.9775/kvfd.2018.20819
- Klem, T.B., Rimstad, E., & Stokstad, M. (2014). Occurrence and phylogenetic analysis of bovine respiratory syncytial virus in outbreaks of respiratory disease in Norway. BMC Veterinary Research, 10, 15. https://doi.org/10.1186/1746-6148-10-15
- Kresic, N., Bedekovic, T., Brnic, D., Simic, I., Lojkic, I., & Turk, N. (2018). Genetic analysis of bovine respiratory syncytial virus in Crotia. Comparative Immunology. Microbiology and Infectious Diseases, 58, 52-57. https://doi.org/10.1016/j.cimid.2018.09.004.
- Kumagai, A., Kawauchi, K., Andoh, K., & Hatama, S. (2021). Sequence and unique phylogeny of G genes of bovine respiratory syncytial viruses circulating in Japan, Journal of Veterinary Diagnosis Investigation 33, 162-166. https://doi.org/10.1177/1040638720975364.
- Kumar, S., Stecher, G., Li, M., Knyaz, C., & Tamura, K. (2018). Mega X: Molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evoluation, 35, 1547-1549.
- Küçük, A., & Yıldırım, Y. (2022). Antigenic and histopathologic evaluation, with molecular characterization and identification of BPIV3 in cattle with respiratory system infections. Large Animal Review, 28, 123-130.
- Langedijk, J.P.M., Meloen, R.H., Taylor, G., Furze, J.M., & van Oirschot, J.T. (1997). Antigenic structure of the central conserved region of protein G of bovine respiratory syncytial virus. Journal of Virology, 71, 4055-4061. https://doi.org/10.1128/JVI.71.5.4055-4061.1997.
- Larsen, L.E. (2000). Bovine respiratory syncytial virus (BRSV): a review. Acta Veterinary Scandinavia, 41, 4055–4061. https://doi.org/10.1186/BF03549652.
- Larsson, A. (2014). AliView: a fast and lightweight alignment viewer and editor for large datasets. Bioinformation, 30, 3276–3278. https://doi.org/10.1093/bioinformatics/btu531
- Leme, R.A., Agnol, A.M.D., Balbo, L.C., Pereira, F.L., Possatti, F., Alfieri, A.F., & Alfieri, A.A. (2020). Molecular characterization of Brazilian wild-type strains of bovine respiratory syncytial virus reveals genetic diversity and a putative new subgroup of the virus. Veterinary Quartely, 40, 83-96. https://doi.org/10.1080/01652176.2020.1733704
- Maclachlan, N.J., Dubovi, E.J., Barthold, S.W., Swayne, D.E., & Winton, J.R. (2017). Paramyxoviridae and Pneumoviridae. In: Maclachlan NJ, Dubovi EJ (Eds.), Fenner’s Veterinary Virology 5th ed. (pp. 327-356.). Elsevier Inc. https://doi.org/10.1016/B978-0-12-800946-8.00017-9Get rights and content
- Mitarai, S., Okuya, K., Miyane, K., Miyamoto, M., Ishikawa, S., Kawaguchi, H., Hatazoe, I., Suda, Y., Arima, E., Nakazato, H., Hobo, S., Matasani, T., & Ozawa, M. (2023). Genetic characterization of bovine respiratory syncytial viruses in Japan between 2017 and 2019. Archive of Virology, 168, 51. https://doi.org/10.1007/s00705-022-05670-w.
- Nath, S.R., Keshaw, T., Samantha, W., McKayla, D.V., Cassandra, T.W., & Claude, D. (2017). Detection of antibodies against bovine respiratory syncytial virus in ruminants of Grenada, West Indies. Journal of Animal Research, 7, 223-226. https://doi.org/10.5958/2277-940X.2017.00033.X
- Ohlson, A., Emanuelson, U., Traven, M., & Alenius, S. (2010). The relationship between antibody status to bovine corona virus and bovine respiratory syncytial virus and disease incidence, reproduction and herd characteristics in dairy herds. Acta Veterinary Scandinavia, 52, 37. https://doi.org/10.1186/1751-0147-52-37
- Postler, T.S., Brown, P.A., Buchholz, U.J., de Swart, R.L., Drexler, J.F., Duprex, P.W., Easton, A.J., Lǐ, J., Spann, K.M., Thornburg, N.J., van den Hoogen, B., Williams, J.V., & Kuhn, J.H. (2021). Rename all species in the family to comply with the ICTV-mandated binomial format (Mononegavirales: Pneumoviridae). ICTV, Access Date: 14.10.2024. https://ictv.global/taxonomy/taxondetails?taxnode_id=202301650&taxon_name=Orthopneumovirus%20bovis
- Rima, B., Collins, P., Easton, A., Fouchier, R., Kurath, G., Lamb, R.A., Lee, B., Maisner, A., Rota, P., & Wang, L. (2017). ICTV Virus Taxonomy Profile: Pneumoviridae. Journal of General Virology, 98, 2912–2913. https://doi.org/10.1099/jgv.0.000959.
- Rio, D.C., Ares Jr, M., Hannon, G.J., & Nilsen T.W. (2010). Purification of RNA Using TRIzol (TRI Reagent). Cold Spring Harb Protoc. https://doi.org/10.1101/pdb.prot5439.
- Schmidt, U., Breyer, J., Polster, U., Gershwin, L.J., & Buchholz, U. (2002). Mucosal immunization with live recombinant bovine respiratory syncytial virus (BRSV) and recombinant BRSV lacking the envelope glycoprotein G protects against challenge with wild-type BRSV. Journal of Virology, 76, 12355–12359.
- Schreiber, P., Matheise, J.P., Dessy, F., Heimann, M., Letesson, J.J., Coppe, P., & Collard, A. (2000). High mortality rate associated with bovine respiratory syncytial virus (BRSV) infection in Belgian white blue calves previously vaccinated with an inactivated vaccine. Journal of Veterinary Medicine B Infectious Diseases and Veterinary Public Health, 47, 535–550. https://doi.org/10.1046/j.1439-0450.2000.00380.x
- Sermiento-Silva, R.E., Nakamura-Lopez, Y., & Vaughan, G. (2012). Epidemiology, molecular epidemiology and evolution of bovine respiratory syncytial virus. Viruses, 4, 3452-3467. https://doi.org/10.3390/v4123452.
- Socha, W., Larska, M., & Rola, J. (2009). Molecular characterisation of the first polish isolates of bovine respiratory syncytial virus. Bulletin of the Veterinary Institute in Pulawy. 53, 569-574.
- Spilki, F.R., Almeida, R.S., Domingues, H.G., D’Arce, R.C.F., Ferreira, H.L., & Campalans, J. (2006). Phylogenetic relationships of Brazilian bovine respiratory syncytial virus isolates and molecular homology modeling of attachment glycoprotein. Virus Research, 116, 30-37. https://doi.org/10.1016/j.virusres.2005.08.010.
- Timurkan, M. O., Aydin, H., & Sait, A. (2019). Identification and molecular characterisation of bovine parainfluenza virus-3 and bovine respiratory syncytial virus-first report from Turkey. Journal of Veterinary Research, 63(2), 167-173.
- Valarcher, J.F., & Taylor, G. (2007). Bovine respiratory syncytial virus infection. Veterinary Research, 38, 153–180. https://doi.org/10.1051/vetres:2006053
- Valarcher, J.F., Schelcher, F., & Bourhy, H. (2000). Evolution of bovine respiratory syncytial virus. Journal of Virology, 74, 10714–10728. https://doi.org/10.1128/jvi.74.22.10714-10728.2000.
- Vilcek, S., Elvander, M., Ballagi-Pordany, A., & Belak, S. (1994). Development of nested PCR assays for detection of bovine respiratory syncytial virus in clinical samples. Journal of Clinical Microbiology, 32, 2225–2231. https://doi.org/10.1128/jcm.32.9.2225-2231.1994
- Yaegashi, G., Seimiya, Y.M., Seki, Y., & Tsunemitsu, H. (2005). Genetic and antigenic analyses of bovine respiratory syncytial virus detected in Japan. The Journal of Veterinary Medicine Science, 67, 145-150. https://doi.org/10.1292/jvms.67.145.
- Yaman, T., Büyükbayram, H., Özyıldız, Z., Terzi, F., Uyar, A., Keles, Ö.F., Özsoy, Ş.Y., & Yener, Z. (2018). Detection of bovine respiratory syncytial virus, pasteurella multocida, and mannheimia haemolytica by immunohistochemical method in naturally-infected cattle. Journal of Veterinary Research, 62, 439-445. https://doi.org/10.2478/jvetres-2018-0070.
- Yazıcı, Z., Ozan, E., Tamer, C., Muftuoglu, B., Barry, G., Kurucay, H.N., Elhag, A.E., Cagirgan, A.A., Gumusova, S., & Albayrak, H. (2020). Circulation of Indigenous Bovine Respiratory Syncytial Virus Strains in Turkish Cattle: The First Isolation and Molecular Characterization. Animals, 10, 1700. https://doi.org/10.3390/ani10091700.
Phylogenetic Analysis and Genetic Characterization of Bovine Respiratory Syncytial Virus G Glycoprotein
Yıl 2024,
Cilt: 3 Sayı: 2, 32 - 39, 23.12.2024
Ali Küçük
,
Özge Sevinç Korkmaz Akar
,
Yakup Yıldırım
,
Kamil Atlı
Öz
Bu araştırmada solunum sistemi enfeksiyonu klinik bulguları gösteren sığırlarda Bovine Respiratory Syncytial Virus (BRSV)’ un moleküler tespiti ve tespit edilen lokal suşların filogenetik analizlerinin gerçekleştirilmesi hedeflenmiştir. Etken tespiti için 96 sığırdan toplanan nazal sürüntü örneklerine spesifik primer setleri kullanılarak Reverz Transkriptaz-nested PCR (RT-nPCR) yöntemi uygulanmıştır. Uygulanan moleküler teknikler sonucunda % 2.08 (2/96) oranında viral nükleik asit tespiti gerçekleştirildi. Bununla birlikte tespit edilen lokal suşların sekans ve filogenetik analizleri gerçekleştirilerek Türkiye ve Dünya’nın farklı bölgelerinden tespit edilmiş farklı BRSV suşları ile karşılaştırmaları yapıldı. Elde edilen genetik verilerden, bu çalışmada tespit edilen izolatların, Türkiye, Fransa ve ABD’ nin farklı bölgelerinden bildirilen BRSV suşları ile birlikte, Subgrup III içerisinde yer aldığı belirlenmiştir. Ayrıca izolatların immünodominant G glikoprotein bölgesinde immünolojik açıdan önemli nokta mutasyonları tespit edilmiştir (Asn(N)179 → Asp(D) / Ala(A) 205 → Thr (T)). Bu sonuç, sığırlar arasında dolaşan BRSV suşlarının patojenitelerini kaybetmeden konak bağışıklık sisteminden kaçabildiklerini ve sığırlarda solunum sistemi enfeksiyon salgınlarına neden olabilecek önemli faktörlerden biri olarak değerlendirilmiştir.
Kaynakça
- Bertolotti, L., Giammarioli, M., & Rosati, S. (2018). Genetic characterization of bovine respiratory syncytial virus strains isolated in Italy: evidence fort he circulation of new divergent clades. Journal of Veterinary Diagnostic Investigation, 30, 300-304. https://doi.org/ 10.1177/1040638717746202.
- Bidokhti, M.R.M., Traven, M., Ohlson, A., Zarnegar, B., Baule, C., Belak, S., Alenius, S., & Liu, L. (2012). Phylogenetic analysis of bovine respiratory syncytial viruses from recent outbreaks in feedlot and dairy cattle herds. Archive of Virology, 157, 601-607. https://doi.org/ 10.1007/s00705-011-1209-3
- Chang, Y., Yue, H., & Tang, C. (2022). Prevalence and molecular characteristics of bovine respiratory syncytial virus in beef cattle in China. Animals, 12, 3511. https://doi.org/10.3390/ani12243511
- Ellis, J. (2013). Bovine respiratory syncytial virus. In: Munir M. (ed), Mononegaviruses of Veterinary Importance: Pathobiology and Molecular Diagnosis (pp.117-140). CPI Group.
- İnce, Ö.B., Şevik, M., Özgür, E.G., & Sait A. (2022). Risk factors and genetic characterization of bovine respiratory syncytial virus in the inner Aegean Region, Turkey. Tropical Animal Health and Production, 54, 4. https://doi.org/10.1007/s11250-021-03022-5.
- Jia, S., Yao, X., Yang, Y., Niu, C., Zhao, Y., Zhang, X., Pan, R., Jiang, X., Xiaobo, S., Qiao, X., Guan, X., & Xu, Y. (2021). Isolation, identification, and phylogenetic analysis of subgroup III strain of bovine respiratory syncytial virus contributed to outbreak of acute respiratory disease among cattle in Northeast China. Virulence, 12, 404-414. https://doi.org/10.1080/21505594.2021.1872178
- Karayel-Hacıoğlu, I., Coşkun, N., Duran-Yelken, S., Sevinç, S., & Alkan, F. (2019). Phylogenetic analysis of bovine respiratory syncytial virus from calves with respiratory disorders. Kafkas Universitesi Veteriner Fakultesi Dergisi. 25, 251-256. https://doi.org/ 10.9775/kvfd.2018.20819
- Klem, T.B., Rimstad, E., & Stokstad, M. (2014). Occurrence and phylogenetic analysis of bovine respiratory syncytial virus in outbreaks of respiratory disease in Norway. BMC Veterinary Research, 10, 15. https://doi.org/10.1186/1746-6148-10-15
- Kresic, N., Bedekovic, T., Brnic, D., Simic, I., Lojkic, I., & Turk, N. (2018). Genetic analysis of bovine respiratory syncytial virus in Crotia. Comparative Immunology. Microbiology and Infectious Diseases, 58, 52-57. https://doi.org/10.1016/j.cimid.2018.09.004.
- Kumagai, A., Kawauchi, K., Andoh, K., & Hatama, S. (2021). Sequence and unique phylogeny of G genes of bovine respiratory syncytial viruses circulating in Japan, Journal of Veterinary Diagnosis Investigation 33, 162-166. https://doi.org/10.1177/1040638720975364.
- Kumar, S., Stecher, G., Li, M., Knyaz, C., & Tamura, K. (2018). Mega X: Molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evoluation, 35, 1547-1549.
- Küçük, A., & Yıldırım, Y. (2022). Antigenic and histopathologic evaluation, with molecular characterization and identification of BPIV3 in cattle with respiratory system infections. Large Animal Review, 28, 123-130.
- Langedijk, J.P.M., Meloen, R.H., Taylor, G., Furze, J.M., & van Oirschot, J.T. (1997). Antigenic structure of the central conserved region of protein G of bovine respiratory syncytial virus. Journal of Virology, 71, 4055-4061. https://doi.org/10.1128/JVI.71.5.4055-4061.1997.
- Larsen, L.E. (2000). Bovine respiratory syncytial virus (BRSV): a review. Acta Veterinary Scandinavia, 41, 4055–4061. https://doi.org/10.1186/BF03549652.
- Larsson, A. (2014). AliView: a fast and lightweight alignment viewer and editor for large datasets. Bioinformation, 30, 3276–3278. https://doi.org/10.1093/bioinformatics/btu531
- Leme, R.A., Agnol, A.M.D., Balbo, L.C., Pereira, F.L., Possatti, F., Alfieri, A.F., & Alfieri, A.A. (2020). Molecular characterization of Brazilian wild-type strains of bovine respiratory syncytial virus reveals genetic diversity and a putative new subgroup of the virus. Veterinary Quartely, 40, 83-96. https://doi.org/10.1080/01652176.2020.1733704
- Maclachlan, N.J., Dubovi, E.J., Barthold, S.W., Swayne, D.E., & Winton, J.R. (2017). Paramyxoviridae and Pneumoviridae. In: Maclachlan NJ, Dubovi EJ (Eds.), Fenner’s Veterinary Virology 5th ed. (pp. 327-356.). Elsevier Inc. https://doi.org/10.1016/B978-0-12-800946-8.00017-9Get rights and content
- Mitarai, S., Okuya, K., Miyane, K., Miyamoto, M., Ishikawa, S., Kawaguchi, H., Hatazoe, I., Suda, Y., Arima, E., Nakazato, H., Hobo, S., Matasani, T., & Ozawa, M. (2023). Genetic characterization of bovine respiratory syncytial viruses in Japan between 2017 and 2019. Archive of Virology, 168, 51. https://doi.org/10.1007/s00705-022-05670-w.
- Nath, S.R., Keshaw, T., Samantha, W., McKayla, D.V., Cassandra, T.W., & Claude, D. (2017). Detection of antibodies against bovine respiratory syncytial virus in ruminants of Grenada, West Indies. Journal of Animal Research, 7, 223-226. https://doi.org/10.5958/2277-940X.2017.00033.X
- Ohlson, A., Emanuelson, U., Traven, M., & Alenius, S. (2010). The relationship between antibody status to bovine corona virus and bovine respiratory syncytial virus and disease incidence, reproduction and herd characteristics in dairy herds. Acta Veterinary Scandinavia, 52, 37. https://doi.org/10.1186/1751-0147-52-37
- Postler, T.S., Brown, P.A., Buchholz, U.J., de Swart, R.L., Drexler, J.F., Duprex, P.W., Easton, A.J., Lǐ, J., Spann, K.M., Thornburg, N.J., van den Hoogen, B., Williams, J.V., & Kuhn, J.H. (2021). Rename all species in the family to comply with the ICTV-mandated binomial format (Mononegavirales: Pneumoviridae). ICTV, Access Date: 14.10.2024. https://ictv.global/taxonomy/taxondetails?taxnode_id=202301650&taxon_name=Orthopneumovirus%20bovis
- Rima, B., Collins, P., Easton, A., Fouchier, R., Kurath, G., Lamb, R.A., Lee, B., Maisner, A., Rota, P., & Wang, L. (2017). ICTV Virus Taxonomy Profile: Pneumoviridae. Journal of General Virology, 98, 2912–2913. https://doi.org/10.1099/jgv.0.000959.
- Rio, D.C., Ares Jr, M., Hannon, G.J., & Nilsen T.W. (2010). Purification of RNA Using TRIzol (TRI Reagent). Cold Spring Harb Protoc. https://doi.org/10.1101/pdb.prot5439.
- Schmidt, U., Breyer, J., Polster, U., Gershwin, L.J., & Buchholz, U. (2002). Mucosal immunization with live recombinant bovine respiratory syncytial virus (BRSV) and recombinant BRSV lacking the envelope glycoprotein G protects against challenge with wild-type BRSV. Journal of Virology, 76, 12355–12359.
- Schreiber, P., Matheise, J.P., Dessy, F., Heimann, M., Letesson, J.J., Coppe, P., & Collard, A. (2000). High mortality rate associated with bovine respiratory syncytial virus (BRSV) infection in Belgian white blue calves previously vaccinated with an inactivated vaccine. Journal of Veterinary Medicine B Infectious Diseases and Veterinary Public Health, 47, 535–550. https://doi.org/10.1046/j.1439-0450.2000.00380.x
- Sermiento-Silva, R.E., Nakamura-Lopez, Y., & Vaughan, G. (2012). Epidemiology, molecular epidemiology and evolution of bovine respiratory syncytial virus. Viruses, 4, 3452-3467. https://doi.org/10.3390/v4123452.
- Socha, W., Larska, M., & Rola, J. (2009). Molecular characterisation of the first polish isolates of bovine respiratory syncytial virus. Bulletin of the Veterinary Institute in Pulawy. 53, 569-574.
- Spilki, F.R., Almeida, R.S., Domingues, H.G., D’Arce, R.C.F., Ferreira, H.L., & Campalans, J. (2006). Phylogenetic relationships of Brazilian bovine respiratory syncytial virus isolates and molecular homology modeling of attachment glycoprotein. Virus Research, 116, 30-37. https://doi.org/10.1016/j.virusres.2005.08.010.
- Timurkan, M. O., Aydin, H., & Sait, A. (2019). Identification and molecular characterisation of bovine parainfluenza virus-3 and bovine respiratory syncytial virus-first report from Turkey. Journal of Veterinary Research, 63(2), 167-173.
- Valarcher, J.F., & Taylor, G. (2007). Bovine respiratory syncytial virus infection. Veterinary Research, 38, 153–180. https://doi.org/10.1051/vetres:2006053
- Valarcher, J.F., Schelcher, F., & Bourhy, H. (2000). Evolution of bovine respiratory syncytial virus. Journal of Virology, 74, 10714–10728. https://doi.org/10.1128/jvi.74.22.10714-10728.2000.
- Vilcek, S., Elvander, M., Ballagi-Pordany, A., & Belak, S. (1994). Development of nested PCR assays for detection of bovine respiratory syncytial virus in clinical samples. Journal of Clinical Microbiology, 32, 2225–2231. https://doi.org/10.1128/jcm.32.9.2225-2231.1994
- Yaegashi, G., Seimiya, Y.M., Seki, Y., & Tsunemitsu, H. (2005). Genetic and antigenic analyses of bovine respiratory syncytial virus detected in Japan. The Journal of Veterinary Medicine Science, 67, 145-150. https://doi.org/10.1292/jvms.67.145.
- Yaman, T., Büyükbayram, H., Özyıldız, Z., Terzi, F., Uyar, A., Keles, Ö.F., Özsoy, Ş.Y., & Yener, Z. (2018). Detection of bovine respiratory syncytial virus, pasteurella multocida, and mannheimia haemolytica by immunohistochemical method in naturally-infected cattle. Journal of Veterinary Research, 62, 439-445. https://doi.org/10.2478/jvetres-2018-0070.
- Yazıcı, Z., Ozan, E., Tamer, C., Muftuoglu, B., Barry, G., Kurucay, H.N., Elhag, A.E., Cagirgan, A.A., Gumusova, S., & Albayrak, H. (2020). Circulation of Indigenous Bovine Respiratory Syncytial Virus Strains in Turkish Cattle: The First Isolation and Molecular Characterization. Animals, 10, 1700. https://doi.org/10.3390/ani10091700.