Research Article
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High mortality rate of shipping fever cases in cattle caused by bovine herpesvirus type 1 (BoHV-1)

Year 2022, Volume: 69 Issue: 1, 69 - 75, 01.01.2022

Eda Baldan Toker , Kadir Yeşilbağ , Özer Ateş Berfin Kadiroğlu , Gizem Aytoğu

https://doi.org/10.33988/auvfd.834671

Abstract

This study reports the high prevalence and molecular characterization of BoHV-1 infection in imported cattle with respiratory system disease after international transport. A high mortality rate of 14.16% (51/360) was reported in a group of animals imported from Hungary to Turkey in 2019. A total of 17 samples were evaluated (3 lung tissue and 14 nasal swab samples) from 15 cattle aged 6 to 9 months not vaccinated against BoHV-1. Virus isolation, polymerase chain reaction (PCR) and restriction endonuclease analysis (REA) procedures were performed within the scope of this study. By virus isolation in MDBK cells, cytopathologic effects was detected in 8 samples (3 lung tissue and 5 nasal swabs samples). The same eight samples were also found positive by BoHV-1 PCR targeting gC (UL44) gene region. According to the sequencing result, the sample (ID: 10054) dropped into a cluster of BoHV-1.1. The REA was applied to the samples to confirm the results of phylogenetic analysis. All of the isolates were identified in the subgroup BoHV-1.1 by REA. These results showed a high mortality risk for imported animals and the possibility for BoHV-1 entering the receiving country via imported animals after transport. This event is a serious problem both for the control of BoHV-1 as well as for animal health and welfare. 

Keywords

Animal transport BoHV-1 PCR Sequencing shipping fever

Supporting Institution

Bursa Uludağ University

Project Number

OUAP(V)-2020/7

Thanks

Dr. E.B. Toker is granted for postdoc position by Turkish Scientific and Technological Research Council (TUBİTAK) Project No: 119 O 571.

References

  • Ackermann M, Engels M (2006): Pro and contra IBR-eradication. Vet Microbiol, 113, 293–302.
  • Autio T, Pohjanvirta T, Holopainen R, et al (2007): Etiology of respiratory disease in non-vaccinated, non-medicated calves in rearing herds. Vet Microbiol, 119, 256–265.
  • Benavides B, Casal J, Diéguez JF, et al (2020): Development of a quantitative risk assessment of bovine viral diarrhea virus and bovine herpesvirus-1 introduction in dairy cattle herds to improve biosecurity. J Dairy Sci, 103, 6454–6472.
  • Bilge-Dagalp S, Farzani TA, Dogan F, et al (2020): Molecular and antigenic characterization of bovine herpesvirus type 1 (BoHV-1) strains from cattle with diverse clinical cases in Turkey. Trop Anim Health Prod, 52, 555–564.
  • Boelaert F, Biront P, Soumare B, et al (2020): Prevalence of bovine herpesvirus-1 in the Belgian cattle population. Prev Vet Med, 45, 285–295.
  • Burgu I, Akca Y (1987): First isolation of IBR virus in Turkey. Trop Anim Health Prod, 19, 56.
  • Carter JJ, Weinberg AD, Pollard A, et al (1989): Inhibition of T-lymphocyte mitogenic responses and effects on cell functions by bovine herpesvirus 1. J Virol, 63, 1525–1530.
  • Chirase NK, Greene LW, Purdy CW, et al (2004): Effect of transport stress on respiratory disease, serum antioxidant status, and serum concentrations of lipid peroxidation biomarkers in beef cattle American. J Vet Res, 65, 860–864.
  • Cho KO, Hasoksuz M, Nielsen PR, et al (2001): Cross-protection studies between respiratory and calf diarrhea and winter dysentery coronavirus strains in calves and RT-PCR and nested PCR for their detection. Arch Virol, 146, 2401-2419.
  • Cowley RE, Holland PL (2011): C-H activation by a terminal imidoiron (III) complex to form a cyclopentadienyliron (II) product. Inorganica Chim Acta, 369, 40–44.
  • Esteves P, Dellagostin O, Pinto L, et al (2008): Phylogenetic comparison of the carboxy-terminal region of glycoprotein C (gC) of bovine herpesviruses (BoHV) 1.1, 1.2 and 5 from South America (SA). Virus Res, 131, 16–22.
  • Hinkley S, Hill AB, Srikumaran S (1998): Bovine herpesvirus-1 infection affects the peptide transport activity in bovine cells. Virus Res, 53, 91–96.
  • International Committee on Taxonomy of Viruses (2019): Virus Taxonomy: 2019 Release. Available at https://talk.ictvonline.org/taxonomy/ (Accessed January 20, 2021).
  • Jacevičius E, Šalomskas A, Milius J, et al (2008): Prevalence and control measures of infectious bovine rhinotracheitis in Lithuania. Anim Heal, 1, 49–53.
  • Jones C, Chowdhury S (2010): Bovine herpesvirus type 1 (BHV-1) is an important cofactor in the bovine respiratory disease complex. Vet Clin North Am-Food Anim Pract, 26, 303–321.
  • Kent JE, Ewbank R (1983): The effect of road transportation on the blood constituents and behaviour of calves. I. six months old. Br Vet J, 139, 228–235.
  • Maidana SS, Miño S, Apostolo RM, et al (2020): A new molecular method for the rapid subtyping of bovine herpesvirus 1 field isolates. J Vet Diagnostic Investig, 32, 112–117.
  • Msolla PM, Wiseman A, Selman IE (1981): The prevalence of serum neutralizing antibodies to infectious bovine rhinotracheitis virus in Scotland. J Hyg, 86, 209–215.
  • Muylkens B, Thiry J, Kirten P, et al (2007): Bovine herpesvirus 1 infection and infectious bovine rhinotracheitis. Vet Res, 38, 181–209.
  • Nandi S, Kumar M, Manohar M, et al (2009): Bovine herpes virus infections in cattle. Anim Heal Res Rev, 10, 86-98.
  • OIE (2017): Infectious bovine rhinotracheitis/ Infectious pustular vulvovaginitis, 1-19. In: OIE Terrestrial Manual.
  • Öner EB, Yeşilbağ K (2018): Seroprevalance of respiratory viruses and detection of persistent BVD virus infection in beef cattle (in Turkish). Ankara Univ Vet Fak Derg, 65, 1–7.
  • Rebuplic of Turkey Ministry of Agriculture and Forestry (2020): Hayvan ve Hayvan Maddeleri Sağlık Sertifikaları (İthalat). Available at https://www.tarimorman. gov.tr/Konular/Veteriner-Hizmetleri/Ihracat-Ithalat/ Ithalat? Ziyaretci=Ihracat-Ithalat. (Accessed January 20, 2021).
  • Rice JA, Carrasco-Medina L, Hodgins DC, et al (2008): Mannheimia haemolytica and bovine resiratory disease. Anim Heal Res Rev, 8, 117–128.
  • Rijsewijk FAM, Kaashoek MJ, Langeveld, JPM, et al (1999): Epitopes on glycoprotein C of bovine herpesvirus-1 (BHV-1) that allow differentiation between BHV-1.1 and BHV-1.2 strains. J Gen Virol, 80, 1477-1483.
  • Tekes L, Markos B, Kecskeméti S, et al (1999): Prevalence of bovine herpesvirus 1 (BHV-1) infection in Hungarian cattle herds. Acta Vet Hung, 47, 303-309.
  • Thiry E, Saliki J, Bublot M, et al (1987): Reactivation of infectious bovine rhinotracheitis virus by transport. Comp Immunol Microbiol Infect Dis, 10, 59-63.
  • Toker EB, Yeşilbağ K (2021): Molecular characterization and comparison of diagnostic methods for bovine respiratory viruses (BPIV-3, BRSV, BVDV, and BoHV-1) in field samples in northwestern Turkey. Trop Anim Health Prod, 53, 1-11.
  • Townley M (1971). Economic loss from an acute IBR outbreak in a dairy herd. Mod Vet Pract, 52, 72–73.
  • Tuncer-Göktuna P, Alpay G, Öner EB, et al (2016): The role of herpesviruses (BoHV-1 and BoHV-4) and pestiviruses (BVDV and BDV) in ruminant abortion cases in western Turkey. Trop Anim Health Prod, 48, 1–6.
  • Turkish Statistical Institute (2019): Dış Ticaret İstatistikleri Ara Malı İthalatı. Available at https://www.tuik.gov.tr/. (Accessed August 20, 2020).
  • Winkler MTC, Doster A, Jones C (1999): Bovine herpesvirus 1 can infect CD4+ t lymphocytes and induce programmed cell death during acute infection of cattle. J Virol, 73, 8657–8668.
  • Winkler MTC, Doster A, Jones C (2000): Persistence and reactivation of bovine herpesvirus 1 in the tonsils of latently infected calves. J Virol, 74, 5337–5346.
  • Yagi Y, Shiono H, Chikayama Y, et al (2004): Transport stress increases somatic cell counts in milk, and enhances the migration capacity of peripheral blood neutrophils of dairy cows. J Vet Med Sci, 66, 381–387.
  • Yates WDG (1982): A review of infectious bovine rhinotracheitis, shipping fever pneumonia and viral-bacterial synergism in respiratory disease of cattle. Can J Comp Med, 46, 225-263.
  • Yeşilbağ K, Güngör B (2008): Seroprevalence of bovine respiratory viruses in North-Western Turkey. Trop Anim Health Prod, 40, 55-60.

Year 2022, Volume: 69 Issue: 1, 69 - 75, 01.01.2022

Eda Baldan Toker , Kadir Yeşilbağ , Özer Ateş Berfin Kadiroğlu , Gizem Aytoğu

https://doi.org/10.33988/auvfd.834671

Abstract

Project Number

OUAP(V)-2020/7

References

  • Ackermann M, Engels M (2006): Pro and contra IBR-eradication. Vet Microbiol, 113, 293–302.
  • Autio T, Pohjanvirta T, Holopainen R, et al (2007): Etiology of respiratory disease in non-vaccinated, non-medicated calves in rearing herds. Vet Microbiol, 119, 256–265.
  • Benavides B, Casal J, Diéguez JF, et al (2020): Development of a quantitative risk assessment of bovine viral diarrhea virus and bovine herpesvirus-1 introduction in dairy cattle herds to improve biosecurity. J Dairy Sci, 103, 6454–6472.
  • Bilge-Dagalp S, Farzani TA, Dogan F, et al (2020): Molecular and antigenic characterization of bovine herpesvirus type 1 (BoHV-1) strains from cattle with diverse clinical cases in Turkey. Trop Anim Health Prod, 52, 555–564.
  • Boelaert F, Biront P, Soumare B, et al (2020): Prevalence of bovine herpesvirus-1 in the Belgian cattle population. Prev Vet Med, 45, 285–295.
  • Burgu I, Akca Y (1987): First isolation of IBR virus in Turkey. Trop Anim Health Prod, 19, 56.
  • Carter JJ, Weinberg AD, Pollard A, et al (1989): Inhibition of T-lymphocyte mitogenic responses and effects on cell functions by bovine herpesvirus 1. J Virol, 63, 1525–1530.
  • Chirase NK, Greene LW, Purdy CW, et al (2004): Effect of transport stress on respiratory disease, serum antioxidant status, and serum concentrations of lipid peroxidation biomarkers in beef cattle American. J Vet Res, 65, 860–864.
  • Cho KO, Hasoksuz M, Nielsen PR, et al (2001): Cross-protection studies between respiratory and calf diarrhea and winter dysentery coronavirus strains in calves and RT-PCR and nested PCR for their detection. Arch Virol, 146, 2401-2419.
  • Cowley RE, Holland PL (2011): C-H activation by a terminal imidoiron (III) complex to form a cyclopentadienyliron (II) product. Inorganica Chim Acta, 369, 40–44.
  • Esteves P, Dellagostin O, Pinto L, et al (2008): Phylogenetic comparison of the carboxy-terminal region of glycoprotein C (gC) of bovine herpesviruses (BoHV) 1.1, 1.2 and 5 from South America (SA). Virus Res, 131, 16–22.
  • Hinkley S, Hill AB, Srikumaran S (1998): Bovine herpesvirus-1 infection affects the peptide transport activity in bovine cells. Virus Res, 53, 91–96.
  • International Committee on Taxonomy of Viruses (2019): Virus Taxonomy: 2019 Release. Available at https://talk.ictvonline.org/taxonomy/ (Accessed January 20, 2021).
  • Jacevičius E, Šalomskas A, Milius J, et al (2008): Prevalence and control measures of infectious bovine rhinotracheitis in Lithuania. Anim Heal, 1, 49–53.
  • Jones C, Chowdhury S (2010): Bovine herpesvirus type 1 (BHV-1) is an important cofactor in the bovine respiratory disease complex. Vet Clin North Am-Food Anim Pract, 26, 303–321.
  • Kent JE, Ewbank R (1983): The effect of road transportation on the blood constituents and behaviour of calves. I. six months old. Br Vet J, 139, 228–235.
  • Maidana SS, Miño S, Apostolo RM, et al (2020): A new molecular method for the rapid subtyping of bovine herpesvirus 1 field isolates. J Vet Diagnostic Investig, 32, 112–117.
  • Msolla PM, Wiseman A, Selman IE (1981): The prevalence of serum neutralizing antibodies to infectious bovine rhinotracheitis virus in Scotland. J Hyg, 86, 209–215.
  • Muylkens B, Thiry J, Kirten P, et al (2007): Bovine herpesvirus 1 infection and infectious bovine rhinotracheitis. Vet Res, 38, 181–209.
  • Nandi S, Kumar M, Manohar M, et al (2009): Bovine herpes virus infections in cattle. Anim Heal Res Rev, 10, 86-98.
  • OIE (2017): Infectious bovine rhinotracheitis/ Infectious pustular vulvovaginitis, 1-19. In: OIE Terrestrial Manual.
  • Öner EB, Yeşilbağ K (2018): Seroprevalance of respiratory viruses and detection of persistent BVD virus infection in beef cattle (in Turkish). Ankara Univ Vet Fak Derg, 65, 1–7.
  • Rebuplic of Turkey Ministry of Agriculture and Forestry (2020): Hayvan ve Hayvan Maddeleri Sağlık Sertifikaları (İthalat). Available at https://www.tarimorman. gov.tr/Konular/Veteriner-Hizmetleri/Ihracat-Ithalat/ Ithalat? Ziyaretci=Ihracat-Ithalat. (Accessed January 20, 2021).
  • Rice JA, Carrasco-Medina L, Hodgins DC, et al (2008): Mannheimia haemolytica and bovine resiratory disease. Anim Heal Res Rev, 8, 117–128.
  • Rijsewijk FAM, Kaashoek MJ, Langeveld, JPM, et al (1999): Epitopes on glycoprotein C of bovine herpesvirus-1 (BHV-1) that allow differentiation between BHV-1.1 and BHV-1.2 strains. J Gen Virol, 80, 1477-1483.
  • Tekes L, Markos B, Kecskeméti S, et al (1999): Prevalence of bovine herpesvirus 1 (BHV-1) infection in Hungarian cattle herds. Acta Vet Hung, 47, 303-309.
  • Thiry E, Saliki J, Bublot M, et al (1987): Reactivation of infectious bovine rhinotracheitis virus by transport. Comp Immunol Microbiol Infect Dis, 10, 59-63.
  • Toker EB, Yeşilbağ K (2021): Molecular characterization and comparison of diagnostic methods for bovine respiratory viruses (BPIV-3, BRSV, BVDV, and BoHV-1) in field samples in northwestern Turkey. Trop Anim Health Prod, 53, 1-11.
  • Townley M (1971). Economic loss from an acute IBR outbreak in a dairy herd. Mod Vet Pract, 52, 72–73.
  • Tuncer-Göktuna P, Alpay G, Öner EB, et al (2016): The role of herpesviruses (BoHV-1 and BoHV-4) and pestiviruses (BVDV and BDV) in ruminant abortion cases in western Turkey. Trop Anim Health Prod, 48, 1–6.
  • Turkish Statistical Institute (2019): Dış Ticaret İstatistikleri Ara Malı İthalatı. Available at https://www.tuik.gov.tr/. (Accessed August 20, 2020).
  • Winkler MTC, Doster A, Jones C (1999): Bovine herpesvirus 1 can infect CD4+ t lymphocytes and induce programmed cell death during acute infection of cattle. J Virol, 73, 8657–8668.
  • Winkler MTC, Doster A, Jones C (2000): Persistence and reactivation of bovine herpesvirus 1 in the tonsils of latently infected calves. J Virol, 74, 5337–5346.
  • Yagi Y, Shiono H, Chikayama Y, et al (2004): Transport stress increases somatic cell counts in milk, and enhances the migration capacity of peripheral blood neutrophils of dairy cows. J Vet Med Sci, 66, 381–387.
  • Yates WDG (1982): A review of infectious bovine rhinotracheitis, shipping fever pneumonia and viral-bacterial synergism in respiratory disease of cattle. Can J Comp Med, 46, 225-263.
  • Yeşilbağ K, Güngör B (2008): Seroprevalence of bovine respiratory viruses in North-Western Turkey. Trop Anim Health Prod, 40, 55-60.
There are 36 citations in total.

Details

Primary Language English
Subjects Veterinary Surgery
Journal Section Research Article
Authors

Eda Baldan Toker 0000-0003-2468-3945

Kadir Yeşilbağ 0000-0003-1793-6879

Özer Ateş 0000-0001-7676-9033

Berfin Kadiroğlu 0000-0001-5969-6127

Gizem Aytoğu 0000-0002-3411-081X

Project Number OUAP(V)-2020/7
Publication Date January 1, 2022
Published in Issue Year 2022Volume: 69 Issue: 1

Cite

APA Toker, E. B., Yeşilbağ, K., Ateş, Ö., Kadiroğlu, B., et al. (2022). High mortality rate of shipping fever cases in cattle caused by bovine herpesvirus type 1 (BoHV-1). Ankara Üniversitesi Veteriner Fakültesi Dergisi, 69(1), 69-75. https://doi.org/10.33988/auvfd.834671
AMA Toker EB, Yeşilbağ K, Ateş Ö, Kadiroğlu B, Aytoğu G. High mortality rate of shipping fever cases in cattle caused by bovine herpesvirus type 1 (BoHV-1). Ankara Univ Vet Fak Derg. January 2022;69(1):69-75. doi:10.33988/auvfd.834671
Chicago Toker, Eda Baldan, Kadir Yeşilbağ, Özer Ateş, Berfin Kadiroğlu, and Gizem Aytoğu. “High Mortality Rate of Shipping Fever Cases in Cattle Caused by Bovine Herpesvirus Type 1 (BoHV-1)”. Ankara Üniversitesi Veteriner Fakültesi Dergisi 69, no. 1 (January 2022): 69-75. https://doi.org/10.33988/auvfd.834671.
EndNote Toker EB, Yeşilbağ K, Ateş Ö, Kadiroğlu B, Aytoğu G (January 1, 2022) High mortality rate of shipping fever cases in cattle caused by bovine herpesvirus type 1 (BoHV-1). Ankara Üniversitesi Veteriner Fakültesi Dergisi 69 1 69–75.
IEEE E. B. Toker, K. Yeşilbağ, Ö. Ateş, B. Kadiroğlu, and G. Aytoğu, “High mortality rate of shipping fever cases in cattle caused by bovine herpesvirus type 1 (BoHV-1)”, Ankara Univ Vet Fak Derg, vol. 69, no. 1, pp. 69–75, 2022, doi: 10.33988/auvfd.834671.
ISNAD Toker, Eda Baldan et al. “High Mortality Rate of Shipping Fever Cases in Cattle Caused by Bovine Herpesvirus Type 1 (BoHV-1)”. Ankara Üniversitesi Veteriner Fakültesi Dergisi 69/1 (January 2022), 69-75. https://doi.org/10.33988/auvfd.834671.
JAMA Toker EB, Yeşilbağ K, Ateş Ö, Kadiroğlu B, Aytoğu G. High mortality rate of shipping fever cases in cattle caused by bovine herpesvirus type 1 (BoHV-1). Ankara Univ Vet Fak Derg. 2022;69:69–75.
MLA Toker, Eda Baldan et al. “High Mortality Rate of Shipping Fever Cases in Cattle Caused by Bovine Herpesvirus Type 1 (BoHV-1)”. Ankara Üniversitesi Veteriner Fakültesi Dergisi, vol. 69, no. 1, 2022, pp. 69-75, doi:10.33988/auvfd.834671.
Vancouver Toker EB, Yeşilbağ K, Ateş Ö, Kadiroğlu B, Aytoğu G. High mortality rate of shipping fever cases in cattle caused by bovine herpesvirus type 1 (BoHV-1). Ankara Univ Vet Fak Derg. 2022;69(1):69-75.
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