Study of prevalence of equine herpes virus types 1 and 4 infections in horse sera from riding clubs of Urmia
Subject Areas :
Veterinary Clinical Pathology
Amir Shafaroodi
1
(Graduate of Veterinary Medicine, Faculty of Veterinary Medicine, Urmia Branch, Islamic Azad
University, Urmia, Iran.)
Arash Araghi-Sooreh
2
(Associate Professor, Department of Clinical Sciences, Urmia Branch, Islamic Azad University, Urmia,
Iran.)
Received: 2023-02-20
Accepted : 2023-06-14
Published : 2023-04-21
Keywords:
horse,
Urmia,
Equine herpes virus,
indirect ELISA,
Abstract :
Herpesviruses can cause significant economic losses to the equine industry worldwide. Equine herpes virus type 1 (EHV-1) and type 4 (EHV-4) cause respiratory signs, abortion, neonatal death and in some cases distal limb edema and myeloencephalopathy in susceptible horses. The aim of this study was to determine the seroprevalence of EHV-1 and EHV-4 infection in club horses of Urmia in relation to age, gender, breed and clinical signs. Sera from 51 horses were tested by indirect enzyme linked immunosorbent assay (iELISA) for detection of specific antibodies against EHV-1 and EHV-4 and data were analyzed by chi-squared, fisher’s exact and logistic regression tests. A total of 9 samples (17.65%) (95% CI: 7.2-28.0) were found to be positive for specific antibodies of EHV-1 and EHV-4. Seropositivity was not affected by age (p=0.593), sex (p=0.651), breed (p=0.874) and clinical signs (p=0.824). Although in regression analysis it was found that odds of infection based on age was increased by 1.51% for every 4 year decrease in age and odds of infection was 1.549% more in females compared with males. Also age, gender and breed of horses explains 0.449, 0.437 and 0.217% of infection rate fluctuations, respectively. In conclusion, the results indicate relatively high exposure of equine herpes virus types 1 and 4 in club horses of Urmia.
References:
Allen, G.P., Kydd, J.H., Slater, J.D. and Smith, K.C. (2004).Equid herpesvirus-1 (EHV-1) and -4 (EHV-4) infections. In: Coetzer, JAW and Tustin, RC (Eds.), Infectious diseases of livestock. 2nd ed., Chapter 76, Cape Town, Oxford Press, pp: 829-859.
Amer, H.M., Shaltout, A.K., El-Sabagh, I.M., El-Sanousi, A.A. and Shalaby, M.A. (2011). Prevalence of equine herpes viruses 1, 2 and 4 in Arabian horse population in Egypt. African Journal of Microbiology Research, 5(27):4805-4811.
Attari, A. and Araghi-Sooreh, A. (2022). Serological survey of influenza A virus infection in horses of some districts of Mahabad city by ELISA method. Veterinary Clinical Pathology, 15(4): 357-367.[In Persian]
Ataseven, V., Dagalp, S., Guzel, M., Basaran, Z., Tan, M. and Geraghiy, B. (2009) Prevalence of equine herpesvirus-1 and equine herpesvirus-4 infections in equidae species in Turkey as determined by ELISA and multiplex nested PCR. Research in Veterinary Science, 86(2): 339-344.
Avci, O., Yapici, O., Bulut, O., Kale, M. and Atli, K. (2018). Detection of equine herpes virus 1, equine herpes virus 4, and equine arteritis virus antibodies in Kyrgizstan by ELISA. Bionature, 38(3):219-224.
Burgess, B.A., Tokateloff, N., Manning, S., Lohmann, K., Lunn, D.P., Hussey, S.B., et al. (2012). Nasal shedding of equine herpesvirus‐1 from horses in an outbreak of equine herpes myeloencephalopathy in Western Canada. Journal of Veterinary Internal Medicine, 26(2): 384-392.
Cruz, F., Fores, P., Mughini-Gras, L., Ireland, J., Moreno, M.A. and Newton, J.R. (2016). Seroprevalence and factors associated with equine herpesvirus type 1 and 4 in Spanish Purebred horses in Spain. Veterinary Record, 178(16): 398-398.
Derbal, S. (2021). Epidemiology of EHV-1 and EHV-4 infections: A review. International Journal of Veterinary Sciences, 7(2): 108-112.
Damiani, A.M., Vries, M., Reimers, G., Winkler, S. and Osterrieder, N. (2014). A severe equine herpesvirus type 1 (EHV-1) abortion outbreak caused by a neuropathogenic strain at a breeding farm in northern Germany. Veterinary Microbiology, 172(3-4): 555-562.
El Brini, Z., Fassi Fihri, O., Paillot, R., Lotfi, C., Amraoui, F. and El Ouadi, H. (2021). Seroprevalence of equine herpesvirus 1 (EHV-1) and equine herpesvirus 4 (EHV-4) in the northern Moroccan horse populations. Animals, 11(10): 2851.
Getachew, M., Alemayehu, F., Chala, C., Amare, B., Kassa, D., Burden, F., et al. (2014). A cross-sectional sero-survey of some infectious diseases of working equids in Central Ethiopia. Journal of Veterinary Medicine and Animal Health, 6(9): 231-238.
Gharekhani, A. and Morshedi, A. (2010). The study of infection rate to Bovine Herpes Virus–1 (BHV-1) in milk samples of dairy cattle in Urmia and Maku by ELISA method. Veterinary Clinical Pathology, 4(3): 915-921.[In Persian]
Gilkerson, J. R., Whalley, J. M., Drummer, H. E., Studdert, M. J. and Love, D. N. (1999) Epidemiological studies of equine herpesvirus 1 (EHV-1) in Thoroughbred foals: a review of studies conducted in the Hunter Valley of New South Wales between 1995 and 1997. Veterinary Microbiology, 68(1-2): 15-25.
Goehring, L.S., Van Winden, S.C., Van Maanen, C. and Van Oldruitenborgh-Oosterbaan, M.C. (2006). Equine herpesvirus type1-associated myeloencephalopathy in the Netherlands: a four year retrospective study (1999–2003). Journal of Veterinary Internal Medicine, 20(3): 601-607.
Ghadrdan Mashhadi, A.R., Makvandi, R., Hadi Nasab, H. and Deifiabad Shapouri, M.R. (2018). Study of infection rate of Herpes virus type 1, 4 in horses of Khuzestan. International Congress of Equine Health and Horse Industry, Iran. pp: 20-28.
Glass, K. and Barnes, B. (2013). Eliminating infectious diseases of livestock: a metapopulation model of infection control. Theoretical Population Biology, 85(1): 63-72.
Hassanpour, A., Rezaei Saber, A.P. and Mosakhani, F. (2010). Serologic investigation of the prevalence of Equine infectious anemia virus in Tabriz area. Veterinary Clinical Pathology, 4(2): 837-841.[In Persian]
Henninger, R.W., Reed, S.M. and Saville, W.J. (2007). Outbreak of neurologic disease caused by equine herpesvirus-1 at a university equestrian center. Journal of Veterinary Internal Medicine, 21(1): 157-165.
Harless, W. and Pusterla, N. (2006). Equine herpesvirus 1 and 4 respiratory disease in the horse. Clinical Techniques in Equine Practice, 5(3): 197-202.
Hartly, C.A., Wilks, C.R., Studdert, M.J. and Gilkerson, J.R. (2005). Comparison of antibody detection assays for the diagnosis of equine herpes virus1 and 4 infections in horses. American Journal of Veterinary Research, 66(5): 921-928.
Momtaz H. and Hemmatzadeh F, (2003). A Serological survey on equine herpes virus 1 and equine herpes virus 4 in the horse using ELISA. Pajouhesh and Sazandegi, 16(259): 63-69. [In Persian]
Mahmoud, H.Y.A.H., Fouad, S.S. and Amin, Y.A. (2022). Review of two viral agents of economic importance to the equine industry (equine herpesvirus-1 and equine arteritis virus). Equine Veterinary Education, 35(2): 92-101.
Matsumura, T., Sugiura, T., Imagawa, H., Fukonaga, Y. and Kamada, M. (1992). Epizootiological aspects of Type-1 and Type-4 equine herpesvirus infections among horse populations. Journal of Veterinary Medical Science, 54(2): 207-211.
Pusterla, N., Barnum, S., Miller, J., Varnell, S., Dallap-Schaer, B., Aceto, H. et al. (2021). Investigation of an EHV-1 outbreak in the United States caused by a new H752 genotype. Pathogens, 10(6): 747-756.
Pusterla, N., Mapes, S., Wademan, C., White, A., Estell, K. and Swain, E. (2012). Investigation of the role of mules as silent shedders of EHV-1 during an outbreak of EHV-1 myeloencephalopathy in California. Veterinary Record, 170(18): 465-465.
Pavulraj, S., Eschke, K., Theisen, J., Westhoff, S., Reimers, G., Andreotti S., et al. (2021). Equine herpesvirus type 4 (EHV-4) outbreak in Germany: virological, serological and molecular investigations. Pathogens, 10(7): 810-832.
Raoofi, , Madadgar, O., Akbarein, H. and Tazikeh, A. (2019). Molecular detection and phylogenetic analysis of equine herpes virus-1 in horses with history or clinical signs in four provinces of Iran. Iranian Journal of Veterinary Medicine, 14(1): 27-36. [In Persian]
Ruiz-Saenz, J., Goez, Y., Urcuqui-Inchima, S., Gongora, A. and Lopez-Herrera, A. (2008). Serological evidence of the infection by equine herpesvirus type 1 and 4 in two regions in Colombia. Revista Colombiana de Ciencias Pecuarias, 21(2): 251-258.
Sarani, A., Mohammadi, G., Mayameei, A. and Akbari, M. (2013). Investigation of equine herpesvirus-1 and 4 infections in equine population of Iran by real-time PCR. Human and Veterinary Medicine, 5(1): 29-33.
Slater, J., Equine herpesviruses. In: Sellon, D. and Long, M. (2007). Equine Infectious Diseases. Chapter 13, St. Louis, USA, Saunders Elsevier, pp: 134-153.
Studdert, M. J., Hartley, C. A., Dynon, K., Sandy, J. R., Slocombe, R. F., Charles, J. A., et al. (2003). Outbreak of equine herpes virus type 1 myeloencephalitis: New insights from virus identification by PCR and the application of an EHV-1-specific antibody detection ELISA. Veterinary Record, 153(14): 417-423.
G., Garvey, M., Cullinane, A., Jourdan, M., Fortier, C., Moreau, P. et al. (2019). Molecular surveillance of EHV-1 Strains Circulating in France during and after the Major 2009 Outbreak in Normandy Involving Respiratory Infection, Neurological Disorder, and Abortion. Viruses, 11(10): 916-927.
Taghipour Bazargani, T., Momtaz, H., Baharlo, F.R. and Ghafari, M. (2014). The first report on myloencephalopathy caused by equine herpes virus type 1 in Iran. Iranian Veterinary Journal. 10(3): 100-103. [In Persian]
Taouji, S., Collobert, C., Gicquel, B., Sailleau, C., Brisseau, N., Moussu, C. et al. (2002). Detection and isolation of equine herpes viruses 1 and 4 from horses in Normandy: an autopsy study of tissue distribution in relation to vaccination status. Journal of Veterinary Medicine, Series B, 49(8): 394-399.
Tazikeh, A., Raoofi, A., Madadgar, O., Akbarein, H. and Ghadrdan-Mashhadi, A. (2019). A survey of equine herpes virus 4 infection in four provinces of Iran using Real Time PCR Taqman assay. Journal of Veterinary Research, 73(4): 483-490. [In Persian]
Traub-Dargatz, J.L., Pelzel-McCluskey, A.M., Creekmore, L.H., Geiser-Novotny, S., Kasari, T.R., Wiedenheft, A.M., et al. (2013). Case-control study of a multistate equine herpesvirus myeloencephalopathy outbreak. Journal of Veterinary Internal Medicine, 27(2): 339-346.
Taktaz Hafshejania I, T., Nekoei, Sh., Vazirian, B., Doosti, A., Khamesipour, F. and Umunna Anyanwu, M. (2015). Molecular detection of equine herpesvirus types 1 and 4 infection in healthy horses in Isfahan central and Shahrekord southwest regions, Iran. BioMedical Research International:
Walker, C., Perotti, V.M., Love, D.N. and Whalley, I.M. (1999). Infection with equine herpesvirus 1 (EHV-1) strain HVS25A in pregnant mice. Journal of Comparative Pathology, 120(1): 15-27.
Welch, H. M., Bridges, C. G., Lyon, A. M., Griffiths, L. and Edington, N. (1992). Latent equid herpesviruses-1 and 4: detection and distinction using the polymerase chain reaction and co-cultivation from lymphoid tissues. Journal of General Virology, 73(2): 261-268.
Yildirim, Y., Yilmaz, V. and Kirmizigul, A.H. (2015). Equine herpes virus type 1 (EHV-1) and 4 (EHV-4) infections in horses and donkeys in northeastern Turkey. Iranian Journal of Veterinary Research, 16(4): 341-344.
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Allen, G.P., Kydd, J.H., Slater, J.D. and Smith, K.C. (2004).Equid herpesvirus-1 (EHV-1) and -4 (EHV-4) infections. In: Coetzer, JAW and Tustin, RC (Eds.), Infectious diseases of livestock. 2nd ed., Chapter 76, Cape Town, Oxford Press, pp: 829-859.
Amer, H.M., Shaltout, A.K., El-Sabagh, I.M., El-Sanousi, A.A. and Shalaby, M.A. (2011). Prevalence of equine herpes viruses 1, 2 and 4 in Arabian horse population in Egypt. African Journal of Microbiology Research, 5(27):4805-4811.
Attari, A. and Araghi-Sooreh, A. (2022). Serological survey of influenza A virus infection in horses of some districts of Mahabad city by ELISA method. Veterinary Clinical Pathology, 15(4): 357-367.[In Persian]
Ataseven, V., Dagalp, S., Guzel, M., Basaran, Z., Tan, M. and Geraghiy, B. (2009) Prevalence of equine herpesvirus-1 and equine herpesvirus-4 infections in equidae species in Turkey as determined by ELISA and multiplex nested PCR. Research in Veterinary Science, 86(2): 339-344.
Avci, O., Yapici, O., Bulut, O., Kale, M. and Atli, K. (2018). Detection of equine herpes virus 1, equine herpes virus 4, and equine arteritis virus antibodies in Kyrgizstan by ELISA. Bionature, 38(3):219-224.
Burgess, B.A., Tokateloff, N., Manning, S., Lohmann, K., Lunn, D.P., Hussey, S.B., et al. (2012). Nasal shedding of equine herpesvirus‐1 from horses in an outbreak of equine herpes myeloencephalopathy in Western Canada. Journal of Veterinary Internal Medicine, 26(2): 384-392.
Cruz, F., Fores, P., Mughini-Gras, L., Ireland, J., Moreno, M.A. and Newton, J.R. (2016). Seroprevalence and factors associated with equine herpesvirus type 1 and 4 in Spanish Purebred horses in Spain. Veterinary Record, 178(16): 398-398.
Derbal, S. (2021). Epidemiology of EHV-1 and EHV-4 infections: A review. International Journal of Veterinary Sciences, 7(2): 108-112.
Damiani, A.M., Vries, M., Reimers, G., Winkler, S. and Osterrieder, N. (2014). A severe equine herpesvirus type 1 (EHV-1) abortion outbreak caused by a neuropathogenic strain at a breeding farm in northern Germany. Veterinary Microbiology, 172(3-4): 555-562.
El Brini, Z., Fassi Fihri, O., Paillot, R., Lotfi, C., Amraoui, F. and El Ouadi, H. (2021). Seroprevalence of equine herpesvirus 1 (EHV-1) and equine herpesvirus 4 (EHV-4) in the northern Moroccan horse populations. Animals, 11(10): 2851.
Getachew, M., Alemayehu, F., Chala, C., Amare, B., Kassa, D., Burden, F., et al. (2014). A cross-sectional sero-survey of some infectious diseases of working equids in Central Ethiopia. Journal of Veterinary Medicine and Animal Health, 6(9): 231-238.
Gharekhani, A. and Morshedi, A. (2010). The study of infection rate to Bovine Herpes Virus–1 (BHV-1) in milk samples of dairy cattle in Urmia and Maku by ELISA method. Veterinary Clinical Pathology, 4(3): 915-921.[In Persian]
Gilkerson, J. R., Whalley, J. M., Drummer, H. E., Studdert, M. J. and Love, D. N. (1999) Epidemiological studies of equine herpesvirus 1 (EHV-1) in Thoroughbred foals: a review of studies conducted in the Hunter Valley of New South Wales between 1995 and 1997. Veterinary Microbiology, 68(1-2): 15-25.
Goehring, L.S., Van Winden, S.C., Van Maanen, C. and Van Oldruitenborgh-Oosterbaan, M.C. (2006). Equine herpesvirus type1-associated myeloencephalopathy in the Netherlands: a four year retrospective study (1999–2003). Journal of Veterinary Internal Medicine, 20(3): 601-607.
Ghadrdan Mashhadi, A.R., Makvandi, R., Hadi Nasab, H. and Deifiabad Shapouri, M.R. (2018). Study of infection rate of Herpes virus type 1, 4 in horses of Khuzestan. International Congress of Equine Health and Horse Industry, Iran. pp: 20-28.
Glass, K. and Barnes, B. (2013). Eliminating infectious diseases of livestock: a metapopulation model of infection control. Theoretical Population Biology, 85(1): 63-72.
Hassanpour, A., Rezaei Saber, A.P. and Mosakhani, F. (2010). Serologic investigation of the prevalence of Equine infectious anemia virus in Tabriz area. Veterinary Clinical Pathology, 4(2): 837-841.[In Persian]
Henninger, R.W., Reed, S.M. and Saville, W.J. (2007). Outbreak of neurologic disease caused by equine herpesvirus-1 at a university equestrian center. Journal of Veterinary Internal Medicine, 21(1): 157-165.
Harless, W. and Pusterla, N. (2006). Equine herpesvirus 1 and 4 respiratory disease in the horse. Clinical Techniques in Equine Practice, 5(3): 197-202.
Hartly, C.A., Wilks, C.R., Studdert, M.J. and Gilkerson, J.R. (2005). Comparison of antibody detection assays for the diagnosis of equine herpes virus1 and 4 infections in horses. American Journal of Veterinary Research, 66(5): 921-928.
Momtaz H. and Hemmatzadeh F, (2003). A Serological survey on equine herpes virus 1 and equine herpes virus 4 in the horse using ELISA. Pajouhesh and Sazandegi, 16(259): 63-69. [In Persian]
Mahmoud, H.Y.A.H., Fouad, S.S. and Amin, Y.A. (2022). Review of two viral agents of economic importance to the equine industry (equine herpesvirus-1 and equine arteritis virus). Equine Veterinary Education, 35(2): 92-101.
Matsumura, T., Sugiura, T., Imagawa, H., Fukonaga, Y. and Kamada, M. (1992). Epizootiological aspects of Type-1 and Type-4 equine herpesvirus infections among horse populations. Journal of Veterinary Medical Science, 54(2): 207-211.
Pusterla, N., Barnum, S., Miller, J., Varnell, S., Dallap-Schaer, B., Aceto, H. et al. (2021). Investigation of an EHV-1 outbreak in the United States caused by a new H752 genotype. Pathogens, 10(6): 747-756.
Pusterla, N., Mapes, S., Wademan, C., White, A., Estell, K. and Swain, E. (2012). Investigation of the role of mules as silent shedders of EHV-1 during an outbreak of EHV-1 myeloencephalopathy in California. Veterinary Record, 170(18): 465-465.
Pavulraj, S., Eschke, K., Theisen, J., Westhoff, S., Reimers, G., Andreotti S., et al. (2021). Equine herpesvirus type 4 (EHV-4) outbreak in Germany: virological, serological and molecular investigations. Pathogens, 10(7): 810-832.
Raoofi, , Madadgar, O., Akbarein, H. and Tazikeh, A. (2019). Molecular detection and phylogenetic analysis of equine herpes virus-1 in horses with history or clinical signs in four provinces of Iran. Iranian Journal of Veterinary Medicine, 14(1): 27-36. [In Persian]
Ruiz-Saenz, J., Goez, Y., Urcuqui-Inchima, S., Gongora, A. and Lopez-Herrera, A. (2008). Serological evidence of the infection by equine herpesvirus type 1 and 4 in two regions in Colombia. Revista Colombiana de Ciencias Pecuarias, 21(2): 251-258.
Sarani, A., Mohammadi, G., Mayameei, A. and Akbari, M. (2013). Investigation of equine herpesvirus-1 and 4 infections in equine population of Iran by real-time PCR. Human and Veterinary Medicine, 5(1): 29-33.
Slater, J., Equine herpesviruses. In: Sellon, D. and Long, M. (2007). Equine Infectious Diseases. Chapter 13, St. Louis, USA, Saunders Elsevier, pp: 134-153.
Studdert, M. J., Hartley, C. A., Dynon, K., Sandy, J. R., Slocombe, R. F., Charles, J. A., et al. (2003). Outbreak of equine herpes virus type 1 myeloencephalitis: New insights from virus identification by PCR and the application of an EHV-1-specific antibody detection ELISA. Veterinary Record, 153(14): 417-423.
G., Garvey, M., Cullinane, A., Jourdan, M., Fortier, C., Moreau, P. et al. (2019). Molecular surveillance of EHV-1 Strains Circulating in France during and after the Major 2009 Outbreak in Normandy Involving Respiratory Infection, Neurological Disorder, and Abortion. Viruses, 11(10): 916-927.
Taghipour Bazargani, T., Momtaz, H., Baharlo, F.R. and Ghafari, M. (2014). The first report on myloencephalopathy caused by equine herpes virus type 1 in Iran. Iranian Veterinary Journal. 10(3): 100-103. [In Persian]
Taouji, S., Collobert, C., Gicquel, B., Sailleau, C., Brisseau, N., Moussu, C. et al. (2002). Detection and isolation of equine herpes viruses 1 and 4 from horses in Normandy: an autopsy study of tissue distribution in relation to vaccination status. Journal of Veterinary Medicine, Series B, 49(8): 394-399.
Tazikeh, A., Raoofi, A., Madadgar, O., Akbarein, H. and Ghadrdan-Mashhadi, A. (2019). A survey of equine herpes virus 4 infection in four provinces of Iran using Real Time PCR Taqman assay. Journal of Veterinary Research, 73(4): 483-490. [In Persian]
Traub-Dargatz, J.L., Pelzel-McCluskey, A.M., Creekmore, L.H., Geiser-Novotny, S., Kasari, T.R., Wiedenheft, A.M., et al. (2013). Case-control study of a multistate equine herpesvirus myeloencephalopathy outbreak. Journal of Veterinary Internal Medicine, 27(2): 339-346.
Taktaz Hafshejania I, T., Nekoei, Sh., Vazirian, B., Doosti, A., Khamesipour, F. and Umunna Anyanwu, M. (2015). Molecular detection of equine herpesvirus types 1 and 4 infection in healthy horses in Isfahan central and Shahrekord southwest regions, Iran. BioMedical Research International:
Walker, C., Perotti, V.M., Love, D.N. and Whalley, I.M. (1999). Infection with equine herpesvirus 1 (EHV-1) strain HVS25A in pregnant mice. Journal of Comparative Pathology, 120(1): 15-27.
Welch, H. M., Bridges, C. G., Lyon, A. M., Griffiths, L. and Edington, N. (1992). Latent equid herpesviruses-1 and 4: detection and distinction using the polymerase chain reaction and co-cultivation from lymphoid tissues. Journal of General Virology, 73(2): 261-268.
Yildirim, Y., Yilmaz, V. and Kirmizigul, A.H. (2015). Equine herpes virus type 1 (EHV-1) and 4 (EHV-4) infections in horses and donkeys in northeastern Turkey. Iranian Journal of Veterinary Research, 16(4): 341-344.
