Standard and molecular methods in the diagnostics of infections caused by equine herpesviruses 1 and 4
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Abstract
Background. Equine herpesvirus type 1 (EHV-1) is responsible for respiratory disease in young animals, abortion in pregnant mares and neurological disease, whilst equine herpesvirus 4 (EHV-4) is mainly the causative agent of respiratory disorders and rarely causes abortion. These viruses are considered as one of the most clinically and economically important pathogens of horses and can be detected in a range of tissues.
Scope and Approach. Serological methods are used to detect the presence and titre of specific antibodies to EHV-1 and EHV-4 in the sera of examined horses and are useful in epizootiological studies. Commercially available ELISA kits are able to differentiate specific EHV-1 and EHV-4 antibodies. EHV-1 and EHV-4 can both be isolated using susceptible cells such as primary horse cell cultures and other non-equine cells with visible cytopathic effect. Since standard diagnostic methods can be time consuming and arduous, the scope of many studies has been to develop and confirm the sensitivity and specificity of molecular diagnostic methods.
Key Findings and Conclusions. Polymerase chain reaction has proved to be a good screening method for the presence of latent infections of horses caused by these viruses, also making possible the rapid identification and differentiation of EHV-1 and- EHV-4 in the examined samples. Real-time PCR is a sensitive, specific and quantitative method that enables the determination of viral kinetics in infected horses. Genome sequencing can be used to discover mutations in the genomes of EHV-1 and EHV-4 as well as to track the spread of their different strains globally.
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References
Allen, G. P. 2006. Antemortem detection of latent infection with neuropathogenic strains of equine herpesvirus-1 in horses. American Journal of Veterinary Research 67: 1401-1405. doi: 10.2460/ajvr.67.8.1401.
Allen, G. P., Bryans J. T. 1986. Molecular epizootiology, pathogenesis, and prophylaxis of equine herpesvirus-1 infections. Progress in Veterinary Microbiology and Immunology 2: 78-144.
Ataseven, V. S., Dağalp S. B., Güzel M., Başaran Z., Tan M. T., Geraghty 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): 339-44. doi: http://dx.doi.org/10.1016/j.rvsc.2008.06.001.
Ataseven, V. S., Çiğdem Oğuzoğlu, T., Dinçer, E., Bilge Dağalp, S. 2016. Partial sequence of the gB gene of equid herpesvirus type 1 isolates associated with abortion in Turkey. Ankara Üniversitesi Veteriner Fakültesi Dergisi 63: 277-281.
Borchers, K., Wolfinger U., Lawrenz B., Schellenbach A., Ludwig H. 1997. Equine herpesvirus 4 DNA in trigeminal ganglia of naturally infected horses detected by direct in situ PCR. Journal of General Virology 78(5): 1109-14. http://dx.doi.org/10.1099/0022-1317-78-5-1109.
Campbell, T. M., Studdert, M. J. 1983. Equine herpesvirus type 1 (EHV-1). Veterinary Bulletin 53: 135-146.
Carvalho, R., L., Passos M. F., Martins, S. 2000. Development of a differential multiplex PCR assay for equine herpesvirus 1 and 4 as a diagnostic tool. Journal of Veterinary Medicine. Series B 47: 351-359. doi: 10.1046/j.1439-0450.2000.00361.x.
Crabb, B. S., Studdert, M. J. 1993. Epitopes of glycoprotein G of equine herpesviruses 4 and 1 located near the C termini elicit type-specific antibody responses in the natural host. Journal of Virology 67: 6332-6338.
Crabb, B. S., Studdert, M. J. 1996. Equine rhinopneumonitis (equine herpesvirus 4) and equine abortion (equine herpesvirus 1). In: Virus Infections of Equines, edited by M. J. Studdert, 11-37. Elsevier.
Crabb, B. S., Drummer H. E., Reubel G. H., McPherson C. M., Bowning G. F., Studdert, M. J. 1995. A type specific, serological test to distinguish antibodies to equine herpesviruses 4 and 1. Archives of Virology 140: 245-258.
Davison, A. J., Eberle R., Ehlers B., Hayward G. S., McGeoch D. J., Minson A. C., Pellett P. E., Roizman B., Studdert M. J., Thiry, E. 2009. The order Herpesvirales. Archives of Virology 154: 171-177. doi: 10.1007/s00705-008-0278-4.
Diallo, I. S., Hewitson G., Wright L. L., Kelly M. A., Rodwell B. J., Corney, B. G. 2007. Multiplex real-time PCR for the detection and differentiation of equid herpesvirus 1 (EHV-1) and equid herpesvirus 4 (EHV-4). Veterinary Microbiology 123(1-3): 93-103. doi: http://dx.doi.org/10.1016/j.vetmic.2007.02.004.
Dunowska, M., Wilks C. R., Studdert M. J., Meers, J. 2002. Equine respiratory viruses in foals in New Zealand. New Zealand Veterinary Journal 50(4): 140-7. doi: http://dx.doi.org/10.1080/00480169.2002.36300.
Gilkerson, J. R., Love D. N., Whalley, J. M. 1997. Serological evidence of equine herpesvirus 1 (EHV- 1) infection in Thoroughbred foals 30-120 days of age. Australian Equine Veterinarian 15: 128-134.
Gilkerson, J. R., Whalley J. M., Drummer H. E., Studdert M. J., Love, D. N. 1999. Epidemiology of EHV-1 and EHV-4 in the mare and foal populations on a Hunter Valley stud farm: are mares the source of EHV-1 for unweaned foals. Veterinary Microbiology 68: 27-34. doi: http://dx.doi.org/10.1016/S0378-1135(99)00058-9.
Gür, S., Yapici, O. 2008. Equine Herpesvirus Type 1 and 4 in Individually Reared Horses in Central and Western Turkey. Acta Veterinaria Brno 77(4): 609-613. doi: https://doi.org/10.2754/avb200877040609.
Hartley, C. A., Wilks C. R., Studdert M. J., Gilkerson, J. R. 2005. Comparison of antibody detection assays for the diagnosis of equine herpesvirus 1 and 4 infections in horses. American Journal of Veterinary Reearch 66(5): 921-8. doi: 10.2460/ajvr.2005.66.921.
Hebia-Fellah, I., Léauté A., Fiéni F., Zientara S., Imbert-Marcille B. M., Besse B., Fortier G., Pronost S., Miszczak F., Ferry B., Thorin C., Pellerin J. L., Bruyas, J. F. 2009. Evaluation of the presence of equine viral herpesvirus 1 (EHV-1) and equine viral herpesvirus 4 (EHV-4) DNA in stallion semen using polymerase chain reaction (PCR). Theriogenology 71(9):1381-9. doi: http://dx.doi.org/10.1016/j.theriogenology.2009.01.009.
Hornyák, A., Bakonyi T., Kulik M., Kecskeméti S., Rusvai, M. 2006. Application of polymerase chain reaction and virus isolation techniques for the detection of viruses in aborted and newborn foals. Acta Veterinaria Hungarica 54(2): 271-9. doi: http://www.akademiai.com/doi/abs/10.1556/AVet.54.2006.2.13.
Hussey, S, B., Clark R., Lunn K. F., Breathnach C., Soboll G., Whalley J. M., Lunn, D. P. 2006. Detection and quantification of equine herpesvirus-1 viremia and nasal shedding by real-time polymerase chain reaction. Journal of Veterinary Diagnostic Investigation. 18(4): 335-42. doi: 10.1177/104063870601800403.
Kirisawa, R., Endo A., Iwai H., Kawakami, Y. 1993. Detection and identification of equine herpesvirus-1 and -4 by polymerase chain reaction. Veterinary Microbiology 36(1-2): 57-67. doi: http://dx.doi.org/10.1016/0378-1135(93)90128-T.
Ko, S., Kang J. G., Yeh J. Y., Moon J. S., Choi G. C., Won S., Chae, J. S. 2013. First report on molecular detection of equine upper respiratory infectious viruses in Republic of Korea. Journal of Equine Veterinary Science 33: 628-636. doi: http://dx.doi.org/10.1016/j.jevs.2012.11.001.
Kydd, J. H., Townsend H. G, Hannant, D. 2006. The equine immune response to equine herpesvirus-1: the virus and its vaccines. Veterinary Immunology and Immunopathology 111: 15-30. doi: http://dx.doi.org/10.1016/j.vetimm.2006.01.005.
Kydd, J. H., Smith K. C., Hannant D., Livesay G. J., Mumford, J. A. 1994. Distribution of equid herpesvirus-1 (EHV-1) in respiratory tract associated lymphoid tissue: implications for cellular immunity. Equine Veterinary Journal 26, 466-473. doi: 10.1111/j.2042-3306.1994.tb04052.x.
Lawrence, G. L., Gilkerson J., Love D. N., Sabine M., Whalley, J. M. 1994. Rapid, single-step differentiation of equid herpesviruses 1 and 4 from clinical material using the polymerase chain reaction and virus-specific primers. Journal of Virological Methods 47: 59-72. doi: http://dx.doi.org/10.1016/0166-0934(94)90066-3.
Lazić, S., Vidić B., Lalić M., Pavlović R., Đurišić, S. 1993. Finding of neutralizing antibodies for the Herpes virus in the blood serum of race horses in Vojvodina (Yugoslavia). Veterinarski glasnik 47 (6): 361-440.
Lazić, S., Petrović T., Bugarski D., Jovičin M., Plavšić B., Lupulović D., Lazić G., Polaček, V. 2016. The program for eradication of infectious bovine rhinotracheitis /infectious pustular vulvovaginitis in the Republic of Serbia, Veterinarski Glasnik 70 (5-6): 185 - 204. doi: 10.2298/VETGL1606185L.
Marenzoni, M. L., Passamonti F., Cappelli K., Veronesi F., Capomaccio S., Supplizi A. V., Valente C., Autorino G., Coletti, M. 2008. Clinical, serological and molecular investigations of EHV-1 and EHV-4 in 15 unweaned thoroughbred foals. The Veterinary Record 162: 337-341. doi: http://dx.doi.org/10.1136/vr.162.11.337.
Mihajlović, B., Rogan D., Krstić, Lj. 1987. Virusni pobačaj kobila. I - Izolovanje i identifikacija virusa. Veterinarski glasnik 41 (10): 741-744.
Milić, N., Jovanović T., Knežević I., Gađanski-Omerović G., Ašanin, R. 1999. Examinations of the immunogenicity of the experimental bivalent subunit vaccines against Herpes simplex virus type 1 and 2. Acta Veterinaria 49(1): 1-15.
Milić, N., Gađanski-Omerović G., Ašanin, R. 1997. Examination of the immunogenicity of experimental polyvalent subunit vaccine against influenza viruses. ActaVeterinaria 47(5-6): 321-330.
Milić, N., Gađanski-Omerović G., Ašanin, R. 1998. Examination of immunogenicity of experimental subunit vaccines against PI3 virus in calves. Acta Veterinaria 48(1): 27-36.
Milić, N., Nišavić J., Radojičić M., Šekler M., Matović K., Vidanović, D. 2009. Uporedno ispitivanje osetljivosti i specifičnosti imunoenzimske probe i testa inhibicije hemaglutinacije u serološkoj dijagnostici Newcastle bolesti živine. Veterinarski Glasnik 63(1-2): 37-44. doi: 10.2298/VETGL0902037M.
Milić, N., Nišavić J., Ašanin R., Knežević A., Ašanin J., Vidanović D., Šekler, M. 2010. Implementation of polymerase chain reaction (PCR) and Real-time pcr in quick identification of bovine herpesvirus 1. Veterinarski Glasnik 64(3-4): 159-167. doi: http://doiserbia.nb.rs/Article.aspx?id=0350-24571004159M#.
Milić, N., Nišavić J., Borozan S., Zorić A., Lazić S., Petrović T., Rašić, Z. 2015. Examination of some biological properties of glycoprotein Subunits of PHY-LMV.42 strain of Newcastle disease virus. Veterinarski Glasnik 69 (5-6): 337-355. doi: 10.2298/VETGL1506337M.
Milić, N., Lazić S., Vidanović D., Šekler M., Nišavić J., Resanović R., Petrović, T. 2012. Molecular characterization of some strains of Newcastle disease virus isolated in province of Vojvodina, Republic of Serbia. Acta Veterinaria 62(4): 365-374. doi: 10.2298/AVB1204365M.
Milić, N., Jovanović T., Gađanski-Omerović G., Knežević I., Ašanin, R. 2001. Examination of humoral and cellular immune response after immunization with subunit vaccine against herpes simplex virus 1 and 2. Acta Veterinaria 51(1): 35-44.
Nišavić, J., Milić N., Knežević A., Jovanović, T. 2010. The application of polymerase chain reaction in detection of bovine herpesvirus 1 in clinical samples. Acta Veterinaria 60(1): 39-48. doi: 10.2298/AVB1001039N.
Nišavić, J., Zorić A., Milić, N. 2016. The application of molecular methods in the diagnostics of infection of swine caused by porcine circovirus 2. Veterinarski Glasnik 70(5-6): 249-258. DOI 10.2298/VETGL1606249N.
Nišavić, J., Kustudić-Nikoletić N., Milić N., Zorić, A. 2016. Examination of the influence of different adjuvants on the immunogenicity of vaccines against parainfluenza 3 virus in cattle. Veterinarski Glasnik 70(3-4): 99-110. doi: 10.2298/VETGL1604099N.
Ohta, M., Manabu N., Koji T., Takashi K., Tomio, M. 2011. Evaluation of the Usefulness of a PCR Assay Performed at a Clinical Laboratory for the Diagnosis of Respiratory Disease Induced by Equine Herpesvirus Type 1 in the Field. Journal of Equine Veterinary Science 22(3): 53-56. doi: http://doi.org/10.1294/jes.22.53.
OIE, 2015. Equine rhinopneumonitis (equine herpesvirus -1 and -4) Available at: http://www.oie.int/fileadmin/Home/eng/Health_standards/tahm/2.05.09_EQUINE_RHINO.pdf. Accessed 19.02.2017.
Patel, J. R., Heldens, J. 2005. Equine herpesviruses 1 (EHV-1) and 4 (EHV-4) epidemiology disease and immunoprophylaxis. The Veterinary Journal 170: 14-23. doi: 10.1016/j.tvjl.2004.04.018.
Petrović, T., Lupulović D., Petrić D., Vasić A., Hrnjaković Cvjetković I., Milošević V., Vidanović D., Šekler M., Lazić S., Đuričić B., Plavšić B., Saiz, J. C. 2015. WNV infection - an emergent vector borne viral infection in Serbia: current situation. Veterinarski Glasnik 69(1-2): 111-126. doi: 10.2298/VETGL1502111P.
Ploszay, G., Rola J., Larska M., Zmudzinski, J. F. 2013. First report on equine herpesvirus type 4 isolation in Poland - evaluation of diagnostic tools. Polish Journal of Veterinary Sciences 16(3): 493-500. doi: 10.2478/pjvs-2013-0069.
Pusterla, N., Mapes S., Wilson, W. D. 2010. Prevalence of equine herpesvirus type 1 in trigeminal ganglia and submandibular lymph nodes of equids examined postmortem.Veterinary Record 167(10): 376-8. doi: 10.1136/vr.c3748.
Pusterla, N., Mapes S., Wilson, W. D. 2012. Prevalence of latent alpha-herpesviruses in Thoroughbred racing horses. Veterinary Journal 193(2): 579-82. doi: 10.1016/j.tvjl.2012.01.030.
Pusterla, N., Wilson W. D., Mapes S., Finno C., Isbell D., Arthur R. M., Ferraro, G. L. 2009. Characterization of viral loads, strain and state of equine herpesvirus-1 using real-time PCR in horses following natural exposure at a racetrack in California. Veterinary Journal 179(2): 230-9. doi: 10.1016/j.tvjl.2007.09.018.
Reed, S. M., Toribio, R. E. 2004. Equine herpesvirus 1 and 4. Veterinary Clinics of North America: Equine Practice 20: 631-642. doi: 10.1016/j.cveq.2004.09.001.
Senthil, N. R., Parameswaran, T. 2014. Seroprevalence of Equine herpes virus (EHV1) in equidae using serum neutralization test. Journal of Research in Agriculture and Animal Science 2(5): 04-06.
Slater, J. 2007. Equine Herpesviruses. In Equine Infectious Diseases, edited by D. Sellon, M. Long, 134-153. Saunders Elsevier.
Slater, J. D., Borchers K., Thackray A. M., Field, H. J. 1994. The trigeminal ganglion is a location for equine herpesvirus 1 latency and reactivation in the horse. Journal of General Virology 75(8): 2007-16. doi: 10.1099/0022-1317-75-8-2007.
Studdert, M. J., Hartley C. A., Dynon K., Sandy J. R., Slocombe R. F., Charles J. A., Milne M. E., Clarke A. F., El-Hage, C. 2003. Outbreak of equine herpesvirus type 1 myeloencephalitis: new insights from virus identification by PCR and the application of an EHV-1-specific antibody detection ELISA. Veterinary Record 153: 417-423. doi: http://dx.doi.org/10.1136/vr.153.14.417.
Telford, E. A., Watson M. S., Perry J., Cullinane A. A., Davison, A. J. 1998. The DNA sequence of equine herpesvirus-4. Journal of General Virology 79: 1197-1203. doi: 10.1099/0022-1317-79-5-1197.
Turan, N., Yildirim F., Altan E., Sennazli G., Gurel A., Diallo I., Yilmaz, H. 2012. Molecular and pathological investigations of EHV-1 and EHV-4 infections in horses in Turkey. Research in Veterinary Science 93(3):1504-7. doi: 10.1016/j.rvsc.2012.01.019.
Wang, L., Raidal S. L., Pizzirani A., Wilcox, G. E. 2007. Detection of respiratory herpesviruses in foals and adult horses determined by nested multiplex PCR. Veterinary Microbiology 121(1-2):18-28. doi: 10.1016/j.vetmic.2006.11.009.
Welch, H. M., Bridges C. G., Lyon A. M., Griffiths L., 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): 261-8. doi: 10.1099/0022-1317-73-2-261.
Yasunaga, S., Maeda K., Matsumura T., Kondo T., Kai, K. 2000. Application of a type-specific enzyme-linked immunosorbent assay for equine herpesvirus types 1 and 4 (EHV-1 and -4) to horse populations inoculated with inactivated EHV-1 vaccine. Journal of Veterinary Medical Science 62(7): 687-91. doi: http://doi.org/10.1292/jvms.62.687.
Yasunaga, S., Maeda K., Matsumura T., Kondo T., Kai K., Iwata H., Inoue, T. 1998. Diagnosis and sero-epizootiology of equine herpesvirus type 1 and type 4 infections in Japan using a type-specific ELISA. Journal of Veterinary Medical Science 60: 1133-1137. doi: http://doi.org/10.1292/jvms.60.1133.