Serological Evidence of Common Equine Viral Infections in a Semi-Isolated, Unvaccinated Population of Hucul Horses
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Ethics Statement
2.2. Specimen
2.3. Virus Isolation
2.4. Serology
2.5. Statistical Analysis
3. Results
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Purzyc, H.A. General characteristic of Hucul horses. Act. Sci. Pol. Med. Vet. 2000, 6, 25–31. [Google Scholar]
- Mackowski, M.; Mucha, S.; Cholewiński, G.; Cieslak, J. Genetic diversity in Hucul and Polish primitive horse breeds. Arch. Anim. Breed. 2015, 58, 23–31. [Google Scholar] [CrossRef]
- Cywińska, A.; Czopowicz, M.; Witkowski, L.; Górecka, R.; Degórski, A.; Guzera, M.; Szczubełek, P.; Turło, A.; Schollenberger, A.; Winnicka, A. Reference intervals for selected hematological and biochemical variables in Hucul horses. Pol. J. Vet. Sci. 2015, 18, 439–445. [Google Scholar] [CrossRef] [Green Version]
- Fornal, A.; Radko, A.; Piestrzyńska-Kajtoch, A. Genetic polymorphism of Hucul horse population based on 17 microsatellite loci. Act. Bioch. Pol. 2013, 60, 761–765. [Google Scholar] [CrossRef] [Green Version]
- Rola, J.; Larska, M.; Rola, J.G.; Belák, S.; Autorino, G.L. Epizootiology and phylogeny of equine arteritis virus in hucul horses. Vet. Microbiol. 2011, 148, 402–407. [Google Scholar] [CrossRef]
- Socha, W.; Sztromwasser, P.; Dunowska, M.; Jaklińska, B.; Rola, J. Spread of equine arteritis virus among Hucul horses with different EqCXCL16 genotypes and analysis of viral quasispecies from semen of selected stallions. Sci. Rep. 2020, 10, 290. [Google Scholar] [CrossRef] [PubMed]
- Bażanów, B.A.; Jackulak, N.A.; Frącka, A.B.; Staroniewicz, Z.M. Abortogenic viruses in horses. Equine Vet. Educ. 2014, 26, 48–55. [Google Scholar] [CrossRef]
- Bażanów, B.A.; Frącka, A.B.; Jackulak, N.A.; Romuk, E.; Gębarowski, T.; Owczarek, A.; Stygar, D. Viral, Serological, and Antioxidant Investigations of Equine Rhinitis A Virus in Serum and Nasal Swabs of Commercially Used Horses in Poland. BioMed Res. Int. 2018, 1–6. [Google Scholar] [CrossRef] [Green Version]
- Bażanów, B.A.; Jansen van Vuren, P.; Szymański, P.; Stygar, D.; Frącka, A.; Twardoń, J.; Kozdrowski, R.; Pawęska, J.T. A Survey on West Nile and Usutu Viruses in Horses and Birds in Poland. Viruses 2018, 10, 87. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bolfa, P.; Barbuceanu, F.; Leau, S.E.; Leroux, C. Equine infectious anaemia in Europe: Time to re-examine the efficacy of monitoring and control protocols. Equine Vet. J. 2016, 48, 140–142. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gerber, H.; Steck, F.; Hofer, B.; Walther, L.; Friedli, U. Serological investigations on equine viral arteritis. In Proceedings of the Fourth International Conference on Equine Infectious Diseases, Lyon, France, 24–27 September 1976; Bryans, J.T., Gerber, H., Eds.; Veterinary Publications: Princeton, NJ, USA, 1978; pp. 461–465. [Google Scholar]
- Gilkerson, J.R.; Whalley, J.M.; Drummer, H.E.; Studdert, M.J.; Love, D.N. 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. Vet. Microbiol. 1999, 68, 27–34. [Google Scholar] [CrossRef]
- Bażanów, B.A.; Jackulak, N.A.; Florek, M.; Staroniewicz, Z. Equid Herpesvirus-Associated Abortion in Poland between 1977–2010. J. Equine Vet. Sci. 2012, 32, 747–751. [Google Scholar] [CrossRef]
- Black, W.; Wilcox, R.; Stevenson, R.; Hartley, C.; Ficorilli, N.; Gilkerson, J.; Studdert, M. Prevalence of serum neutralising antibody to equine rhinitis A virus (ERAV), equine rhinitis B virus 1 (ERBV1) and ERBV2. Vet. Microbiol. 2007, 119, 65–71. [Google Scholar] [CrossRef] [PubMed]
- Burrows, R.; Denyer, M.; Goodridge, D.; Hamilton, F. Field and laboratory studies of equine influenza viruses isolated in 1979. Vet. Rec. 1981, 109, 353–356. [Google Scholar] [CrossRef] [PubMed]
- Kriegshäuser, G.; Deutz, A.; Kuechler, E.; Skern, T.; Lussy, H.; Nowotny, N. Prevalence of neutralizing antibodies to Equine rhinitis A and B virus in horses and man. Vet. Microbiol. 2005, 106, 293–296. [Google Scholar] [CrossRef] [PubMed]
- Nikolay, B. A review of West Nile and Usutu virus co-circulation in Europe: How much do transmission cycles overlap? Trans. R. Soc. Trop. Med. Hyg. 2015, 109, 609. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Moniuszko-Malinowska, A.; Czupryna, P.; Dunaj, J.; Zajkowska, J.; Siemieniako, A.; Pancewicz, S. West Nile virus and USUTU--a threat to Poland. Przegl. Epidemiol. 2016, 70, 7–10. [Google Scholar] [PubMed]
- Issel, C.J.; Adams, W.V. Detection of equine infectious anemia virus in a horse with an equivocal agar gel immunodiffusion test reaction. J. Am. Vet. Med. Assoc. 1982, 180, 276–278. [Google Scholar] [PubMed]
- Halliday, J.E.B.; Meredith, A.L.; Knobel, D.L.; Shaw, D.J.; Bronsvoort, B.M.d.C.; Cleaveland, S. A framework for evaluating animals as sentinels for infectious disease surveillance. J. R. Soc. Interface 2007, 4, 973–984. [Google Scholar] [CrossRef]
- Timoney, J.; Gillespie, J.H.; Scott, F.W.; Barlough, J.E. Laboratory diagnosis of viral infection. In Hagan and Bruner’s Microbiology and Infectious Diseases of Domestic Animals, 8th ed.; Cornell University Press: Ithaca, NY, USA, 1988; pp. 467–468. [Google Scholar]
- Cullinane, A. Equine influenza (infection with equine influenza virus). In Manual of Diagnostic Tests and Vaccines for Terrestrial Animals 2019, 8th ed.; OIE World Organisation for Animal Health: Paris, France, 2020; pp. 1–19. [Google Scholar]
- Timoney, P.J. Equine viral arteritis (infection with equine arteritis virus). In Manual of Diagnostic Tests and Vaccines for Terrestrial Animals 2019, 8th ed.; OIE World Organisation for Animal Health: Paris, France, 2020; pp. 1333–1349. [Google Scholar]
- Elton, D.; Bryant, N. Equine rhinopneumonitis (equine herpesvirus-1 and -4). In Manual of Diagnostic Tests and Vaccines for Terrestrial Animals 2019, 8th ed.; OIE World Organisation for Animal Health: Paris, France, 2020; pp. 1320–1332. [Google Scholar]
- Carman, S.; Rosendal, S.; Huber, L.; Gyles, C.; McKee, S.; Willoughby, R.A.; Dubovi, E.; Thorsen, J.; Lein, D. Infectious agents in acute respiratory disease in horses in Ontario. J. Vet. Diagn. Investig. 1997, 9, 17–23. [Google Scholar] [CrossRef] [Green Version]
- Zhang, W.; Besselaar, T.G. The laboratory diagnosis and virological surveillance of influenza. In Manual for the Laboratory Diagnosis and Virological Surveillance of Influenza; World Health Organization: Geneva, Switzerland, 2011; pp. 59–63. [Google Scholar]
- Ludolfs, D.; Niedrig, M.; Paweska, J.T.; Schmitz, H. Reverse ELISA for the detection of anti-West Nile virus antibodies in humans. Eur. J. Clin. Microbiol. Infect. Dis. 2007, 26, 467–473. [Google Scholar] [CrossRef]
- Oliveira, F.G.; Diniz, R.S.; Camargos, M.F.; de Oliveira, A.M.; de Souza Rajão, D.; Braz, G.F.; Leite, R.C.; Pimenta dos Reis, J.K. Comparative study of agar gel immunodiffusion (AGID) protocols for the diagnosis of equine infectious anemia in Brazil. Sem. Cien. Agra. 2013, 34, 3909–3916. [Google Scholar] [CrossRef] [Green Version]
- Mealey, R.H. Equine Infectious Anaemia. In Equine Infectious Diseases, 1st ed.; Sellon, D.C., Long, M.T., Eds.; Saunders Elsevier: Amsterdam, The Netherlands, 2007; pp. 213–219. [Google Scholar]
- Golnik, W.; Bażanów, B.; Florek, M.; Pawęska, J. Prevalence of equine arteritis and West Nile virus–specific antibodies in thoroughbred horses in Poland. Ann. Univ. Mariae Curie-Sklodowska 2008, 21, 1–4. [Google Scholar] [CrossRef]
- Bażanów, B.A.; Frącka, A.B.; Jackulak, N.A.; Staroniewicz, Z.M.; Ploch, S.M. A 34-year retrospective study of equine viral abortion in Poland. Pol. J. Vet. Sci. 2014, 17, 607–612. [Google Scholar] [CrossRef]
- Equine viral arteritis: Not just a reproductive disease. Vet. Rec. 2019, 184, 791–793. [CrossRef] [PubMed]
- Cruz-Lopez, F.; Newton, R.; Sanchez-Rodriguez, A.; Ireland, J.; Mughini-Gras, L.; Moreno, M.A.; Fores, P. Equine viral arteritis in breeding and sport horses in central Spain. Res. Vet. Sci. 2017, 115, 88–91. [Google Scholar] [CrossRef] [PubMed]
- Lazić, S.; Lupulović, D.; Gaudaire, D.; Petrovic, T.; Lazić, G.; Hans, A. Serological evidence of equine arteritis virus infection and phylogenetic analysis of viral isolates in semen of stallions from Serbia. BMC Vet. Res. 2017, 13, 316. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Newton, J.R.; Wood, J.L.; Castillo-Olivares, F.J.; Mumford, J.A. Serological surveillance of equine viral arteritis in the United Kingdom since the outbreak in 1993. Vet. Rec. 1999, 145, 511–516. [Google Scholar] [CrossRef]
- Kölbl, S.; Schuller, W.; Pabst, J. Serologische Untersuchungen zur aktuellen Verseuchung österreichischer Pferde mit dem Virus der Equinen Arteritis [Serological studies of the recent infections of Austrian horses with the equine arteritis virus]. Dtsch. Tierarztl. Wochenschr. 1991, 98, 43–45. (In German) [Google Scholar]
- Szeredi, L.; Hornyák, A.; Pálfi, V.; Molnár, T.; Glávits, R.; Dénes, B. Study on the epidemiology of equine arteritis virus infection with different diagnostic techniques by investigating 96 cases of equine abortion in Hungary. Vet. Microbiol. 2005, 108, 235–242. [Google Scholar] [CrossRef]
- Grądzki, Z.; Boguta, L. Seroprevalence of EHV1 and EHV4 in the horse population of the southeastern part of Poland. Med. Wet. 2009, 65, 188–193. [Google Scholar]
- Patel, J.R.; Heldens, J. Equine herpesviruses 1 (EHV-1) and 4 (EHV-4)—Epidemiology, disease and immunoprophylaxis: A brief review. Vet. J. 2005, 170, 14–23. [Google Scholar] [CrossRef] [PubMed]
- Cruz, F.; Fores, P.; Mughini-Gras, L.; Ireland, J.; Moreno, M.A.; Newton, J.R. Seroprevalence and factors associated with equine herpesvirus type 1 and 4 in Spanish Purebred horses in Spain. Vet. Rec. 2016, 178, 398. [Google Scholar] [CrossRef] [PubMed]
- Holmes, D.F.; Kemen, M.J.; Coggins, L. Equine rhinovirus infection—Serologic evidence of infection in selected horse population. In Equine Infectious Diseases, 4th ed.; Bryans, J.T., Gerber, H., Eds.; Karger: Basel, Switzerland, 1978; pp. 315–319. [Google Scholar]
- De Boer, G.F.; Osterhaus, A.D.; van Oirschot, J.T.; Wemmenhove, R. Prevalence of antibodies to equine viruses in the Netherlands. Vet. Q. 1979, 1, 65–74. [Google Scholar] [CrossRef] [PubMed]
- Daly, J.M.; Yates, P.J.; Newton, J.R.; Park, A.; Henley, W.; Wood, J.L.N.; Davis-Poynter, N.; Mumford, J.A. Evidence supporting the inclusion of strains from each of the two co-circulating lineages of H3N8 equine influenza virus in vaccines. Vaccine 2004, 22, 4101–4109. [Google Scholar] [CrossRef]
- Webster, R.G. Are equine 1 influenza viruses still present in horses? Equine Vet. J. 1993, 25, 537–538. [Google Scholar] [CrossRef]
- Paillot, R.; Pitel, P.H.; Pronost, S.; Legrand, L.; Fougerolle, S.; Jourdan, M.; Marcillaud-Pitel, C. Florida clade 1 equine influenza virus in France. Vet. Rec. 2019, 184, 101. [Google Scholar] [CrossRef]
- Nemoto, M.; Ohta, M.; Yamanaka, T.; Kambayashi, Y.; Bannai, H.; Tsujimura, K.; Yamayoshi, S.; Kawaoka, Y.; Cullinane, A. Antigenic differences between equine influenza virus vaccine strains and Florida sublineage clade 1 strains isolated in Europe in 2019. Vet. J. 2021, 272, 105674. [Google Scholar] [CrossRef]
- Sovinová, O.; Tumová, B.; Pouska, F.; Nemec, J. Isolation of a virus causing respiratory disease in horses. Acta Virol. 1958, 2, 51–61. [Google Scholar]
- Guo, Y.; Wang, M.; Kawaoka, Y.; Gorman, O.; Ito, T.; Saito, T.; Webster, R.G. Characterisation of a new avian-like influenza A virus from horses in China. Virology 1992, 188, 245–255. [Google Scholar] [CrossRef]
- Adeyefa, C.A.O.; James, M.L.; McCauley, J.W. Antigenic and genetic analysis of equine influenza viruses from tropical Africa in 1991. Epidemiol. Infect. 1996, 117, 367–374. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Guo, L.; Wang, D.; Zhou, H.; Wu, C.; Gao, X.; Xiao, Y.; Ren, L.; Paranhos-Baccalà, G.; Shu, Y.; Jin, Q.; et al. Cross-reactivity between avian influenza A (H7N9) virus and divergent H7 subtypic- and heterosubtypic influenza A viruses. Sci. Rep. 2016, 6, 22045. [Google Scholar] [CrossRef] [Green Version]
- Soilemetzidou, E.S.; de Bruin, E.; Eschke, K.; Azab, W.; Osterrieder, N.; Czirják, G.Á.; Buuveibaatar, B.; Kaczensky, P.; Koopmans, M.; Walzer, C.; et al. Bearing the brunt: Mongolian khulan (Equus hemionus hemionus) are exposed to multiple influenza A strains. Vet. Microbiol. 2020, 242, 108605. [Google Scholar] [CrossRef] [PubMed]
- Olusa, T.A.O.; Adegunwa, A.K.; Aderonmu, A.A.; Adeyefa, C.A.O. Serologic evidence of equine H7 influenza virus in polo horses in Nigeria. Sci. World J. 2010, 5, 17–19. [Google Scholar] [CrossRef]
- Spokes, P.J.; Marich, A.J.; Musto, J.A.; Ward, K.A.; Craig, A.T.; McAnulty, J.M. Investigation of equine influenza transmission in NSW: Walk, wind or wing? N. S. W. Public Health Bull. 2009, 20, 152–156. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cadar, D.; Becker, N.; de Mendonca Campos, R.; Börstler, J.; Jöst, H.; Schmidt-Chanasit, J. Usutu virus in bats, Germany, 2013. Emerg. Infect. Dis. 2014, 20, 1771–1773. [Google Scholar] [CrossRef] [PubMed]
- Allering, L.; Jöst, H.; Emmerich, P.; Günther, S.; Lattwein, E.; Schmidt, M.; Seifried, E.; Sambri, V.; Hourfar, K.; Schmidt-Chanasit, J. Detection of Usutu virus infection in a healthy blood donor from south-west Germany, 2012. Eurosurveillance 2012, 17. [Google Scholar] [CrossRef]
- Barbic, L.; Vilibic-Cavlek, T.; Listes, E.; Stevanovic, V.; Gjenero-Margan, I.; Ljubin-Sternak, S.; Pem-Novosel, I.; Listes, I.; Mlinaric-Galinovic, G.; Di Gennaro, A.; et al. Demonstration of Usutu virus antibodies in horses, Croatia. Vector-Borne Zoonotic Dis. 2013, 13, 772–774. [Google Scholar] [CrossRef] [PubMed]
- Vilibic-Cavlek, T.; Petrovic, T.; Savic, V.; Barbic, L.; Tabain, I.; Stevanovic, V.; Klobucar, A.; Mrzljak, A.; Ilic, M.; Bogdanic, M.; et al. Epidemiology of Usutu Virus: The European Scenario. Pathogens 2020, 9, 699. [Google Scholar] [CrossRef]
- Juricová, Z.; Pinowski, J.; Literák, I.; Hahm, K.H.; Romanowski, J. Antibodies to alphavirus, flavivirus, and bunyavirus arboviruses in house sparrows (Passer domesticus) and tree sparrows (P. montanus) in Poland. Avian. Dis. 1998, 42, 182–185. [Google Scholar] [CrossRef]
- Vilibic-Cavlek, T.; Savic, V.; Petrovic, T.; Toplak, I.; Barbic, L.; Petric, D.; Tabain, I.; Hrnjakovic-Cvjetkovic, I.; Bogdanic, M.; Klobucar, A.; et al. Emerging Trends in the Epidemiology of West Nile and Usutu Virus Infections in Southern Europe. Front. Vet. Sci. 2019, 6, 437. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- OIE Equine Infectious Anaemia, Poland. Available online: https://www.oie.int/wahis_2/public/wahid.php/Reviewreport/Review?page_refer=MapFullEventReport&reportid=17935 (accessed on 17 June 2015).
Virus Tested | Number of Positive Results/Number of the Horses Tested | Percentage of Seropositive Horses (%) |
---|---|---|
equine arteritis virus | 0/20 | 0 |
equine herpes virus 1 | 12/20 | 60 |
equine rhinitis A virus | 1/20 | 5 |
equine influenza A virus H7N7 | 13/20 | 65 |
equine influenza A virus H3N8 | 12/20 | 60 |
Usutu virus | 5/20 | 25 |
West Nile virus | 0/20 | 0 |
equine infectious anaemia virus | 0/20 | 0 |
No. | Sex | Age (Years) | Obtained Titres of Antibodies | |||||||
---|---|---|---|---|---|---|---|---|---|---|
EAV | EHV1 | ERAV | H7N7 | H3N8 | USUV | WNV | EIAV | |||
1 | mare | 10 | 0 | 0 | 0 | 40 | 20 | 40 | 0 | 0 |
2 | mare | 9 | 0 | 16 | 0 | 0 | 20 | 80 | 0 | 0 |
3 | mare | 5 | 0 | 0 | 0 | 20 | 0 | 20 | 0 | 0 |
4 | mare | 10 | 0 | 32 | 8 | 0 | 0 | 20 | 0 | 0 |
5 | mare | 5 | 0 | 0 | 0 | 20 | 0 | 0 | 0 | 0 |
6 | mare | 8 | 0 | 0 | 0 | 0 | 80 | 0 | 0 | 0 |
7 | mare | 10 | 0 | 0 | 0 | 20 | 20 | 0 | 0 | 0 |
8 | mare | 5 | 0 | 8 | 0 | 40 | 40 | 0 | 0 | 0 |
9 | mare | 5 | 0 | 32 | 0 | 40 | 40 | 0 | 0 | 0 |
10 | mare | 9 | 0 | 32 | 0 | 0 | 40 | 0 | 0 | 0 |
11 | stallion | 5 | 0 | 0 | 0 | 80 | 40 | 0 | 0 | 0 |
12 | stallion | 6 | 0 | 32 | 0 | 20 | 0 | 10 | 0 | 0 |
13 | stallion | 6 | 0 | 8 | 0 | 20 | 20 | 0 | 0 | 0 |
14 | stallion | 5 | 0 | 32 | 0 | 0 | 0 | 0 | 0 | 0 |
15 | stallion | 5 | 0 | 16 | 0 | 20 | 0 | 0 | 0 | 0 |
16 | stallion | 5 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 |
17 | stallion | 9 | 0 | 16 | 0 | 20 | 20 | 0 | 0 | 0 |
18 | stallion | 10 | 0 | 8 | 0 | 0 | 20 | 0 | 0 | 0 |
19 | stallion | 9 | 0 | 16 | 0 | 20 | 0 | 0 | 0 | 0 |
20 | stallion | 5 | 0 | 0 | 0 | 20 | 20 | 0 | 0 | 0 |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Bażanów, B.; Pawęska, J.T.; Pogorzelska, A.; Florek, M.; Frącka, A.; Gębarowski, T.; Chwirot, W.; Stygar, D. Serological Evidence of Common Equine Viral Infections in a Semi-Isolated, Unvaccinated Population of Hucul Horses. Animals 2021, 11, 2261. https://doi.org/10.3390/ani11082261
Bażanów B, Pawęska JT, Pogorzelska A, Florek M, Frącka A, Gębarowski T, Chwirot W, Stygar D. Serological Evidence of Common Equine Viral Infections in a Semi-Isolated, Unvaccinated Population of Hucul Horses. Animals. 2021; 11(8):2261. https://doi.org/10.3390/ani11082261
Chicago/Turabian StyleBażanów, Barbara, Janusz T. Pawęska, Aleksandra Pogorzelska, Magdalena Florek, Agnieszka Frącka, Tomasz Gębarowski, Wojciech Chwirot, and Dominika Stygar. 2021. "Serological Evidence of Common Equine Viral Infections in a Semi-Isolated, Unvaccinated Population of Hucul Horses" Animals 11, no. 8: 2261. https://doi.org/10.3390/ani11082261
APA StyleBażanów, B., Pawęska, J. T., Pogorzelska, A., Florek, M., Frącka, A., Gębarowski, T., Chwirot, W., & Stygar, D. (2021). Serological Evidence of Common Equine Viral Infections in a Semi-Isolated, Unvaccinated Population of Hucul Horses. Animals, 11(8), 2261. https://doi.org/10.3390/ani11082261