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Viruses2019; 11(10); 916; doi: 10.3390/v11100916

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.

Abstract: Equine herpesvirus 1 (EHV-1) is an Alphaherpesvirus infecting not only horses but also other equid and non-equid mammals. It can cause respiratory distress, stillbirth and neonatal death, abortion, and neurological disease. The different forms of disease induced by EHV-1 infection can have dramatic consequences on the equine industry, and thus the virus represents a great challenge for the equine and scientific community. This report describes the progress of a major EHV-1 outbreak that took place in Normandy in 2009, during which the three forms of disease were observed. A collection of EHV-1 strains isolated in France and Belgium from 2012 to 2018 were subsequently genetically analysed in order to characterise EHV-1 strain circulation. The open reading frame 30 (ORF30) non-neuropathogenic associated mutation A was the most represented among 148 samples analysed in this study. ORF30 was also sequenced for 14 strains and compared to previously published sequences. Finally, a more global phylogenetic approach was performed based on a recently described Multilocus Sequence Typing (MLST) method. French and Belgian strains were clustered with known strains isolated in United Kingdom and Ireland, with no correlation between the phylogeny and the time of collection or location. This new MLST approach could be a tool to help understand epidemics in stud farms.
Publication Date: 2019-10-04 PubMed ID: 31590336PubMed Central: PMC6832873DOI: 10.3390/v11100916Google Scholar: Lookup
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  • Journal Article
  • Research Support
  • Non-U.S. Gov't

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research paper investigates the molecular patterns of the Equine herpesvirus 1 (EHV-1) that circulated in France during and after an outbreak in 2009. It also explores how the virus might have evolved and migrated over time by genetically analysing samples taken from 2012 to 2018 in France and Belgium.

Context and Purpose

  • The research focuses on Equine herpesvirus 1 (EHV-1), a type of Alphaherpesvirus. This virus affects horses, other equid mammals, and non-equid animals leading to various diseases such as respiratory infection, abortion, stillbirth/neonatal death, and neurological disorders.
  • Different forms of the disease caused by EHV-1 infection can have significant ramifications for the equine industry. Therefore, there is a strong need for effective monitoring and treatment options to control its spread.
  • The specific interest in this study is to understand the progression and characteristics of EHV-1 during an outbreak in Normandy, France, in 2009, as well as its subsequent spread over a span of six years (2012 to 2018) in France and Belgium.

Procedures and Findings

  • The researchers analysed a collection of EHV-1 strains that were isolated from 2012 to 2018. Genetic analysis was conducted to characterise the circulation of these strains.
  • The emphasis was on the non-neuropathogenic associated mutation A in the open reading frame 30 (ORF30), the most represented mutation among the 148 samples analysed.
  • In addition to this, ORF30 of 14 strains was sequenced and compared with previously published sequences aiding the understanding of the genetic lineage and potential mutative behaviours of the virus.

Analysis Technique and Conclusions

  • A phylogenetic approach based on the Multilocus Sequence Typing (MLST) method was used for a more global approach. This method classifies different strains of the same species based on the sequences of several housekeeping genes.
  • The analysis showed that French and Belgian strains clustered with known strains isolated in the UK and Ireland. It was found that there was no correlation between the phylogeny and the time of collection or location.
  • The researchers concluded that this new MLST approach could be a useful tool to help understand epidemics in stud farms and prepare better for them.

Cite This Article

APA
Sutton G, Garvey M, Cullinane A, Jourdan M, Fortier C, Moreau P, Foursin M, Gryspeerdt A, Maisonnier V, Marcillaud-Pitel C, Legrand L, Paillot R, Pronost S. (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. https://doi.org/10.3390/v11100916

Publication

ISSN: 1999-4915
NlmUniqueID: 101509722
Country: Switzerland
Language: English
Volume: 11
Issue: 10
PII: 916

Researcher Affiliations

Sutton, Gabrielle
  • LABÉO Frank Duncombe, 14280 Saint-Contest, France. gabrielle.sutton@laboratoire-labeo.fr.
  • NORMANDIE UNIV, UNICAEN, BIOTARGEN, 14000 Caen, France. gabrielle.sutton@laboratoire-labeo.fr.
Garvey, Marie
  • Irish Equine Centre, Johnstown, Naas, County Kildare, W91 RH93, Ireland. MGarvey@irishequinecentre.ie.
Cullinane, Ann
  • Irish Equine Centre, Johnstown, Naas, County Kildare, W91 RH93, Ireland. ACullinane@irishequinecentre.ie.
Jourdan, Marion
  • RESPE, 14280 Saint-Contest, France. technicien@respe.net.
Fortier, Christine
  • LABÉO Frank Duncombe, 14280 Saint-Contest, France. christine.fortier@laboratoire-labeo.fr.
  • NORMANDIE UNIV, UNICAEN, BIOTARGEN, 14000 Caen, France. christine.fortier@laboratoire-labeo.fr.
Moreau, Peggy
  • Clinique équine de la Boisrie, 61500, Chailloué, France. peg_moreau@yahoo.fr.
Foursin, Marc
  • Clinique équine de la Boisrie, 61500, Chailloué, France. clin.eq.laboisrie@laposte.net.
Gryspeerdt, Annick
  • Equi Focus Point Belgium, 8900 Ypres, Belgium. loic.legrand@laboratoire-labeo.fr.
Maisonnier, Virginie
  • RESPE, 14280 Saint-Contest, France. contact@respe.net.
Marcillaud-Pitel, Christel
  • RESPE, 14280 Saint-Contest, France. romain.paillot@laboratoire-labeo.fr.
Legrand, Loïc
  • LABÉO Frank Duncombe, 14280 Saint-Contest, France. stephane.pronost@laboratoire-labeo.fr.
  • NORMANDIE UNIV, UNICAEN, BIOTARGEN, 14000 Caen, France. stephane.pronost@laboratoire-labeo.fr.
Paillot, Romain
  • LABÉO Frank Duncombe, 14280 Saint-Contest, France. c.marcillaud-pitel@respe.net.
  • NORMANDIE UNIV, UNICAEN, BIOTARGEN, 14000 Caen, France. c.marcillaud-pitel@respe.net.
Pronost, Stéphane
  • LABÉO Frank Duncombe, 14280 Saint-Contest, France. annick.gryspeerdt@gmail.com.
  • NORMANDIE UNIV, UNICAEN, BIOTARGEN, 14000 Caen, France. annick.gryspeerdt@gmail.com.

MeSH Terms

  • Abortion, Veterinary / epidemiology
  • Abortion, Veterinary / virology
  • Animals
  • Belgium / epidemiology
  • DNA, Viral / genetics
  • Disease Outbreaks
  • Female
  • France / epidemiology
  • Herpesviridae Infections / epidemiology
  • Herpesvirus 1, Equid / classification
  • Herpesvirus 1, Equid / genetics
  • Herpesvirus 1, Equid / isolation & purification
  • Horse Diseases / epidemiology
  • Horse Diseases / virology
  • Horses
  • Male
  • Multilocus Sequence Typing
  • Nervous System Diseases / epidemiology
  • Open Reading Frames
  • Phylogeny
  • Respiratory Tract Infections / epidemiology
  • Respiratory Tract Infections / veterinary
  • United Kingdom

Conflict of Interest Statement

The authors declare no conflict of interest.

References

This article includes 44 references
  1. Davison AJ, Eberle R, Ehlers B, Hayward GS, McGeoch DJ, Minson AC, Pellett PE, Roizman B, Studdert MJ, Thiry E. The order Herpesvirales.. Arch Virol 2009;154(1):171-7.
    doi: 10.1007/s00705-008-0278-4pmc: PMC3552636pubmed: 19066710google scholar: lookup
  2. Abdelgawad A, Azab W, Damiani AM, Baumgartner K, Will H, Osterrieder N, Greenwood AD. Zebra-borne equine herpesvirus type 1 (EHV-1) infection in non-African captive mammals.. Vet Microbiol 2014 Feb 21;169(1-2):102-6.
    doi: 10.1016/j.vetmic.2013.12.011pubmed: 24440374google scholar: lookup
  3. Wohlsein P, Lehmbecker A, Spitzbarth I, Algermissen D, Baumgärtner W, Böer M, Kummrow M, Haas L, Grummer B. Fatal epizootic equine herpesvirus 1 infections in new and unnatural hosts.. Vet Microbiol 2011 May 5;149(3-4):456-60.
    doi: 10.1016/j.vetmic.2010.11.024pubmed: 21167662google scholar: lookup
  4. Chowdhury SI, Ludwig H, Buhk HJ. Molecular biological characterization of equine herpesvirus type 1 (EHV-1) isolates from ruminant hosts.. Virus Res 1988 Sep;11(2):127-39.
    doi: 10.1016/0168-1702(88)90038-Xpubmed: 2849252google scholar: lookup
  5. Ghanem YM, Fukushi H, Ibrahim ES, Ohya K, Yamaguchi T, Kennedy M. Molecular phylogeny of equine herpesvirus 1 isolates from onager, zebra and Thomson's gazelle.. Arch Virol 2008;153(12):2297-302.
    doi: 10.1007/s00705-008-0247-ypubmed: 19002555google scholar: lookup
  6. Dayaram A, Franz M, Schattschneider A, Damiani AM, Bischofberger S, Osterrieder N, Greenwood AD. Long term stability and infectivity of herpesviruses in water.. Sci Rep 2017 Apr 21;7:46559.
    doi: 10.1038/srep46559pmc: PMC5399353pubmed: 28429732google scholar: lookup
  7. Paillot R, Case R, Ross J, Newton R, Nugent J. Equine Herpes Virus-1: Virus, Immunity and Vaccines. Open Vet. Sci. J. 2008;2:68–91.
  8. Lunn DP, Davis-Poynter N, Flaminio MJ, Horohov DW, Osterrieder K, Pusterla N, Townsend HG. Equine herpesvirus-1 consensus statement.. J Vet Intern Med 2009 May-Jun;23(3):450-61.
  9. Chesters PM, Allsop R, Purewal A, Edington N. Detection of latency-associated transcripts of equid herpesvirus 1 in equine leukocytes but not in trigeminal ganglia.. J Virol 1997 May;71(5):3437-43.
  10. Aleman M, Pickles KJ, Simonek G, Madigan JE. Latent equine herpesvirus-1 in trigeminal ganglia and equine idiopathic headshaking.. J Vet Intern Med 2012 Jan-Feb;26(1):192-4.
  11. Rock DL. The molecular basis of latent infections by alphaherpesviruses. Semin. Virol. 1993;4:157–165.
    doi: 10.1006/smvy.1993.1011google scholar: lookup
  12. Gulati BR, Sharma H, Riyesh T, Khurana SK, Kapoor S. Viral and Host Strategies for Regulation of Latency and Reactivation in Equid Herpesviruses. Asian J. Anim. Vet. Adv. 2015;10:669–689.
  13. Telford EA, Watson MS, McBride K, Davison AJ. The DNA sequence of equine herpesvirus-1.. Virology 1992 Jul;189(1):304-16.
    doi: 10.1016/0042-6822(92)90706-Upubmed: 1318606google scholar: lookup
  14. Bryant NA, Wilkie GS, Russell CA, Compston L, Grafham D, Clissold L, McLay K, Medcalf L, Newton R, Davison AJ, Elton DM. Genetic diversity of equine herpesvirus 1 isolated from neurological, abortigenic and respiratory disease outbreaks.. Transbound Emerg Dis 2018 Jun;65(3):817-832.
    doi: 10.1111/tbed.12809pmc: PMC5947664pubmed: 29423949google scholar: lookup
  15. Cuxson JL, Hartley CA, Ficorilli NP, Symes SJ, Devlin JM, Gilkerson JR. Comparing the genetic diversity of ORF30 of Australian isolates of 3 equid alphaherpesviruses.. Vet Microbiol 2014 Feb 21;169(1-2):50-7.
    doi: 10.1016/j.vetmic.2013.12.007pubmed: 24418044google scholar: lookup
  16. Crowhurst FA, Dickinson G, Burrows R. An outbreak of paresis in mares and geldings associated with equid herpesvirus 1.. Vet Rec 1981 Dec 12;109(24):527-8.
    pubmed: 6280366
  17. Mumford JA, Rossdale PD, Jessett DM, Gann SJ, Ousey J, Cook RF. Serological and virological investigations of an equid herpesvirus 1 (EHV-1) abortion storm on a stud farm in 1985.. J Reprod Fertil Suppl 1987;35:509-18.
    pubmed: 2824770
  18. Anagha G, Gulati BR, Riyesh T, Virmani N. Genetic characterization of equine herpesvirus 1 isolates from abortion outbreaks in India.. Arch Virol 2017 Jan;162(1):157-163.
    doi: 10.1007/s00705-016-3097-zpubmed: 27699511google scholar: lookup
  19. Nugent J, Birch-Machin I, Smith KC, Mumford JA, Swann Z, Newton JR, Bowden RJ, Allen GP, Davis-Poynter N. Analysis of equid herpesvirus 1 strain variation reveals a point mutation of the DNA polymerase strongly associated with neuropathogenic versus nonneuropathogenic disease outbreaks.. J Virol 2006 Apr;80(8):4047-60.
  20. Goodman LB, Loregian A, Perkins GA, Nugent J, Buckles EL, Mercorelli B, Kydd JH, Palù G, Smith KC, Osterrieder N, Davis-Poynter N. A point mutation in a herpesvirus polymerase determines neuropathogenicity.. PLoS Pathog 2007 Nov;3(11):e160.
  21. Pronost S, Léon A, Legrand L, Fortier C, Miszczak F, Freymuth F, Fortier G. Neuropathogenic and non-neuropathogenic variants of equine herpesvirus 1 in France.. Vet Microbiol 2010 Oct 26;145(3-4):329-33.
    doi: 10.1016/j.vetmic.2010.03.031pubmed: 20427133google scholar: lookup
  22. Allen GP. Development of a real-time polymerase chain reaction assay for rapid diagnosis of neuropathogenic strains of equine herpesvirus-1.. J Vet Diagn Invest 2007 Jan;19(1):69-72.
    doi: 10.1177/104063870701900110pubmed: 17459834google scholar: lookup
  23. Van de Walle GR, Goupil R, Wishon C, Damiani A, Perkins GA, Osterrieder N. A single-nucleotide polymorphism in a herpesvirus DNA polymerase is sufficient to cause lethal neurological disease.. J Infect Dis 2009 Jul 1;200(1):20-5.
    doi: 10.1086/599316pubmed: 19456260google scholar: lookup
  24. Franz M, Goodman LB, Van de Walle GR, Osterrieder N, Greenwood AD. A Point Mutation in a Herpesvirus Co-Determines Neuropathogenicity and Viral Shedding.. Viruses 2017 Jan 10;9(1).
    doi: 10.3390/v9010006pmc: PMC5294975pubmed: 28075374google scholar: lookup
  25. Gryspeerdt A, Vandekerckhove A, Van Doorsselaere J, Van de Walle G, Nauwynck H. Description of an unusually large outbreak of nervous system disorders caused by equine herpesvirus 1 (EHV1) in 2009 in Belgium. Vlaams Diergeneeskundig Tijdschrif. 2011;80:147–153.
  26. Garvey M, Lyons R, Hector RD, Walsh C, Arkins S, Cullinane A. Molecular Characterisation of Equine Herpesvirus 1 Isolates from Cases of Abortion, Respiratory and Neurological Disease in Ireland between 1990 and 2017.. Pathogens 2019 Jan 15;8(1).
    doi: 10.3390/pathogens8010007pmc: PMC6471309pubmed: 30650561google scholar: lookup
  27. Pronost S, Legrand L, Pitel PH, Wegge B, Lissens J, Freymuth F, Richard E, Fortier G. Outbreak of equine herpesvirus myeloencephalopathy in France: a clinical and molecular investigation.. Transbound Emerg Dis 2012 Jun;59(3):256-63.
  28. Diallo IS, Hewitson G, Wright L, Rodwell BJ, Corney BG. Detection of equine herpesvirus type 1 using a real-time polymerase chain reaction.. J Virol Methods 2006 Jan;131(1):92-8.
  29. Thieulent CJ, Hue ES, Fortier CI, Dallemagne P, Zientara S, Munier-Lehmann H, Hans A, Fortier GD, Pitel PH, Vidalain PO, Pronost SL. Screening and evaluation of antiviral compounds against Equid alpha-herpesviruses using an impedance-based cellular assay.. Virology 2019 Jan 2;526:105-116.
    doi: 10.1016/j.virol.2018.10.013pubmed: 30388626google scholar: lookup
  30. Hall T. BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 1999;41:95–98.
  31. CodonCode Aligner. [(accessed on 27 September 2019)]; Available online: https://www.codoncode.com.
  32. Kumar S, Stecher G, Tamura K. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets.. Mol Biol Evol 2016 Jul;33(7):1870-4.
    doi: 10.1093/molbev/msw054pmc: PMC8210823pubmed: 27004904google scholar: lookup
  33. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees.. Mol Biol Evol 1987 Jul;4(4):406-25.
  34. Jones DT, Taylor WR, Thornton JM. The rapid generation of mutation data matrices from protein sequences.. Comput Appl Biosci 1992 Jun;8(3):275-82.
    doi: 10.1093/bioinformatics/8.3.275pubmed: 1633570google scholar: lookup
  35. Madeira F, Park YM, Lee J, Buso N, Gur T, Madhusoodanan N, Basutkar P, Tivey ARN, Potter SC, Finn RD, Lopez R. The EMBL-EBI search and sequence analysis tools APIs in 2019.. Nucleic Acids Res 2019 Jul 2;47(W1):W636-W641.
    doi: 10.1093/nar/gkz268pmc: PMC6602479pubmed: 30976793google scholar: lookup
  36. PopART. [(accessed on 27 September 2019)]; Available online: http://popart.otago.ac.nz.
  37. Huson DH, Bryant D. Application of phylogenetic networks in evolutionary studies.. Mol Biol Evol 2006 Feb;23(2):254-67.
    doi: 10.1093/molbev/msj030pubmed: 16221896google scholar: lookup
  38. Bryant D, Moulton V. Neighbor-net: an agglomerative method for the construction of phylogenetic networks.. Mol Biol Evol 2004 Feb;21(2):255-65.
    doi: 10.1093/molbev/msh018pubmed: 14660700google scholar: lookup
  39. Walter J, Seeh C, Fey K, Bleul U, Osterrieder N. Clinical observations and management of a severe equine herpesvirus type 1 outbreak with abortion and encephalomyelitis.. Acta Vet Scand 2013 Mar 5;55(1):19.
    doi: 10.1186/1751-0147-55-19pmc: PMC3630004pubmed: 23497661google scholar: lookup
  40. Vissani MA, Becerra ML, Olguín Perglione C, Tordoya MS, Miño S, Barrandeguy M. Neuropathogenic and non-neuropathogenic genotypes of Equid Herpesvirus type 1 in Argentina.. Vet Microbiol 2009 Nov 18;139(3-4):361-4.
    doi: 10.1016/j.vetmic.2009.06.025pubmed: 19589651google scholar: lookup
  41. Pronost S, Cook RF, Fortier G, Timoney PJ, Balasuriya UB. Relationship between equine herpesvirus-1 myeloencephalopathy and viral genotype.. Equine Vet J 2010 Nov;42(8):672-4.
  42. Lechmann J, Schoster A, Ernstberger M, Fouché N, Fraefel C, Bachofen C. A novel PCR protocol for detection and differentiation of neuropathogenic and non-neuropathogenic equid alphaherpesvirus 1.. J Vet Diagn Invest 2019 Sep;31(5):696-703.
    doi: 10.1177/1040638719871975pmc: PMC6727124pubmed: 31477001google scholar: lookup
  43. Liu S, Knafels JD, Chang JS, Waszak GA, Baldwin ET, Deibel MR Jr, Thomsen DR, Homa FL, Wells PA, Tory MC, Poorman RA, Gao H, Qiu X, Seddon AP. Crystal structure of the herpes simplex virus 1 DNA polymerase.. J Biol Chem 2006 Jun 30;281(26):18193-200.
    doi: 10.1074/jbc.M602414200pubmed: 16638752google scholar: lookup
  44. Zarrouk K, Piret J, Boivin G. Herpesvirus DNA polymerases: Structures, functions and inhibitors.. Virus Res 2017 Apr 15;234:177-192.

Citations

This article has been cited 11 times.
  1. Li Z, He Y, Ge L, Quan R, Chen J, Hu Y, Sa R, Liu J, Ran D, Fu Q, Shi H. Berbamine, a bioactive alkaloid, suppresses equine herpesvirus type 1 in vitro and in vivo.. Front Vet Sci 2023;10:1163780.
    doi: 10.3389/fvets.2023.1163780pubmed: 37303732google scholar: lookup
  2. Thieulent CJ, Sutton G, Toquet MP, Fremaux S, Hue E, Fortier C, Pléau A, Deslis A, Abrioux S, Guitton E, Pronost S, Paillot R. Oral Administration of Valganciclovir Reduces Clinical Signs, Virus Shedding and Cell-Associated Viremia in Ponies Experimentally Infected with the Equid Herpesvirus-1 C(2254) Variant.. Pathogens 2022 May 4;11(5).
    doi: 10.3390/pathogens11050539pubmed: 35631060google scholar: lookup
  3. Nielsen SS, Alvarez J, Bicout DJ, Calistri P, Canali E, Drewe JA, Garin-Bastuji B, Gonzales Rojas JL, Gortázar C, Herskin M, Michel V, Miranda Chueca MÁ, Roberts HC, Padalino B, Pasquali P, Spoolder H, Ståhl K, Calvo AV, Viltrop A, Winckler C, Carvelli A, Paillot R, Broglia A, Kohnle L, Baldinelli F, Van der Stede Y. Assessment of listing and categorisation of animal diseases within the framework of the Animal Health Law (Regulation (EU) No 2016/429): infection with Equine Herpesvirus-1.. EFSA J 2022 Jan;20(1):e07036.
    doi: 10.2903/j.efsa.2022.7036pubmed: 35035581google scholar: lookup
  4. Sutton G, Normand C, Carnet F, Couroucé A, Garvey M, Castagnet S, Fortier CI, Hue ES, Marcillaud-Pitel C, Legrand L, Paillot R, Pitel PH, Cullinane A, Pronost S. Equine Herpesvirus 1 Variant and New Marker for Epidemiologic Surveillance, Europe, 2021.. Emerg Infect Dis 2021 Oct;27(10):2738-2739.
    doi: 10.3201/eid2710.210704pubmed: 34546162google scholar: lookup
  5. Moustafa AM, Planet PJ. Emerging SARS-CoV-2 Diversity Revealed by Rapid Whole-Genome Sequence Typing.. Genome Biol Evol 2021 Sep 1;13(9).
    doi: 10.1093/gbe/evab197pubmed: 34432021google scholar: lookup
  6. Vereecke N, Carnet F, Pronost S, Vanschandevijl K, Theuns S, Nauwynck H. Genome Sequences of Equine Herpesvirus 1 Strains from a European Outbreak of Neurological Disorders Linked to a Horse Gathering in Valencia, Spain, in 2021.. Microbiol Resour Announc 2021 May 20;10(20).
    doi: 10.1128/MRA.00333-21pubmed: 34016681google scholar: lookup
  7. Kang HW, Lee EY, Lee KK, Ko MK, Park JY, Kim YH, Lee K, Choi EJ, Kim J, So B, Park CK, Jeoung HY. Evaluation of the Variability of the ORF34, ORF68, and MLST Genes in EHV-1 from South Korea.. Pathogens 2021 Apr 2;10(4).
    doi: 10.3390/pathogens10040425pubmed: 33918404google scholar: lookup
  8. Sutton G, Thieulent C, Fortier C, Hue ES, Marcillaud-Pitel C, Pléau A, Deslis A, Guitton E, Paillot R, Pronost S. Identification of a New Equid Herpesvirus 1 DNA Polymerase (ORF30) Genotype with the Isolation of a C(2254)/H(752) Strain in French Horses Showing no Major Impact on the Strain Behaviour.. Viruses 2020 Oct 13;12(10).
    doi: 10.3390/v12101160pubmed: 33066315google scholar: lookup
  9. Stasiak K, Dunowska M, Rola J. Outbreak of equid herpesvirus 1 abortions at the Arabian stud in Poland.. BMC Vet Res 2020 Oct 6;16(1):374.
    doi: 10.1186/s12917-020-02586-ypubmed: 33023592google scholar: lookup
  10. Paillot R. Special Issue "Equine Viruses": Old "Friends" and New Foes?. Viruses 2020 Jan 29;12(2).
    doi: 10.3390/v12020153pubmed: 32013127google scholar: lookup
  11. Lecollinet S, Pronost S, Coulpier M, Beck C, Gonzalez G, Leblond A, Tritz P. Viral Equine Encephalitis, a Growing Threat to the Horse Population in Europe?. Viruses 2019 Dec 24;12(1).
    doi: 10.3390/v12010023pubmed: 31878129google scholar: lookup