Analyze Diet
Journal of virology2006; 80(8); 4047-4060; doi: 10.1128/JVI.80.8.4047-4060.2006

Analysis of equid herpesvirus 1 strain variation reveals a point mutation of the DNA polymerase strongly associated with neuropathogenic versus nonneuropathogenic disease outbreaks.

Abstract: Equid herpesvirus 1 (EHV-1) can cause a wide spectrum of diseases ranging from inapparent respiratory infection to the induction of abortion and, in extreme cases, neurological disease resulting in paralysis and ultimately death. It has been suggested that distinct strains of EHV-1 that differ in pathogenic capacity circulate in the field. In order to investigate this hypothesis, it was necessary to identify genetic markers that allow subgroups of related strains to be identified. We have determined all of the genetic differences between a neuropathogenic strain (Ab4) and a nonneuropathogenic strain (V592) of EHV-1 and developed PCR/sequencing procedures enabling differentiation of EHV-1 strains circulating in the field. The results indicate the occurrence of several major genetic subgroups of EHV-1 among isolates recovered from outbreaks over the course of 30 years, consistent with the proposal that distinct strains of EHV-1 circulate in the field. Moreover, there is evidence that certain strain groups are geographically restricted, being recovered predominantly from outbreaks occurring in either North America or Europe. Significantly, variation of a single amino acid of the DNA polymerase is strongly associated with neurological versus nonneurological disease outbreaks. Strikingly, this variant amino acid occurs at a highly conserved position for herpesvirus DNA polymerases, suggesting an important functional role.
Publication Date: 2006-03-31 PubMed ID: 16571821PubMed Central: PMC1440451DOI: 10.1128/JVI.80.8.4047-4060.2006Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
  • 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.

This research investigated the genetic differences in strains of equid herpesvirus 1 (EHV-1) and discovered a single DNA polymerase variation strongly linked to outbreaks of neurological versus nonneurological diseases.

Background and Objectives

  • EQUID herpesvirus 1 (EHV-1) is known for causing various diseases, including respiratory infections, abortion, paralysis and sometimes death in extreme conditions. The study sought to understand whether specific EHV-1 strains with different pathogenic capacities were present continuously.
  • The need to identify genetic indicators that could help identify related strain groups was crucial to this investigation.

Methodology

  • The study focused on the genetic differences between a neuropathogenic strain (Ab4) and a nonneuropathogenic strain (V592) of EHV-1.
  • PCR/sequencing procedures were developed to differentiate circulating EHV-1 strains.

Results and Discussion

  • The study found several major genetic subgroups of EHV-1 among isolates collected from outbreaks over a 30-year span. This finding was consistent with the hypothesis that distinct EHV-1 strains are continually present in the field.
  • It was also discovered that certain strain groups were geographically bound, being predominantly found in North America or Europe.
  • Notably, the single amino acid variation in the DNA polymerase was firmly linked to neurological versus nonneurological disease outbreaks. The role of this variant was emphasized due to its position at a highly conserved location for herpesvirus DNA polymerases.

Implications

  • The study has significant implications for understanding the nature of EHV-1 strains and their distinct impacts, potentially paving the way for more effective and precise responses to different EHV-1 outbreak types in the future.
  • The specific DNA polymerase variation identified could serve as a vital marker for predicting the nature of disease outbreaks, whether neurological or nonneurological.

Cite This Article

APA
Nugent J, Birch-Machin I, Smith KC, Mumford JA, Swann Z, Newton JR, Bowden RJ, Allen GP, Davis-Poynter N. (2006). 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, 80(8), 4047-4060. https://doi.org/10.1128/JVI.80.8.4047-4060.2006

Publication

ISSN: 0022-538X
NlmUniqueID: 0113724
Country: United States
Language: English
Volume: 80
Issue: 8
Pages: 4047-4060

Researcher Affiliations

Nugent, J
  • Animal Health Trust, Lanwades Park, Kentford, Newmarket, Suffolk CB8 7UU, United Kingdom.
Birch-Machin, I
    Smith, K C
      Mumford, J A
        Swann, Z
          Newton, J R
            Bowden, R J
              Allen, G P
                Davis-Poynter, N

                  MeSH Terms

                  • Amino Acid Sequence
                  • Animals
                  • Base Sequence
                  • DNA-Directed DNA Polymerase / chemistry
                  • DNA-Directed DNA Polymerase / genetics
                  • Disease Outbreaks
                  • Herpesvirus 1, Equid / classification
                  • Herpesvirus 1, Equid / genetics
                  • Herpesvirus 1, Equid / pathogenicity
                  • Horse Diseases / epidemiology
                  • Horses
                  • Molecular Sequence Data
                  • Open Reading Frames
                  • Point Mutation
                  • Polymorphism, Single Nucleotide

                  References

                  This article includes 62 references
                  1. Allen GP, Kydd JH, Slater JD, Smith KC. Advances in understanding the pathogenesis, epidemiology and immunological control of equid herpes-1 (EHV-1) abortion. Equine infectious diseases VIII p. 129-146.
                  2. Allen GP, Yeargan MR, Bryans JT. Alterations in the equine herpesvirus 1 genome after in vitro and in vivo virus passage.. Infect Immun 1983 Apr;40(1):436-9.
                    pmc: PMC264868pubmed: 6299965doi: 10.1128/iai.40.1.436-439.1983google scholar: lookup
                  3. Allen GP, Yeargan MR, Turtinen LW, Bryans JT. A new field strain of equine abortion virus (equine herpesvirus-1) among Kentucky horses.. Am J Vet Res 1985 Jan;46(1):138-40.
                    pubmed: 2982294
                  4. Allen GP, Yeargan MR, Turtinen LW, Bryans JT, McCollum WH. Molecular epizootiologic studies of equine herpesvirus-1 infections by restriction endonuclease fingerprinting of viral DNA.. Am J Vet Res 1983 Feb;44(2):263-71.
                    pubmed: 6299145
                  5. Bandelt HJ, Forster P, Sykes BC, Richards MB. Mitochondrial portraits of human populations using median networks.. Genetics 1995 Oct;141(2):743-53.
                    pmc: PMC1206770pubmed: 8647407doi: 10.1093/genetics/141.2.743google scholar: lookup
                  6. Bass EP. Immunization with a modified live virus equine rhinopneumonitis vaccine and an aluminum hydroxide absorbed equine influenza vaccine. Proc. Am. Assoc. Equine Pract. 24:65-74.
                  7. Beckenaur WH, Bass EP. A modified live virus vaccine for equine rhinopneumonitis. J. Am. Vet. Med. Assoc. 163:1182.
                  8. Binns MM, McCann S, Zhang L, Wood J, Mumford JA. Molecular epidemiology of EHV-1 and EHV-4: a search for variable restriction sites. Equine infectious diseases VII p. 237-241.
                  9. Blunden AS, Whitwell KE, Pegler KM. An outbreak of paralysis associated with equine herpes virus type 1 infection in a livery stable. Prog. Vet. Neurol. 3:95-100.
                  10. Chou S. Comparative analysis of sequence variation in gp116 and gp55 components of glycoprotein B of human cytomegalovirus.. Virology 1992 May;188(1):388-90.
                    pubmed: 1314465doi: 10.1016/0042-6822(92)90771-ggoogle scholar: lookup
                  11. Chou S, Lurain NS, Weinberg A, Cai GY, Sharma PL, Crumpacker CS. Interstrain variation in the human cytomegalovirus DNA polymerase sequence and its effect on genotypic diagnosis of antiviral drug resistance. Adult AIDS Clinical Trials Group CMV Laboratories.. Antimicrob Agents Chemother 1999 Jun;43(6):1500-2.
                    pmc: PMC89307pubmed: 10348781doi: 10.1128/aac.43.6.1500google scholar: lookup
                  12. Chou S, Lurain NS, Thompson KD, Miner RC, Drew WL. Viral DNA polymerase mutations associated with drug resistance in human cytomegalovirus.. J Infect Dis 2003 Jul 1;188(1):32-9.
                    pubmed: 12825168doi: 10.1086/375743google scholar: lookup
                  13. Chou SW, Dennison KM. Analysis of interstrain variation in cytomegalovirus glycoprotein B sequences encoding neutralization-related epitopes.. J Infect Dis 1991 Jun;163(6):1229-34.
                    pubmed: 1709960doi: 10.1093/infdis/163.6.1229google scholar: lookup
                  14. 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
                  15. Darlington J, Super M, Patel K, Grundy JE, Griffiths PD, Emery VC. Use of the polymerase chain reaction to analyse sequence variation within a major neutralizing epitope of glycoprotein B (gp58) in clinical isolates of human cytomegalovirus.. J Gen Virol 1991 Aug;72 ( Pt 8):1985-9.
                    pubmed: 1714945doi: 10.1099/0022-1317-72-8-1985google scholar: lookup
                  16. Davis-Poynter NJ, Nugent J, Birch-Machin I, Allen GP. Viral marker. .
                  17. Edington N, Bridges CG, Patel JR. Endothelial cell infection and thrombosis in paralysis caused by equid herpesvirus-1: equine stroke.. Arch Virol 1986;90(1-2):111-24.
                    pubmed: 3015074doi: 10.1007/bf01314149google scholar: lookup
                  18. Gibbs JS, Chiou HC, Bastow KF, Cheng YC, Coen DM. Identification of amino acids in herpes simplex virus DNA polymerase involved in substrate and drug recognition.. Proc Natl Acad Sci U S A 1988 Sep;85(18):6672-6.
                    pmc: PMC282039pubmed: 2842788doi: 10.1073/pnas.85.18.6672google scholar: lookup
                  19. Greenwood RE, Simson AR. Clinical report of a paralytic syndrome affecting stallions, mares and foals on a thoroughbred studfarm.. Equine Vet J 1980 Jul;12(3):113-7.
                  20. Haberland M, Meyer-K Nig U, Hufert FT. Variation within the glycoprotein B gene of human cytomegalovirus is due to homologous recombination.. J Gen Virol 1999 Jun;80 ( Pt 6):1495-1500.
                    pubmed: 10374968doi: 10.1099/0022-1317-80-6-1495google scholar: lookup
                  21. Hall TA. Bioedit: a userfriendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41:95-98.
                  22. Huang JA, Ficorilli N, Hartley CA, Allen GP, Studdert MJ. Polymorphism of open reading frame 71 of equine herpesvirus-4 (EHV-4) and EHV-1.. J Gen Virol 2002 Mar;83(Pt 3):525-531.
                    pubmed: 11842247doi: 10.1099/0022-1317-83-3-525google scholar: lookup
                  23. Hwang CB, Ruffner KL, Coen DM. A point mutation within a distinct conserved region of the herpes simplex virus DNA polymerase gene confers drug resistance.. J Virol 1992 Mar;66(3):1774-6.
                  24. Kamiyama T, Kurokawa M, Shiraki K. Characterization of the DNA polymerase gene of varicella-zoster viruses resistant to acyclovir.. J Gen Virol 2001 Nov;82(Pt 11):2761-2765.
                    pubmed: 11602787doi: 10.1099/0022-1317-82-11-2761google scholar: lookup
                  25. Kirisawa R, Ohmori H, Iwai H, Kawakami Y. The genomic diversity among equine herpesvirus-1 strains isolated in Japan.. Arch Virol 1993;129(1-4):11-22.
                    pubmed: 8385910doi: 10.1007/bf01316881google scholar: lookup
                  26. Kumar S, Tamura K, Jakobsen IB, Nei M. MEGA2: molecular evolutionary genetics analysis software.. Bioinformatics 2001 Dec;17(12):1244-5.
                  27. Liu IKM, Castleman W. Equine posterior paresis associated with equine herpesvirus 1 vaccine in California: a preliminary report. J. Eqine Med. Surg. 12:397-401.
                  28. Loparev VN, Gonzalez A, Deleon-Carnes M, Tipples G, Fickenscher H, Torfason EG, Schmid DS. Global identification of three major genotypes of varicella-zoster virus: longitudinal clustering and strategies for genotyping.. J Virol 2004 Aug;78(15):8349-58.
                  29. Matthews JT, Terry BJ, Field AK. The structure and function of the HSV DNA replication proteins: defining novel antiviral targets.. Antiviral Res 1993 Feb;20(2):89-114.
                    pubmed: 8384825doi: 10.1016/0166-3542(93)90001-ygoogle scholar: lookup
                  30. Mayr A. Vaccination of horses against equine herpesvirus 1 infection. Equine infectious diseases II p. 41-45.
                  31. Mayr A, Pette J, Petzoldt K, Wagener K. [Studies on the development of a live vaccine against rhinopneumonitis (mare abortion) of horses].. Zentralbl Veterinarmed B 1968 Apr;15(3):406-18.
                    pubmed: 5692868
                  32. McCann SH, Mumford JA, Binns MM. Development of PCR assays to detect genetic variation amongst equine herpesvirus-1 isolates as an aid to epidemiological investigation.. J Virol Methods 1995 Mar;52(1-2):183-94.
                    pubmed: 7769032doi: 10.1016/0166-0934(94)00162-agoogle scholar: lookup
                  33. McCartan CG, Russell MM, Wood JL, Mumford JA. Clinical, serological and virological characteristics of an outbreak of paresis and neonatal foal disease due to equine herpesvirus-1 on a stud farm.. Vet Rec 1995 Jan 7;136(1):7-12.
                    pubmed: 7900264doi: 10.1136/vr.136.1.7google scholar: lookup
                  34. Meindl A, Osterrieder N. The equine herpesvirus 1 Us2 homolog encodes a nonessential membrane-associated virion component.. J Virol 1999 Apr;73(4):3430-7.
                  35. Meyer H, Hübert PH, Eichhorn W. Changes in restriction enzyme pattern of the equine herpes virus type 1 (EHV-1) strain Rac H DNA during attenuation.. Zentralbl Veterinarmed B 1987 Jun;34(4):310-3.
                  36. Muir WB, Nichols R, Breuer J. Phylogenetic analysis of varicella-zoster virus: evidence of intercontinental spread of genotypes and recombination.. J Virol 2002 Feb;76(4):1971-9.
                  37. Mumford JA, Edington N. EHV1 and equine paresis.. Vet Rec 1980 Mar 22;106(12):277.
                    pubmed: 6246670doi: 10.1136/vr.106.12.277-agoogle scholar: lookup
                  38. Mumford JA, Hannant D, Jessett DM, O'Neill T, Smith KC, Ostlund EN. Abortigenic and neurological disease caused by experimental infection with equid herpesvirus-1. Equine infectious diseases VII p. 261-275.
                  39. 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
                  40. Norberg P, Bergström T, Rekabdar E, Lindh M, Liljeqvist JA. Phylogenetic analysis of clinical herpes simplex virus type 1 isolates identified three genetic groups and recombinant viruses.. J Virol 2004 Oct;78(19):10755-64.
                  41. Palfi V, Christensen LS. Analyses of restriction fragment patterns (RFPs) and pathogenicity in baby mice of equine herpesvirus 1 and 4 (EHV-1 and EHV-4) strains circulating in Danish horses.. Vet Microbiol 1995 Nov;47(1-2):199-204.
                    pubmed: 8604552doi: 10.1016/0378-1135(95)00053-dgoogle scholar: lookup
                  42. Patel JR, Edington N, Mumford JA. Variation in cellular tropism between isolates of equine herpesvirus-1 in foals.. Arch Virol 1982;74(1):41-51.
                    pubmed: 6297429doi: 10.1007/bf01320781google scholar: lookup
                  43. Pignatelli S, Dal Monte P, Landini MP. gpUL73 (gN) genomic variants of human cytomegalovirus isolates are clustered into four distinct genotypes.. J Gen Virol 2001 Nov;82(Pt 11):2777-2784.
                    pubmed: 11602789doi: 10.1099/0022-1317-82-11-2777google scholar: lookup
                  44. Platt H, Singh H, Whitwell KE. Pathological observations on an outbreak of paralysis in broodmares.. Equine Vet J 1980 Jul;12(3):118-26.
                  45. Purdy CW, Porter RC, Ford SJ. Equine rhinopneumonitis vaccine: immunogenicity and safety in foals.. Am J Vet Res 1978 May;39(5):745-52.
                    pubmed: 215062
                  46. Purdy CW, Ford SJ, Porter RC. Equine rhinopneumonitis vaccine: immunogenicity and safety in adult horses, including pregnant mares.. Am J Vet Res 1978 Mar;39(3):377-83.
                    pubmed: 205144
                  47. Purdy CW, Ford SJ, Grant WF. Equine rhinopneumonitis virus (herpesvirus type 1): attenuation in stable monkey cell line.. Am J Vet Res 1977 Aug;38(8):1211-5.
                    pubmed: 199093
                  48. Rasmussen L, Geissler A, Winters M. Inter- and intragenic variations complicate the molecular epidemiology of human cytomegalovirus.. J Infect Dis 2003 Mar 1;187(5):809-19.
                    pubmed: 12599055doi: 10.1086/367900google scholar: lookup
                  49. Rawlinson WD, Farrell HE, Barrell BG. Analysis of the complete DNA sequence of murine cytomegalovirus.. J Virol 1996 Dec;70(12):8833-49.
                  50. Sakaoka H, Kurita K, Iida Y, Takada S, Umene K, Kim YT, Ren CS, Nahmias AJ. Quantitative analysis of genomic polymorphism of herpes simplex virus type 1 strains from six countries: studies of molecular evolution and molecular epidemiology of the virus.. J Gen Virol 1994 Mar;75 ( Pt 3):513-27.
                    pubmed: 8126449doi: 10.1099/0022-1317-75-3-513google scholar: lookup
                  51. Smith KC, Whitwell KE, Mumford JA, Hannant D, Blunden AS, Tearle JP. Virulence of the V592 isolate of equid herpesvirus-1 in ponies.. J Comp Pathol 2000 May;122(4):288-97.
                    pubmed: 10805982doi: 10.1053/jcpa.1999.0373google scholar: lookup
                  52. Smith KC, Whitwell KE, Binns MM, Dolby CA, Hannant D, Mumford JA. Abortion of virologically negative foetuses following experimental challenge of pregnant pony mares with equid herpesvirus 1.. Equine Vet J 1992 Jul;24(4):256-9.
                  53. Staden R. The Staden sequence analysis package.. Mol Biotechnol 1996 Jun;5(3):233-41.
                    pubmed: 8837029doi: 10.1007/bf02900361google scholar: lookup
                  54. Studdert MJ, Crabb BS, Ficorilli N. The molecular epidemiology of equine herpesvirus 1 (equine abortion virus) in Australasia 1975 to 1989.. Aust Vet J 1992 May;69(5):104-11.
                  55. Tearle JP, Smith KC, Platt AJ, Hannant D, Davis-Poynter NJ, Mumford JA. In vitro characterisation of high and low virulence isolates of equine herpesvirus-1 and -4.. Res Vet Sci 2003 Aug;75(1):83-6.
                    pubmed: 12801466doi: 10.1016/s0034-5288(03)00031-6google scholar: lookup
                  56. Telford EA, Watson MS, McBride K, Davison AJ. The DNA sequence of equine herpesvirus-1.. Virology 1992 Jul;189(1):304-16.
                    pubmed: 1318606doi: 10.1016/0042-6822(92)90706-ugoogle scholar: lookup
                  57. van Maanen C, Sloet van Oldruitenborgh-Oosterbaan MM, Damen EA, Derksen AG. Neurological disease associated with EHV-1-infection in a riding school: clinical and virological characteristics.. Equine Vet J 2001 Mar;33(2):191-6.
                  58. Wagenaar TR, Chow VT, Buranathai C, Thawatsupha P, Grose C. The out of Africa model of varicella-zoster virus evolution: single nucleotide polymorphisms and private alleles distinguish Asian clades from European/North American clades.. Vaccine 2003 Mar 7;21(11-12):1072-81.
                    pubmed: 12559782doi: 10.1016/s0264-410x(02)00559-5google scholar: lookup
                  59. Wang TS. Eukaryotic DNA polymerases.. Annu Rev Biochem 1991;60:513-52.
                  60. Whitwell KE, Blunden AS. Pathological findings in horses dying during an outbreak of the paralytic form of Equid herpesvirus type 1 (EHV-1) infection.. Equine Vet J 1992 Jan;24(1):13-9.
                  61. Wilson WD. Equine herpesvirus 1 myeloencephalopathy.. Vet Clin North Am Equine Pract 1997 Apr;13(1):53-72.
                    pubmed: 9106343doi: 10.1016/s0749-0739(17)30255-9google scholar: lookup
                  62. Zweygberg Wirgart B, Brytting M, Linde A, Wahren B, Grillner L. Sequence variation within three important cytomegalovirus gene regions in isolates from four different patient populations.. J Clin Microbiol 1998 Dec;36(12):3662-9.

                  Citations

                  This article has been cited 70 times.
                  1. Black JB, Frampton AR. Anti-inflammatory compounds reduce equine herpesvirus type 1 replication and cell-to-cell spread.. Front Vet Sci 2023;10:1165917.
                    doi: 10.3389/fvets.2023.1165917pubmed: 37275614google scholar: lookup
                  2. Klouth E, Zablotski Y, Petersen JL, de Bruijn M, Gröndahl G, Müller S, Goehring LS. Epidemiological Aspects of Equid Herpesvirus-Associated Myeloencephalopathy (EHM) Outbreaks.. Viruses 2022 Nov 21;14(11).
                    doi: 10.3390/v14112576pubmed: 36423188google scholar: lookup
                  3. Tsai MS, François S, Newman C, Macdonald DW, Buesching CD. Infection with a Recently Discovered Gammaherpesvirus Variant in European Badgers, Meles meles, is Associated with Higher Relative Viral Loads in Blood.. Pathogens 2022 Oct 6;11(10).
                    doi: 10.3390/pathogens11101154pubmed: 36297210google scholar: lookup
                  4. 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
                  5. Hu Y, Jia Q, Liu J, Sun W, Bao Z, Che C, Wu G, Fan B, Jarhen, Ran D. Molecular characteristics and pathogenicity of an equid alphaherpesvirus 1 strain isolated in China.. Virus Genes 2022 Aug;58(4):284-293.
                    doi: 10.1007/s11262-022-01910-ypubmed: 35567668google scholar: lookup
                  6. Sierra E, Fernández A, Fernández-Maldonado C, Sacchini S, Felipe-Jiménez I, Segura-Göthlin S, Colom-Rivero A, Câmara N, Puig-Lozano R, Rambaldi AM, Suárez-Santana C, Arbelo M. Molecular Characterization of Herpesviral Encephalitis in Cetaceans: Correlation with Histopathological and Immunohistochemical Findings.. Animals (Basel) 2022 Apr 29;12(9).
                    doi: 10.3390/ani12091149pubmed: 35565575google scholar: lookup
                  7. Carvelli A, Nielsen SS, Paillot R, Broglia A, Kohnle L. Clinical impact, diagnosis and control of Equine Herpesvirus-1 infection in Europe.. EFSA J 2022 Apr;20(4):e07230.
                    doi: 10.2903/j.efsa.2022.7230pubmed: 35414834google scholar: lookup
                  8. Tong P, Duan R, Palidan N, Deng H, Duan L, Ren M, Song X, Jia C, Tian S, Yang E, Kuang L, Xie J. Outbreak of neuropathogenic equid herpesvirus 1 causing abortions in Yili horses of Zhaosu, North Xinjiang, China.. BMC Vet Res 2022 Mar 1;18(1):83.
                    doi: 10.1186/s12917-022-03171-1pubmed: 35232435google scholar: lookup
                  9. 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
                  10. Agerholm JS, Klas EM, Damborg P, Borel N, Pedersen HG, Christoffersen M. A Diagnostic Survey of Aborted Equine Fetuses and Stillborn Premature Foals in Denmark.. Front Vet Sci 2021;8:740621.
                    doi: 10.3389/fvets.2021.740621pubmed: 34859085google scholar: lookup
                  11. 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
                  12. Vandenberghe E, Boshuizen B, Delesalle CJG, Goehring LS, Groome KA, van Maanen K, de Bruijn CM. New Insights into the Management of an EHV-1 (Equine Hospital) Outbreak.. Viruses 2021 Jul 22;13(8).
                    doi: 10.3390/v13081429pubmed: 34452295google scholar: lookup
                  13. Pusterla N, Barnum S, Miller J, Varnell S, Dallap-Schaer B, Aceto H, Simeone A. Investigation of an EHV-1 Outbreak in the United States Caused by a New H(752) Genotype.. Pathogens 2021 Jun 13;10(6).
                    doi: 10.3390/pathogens10060747pubmed: 34199153google scholar: lookup
                  14. Samoilowa S, Giessler KS, Torres CEM, Hussey GS, Allum A, Fux R, Jerke C, Kiupel M, Matiasek K, Sledge DG, Goehring LS. Equid herpesvirus-1 Distribution in Equine Lymphoid and Neural Tissues 70 Days Post Infection.. Pathogens 2021 Jun 5;10(6).
                    doi: 10.3390/pathogens10060707pubmed: 34198884google scholar: lookup
                  15. 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
                  16. Klouth E, Zablotski Y, Goehring LS. Apparent Breed Predilection for Equid Herpesvirus-1-Associated Myeloencephalopathy (EHM) in a Multiple-Breed Herd.. Pathogens 2021 Apr 29;10(5).
                    doi: 10.3390/pathogens10050537pubmed: 33947126google scholar: lookup
                  17. 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
                  18. Laval K, Poelaert KCK, Van Cleemput J, Zhao J, Vandekerckhove AP, Gryspeerdt AC, Garré B, van der Meulen K, Baghi HB, Dubale HN, Zarak I, Van Crombrugge E, Nauwynck HJ. The Pathogenesis and Immune Evasive Mechanisms of Equine Herpesvirus Type 1.. Front Microbiol 2021;12:662686.
                    doi: 10.3389/fmicb.2021.662686pubmed: 33746936google scholar: lookup
                  19. Zarski LM, Giessler KS, Jacob SI, Weber PSD, McCauley AG, Lee Y, Soboll Hussey G. Identification of Host Factors Associated with the Development of Equine Herpesvirus Myeloencephalopathy by Transcriptomic Analysis of Peripheral Blood Mononuclear Cells from Horses.. Viruses 2021 Feb 24;13(3).
                    doi: 10.3390/v13030356pubmed: 33668216google scholar: lookup
                  20. 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
                  21. 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
                  22. Akter R, Legione A, Sansom FM, El-Hage CM, Hartley CA, Gilkerson JR, Devlin JM. Detection of Coxiella burnetii and equine herpesvirus 1, but not Leptospira spp. or Toxoplasma gondii, in cases of equine abortion in Australia - a 25 year retrospective study.. PLoS One 2020;15(5):e0233100.
                    doi: 10.1371/journal.pone.0233100pubmed: 32453753google scholar: lookup
                  23. Dunuwille WMB, YousefiMashouf N, Balasuriya UBR, Pusterla N, Bailey E. Genome-wide association study for host genetic factors associated with equine herpesvirus type-1 induced myeloencephalopathy.. Equine Vet J 2020 Nov;52(6):794-798.
                    doi: 10.1111/evj.13261pubmed: 32153055google scholar: lookup
                  24. Lassalle F, Beale MA, Bharucha T, Williams CA, Williams RJ, Cudini J, Goldstein R, Haque T, Depledge DP, Breuer J. Whole genome sequencing of Herpes Simplex Virus 1 directly from human cerebrospinal fluid reveals selective constraints in neurotropic viruses.. Virus Evol 2020 Jan;6(1):veaa012.
                    doi: 10.1093/ve/veaa012pubmed: 32099667google scholar: lookup
                  25. 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
                  26. Oladunni FS, Horohov DW, Chambers TM. EHV-1: A Constant Threat to the Horse Industry.. Front Microbiol 2019;10:2668.
                    doi: 10.3389/fmicb.2019.02668pubmed: 31849857google scholar: lookup
                  27. 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. 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 2019 Oct 4;11(10).
                    doi: 10.3390/v11100916pubmed: 31590336google scholar: lookup
                  28. Preziuso S, Sgorbini M, Marmorini P, Cuteri V. Equid alphaherpesvirus 1 from Italian Horses: Evaluation of the Variability of the ORF30, ORF33, ORF34 and ORF68 Genes.. Viruses 2019 Sep 13;11(9).
                    doi: 10.3390/v11090851pubmed: 31540321google scholar: lookup
                  29. Oladunni FS, Sarkar S, Reedy S, Balasuriya UBR, Horohov DW, Chambers TM. Equid Herpesvirus 1 Targets the Sensitization and Induction Steps To Inhibit the Type I Interferon Response in Equine Endothelial Cells.. J Virol 2019 Dec 1;93(23).
                    doi: 10.1128/JVI.01342-19pubmed: 31511388google scholar: lookup
                  30. 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: 10.1177/1040638719871975pubmed: 31477001google scholar: lookup
                  31. Schnabel CL, Babasyan S, Rollins A, Freer H, Wimer CL, Perkins GA, Raza F, Osterrieder N, Wagner B. An Equine Herpesvirus Type 1 (EHV-1) Ab4 Open Reading Frame 2 Deletion Mutant Provides Immunity and Protection from EHV-1 Infection and Disease.. J Virol 2019 Nov 15;93(22).
                    doi: 10.1128/JVI.01011-19pubmed: 31462575google scholar: lookup
                  32. Tsujimura K, Bannai H, Nemoto M, Kokado H. Loop-mediated isothermal amplification-fluorescent loop primer assay for the genotyping of a single nucleotide polymorphism at position 2254 in the viral DNA polymerase gene of equid alphaherpesvirus 1.. J Vet Diagn Invest 2019 Jul;31(4):640-644.
                    doi: 10.1177/1040638719856404pubmed: 31170890google scholar: lookup
                  33. Poelaert KCK, Van Cleemput J, Laval K, Descamps S, Favoreel HW, Nauwynck HJ. Beyond Gut Instinct: Metabolic Short-Chain Fatty Acids Moderate the Pathogenesis of Alphaherpesviruses.. Front Microbiol 2019;10:723.
                    doi: 10.3389/fmicb.2019.00723pubmed: 31024501google scholar: lookup
                  34. Holz CL, Sledge DG, Kiupel M, Nelli RK, Goehring LS, Soboll Hussey G. Histopathologic Findings Following Experimental Equine Herpesvirus 1 Infection of Horses.. Front Vet Sci 2019;6:59.
                    doi: 10.3389/fvets.2019.00059pubmed: 30886853google scholar: lookup
                  35. Poelaert KCK, Van Cleemput J, Laval K, Favoreel HW, Couck L, Van den Broeck W, Azab W, Nauwynck HJ. Equine Herpesvirus 1 Bridles T Lymphocytes To Reach Its Target Organs.. J Virol 2019 Apr 1;93(7).
                    doi: 10.1128/JVI.02098-18pubmed: 30651370google scholar: lookup
                  36. 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/pathogens8010007pubmed: 30650561google scholar: lookup
                  37. Matczuk AK, Skarbek M, Jackulak NA, Bażanów BA. Molecular characterisation of equid alphaherpesvirus 1 strains isolated from aborted fetuses in Poland.. Virol J 2018 Dec 3;15(1):186.
                    doi: 10.1186/s12985-018-1093-5pubmed: 30509297google scholar: lookup
                  38. Wimer CL, Schnabel CL, Perkins G, Babasyan S, Freer H, Stout AE, Rollins A, Osterrieder N, Goodman LB, Glaser A, Wagner B. The deletion of the ORF1 and ORF71 genes reduces virulence of the neuropathogenic EHV-1 strain Ab4 without compromising host immunity in horses.. PLoS One 2018;13(11):e0206679.
                    doi: 10.1371/journal.pone.0206679pubmed: 30440016google scholar: lookup
                  39. Poelaert KCK, Van Cleemput J, Laval K, Favoreel HW, Soboll Hussey G, Maes RK, Nauwynck HJ. Abortigenic but Not Neurotropic Equine Herpes Virus 1 Modulates the Interferon Antiviral Defense.. Front Cell Infect Microbiol 2018;8:312.
                    doi: 10.3389/fcimb.2018.00312pubmed: 30258819google scholar: lookup
                  40. Schnabel CL, Wimer CL, Perkins G, Babasyan S, Freer H, Watts C, Rollins A, Osterrieder N, Wagner B. Deletion of the ORF2 gene of the neuropathogenic equine herpesvirus type 1 strain Ab4 reduces virulence while maintaining strong immunogenicity.. BMC Vet Res 2018 Aug 22;14(1):245.
                    doi: 10.1186/s12917-018-1563-4pubmed: 30134896google scholar: lookup
                  41. 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.12809pubmed: 29423949google scholar: lookup
                  42. Garvey M, Suárez NM, Kerr K, Hector R, Moloney-Quinn L, Arkins S, Davison AJ, Cullinane A. Equid herpesvirus 8: Complete genome sequence and association with abortion in mares.. PLoS One 2018;13(2):e0192301.
                    doi: 10.1371/journal.pone.0192301pubmed: 29414990google scholar: lookup
                  43. Shakya AK, O'Callaghan DJ, Kim SK. Comparative Genomic Sequencing and Pathogenic Properties of Equine Herpesvirus 1 KyA and RacL11.. Front Vet Sci 2017;4:211.
                    doi: 10.3389/fvets.2017.00211pubmed: 29312962google scholar: lookup
                  44. Paillot R, Marcillaud Pitel C, D'Ablon X, Pronost S. Equine Vaccines: How, When and Why? Report of the Vaccinology Session, French Equine Veterinarians Association, 2016, Reims.. Vaccines (Basel) 2017 Dec 4;5(4).
                    doi: 10.3390/vaccines5040046pubmed: 29207516google scholar: lookup
                  45. Kolb AW, Lewin AC, Moeller Trane R, McLellan GJ, Brandt CR. Phylogenetic and recombination analysis of the herpesvirus genus varicellovirus.. BMC Genomics 2017 Nov 21;18(1):887.
                    doi: 10.1186/s12864-017-4283-4pubmed: 29157201google scholar: lookup
                  46. Stasiak K, Dunowska M, Hills SF, Rola J. Genetic characterization of equid herpesvirus type 1 from cases of abortion in Poland.. Arch Virol 2017 Aug;162(8):2329-2335.
                    doi: 10.1007/s00705-017-3376-3pubmed: 28451902google scholar: lookup
                  47. Cymerys J, Słońska A, Tucholska A, Golke A, Chmielewska A, Bańbura MW. Influence of long-term equine herpesvirus type 1 (EHV-1) infection on primary murine neurons-the possible effects of the multiple passages of EHV-1 on its neurovirulence.. Folia Microbiol (Praha) 2018 Jan;63(1):1-11.
                    doi: 10.1007/s12223-017-0528-5pubmed: 28409422google scholar: lookup
                  48. Zhao J, Poelaert KCK, Van Cleemput J, Nauwynck HJ. CCL2 and CCL5 driven attraction of CD172a(+) monocytic cells during an equine herpesvirus type 1 (EHV-1) infection in equine nasal mucosa and the impact of two migration inhibitors, rosiglitazone (RSG) and quinacrine (QC).. Vet Res 2017 Feb 27;48(1):14.
                    doi: 10.1186/s13567-017-0419-4pubmed: 28241864google scholar: lookup
                  49. 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/v9010006pubmed: 28075374google scholar: lookup
                  50. Wagner B, Perkins G, Babasyan S, Freer H, Keggan A, Goodman LB, Glaser A, Torsteinsdóttir S, Svansson V, Björnsdóttir S. Neonatal Immunization with a Single IL-4/Antigen Dose Induces Increased Antibody Responses after Challenge Infection with Equine Herpesvirus Type 1 (EHV-1) at Weanling Age.. PLoS One 2017;12(1):e0169072.
                    doi: 10.1371/journal.pone.0169072pubmed: 28045974google scholar: lookup
                  51. Izume S, Kirisawa R, Ohya K, Ohnuma A, Kimura T, Omatsu T, Katayama Y, Mizutani T, Fukushi H. The full genome sequences of 8 equine herpesvirus type 4 isolates from horses in Japan.. J Vet Med Sci 2017 Jan 24;79(1):206-212.
                    doi: 10.1292/jvms.16-0506pubmed: 27840393google scholar: lookup
                  52. Negussie H, Li Y, Tessema TS, Nauwynck HJ. Replication characteristics of equine herpesvirus 1 and equine herpesvirus 3: comparative analysis using ex vivo tissue cultures.. Vet Res 2016 Jan 15;47:19.
                    doi: 10.1186/s13567-016-0305-5pubmed: 26768993google scholar: lookup
                  53. Mori E, Lara Mdo C, Cunha EM, Villalobos EM, Mori CM, Soares RM, Brandão PE, Fernandes WR, Richtzenhain LJ. Molecular characterization of Brazilian equid herpesvirus type 1 strains based on neuropathogenicity markers.. Braz J Microbiol 2015 Jun;46(2):565-70.
                    doi: 10.1590/S1517-838246220140096pubmed: 26273275google scholar: lookup
                  54. Stasiak K, Rola J, Ploszay G, Socha W, Zmudzinski JF. Detection of the neuropathogenic variant of equine herpesvirus 1 associated with abortions in mares in Poland.. BMC Vet Res 2015 May 1;11:102.
                    doi: 10.1186/s12917-015-0416-7pubmed: 25929692google scholar: lookup
                  55. Rebelo AR, Carman S, Shapiro J, van Dreumel T, Hazlett M, Nagy É. Equid herpesvirus 9 (EHV-9) isolates from zebras in Ontario, Canada, 1989 to 2007.. Can J Vet Res 2015 Apr;79(2):155-9.
                    pubmed: 25852233
                  56. Guo X, Izume S, Okada A, Ohya K, Kimura T, Fukushi H. Full genome sequences of zebra-borne equine herpesvirus type 1 isolated from zebra, onager and Thomson's gazelle.. J Vet Med Sci 2014 Sep;76(9):1309-12.
                    doi: 10.1292/jvms.14-0183pubmed: 24920546google scholar: lookup
                  57. Hussey GS, Goehring LS, Lunn DP, Hussey SB, Huang T, Osterrieder N, Powell C, Hand J, Holz C, Slater J. Experimental infection with equine herpesvirus type 1 (EHV-1) induces chorioretinal lesions.. Vet Res 2013 Dec 5;44(1):118.
                    doi: 10.1186/1297-9716-44-118pubmed: 24308772google scholar: lookup
                  58. Marenzoni ML, Bietta A, Lepri E, Casagrande Proietti P, Cordioli P, Canelli E, Stefanetti V, Coletti M, Timoney PJ, Passamonti F. Role of equine herpesviruses as co-infecting agents in cases of abortion, placental disease and neonatal foal mortality.. Vet Res Commun 2013 Dec;37(4):311-7.
                    doi: 10.1007/s11259-013-9578-6pubmed: 24052369google scholar: lookup
                  59. 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: 10.1186/1751-0147-55-19pubmed: 23497661google scholar: lookup
                  60. Yeo WM, Osterrieder N, Stokol T. Equine herpesvirus type 1 infection induces procoagulant activity in equine monocytes.. Vet Res 2013 Mar 11;44(1):16.
                    doi: 10.1186/1297-9716-44-16pubmed: 23497076google scholar: lookup
                  61. Carmichael RJ, Whitfield C, Maxwell LK. Pharmacokinetics of ganciclovir and valganciclovir in the adult horse.. J Vet Pharmacol Ther 2013 Oct;36(5):441-9.
                    doi: 10.1111/jvp.12029pubmed: 23301502google scholar: lookup
                  62. Smith KL, Li Y, Breheny P, Cook RF, Henney PJ, Sells S, Pronost S, Lu Z, Crossley BM, Timoney PJ, Balasuriya UB. New real-time PCR assay using allelic discrimination for detection and differentiation of equine herpesvirus-1 strains with A2254 and G2254 polymorphisms.. J Clin Microbiol 2012 Jun;50(6):1981-8.
                    doi: 10.1128/JCM.00135-12pubmed: 22493339google scholar: lookup
                  63. Azab W, Osterrieder N. Glycoproteins D of equine herpesvirus type 1 (EHV-1) and EHV-4 determine cellular tropism independently of integrins.. J Virol 2012 Feb;86(4):2031-44.
                    doi: 10.1128/JVI.06555-11pubmed: 22171258google scholar: lookup
                  64. Szpara ML, Tafuri YR, Parsons L, Shamim SR, Verstrepen KJ, Legendre M, Enquist LW. A wide extent of inter-strain diversity in virulent and vaccine strains of alphaherpesviruses.. PLoS Pathog 2011 Oct;7(10):e1002282.
                    doi: 10.1371/journal.ppat.1002282pubmed: 22022263google scholar: lookup
                  65. Del Medico Zajac MP, Romera SA, Ladelfa MF, Kotsias F, Delgado F, Thiry J, Meurens F, Keil G, Thiry E, Muylkens B. In vitro-generated interspecific recombinants between bovine herpesviruses 1 and 5 show attenuated replication characteristics and establish latency in the natural host.. BMC Vet Res 2011 May 18;7:19.
                    doi: 10.1186/1746-6148-7-19pubmed: 21592326google scholar: lookup
                  66. Soboll Hussey G, Hussey SB, Wagner B, Horohov DW, Van de Walle GR, Osterrieder N, Goehring LS, Rao S, Lunn DP. Evaluation of immune responses following infection of ponies with an EHV-1 ORF1/2 deletion mutant.. Vet Res 2011 Feb 7;42(1):23.
                    doi: 10.1186/1297-9716-42-23pubmed: 21314906google scholar: lookup
                  67. Davison AJ. Herpesvirus systematics.. Vet Microbiol 2010 Jun 16;143(1):52-69.
                    doi: 10.1016/j.vetmic.2010.02.014pubmed: 20346601google scholar: lookup
                  68. Brosnahan MM, Damiani A, van de Walle G, Erb H, Perkins GA, Osterrieder N. The effect of siRNA treatment on experimental equine herpesvirus type 1 (EHV-1) infection in horses.. Virus Res 2010 Feb;147(2):176-81.
                  69. Martín Ocampos GP, Fuentealba NA, Sguazza GH, Jones LR, Cigliano MM, Barbeito CG, Galosi CM. Genomic and phylogenetic analysis of Argentinian Equid Herpesvirus 1 strains.. Virus Genes 2009 Feb;38(1):113-7.
                    doi: 10.1007/s11262-008-0301-6pubmed: 19023651google scholar: lookup
                  70. 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.
                    doi: 10.1371/journal.ppat.0030160pubmed: 17997600google scholar: lookup