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Viruses2021; 13(10); doi: 10.3390/v13101917

First Clinical Case of Equine Parvovirus-Hepatitis-Related Theiler’s Disease in Asia.

Abstract: Equine parvovirus-hepatitis (EqPV-H) is a newly identified etiologic agent of Theiler's disease (TD). We present a case of EqPV-H-related fulminant hepatitis in a 14-year-old thoroughbred mare in Korea. The mare had acute hepatopathy and gastrointestinal symptoms, with abnormal liver-related blood parameters. The horse was born in the USA and imported to Korea in 2017, with no history of administration of equine biological products after entry into Korea. The horse was diagnosed with EqPV-H-associated hepatitis after abdominal ultrasonography, laparotomy, and nested polymerase chain reaction (PCR) and in situ hybridization (ISH) assays. The serum, nasal swab, oral swab, and liver biopsy were positive for EqPV-H according to the PCR assay. Genetic analysis of the partial NS1 gene of EqPV-H showed a unique nucleotide substitution, distinct from that in previously deposited strains. EqPV-H DNA was found not only in hepatocytes but also in bile duct epithelium and Kupffer cells, particularly via ISH. To the best of our knowledge, this is the first case of EqPV-H-associated TD in Asia, providing the first clinical evidence for viral shedding from the mouth and nose, and identification of EqPV-H in the liver. This study contributes to a better understanding of the pathological features of EqPV-H-associated TD.
Publication Date: 2021-09-24 PubMed ID: 34696347PubMed Central: PMC8541225DOI: 10.3390/v13101917Google Scholar: Lookup
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  • Journal Article
  • Research Support
  • Non-U.S. Gov't

Summary

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This research presents the first confirmed case in Asia of Theiler’s disease in horses caused by the newly identified Equine Parvovirus-Hepatitis (EqPV-H) through an in-depth case study of a thoroughbred mare in Korea.

Case Presentation

  • The study relates to a thoroughbred mare from the USA, aged 14 years, who was imported to Korea in 2017. The mare exhibited signs of acute hepatopathy (liver disease) and gastrointestinal symptoms and showed abnormal liver-related blood parameters.
  • The horse had no history of receiving any equine biological products after being brought to Korea.

Methods and Diagnosis

  • The diagnosis of EqPV-H-associated hepatitis was made through a combination of techniques including abdominal ultrasonography, surgery (laparotomy), and highly sensitive laboratory tests such as nested polymerase chain reaction (PCR) and in situ hybridization (ISH) assays. These methods helped to identify and confirm the presence of the EqPV-H virus in the horse’s system.
  • The researchers found that the serum (the clear, yellowish part of blood), nasal swab, oral swab, and a sample of liver tissue were all positive for EqPV-H according to the PCR test.
  • A unique nucleotide substitution was detected through genetic analysis of a section of the EqPV-H virus known as the NS1 gene, which was different than strains previously recorded in scientific literature.

Significance and Findings

  • This is the first confirmed case of EqPV-H-associated Theiler’s disease in Asia, adding to global knowledge of the disease’s spread and prevalence.
  • The study also provides the first clinical evidence for viral shedding (release of virus particles) from the mouth and nose of an infected horse, indicating possible routes of transmission.
  • The DNA of EqPV-H was not only found in liver cells (hepatocytes) but also in other types of liver cells known as bile duct epithelium and Kupffer cells. This discovery was facilitated by the ISH technique.
  • The findings contribute to a better understanding of the pathological features – the visible effects on organs and tissues – of EqPV-H-associated Theiler’s disease, furthering our knowledge of this equine disease and potentially improving diagnosis, treatment, and prevention efforts.

Cite This Article

APA
Yoon J, Park T, Kim A, Park J, Park BJ, Ahn HS, Go HJ, Kim DH, Jung S, Seo Y, Lee JB, Park SY, Song CS, Lee SW, Choi IS. (2021). First Clinical Case of Equine Parvovirus-Hepatitis-Related Theiler’s Disease in Asia. Viruses, 13(10). https://doi.org/10.3390/v13101917

Publication

ISSN: 1999-4915
NlmUniqueID: 101509722
Country: Switzerland
Language: English
Volume: 13
Issue: 10

Researcher Affiliations

Yoon, Jungho
  • Equine Clinic, Jeju Stud Farm, Korea Racing Authority, Jeju 63346, Korea.
  • Department of Infectious Diseases, College of Veterinary Medicine, Konkuk University, Seoul 05029, Korea.
Park, Taemook
  • Equine Clinic, Jeju Stud Farm, Korea Racing Authority, Jeju 63346, Korea.
Kim, Ahram
  • Equine Clinic, Jeju Stud Farm, Korea Racing Authority, Jeju 63346, Korea.
Park, Jongyoung
  • Equine Clinic, Jeju Stud Farm, Korea Racing Authority, Jeju 63346, Korea.
Park, Byung-Joo
  • Department of Infectious Diseases, College of Veterinary Medicine, Konkuk University, Seoul 05029, Korea.
Ahn, Hee-Seop
  • Department of Infectious Diseases, College of Veterinary Medicine, Konkuk University, Seoul 05029, Korea.
Go, Hyeon-Jeong
  • Department of Infectious Diseases, College of Veterinary Medicine, Konkuk University, Seoul 05029, Korea.
Kim, Dong-Hwi
  • Department of Infectious Diseases, College of Veterinary Medicine, Konkuk University, Seoul 05029, Korea.
Jung, Soontag
  • Department of Food and Nutrition, College of Biotechnology and Natural Resources, Chung-Ang University, Anseong 17546, Korea.
Seo, Yeeun
  • Department of Food and Nutrition, College of Biotechnology and Natural Resources, Chung-Ang University, Anseong 17546, Korea.
Lee, Joong-Bok
  • Department of Infectious Diseases, College of Veterinary Medicine, Konkuk University, Seoul 05029, Korea.
Park, Seung-Yong
  • Department of Infectious Diseases, College of Veterinary Medicine, Konkuk University, Seoul 05029, Korea.
Song, Chang-Seon
  • Department of Infectious Diseases, College of Veterinary Medicine, Konkuk University, Seoul 05029, Korea.
Lee, Sang-Won
  • Department of Infectious Diseases, College of Veterinary Medicine, Konkuk University, Seoul 05029, Korea.
Choi, In-Soo
  • Department of Infectious Diseases, College of Veterinary Medicine, Konkuk University, Seoul 05029, Korea.

MeSH Terms

  • Animals
  • Asia
  • Enterovirus Infections / virology
  • Female
  • Hepatitis, Viral, Animal / virology
  • Hepatocytes / pathology
  • Horse Diseases / virology
  • Horses
  • Liver / pathology
  • Parvoviridae Infections / veterinary
  • Parvoviridae Infections / virology
  • Parvovirinae / classification
  • Parvovirus
  • Phylogeny
  • Polymerase Chain Reaction
  • Republic of Korea
  • Virus Shedding

Conflict of Interest Statement

The authors declare no conflict of interest.

References

This article includes 30 references
  1. Theiler A. Acute Liver Atrophy and Parenchymatous Hepatitis in Horses. Cab Direct Glasgow, Scotland: 1919. pp. 7–165. Union of South Africa, 5th and 6th Reports of the Director of Veterinary Research.
  2. Ramsauer AS, Badenhorst M, Cavalleri JM. Equine Parvovirus Hepatitis. Equine Vet. J. 2021.
    doi: 10.1111/evj.13477pmc: PMC8457058pubmed: 34101906google scholar: lookup
  3. Tomlinson JE, Jager M, Struzyna A, Laverack M, Fortier LA, Dubovi E, Foil LD, Burbelo PD, Divers TJ, Van de Walle GR. Tropism, pathology, and transmission of equine parvovirus-hepatitis. Emerg. Microbes Infect. 2020;9:651–663.
  4. Tomlinson JE, Van de Walle GR, Divers TJ. What do we know about hepatitis viruses in horses?. Vet. Clin. Equine Pract. 2019;35:351–362.
    doi: 10.1016/j.cveq.2019.03.001pubmed: 31084975google scholar: lookup
  5. Tomlinson JE, Tennant BC, Struzyna A, Mrad D, Browne N, Whelchel D, Johnson PJ, Jamieson C, Löhr CV, Bildfell R. Viral testing of 10 cases of Theiler’s disease and 37 in-contact horses in the absence of equine biologic product administration: A prospective study (2014–2018). J. Vet. Intern. Med. 2019;33:258–265.
    doi: 10.1111/jvim.15362pmc: PMC6335540pubmed: 30520132google scholar: lookup
  6. Tomlinson JE, Kapoor A, Kumar A, Tennant BC, Laverack MA, Beard L, Delph K, Davis E, Schott II H, Lascola K. Viral testing of 18 consecutive cases of equine serum hepatitis: A prospective study (2014–2018). J. Vet. Intern. Med. 2019;33:251–257.
    doi: 10.1111/jvim.15368pmc: PMC6335536pubmed: 30520162google scholar: lookup
  7. Panciera RJ. Serum hepatitis in the horse. J. Am. Vet. Med Assoc. 1969;155:408–410.
    pubmed: 5816124
  8. Chandriani S, Skewes-Cox P, Zhong W, Ganem DE, Divers TJ, Van Blaricum AJ, Tennant BC, Kistler AL. Identification of a previously undescribed divergent virus from the Flaviviridae family in an outbreak of equine serum hepatitis. Proc. Natl. Acad. Sci. USA. 2013;110:E1407–E1415.
    doi: 10.1073/pnas.1219217110pmc: PMC3625295pubmed: 23509292google scholar: lookup
  9. Burbelo PD, Dubovi EJ, Simmonds P, Medina JL, Henriquez JA, Mishra N, Wagner J, Tokarz R, Cullen JM, Iadarola MJ. Serology-enabled discovery of genetically diverse hepaciviruses in a new host. J. Virol. 2012;86:6171–6178.
    doi: 10.1128/JVI.00250-12pmc: PMC3372197pubmed: 22491452google scholar: lookup
  10. Kapoor A, Simmonds P, Cullen JM, Scheel TK, Medina JL, Giannitti F, Nishiuchi E, Brock KV, Burbelo PD, Rice CM. Identification of a pegivirus (GB virus-like virus) that infects horses. J. Virol. 2013;87:7185–7190.
    doi: 10.1128/JVI.00324-13pmc: PMC3676142pubmed: 23596285google scholar: lookup
  11. Divers TJ, Tennant BC, Kumar A, McDonough S, Cullen J, Bhuva N, Jain K, Chauhan LS, Scheel TKH, Lipkin WI. New parvovirus associated with serum hepatitis in horses after inoculation of common biological product. Emerg. Infect. Dis. 2018;24:303.
    doi: 10.3201/eid2402.171031pmc: PMC5782890pubmed: 29350162google scholar: lookup
  12. Tomlinson JE, Wolfisberg R, Fahnøe U, Sharma H, Renshaw R, Nielsen L, Nishiuchi E, Holm C, Dubovi E, Rosenberg BR. Equine pegiviruses cause persistent infection of bone marrow and are not associated with hepatitis. PLoS Pathog. 2020;16:e1008677.
  13. Tegtmeyer B, Echelmeyer J, Pfankuche VM, Puff C, Todt D, Fischer N, Durham A, Feige K, Baumgärtner W, Steinmann E. Chronic equine hepacivirus infection in an adult gelding with severe hepatopathy. Vet. Med. Sci. 2019;5:372–378.
    doi: 10.1002/vms3.181pmc: PMC6682795pubmed: 31267690google scholar: lookup
  14. Reinecke B, Köhn M, Brüggemann Y, Kinast V, Todt D, Stang A, Badenhorst M, Koeppel K, Guthrie A, Groner U. Clinical Course of Infection and Cross-Species Detection of Equine Parvovirus-Hepatitis. Viruses 2021;13:1454.
    doi: 10.3390/v13081454pmc: PMC8402690pubmed: 34452320google scholar: lookup
  15. Badenhorst M, de Heus P, Auer A, Tegtmeyer B, Stang A, Dimmel K, Tichy A, Kubacki J, Bachofen C, Steinmann E. Active equine parvovirus-hepatitis infection is most frequently detected in Austrian horses of advanced age. Equine Vet. J. 2021.
    doi: 10.1111/evj.13444pmc: PMC9292856pubmed: 33704819google scholar: lookup
  16. Lu G, Wu L, Ou J, Li S. Equine Parvovirus-Hepatitis in China: Characterization of Its Genetic Diversity and Evidence for Natural Recombination Events Between the Chinese and American Strains. Front. Vet. Sci. 2020;7:121.
    doi: 10.3389/fvets.2020.00121pmc: PMC7076910pubmed: 32211433google scholar: lookup
  17. Meister TL, Tegtmeyer B, Brüggemann Y, Sieme H, Feige K, Todt D, Stang A, Cavalleri J, Steinmann E. Characterization of equine parvovirus in thoroughbred breeding horses from Germany. Viruses 2019;11:965.
    doi: 10.3390/v11100965pmc: PMC6833105pubmed: 31635426google scholar: lookup
  18. Altan E, Li Y, Sabino-Santos G Jr, Sawaswong V, Barnum S, Pusterla N, Deng X, Delwart E. Viruses in horses with neurologic and respiratory diseases. Viruses 2019;11:942.
    doi: 10.3390/v11100942pmc: PMC6832430pubmed: 31614994google scholar: lookup
  19. Lu G, Sun L, Ou J, Xu H, Wu L, Li S. Identification and genetic characterization of a novel parvovirus associated with serum hepatitis in horses in China. Emerg. Microbes Infect. 2018;7:1–7.
    doi: 10.1038/s41426-018-0174-2pmc: PMC6198012pubmed: 30348940google scholar: lookup
  20. de Moraes MVDS, Salgado CRS, Godoi TLOS, de Almeida FQ, Chalhoub FLL, de Filippis AMB, de Souza AM, de Oliveira JM, Figueiredo AS. Equine parvovirus-hepatitis is detected in South America, Brazil. Transbound. Emerg. Dis. 2021.
    doi: 10.1111/tbed.14226pubmed: 34236767google scholar: lookup
  21. García-Bocanegra I, Rivero A, Caballero-Gómez J, López-López P, Cano-Terriza D, Frías M, Jiménez-Ruiz S, Risalde MA, Gómez-Villamandos JC, Rivero-Juarez A. Hepatitis E virus infection in equines in Spain. Transbound. Emerg. Dis. 2019;66:66–71.
    doi: 10.1111/tbed.12962pubmed: 30047239google scholar: lookup
  22. Kim HS, Moon HW, Sung HW, Kwon HM. First identification and phylogenetic analysis of equine hepacivirus in Korea. Infect. Genet. Evol. 2017;49:268–272.
    doi: 10.1016/j.meegid.2017.01.030pubmed: 28161473google scholar: lookup
  23. Kapoor A, Simmonds P, Gerold G, Qaisar N, Jain K, Henriquez JA, Firth C, Hirschberg DL, Rice CM, Shields S. Characterization of a canine homolog of hepatitis C virus. Proc. Natl. Acad. Sci. USA. 2011;108:11608–11613.
    doi: 10.1073/pnas.1101794108pmc: PMC3136326pubmed: 21610165google scholar: lookup
  24. Mizuo H, Suzuki K, Takikawa Y, Sugai Y, Tokita H, Akahane Y, Itoh K, Gotanda Y, Takahashi M, Nishizawa T. Polyphyletic strains of hepatitis E virus are responsible for sporadic cases of acute hepatitis in Japan. J. Clin. Microbiol. 2002;40:3209–3218.
  25. Park H, Jung S, Shin H, Ha SD, Park TJ, Park JP, Seo DJ, Choi C. Localization and persistence of hepatitis A virus in artificially contaminated oysters. Int. J. Food Microbiol. 2019;299:58–63.
  26. Seo DJ, Jung D, Jung S, Ha SK, Ha SD, Choi IS, Myoung J, Choi C. Experimental miniature piglet model for the infection of human norovirus GII. J. Med. Virol. 2018;90:655–662.
    doi: 10.1002/jmv.24991pubmed: 29106738google scholar: lookup
  27. Kopper J, Schott H, Divers T, Mullaney T, Huang L, Noland E, Smedley R. Theiler’s disease associated with administration of tetanus antitoxin contaminated with nonprimate (equine) hepacivirus and equine parvovirus-hepatitis virus. Equine Vet. Educ. 2020;32:e5–e9.
    doi: 10.1111/eve.12999google scholar: lookup
  28. Vengust M, Jager MC, Zalig V, Cociancich V, Laverack M, Renshaw RW, Dubovi E, Tomlinson JE, Van de Walle GR, Divers TJ. First report of equine parvovirus-hepatitis-associated Theiler’s disease in Europe. Equine Vet. J. 2020;52:841–847.
    doi: 10.1111/evj.13254pmc: PMC7483838pubmed: 32145096google scholar: lookup
  29. Underwood C, Southwood LL, Walton RM, Johnson AL. Hepatic and metabolic changes in surgical colic patients: A pilot study. J. Vet. Emerg. Crit. Care. 2010;20:578–586.
  30. Sharkey LC, DeWitt S, Stockman C. Neurologic signs and hyperammonemia in a horse with colic. Vet. Clin. Pathol. 2006;35:254–258.