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PloS one2023; 18(9); e0290309; doi: 10.1371/journal.pone.0290309

First identification and characterization of ovine gammaherpesvirus type 2 in horses and artiodactyla from an outbreak of malignant catarrhal fever in Mexico.

Abstract: Ovine gammaherpesvirus 2 (OvHV-2), a member of the genus Macavirus, causes sheep-associated malignant catarrhal fever (SA-MCF), a fatal lymphoproliferative disease affecting a wide variety of ungulates in addition to horses. This study described an outbreak of SA-MCF in Mexico and the identification of the OvHV-2 virus in primary rabbit testis cultures through the generation of intranuclear inclusion bodies, syncytia, immunofluorescence (IF), immunocytochemistry (ICC), immunohistochemistry (IHC), endpoint polymerase chain reaction (PCR), and partial sequencing of the ORF75 gene. The animals involved in this outbreak showed mucogingival ulcers in the vestibule of the mouth and tongue, hypersalivation, corneal opacity, reduced food consumption, and weight loss of variable severity. These clinical signs and the histopathological findings suggested the diagnosis of SA-MCF. Buffy coat fractions from the anticoagulated blood samples of ill animals were collected and analyzed by PCR. Positive buffy coats were used to inoculate the primary cell cultures of rabbit testis to identify the virus. Small clusters of refractile cytomegalic cells, characteristic of viral cytopathic effects, were observed between 48 and 72 h post-infection. Furthermore, intranuclear acidophilic inclusion bodies (IBs) were identified in the inoculated primary culture cells, and the cytoplasm showed immunoreactivity with hyperimmune rabbit serum against OvHV-2. Moreover, in the liver histological sections from sick deer, immunoreactive juxtanuclear IBs were identified with the same rabbit hyperimmune serum. The obtained sequences were aligned with the OvHV-2 sequences reported in GenBank and revealed a nucleotide identity higher than 98%. Based on the evidence provided in this study, we conclude that the outbreak of SA-MCF in the municipality of Tequisquiapan in the state of Queretaro, Mexico, was caused by OvHV-2. This is the second study reporting that horses are susceptible to OvHV-2 infection and can develop SA-MCF. We identified for the first time in Mexico, the presence of OvHV-2 in buffy coats from horses and Artiodactyla.
Copyright: © 2023 Madrigal-Valencia et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
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Publication Date: 2023-09-01 PubMed ID: 37656696PubMed Central: PMC10473478DOI: 10.1371/journal.pone.0290309Google Scholar: Lookup
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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 study investigates an outbreak of sheep-associated malignant catarrhal fever (SA-MCF) in Mexico, specifically tying it to ovine gammaherpesvirus 2 (OvHV-2). It presents evidence that horses, alongside a variety of ungulates, can be susceptible to OvHV-2 infection and develop SA-MCF, based on clinical signs, as well as results from immunological techniques, and polymerase chain reaction, leading to the identification of OvHV-2 in previously unrecorded animal species.

Background

  • The research is focused on exploring an outbreak of SA-MCF, a fatal disease prevalent among horses and many ungulate species, in Mexico.
  • The investigated cause for this disease is the OvHV-2 virus, which is a member of the genus Macavirus.

Methods and Findings

  • The investigators used several methodologies such as immunofluorescence, immunocytochemistry, immunohistochemistry, and endpoint polymerase chain reaction to identify the presence of OvHV-2 in primary rabbit testis cultures.
  • Histopathological findings and clinical signs such as mucogingival ulcers, hypersalivation, corneal opacity, reduced food intake, and varying degrees of weight loss, were indicative of SA-MCF.
  • The blood from affected animals was analyzed, with positive samples being used to inoculate primary cell cultures of rabbit testis.
  • Post-infection, at between 48 and 72 hours, cellular changes indicative of viral effects were noted.
  • With the help of immunoreactivity techniques, intranuclear acidophilic inclusion bodies were identified in the inoculated primary culture cells, and similar findings were observed in liver sections from ill deer.
  • This, coupled with a DNA sequence match exceeding 98% with OvHV-2 sequences from GenBank, cemented the identification of OvHV-2 as the causative agent for the investigated disease outbreak.

Conclusion

  • It was concluded that the outbreak of SA-MCF in the region was caused by OvHV-2 based on the results obtained.
  • This study marks the second instance where horses were found to be susceptible to OvHV-2 induced SA-MCF.
  • The presence of OvHV-2 was reported for the first time in Mexico in the blood samples from horses and Artiodactyla.

Cite This Article

APA
Madrigal-Valencia TL, Saavedra-Montañez M, Pérez-Torres A, Hernández J, Segalés J, Hernández YD, Candanosa-Aranda IE, Pérez-Guiot A, Ramírez-Mendoza H. (2023). First identification and characterization of ovine gammaherpesvirus type 2 in horses and artiodactyla from an outbreak of malignant catarrhal fever in Mexico. PLoS One, 18(9), e0290309. https://doi.org/10.1371/journal.pone.0290309

Publication

PloS one
ISSN: 1932-6203
NlmUniqueID: 101285081
Country: United States
Language: English
Volume: 18
Issue: 9
Pages: e0290309

Researcher Affiliations

Madrigal-Valencia, Tania Lucia
  • Departamento de Microbiología e Inmunología, Facultad de Medicina Veterinaria y Zootecnia, UNAM, Mexico City, Mexico.
Saavedra-Montañez, Manuel
  • Departamento de Microbiología e Inmunología, Facultad de Medicina Veterinaria y Zootecnia, UNAM, Mexico City, Mexico.
Pérez-Torres, Armando
  • Departamento de Biología Celular y Tisular, Facultad de Medicina, Universidad Nacional Autónoma de México (UNAM), Mexico City, Mexico.
Hernández, Jesús
  • Laboratorio de Inmunología, Centro de Investigación en Alimentación y Desarrollo, A.C. (CIAD), Hermosillo, Sonora, Mexico.
Segalés, Joaquim
  • Unitat Mixta d'Investigació IRTA-UAB en Sanitat Animal, Centre de Recerca en Sanitat Animal (CReSA), Campus de la Universitat Autònoma de Barcelona (UAB), Bellaterra, Barcelona, Catalonia, España.
  • Department de Sanitat i Anatomia Animals, Facultat de Veterinària, Campus de la Universitat Autònoma de Barcelona (UAB), Bellaterra, Barcelona, Catalonia, España.
Hernández, Yesmín Domínguez
  • Centro de Enseñanza, investigación y Extensión en Producción Animal en Altiplano (CEIEPAA), Facultad de Medicina Veterinaria y Zootecnia (FMVZ), Universidad Nacional Autónoma de México (UNAM), Tequisquiapan, Queretaro, Mexico.
Candanosa-Aranda, Irma Eugenia
  • Centro de Enseñanza, investigación y Extensión en Producción Animal en Altiplano (CEIEPAA), Facultad de Medicina Veterinaria y Zootecnia (FMVZ), Universidad Nacional Autónoma de México (UNAM), Tequisquiapan, Queretaro, Mexico.
Pérez-Guiot, Alfredo
  • División de Ciencias de la Vida, Campus Irapuato-Salamanca, Universidad de Guanajuato, ExHda El Copal, Irapuato, Guanajuato, Mexico.
Ramírez-Mendoza, Humberto
  • Departamento de Microbiología e Inmunología, Facultad de Medicina Veterinaria y Zootecnia, UNAM, Mexico City, Mexico.

MeSH Terms

  • Animals
  • Cattle
  • Male
  • Rabbits
  • Artiodactyla
  • Deer
  • Disease Outbreaks / veterinary
  • Gammaherpesvirinae / genetics
  • Horses
  • Malignant Catarrh / epidemiology
  • Mexico / epidemiology
  • Sheep

Conflict of Interest Statement

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. We would greatly appreciate your consideration for the manuscript entitled “Isolation and identification of Ovine gammaherpesvirus type 2 in an outbreak of Malignant Catarrhal Fever in Artiodactyla and horses in Mexico” for publication as a regular manuscript at PLOS ONE. This manuscript is product of the work of Tania Lucia Madrigal-Valencia, Manuel Saavedra-Montañez, Armando Pérez-Torres, Jesús Hernández, Joaquim Segalés, Yesmín Domínguez Hernández, Irma Eugenia Candanosa-Aranda, Alfredo Pérez-Guiot, and Humberto Ramírez-Mendoza. All of us have contributed to this work and we agree on its potential publication. The manuscript has been previously reviewed by Elsevier Language Editing Services (Order reference: ASLESTD0330355). We have agreed that Dr. Humberto Ramírez-Mendoza will act as corresponding author on our behalf regarding any subsequent processing of the paper.

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  1. Gupta A, Li R, Shair K, Gao SJ. Model Systems of Gammaherpesvirus Infection, Immunity, and Disease. J Med Virol 2025 Sep;97(9):e70581.
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  2. Bastawecy IM, Abdelmonem M, Afify AF, Saad N, Shirosaki Y, Abdullah CAC, El Naggar RF, Rohaim MA, Munir M. Viral contamination in cell culture: analyzing the impact of Epstein Barr virus and Ovine Herpesvirus 2. Front Microbiol 2025;16:1442321.
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  3. Shyamsundar KA, Rathnamma D, Gulati BR, Isloor S, Chandranaik BM, Sharada R, Shivashankar BP, Suresh KP, Ranganatha S, Patil SS. Transmission patterns of malignant catarrhal fever in sheep and cattle in Karnataka, India. Vet Res Commun 2024 Oct;48(5):3437-3443.
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