Analyze Diet
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.
Publication Date: 2023-09-01 PubMed ID: 37656696PubMed Central: PMC10473478DOI: 10.1371/journal.pone.0290309Google 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 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

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.

References

This article includes 49 references
  1. O’toole D, Li H. The Pathology of malignant catarrhal fever, with an emphasis on ovine herpesvirus 2. Vet Pathol 2014;51:437–52.
    doi: 10.1177/0300985813520435pubmed: 24503439google scholar: lookup
  2. Russell GC, Stewart JP, Haig DM. Malignant catarrhal fever: a review. Vet J 2009;179:324–35.
    doi: 10.1016/j.tvjl.2007.11.007pubmed: 18760944google scholar: lookup
  3. Amoroso MG, Galiero G, Fusco G. Genetic characterization of ovine herpesvirus 2 strains involved in water buffaloes malignant catarrhal fever outbreaks in Southern Italy. Vet Microbiol 2017;199:31–5.
    doi: 10.1016/j.vetmic.2016.12.020pubmed: 28110782google scholar: lookup
  4. Li H, Brooking A, Cunha CW, Highland MA, O’Toole D, Knowles DP. Experimental induction of malignant catarrhal fever in pigs with ovine herpesvirus 2 by intranasal nebulization. Vet Microbiol 2012;159:485–9.
    doi: 10.1016/j.vetmic.2012.04.016pubmed: 22560763google scholar: lookup
  5. Foyle KL, Fuller HE, Higgins RJ, Russell GC, Willoughby K, Rosie WG. Malignant catarrhal fever in sika deer (Cervus nippon) in the UK. Vet Rec 2009;165:445–7.
    doi: 10.1136/vr.165.15.445pubmed: 19820260google scholar: lookup
  6. Costa ÉA, Bomfim MRQ, Da Fonseca FG, Drumond BP, Coelho FM, Vasconcelos AC. Ovine herpesvirus 2 infection in Foal, Brazil. Emerg Infect Dis 2009;15:844–5.
    doi: 10.3201/eid1505.081664pmc: PMC2687043pubmed: 19402994google scholar: lookup
  7. Gailbreath KL, Taus NS, Cunha CW, Knowles DP, Li H. Experimental infection of rabbits with ovine herpesvirus 2 from sheep nasal secretions. Vet Microbiol 2008;132:65–73.
    doi: 10.1016/j.vetmic.2008.04.035pubmed: 18539411google scholar: lookup
  8. Li H, Cunha CW, Taus NS. Malignant catarrhal fever: understanding molecular diagnostics in context of epidemiology. Int J Mol Sci 2011;12:6881–93.
    doi: 10.3390/ijms12106881pmc: PMC3211016pubmed: 22072925google scholar: lookup
  9. Nelson DD, Taus NS, Schneider DA, Cunha CW, Davis WC, Brown WC. Fibroblasts express OvHV-2 capsid protein in vasculitis lesions of American bison (Bison bison) with experimental sheep-associated malignant catarrhal fever. Vet Microbiol 2013;166:486–92.
    doi: 10.1016/j.vetmic.2013.07.021pubmed: 23953727google scholar: lookup
  10. Sood R, Kumar N, Bhatia S. Malignant catarrhal fever. Emerging and re-emerging infectious diseases of livestock 2017:347–62.
  11. O’Toole D, Li H, Sourk C, Montgomery DL, Crawford TB. Malignant catarrhal fever in a bison (Bison bison) feedlot, 1993–2000. J Vet Diagn Invest 2002;14:183–93.
    doi: 10.1177/104063870201400301pubmed: 12033673google scholar: lookup
  12. Traul DL, Taus NS, Oaks JL, O’Toole D, Rurangirwa FR, Baszler T V.. Validation of nonnested and real-time PCR for diagnosis of sheep-associated malignant catarrhal fever in clinical samples. J Vet Diagn Invest 2007;19:405–8.
    doi: 10.1177/104063870701900412pubmed: 17609352google scholar: lookup
  13. Wan SK, Castro AE, Heuschele WP, Ramsay EC. Enzyme-linked immunosorbent assay for the detection of antibodies to the alcelaphine herpesvirus of malignant catarrhal fever in exotic ruminants. Am J Vet Res 1988;49:164–8.
    pubmed: 3348526
  14. Rossiter PB. Immunofluorescence and immunoperoxidase techniques for detecting antibodies to malignant catarrhal fever in infected cattle. Trop Anim Health Prod 1981;13:189–92.
    doi: 10.1007/BF02237922pubmed: 7046177google scholar: lookup
  15. Herring A, Reid H, Inglis N, Pow I. Immunoblotting analysis of the reaction of wildebeest, sheep and cattle sera with the structural antigens of alcelaphine herpesvirus-1 (malignant catarrhal fever virus). Vet Microbiol 1989;19:205–15.
    doi: 10.1016/0378-1135(89)90067-9pubmed: 2718352google scholar: lookup
  16. Sentsui H, Nishimori T, Nagai I, Nishioka N. Detection of sheep-associated malignant catarrhal fever virus antibodies by complement fixation tests. J Vet Med Sci 1996;58:1–5.
    doi: 10.1292/jvms.58.1pubmed: 8645750google scholar: lookup
  17. Li H, Shen DT, Knowles DP, Gorham JR, Crawford TB. Competitive inhibition enzyme-linked immunosorbent assay for antibody in sheep and other ruminants to a conserved epitope of malignant catarrhal fever virus. J Clin Microbiol 1994;32:1674–9.
  18. Mushi EZ, Plowright W. A microtitre technique for the assay of malignant catarrhal fever virus and neutralizing antibody. Res Vet Sci 1979;27:230–2.
    doi: 10.1016/S0034-5288(18)32835-2pubmed: 523811google scholar: lookup
  19. Decaro N, Tinelli A, Pratelli A, Martella V, Tempesta M, Buonavoglia C. First two confirmed cases of malignant catarrhal fever in Italy. New Microbiol 2003;26:339–44.
    pubmed: 14596344
  20. Dubuisson J, Thiry E, Bublot M, Sneyers M, Boulanger D, Guillaume J. Production and characterization of monoclonal antibodies to bovid herpesvirus-4. Vet Microbiol 1989;19:305–15.
    doi: 10.1016/0378-1135(89)90096-5pubmed: 2546320google scholar: lookup
  21. Li H, Shen DT, O’Toole D, Knowles DP, Gorham JR, Crawford TB. Investigation of sheep-associated malignant catarrhal fever virus infection in ruminants by PCR and competitive inhibition enzyme-linked immunosorbent assay. J Clin Microbiol 1995;33:2048–53.
  22. Plowright W, Ferris RD, Scott GR. Blue wildebeest and the aetiological agent of bovine malignant catarrhal fever. Nature 1960;188:1167–9.
    doi: 10.1038/1881167a0pubmed: 13736396google scholar: lookup
  23. Alhajri SM, Cunha CW, Knowles DP, Li H, Taus NS. Evaluation of glycoprotein Ov8 as a potential antigen for an OvHV-2-specific diagnostic assay. PLoS One 2018;13:e0200130.
  24. Plowright W, Ferris RD. The preparation of bovine thyroid monolayers for use in virological investigations. Res Vet Sci 1961;2:149–53.
  25. Castro AE, Daley GG, Zimmer MA, Whitenack DL, Jensen J. Malignant catarrhal fever in an Indian gaur and greater kudu: experimental transmission, isolation, and identification of a herpesvirus. Am J Vet Res 1982;43:5–11.
    pubmed: 7091816
  26. Hristov M V, Peshev RD. Isolation, and identification of malignant catarrhal fever virus in cell cultures. Bulg J Vet Med 2016;19:263–73.
    doi: 10.15547/BJVM.935google scholar: lookup
  27. Li H, Taus NS, Jones C, Murphy B, Evermann JF, Crawford TB. A devastating outbreak of malignant catarrhal fever in a bison feedlot. J Vet Diagn Invest 2006;18:119–23.
    doi: 10.1177/104063870601800120pubmed: 16566270google scholar: lookup
  28. Headley SA, de Oliveira TES, Cunha CW. A review of the epidemiological, clinical, and pathological aspects of malignant catarrhal fever in Brazil. Braz J Microbiol 2020;51:1405–32.
    doi: 10.1007/s42770-020-00273-6pmc: PMC7455687pubmed: 32542424google scholar: lookup
  29. Aluja A, Rocha TC De, Velázquez A. Fiebre catarral maligna. Rev Mex Cienc Pecu 1969:1–8.
    doi: 10.22319/RMCP.V0I12google scholar: lookup
  30. Pérez-Guiot A, Páez-Trejo A, Domínguez-Hernández Y, Carranza-Velázquez J, Hernández-García D, Carrisoza-Urbina I. Malignant catarrhal fever associated with ovine gammaherpesvirus-2 in domestic ruminants in Queretaro, Mexico. Pak Vet J 2022;43:61–6.
    doi: 10.29261/pakvetj/2022.076google scholar: lookup
  31. English D, Andersen BR. Single-step separation of red blood cells. Granulocytes and mononuclear leukocytes on discontinuous density gradients of Ficoll-Hypaque. J Immunol Methods 1974;5:249–52.
    doi: 10.1016/0022-1759(74)90109-4pubmed: 4427075google scholar: lookup
  32. Baxter SIF, Pow I, Bridgen A, Reid HW. PCR detection of the sheep-associated agent of malignant catarrhal fever. Arch Virol 1993;132:145–59.
    doi: 10.1007/BF01309849pubmed: 8352654google scholar: lookup
  33. . High Pure PCR Template Preparation Kit. Roche 2020;27.
  34. Reed LJ, Muench H. A simple method of estimating fifty percent endpoints. Am J Epidemiol 1938;27:493–7.
  35. Hall TA. BioEdit a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Scientific Research Publishing 1999:95–8.
  36. Tamura K, Stecher G, Kumar S. MEGA11: molecular evolutionary genetics analysis version 11. Mol Biol Evol 2021;38:3022–7.
    doi: 10.1093/molbev/msab120pmc: PMC8233496pubmed: 33892491google scholar: lookup
  37. Johnson M, Zaretskaya I, Raytselis Y, Merezhuk Y, McGinnis S, Madden TL. NCBI BLAST: a better web interface. Nucleic Acids Res 2008;36.
    doi: 10.1093/NAR/GKN201pmc: PMC2447716pubmed: 18440982google scholar: lookup
  38. Posada D. jModelTest: phylogenetic model averaging. Mol Biol Evol 2008;25:1253–6.
    doi: 10.1093/molbev/msn083pubmed: 18397919google scholar: lookup
  39. Tamura K, Nei M. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 1993;10:512–26.
  40. Orós J, Poveda JB, Rodríguez JL, Franklin CL, Fernández A. Natural cilia-associated respiratory bacillus infection in rabbits used for elaboration of hyperimmune serum against Mycoplasma sp. Zentralbl Veterinarmed B 1997;44:313–7.
  41. Headley SA, de Lemos GAA, Dall Agnol AM, Xavier AAC, Depes VCA, Yasumitsu CY. Ovine gammaherpesvirus 2 infections in cattle without typical manifestations of sheep-associated malignant catarrhal fever and concomitantly infected with bovine coronavirus. Braz J Microbiol 2022;53:433–46.
    doi: 10.1007/s42770-021-00653-6pmc: PMC8590972pubmed: 34780031google scholar: lookup
  42. Brown CC, Bloss LL. An epizootic of malignant catarrhal fever in a large captive herd of white-tailed deer (Odocoileus virginianus). J Wildl Dis 1992;28:301–5.
    doi: 10.7589/0090-3558-28.2.301pubmed: 1602586google scholar: lookup
  43. Rossiter PB. A lack of readily demonstrable virus antigens in the tissues of rabbits and cattle infected with malignant catarrhal fever virus. Br Vet J 1980;136:478–83.
    doi: 10.1016/s0007-1935(17)32190-5pubmed: 6784880google scholar: lookup
  44. Wright H, Stewart JP, Ireri RG, Campbell I, Pow I, Reid HW. Genome re-arrangements associated with loss of pathogenicity of the γ-herpesvirus alcelaphine herpesvirus-1. Res Vet Sci 2003;75:163–8.
    doi: 10.1016/S0034-5288(03)00043-2pubmed: 12893166google scholar: lookup
  45. Martins M de SN, Castro AMMG de, Lima M dos S, Pinto V da SC, Silva TG da, Fava C Del. Malignant Catarrhal Fever in Brazilian cattle presenting with neurological syndrome. Braz J Microbiol 2017;48:366–72.
    doi: 10.1016/j.bjm.2016.10.021pmc: PMC5470442pubmed: 28081979google scholar: lookup
  46. Russell GC, Scholes SF, Twomey DF, Courtenay AE, Grant DM, Lamond B. Analysis of the genetic diversity of ovine herpesvirus 2 in samples from livestock with malignant catarrhal fever. Vet Microbiol 2014;172:63–71.
    doi: 10.1016/j.vetmic.2014.04.011pubmed: 24846753google scholar: lookup
  47. Hart J, Ackermann M, Jayawardane G, Russell G, Haig DM, Reid H. Complete sequence and analysis of the ovine herpesvirus 2 genome. J Gen Virol 2007;88:28–39.
    doi: 10.1099/vir.0.82284-0pubmed: 17170433google scholar: lookup
  48. Goss LW, Cole CR, Kissling RE. The pathology of malignant catarrhal fever (Bovine epitheliosis): with special reference to cytoplasmic inclusions. Am J Pathol 1947;23:837.
    pmc: PMC1934312pubmed: 19970964
  49. Severi B, Landini MP, Cenacchi G, Zini N, Maraldi NM. Human cytomegalovirus nuclear and cytoplasmic dense bodies. Arch Virol 1992;123:193–207.
    doi: 10.1007/BF01317149pubmed: 1372496google scholar: lookup