1887

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Volume 86, Issue 11

Antigenic and genetic characterization of rabies viruses isolated from domestic and wild animals of Brazil identifies the hoary fox as a rabies reservoir Free

Abstract

Fifty Brazilian rabies viruses, collected from many different animal species and several regions of the country, were characterized by partial sequencing of the central, variable region of the gene, a locus useful for sensitive molecular epidemiological studies. Phylogenetic analysis of the sequences, which included comparison with other rabies strains recovered from throughout the Americas, identified three main groups of Brazilian viruses, arbitrarily designated BRL-1 to BRL-3. BRL-1 was found in terrestrial carnivores and clusters with other American strains of the cosmopolitan lineage. BRL-2 comprised two distinct isolates, recovered from two species of non-haematophagous bats, that had evolutionary links to insectivorous-bat-derived strains of North America. BRL-3 consisted of isolates from vampire bats and from livestock species probably infected via contact with vampire bats. The terrestrial group was further subdivided into three subtypes: BRL-1a was associated exclusively with dogs and cats, while BRL-1b and BRL-1c were found exclusively in hoary foxes. These observations strongly support the role of the Brazilian hoary fox as a rabies reservoir. Screening of representative Brazilian rabies viruses against a collection of anti-rabies monoclonal antibodies (mAbs) identified a small panel of mAbs that could be used to discriminate between all Brazilian subgroups as defined by genetic classification in this study.

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2005-11-01
2024-04-19
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References

  1. Araújo F. A. A. 2002; Raiva humana no Brasil: 1992-2001 . ( Human rabies in Brazil: 1992-2001 ). 90 f. Master in Veterinary Medicine thesis - Escola de Veterinária, Universidade Federal de Minas Gerais Belo Horizonte, Minas Gerais, Brazil:
     [Google Scholar]
  2. Badrane H., Tordo N. 2001; Host switching in Lyssavirus history from the chiroptera to the carnivore orders. J Virol 75:8096–8104 [CrossRef]
     [Google Scholar]
  3. Barros J. S., de Freitas C. E. A. A., de Sousa F. S. 1989; Raiva em animais silvestres no Estado do Ceará particularmente na raposa ( Dusicyon vetulus ). Zoonoses Rev Int 1:9–13
     [Google Scholar]
  4. Bordignon J., Brasil-dos-Anjos G., Bueno C. R., Salvatiera-Oporto J., Dávila A. M. R., Grisard E. C., Zanetti C. R. 2005; Detection and characterization of rabies virus in Southern Brazil by PCR amplification and sequencing of the nucleoprotein gene. Arch Virol 150:695–708 [CrossRef]
     [Google Scholar]
  5. Bourhy H., Kissi B., Tordo N. 1993; Molecular diversity of the Lyssavirus genus. Virology 194:70–81 [CrossRef]
     [Google Scholar]
  6. Bourhy H., Kissi B., Audry L., Smreczak M., Sadkowska-Todys M., Kulonen K., Tordo N., Zmudzinski J. F., Holmes E. C. 1999; Ecology and evolution of rabies virus in Europe. J Gen Virol 80:2545–2557
     [Google Scholar]
  7. Cisterna D., Bonaventura R., Caillou S. 10 other authors 2005; Antigenic and molecular characterization of rabies virus in Argentina. Virus Res 109:139–147 [CrossRef]
     [Google Scholar]
  8. Dean D. J., Ableseth M. K., Atanasiu P. 1996; The fluorescent antibody test. In Laboratory Techniques in Rabies , 4th edn. pp  88–95 Edited by Meslin F. X., Kaplan M. M., Koprowski H. Geneva: World Health Organization;
     [Google Scholar]
  9. Delpietro H. A., Gury-Dhomen F., Larghi O. P., Mena-Segura C., Abramo L. 1997; Monoclonal antibody characterization of rabies virus strains isolated in the River Plate Basin. Zentrabl Veterinaermed B 44:477–483
     [Google Scholar]
  10. De Mattos C. A., De Mattos C. C., Smith J. S., Miller E. T., Papo S., Utrera A., Osburn B. I. 1996; Genetic characterization of rabies field isolates from Venezuela. J Clin Microbiol 34:1553–1558
     [Google Scholar]
  11. De Mattos C. A., Favi M., Yung V., Pavletic C., De Mattos C. C. 2000; Bat rabies in urban centers in Chile. J Wildl Dis 36:231–240 [CrossRef]
     [Google Scholar]
  12. Diaz A. M., Papo S., Rodriguez A., Smith J. S. 1994; Antigenic analysis of rabies-virus isolates from Latin América and Caribbean. Zentralbl Veterinaermed B 41:153–160
     [Google Scholar]
  13. Favoretto S. R., De Mattos C. C., Morais N. B., Alves Araújo F. A., De Mattos C. A. 2001; Rabies in marmosets ( Callithrix jacchus ), Ceará, Brazil. Emerg Infect Dis 7:1062–1065 [CrossRef]
     [Google Scholar]
  14. Favoretto S. R., Carrieri M. L., Cunha E. M. S., Aguiar E. A. C., Silva L. H. Q., Sodré M. M., Souza M. C. A. M., Kotait I. 2002; Antigenic typing of Brazilian rabies virus samples isolated from animals and humans, 1989-2000. Rev Inst Med Trop Sao Paulo 44:91–95
     [Google Scholar]
  15. Felsenstein J. 1993; phylip: phylogeny inference package. (Version 3.52c) Department of Genome Sciences, University of Washington; Seattle, WA, USA:
  16. Fooks A. R. 2004; The challenge of new and emerging lyssaviruses. Expert Rev Vaccines 3:333–336 [CrossRef]
     [Google Scholar]
  17. Gomes A. A. B. 2004; Epidemiologia da raiva: caracterização de vírus isolados de animais domésticos e silvestres do semi-árido paraibano da região de Patos, Nordeste do Brasil. (Epidemiology of rabies: characterization of viruses isolated from domestic and wild animals of the semi-arid region of Patos, state of Paraíba. North-Eastern Brazil;107 f Doctorate in Veterinary Medicine thesis - Faculty of Veterinary Medicine and Zootechny University of São Paulo, São Paulo;
     [Google Scholar]
  18. Guerra M. A., Curns A. T., Rupprecht C. E., Hanlon C. A., Krebs J. W., Childs J. E. 2003; Skunk and raccoon rabies in the eastern United States: temporal and spatial analysis. Emerg Infect Dis 9:1143–1150 [CrossRef]
     [Google Scholar]
  19. Ito M., Arai Y. T., Itou T., Sakei T., Ito F. H., Takasaki T., Kurane I. 2001a; Genetic characterization and geographic distribution of rabies virus isolates in Brazil: identification of two reservoirs, dogs and vampire bats. Virology 284:214–222 [CrossRef]
     [Google Scholar]
  20. Ito M., Itou T., Sakai T., Santos M. F. C., Arai Y. T., Takasaki T., Kurane I., Ito F. H. 2001b; Detection of rabies virus RNA isolated from several species of animals in Brazil by RT-PCR. J Vet Med Sci 63:1309–1313 [CrossRef]
     [Google Scholar]
  21. Ito M., Itou T., Shoji Y., Sakai T., Ito F. H., Arai Y. T., Takasaki T., Kurane I. 2003; Discrimination between dog-related and vampire bat-related rabies viruses in Brazil by strain-specific reverse transcriptase-polymerase chain reaction and restriction fragment length polymorphism analysis. J Clin Virol 26:317–330 [CrossRef]
     [Google Scholar]
  22. Johnson N., Black C., Smith J., Un H., McElhinney L. M., Aylan O., Fooks A. R. 2003; Rabies emergence among foxes in Turkey. J Wildl Dis 39:262–270 [CrossRef]
     [Google Scholar]
  23. Kissi B., Tordo N., Bourhy H. 1995; Genetic polymorphism in the rabies virus nucleoprotein gene. Virology 209:526–537 [CrossRef]
     [Google Scholar]
  24. Koprowski H. 1996; The mouse inoculation test. In Laboratory Techniques in Rabies , 4th edn. pp  80–87 Edited by Meslin F. X., Kaplan M. M., Koprowsky H. Geneva: World Health Organization;
     [Google Scholar]
  25. Krebs J. W., Wheeling J. T., Childs J. E. 2003; Rabies surveillance in the United States during 2002. J Am Vet Med Assoc 223:1736–1748 [CrossRef]
     [Google Scholar]
  26. Le Mercier P., Jacob Y., Tordo N. 1997; The complete Mokola virus genome sequence: structure of the RNA-dependent RNA polymerase. J Gen Virol 78:1571–1576
     [Google Scholar]
  27. Ministério Da Saúde. 2004; Programa nacional de profilaxia da raiva. Casos de raiva humana notificados, e percentual de casos transmitidos segundo a espécie animal. Brasília 2004 Brazilian Ministry of Health annual disease report http://portal.saude.gov.br/portal/svs/visualizar_texto.cfm?idtxt=21906
     [Google Scholar]
  28. Morais N. B., Rolim B. N., Chaves H. H. M., Brito-Neto J., Silva L. M. 2000; Rabies in tamarins ( Callithrix jacchus ) in the State of Ceará, Brazil, a distinct viral variant?. Mem Inst Oswaldo Cruz 95:609–610 [CrossRef]
     [Google Scholar]
  29. Nadin-Davis S. A. 1998; Polymerase chain reaction protocols for rabies virus discrimination. J Virol Methods 75:1–8 [CrossRef]
     [Google Scholar]
  30. Nadin-Davis S. A., Bingham J. 2004; Europe as a source of rabies for the rest of the world. In Historical Perspective of Rabies in Europe and the Mediterranean Basin pp  259–280 Edited by King A. A., Fooks A. R., Aubert M., Wandeler A. I. Paris: OIE Press;
     [Google Scholar]
  31. Nadin-Davis S. A., Huang W., Armstrong J., Casey G. A., Bahloul C., Tordo N., Wandeler A. I. 2001; Antigenic and genetic divergence of rabies viruses from bat species indigenous to Canada. Virus Res 74:139–156 [CrossRef]
     [Google Scholar]
  32. Nadin-Davis S. A., Abdel-Malik M., Armstrong J., Wandeler A. I. 2002; Lyssavirus P gene characterization provides insights into the phylogeny of the genus and identifies structural similarities and diversity within the encoded phosphoprotein. Virology 298:286–305 [CrossRef]
     [Google Scholar]
  33. Nadin-Davis S. A., Simani S., Armstrong J., Fayaz A., Wandeler A. I. 2003; Molecular and antigenic characterization of rabies viruses from Iran identifies variants with distinct epidemiological origins. Epidemiol Infect 131:777–790 [CrossRef]
     [Google Scholar]
  34. Nel L., Jacobs J., Jaftha J., Meredith C. 1997; Natural spillover of a distinctly canidae-associated biotype of rabies virus into an expanded wildlife host range in southern Africa. Virus Genes 15:79–82 [CrossRef]
     [Google Scholar]
  35. Organización Pan-Americana de la Salud (OPAS) 2001 Boletín: vigilância epidemiológica de la rabia em las Américas XXXIII p p– 40 Rio de Janeiro: Organización Pan-Americana de la Salud;
     [Google Scholar]
  36. Páez A., Nũnez C., Garcĩa C., Bóshell J. 2003; Molecular epidemiology of rabies epizootics in Colombia: evidence for human and dog rabies associated with bats. J Gen Virol 84:795–802 [CrossRef]
     [Google Scholar]
  37. Páez A., Saad C., Nũnez C., Bóshell J. 2005; Molecular epidemiology of rabies in northern Colombia 1994-2003. Evidence for human and fox rabies associated with dogs. Epidemiol Infect 133:529–536 [CrossRef]
     [Google Scholar]
  38. Page R. D. M. 1996; treeview: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358
     [Google Scholar]
  39. Poisson N., Real E., Gaudin Y., Vaney M.-C., King S., Jacob Y., Tordo N., Blondel D. 2001; Molecular basis for the interaction between rabies virus phosphoprotein P and the dynein light chain LC8: dissociation of dynein-binding properties and transcriptional functionality of P. J Gen Virol 82:2691–2696
     [Google Scholar]
  40. Roehe P. M., Pantoja L. D., Shaefer R., Nardi N. B., King A. A. 1997; Analysis of Brazilian rabies isolates with monoclonal antibodies to lyssavirus antigens. Rev Microbiol 28:288–292
     [Google Scholar]
  41. Romijn P. C., Van der Heide R., Cattaneo C. A., Silva R. D. E. C., Van der Poel W. H. 2003; Study of lyssaviruses of bat origin as a source of rabies for other animal species in the State of Rio de Janeiro, Brazil. Am J Trop Med Hyg 69:81–86
     [Google Scholar]
  42. Sato G., Itou T., Shoji Y. 9 other authors 2004; Genetic and phylogenetic analysis of glycoprotein of rabies virus isolated from several species in Brazil. J Vet Med Sci 66:747–753 [CrossRef]
     [Google Scholar]
  43. Sato G., Tanabe H., Shoji Y., Itou T., Ito F. H., Sato T., Sakai T. 2005; Rapid discrimination of rabies viruses isolated from various host species in Brazil by multiplex reverse transcription-polymerase chain reaction. J Clin Virol 33:267–273 [CrossRef]
     [Google Scholar]
  44. Schaefer R., Batista H. B. R., Franco A. C., Rijsewijk F. A. M., Roehe P. M. 2005; Studies on antigenic and genomic properties of Brazilian rabies virus isolates. Vet Microbiol 107:161–170 [CrossRef]
     [Google Scholar]
  45. Shoji Y., Kobayashi Y., Sato G. 10 other authors 2004; Genetic characterization of rabies viruses isolated from frugivorous bat ( Artibeus spp.) in Brazil. J Vet Med Sci 666:1271–1273
     [Google Scholar]
  46. Stankov S. 2001; Typing of field rabies virus strains in FR Yugoslavia by limited sequence analysis and monoclonal antibodies. Med Pregl 54:446–452
     [Google Scholar]
  47. Thompson J. D., Gibson T. J., Plewniak F., Jeanmougin F., Higgins D. G. 1997; The Clustal_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882 [CrossRef]
     [Google Scholar]
  48. Tordo N., Poch O., Ermine A., Keith G., Rougeon F. 1986; Walking along the rabies genome: is the large G-L intergenic region a remnant gene?. Proc Natl Acad Sci U S A 83:3914–3918 [CrossRef]
     [Google Scholar]
  49. Tordo N., Charlton K., Wandeler A. 1998; Rhabdoviruses: rabies. In Topley and Wilson's Microbiology and Microbial Infections pp  666–692 Edited by Collier L. H. London: Arnold Press;
     [Google Scholar]
  50. Velasco-Villa A., Gómez-Sierra M., Hernández-Rodríguez G., Juárez-Islas V., Meléndez-Félix A., Vargas-Pino F., Velázquez-Monroy O., Flisser A. 2002; Antigenic diversity and distribution of rabies virus in Mexico. J Clin Microbiol 40:951–958 [CrossRef]
     [Google Scholar]
  51. Yung V., Favi M., Fernández J. 2002; Genetic and antigenic typing of rabies virus in Chile. Arch Virol 147:2197–2205 [CrossRef]
     [Google Scholar]
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Antigenic and genetic characterization of rabies viruses isolated from domestic and wild animals of Brazil identifies the hoary fox as a rabies reservoir
J. Gen. Virol. 86, 3153 (2005); https://doi.org/10.1099/vir.0.81223-0
/content/journal/jgv/10.1099/vir.0.81223-0
/content/journal/jgv/10.1099/vir.0.81223-0
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