Elsevier

Virus Research

Volume 111, Issue 1, July 2005, Pages 13-27
Virus Research

Molecular epizootiology of rabies associated with terrestrial carnivores in Mexico

https://doi.org/10.1016/j.virusres.2005.03.007Get rights and content

Abstract

Epizootiological patterns of rabies are described, using antigenic and genetic analysis of samples obtained from infected domestic and wild mammals in 20 Mexican states during 1976–2002. Two independent origins are suggested for rabies in Mexican carnivores. One group shares ancestry with canine rabies, while the other group appears to share a common origin with bat rabies in North America. More than 12 sublineages were found in rabid dog populations, suggesting at least six major spatio-temporal foci. Coyote rabies was found as independent enzootic foci that probably emerged via spillover from dog rabies, translocated from major foci in the southcentral and western regions of Mexico. One focus of gray fox rabies was widely distributed in northwestern Mexico, overlapping with a focus in the same species in the southwestern United States. A skunk rabies focus distributed in the northcentral Mexican states appears to share a common origin with bat rabies foci in North America, and is a close relative of southcentral skunk and raccoon rabies in the United States. Two other skunk foci share a common ancestor with canine rabies and were distributed in northwest Mexico and Yucatan.

Introduction

Rabies has been recorded since the first human civilizations, with the dog as the main transmitter (Wilkinson, 2002). In developed countries, traditional descriptive approaches have been applied to infer patterns of disease transmission to humans (Krebs et al., 2003). This approach has been reinforced by the process of rabies virus typing at the antigenic and genetic level (Bourhy et al., 1993, Rupprecht et al., 1987, Smith et al., 1992). The detection and analysis of subtle differences within the rabies virus proteins and genes have permitted the identification of viral variants specifically maintained by different animals, such as dogs, foxes, raccoons, skunks, and bats. The combined use of those latter approaches, together with an efficient surveillance system for disease detection in animal populations, have allowed detailed descriptions of the distributions of major rabies foci, as well as the likely hosts responsible for maintenance (Bourhy et al., 1999, Nadin-Davis et al., 1999, Smith et al., 1995). Data provided by such molecular approaches have permitted insights to virus-reservoir relationships, patterns of transmission and dissemination, as well as viral evolution (Badrane and Tordo, 2001; Bourhy et al., 1993, Bourhy et al., 1999, Holmes et al., 2002, Nadin-Davis et al., 1999, Smith et al., 1995). In contrast, developing countries are faced with less than ideal surveillance in animal populations. The reduced resources available are prioritized for diseases with overwhelming human morbidity and mortality. Often, sample availability is limited and wholly dependent upon human rabies occurrence or the perception of major outbreaks. During the past decade, different analytical approaches have been applied to Mexican rabies virus samples. These approaches have provided insights regarding rabies virus diversity and the likely reservoirs responsible for transmission and maintenance (De Mattos et al., 1999, Loza-Rubio et al., 1999, Velasco-Villa et al., 2002). However, previous studies have been limited by sample sizes or the approach applied, to address the deeper descriptive epizootiology of rabies in Mexico. In the present work, we incorporate 138 sequences comprising a 30-year period. The objective of this study was the molecular analysis of rabies viruses associated with terrestrial carnivores in Mexico, describing updated disease distributions, suggested trends of interspecies transmission, and predicted patterns of dissemination, by using 88 amino acids of the nucleoprotein C terminus.

Section snippets

Antigenic characterization

The rabies virus N protein was characterized with a panel of eight monoclonal antibodies, previously used to infer rabies virus reservoir species associations in Latin America and the Caribbean (Diaz et al., 1994). This reduced panel was able to identify 11 reactivity patterns associated with different animals involved with rabies virus maintenance and transmission in Mexico and South America (Table 1).

Samples and sequences

In the present study, 138 sequences were analyzed, including the outgroup represented by the

Results

Analysis of the 136 sequences indicated the occurrence of 142 conserved sites, 178 variable sites, and 160 parsimonious informative sites. The nucleotide identity in the 136 sequences ranged from 78.7 to 100% with an average of 90.3%, whereas the amino acid identity ranged from 89 to 100% with an average of 97.2%. Similarly, consensus sequences varied from 79.3 to 97.7% with an average of 89.5% for nucleotide identity, and from 90.8 to 100%, with an average of 97% for amino acid identity (Table

Discussion

Overall, a relatively high degree of variation was found within the last 264 nucleotides encoding for 88 amino acids at the C terminus of the rabies virus nucleoprotein. Most regions contributing to putative B and Th cell epitopes were retained, as was the putative phosphorylation site, at Ser 389 (Dietzschold et al., 1987, Ertl et al., 1991). Some amino acid positions conserved along time were found in association with specific lineages, suggesting that traces of positive selection may also be

Acknowledgments

We thank our colleagues working at the National Network of Public Health Rabies Laboratories in Mexico and in the US as well as the epidemiologists and personnel of the rabies control program in Mexico, who provided samples and epidemiological information about them; Jose Luis Marrufo Olivares and Isaias Sauri from the Laboratorio Central Regional of Merida, Yucatan for providing information about Yucatan samples; and to Caroline J. Henderson, Jennifer M. Snaman and Leslie Real who kindly

References (39)

  • H. Badrane et al.

    Host switching in Lyssavirus history from the chiroptera to the carnivora orders

    J. Virol.

    (2001)
  • H. Bourhy et al.

    Ecology and evolution of rabies virus in Europe

    J. Gen. Virol.

    (1999)
  • D. David et al.

    Molecular epidemiology of rabies virus samples from Israel and other middle- and near-eastern countries

    J. Clin. Microbiol.

    (2000)
  • C.C. De Mattos et al.

    Molecular characterization of rabies virus samples from Mexico: implications for transmission dynamics and human risk

    Am. J. Trop. Med. Hyg.

    (1999)
  • A.M. Diaz et al.

    Antigenic analysis of rabies-virus samples from Latin America and the Caribbean

    J. Vet. Med. Series B

    (1994)
  • H. Ertl et al.

    T helper cell epitope of rabies virus nucleoprotein defined by tri- and tetrapeptides

    Eur. J. Immunol.

    (1991)
  • J.E. Fa et al.

    Patrones de Diversidad de Mamíferos en México

  • J. Felsenstein

    Confidence limits on phylogenies: an approach using the bootstrap

    Evolution

    (1985)
  • M.A. Guerra et al.

    Skunk and raccoon rabies in the eastern United States: temporal and spatial analysis

    Emerg. Infect. Dis.

    (2003)
  • Cited by (0)

    View full text