Rabies viruses are members of the genus Lyssavirus within the Rhabdoviridae family. To date, 16 species in the genus Lyssavirus have been recognized by the International Committee on Taxonomy of Viruses.1
Rabies is responsible for at least 60,000 human deaths every year.2 Virus transmission most often occurs following a bite from an infected animal or as a result of fresh saliva from an infected animal coming into contact with a break in the skin or the mucous membranes of another mammal.3 In Mexico, where dog-to-dog transmission has been controlled through vaccination, infected bats, skunks, and foxes represent the major risk of rabies transmission to humans.
Currently, > 1,116 bats species have been identified worldwide,4 and 139 bat species have been identified in Mexico,5 of which 31 have been found to be infected with rabies virus. Thirty-seven bat species have been identified in the Mexican state of Nuevo Leon, including the insectivorous Mexican free-tailed bat (Tadarida brasiliensis mexicana), which reportedly caused the first documented human death from rabies in Mexico.6,7
Genetic variants of rabies viruses can be identified antigenically with a panel of 8 monoclonal antibodies standardized by the CDC in Atlanta.8 This panel identifies 11 reaction patterns that correspond to the major RVVs circulating in Latin American and Caribbean countries.9,10 The rabies virus is a single-stranded RNA virus with an approximately 12-kilo-base genome encoding 5 viral proteins (nucleoprotein, phosphoprotein, matrix protein, glycoprotein, and an RNA-dependent polymerase),11 and it is possible to detect rabies virus through genomic sequencing of the nucleoprotein gene.7 The nucleoprotein gene is the most widely used target for rabies diagnosis,12 and sequencing it provides important data for epidemiological and evolutionary studies of all species of Lyssavirus.13
Domestic rabies, specifically rabies caused by the dog-coyote RVV, became enzootic in 1980 in coyotes (Canis latrans) along the border between Mexico and the United States. Sometime after that, the virus was translocated to various states, including Alabama and Florida, causing a local outbreak in domestic dogs in 1994.14 However, as a result of intense oral vaccination programs in the United States, the dog-coyote RVV has been considered, on the basis of results of phylogenetic analyses, to have been eliminated from the United States since 2004.15,16 Nevertheless, new cases of rabies caused by the dog-coyote RVV were reported in areas of the Mexican states of Coahuila and Tamaulipas near the US border between 2000 and 2002. In Nuevo Leon State, rabies was detected in coyotes and dogs before 1998; however, the antigenic variants and genomic sequences of these viruses were not determined.
Three bat species—T brasiliensis mexicana, Lasiurus cinereus, and Lasiurus ega—are particularly abundant in parts of Nuevo Leon State near the US border. These areas are also home to a variety of other mammals, such as gray foxes and various species of skunks and coyotes, that are potential rabies virus reservoirs and could possibly migrate to the United States.6 Recently, increased surveillance has led to the discovery of new cases of rabies involving bats and terrestrial carnivores in Nuevo Leon State. The objectives of the study reported here were to identify the RVVs involved in these cases and establish the phylogenetic relationship of these variants with variants causing historical and recent cases of rabies in border areas between Nuevo Leon and Texas and rabies in insectivorous bats in Mexico and Latin America.
Mauricio Gómez-Sierra and Albert Sandoval-Borja were technicians in the rabies laboratory at Instituto de Diagnóstico y Referencia Epidemiológicos, Ciudad de México at the time of the study.
No third-party funding or support was received in connection with this study or the writing or publication of the manuscript. The authors declare that there were no financial or other types of conflict of interest.
The findings and conclusions in this report are those of the authors and do not necessarily represent the official opinion of the Ministry of Health in México.
The authors thank the following members of the community health staff of the Public Health State Laboratory of Nuevo León and the Instituto de Diagnóstico y Referencia Epidemiológicos in México City for technical support: Anabella Morales Rubalcaba, Alejandra Marines, Alma Lizaran Meneses, Alejandra García Muñiz, David Herrera Hernández, Israel Animas Vargas, David Martínez Solís, and Beatriz Escamilla Ríos. They also thank Sergio Lozano-Rodríguez, MD, for help in writing the manuscript.
Nidia Aréchiga-Ceballos: https://orcid.org/0000-0002-7450-3060.
Rabies virus variant
QIAamp Viral RNA Mini Kit, Qiagen, Venlo, Netherlands.
Titan One Tube RT-PCR System, Roche Diagnostics GmbH, Mannheim, Germany.
BigDye Terminator v3.1 Cycle Sequencing Kit, ThermoFisher Scientific, Waltham, Mass.
PRISM 3130xl Genetic Analyzer, Applied Biosystems, Foster City, Calif.
ChromasPro, version 1.5, Technelysium Pty Ltd, South Brisbane, Australia.
Clustal W. Multiple Sequence Alignment, Kyoto University Bioinformatics Center. Available at: www.genome.jp/tools-bin/clustalw. Accessed Oct 18, 2019.
BEAST, version 1.8, Bayesian Evolutionary Analysis Sampling Trees. Available at: beast.community. Accessed Oct 18, 2019.
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Reference rabies virus sequences used for comparison with RVVs isolated from 15 bats and terrestrial mammals in Nuevo Leon State in which rabies was diagnosed between 2008 and 2015 and from a cow (Bos taurus) in Coahuila State in which rabies was diagnosed in 2006.
|Mexico||United States||Canada||Brazil and El Salvador|
|GenBank Accession No.||Year||State||GenBank Accession No.||Year||State||GenBank Accession No.||Year||GenBank Accession No.||Year|
|FJ228488||2004||San Luis Potosi||GU644727||2002||Texas||AF344304||1997|
|FJ228484||2002||San Luis Potosi||GU644728||2003||Texas|