Enzootic and Epizootic Rabies Associated with Vampire Bats, Peru

Rene Edgar Condori-Condori

, Daniel G. Streicker, Cesar Cabezas-Sanchez, and Andres Velasco-Villa

Author affiliations: University of Georgia, Athens, Georgia, USA (R.E. Condori-Condori, D.G. Streicker); Centers for Disease Control and Prevention, Atlanta, Georgia, USA (R.E. Condori-Condori, D.G. Streicker, A. Velasco-Villa); Instituto Nacional de Salud Centro Nacional de Salud Pública, Lima, Peru (R.E. Condori-Condori, C. Cabezas-Sanchez)

Abstract

During the past decade, incidence of human infection with rabies virus (RABV) spread by the common vampire bat (Desmodus rotundus) increased considerably in South America, especially in remote areas of the Amazon rainforest, where these bats commonly feed on humans. To better understand the epizootiology of rabies associated with vampire bats, we used complete sequences of the nucleoprotein gene to infer phylogenetic relationships among 157 RABV isolates collected from humans, domestic animals, and wildlife, including bats, in Peru during 2002–2007. This analysis revealed distinct geographic structuring that indicates that RABVs spread gradually and involve different vampire bat subpopulations with different transmission cycles. Three putative new RABV lineages were found in 3 non–vampire bat species that may represent new virus reservoirs. Detection of novel RABV variants and accurate identification of reservoir hosts are critically important for the prevention and control of potential virus transmission, especially to humans.

Rabies virus (RABV; family Rhabdoviridae, genus Lyssavirus) is a bullet-shaped, single-stranded, negative-sense RNA virus with a 12-kb genome that encodes 5 structural proteins: nucleoprotein (N), phosphoprotein, matrix protein, glycoprotein, and polymerase (1). Over the course of its evolutionary history, RABV has established independent transmission cycles in diverse species of mesocarnivores and bats. Rabies disease remains a serious public health concern in several countries of Asia, Africa, and the Americas, where it is estimated that > 50,000 fatal infections occur annually (2).
In Latin America, rabies diseases are classified into 2 major epidemiologic forms, urban rabies and sylvatic rabies. For the former, dogs are the main viral reservoir host; for the latter, several species of wild carnivores and bats maintain independent rabies enzootics. Because of the widespread control of urban rabies through vaccination of domestic dogs, the common vampire bat (Desmodus rotundus) has emerged as the principal RABV reservoir host along the species’ natural range from Mexico to South America (3,4). The transmission and maintenance of RABV in natural populations of D. rotundus bats remains poorly understood, particularly within ongoing epizootics and enzootics occurring in different regions of the Americas (5,6). Active programs for the control of vampire bat–associated rabies in Latin America rely primarily on reduction of vampire bat populations by culling (7,8). Nonetheless, cross-species transmission to humans and domestic animals persists, even in areas where culling occurs regularly.
In Peru and other countries within the Amazon rainforest region, RABV transmitted by vampire bats has acquired greater epidemiologic importance because of the more frequent detection of human rabies outbreaks. This increase may reflect enhanced laboratory-based surveillance; increased awareness among public health stakeholders; or ecologic changes that promote greater contact between bats and humans, such as depletion of vampire bats’ natural prey community through hunting or habitat fragmentation. During 2002–2007, a total of 293 (77%) of the rabies cases diagnosed by the Instituto Nacional de Salud in Peru were associated with vampire bat RABV variants; the remaining 87 (23%) were attributed to RABV variants associated with dogs. In communities where vampire bats commonly feed on humans, the frequency of outbreaks depends on the transmission dynamics within the local vampire bat populations (9,10). Unfortunately, recent outbreaks in native communities of the Amazon region have been poorly characterized because of cultural constraints and local beliefs that have precluded investigators from obtaining diagnostic specimens (11).
Molecular epidemiology has been extensively used to determine RABV reservoir hosts in a given region or country, define the geographic distribution of the disease associated with those hosts, infer the temporal and spatial spread of the disease, identify spillover infections to nonreservoir species, describe novel RABV variants, and detect putative host shifts (12). The spatiotemporal epidemiology and genetic diversity of vampire bat–associated rabies in Peru have not been explored; a laboratory-based investigation conducted in 1999 addressed the comprehensive characterization of RABV in only 2 humans (11). Given the increasing importance of vampire bat–associated rabies in the Peruvian Amazon, comprehensive surveys of virus diversity and elucidation of geographic boundaries are needed to clarify the frequency and duration of rabies outbreaks. The goals of our study were to 1) determine the genetic diversity and geographic distribution of RABV infection associated with vampire bats; 2) clarify disease dissemination trends among affected areas; 3) detect the origins of spillover infections to other mammals; and 4) identify novel RABV lineages.