Non‐human primates as a reservoir for rabies virus in Brazil

Abstract

Rabies virus (RABV) does not persist in the environment as it is a very fragile agent. The primary hosts are mammalian species in the orders Carnivora and Chiroptera. Since the late 1980s, RABV has been isolated from non‐human primates, Callithrix jacchus (the white‐tufted marmoset), in four coastal states (Rio Grande do Norte, Ceará, Piauí and Pernambuco) in north‐eastern Brazil, where this species is indigenous. The original habitat of C. jacchus consisted of two Brazilian biomes, the Atlantic Forest and the Caatinga. However, these marmosets have since adapted to other ecosystems as a result of human activities. Between 1988 and 1989, RABV isolates were obtained from white‐tufted marmosets in the state of Rio Grande do Norte, but antigenic and genetic identification studies were not conducted at that time. In the following years, three additional states reported cases (Ceará, Piauí and Pernambuco). In two of these states (Ceará and Piauí), human cases of rabies transmitted by marmosets were reported. According to Brazilian Health Ministry data, at least 19 human cases in which this species was the source of infection were registered in between 1990 and 2016. Recent findings in laboratory tests of 12 rabid samples from humans and marmosets and the regional transmission among these animals for over 20 years, together with the gradual increase in the affected geographic area, support the concept of the emergence of a new RABV reservoir. Regional tourism, the wild animal trade and the cultural practice of maintaining these animals as pets, particularly in coastal regions, appear to be major risk factors for the increase in human cases. Additional epidemiological and ecological studies are required to better understand local disease dynamics and to identify ideal opportunities for prevention and control of this fatal infection.

Rabies in Callithrix sp. in the urban area of Niterói, Rio de Janeiro, Brazil

“…Although rabies cases 5 in primates in Northeastern Brazil are uncommon, there is an endemic transmission cycle involving Callithrix jacchus, with transmission to humans. In this cycle, unlike the one in Niterói, a virus variant was identified with no genetic relationship or antigenic proximity with the variants already recorded in the Americas for terrestrial mammals and bats 6,7 . However, Kobayashi et al 8 identified a case of rabies in a tufted capuchin monkey (Cebus apella) in the state of Mato Grosso, in 2010, that was also related to the bats' variant, as in the case in Niterói.…”

Rabies surveillance in wild mammals in South of Brazil

“…Among these, 86% were canids ( Cerdocyon thous or Lycalopex vetulus ) and 11% were non‐human primates (NHP) mainly including marmosets and only one case in a capuchin monkey (Rocha et al, ). These results may be biased because of the wide geographical distribution and the proximity between marmosets and humans (Aguiar et al, ), sometimes kept as a pet, thus the majority of the NHP samples sent to analysis at Brazil are marmosets (Favoretto et al, ; Kotait et al, ). Cross‐species infections between wild animals have also been reported.…”

“…Importantly, detection of RVNA is not enough to identify what are the bioecological drivers and the variant of RABV that are acting (Rupprecht et al, ). This difficulty of inferring stresses the need to assess rabies circulation in wildlife using other approaches including direct fluorescent antibody test, genetic characterization and virus isolation from sick animals as performed on marmosets and foxes (Carnieli et al, ; Kotait et al, ).…”

“…However, the circulation of RABV in wildlife, and particularly in bats, has now become a major concern for public health (Fisher, Streicker, & Schnell, ; Freire de Carvalho et al, ; Lee et al ,; Rupprecht et al, ).In the last decade, most human deaths in Brazil are attributed to spillover from the vampire bat Desmodus rotundus (Secretaria de Vigilancia em Saude & Ministerio da Saude, ) . Foxes (i.e., crab‐eating fox Cerdocyon tho us) and primates (i.e., marmoset Callithrix jacchus ) have also been identified as reservoirs of RABV variants (Antunes et al, ; Favoretto et al, ; Kotait, De, Maria, & Carrieri, ; Páez, Saad, Núñez, & Bóshell, ) and can transmit rabies to humans (Freire de Carvalho et al, ; Velasco‐villa et al, ). In addition, serological studies have shown evidence of exposure to RABV in the absence of clinical signs in several primates and marsupials species (Antunes et al, ; Araujo et al, ).…”

“…Seropositive capuchin monkeys and crab‐eating foxes from the biome Atlantic Forest in the State of São Paulo (Almeida, Massad, Aguiar, Martorelli, & Joppert, ; Antunes et al, ; Araujo et al, ; Machado et al, ) and from the biomes Pantanal and Cerrado in the Midwest (Jorge et al, ) have also been described. Also in the Northeast region of Brazil, marmosets are considered reservoirs of a particular RABV variant (Antunes et al, ; Favoretto et al, ; Kotait et al, ). Nevertheless, very limited information is available on the circulation of rabies in wild animals from the biomes Pampa and Atlantic Forest, in Southern Brazil (Figure ).…”