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NATURAL EXPOSURE TO CHIKUNGUNYA VIRUS IN GOLDEN-HEADED LION TAMARIN (LEONTOPITHECUS CHRYSOMELAS, KUHL, 1820) FROM NON-PROTECTED AREAS IN SOUTHERN BAHIA, BRAZIL: IMPLICATIONS AND SIGNIFICANCE
Mosquitoes
Brazil
Antibodies
Chikungunya infection
Arboviruses
Tamarins
Article-level metrics
Author summary: Chikungunya virus (CHIKV) is an arbovirus, where in Africa non-human-primates (NHPs) are hosts of the sylvatic transmission cycle. Since 2014 in Brazil CHIKV is maintained in urban cycles, involving humans and Aedes aegypti mosquitoes. We have limited knowledge regarding CHIKV occurrence and implications in rural and sylvatic cycles where neotropical NHPs are present. In 2021 and 2022, we studied Culicidae mosquitoes and Leontopithecus chrysomelas (golden-headed lion tamarin -GHLT-), an endangered species endemic to the Atlantic Forest in Southern Bahia State, Brazil, at Ilhéus and Una municipalities. There was no evidence of genetic material of the virus in the GHLT and mosquitos, but we did find neutralizing antibodies as evidence of natural CHIKV exposure among free GHLT, that were present for at least five months. This could mean that GHLTs i) are susceptible to CHIKV infection, ii) may have a potential role as reservoir, and iii) are also important to include it in the epidemiological surveillance of arboviruses. Although we did not find a difference in the antibody titles in the tamarins between inhabiting the different land covers and soil uses, this endangered species could be infected in anthropogenic altered regions such as rural areas, as a consequence of anthropogenic pressure.
Author
Bernal Valle, Sofía
Mares-Guia, Maria Angélica Monteiro de Mello
Abreu, Filipe Vieira Santos de
Campos, Fabrício Souza
Oliveira, Cirilo Henrique de
Ramos, Antônio Victor Veloso
Lordelo, Reizane Pereira
De Vleeschouwer, Kristel
Oliveira, Leonardo de Carvalho
Fehlberg, Hllytchaikra Ferraz
Filippis, Ana Maria Bispo de
Ribeiro, Bergmann Morais
Roehe, Paulo Michel
Sevá, Anaiá da Paixão
Teixeira, Danilo Simonini
Albuquerque, George Rêgo
Mares-Guia, Maria Angélica Monteiro de Mello
Abreu, Filipe Vieira Santos de
Campos, Fabrício Souza
Oliveira, Cirilo Henrique de
Ramos, Antônio Victor Veloso
Lordelo, Reizane Pereira
De Vleeschouwer, Kristel
Oliveira, Leonardo de Carvalho
Fehlberg, Hllytchaikra Ferraz
Filippis, Ana Maria Bispo de
Ribeiro, Bergmann Morais
Roehe, Paulo Michel
Sevá, Anaiá da Paixão
Teixeira, Danilo Simonini
Albuquerque, George Rêgo
Affilliation
Universidade Estadual de Santa Cruz. Departamento de Ciências Agrárias e Ambientais. Ilhéus, BA, Brasil / Universidade Estadual de Santa Cruz. Departamento de Ciências Agrárias e Ambientais. Hospital Veterinário. Núcleo de Atendimento e Pesquisa de Animais Silvestres. Ilhéus, BA, Brasil / Universidade Estadual de Santa Cruz. Ilhéus, BA, Brasil.
Fundação Oswaldo Cruz. Instituto Oswaldo Cruz. Laboratório de Arbovírus e Vírus Hemorrágicos. Rio de Janeiro, RJ, Brasil.
Instituto Federal do Norte de Minas Gerais. Laboratório de Comportamento de Insetos. Salinas, MG, Brasil.
Universidade Federal do Rio Grande do Sul. Instituto de Ciências Básicas da Saúde. Porto Alegre, RS, Brasil.
Instituto Federal do Norte de Minas Gerais. Laboratório de Comportamento de Insetos. Salinas, MG, Brasil.
Universidade Estadual de Santa Cruz. Departamento de Ciências Agrárias e Ambientais. Ilhéus, BA, Brasil / Universidade Estadual de Santa Cruz. Departamento de Ciências Agrárias e Ambientais. Hospital Veterinário. Núcleo de Atendimento e Pesquisa de Animais Silvestres. Ilhéus, BA, Brasil.
Universidade Estadual de Santa Cruz. Departamento de Ciências Agrárias e Ambientais. Ilhéus, BA, Brasil.
Antwerp ZOO Centre for Research and Conservation. Projeto BioBrasil. Antwerp, Belgium.
Universidade Estadual de Santa Cruz. Ilhéus, BA, Brasil / Bicho do Mato Instituto de Pesquisa. Belo Horizonte, MG, Brasil.
Universidade Estadual de Santa Cruz. Departamento de Ciências Agrárias e Ambientais. Ilhéus, BA, Brasil.
Fundação Oswaldo Cruz. Instituto Oswaldo Cruz. Laboratório de Arbovírus e Vírus Hemorrágicos. Rio de Janeiro, RJ, Brasil.
Universidade de Brasília. Instituto de Ciências Biológicas. Departamento de Biologia Celular. Laboratório de Baculovírus. Brasília, DF, Brasil.
Universidade Federal do Rio Grande do Sul. Instituto de Ciências Básicas da Saúde. Porto Alegre, RS, Brasil.
Universidade Estadual de Santa Cruz. Departamento de Ciências Agrárias e Ambientais. Ilhéus, BA, Brasil.
Universidade Estadual de Santa Cruz. Departamento de Ciências Agrárias e Ambientais. Ilhéus, BA, Brasil / Universidade Estadual de Santa Cruz. Departamento de Ciências Agrárias e Ambientais. Hospital Veterinário. Núcleo de Atendimento e Pesquisa de Animais Silvestres. Ilhéus, BA, Brasil.
Universidade Estadual de Santa Cruz. Departamento de Ciências Agrárias e Ambientais. Ilhéus, BA, Brasil.
Fundação Oswaldo Cruz. Instituto Oswaldo Cruz. Laboratório de Arbovírus e Vírus Hemorrágicos. Rio de Janeiro, RJ, Brasil.
Instituto Federal do Norte de Minas Gerais. Laboratório de Comportamento de Insetos. Salinas, MG, Brasil.
Universidade Federal do Rio Grande do Sul. Instituto de Ciências Básicas da Saúde. Porto Alegre, RS, Brasil.
Instituto Federal do Norte de Minas Gerais. Laboratório de Comportamento de Insetos. Salinas, MG, Brasil.
Universidade Estadual de Santa Cruz. Departamento de Ciências Agrárias e Ambientais. Ilhéus, BA, Brasil / Universidade Estadual de Santa Cruz. Departamento de Ciências Agrárias e Ambientais. Hospital Veterinário. Núcleo de Atendimento e Pesquisa de Animais Silvestres. Ilhéus, BA, Brasil.
Universidade Estadual de Santa Cruz. Departamento de Ciências Agrárias e Ambientais. Ilhéus, BA, Brasil.
Antwerp ZOO Centre for Research and Conservation. Projeto BioBrasil. Antwerp, Belgium.
Universidade Estadual de Santa Cruz. Ilhéus, BA, Brasil / Bicho do Mato Instituto de Pesquisa. Belo Horizonte, MG, Brasil.
Universidade Estadual de Santa Cruz. Departamento de Ciências Agrárias e Ambientais. Ilhéus, BA, Brasil.
Fundação Oswaldo Cruz. Instituto Oswaldo Cruz. Laboratório de Arbovírus e Vírus Hemorrágicos. Rio de Janeiro, RJ, Brasil.
Universidade de Brasília. Instituto de Ciências Biológicas. Departamento de Biologia Celular. Laboratório de Baculovírus. Brasília, DF, Brasil.
Universidade Federal do Rio Grande do Sul. Instituto de Ciências Básicas da Saúde. Porto Alegre, RS, Brasil.
Universidade Estadual de Santa Cruz. Departamento de Ciências Agrárias e Ambientais. Ilhéus, BA, Brasil.
Universidade Estadual de Santa Cruz. Departamento de Ciências Agrárias e Ambientais. Ilhéus, BA, Brasil / Universidade Estadual de Santa Cruz. Departamento de Ciências Agrárias e Ambientais. Hospital Veterinário. Núcleo de Atendimento e Pesquisa de Animais Silvestres. Ilhéus, BA, Brasil.
Universidade Estadual de Santa Cruz. Departamento de Ciências Agrárias e Ambientais. Ilhéus, BA, Brasil.
Abstract
Chikungunya virus (CHIKV) is primarily associated with non-human-primates (NHPs) in Africa, which also infect humans. Since its introduction to Brazil in 2014, CHIKV has predominantly thrived in urban cycles, involving Aedes aegypti mosquitoes. Limited knowledge exists regarding CHIKV occurrence and implications in rural and sylvatic cycles where neotropical NHPs are potential hosts, from which we highlight Leontopithecus chrysomelas (Kuhl, 1820), the golden-headed lion tamarin (GHLT), an endangered species endemic to the Atlantic Forest (AF) in Southern Bahia State, Brazil. The present study investigated wild GHLT groups across two municipalities, Ilhéus and Una, Bahia. Surveys were conducted in three groups within cocoa agroforests (cabrucas) in Ilhéus, and four groups in anthropized forest and agroforestry fragments in Una, between 2021 and 2022. Thirty-two GHLT specimens were captured and chemically immobilized, examined and submitted to blood sample collection; nine specimens were later recaptured in 2022, totaling 41 samples. CHIKV viremia was not detected in any specimens (as assayed by RT-qPCR). Plaque reduction neutralization test (PRNT90) detected CHIKV antibodies in two (6.3%) GHLTs, with 10–20 antibody titers. Seroprevalence in 2021 was 5.6% and in 2022 was 8.7% with an incidence of 4.5%, whereas, a male adult tested seropositive in both years, suggesting either natural re-exposure and antibody maintenance over time. All samples tested seronegative for Mayaro Virus. Eight mosquito species from the Culicidae family were collected, identified and assayed for CHIKV genomes, showing negative results. This study provides the first evidence of natural CHIKV exposure among free-living GHLTs in Brazil, emphasizing their susceptibility and potential role as reservoirs. These findings underscore the possible consequences of anthropic disturbances in the Brazilian AF, without a seroprevalence difference between non-protected forest formations, agroforest fragments and various mosaic farming landscapes in South Bahia, and highlight the importance of conservation efforts for this endemic and endangered primate species.
Keywords
Chikungunya virusMosquitoes
Brazil
Antibodies
Chikungunya infection
Arboviruses
Tamarins
Article-level metrics
Publisher
Public Library of Science
Citation
BERNAL VALLE, Sofía et al. Natural exposure to chikungunya virus in golden-headed lion tamarin (Leontopithecus chrysomelas, Kuhl, 1820) from non-protected areas in southern Bahia, Brazil: implications and significance. PLoS Neglected Tropical Diseases, v. 19, n. 1, p. 1-21, 24 Jan. 2025.DOI
10.1371/journal.pntd.0012695ISSN
1935-2727Notes
Produção científica do Laboratório de Arbovírus e Vírus Hemorrágicos.Author summary: Chikungunya virus (CHIKV) is an arbovirus, where in Africa non-human-primates (NHPs) are hosts of the sylvatic transmission cycle. Since 2014 in Brazil CHIKV is maintained in urban cycles, involving humans and Aedes aegypti mosquitoes. We have limited knowledge regarding CHIKV occurrence and implications in rural and sylvatic cycles where neotropical NHPs are present. In 2021 and 2022, we studied Culicidae mosquitoes and Leontopithecus chrysomelas (golden-headed lion tamarin -GHLT-), an endangered species endemic to the Atlantic Forest in Southern Bahia State, Brazil, at Ilhéus and Una municipalities. There was no evidence of genetic material of the virus in the GHLT and mosquitos, but we did find neutralizing antibodies as evidence of natural CHIKV exposure among free GHLT, that were present for at least five months. This could mean that GHLTs i) are susceptible to CHIKV infection, ii) may have a potential role as reservoir, and iii) are also important to include it in the epidemiological surveillance of arboviruses. Although we did not find a difference in the antibody titles in the tamarins between inhabiting the different land covers and soil uses, this endangered species could be infected in anthropogenic altered regions such as rural areas, as a consequence of anthropogenic pressure.
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