Howler monkeys are the reservoir of malarial parasites causing zoonotic infections in the Atlantic forest of Rio de Janeiro.
Filipe Vieira Santos de Abreu, Edmilson Dos Santos, Aline Rosa Lavigne Mello, Larissa Rodrigues Gomes, Denise Anete Madureira de Alvarenga, Marcelo Quintela Gomes, Waldemir Paix��o Vargas, Cesare Bianco-J��nior, Anielle de Pina-Costa, Danilo Simonini Teixeira, Alessandro Pecego Martins Romano, Pedro Paulo de Abreu Manso, Marcelo Pelajo-Machado, Patr��cia Brasil, Cl��udio Tadeu Daniel-Ribeiro, Cristiana Ferreira Alves de Brito, Maria de F��tima Ferreira-da-Cruz, Ricardo Louren��o-de-Oliveira
Author Information
Filipe Vieira Santos de Abreu: Laborat��rio de Mosquitos Transmissores de Hematozo��rios, Instituto Oswaldo Cruz, Fiocruz, Rio de Janeiro, RJ, Brazil. ORCID
Edmilson Dos Santos: Divis��o de Vigil��ncia Ambiental em Sa��de, Secretaria de Sa��de do Rio Grande do Sul, Porto Alegre, RS, Brazil.
Aline Rosa Lavigne Mello: Laborat��rio de Pesquisa em Mal��ria, Instituto Oswaldo Cruz, Fiocruz, Rio de Janeiro, RJ, Brazil.
Larissa Rodrigues Gomes: Laborat��rio de Pesquisa em Mal��ria, Instituto Oswaldo Cruz, Fiocruz, Rio de Janeiro, RJ, Brazil.
Denise Anete Madureira de Alvarenga: Laborat��rio de Mal��ria, Instituto Ren�� Rachou, Fiocruz, Belo Horizonte, MG, Brazil. ORCID
Marcelo Quintela Gomes: Laborat��rio de Mosquitos Transmissores de Hematozo��rios, Instituto Oswaldo Cruz, Fiocruz, Rio de Janeiro, RJ, Brazil.
Waldemir Paix��o Vargas: Grupo de Pesquisa e Epidemiologia Espacial, Departamento de Endemias Samuel Pessoa, Escola Nacional de Sa��de P��blica Sergio Arouca, Fiocruz, Rio de Janeiro, RJ, Brasil.
Cesare Bianco-J��nior: Laborat��rio de Pesquisa em Mal��ria, Instituto Oswaldo Cruz, Fiocruz, Rio de Janeiro, RJ, Brazil.
Anielle de Pina-Costa: Centro de Pesquisa, Diagn��stico e Treinamento em Mal��ria, Instituto Oswaldo Cruz, Fiocruz, Rio de Janeiro, RJ, Brazil.
Danilo Simonini Teixeira: N��cleo de Atendimento e Pesquisa de Animais Silvestres, Universidade Estadual de Santa Cruz, UESC, Ilh��us, BA, Brazil.
Alessandro Pecego Martins Romano: Secretaria de Vigil��ncia em Sa��de, Minist��rio da Sa��de, Bras��lia, DF, Brazil.
Pedro Paulo de Abreu Manso: Laborat��rio de Patologia, Instituto Oswaldo Cruz, Fiocruz, Rio de Janeiro, RJ, Brazil.
Marcelo Pelajo-Machado: Laborat��rio de Patologia, Instituto Oswaldo Cruz, Fiocruz, Rio de Janeiro, RJ, Brazil.
Patr��cia Brasil: Centro de Pesquisa, Diagn��stico e Treinamento em Mal��ria, Instituto Oswaldo Cruz, Fiocruz, Rio de Janeiro, RJ, Brazil.
Cl��udio Tadeu Daniel-Ribeiro: Laborat��rio de Pesquisa em Mal��ria, Instituto Oswaldo Cruz, Fiocruz, Rio de Janeiro, RJ, Brazil.
Cristiana Ferreira Alves de Brito: Laborat��rio de Mal��ria, Instituto Ren�� Rachou, Fiocruz, Belo Horizonte, MG, Brazil.
Maria de F��tima Ferreira-da-Cruz: Laborat��rio de Pesquisa em Mal��ria, Instituto Oswaldo Cruz, Fiocruz, Rio de Janeiro, RJ, Brazil.
Ricardo Louren��o-de-Oliveira: Laborat��rio de Mosquitos Transmissores de Hematozo��rios, Instituto Oswaldo Cruz, Fiocruz, Rio de Janeiro, RJ, Brazil.
BACKGROUND: Although malaria cases have substantially decreased in Southeast Brazil, a significant increase in the number of Plasmodium vivax-like autochthonous human cases has been reported in remote areas of the Atlantic Forest in the past few decades in Rio de Janeiro (RJ) state, including an outbreak during 2015-2016. The singular clinical and epidemiological aspects in several human cases, and collectively with molecular and genetic data, revealed that they were due to the non-human primate (NHP) parasite Plasmodium simium; however, the understanding of the autochthonous malarial epidemiology in Southeast Brazil can only be acquired by assessing the circulation of NHP Plasmodium in the foci and determining its hosts. METHODOLOGY: A large sampling effort was carried out in the Atlantic forest of RJ and its bordering states (Minas Gerais, S��o Paulo, Esp��rito Santo) for collecting and examining free-living NHPs. Blood and/or viscera were analyzed for Plasmodium infections via molecular and microscopic techniques. PRINCIPAL FINDINGS: In total, 146 NHPs of six species, from 30 counties in four states, were tested, of which majority were collected from RJ. Howler monkeys (Alouatta clamitans) were the only species found infected. In RJ, 26% of these monkeys tested positive, of which 17% were found to be infected with P. simium. Importantly, specific single nucleotide polymorphisms-the only available genetic markers that differentiate P. simium from P. vivax-were detected in all P. simium infected A. clamitans despite their geographical origin of malarial foci. Interestingly, 71% of P. simium infected NHPs were from the coastal slope of a mountain chain (Serra do Mar), where majority of the human cases were found. Plasmodium brasilianum/malariae was initially detected in 14% and 25% free-living howler monkeys in RJ and in the Esp��rito Santo (ES) state, respectively. Moreover, the malarial pigment was detected in the spleen fragments of 50% of a subsample comprising dead howler monkeys in both RJ and ES. All NHPs were negative for Plasmodium falciparum. CONCLUSIONS/SIGNIFICANCE: Our data indicate that howler monkeys act as the main reservoir for the Atlantic forest human malarial parasites in RJ and other sites in Southeast Brazil and reinforce its zoonotic characteristics.
