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Howler monkeys are the reservoir of malarial parasites causing zoonotic infections in the Atlantic forest of Rio de Janeiro

Posted on 2019-12-09 - 18:31

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, São Paulo, Espírito 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 Espírito 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.

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AUTHORS (18)

Filipe Vieira Santos de Abreu
Edmilson dos Santos
Aline Rosa Lavigne Mello
Larissa Rodrigues Gomes
Denise Anete Madureira de Alvarenga
Marcelo Quintela Gomes
Waldemir Paixão Vargas
Cesare Bianco-Júnior
Anielle de Pina-Costa
Danilo Simonini Teixeira
Alessandro Pecego Martins Romano
Pedro Paulo de Abreu Manso
Marcelo Pelajo-Machado
Patrícia Brasil
Cláudio Tadeu Daniel-Ribeiro
Cristiana Ferreira Alves de Brito
Maria de Fátima Ferreira-da-Cruz
Ricardo Lourenço-de-Oliveira
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