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

Autor: Cristiana Ferreira Alves de Brito, Cláudio Tadeu Daniel-Ribeiro, Marcelo Pelajo-Machado, Anielle de Pina-Costa, Patrícia Brasil, Maria de Fátima Ferreira-da-Cruz, Filipe Vieira Santos de Abreu, Denise Anete Madureira de Alvarenga, Alessandro Pecego Martins Romano, Ricardo Lourenço-de-Oliveira, Waldemir Paixão Vargas, Aline Rosa Lavigne Mello, Edmilson Moutinho dos Santos, Larissa Rodrigues Gomes, Cesare Bianco-Junior, Pedro Paulo de Abreu Manso, Danilo Simonini Teixeira, Marcelo Quintela Gomes
Jazyk: angličtina
Rok vydání: 2019
Předmět:
0301 basic medicine
Plasmodium
Physiology
RC955-962
Forests
Monkeys
Geographical locations
0302 clinical medicine
Zoonoses
Arctic medicine. Tropical medicine
Medicine and Health Sciences
Parasite hosting
Primate
Alouatta
Protozoans
Mammals
biology
Zoonotic Infection
Monkey Diseases
Malarial Parasites
Eukaryota
Body Fluids
Blood
Infectious Diseases
Vertebrates
Anatomy
Public aspects of medicine
RA1-1270
Brazil
Research Article
Primates
Espirito santo
030231 tropical medicine
Zoology
03 medical and health sciences
biology.animal
Parasite Groups
parasitic diseases
Parasitic Diseases
medicine
Animals
Humans
Atlantic forest
Disease Reservoirs
Public Health
Environmental and Occupational Health
Organisms
Biology and Life Sciences
Outbreak
Plasmodium falciparum
South America
Tropical Diseases
medicine.disease
biology.organism_classification
Parasitic Protozoans
Malaria
030104 developmental biology
Genetic marker
Amniotes
Parasitology
People and places
Apicomplexa
Zdroj: PLoS Neglected Tropical Diseases, Vol 13, Iss 12, p e0007906 (2019)
PLoS Neglected Tropical Diseases
DOI: 10.1101/715623
Popis: 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.
Author summary The present work comprises an unprecedented capture effort and large-scale field survey of Plasmodium species in non-human primates (NHPs) in RJ, a state recording three-decade history of autochthonous human cases of benign tertian malaria lacking epidemiological clarification of their origin. This is the first study to describe the infection rates by Plasmodium spp. in free-living NHPs in RJ, thereby matching the spatial distribution of P. simium in NHP with that of the local human cases of benign tertian malaria occurring due to this parasite. This study confirmed howler monkeys as the only reservoir of this zoonotic malarial parasite in RJ and reported that specific single nucleotide polymorphisms were present in all P. simium infected howler monkeys, despite their geographical origin of malarial foci. Moreover, this is the first study to record P. brasilianum/malariae in free-living NHPs from RJ, and to illustrate their widespread distribution in this state. Collectively, these findings help us in evaluating the simian malaria prevalence in the Atlantic Forests and in assessing the zoonotic characteristics of autochthonous human malaria in Rio de Janeiro, thus providing assistance in shaping surveillance and control.
Databáze: OpenAIRE
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