New potential Plasmodium brasilianum hosts: tamarin and marmoset monkeys (family Callitrichidae)

Abstract

BackgroundNon-human primates (NHPs) as a source for Plasmodium infections in humans are a challenge for malaria elimination. In Brazil, two species of Plasmodium have been described infecting NHPs, Plasmodium brasilianum and Plasmodium simium. Both species are infective to man. Plasmodium brasilianum resembles morphologically, genetically and immunologically the human quartan Plasmodium malariae. Plasmodium brasilianum naturally infects species of non-human primates from all New World monkey families from a large geographic area. In the family Callitrichidae only the genus Saguinus has been described infected so far. The present study describes the natural infection of P. brasilianum in tamarins and marmosets of the genera Callithrix, Mico and Leontopithecus in the Atlantic forest.MethodsOne hundred and twenty-two NHPs of the family Callitrichidae housed in the Primate Centre of Rio de Janeiro (CPRJ) were sampled in June 2015, and January and July 2016. The CPRJ is located in the Atlantic forest in the Guapimirim municipality, in the Rio de Janeiro state, where human autochthonous cases of malaria have been reported. The samples were screened for the presence of Plasmodium using optical microscopy and nested PCR for detection of 18S small subunit rRNA gene. The amplicon was sequenced to confirm the molecular diagnosis.ResultsThe frequency of Plasmodium infections detected by nested PCR in New World monkeys of the family Callitrichidae was 6.6%. For the first time, Callitrichidae primates of genera Callithrix, Mico and Leontopithecus were found naturally infected with P. brasilianum. Infection was confirmed by sequencing a small fragment of 18S rRNA gene, although no parasites were detected in blood smears.ConclusionsThe reported P. brasilianum infection in NHP species maintained in captivity suggests that infection can be favoured by the presence of vectors and the proximity between known (and unknown) hosts of malaria. Thus, the list of potential malaria reservoirs needs to be further explored.Electronic supplementary materialThe online version of this article (doi:10.1186/s12936-017-1724-0) contains supplementary material, which is available to authorized users.

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

“…For the first time, infection rates by Plasmodium were described, spatial distribution of P. simium in NHP was matched with local human cases of P. simiun malaria previously recorded, howler monkeys were disclosed as the only confirmed reservoir of this zoonotic malaria in the state and the presence of the so-called specific SNP was demonstrated in all P. simium infected howlers, regardless geographical origin of malaria foci. Although P. brasilianum/malariae has already been found in captive NHPs from RJ [13], it is also the first time that this parasite species was recorded in free-living NHPs from Rio de Janeiro and the widespread distribution of this quartan-malaria parasite and its zoonotic potential in the state were illustrated.…”

“…Recently, DNA but not blood forms of P. simium was detected in captive Cebus and Sapajus from the Southeast, whose role as reservoir for the zoonotic malaria in the region is still unclear [28]. P. brasilianum DNA was detected in captive capuchin, titi, howler and owl monkeys, besides tamarins and marmosets [13,28], most of which was exotic species to the Brazilian Southeast. All these NHPs were confined in a breeding institution (Center of Primatology of Rio de Janeiro - CPRJ) located in a cleared area of the enzootic simian malaria forest in RJ.…”

Forêts tropicales, changements d’usage des sols et risques infectieux émergents

“…Dans la forêt atlantique brésilienne, P. simium avait été décrit chez les singes de la famille des Atelidés [24], puis chez les singes de deux autres familles, celles des Cébidés et des Callithricidés [34,35]. La proximité génétique démontrée de P. simium avec P. vivax [36] a remis en avant la possibilité d'infection de l'humain par le parasite simien, voire à suggérer que le complexe P. vivax/simium, comme le complexe P. malaria/brasilianum, devaient être bien considérés comme des zoonoses [37].…”

Plasmodium vivax and Plasmodium falciparum infection in Neotropical primates in the western Amazon, Brazil

“…The aetiological agents of human malaria also infect NHP and these mammals can act as reservoirs in different Brazilian biomes, which may have implications for public health (Araújo et al, ; Duarte et al, ; Costa et al, ; Figueiredo, Di Santini, Figueiredo, & Machado, ; Yamasaki et al,). Aetiological agents of simian malaria, such as P. brasilianum and P. simium , have also been diagnosed in Neotropical primates in Brazil (Alvarenga et al, , ; Arruda, ; Deane, ). Although NHPs are considered reservoirs of Plasmodium spp., these primates may present clinical symptoms similar to those seen in human malaria, such as fever, lethargy, apathy, dyspnoea, and cerebral compromise (Costa et al, ; Ibiwoye, Howard, Sibbons, Hasan, & Van Velzen, ; Ozwara et al, ).…”