Simian malaria in the Brazilian Atlantic forest: first description of natural infection of capuchin monkeys (Cebinae subfamily) by Plasmodium simium

Abstract

BackgroundIn Brazil, two species of Plasmodium have been described infecting non-human primates, Plasmodium brasilianum and Plasmodium simium. These species are morphologically, genetically and immunologically indistinguishable from the human Plasmodium malariae and Plasmodium vivax parasites, respectively. Plasmodium simium has been observed naturally infecting monkeys of the genera Alouatta and Brachyteles in a restricted area of the Atlantic Forest in the south and southeast regions of Brazil. However, its reported geographical distribution and the diversity of its vertebrate hosts may be underestimated, since available data were largely based on analyses by microscopic examination of peripheral blood, a method with limited sensitivity, considering the potential sub-patent feature of these infections. The present study describes, for the first time, the natural infection of P. simium in capuchin monkeys from the Brazilian Atlantic Forest.MethodsBlood samples from 30 non-human primates belonging to nine species kept in the Primate Centre of Rio de Janeiro were collected. Fragments of spleen and liver from one dead monkey found in the neighborhoods of the Primate Centre were also analysed. Molecular diagnosis was performed by nested PCR (18SSU rRNA) and the amplified fragment was sequenced.ResultsThirty per cent of the captive animals were infected with P. simium and/or P. brasilianum. The dead monkey tested positive for DNA of P. simium. For the first time, Cebinae primates (two specimens of genus Cebus and two of genus Sapajos) were found naturally infected by P. simium. The infection was confirmed by sequencing a small fragment of 18SSU rRNA.ConclusionThe results highlight the possibility of infection by P. simium in other species of non-human primates whose impact could be significant for the malaria epidemiology among non-human primates and, if it becomes clear that this P. simium is able to infect monkeys and, eventually, man, also for the maintenance of transmission of human malaria in the context of a zoonosis in areas under influence of the Atlantic Forest.Electronic supplementary materialThe online version of this article (doi:10.1186/s12936-015-0606-6) contains supplementary material, which is available to authorized users.

Plasmodium simiumcausing human malaria: a zoonosis with outbreak potential in the Rio de Janeiro Brazilian Atlantic forest

“…14 Samples from both organs were positive for P. vivax/P.simium DNA. 15 DNA was also extracted from blood of two A. clamitans, one of them captured in 2016 at Vale das Princesas, Miguel Pereira (a site where human cases have also been reported in the Rio de Janeiro state), which tested positive for both P. vivax/P. simium and P. brasilianum/malariae, and one other from Macaé (another locality with human cases), also positive for P. vivax/P.…”

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

“…A. g. clamitans was also the only free-living NHP from RJ in which blood forms by microscopy and plasmodial DNA were detected. 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.…”

“…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.…”

“…Giemsa-stained thick and thin blood films were examined in the microscopy under a x100 oil-immersion objective by two trained and independent microscopists. DNA was extracted from blood clots as previously described [27]; extractions from liver samples [28] were done using the QIAGEN DNeasy mini kit according to manufacturer’s instructions. Molecular diagnosis was made through conventional PCR.…”

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, ).…”