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doi: 10.1186/s12936-015-0606-6.

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

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

Denise Anete Madureira de Alvarenga et al. Malar J. .

Abstract

Background: In 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.

Methods: Blood 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.

Results: Thirty 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.

Conclusion: The 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.

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Figures

Figure 1
Figure 1
Maps of Brazil and of the State of Rio de Janeiro. Municipality of Guapimirim and its coordinates (red in Rio de Janeiro State map), in Serra dos Órgãos, where the Primate Centre of Rio de Janeiro (CPRJ) is located, in an area under influence of the Atlantic Forest, about l00 km from the city of Rio de Janeiro. Figure modified from Wikimedia Commons: http://commons.wikimedia.org/wiki/File:RiodeJaneiro_Municip_Guapimirim.svg.
Figure 2
Figure 2
Molecular diagnosis of Plasmodium infection by nested-PCR of 30 non-human primate samples. Molecular diagnosis of Plasmodium infection by nested-PCR in 30 non-human primates from CPRJ using specific primers for P. falciparum (Pf), P. vivax (Pv) and Plasmodium malariae (Pm). Plasmodium simium was identified in Sapajus xanthosternos (2324), Sapajus robustus (2209) and Cebus sp. (2503 and 2559); and P. brasilianum was detected in Sapajus xanthosternos (2005 and 2539), Callicebus personatus (2466), Aotus nigriceps (2203), Sapajus robustus (2209) and Alouatta g. clamitans (2443). Agarose gels, 1.5% stained with ethidium bromide. Numbers above gels indicated the non-human primates according to Additional file 1. Pf+, Pv + and Pm+: positive control (DNA species-specific) and Ctr -: negative control (without DNA), MM – 1 kb Plus Ladder.
Figure 3
Figure 3
Molecular diagnosis of Plasmodium infection by nested-PCR in organ fragments of dead monkey. DNA extracted from spleen and liver samples of dead wild Alouatta g. clamitans found near the campus of the CPRJ (sample MP1943) was amplified by using primers specific for P. vivax (Pv). Agarose gel, 1.5% stained with ethidium bromide. C+ − positive control for P. vivax and CN – negative control (without DNA), M – Ladder 100 bp.
Figure 4
Figure 4
Multiple sequence alignment of Plasmodium 18SSU rRNA fragment performed by the muscle algorithm. The 18SSU rRNA partial sequences (second amplicon from Nested-PCR) obtained herein are from parasites of: Sapajus xanthosternos (sample 2324), Cebus sp. (2559 and 2503), dead wild Alouatta g. clamitans (MP1943). These sequences were compared to sequences from Plasmodium species available in GenBank [accession number]: P. vivax [GenBank: AY579418.1], Plasmodium cynomolgi [Genbank:JQ794445.1], Plasmodium knowlesi [GenBank: AY579417], P. falciparum [GenBank: JQ627150.1], P. malariae [GenBank: GU815531.1], P. brasilianum [GenBank: KC906730.1] and Plasmodium ovale [GenBank: KF018663.1].
Figure 5
Figure 5
Topology of the phylogenetic tree of 18SSU rRNA. Topology of the phylogenetic tree of 18SSU rRNA with the four sequences of P. simium obtained from: Sapajus xanthosternos (2324), Cebus sp. (2503 and 2559) and death wild Alouatta g. clamitans (MP1943). The same sequences from the other species were used as in Figure 4. The tree was generated using the method of maximum likelihood and Tamura 3-parameter model with 5,000 replicates (bootstraps >60% showed in the branches).

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