Monkeys of the rainforest in French Guiana are natural reservoirs for P. brasilianum/P. malariae malaria

Abstract

Monkey blood samples were collected from 214 monkeys relocated as part of the wildlife rescue organized in French Guiana during the filling of the Petit Saut Dam on the Sinnamary River. These samples were tested for malaria parasites by microscopy of thick blood filsm and by nested PCR for small subunit rRNA genes (SSUrRNA). Parasitic blood forms similar to Plasmodium brasilianum were detected in 4 monkey species: Alouatta seniculus macconnelli, Saguinus midas midas, Pithecia pithecia and Ateles paniscus paniscus, with the highest prevalence in Alouatta monkeys. PCR was more sensitive than the conventional method for detecting low-grade parasitaemia in positive monkeys. The examination of blood films indicated that 5.6% of the animals carried parasites whereas the nested PCR for ribosomal DNA indicated a prevalence of 11.3%. The P. brasilianum SSUrRNA gene sequence was analysed and aligned with those from P. malariae, P. falciparum and P. vivax. This suggested that P. brasilianum and P. malariae are very closely related. Similar results were obtained from analysis of the sequences in P. malariae and P. brasilianum isolates of a polymorphic gene fragment analogous to the merozoite surface protein-1 (MSP-1) gene of P. falciparum. The P. brasilianum/P. malariae sequences were more similar to those of P. vivax than to those of P. falciparum, at least in the gene region examined. The high degree of DNA homology in the sequences of the SSUrRNA and msp1-like genes is consistent with other characterizations demonstrating a taxonomic relationship between P. brasilianum and P. malariae species. Our results provide further evidence that P. brasilianum and P. malariae are virtually identical and should probably be considered to be a single malaria species. This raises the question as to whether monkeys living in the rainforest are natural reservoirs for both simian and human malaria. These results have implications for the interpretation of the current epidemiological situation in French Guiana.

Natural Plasmodium infection in neotropical primates in the island of São Luís, state of Maranhão, Brazil

“…The results from the present study do not diverge from the results already described in the literature, in which P. malariae is the most widely identified species in primates in Brazil. This highlights that this species is both molecularly and morphologically identical to P. brasilianum, the species that infects neotropical primates (LAL et al, 1988;FANDEUR et al, 2000;CARTER & MENDIS, 2002;LECLERC et al, 2004). These results corroborate the results found in French Guiana, which identified P. brasilianum in 17 NHP (n = 154), through the nested PCR, (FANDEUR et al, 2000).…”

“…This highlights that this species is both molecularly and morphologically identical to P. brasilianum, the species that infects neotropical primates (LAL et al, 1988;FANDEUR et al, 2000;CARTER & MENDIS, 2002;LECLERC et al, 2004). These results corroborate the results found in French Guiana, which identified P. brasilianum in 17 NHP (n = 154), through the nested PCR, (FANDEUR et al, 2000). Moreover, in Brazil, in a study on neotropical primates in two different biomes, the Atlantic forest (n = 71, positivity = 12.6%) and the semi-deciduous Atlantic forest (n = 235, positivity = 6.7%), the greatest positivity was for P. malariae/P.…”

“…Moreover, in the state of São Paulo, P. brasilianum was diagnosed on one blood sample slide out of a total of 50 from free-living howler monkeys (Alouatta guariba clamitans) (YAMASAKI et al, 2011). In addition, in French Guiana, among 214 free-living NHP that were investigated, P. brasilianum was detected through optical microscopy in ten samples (4.7%), of which eight were from Alouatta seniculus and two from Saguinus midas (FANDEUR et al, 2000). Optical microscopy did not allow identification of species within the genus Plasmodium because only one stage of development was found (trophozoites).…”

“…It is considered to be the same species that parasitizes NHP, which is called in such cases P. brasilianum. Thus, the name P. malariae/brasilianum can be accepted (FANDEUR et al, 2000).…”

Anopheles darlingi bionomics and transmission of Plasmodium falciparum, Plasmodium vivax and Plasmodium malariae in Amerindian villages of the Upper-Maroni Amazonian forest, French Guiana

“…P. malariae usually exhibits low parasitaemia and is not easily detected by microscopists. Another hypothesis is supported by the possible existence of the simian parasite P. brasilianum in the Upper-Maroni area (Fandeur et al 2000). The monoclonal antibodies used in our ELISA to identify P. malariae also detect P. brasilianum sporozoites (Cochrane et al 1984).…”