Abstract
BackgroundRecently an unexpectedly high prevalence of Plasmodium falciparum was found in asymptomatic blood donors living in the southeastern Brazilian Atlantic forest. The bromeliad-malaria paradigm assumes that transmission of Plasmodium vivax and Plasmodium malariae involves species of the subgenus Kerteszia of Anopheles and only a few cases of P. vivax malaria are reported annually in this region. The expectations of this paradigm are a low prevalence of P. vivax and a null prevalence of P. falciparum. Therefore, the aim of this study was to verify if P. falciparum is actively circulating in the southeastern Brazilian Atlantic forest remains.MethodsIn this study, anophelines were collected with Shannon and CDC-light traps in seven distinct Atlantic forest landscapes over a 4-month period. Field-collected Anopheles mosquitoes were tested by real-time PCR assay in pools of ten, and then each mosquito from every positive pool, separately for P. falciparum and P. vivax. Genomic DNA of P. falciparum or P. vivax from positive anophelines was then amplified by traditional PCR for sequencing of the 18S ribosomal DNA to confirm Plasmodium species. Binomial probabilities were calculated to identify non-random results of the P. falciparum-infected anopheline findings.ResultsThe overall proportion of anophelines naturally infected with P. falciparum was 4.4% (21/480) and only 0.8% (4/480) with P. vivax. All of the infected mosquitoes were found in intermixed natural and human-modified environments and most were Anopheles cruzii (22/25 = 88%, 18 P. falciparum plus 4 P. vivax). Plasmodium falciparum was confirmed by sequencing in 76% (16/21) of positive mosquitoes, whereas P. vivax was confirmed in only 25% (1/4). Binomial probabilities suggest that P. falciparum actively circulates throughout the region and that there may be a threshold of the forested over human-modified environment ratio upon which the proportion of P. falciparum-infected anophelines increases significantly.ConclusionsThese results show that P. falciparum actively circulates, in higher proportion than P. vivax, among Anopheles mosquitoes of fragments of the southeastern Brazilian Atlantic forest. This finding challenges the classical bromeliad-malaria paradigm, which considers P. vivax circulation as the driver for the dynamics of residual malaria transmission in this region.Electronic supplementary materialThe online version of this article (doi:10.1186/s12936-015-0680-9) contains supplementary material, which is available to authorized users.
Highlights
An unexpectedly high prevalence of Plasmodium falciparum was found in asymptomatic blood donors living in the southeastern Brazilian Atlantic forest
Results of the present study showed that P. falciparum and P. vivax are present and infect anophelines in forestfragmented areas of the southeastern Atlantic forest where bromeliads are common and dense [36]
The bromeliad-malaria explanation was largely adopted by malariologists, and became a paradigm to explain the dynamics of residual malaria that still occur in areas of the Atlantic forest where Anopheles (Kerteszia) species are abundant and are primary vectors of P. vivax and P. malariae [2,3]
Summary
An unexpectedly high prevalence of Plasmodium falciparum was found in asymptomatic blood donors living in the southeastern Brazilian Atlantic forest. Transmission was successfully controlled and malaria incidence decreased to a hypo-endemic level by an aggressive vector control program that included complete deforestation of areas where the incidence of the disease was high and Kerteszia species were the primary vectors This massive effort to destroy bromeliads diminished the abundance of Kerteszia mosquitoes and eliminated the burden of malaria on humans [11]. The high frequency of reactions against the repetitive epitopes of the circumsporozoite protein (CSP) of Plasmodium falciparum and P. vivax suggests that the infection of nonhuman primates [16,17] by these Plasmodium species has been neglected Taken together, these results indicate that the bromeliad-malaria hypothesis, which does not encompass the potential circulation of P. falciparum in areas of Atlantic forest, needs to be re-evaluated
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