Plasmodium falciparum in the southeastern Atlantic forest: a challenge to the bromeliad-malaria paradigm?

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.

Spotlight on Plasmodium falciparum evolutionary system in the southeastern Atlantic forest

“…We found 4.4% (21/480) of P. falciparum-infected anophelines and 99% similarity of the P. falciparum 18S rDNA fragments shared with P. falciparum sequences previously isolated from wild monkeys in Amazonia (Laporta et al 2015). With the real-time quantitative curves from Laporta et al 2015, we estimated the average number of P. falciparum sporozoites per anopheline (Figure 1).…”

“…Anopheles darlingi is associated with forest fringe, resulting in the current paradigm of malaria transmission called 'the frontier malaria' in Amazon (Barros & Honório 2015). Plasmodium falciparum transmission in the southeastern Atlantic forest , Laporta et al 2015 could also be explained by means of biology of the main malarial vector in this system, An. cruzii.…”

“…The main characteristics are: very few annually reported Plasmodium vivax cases among residents and high abundance of the primary vector Anopheles cruzii, a forest-loving bromeliad-mosquito species (Gadelha 1994). This paradigmatic scenario has been challenged recently, resulting in a new puzzle to be solved , Laporta et al 2015. While these authors recognize that systematic studies and specific funding are needed, an effort towards solving that puzzle is made and thus a novel theoretical view is hypothesized in the present work.…”

“…Additionally, out of twenty-one (4.4%) P. falciparum-infected anophelines found in the southeastern Atlantic forest, eighteen (3.75%) were An. cruzii (Laporta et al 2015). Considering that An.…”

“…Following, a high proportion of P. falciparum was found throughout the southeastern Atlantic forest, mainly in An. cruzii mosquitoes, and infecting high fractions of asymptomatic human hosts and potentially circulating among reservoir monkeys , Laporta et al 2015.…”