Mitochondrial genome of Plasmodium vivax/simium detected in an endemic region for malaria in the Atlantic Forest of Espírito Santo state, Brazil: do mosquitoes, simians and humans harbour the same parasite?

Abstract

BackgroundThe transmission of malaria in the extra-Amazonian regions of Brazil, although interrupted in the 1960s, has persisted to the present time in some areas of dense Atlantic Forest, with reports of cases characterized by particular transmission cycles and clinical presentations. Bromeliad-malaria, as it is named, is particularly frequent in the state of Espírito Santo, with Plasmodium vivax being the parasite commonly recognized as the aetiologic agent of human infections. With regard to the spatial and temporal distances between cases reported in this region, the transmission cycle does not fit the traditional malaria cycle. The existence of a zoonosis, with infected simians participating in the epidemiology, is therefore hypothesized. In the present study, transmission of bromeliad-malaria in Espírito Santo is investigated, based on the complete mitochondrial genome of DNA extracted from isolates of Plasmodium species, which had infected humans, a simian from the genus Allouata, and Anopheles mosquitoes. Plasmodium vivax/simium was identified in the samples by both nested PCR and real-time PCR. After amplification, the mitochondrial genome was completely sequenced and compared with a haplotype network which included all sequences of P. vivax/simium mitochondrial genomes sampled from humans and simians from all regions in Brazil.ResultsThe haplotype network indicates that humans and simians from the Atlantic Forest become infected by the same haplotype, but some isolates from humans are not identical to the simian isolate. In addition, the plasmodial DNA extracted from mosquitoes revealed sequences different from those obtained from simians, but similar to two isolates from humans.ConclusionsThese findings strengthen support for the hypothesis that in the Atlantic Forest, and especially in the state with the highest frequency of bromeliad-malaria in Brazil, parasites with similar molecular backgrounds are shared by humans and simians. The recognized identity between P. vivax and P. simium at the species level, the sharing of haplotypes, and the participation of the same vector in transmitting the infection to both host species indicate interspecies transference of the parasites. However, the intensity, frequency and direction of this transfer remain to be clarified.Electronic supplementary materialThe online version of this article (10.1186/s12936-017-2080-9) contains supplementary material, which is available to authorized users.

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

“…Despite efforts, we failed in capturing howlers in four malaria foci due to some local hindrances such as the steep terrain, hunt pressure and low A. g. clamitans population densities [23]. Nevertheless, the strong geographical overlap of howler monkey and human infections by parasites displaying specific P. simium SNPs in 83.3% (five out of six) of malaria foci, strengthens the importance of howlers as main reservoir of benign tertian human malaria over the zoonotic transmission areas in Southeast Brazil [4,5,20,21]. Howlers have also been by far the NHP most commonly found parasitized with both P. simium and P. brasilianum in Southern and Southeastern Brazil [5].…”

“…2). Curiously, despite this coincident distribution and similar frequency of P. brasilianum / malariae and P. simium in RJ, autochthonous human cases in this and in other Atlantic forest states of Southeast Brazil (SP and ES) have been diagnosed microscopically and/or molecularly as benign tertian malaria due to P. simium for decades [1,4,5,7,21,40,41]. In reality, P. simium was only identified by molecular tests and DNAmt sequencing as the causative agent in the 2015-2016 malaria outbreak in RJ, whose patients were essentially non-residents of foci [2].…”

“…Previous sampling efforts of examining free-living NHPs in the Southeastern Atlantic Forest over the last 30 years showed limited geographical coverage, with samplings essentially limited to wildlife rescues or carried out in areas close to cities, or were based on few individuals [4,20,21]. As a result, our data contribute to understanding the simian malaria parasite distribution and frequency as well as the zoonotic character of autochthonous human malaria in Rio de Janeiro, which in turn provides subsidies for shaping surveillance and control.…”

“…More recently, molecular studies of parasites infecting humans and four howlers clearly demonstrated that they shared the same P. simium parasite. [2,7,20,21]. However, so far scarce number of wild NHPs of few species from only three out of numerous autochthonous malaria foci in RJ and surroundings could be examined [2].…”

Capture of Alouatta guariba clamitans for the surveillance of sylvatic yellow fever and zoonotic malaria: Which is the best strategy in the tropical Atlantic Forest?

“…In Brazil, since 1966, human autochthonous malaria in areas under the influence of the Atlantic forest has been suspected to have simian origin caused by Plasmodium simium , the original and primary host being howler monkeys, genus Alouatta (Deane, ). The confirmation of this zoonotic cycle has only been achieved very recently by molecular examination of local Alouatta (Brasil et al, ; Buery et al, ).…”