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

BACKGROUND: Recently 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 subg...

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Autores principales: Laporta, Gabriel Zorello, Burattini, Marcelo Nascimento, Levy, Debora, Fukuya, Linah Akemi, de Oliveira, Tatiane Marques Porangaba, Maselli, Luciana Morganti Ferreira, Conn, Jan Evelyn, Massad, Eduardo, Bydlowski, Sergio Paulo, Sallum, Maria Anice Mureb
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4417526/
https://www.ncbi.nlm.nih.gov/pubmed/25909655
http://dx.doi.org/10.1186/s12936-015-0680-9
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author Laporta, Gabriel Zorello
Burattini, Marcelo Nascimento
Levy, Debora
Fukuya, Linah Akemi
de Oliveira, Tatiane Marques Porangaba
Maselli, Luciana Morganti Ferreira
Conn, Jan Evelyn
Massad, Eduardo
Bydlowski, Sergio Paulo
Sallum, Maria Anice Mureb
author_facet Laporta, Gabriel Zorello
Burattini, Marcelo Nascimento
Levy, Debora
Fukuya, Linah Akemi
de Oliveira, Tatiane Marques Porangaba
Maselli, Luciana Morganti Ferreira
Conn, Jan Evelyn
Massad, Eduardo
Bydlowski, Sergio Paulo
Sallum, Maria Anice Mureb
author_sort Laporta, Gabriel Zorello
collection PubMed
description BACKGROUND: Recently 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. METHODS: In 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. RESULTS: The 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. CONCLUSIONS: These 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 MATERIAL: The online version of this article (doi:10.1186/s12936-015-0680-9) contains supplementary material, which is available to authorized users.
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spelling pubmed-44175262015-05-04 Plasmodium falciparum in the southeastern Atlantic forest: a challenge to the bromeliad-malaria paradigm? Laporta, Gabriel Zorello Burattini, Marcelo Nascimento Levy, Debora Fukuya, Linah Akemi de Oliveira, Tatiane Marques Porangaba Maselli, Luciana Morganti Ferreira Conn, Jan Evelyn Massad, Eduardo Bydlowski, Sergio Paulo Sallum, Maria Anice Mureb Malar J Research BACKGROUND: Recently 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. METHODS: In 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. RESULTS: The 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. CONCLUSIONS: These 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 MATERIAL: The online version of this article (doi:10.1186/s12936-015-0680-9) contains supplementary material, which is available to authorized users. BioMed Central 2015-04-25 /pmc/articles/PMC4417526/ /pubmed/25909655 http://dx.doi.org/10.1186/s12936-015-0680-9 Text en © Laporta et al.; licensee BioMed Central. 2015 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Laporta, Gabriel Zorello
Burattini, Marcelo Nascimento
Levy, Debora
Fukuya, Linah Akemi
de Oliveira, Tatiane Marques Porangaba
Maselli, Luciana Morganti Ferreira
Conn, Jan Evelyn
Massad, Eduardo
Bydlowski, Sergio Paulo
Sallum, Maria Anice Mureb
Plasmodium falciparum in the southeastern Atlantic forest: a challenge to the bromeliad-malaria paradigm?
title Plasmodium falciparum in the southeastern Atlantic forest: a challenge to the bromeliad-malaria paradigm?
title_full Plasmodium falciparum in the southeastern Atlantic forest: a challenge to the bromeliad-malaria paradigm?
title_fullStr Plasmodium falciparum in the southeastern Atlantic forest: a challenge to the bromeliad-malaria paradigm?
title_full_unstemmed Plasmodium falciparum in the southeastern Atlantic forest: a challenge to the bromeliad-malaria paradigm?
title_short Plasmodium falciparum in the southeastern Atlantic forest: a challenge to the bromeliad-malaria paradigm?
title_sort plasmodium falciparum in the southeastern atlantic forest: a challenge to the bromeliad-malaria paradigm?
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4417526/
https://www.ncbi.nlm.nih.gov/pubmed/25909655
http://dx.doi.org/10.1186/s12936-015-0680-9
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