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

Author(s)

Laporta, Gabriel Zorello ^{[1, 2]} ; Burattini, Marcelo Nascimento ^{[2, 3]} ; Levy, Debora ^[4] ; Fukuya, Linah Akemi ^[5] ; Porangaba de Oliveira, Tatiane Marques ^[1] ; Ferreira Maselli, Luciana Morganti ^{[4, 5]} ; Conn, Jan Evelyn ^{[6, 7]} ; Massad, Eduardo ^[2] ; Bydlowski, Sergio Paulo ^[4] ; Mureb Sallum, Maria Anice ^[1]

Affiliation

^[1] Univ Sao Paulo, Fac Saude Publ, Dept Epidemiol, BR-01246904 Sao Paulo, SP - Brazil

^[2] Univ Sao Paulo, Fac Med, Lab Informat Med LIM 01, BR-05405000 Sao Paulo, SP - Brazil

^[3] Univ Fed Sao Paulo, Escola Paulista Med, Hosp Sao Paulo, Div Doencas Infecc, BR-04024002 Sao Paulo - Brazil

^[4] Univ Sao Paulo, Fac Med, Lab Genet & Hematol Mol LIM 31, BR-05403000 Sao Paulo, SP - Brazil

^[5] Univ Sao Paulo, Fac Med, Fundacao Prosangue Hemoctr Sao Paulo, Divisao Pesquisa, BR-05403000 Sao Paulo, SP - Brazil

^[6] Wadsworth Ctr, Dept Hlth, Slingerlands, NY 12159 - USA

^[7] SUNY Albany, Sch Publ Hlth, Dept Biomed Sci, Albany, NY 12222 - USA

• Document type: Journal article
• Source: Malaria Journal; v. 14, APR 25 2015.
• Web of Science Citations: 12

Abstract

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 Plasmodium vivax malaria are reported annually in this region. The expectations of this paradigm are a low prevalence of Plasmodium vivax and a null prevalence of Plasmodium falciparum. Therefore, the aim of this study was to verify if Plasmodium 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 Plasmodium falciparum and Plasmodium vivax. Genomic DNA of Plasmodium falciparum or Plasmodium 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 Plasmodium falciparum-infected anopheline findings. Results: The overall proportion of anophelines naturally infected with Plasmodium falciparum was 4.4% (21/480) and only 0.8% (4/480) with Plasmodium vivax. All of the infected mosquitoes were found in intermixed natural and human-modified environments and most were Anopheles cruzii (22/25 = 88%, 18 Plasmodium falciparum plus 4 Plasmodium vivax). Plasmodium falciparum was confirmed by sequencing in 76% (16/21) of positive mosquitoes, whereas Plasmodium vivax was confirmed in only 25% (1/4). Binomial probabilities suggest that Plasmodium 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 Plasmodium falciparum-infected anophelines increases significantly. Conclusions: These results show that Plasmodium falciparum actively circulates, in higher proportion than Plasmodium vivax, among Anopheles mosquitoes of fragments of the southeastern Brazilian Atlantic forest. This finding challenges the classical bromeliad-malaria paradigm, which considers Plasmodium vivax circulation as the driver for the dynamics of residual malaria transmission in this region. (AU)

• FAPESP's process: 12/09939-5 - Understanding the effects of landscape and biodiversity on dynamics of malaria transmission
• Grantee: Gabriel Zorello Laporta
• Support type: Scholarships in Brazil - Post-Doctorate
• FAPESP's process: 09/53141-5 - Importance of subclinical malaria detection in blood donors from non-endemic areas
• Grantee: Sergio Paulo Bydlowski
• Support type: Research Grants - Research in Public Policies for the National Health Care System (PP-SUS)
• FAPESP's process: 11/20397-7 - Morphological and molecular taxonomy and phylogeny of Nyssorhynchus subgenus of Anopheles (Diptera: Culicidae), with special emphasis on Anopheles darlingi from Mata Atlântica
• Grantee: Maria Anice Mureb Sallum
• Support type: Regular Research Grants
• FAPESP's process: 14/09774-1 - Dynamics of malaria transmission under distinct landscape fragmentation thresholds
• Grantee: Gabriel Zorello Laporta
• Support type: BIOTA-FAPESP Program - Young Investigators Grants