Skip to main content
Top
Published in: Malaria Journal 1/2017

Open Access 01-12-2017 | Research

Reassessment of asymptomatic carriers of Plasmodium spp. in an endemic area with a very low incidence of malaria in extra-Amazonian Brazil

Authors: Filomena E. C. de Alencar, Rosely dos Santos Malafronte, Crispim Cerutti Jr., Lícia Natal Fernandes, Julyana Cerqueira Buery, Blima Fux, Helder Ricas Rezende, Angelica Espinosa Miranda

Published in: Malaria Journal | Issue 1/2017

Login to get access

Abstract

Background

Regions with residual transmission are potential obstacles to the elimination of malaria. It is, therefore, essential to understand the factors associated with the maintenance of endemic malaria in these areas. The objective was to investigate whether the status of asymptomatic carriers of Plasmodium spp. DNA is maintained in the long term in an extra-Amazonian region of Brazil with low incidence, residual malaria transmission.

Methods

Asymptomatic carriers of Plasmodium DNA detected in a survey carried out between 2001 and 2004 were reassessed between 2010 and 2011 using questionnaires, PCR and thick and thin blood smear tests three times at 3-month intervals.

Results

Of the 48 carriers detected between 2001 and 2004, 37 were located. Of these, only two had positive PCR results and, as in the first survey, Plasmodium malariae DNA was detected.

Conclusion

The findings suggest that untreated dwellers from this extra-Amazonian region, who initially harbour malaria parasites, may become negative without ever developing apparent symptoms of the disease. Although the possibility of re-infection cannot be ruled out, the finding of two individuals harbouring P. malariae, both in the first and in the second survey, may be compatible with a long-term carrier state for this parasite. Since most clinical cases of malaria in the region are a consequence of infection by Plasmodium vivax, the epidemiological impact of such long-term carriage would be limited.
Literature
1.
go back to reference WHO. World malaria report 2016. Geneva: World Health Organization; 2016. WHO. World malaria report 2016. Geneva: World Health Organization; 2016.
2.
go back to reference de Pina-Costa A, Brasil P, Di Santi SM, de Araujo MP, Suárez-Mutis MC, Santelli AC, et al. Malaria in Brazil: what happens outside the Amazonian endemic region. Mem Inst Oswaldo Cruz. 2014;109:618–33.CrossRefPubMedPubMedCentral de Pina-Costa A, Brasil P, Di Santi SM, de Araujo MP, Suárez-Mutis MC, Santelli AC, et al. Malaria in Brazil: what happens outside the Amazonian endemic region. Mem Inst Oswaldo Cruz. 2014;109:618–33.CrossRefPubMedPubMedCentral
4.
go back to reference Cerutti C Jr, Boulos M, Coutinho AF, Hatab MCLD, Falqueto A, Rezende HR, et al. Epidemiologic aspects of the malaria transmission cycle in an area of very low incidence in Brazil. Malar J. 2007;6:33.CrossRefPubMed Cerutti C Jr, Boulos M, Coutinho AF, Hatab MCLD, Falqueto A, Rezende HR, et al. Epidemiologic aspects of the malaria transmission cycle in an area of very low incidence in Brazil. Malar J. 2007;6:33.CrossRefPubMed
6.
go back to reference Duarte AMRC, Malafronte RS, Cerutti C, Curado I, de Paiva BR, Maeda AY, et al. Natural Plasmodium infections in Brazilian wild monkeys: reservoirs for human infections? Acta Trop. 2008;107:179–85.CrossRefPubMed Duarte AMRC, Malafronte RS, Cerutti C, Curado I, de Paiva BR, Maeda AY, et al. Natural Plasmodium infections in Brazilian wild monkeys: reservoirs for human infections? Acta Trop. 2008;107:179–85.CrossRefPubMed
7.
go back to reference Yamasaki T, Duarte AM, Curado I, Summa ME, Neves DV, Wunderlich G, et al. Detection of etiological agents of malaria in howler monkeys from Atlantic Forests, rescued in regions of São Paulo city, Brazil. J Med Primatol. 2011;40:392–400.CrossRefPubMed Yamasaki T, Duarte AM, Curado I, Summa ME, Neves DV, Wunderlich G, et al. Detection of etiological agents of malaria in howler monkeys from Atlantic Forests, rescued in regions of São Paulo city, Brazil. J Med Primatol. 2011;40:392–400.CrossRefPubMed
8.
go back to reference Li J, Collins WE, Wirtz RA, Rathore D, Lal A, McCutchan TF. Geographic subdivision of the range of the malaria parasite Plasmodium vivax. Emerg Infect Dis. 2001;7:35–42.CrossRefPubMedPubMedCentral Li J, Collins WE, Wirtz RA, Rathore D, Lal A, McCutchan TF. Geographic subdivision of the range of the malaria parasite Plasmodium vivax. Emerg Infect Dis. 2001;7:35–42.CrossRefPubMedPubMedCentral
9.
go back to reference Tazi L, Ayala FJ. Unresolved direction of host transfer of Plasmodium vivax v. P. simium and P. malariae v. P. brasilianum. Infect Genet Evol. 2011;11:209–21.CrossRefPubMed Tazi L, Ayala FJ. Unresolved direction of host transfer of Plasmodium vivax v. P. simium and P. malariae v. P. brasilianum. Infect Genet Evol. 2011;11:209–21.CrossRefPubMed
10.
go back to reference WHO. Basic malaria microscopy. Geneva: World Health Organization; 1991. WHO. Basic malaria microscopy. Geneva: World Health Organization; 1991.
11.
go back to reference Win TT, Lin K, Mizuno S, Zhou M, Liu Q, Ferreira MU, et al. Wide distribution of Plasmodium ovale in Myanmar. Trop Med Int Health. 2002;7:231–9.CrossRefPubMed Win TT, Lin K, Mizuno S, Zhou M, Liu Q, Ferreira MU, et al. Wide distribution of Plasmodium ovale in Myanmar. Trop Med Int Health. 2002;7:231–9.CrossRefPubMed
12.
go back to reference Alves FP, Durlacher RR, Menezes MJ, Krieger H, Silva LH, Camargo EP. High prevalence of asymptomatic Plasmodium vivax and Plasmodium falciparum infections in native Amazonian populations. Am J Trop Med Hyg. 2002;66:641–8.CrossRefPubMed Alves FP, Durlacher RR, Menezes MJ, Krieger H, Silva LH, Camargo EP. High prevalence of asymptomatic Plasmodium vivax and Plasmodium falciparum infections in native Amazonian populations. Am J Trop Med Hyg. 2002;66:641–8.CrossRefPubMed
13.
go back to reference Branch O, Casapia WM, Gamboa DV, Hernandez JN, Alava FF, Roncal N, et al. Clustered local transmission and asymptomatic Plasmodium falciparum and Plasmodium vivax malaria infections in a recently emerged, hypoendemic Peruvian Amazon community. Malar J. 2005;4:27.CrossRefPubMedPubMedCentral Branch O, Casapia WM, Gamboa DV, Hernandez JN, Alava FF, Roncal N, et al. Clustered local transmission and asymptomatic Plasmodium falciparum and Plasmodium vivax malaria infections in a recently emerged, hypoendemic Peruvian Amazon community. Malar J. 2005;4:27.CrossRefPubMedPubMedCentral
14.
go back to reference Harris I, Sharrock WW, Bain LM, Gray KA, Bobogare A, Boaz L, et al. A large proportion of asymptomatic Plasmodium infections with low and sub-microscopic parasite densities in the low transmission setting of Temotu Province, Solomon Islands: challenges for malaria diagnostics in an elimination setting. Malar J. 2010;9:254.CrossRefPubMedPubMedCentral Harris I, Sharrock WW, Bain LM, Gray KA, Bobogare A, Boaz L, et al. A large proportion of asymptomatic Plasmodium infections with low and sub-microscopic parasite densities in the low transmission setting of Temotu Province, Solomon Islands: challenges for malaria diagnostics in an elimination setting. Malar J. 2010;9:254.CrossRefPubMedPubMedCentral
15.
go back to reference Lin JT, Saunders DL, Meshnick SR. The role of submicroscopic parasitemia in malaria transmission: what is the evidence? Trends Parasitol. 2014;30:183–90.CrossRefPubMedPubMedCentral Lin JT, Saunders DL, Meshnick SR. The role of submicroscopic parasitemia in malaria transmission: what is the evidence? Trends Parasitol. 2014;30:183–90.CrossRefPubMedPubMedCentral
16.
go back to reference Maselli LM, Levy D, Laporta GZ, Monteiro AM, Fukuya LA, Ferreira-da-Cruz MF, et al. Detection of Plasmodium falciparum and Plasmodium vivax subclinical infection in non-endemic region: implications for blood transfusion and malaria epidemiology. Malar J. 2014;13:224.CrossRefPubMedPubMedCentral Maselli LM, Levy D, Laporta GZ, Monteiro AM, Fukuya LA, Ferreira-da-Cruz MF, et al. Detection of Plasmodium falciparum and Plasmodium vivax subclinical infection in non-endemic region: implications for blood transfusion and malaria epidemiology. Malar J. 2014;13:224.CrossRefPubMedPubMedCentral
17.
go back to reference Baum E, Sattabongkot J, Sirichaisinthop J, Kiattibutr K, Davies DH, Jain A, et al. Submicroscopic and asymptomatic Plasmodium falciparum and Plasmodium vivax infections are common in western Thailand—molecular and serological evidence. Malar J. 2015;14:95.CrossRefPubMedPubMedCentral Baum E, Sattabongkot J, Sirichaisinthop J, Kiattibutr K, Davies DH, Jain A, et al. Submicroscopic and asymptomatic Plasmodium falciparum and Plasmodium vivax infections are common in western Thailand—molecular and serological evidence. Malar J. 2015;14:95.CrossRefPubMedPubMedCentral
18.
go back to reference Schneider P, Bousema JT, Gouagna LC, Otieno S, van de Vegte-Bolmer M, Omar SA, et al. Submicroscopic Plasmodium falciparum gametocyte densities frequently result in mosquito infection. Am J Trop Med Hyg. 2007;76:470–4.PubMed Schneider P, Bousema JT, Gouagna LC, Otieno S, van de Vegte-Bolmer M, Omar SA, et al. Submicroscopic Plasmodium falciparum gametocyte densities frequently result in mosquito infection. Am J Trop Med Hyg. 2007;76:470–4.PubMed
19.
20.
go back to reference Stepniewska K, Price RN, Sutherland CJ, Drakeley CJ, von Seidlein L, Nosten F, et al. Plasmodium falciparum gametocyte dynamics in areas of different malaria endemicity. Malar J. 2008;7:249.CrossRefPubMedPubMedCentral Stepniewska K, Price RN, Sutherland CJ, Drakeley CJ, von Seidlein L, Nosten F, et al. Plasmodium falciparum gametocyte dynamics in areas of different malaria endemicity. Malar J. 2008;7:249.CrossRefPubMedPubMedCentral
21.
go back to reference Wampfler R, Mwingira F, Javati S, Robinson L, Betuela I, Siba P, et al. Strategies for detection of Plasmodium species gametocytes. PLoS ONE. 2013;8:e76316.CrossRefPubMedPubMedCentral Wampfler R, Mwingira F, Javati S, Robinson L, Betuela I, Siba P, et al. Strategies for detection of Plasmodium species gametocytes. PLoS ONE. 2013;8:e76316.CrossRefPubMedPubMedCentral
22.
go back to reference Ouédraogo AL, Bousema T, Schneider P, De Vlas SJ, Ilboudo-Sanogo E, Cuzin-Ouattara N, et al. Substantial contribution of submicroscopical Plasmodium falciparum gametocyte carriage to the infectious reservoir in an area of seasonal transmission. PLoS ONE. 2009;4:e8410.CrossRefPubMedPubMedCentral Ouédraogo AL, Bousema T, Schneider P, De Vlas SJ, Ilboudo-Sanogo E, Cuzin-Ouattara N, et al. Substantial contribution of submicroscopical Plasmodium falciparum gametocyte carriage to the infectious reservoir in an area of seasonal transmission. PLoS ONE. 2009;4:e8410.CrossRefPubMedPubMedCentral
23.
go back to reference Bousema T, Drakeley C. Epidemiology and infectivity of Plasmodium falciparum and Plasmodium vivax gametocytes in relation to malaria control and elimination. Clin Microbiol Rev. 2011;24:377–410.CrossRefPubMedPubMedCentral Bousema T, Drakeley C. Epidemiology and infectivity of Plasmodium falciparum and Plasmodium vivax gametocytes in relation to malaria control and elimination. Clin Microbiol Rev. 2011;24:377–410.CrossRefPubMedPubMedCentral
24.
go back to reference Pett H, Gonçalves BP, Dicko A, Nébié I, Tiono AB, Lanke K, et al. Comparison of molecular quantification of Plasmodium falciparum gametocytes by Pfs25 qRT-PCR and QT-NASBA in relation to mosquito infectivity. Malar J. 2016;15:539.CrossRefPubMedPubMedCentral Pett H, Gonçalves BP, Dicko A, Nébié I, Tiono AB, Lanke K, et al. Comparison of molecular quantification of Plasmodium falciparum gametocytes by Pfs25 qRT-PCR and QT-NASBA in relation to mosquito infectivity. Malar J. 2016;15:539.CrossRefPubMedPubMedCentral
25.
go back to reference Vallejo AF, Garcia J, Amado-Garavito AB, Arévalo-Herrera M, Herrera S. Plasmodium vivax gametocyte infectivity in sub-microscopic infections. Malar J. 2016;15:48.CrossRefPubMedPubMedCentral Vallejo AF, Garcia J, Amado-Garavito AB, Arévalo-Herrera M, Herrera S. Plasmodium vivax gametocyte infectivity in sub-microscopic infections. Malar J. 2016;15:48.CrossRefPubMedPubMedCentral
26.
go back to reference Alves FP, Gil LH, Marrelli MT, Ribolla PE, Camargo EP, Da Silva LH. Asymptomatic carriers of Plasmodium spp. as infection source for malaria vector mosquitoes in the Brazilian Amazon. J Med Entomol. 2005;42:777–9.CrossRefPubMed Alves FP, Gil LH, Marrelli MT, Ribolla PE, Camargo EP, Da Silva LH. Asymptomatic carriers of Plasmodium spp. as infection source for malaria vector mosquitoes in the Brazilian Amazon. J Med Entomol. 2005;42:777–9.CrossRefPubMed
27.
go back to reference Rubio JM, Benito A, Roche J, Berzosa PJ, García ML, Micó M, et al. Semi-nested, multiplex polymerase chain reaction for detection of human malaria parasites and evidence of Plasmodium vivax infection in Equatorial Guinea. Am J Trop Med Hyg. 1999;60:183–7.CrossRefPubMed Rubio JM, Benito A, Roche J, Berzosa PJ, García ML, Micó M, et al. Semi-nested, multiplex polymerase chain reaction for detection of human malaria parasites and evidence of Plasmodium vivax infection in Equatorial Guinea. Am J Trop Med Hyg. 1999;60:183–7.CrossRefPubMed
28.
go back to reference Mendrone A Jr, Cerutti C Jr, Levi JE, Boulos M, Sanchez MC, Malafronte R dos S, et al. Unexpected detection of Plasmodium vivax and Plasmodium falciparum DNA in asymptomatic blood donors: fact or artifact? Malar J. 2014;13:336.CrossRefPubMedPubMedCentral Mendrone A Jr, Cerutti C Jr, Levi JE, Boulos M, Sanchez MC, Malafronte R dos S, et al. Unexpected detection of Plasmodium vivax and Plasmodium falciparum DNA in asymptomatic blood donors: fact or artifact? Malar J. 2014;13:336.CrossRefPubMedPubMedCentral
29.
go back to reference Laporta GZ, Burattini MN, Levy D, Fukuya LA, Oliveira TMP, et al. Plasmodium falciparum in the southeastern Atlantic forest: a challenge to the bromeliad-malaria paradigm? Malar J. 2015;14:181.CrossRefPubMedPubMedCentral Laporta GZ, Burattini MN, Levy D, Fukuya LA, Oliveira TMP, et al. Plasmodium falciparum in the southeastern Atlantic forest: a challenge to the bromeliad-malaria paradigm? Malar J. 2015;14:181.CrossRefPubMedPubMedCentral
Metadata
Title
Reassessment of asymptomatic carriers of Plasmodium spp. in an endemic area with a very low incidence of malaria in extra-Amazonian Brazil
Authors
Filomena E. C. de Alencar
Rosely dos Santos Malafronte
Crispim Cerutti Jr.
Lícia Natal Fernandes
Julyana Cerqueira Buery
Blima Fux
Helder Ricas Rezende
Angelica Espinosa Miranda
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2017
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-017-2103-6

Other articles of this Issue 1/2017

Malaria Journal 1/2017 Go to the issue