Age-Dependent Acquisition of Protective Immunity to Malaria in Riverine Populations of the Amazon Basin of Brazil

Simone Ladeia-Andrade Department of Tropical Medicine, Oswaldo Cruz Institute, Rio de Janeiro, Brazil; Department of Parasitology, Institute of Biomedical Sciences, University of São Paulo, São Paulo, Brazil; Laboratory of Seroepidemiology, Superintendency for the Control of Endemies, São Paulo, Brazil

Search for other papers by Simone Ladeia-Andrade in
Current site
Google Scholar
PubMed
Close
,
Marcelo Urbano Ferreira Department of Tropical Medicine, Oswaldo Cruz Institute, Rio de Janeiro, Brazil; Department of Parasitology, Institute of Biomedical Sciences, University of São Paulo, São Paulo, Brazil; Laboratory of Seroepidemiology, Superintendency for the Control of Endemies, São Paulo, Brazil

Search for other papers by Marcelo Urbano Ferreira in
Current site
Google Scholar
PubMed
Close
,
Maria Esther de Carvalho Department of Tropical Medicine, Oswaldo Cruz Institute, Rio de Janeiro, Brazil; Department of Parasitology, Institute of Biomedical Sciences, University of São Paulo, São Paulo, Brazil; Laboratory of Seroepidemiology, Superintendency for the Control of Endemies, São Paulo, Brazil

Search for other papers by Maria Esther de Carvalho in
Current site
Google Scholar
PubMed
Close
,
Izilda Curado Department of Tropical Medicine, Oswaldo Cruz Institute, Rio de Janeiro, Brazil; Department of Parasitology, Institute of Biomedical Sciences, University of São Paulo, São Paulo, Brazil; Laboratory of Seroepidemiology, Superintendency for the Control of Endemies, São Paulo, Brazil

Search for other papers by Izilda Curado in
Current site
Google Scholar
PubMed
Close
, and
José Rodrigues Coura Department of Tropical Medicine, Oswaldo Cruz Institute, Rio de Janeiro, Brazil; Department of Parasitology, Institute of Biomedical Sciences, University of São Paulo, São Paulo, Brazil; Laboratory of Seroepidemiology, Superintendency for the Control of Endemies, São Paulo, Brazil

Search for other papers by José Rodrigues Coura in
Current site
Google Scholar
PubMed
Close
Restricted access

Five community-based cross-sectional surveys of malaria morbidity and associated risk factors in remote riverine populations in northwestern Brazil showed average parasite rates of 4.2% (thick-smear microscopy) and 14.4% (polymerase chain reaction [PCR]) in the overall population, with a spleen rate of 13.9% among children 2–9 years of age. Plasmodium vivax was 2.8 times more prevalent than P. falciparum, with rare instances of P. malariae and mixed-species infections confirmed by PCR; 9.6% of asymptomatic subjects had parasitemias detected by PCR. Low-grade parasitemia detected by PCR only was a risk factor for anemia, after controlling for age and other covariates. Although clinical and subclinical infections occurred in all age groups, the risk of infection and disease decreased significantly with increasing age, after adjustment for several covariates in multilevel logistic regression models. These findings suggest that the continuous exposure to hypo- or mesoendemic malaria may induce significant anti-parasite and anti-disease immunity in native Amazonians.

Author Notes

  • 1

    Marques AC, 1987. Human migration and the spread of malaria in Brazil. Parasitol Today 3 :166–170.

  • 2

    Castro MC, Monte-Mór L, Sawyer DO, Singer BH, 2006. Malaria risk on the Amazon frontier. Proc Natl Acad Sci USA 103 :2452–2457.

  • 3

    Camargo LMA, dal Colletto GM, Ferreira M, Gurgel SM, Escobar AL, Marques A, Krieger H, Camargo EP, Silva LHP, 1996. Hypoendemic malaria in Rondonia (Brazil, Western Amazon Region): seasonal variation and risk groups in an urban locality. Am J Trop Med Hyg 55 :32–38.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    Camargo LMA, Ferreira MU, Krieger H, Camargo EP, Silva LHP, 1994. Unstable Hypoendemic malaria in Rondonia (Western Amazon Region, Brazil): epidemic outbreaks and work-associated incidence in an agro-industrial rural settlement. Am J Trop Med Hyg 51 :16–25.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Prata A, Urdaneta M, McGreevy PB, Tada MS, 1988. Infrequency of asymptomatic malaria in an endemic area in Amazonas, Brazil. Rev Soc Bras Med Trop 23 :51–54.

  • 6

    Macdonald G, 1957. The Epidemiology and Control of Malaria. London: Oxford University Press.

    • PubMed
    • Export Citation
  • 7

    Alves FP, Durlacher RR, Menezes MJ, Krieger H, Silva LHP, Camargo EP, 2002. High prevalence of asymptomatic Plasmodium vivax and Plasmodium falciparum infections in native Amazonian populations. Am J Trop Med Hyg 66 :641–648.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Branch OL, Casapia WP, Gamboa DV, Hernandez JN, Alava FF, Roncal N, Alvarez E, Perez EK, Gotuzzo E, 2005. Clustered local transmission and asymptomatic Plasmodium falciparum and Plasmodium vivax malarial infections in a recently emerged, hypoendemic Peruvian Amazon community. Malar J 4 :27.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Roshanravan B, Kari E, Gilman RH, Cabrera L, Lee E, Metcalfe J, Calderón M, Lescano AG, Montenegro SH, Calampa C, Vinetz JM, 2003. Endemic malaria in the Peruvian Amazon region of Iquitos. Am J Trop Med Hyg 69 :45–52.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Hackett LW, 1944. Spleen measurement in malaria. J Natl Malar Soc 3 :121–133.

  • 11

    Win TT, Lin K, Mizuno S, Zhou M, Liu Q, Ferreira MU, Tantular IS, Kojima S, Ishii A, Kawamoto F, 2002. Wide distribution of Plasmodium ovale in Myanmar. Trop Med Int Health 7 :231–239.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Plowe CV, Djimde A, Bouare M, Duombo O, Wellems TM, 1995. Pyrimethamine and proguanil resistance conferring mutations in Plasmodium falciparum dihydrofolate reductase: polymerase chain reaction methods for surveillance in Africa. Am J Trop Med Hyg 52 :565–568.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    World Health Organization, 2001. Iron Deficiency Anemia: Assessment, Prevention and Control. Geneva: World Health Organization.

    • PubMed
    • Export Citation
  • 14

    Carvalho ME, Ferreira MU, Souza MRD, Ninomia RT, Matos GF, Camargo LMA, Ferreira CS, 1992. Malaria seroepidemiology: comparison between indirect fluorescent antibody test and enzyme immunoassay using bloodspot eluates. Mem Inst Oswaldo Cruz 87 :205–208.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Sulzer AJ, Wilson M, 1967. The use of thick-smear antigen slides in the malaria indirect fluorescent antibody test. J Parasitol 53 :1110–1111.

  • 16

    Snow RW, Gilles HM, 2002. The epidemiology of malaria. Warrell DA, Gilles HM, eds. Bruce Chwatt’s Essential Malariology. Fourth edition. London: Edward Arnold, 85–106.

    • PubMed
    • Export Citation
  • 17

    Giha HA, Rosthoj S, Dodoo D, Hviid L, Satti GMH, Scheike T, Arnot DE, Theander TG, 2000. The epidemiology of febrile malaria episodes in an area of unstable and seasonal transmission. Trans R Soc Trop Med Hyg 94 :645–651.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    Ekvall H, 2003. Malaria and anemia. Curr Opin Hematol 10 :108–114.

  • 19

    Erhart A, Thang ND, Hung NQ, Toi LV, Hung LX, Tuy TQ, Cong LD, Speybroeck N, Coosemans M, D’Alessandro U, 2005. Forest malaria in Vietnam: a challenge for control. Am J Trop Med Hyg 70 :110–118.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Anderson TJC, Haubold B, Williams JT, Estrada-Franco JG, Richardson L, Mollinedo R, Bockarie M, Mokili J, Mharakurwa S, French N, Whitworth J, Velez ID, Brockman A, Nosten F, Ferreira MU, Day KP, 2000. Microsatellite markers reveal a spectrum of population structures in the malaria parasite Plasmodium falciparum. Mol Biol Evol 17 :1467–1482.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21

    Albrecht L, Merino EF, Hoffmann EHE, Ferreira MU, de Mattos Ferreira RG, Osakabe AL, Dalla Martha RC, Ramharter M, Durham AM, Ferreira JE, del Portillo HA, Wunderlich G, 2006. Extense variant gene family repertoire overlap in Western Amazon Plasmodium falciparum isolates. Mol Biochem Parasitol 150 :157–165.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

    Bull PC, Marsh K, 2002. The role of antibodies to Plasmodium falciparum-infected-erythrocyte surface antigens in naturally acquired immunity to malaria. Trends Microbiol 10 :55–58.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    Macauley C, 2005. Aggressive active case detection: a malaria control strategy based on the Brazilian model. Soc Sci Med 60 :563–573.

  • 24

    Cavasini MTV, Ribeiro WL, Kawamoto F, Ferreira MU, 2000. How prevalent is Plasmodium malariae in Rondônia, Western Brazilian Amazon? Rev Soc Bras Med Trop 33 :489–492.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    Scopel KKG, Fontes CJF, Nunes AC, Horta MF, Braga EM, 2004. High prevalence of Plamodium malariae infections in a Brazilian Amazon endemic area (Apiacás–Mato Grosso State) as detected by polymerase chain reaction. Acta Trop 90 :61–64.

    • PubMed
    • Search Google Scholar
    • Export Citation
Past two years Past Year Past 30 Days
Abstract Views 1290 1214 244
Full Text Views 366 16 4
PDF Downloads 136 15 0
 

 

 

 
 
Affiliate Membership Banner
 
 
Research for Health Information Banner
 
 
CLOCKSS
 
 
 
Society Publishers Coalition Banner
Save