Volume 99, Issue 4
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645



Community prevalence of infection is a widely used, standardized metric for evaluating malaria endemicity. Conventional methods for measuring prevalence include light microscopy and rapid diagnostic tests (RDTs), but their detection thresholds are inadequate for diagnosing low-density infections. The significance of submicroscopic malaria infections is poorly understood in Madagascar, a country of heterogeneous malaria epidemiology. A cross-sectional community survey in the western foothills of Madagascar during the March 2014 transmission season found malaria infection to be predominantly submicroscopic and asymptomatic. Prevalence of infection diagnosed by microscopy, RDT, and molecular diagnosis was 2.4%, 4.1%, and 13.8%, respectively. This diagnostic discordance was greatest for infection, which was 98.5% submicroscopic. Village location, insecticide-treated bednet ownership, and fever were significantly associated with infection outcomes, as was presence of another infected individual in the household. Duffy-negative individuals were diagnosed with , but with reduced odds relative to Duffy-positive hosts. The observation of high proportions of submicroscopic infections calls for a wider assessment of the parasite reservoir in other regions of the island, particularly given the country’s current focus on malaria elimination and the poorly documented distribution of the non– parasite species.


Article metrics loading...

The graphs shown below represent data from March 2017
Loading full text...

Full text loading...



  1. National Malaria Control Programme of Madagascar, 2017. National Strategic Plan for Malaria Control in Madagascar 2018–2022. Progressive Malaria Elimination from Madagascar. Madagascar: Ministry of Health of Madagascar.
  2. Howes RE, Mioramalala SA, Ramiranirina B, Franchard T, Rakotorahalahy AJ, Bisanzio D, Gething PW, Zimmerman PA, Ratsimbasoa A, , 2016. Contemporary epidemiological overview of malaria in Madagascar: operational utility of reported routine case data for malaria control planning. Malar J 15: 502. [Google Scholar]
  3. Kang SY, 2018. Spatio-temporal mapping of Madagascar’s malaria indicator survey results to assess Plasmodium falciparum endemicity trends between 2011 and 2016. BMC Med 16: 71. [Google Scholar]
  4. Institut National de la Statistique (INSTAT), Programme National de Lutte contre le Paludisme (PNLP), and ICF International, 2011. Madagascar Malaria Indicator Survey 2011 [Enquête sur les Indicateurs du Paludisme (EIPM)]. Calverton, MC: INSTAT, PNLP, and ICF International.
  5. Institut National de la Statistique (INSTAT), Programme National de Lutte contre le Paludisme (PNLP), Institut Pasteur de Madagascar (IPM), and ICF International, 2013. Madagascar Malaria Indicator Survey 2013 [Enquête sur les Indicateurs du Paludisme (EIPM)]. Calverton, MC: INSTAT, PNLP, IPM and ICF International.
  6. Institut National de la Statistique (INSTAT), Programme National de Lutte contre le Paludisme (PNLP), Institut Pasteur de Madagascar (IPM), and ICF International, 2016. Madagascar Malaria Indicator Survey 2016 [Enquête sur les Indicateurs du Paludisme (EIPM)]. Calverton, MD: INSTAT, PNLP, IPM and ICF International.
  7. malERA Refresh Consultative Panel on Characterising the Reservoir and Measuring Transmission, 2017. malERA: an updated research agenda for characterising the reservoir and measuring transmission in malaria elimination and eradication. PLoS Med 14: e1002452. [Google Scholar]
  8. Cohen JM, Le Menach A, Pothin E, Eisele TP, Gething PW, Eckhoff PA, Moonen B, Schapira A, Smith DL, , 2017. Mapping multiple components of malaria risk for improved targeting of elimination interventions. Malar J 16: 459. [Google Scholar]
  9. Menard D, 2010. Plasmodium vivax clinical malaria is commonly observed in Duffy-negative Malagasy people. Proc Natl Acad Sci USA 107: 59675971. [Google Scholar]
  10. Mehlotra RK, 2017. Long-term in vitro culture of Plasmodium vivax isolates from Madagascar maintained in Saimiri boliviensis blood. Malar J 16: 442. [Google Scholar]
  11. WHO, 2017. World Malaria Report 2017. Geneva, Switzerland: World Health Organization.
  12. Miller LH, Mason SJ, Clyde DF, McGinniss MH, , 1976. The resistance factor to Plasmodium vivax in blacks. The Duffy-blood-group genotype, FyFy. N Engl J Med 295: 302304. [Google Scholar]
  13. Howes RE, 2011. The global distribution of the Duffy blood group. Nat Commun 2: 266. [Google Scholar]
  14. Howes RE, 2015. Plasmodium vivax transmission in Africa. PLoS Negl Trop Dis 9: e0004222. [Google Scholar]
  15. Zimmerman PA, , 2017. Plasmodium vivax infection in Duffy-negative people in Africa. Am J Trop Med Hyg 97: 636638. [Google Scholar]
  16. Tofanelli S, Bertoncini S, Castri L, Luiselli D, Calafell F, Donati G, Paoli G, , 2009. On the origins and admixture of Malagasy: new evidence from high-resolution analyses of paternal and maternal lineages. Mol Biol Evol 26: 21092124. [Google Scholar]
  17. Ratovonjato J, 2014. Entomological and parasitological impacts of indoor residual spraying with DDT, alphacypermethrin and deltamethrin in the western foothill area of Madagascar. Malar J 13: 21. [Google Scholar]
  18. National Malaria Control Programme of Madagascar, 2015. National Strategic Plan for Malaria Control in Madagascar 2013–2017: Consolidating the Gains with a View to Elimination of Malaria from Madagascar, 2015–2017 Revision. Madagascar: Ministry of Health of Madagascar.
  19. McNamara DT, Kasehagen LJ, Grimberg BT, Cole-Tobian J, Collins WE, Zimmerman PA, , 2006. Diagnosing infection levels of four human malaria parasite species by a polymerase chain reaction/ligase detection reaction fluorescent microsphere-based assay. Am J Trop Med Hyg 74: 413421. [Google Scholar]
  20. Farr TG, 2007. The shuttle radar topography mission. Rev Geophys 45: RG2004. [Google Scholar]
  21. World Wildlife Fund (WWF) and U.S. Geological Survey, 2007. HydroSHEDS Database. Available at: http://hydrosheds.org/. Accessed January 29, 2018.
  22. WHO, 2011. Haemoglobin Concentrations for the Diagnosis of Anaemia and Assessment of Severity. Geneva, Switzerland: World Health Organization.
  23. Waltmann A, 2015. High rates of asymptomatic, sub-microscopic Plasmodium vivax infection and disappearing Plasmodium falciparum malaria in an area of low transmission in Solomon Islands. PLoS Negl Trop Dis 9: e0003758. [Google Scholar]
  24. Rosas-Aguirre A, Ponce OJ, Carrasco-Escobar G, Speybroeck N, Contreras-Mancilla J, Gamboa D, Pozo E, Herrera S, Llanos-Cuentas A, , 2015. Plasmodium vivax malaria at households: spatial clustering and risk factors in a low endemicity urban area of the northwestern Peruvian coast. Malar J 14: 176. [Google Scholar]
  25. Okell LC, Bousema T, Griffin JT, Ouedraogo AL, Ghani AC, Drakeley CJ, , 2012. Factors determining the occurrence of submicroscopic malaria infections and their relevance for control. Nat Commun 3: 1237. [Google Scholar]
  26. Cheng Q, Cunningham J, Gatton ML, , 2015. Systematic review of sub-microscopic P. vivax infections: prevalence and determining factors. PLoS Negl Trop Dis 9: e3413. [Google Scholar]
  27. Ihantamalala FA, Rakotoarimanana FMJ, Ramiadantsoa T, Rakotondramanga JM, Pennober G, Rakotomanana F, Cauchemez S, Metcalf CJE, Herbreteau V, Wesolowski A, , 2018. Spatial and temporal dynamics of malaria in Madagascar. Malar J 17: 58. [Google Scholar]
  28. Girond F, 2017. Analysing trends and forecasting malaria epidemics in Madagascar using a sentinel surveillance network: a web-based application. Malar J 16: 72. [Google Scholar]
  29. Kesteman T, 2016. Multiple causes of an unexpected malaria outbreak in a high-transmission area in Madagascar. Malar J 15: 57. [Google Scholar]
  30. Menard D, 2013. Whole genome sequencing of field isolates reveals a common duplication of the Duffy binding protein gene in Malagasy Plasmodium vivax strains. PLoS Negl Trop Dis 7: e2489. [Google Scholar]
  31. Gruenberg M, 2018. Plasmodium vivax molecular diagnostics in community surveys: pitfalls and solutions. Malar J 17: 55. [Google Scholar]
  32. Churcher TS, Trape JF, Cohuet A, , 2015. Human-to-mosquito transmission efficiency increases as malaria is controlled. Nat Commun 6: 6054. [Google Scholar]
  33. Churcher TS, Bousema T, Walker M, Drakeley C, Schneider P, Ouedraogo AL, Basanez MG, , 2013. Predicting mosquito infection from Plasmodium falciparum gametocyte density and estimating the reservoir of infection. eLife 2: e00626. [Google Scholar]
  34. Bousema T, Okell L, Felger I, Drakeley C, , 2014. Asymptomatic malaria infections: detectability, transmissibility and public health relevance. Nat Rev Microbiol 12: 833840. [Google Scholar]
  35. Okell LC, Griffin JT, Kleinschmidt I, Hollingsworth TD, Churcher TS, White MJ, Bousema T, Drakeley CJ, Ghani AC, , 2011. The potential contribution of mass treatment to the control of Plasmodium falciparum malaria. PLoS One 6: e20179. [Google Scholar]
  36. Bjorkman A, Cook J, Sturrock H, Msellem M, Ali A, Xu W, Molteni F, Gosling R, Drakeley C, Mårtensson A, , 2017. Spatial distribution of falciparum malaria infections in Zanzibar: implications for focal drug administration strategies targeting asymptomatic parasite carriers. Clin Infect Dis 64: 12361243. [Google Scholar]

Data & Media loading...

Supplemental figures and tables

  • Received : 16 May 2018
  • Accepted : 20 Jul 2018
  • Published online : 04 Sep 2018

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error