Volume 97, Issue 6
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645



In areas of seasonal malaria transmission, the incidence rate of malaria infection is presumed to be near zero at the end of the dry season. Asymptomatic individuals may constitute a major parasite reservoir during this time. We conducted a longitudinal analysis of the spatio-temporal distribution of clinical malaria and asymptomatic parasitemia over time in a Malian town to highlight these malaria transmission dynamics. For a cohort of 300 rural children followed over 2009–2014, periodicity and phase shift between malaria and rainfall were determined by spectral analysis. Spatial risk clusters of clinical episodes or carriage were identified. A nested-case-control study was conducted to assess the parasite carriage factors. Malaria infection persisted over the entire year with seasonal peaks. High transmission periods began 2–3 months after the rains began. A cluster with a low risk of clinical malaria in the town center persisted in high and low transmission periods. Throughout 2009–2014, cluster locations did not vary from year to year. Asymptomatic and gametocyte carriage were persistent, even during low transmission periods. For high transmission periods, the ratio of asymptomatic to clinical cases was approximately 0.5, but was five times higher during low transmission periods. Clinical episodes at previous high transmission periods were a protective factor for asymptomatic carriage, but carrying parasites without symptoms at a previous high transmission period was a risk factor for asymptomatic carriage. Stable malaria transmission was associated with sustained asymptomatic carriage during dry seasons. Control strategies should target persistent low-level parasitemia clusters to interrupt transmission.

[open-access] This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.


Article metrics loading...

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

Full text loading...



  1. Greenwood BM, , 2008. Control to elimination: implications for malaria research. Trends Parasitol 24: 449454. [Google Scholar]
  2. Karema C, 2012. Trends in malaria cases, hospital admissions and deaths following scale-up of anti-malarial interventions, 2000–2010, Rwanda. Malar J 11: 236. [Google Scholar]
  3. Masaninga F, 2013. Review of the malaria epidemiology and trends in Zambia. Asian Pac J Trop Biomed 3: 8994. [Google Scholar]
  4. Trape JF, 2014. The rise and fall of malaria in a west African rural community, Dielmo, Senegal, from 1990 to 2012: 22 year longitudinal study. Lancet Infect Dis 14: 476488. [Google Scholar]
  5. Coulibaly D, 2013. Spatio-temporal analysis of malaria within a transmission season in Bandiagara, Mali. Malar J 12: 82. [Google Scholar]
  6. Babiker HA, Abdel-Muhsin AM, Ranford-Cartwright LC, Satti G, Walliker D, , 1998. Characteristics of Plasmodium falciparum parasites that survive the lengthy dry season in eastern Sudan where malaria transmission is markedly seasonal. Am J Trop Med Hyg 59: 582590. [Google Scholar]
  7. Sagna AB, 2013. Plasmodium falciparum infection during dry season: IgG responses to Anopheles gambiae salivary gSG6-P1 peptide as sensitive biomarker for malaria risk in northern Senegal. Malar J 12: 301. [Google Scholar]
  8. Lindblade KA, Steinhardt L, Samuels A, Kachur SP, Slutsker L, , 2013. The silent threat: asymptomatic parasitemia and malaria transmission. Expert Rev Anti Infect Ther 11: 623639. [Google Scholar]
  9. Carter R, Mendis KN, Roberts D, , 2000. Spatial targeting of interventions against malaria. Bull World Health Organ 78: 14011411. [Google Scholar]
  10. Bousema T, Griffin JT, Sauerwein RW, Smith DL, Churcher TS, Takken W, Ghani A, Drakeley C, Gosling R, , 2012. Hitting hotspots: spatial targeting of malaria for control and elimination. PLoS Med 9: e1001165. [Google Scholar]
  11. Bejon P, 2010. Stable and unstable malaria hotspots in longitudinal cohort studies in Kenya. PLoS Med 7: e1000304. [Google Scholar]
  12. Bousema T, 2010. Identification of hot spots of malaria transmission for targeted malaria control. J Infect Dis 201: 17641774. [Google Scholar]
  13. WHO, 2012. Disease Surveillance for Malaria Elimination: An Operational Manual. Geneva, Switzerland: World Health Organization. Available at: http://www.who.int/malaria/publications/atoz/9789241503334/en/. Accessed July 2015.
  14. Plowe CV, Djimde A, Wellems TE, Diop S, Kouriba B, Doumbo OK, , 1996. Community pyrimethamine-sulfadoxine use and prevalence of resistant Plasmodium falciparum genotypes in Mali: a model for deterring resistance. Am J Trop Med Hyg 55: 467471. [Google Scholar]
  15. Coulibaly D, 2002. Impact of preseason treatment on incidence of falciparum malaria and parasite density at a site for testing malaria vaccines in Bandiagara, Mali. Am J Trop Med Hyg 67: 604610. [Google Scholar]
  16. Lyke KE, Dicko A, Kone A, Coulibaly D, Guindo A, Cissoko Y, Traore K, Plowe CV, Doumbo OK, , 2004. Incidence of severe Plasmodium falciparum malaria as a primary endpoint for vaccine efficacy trials in Bandiagara, Mali. Vaccine 22: 31693174. [Google Scholar]
  17. Coulibaly D, 2014. Stable malaria incidence despite scaling up control strategies in a malaria vaccine-testing site in Mali. Malar J 13: 374. [Google Scholar]
  18. Cazelles B, Chavez M, Magny GC, Guégan JF, Hales S, , 2007. Time-dependent spectral analysis of epidemiological time-series with wavelets. J R Soc Interface 4: 625636. [Google Scholar]
  19. Cazelles B, Cazelles K, Chavez M, , 2013. Wavelet analysis in ecology and epidemiology: impact of statistical tests. J R Soc Interface 11: 20130585. [Google Scholar]
  20. Kulldorff M, , 1997. A spatial scan statistic. Commun Stat Theory Methods 26: 14811496. [Google Scholar]
  21. Essebag V, Genest J, Jr Suissa S, Pilote L, , 2003. The nested case-control study in cardiology. Am Heart J 146: 581590. [Google Scholar]
  22. Waniez P, , 2015. PhilcartoTm Version 6.72. CNRS and Université de Bordeaux, France. Available at: http://philcarto.free.fr. Accessed August 3, 2015.
  23. WHO, 2012. Global Malaria Programme. Seasonal Malaria Chemoprevention (SMC) for Plasmodium falciparum Malaria Control in Highly Seasonal Transmission Areas of the Sahel Sub-region in Africa. WHO Policy Recommendation. Geneva, Switzerland: World Health Organization.
  24. Gaudart J, 2006. Space-time clustering of childhood malaria at the household level: a dynamic cohort in a Mali village. BMC Public Health 6: 286–286. [Google Scholar]
  25. Nassir E, Abdel-Muhsin AM, Suliaman S, Kenyon F, Kheir A, Geha H, Ferguson HM, Walliker D, Babiker HA, , 2005. Impact of genetic complexity on longevity and gametocytogenesis of Plasmodium falciparum during the dry and transmission-free season of eastern Sudan. Int J Parasitol 35: 4955. [Google Scholar]
  26. Doolan DL, Dobano C, Baird JK, , 2009. Acquired immunity to malaria. Clin Microbiol Rev 22: 1336. [Google Scholar]
  27. Sondén K, Doumbo S, Hammar U, Vafa Homann M, Ongoiba A, Traoré B, Bottai M, Crompton PD, Färnert A, , 2015. Asymptomatic multiclonal Plasmodium falciparum infections carried through the dry season predict protection against subsequent clinical malaria. J Infect Dis 212: 608616. [Google Scholar]
  28. Trape JF, Zoulani A, Quinet MC, , 1987. Assessment of the incidence and prevalence of clinical malaria in semi-immune children exposed to intense and perennial transmission. Am J Epidemiol 126: 193201. [Google Scholar]
  29. Coleman RE, Maneechai N, Rachapaew N, Kumpitak C, Soyseng V, Miller RS, Thimasarn K, Sattabongkot J, , 2002. Field evaluation of the ICT Malaria Pf/Pv immunochromatographic test for the detection of asymptomatic malaria in a Plasmodium falciparum/vivax endemic area in Thailand. Am J Trop Med Hyg 66: 379383. [Google Scholar]

Data & Media loading...

Supplemental Figure

  • Received : 30 Jan 2017
  • Accepted : 17 Jul 2017
  • Published online : 30 Oct 2017

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