Epidemiology of malaria in a village in the Rufiji River Delta, Tanzania: declining transmission over 25 years revealed by different parasitological metrics
Anna Färnert, Victor Yman, Manijeh Vafa Homann, Grace Wandell, Leah Mhoja, Marita Johansson, Salome Jesaja, Johanna Sandlund, Kazuyuki Tanabe, Ulf Hammar, Matteo Bottai, Zulfiqarali G Premji, Anders Björkman, Ingegerd Rooth, Anna Färnert, Victor Yman, Manijeh Vafa Homann, Grace Wandell, Leah Mhoja, Marita Johansson, Salome Jesaja, Johanna Sandlund, Kazuyuki Tanabe, Ulf Hammar, Matteo Bottai, Zulfiqarali G Premji, Anders Björkman, Ingegerd Rooth
Abstract
Background: Assessments of the epidemiology of malaria over time are needed to understand changes in transmission and guide control and elimination strategies.
Methods: A longitudinal population study was established in 1985 in Nyamisati village in the Rufiji River Delta, Tanzania. A physician and research team lived in the village 1984-2000. Parasite prevalence by microscopy and two PCR methods, spleen rates and haemoglobin levels were measured in repeated cross-sectional surveys between 1985 and 2010. Passive surveillance of malaria cases was maintained until end 1999. Bed nets were distributed after the surveys 1993, 1999 and 2010.
Results: In 1985, overall parasite prevalence by microscopy was 70% (90% in children ages two to nine years). The prevalence decreased gradually by microscopy (38.9% 1994, 26.7% 1999) and msp2-PCR (58.7% 1994, 44.8% 1999), whereas real-time PCR prevalence remained higher throughout the 1990s (69.4% 1994, 64.8% 1999). In 2010, parasite prevalence was 17.8% by real-time PCR and 16.3% by msp2-PCR, and estimated to 4.8% by microscopy. Spleen rates in children ages two to nine years decreased earlier than parasite prevalence, from >75 to 42% in the 1980s, to nil during the 1990s. The prevalence of severe and moderate anaemia decreased from 41.1 to 13.1%. No deaths at the time of acute malaria were recorded when the research team lived in the village.
Conclusions: A marked decline in malaria transmission was observed over 25 years. The decrease was detected after the arrival of the research team and continued gradually both before and after distribution of bed nets. Spleen rates and microscopy identified early changes when transmission was still intense, whereas real-time PCR was a more sensitive metric when transmission was reduced. The study provides historical data on malaria within a closely monitored rural village and contributes to the understanding of changing epidemiology in sub-Saharan Africa.
Figures
References
- WHO: World Malaria Report 2013. Geneva: World Health Organization; Accessed August 1 2014
- malERA Consultative Group on Monitoring, Evaluation, and Surveillance A research agenda for malaria eradication: monitoring, evaluation, and surveillance. PLoS Med. 2011;8:e1000400. doi: 10.1371/journal.pmed.1000400.
- Rooth I. PhD thesis. 1992. Malaria Morbidity and Control in a Tanzanian Village.
- Rooth I, Björkman A. Fever episodes in a holoendemic malaria area of Tanzania: parasitological and clinical findings and diagnostic aspects related to malaria. Trans R Soc Trop Med Hyg. 1992;86:479–482. doi: 10.1016/0035-9203(92)90076-O.
- Rooth I, Sinani HM, Björkman A. Proguanil daily or chloroproguanil twice weekly are efficacious against falciparum malaria in a holoendemic area of Tanzania. Am J Trop Med Hyg. 1991;94:45–49.
- Rooth I, Björkman A. Suppression of Plasmodium falciparum infections during concomitant measles or influenza but not during pertussis. Am J Trop Med Hyg. 1992;47:675–681.
- Färnert A, Snounou G, Rooth I, Björkman A. Daily dynamics of Plasmodium falciparum subpopulations in asymptomatic children in a holoendemic area. Am J Trop Med Hyg. 1997;56:538–547.
- Färnert A, Rooth I, Svensson Å, Snounou G, Björkman A. Complexity of plasmodium falciparum infections is consistent over time and protects against clinical disease in Tanzanian children. J Infect Dis. 1999;179:989–995. doi: 10.1086/314652.
- Bereczky S, Liljander A, Rooth I, Faraja L, Granath F, Montgomery SM, Färnert A. Multiclonal asymptomatic Plasmodium falciparum infections predict a reduced risk of malaria disease in a Tanzanian population. Microbes Infect. 2007;9:103–110. doi: 10.1016/j.micinf.2006.10.014.
- Färnert A, Lebbad M, Faraja L, Rooth I. Extensive dynamics of Plasmodium falciparum densities, stages and genotyping profiles. Malar J. 2008;7:241. doi: 10.1186/1475-2875-7-241.
- Tanabe K, Sakihama N, Rooth I, Björkman A, Färnert A. High frequency of recombination-driven allelic diversity and temporal variation of Plasmodium falciparum msp1 in Tanzania. Am J Trop Med Hyg. 2007;76:1037–1045.
- Tanabe K, Arisue N, Palacpac NMQ, Yagi M, Tougan T, Honma H, Ferreira MU, Färnert A, Björkman A, Kaneko A, Nakamura M, Hirayama K, Mita T, Horii T. Geographic differentiation of polymorphism in the Plasmodium falciparum malaria vaccine candidate gene SERA5. Vaccine. 2012;30:1583–1593. doi: 10.1016/j.vaccine.2011.12.124.
- Rooth I, Perlmann H, Björkman A. Plasmodium falciparum reinfection in children from a holoendemic area in relation to seroreactivities against oligopeptides from different malaria antigens. Am J Trop Med Hyg. 1991;45:309–318.
- Bereczky S, Montgomery SM, Troye-Blomberg M, Rooth I, Shaw MA, Färnert A. Elevated anti-malarial IgE in asymptomatic individuals is associated with reduced risk for subsequent clinical malaria. Int J Parasitol. 2004;34:935–942. doi: 10.1016/j.ijpara.2004.04.007.
- Reddy SB, Anders RF, Beeson JG, Färnert A, Kironde F, Berenzon SK, Wahlgren M, Linse S, Persson KEM. High affinity antibodies to Plasmodium falciparum merozoite antigens are associated with protection from malaria. PLoS One. 2012;7:e32242. doi: 10.1371/journal.pone.0032242.
- Rono J, Osier F, Olsson D, Montgomery S, Mhoja L, Rooth I, Marsh K, Färnert A. Breadth of anti-merozoite antibody responses is associated with the genetic diversity of asymptomatic Plasmodium falciparum infections and protection against clinical malaria. Clin Infect Dis. 2013;57:1409–1416. doi: 10.1093/cid/cit556.
- Carpenter D, Abushama H, Bereczky S, Farnert A, Rooth I, Troye-Blomberg M, Quinnell RJ, Shaw MA. Immunogenetic control of antibody responsiveness in a malaria endemic area. Hum Immunol. 2007;68:165–169. doi: 10.1016/j.humimm.2006.12.002.
- Carpenter D, Rooth I, Färnert A, Abushama H, Quinnell RJ, Shaw MA. Genetics of susceptibility to malaria related phenotypes. Infect Genet Evol. 2009;9:97–103. doi: 10.1016/j.meegid.2008.10.008.
- Bhattarai A, Ali AS, Kachur SP, Mårtensson A, Abbas AK, Khatib R, Al-Mafazy AW, Ramsan M, Rotllant G, Gerstenmaier JF, Molteni F, Abdulla S, Montgomery SM, Kaneko A, Björkman A. Impact of artemisinin-based combination therapy and insecticide-treated nets on malaria burden in Zanzibar. PLoS Med. 2007;4:e309. doi: 10.1371/journal.pmed.0040309.
- O’Meara WP, Bejon P, Mwangi TW, Okiro EA, Peshu N, Snow RW, Newton CR, Marsh K. Effect of a fall in malaria transmission on morbidity and mortality in Kilifi, Kenya. Lancet. 2008;372:1555–1562. doi: 10.1016/S0140-6736(08)61655-4.
- Ceesay SJ, Casals-Pascual C, Erskine J, Anya SE, Duah NO, Fulford AJ, Sesay SS, Abubakar I, Dunyo S, Sey O, Palmer A, Fofana M, Corrah T, Bojang KA, Whittle HC, Greenwood BM, Conway DJ. Changes in malaria indices between 1999 and 2007 in The Gambia: a retrospective analysis. Lancet. 2008;372:1545–1554. doi: 10.1016/S0140-6736(08)61654-2.
- Kilian A, Boulay M, Koenker H, Lynch M. How many mosquito nets are needed to achieve universal coverage? Recommendations for the quantification and allocation of long-lasting insecticidal nets for mass campaigns. Malar J. 2010;9:330.
- Hackett LW. Spleen measurement in malaria. J Nat Malar Soc. 1944;3:121–123.
- Shokoples SE, Ndao M, Kowalewska-Grochowska K, Yanow SK. Multiplexed real-time PCR assay for discrimination of Plasmodium species with improved sensitivity for mixed infections. J Clin Microbiol. 2009;47:975–980. doi: 10.1128/JCM.01858-08.
- Liljander A, Wiklund L, Falk N, Kweku M, Mårtensson A, Felger I, Färnert A. Optimization and validation of multi-coloured capillary electrophoresis for genotyping of Plasmodium falciparum merozoite surface proteins (msp1 and 2) Malar J. 2009;8:78. doi: 10.1186/1475-2875-8-78.
- Okell LC, Bousema T, Griffin JT, Ouédraogo AL, Ghani AC, Drakeley CJ. Factors determining the occurrence of submicroscopic malaria infections and their relevance for control. Nat Commun. 2012;3:1237. doi: 10.1038/ncomms2241.
- WHO . Haemoglobin Concentrations for the Diagnosis of Anaemia and Assessment of Severity. Geneva: World Health Organization; 2011. Vitamin and Mineral Nutrition Information System.
- National Bureau of Statistics Tanzania . Village Statistics-Census. 2012.
- WHO . Terminology of Malaria and of Malaria Eradication: Report of a Drafting Committee. Geneva: World Health Organization; 1963.
- Ishengoma DS, Mmbando BP, Segeja MD, Alifrangis M, Lemnge MM, Bygbjerg IC. Declining burden of malaria over two decades in a rural community of Muheza district, north-eastern Tanzania. Malar J. 2013;12:338. doi: 10.1186/1475-2875-12-338.
- Trape JF, Tall A, Sokhna C, Ly AB, Diagne N, Ndiath O, Mazenot C, Richard V, Badiane A, Dieye-Ba F, Faye J, Ndiaye G, Diene Sarr F, Roucher C, Bouganali C, Bassène H, Touré-Baldé A, Roussilhon C, Perraut R, Spiegel A, Sarthou JL, da Silva LP, Mercereau-Puijalon O, Druilhe P, Rogier C. The rise and fall of malaria in a west African rural community, Dielmo, Senegal, from 1990 to 2012: a 22 year longitudinal study. Lancet Infect Dis. 2014;14:476–488. doi: 10.1016/S1473-3099(14)70712-1.
- Tusting LS, Bousema T, Smith DL, Drakeley C. Measuring changes in Plasmodium falciparum transmission: precision, accuracy and costs of metrics. Adv Parasitol. 2014;84:151–208. doi: 10.1016/B978-0-12-800099-1.00003-X.
- Hay S, Smith DL, Snow RW. Measuring malaria endemicity from intense to interrupted transmission. Lancet Infect Dis. 2008;8:369–378. doi: 10.1016/S1473-3099(08)70069-0.
- WHO . Disease Surveillance for Malaria Control. Geneva: World Health Organization; 2012.
- Langsley G, Hyde JE, Goman M, Scaife JG. Cloning and characterisation of the rRNA genes from the human malaria parasite Plasmodium falciparum. Nucleic Acids Res. 1983;11:8703–8717. doi: 10.1093/nar/11.24.8703.
- Smythe JA, Coppel RL, Day KP, Martin RK, Oduola AM, Kemp DJ, Anders RF. Structural diversity in the Plasmodium falciparum merozoite surface antigen 2. Proc Natl Acad Sci U S A. 1991;88:1751–1755. doi: 10.1073/pnas.88.5.1751.
- Lindblade KA, Steinhardt L, Samuels A, Kachur SP, Slutsker L. The silent threat: asymptomatic parasitemia and malaria transmission. Expert Rev Anti Infect Ther. 2013;11:623–639. doi: 10.1586/eri.13.45.
- Satoguina J, Walther B, Drakeley C, Nwakanma D, Oriero EC, Correa S, Corran P, Conway DJ, Walther M. Comparison of surveillance methods applied to a situation of low malaria prevalence at rural sites in The Gambia and Guinea Bissau. Malar J. 2009;8:274. doi: 10.1186/1475-2875-8-274.
- Mmbando BP, Vestergaard LS, Kitua AY, Lemnge MM, Theander TG, Lusingu JPA. A progressive declining in the burden of malaria in north-eastern Tanzania. Malar J. 2010;9:216. doi: 10.1186/1475-2875-9-216.
- Rooth I. Annual Report. Dar es Salaam, Tanzania: Mchukwi Hospital; 1984.
- Maitland K, Williams TN, Peto TE, Day KP, Clegg JB, Weatherall DJ, Bowden DK. Absence of malaria-specific mortality in children in an area of hyperendemic malaria. Trans R Soc Trop Med Hyg. 1997;91:562–566. doi: 10.1016/S0035-9203(97)90026-2.
- National Bureau of Statistics Tanzania (NBS) and ICF Macro . Tanzania Demographic and Health Survey 2010. Tanzania: NBS; 2011.
- Abdalla S, Weatherall DJ, Wickramasinghe SN, Hughes M. The anaemia of P. falciparum malaria. Br J Haematol. 1980;46:171–183. doi: 10.1111/j.1365-2141.1980.tb05956.x.
- Jagannathan P, Muhindo MK, Kakuru A, Arinaitwe E, Greenhouse B, Tappero J, Rosenthal PJ, Kaharuza F, Kamya MR, Dorsey G. Increasing incidence of malaria in children despite insecticide-treated bed nets and prompt anti-malarial therapy in Tororo, Uganda. Malar J. 2012;11:435. doi: 10.1186/1475-2875-11-435.
- Khatib RA, Selemani M, Mrisho GA, Masanja IM, Amuri M, Njozi MH, Kajungu D, Kuepfer I, Abdulla SM, de Savigny D. Access to artemisinin-based anti-malarial treatment and its related factors in rural Tanzania. Malar J. 2013;12:155. doi: 10.1186/1475-2875-12-155.
- Meyrowitsch DW, Pedersen EM, Alifrangis M, Scheike TH, Malecela MN, Magesa SM, Derua YA, Rwegoshora RT, Michael E, Simonsen PE. Is the current decline in malaria burden in sub-Saharan Africa due to a decrease in vector population? Malar J. 2011;10:188. doi: 10.1186/1475-2875-10-188.
- Derua YA, Alifrangis M, Hosea KM, Meyrowitsch DW, Magesa SM, Pedersen EM, Simonsen PE. Change in composition of the Anopheles gambiae complex and its possible implications for the transmission of malaria and lymphatic filariasis in north-eastern Tanzania. Malar J. 2012;11:188. doi: 10.1186/1475-2875-11-188.
- Kigadye ES, Nkwengulila G, Magesa SM, Abdulla S. Diversity, spatial and temporal abundance of Anopheles gambiae complex in the Rufiji River basin, south-eastern Tanzania. Tanzan J Health Res. 2010;12:68–72. doi: 10.4314/thrb.v12i1.56320.
- Hay SI, Omumbo JA, Craig MH, Snow RW. Earth observation, geographic information systems and Plasmodium falciparum malaria in sub-Saharan Africa. Adv Parasitol. 2000;47:173–215. doi: 10.1016/S0065-308X(00)47009-0.
- Khatib RA, Skarbinski J, Njau JD, Goodman CA, Elling BF, Kahigwa E, Roberts JM, MacArthur JR, Gutman JR, Kabanywanyi AM, Smith EE, Somi MF, Lyimo T, Mwita A, Genton B, Tanner M, Mills A, Mshinda H, Bloland PB, Abdulla SM, Kachur SP. Routine delivery of artemisinin-based combination treatment at fixed health facilities reduces malaria prevalence in Tanzania: an observational study. Malar J. 2012;11:140. doi: 10.1186/1475-2875-11-140.
- Tusting LS, Willey B, Lucas H, Thompson J, Kafy HT, Smith R, Lindsay SW. Socioeconomic development as an intervention against malaria: a systematic review and meta-analysis. Lancet. 2013;382:963–972. doi: 10.1016/S0140-6736(13)60851-X.
Source: PubMed