Longitudinal estimation of Plasmodium falciparum prevalence in relation to malaria prevention measures in six sub-Saharan African countries

Chris Drakeley, Salim Abdulla, Selidji Todagbe Agnandji, José Francisco Fernandes, Peter Kremsner, Bertrand Lell, Ludovic Mewono, Bache Emmanuel Bache, Michael Gabriel Mihayo, Omar Juma, Marcel Tanner, Marc Christian Tahita, Halidou Tinto, Salou Diallo, Palpouguini Lompo, Umberto D'Alessandro, Bernhards Ogutu, Lucas Otieno, Solomon Otieno, Walter Otieno, Janet Oyieko, Kwaku Poku Asante, Dominic Bon-Ereme Dery, George Adjei, Elisha Adeniji, Dorcas Atibilla, Seth Owusu-Agyei, Brian Greenwood, Samwel Gesase, John Lusingu, Coline Mahende, Robert Mongi, Method Segeja, Samuel Adjei, Tsiri Agbenyega, Alex Agyekum, Daniel Ansong, John Tanko Bawa, Harry Owusu Boateng, Léonard Dandalo, Veronica Escamilla, Irving Hoffman, Peter Maenje, Francis Martinson, Terrell Carter, Didier Leboulleux, David C Kaslow, Effua Usuf, Jean-Yves Pirçon, Edith Roset Bahmanyar, Chris Drakeley, Salim Abdulla, Selidji Todagbe Agnandji, José Francisco Fernandes, Peter Kremsner, Bertrand Lell, Ludovic Mewono, Bache Emmanuel Bache, Michael Gabriel Mihayo, Omar Juma, Marcel Tanner, Marc Christian Tahita, Halidou Tinto, Salou Diallo, Palpouguini Lompo, Umberto D'Alessandro, Bernhards Ogutu, Lucas Otieno, Solomon Otieno, Walter Otieno, Janet Oyieko, Kwaku Poku Asante, Dominic Bon-Ereme Dery, George Adjei, Elisha Adeniji, Dorcas Atibilla, Seth Owusu-Agyei, Brian Greenwood, Samwel Gesase, John Lusingu, Coline Mahende, Robert Mongi, Method Segeja, Samuel Adjei, Tsiri Agbenyega, Alex Agyekum, Daniel Ansong, John Tanko Bawa, Harry Owusu Boateng, Léonard Dandalo, Veronica Escamilla, Irving Hoffman, Peter Maenje, Francis Martinson, Terrell Carter, Didier Leboulleux, David C Kaslow, Effua Usuf, Jean-Yves Pirçon, Edith Roset Bahmanyar

Abstract

Background: Plasmodium falciparum prevalence (PfPR) is a widely used metric for assessing malaria transmission intensity. This study was carried out concurrently with the RTS,S/AS01 candidate malaria vaccine Phase III trial and estimated PfPR over ≤ 4 standardized cross-sectional surveys.

Methods: This epidemiology study (NCT01190202) was conducted in 8 sites from 6 countries (Burkina Faso, Gabon, Ghana, Kenya, Malawi, and Tanzania), between March 2011 and December 2013. Participants were enrolled in a 2:1:1 ratio according to age category: 6 months-4 years, 5-19 years, and ≥ 20 years, respectively, per year and per centre. All sites carried out surveys 1-3 while survey 4 was conducted only in 3 sites. Surveys were usually performed during the peak malaria parasite transmission season, in one home visit, when medical history and malaria risk factors/prevention measures were collected, and a blood sample taken for rapid diagnostic test, microscopy, and haemoglobin measurement. PfPR was estimated by site and age category.

Results: Overall, 6401 (survey 1), 6411 (survey 2), 6400 (survey 3), and 2399 (survey 4) individuals were included in the analyses. In the 6 months-4 years age group, the lowest prevalence (assessed using microscopy) was observed in 2 Tanzanian centres (4.6% for Korogwe and 9.95% for Bagamoyo) and Lambaréné, Gabon (6.0%), while the highest PfPR was recorded for Nanoro, Burkina Faso (52.5%). PfPR significantly decreased over the 3 years in Agogo (Ghana), Kombewa (Kenya), Lilongwe (Malawi), and Bagamoyo (Tanzania), and a trend for increased PfPR was observed over the 4 surveys for Kintampo, Ghana. Over the 4 surveys, for all sites, PfPR was predominantly higher in the 5-19 years group than in the other age categories. Occurrence of fever and anaemia was associated with high P. falciparum parasitaemia. Univariate analyses showed a significant association of anti-malarial treatment in 4 surveys (odds ratios [ORs]: 0.52, 0.52, 0.68, 0.41) and bed net use in 2 surveys (ORs: 0.63, 0.68, 1.03, 1.78) with lower risk of malaria infection.

Conclusion: Local PfPR differed substantially between sites and age groups. In children 6 months-4 years old, a significant decrease in prevalence over the 3 years was observed in 4 out of the 8 study sites. Trial registration Clinical Trials.gov identifier: NCT01190202:NCT. GSK Study ID numbers: 114001.

Keywords: Anaemia; Epidemiology; Malaria; Plasmodium falciparum; Prevalence; Transmission.

Figures

Fig. 1
Fig. 1
Flow diagram. N number of participants
Fig. 2
Fig. 2
Decrease of Plasmodium falciparum prevalence over the study period, by site and age group. M month, Y year
Fig. 3
Fig. 3
Plasmodium falciparum prevalence by age, in the 6 months–4 years category, by site and study year. M month, Y year
Fig. 4
Fig. 4
Prevalence of fever (a), anaemia and severe anaemia and haemoglobin concentration (b) for the 6 months–4 years age category, by parasite-density category and site. M month, Y year. Prevalence was calculated as the percentage of children with reported fever/anaemia/severe anaemia in each parasite-density category. The sites are ordered according to increasing values of Plasmodium falciparum prevalence in the first survey

References

    1. WHO. Malaria fact sheet. Geneva: World Health Organization. . Accessed 22 Mar 2017.
    1. Snow RW, Marsh K. The consequences of reducing transmission of Plasmodium falciparum in Africa. Adv Parasitol. 2002;52:235–264. doi: 10.1016/S0065-308X(02)52013-3.
    1. Snow RW, Omumbo JA, Lowe B, Molyneux CS, Obiero JO, Palmer A, et al. Relation between severe malaria morbidity in children and level of Plasmodium falciparum transmission in Africa. Lancet. 1997;349:1650–1654. doi: 10.1016/S0140-6736(97)02038-2.
    1. Hay SI, 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.
    1. Smith DL, Guerra CA, Snow RW, Hay SI. Standardizing estimates of the Plasmodium falciparum parasite rate. Malar J. 2007;6:131. doi: 10.1186/1475-2875-6-131.
    1. O’Meara WP, Collins WE, McKenzie FE. Parasite prevalence: a static measure of dynamic infections. Am J Trop Med Hyg. 2007;77:246–249.
    1. Bhatt S, Weiss DJ, Cameron E, Bisanzio D, Mappin B, Dalrymple U, et al. The effect of malaria control on Plasmodium falciparum in Africa between 2000 and 2015. Nature. 2015;526:207–211. doi: 10.1038/nature15535.
    1. The RTS,S Clinical Trials Partnership First results of phase 3 trial of RTS,S/AS01 malaria vaccine in African children. N Engl J Med. 2011;365:1863–1875. doi: 10.1056/NEJMoa1102287.
    1. The RTS,S Clinical Trials Partnership A phase 3 trial of RTS,S/AS01 malaria vaccine in African infants. N Engl J Med. 2012;367:2284–2295. doi: 10.1056/NEJMoa1208394.
    1. The RTS,S Clinical Trials Partnership Efficacy and safety of the RTS,S/AS01 malaria vaccine during 18 months after vaccination: a phase 3 randomized, controlled trial in children and young infants at 11 African sites. PLoS Med. 2014;11:e1001685. doi: 10.1371/journal.pmed.1001685.
    1. The RTS,S Clinical Trials Partnership Efficacy and safety of RTS,S/AS01 malaria vaccine with or without a booster dose in infants and children in Africa: final results of a phase 3, individually randomised, controlled trial. Lancet. 2015;386:31–45. doi: 10.1016/S0140-6736(15)60721-8.
    1. Malaria Atlas Project. . Accessed 2 Mar 2017.
    1. Malaria Indicators Surveys. . Accessed 2 Mar 2017.
    1. International Conference on Harmonization of Technical Requirements for Registration of Pharmaceuticals for Human Use (ICH): Guidance for industry: E6 good clinical practice: consolidated guidance. 1996. 38–42: 50–8. . Accessed 22 Mar 2017.
    1. Planche T, Krishna S, Kombila M, Engel K, Faucher JF, Ngou-Milama E, et al. Comparison of methods for the rapid laboratory assessment of children with malaria. Am J Trop Med Hyg. 2001;65:599–602. doi: 10.4269/ajtmh.2001.65.599.
    1. Greenwood BM, Armstrong JR. Comparison of two simple methods for determining malaria parasite density. Trans R Soc Trop Med Hyg. 1991;85:186–188. doi: 10.1016/0035-9203(91)90015-Q.
    1. Ministry of Health, Republic of Ghana. Standard treatment guidelines. 6th ed. 2010. . Accessed 22 Mar 2017.
    1. United Nations Children’s Fund, United Nations University, World Health Organization. Iron deficiency anaemia assessment, prevention, and control—a guide for programme managers (WHO/NHD/01.3). 2001. . Accessed 4 April 2017.
    1. Stoltzfus RJ, Dreyfuss ML. Guidelines for the use of iron supplements to prevent and treat iron deficiency anemia. Washington DC, ILSI PRESS; 1993. . Accessed 2 Mar 2017.
    1. Corran P, Coleman P, Riley E, Drakeley C. Serology: a robust indicator of malaria transmission intensity? Trends Parasitol. 2007;23:575–582. doi: 10.1016/j.pt.2007.08.023.
    1. Freeman MF, Tukey JW. Transformations related to the angular and the square root. Ann Math Stat. 1950;21:607–611. doi: 10.1214/aoms/1177729756.
    1. Miller JJ. The inverse of the Freeman-Tukey double arcsine transformation. Am Stat. 1978;32:138.
    1. WHO. Malaria in children under five. Geneva: World Health Organization. . Accessed 22 Mar 2017.
    1. Diallo A, Sie A, Sirima S, Sylla K, Ndiaye M, Bountogo M, et al. An epidemiological study to assess Plasmodium falciparum parasite prevalence and malaria control measures in Burkina Faso and Senegal. Malar J. 2017;16:63. doi: 10.1186/s12936-017-1715-1.
    1. Geiger C, Agustar HK, Compaore G, Coulibaly B, Sie A, Becher H, et al. Declining malaria parasite prevalence and trends of asymptomatic parasitaemia in a seasonal transmission setting in North-Western Burkina Faso between 2000 and 2009–2012. Malar J. 2013;12:27. doi: 10.1186/1475-2875-12-27.
    1. Idris ZM, Chan CW, Kongere J, Gitaka J, Logedi J, Omar A, et al. High and heterogeneous prevalence of asymptomatic and sub-microscopic malaria infections on Islands in Lake Victoria, Kenya. Sci Rep. 2016;6:36958. doi: 10.1038/srep36958.
    1. Mwesigwa J, Okebe J, Affara M, Di Tanna GL, Nwakanma D, Janha O, et al. On-going malaria transmission in The Gambia despite high coverage of control interventions: a nationwide cross-sectional survey. Malar J. 2015;14:314. doi: 10.1186/s12936-015-0829-6.
    1. Mwingira F, Genton B, Kabanywanyi A-NM, Felger I. Comparison of detection methods to estimate asexual Plasmodium falciparum parasite prevalence and gametocyte carriage in a community survey in Tanzania. Malar J. 2014;13:433. doi: 10.1186/1475-2875-13-433.
    1. Tanzania Commission for AIDS (TACAIDS) ZAC. Tanzania HIV/AIDS and Malaria Indicator Survey 2011–2012. Dar es Salaam, Tanzania: TACAIDS, ZAC, NBS, OCGS, and ICF International; 2013. . Accessed 23 Mar 2017.
    1. Buchwald AG, Coalson JE, Cohee LM, Walldorf JA, Chimbiya N, Bauleni A, et al. Insecticide-treated net effectiveness at preventing Plasmodium falciparum infection varies by age and season. Malar J. 2017;16:32. doi: 10.1186/s12936-017-1686-2.
    1. Mawili-Mboumba DP, Bouyou Akotet MK, Kendjo E, Nzamba J, Medang MO, Mbina JR, et al. Increase in malaria prevalence and age of at risk population in different areas of Gabon. Malar J. 2013;12:3. doi: 10.1186/1475-2875-12-3.
    1. Kelly-Hope LA, McKenzie FE. The multiplicity of malaria transmission: a review of entomological inoculation rate measurements and methods across sub-Saharan Africa. Malar J. 2009;8:19. doi: 10.1186/1475-2875-8-19.
    1. Shaukat AM, Breman JG, McKenzie FE. Using the entomological inoculation rate to assess the impact of vector control on malaria parasite transmission and elimination. Malar J. 2010;9:122. doi: 10.1186/1475-2875-9-122.
    1. Leach A, Vekemans J, Lievens M, Ofori-Anyinam O, Cahill C, Owusu-Agyei S, et al. Design of a phase III multicenter trial to evaluate the efficacy of the RTS, S/AS01 malaria vaccine in children across diverse transmission settings in Africa. Malar J. 2011;10:224. doi: 10.1186/1475-2875-10-224.
    1. Olumese P. Seasonal Malaria Chemoprevention: WHO policy and perspectives. ACCESS SMC Meeting. Transforming the malaria landscape in the Sahel: seasonal malaria chemoprevention. 9 June 2016, London, UK. . Accessed 4 Apr 2017.
    1. Yakasai AM, Hamza M, Dalhat MM, Bello M, Gadanya MA, Yaqub ZM, et al. Adherence to artemisinin-based combination therapy for the treatment of uncomplicated malaria: a systematic review and meta-analysis. J Trop Med. 2015;2015:189232. doi: 10.1155/2015/189232.
    1. 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.
    1. Louis VR, Schoeps A, Tiendrebeogo J, Beiersmann C, Ye M, Damiba MR, et al. An insecticide-treated bed-net campaign and childhood malaria in Burkina Faso. Bull World Health Organ. 2015;93:750–758. doi: 10.2471/BLT.14.147702.
    1. Asante KP, Zandoh C, Dery DB, Brown C, Adjei G, Antwi-Dadzie Y, et al. Malaria epidemiology in the Ahafo area of Ghana. Malar J. 2011;10:211. doi: 10.1186/1475-2875-10-211.
    1. Binka FN, Kubaje A, Adjuik M, Williams LA, Lengeler C, Maude GH, et al. Impact of permethrin impregnated bednets on child mortality in Kassena-Nankana district, Ghana: a randomized controlled trial. Trop Med Int Health. 1996;1:147–154. doi: 10.1111/j.1365-3156.1996.tb00020.x.
    1. Fegan GW, Noor AM, Akhwale WS, Cousens S, Snow RW. Effect of expanded insecticide-treated bednet coverage on child survival in rural Kenya: a longitudinal study. Lancet. 2007;370:1035–1039. doi: 10.1016/S0140-6736(07)61477-9.
    1. Lindblade KA, Eisele TP, Gimnig JE, Alaii JA, Odhiambo F, ter Kuile FO, et al. Sustainability of reductions in malaria transmission and infant mortality in western Kenya with use of insecticide-treated bednets: 4 to 6 years of follow-up. JAMA. 2004;291:2571–2580. doi: 10.1001/jama.291.21.2571.
    1. Lindblade KA, Gimnig JE, Kamau L, Hawley WA, Odhiambo F, Olang G, et al. Impact of sustained use of insecticide-treated bednets on malaria vector species distribution and culicine mosquitoes. J Med Entomol. 2006;43:428–432. doi: 10.1093/jmedent/43.2.428.
    1. Namountougou M, Diabate A, Etang J, Bass C, Sawadogo SP, Gnankinie O, et al. First report of the L1014S kdr mutation in wild populations of Anopheles gambiae M and S molecular forms in Burkina Faso (West Africa) Acta Trop. 2013;125:123–127. doi: 10.1016/j.actatropica.2012.10.012.
    1. Namountougou M, Simard F, Baldet T, Diabate A, Ouedraogo JB, Martin T, et al. Multiple insecticide resistance in Anopheles gambiae s.l. populations from Burkina Faso, West Africa. PLoS ONE. 2012;7:e48412. doi: 10.1371/journal.pone.0048412.
    1. Otten M, Aregawi M, Were W, Karema C, Medin A, Bekele W, et al. Initial evidence of reduction of malaria cases and deaths in Rwanda and Ethiopia due to rapid scale-up of malaria prevention and treatment. Malar J. 2009;8:14. doi: 10.1186/1475-2875-8-14.
    1. Zhou G, Afrane YA, Vardo-Zalik AM, Atieli H, Zhong D, Wamae P, et al. Changing patterns of malaria epidemiology between 2002 and 2010 in Western Kenya: the fall and rise of malaria. PLoS ONE. 2011;6:e20318. doi: 10.1371/journal.pone.0020318.
    1. Lengeler C. Insecticide-treated bed nets and curtains for preventing malaria. Cochrane Database Syst Rev. 2004;(2):CD000363. doi:10.1002/14651858.CD000363.pub2
    1. Clarke SE, Brooker S, Njagi JK, Njau E, Estambale B, Muchiri E, et al. Malaria morbidity among school children living in two areas of contrasting transmission in western Kenya. Am J Trop Med Hyg. 2004;71:732–738.
    1. Marsh K, Snow RW. Malaria transmission and morbidity. Parassitologia. 1999;41:241–246.
    1. Saute F, Aponte J, Almeda J, Ascaso C, Abellana R, Vaz N, et al. Malaria in southern Mozambique: malariometric indicators and malaria case definition in Manhica district. Trans R Soc Trop Med Hyg. 2003;97:661–666. doi: 10.1016/S0035-9203(03)80098-6.
    1. Filipe JA, Riley EM, Drakeley CJ, Sutherland CJ, Ghani AC. Determination of the processes driving the acquisition of immunity to malaria using a mathematical transmission model. PLoS Comput Biol. 2007;3:e255. doi: 10.1371/journal.pcbi.0030255.
    1. Asante KP, Owusu-Agyei S, Cairns M, Boamah E, Manu G, Twumasi M, et al. Non-malaria fevers in a high malaria endemic area of Ghana. BMC Infect Dis. 2016;16:327. doi: 10.1186/s12879-016-1654-4.
    1. Parr JB, Belson C, Patel JC, Hoffman IF, Kamthunzi P, Martinson F, et al. Estimation of Plasmodium falciparum transmission intensity in Lilongwe, Malawi, by microscopy, rapid diagnostic testing, and nucleic acid detection. Am J Trop Med Hyg. 2016;95:373–377. doi: 10.4269/ajtmh.16-0156.
    1. WHO. Malaria vector control and personal protection: Report of a WHO study group. Geneva: World Health Organization; 2006. p. 62. WHO Technical Report series No. 936.
    1. Greenwood BM, Bojang K, Whitty CJ, Targett GA. Malaria. Lancet. 2005;365:1487–1498. doi: 10.1016/S0140-6736(05)66420-3.
    1. Shiff C. Integrated approach to malaria control. Clin Microbiol Rev. 2002;15:278–293. doi: 10.1128/CMR.15.2.278-293.2002.
    1. Snow RW, Marsh K, le Sueur D. The need for maps of transmission intensity to guide malaria control in Africa. Parasitol Today. 1996;12:455–457. doi: 10.1016/S0169-4758(96)30032-X.
    1. Vandoolaeghe P, Schuerman L. The RTS, S/AS01 malaria vaccine in children 5 to 17 months of age at first vaccination. Expert Rev Vaccines. 2016;15:1481–1493. doi: 10.1080/14760584.2016.1236689.

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