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Published in: Malaria Journal 1/2017

Open Access 01-12-2017 | Research

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

Authors: 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

Published in: Malaria Journal | Issue 1/2017

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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
Appendix
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Literature
2.
go back to reference Snow RW, Marsh K. The consequences of reducing transmission of Plasmodium falciparum in Africa. Adv Parasitol. 2002;52:235–64.CrossRefPubMed Snow RW, Marsh K. The consequences of reducing transmission of Plasmodium falciparum in Africa. Adv Parasitol. 2002;52:235–64.CrossRefPubMed
3.
go back to reference 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;349:1650–4.CrossRefPubMed 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;349:1650–4.CrossRefPubMed
6.
go back to reference O’Meara WP, Collins WE, McKenzie FE. Parasite prevalence: a static measure of dynamic infections. Am J Trop Med Hyg. 2007;77:246–9.PubMedPubMedCentral O’Meara WP, Collins WE, McKenzie FE. Parasite prevalence: a static measure of dynamic infections. Am J Trop Med Hyg. 2007;77:246–9.PubMedPubMedCentral
7.
go back to reference 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;526:207–11.CrossRefPubMedPubMedCentral 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;526:207–11.CrossRefPubMedPubMedCentral
8.
go back to reference 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;365:1863–75.CrossRef 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;365:1863–75.CrossRef
9.
go back to reference The RTS,S Clinical Trials Partnership. A phase 3 trial of RTS,S/AS01 malaria vaccine in African infants. N Engl J Med. 2012;367:2284–95.CrossRef The RTS,S Clinical Trials Partnership. A phase 3 trial of RTS,S/AS01 malaria vaccine in African infants. N Engl J Med. 2012;367:2284–95.CrossRef
10.
go back to reference 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.CrossRef 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.CrossRef
11.
go back to reference 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.CrossRef 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.CrossRef
15.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
16.
go back to reference Greenwood BM, Armstrong JR. Comparison of two simple methods for determining malaria parasite density. Trans R Soc Trop Med Hyg. 1991;85:186–8.CrossRefPubMed Greenwood BM, Armstrong JR. Comparison of two simple methods for determining malaria parasite density. Trans R Soc Trop Med Hyg. 1991;85:186–8.CrossRefPubMed
20.
go back to reference Corran P, Coleman P, Riley E, Drakeley C. Serology: a robust indicator of malaria transmission intensity? Trends Parasitol. 2007;23:575–82.CrossRefPubMed Corran P, Coleman P, Riley E, Drakeley C. Serology: a robust indicator of malaria transmission intensity? Trends Parasitol. 2007;23:575–82.CrossRefPubMed
21.
go back to reference Freeman MF, Tukey JW. Transformations related to the angular and the square root. Ann Math Stat. 1950;21:607–11.CrossRef Freeman MF, Tukey JW. Transformations related to the angular and the square root. Ann Math Stat. 1950;21:607–11.CrossRef
22.
go back to reference Miller JJ. The inverse of the Freeman-Tukey double arcsine transformation. Am Stat. 1978;32:138. Miller JJ. The inverse of the Freeman-Tukey double arcsine transformation. Am Stat. 1978;32:138.
24.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
25.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
26.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
27.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
28.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
30.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
31.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
32.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
33.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
34.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
36.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
37.
go back to reference Lindblade KA, Steinhardt L, Samuels A, Kachur SP, Slutsker L. The silent threat: asymptomatic parasitemia and malaria transmission. Expert Rev Anti Infect Ther. 2013;11:623–39.CrossRefPubMed Lindblade KA, Steinhardt L, Samuels A, Kachur SP, Slutsker L. The silent threat: asymptomatic parasitemia and malaria transmission. Expert Rev Anti Infect Ther. 2013;11:623–39.CrossRefPubMed
38.
go back to reference 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;93:750–8.CrossRefPubMedPubMedCentral 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;93:750–8.CrossRefPubMedPubMedCentral
39.
40.
go back to reference 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;1:147–54.CrossRefPubMed 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;1:147–54.CrossRefPubMed
41.
go back to reference 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;370:1035–9.CrossRefPubMedPubMedCentral 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;370:1035–9.CrossRefPubMedPubMedCentral
42.
go back to reference 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;291:2571–80.CrossRefPubMed 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;291:2571–80.CrossRefPubMed
43.
go back to reference 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;43:428–32.CrossRefPubMed 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;43:428–32.CrossRefPubMed
44.
go back to reference 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;125:123–7.CrossRefPubMed 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;125:123–7.CrossRefPubMed
45.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
46.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
47.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
49.
go back to reference 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;71:732–8.PubMed 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;71:732–8.PubMed
50.
go back to reference Marsh K, Snow RW. Malaria transmission and morbidity. Parassitologia. 1999;41:241–6.PubMed Marsh K, Snow RW. Malaria transmission and morbidity. Parassitologia. 1999;41:241–6.PubMed
51.
go back to reference 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;97:661–6.CrossRefPubMed 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;97:661–6.CrossRefPubMed
52.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
53.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
54.
go back to reference 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;95:373–7.CrossRefPubMedPubMedCentral 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;95:373–7.CrossRefPubMedPubMedCentral
55.
go back to reference 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. 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.
58.
go back to reference Snow RW, Marsh K, le Sueur D. The need for maps of transmission intensity to guide malaria control in Africa. Parasitol Today. 1996;12:455–7.CrossRef Snow RW, Marsh K, le Sueur D. The need for maps of transmission intensity to guide malaria control in Africa. Parasitol Today. 1996;12:455–7.CrossRef
59.
go back to reference 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;15:1481–93.CrossRefPubMed 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;15:1481–93.CrossRefPubMed
Metadata
Title
Longitudinal estimation of Plasmodium falciparum prevalence in relation to malaria prevention measures in six sub-Saharan African countries
Authors
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
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2017
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-017-2078-3

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