Skip to main content
Top
Published in: Malaria Journal 1/2020

01-12-2020 | Malaria | Research

Rapid shifts in the age-specific burden of malaria following successful control interventions in four regions of Uganda

Authors: Simon P. Kigozi, Ruth N. Kigozi, Adrienne Epstein, Arthur Mpimbaza, Asadu Sserwanga, Adoke Yeka, Joaniter I. Nankabirwa, Katherine Halliday, Rachel L. Pullan, Damian Rutazaana, Catherine M. Sebuguzi, Jimmy Opigo, Moses R. Kamya, Sarah G. Staedke, Grant Dorsey, Bryan Greenhouse, Isabel Rodriguez-Barraquer

Published in: Malaria Journal | Issue 1/2020

Login to get access

Abstract

Background

Malaria control using long-lasting insecticidal nets (LLINs) and indoor residual spraying of insecticide (IRS) has been associated with reduced transmission throughout Africa. However, the impact of transmission reduction on the age distribution of malaria cases remains unclear.

Methods

Over a 10-year period (January 2009 to July 2018), outpatient surveillance data from four health facilities in Uganda were used to estimate the impact of control interventions on temporal changes in the age distribution of malaria cases using multinomial regression. Interventions included mass distribution of LLINs at all sites and IRS at two sites.

Results

Overall, 896,550 patient visits were included in the study; 211,632 aged < 5 years, 171,166 aged 5–15 years and 513,752 > 15 years. Over time, the age distribution of patients not suspected of malaria and those malaria negative either declined or remained the same across all sites. In contrast, the age distribution of suspected and confirmed malaria cases increased across all four sites. In the two LLINs-only sites, the proportion of malaria cases in < 5 years decreased from 31 to 16% and 35 to 25%, respectively. In the two sites receiving LLINs plus IRS, these proportions decreased from 58 to 30% and 64 to 47%, respectively. Similarly, in the LLINs-only sites, the proportion of malaria cases > 15 years increased from 40 to 61% and 29 to 39%, respectively. In the sites receiving LLINs plus IRS, these proportions increased from 19 to 44% and 18 to 31%, respectively.

Conclusions

These findings demonstrate a shift in the burden of malaria from younger to older individuals following implementation of successful control interventions, which has important implications for malaria prevention, surveillance, case management and control strategies.
Appendix
Available only for authorised users
Literature
1.
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
2.
go back to reference Murray CJ, Ortblad KF, Guinovart C, Lim SS, Wolock TM, Roberts DA, et al. Global, regional, and national incidence and mortality for HIV, tuberculosis, and malaria during 1990–2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet. 2014;384:1005–70.CrossRefPubMedPubMedCentral Murray CJ, Ortblad KF, Guinovart C, Lim SS, Wolock TM, Roberts DA, et al. Global, regional, and national incidence and mortality for HIV, tuberculosis, and malaria during 1990–2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet. 2014;384:1005–70.CrossRefPubMedPubMedCentral
3.
go back to reference Noor AM, Kinyoki DK, Mundia CW, Kabaria CW, Mutua JW, Alegana VA, et al. The changing risk of Plasmodium falciparum malaria infection in Africa: 2000-10: a spatial and temporal analysis of transmission intensity. Lancet. 2014;383:1739–47.CrossRefPubMedPubMedCentral Noor AM, Kinyoki DK, Mundia CW, Kabaria CW, Mutua JW, Alegana VA, et al. The changing risk of Plasmodium falciparum malaria infection in Africa: 2000-10: a spatial and temporal analysis of transmission intensity. Lancet. 2014;383:1739–47.CrossRefPubMedPubMedCentral
4.
go back to reference Nkumama IN, O’Meara WP, Osier FHA. Changes in malaria epidemiology in Africa and new challenges for elimination. Trends Parasitol. 2017;33:128–40.CrossRefPubMed Nkumama IN, O’Meara WP, Osier FHA. Changes in malaria epidemiology in Africa and new challenges for elimination. Trends Parasitol. 2017;33:128–40.CrossRefPubMed
5.
go back to reference WHO. World Malaria Report 2008. Geneva, World Health Organization, 2008. WHO. World Malaria Report 2008. Geneva, World Health Organization, 2008.
6.
go back to reference WHO. Malaria surveillance, monitoring & evaluation: a reference manual. Geneva, World Health Organization, 2018:8. WHO. Malaria surveillance, monitoring & evaluation: a reference manual. Geneva, World Health Organization, 2018:8.
7.
go back to reference Molineaux L, Gramiccia G. The Garki Project: Research on the epidemiology and control of malaria in the Sudan Savanna of West Africa. Geneva: World Health Organization; 1980. Molineaux L, Gramiccia G. The Garki Project: Research on the epidemiology and control of malaria in the Sudan Savanna of West Africa. Geneva: World Health Organization; 1980.
8.
go back to reference Carneiro I, Roca-Feltrer A, Griffin JT, Smith L, Tanner M, Schellenberg JA, et al. Age-patterns of malaria vary with severity, transmission intensity and seasonality in sub-Saharan Africa: a systematic review and pooled analysis. PLoS ONE. 2010;5:e8988.CrossRefPubMedPubMedCentral Carneiro I, Roca-Feltrer A, Griffin JT, Smith L, Tanner M, Schellenberg JA, et al. Age-patterns of malaria vary with severity, transmission intensity and seasonality in sub-Saharan Africa: a systematic review and pooled analysis. PLoS ONE. 2010;5:e8988.CrossRefPubMedPubMedCentral
9.
go back to reference Schellenberg D, Menendez C, Aponte J, Guinovart C, Mshinda H, Tanner M, et al. The changing epidemiology of malaria in Ifakara Town, southern Tanzania. Trop Med Int Health. 2004;9:68–76.CrossRefPubMed Schellenberg D, Menendez C, Aponte J, Guinovart C, Mshinda H, Tanner M, et al. The changing epidemiology of malaria in Ifakara Town, southern Tanzania. Trop Med Int Health. 2004;9:68–76.CrossRefPubMed
10.
go back to reference Ceesay SJ, Casals-Pascual C, Erskine J, Anya SE, Duah NO, Fulford AJ, et al. Changes in malaria indices between 1999 and 2007 in The Gambia: a retrospective analysis. Lancet. 2008;372:1545–54.CrossRefPubMedPubMedCentral Ceesay SJ, Casals-Pascual C, Erskine J, Anya SE, Duah NO, Fulford AJ, et al. Changes in malaria indices between 1999 and 2007 in The Gambia: a retrospective analysis. Lancet. 2008;372:1545–54.CrossRefPubMedPubMedCentral
11.
go back to reference WHO. World Malaria Report 2017. Geneva, World Health Organization, 2017. WHO. World Malaria Report 2017. Geneva, World Health Organization, 2017.
12.
go back to reference Nguyen HV, van den Eede P, van Overmeir C, Thang ND, le Hung X, D’Alessandro U, et al. Marked age-dependent prevalence of symptomatic and patent infections and complexity of distribution of human Plasmodium species in central Vietnam. Am J Trop Med Hyg. 2012;87:989–95.CrossRefPubMedPubMedCentral Nguyen HV, van den Eede P, van Overmeir C, Thang ND, le Hung X, D’Alessandro U, et al. Marked age-dependent prevalence of symptomatic and patent infections and complexity of distribution of human Plasmodium species in central Vietnam. Am J Trop Med Hyg. 2012;87:989–95.CrossRefPubMedPubMedCentral
13.
go back to reference Nankabirwa J, Wandera B, Kiwanuka N, Staedke SG, Kamya MR, Brooker SJ. Asymptomatic Plasmodium infection and cognition among primary schoolchildren in a high malaria transmission setting in Uganda. Am J Trop Med Hyg. 2013;88:1102–8.CrossRefPubMedPubMedCentral Nankabirwa J, Wandera B, Kiwanuka N, Staedke SG, Kamya MR, Brooker SJ. Asymptomatic Plasmodium infection and cognition among primary schoolchildren in a high malaria transmission setting in Uganda. Am J Trop Med Hyg. 2013;88:1102–8.CrossRefPubMedPubMedCentral
14.
go back to reference WHO. Global technical strategy for malaria 2016-2030. Geneva, World Health Organization, 2015. WHO. Global technical strategy for malaria 2016-2030. Geneva, World Health Organization, 2015.
15.
go back to reference Fekadu M, Yenit MK, Lakew AM. The prevalence of asymptomatic malaria parasitemia and associated factors among adults in Dembia district, northwest Ethiopia, 2017. Arch Public Health. 2018;76:74.CrossRefPubMedPubMedCentral Fekadu M, Yenit MK, Lakew AM. The prevalence of asymptomatic malaria parasitemia and associated factors among adults in Dembia district, northwest Ethiopia, 2017. Arch Public Health. 2018;76:74.CrossRefPubMedPubMedCentral
16.
go back to reference Oladeinde BH, Omoregie R, Osakue EO, Onaiwu TO. Asymptomatic Malaria among Blood Donors in Benin City Nigeria. Iran J Parasitol. 2014;9:415–22.PubMedPubMedCentral Oladeinde BH, Omoregie R, Osakue EO, Onaiwu TO. Asymptomatic Malaria among Blood Donors in Benin City Nigeria. Iran J Parasitol. 2014;9:415–22.PubMedPubMedCentral
17.
go back to reference WHO. World Malaria Report 2005. Geneva, World Health Organization and UNICEF; 2005. WHO. World Malaria Report 2005. Geneva, World Health Organization and UNICEF; 2005.
18.
go back to reference WHO. World Malaria Report 2010. Geneva, World Health Organization, 2010. WHO. World Malaria Report 2010. Geneva, World Health Organization, 2010.
19.
go back to reference Ministry of Health. The Uganda Malaria Reduction Strategic Plan 2014-2020. Uganda: Kampala; 2014. Ministry of Health. The Uganda Malaria Reduction Strategic Plan 2014-2020. Uganda: Kampala; 2014.
20.
go back to reference Uganda Bureau of Statistics (UBOS) and Macro International Inc. Uganda Demographic and Health Survey 2006. Calverton, Maryland, USA: 2007. Uganda Bureau of Statistics (UBOS) and Macro International Inc. Uganda Demographic and Health Survey 2006. Calverton, Maryland, USA: 2007.
21.
go back to reference Ministry of Health. Uganda National Malaria Control Strategyic Plan 2010/11 - 2014/15. Uganda: Kampala; 2011. Ministry of Health. Uganda National Malaria Control Strategyic Plan 2010/11 - 2014/15. Uganda: Kampala; 2011.
22.
go back to reference Wanzira H, Katamba H, Rubahika D. Use of long-lasting insecticide-treated bed nets in a population with universal coverage following a mass distribution campaign in Uganda. Malar J. 2016;15:311.CrossRefPubMedPubMedCentral Wanzira H, Katamba H, Rubahika D. Use of long-lasting insecticide-treated bed nets in a population with universal coverage following a mass distribution campaign in Uganda. Malar J. 2016;15:311.CrossRefPubMedPubMedCentral
23.
go back to reference Ministry of Health. Annual Health Sector Performance Report - FY 2010/2011. Uganda: Kampala; 2011. Ministry of Health. Annual Health Sector Performance Report - FY 2010/2011. Uganda: Kampala; 2011.
24.
go back to reference Uganda Bureau of Statistics, NMCP. Uganda malaria indicator survey 2014-15. Kampala, Uganda, and Rockville, Maryland, 2015. Uganda Bureau of Statistics, NMCP. Uganda malaria indicator survey 2014-15. Kampala, Uganda, and Rockville, Maryland, 2015.
25.
go back to reference Ministry of Health. Annual Health Sector Performance Report - FY 2016/2017. Uganda: Kampala; 2017. Ministry of Health. Annual Health Sector Performance Report - FY 2016/2017. Uganda: Kampala; 2017.
26.
go back to reference Ssempiira J, Kissa J, Nambuusi B, Kyozira C, Rutazaana D, Mukooyo E, et al. The effect of case management and vector-control interventions on space-time patterns of malaria incidence in Uganda. Malar J. 2018;17:162.CrossRefPubMedPubMedCentral Ssempiira J, Kissa J, Nambuusi B, Kyozira C, Rutazaana D, Mukooyo E, et al. The effect of case management and vector-control interventions on space-time patterns of malaria incidence in Uganda. Malar J. 2018;17:162.CrossRefPubMedPubMedCentral
27.
go back to reference Ministry of Health. Annual Health Sector Performance Report - FY 2014/2015. Uganda: Kampala; 2015. Ministry of Health. Annual Health Sector Performance Report - FY 2014/2015. Uganda: Kampala; 2015.
28.
go back to reference Uganda Bureau of Statistics, NMCP. Uganda Malaria Indicator Survey. Calverton, Maryland. USA: UBOS and ICF Macro; 2009. p. 2010. Uganda Bureau of Statistics, NMCP. Uganda Malaria Indicator Survey. Calverton, Maryland. USA: UBOS and ICF Macro; 2009. p. 2010.
29.
go back to reference Sserwanga A, Harris JC, Kigozi R, Menon M, Bukirwa H, Gasasira A, et al. Improved malaria case management through the implementation of a health facility-based sentinel site surveillance system in Uganda. PLoS ONE. 2011;6:e16316.CrossRefPubMedPubMedCentral Sserwanga A, Harris JC, Kigozi R, Menon M, Bukirwa H, Gasasira A, et al. Improved malaria case management through the implementation of a health facility-based sentinel site surveillance system in Uganda. PLoS ONE. 2011;6:e16316.CrossRefPubMedPubMedCentral
30.
go back to reference Kigozi R, Baxi SM, Gasasira A, Sserwanga A, Kakeeto S, Nasr S, et al. Indoor residual spraying of insecticide and malaria morbidity in a high transmission intensity area of Uganda. PLoS ONE. 2012;7:e42857.CrossRefPubMedPubMedCentral Kigozi R, Baxi SM, Gasasira A, Sserwanga A, Kakeeto S, Nasr S, et al. Indoor residual spraying of insecticide and malaria morbidity in a high transmission intensity area of Uganda. PLoS ONE. 2012;7:e42857.CrossRefPubMedPubMedCentral
31.
go back to reference Okello PE, Van Bortel W, Byaruhanga AM, Correwyn A, Roelants P, Talisuna A, et al. Variation in malaria transmission intensity in seven sites throughout Uganda. Am J Trop Med Hyg. 2006;75:219–25.CrossRefPubMed Okello PE, Van Bortel W, Byaruhanga AM, Correwyn A, Roelants P, Talisuna A, et al. Variation in malaria transmission intensity in seven sites throughout Uganda. Am J Trop Med Hyg. 2006;75:219–25.CrossRefPubMed
33.
go back to reference Teklehaimanot A, Sachs JD, Curtis C. Malaria control needs mass distribution of insecticidal bednets. Lancet. 2007;369:2143–6.CrossRefPubMed Teklehaimanot A, Sachs JD, Curtis C. Malaria control needs mass distribution of insecticidal bednets. Lancet. 2007;369:2143–6.CrossRefPubMed
34.
go back to reference Katureebe A, Zinszer K, Arinaitwe E, Rek J, Kakande E, Charland K, et al. Measures of malaria burden after long-lasting insecticidal net distribution and indoor residual spraying at three sites in Uganda: a prospective observational study. PLoS Med. 2016;13:e1002167.CrossRefPubMedPubMedCentral Katureebe A, Zinszer K, Arinaitwe E, Rek J, Kakande E, Charland K, et al. Measures of malaria burden after long-lasting insecticidal net distribution and indoor residual spraying at three sites in Uganda: a prospective observational study. PLoS Med. 2016;13:e1002167.CrossRefPubMedPubMedCentral
36.
go back to reference Team RC. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing; 2018. Team RC. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing; 2018.
37.
go back to reference Raouf S, Mpimbaza A, Kigozi R, Sserwanga A, Rubahika D, Katamba H, et al. Resurgence of malaria following discontinuation of indoor residual spraying of insecticide in an area of Uganda with previously high-transmission intensity. Clin Infect Dis. 2017;65:453–60.CrossRefPubMedPubMedCentral Raouf S, Mpimbaza A, Kigozi R, Sserwanga A, Rubahika D, Katamba H, et al. Resurgence of malaria following discontinuation of indoor residual spraying of insecticide in an area of Uganda with previously high-transmission intensity. Clin Infect Dis. 2017;65:453–60.CrossRefPubMedPubMedCentral
38.
go back to reference O’Meara WP, Mangeni JN, Steketee R, Greenwood B. Changes in the burden of malaria in sub-Saharan Africa. Lancet Infect Dis. 2010;10:545–55.CrossRefPubMed O’Meara WP, Mangeni JN, Steketee R, Greenwood B. Changes in the burden of malaria in sub-Saharan Africa. Lancet Infect Dis. 2010;10:545–55.CrossRefPubMed
39.
go back to reference Farnert A, Yman V, Homann MV, Wandell G, Mhoja L, Johansson M, et al. Epidemiology of malaria in a village in the Rufiji River Delta, Tanzania: declining transmission over 25 years revealed by different parasitological metrics. Malar J. 2014;13:459.CrossRefPubMedPubMedCentral Farnert A, Yman V, Homann MV, Wandell G, Mhoja L, Johansson M, et al. Epidemiology of malaria in a village in the Rufiji River Delta, Tanzania: declining transmission over 25 years revealed by different parasitological metrics. Malar J. 2014;13:459.CrossRefPubMedPubMedCentral
40.
go back to reference Vliegenthart-Jongbloed K, de Mendonca Melo M, van Wolfswinkel ME, Koelewijn R, van Hellemond JJ, van Genderen PJ. Severity of imported malaria: protective effect of taking malaria chemoprophylaxis. Malar J. 2013;12:265.CrossRefPubMedPubMedCentral Vliegenthart-Jongbloed K, de Mendonca Melo M, van Wolfswinkel ME, Koelewijn R, van Hellemond JJ, van Genderen PJ. Severity of imported malaria: protective effect of taking malaria chemoprophylaxis. Malar J. 2013;12:265.CrossRefPubMedPubMedCentral
41.
go back to reference O’Meara WP, Bejon P, Mwangi TW, Okiro EA, Peshu N, Snow RW, et al. Effect of a fall in malaria transmission on morbidity and mortality in Kilifi. Kenya. Lancet. 2008;372:1555–62.CrossRefPubMed O’Meara WP, Bejon P, Mwangi TW, Okiro EA, Peshu N, Snow RW, et al. Effect of a fall in malaria transmission on morbidity and mortality in Kilifi. Kenya. Lancet. 2008;372:1555–62.CrossRefPubMed
42.
go back to reference Ferrari G, Ntuku HM, Ross A, Schmidlin S, Kalemwa DM, Tshefu AK, et al. Identifying risk factors for Plasmodium infection and anaemia in Kinshasa. Democratic Republic of Congo. Malar J. 2016;15:362.PubMed Ferrari G, Ntuku HM, Ross A, Schmidlin S, Kalemwa DM, Tshefu AK, et al. Identifying risk factors for Plasmodium infection and anaemia in Kinshasa. Democratic Republic of Congo. Malar J. 2016;15:362.PubMed
43.
go back to reference Arinaitwe E, Dorsey G, Nankabirwa JI, Kigozi SP, Katureebe A, Kakande E, et al. Association between recent overnight travel and risk of malaria: a prospective cohort study at three sites in Uganda. Clin Infect Dis. 2018;68:313–20.CrossRefPubMedCentral Arinaitwe E, Dorsey G, Nankabirwa JI, Kigozi SP, Katureebe A, Kakande E, et al. Association between recent overnight travel and risk of malaria: a prospective cohort study at three sites in Uganda. Clin Infect Dis. 2018;68:313–20.CrossRefPubMedCentral
44.
go back to reference Mutegeki E, Chimbari MJ, Mukaratirwa S. Assessment of individual and household malaria risk factors among women in a South African village. Acta Trop. 2017;175:71–7.CrossRefPubMed Mutegeki E, Chimbari MJ, Mukaratirwa S. Assessment of individual and household malaria risk factors among women in a South African village. Acta Trop. 2017;175:71–7.CrossRefPubMed
45.
go back to reference Lowa M, Sitali L, Siame M, Musonda P. Human mobility and factors associated with malaria importation in Lusaka district, Zambia: a descriptive cross sectional study. Malar J. 2018;17:404.CrossRefPubMedPubMedCentral Lowa M, Sitali L, Siame M, Musonda P. Human mobility and factors associated with malaria importation in Lusaka district, Zambia: a descriptive cross sectional study. Malar J. 2018;17:404.CrossRefPubMedPubMedCentral
46.
go back to reference Erhart A, Ngo DT, Phan VK, Ta TT, Van Overmeir C, Speybroeck N, et al. Epidemiology of forest malaria in central Vietnam: a large scale cross-sectional survey. Malar J. 2005;4:58.CrossRefPubMedPubMedCentral Erhart A, Ngo DT, Phan VK, Ta TT, Van Overmeir C, Speybroeck N, et al. Epidemiology of forest malaria in central Vietnam: a large scale cross-sectional survey. Malar J. 2005;4:58.CrossRefPubMedPubMedCentral
47.
go back to reference Yang Y, Liu Y, Xie Z, Wu S, Yang L, Li W, et al. Epidemiology of malaria in Yulin, South China 1999-2016: imported malaria threatens zero local case status. Vector Borne Zoonotic Dis. 2018;18:533–8.CrossRefPubMed Yang Y, Liu Y, Xie Z, Wu S, Yang L, Li W, et al. Epidemiology of malaria in Yulin, South China 1999-2016: imported malaria threatens zero local case status. Vector Borne Zoonotic Dis. 2018;18:533–8.CrossRefPubMed
48.
go back to reference Janko MM, Irish SR, Reich BJ, Peterson M, Doctor SM, Mwandagalirwa MK, et al. The links between agriculture, Anopheles mosquitoes, and malaria risk in children younger than 5 years in the Democratic Republic of the Congo: a population-based, cross-sectional, spatial study. Lancet Planet Health. 2018;2:e74–82.CrossRefPubMedPubMedCentral Janko MM, Irish SR, Reich BJ, Peterson M, Doctor SM, Mwandagalirwa MK, et al. The links between agriculture, Anopheles mosquitoes, and malaria risk in children younger than 5 years in the Democratic Republic of the Congo: a population-based, cross-sectional, spatial study. Lancet Planet Health. 2018;2:e74–82.CrossRefPubMedPubMedCentral
49.
go back to reference Naidoo S, London L, Burdorf A, Naidoo RN, Kromhout H. Occupational activities associated with a reported history of malaria among women working in small-scale agriculture in South Africa. Am J Trop Med Hyg. 2011;85:805–10.CrossRefPubMedPubMedCentral Naidoo S, London L, Burdorf A, Naidoo RN, Kromhout H. Occupational activities associated with a reported history of malaria among women working in small-scale agriculture in South Africa. Am J Trop Med Hyg. 2011;85:805–10.CrossRefPubMedPubMedCentral
50.
go back to reference Kigozi SP, Pindolia DK, Smith DL, Arinaitwe E, Katureebe A, Kilama M, et al. Associations between urbanicity and malaria at local scales in Uganda. Malar J. 2015;14:374.CrossRefPubMedPubMedCentral Kigozi SP, Pindolia DK, Smith DL, Arinaitwe E, Katureebe A, Kilama M, et al. Associations between urbanicity and malaria at local scales in Uganda. Malar J. 2015;14:374.CrossRefPubMedPubMedCentral
52.
go back to reference Woldu DO, Haile ZT. Gender roles and perceptions of malaria risk in agricultural communities of Mwea Division in Central Kenya. Women Health. 2015;55:227–43.CrossRefPubMed Woldu DO, Haile ZT. Gender roles and perceptions of malaria risk in agricultural communities of Mwea Division in Central Kenya. Women Health. 2015;55:227–43.CrossRefPubMed
53.
go back to reference Essendi WM, Vardo-Zalik AM, Lo E, Machani MG, Zhou G, Githeko AK, et al. Epidemiological risk factors for clinical malaria infection in the highlands of Western Kenya. Malar J. 2019;18:211.CrossRefPubMedPubMedCentral Essendi WM, Vardo-Zalik AM, Lo E, Machani MG, Zhou G, Githeko AK, et al. Epidemiological risk factors for clinical malaria infection in the highlands of Western Kenya. Malar J. 2019;18:211.CrossRefPubMedPubMedCentral
54.
go back to reference Laban NM, Kobayashi T, Hamapumbu H, Sullivan D, Mharakurwa S, Thuma PE, et al. Comparison of a PfHRP2-based rapid diagnostic test and PCR for malaria in a low prevalence setting in rural southern Zambia: implications for elimination. Malar J. 2015;14:25.CrossRefPubMedPubMedCentral Laban NM, Kobayashi T, Hamapumbu H, Sullivan D, Mharakurwa S, Thuma PE, et al. Comparison of a PfHRP2-based rapid diagnostic test and PCR for malaria in a low prevalence setting in rural southern Zambia: implications for elimination. Malar J. 2015;14:25.CrossRefPubMedPubMedCentral
55.
go back to reference Hawley WA, Phillips-Howard PA, ter Kuile FO, Terlouw DJ, Vulule JM, Ombok M, et al. Community-wide effects of permethrin-treated bed nets on child mortality and malaria morbidity in western Kenya. Am J Trop Med Hyg. 2003;68:121–7.CrossRefPubMed Hawley WA, Phillips-Howard PA, ter Kuile FO, Terlouw DJ, Vulule JM, Ombok M, et al. Community-wide effects of permethrin-treated bed nets on child mortality and malaria morbidity in western Kenya. Am J Trop Med Hyg. 2003;68:121–7.CrossRefPubMed
Metadata
Title
Rapid shifts in the age-specific burden of malaria following successful control interventions in four regions of Uganda
Authors
Simon P. Kigozi
Ruth N. Kigozi
Adrienne Epstein
Arthur Mpimbaza
Asadu Sserwanga
Adoke Yeka
Joaniter I. Nankabirwa
Katherine Halliday
Rachel L. Pullan
Damian Rutazaana
Catherine M. Sebuguzi
Jimmy Opigo
Moses R. Kamya
Sarah G. Staedke
Grant Dorsey
Bryan Greenhouse
Isabel Rodriguez-Barraquer
Publication date
01-12-2020
Publisher
BioMed Central
Keyword
Malaria
Published in
Malaria Journal / Issue 1/2020
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-020-03196-7

Other articles of this Issue 1/2020

Malaria Journal 1/2020 Go to the issue
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.