Lane C, 1931. Housing and Malaria: A Critical Summary of the Literature Dealing with This Subject. Geneva, Switzerland: League of Nations, Health Organisation.
Celli A, 1900. The new prophylaxis against malaria in Lazio. Lancet 156: 1603–1606.
Tusting LS, Ippolito MM, Willey BA, Kleinschmidt I, Dorsey G, Gosling RD, Lindsay SW, 2015. The evidence for improving housing to reduce malaria: a systematic review and meta-analysis. Malar J 14: 209.
Furnival-Adams J, Olanga EA, Napier M, Garner P, 2020. House modifications for preventing malaria. Cochrane Database Syst Rev 10: CD013398.
Mukonka VM et al. 2014. High burden of malaria following scale-up of control interventions in Nchelenge district, Luapula province, Zambia. Malar J 13: 153.
Eisele TP et al. 2016. Short-term impact of mass drug administration with dihydroartemisinin plus piperaquine on malaria in southern province Zambia: a cluster-randomized controlled trial. J Infect Dis 214: 1831–1839.
Moss WJ et al. 2015. Malaria epidemiology and control within the international centers of excellence for malaria research. Am J Trop Med Hyg 93 (Suppl 3): 5–15.
Chanda E, Kamuliwo M, Steketee RW, Macdonald MB, Babaniyi O, Mukonka VM, 2012. An overview of the malaria control programme in Zambia. ISRN Prev Med 2013: 495037.
Chizema-Kawesha E, Miller JM, Steketee RW, Mukonka VM, Mukuka C, Mohamed AD, Miti SK, Campbell CC, 2010. Scaling up malaria control in Zambia: progress and impact 2005–2008. Am J Trop Med Hyg 83: 480–488.
Kent RJ, Thuma PE, Mharakurwa S, Norris DE, 2007. Seasonality, blood feeding behavior, and transmission of Plasmodium falciparum by Anopheles arabiensis after an extended drought in southern Zambia. Am J Trop Med Hyg 76: 267–274.
Ippolito MM, Searle KM, Hamapumbu H, Shields TM, Stevenson JC, Thuma PE, Moss WJ; For The Southern Africa International Center Of Excellence For Malaria Research, 2017. House structure is associated with Plasmodium falciparum infection in a low-transmission setting in southern Zambia. Am J Trop Med Hyg 97: 1561–1567.
Paaijmans KP, Thomas MB, 2011. The influence of mosquito resting behaviour and associated microclimate for malaria risk. Malar J 10: 183.
Kirby MJ, West P, Green C, Jasseh M, Lindsay SW, 2008. Risk factors for house-entry by culicine mosquitoes in a rural town and satellite villages in the Gambia. Parasit Vectors 1: 41.
Lindsay SW, Snow RW, 1988. The trouble with eaves; house entry by vectors of malaria. Trans R Soc Trop Med Hyg 82: 645–646.
Njie M, Dilger E, Lindsay SW, Kirby MJ, 2009. Importance of eaves to house entry by anopheline, but not culicine, mosquitoes. J Med Entomol 46: 505–510.
Lindsay SW et al. 2019. Reduced mosquito survival in metal-roof houses may contribute to a decline in malaria transmission in sub-Saharan Africa. Sci Rep 9: 7770.
Jatta E, Jawara M, Bradley J, Jeffries D, Kandeh B, Knudsen JB, Wilson AL, Pinder M, D'Alessandro U, Lindsay SW, 2018. How house design affects malaria mosquito density, temperature, and relative humidity: an experimental study in rural Gambia. Lancet Planet Health 2: e498–e508.
Lahondere C, Lazzari CR, 2012. Mosquitoes cool down during blood feeding to avoid overheating. Curr Biol 22: 40–45.
Iwashita H, Dida G, Futami K, Kaneko S, Horio M, Kawada H, Maekawa Y, Aoki Y, Minakawa N, 2010. Sleeping arrangement and house structure affect bed net use in villages along Lake Victoria. Malar J 9: 176.
Correa A, Galardo AKR, Lima LA, Câmara DCP, Müller JN, Barroso JFS, Lapouble OMM, Rodovalho CM, Ribeiro KAN, Lima JBP, 2019. Efficacy of insecticides used in indoor residual spraying for malaria control: an experimental trial on various surfaces in a “test house”. Malar J 18: 345.
Desalegn Z, Wegayehu T, Massebo F, 2018. Wall-type and indoor residual spraying application quality affect the residual efficacy of indoor residual spray against wild malaria vector in southwest Ethiopia. Malar J 17: 300.
Tusting LS, Willey B, Lucas H, Thompson J, Kafy HT, Smith R, Lindsay SW, 2013. Socioeconomic development as an intervention against malaria: a systematic review and meta-analysis. Lancet 382: 963–972.
Worrall E, Basu S, Hanson K, 2005. Is malaria a disease of poverty? A review of the literature. Trop Med Int Health 10: 1047–1059.
Griliches Z, Mason WM, 1972. Education, income, and ability. J Political Economy 80: S74–S103.
Ahmed SM, Haque R, Haque U, Hossain A, 2009. Knowledge on the transmission, prevention and treatment of malaria among two endemic populations of Bangladesh and their health-seeking behaviour. Malar J 8: 173.
Gingrich CD, Hanson K, Marchant T, Mulligan JA, Mponda H, 2011. Price subsidies and the market for mosquito nets in developing countries: a study of Tanzania’s discount voucher scheme. Soc Sci Med 73: 160–168.
Hanson K, Worrall E, 2002. Social Marketing of Insecticide Treated Nets – Phase 2 (SMITN2), Tanzania: End of Project Household Survey Analysis. London, United Kingdom: Malaria Consortium, 43.
Matovu F, Goodman C, Wiseman V, Mwengee W, 2009. How equitable is bed net ownership and utilisation in Tanzania? A practical application of the principles of horizontal and vertical equity. Malar J 8: 109.
Rashed S, Johnson H, Dongier P, Moreau R, Lee C, Lambert J, Schaefer C, 2000. Economic impact of febrile morbidity and use of permethrin-impregnated bed nets in a malarious area II. Determinants of febrile episodes and the cost of their treatment and malaria prevention. Am J Trop Med Hyg 62: 181–186.
Ziba C, Slutsker L, Chitsulo L, Steketee RW, 1994. Use of malaria prevention measures in Malawian households. Trop Med Parasitol 45: 70–73.
Barat LM, Palmer N, Basu S, Worrall E, Hanson K, Mills A, 2004. Do malaria control interventions reach the poor? A view through the equity lens. Am J Trop Med Hyg 71 (Suppl 2): 174–178.
Saaka M, Oosthuizen J, Beatty S, 2009. Effect of joint iron and zinc supplementation on malarial infection and anaemia. East Afr J Public Health 6: 55–62.
Babyak MA, 2009. Understanding confounding and mediation. Evid Based Ment Health 12: 68–71.
Imai K, Keele L, Tingley D, 2010. A general approach to causal mediation analysis. Psychol Methods 15: 309–334.
Handema R, Daka V, Chileshe J, Nambozi M, Kasongo W, 2018. Field evaluation of the illipro-10 illumigene malaria diagnostic by amplification of plasmodium spp. DNA. Am J Trop Med Hyg 99 (Suppl 4): 91.
Pinchoff J, Chaponda M, Shields TM, Sichivula J, Muleba M, Mulenga M, Kobayashi T, Curriero FC, Moss WJ; Southern Africa International Centers of Excellence for Malaria Research, 2016. Individual and household level risk factors associated with malaria in Nchelenge District, a region with perennial transmission: a serial cross-sectional study from 2012 to 2015. PLoS One 11: e0156717.
Das S, Muleba M, Stevenson JC, Norris DE, 2016. Habitat partitioning of malaria vectors in Nchelenge district, Zambia. Am J Trop Med Hyg 94: 1234–1244.
Stevenson JC et al. 2016. Spatio-temporal heterogeneity of malaria vectors in northern Zambia: implications for vector control. Parasit Vectors 9: 510.
Hast MA et al. 2019. The impact of 3 years of targeted indoor residual spraying with pirimiphos-methyl on malaria parasite prevalence in a high-transmission area of northern Zambia. Am J Epidemiol 188: 2120–2130.
Ippolito MM et al. 2018. Risk factors for mortality in children hospitalized with severe malaria in northern Zambia: a retrospective case-control study. Am J Trop Med Hyg 98: 1699–1704.
Kamau E, Tolbert LS, Kortepeter L, Pratt M, Nyakoe N, Muringo L, Ogutu B, Waitumbi JN, Ockenhouse CF, 2011. Development of a highly sensitive genus-specific quantitative reverse transcriptase real-time PCR assay for detection and quantitation of Plasmodium by amplifying RNA and DNA of the 18S rRNA genes. J Clin Microbiol 49: 2946–2953.
Taylor BJ, Lanke K, Banman SL, Morlais I, Morin MJ, Bousema T, Rijpma SR, Yanow SK, 2017. A direct from blood reverse transcriptase polymerase chain reaction assay for monitoring falciparum malaria parasite transmission in elimination settings. Am J Trop Med Hyg 97: 533–543.
Bousema T et al. 2010. Identification of hot spots of malaria transmission for targeted malaria control. J Infect Dis 201: 1764–1774.
Mmbando BP, Kamugisha ML, Lusingu JP, Francis F, Ishengoma DS, Theander TG, Lemnge MM, Scheike TH, 2011. Spatial variation and socio-economic determinants of Plasmodium falciparum infection in northeastern Tanzania. Malar J 10: 145.
Ouma P, van Eijk AM, Hamel MJ, Parise M, Ayisi JG, Otieno K, Kager PA, Slutsker L, 2007. Malaria and anaemia among pregnant women at first antenatal clinic visit in Kisumu, western Kenya. Trop Med Int Health 12: 1515–1523.
Rulisa S, Kateera F, Bizimana JP, Agaba S, Dukuzumuremyi J, Baas L, de Dieu Harelimana J, Mens PF, Boer KR, de Vries PJ, 2013. Malaria prevalence, spatial clustering and risk factors in a low endemic area of eastern Rwanda: a cross sectional study. PLoS One 8: e69443.
Sintasath DM, Ghebremeskel T, Lynch M, Kleinau E, Bretas G, Shililu J, Brantly E, Graves PM, Beier JC, 2005. Malaria prevalence and associated risk factors in Eritrea. Am J Trop Med Hyg 72: 682–687.
Temu EA, Coleman M, Abilio AP, Kleinschmidt I, 2012. High prevalence of malaria in Zambezia, Mozambique: the protective effect of IRS versus increased risks due to pig-keeping and house construction. PLoS One 7: e31409.
Wanzirah H et al. 2015. Mind the gap: house structure and the risk of malaria in Uganda. PLoS One 10: e0117396.
Ye Y, Hoshen M, Louis V, Seraphin S, Traore I, Sauerborn R, 2006. Housing conditions and Plasmodium falciparum infection: protective effect of iron-sheet roofed houses. Malar J 5: 8.
Ondiba IM, Oyieke FA, Ong’amo GO, Olumula MM, Nyamongo IK, Estambale BBA, 2018. Malaria vector abundance is associated with house structures in Baringo county, Kenya. PLoS One 13: e0198970.
Shapiro LLM, Whitehead SA, Thomas MB, 2017. Quantifying the effects of temperature on mosquito and parasite traits that determine the transmission potential of human malaria. PLoS Biol 15: e2003489.
Murdock CC, Sternberg ED, Thomas MB, 2016. Malaria transmission potential could be reduced with current and future climate change. Sci Rep 6: 27771.
Animut A, Balkew M, Lindtjorn B, 2013. Impact of housing condition on indoor-biting and indoor-resting Anopheles arabiensis density in a highland area, central Ethiopia. Malar J 12: 393.
Toe LP et al. 2009. Decreased motivation in the use of insecticide-treated nets in a malaria endemic area in Burkina Faso. Malar J 8: 175.
von Seidlein L, Ikonomidis K, Bruun R, Jawara M, Pinder M, Knols BG, Knudsen JB, 2012. Airflow attenuation and bed net utilization: observations from Africa and Asia. Malar J 11: 200.
Biritwum RB, Welbeck J, Barnish G, 2000. Incidence and management of malaria in two communities of different socio—economic level, in Accra, Ghana. Ann Trop Med Parasitol 94: 771–778.
Mugisha F, Kouyate B, Gbangou A, Sauerborn R, 2002. Examining out ‐ of ‐ pocket expenditure on health care in Nouna, Burkina Faso: implications for health policy. Trop Med Int Health 7: 187–196.
Kreuels B, Kobbe R, Adjei S, Kreuzberg C, von Reden C, Bäter K, Klug S, Busch W, Adjei O, May J, 2008. Spatial variation of malaria incidence in young children from a geographically homogeneous area with high endemicity. J Infect Dis 197: 85–93.
Pullan RL, Kabatereine NB, Bukirwa H, Staedke SG, Brooker S, 2011. Heterogeneities and consequences of Plasmodium species and hookworm coinfection: a population based study in Uganda. J Infect Dis 203: 406–417.
Slutsker L et al. 1996. Malaria infection in infancy in rural Malawi. Am J Trop Med Hyg 55 (Suppl 1): 71–76.
Fawole OI, Onadeko MO, 2001. Knowledge and home management of malaria fever by mothers and care givers of under five children. West Afr J Med 20: 152–157.
Nuwaha F, 2001. Factors influencing the use of bed nets in Mbarara municipality of Uganda. Am J Trop Med Hyg 65: 877–882.
Kaona F, Siajunza M, Manyando C, Khondowe S, Ngoma G, 2000. Utilisation of malarial drugs at a household level: results from a KAP study in Choma, southern province and Mporokoso, northern province of Zambia. Cent Afr J Med 46: 268–270.
Walldorf JA et al. 2015. School-age children are a reservoir of malaria infection in Malawi. PLoS One 10: e0134061.
Sergent E, Parrot LL, 1935. Immunité, la Prémunition et la Résistance Innée. Archives de l'Institut Pasteur d'Algérie, TXIII(279).
Ippolito MM, Chary A, Daniel M, Barnoya J, Monroe A, Eakin M, 2017. Expectations of health care quality among rural Maya villagers in Solola department, Guatemala: a qualitative analysis. Int J Equity Health 16: 51.
Molineaux L, Grammiccia G, 1980. The Garki Project: Research on the Epidemiology and Control of Malaria in the Sudan Savanna of West Africa. Geneva, Switzerland: World Health Organization.
Sachs J, Malaney P, 2002. The economic and social burden of malaria. Nature 415: 680–685.
Government of the Republic of Zambia, 2020. Zambia National Public Health Act. Act IX § 67. Lusaka, Zambia: National Assembly of Zambia.
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Since the late nineteenth century, the importance of house structure as a determinant of malaria risk has been recognized. Few studies to date have examined the association of housing and malaria in clinical populations. We conducted a cross-sectional study of febrile patients (n = 282) at two rural health clinics in a high malaria-transmission area of northern Zambia. Participants underwent testing for Plasmodium falciparum infection by PCR. Demographic and other risk factors including house structure, indoor residual spraying (IRS), bed net use, education level, and household income were collected. Data were fitted to logistic regression models for relational and mediation analyses. Residing in a house with a thatch roof was associated with higher odds of malaria than residing in a house with corrugated metal (odds ratio: 2.6; 95% CI: 1.0–6.3, P = 0.04). Lower income and educational attainment were also associated with greater odds of malaria. Living under a thatch roof accounted for 24% (95% CI: 14–82) of the effect of household income on malaria risk, and income accounted for 11% (95% CI: 8–19) of the effect of education. Neither IRS nor bed net use was associated with malaria risk despite large, local investments in these vector control interventions. The findings testify to malaria as a disease of rural poverty and contribute further evidence to the utility of housing improvements in vector control programs.
Disclosure: Data can be made available by the authors upon reasonable request. Verbal consent was obtained for photography.
Financial support: The parent study was funded by Meridian Bioscience (USA) and Sep Sci (Zambia). J. S., M. M., W. J. M., and M. M. I. were supported by the National Institutes of Health (U19AI089680). J. L. S. and M. M. I. were supported by the Johns Hopkins Malaria Research Institute and Bloomberg Philanthropies. M. M. I. was supported by the National Institutes of Health (K23AI139343), the Sherrilyn and Ken Fisher Center for Environmental Infectious Disease at Johns Hopkins University, and the Burroughs Wellcome Fund-American Society of Tropical Medicine and Hygiene Postdoctoral Fellowship in Tropical Infectious Diseases. The contents of this article are solely the responsibility of the authors and do not necessarily represent the official view of the Fisher Center or Johns Hopkins University School of Medicine.
Authors’ addresses: Jay Sikalima, Laboratory Tropical Medicine, Tropical Diseases Research Centre (TDRC), Ndola, Zambia, E-mail: firstname.lastname@example.org. Jessica L. Schue, Department of International Health, Johns Hopkins University Bloomberg School of Public Health, Baltimore, MD, E-mail: email@example.com. Sarah E. Hill, Johns Hopkins University School of Medicine, Baltimore, MD, E-mail: firstname.lastname@example.org. Modest Mulenga and Victor Daka, Department of Public Health, Copperbelt University, Ndola, Zambia, E-mails: email@example.com and firstname.lastname@example.org. Ray Handema and Webster Kasongo, Department of Clinical Research, TDRC, Ndola, Zambia, E-mails: email@example.com and firstname.lastname@example.org. Justin Chileshe, Department of Parasitology, Tropical Diseases Research Centre, Ndola, Zambia, E-mail: email@example.com. Mike Chaponda, Department of Health, Tropical Diseases Research Centre, Mansa, Zambia, E-mail: firstname.lastname@example.org. Jean-Bertin Bukasa Kabuya, Department of Health, Tropical Diseases Research Centre, Ndola, Zambia, E-mail: email@example.com. William J. Moss, Department of Epidemiology, Johns Hopkins University Bloomberg School of Public Health, Baltimore, MD, E-mail: firstname.lastname@example.org. Matthew M. Ippolito, Department of Medicine, Johns Hopkins University, Baltimore, MD, E-mail: email@example.com.