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House Structure Is Associated with Plasmodium falciparum Infection in a Low-Transmission Setting in Southern Zambia
Matthew M. Ippolito
Matthew M. Ippolito
Divisions of Infectious Diseases and Clinical Pharmacology, Department of Medicine, Johns Hopkins University School of Medicine, Baltimore, Maryland;
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Kelly M. Searle
Kelly M. Searle
Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland;
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Harry Hamapumbu
Harry Hamapumbu
Macha Research Trust, Macha Hospital, Choma District, Zambia;
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Timothy M. Shields
Timothy M. Shields
Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland;
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Jennifer C. Stevenson
Jennifer C. Stevenson
Macha Research Trust, Macha Hospital, Choma District, Zambia;
The W. Harry Feinstone Department of Molecular Microbiology and Immunology, The Johns Hopkins Malaria Research Institute, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland
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The W. Harry Feinstone Department of Molecular Microbiology and Immunology, The Johns Hopkins Malaria Research Institute, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland
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Philip E. Thuma
Philip E. Thuma
The W. Harry Feinstone Department of Molecular Microbiology and Immunology, The Johns Hopkins Malaria Research Institute, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland
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William J. Moss
William J. Moss
Macha Research Trust, Macha Hospital, Choma District, Zambia;
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for the Southern Africa International Center of Excellence for Malaria Research
for the Southern Africa International Center of Excellence for Malaria Research
Divisions of Infectious Diseases and Clinical Pharmacology, Department of Medicine, Johns Hopkins University School of Medicine, Baltimore, Maryland;
Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland;
Macha Research Trust, Macha Hospital, Choma District, Zambia;
The W. Harry Feinstone Department of Molecular Microbiology and Immunology, The Johns Hopkins Malaria Research Institute, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland
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Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland;
Macha Research Trust, Macha Hospital, Choma District, Zambia;
The W. Harry Feinstone Department of Molecular Microbiology and Immunology, The Johns Hopkins Malaria Research Institute, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland
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House structure may influence the risk of malaria by affecting mosquito entry and indoor resting. Identification of construction features associated with protective benefits could inform vector control approaches, even in low-transmission settings. We examined the association between house structure and malaria prevalence in a cross-sectional analysis of 2,788 children and adults residing in 866 houses in a low-transmission area of Southern Province, Zambia, over the period 2008–2012. Houses were categorized according to wall (brick/cement block or mud/grass) and roof (metal or grass) material. Malaria was assessed by point-of-care rapid diagnostic test (RDT) for Plasmodium falciparum. We identified 52 RDT-positive individuals residing in 41 houses, indicating an overall prevalence in the sample of 1.9%, ranging from 1.4% to 8.8% among the different house types. Occupants of higher quality houses had reduced odds of P. falciparum malaria compared with those in the lowest quality houses after controlling for bed net use, indoor insecticide spraying, clustering by house, cohabitation with another RDT-positive individual, transmission season, ecologic risk defined as nearest distance to a Strahler-classified third-order stream, education, age, and gender (adjusted odds ratio [OR]: 0.26, 95% confidence interval [CI]: 0.09–0.73, P = 0.01 for houses with brick/cement block walls and metal roof; OR: 0.22, 95% CI: 0.09–0.52, P < 0.01 for houses with brick/cement block walls and grass roof). Housing improvements offer a promising approach to vector control in low-transmission settings that circumvents the threat posed by insecticide resistance, and may confer a protective benefit of similar magnitude to current vector control strategies.
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Author Notes
Authors’ addresses: Matthew M. Ippolito, Divisions of Infectious Diseases and Clinical Pharmacology, Department of Medicine, Johns Hopkins University School of Medicine, Baltimore, MD, E-mail: mippolito@jhu.edu. Kelly M. Searle, Timothy M. Shields, and William J. Moss, Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, E-mails: ksearle1@jhu.edu, tshields@jhu.edu, and wmoss1@jhu.edu. Harry Hamapumbu and Philip E. Thuma, Macha Research Trust, Macha Hospital, Choma District, Zambia, E-mails: harry.hamapumbu@macharesearch.org and phil.thuma@macharesearch.org. Jennifer C. Stevenson, The W. Harry Feinstone Department of Molecular Microbiology and Immunology, Johns Hopkins Malaria Research Institute, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, and Macha Research Trust, Macha Hospital, Choma District, Zambia, E-mail: jennyc.stevenson@macharesearch.org.
Financial support: This work was supported by the Johns Hopkins Malaria Research Institute, the Bloomberg Family Foundation, and the Division of Microbiology and Infectious Diseases, National Institute of Allergy and Infectious Diseases as part of the International Centers of Excellence for Malaria Research (U19AI089680). Matthew M. Ippolito was additionally supported by the National Institute of General Medical Sciences (T32GM066691) and the Sherrilyn and Ken Fisher Center for Environmental Infectious Diseases, Division of Infectious Diseases of the Johns Hopkins University School of Medicine.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Bhatt S et al. 2015. The effect of malaria control on Plasmodium falciparum in Africa between 2000 and 2015. Nature 526: 207–211.
-
2.
World Health Organzation, 2015. World Malaria Report. Geneva, Switzerland: WHO Global Malaria Programme.
-
3.
Reyburn H, 2010. New WHO guidelines for the treatment of malaria. BMJ 340: c2637.
-
4.
Quinones ML et al. 2015. Insecticide resistance in areas under investigation by the International Centers of Excellence for Malaria Research: a challenge for malaria control and elimination. Am J Trop Med Hyg 93: 69–78.
-
5.
Huho B, et al., 2013. Consistently high estimates for the proportion of human exposure to malaria vector populations occurring indoors in rural Africa. Int J Epidemiol 42: 235–247.
-
6.
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.
-
7.
Tusting LS, Bottomley C, Gibson H, Kleinschmidt I, Tatem AJ, Lindsay SW, Gething PW, 2017. Housing improvements and malaria risk in sub-Saharan Africa: a multi-country analysis of survey data. PLoS Med 14: e1002234.
-
8.
Lane C, 1931. Housing and Malaria: A Critical Summary of the Literature Dealing with This Subject. Geneva, Switzerland: League of Nations: Health Organisation.
-
9.
Celli A, 1900. The new prophylaxis against malaria in Lazio. Lancet 156: 1603–1606.
-
10.
Harrison G, 1978. Mosquitoes, Malaria, and Man: A History of the Hostilities Since 1880. Dutton.
-
11.
Ogoma SB, Lweitoijera DW, Ngonyani H, Furer B, Russell TL, Mukabana WR, Killeen GF, Moore SJ, 2010. Screening mosquito house entry points as a potential method for integrated control of endophagic filariasis, arbovirus and malaria vectors. PLoS Negl Trop Dis 4: e773.
-
12.
Massebo F, Lindtjorn B, 2013. The effect of screening doors and windows on indoor density of Anopheles arabiensis in south-west Ethiopia: a randomized trial. Malar J 12: 319.
-
13.
Kirby MJ, Ameh D, Bottomley C, Green C, Jawara M, Milligan PJ, Snell PC, Conway DJ, Lindsay SW, 2009. Effect of two different house screening interventions on exposure to malaria vectors and on anaemia in children in The Gambia: a randomised controlled trial. Lancet 374: 998–1009.
-
14.
Kampango A, Braganca M, Sousa B, Charlwood JD, 2013. Netting barriers to prevent mosquito entry into houses in southern Mozambique: a pilot study. Malar J 12: 99.
-
15.
Adiamah JH, Koram KA, Thomson MC, Lindsay SW, Todd J, Greenwood BM, 1993. Entomological risk factors for severe malaria in a peri-urban area of The Gambia. Ann Trop Med Parasitol 87: 491–500.
-
16.
Koram KA, Bennett S, Adiamah JH, Greenwood BM, 1995. Socio-economic determinants are not major risk factors for severe malaria in Gambian children. Trans R Soc Trop Med Hyg 89: 151–154.
-
17.
Brooker S, Clarke S, Njagi JK, Polack S, Mugo B, Estambale B, Muchiri E, Magnussen P, Cox J, 2004. Spatial clustering of malaria and associated risk factors during an epidemic in a highland area of western Kenya. Trop Med Int Health 9: 757–766.
-
18.
Nkuo-Akenji T, Ntonifor NN, Ndukum MB, Abongwa EL, Nkwescheu A, Anong DN, Songmbe M, Boyo MG, Ndamukong KN, Titanji VP, 2006. Environmental factors affecting malaria parasite prevalence in rural Bolifamba, South West Cameroon. Afr J Health Sci 13: 40–46.
-
19.
Somi MF, Butler JR, Vahid F, Njau J, Kachur SP, Abdulla S, 2007. Is there evidence for dual causation between malaria and socioeconomic status? Findings from rural Tanzania. Am J Trop Med Hyg 77: 1020–1027.
-
20.
Ernst KC, Lindblade KA, Koech D, Sumba PO, Kuwuor DO, John CC, Wilson ML, 2009. Environmental, socio-demographic and behavioural determinants of malaria risk in the western Kenyan highlands: a case-control study. Trop Med Int Health 14: 1258–1265.
-
21.
Siri JG, Wilson ML, Murray S, Rosen DH, Vulule JM, Slutsker L, Lindblade KA, 2010. Significance of travel to rural areas as a risk factor for malarial anemia in an urban setting. Am J Trop Med Hyg 82: 391–397.
-
22.
Yamamoto S, Louis VR, Sie A, Sauerborn R, 2010. Household risk factors for clinical malaria in a semi-urban area of Burkina Faso: a case-control study. Trans R Soc Trop Med Hyg 104: 61–65.
-
23.
Winskill P, Rowland M, Mtove G, Malima RC, Kirby MJ, 2011. Malaria risk factors in north-east Tanzania. Malar J 10: 98.
-
24.
Yukich JO, Taylor C, Eisele TP, Reithinger R, Nauhassenay H, Berhane Y, Keating J, 2013. Travel history and malaria infection risk in a low-transmission setting in Ethiopia: a case control study. Malar J 12: 33.
-
25.
Magalhaes RJ, Langa A, Sousa-Figueiredo JC, Clements AC, Nery SV, 2012. Finding malaria hot-spots in northern Angola: the role of individual, household and environmental factors within a meso-endemic area. Malar J 11: 385.
-
26.
Townes LR, Mwandama D, Mathanga DP, Wilson ML, 2013. Elevated dry-season malaria prevalence associated with fine-scale spatial patterns of environmental risk: a case-control study of children in rural Malawi. Malar J 12: 407.
-
27.
Tilaye T, Deressa W, 2007. Prevalence of urban malaria and associated factors in Gondar Town, Northwest Ethiopia. Ethiop Med J 45: 151–158.
-
28.
Ong’echa JM et al. 2006. Parasitemia, anemia, and malarial anemia in infants and young children in a rural holoendemic Plasmodium falciparum transmission area. Am J Trop Med Hyg 74: 376–385.
-
29.
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.
-
30.
Bousema T et al. 2010. Identification of hot spots of malaria transmission for targeted malaria control. J Infect Dis 201: 1764–1774.
-
31.
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.
-
32.
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.
-
33.
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.
-
34.
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.
-
35.
Rulisa S et al. 2013. Malaria prevalence, spatial clustering and risk factors in a low endemic area of eastern Rwanda: a cross sectional study. PLoS One 8: e69443.
-
36.
Wanzirah H et al. 2015. Mind the gap: house structure and the risk of malaria in Uganda. PLoS One 10: e0117396.
-
37.
Ghebreyesus TA, Haile M, Witten KH, Getachew A, Yohannes M, Lindsay SW, Byass P, 2000. Household risk factors for malaria among children in the Ethiopian highlands. Trans R Soc Trop Med Hyg 94: 17–21.
-
38.
Snyman K et al. 2015. Poor housing construction associated with increased malaria incidence in a cohort of young Ugandan children. Am J Trop Med Hyg 92: 1207–1213.
-
39.
Sutcliffe CG, Kobayashi T, Hamapumbu H, Shields T, Mharakurwa S, Thuma PE, Louis TA, Glass G, Moss WJ, 2012. Reduced risk of malaria parasitemia following household screening and treatment: a cross-sectional and longitudinal cohort study. PLoS One 7: e31396.
-
40.
Moss WJ et al. 2015. Malaria epidemiology and control within the International Centers of Excellence for Malaria Research. Am J Trop Med Hyg 93: 5–15.
-
41.
Chanda E, Kamuliwo M, Steketee RW, Macdonald MB, Babaniyi O, Mukonka VM, 2013. An overview of the malaria control programme in Zambia. ISRN Prev Med 2013: 495037.
-
42.
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.
-
43.
Moss WJ, Norris DE, Mharakurwa S, Scott A, Mulenga M, Mason PR, Chipeta J, Thuma PE, Southern Africa IT, 2012. Challenges and prospects for malaria elimination in the southern Africa region. Acta Trop 121: 207–211.
-
44.
Moss WJ, Hamapumbu H, Kobayashi T, Shields T, Kamanga A, Clennon J, Mharakurwa S, Thuma PE, Glass G, 2011. Use of remote sensing to identify spatial risk factors for malaria in a region of declining transmission: a cross-sectional and longitudinal community survey. Malar J 10: 163.
-
45.
Lengeler C, 2004. Insecticide-treated bed nets and curtains for preventing malaria. Cochrane Database Syst Rev CD000363.
-
46.
Pluess B, Tanser FC, Lengeler C, Sharp BL, 2010. Indoor residual spraying for preventing malaria. Cochrane Database Syst Rev CD006657.
-
47.
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.
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