The evidence for improving housing to reduce malaria: a systematic review and meta-analysis

1Despite considerable advances in malaria control since 2000, with a 30 % fall in incidence in all age groups worldwide, the disease remains a major global public health problem with an estimated 198 million cases in 2013. Reductions have been achieved mainly through extensive long-lasting insecticide-treated net (LLIN) distribution and indoor residual spraying (IRS) campaigns. However, the future success of these interventions may be undermined by the spread of insecticide-resistant mosquitoes, creating a need for supplementary interventions not reliant on current insecticides. Interestingly, in some locations malaria has declined before intervention scale-up, suggesting additional causes of the reduction. Since malaria is a disease of poverty and the environment, there is increasing interest in the potential contribution of socio-economic development to malaria control, and in coordinating with sectors outside health, including agriculture, water and sanitation, education, city planning and housing, to meet long-term sustainable development goals.

2Housing improvements, traditionally a key pillar of public health, remain underexploited in malaria control. Yet in sub-Saharan Africa (SSA), where up to 80-100 % of malaria transmission occurs indoors at night, the home can be a place of high risk. House screening was the first intervention trialed in Italy after the link between malaria and mosquitoes was discovered. Screening homes was subsequently shown to reduce malaria risk in India, South Africa and the USA and better housing contributed to malaria elimination in the USA and Europe. More recent studies indicate that well-built, modern housing can be protective in many tropical countries and that simple features, including closed eaves (the gap between the top of the wall and the over-hanging roof), brick walls, tiled or metal roofs, or ceilings can reduce mosquito house entry. In a randomized-controlled trial (RCT) in The Gambia, untreated door and window screens and closed eaves halved the prevalence of anaemia in children.

3Ninety per cent of malaria deaths in five year-olds occur in Africa, the economy of which is rapidly growing, with a 6 % annual increase in gross domestic product expected until 2025. Increased personal wealth is precipitating continent-wide housing improvements, such as the replacement of traditional thatch with metal and tiled roofs (Fig. 1). The expanding population, expected to triple to 1.23 billion by 2050, also needs accommodating, with an estimated 144 million new houses required by 2030 in rural areas alone. This economic and cultural transition presents an opportunity to document and influence incremental housing improvements that might protect against malaria, and to build healthy homes.

4Yet despite the historical precedent for improving housing to control malaria, few rigorously conducted studies exist. Furthermore, the evidence on housing and malaria has not been systematically characterized, with no specific evaluation of the size and consistency of the direction of effect, nor the quality of the evidence. The recent Multisectoral Action Framework for Malaria emphasizes throughout the need for good housing, yet there is a paucity of evidence supporting this recommendation and uncertainty about how to select, scale-up and sustain intervention. Here the potential for modern house construction to reduce malaria risk was evaluated. Specifically, the first systematic review and meta-analysis was conducted to assess whether ‘modern’ homes are associated with reduced exposure to infectious bites, malaria infection and clinical malaria in people of all ages in malaria-endemic regions, compared to ‘traditional’ homes. Since few intervention studies exist, observational study designs were also included. The study aimed first to characterize all published and unpublished data and second to assess the strength and quality of these data, in order to rigorously evaluate the evidence for the impact of housing improvements on malaria.

5Recommendations of the Preferred Reporting Items for Systematic Reviews and Meta-analysis of Observational Studies in Epidemiology groups were followed. The study is registered with the International Prospective Register of Systematic Reviews. The study aimed to compare modern with traditional homes in any malaria-endemic settings. In SSA, traditional homes were considered to have mud walls, thatched roofs and earth floors, except in areas of exceptionally high rainfall including Equatorial Guinea, where concrete or wood is the basic wall material. Traditional homes were considered to have mud or stone walls, thatched, wood or mud roofs, and earth floors in North Africa, wood or bamboo walls, thatched roofs and earth or wooden floors in Southeast and South Asia, and adobe or mud and wood walls, thatched roofs and earth floors in South America. Universally, traditional homes were considered to have open eaves, no ceiling and no screening.

6Studies were included with participants of any ages (excluding migrants, displaced people or military) and conducted in real (not experimental) houses, that compared modern with traditional house features and that measured any outcomes of interest. Both observational and intervention study designs were included: (1) case–control; (2) cohort; (3) cross-sectional studies; (4) randomized-controlled trials (RCTs); (5) controlled before-and-after studies, if arms were comparable at baseline and there was at least one unit per arm; (6) cross-over studies, if there were at least one unit per arm; and, (7) interrupted time-series studies. Studies were excluded if arm follow-up periods differed.

7Epidemiological outcomes in human subjects were: clinical malaria (fever with parasitaemia confirmed by microscopy or rapid diagnostic test (RDT), in any age group); malaria infection (confirmed by microscopy or RDT, in any age group); and, anaemia in children aged under 11 years. Entomological outcomes were: entomological inoculation rate (EIR, the estimated number of bites by infectious mosquitoes per person per time period, measured directly using human baits or indirectly using light traps or other methods); human biting rate (HBR, the number of mosquitoes per person per time period); and, indoor density of adult vector mosquitoes (number of mosquitoes per house or person).

8PubMed, Embase, LILACS, the Meta-Register of Controlled Trials, Cochrane Infectious Diseases Group Specialized Register, and Cochrane Central Register of Controlled Trials were searched with no language restrictions, using specified search terms (Additional file 1) to identify studies published from 1 January, 1900 to 13 December, 2013. The following databases were searched: US Armed Forces Pest Management Board online database (1900–1947) and proceedings of the MIM Pan-African Malaria Conferences (2005 and 2013), American Society of Tropical Medicine and Hygiene (2004–2013) and Society for Vector Ecology (2010–2012). Reference lists of identified studies were searched. Authors were contacted for additional references. LST and MI independently screened titles and abstracts before screening the full text of relevant studies using a standard form. Disagreements were resolved by SWL.

9Study characteristics (participants, sampling, exposures, comparisons, outcomes, study design, setting, sample size, follow-up period, vector(s), LLIN and IRS coverage, transmission intensity, and funding) were extracted by LST and a 10 % sub-sample randomly selected for validation (MI). Study authors were contacted for missing data.

10Risk of bias for RCTs, controlled before-and-after studies, cross-over studies and interrupted time-series studies was assessed using the Effective Practice and Organization of Care (EPOC) tool, and for case–control, cohort and cross-sectional studies using the Newcastle-Ottawa Scale. Risk of bias across studies (publication bias) was assessed using funnel plots and Egger’s test for funnel plot asymmetry. Quality and strength of the evidence were evaluated for the main comparison (modern versus traditional homes) using the Grading of Recommendations, Assessment, Development and Evaluation (GRADE) approach.

11Analyses were structured first by house feature, second by outcome and third by study design. All eligible studies were included in a qualitative synthesis. Studies were also included in a quantitative analysis, comparing modern with traditional house features, if crude or adjusted odds ratios (ORs) or rate ratios (RRs) with 95 % confidence intervals (CI), or sufficient data to calculate crude effects, were reported. Specifically, epidemiological data were combined in meta-analysis and entomological data presented in tables. Analyses were done in Stata13 and RevMan5.

12Study effects were combined in the meta-analysis using the generic inverse variance method, which assigns each effect a weight equal to the inverse of its variance. Pooled ORs or RRs were calculated using fixed-effects meta-analysis where significant heterogeneity was not detected and random effects where significant heterogeneity was found (I2 > 50 %). Separate meta-analyses were done for crude and adjusted results.

13Data and study characteristics were presented in tables. Where no effect measure was reported the crude effect was calculated as the ratio of the outcomes in the treatment and control groups. Ninety-five per cent CIs were calculated by estimating the standard errors of the outcomes from their stated 95 % CI. Where 95 % CIs of outcomes were non-symmetrical, it was assumed that standard errors and CIs were calculated on log-transformed values.

14The search yielded 15,526 studies after removing duplicates (Fig. 2). Ninety met the inclusion criteria, of which 18 were included in the qualitative synthesis only and 72 were included in the quantitative analysis (Additional file 2). Of these 72 studies, 53 reported epidemiological outcomes (included in the meta-analysis) and 25 reported entomological outcomes (presented in Tables).

15The six intervention studies dated from 2009 to 2013. All were conducted in rural SSA, using house screening as the intervention. One study, a cluster RCT (cRCT) in The Gambia, collected both epidemiological and entomological outcomes and was included in the meta-analysis. Five studies collected entomological data only: three pilot RCTs in Ethiopia, Mozambique and Tanzania, one randomized cross-over trial in The Gambia, and one non-randomized, cross-over trial in Tanzania. The 84 observational studies, dating from 1935 to 2015, had cross-sectional (n = 39), cohort (n = 30), and case–control (n = 15) designs. These were conducted mainly in SSA (n = 58) and Asia (n = 13) and largely in rural settings (n = 62) (Additional file 2). In the 53 observational studies included in the meta-analysis, comparisons included modern versus traditional housing (n = 15); modern versus traditional wall (n = 22), roof (n = 18), and floor (n = 4) materials and closed versus open eaves (n = 11).

16High risk of bias was found across numerous domains of the EPOC risk of bias for intervention studies, particularly for allocation concealment, length of follow-up and blinding (Additional file 3). Risk of bias within individual case–control, cross-sectional and cohort studies was generally high (Additional file 3). Across studies, there was no evidence of publication bias in the meta-analysis of house type and malaria infection (Additional file 4), with no evidence of funnel plot asymmetry (bias coefficient 0.52, 95 % CI −1.61 to 2.65, p = 0.60). There were insufficient studies to test for asymmetry in the meta-analysis of house type and clinical malaria. GRADE quality of the evidence for the main comparison, modern versus traditional housing, ranged from very low to low (Table 1).

17Residents of modern homes had lower odds of malaria infection than residents of traditional homes (crude OR 0°46, 95 % CI 0°33–0°62, p <0°001, nine studies, low quality evidence; adjusted OR 0°53, 95 % CI 0°42–0°67, p <0°001, five studies, very low quality evidence) (Fig. 3, Table 2). Modern homes were associated with lower odds and incidence rate of clinical malaria (case–control and cross-sectional studies: crude OR 0°32, 95 % CI 0°19–0°54, p <0°001, one study, very low quality evidence; adjusted OR 0°35, 95 % CI 0°20–0°62, p < 0°001, one study, very low quality evidence; cohort studies: crude RR 0°22, 95 % CI 0°14–0°35, p <0°001, three studies, low quality evidence; adjusted RR 0°55, 95 % CI 0°36–0°84, p = 0.005, three studies, very low quality evidence) (Fig. 4). In seven studies with entomological outcomes, modern housing was associated with no effect to a 66 % reduction in density of adult anophelines (Additional file 5).

18In one cRCT in The Gambia, full or ceiling screening reduced anaemia in children by 48 % (adjusted OR 0°52, 95 % CI 0°34–0°80, p = 0°003), with no effect on malaria infection. Screening was not consistently associated with lower odds of anaemia in children or malaria infection in seven case–control, cross-sectional and cohort studies, but was associated with a lower incidence of clinical malaria in three cohort studies (Table 2).

19Modern wall materials were associated with an approximately quarter reduction in the odds of malaria infection, although results were inconsistent for incidence of clinical malaria. Modern roof materials were not consistently associated with reduced odds of infection, but were associated with up to a two thirds reduction in the incidence of clinical malaria. There was inconsistent evidence that modern floor materials gave protection against any epidemiological outcome (Table 2).

20Closed eaves were associated with a quarter reduction in the odds of malaria infection and a quarter to a half reduction in clinical malaria in five case–control and cross-sectional studies and two cohort studies. The presence (versus absence) of a ceiling was associated with a third reduction in the odds of clinical malaria. In one cross-sectional study, house elevation was not associated with the odds of malaria infection (Table 2).

21In this systematic review and meta-analysis to assess whether modern housing is associated with a lower risk of malaria than traditional housing, 84 observational and six intervention studies were included. In eleven case–control, cohort and cross-sectional studies in East Timor, Egypt, Ethopia, Greece, Malawi, Sri Lanka, Thailand, Uganda, and Yemen, the odds of malaria infection were halved in modern versus traditional homes. In one case–control study in Mexico, the odds of clinical malaria were reduced by two thirds. In four cohort studies in Ethiopia, Tanzania and Uganda, the incidence of clinical malaria was halved in modern versus traditional homes.

22Although house screening was the first intervention trialled against malaria, few intervention studies have rigorously evaluated the effect of housing on malaria. Observational studies were therefore also included here, which were most likely subject to selection and measurement bias, low comparability between groups, residual confounding by wealth, and geographical clustering of socio-economic status, house design and malaria. Although we found no evidence of publication bias across studies, we had limited power to detect publication bias due to the relatively small number of studies included. Therefore it is highly possible that publication bias, selective outcome reporting, small-study effects, or selective analysis reporting were present across studies. Overall GRADE quality of evidence was judged to be ‘very low’ to ‘low’, indicating considerable uncertainty in the estimated effects. Despite this, the relative consistency of the size and direction of effect across studies and settings indicates some protection by modern housing, compared to traditional homes, in urban and rural settings in Africa, Asia and South America. Specifically, wall and roof materials other than traditional wood, mud and thatch, and modern house designs encompassing closed eaves, screened doors and windows, and ceilings, may help reduce mosquito house entry and malaria transmission, and therefore merit further field evaluation.

23Good housing can help protect by blocking the entry routes of malaria vectors, which vary by species and region. Overall, the reduced prevalence and incidence of malaria in modern versus traditional homes indicates that this classification was a good proxy for overall ease of entry by mosquitoes across different settings. Closed eaves are likely to be protective in sub-Saharan Africa since the primary African vector Anopheles gambiae s.l. locates hosts by following odour plumes close to the ground and flying upwards when a vertical surface is reached. Open eaves then funnel mosquitoes inside. The presence of a ceiling possibly replicates the protective effect of closed eaves. Conversely, eaves may be less important in South East Asia, where vector entry differs. For example, open verandas are a key feature for house entry by Anopheles philippinensis in Laos PDR. Screening doors and windows can help to directly block vector entry, while modern wall and roof materials may contain fewer gaps, alter the attractiveness of the interior environment to mosquitoes or provide fewer resting sites for mosquitoes than traditional materials such as mud or thatch. It has also been hypothesized that metal-roofed homes are hotter and less conductive for mosquito survival; in Tanzania, the mean physiological age of vectors and sporozoite rate was observed to be lower in more modern versus traditional villages. Understanding the mechanism of protection of different house features against individual vectors is important for identifying potential synergy or discordance with IRS and LLINs.

24Housing is incrementally improving across much of SSA as living standards increase. The present analysis suggests that modern house improvements should be further evaluated in relation to malaria, in addition to specific house modifications including screening. If effective, housing could help reduce reliance on insecticides by providing an additional and more permanent intervention where LLINs and IRS are compromised by behavioural and physiological resistant vectors. Furthermore, since malaria has declined in many African countries, often prior to specific intervention, further research to evaluate the contribution of housing improvements and the expansion of urban environments less conducive to malaria transmission is advocated. Improving the home environment aligns with integrated vector management (IVM) and may help protect against other vector-borne diseases, such as filariasis, cutaneous leishmaniasis, Japanese encephalitis, and dengue, where vectors enter houses, and diarrhoeal disease, through better water, sanitation and hygiene (WASH). Since global housing programmes are key strategies of UN-HABITAT and Habitat for Humanity among other organisations, a pipeline for building malaria-safe homes already exists.

25Improving housing will not be equally effective everywhere, since outdoor transmission can limit the efficacy of interventions centered on the home. Future research should address questions of equity by investigating whether mosquitoes diverted from improved houses may increase exposure among unprotected neighbours. Potentially damaging health effects must also be considered, such as an increased risk of respiratory diseases if airflow is restricted in the presence of certain cooking fuels. It is also shown here that the evidence base for housing needs strengthening, with only one intervention study that measured clinical outcomes. Therefore further small-scale experimental studies to pinpoint exactly which house features can reduce vector entry cost effectively in different settings, RCTs with epidemiological outcomes, and concurrent studies addressing how to incorporate protective features into local house designs and building regulations are needed.

26Despite low quality evidence, the direction and consistency of effects indicate that housing is an important risk factor for malaria. Future research should evaluate the protective effect of both specific house features and incremental housing improvements associated with socio-economic development. Investment in such research and in housing programmes should be considered a natural component of malaria control efforts and a close complement to IVM and WASH as part of long-term, sustainable development.