Cooking outdoors or with cleaner fuels does not increase malarial risk in children under 5 years: a cross-sectional study of 17 sub-Saharan African countries

Smoke from solid biomass cooking is often stated to reduce household mosquito levels and, therefore, malarial transmission. However, household air pollution (HAP) from solid biomass cooking is estimated to be responsible for 1.67 times more deaths in children aged under 5 years compared to malaria globally. This cross-sectional study investigates the association between malaria and (i) cleaner fuel usage; (ii) wood compared to charcoal fuel; and, (iii) household cooking location, among children aged under 5 years in sub-Saharan Africa (SSA). Population-based data was obtained from Demographic and Health Surveys (DHS) for 85,263 children within 17 malaria-endemic sub-Saharan countries who were who were tested for malaria with a malarial rapid diagnostic test (RDT) or microscopy. To assess the independent association between malarial diagnosis (positive, negative), fuel type and cooking location (outdoor, indoor, attached to house), multivariable logistic regression was used, controlling for individual, household and contextual confounding factors. Household use of solid biomass fuels and kerosene cooking fuels was associated with a 57% increase in the odds ratio of malarial infection after adjusting for confounding factors (RDT adjusted odds ratio (AOR):1.57 [1.30–1.91]; Microscopy AOR: 1.58 [1.23–2.04]) compared to cooking with cleaner fuels. A similar effect was observed when comparing wood to charcoal among solid biomass fuel users (RDT AOR: 1.77 [1.54–2.04]; Microscopy AOR: 1.21 [1.08–1.37]). Cooking in a separate building was associated with a 26% reduction in the odds of malarial infection (RDT AOR: 0.74 [0.66–0.83]; Microscopy AOR: 0.75 [0.67–0.84]) compared to indoor cooking; however no association was observed with outdoor cooking. Similar effects were observed within a sub-analysis of malarial mesoendemic areas only. Cleaner fuels and outdoor cooking practices associated with reduced smoke exposure were not observed to have an adverse effect upon malarial infection among children under 5 years in SSA. Further mixed-methods research will be required to further strengthen the evidence base concerning this risk paradigm and to support appropriate public health messaging in this context.


Background
Smoke arising from solid biomass cooking (wood, dung, charcoal, crop residue) is widely perceived to act as a mosquito repellent among communities [1][2][3], therefore protecting against mosquito-borne disease. However, solid biomass cooking produces health harming levels of household air pollution (HAP), estimated to be responsible for around 450,000 deaths in children aged under 5 years worldwide [4], compared to only 274,000 estimated deaths from malaria in 2019 [1]. This discordance in perceived compared to actual health risks associated with malarial transmission could impact upon uptake of structural interventions (e.g., cleaner fuel transition [LPG, electricity, biogas]) and behavioural changes intended to reduce harmful HAP exposure, notably among those living in endemic malarial regions.
Sub-Saharan Africa (SSA) has the highest malarial prevalence globally with 94% of cases and deaths, caused by predominantly by Plasmodium falciparum [5]. Identified risk factors for malarial infection include poor household construction [6][7][8] (e.g., open eaves), animals sleeping in the house [9] and presence of standing water near the house [10,11]. The use of mosquito nets, household insecticidal spraying, and larval source management [12] have become common practice advocated in malarial prevention, driven in part by the World Health Organization's (WHO) coordinated response [5]. Another, common preventive measure is use of mosquito repellent smoke from the burning of certain types of plant materials, such as churai in West Africa [2,13].
There is little evidence supporting reduced mosquito infiltration [14,15] or malarial transmission associated with solid biomass fuel cooking [2,16]; although there is some evidence that solid biomass cooking reduces the risk of arboviruses in Guatemala [17]. Therefore, to better understand this disease risk paradigm, this study investigates the association of malarial acquisition among children aged under 5 years with regard to: (i) cleaner or solid biomass fuels and kerosene cooking; (ii) charcoal or wood fuel usage; and (iii) indoor and outdoor cooking, within households in 17 SSA countries using the population-based Demographic and Health Survey (DHS) data.

Data sources
This cross-sectional study uses publicly available survey data for 17 malarial-endemic SSA countries with available malarial data (Fig. 1), obtained from the DHS program supported by the United States Agency for International Development (USAID) within the last 10 years (2010-2020). The DHS undertakes full surveys every 5 years, and intermediate Malaria Indicators Surveys (MIS) [18]; only some of the full DHS survey modules undertake malarial testing. For those DHS surveys including malaria modules, malarial testing is undertaken by trained fieldworkers on a sub-sample of eligible children aged 6-59 months using a malarial rapid diagnostic test (RDT) [18]. A two-stage stratified sampling technique was employed to obtain a representative population-based sample, with residential households randomly selected. Eligible households included those with an ever-married (married, widowed or divorced) woman aged between 15 and 49 years and resident the night before the survey. Ethical approval for data collection was gained from the relevant government authority [18], and authorization for data access was provided by the DHS.
Malarial endemicity was generated for each cluster by assessment of malarial prevalence obtained from the open source Malaria Atlas Project [19] within eligible countries, and defined as holoendemic (> 75%), hyperendemic (51-75%), mesoendemic (11-50%), hypoendemic (< 10%) [20]. Those data points that fell within hypoendemic areas were excluded from the analysis due to lower rate of malarial infection and testing. Malarial prevalence data were geocoded to the cluster geographic coordinates using the spatial analyst tool in ArcMAP 10.7 [21]; a method that has been previously used for this purpose [22].
As the wealth index provided by DHS contains cooking fuel as an indicator variable, a new modified wealth index was calculated in SPSS [23] using principal component analysis [24] to prevent circularity [8]. The index indicator variables included source of drinking water, house construction material, provision of a toilet facility and household assets, which varied by country (Additional file 1).

Measure of malarial diagnosis
A malarial infection was determined by a positive RDT (n = 17 countries) and in some countries a subsequent blood smear test via microscopy taken at the point of interview (n = 11 countries), both of which were modelled as a binary (negative, positive) outcome variable, in separate analysis within this study. The RDT was undertaken using the SD BIOLINE Malaria Ag test, in all countries, which has estimated sensitivity of 99.7% and specificity of 99.5% [25]. Whereas, only certain countries collected blood samples which were collected with the parasites detected in the blood at time of survey using microscopy [18], with estimated sensitivity of 95.7% and specificity of 97.9% [26].

Explanatory variables
Covariates were included for the relevant contextual, household and individual factors identified as influencing both HAP exposure and malarial risk. Covariates were included in regression models as categorical variables other than household altitude, which was modelled as a continuous variable. Regional level variables were: malarial endemicity (mesoendemic, hyperendemic and holoendemic), season (dry, wet), rural or urban residence (rural, urban), cluster altitude (metres). Household level variables were: number of household members (≤ 6, > 6), household smoking (no, yes), modified wealth index (lowest, low, middle, high, highest), biomass cooking fuel type (where applicable; kerosene, coal/lignite, charcoal, wood, straw/shrubs/grass, agricultural crop, animal dung), household insecticide spraying within the last 12 months (no, yes) and dwelling construction (traditional, modern). Child variables were: age (< 1, 1, 2, 3, 4 years), birth order (first born, not first born), child's sex (male, female), slept under mosquito net last night (no, yes-treated (ITN) net, yes-untreated net). The season variable is created using regional and country level information from the CIA fact book [27] and the World Bank climate change knowledge portal [28]. The household construction variable is a composite variable derived from the wall, roof and floor material. Firstly, each of the three materials were categorized into natural, rudimentary and finished construction material using the criteria outlined by Tusting et al. [8], followed by the creation of the household construction variable where modern household construction was define as wall, roof and floor being made of finished materials.

Data analysis
Data preparation and analysis was undertaken in R studio [29]. Each variable was described within the combined dataset using number of cases (n), and percentage (%) and median and Interquartile range (IQR) for continuous variables. The level of missing data ranged from 0 to 48% of clinically relevant variables at a country level, which was imputed using the MICE package [30] with 50 iterations [31,32]; to prevent bias from list-wise deletion [33]. To test the association between cooking practices and malarial infection, multivariable logistic regression using the survey package [34], was used to account for the complex sampling strategy; reporting adjusted odds ratios (AOR) and 95% confidence intervals (95% CI). The MIS survey did not contain information on cooking location and household smoking, therefore a sub-analysis was undertaken using countries where these variables were available for analysis. Sub-analyses were also undertaken for rural, urban, wood cooking fuel houses and mesoendemic areas. In addition, the analysis was repeated to include additional covariates among a sub-set of countries where additional variables of interest were available. This enabled investigation of the influence of (i) household cooking location; (ii) household smoking; and (iii) household insecticidal spraying, as some of the variables are missing from certain countries.

Results
This  (Table 2). Malarial infection was positively identified by RDT among 34.6% of children in the combined dataset at the time of testing, with the highest point prevalence in Guinea 2012 (51.8%) and lowest in Tanzania 2017 (7.07%) ( Table 3). However, where microscopy was undertaken malarial infection was identified in 28.2% of children, with the highest prevalence in Guinea 2012 (48.7%) and lowest in Uganda 2018-2019 (11.3%). Of the areas surveyed, most were in mesoendemic areas (  (Table 3).

Analysis 1-Solid biomass fuel usage and risk of malarial infection
In pooled analyses, cooking with solid biomass fuels and kerosene fuels was observed to be independently associated with a 57% increase in the adjusted odds ratio for malarial infection, compared to cleaner cooking (electricity, LPG) ( Fig. 3) (Table 4).

Analysis 2-Biomass fuel type and risk of malarial infection
Among biomass fuel households only, use of wood compared to charcoal fuel was associated with an increased adjusted odds ratio of malarial infection (

Analysis 3-Household cooking location and risk of malarial infection
No significant association was observed between household cooking location and malaria adjusted odds ratio (RDT AOR: 0.94 [0.83-1.05]; Microscopy AOR: 0.97 [95% CI 0.83-1.05]) (Fig. 5). In comparison, cooking in a separate building was associated with a reduced adjusted odds ratio of malarial infection by 74% compared to indoor cooking (      (Table 4).

Discussion
This large exploratory study of over 85,000 children aged under 5 years living in 17 malaria-endemic SSA found no evidence to suggest that use of cleaner fuels (e.g., LPG, electricity, biogas), charcoal vs wood, or outdoor cooking location are associated with an increased risk of malarial infection. Indeed, the findings suggest that solid biomass fuel usage may be associated with a higher incidence of malarial infection among children in SSA. There are a number of factors that may account for the increase in infections, such as the longer cooking times and thus of carbon dioxide production [35], a major mosquito attractant [36], found with solid biomass fuel cooking [37]. Additionally, the use of solid biomass fuels, particularly wood, crop residue and dung, require women, to typically collect fallen or harvest branches from woods and forests where mosquitoes commonly reside, often taking children under 5 years on their backs, thereby increasing risk of mosquito bites. It is highly likely that risk of within household acquisition of malaria is also influenced by socioeconomic factors such as household construction characteristics (eaves space, wall type) and living conditions [8,[38][39][40][41] which are not fully captured in the DHS composite wealth index. It is also recognized that use of cleaner domestic energy sources, cooking in a separate building and selection of biomass cooking fuel type may reflect socio-economic determinants, also related to malarial microepidemiology at the household level [42,43]. The child's age is also a key factor in malarial infection risk, with an observed increased risk with increasing age, potentially reflecting behavioural, nutritional or exposure differences. In terms of modifiable factors for malarial infection prevention and control, there is strong evidence supporting the sustained use of ITN bed nets, larval source management and household insecticide spraying [12]; of which only ITN bed nets could be controlled for in the main analyses. The importance of household insecticide spraying can be seen in the subsidiary analysis undertaken among countries for which this information was available, identifying that there was no association with type of biomass fuel and malarial infection risk (RDT: AOR 1.23 [0.94-1.61]; Microscopy AOR: 1.07 [0.77-1.47]; Table 4); however, this sub-analysis is likely to be underpowered and should be interpreted with caution.
The analyses presented also did not explore broader contextual factors associated with household or village level clustering of malarial transmission, including position of households in relation to mosquito sites and local attitudes to malarial treatment which are recognized to influence local variations in malarial prevalence [44]. The DHS dataset did not contain information on cooking practices such as timing or duration, both of which     influence the amount of smoke produced and therefore HAP exposure, and may also generate higher localized levels of indoor CO 2 [35] thereby attracting mosquitoes into the home [36]. In addition, season could only be accounted for at country or broader regional level, which does not take into account microclimates, in addition, the DHS is normally undertaken in the dry season and the MIS in the wet season when the malarial transmission risk is increased [18]. HAP interventions should be developed to include activities which communicate that cooking practices which produce less smoke do not increase risk of malaria transmission to residents. It is also important to reinforce health protection advice regarding evidence-based measures for mosquito control. Further qualitative and quantitative research is merited, for a detailed investigation of the relationships between cooking location, fuel choice and risk of malarial acquisition, considering a wider range of transmission risk factors at a local level. The rural-urban differences in cooking activity patterns, which can be most clearly noted within the differences observed in distribution between fuel types, is likely to reflect relative economic development, improved access to cleaner fuel sources in urban areas and reduced potential for cohabitation with livestock [45]. However, the rural-urban divide was not as distinct within the cleaner fuel or cooking location sub-analysis, indicating that other contextual and compositional factors exist which may influence malarial infection risk (e.g., nutrition). Although season, malarial endemicity and altitude were captured as confounding factors within our analyses, information was not available for other contextual factors of relevance to malarial infection risk, such as temperature [46].
Additionally, although the cooking practices are reported at the time of interview, this survey question does not take into consideration longer-term trends which may vary on a seasonal basis. Further prospective research is required to better understand environmental influences upon malarial microepidemiology including objective pollutant exposure assessment, capture of household design characteristics, lifestyle and time-activity factors to assess relationships with mosquito breeding conditions, malarial parasitaemia and outcomes among adults and children.

Conclusion
This large-scale observational study suggests that use of cleaner fuels and outdoor cooking practices typically associated with lower levels of household smoke, were not associated with an increased malarial acquisition risk among children living in SSA. Further mixed-methods research is required to better understand the relationships between cooking practices, cooking fuel emissions, mosquito activity and risk of malarial acquisition at household and community levels in this world region.