Reduced mosquito survival in metal-roof houses may contribute to a decline in malaria transmission in sub-Saharan Africa

Abstract

In The Gambia, metal-roof houses were hotter during the day than thatched-roof houses. After 24 h, the mortality of Anopheles gambiae, the principal African malaria vector, was 38% higher in metal-roof houses than thatched ones. During the day, mosquitoes in metal-roof houses moved from the hot roof to cooler places near the floor, where the temperature was still high, reaching 35 °C. In laboratory studies, at 35 °C few mosquitoes survived 10 days, the minimum period required for malaria parasite development. Analysis of epidemiological data showed there was less malaria and lower vector survival rates in Gambian villages with a higher proportion of metal roofs. Our findings are consistent with the hypothesis that the indoor climate of metal-roof houses, with higher temperatures and lower humidity, reduces survivorship of indoor-resting mosquitoes and may have contributed to the observed reduction in malaria burden in parts of sub-Saharan Africa.

Figure 1

Types of study houses used in the mosquito survival experiments. Where (A) is a traditional thatched-roof house, (B) is a ventilated metal-roof house, (C) is a close-up of a screened window positioned in the gable ends of a ventilated house and (D) is a traditional metal roofed house without ventilation. Photographs by SW Lindsay.

Figure 2

Survival of An. coluzzii in Gambian houses where (A) compares thatched-houses (blue) with ventilated metal-roof houses (red), (B) compares thatched-houses (blue) with unventilated metal-roofed houses (grey), (C) is indoor temperature in thatched-houses (blue) and ventilated metal-roofed houses (red) in 2016 and (D) is indoor temperature in thatched-houses (blue) and unventilated metal-roofed houses in 2017. Mortality after 48 h is a measure of mortality from 0 to 48 h. Error bars are standard errors. Blue shaded areas in (C,D) represents hours of darkness. In 2016, the mean indoor temperature in ventilated metal-roofed houses was temperature 29.7 °C (28.8–30.6 °C) and 28.7 °C (95% CIs = 28.0–29.4 °C) in thatched houses, whilst the maximum indoor temperature was 34.7 °C (95% CIs = 33.8–35.6 °C) in metal-roofed houses and 33.1 °C (95% CI = 32.1–34.1 °C) in thatched ones. In 2017, the mean indoor temperature in unventilated metal-roofed houses during the day was 30.3 °C (95% CIs = 29.5–31.1 °C) and 29.4 °C (28.7–30.1 °C) in thatched houses, whilst the maximum indoor temperature was 35.5 °C (95% CIs = 34.8–36.2) in unventilated metal-roofed houses and 34.5 °C (95% CI = 33.7–35.3 °C) in thatch-roofed houses.

Figure 3

Survival of female An. gambiae s.s. maintained at different combinations of temperature and relative humidity (RH). The red broken line represents the minimum period for maturation of P. falciparum in the vector (10 days). Error bars are 95% confidence intervals. Rate ratios are shown in Supplementary Material (Table 2).

Figure 4

Distribution of (A) cumulative parasite prevalence in monthly surveys from June to December 2013 in children 6 months to 15 years old, (B) proportion of parous An. gambiae s.l., and (C) proportion of houses with metal roofs in 12 sites in The Gambia. Where 1 is Bessi, 2 is Ndemban Tenda, 3 is Chogen Wellingara, 4 is Yallal Ba, 5 is Dongoro Ba, 6 is Sinchu Njengudi, 7 is Ngeden, 8 is Sare Seedy, 9 is Njaiye, 10 is Madina Samak, 11 is Sare Wuro and 12 is Gunjur Koto. Non-metal roofs included thatched and tiled houses.