The impact of indoor residual spraying on Plasmodium falciparum microsatellite variation in an area of high seasonal malaria transmission in Ghana, West Africa

Here, we report the first population genetic study to examine the impact
of indoor residual spraying (IRS) on Plasmodium falciparum in humans. This
study was conducted in an area of high seasonal malaria transmission in
Bongo District, Ghana. IRS was implemented during the dry season
(November-May) in three consecutive years between 2013 and 2015 to reduce
transmission and attempt to bottleneck the parasite population in humans
towards lower diversity with greater linkage disequilibrium. The study was
done against a background of widespread use of long-lasting insecticidal
nets, typical for contemporary malaria control in West Africa.
Microsatellite genotyping with 10 loci was used to construct 392 P.
falciparum multilocus infection haplotypes collected from two
age-stratified cross-sectional surveys at the end of the wet seasons pre-
and post-IRS. Three-rounds of IRS, under operational conditions, led to a
>90% reduction in transmission intensity and a 35.7% reduction in
the P. falciparum prevalence (p < .001). Despite these declines,
population genetic analysis of the infection haplotypes revealed no
dramatic changes with only a slight, but significant increase in genetic
diversity (He : pre-IRS = 0.79 vs. post-IRS = 0.81, p = .048).
Reduced relatedness of the parasite population (p < .001) was
observed post-IRS, probably due to decreased opportunities for
outcrossing. Spatiotemporal genetic differentiation between the pre- and
post-IRS surveys (D = 0.0329 [95% CI: 0.0209 - 0.0473], p = .034) was
identified. These data provide a genetic explanation for the resilience of
P. falciparum to short-term IRS programmes in high-transmission settings
in sub-Saharan Africa.