The ecology and behaviour of insecticide resistant malaria vectors and implications for control in Burkina Faso

Sanou, Antoine (2020) The ecology and behaviour of insecticide resistant malaria vectors and implications for control in Burkina Faso. PhD thesis, University of Glasgow.

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Long-Lasting Insecticide-Treated Nets (LLINs) and Indoor Residual Spraying (IRS) are the most common and successful methods for malaria vector control in Africa. There is growing evidence of shifts in mosquito vector biting and resting behaviours in several African settings where high LLIN coverage has been achieved. These changes, combined with growing insecticide resistance, may reduce intervention success by decreasing the contact between vectors and insecticide-treated surfaces. While insecticide resistance in malaria vectors has been widely investigated, less is known about the implications of mosquito behavioural changes to malaria control. In recent years, LLIN programmes appear to have a reducing impact in a small number of high burden African countries including Burkina Faso. This reducing effectiveness is hypothesized to be the result of insecticide resistance, but the potential additional contribution of mosquito behavioural avoidance strategies has not yet been investigated in Burkina Faso. The aim of this PhD was to investigate the contribution of insecticide resistance and mosquito behaviours to the persistence of malaria transmission in southwestern Burkina Faso following a national LLIN-distribution campaign. Specific objectives were to (i) evaluate the performance of a new mosquito sampling method, the Mosquito Electrocuting Trap (MET) to measure spatial and temporal variation in human exposure to malaria vectors; and characterize the spatial, seasonal and longer-term trends in (ii) vector ecology and behaviours, (iii) insecticide resistance within Anopheles gambiae sensu lato (s.l.) and (iv) malaria vector survival and transmission potential in rural Burkina Faso.
A two-year programme of longitudinal mosquito vector surveillance was initiated within 12 villages of south-western Burkina Faso in 2016, shortly after completion of a mass LLIN distribution. Host seeking malaria vectors were sampled monthly using Human Landing Catches (HLC) and METs conducted inside houses and in the surrounding outdoor area (911 households in total). Resting bucket traps (RBTs) were used to sample indoor and outdoor resting vectors. In an initial study (Chapter 2), I evaluated the performance of the MET relative to the HLC for sampling host-seeking malaria vectors over 15 months in 12 villages. Overall, the MET caught proportionately fewer An. gambiae s.l. than the HLC (mean estimated number of 0.78 versus 1.82 indoors, and 1.05 versus 2.04 outdoors). However provided a consistent representation of vector species composition, seasonal and spatial dynamics, biting behaviour (e.g. location and time) and malaria infection rates relative. The MET slightly underestimated the proportion of bites that could be prevented by LLINs relative to the HLC (5%). However, given the major advantage of the MET of reducing human infection risk during sampling, I conclude these limitations are acceptable and that the MET presents a promising and safer alternative for monitoring human exposure to malaria vectors in outdoor environments.
Vector sampling was extended (using HLCs and RBTs) to investigate longer-term temporal changes in vector ecology and behaviour (Chapter 3). Analysis of a subset (20%) of the An. gambiae s.l. (N= 7852) indicated that An. coluzzii (53.82%) and An. gambiae (45.9%) were the main vector species. There was substantial variation in vector abundance between sites and seasons, with a predicted ~23% reduction in An. gambiae s.l. biting density from start to end of study. A higher proportion of outdoor biting (~54%) was detected than expected from previous studies; but there was no evidence of spatial, seasonal or longer-term changes in exophagy. Species level analyses indicated that revealed moderate but statistically significant different in the exophagy and biting time between An. coluzzii and An. gambiae. Combining information on biting times and location (indoors versus outdoors), I estimated that ~85% of exposure could be prevented using good quality and effective LLINs during standard sleeping hours (10 pm – 5 am).
Bioassays were conducted on the An. gambiae s.l. population at 9 out of the original 12 study villages to estimate spatial, seasonal and longer-term variation in insecticide resistance (IR) over the study period. Overall, only 23% of An. gambiae s.l. exposed to a diagnostic dose of deltamethrin were killed within 24 hours; indicating that all surveyed populations are resistant. Furthermore, IR increased over the study period, with significant reduction in mortality after exposure to deltamethrin in bioassays. There was no evidence of variation in IR between An. gambiae and An. coluzzii.
Finally, the transmission potential of An. gambiae s.l. in this area was investigated through assessment of mosquito parity rates (a proxy of survival), malaria infection rates and estimation of annual Entomological Inoculation Rates (EIR; Chapter 5). The daily survival rate of malaria vectors in this area was > 90%), but with variation between villages and seasons. After controlling for this spatial and seasonal variation, there was evidence of a longer-term increase in vector survival over the study period. In contrast, both mosquito vector biting densities and their malaria infection rates declined over the study period. This resulted in a drop in the predicted EIR from 320 to 105 infective bites per person/year respectively in year 1 and 2. Considering the proportion of exposure estimated to be preventable by effective LLIN use (~85%, Chapter 2 &3), I estimated that residents in this area are still exposed to ~32 infective bites per person per year even when this intervention is used. This confirms that even with 100% coverage and usage of highly effective LLINs, high levels of transmission will persist in this setting.
Taking the case of Burkina Faso as an example, results obtained here confirm that both IR and outdoor biting by malaria vectors are contributing to the persistence of transmission in high burden African countries. Consequently, a successful vector control programme in this context need a clear insecticide resistance management plan and supplementary tools that target vectors feeding and resting outdoors.

Item Type: Thesis (PhD)
Qualification Level: Doctoral
Keywords: Anopheles gambiae s.l., ecology, biting and resting, behaviours, Mosquito Electrocuting Trap, insecticide resistance, Malaria transmission potentials, The Cascades Region, Burkina Faso.
Colleges/Schools: College of Medical Veterinary and Life Sciences > Institute of Biodiversity Animal Health and Comparative Medicine
Funder's Name: Wellcome Trust
Supervisor's Name: Ferguson, Professor M. Heather and Matthiopoulos, Professor Jason
Date of Award: 2020
Depositing User: Dr Antoine Sanou
Unique ID: glathesis:2020-81392
Copyright: Copyright of this thesis is held by the author.
Date Deposited: 22 Jun 2020 05:54
Last Modified: 15 Sep 2022 14:23
Thesis DOI: 10.5525/gla.thesis.81392
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