Assessing the impacts of multi-scale environmental change on vector ecology and malaria transmission in eastern Rwanda Open Access
Hennessee, Ian (Spring 2022)
Published
Abstract
Background:
Cleaner cooking fuels are increasingly promoted to reduce morbidity and mortality from household air pollution in low and middle income countries such as Rwanda. However, smoke is a traditional insect repellent and it is unknown whether the replacement of smoky biomass fuels with cleaner fuels could alter vector behavior and exposure to malaria or other vector-borne diseases (VBDs). Additionally, Rwanda experienced a 20-fold increase in reported malaria cases in the last decade. The Ministry of Health hypothesized that environmental changes such as increased temperatures as well as insecticide resistance could have driven these trends, but no scientific studies have assessed their effects on vector ecology and the root causes of the malaria resurgence. An improved understanding of the impacts of these multi-scale environmental changes is necessary to mitigate potential risks and tailor appropriate malaria control interventions.
Methods:
In Aim 1 we employed a semi-field, Latin square design to experimentally investigate the effects of traditional and cleaner fuels on Anopheles mosquito behavior in rural Rwanda. Aim 2 consisted of a randomized controlled trial to assess the effects of liquified petroleum gas (LPG) adoption on vector density among houses that traditionally cook with biomass fuels. Finally, Aim 3 used a retrospective observational design to examine the effects of insecticide resistance, vector control, and regional warming on Anopheles bionomics and malaria incidence in eastern Rwanda.
Findings:
In Aim 1, household entry and host-seeking by lab-reared Anopheles mosquitoes were higher in experimental huts that cooked with LPG compared to traditional biomass fuels, whereas mosquito mortality was lower. Lower PM2.5 and temperatures in LPG huts appeared to meditate this effect. However, in field conditions in Aim 2 we did not find a statistically significant difference in Anopheles or culicine density among intervention houses that received LPG stoves and fuel compared to control houses which cooked with biomass. In contrast, synanthropic fly density was reduced by 61% in intervention houses. Finally, in Aim 3 we found that insecticide resistance and regional warming were associated with the reemergence of An. gambiae after it was previously controlled in the early 2010s. The reemergence of this vector combined with a >2°C increase in regional temperatures drove a dramatic malaria resurgence in eastern Rwanda from 2010 to 2016, but An. gambiae and malaria transmission were controlled following implementation of non-pyrethroid indoor residual spraying (IRS) campaigns in the latter half of the decade.
Conclusions:
Environmental changes at multiple scales can have important implications for vector ecology and transmission of malaria and other VBDs in Rwanda. Although we found experimental evidence that the adoption of cleaner fuels can affect Anopheles behavior, other environmental determinants were more important drivers of mosquito density in field conditions. Reductions in flies could constitute a health co-benefit of LPG adoption in this setting. At a larger scale, insecticide resistance and regional warming are major threats to vector control and malaria prevention in Rwanda. However, the success of non-pyrethroid IRS suggests that existing control measures can mitigate vector reemergence and climate-related malaria increases, providing insecticide resistance is managed.
Table of Contents
1 Chapter 1 1
1.1 Introduction 1
1.2 Dissertation aims 3
1.2.1 Research Aim 1 3
1.2.2 Research Aim 2: 4
1.2.3 Research Aim 3: 4
2 Literature review 5
2.1 Epidemiology and entomology of malaria in Rwanda 5
2.1.1 Epidemiological situation 5
2.1.2 Entomological situation 8
2.2 Importance of culicine mosquitoes and associated arboviruses in Rwanda 9
2.3 Importance of synanthropic flies as mechanical vectors of enteric pathogens in Rwanda 10
2.4 Effects of biomass smoke on disease vectors and vector-borne disease risk 11
2.4.1 Background 11
2.4.2 Direct impacts on Anopheles mosquito behavior: 11
2.4.3 Indirect impacts on Anopheles mosquito behavior 19
2.4.4 Epidemiological outcomes - malaria 21
2.4.5 Impacts of fuel combustion on culicine mosquito behavior and arbovirus transmission 23
2.4.6 Impacts of cooking fuels on domestic filth fly behavior and enteric pathogen exposure risk 25
2.4.7 Literature gaps: 26
2.5 Potential impacts of land-use, climate change, and vector control on vector ecology and malaria transmission in Rwanda 28
3 Research Aim 1. Assessing the Effects of Cooking Fuels on Anopheles Mosquito Behavior: An Experimental Study in Rural Rwanda 35
3.1 Introduction 35
3.2 Materials & Methods 36
3.2.1 Research objectives 36
3.2.2 Study location 37
3.2.3 Experimental huts 37
3.2.4 Trap design and hut modifications 37
3.2.5 Laboratory methods for raising mosquitoes 40
3.2.6 Fuels tested 40
3.2.7 Schedule and timeline of experiments 41
3.2.8 Experimental procedures 41
3.2.9 Primary outcomes 44
3.2.10 Statistical analysis 46
3.2.11 Ethics 47
3.3 Results 47
3.3.1 Baseline 47
3.3.2 Household entry 48
3.3.3 Host-seeking 50
3.3.4 Household exit 51
3.3.5 Mortality 52
3.3.6 Effects of PM2.5, temperature, and relative humidity 52
3.4 Discussion 55
3.5 Conclusion 59
4 Research Aim 2. Effects of cooking with liquid petroleum gas fuel versus solid biomass on mosquito and fly density in the home: a randomized controlled trial in Eastern Province, Rwanda 60
4.1 Introduction 60
4.1.1 Background 60
4.1.2 Research objective 62
4.2 Materials and methods 62
4.2.1 Study design 62
4.2.2 Sample size and eligibility 63
4.2.3 Study setting 64
4.2.4 Procedures 64
4.2.5 Outcomes 67
4.2.6 Statistical analysis 69
4.2.7 Ethics 70
4.3 Results 70
4.3.1 Study population characteristics 70
4.3.2 Entomological outcomes 75
4.3.3 Secondary outcomes: Malaria and Diarrhea 78
4.4 Discussion 80
4.5 Conclusions 83
5 Research Aim 3. Impacts of insecticide resistance and environmental change on Anopheles gambiae reemergence and resurgent malaria transmission in eastern Rwanda, 2010 – 2020 85
5.1 Background 85
5.2 Methods 88
5.2.1 Study setting: 88
5.2.2 Entomological data 89
5.2.3 Epidemiological data 91
5.2.4 Outcomes 91
5.2.5 Independent variables 93
5.2.6 Statistical analysis 95
5.2.7 Ethical considerations 96
5.3 Results 97
5.3.1 Malaria trends and HLC results 97
5.3.2 Objective 1: Comparing An. gambiae and An. arabiensis 98
5.3.3 Objective 2a: Changes in species composition from 2010 to 2020 100
5.3.4 Objective 2b: Causes of increased malaria incidence 103
5.4 Discussion 105
5.5 Conclusions: 111
6 Summary, reflections, and directions for future research 112
6.1 Summary of findings 112
6.2 Reflections and directions for future research 119
A. Appendix A: Research Aim 2 Supplemental Materials 125
Independent variables 125
Supplemental tables 127
B. Appendix B: Research Aim 3 Supplemental Materials 132
Supplemental figures 132
Supplemental methods 138
References 140
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