Investigating the association between household exposure to Anopheles stephensi and malaria in Sudan and Ethiopia: A case-control study protocol.

BACKGROUND: Endemic African malaria vectors are poorly adapted to typical urban ecologies. However, Anopheles stephensi, an urban malaria vector formerly confined to South Asia and the Persian Gulf, was recently detected in Africa and may change the epidemiology of malaria across the continent. Little is known about the public health implications of An. stephensi in Africa. This study is designed to assess the relative importance of household exposure to An. stephensi and endemic malaria vectors for malaria risk in urban Sudan and Ethiopia. METHODS: Case-control studies will be conducted in 3 urban settings (2 in Sudan, 1 in Ethiopia) to assess the association between presence of An. stephensi in and around households and malaria. Cases, defined as individuals positive for Plasmodium falciparum and/or P. vivax by microscopy/rapid diagnostic test (RDT), and controls, defined as age-matched individuals negative for P. falciparum and/or P. vivax by microscopy/RDT, will be recruited from public health facilities. Both household surveys and entomological surveillance for adult and immature mosquitoes will be conducted at participant homes within 48 hours of enrolment. Adult and immature mosquitoes will be identified by polymerase chain reaction (PCR). Conditional logistic regression will be used to estimate the association between presence of An. stephensi and malaria status, adjusted for co-occurrence of other malaria vectors and participant gender. CONCLUSIONS: Findings from this study will provide evidence of the relative importance of An. stephensi for malaria burden in urban African settings, shedding light on the need for future intervention planning and policy development.

Spatiotemporal distribution and bionomics of Anopheles stephensi in different eco-epidemiological settings in Ethiopia.

BACKGROUND: Malaria is a major public health concern in Ethiopia, and its incidence could worsen with the spread of the invasive mosquito species Anopheles stephensi in the country. This study aimed to provide updates on the distribution of An. stephensi and likely household exposure in Ethiopia. METHODS: Entomological surveillance was performed in 26 urban settings in Ethiopia from 2021 to 2023. A kilometer-by-kilometer quadrant was established per town, and approximately 20 structures per quadrant were surveyed every 3 months. Additional extensive sampling was conducted in 50 randomly selected structures in four urban centers in 2022 and 2023 to assess households' exposure to An. stephensi. Prokopack aspirators and CDC light traps were used to collect adult mosquitoes, and standard dippers were used to collect immature stages. The collected mosquitoes were identified to species level by morphological keys and molecular methods. PCR assays were used to assess Plasmodium infection and mosquito blood meal source. RESULTS: Catches of adult An. stephensi were generally low (mean: 0.15 per trap), with eight positive sites among the 26 surveyed. This mosquito species was reported for the first time in Assosa, western Ethiopia. Anopheles stephensi was the predominant species in four of the eight positive sites, accounting for 75-100% relative abundance of the adult Anopheles catches. Household-level exposure, defined as the percentage of households with a peridomestic presence of An. stephensi, ranged from 18% in Metehara to 30% in Danan. Anopheles arabiensis was the predominant species in 20 of the 26 sites, accounting for 42.9-100% of the Anopheles catches. Bovine blood index, ovine blood index and human blood index values were 69.2%, 32.3% and 24.6%, respectively, for An. stephensi, and 65.4%, 46.7% and 35.8%, respectively, for An. arabiensis. None of the 197 An. stephensi mosquitoes assayed tested positive for Plasmodium sporozoite, while of the 1434 An. arabiensis mosquitoes assayed, 62 were positive for Plasmodium (10 for P. falciparum and 52 for P. vivax). CONCLUSIONS: This study shows that the geographical range of An. stephensi has expanded to western Ethiopia. Strongly zoophagic behavior coupled with low adult catches might explain the absence of Plasmodium infection. The level of household exposure to An. stephensi in this study varied across positive sites. Further research is needed to better understand the bionomics and contribution of An. stephensi to malaria transmission.

Influence of larval growth and habitat shading on retreatment frequencies of biolarvicides against malaria vectors.

Effective larviciding for malaria control requires detailed studies of larvicide efficacies, aquatic habitat characteristics, and life history traits of target vectors. Mosquitoes with brief larval phases present narrower timeframes for biolarvicidal effects than mosquitoes with extended periods. We evaluated two biolarvicides, VectoBac (Bacillus thuringiensis israelensis (Bti)) and VectoMax (Bti and Bacillus sphaericus) against Anopheles funestus and Anopheles arabiensis in shaded and unshaded habitats; and explored how larval development might influence retreatment intervals. These tests were done in semi-natural habitats using field-collected larvae, with untreated habitats as controls. Additionally, larval development was assessed in semi-natural and natural habitats in rural Tanzania, by sampling daily and recording larval developmental stages. Both biolarvicides reduced larval densities of both species by >98% within 72 h. Efficacy lasted one week in sun-exposed habitats but remained >50% for two weeks in shaded habitats. An. funestus spent up to two weeks before pupating (13.2(10.4-16.0) days in semi-natural; 10.0(6.6-13.5) in natural habitats), while An. arabiensis required slightly over one week (8.2 (5.8-10.6) days in semi-natural; 8.3 (5.0-11.6) in natural habitats). The findings suggest that weekly larviciding, which is essential for An. arabiensis might be more effective for An. funestus whose prolonged aquatic growth allows for repeated exposures. Additionally, the longer residual effect of biolarvicides in shaded habitats indicates they may require less frequent treatments compared to sun-exposed areas.

Changes in contributions of different Anopheles vector species to malaria transmission in east and southern Africa from 2000 to 2022.

BACKGROUND: Malaria transmission in Africa is facilitated by multiple species of Anopheles mosquitoes. These vectors have different behaviors and vectorial capacities and are affected differently by vector control interventions, such as insecticide-treated nets and indoor residual spraying. This review aimed to assess changes in the contribution of different vector species to malaria transmission in east and southern Africa over 20 years of widespread insecticide-based vector control. METHODS: We searched PubMed, Global Health, and Web of Science online databases for articles published between January 2000 and April 2023 that provided species-specific sporozoite rates for different malaria vectors in east and southern Africa. We extracted data on study characteristics, biting rates, sporozoite infection proportions, and entomological inoculation rates (EIR). Using EIR data, the proportional contribution of each species to malaria transmission was estimated. RESULTS: Studies conducted between 2000 and 2010 identified the Anopheles gambiae complex as the primary malaria vector, while studies conducted from 2011 to 2021 indicated the dominance of Anopheles funestus. From 2000 to 2010, in 57% of sites, An. gambiae demonstrated higher parasite infection prevalence than other Anopheles species. Anopheles gambiae also accounted for over 50% of EIR in 76% of the study sites. Conversely, from 2011 to 2021, An. funestus dominated with higher infection rates than other Anopheles in 58% of sites and a majority EIR contribution in 63% of sites. This trend coincided with a decline in overall EIR and the proportion of sporozoite-infected An. gambiae. The main vectors in the An. gambiae complex in the region were Anopheles arabiensis and An. gambiae sensu stricto (s.s.), while the important member of the An. funestus group was An. funestus s.s. CONCLUSION: The contribution of different vector species in malaria transmission has changed over the past 20 years. As the role of An. gambiae has declined, An. funestus now appears to be dominant in most settings in east and southern Africa. Other secondary vector species may play minor roles in specific localities. To improve malaria control in the region, vector control should be optimized to match these entomological trends, considering the different ecologies and behaviors of the dominant vector species.

Integrating vector control within an emerging agricultural system in a region of climate vulnerability in southern Malawi: A focus on malaria, schistosomiasis, and arboviral diseases.

Infectious diseases are emerging at an unprecedented rate while food production intensifies to keep pace with population growth. Large-scale irrigation schemes have the potential to permanently transform the landscape with health, nutritional and socio-economic benefits; yet, this also leads to a shift in land-use patterns that can promote endemic and invasive insect vectors and pathogens. The balance between ensuring food security and preventing emerging infectious disease is a necessity; yet the impact of irrigation on vector-borne diseases at the epidemiological, entomological and economic level is uncertain and depends on the geographical and climatological context. Here, we highlight the risk factors and challenges facing vector-borne disease surveillance and control in an emerging agricultural ecosystem in the lower Shire Valley region of southern Malawi. A phased large scale irrigation programme (The Shire Valley Transformation Project, SVTP) promises to transform over 40,000 ha into viable and resilient farmland, yet the valley is endemic for malaria and schistosomiasis and experiences frequent extreme flooding events following tropical cyclones. The latter exacerbate vector-borne disease risk while simultaneously making any empirical assessment of that risk a significant hurdle. We propose that the SVTP provides a unique opportunity to take a One Health approach at mitigating vector-borne disease risk while maintaining agricultural output. A long-term and multi-disciplinary approach with buy-in from multiple stakeholders will be needed to achieve this goal.

Effect of passive and active ventilation on malaria mosquito house entry and human comfort: an experimental study in rural Gambia.

Rural houses in sub-Saharan Africa are typically hot and allow malaria mosquitoes inside. We assessed whether passive or active ventilation can reduce house entry of malaria mosquitoes and cool a bedroom at night in rural Gambia. Two identical experimental houses were used: one ventilated and one unventilated (control). We evaluated the impact of (i) passive ventilation (solar chimney) and (ii) active ventilation (ceiling fan) on the number of mosquitoes collected indoors and environmental parameters (temperature, humidity, CO2, evaporation). Although the solar chimney did not reduce entry of Anopheles gambiae sensu lato, the ceiling fan reduced house entry by 91% compared with the control house. There were no differences in indoor nightly temperature, humidity or CO2 between intervention and control houses in either experiment. The solar chimney did not improve human comfort assessed using psychrometric analysis. While the ceiling fan improved human comfort pre-midnight, in the morning it was too cool compared with the control house, although this could be remedied through provision of blankets. Further improvements to the design of the solar chimney are needed. High air velocity in the ceiling fan house probably reduced mosquito house entry by preventing mosquito flight. Improved ventilation in houses may reduce malaria transmission.

Review of the ecology and behaviour of Aedes aegypti and Aedes albopictus in Western Africa and implications for vector control.

Western Africa is vulnerable to arboviral disease transmission, having recently experienced major outbreaks of chikungunya, dengue, yellow fever and Zika. However, there have been relatively few studies on the natural history of the two major human arbovirus vectors in this region, Aedes aegypti and Ae. albopictus, potentially limiting the implementation of effective vector control. We systematically searched for and reviewed relevant studies on the behaviour and ecology of Ae. aegypti and Ae. albopictus in Western Africa, published over the last 40 years. We identified 73 relevant studies, over half of which were conducted in Nigeria, Senegal, or Côte d'Ivoire. Most studies investigated the ecology of Ae. aegypti and Ae. albopictus, exploring the impact of seasonality and land cover on mosquito populations and identifying aquatic habitats. This review highlights the adaptation of Ae. albopictus to urban environments and its invasive potential, and the year-round maintenance of Ae. aegypti populations in water storage containers. However, important gaps were identified in the literature on the behaviour of both species, particularly Ae. albopictus. In Western Africa, Ae. aegypti and Ae. albopictus appear to be mainly anthropophilic and to bite predominantly during the day, but further research is needed to confirm this to inform planning of effective vector control strategies. We discuss the public health implications of these findings and comment on the suitability of existing and novel options for control in Western Africa.

Correction: Integrated Aedes management for the control of Aedes-borne diseases.

[This corrects the article DOI: 10.1371/journal.pntd.0006845.].

Risk of Plasmodium falciparum infection in south-west Burkina Faso: potential impact of expanding eligibility for seasonal malaria chemoprevention.

Burkina Faso has one of the highest malaria burdens in sub-Saharan Africa despite the mass deployment of insecticide-treated nets (ITNs) and use of seasonal malaria chemoprevention (SMC) in children aged up to 5 years. Identification of risk factors for Plasmodium falciparum infection in rural Burkina Faso could help to identify and target malaria control measures. A cross-sectional survey of 1,199 children and adults was conducted during the peak malaria transmission season in the Cascades Region of south-west Burkina Faso in 2017. Logistic regression was used to identify risk factors for microscopically confirmed P. falciparum infection. A malaria transmission dynamic model was used to determine the impact on malaria cases averted of administering SMC to children aged 5-15 year old. P. falciparum prevalence was 32.8% in the study population. Children aged 5 to < 10 years old were at 3.74 times the odds (95% CI = 2.68-5.22, P < 0.001) and children aged 10 to 15 years old at 3.14 times the odds (95% CI = 1.20-8.21, P = 0.02) of P. falciparum infection compared to children aged less than 5 years old. Administration of SMC to children aged up to 10 years is predicted to avert an additional 57 malaria cases per 1000 population per year (9.4% reduction) and administration to children aged up to 15 years would avert an additional 89 malaria cases per 1000 population per year (14.6% reduction) in the Cascades Region, assuming current coverage of pyrethroid-piperonyl butoxide ITNs. Malaria infections were high in all age strata, although highest in children aged 5 to 15 years, despite roll out of core malaria control interventions. Given the burden of infection in school-age children, extension of the eligibility criteria for SMC could help reduce the burden of malaria in Burkina Faso and other countries in the region.

Risk factors associated with house entry of malaria vectors in an area of Burkina Faso with high, persistent malaria transmission and high insecticide resistance.

BACKGROUND: In rural Burkina Faso, the primary malaria vector Anopheles gambiae sensu lato (s.l.) primarily feeds indoors at night. Identification of factors which influence mosquito house entry could lead to development of novel malaria vector control interventions. A study was therefore carried out to identify risk factors associated with house entry of An. gambiae s.l. in south-west Burkina Faso, an area of high insecticide resistance. METHODS: Mosquitoes were sampled monthly during the malaria transmission season using CDC light traps in 252 houses from 10 villages, each house sleeping at least one child aged five to 15 years old. Potential risk factors for house entry of An. gambiae s.l. were measured, including socio-economic status, caregiver's education and occupation, number of people sleeping in the same part of the house as the child, use of anti-mosquito measures, house construction and fittings, proximity of anopheline aquatic habitats and presence of animals near the house. Mosquito counts were compared using a generalized linear mixed-effect model with negative binomial and log link function, adjusting for repeated collections. RESULTS: 20,929 mosquitoes were caught, of which 16,270 (77.7%) were An. gambiae s.l. Of the 6691 An. gambiae s.l. identified to species, 4101 (61.3%) were An. gambiae sensu stricto and 2590 (38.7%) Anopheles coluzzii. Having a metal-roof on the child's sleeping space (IRR = 0.55, 95% CI 0.32-0.95, p = 0.03) was associated with fewer malaria vectors inside the home. CONCLUSION: This study demonstrated that the rate of An. gambiae s.l. was 45% lower in sleeping spaces with a metal roof, compared to those with thatch roofs. Improvements in house construction, including installation of metal roofs, should be considered in endemic areas of Africa to reduce the burden of malaria.