Volume 29, Number 4—April 2023
Effects of Seasonal Conditions on Abundance of Malaria Vector Anopheles stephensi Mosquitoes, Djibouti, 2018–2021
We describe the influence of seasonal meteorologic variations and rainfall events on Anopheles stephensi mosquito populations during a 40-month surveillance study at a US military base in Djibouti. Focusing surveillance and risk mitigation for An. stephensi mosquitoes when climatic conditions are optimal presents an opportunity for malaria prevention and control in eastern Africa.
Anopheles stephensi mosquitoes, an urban malaria vector, have established robust populations in the Horn of Africa. Since the mosquito’s detection in 2012 (1), malaria cases in Djibouti increased 42.9-fold during 2013–2021, reaching ≈72,300 cases (2). Before introduction of An. stephensi mosquitoes, Djibouti was approaching the preelimination phase for malaria (3). Because An. stephensi mosquitoes are competent vectors for Plasmodium falciparum and P. vivax parasites (3), WHO considers this mosquito species a major threat to malaria elimination in Africa (4). An. stephensi mosquitoes have also been detected in Sudan, Ethiopia, and Somalia (5–8). Understanding An. stephensi mosquito adaptation to environmental conditions affecting population dynamics in urban settings is crucial in Africa. An. stephensi mosquitoes abundance (number of mosquitoes collected per trap night) changed from seasonal during fall–spring 2013–2016 to year-round in 2017 (3). Since An. stephensi mosquitoes were introduced, malaria cases have increased among military personnel, some immunologically naive, deployed as members of multinational militaries in Djibouti (9). Camp Lemonnier (CLDJ), a US naval base, has urban characteristics similar to the city of Djibouti, in which it is located. For this study, we monitored vector dynamics on the base, providing data to help inform health protection strategies among both military and civilian populations.
In coordination with the CLDJ Expeditionary Medical Facility, during January 2018–April 2021, we conducted weekly mosquito surveillance at 32 on-base sites covering 2 km2 and stored information in dataset A. In October 2019, we began identifying monthly captures of An. stephensi mosquitoes specifically (i.e., identified at the species level) (dataset B). We set US Centers for Disease Control and Prevention (CDC) CO2-baited Miniature Light traps (https://www.cdc.gov/mosquitoes/guidelines/west-nile/surveillance/environmental-surveillance.html) and Woodstream Mosquito Magnet (MM) propane-generated CO2 traps (https://www.woodstream.com) overnight near dwellings, dining areas, sport facilities, and other areas frequented by humans. We identified Anopheles species on the basis of criteria published elsewhere (10,11). We analyzed abundance data in the context of specific weather events and seasonal climatic trends at the time of collection. We obtained meteorologic data from several sources (Appendix), using latitude 11.54733 N and longitude 43.15948 E (0.6–1.2 km from study sites) for location and a locally appropriate meteorologic calendar to determine seasons. We assessed the effects on An. stephensi mosquito abundance of monthly mean temperatures and rainfall amounts at time of precipitation and at 2-week, and 1- and 2-month lag times (i.e., time after rainfall). We did not consider longer lag times because of the likely effects of evaporation.
We used the Shapiro-Wilk test to check normal distribution of An. stephensi mosquito data and Pearson correlation coefficient to evaluate relationships between mosquito abundance and climatic variables. We categorized temperatures as either above or equal to or below median annual temperature (30°C). We grouped rainfall data according to frequency at each of 5 levels: 0, 0.2–4.9, 5–21, 21.1–39.9, and 40–155 mm/week. We used Poisson regression for univariate and multivariate analyses to determine associations between mosquito abundance and predictor variables, and used PROC GENMOD in SAS version 9.4 (SAS Institute, Inc., https://www.sas.com) to perform logistic regression. We expressed results in incidence rate ratios (IRR) and used p = 0.05 as the cutoff for statistical significance.
An. stephensi represented 95.6% of all Anopheles spp. mosquitoes we identified. Using dataset B to compare effectiveness of trap types, we found that MM traps captured 25.6% more An. stephensi mosquitoes than did CDC traps (IRR 2.3; p<0.0001) (Appendix Table, Figure). Univariate regression analysis of datasets A and B (Appendix Table) demonstrated that An. stephensi mosquito populations persisted year-round. Related to seasonal distribution, in dataset A, winter accounted for 56.4% of Anopheles spp. mosquito captures; spring, 28.1%; fall, 9.8%; and summer, 5.7%. In dataset B, winter accounted for 55.2% of An. stephensi mosquito captures; spring, 37.1%; fall, 6.9%; and summer, 0.8%. Associations between An. stephensi mosquito abundance and monthly mean temperatures (Figure 1) were positive for temperatures <30 (IRR 5.5 for dataset A, 7.4 for dataset B; p<0.0001). In dataset A, 85% of Anopheles spp. mosquitoes were collected at temperatures ≤30°C; for dataset B, the percentage was 94% of An. stephensi mosquitoes (Appendix Table).
Mosquito abundance increased 4–8 weeks after flooding in November 2019 (Figure 2). We also analyzed data on mosquito abundance 2 weeks and 1 and 2 months after rainfall throughout September 2019–August 2020, during which time 2 floods occurred (Table 1). Regression analysis showed significant associations between rainfall and Anopheles mosquito abundance recorded 2 weeks (IRR 2.4), 1 month (IRR 2.99), and 2 months (IRR 2.75) after periods of rainfall 21.1–39.9 mm/week (p<0.0001), corresponding to average mosquito counts of 9.6 (2 weeks), 11.3 (1 month), and 11.0 (2 months) after the rainfall. Unexpectedly, mosquito abundance also increased significantly 2 weeks (IRR 2.59), 1 month (IRR 2.58), and 2 months (IRR 2.00; p <0.0001) after periods of rainfall of just 0.2–4.9 mm/week. Multivariate analysis indicated that season and temperature were the variables most significantly associated with mosquito abundance when analyzed with no lag or 1-month rainfall lag effect. Winter (IRR 4.2 [no lag], 4.1 [1-month lag]; p<0.0001) and spring (IRR 2.8 [no lag], 2.9 [1-month lag]; p<0.0001) were the factors most associated with increases in Anopheles mosquitoes, followed by temperatures ≤30°C (IRR 2.4 [no lag], 2.2 [1-month lag]; p<0.0001) (Table 2).
We speculate that the slow continuous release of CO2 of MM traps contributed to higher captures of An. stephensi mosquitoes than for CDC traps. In a study in Malaysia, MM traps performed 3-fold better than CDC traps for capturing Anopheles spp. mosquitoes (12), demonstrating the suitability of MM traps for An. stephensi mosquito surveillance in urban settings and areas with limited or no access to dry ice (13).
An. stephensi mosquitoes were present year-round but at substantially higher populations during winter (mean temperature 26°C, average rainfall 2.3 mm/week) and spring (mean temperature 29°C, average rainfall 7.3 mm/week). A previous study observed a similar link between temperature and An. stephensi mosquito populations, with 29°C assessed as optimal (14). We linked the bionomics of An. stephensi mosquito abundance in urban areas to human-modified conditions, such as air conditioning–produced condensation, water storage tanks, open jerry cans, and water-filled tires following rainfall, all of which increased favorable mosquito habitats (1) and in which we observed larval habitats around CLDJ. Flash flooding in Djibouti did not increase An. stephensi mosquito abundance. In fact, flooding might have destroyed laid eggs, hatched larvae, and temporary larval habitats, as was reported in China (15), possibly explaining higher population growth after periods of rainfall of 21.1–39.9 mm/week than 40–155 mm/week. Because breeding sites in urban areas depend as much on human-generated water sources as rainfall, adult mosquitoes were able to persist even during periods of low precipitation (14). We found that periods of rainfall at 21.1–39.9 mm/week and temperatures slightly <30°C were optimal for adult An. stephensi mosquito abundance. Therefore, surveillance and control efforts should be most intense during times of the year when these conditions are common. However, because An. stephensi mosquitoes are present year-round, prevention and control measures cannot be relaxed during any season (Appendix).
Although our study was set at CLDJ facilities, conditions were comparable to other urban settings in Djibouti, which should encourage local health authorities to benefit from our data. The persistence of mosquito populations at CLDJ, which regularly monitors and employs control efforts, should raise the alarm for increased malaria risk in densely populated city areas with fewer public health and disease control resources. Given limited resources, we recommend targeted reduction of An. stephensi larval habitat in this area.
Dr. Zayed is an entomologist at the US Naval Medical Research Unit-3, Cairo, with academic and research involvement in Middle Eastern countries. Her primary research interests are vector surveillance and control.
We are greatly indebted to Expeditionary Medical Facility HM1 (hospital corpsman first class) Bicomong, HM2 Fletcher, HM2 McClinton, HM2 Foley, HM3 Begley, J. Flores, and Camp Lemonnier Djibouti for support in collecting and identifying mosquitoes.
This work was financially supported by Armed Forces Health Surveillance Division, Global Emerging Infections Surveillance (GEIS) Branch: P0137_20_N3_05.02 and P0042_21_N3.
Views expressed in this article reflect the results of research conducted by the author and do not necessarily reflect official policies or positions of the US Department of the Navy, Department of Defense, or federal government. Authors are military service members or federal/contracted employees of the US government. This work was prepared as part of official duties. Title 17 U.S.C. 105 provides that copyright protection under this title is not available for any work of the US government. Title 17 U.S.C. 101 defines a US government work as work prepared by a military service member or employee of the US government as part of that person's official duties.
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TablesCite This Article
Original Publication Date: March 16, 2023
Table of Contents – Volume 29, Number 4—April 2023
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Address of correspondence: Alia Zayed, US Naval Medical Research Unit No. 3, Cairo Detachment, Cairo, Egypt