Heterogeneous feeding patterns of the dengue vector, Aedes aegypti, on individual human hosts in rural Thailand

Abstract

Background: Mosquito biting frequency and how bites are distributed among different people can have significant epidemiologic effects. An improved understanding of mosquito vector-human interactions would refine knowledge of the entomological processes supporting pathogen transmission and could reveal targets for minimizing risk and breaking pathogen transmission cycles.

Methodology and principal findings: We used human DNA blood meal profiling of the dengue virus (DENV) vector, Aedes aegypti, to quantify its contact with human hosts and to infer epidemiologic implications of its blood feeding behavior. We determined the number of different people bitten, biting frequency by host age, size, mosquito age, and the number of times each person was bitten. Of 3,677 engorged mosquitoes collected and 1,186 complete DNA profiles, only 420 meals matched people from the study area, indicating that Ae. aegypti feed on people moving transiently through communities to conduct daily business. 10-13% of engorged mosquitoes fed on more than one person. No biting rate differences were detected between high- and low-dengue transmission seasons. We estimate that 43-46% of engorged mosquitoes bit more than one person within each gonotrophic cycle. Most multiple meals were from residents of the mosquito collection house or neighbors. People ≤ 25 years old were bitten less often than older people. Some hosts were fed on frequently, with three hosts bitten nine times. Interaction networks for mosquitoes and humans revealed biologically significant blood feeding hotspots, including community marketplaces.

Conclusion and significance: High multiple-feeding rates and feeding on community visitors are likely important features in the efficient transmission and rapid spread of DENV. These results help explain why reducing vector populations alone is difficult for dengue prevention and support the argument for additional studies of mosquito feeding behavior, which when integrated with a greater understanding of human behavior will refine estimates of risk and strategies for dengue control.

Figure 1. Human DNA concentration in mosquitoes over time expressed in hours and degree days (DD) for Ae. aegypti blood meals.

DD estimates were calculated as described previously .

Figure 2. Regression of female Ae. aegypti feeding on hosts of known mass (product of height×weight) in large field cage studies (July and January 2003).

Figure 3. Proportion of blood from multiple hosts detected in 430 amplified and matched blood meals over multiple villages, seasons and years in Mae Sot, Thailand.

Villages designations are: PL = Pailom, LB = Lao Bao, MD = Mae Dow.

Figure 4. Interaction networks for Pai Lom (bottom) and Lao Bao (top) during the rainy season of 2002.

Black lines represent roads. Dots represent the location of households, triangles indicate local markets and gray lines represent mosquito meals from one house connected to human hosts in another house.

Figure 5. Local clustering for house resident meals for Lao Bao (top) and Pai Lom (bottom) during the rainy season of 2002 with neighbors defined at 40 m and significance evaluated using 9,999 randomizations.

Red and blue indicate the presence of hot and cold spots, respectively. Triangle indicates the local market. Black lines represent roads.