Infected Mosquitoes Have Altered Behavior to Repellents: A Systematic Review and Meta-analysis

Lajeunesse, M. J. and Avello, D. A. and Behrmann, M. S. and Buschbacher, T. J. and Carey, K. and Carroll, J. and Chafin, T. J. and Elkott, F. and Faust, A. M. and Fauver, H. and Figueroa, G. D. and Flaig, L. L. and Gauta, S. A. and Gonzalez, C. and Graham, R. M. and Hamdan, K. and Hanlon, T. and Hashami, S. N. and Huynh, D. and Knaffl, J. L. and Lanzas, M. and Libell, N. M. and McCabe, C. and Metzger, J. and Mitchell, I. and Morales, M. A. and Nayyar, Y. R. and Perkins, A. and Phan, T. A. and Pidgeon, N. T. and Ritter, C. L. and Rosales, V. C. and Santiago, O. and Stephens, R. and Taylor, E. J. and Thomas, A. J. and Yanez, N. E.

J Med Entomol (2020) 57: 542–550

DOI: 10.1093/jme/tjz209

Abstract

Here we conducted a systematic review and meta-analysis to reach a consensus on whether infected and uninfected mosquitoes respond differently to repellents. After screening 2,316 published studies, theses, and conference abstracts, we identified 18 studies that tested whether infection status modulated the effectiveness of repellents. Thirteen of these studies had outcomes available for meta-analysis, and overall, seven repellents were tested (typically DEET with 62% of outcomes), six mosquito species had repellence behaviors measured (typically Aedes aegypti (L.) (Diptera: Culicidae) mosquitoes with 71% of outcomes), and a broad diversity of infections were tested including Sindbis virus (Togaviridae: Alphavirus) (33% of outcomes), Dengue (Flaviviridae: Flavivirus) (31%), malaria (Plasmodium berghei Vincke & Lips (Haemospororida: Plasmodiidae) or P. falciparum Welch (Haemospororida: Plasmodiidae); 25%), Zika (Flaviviridae: Flavivirus) (7%), and microsporidia (4%). Pooling all outcomes with meta-analysis, we found that repellents were less effective against infected mosquitoes-marking an average 62% reduction in protective efficacy relative to uninfected mosquitoes (pooled odds ratio = 0.38, 95% confidence interval = 0.22-0.66; k = 96). Older infected mosquitoes were also more likely to show altered responses and loss of sensitivity to repellents, emphasizing the challenge of distinguishing between age or incubation period effects. Plasmodium- or Dengue-infected mosquitoes also did not show altered responses to repellents; however, Dengue-mosquito systems used inoculation practices that can introduce variability in repellency responses. Given our findings that repellents offer less protection against infected mosquitoes and that these vectors are the most dangerous in terms of disease transmission, then trials on repellent effectiveness should incorporate infected mosquitoes to improve predictability in blocking vector-human contact.

Citation

Lajeunesse, M. J., Avello, D. A., Behrmann, M. S., Buschbacher, T. J., Carey, K., Carroll, J., Chafin, T. J., Elkott, F., Faust, A. M., Fauver, H., Figueroa, G. D., Flaig, L. L., Gauta, S. A., Gonzalez, C., Graham, R. M., Hamdan, K., Hanlon, T., Hashami, S. N., Huynh, D., … Yanez, N. E. (2020). Infected Mosquitoes Have Altered Behavior to Repellents: A Systematic Review and Meta-analysis. J Med Entomol, 57(2), 542–550. https://doi.org/10.1093/jme/tjz209 Animals, *feeding behavior, *malaria, *mosquito repellent and attractant, *mosquito-borne disease, Aedes/*drug effects/parasitology/physiology/virology, Anopheles/*drug effects/parasitology/physiology/virology, Culex/*drug effects/parasitology/physiology/virology, Insect Repellents/*pharmacology, Mosquito Control/*statistics & numerical data, Mosquito Vectors/*drug effects/parasitology/physiology/virology

Keywords

• Animals
• *feeding behavior
• *malaria
• *mosquito repellent and attractant
• *mosquito-borne disease
• Aedes/*drug effects/parasitology/physiology/virology
• Anopheles/*drug effects/parasitology/physiology/virology
• Culex/*drug effects/parasitology/physiology/virology
• Insect Repellents/*pharmacology
• Mosquito Control/*statistics & numerical data
• Mosquito Vectors/*drug effects/parasitology/physiology/virology