Loss of Household Protection from Use of Insecticide-Treated Nets against Pyrethroid-Resistant Mosquitoes, Benin

Alex Asidi, Raphael N’Guessan, Martin Akogbeto, Chris Curtis¹, and Mark Rowland

Author affiliations: London School of Hygiene & Tropical Medicine, London, UK (A. Asidi, R. N’Guessan, C. Curtis, M. Rowland); and; Centre de Recherche Entomologique de Cotonou, Cotonou, Benin (A. Asidi, R. N’Guessan, M. Akogbeto)

Abstract

Pyrethroid resistance is becoming widespread in Anopheles gambiae mosquitoes, coinciding with expanded use of insecticide-treated nets (ITNs) throughout Africa. To investigate whether nets in use are still protective, we conducted household trials in northern and southern Benin, where An. gambiae mosquitoes are susceptible and resistant, respectively, to pyrethroids. Rooms were fitted with window traps and monitored for mosquito biting and survival rates before and after the nets were treated with pyrethroid. Sleeping under an ITN in the location with resistant mosquitoes was no more protective than sleeping under an untreated net, regardless of its physical condition. By contrast, sleeping under an ITN in the location with susceptible mosquitoes decreased the odds of biting by 66%. ITNs provide little or no protection once the mosquitoes become resistant and the netting acquires holes. Resistance seriously threatens malaria control strategies based on ITN.

Insecticide-treated nets (ITNs) and long-lasting insecticidal nets (LLINs) are the primary interventions for preventing malaria in sub-Saharan Africa (1,2). Nets accumulate holes through wear and tear during the course of everyday use, but the pyrethroid treatment continues to provide personal protection and to reduce vector capacity through excito-repellency and the killing of mosquitoes that contact the net (3,4). During the last decade, pyrethroid resistance in Anopheles gambiae mosquitoes became widespread in western Africa and spread to or developed in eastern Africa (5–9). As coverage of LLINs expands across the continent under programs supported by the President’s Malaria Initiative and Global Fund (10), resistance will inevitably increase (11–13).

Although resistance is perceived as a serious threat to the future of malaria control, the current distribution of resistance is patchy, and its severity seems to differ from 1 location to another. In the western African country of Benin, pyrethroid resistance has evolved in the M (Mopti) molecular form of An. gambiae mosquitoes that appears to combine the knockdown resistance (kdr) gene with oxidase mechanisms (14,15). Carriers of this resistance were not controlled by pyrethroid treatments in experimental hut trials of ITNs or the leading brands of LLINs, PermaNet 2.0 (Vestergaard Frandsen SA, Aarhus, Denmark) and Olyset (Sumitomo Chemicals, Osaka, Japan) (16,17). However, further west in Côte d’Ivoire, the kdr in An. gambiae S (Savannah) form mosquitoes conferred only limited resistance, and trials of ITNs continued to protect against mosquito blood feeding (biting) and malaria transmission by this species (18–20).

Results from experimental hut trials in Benin raise an alarm. Of key concern is whether ITNs that are subject to wear and tear under everyday household conditions fail to protect ITN users now that An. gambiae mosquitoes are becoming resistant. Modern mosquito nets lack physical durability, and household nets can accrue an average of 12–20 holes during 1–2 years of use (21). Net replacement schemes struggle to meet demand at this level of deterioration and attrition. To assess protection conferred by in-use polyester nets, we compared nets in households of northern Benin, where An. gambiae mosquitoes are mostly susceptible to pyrethroids, with nets in households of southern Benin, where An. gambiae mosquitoes are mostly resistant (7,16,22). Residents of the selected households were all regular users of nets.