Interventions that effectively target Anopheles funestus mosquitoes could significantly improve control of persistent malaria transmission in south-eastern Tanzania

PLoS One. 2017 May 18;12(5):e0177807. doi: 10.1371/journal.pone.0177807. eCollection 2017.

Abstract

Malaria is transmitted by many Anopheles species whose proportionate contributions vary across settings. We re-assessed the roles of Anopheles arabiensis and Anopheles funestus, and examined potential benefits of species-specific interventions in an area in south-eastern Tanzania, where malaria transmission persists, four years after mass distribution of long-lasting insecticide-treated nets (LLINs). Monthly mosquito sampling was done in randomly selected households in three villages using CDC light traps and back-pack aspirators, between January-2015 and January-2016, four years after the last mass distribution of LLINs in 2011. Multiplex polymerase chain reaction (PCR) was used to identify members of An. funestus and Anopheles gambiae complexes. Enzyme-linked immunosorbent assay (ELISA) was used to detect Plasmodium sporozoites in mosquito salivary glands, and to identify sources of mosquito blood meals. WHO susceptibility assays were done on wild caught female An. funestus s.l, and physiological ages approximated by examining mosquito ovaries for parity. A total of 20,135 An. arabiensis and 4,759 An. funestus were collected. The An. funestus group consisted of 76.6% An. funestus s.s, 2.9% An. rivulorum, 7.1% An. leesoni, and 13.4% unamplified samples. Of all mosquitoes positive for Plasmodium, 82.6% were An. funestus s.s, 14.0% were An. arabiensis and 3.4% were An. rivulorum. An. funestus and An. arabiensis contributed 86.21% and 13.79% respectively, of annual entomological inoculation rate (EIR). An. arabiensis fed on humans (73.4%), cattle (22.0%), dogs (3.1%) and chicken (1.5%), but An. funestus fed exclusively on humans. The An. funestus populations were 100% susceptible to organophosphates, pirimiphos methyl and malathion, but resistant to permethrin (10.5% mortality), deltamethrin (18.7%), lambda-cyhalothrin (18.7%) and DDT (26.2%), and had reduced susceptibility to bendiocarb (95%) and propoxur (90.1%). Parity rate was higher in An. funestus (65.8%) than An. arabiensis (44.1%). Though An. arabiensis is still the most abundant vector species here, the remaining malaria transmission is predominantly mediated by An. funestus, possibly due to high insecticide resistance and high survival probabilities. Interventions that effectively target An. funestus mosquitoes could therefore significantly improve control of persistent malaria transmission in south-eastern Tanzania.

MeSH terms

  • Animals
  • Anopheles / physiology*
  • Endemic Diseases / prevention & control
  • Female
  • Insect Vectors / physiology*
  • Insecticides / pharmacology
  • Malaria / epidemiology
  • Malaria / prevention & control*
  • Malaria / transmission*
  • Mosquito Control*
  • Parity / drug effects
  • Plasmodium malariae / physiology
  • Sporozoites / drug effects
  • Sporozoites / physiology
  • Survival Analysis
  • Tanzania / epidemiology

Substances

  • Insecticides

Grant support

EK was supported by Wellcome Trust and the Association of Physicians of Great Britain and Ireland for funding this research (Grant Number: 100540/Z/12/Z), EK is also supported by the Consortium for Advanced Research Training in Africa (CARTA), which is jointly led by the African Population and Health Research Center and the University of the Witwatersrand and funded by the Wellcome Trust (UK) (Grant No: 087547/Z/08/Z), the Carnegie Corporation of New York (Grant No--B 8606.R02), Sida (Grant No:54100029)), NSM received financial supports from Wellcome Masters Fellowship, Grant number: WT104029/Z/14/Z. FOO is also supported by a Wellcome Trust Intermediate Research Fellowship (Grant number: WT102350/Z/13/Z) and a grant from World Health Organization, Special Program for Research and Training in Tropical Diseases (Grant No. B40445). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.