Increased proportions of outdoor feeding among residual malaria vector populations following increased use of insecticide-treated nets in rural Tanzania
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BACKGROUND: Insecticide-treated nets (ITNs) and indoor residual spraying (IRS) represent the front-line tools for malaria vector control globally, but are optimally effective where the majority of baseline transmission occurs indoors. In the surveyed area of rural southern Tanzania, bed net use steadily increased over the last decade, reducing malaria transmission intensity by 94%. METHODS: Starting before bed nets were introduced (1997), and then after two milestones of net use had been reached-75% community-wide use of untreated nets (2004) and then 47% use of ITNs (2009)-hourly biting rates of malaria vectors from the Anopheles gambiae complex and Anopheles funestus group were surveyed. RESULTS: In 1997, An. gambiae s.l. and An. funestus mosquitoes exhibited a tendency to bite humans inside houses late at night. For An. gambiae s.l., by 2009, nocturnal activity was less (p = 0.0018). At this time, the sibling species composition of the complex had shifted from predominantly An. gambiae s.s. to predominantly An. arabiensis. For An. funestus, by 2009, nocturnal activity was less (p = 0.0054) as well as the proportion biting indoors (p < 0.0001). At this time, An. funestus s.s. remained the predominant species within this group. As a consequence of these altered feeding patterns, the proportion (mean ± standard error) of human contact with mosquitoes (bites per person per night) occurring indoors dropped from 0.99 ± 0.002 in 1997 to 0.82 ± 0.008 in 2009 for the An. gambiae complex (p = 0.0143) and from 1.00 ± <0.001 to only 0.50 ± 0.048 for the An. funestus complex (p = 0.0004) over the same time period. CONCLUSIONS: High usage of ITNs can dramatically alter African vector populations so that intense, predominantly indoor transmission is replaced by greatly lowered residual transmission, a greater proportion of which occurs outdoors. Regardless of the underlying mechanism, the residual, self-sustaining transmission will respond poorly to further insecticidal measures within houses. Additional vector control tools which target outdoor biting mosquitoes at the adult or immature stages are required to complement ITNs and IRS.
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Some investigators attribute outdoor feeding by Anopheles coluzzii and Anopheles gambiae s.s. to a behavioural response to protracted use of pyrethroid-treated bed nets.
“Some investigators attribute this to a behavioural response by vectors to the protracted use of pyrethroid-treated bed nets [15, 16].”
From Sibling species of the major malaria vector Anopheles gambiae display divergent preferences for aquatic breeding sites in southern Nigeria (2024) · cites this paper as [16]
The Discussion (page unavailable) suggests that prolonged ITN use could favour outdoor biting through behavioural avoidance or selection, but it makes that suggestion for An. funestus s.s. For An. gambiae s.l., the Discussion instead identifies a shift in sibling-species composition as the most likely explanation; the paper does not address An. coluzzii or establish this response in An. gambiae s.s. (LLM, conf=0.84)
Experimental — accuracy not yet measuredWhen one considers the human population at risk of transmission outdoors, the niche for spatial repellents becomes increasingly evident due to the lack of current control products for those humans becoming infected in these areas.
“When one considers the human population at risk of transmission outdoors, the niche for spatial repellents becomes increasingly evident due to the lack of current control products for those humans becoming infected in these areas [34,35] (Figure 3).”
From Spatial repellents: from discovery and development to evidence-based validation (2012) · cites this paper as [35]
The Discussion says outdoor-biting mosquitoes respond poorly to measures used inside houses and that complementary tools, including repellents, are needed. It does not specifically identify spatial repellents or establish that no current products protect people exposed outdoors. (LLM, conf=0.82)
Experimental — accuracy not yet measuredEcological shifts in vector composition and shifts in vector behaviour have been reported.
“ecological shifts in vector composition and shifts in vector behaviour have been reported [19, 20].”
From Spatial temporal distribution of Anopheles mosquitoes in different ecological zones of Ghana (2026) · cites this paper as [19]
The observation of An. gambiae s.s in the Sahel zone, where more outdoor mosquitoes fed on humans, may suggest potential shifts in biting behaviour in Anopheles gambiae mosquitoes.
“The observation of An. gambiae s.s in the sahel zone, where more outdoor mosquitoes fed on humans, may suggest potential shifts in biting behaviour in Anopheles gambiae mosquitoes, as reported in other studies [19, 20, 33].”
From Spatial temporal distribution of Anopheles mosquitoes in different ecological zones of Ghana (2026) · cites this paper as [19]
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- Authors
- Russell, T. L., Govella, N. J., Azizi, S., Drakeley, C. J., Kachur, S. P., & Killeen, G. F.
- Affiliations
- Ifakara Health Institute (TZ)
- Centers for Disease Control and Prevention (US)
- Corresponding author
- Russell, Tanya L
- Venue
- Malaria Journal
- Published
- 2011-04-09
- Volume
- 10
- Issue
- 1
- Pages
- 80-80
- ISSN
- 1475-2875 (ISSN-L)
- PMC
- PMC3084176
- OpenAlex
- W2103610338
- Cited by
- 698
- References
- 55
- Citations by year
- 2026: 14 · 2025: 34 · 2024: 52 · 2023: 44 · 2022: 60 · 2021: 69 · 2020: 56 · 2019: 51 · 2018: 43 · 2017: 53 · 2016: 54 · 2015: 41 · 2014: 35 · 2013: 50 · 2012: 33
- FWCI
- 39.63
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Malaria Journal (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- LSTM Online Archive (Liverpool School of Tropical Medicine) (acceptedVersion)
- IHI Repository (acceptedVersion)
- LSHTM Research Online (London School of Hygiene and Tropical Medicine) (acceptedVersion)
- ResearchOnline at James Cook University (James Cook University) (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Funders
- Bill and Melinda Gates Foundation (45114, 51431)
- Wellcome Trust (076806)
- Topics
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Malaria Research and Control
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Mosquito-borne diseases and control
- Life Sciences › Immunology and Microbiology › Parasitology › Bird parasitology and diseases
- Keywords
- insecticide-treated nets, malaria vector control, Anopheles gambiae s.l., Anopheles funestus, Anopheles arabiensis, indoor biting, residual malaria transmission, bed net use, rural Tanzania, indoor residual spraying, malaria transmission intensity
- MeSH terms
- Animals, Anopheles, Feeding Behavior, Humans, Human Activities, Insect Vectors, Malaria, Mosquito Control, Rural Population, Tanzania, Insecticide-Treated Bednets
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