The DOI matches its Crossref record; 54 of the 55 references it cites were found in a registry or an index.
Increased proportions of outdoor feeding among residual malaria vector populations following increased use of insecticide-treated nets in rural Tanzania
Open accessAbstract
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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![Figure 3 The hourly indoor and outdoor profile of human contact with Anopheles gambiae s.l. (A - C) and Anopheles funestus (D - F) bites in the Kilombero Valley, Tanzania during 1997, 2004 and 2009. This stacked line graph presents estimates of human indoor and outdoor contact rates, taking into consideration the movement pattern of people by weighting the mean indoor and outdoor biting rates throughout the night by the proportion of humans that are typically indoors or outdoors at each time period [3]. The value of 1 was added to each mean to avoid zero values for presentation using a log scale.](/paper-figures/33c590dab3ae4e349bbcaef4968e2cf9/increased-proportions-of-outdoor-feeding-among-residual-malaria-vector-figure-3.jpg)
![Figure 5 The sibling species composition of the Anopheles gambiae s.l. complex (A) and monthly rainfall (B) between 2002 and 2009. For (A), the plotted line represents the predicted fit (β) of a GLM with a binary distribution and a logistic link function (Solid line = fitted; Dashed lines = se). References: 2002: [19]; 2003: [30]; 2005: [31]; 2007: [26,32]; 2008: [33] and Moore et al. Unpublished data; 2009: [34] and current data.](/paper-figures/49640f578a4f4eb5801501fe0d21d75a/increased-proportions-of-outdoor-feeding-among-residual-malaria-vector-figure-5.jpg)
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“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]
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“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]
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“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]
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“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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Citations
Cites
Insecticide-treated bed nets and curtains for preventing malaria
Lengeler, C. (2004) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd000363.pub2 · Cited by 1,700
Identification of Single Specimens of the Anopheles Gambiae Complex by the Polymerase Chain Reaction
Scott, J. A., Brogdon, W. G., & Collins, F. H. (1993) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.1993.49.520 · Cited by 1,634
Silver, J. B. (2007) · Springer eBooks · doi:10.1007/978-1-4020-6666-5 · Cited by 1,005
A supplement to the Anophelinae of Africa south of the Sahara (Afrotropical Region).
Gillies, M. T., & Coetzee, M. (1987) · IHI Repository · Cited by 812
The Anophelinae of Africa south of the Sahara (Ethiopian Zoogeographical Region).
Gillies, M. T., & Meillon, B. D. (1968) · Cited by 776
Habicht, J. (1999) · International Journal of Epidemiology · doi:10.1093/ije/28.1.10 · Cited by 729
Koekemoer, L. L., Kamau, L., Hunt, R. H., & Coetzee, M. (2002) · The American journal of tropical medicine and hygiene · doi:10.4269/ajtmh.2002.66.804 · Cited by 641
HAWLEY, W. A., PHILLIPS-HOWARD, P. A., TER KUILE, F. O., TERLOUW, D. J., VULULE, J. M., OMBOK, M., NAHLEN, B. L., GIMNIG, J. E., KARIUKI, S. K., KOLCZAK, M. S., et al. (2003) · The American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.2003.68.121 · Cited by 613
Griffin, J. T., Hollingsworth, T. D., Okell, L. C., Churcher, T. S., White, M., Hinsley, W., Bousema, T., Drakeley, C. J., Ferguson, N. M., Basáñez, M.-G., et al. (2010) · PLoS Medicine · doi:10.1371/journal.pmed.1000324 · Cited by 595
Self-citationChanges in the burden of malaria in sub-Saharan Africa
O’Meara, W. P., Mangeni, J. N., Steketee, R. W., & Greenwood, B. M. (2010) · The Lancet Infectious Diseases · doi:10.1016/s1473-3099(10)70096-7 · Cited by 517
Cited by
Sorted by citations
Host Preferences of Blood-Feeding Mosquitoes
Takken, W., & Verhulst, N. O. (2012) · Annual Review of Entomology · doi:10.1146/annurev-ento-120811-153618 · Cited by 705
Hitting Hotspots: Spatial Targeting of Malaria for Control and Elimination
Bousema, T., Griffin, J. T., Sauerwein, R. W., Smith, D. L., Churcher, T. S., Takken, W., Ghani, A. C., DRAKELEY, C. J., & Gosling, R. D. (2012) · PLoS Medicine · doi:10.1371/journal.pmed.1001165 · Cited by 566
Self-citationCharacterizing, controlling and eliminating residual malaria transmission
Killeen, G. F. (2014) · Malaria Journal · doi:10.1186/1475-2875-13-330 · Cited by 506
Self-citationDavid, J., Ismail, H. M., Chandor-Proust, A., & Paine, M. J. I. (2013) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2012.0429 · Cited by 417
Reddy, M. R., Overgaard, H. J., Abaga, S., Reddy, V. P., Caccone, A., Kiszewski, A. E., & Slotman, M. A. (2011) · Malaria Journal · doi:10.1186/1475-2875-10-184 · Cited by 390
Metadata
- 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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