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Cited by 698Malaria Research and ControlMosquito-borne diseases and controlBird parasitology and diseases

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Increased proportions of outdoor feeding among residual malaria vector populations following increased use of insecticide-treated nets in rural Tanzania

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Russell, Tanya L, Govella, Nicodem J, Azizi, Salum, Drakeley, Christopher J, Kachur, S Patrick, Killeen, Gerry F·2011·Malaria Journal
DOI 10.1186/1475-2875-10-80PMC PMC3084176
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Abstract

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 1 Kilombero and Ulanga districts (8.1°S and 36.6°E) in Tanzania showing Njagi and Lupiro villages.
Figure 1 Kilombero and Ulanga districts (8.1°S and 36.6°E) in Tanzania showing Njagi and Lupiro villages.CC BY · PubMed Central
Figure 2 The hourly indoor and outdoor biting profile of Anopheles gambiae s.l. (A - C) and Anopheles funestus (D - F) in the Kilombero Valley, Tanzania during 1997, 2004 and 2009. The grey shading represents the proportion of the human population indoors. The value of 1 was added to each mean to avoid zero values for presentation using a log scale.
Figure 2 The hourly indoor and outdoor biting profile of Anopheles gambiae s.l. (A - C) and Anopheles funestus (D - F) in the Kilombero Valley, Tanzania during 1997, 2004 and 2009. The grey shading represents the proportion of the human population indoors. The value of 1 was added to each mean to avoid zero values for presentation using a log scale.CC BY · PubMed Central
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.
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.CC BY · PubMed Central
Figure 4 Graphical comparison of the historical and recent estimates of the proportion of human contact with Anophelines occurring indoors (πi). The proportion of human contact with mosquito bites occurring indoor (πi) was calculated by taking into consideration the movement pattern of people using two methods: (A) 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 and (B) using the formula: (I21→05 hrs)/(I21→05 hrs + O05→21 hrs).
Figure 4 Graphical comparison of the historical and recent estimates of the proportion of human contact with Anophelines occurring indoors (πi). The proportion of human contact with mosquito bites occurring indoor (πi) was calculated by taking into consideration the movement pattern of people using two methods: (A) 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 and (B) using the formula: (I21→05 hrs)/(I21→05 hrs + O05→21 hrs).CC BY · PubMed Central
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.
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.CC BY · PubMed Central

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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
ORCID
Venue
Malaria Journal
Publisher
Springer Science and Business Media LLC
Published
2011-04-09
Volume
10
Issue
1
Pages
80-80
ISSN
1475-2875 (ISSN-L)
DOI
10.1186/1475-2875-10-80
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
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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