Estimating the annual entomological inoculation rate for Plasmodium falciparum transmitted by Anopheles gambiae s.l. using three sampling methods in three sites in Uganda

Maxwell Kilama, David L. Smith, Robert Hutchinson, Ruth Kigozi, Adoke Yeka, Geoff Lavoy, Moses R. Kamya, Sarah G. Staedke, Martin J. Donnelly, Chris Drakeley, Bryan Greenhouse, Grant Dorsey, Steve W. Lindsay

Research output: Contribution to journalArticle

Abstract

Background: The Plasmodium falciparum entomological inoculation rate (PfEIR) is a measure of exposure to infectious mosquitoes. It is usually interpreted as the number of P. falciparum infective bites received by an individual during a season or annually (aPfEIR). In an area of perennial transmission, the accuracy, precision and seasonal distribution (i.e., month by month) of aPfEIR were investigated. Data were drawn from three sites in Uganda with differing levels of transmission where falciparum malaria is transmitted mainly by Anopheles gambiae s.l. Estimates of aPfEIR derived from human-landing catches - the classic method for estimating biting rates - were compared with data from CDC light traps, and with catches of knock down and exit traps separately and combined. Methods. Entomological surveillance was carried out over one year in 2011/12 in three settings: Jinja, a peri-urban area with low transmission; Kanungu, a rural area with moderate transmission; and Nagongera, Tororo District, a rural area with exceptionally high malaria transmission. Three sampling approaches were used from randomly selected houses with collections occurring once a month: human-landing collections (eight houses), CDC light traps (100 houses) and paired knock-down and exit traps each month (ten houses) for each setting. Up to 50 mosquitoes per month from each household were tested for sporozoites with P. falciparum by ELISA. Human biting rate (HBR) data were estimated month by month. P. falciparum Sporozoite rate (PfSR) for yearly and monthly data and confidence intervals were estimated using the binomial exact test. Monthly and yearly estimates of the HBR, the PfSR, and the PfEIR were estimated and compared. Results: The estimated aPfEIR values using human-landing catch data were 3.8 (95% Confidence Intervals, CI 0-11.4) for Jinja, 26.6 (95% CI 7.6-49.4) for Kanungu, and 125 (95% CI 72.2-183.0) for Tororo. In general, the monthly PfEIR values showed strong seasonal signals with two peaks from May-June and October-December, although the precise timing of the peaks differed between sites. Estimated HBRs using human-landing catches were strongly correlated with those made using CDC light traps (r2 = 0.67, p <0.001), and with either knock-down catches (r2 = 0.56, p <0.001) and exit traps (r2 = 0.82, p <0.001) or the combined catches (r2 = 0.73, p <0.001). Using CDC light trap catch data, the PfSR in Tororo was strongly negatively correlated with monthly HBR (r 2 = 0.44, p = 0.01). In other sites, no patterns in the PfSR were discernible because either the number P. falciparum of sporozoite positive mosquitoes or the total number of mosquitoes caught was too low. Conclusions: In these settings, light traps provide an alternative method for sampling indoor-resting mosquitoes to human-landing catches and have the advantage that they protect individuals from being bitten during collection, are easy to use and are not subject to collector bias. Knock-down catches and exit traps could also be used to replace human-landing catches. Although these are cheaper, they are subject to collector bias.

Original languageEnglish (US)
Article number111
JournalMalaria Journal
Volume13
Issue number1
DOIs
StatePublished - Mar 21 2014

Fingerprint

Anopheles gambiae
Uganda
Plasmodium falciparum
Sporozoites
Culicidae
Centers for Disease Control and Prevention (U.S.)
Light
Confidence Intervals
Falciparum Malaria
Bites and Stings
Malaria
Enzyme-Linked Immunosorbent Assay

Keywords

  • Anopheles gambiae s.l
  • CDC light traps
  • Entomological inoculation rate
  • Human-landing catches
  • Malaria
  • Plasmodium falciparum
  • Uganda

ASJC Scopus subject areas

  • Infectious Diseases
  • Parasitology

Cite this

Estimating the annual entomological inoculation rate for Plasmodium falciparum transmitted by Anopheles gambiae s.l. using three sampling methods in three sites in Uganda. / Kilama, Maxwell; Smith, David L.; Hutchinson, Robert; Kigozi, Ruth; Yeka, Adoke; Lavoy, Geoff; Kamya, Moses R.; Staedke, Sarah G.; Donnelly, Martin J.; Drakeley, Chris; Greenhouse, Bryan; Dorsey, Grant; Lindsay, Steve W.

In: Malaria Journal, Vol. 13, No. 1, 111, 21.03.2014.

Research output: Contribution to journalArticle

Kilama, M, Smith, DL, Hutchinson, R, Kigozi, R, Yeka, A, Lavoy, G, Kamya, MR, Staedke, SG, Donnelly, MJ, Drakeley, C, Greenhouse, B, Dorsey, G & Lindsay, SW 2014, 'Estimating the annual entomological inoculation rate for Plasmodium falciparum transmitted by Anopheles gambiae s.l. using three sampling methods in three sites in Uganda', Malaria Journal, vol. 13, no. 1, 111. https://doi.org/10.1186/1475-2875-13-111
Kilama, Maxwell ; Smith, David L. ; Hutchinson, Robert ; Kigozi, Ruth ; Yeka, Adoke ; Lavoy, Geoff ; Kamya, Moses R. ; Staedke, Sarah G. ; Donnelly, Martin J. ; Drakeley, Chris ; Greenhouse, Bryan ; Dorsey, Grant ; Lindsay, Steve W. / Estimating the annual entomological inoculation rate for Plasmodium falciparum transmitted by Anopheles gambiae s.l. using three sampling methods in three sites in Uganda. In: Malaria Journal. 2014 ; Vol. 13, No. 1.
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abstract = "Background: The Plasmodium falciparum entomological inoculation rate (PfEIR) is a measure of exposure to infectious mosquitoes. It is usually interpreted as the number of P. falciparum infective bites received by an individual during a season or annually (aPfEIR). In an area of perennial transmission, the accuracy, precision and seasonal distribution (i.e., month by month) of aPfEIR were investigated. Data were drawn from three sites in Uganda with differing levels of transmission where falciparum malaria is transmitted mainly by Anopheles gambiae s.l. Estimates of aPfEIR derived from human-landing catches - the classic method for estimating biting rates - were compared with data from CDC light traps, and with catches of knock down and exit traps separately and combined. Methods. Entomological surveillance was carried out over one year in 2011/12 in three settings: Jinja, a peri-urban area with low transmission; Kanungu, a rural area with moderate transmission; and Nagongera, Tororo District, a rural area with exceptionally high malaria transmission. Three sampling approaches were used from randomly selected houses with collections occurring once a month: human-landing collections (eight houses), CDC light traps (100 houses) and paired knock-down and exit traps each month (ten houses) for each setting. Up to 50 mosquitoes per month from each household were tested for sporozoites with P. falciparum by ELISA. Human biting rate (HBR) data were estimated month by month. P. falciparum Sporozoite rate (PfSR) for yearly and monthly data and confidence intervals were estimated using the binomial exact test. Monthly and yearly estimates of the HBR, the PfSR, and the PfEIR were estimated and compared. Results: The estimated aPfEIR values using human-landing catch data were 3.8 (95{\%} Confidence Intervals, CI 0-11.4) for Jinja, 26.6 (95{\%} CI 7.6-49.4) for Kanungu, and 125 (95{\%} CI 72.2-183.0) for Tororo. In general, the monthly PfEIR values showed strong seasonal signals with two peaks from May-June and October-December, although the precise timing of the peaks differed between sites. Estimated HBRs using human-landing catches were strongly correlated with those made using CDC light traps (r2 = 0.67, p <0.001), and with either knock-down catches (r2 = 0.56, p <0.001) and exit traps (r2 = 0.82, p <0.001) or the combined catches (r2 = 0.73, p <0.001). Using CDC light trap catch data, the PfSR in Tororo was strongly negatively correlated with monthly HBR (r 2 = 0.44, p = 0.01). In other sites, no patterns in the PfSR were discernible because either the number P. falciparum of sporozoite positive mosquitoes or the total number of mosquitoes caught was too low. Conclusions: In these settings, light traps provide an alternative method for sampling indoor-resting mosquitoes to human-landing catches and have the advantage that they protect individuals from being bitten during collection, are easy to use and are not subject to collector bias. Knock-down catches and exit traps could also be used to replace human-landing catches. Although these are cheaper, they are subject to collector bias.",
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TY - JOUR

T1 - Estimating the annual entomological inoculation rate for Plasmodium falciparum transmitted by Anopheles gambiae s.l. using three sampling methods in three sites in Uganda

AU - Kilama, Maxwell

AU - Smith, David L.

AU - Hutchinson, Robert

AU - Kigozi, Ruth

AU - Yeka, Adoke

AU - Lavoy, Geoff

AU - Kamya, Moses R.

AU - Staedke, Sarah G.

AU - Donnelly, Martin J.

AU - Drakeley, Chris

AU - Greenhouse, Bryan

AU - Dorsey, Grant

AU - Lindsay, Steve W.

PY - 2014/3/21

Y1 - 2014/3/21

N2 - Background: The Plasmodium falciparum entomological inoculation rate (PfEIR) is a measure of exposure to infectious mosquitoes. It is usually interpreted as the number of P. falciparum infective bites received by an individual during a season or annually (aPfEIR). In an area of perennial transmission, the accuracy, precision and seasonal distribution (i.e., month by month) of aPfEIR were investigated. Data were drawn from three sites in Uganda with differing levels of transmission where falciparum malaria is transmitted mainly by Anopheles gambiae s.l. Estimates of aPfEIR derived from human-landing catches - the classic method for estimating biting rates - were compared with data from CDC light traps, and with catches of knock down and exit traps separately and combined. Methods. Entomological surveillance was carried out over one year in 2011/12 in three settings: Jinja, a peri-urban area with low transmission; Kanungu, a rural area with moderate transmission; and Nagongera, Tororo District, a rural area with exceptionally high malaria transmission. Three sampling approaches were used from randomly selected houses with collections occurring once a month: human-landing collections (eight houses), CDC light traps (100 houses) and paired knock-down and exit traps each month (ten houses) for each setting. Up to 50 mosquitoes per month from each household were tested for sporozoites with P. falciparum by ELISA. Human biting rate (HBR) data were estimated month by month. P. falciparum Sporozoite rate (PfSR) for yearly and monthly data and confidence intervals were estimated using the binomial exact test. Monthly and yearly estimates of the HBR, the PfSR, and the PfEIR were estimated and compared. Results: The estimated aPfEIR values using human-landing catch data were 3.8 (95% Confidence Intervals, CI 0-11.4) for Jinja, 26.6 (95% CI 7.6-49.4) for Kanungu, and 125 (95% CI 72.2-183.0) for Tororo. In general, the monthly PfEIR values showed strong seasonal signals with two peaks from May-June and October-December, although the precise timing of the peaks differed between sites. Estimated HBRs using human-landing catches were strongly correlated with those made using CDC light traps (r2 = 0.67, p <0.001), and with either knock-down catches (r2 = 0.56, p <0.001) and exit traps (r2 = 0.82, p <0.001) or the combined catches (r2 = 0.73, p <0.001). Using CDC light trap catch data, the PfSR in Tororo was strongly negatively correlated with monthly HBR (r 2 = 0.44, p = 0.01). In other sites, no patterns in the PfSR were discernible because either the number P. falciparum of sporozoite positive mosquitoes or the total number of mosquitoes caught was too low. Conclusions: In these settings, light traps provide an alternative method for sampling indoor-resting mosquitoes to human-landing catches and have the advantage that they protect individuals from being bitten during collection, are easy to use and are not subject to collector bias. Knock-down catches and exit traps could also be used to replace human-landing catches. Although these are cheaper, they are subject to collector bias.

AB - Background: The Plasmodium falciparum entomological inoculation rate (PfEIR) is a measure of exposure to infectious mosquitoes. It is usually interpreted as the number of P. falciparum infective bites received by an individual during a season or annually (aPfEIR). In an area of perennial transmission, the accuracy, precision and seasonal distribution (i.e., month by month) of aPfEIR were investigated. Data were drawn from three sites in Uganda with differing levels of transmission where falciparum malaria is transmitted mainly by Anopheles gambiae s.l. Estimates of aPfEIR derived from human-landing catches - the classic method for estimating biting rates - were compared with data from CDC light traps, and with catches of knock down and exit traps separately and combined. Methods. Entomological surveillance was carried out over one year in 2011/12 in three settings: Jinja, a peri-urban area with low transmission; Kanungu, a rural area with moderate transmission; and Nagongera, Tororo District, a rural area with exceptionally high malaria transmission. Three sampling approaches were used from randomly selected houses with collections occurring once a month: human-landing collections (eight houses), CDC light traps (100 houses) and paired knock-down and exit traps each month (ten houses) for each setting. Up to 50 mosquitoes per month from each household were tested for sporozoites with P. falciparum by ELISA. Human biting rate (HBR) data were estimated month by month. P. falciparum Sporozoite rate (PfSR) for yearly and monthly data and confidence intervals were estimated using the binomial exact test. Monthly and yearly estimates of the HBR, the PfSR, and the PfEIR were estimated and compared. Results: The estimated aPfEIR values using human-landing catch data were 3.8 (95% Confidence Intervals, CI 0-11.4) for Jinja, 26.6 (95% CI 7.6-49.4) for Kanungu, and 125 (95% CI 72.2-183.0) for Tororo. In general, the monthly PfEIR values showed strong seasonal signals with two peaks from May-June and October-December, although the precise timing of the peaks differed between sites. Estimated HBRs using human-landing catches were strongly correlated with those made using CDC light traps (r2 = 0.67, p <0.001), and with either knock-down catches (r2 = 0.56, p <0.001) and exit traps (r2 = 0.82, p <0.001) or the combined catches (r2 = 0.73, p <0.001). Using CDC light trap catch data, the PfSR in Tororo was strongly negatively correlated with monthly HBR (r 2 = 0.44, p = 0.01). In other sites, no patterns in the PfSR were discernible because either the number P. falciparum of sporozoite positive mosquitoes or the total number of mosquitoes caught was too low. Conclusions: In these settings, light traps provide an alternative method for sampling indoor-resting mosquitoes to human-landing catches and have the advantage that they protect individuals from being bitten during collection, are easy to use and are not subject to collector bias. Knock-down catches and exit traps could also be used to replace human-landing catches. Although these are cheaper, they are subject to collector bias.

KW - Anopheles gambiae s.l

KW - CDC light traps

KW - Entomological inoculation rate

KW - Human-landing catches

KW - Malaria

KW - Plasmodium falciparum

KW - Uganda

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