Skip to main content
Top
Published in: Malaria Journal 1/2013

Open Access 01-12-2013 | Research

Standardizing operational vector sampling techniques for measuring malaria transmission intensity: evaluation of six mosquito collection methods in western Kenya

Authors: Jacklyn Wong, Nabie Bayoh, George Olang, Gerry F Killeen, Mary J Hamel, John M Vulule, John E Gimnig

Published in: Malaria Journal | Issue 1/2013

Login to get access

Abstract

Background

Operational vector sampling methods lack standardization, making quantitative comparisons of malaria transmission across different settings difficult. Human landing catch (HLC) is considered the research gold standard for measuring human-mosquito contact, but is unsuitable for large-scale sampling. This study assessed mosquito catch rates of CDC light trap (CDC-LT), Ifakara tent trap (ITT), window exit trap (WET), pot resting trap (PRT), and box resting trap (BRT) relative to HLC in western Kenya to 1) identify appropriate methods for operational sampling in this region, and 2) contribute to a larger, overarching project comparing standardized evaluations of vector trapping methods across multiple countries.

Methods

Mosquitoes were collected from June to July 2009 in four districts: Rarieda, Kisumu West, Nyando, and Rachuonyo. In each district, all trapping methods were rotated 10 times through three houses in a 3 × 3 Latin Square design. Anophelines were identified by morphology and females classified as fed or non-fed. Anopheles gambiae s.l. were further identified as Anopheles gambiae s.s. or Anopheles arabiensis by PCR. Relative catch rates were estimated by negative binomial regression.

Results

When data were pooled across all four districts, catch rates (relative to HLC indoor) for An. gambiae s.l (95.6% An. arabiensis, 4.4% An. gambiae s.s) were high for HLC outdoor (RR = 1.01), CDC-LT (RR = 1.18), and ITT (RR = 1.39); moderate for WET (RR = 0.52) and PRT outdoor (RR = 0.32); and low for all remaining types of resting traps (PRT indoor, BRT indoor, and BRT outdoor; RR < 0.08 for all). For Anopheles funestus, relative catch rates were high for ITT (RR = 1.21); moderate for HLC outdoor (RR = 0.47), CDC-LT (RR = 0.69), and WET (RR = 0.49); and low for all resting traps (RR < 0.02 for all). At finer geographic scales, however, efficacy of each trap type varied from district to district.

Conclusions

ITT, CDC-LT, and WET appear to be effective methods for large-scale vector sampling in western Kenya. Ultimately, choice of collection method for operational surveillance should be driven by trap efficacy and scalability, rather than fine-scale precision with respect to HLC. When compared with recent, similar trap evaluations in Tanzania and Zambia, these data suggest that traps which actively lure host-seeking females will be most useful for surveillance in the face of declining vector densities.
Appendix
Available only for authorised users
Literature
1.
go back to reference Beier JC, Killeen GF, Githure J: Entomologic inoculation rates and Plasmodium falciparum malaria prevalence in Africa. Am J Trop Med Hyg. 1999, 61: 109-113.PubMed Beier JC, Killeen GF, Githure J: Entomologic inoculation rates and Plasmodium falciparum malaria prevalence in Africa. Am J Trop Med Hyg. 1999, 61: 109-113.PubMed
2.
go back to reference Kelly-Hope LA, McKenzie FE: The multiplicity of malaria transmission: a review of entomological inoculation rate measurements and methods across sub-Saharan Africa. Malar J. 2009, 8: 19-10.1186/1475-2875-8-19.PubMedCentralCrossRefPubMed Kelly-Hope LA, McKenzie FE: The multiplicity of malaria transmission: a review of entomological inoculation rate measurements and methods across sub-Saharan Africa. Malar J. 2009, 8: 19-10.1186/1475-2875-8-19.PubMedCentralCrossRefPubMed
3.
go back to reference Robert V, MacIntyre K, Keating J, Trape JF, Duchemin JB, Warren M, Beier JC: Malaria transmission in urban sub-Saharan Africa. Am J Trop Med Hyg. 2003, 68: 169-176.PubMed Robert V, MacIntyre K, Keating J, Trape JF, Duchemin JB, Warren M, Beier JC: Malaria transmission in urban sub-Saharan Africa. Am J Trop Med Hyg. 2003, 68: 169-176.PubMed
4.
go back to reference Hay SI, Rogers DJ, Toomer JF, Snow R: Annual Plasmodium falciparum entomological inoculation rates across Africa: literature survey, internet access and review. Trans R Soc Trop Med Hyg. 2000, 94: 113-127. 10.1016/S0035-9203(00)90246-3.PubMedCentralCrossRefPubMed Hay SI, Rogers DJ, Toomer JF, Snow R: Annual Plasmodium falciparum entomological inoculation rates across Africa: literature survey, internet access and review. Trans R Soc Trop Med Hyg. 2000, 94: 113-127. 10.1016/S0035-9203(00)90246-3.PubMedCentralCrossRefPubMed
5.
go back to reference World Health Organizaion: Malaria Entomology and Vector Control: Learner’s Guide. 2003, Geneva: World Health Organizaion World Health Organizaion: Malaria Entomology and Vector Control: Learner’s Guide. 2003, Geneva: World Health Organizaion
6.
go back to reference Service MW: A critical review of procedures for sampling populations of adult mosquitoes. Bull Entomol Res. 1977, 67: 343-382. 10.1017/S0007485300011184.CrossRef Service MW: A critical review of procedures for sampling populations of adult mosquitoes. Bull Entomol Res. 1977, 67: 343-382. 10.1017/S0007485300011184.CrossRef
7.
go back to reference Lindsay SW, Adiamah JH, Miller JE, Pleass RJ, Armstrong JRM: Variation in attractiveness of human-subjects to malaria mosquitoes (Diptera, Culicidae) in The Gambia. J Med Entomol. 1993, 30: 368-373.CrossRefPubMed Lindsay SW, Adiamah JH, Miller JE, Pleass RJ, Armstrong JRM: Variation in attractiveness of human-subjects to malaria mosquitoes (Diptera, Culicidae) in The Gambia. J Med Entomol. 1993, 30: 368-373.CrossRefPubMed
8.
go back to reference Knols BGJ, de Jong R, Takken W: Differential attractiveness of isolated humans to mosquitoes in Tanzania. Trans R Soc Trop Med Hyg. 1995, 89: 604-606. 10.1016/0035-9203(95)90406-9.CrossRefPubMed Knols BGJ, de Jong R, Takken W: Differential attractiveness of isolated humans to mosquitoes in Tanzania. Trans R Soc Trop Med Hyg. 1995, 89: 604-606. 10.1016/0035-9203(95)90406-9.CrossRefPubMed
9.
go back to reference Mathenge EM, Killeen GF, Oulo DO, Irungu LW, Ndegwa PN: Development of an exposure-free bednet trap for sampling Afrotropical malaria vectors. Med Vet Entomol. 2002, 16: 67-74. 10.1046/j.0269-283x.2002.00350.x.CrossRefPubMed Mathenge EM, Killeen GF, Oulo DO, Irungu LW, Ndegwa PN: Development of an exposure-free bednet trap for sampling Afrotropical malaria vectors. Med Vet Entomol. 2002, 16: 67-74. 10.1046/j.0269-283x.2002.00350.x.CrossRefPubMed
10.
go back to reference Ndiath M, Mazenot C, Gaye A, Konate L, Bouganali C: Methods to collect Anopheles mosquitoes and evaluate malaria transmission: a comparative study in two villages in Senegal. Malar J. 2011, 10: 270-10.1186/1475-2875-10-270.PubMedCentralCrossRefPubMed Ndiath M, Mazenot C, Gaye A, Konate L, Bouganali C: Methods to collect Anopheles mosquitoes and evaluate malaria transmission: a comparative study in two villages in Senegal. Malar J. 2011, 10: 270-10.1186/1475-2875-10-270.PubMedCentralCrossRefPubMed
11.
go back to reference Lines JD, Curtis CF, Wilkes TJ, Njunwa KJ: Monitoring human-biting mosquitoes (Diptera: Culicidae) in Tanzania with light-traps hung beside mosquito nets. Bull Entomol Res. 1991, 81: 77-84. 10.1017/S0007485300053268.CrossRef Lines JD, Curtis CF, Wilkes TJ, Njunwa KJ: Monitoring human-biting mosquitoes (Diptera: Culicidae) in Tanzania with light-traps hung beside mosquito nets. Bull Entomol Res. 1991, 81: 77-84. 10.1017/S0007485300053268.CrossRef
12.
go back to reference Costantini C, Sagnon NF, Sanogo E, Merzagora L, Coluzzi M: Relationship to human biting collections and influence of light and bednet in CDC light-trap catches of West African malaria vectors. Bull Entomol Res. 1998, 88: 503-511. 10.1017/S000748530002602X.CrossRef Costantini C, Sagnon NF, Sanogo E, Merzagora L, Coluzzi M: Relationship to human biting collections and influence of light and bednet in CDC light-trap catches of West African malaria vectors. Bull Entomol Res. 1998, 88: 503-511. 10.1017/S000748530002602X.CrossRef
13.
go back to reference Magbity EB, Lines JD, Marbiah MT, David K, Peterson E: How reliable are light traps in estimating biting rates of adult Anopheles gambiae s.l. (Diptera: Culicidae) in the presence of treated bed nets?. Bull Entomol Res. 2002, 92: 71-76.CrossRefPubMed Magbity EB, Lines JD, Marbiah MT, David K, Peterson E: How reliable are light traps in estimating biting rates of adult Anopheles gambiae s.l. (Diptera: Culicidae) in the presence of treated bed nets?. Bull Entomol Res. 2002, 92: 71-76.CrossRefPubMed
14.
go back to reference Shiff CJ, Minjas JN, Hall T, Hunt RH, Lyimo S: Malaria infection potential of Anopheline mosquitos sampled by light trapping indoors in coastal Tanzanian villages. Med Vet Entomol. 1995, 9: 256-262. 10.1111/j.1365-2915.1995.tb00131.x.CrossRefPubMed Shiff CJ, Minjas JN, Hall T, Hunt RH, Lyimo S: Malaria infection potential of Anopheline mosquitos sampled by light trapping indoors in coastal Tanzanian villages. Med Vet Entomol. 1995, 9: 256-262. 10.1111/j.1365-2915.1995.tb00131.x.CrossRefPubMed
15.
go back to reference Sikaala CH, Killeen GF, Chanda J, Chinula D, Miller JM, Russell TL, Seyoum A: Evaluation of alternaive mosquito sampling methods for malaria vectors in lowland south-east Zambia. Parasit Vectors. 2013, 6: 91-10.1186/1756-3305-6-91.PubMedCentralCrossRefPubMed Sikaala CH, Killeen GF, Chanda J, Chinula D, Miller JM, Russell TL, Seyoum A: Evaluation of alternaive mosquito sampling methods for malaria vectors in lowland south-east Zambia. Parasit Vectors. 2013, 6: 91-10.1186/1756-3305-6-91.PubMedCentralCrossRefPubMed
16.
go back to reference Mbogo CN, Glass GE, Forster D, Kabiru EW, Githure JI, Ouma JH, Beier JC: Evaluation of light traps for sampling Anopheline mosquitoes in Kilifi, Kenya. J Am Mosq Control Assoc. 1993, 9: 260-263.PubMed Mbogo CN, Glass GE, Forster D, Kabiru EW, Githure JI, Ouma JH, Beier JC: Evaluation of light traps for sampling Anopheline mosquitoes in Kilifi, Kenya. J Am Mosq Control Assoc. 1993, 9: 260-263.PubMed
17.
go back to reference Govella NJ, Chaki PP, Mpangile JM, Killeen GF: Monitoring mosquitoes in urban Dar es Salaam: evaluation of resting boxes, window exit traps, CDC light traps, Ifakara tent traps and human landing catches. Parasit Vectors. 2011, 4: 40-10.1186/1756-3305-4-40.PubMedCentralCrossRefPubMed Govella NJ, Chaki PP, Mpangile JM, Killeen GF: Monitoring mosquitoes in urban Dar es Salaam: evaluation of resting boxes, window exit traps, CDC light traps, Ifakara tent traps and human landing catches. Parasit Vectors. 2011, 4: 40-10.1186/1756-3305-4-40.PubMedCentralCrossRefPubMed
18.
go back to reference Overgaard HJ, Saebo S, Reddy MR, Reddy VP, Abaga S, Matias A, Slotman MA: Light traps fail to estimate reliable malaria mosquito biting rates on Bioko Island, Equatorial Guinea. Malar J. 2012, 11: 56-10.1186/1475-2875-11-56.PubMedCentralCrossRefPubMed Overgaard HJ, Saebo S, Reddy MR, Reddy VP, Abaga S, Matias A, Slotman MA: Light traps fail to estimate reliable malaria mosquito biting rates on Bioko Island, Equatorial Guinea. Malar J. 2012, 11: 56-10.1186/1475-2875-11-56.PubMedCentralCrossRefPubMed
19.
go back to reference Davis JR, Hall T, Chee EM, Majala A, Minjas J, Shiff : Comparison of sampling anopheline mosquitoes by light-trap and human-bait collections indoors at Bagamoyo, Tanzania. Med Vet Entomol. 1995, 9: 249-255. 10.1111/j.1365-2915.1995.tb00130.x.CrossRefPubMed Davis JR, Hall T, Chee EM, Majala A, Minjas J, Shiff : Comparison of sampling anopheline mosquitoes by light-trap and human-bait collections indoors at Bagamoyo, Tanzania. Med Vet Entomol. 1995, 9: 249-255. 10.1111/j.1365-2915.1995.tb00130.x.CrossRefPubMed
20.
go back to reference Odiere M, Bayoh MN, Vulule J, Irungu L, Walker E: Sampling outdoor, resting Anopheles gambiae and other mosquitoes (Diptera: Culicidae) in Western Kenya with clay pots. J Med Entomol. 2007, 44: 14-22. 10.1603/0022-2585(2007)44[14:SORAGA]2.0.CO;2.PubMedCentralCrossRefPubMed Odiere M, Bayoh MN, Vulule J, Irungu L, Walker E: Sampling outdoor, resting Anopheles gambiae and other mosquitoes (Diptera: Culicidae) in Western Kenya with clay pots. J Med Entomol. 2007, 44: 14-22. 10.1603/0022-2585(2007)44[14:SORAGA]2.0.CO;2.PubMedCentralCrossRefPubMed
21.
go back to reference Mnzava AEP, Rwegoshora RT, Wilkes TJ, Tanner M, Curtis CF: Anopheles arabiensis and Anopheles gambiae chromosomal inversion polymorphism, feeding and resting behavior in relation to insecticide house-spraying in Tanzania. Med Vet Entomol. 1995, 9: 316-324. 10.1111/j.1365-2915.1995.tb00140.x.CrossRefPubMed Mnzava AEP, Rwegoshora RT, Wilkes TJ, Tanner M, Curtis CF: Anopheles arabiensis and Anopheles gambiae chromosomal inversion polymorphism, feeding and resting behavior in relation to insecticide house-spraying in Tanzania. Med Vet Entomol. 1995, 9: 316-324. 10.1111/j.1365-2915.1995.tb00140.x.CrossRefPubMed
22.
go back to reference Govella N, Moore JD, Killeen GF: An exposure-free tool for monitoring adult malaria mosquito populations. Am J Trop Med Hyg. 2010, 83: 596-600. 10.4269/ajtmh.2010.09-0682.PubMedCentralCrossRefPubMed Govella N, Moore JD, Killeen GF: An exposure-free tool for monitoring adult malaria mosquito populations. Am J Trop Med Hyg. 2010, 83: 596-600. 10.4269/ajtmh.2010.09-0682.PubMedCentralCrossRefPubMed
23.
go back to reference Sikulu M, Govella NJ, Ogoma SB, Mpangile J, Kambi SH, Kannady K, Chaki PC, Mukabana WR, Killeen GF: Comparative evaluation of the Ifakara tent trap-B, the standardized resting boxes and the human landing catch for sampling malaria vectors and other mosquitoes in urban Dar es Salaam, Tanzania. Malar J. 2009, 8: 197-10.1186/1475-2875-8-197.PubMedCentralCrossRefPubMed Sikulu M, Govella NJ, Ogoma SB, Mpangile J, Kambi SH, Kannady K, Chaki PC, Mukabana WR, Killeen GF: Comparative evaluation of the Ifakara tent trap-B, the standardized resting boxes and the human landing catch for sampling malaria vectors and other mosquitoes in urban Dar es Salaam, Tanzania. Malar J. 2009, 8: 197-10.1186/1475-2875-8-197.PubMedCentralCrossRefPubMed
24.
go back to reference Govella NJ, Chaki PP, Geissbuhler Y, Kannady K, Okumu F, Charlwood JD, Anderson RA, Killeen GF: A new tent trap for sampling exophagic and endophagic members of the Anopheles gambiae complex. Malar J. 2009, 8: 157-10.1186/1475-2875-8-157.PubMedCentralCrossRefPubMed Govella NJ, Chaki PP, Geissbuhler Y, Kannady K, Okumu F, Charlwood JD, Anderson RA, Killeen GF: A new tent trap for sampling exophagic and endophagic members of the Anopheles gambiae complex. Malar J. 2009, 8: 157-10.1186/1475-2875-8-157.PubMedCentralCrossRefPubMed
25.
go back to reference Bloland PB, Ruebush TK, McCormick JB, Ayisi J, Boriga DA, Oloo AJ, Beach R, Hawley W, Lal A, Nahlen B, Udhayakumar V, Campbell CC: Longitudinal cohort study of the epidemiology of malaria infections in an area of intense malaria transmission I. Description of study site, general methodology, and study population. Am J Trop Med Hyg. 1999, 60: 635-640.PubMed Bloland PB, Ruebush TK, McCormick JB, Ayisi J, Boriga DA, Oloo AJ, Beach R, Hawley W, Lal A, Nahlen B, Udhayakumar V, Campbell CC: Longitudinal cohort study of the epidemiology of malaria infections in an area of intense malaria transmission I. Description of study site, general methodology, and study population. Am J Trop Med Hyg. 1999, 60: 635-640.PubMed
26.
go back to reference Phillips-Howard PA, ter Kuile FO, Nahlen BL, Alaii JA, Gimnig JE, Kolczak MS, Terlouw DJ, Kariuki SK, Shi YP, Kachur SP, Hightower AW, Hawley WA: The efficacy of permethrin-treated bed nets on child mortality and morbidity in western Kenya II. Study design and methods. Am J Trop Med Hyg. 2003, 68 (Suppl 4): 10-15.PubMed Phillips-Howard PA, ter Kuile FO, Nahlen BL, Alaii JA, Gimnig JE, Kolczak MS, Terlouw DJ, Kariuki SK, Shi YP, Kachur SP, Hightower AW, Hawley WA: The efficacy of permethrin-treated bed nets on child mortality and morbidity in western Kenya II. Study design and methods. Am J Trop Med Hyg. 2003, 68 (Suppl 4): 10-15.PubMed
27.
go back to reference Gimnig JE, Vulule JM, Lo TQ, Kamau L, Kolczak MS, Phillips-Howard PA, Mathenge EM, ter Kuile FO, Nahlen BL, Hightower AW, Hawley WA: Impact of permethrin-treated bed nets on entomologic indices in an area of intense year-round malaria transmission. Am J Trop Med Hyg. 2003, 68 (Suppl 4): 16-22.PubMed Gimnig JE, Vulule JM, Lo TQ, Kamau L, Kolczak MS, Phillips-Howard PA, Mathenge EM, ter Kuile FO, Nahlen BL, Hightower AW, Hawley WA: Impact of permethrin-treated bed nets on entomologic indices in an area of intense year-round malaria transmission. Am J Trop Med Hyg. 2003, 68 (Suppl 4): 16-22.PubMed
28.
go back to reference Phillips-Howard PA, Nahlen BL, Alaii JA, ter Kuile FO, Gimnig JE, Terlouw DJ, Kachur SP, Hightower AW, Lal AA, Schoute E, Oloo AJ, Hawley WA: The efficacy of permethrin-treated bed nets on child mortality and morbidity in western Kenya I. Development of infrastructure and description of study site. Am J Trop Med Hyg. 2003, 68 (Suppl 4): 3-9.PubMed Phillips-Howard PA, Nahlen BL, Alaii JA, ter Kuile FO, Gimnig JE, Terlouw DJ, Kachur SP, Hightower AW, Lal AA, Schoute E, Oloo AJ, Hawley WA: The efficacy of permethrin-treated bed nets on child mortality and morbidity in western Kenya I. Development of infrastructure and description of study site. Am J Trop Med Hyg. 2003, 68 (Suppl 4): 3-9.PubMed
29.
go back to reference Hamel MJ, Adazu K, Obor D, Sewe M, Vulule J, Williamson JM, Slutsker L, Feikin DR, Laserson KF: A reversal in reductions of child mortality in western Kenya, 2003–2009. Am J Trop Med Hyg. 2011, 85: 597-605. 10.4269/ajtmh.2011.10-0678.PubMedCentralCrossRefPubMed Hamel MJ, Adazu K, Obor D, Sewe M, Vulule J, Williamson JM, Slutsker L, Feikin DR, Laserson KF: A reversal in reductions of child mortality in western Kenya, 2003–2009. Am J Trop Med Hyg. 2011, 85: 597-605. 10.4269/ajtmh.2011.10-0678.PubMedCentralCrossRefPubMed
30.
go back to reference Beier JC, Perkins PV, Onyango FK, Gargan TP, Oster CN, Whitmire RE, Koech DK, Roberts CR: Characterization of malaria transmission by Anopheles (Diptera, Culicidae) in western Kenya in preparation for malaria vaccine trials. J Med Entomol. 1990, 27: 570-577.CrossRefPubMed Beier JC, Perkins PV, Onyango FK, Gargan TP, Oster CN, Whitmire RE, Koech DK, Roberts CR: Characterization of malaria transmission by Anopheles (Diptera, Culicidae) in western Kenya in preparation for malaria vaccine trials. J Med Entomol. 1990, 27: 570-577.CrossRefPubMed
31.
go back to reference Beier JC, Oster CN, Onyango FK, Bales JD, Sherwood JA, Perkins PV, Chumo DK, Koech DV, Whitmire RE, Roberts CR, Diggs CL, Hoffman SL: Plasmodium falciparum incidence relative to entomological inoculation rates at a site proposed for testing malaria vaccines in western Kenya. Am J Trop Med Hyg. 1994, 50: 529-536.PubMed Beier JC, Oster CN, Onyango FK, Bales JD, Sherwood JA, Perkins PV, Chumo DK, Koech DV, Whitmire RE, Roberts CR, Diggs CL, Hoffman SL: Plasmodium falciparum incidence relative to entomological inoculation rates at a site proposed for testing malaria vaccines in western Kenya. Am J Trop Med Hyg. 1994, 50: 529-536.PubMed
32.
go back to reference Lindblade KA, Gimnig JE, Kamau L, Hawley WA, Odhiambo F, Olang G, ter Kuile FO, Vulule JM, Slutsker L: Impact of sustained use of insecticide-treated bednets on malaria vector species distribution and culicine mosquitoes. J Med Entomol. 2006, 43: 428-432. 10.1603/0022-2585(2006)043[0428:IOSUOI]2.0.CO;2.CrossRefPubMed Lindblade KA, Gimnig JE, Kamau L, Hawley WA, Odhiambo F, Olang G, ter Kuile FO, Vulule JM, Slutsker L: Impact of sustained use of insecticide-treated bednets on malaria vector species distribution and culicine mosquitoes. J Med Entomol. 2006, 43: 428-432. 10.1603/0022-2585(2006)043[0428:IOSUOI]2.0.CO;2.CrossRefPubMed
33.
go back to reference Bayoh MN, Mathias D, Odiere M, Mutuku F, Kamau L, Gimnig J, Vulule J, Hawley W, Hamel M, Walker E: Anopheles gambiae: historical population decline associated with regional distribution of insecticide-treated bed nets in western Nyanza Province, Kenya. Malar J. 2010, 9: 62-10.1186/1475-2875-9-62.PubMedCentralCrossRefPubMed Bayoh MN, Mathias D, Odiere M, Mutuku F, Kamau L, Gimnig J, Vulule J, Hawley W, Hamel M, Walker E: Anopheles gambiae: historical population decline associated with regional distribution of insecticide-treated bed nets in western Nyanza Province, Kenya. Malar J. 2010, 9: 62-10.1186/1475-2875-9-62.PubMedCentralCrossRefPubMed
34.
go back to reference Gillies MT, Coetzee M: A supplement to the Anophelinae of Africa South of the Sahara (Afrotropical region). 1987, Johannesburg: South African Medical Research Institute Gillies MT, Coetzee M: A supplement to the Anophelinae of Africa South of the Sahara (Afrotropical region). 1987, Johannesburg: South African Medical Research Institute
35.
go back to reference Gillies MT, De Meillon B: The Anophelinae of Africa South of the Sahara (Ethiopian zoogeographical region). 1968, Johannesburg: South African Institute for Medical Research Gillies MT, De Meillon B: The Anophelinae of Africa South of the Sahara (Ethiopian zoogeographical region). 1968, Johannesburg: South African Institute for Medical Research
36.
go back to reference Scott JA, Brogdon WG, Collins FH: Identification of single specimens of the Anopheles gambiae complex by the polymerase chain reaction. Am J Trop Med Hyg. 1993, 49: 520-529.PubMed Scott JA, Brogdon WG, Collins FH: Identification of single specimens of the Anopheles gambiae complex by the polymerase chain reaction. Am J Trop Med Hyg. 1993, 49: 520-529.PubMed
37.
go back to reference Burkot TR, Williams JL, Schneider I: Identification of Plasmodium falciparum- infected mosquitoes by a double antibody enzyme-linked immunosorbent assay. Am J Trop Med Hyg. 1984, 33: 783-788.PubMed Burkot TR, Williams JL, Schneider I: Identification of Plasmodium falciparum- infected mosquitoes by a double antibody enzyme-linked immunosorbent assay. Am J Trop Med Hyg. 1984, 33: 783-788.PubMed
38.
go back to reference Hightower A, Kiptui R, Manya A, Wolkon A, Vanden Eng J, Hamel M, Noor A, Sharif S, Buluma R, Vulule J, Laserson K, Slutsker L, Akhwale W: Bed net ownership in Kenya: the impact of 3.4 million free bed nets. Malar J. 2010, 9: 183-10.1186/1475-2875-9-183.PubMedCentralCrossRefPubMed Hightower A, Kiptui R, Manya A, Wolkon A, Vanden Eng J, Hamel M, Noor A, Sharif S, Buluma R, Vulule J, Laserson K, Slutsker L, Akhwale W: Bed net ownership in Kenya: the impact of 3.4 million free bed nets. Malar J. 2010, 9: 183-10.1186/1475-2875-9-183.PubMedCentralCrossRefPubMed
39.
go back to reference Yates A, N’Guessan R, Kaur H, Akogbeto M, Rowland M: Evaluation of KO-Tab 1-2-3(R): a wash-resistant ‘dip-it-yourself’ insecticide formulation for long-lasting treatment of mosquito nets. Malar J. 2005, 4: 52-10.1186/1475-2875-4-52.PubMedCentralCrossRefPubMed Yates A, N’Guessan R, Kaur H, Akogbeto M, Rowland M: Evaluation of KO-Tab 1-2-3(R): a wash-resistant ‘dip-it-yourself’ insecticide formulation for long-lasting treatment of mosquito nets. Malar J. 2005, 4: 52-10.1186/1475-2875-4-52.PubMedCentralCrossRefPubMed
40.
go back to reference Mboera LEG: Sampling techniques for adult Afrotropical malaria vectors and their reliability in the estimation of entomological inoculation rate. Tanzan Health Res Bull. 2005, 7: 117-124.PubMed Mboera LEG: Sampling techniques for adult Afrotropical malaria vectors and their reliability in the estimation of entomological inoculation rate. Tanzan Health Res Bull. 2005, 7: 117-124.PubMed
41.
go back to reference Hii JLK, Smith T, Mai A, Ibam E, Alpers MP: Comparison between anopheline mosquitoes (Diptera: Culicidae) caught using different methods in a malaria endemic area of Papua New Guinea. Bull Entomol Res. 2000, 90: 211-219.CrossRefPubMed Hii JLK, Smith T, Mai A, Ibam E, Alpers MP: Comparison between anopheline mosquitoes (Diptera: Culicidae) caught using different methods in a malaria endemic area of Papua New Guinea. Bull Entomol Res. 2000, 90: 211-219.CrossRefPubMed
42.
go back to reference Mathenge E, Misiani G, Oulo D, Irungu L, Ndegwa P, Smith T, Killeen G, Knols B: Comparative performance of the Mbita trap, CDC light trap and the human landing catch in the sampling of Anopheles arabiensis, An. funestus and culicine species in a rice irrigation in western Kenya. Malar J. 2005, 4: 7-10.1186/1475-2875-4-7.PubMedCentralCrossRefPubMed Mathenge E, Misiani G, Oulo D, Irungu L, Ndegwa P, Smith T, Killeen G, Knols B: Comparative performance of the Mbita trap, CDC light trap and the human landing catch in the sampling of Anopheles arabiensis, An. funestus and culicine species in a rice irrigation in western Kenya. Malar J. 2005, 4: 7-10.1186/1475-2875-4-7.PubMedCentralCrossRefPubMed
43.
go back to reference Githeko AK, Service MW, Mbogo CM, Atieli FA, Juma FO: Sampling Anopheles arabiensis, A. gambiae sensu lato and A. funestus (Diptera: Culicidae) with CDC light-traps near a rice irrigation area and a sugarcane belt in western Kenya. Bull Entomol Res. 1994, 84: 319-324. 10.1017/S0007485300032430.CrossRef Githeko AK, Service MW, Mbogo CM, Atieli FA, Juma FO: Sampling Anopheles arabiensis, A. gambiae sensu lato and A. funestus (Diptera: Culicidae) with CDC light-traps near a rice irrigation area and a sugarcane belt in western Kenya. Bull Entomol Res. 1994, 84: 319-324. 10.1017/S0007485300032430.CrossRef
44.
go back to reference Okumu FO, Moore J, Mbeyela E, Sherlock M, Sangusangu R, Ligamba G, Russell T, Moore SJ: A modified experimental hut design for studying responses of disease-transmitting mosquitoes to indoor interventions: the Ifakara experimental huts. PLoS One. 2012, 7: e30967-10.1371/journal.pone.0030967.PubMedCentralCrossRefPubMed Okumu FO, Moore J, Mbeyela E, Sherlock M, Sangusangu R, Ligamba G, Russell T, Moore SJ: A modified experimental hut design for studying responses of disease-transmitting mosquitoes to indoor interventions: the Ifakara experimental huts. PLoS One. 2012, 7: e30967-10.1371/journal.pone.0030967.PubMedCentralCrossRefPubMed
45.
go back to reference van den Bijllaardt W, ter Braak R, Shekalaghe S, Otieno S, Mahande A, Sauerwein R, Takken W, Bousema T: The suitability of clay pots for indoor sampling of mosquitoes in an arid area in northern Tanzania. Acta Trop. 2009, 111: 197-199. 10.1016/j.actatropica.2009.04.003.CrossRefPubMed van den Bijllaardt W, ter Braak R, Shekalaghe S, Otieno S, Mahande A, Sauerwein R, Takken W, Bousema T: The suitability of clay pots for indoor sampling of mosquitoes in an arid area in northern Tanzania. Acta Trop. 2009, 111: 197-199. 10.1016/j.actatropica.2009.04.003.CrossRefPubMed
46.
go back to reference Burkot TR, Russell TL, Reimer LJ, Bugoro H, Beebe NW, Cooper RD, Sukawati S, Collins FH, Lobo NF: Barrier screens: a method to sample blood-fed and host-seeking exophilic mosquitoes. Malar J. 2013, 12: 49-10.1186/1475-2875-12-49.PubMedCentralCrossRefPubMed Burkot TR, Russell TL, Reimer LJ, Bugoro H, Beebe NW, Cooper RD, Sukawati S, Collins FH, Lobo NF: Barrier screens: a method to sample blood-fed and host-seeking exophilic mosquitoes. Malar J. 2013, 12: 49-10.1186/1475-2875-12-49.PubMedCentralCrossRefPubMed
47.
go back to reference Chaki PP, Mlacha Y, Msellemu D, Muhili A, Malishee AD, Mtema ZJ, Kiware SS, Zhou Y, Lobo NF, Russell TL, Dongus S, Govella NJ, Killeen GF: An affordable, quality-assured community-based system for high-resolution entomological surveillance of vector mosquitoes that reflects human malaria infection risk patterns. Malar J. 2012, 11: 172-10.1186/1475-2875-11-172.PubMedCentralCrossRefPubMed Chaki PP, Mlacha Y, Msellemu D, Muhili A, Malishee AD, Mtema ZJ, Kiware SS, Zhou Y, Lobo NF, Russell TL, Dongus S, Govella NJ, Killeen GF: An affordable, quality-assured community-based system for high-resolution entomological surveillance of vector mosquitoes that reflects human malaria infection risk patterns. Malar J. 2012, 11: 172-10.1186/1475-2875-11-172.PubMedCentralCrossRefPubMed
48.
go back to reference Russell TL, Govella NJ, Azizi S, Drakeley CJ, Kachur SP, Killeen GF: Increased proportions of outdoor feeding among residual malaria vector populations following increased use of insecticide-treated nets in rural Tanzania. Malar J. 2011, 10: 80-10.1186/1475-2875-10-80.PubMedCentralCrossRefPubMed Russell TL, Govella NJ, Azizi S, Drakeley CJ, Kachur SP, Killeen GF: Increased proportions of outdoor feeding among residual malaria vector populations following increased use of insecticide-treated nets in rural Tanzania. Malar J. 2011, 10: 80-10.1186/1475-2875-10-80.PubMedCentralCrossRefPubMed
49.
go back to reference Bugoro H, Cooper RD, Butafa C, Iro’ofa C, Mackenzie DO, Chen CC, Russell TL: Bionomics of the malaria vector Anopheles farauti in Temotu Province, Solomon Islands: issues for malaria elimination. Malar J. 2011, 10: 133-10.1186/1475-2875-10-133.PubMedCentralCrossRefPubMed Bugoro H, Cooper RD, Butafa C, Iro’ofa C, Mackenzie DO, Chen CC, Russell TL: Bionomics of the malaria vector Anopheles farauti in Temotu Province, Solomon Islands: issues for malaria elimination. Malar J. 2011, 10: 133-10.1186/1475-2875-10-133.PubMedCentralCrossRefPubMed
50.
go back to reference Reddy MR, Overgaard HJ, Abaga S, Reddy VP, Caccone A, Kiszewski AE, Slotman MA: Outdoor host seeking behaviour of Anopheles gambiae mosquitoes following initiation of malaria vector control on Bioko Island, Equatorial Guinea. Malar J. 2011, 10: 184-10.1186/1475-2875-10-184.PubMedCentralCrossRefPubMed Reddy MR, Overgaard HJ, Abaga S, Reddy VP, Caccone A, Kiszewski AE, Slotman MA: Outdoor host seeking behaviour of Anopheles gambiae mosquitoes following initiation of malaria vector control on Bioko Island, Equatorial Guinea. Malar J. 2011, 10: 184-10.1186/1475-2875-10-184.PubMedCentralCrossRefPubMed
51.
go back to reference Mzilahowa T, Hastings IM, Molyneux ME, McCall PJ: Entomological indices of malaria transmission in Chikhwawa district, Southern Malawi. Malar J. 2012, 11: 380-10.1186/1475-2875-11-380.PubMedCentralCrossRefPubMed Mzilahowa T, Hastings IM, Molyneux ME, McCall PJ: Entomological indices of malaria transmission in Chikhwawa district, Southern Malawi. Malar J. 2012, 11: 380-10.1186/1475-2875-11-380.PubMedCentralCrossRefPubMed
52.
go back to reference Mutuku FM, King CH, Mungai P, Mbogo C, Mwangangi J, Muchiri EM, Walker ED, Kitron U: Impact of insecticide-treated bed nets on malaria transmission indices on the south coast of Kenya. Malar J. 2011, 10: 356-10.1186/1475-2875-10-356.PubMedCentralCrossRefPubMed Mutuku FM, King CH, Mungai P, Mbogo C, Mwangangi J, Muchiri EM, Walker ED, Kitron U: Impact of insecticide-treated bed nets on malaria transmission indices on the south coast of Kenya. Malar J. 2011, 10: 356-10.1186/1475-2875-10-356.PubMedCentralCrossRefPubMed
53.
go back to reference Okumu FO, Killeen GF, Ogoma S, Biswaro L, Smallegange RC, Mbeyela E, Titus E, Munk C, Ngonyani H, Takken W, Mshinda H, Mukabana WR, Moore SJ: Development and field evaluation of a synthetic mosquito lure that is more attractive than humans. PLoS One. 2010, 5: e8951-10.1371/journal.pone.0008951.PubMedCentralCrossRefPubMed Okumu FO, Killeen GF, Ogoma S, Biswaro L, Smallegange RC, Mbeyela E, Titus E, Munk C, Ngonyani H, Takken W, Mshinda H, Mukabana WR, Moore SJ: Development and field evaluation of a synthetic mosquito lure that is more attractive than humans. PLoS One. 2010, 5: e8951-10.1371/journal.pone.0008951.PubMedCentralCrossRefPubMed
54.
go back to reference Mbogo CM, Mwangangi JM, Nzovu J, Gu WD, Yan GY, Gunter JT, Swalm C, Keating J, Regens JL, Shililu JI, Githure JI, Beier JC: Spatial and temporal heterogeneity of Anopheles mosquitoes and Plasmodium falciparum transmission along the Kenyan coast. Am J Trop Med Hyg. 2003, 68: 734-742.PubMed Mbogo CM, Mwangangi JM, Nzovu J, Gu WD, Yan GY, Gunter JT, Swalm C, Keating J, Regens JL, Shililu JI, Githure JI, Beier JC: Spatial and temporal heterogeneity of Anopheles mosquitoes and Plasmodium falciparum transmission along the Kenyan coast. Am J Trop Med Hyg. 2003, 68: 734-742.PubMed
55.
go back to reference Shililu J, Ghebremeskel T, Mengistu S, Fekadu H, Zerom M, Mbogo C, Githure J, Novak R, Brantly E, Beier JC: High seasonal variation in entomologic inoculation rates in Eritrea, a semi-arid region of unstable malaria in Africa. Am J Trop Med Hyg. 2003, 69: 607-613.PubMed Shililu J, Ghebremeskel T, Mengistu S, Fekadu H, Zerom M, Mbogo C, Githure J, Novak R, Brantly E, Beier JC: High seasonal variation in entomologic inoculation rates in Eritrea, a semi-arid region of unstable malaria in Africa. Am J Trop Med Hyg. 2003, 69: 607-613.PubMed
56.
go back to reference Drakeley C, Schellenberg D, Kihonda J, Sousa CA, Arez AP, Lopes D, Lines J, Mshinda H, Lengeler C, Schellenberg JA, Tanner M, Alonso P: An estimation of the entomological inoculation rate for Ifakara: a semi-urban area in a region of intense malaria transmission in Tanzania. Trop Med Int Health. 2003, 8: 767-774. 10.1046/j.1365-3156.2003.01100.x.CrossRefPubMed Drakeley C, Schellenberg D, Kihonda J, Sousa CA, Arez AP, Lopes D, Lines J, Mshinda H, Lengeler C, Schellenberg JA, Tanner M, Alonso P: An estimation of the entomological inoculation rate for Ifakara: a semi-urban area in a region of intense malaria transmission in Tanzania. Trop Med Int Health. 2003, 8: 767-774. 10.1046/j.1365-3156.2003.01100.x.CrossRefPubMed
57.
go back to reference Greenwood BM: The microepidemiology of malaria and its importance to malaria control. Trans R Soc Trop Med Hyg. 1989, 83 (Suppl): 25-29.CrossRefPubMed Greenwood BM: The microepidemiology of malaria and its importance to malaria control. Trans R Soc Trop Med Hyg. 1989, 83 (Suppl): 25-29.CrossRefPubMed
58.
go back to reference Okumu FO, Kotas ME, Kihonda J, Mathenge EM, Killeen GF, Moore SJ: Comparative evaluation of methods used for sampling malaria vectors in the Kilombero Valley, south eastern Tanzania. Open Trop Med J. 2008, 1: 51-55. 10.2174/1874315300801010051.CrossRef Okumu FO, Kotas ME, Kihonda J, Mathenge EM, Killeen GF, Moore SJ: Comparative evaluation of methods used for sampling malaria vectors in the Kilombero Valley, south eastern Tanzania. Open Trop Med J. 2008, 1: 51-55. 10.2174/1874315300801010051.CrossRef
59.
go back to reference Magbity EB, Lines JD: Spatial and temporal distribution of Anopheles gambiae s.l. (Diptera: Culicidae) in two Tanzanian villages: implication for designing mosquito sampling routines. Bull Entomol Res. 2002, 92: 483-488.CrossRefPubMed Magbity EB, Lines JD: Spatial and temporal distribution of Anopheles gambiae s.l. (Diptera: Culicidae) in two Tanzanian villages: implication for designing mosquito sampling routines. Bull Entomol Res. 2002, 92: 483-488.CrossRefPubMed
Metadata
Title
Standardizing operational vector sampling techniques for measuring malaria transmission intensity: evaluation of six mosquito collection methods in western Kenya
Authors
Jacklyn Wong
Nabie Bayoh
George Olang
Gerry F Killeen
Mary J Hamel
John M Vulule
John E Gimnig
Publication date
01-12-2013
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2013
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/1475-2875-12-143

Other articles of this Issue 1/2013

Malaria Journal 1/2013 Go to the issue
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.