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

Malaria Journal

Volumn 12, Issue 1, 2013, Pages

  Wong, Jacklyn ^a   Bayoh, Nabie ^a,b   Olang, George ^a,b   Killeen, Gerry F ^c,d   Hamel, Mary J ^a,b   Vulule, John M ^b   Gimnig, John E ^a  

^a CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

^b KENYA MEDICAL RESEARCH INSTITUTE   (Kenya)

^c LIVERPOOL SCHOOL OF TROPICAL MEDICINE   (United Kingdom)

^d IFAKARA HEALTH INSTITUTE   (Tanzania)

Author keywords

Anopheles arabiensis; Anopheles funestus; Anopheles gambiae; CDC light trap; Human biting rate; Human landing catch; Ifakara tent trap; Mosquito sampling; Window exit trap

Indexed keywords

ADULT; ANOPHELES ARABIENSIS; ANOPHELES FUNESTUS; ANOPHELES GAMBIAE; ARTICLE; BOX RESTING TRAP; CENTERS FOR DISEASE CONTROL AND PREVENTION MINIATURE LIGHT TRAP; DISEASE TRANSMISSION; FEMALE; HUMAN; HUMAN LANDING CATCH; IFAKARA TENT TRAP; KENYA; MALARIA; MALE; MORPHOLOGY; NONHUMAN; PARASITE VECTOR; POLYMERASE CHAIN REACTION; POT RESTING TRAP; RURAL AREA; SAMPLING; STANDARDIZATION; WINDOW EXIT TRAP;

ADULT; ANIMALS; CHILD, PRESCHOOL; CULICIDAE; DISEASE VECTORS; ENTOMOLOGY; FEMALE; HUMANS; INFANT; KENYA; MALARIA; MALE; POPULATION DENSITY;

EID: 84876807441     PISSN: None     EISSN: 14752875     Source Type: Journal    
DOI: 10.1186/1475-2875-12-143     Document Type: Article

References (59)

1. Entomologic inoculation rates and Plasmodium falciparum malaria prevalence in Africa. Beier JC, Killeen GF, Githure J, Am J Trop Med Hyg 1999 61 109 113 10432066
2. The multiplicity of malaria transmission: a review of entomological inoculation rate measurements and methods across sub-Saharan Africa. Kelly-Hope LA, McKenzie FE, Malar J 2009 8 19 10.1186/1475-2875-8-19 19166589
3. Malaria transmission in urban sub-Saharan Africa. Robert V, MacIntyre K, Keating J, Trape JF, Duchemin JB, Warren M, Beier JC, Am J Trop Med Hyg 2003 68 169 176 12641407
4. Annual Plasmodium falciparum entomological inoculation rates across Africa: literature survey, internet access and review. Hay SI, Rogers DJ, Toomer JF, Snow R, Trans R Soc Trop Med Hyg 2000 94 113 127 10.1016/S0035-9203(00) 90246-3 10897348
5. World Health Organizaion, Malaria Entomology and Vector Control: Learner's Guide Geneva: World Health Organizaion 2003
6. A critical review of procedures for sampling populations of adult mosquitoes. Service MW, Bull Entomol Res 1977 67 343 382 10.1017/ S0007485300011184
7. Variation in attractiveness of human-subjects to malaria mosquitoes (Diptera, Culicidae) in The Gambia. Lindsay SW, Adiamah JH, Miller JE, Pleass RJ, Armstrong JRM, J Med Entomol 1993 30 368 373 8459413
8. Differential attractiveness of isolated humans to mosquitoes in Tanzania. Knols BGJ, de Jong R, Takken W, Trans R Soc Trop Med Hyg 1995 89 604 606 10.1016/0035-9203(95)90406-9 8594668
9. Development of an exposure-free bednet trap for sampling Afrotropical malaria vectors. Mathenge EM, Killeen GF, Oulo DO, Irungu LW, Ndegwa PN, Med Vet Entomol 2002 16 67 74 10.1046/j.0269-283x.2002.00350.x 11963983
10. Methods to collect Anopheles mosquitoes and evaluate malaria transmission: a comparative study in two villages in Senegal. Ndiath M, Mazenot C, Gaye A, Konate L, Bouganali C, Malar J 2011 10 270 10.1186/1475-2875-10-270 21929747
11. Monitoring human-biting mosquitoes (Diptera: Culicidae) in Tanzania with light-traps hung beside mosquito nets. Lines JD, Curtis CF, Wilkes TJ, Njunwa KJ, Bull Entomol Res 1991 81 77 84 10.1017/S0007485300053268
12. Relationship to human biting collections and influence of light and bednet in CDC light-trap catches of West African malaria vectors. Costantini C, Sagnon NF, Sanogo E, Merzagora L, Coluzzi M, Bull Entomol Res 1998 88 503 511 10.1017/S000748530002602X
13. How reliable are light traps in estimating biting rates of adult Anopheles gambiae s.l. (Diptera: Culicidae) in the presence of treated bed nets? Magbity EB, Lines JD, Marbiah MT, David K, Peterson E, Bull Entomol Res 2002 92 71 76 12020364
14. Malaria infection potential of Anopheline mosquitos sampled by light trapping indoors in coastal Tanzanian villages. Shiff CJ, Minjas JN, Hall T, Hunt RH, Lyimo S, Med Vet Entomol 1995 9 256 262 10.1111/j.1365-2915.1995. tb00131.x 7548942
15. Evaluation of alternaive mosquito sampling methods for malaria vectors in lowland south-east Zambia. Sikaala CH, Killeen GF, Chanda J, Chinula D, Miller JM, Russell TL, Seyoum A, Parasit Vectors 2013 6 91 10.1186/1756-3305-6-91 23570257
16. Evaluation of light traps for sampling Anopheline mosquitoes in Kilifi, Kenya. Mbogo CN, Glass GE, Forster D, Kabiru EW, Githure JI, Ouma JH, Beier JC, J Am Mosq Control Assoc 1993 9 260 263 8245934
17. Monitoring mosquitoes in urban Dar es Salaam: evaluation of resting boxes, window exit traps, CDC light traps, Ifakara tent traps and human landing catches. Govella NJ, Chaki PP, Mpangile JM, Killeen GF, Parasit Vectors 2011 4 40 10.1186/1756-3305-4-40 21418622
18. Light traps fail to estimate reliable malaria mosquito biting rates on Bioko Island, Equatorial Guinea. Overgaard HJ, Saebo S, Reddy MR, Reddy VP, Abaga S, Matias A, Slotman MA, Malar J 2012 11 56 10.1186/1475-2875-11-56 22364588
19. Comparison of sampling anopheline mosquitoes by light-trap and human-bait collections indoors at Bagamoyo, Tanzania. Davis JR, Hall T, Chee EM, Majala A, Minjas J, Shiff, Med Vet Entomol 1995 9 249 255 10.1111/j.1365-2915.1995. tb00130.x 7548941
20. Sampling outdoor, resting Anopheles gambiae and other mosquitoes (Diptera: Culicidae) in Western Kenya with clay pots. Odiere M, Bayoh MN, Vulule J, Irungu L, Walker E, J Med Entomol 2007 44 14 22 10.1603/0022-2585(2007) 44[14:SORAGA]2.0.CO;2 17294916
21. Anopheles arabiensis and Anopheles gambiae chromosomal inversion polymorphism, feeding and resting behavior in relation to insecticide house-spraying in Tanzania. Mnzava AEP, Rwegoshora RT, Wilkes TJ, Tanner M, Curtis CF, Med Vet Entomol 1995 9 316 324 10.1111/j.1365-2915.1995.tb00140.x 7548951
22. An exposure-free tool for monitoring adult malaria mosquito populations. Govella N, Moore JD, Killeen GF, Am J Trop Med Hyg 2010 83 596 600 10.4269/ajtmh.2010.09-0682 20810826
23. 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. Sikulu M, Govella NJ, Ogoma SB, Mpangile J, Kambi SH, Kannady K, Chaki PC, Mukabana WR, Killeen GF, Malar J 2009 8 197 10.1186/1475-2875-8-197 19674477
24. A new tent trap for sampling exophagic and endophagic members of the Anopheles gambiae complex. Govella NJ, Chaki PP, Geissbuhler Y, Kannady K, Okumu F, Charlwood JD, Anderson RA, Killeen GF, Malar J 2009 8 157 10.1186/1475-2875-8-157 19602253
25. 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. Bloland PB, Ruebush TK, McCormick JB, Ayisi J, Boriga DA, Oloo AJ, Beach R, Hawley W, Lal A, Nahlen B, Udhayakumar V, Campbell CC, Am J Trop Med Hyg 1999 60 635 640 10348240
26. The efficacy of permethrin-treated bed nets on child mortality and morbidity in western Kenya II. Study design and methods. 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, Am J Trop Med Hyg 2003 68 Suppl 4 10 15 12749480
27. Impact of permethrin-treated bed nets on entomologic indices in an area of intense year-round malaria transmission. Gimnig JE, Vulule JM, Lo TQ, Kamau L, Kolczak MS, Phillips-Howard PA, Mathenge EM, ter Kuile FO, Nahlen BL, Hightower AW, Hawley WA, Am J Trop Med Hyg 2003 68 Suppl 4 16 22 12749481
28. The efficacy of permethrin-treated bed nets on child mortality and morbidity in western Kenya I. Development of infrastructure and description of study site. 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, Am J Trop Med Hyg 2003 68 Suppl 4 3 9 12749479
29. A reversal in reductions of child mortality in western Kenya, 2003-2009. Hamel MJ, Adazu K, Obor D, Sewe M, Vulule J, Williamson JM, Slutsker L, Feikin DR, Laserson KF, Am J Trop Med Hyg 2011 85 597 605 10.4269/ajtmh.2011.10-0678 21976557
30. Characterization of malaria transmission by Anopheles (Diptera, Culicidae) in western Kenya in preparation for malaria vaccine trials. Beier JC, Perkins PV, Onyango FK, Gargan TP, Oster CN, Whitmire RE, Koech DK, Roberts CR, J Med Entomol 1990 27 570 577 2388233
31. Plasmodium falciparum incidence relative to entomological inoculation rates at a site proposed for testing malaria vaccines in western Kenya. Beier JC, Oster CN, Onyango FK, Bales JD, Sherwood JA, Perkins PV, Chumo DK, Koech DV, Whitmire RE, Roberts CR, Diggs CL, Hoffman SL, Am J Trop Med Hyg 1994 50 529 536 7911282
32. Impact of sustained use of insecticide-treated bednets on malaria vector species distribution and culicine mosquitoes. Lindblade KA, Gimnig JE, Kamau L, Hawley WA, Odhiambo F, Olang G, ter Kuile FO, Vulule JM, Slutsker L, J Med Entomol 2006 43 428 432 10.1603/0022-2585(2006)043[0428:IOSUOI]2.0.CO;2 16619629
33. Anopheles gambiae: historical population decline associated with regional distribution of insecticide-treated bed nets in western Nyanza Province, Kenya. Bayoh MN, Mathias D, Odiere M, Mutuku F, Kamau L, Gimnig J, Vulule J, Hawley W, Hamel M, Walker E, Malar J 2010 9 62 10.1186/1475-2875-9-62 20187956
34. Gillies MT, Coetzee M, A supplement to the Anophelinae of Africa South of the Sahara (Afrotropical region) Johannesburg: South African Medical Research Institute 1987
35. Gillies MT, De Meillon B, The Anophelinae of Africa South of the Sahara (Ethiopian zoogeographical region) Johannesburg: South African Institute for Medical Research 1968
36. Identification of single specimens of the Anopheles gambiae complex by the polymerase chain reaction. Scott JA, Brogdon WG, Collins FH, Am J Trop Med Hyg 1993 49 520 529 8214283
37. Identification of Plasmodium falciparum-infected mosquitoes by a double antibody enzyme-linked immunosorbent assay. Burkot TR, Williams JL, Schneider I, Am J Trop Med Hyg 1984 33 783 788 6385740
38. Bed net ownership in Kenya: the impact of 3.4 million free bed nets. 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, Malar J 2010 9 183 10.1186/1475-2875-9-183 20576145
39. Evaluation of KO-Tab 1-2-3(R): a wash-resistant 'dip-it-yourself' insecticide formulation for long-lasting treatment of mosquito nets. Yates A, N'Guessan R, Kaur H, Akogbeto M, Rowland M, Malar J 2005 4 52 10.1186/1475-2875-4-52 16269088
40. Sampling techniques for adult Afrotropical malaria vectors and their reliability in the estimation of entomological inoculation rate. Mboera LEG, Tanzan Health Res Bull 2005 7 117 124 16941936
41. Comparison between anopheline mosquitoes (Diptera: Culicidae) caught using different methods in a malaria endemic area of Papua New Guinea. Hii JLK, Smith T, Mai A, Ibam E, Alpers MP, Bull Entomol Res 2000 90 211 219 10996862
42. 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. Mathenge E, Misiani G, Oulo D, Irungu L, Ndegwa P, Smith T, Killeen G, Knols B, Malar J 2005 4 7 10.1186/1475-2875-4-7 15667666
43. 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. Githeko AK, Service MW, Mbogo CM, Atieli FA, Juma FO, Bull Entomol Res 1994 84 319 324 10.1017/S0007485300032430
44. A modified experimental hut design for studying responses of disease-transmitting mosquitoes to indoor interventions: the Ifakara experimental huts. Okumu FO, Moore J, Mbeyela E, Sherlock M, Sangusangu R, Ligamba G, Russell T, Moore SJ, PLoS One 2012 7 30967 10.1371/journal.pone. 0030967 22347415
45. The suitability of clay pots for indoor sampling of mosquitoes in an arid area in northern Tanzania. van den Bijllaardt W, ter Braak R, Shekalaghe S, Otieno S, Mahande A, Sauerwein R, Takken W, Bousema T, Acta Trop 2009 111 197 199 10.1016/j.actatropica.2009.04.003 19524083
46. Barrier screens: a method to sample blood-fed and host-seeking exophilic mosquitoes. Burkot TR, Russell TL, Reimer LJ, Bugoro H, Beebe NW, Cooper RD, Sukawati S, Collins FH, Lobo NF, Malar J 2013 12 49 10.1186/1475-2875-12-49 23379959
47. An affordable, quality-assured community-based system for high-resolution entomological surveillance of vector mosquitoes that reflects human malaria infection risk patterns. 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, Malar J 2012 11 172 10.1186/1475-2875-11-172 22624853
48. Increased proportions of outdoor feeding among residual malaria vector populations following increased use of insecticide-treated nets in rural Tanzania. Russell TL, Govella NJ, Azizi S, Drakeley CJ, Kachur SP, Killeen GF, Malar J 2011 10 80 10.1186/1475-2875-10-80 21477321
49. Bionomics of the malaria vector Anopheles farauti in Temotu Province, Solomon Islands: issues for malaria elimination. Bugoro H, Cooper RD, Butafa C, Iro'ofa C, Mackenzie DO, Chen CC, Russell TL, Malar J 2011 10 133 10.1186/1475-2875-10-133 21592366
50. Outdoor host seeking behaviour of Anopheles gambiae mosquitoes following initiation of malaria vector control on Bioko Island, Equatorial Guinea. Reddy MR, Overgaard HJ, Abaga S, Reddy VP, Caccone A, Kiszewski AE, Slotman MA, Malar J 2011 10 184 10.1186/1475-2875-10-184 21736750
51. Entomological indices of malaria transmission in Chikhwawa district, Southern Malawi. Mzilahowa T, Hastings IM, Molyneux ME, McCall PJ, Malar J 2012 11 380 10.1186/1475-2875-11-380 23171123
52. Impact of insecticide-treated bed nets on malaria transmission indices on the south coast of Kenya. Mutuku FM, King CH, Mungai P, Mbogo C, Mwangangi J, Muchiri EM, Walker ED, Kitron U, Malar J 2011 10 356 10.1186/1475-2875-10-356 22165904
53. Development and field evaluation of a synthetic mosquito lure that is more attractive than humans. 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, PLoS One 2010 5 8951 10.1371/journal.pone.0008951 20126628
54. Spatial and temporal heterogeneity of Anopheles mosquitoes and Plasmodium falciparum transmission along the Kenyan coast. Mbogo CM, Mwangangi JM, Nzovu J, Gu WD, Yan GY, Gunter JT, Swalm C, Keating J, Regens JL, Shililu JI, Githure JI, Beier JC, Am J Trop Med Hyg 2003 68 734 742 12887036
55. High seasonal variation in entomologic inoculation rates in Eritrea, a semi-arid region of unstable malaria in Africa. Shililu J, Ghebremeskel T, Mengistu S, Fekadu H, Zerom M, Mbogo C, Githure J, Novak R, Brantly E, Beier JC, Am J Trop Med Hyg 2003 69 607 613 14740876
56. An estimation of the entomological inoculation rate for Ifakara: a semi-urban area in a region of intense malaria transmission in Tanzania. Drakeley C, Schellenberg D, Kihonda J, Sousa CA, Arez AP, Lopes D, Lines J, Mshinda H, Lengeler C, Schellenberg JA, Tanner M, Alonso P, Trop Med Int Health 2003 8 767 774 10.1046/j.1365-3156.2003.01100.x 12950662
57. The microepidemiology of malaria and its importance to malaria control. Greenwood BM, Trans R Soc Trop Med Hyg 1989 83 Suppl 25 29 2576161
58. Comparative evaluation of methods used for sampling malaria vectors in the Kilombero Valley, south eastern Tanzania. Okumu FO, Kotas ME, Kihonda J, Mathenge EM, Killeen GF, Moore SJ, Open Trop Med J 2008 1 51 55 10.2174/1874315300801010051
59. Spatial and temporal distribution of Anopheles gambiae s.l. (Diptera: Culicidae) in two Tanzanian villages: implication for designing mosquito sampling routines. Magbity EB, Lines JD, Bull Entomol Res 2002 92 483 488 17598299