Monitoring malaria vector control interventions: Effectiveness of five different adult mosquito sampling methods

Journal of Medical Entomology

Volumn 50, Issue 5, 2013, Pages 1140-1151

  Onyango, Shirley A ^a   Kitron, Uriel ^b   Mungai, Peter ^c   Muchiri, Eric M ^d   Kokwaro, Elizabeth ^a   King, Charles H ^c   Mutuku, Francis M ^b  

^a KENYATTA UNIVERSITY   (Kenya)

^b EMORY UNIVERSITY   (United States)

^c CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d Ministry of Public Health and Sanitation   (Kenya)

Author keywords

light trap; low vector density; mosquito surveillance; Prokopack; trapping method

Indexed keywords

ANIMAL; ARTICLE; CLASSIFICATION; DISEASE CARRIER; ENVIRONMENT; ENZYME LINKED IMMUNOSORBENT ASSAY; EVALUATION STUDY; FEMALE; KENYA; LYMPHATIC FILARIASIS; MALARIA FALCIPARUM; MALE; METHODOLOGY; MOSQUITO; PARASITOLOGY; PHYSIOLOGY; PLASMODIUM FALCIPARUM; SPECIES DIFFERENCE;

ANIMALS; CULICIDAE; ELEPHANTIASIS, FILARIAL; ENVIRONMENT; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; INSECT VECTORS; KENYA; MALARIA, FALCIPARUM; MALE; MOSQUITO CONTROL; PLASMODIUM FALCIPARUM; SPECIES SPECIFICITY;

EID: 84884642262     PISSN: 00222585     EISSN: None     Source Type: Journal    
DOI: 10.1603/ME12206     Document Type: Article

References (59)

1. Bayoh, M. N., D. Mathias, M. Odiere, F. Mutuku, L. Kamau, J. E. Gimnig, J. M. Vulule, W. Hawley, M. Hamel, and E. D. Walker. 2010. Anopheles gambiae: Historical population decline associated with regional distribution of insecticide treated bed nets in western Nyanza Province, Kenya. Malar. J. 9: 62.
2. Beier, J. C., P. V. Perkins, R. A. Wirtz, J. Koros, D. Diggs, T. P. Gargan, and D. K. Koech. 1988. Bloodmeal identification by direct enzyme-linked immunosorbent assay (ELISA), tested on Anopheles (Diptera: Culicidae) in Kenya. J. Med. Entomol. 25: 9-16.
3. Bhattarai, A., A. S. Ali, S. P. Kachur, A. Martensson, A. K. Abbas, R. Khatib, A. Al-mafazy, M. Ramsan, G. Rotllant, J. F. Gerstenmaier, et al. 2007. Impact of artemisininbased combination therapy and insecticide-treated nets on malaria burden in Zanzibar. PLoS Med. 4: E309.
4. Bijllaardt, W., R. Braak, S. Shekalaghe, S. Otieno, A. Mahande, R. Sauerwein, W. Takken, and T. Bousema. 2009. The suitability of clay pots for indoor sampling of mosquitoes in an arid area in northern Tanzania. Acta Trop. 111: 197-199.
5. Bockarie, M. J., E. M. Pedersen, G. B. White, and E. Michael. 2009. Role of vector control in the global program to eliminate lymphatic filariasis. Annu. Rev. Entomol. 54: 469-487.
6. Bødker, R., J. Akida, D. Shayo, W. Kisinza, H. A. Msangeni, E. M. Pedersen, and S. W. Lindsay. 2003. Relationship between altitude and intensity of malaria transmission in the Usambara Mountains, Tanzania. J. Med. Entomol. 40: 706-717.
7. Bögh, C., E. M. Pedersen, D. A. Mukoko, and J. H. Ouma. 1998. Permethrin-impregnated bednet effects on resting and feeding behaviour of lymphatic filariasis vector mosquitoes in Kenya. Med. Vet. Entomol. 12: 52-59.
8. Ceesay, S. J., C. Casals-Pascual, J. Erskine, S. E. Anya, N. O. Duah, A. J. Fulford, S. S. Sesay, I. Abubakar, S. Dunyo, O. P. Sey, et al. 2008. Changes in malaria indices between 1999 and 2007 in The Gambia: A retrospective analysis. Lancet 372: 1545-1554.
9. Costantini, C., N. Sagnon, E. Sanogo, L. Merzagora, and M. Coluzzi. 1998. Relationship to human biting collections and inßuence of light and bednet in CDC light-trap catches of west African malaria vectors. Bull. Entomol. Res. 88: 503-511.
10. Davis, J. R., T. Hall, E. M. Chee, A. Majala, J. Minjas, and C. J. Shiff. 1995. Comparison of sampling anopheline mosquitoes by light-trap and human-bait collections indoors at Bagamoyo, Tanzania. Med. Vet. Entomol. 9: 249-255.
11. Derua, Y. A., M. Alifrangis, K. M. Hosea, D. W. Meyrowitsch, S. M. Magesa, E. M. Pedersen, and P. E. Simonsen. 012. Change in composition of the Anopheles gambiae complex and its possible implications for the transmission of malaria and lymphatic filariasis in north-eastern Tanzania. Malar. J. 11: 188.
12. Dondorp, A. M., F. Nosten, P. Yi, D. Das, A. P. Phyo, J. Tarning, K. M. Lwin, F. Ariey, W. Hanpithakpong, S. J. Lee, et al. 2009. Artemisinin resistance in Plasmodium falciparum malaria. N. Engl. J. Med. 361: 455-467.
13. Fornadel, C. M., L. C. Norris, and D. E. Norris. 2010. Centers for disease control light traps for monitoring Anopheles arabiensis human biting rates in an area with low vector density and high insecticide-treated bed net use. Am. J. Trop. Med. Hyg. 83: 838-842.
14. Geissbühler, Y., P. Chaki, B. Emidi, N. J. Govella, R. Shirima, V. Mayagaya, D. Mtasiwa, H. Mshinda, U. Fillinger, S. W. Lindsay, et al. 2007. Interdependence of domestic malaria prevention measures and mosquito-human interactions in urban Dar es Salaam, Tanzania. Malar. J. 6: 126.
15. Gillies, M. T., and M. Coetzee. 1987. A supplement to the Anophelinae of Africa south of the Sahara (Afrotropical region). South African Institute for Medical Research, Johannesburg.
16. Gimnig, J. E., J. M. Vulule, T. Q. Lo, L. Kamau, M. S. Kolczak, P. A. Phillips-Howard, E. M. Mathenge, F. O. ter Kuile, B. L. Nahlen, and A. W. Hightower. 2003. Impact of permethrin-treated bednets on entomological indices in an area of intense year-round malaria transmission. Am. J. Trop. Med. Hyg. 68: 16-22.
17. Govella, N. J., P. Chaki, Y. Geissbühler, K. Kannady, F. O. Okumu,D. Charlwood, R. A. Anderson, and G. F. Killeen. 2009. A new tent trap for sampling exophagic and endophagic members of the Anopheles gambiae complex. Malar. J. 8: 157.
18. Govella, N. J., P. Chaki, J. M. Mpangile, and G. F. Killeen. 2011. 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 4: 40.
19. Jaenisch, T., D. J. Sullivan, A. Dutta, S. Deb, M. Ramsan, M. K. Othman, R. Gaczkowski, J. Tielsch, and S. Sazawal. 2010. Malaria incidence and prevalence on Pemba Island before the onset of the successful control intervention on the Zanzibar archipelago. Malar. J. 9: 32.
20. Jambou, R., E. Legrand, M. Niang, N. Khim, P. Lim, B. Volney, M. T. Ekala, C. Bouchier, P. Esterre, T. Fandeur, et al. 2005. Resistance of Plasmodium falciparum field isolates to in-vitro artemether and point mutations of the SERCA-type PfATPase6. Lancet 366: 1960-1963.
21. Kawada, H., K. Futami, O. Komagata, S. Kasai, T. Tomita, G. Sonye, C. Mwatele, S. M. Njenga, C. Mwandawiro, N. Minakawa, et al. 2011. Distribution of a knockdown resistance mutation (L1014S) in Anopheles gambiae s.s. and Anopheles arabiensis in western and southern Kenya. PLoS ONE 6: E24323. (doi:24310.21371/journal. pone.0024323).
22. Kenya National Central Bureau of Statistics. 2009. Population and housing census, population distribution by administrative areas and urban centers. Central Bureau of Statistics, Nairobi, Kenya.
23. Kulkarni, M. A., E. Kweka, E. Nyale, E. Lyatuu, F. W. Mosha, D. Chandramohan, M. E. Rau, and C. Drakeley. 2006. Entomological evaluation of malaria vectors at different altitudes in Hai district, northeastern Tanzania. J. Med. Entomol. 43: 580-588.
24. Kweka, E., B. J. Mwanǵonde, E. Kimaro, S. Msangi, C. P. Massenga, and A. Mahande. 2009. A resting box for outdoor sampling of adult Anopheles arabiensis in rice irrigation schemes of lower Moshi, northern Tanzania. Malar. J. 8: 82.
25. Lee, P. W., C. T. Liu, H. S. Rampao, V. E. do Rosario, and M. F. Shaio. 2010. Pre-elimination of malaria on the island of Prõńcipe. Malar. J. 9: 26.
26. Lines, J. D., C. F. Curtis, T. J. Wilkes, and K. J. Njunwa. 1991. Monitoring human biting mosquitoes (Diptera: Culicidae) in Tanzania with light traps hung besides mosquito nets. Bull. Entomol. Res. 81: 77-84.
27. Lyimo, I. N., and H. M. Ferguson. 2009. Ecological and evolutionary determinants of host species choice in mosquito vectors. Trends Parasitol. 25: 189-196.
28. Magbity, E. B., J. D. Lines, M. T. Marbiah, K. David, and E. Peterson. 2002. Howreliable 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. 92: 71-76.
29. Maia, M. F., A. Robinson, A. John, J. Mgando, E. Simfukwe, and S. J. Moore. 2011. Comparison of theCDCBackpack aspirator and the Prokopack aspirator for sampling indoor-and outdoor-resting mosquitoes in southern Tanzania. Parasit. Vectors. 4: 124.
30. Mathenge, E. M., G. O. Omweri, L. Irungu, P. N. Ndegwa, E. Walczak, T. A. Smith, G. F. Killeen, and B. G. Knols. 2004. Comparative field evaluation of the Mbita trap, CDClight trap and the human landing catch for sampling of malaria vectors in western Kenya. Am. J. Trop. Med. Hyg. 70: 33-37.
31. Mathenge, E. M., G. O. Misiani, D. O. Oulo, L. Irungu, P. N. Ndegwa, T. A. Smith, G. F. Killeen, and B. G. Knols. 2005. 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. 4: 7.
32. Mathias, D. K., E. Ochomo, F. Atieli, M. Ombok, M. N. Bayoh, G. Olang, D. Muhia, L. Kamau, J. Vulule, M. J. Hamel, et al. 2011. Spatial and temporal variation in the kdr allele L1014S in Anopheles gambiae s.s. and phenotypic variability in susceptibility to insecticides in western Kenya. Malar. J. 10: 10.
33. Mboera, L. E. 2005. Sampling techniques for adult Afrotropical malaria vectors and their reliability in the estimation of entomological inoculation rate. Tanzan. Health Res. Bull. 7: 117-124.
34. Mbogo, C. M., J. M. Mwangangi, J. Nzovu, W. Gu, G. Yan, J. Gunter, C. Swalm, J. Keating, J. L. Regens, J. I. Shililu, et al. 2003. Spatial and temporal heterogeneity of Anopheles mosquitoes and Plasmodium falciparum transmission along the Kenyan coast. Am. J. Trop. Med. Hyg. 68: 734-742.
35. Mbogo, C. N., G. E. Glass, D. Forster, E. W. Kabiru, J. I. Githure, J. H. Ouma, and J. C. Beier. 1993. Evaluation of light traps for sampling anopheline mosquitoes in Kilifi, Kenya. J. Am. Mosq. Control Assoc. 92: 260-263.
36. Meyrowitsch, D. W., E. M. Pedersen, M. Alifrangis, T. H. Scheike, M. N. Malecela, S. M. Magesa, Y. A. Derua, R. T. Rwegoshora, E. Michael, and P. E. Simonsen. 2011. Is the current decline in malaria burden in sub-Saharan Africa due to a decrease in vector populatioñ Malar. J. 10: 188.
37. Mutuku, F. M., C. H. King, P. Mungai, C. M. Mbogo, J. M. Mwangangi, E. M. Muchiri, E. D. Walker, and U. Kitron. 2011. Impact of insecticide treated bednets on malaria transmission indices on the south coast of Kenya. Malar. J. 10: 356.
38. Muturi, E. J., C. M. Mbogo, J. M. Mwangangi, Z. W. Ngànǵa, E. W. Kabiru, C. Mwandawiro, and J. C. Beier. 2006. Concomitant infections of Plasmodium falciparum and Wuchereria bancrofti on the Kenyan coast. Filaria J. 5: 8.
39. Muturi, E. J., C. M. Mbogo, Z. W. Ng̀anǵa, E. W. Kabiru, C. Mwandawiro, R. J. Novak, and J. C. Beier. 2006. Relationship between malaria and filariasis transmission indices in an endemic area along the Kenyan Coast. J. Vector Borne Dis. 43: 77-83.
40. Najera, J. O., M. Gonzalez-Silva, and P. L. Alonso. 2011. Some lessons for the future from the global malaria eradication programme (1955-1969). PLoS Med. 8: E1000412.
41. Ndenga, B., A. Githeko, E. Omukunda, G. Munyekenye, H. Atieli, P. Wamai, C. Mbogo, N. Minakawa, G. Zhou, and G. Yan. 2006. Population dynamics of malaria vectors in western Kenya highlands. J. Med. Entomol. 42: 200-206.
42. Ndiath, M. O., C. Mazenot, A. Gaye, L. Konate, C. Bouganali, O. Faye, C. Sokhna, and J. F. Trape. 2011. Methods to collect Anopheles mosquitoes and evaluate malaria transmission: A comparative study in two villages in Senegal. Malar. J. 10: 270.
43. O'Meara, W. P., P. Bejon, T. W. Mwangi, E. A. Okiro, N. Peshu, R. W. Snow, C. R. Newton, and K. Marsh. 2008. Effect of a fall in malaria transmission on morbidity and mortality in Kilifi, Kenya. Lancet 372: 1555-1562.
44. Odiere, M.,M.N. Bayoh, J. E. Gimnig, J.M.Vulule, L. Irungu, and E. D. Walker. 2007. Sampling outdoor, resting Anopheles gambiae and other mosquitoes (Diptera: Culicidae) in western Kenya with clay pots. J. Med. Entomol. 44: 14-22.
45. Okumu, F. O., M. E. Kotas, J. Kihonda, E. M. Mathenge, G. F. Killeen, and S. J. Moore. 2008. Comparative evaluation of methods used for sampling malaria vectors in the Kilombero valley, south eastern Tanzania. Open Trop. Med. J. 1: 51-55.
46. Overgaard, H. J., S. Sæbø,M. R. Reddy, V. P. Reddy, S. Abaga, A. Matias, and M. A. Slotman. 2012. Light traps fail to estimate reliable malaria mosquito biting rates on Bioko Island, Equatorial Guinea. Malar. J. 11: 56.
47. Pedersen, E. M., and D. A. Mukoko. 2002. Impact of insecticide-treated materials on filaria transmission by the various species of vector mosquito in Africa. Ann. Trop. Med. Parasitol. 96: S91-S95.
48. Ranson, H., R.N-Guessan, J Lines, N. Moiroux, Z. Nkuni, and V. Corbel. 2011. Pyrethroid resistance in African anopheline mosquitoes: What are the implications for malaria control? Trends Parasitol. 27: 91-97.
49. Russell, T. L., N. J. Govella, S. Azizi, C. J. Drakeley, S. P. Kachur, and G. F. Killeen. 2011. Increased proportions of outdoor feeding among residual malaria vector populations following increased use of insecticide-treated nets in rural Tanzania. Malar. J. 10: 80.
50. Rwegoshora, R. T., E. M. Pedersen, D. A. Mukoko, D. W. Meyrowitsch, N. Masese, M. N. Malecela-Lazaro, J. H. Ouma, E. Michael, and P. E. Simonsen. 2005. Bancroftian filariasis: Patterns of vector abundance and transmission in two East African communities with different levels of endemicity. Ann. Trop. Med. Parasitol. 99: 253-265.
51. Sikulu, M., N. J. Govella, S. B. Ogoma, J. M. Mpangile, S. H. Kambi, K. Kannady, P. Chaki, R. W. Mukabana, and G. Killeen. 2009. Comparative evaluation of the Ifakara tent trap-B, standardized resting boxes and human landing catch for sampling malaria vectors and other mosquitoes in urban Dar es Salaam, Tanzania. Malar. J. 8: 197.
52. Tatem, A. J., D. L. Smith, P.W.Gething, C.W.Kabaria, R.W. Snow, and S. I. Hay. 2010. Ranking of elimination feasibility between malaria-endemic countries. Lancet 376: 1579-1591.
53. The malERA Consultative Group on Vector Control. 2011. Aresearch agenda for malaria eradication: Vector control. PLoS Med. 8: E1000401.
54. Trape, J. F., A. Tall, N. Diagne, O. Ndiath, A. B. Ly, J. Faye, F. Dieye-Ba, C. Roucher, C. Bouganali, A. Badiane, et al. 2011. Malaria morbidity and pyrethroid resistance after the introduction of insecticide-treated bednets and artemisinin-based combination therapies: A longitudinal study. Lancet Infect. Dis. 11: 925-932.
55. Vazquez-Prokopec, G. M., W. A. Galvin, R. Kelly, and U. Kitron. 2009. Anew, cost-effective, battery-powered aspirator for adult mosquito collections. J. Med. Entomol. 46: 1256-1259.
56. White, G. B. 1974. Anopheles gambiae complex and disease transmission in Africa. Trans. R. Soc. Trop. Med. Hyg. 68: 278-298.
57. World Health Organization. 2003. Malaria entomology and vector control: LearnerÕs guide Geneva. World Health Organization, Geneva, Switzerland. (http://www.who. 18 Rev. 1 Part I
58. Wirtz, R. A., F. Zavala, Y. Charoenvit, G. H. Campbell, T. R. Burkot, I. Schneider, K. M. Esser, R. L. Beaudoin, and R. G. Andre. 1987. Comparative testing of monoclonal antibodies against Plasmodium falciparum sporozoites for ELISA development. Bull. W.H.O. 65: 39-45.
59. Yohannes, M., and E. Boelee. 2012. Early biting rhythm in the afro-tropical vector of malaria, Anopheles arabiensis, and challenges for its control in Ethiopia. Med. Vet. Entomol. 26: 103-105.