Characterization of malaria transmission by vector populations for improved interventions during the dry season in the Kpone-on-Sea area of coastal Ghana
Malaria is a major public health problem in Ghana. We present a site-specific entomological study of malaria vectors and transmission indices as part of an effort to develop a site for the testing of improved control strategies including possible vaccine trials.
Pyrethrum spray catches (PSC), and indoor and outdoor human landing collections of adult female anopheline mosquitoes were carried out over a six-month period (November 2005 - April 2006) at Kpone-on-Sea, a fishing village in southern Ghana. These were morphologically identified to species level and sibling species of the Anopheles gambiae complex further characterized by the polymerase chain reaction (PCR). Enzyme-linked immunosorbent assay was used to detect Plasmodium falciparum mosquito infectivity and host blood meal sources. Parity rate was examined based on dilatation of ovarian tracheoles following dissection.
Of the 1233 Anopheles mosquitoes collected, An. gambiae s.l. was predominant (99.5%), followed by An. funestus (0.4%) and An. pharoensis (0.1%). All An. gambiae s.l. examined (480) were identified as An. gambiae s.s. with a majority of M molecular form (98.2%) and only 1.8% S form with no record of M/S hybrid. A significantly higher proportion of anophelines were observed outdoors relative to indoors (χ 2 = 159.34, df = 1, p < 0.0000). Only An. gambiae M molecular form contributed to transmission with a high degree of anthropophily, parity rate and an estimated entomological inoculation rate (EIR) of 62.1 infective bites/person/year. The Majority of the infective bites occurred outdoors after 09.00 pm reaching peaks between 12.00-01.00 am and 03.00-04.00 am.
Anopheles gambiae M molecular form is responsible for maintaining the status quo of malaria in the surveyed site during the study period. The findings provide a baseline for evidence-based planning and implementation of improved malaria interventions. The plasticity observed in biting patterns especially the combined outdoor and early biting behavior of the vector may undermine the success of insecticide-based strategies using insecticide treated nets (ITN) and indoor residual spray (IRS). As such, novel or improved vector interventions should be informed by the local malaria epidemiology data as it relates to vector behavior.
- Touré YT, Oduola AMJ, Morel CM: The Anopheles gambiae genome: next steps for malaria vector control. Trends Parasitol 2004,20(3):142–149. CrossRef
- Griffin JT, Hollingsworth TD, Okell LC, Churcher TS, White M, Hinsley W, Bousema T, Drakeley CJ, Ferguson NM, Basáñez M-G, Ghani AC: Reducing Plasmodium falciparum malaria transmission in Africa: a model-based evaluation of intervention strategies. PLoS Med 2010,7(8):e1000324. CrossRef
- Burkot TR, Graves PM: The value of vector-based estimates of malaria transmission. Ann Trop Med Parasitol 1995, 89:125–134.
- Coosemans M, Wery M, Mouchet J, Carnevale P: Transmission factors in malaria epidemiology and control in África. Mem Inst Oswaldo Cruz 1992, 87:385–391. CrossRef
- Smith T, Charlwood JD, Takken W, Tanner M, Spiegelhalter DJ: Mapping the densities of malaria vectors within a single village. Acta Trop 1995, 59:1–18. CrossRef
- National Research Council: Background: malaria as a disease. In Malaria: Obstacles and Opportunities. Edited by: Oaks SCJ, Mitchell VS, Pearson GW, Carpenter CCJ. Washington DC: The National Academies Press; 1991:22–36.
- Fontenille D, Simard F: Unraveling complexities in the human malaria transmission dynamics in Africa through a comprehensive knowledge of vector populations. Comp Immunol Microbiol Dis 2004, 27:357–375. CrossRef
- Antonio-Nkonjio C, Kerah CH, Simard F, Awono-Ambene P, Chouaibou M, Tchuinkam T, Fontenille D: Complexity of malaria vectorial system in Cameroon: contribution of secondary vectors to malaria transmission. J Med Entomol 2006, 43:1215–1221. CrossRef
- Pates H, Curtis C: Mosquito behavior and vector control. Annu Rev Entomol 2005, 50:53–70. CrossRef
- Trung HD, Van Bortel W, Sochantha T, Keokenchanh K, Briet OJT, Coosemans M: Behavioral heterogeneity of Anopheles species in ecologically different localities in Southeast Asia: a challenge for vector control. Trop Med Int Health 2005,10(3):251–262. CrossRef
- Coluzzi M, Sabatini A, Petrarca V, Di Deco MA: Behavioral divergences between mosquitoes with different inversion karyotypes in polymorphic populations of the Anopheles gambiae complex. Nature 1977,266(5605):832–833. CrossRef
- Molineaux L, Shidrawi GR, Clarke JL, Boulzaguet JR, Ashkar TS: Assessment of insecticidal impact on the malaria mosquito's vectorial capacity, from data on the man-biting rate and age-composition. Bull World Health Organ 1979,57(2):265–274.
- Riehle MM, Guelbeogo WM, Gneme A, Eiglmeier K, Holm I, Bischoff E, Garnier T, Snyder GM, Li X, Markianos K, Sagnon N, Vernick KD: A cryptic subgroup of Anopheles gambiae is highly susceptible to human malaria parasites. Science 2011, 331:596. CrossRef
- Banerjee A, Nayak B: Epidemiological and entomological correlation of malaria transmission in an Air Force station. MJAFI 2001,57(3):191–193.
- Himeidan YE, Elzaki MM, Kweka EJ, Ibrahim M, Elhassan IM: Pattern of malaria transmission along the Rahad River basin. Eastern Sudan. Parasit Vectors 2011, 4:109. CrossRef
- Adams I, Darko D, Accorsi S: Malaria: a burden explored. Bull Health Information 2004,1(1):28–34.
- Bell D, Wongsrichanalai C, Barnwell JW: Ensuring quality and access for malaria diagnosis: how can it be achieved? Nat Rev Microbiol 2006, 44:S7-S20. CrossRef
- Greenwood BM: Control to elimination: implications for malaria research. Trends Parasitol 2008,24(10):449–454. CrossRef
- The malERA Consultative Group on Monitoring: Evaluation, and Surveillance: A research agenda for malaria eradication: monitoring, evaluation, and surveillance. PLoS Med 2011, 8:e1000400. CrossRef
- Quakyi IA, Addison AE, Bosompem K, Wilson MD, Kumar N, Boakye DA, Adjei A, Armah H, Koram KA, Quansah AG, Dodo A, Appawu MA, Mensah G, Mckakpo U, Amarh D, Lomotey F, Brown C, Ankrah I, Bruce J, Madjitey P, Adjei R, Amankwah P, Laar AK, Soyiri IN, Koranchie P, Tagoe BA: Malaria in Kpone-on-Sea: a fishing village in southern Ghana (I) Prevalence Studies, Report to WHO/TDR. 2004.
- Gillies MT, De Meillon B: The Anophelinae of Africa South of the Sahara (Ethiopian Zoogeographical region). 2nd edition. Johannesburg, South Africa: South African Institute of Medical Research; 1968.
- Gillies MT, Coetzee M: A supplement to the Anophelinae of Africa South of the Sahara. Johannesburg: South African Institute for Medical Research; 1987.
- Detinova TS: Age grouping methods in Dipterans of medical importance. In WHO Monograph Series vol. 47. Geneva: WHO; 1962:216.
- Scott JA, Brogdou WG, Collins FH: Identification of single specimens of the Anopheles gambiae. Am J Trop Med Hyg 1993, 49:520–529.
- Favia G, Della Torré A, Bagayoko M, Lanfrancotti A, Sagnon NF, Toure TT, Coluzzi M: Molecular identification of sympatric chromosomal forms of Anopheles gambiae and further evidence of their reproductive isolation. Insect Mol Biol 1997,6(4):377–383. CrossRef
- Wirtz RA, Burkot TR, Graves PM, Andre RG: Field evaluation of enzyme-linked immunosorbent assays for Plasmodium falciparum and Plasmodium vivax sporozoites in mosquitoes (Diptera: Culicidae) from Papua New Guinea. J Med Entomol 1987,24(4):233–237.
- Beier JC, Perkins PV, Wirtz RA, Koros JK, Diggs D, Gargan TP, Koech DK: Bloodmeal identification by direct enzyme-linked immunosorbent assay (ELISA), tested on Anopheles (Diptera: Culicidae) in Kenya. J Med Entomol 1988, 25:9–16.
- Lines JD, Curtis CF, Wilkes TJ, Njunwa KJ: Monitoring human-biting mosquitoes (Diptera: Culicidae) in Tanzania with light-traps hung beside mosquito nets. B Entomol Res 1991, 81:77–84. CrossRef
- Development Core Team R: R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2010.
- Appawu MA, Baffoe-Wilmot A, Afari EA, Dunyo S, Koram KA, Nkrumah FK: Malaria vectors in two ecological zones in southern Ghana. Afr Entomol 2001,9(1):59–65.
- Okoye PN, Wilson MD, Boakye DA, Brown CB: Impact of the Okyereko irrigation project in Ghana on the risk of human malaria infection by Anopheles species (Diptera: Culicidae). Afr Entomol 2005,13(2):249–253.
- Bigoga JD, Manga L, Titanji VPK, Coetzee M, Leke RGF: Malaria vectors and transmission dynamics in coastal south-western Cameroon. Malaria J 2007, 6:5. CrossRef
- Akogbeto M: Le paludisme côtier lagunaire à Cotonou: données entomologiques, Cahiers d'études et de recherches francophones. Sante 2000, 10:267–275.
- Diop A, Molez JF, Konate L, Fontenille D, Gaye O, Diouf M, Diagne M, Faye O: Role of Anopheles melas Theobald (1903) on malaria transmission in a mangrove swamp in Senegal. Parasite 2002, 9:239–246.
- Awolola TS, Okwa O, Hunt TH, Ogunrinade AF, Coetzee M: Dynamics of the malaria-vector populations in coastal Lagos, south-western Nigeria. Ann Trop Med Parasitol 2002, 96:75–82. CrossRef
- Ijumba JN, Lindsay SW: Impact of irrigation on malaria in Africa: paddies paradox. Med Vet Entomol 2001, 15:1–11. CrossRef
- Touré YT, Dolo G, Petrarca V, Traore SF, Bouare M, Dao A, Carnahan J, Taylor CE: Mark-release recapture experiments with Anopheles gambiae s.l. in Banambani village, Mali, to determine population size and structure. Med Vet Entomol 1994,12(1):74–83. CrossRef
- Minakawa N, Githure JI, Beir JC, Yan G: Anopheline mosquito survival strategies during the dry period in western Kenya. J Med Entomol 2003, 38:388–392. CrossRef
- Appawu M, Owusu-Agyei S, Dadzie S, Asoala V, Anto F, Koram K, Rogers W, Nkrumah F, Hoffman SL, Fryauff DJ: Malaria transmission dynamics at a site in northern Ghana proposed for testing malaria vaccines. Trop Med Int Health 2004, 9:164–170. CrossRef
- Wondji CS, Simard F, Fontenille D: Evidence for genetic differentiation between the molecular forms M and S within the Forest chromosomal form of Anopheles gambiae in an area of sympatry. Insect Mol Biol 2002, 11:11–19. CrossRef
- Lehmann TLM, Elissa N, Maega BT, Chimumbwa JM, Watsenga FT, Wondji CS, Simard F, Hawley WA: Population structure of Anopheles gambiae in Africa. J Hered 2003, 94:133–147. CrossRef
- Ferguson HM, Dornhaus A, Beeche A, Borgemeister C, Gottlieb M, Mulla MS, Gimnig JE, Fish D, Killeen GF: Ecology: a prerequisite for malaria elimination and eradication. PLoS Med 2010,7(8):e1000303. CrossRef
- Govella NJ, Okumu FO, Killeen GF: Insecticide-treated nets can reduce malaria transmission by mosquitoes which feed outdoors. Am J Trop Med Hyg 2010, 82:415–419. CrossRef
- Townson H, Nathan MB, Zaim M, Guillet P, Manga L, Bos R, Kindhauser M: Exploiting the potential of vector control for disease prevention. Bull World Health Organ 2005, 83:942–947.
- Service MW: Mosquito ecology: field sampling methods. London: Applied Science publishers; 1976.
- Ghosh AK, Ribolla PE, Jacobs-Lorena M: The journey of the malaria parasite in the mosquito: hopes for the new century. Parasitol Today 2000,16(5):196–201. CrossRef
- Costantini C, Sagnon N, Della Torre A, Diallo M, Brady J, Gibson G, Coluzzi M: Odor-mediated host preferences of West African mosquitoes, with particular reference to malaria vectors. Am J Trop Med Hyg 1998, 58:56–63.
- Omer SM, Cloudsley-Thompson JL: Survival of female Anopheles gambiae Giles through a 9-month dry season in Sudan. Bull World Health Organ 1970, 42:319–330.
- Hay SI, Rogers DJ, Toomer JF, Snow RW: Annual Plasmodium falciparum entomological inoculation rate [EIR] across Africa: literature survey, internet access and review. Trans R Soc Trop Med Hyg 2000, 94:113–127. CrossRef
- Takken W, Lindsay S: Factors affecting the vectorial competence of Anopheles gambiae: a question of scale. In Ecological Aspects for Application of Genetically Modified mosquitoes. Edited by: Takken W, Scott TW. Wageningen: Kluwer Academic Publishers; 2003:83.
- Characterization of malaria transmission by vector populations for improved interventions during the dry season in the Kpone-on-Sea area of coastal Ghana
- Open Access
- Available under Open Access This content is freely available online to anyone, anywhere at any time.
Parasites & Vectors
- Online Date
- September 2012
- Online ISSN
- BioMed Central
- Additional Links
- Anopheles gambiae M molecular form
- Plasmodium falciparum
- Malaria transmission
- Biting pattern
- Parity rate
- Author Affiliations
- 1. School of Public Health, University of Ghana, Legon, Ghana
- 2. Noguchi Memorial Institute for Medical Research, University of Ghana, Legon, Ghana