Cited by 203Malaria Research and ControlMosquito-borne diseases and controlBird parasitology and diseases

The multiplicity of malaria transmission: a review of entomological inoculation rate measurements and methods across sub-Saharan Africa

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Kelly-Hope, Louise A, McKenzie, F Ellis·2009·Malaria Journal

Abstract

Plasmodium falciparum malaria is a serious tropical disease that causes more than one million deaths each year, most of them in Africa. It is transmitted by a range of Anopheles mosquitoes and the risk of disease varies greatly across the continent. The "entomological inoculation rate" is the commonly-used measure of the intensity of malaria transmission, yet the methods used are currently not standardized, nor do they take the ecological, demographic, and socioeconomic differences across populations into account. To better understand the multiplicity of malaria transmission, this study examines the distribution of transmission intensity across sub-Saharan Africa, reviews the range of methods used, and explores ecological parameters in selected locations. It builds on an extensive geo-referenced database and uses geographical information systems to highlight transmission patterns, knowledge gaps, trends and changes in methodologies over time, and key differences between land use, population density, climate, and the main mosquito species. The aim is to improve the methods of measuring malaria transmission, to help develop the way forward so that we can better assess the impact of the large-scale intervention programmes, and rapid demographic and environmental change taking place across Africa.

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  • Large, poorly quantified errors can arise in measuring VC because of the methods used to catch mosquitoes and estimate bionomic parameters.

    “large, poorly quantified errors can arise because of the methods used to catch mosquitoes and estimate bionomic parameters80”

    From Recasting the theory of mosquito-borne pathogen transmission dynamics and control (2014) · cites this paper as [80]

    The Results (APfEIR measurement methods; page not provided) report substantial variability in mosquito-sampling methods, and the Conclusion says studies often omitted collection details or failed to account for species’ feeding and resting patterns. Those passages support concern about poorly characterized measurement error, but the paper addresses entomological inoculation rate, not errors in vectorial capacity (VC) estimates or in estimating bionomic parameters. (LLM, conf=0.85)

    Experimental — accuracy not yet measured

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  1. Service MW Studies on sampling larval populations of the Anopheles gambiae complex Bull World Health Organ 1971 45 169 180 5316615 PMC2427901
  2. Service MW A critical review of procedures for sampling populations of adult mosquitoes Bull of Entomol Res 1977 67 343 382
  3. Hay SI Rogers DJ Toomer JF Snow RW Annual Plasmodium falciparum entomological inoculation rates (EIR) across Africa: literature survey, Internet access and review Trans R Soc Trop Med Hyg 2000 94 113 127 10897348 10.1016/S0035-9203(00)90246-3 PMC3204456 · DOI · Paper page
  4. 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 12641407
  5. Hay SI Guerra CA Tatem AJ Atkinson PM Snow RW Urbanization, malaria transmission and disease burden in Africa Nat Rev Microbiol 2005 3 81 90 15608702 10.1038/nrmicro1069 PMC3130901 · DOI · Paper page
  6. 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 16941936
  7. MacDonald G The epidemiology and control of malaria 1957 Oxford University Press, London
  8. Birley MH Charlewood JD Sporozoite rate and malaria prevalence Parasitol Today 1987 3 231 232 15462964 10.1016/0169-4758(87)90145-1 · DOI
  9. Hay SI Smith D Snow R Measuring malaria endemicity from intense to interrupted transmission Lancet Infect Dis 2008 8 369 378 18387849 10.1016/S1473-3099(08)70069-0 PMC2653619 · DOI
  10. Smith T Killeen GF Lengeler C Tanner M Relationships between the outcome of Plasmodium falciparum infection and the intensity of transmission in Africa Am J Trop Med Hyg 2004 71 80 86 15331822
  11. Killeen GF Ross A Smith T Infectiousness of malaria-endemic human populations to vectors Am J Trop Med Hyg 2006 75 38 45 16931814
  12. Fontenille D Lochouarn L Diagne N Sokhna C Lemasson JJ Diatta M Konate L Faye F Rogier C Trape JF High annual and seasonal variations in malaria transmission by anophelines and vector species composition in Dielmo, a holoendemic area in Senegal Am J Trop Med Hyg 1997 56 247 253 9129525
  13. Fontenille D Lochouarn L Diatta M Sokhna C Dia I Diagne N Lemasson JJ Ba K Tall A Rogier C Trape JF Four years' entomological study of the transmission of seasonal malaria in Senegal and the bionomics of Anopheles gambiae and A. arabiensis Trans R Soc Trop Med Hyg 1997 91 647 652 9509170 10.1016/S0035-9203(97)90506-X · DOI
  14. Killeen GF Tami A Kihonda J Okumu FO Kotas ME Grundmann H Kasigudi N Ngonyani H Mayagaya V Nathan R Abdulla S Charlwood JD Smith TA Lengeler C Cost-sharing strategies combining targeted public subsidies with private-sector delivery achieve high bednet coverage and reduced malaria transmission in Kilombero Valley, southern Tanzania BMC Infect Dis 2007 7 121 17961211 10.1186/1471-2334-7-121 PMC2211306 · DOI
  15. Killeen GF Smith TA Ferguson HM Mshinda H Abdulla S Lengeler C Kachur SP Preventing childhood malaria in Africa by protecting adults from mosquitoes with insecticide-treated nets PLoS Med 2007 4 e229 17608562 10.1371/journal.pmed.0040229 PMC1904465 · DOI
  16. Killeen GF Kihonda J Lyimo E Oketch FR Kotas ME Mathenge E Schellenberg JA Lengeler C Smith TA Drakeley CJ Quantifying behavioural interactions between humans and mosquitoes: evaluating the protective efficacy of insecticidal nets against malaria transmission in rural Tanzania BMC Infect Dis 2006 6 161 17096840 PMC1657018
  17. Craig MH Snow RW Le Suer D A climate-based distribution model of malaria transmission in sub-Saharan Africa Parasitology Today 1999 15 105 111 10322323 10.1016/S0169-4758(99)01396-4 · DOI · Paper page
  18. Sutton P Roberts D Elvidge C Baugh K Census from Heaven: an estimate of the global human population using nighttime satellite imagery Int J Remote Sens 2001 22 3061 3076 10.1080/01431160010007015 · DOI
  19. 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 8214283
  20. Rossi P Belli A Mancini L Sabatinelli G Enquête entomologique longitudinale sur la transmission du paludisme à Ouagadougou (Burkina Faso) Parassitologia 1986 28 1 15 [in French] 3455529
  21. Akogbéto M Chippaux JP Coluzzi M Le paludisme urbain côtier à Cotonou (République du Bénin). Étude entomologique Revue d'Epidémiologie et Santé Publique 1992 40 233 239 [in French] 1462029
  22. Akogbeto M Étude entomologique sur la transmission du paludisme côtièr lagunaire: cas d'un village construit sur un lac d'eau sâumatre Annales de la Société Belge de Médecine Tropicale 1995 75 219 227 [in French] 8849299
  23. Akogbéto M Nahum A Impact des moustiquaires impregnees de deltamethrine sur la transmission du paludisme dans un milieu cotier lagunaire, Benin Bulletin de la Société de Pathologie Exotique 1996 89 291 298 [in French] 9053053
  24. Karch S Asidi N Manzambi ZM Salaun JJ La faune anophélienne et la transmission du paludisme humain àKinshasa (Zaïre) Bulletin de la Société de Pathologie Exotique 1992 85 304 309 [in French] 1446181
  25. Karch S Garin B Asidi N Manzambi Z Salaun JJ Mouchet J Moustiquaires imprégnées contre le paludisme au Zaïre Annales de la Société Belge de Médecine Tropicale 1993 73 37 53 [in French] 8323407
  26. Trape JF Zoulani A Études sur le paludisme dans une zone de mosaïque forêt-savane d'Afrique centrale, la region de Brazzaville. I. Résultats des enquêtes entomologiques Bulletin de la Société de Pathologie Exotique 1987 80 84 99 [in French] 3608001
  27. Trape JF Zoulani A Malaria and urbanization in Central Africa: the example of Brazzaville. Part II: results of entomological surveys and epidemiological analysis Trans R Soc Trop Med Hyg 1987 81 10 18 2901796 10.1016/0035-9203(87)90472-X · DOI
  28. The US President's Malaria Initiative Lancet 2006 368 1 16815354 10.1016/S0140-6736(06)68939-3 · DOI
  29. Loewenberg S The US President's Malaria Initiative: 2 years on Lancet 2007 370 1893 1894 18074434 10.1016/S0140-6736(07)61795-4 · DOI
  30. Is malaria eradication possible? Lancet 2007 370 1459 17964329 10.1016/S0140-6736(07)61609-2 · DOI
  31. Roberts L Enserink M Malaria. Did they really say... eradication? Science 2007 318 1544 1545 18063766 10.1126/science.318.5856.1544 · DOI
  32. Bryan JH Anopheles gambiae and A. melas at Brefet, The Gambia, and their role in malaria transmission Ann Trop Med Parasitol 1983 77 1 12 6882050
  33. Mbogo CM Mwangangi JM Nzovu J Gu W Yan G 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 12887036
  34. Bigoga JD Manga L Titanji VP Coetzee M Leke RG Malaria vectors and transmission dynamics in coastal south-western Cameroon Malar J 2007 6 5 17233883 10.1186/1475-2875-6-5 PMC1783660 · DOI · Paper page
  35. Sylla EH Lell B Kun JF Kremsner PG Plasmodium falciparum transmission intensity and infection rates in children in Gabon Parasitol Res 2001 87 530 533 11484848 10.1007/s004360100407 · DOI
  36. Hay SI Randolph SE Rogers DF Baker JR Muller R Rollinson D Remote Sensing and Geographical Information Systems in Epidemiology (Advances in Parasitology) Academic Press 2000
  37. Sibley CH Barnes KI Watkins WM Plowe CV A network to monitor antimalarial drug resistance: a plan for moving forward Trends Parasitol 2008 24 43 48 Epub 2007 Nov 26. Review 18042432 10.1016/j.pt.2007.09.008 · DOI
  38. 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 8245934
  39. Davis JR Hall T Chee EM Majala A Minjas J Shiff CJ Comparison of sampling anopheline mosquitoes by light-trap and human-bait collections indoors at Bagamoyo, Tanzania Med Vet Entomol 1995 9 249 255 7548941 10.1111/j.1365-2915.1995.tb00130.x · DOI
  40. Mathenge EM Omweri GO Irungu LW Ndegwa PN Walczak E Smith TA Killeen GF Knols BGJ Comparative field evaluation of the Mbita trap, CDC light trap and the human landing catch for sampling of malaria vectors in western Kenya Am J Trop Med Hyg 2004 70 33 37 14971695
  41. Magbity EB Lines JD Spatial and temporal distribution of Anopheles gambiae s.l. (Diptera: Culicidae) in two Tanzanian villages: implications for designing mosquito sampling routines Bull Entomol Res 2002 92 483 488 17598299 10.1079/BER2002200 · DOI
  42. Mathenge EM Misiani GO Oulo DO Irungu LW Ndegwa PN Smith TA Killeen GF Knols BG 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 15667666 10.1186/1475-2875-4-7 PMC548676 · DOI
  43. Beier JC Perkins PV Wirtz RA Whitmire RE Mugambi M Hockmeyer WT Field evaluation of an enzyme-linked immunosorbent assay (ELISA) for Plasmodium falciparum sporozoite detection in anopheline mosquitoes from Kenya Am J Trop Med Hyg 1987 36 459 468 3555134
  44. Beier MS Schwartz IK Beier JC Perkins PV Onyango F Koros JK Campbell GH Andrysiak PM Brandling-Bennett AD Identification of malaria species by ELISA in sporozoite and oocyst infected Anopheles from western Kenya Am J Trop Med Hyg 1988 39 323 327 3056055
  45. Beier JC Perkins PV Koros JK Onyango FK Gargan TP Wirtz RA Koech DK Roberts CR Malaria sporozoite detection by dissection and ELISA to assess infectivity of afrotropical Anopheles (Diptera: Culicidae) J Med Entomol 1990 27 377 384 2185363
  46. Boudin C Robert V Verhave JP Carnevale P Ambroise-Thomas P Plasmodium falciparum and P. malariae epidemiology in a West African village Bull World Health Organ 1991 69 199 205 1677615 PMC2393086
  47. Adungo NI Mahadevan S Mulaya NL Situbi AP Githure JI Comparative determination of Plasmodium falciparum sporozoite rates in Afrotropical Anopheles from Kenya by dissection and ELISA Ann Trop Med Parasitol 1991 85 387 394 1796878
  48. Sokhna CS Diagne N Lochouarn L Rogier C Trape JF Spiegel A Fontenille D Comparative evaluation of the plasmodial infection of Anopheles using ELISA and dissection. Consequences for the estimation of the transmission of malaria in 1995 in Ndiop, Senegal Parasite 1998 5 273 279 [in French] 9772726
  49. Fontenille D Meunier JY Nkondjio CA Tchuinkam T Use of circumsporozoite protein enzyme-linked immunosorbent assay compared with microscopic examination of salivary glands for calculation of malaria infectivity rates in mosquitoes (Diptera: Culicidae) from Cameroon J Med Entomol 2001 38 451 454 11372973
  50. Sylla EH Kun JF Kremsner PG Mosquito distribution and entomological inoculation rates in three malaria-endemic areas in Gabon Trans R Soc Trop Med Hyg 2000 94 652 656 11198649 10.1016/S0035-9203(00)90219-0 · DOI
  51. Drakeley CJ Corran PH Coleman PG Tongren JE McDonald SL Carneiro I Malima R Lusingu J Manjurano A Nkya WM Lemnge MM Cox J Reyburn H Riley EM Estimating medium- and long-term trends in malaria transmission by using serological markers of malaria exposure Proc Natl Acad Sci USA 2005 102 5108 5113 15792998 10.1073/pnas.0408725102 PMC555970 · DOI
  52. Corran P Coleman P Riley E Drakeley C Serology: a robust indicator of malaria transmission intensity? Trends Parasitol 2007 23 575 82 Epub 2007 Nov 7. Review 17988945 10.1016/j.pt.2007.08.023 · DOI
  53. Sarr JB Remoue F Samb B Dia I Guindo S Sow C Maiga S Tine S Thiam C Schacht AM Simondon F Konate L Riveau G Evaluation of antibody response to Plasmodium falciparum in children according to exposure of Anopheles gambiae s.l or Anopheles funestus vectors Malar J 2007 6 117 17764568 10.1186/1475-2875-6-117 PMC2008208 · DOI
  54. 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 7785522 10.1016/0001-706X(94)00082-C · DOI
  55. Ribeiro JM Seulu F Abose T Kidane G Teklehaimanot A Temporal and spatial distribution of anopheline mosquitoes in an Ethiopian village: implications for malaria control strategies Bull World Health Organ 1996 74 299 305 8789928 PMC2486923
  56. Mboera LE Kihonda J Braks MA Knols BG Influence of centers for disease control light trap position, relative to a human-baited bed net, on catches of Anopheles gambiae Short report: and Culex quinquefasciatus in Tanzania Am J Trop Med Hyg 1998 59 595 596 9790436
  57. Oyewole IO Awolola TS Impact of urbanisation on bionomics and distribution of malaria vectors in Lagos, southwestern Nigeria J Vector Borne Dis 2006 43 173 178 17175702
  58. Rossi P Belli A Mancini L Sabatinelli G Enquête entomologique longitudinale sur la transmission du paludisme à Ouagadougou (Burkina Faso) Parassitologia 1986 28 1 15 [in French] 3455529
  59. Modiano D Petrarca V Sirima BS Nebié I Diallo D Esposito F Coluzzi M Different response to Plasmodium falciparum malaria in West African sympatric ethnic groups Proc Natl Acad Sci USA 1996 93 13206 13211 8917569 10.1073/pnas.93.23.13206 PMC24071 · DOI
  60. Aniedu I Dynamics of malaria transmission near two permanent breeding sites in Baringo district, Kenya Indian J Med Res 1995 105 206 211 9183076
  61. Tirados I Costantini C Gibson G Torr SJ Blood-feeding behaviour of the malarial mosquito Anopheles arabiensis: implications for vector control Med Vet Entomol 2006 20 425 437 17199754 10.1111/j.1365-2915.2006.652.x · DOI
  62. Björkman A Hedman P Brohult J Willcox M Diamant I Pehrsson PO Rombo L Bengtsson E Different malaria control activities in an area of Liberia- effects on malariometric parameters Ann Trop Med Parasitol 1985 79 239 246 3896168
  63. Trape JF Rogier C Konate L Diagne N Bouganali H Canque B Legros F Badji A Ndiaye G Ndiaye P Brahimi K Faye O Druilhe P Pereira Da Silva L The Dielmo Project: a longitudinal study of natural malaria infection and the mechanisms of protective immunity in a community living in a holoendemic area of Senegal Am J Trop Med Hyg 1994 51 123 137 8074247
  64. Elissa N Karch S Bureau P Ollomo B Lawoko M Yangari P Ebang B Georges AJ Malaria transmission in a region of savanna forest mosaic, Haut-Ogooue, Gabon J Am Mosquito Control Assoc 1999 15 15 23 10342264
  65. Elissa N Migot-Nabias F Luty A Renaut A Touré F Vaillant M Lawoko M Yangari P Mayombo J Lekoulou F Tshipamba P Moukagni R Millet P Deloron P Relationship between entomological inoculation rate, Plasmodium falciparum prevalence rate, and incidence of malaria attack in rural Gabon Acta Tropica 2003 85 355 361 12659973 10.1016/S0001-706X(02)00266-8 · DOI
  66. Okello PE Van Bortel W Byaruhanga AM Correwyn A Roelants P Talisuna A D'Alessandro U Coosemans M Variation in malaria transmission intensity in seven sites throughout Uganda Am J Trop Med Hyg 2006 75 219 225 16896122
  67. Meissner PE Mandi G Mockenhaupt FP Witte S Coulibaly B Mansmann U Frey C Merkle H Burhenne J Walter-Sack I Müller O Marked differences in the prevalence of chloroquine resistance between urban and rural communities in Burkina Faso Acta Trop 2008 105 81 86 Epub 2007 Aug 15 17904509 10.1016/j.actatropica.2007.07.014 · DOI

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Authors
Kelly-Hope, L. A., & McKenzie, F. E.
Affiliations
National Institutes of Health (US)
Venue
Malaria Journal
Published
2009-01-23
Volume
8
Issue
1
Pages
19-19
ISSN
1475-2875 (ISSN-L)
OpenAlex
W2112338101
Cited by
203
References
3
Citations by year
2026: 5 · 2025: 8 · 2024: 9 · 2023: 7 · 2022: 7 · 2021: 6 · 2020: 11 · 2019: 7 · 2018: 12 · 2017: 10 · 2016: 16 · 2015: 22 · 2014: 17 · 2013: 22 · 2012: 18
FWCI
1.99
Type
journal article
Language
en
Open access
Locations
  • Malaria Journal (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • LSTM Online Archive (Liverpool School of Tropical Medicine) (acceptedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Topics
  • Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Malaria Research and Control
  • Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Mosquito-borne diseases and control
  • Life Sciences › Immunology and Microbiology › Parasitology › Bird parasitology and diseases
Keywords
malaria transmission intensity, entomological inoculation rate, Plasmodium falciparum, Anopheles, sub-Saharan Africa, mosquito species composition, land use, population density, climate
MeSH terms
Animals, Insect Bites and Stings, Insect Vectors, Mosquito Control, Plasmodium falciparum, Population Density, Socioeconomic Factors, Malaria, Falciparum, Africa South of the Sahara, Endemic Diseases

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