Ranking malaria risk factors to guide malaria control efforts in African highlands

PLoS ONE

Volumn 4, Issue 11, 2009, Pages

  Protopopoff, Natacha ^a,b   Van Bortel, Wim ^a   Speybroeck, Niko ^a,c   Van Geertruyden, Jean Pierre ^a   Baza, Dismas ^d   D'Alessandro, Umberto ^a   Coosemans, Marc ^a,e  

^a INSTITUTE OF TROPICAL MEDICINE   (Belgium)

^b MÉDECINS SANS FRONTIÈRES   (Belgium)

^c UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^d Ministry of Health   (Burundi)

^e UNIVERSITY OF ANTWERP   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

AFRICA; ANOPHELES; ARTICLE; CLASSIFICATION AND REGRESSION TREE; DISEASE CARRIER; DISEASE TRANSMISSION; EPIDEMIC; HEALTH STATUS; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; MALARIA; MALARIA CONTROL; MALNUTRITION; NONHUMAN; PREVALENCE; RISK FACTOR; SEASONAL VARIATION; STATISTICAL ANALYSIS; ADOLESCENT; ADULT; ANIMAL; BED; BED NET; BURUNDI; CHILD; DECISION SUPPORT SYSTEM; FEMALE; GENETICS; HUMAN; MALE; METHODOLOGY; MOSQUITO; MULTIVARIATE ANALYSIS; REGRESSION ANALYSIS; TEMPERATURE;

INSECTICIDE;

ADOLESCENT; ADULT; ANIMALS; ANOPHELES; BEDDING AND LINENS; BURUNDI; CHILD; DECISION SUPPORT TECHNIQUES; FEMALE; HUMANS; INSECT VECTORS; INSECTICIDES; MALARIA; MALE; MOSQUITO CONTROL; MOSQUITO NETS; MULTIVARIATE ANALYSIS; REGRESSION ANALYSIS; RISK FACTORS; TEMPERATURE;

EID: 71049186047     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0008022     Document Type: Article

References (100)

1. Mouchet J, Manguin S, Sircoulon J, Laventure S, Faye O, et al. (1998) Evolution of malaria in Africa for the past 40 years: impact of climatic and human factors. J Am Mosq Control Assoc 14: 121-130.
2. Lindsay SW, Martens WJ (1998) Malaria in the African highlands: past, present and future. Bull World Health Organ 76: 33-45.
3. Hay SI, Noor AM, Simba M, Busolo M, Guyatt HL, et al. (2002) Clinical epidemiology of malaria in the highlands of western Kenya. Emerg Infect Dis 8: 543-548.
4. Malakooti MA, Biomndo K, Shanks GD (1998) Reemergence of epidemic malaria in the highlands of western Kenya. Emerg Infect Dis 4: 671-676.
5. Lindblade KA, Walker ED, Onapa AW, Katungu J, Wilson ML (1999) Highland malaria in Uganda: prospective analysis of an epidemic associated with El Nino. Trans R Soc Trop Med Hyg 93: 480-487.
6. Mouchet J, Laventure S, Blanchy S, Fioramonti R, Rakotonjanabelo A, et al. (1997) La reconquête des hautes terres de Madagascar par le paludisme. Bull Soc Pathol Exot 90: 162-168.
7. Negash K, Kebede A, Medhin A, Argaw D, Babaniyi O, et al. (2005) Malaria epidemics in the highlands of Ethiopia. East Afr Med J 82: 186-192.
8. Zhou G, Minakawa N, Githeko AK, Yan G (2004) Association between climate variability and malaria epidemics in the East African highlands. Proc Natl Acad Sci U S A 101: 2375-2380.
9. WHO (2006) The Africa malaria report 2006.
10. WHO (2000) The African summit on Roll Back Malaria.;WHO/CDS/RBM/2000.17:.
11. Held TK, Weinke T, Mansmann U, Trautmann M, Pohle HD (1994) Malaria prophylaxis: identifying risk groups for non-compliance. Q J Med 87: 17-22.
12. Thang ND, Erhart A, Speybroeck N, Hung lX, Thuan lK, et al. (2008) Malaria in central Vietnam: analysis of risk factors by multivariate analysis and classification tree models. Malar J 7: 28.
13. Speybroeck N, Berkvens D, Mfoukou-Ntsakala A, Aerts M, Hens N, et al. (2004) Classification trees versus multinomial models in the analysis of urban farming systems in Central Africa. Agric Syst 80: 133-149.
14. Protopopoff N, Van Bortel W, Marcotty T, Van Herp M, Maes P, et al. (2007) Spatial targeted vector control in the highlands of Burundi and its impact on malaria transmission. Malar J 6: 158.
15. Protopopoff N, Van Bortel W, Marcotty T, Van Herp M, Maes P, et al. (2008) Spatial targeted vector control is able to reduce malaria prevalence in the highlands of Burundi. Am J Trop Med Hyg 79: 12-18.
16. Breiman L, Friedman JH, Stone CJ, Olshen RA (1993) Classification and regression trees. New York: Chapman and Hall.
17. McCarthy FD, Wolf H, Wu Y (2000) The growth costs of Malaria. National Bureau of Economic Research, inc NBER working papers 7541.
18. Bodker R, Msangeni HA, Kisinza W, Lindsay SW (2006) Relationship between the intensity of exposure to malaria parasites and infection in the Usambara Mountains, Tanzania. Am J Trop Med Hyg 74: 716-723.
19. Fontaine RE, Najjar AE, Prince JS (1961) The 1958 malaria epidemic in Ethiopia. Am J Trop Med Hyg 10: 795-803.
20. Shankar AH (2000) Nutritional modulation of malaria morbidity and mortality. J Infect Dis 182 Suppl 1: S37-S53.
21. Craig MH, Kleinschmidt I, Le Sueur D, Sharp BL (2004) Exploring 30 years of malaria case data in KwaZulu-Natal, South Africa: part II. The impact of non-climatic factors. Trop Med Int Health 9: 1258-1266.
22. Van Geertruyden JP, Menten J, Colebunders R, Korenromp E, D'Alessandro U (2008) The impact of HIV-1 on the malaria parasite biomass in adults in sub-Saharan Africa contributes to the emergence of antimalarial drug resistance. Malar J 7: 134.
23. Elghazali G, Adam I, Hamad A, El Bashir MI (2003) Plasmodium falciparum infection during pregnancy in an unstable transmission area in eastern Sudan. East Mediterr Health J 9: 570-580.
24. Menendez C (1995) Malaria during pregnancy: a priority area of malaria research and control. Parasitol Today 11: 178-183.
25. Van Eijk AM, Ayisi JG, Ter Kuile FO, Otieno JA, Misore AO, et al. (2004) Effectiveness of intermittent preventive treatment with sulphadoxine-pyrimethamine for control of malaria in pregnancy in western Kenya: a hospital-based study. Trop Med Int Health 9: 351-360.
26. Massaga JJ, Kitua AY, Lemnge MM, Akida JA, Malle LN, et al. (2003) Effect of intermittent treatment with amodiaquine on anaemia and malarial fevers in infants in Tanzania: a randomised placebo-controlled trial. Lancet 361: 1853-1860.
27. Bodker R, Kisinza W, Malima R, Msangeni H, Lindsay S (2000) Resurgence of malaria in the Usambara mountains, Tanzania, an epidemic of drug-resistant parasites. Glob Change Hum Health 1: 134-153.
28. Shanks GD, Biomndo K, Hay SI, Snow RW (2000) Changing patterns of clinical malaria since 1965 among a tea estate population located in the Kenyan highlands. Trans R Soc Trop Med Hyg 94: 253-255.
29. Hay SI, Rogers DJ, Randolph SE, Stern DI, Cox J, et al. (2002) Hot topic or hot air? Climate change and malaria resurgence in East African highlands. Trends Parasitol 18: 530-534.
30. Bjorkman A, Bhattarai A (2005) Public health impact of drug resistant Plasmodium falciparum malaria. Acta Trop 94: 163-169.
31. Trape JF (2001) The public health impact of chloroquine resistance in Africa. Am J Trop Med Hyg 64: 12-17.
32. Bousema JT, Gouagna LC, Meutstege AM, Okech BE, Akim NI, et al. (2003) Treatment failure of pyrimethamine-sulphadoxine and induction of Plasmodium falciparum gametocytaemia in children in western Kenya. Trop Med Int Health 8: 427-430.
33. Sowunmi A, Fateye BA (2003) Plasmodium falciparum gametocytaemia in Nigerian children: before, during and after treatment with antimalarial drugs. Trop Med Int Health 8: 783-792.
34. Nosten F, Van Vugt M, Price R, Luxemburger C, Thway KL, et al. (2000) Effects of artesunate-mefloquine combination on incidence of Plasmodium falciparum malaria and mefloquine resistance in western Thailand: a prospective study. Lancet 356: 297-302.
35. Barnes KI, Durrheim DN, Little F, Jackson A, Mehta U, et al. (2005) Effect of artemether-lumefantrine policy and improved vector control on malaria burden in KwaZulu-Natal, South Africa. PLoS Med 2: e330.
36. Martens P, Hall L (2000) Malaria on the move: human population movement and malaria transmission. Emerg Infect Dis 6: 103-109.
37. Hay SI, Guerra CA, Tatem AJ, Noor AM, Snow RW (2004) The global distribution and population at risk of malaria: past, present, and future. Lancet Infect Dis 4: 327-336.
38. Moffett A, Shackelford N, Sarkar S (2007) Malaria in Africa: vector species' niche models and relative risk maps. PLoS ONE 2: e824.
39. MacDonald G (1957) The epidemiology and control of malaria. London: Oxford University Press.
40. Garnham PCC (1945) Malaria epidemics at exceptionally high altitudes in Kenya. Br Med J 2: 45-47.
41. Warrell DA, Gilles HM (2002) Essential Malariology. Arnold.
42. Balls MJ, Bodker R, Thomas CJ, Kisinza W, Msangeni HA, et al. (2004) Effect of topography on the risk of malaria infection in the Usambara Mountains, Tanzania. Trans R Soc Trop Med Hyg 98: 400-408.
43. Bayoh MN, Lindsay SW (2004) Temperature-related duration of aquatic stages of the Afrotropical malaria vector mosquito Anopheles gambiae in the laboratory. Med Vet Entomol 18: 174-179.
44. Koenraadt CJ, Paaijmans KP, Schneider P, Githeko AK, Takken W (2006) Low larval vector survival explains unstable malaria in the western Kenya highlands. Trop Med Int Health 11: 1195-1205.
45. Vincke IH, Jadin JB (1946) Contribution à l'étude de l'anophélisme en pays d'altitude. Ann Soc Belg Med Trop 26: 483-500.
46. Abeku TA, Van Oormarssen GJ, Borsboom G, de Vlas SJ, Habbema JD (2003) Spatial and temporal variations of malaria epidemic risk in Ethiopia: factors involved and implications. Acta Trop 87: 331-340.
47. Lindblade KA, Walker ED, Onapa AW, Katungu J,Wilson ML (2000) Land use change alters malaria transmission parameters by modifying temperature in a highland area of Uganda. Trop Med Int Health 5: 263-274.
48. Afrane YA, Lawson BW, Githeko AK, Yan G (2005) Effects of microclimatic changes caused by land use and land cover on duration of gonotrophic cycles of Anopheles gambiae (Diptera: Culicidae) in western Kenya highlands. J Med Entomol 42: 974-980.
49. Munga S, Minakawa N, Zhou G, Mushinzimana E, Barrack OO, et al. (2006) Association between land cover and habitat productivity of malaria vectors in western Kenyan highlands. Am J Trop Med Hyg 74: 69-75.
50. Loevinsohn ME (1994) Climatic warming and increased malaria incidence in Rwanda. Lancet 343: 714-718.
51. Minakawa N, Sonye G, Mogi M, Githeko A, Yan G (2002) The effects of climatic factors on the distribution and abundance of malaria vectors in Kenya. J Med Entomol 39: 833-841.
52. Pascual M, Ahumada JA, Chaves LF, Rodo X, Bouma M (2006) Malaria resurgence in the East African highlands: temperature trends revisited. Proc Natl Acad Sci U S A 103: 5829-5834.
53. Paaijmans KP, Wandago MO, Githeko AK, Takken W (2007) Unexpected high losses of Anopheles gambiae larvae due to rainfall. PLoS ONE 2: e1146.
54. Kilian AH, Langi P, Talisuna A, Kabagambe G (1999) Rainfall pattern, El Nino and malaria in Uganda. Trans R Soc Trop Med Hyg 93: 22-23.
55. Lindsay SW, Bodker R, Malima R, Msangeni HA, Kisinza W (2000) Effect of 1997-98 El Nino on highland malaria in Tanzania. Lancet 355: 989-990.
56. Minakawa N, Sonye G, Mogi M, Yan G (2004) Habitat characteristics of Anopheles gambiae s.s. larvae in a Kenyan highland. Med Vet Entomol 18: 301-305.
57. Zhou G, Minakawa N, Githeko A, Yan G (2004) Spatial distribution patterns of malaria vectors and sample size determination in spatially heterogeneous environments: a case study in the west Kenyan highland. J Med Entomol 41: 1001-1009.
58. Minakawa N, Munga S, Atieli F, Mushinzimana E, Zhou G, et al. (2005) Spatial distribution of anopheline larval habitats in Western Kenyan highlands: effects of land cover types and topography. Am J Trop Med Hyg 73: 157-165.
59. Khaemba BM, Mutani A, Bett MK (1994) Studies of anopheline mosquitoes transmitting malaria in a newly developed highland urban area: a case study of Moi University and its environs. East Afr Med J 71: 159-164.
60. Ijumba JN, Lindsay SW (2001) Impact of irrigation on malaria in Africa: paddies paradox. Med Vet Entomol 15: 1-11.
61. Sissoko MS, Dicko A, Briet OJ, Sissoko M, Sagara I, et al. (2004) Malaria incidence in relation to rice cultivation in the irrigated Sahel of Mali. Acta Trop 89: 161-170.
62. Garnham PCC, Wilson DB, Wilson ME (1948) Malaria in Kigezi, Uganda. Trop Med Hyg 51: 156-159.
63. Schwetz J (1948) Paludisme endémique et paludisme epidémique dans des régions de haute altitude de l'Afrique centrale. Acta Trop 5: 78-81.
64. Carlson JC, Byrd BD, Omlin FX (2004) Field assessments in western Kenya link malaria vectors to environmentally disturbed habitats during the dry season. BMC Public Health 4: 33.
65. Stevens PA (1984) Environmental management activities in malaria control in Africa. Bull World Health Organ 62 Suppl: 77-80.
66. Utzinger J, Tozan Y, Singer BH (2001) Efficacy and cost-effectiveness of environmental management for malaria control. Trop Med Int Health 6: 677-687.
67. Yohannes M, Haile M, Ghebreyesus TA, Witten KH, Getachew A, et al. (2005) Can source reduction of mosquito larval habitat reduce malaria transmission in Tigray, Ethiopia? Trop Med Int Health 10: 1274-1285.
68. Curtis CF, Jana-Kara B, Maxwell CA (2003) Insecticide treated nets: impact on vector populations and relevance of initial intensity of transmission and pyrethroid resistance. J Vector Borne Dis 40: 1-8.
69. Mathenge EM, Gimnig JE, Kolczak M, Ombok M, Irungu LW, et al. (2001) Effect of permethrin-impregnated nets on exiting behavior, blood feeding success, and time of feeding of malaria mosquitoes (Diptera: Culicidae) in western Kenya. J Med Entomol 38: 531-536.
70. Lindsay SW, Adiamah JH, Miller JE, Armstrong JR (1991) Pyrethroid-treated bednet effects on mosquitoes of the Anopheles gambiae complex in The Gambia. Med Vet Entomol 5: 477-483.
71. Hargreaves K, Koekemoer LL, Brooke BD, Hunt RH, Mthembu J, et al. (2000) Anopheles funestus resistant to pyrethroid insecticides in South Africa. Med Vet Entomol 14: 181-189.
72. Sharp BL, Ridl FC, Govender D, Kuklinski J, Kleinschmidt I (2007) Malaria vector control by indoor residual insecticide spraying on the tropical island of Bioko, Equatorial Guinea. Malar J 6: 52.
73. Gamage-Mendis AC, Carter R, Mendis C, De Zoysa AP, Herath PR, et al. (1991) Clustering of malaria infections within an endemic population: risk of malaria associated with the type of housing construction. Am J Trop Med Hyg 45: 77-85.
74. Ghebreyesus TA, Haile M, Witten KH, Getachew A, Yohannes M, et al. (2000) Household risk factors for malaria among children in the Ethiopian highlands. Trans R Soc Trop Med Hyg 94: 17-21.
75. Deressa W, Ali A, Berhane Y (2007) Household and socioeconomic factors associated with childhood febrile illnesses and treatment seeking behaviour in an area of epidemic malaria in rural Ethiopia. Trans R Soc Trop Med Hyg 101: 939-947.
76. Saegerman C, Speybroeck N, Roels S, Vanopdenbosch E, Thiry E, et al. (2004) Decision support tools for clinical diagnosis of disease in cows with suspected bovine spongiform encephalopathy. J Clin Microbiol 42: 172-178.
77. Gaudart J, Poudiougou B, Ranque S, Doumbo O (2005) Oblique decision trees for spatial pattern detection: optimal algorithm and application to malaria risk. BMC Med Res Methodol 5: 22.
78. Bodker R, Akida J, Shayo D, Kisinza W, Msangeni HA, et al. (2003) Relationship between altitude and intensity of malaria transmission in the Usambara Mountains, Tanzania. J Med Entomol 40: 706-717.
79. Coosemans MH (1985) Comparaison de l'endémie malarienne dans une zone de riziculture et dans une zone de culture de coton dans la plaine de la Rusizi, Burundi. Ann Soc Belg Med Trop 65 Suppl 2: 187-200.
80. Protopopoff N, Van Herp M, Maes P, Reid T, Baza D, et al. (2007) Vector control in a malaria epidemic occurring within a complex emergency situation in Burundi: A case study. Malar J 6: 93.
81. Teklehaimanot HD, Lipsitch M, Teklehaimanot A, Schwartz J (2004) Weather-based prediction of Plasmodium falciparum malaria in epidemic-prone regions of Ethiopia I. Patterns of lagged weather effects reflect biological mechanisms. Malar J 3: 41.
82. Protopopoff N, Verhaeghen K, Van Bortel W, Roelants P, Marcotty T, et al. (2008) A significant increase in kdr in Anopheles gambiae is associated with an intensive vector control intervention in Burundi highlands. Trop Med Int Health 13: 1479-1487.
83. Seyoum A, Balcha F, Balkew M, Ali A, Gebre-Michael T (2002) Impact of cattle keeping on human biting rate of anopheline mosquitoes and malaria transmission around Ziway, Ethiopia. East Afr Med J 79: 485-490.
84. Rogers DJ, Randolph SE (2000) The global spread of malaria in a future, warmer world. Science 289: 1763-1766.
85. Thomas CJ, Davies G, Dunn CE (2004) Mixed picture for changes in stable malaria distribution with future climate in Africa. Trends Parasitol 20: 216-220.
86. Tanser FC, Sharp B, Le Sueur D (2003) Potential effect of climate change on malaria transmission in Africa. Lancet 362: 1792-1798.
87. Martens WJ, Niessen LW, Rotmans J, Jetten TH, McMichael AJ (1995) Potential impact of global climate change on malaria risk. Environ Health Perspect 103: 458-464.
88. Patz JA, Hulme M, Rosenzweig C, Mitchell TD, Goldberg RA, et al. (2002) Climate change: Regional warming and malaria resurgence. Nature 420: 627-628.
89. Hay SI, Cox J, Rogers DJ, Randolph SE, Stern DI, et al. (2002) Climate change and the resurgence of malaria in the East African highlands. Nature 415: 905-909.
90. Shanks GD, Hay SI, Stern DI, Biomndo K, Snow RW (2002) Meteorologic influences on Plasmodium falciparum malaria in the Highland Tea Estates of Kericho, Western Kenya. Emerg Infect Dis 8: 1404-1408.
91. Small J, Goetz SJ, Hay SI (2003) Climatic suitability for malaria transmission in Africa, 1911-1995. Proc Natl Acad Sci U S A 100: 15341-15345.
92. Bonora S, De Rosa FG, Boffito M, Di Perri G, Rossati A (2001) Rising temperature and the malaria epidemic in Burundi. Trends Parasitol 17: 572-573.
93. Gomez-Elipe A, Otero A, Van Herp M, Aguirre-Jaime A (2007) Forecasting malaria incidence based on monthly case reports and environmental factors in Karuzi, Burundi, 1997-2003. Malar J 6: 129.
94. Lindblade KA, Walker ED, Wilson ML (2000) Early warning of malaria epidemics in African highlands using Anopheles (Diptera: Culicidae) indoor resting density. J Med Entomol 37: 664-674.
95. Abeku TA (2007) Response to malaria epidemics in Africa. Emerg Infect Dis 13: 681-686.
96. Shiff C (2002) Integrated approach to malaria control. Clin Microbiol Rev 15: 278-293.
97. Walker K, Lynch M (2007) Contributions of Anopheles larval control to malaria suppression in tropical Africa: review of achievements and potential. Med Vet Entomol 21: 2-21.
98. Ault SK (1994) Environmental management: a re-emerging vector control strategy. Am J Trop Med Hyg 50: 35-49.
99. Killeen GF, Seyoum A, Knols BG (2004) Rationalizing historical successes of malaria control in Africa in terms of mosquito resource availability management. Am J Trop Med Hyg 71: 87-93.
100. Zhou G, Munga S, Minakawa N, Githeko AK, Yan G (2007) Spatial relationship between adult malaria vector abundance and environmental factors in Western Kenya highlands. Am J Trop Med Hyg 77: 29-35.