Author:
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Reference Manager
BibTeX
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EndNote
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1.
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Maitland K, Marsh K, 2004. Pathophysiology of severe malaria in children. Acta Trop 90: 131–140.
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11.
Mbogo CN, Kabiru EW, Glass GE, Forster D, Snow RW, Khamala CP, Ouma JH, Githure JI, Marsh K, Beier JC, 1999. Vector-related case-control study of severe malaria in Kilifi District, Kenya. Am J Trop Med Hyg 60: 781–785.
-
12.
Snow RW, Peshu N, Forster D, Bomu G, Mitsanze E, Ngumbao E, Chisengwa R, Schellenberg JR, Hayes RJ, Newbold CI, Marsh K, 1998. Environmental and entomological risk factors for the development of clinical malaria among children on the Kenyan coast. Trans R Soc Trop Med Hyg 92: 381–385.
-
13.
Ong'echa JM, Keller CC, Were T, Ouma C, Otieno RO, Landis-Lewis Z, Ochiel D, Slingluff JL, Mogere S, Ogonji GA, Orago AS, Vulule JM, Kaplan SS, Day RD, Perkins DJ, 2006. Parasitemia, anemia, and malarial anemia in infants and young children in a rural holoendemic Plasmodium falciparum transmission area. Am J Trop Med Hyg 74: 376–385.
-
14.
Luckner D, Lell B, Greve B, Lehman LG, Schmidt-Ott RJ, Matousek P, Herbich K, Schmid D, Mba R, Kremsner PG, 1998. No influence of socioeconomic factors on severe malarial anaemia, hyperparasitaemia or reinfection. Trans R Soc Trop Med Hyg 92: 478–481.
-
15.
Carme B, Plassart H, Senga P, Nzingoula S, 1994. Cerebral malaria in African children: socioeconomic risk factors in Brazzaville, Congo. Am J Trop Med Hyg 50: 131–136.
-
16.
Kahigwa E, Schellenberg D, Sanz S, Aponte JJ, Wigayi J, Mshinda H, Alonso P, Menendez C, 2002. Risk factors for presentation to hospital with severe anaemia in Tanzanian children: a case-control study. Trop Med Int Health 7: 823–830.
-
17.
D'Alessandro U, Olaleye BO, McGuire W, Langerock P, Bennett S, Aikins MK, Thomson MC, Cham MK, Cham BA, Greenwood BM, 1995. Mortality and morbidity from malaria in Gambian children after introduction of an impregnated bednet programme. Lancet 345: 479–483.
-
18.
Nevill CG, Some ES, Mung'ala VO, Mutemi W, New L, Marsh K, Lengeler C, Snow RW, 1996. Insecticide-treated bednets reduce mortality and severe morbidity from malaria among children on the Kenyan coast. Trop Med Int Health 1: 139–146.
-
19.
Holtz TH, Marum LH, Mkandala C, Chizani N, Roberts JM, Macheso A, Parise ME, Kachur SP, 2002. Insecticide-treated bednet use, anaemia, and malaria parasitaemia in Blantyre District, Malawi. Trop Med Int Health 7: 220–230.
-
20.
ter Kuile FO, Terlouw DJ, Kariuki SK, Phillips-Howard PA, Mirel LB, Hawley WA, Friedman JF, Shi YP, Kolczak MS, Lal AA, Vulule JM, Nahlen BL, 2003. Impact of permethrin-treated bed nets on malaria, anemia, and growth in infants in an area of intense perennial malaria transmission in western Kenya. Am J Trop Med Hyg 68: 68–77.
-
21.
Mathanga DP, Campbell CH, Taylor TE, Barlow R, Wilson ML, 2005. Reduction of childhood malaria by social marketing of insecticide-treated nets: a case-control study of effectiveness in Malawi. Am J Trop Med Hyg 73: 622–625.
-
22.
UNFPA, 2008. World Urbanization Prospects: The 2007 Revision. United Nations Population Division. Available at: http://esa.un.org/unup/.
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Trape JF, Lefebvre-Zante E, Legros F, Ndiaye G, Bouganali H, Druilhe P, Salem G, 1992. Vector density gradients and the epidemiology of urban malaria in Dakar, Senegal. Am J Trop Med Hyg 47: 181–189.
-
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Afolabi BM, Salako LA, Mafe AG, Ovwigho UB, Rabiu KA, Sanyaolu NO, Ibrahim MM, 2001. Malaria in the first 6 months of life in urban African infants with anemia. Am J Trop Med Hyg 65: 822–827.
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Modiano D, Sirima BS, Sawadogo A, Sanou I, Pare J, Konate A, Pagnoni F, 1998. Severe malaria in Burkina Faso: influence of age and transmission level on clinical presentation. Am J Trop Med Hyg 59: 539–542.
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Trape JF, 1997. Which strategy for malaria control in Africa? Parasitol Today 13: 125–126.
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27.
Gay-Andrieu F, Adehossi E, Lacroix V, Gagara M, Ibrahim ML, Kourna H, Boureima H, 2005. Epidemiological, clinical and biological features of malaria among children in Niamey, Niger. Malar J 4: 10.
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Klinkenberg E, McCall PJ, Wilson MD, Akoto AO, Amerasinghe FP, Bates I, Verhoeff FH, Barnish G, Donnelly MJ, 2006. Urban malaria and anaemia in children: a cross-sectional survey in two cities of Ghana. Trop Med Int Health 11: 578–588.
-
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Nieto T, Mendez F, Carrasquilla G, 1999. Knowledge, beliefs and practices relevant for malaria control in an endemic urban area of the Colombian Pacific. Soc Sci Med 49: 601–609.
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Snow RW, Peshu N, Forster D, Mwenesi H, Marsh K, 1992. The role of shops in the treatment and prevention of childhood malaria on the coast of Kenya. Trans R Soc Trop Med Hyg 86: 237–239.
-
31.
Molyneux CS, Mung'ala-Odera V, Harpham T, Snow RW, 1999. Maternal responses to childhood fevers: a comparison of rural and urban residents in coastal Kenya. Trop Med Int Health 4: 836–845.
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Significance of Travel to Rural Areas as a Risk Factor for Malarial Anemia in an Urban Setting
Jose G. Siri
Jose G. Siri
Department of Epidemiology, and Department of Bioststistics, School of Public Health, University of Michigan, Ann Arbor, Michigan; Division of Parasitic Diseases, National Center for Zoonotic, Vector-Borne and Enteric Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia; Centre for Vector Biology and Control Research, Kenya Medical Research Institute, Kisumu, Kenya
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Mark L. Wilson
Mark L. Wilson
Department of Epidemiology, and Department of Bioststistics, School of Public Health, University of Michigan, Ann Arbor, Michigan; Division of Parasitic Diseases, National Center for Zoonotic, Vector-Borne and Enteric Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia; Centre for Vector Biology and Control Research, Kenya Medical Research Institute, Kisumu, Kenya
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Susan Murray
Susan Murray
Department of Epidemiology, and Department of Bioststistics, School of Public Health, University of Michigan, Ann Arbor, Michigan; Division of Parasitic Diseases, National Center for Zoonotic, Vector-Borne and Enteric Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia; Centre for Vector Biology and Control Research, Kenya Medical Research Institute, Kisumu, Kenya
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Daniel H. Rosen
Daniel H. Rosen
Department of Epidemiology, and Department of Bioststistics, School of Public Health, University of Michigan, Ann Arbor, Michigan; Division of Parasitic Diseases, National Center for Zoonotic, Vector-Borne and Enteric Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia; Centre for Vector Biology and Control Research, Kenya Medical Research Institute, Kisumu, Kenya
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John M. Vulule
John M. Vulule
Department of Epidemiology, and Department of Bioststistics, School of Public Health, University of Michigan, Ann Arbor, Michigan; Division of Parasitic Diseases, National Center for Zoonotic, Vector-Borne and Enteric Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia; Centre for Vector Biology and Control Research, Kenya Medical Research Institute, Kisumu, Kenya
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Laurence Slutsker
Laurence Slutsker
Department of Epidemiology, and Department of Bioststistics, School of Public Health, University of Michigan, Ann Arbor, Michigan; Division of Parasitic Diseases, National Center for Zoonotic, Vector-Borne and Enteric Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia; Centre for Vector Biology and Control Research, Kenya Medical Research Institute, Kisumu, Kenya
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Kim A. Lindblade
Kim A. Lindblade
Department of Epidemiology, and Department of Bioststistics, School of Public Health, University of Michigan, Ann Arbor, Michigan; Division of Parasitic Diseases, National Center for Zoonotic, Vector-Borne and Enteric Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia; Centre for Vector Biology and Control Research, Kenya Medical Research Institute, Kisumu, Kenya
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The epidemiology of malaria in urban environments is poorly characterized, yet increasingly problematic. We conducted an unmatched case–control study of risk factors for malarial anemia with high parasitemia in urban Kisumu, Kenya, from June 2002 through February 2003. Cases (n = 80) were hospital patients with a hemoglobin level ≤ 8 g/dL and a Plasmodium parasite density ≥ 10,000/μL. Controls (n = 826) were healthy respondents to a concurrent citywide knowledge, attitude, and practice survey. Children who reported spending at least one night per month in a rural area were especially at risk (35% of cases; odds ratio = 9.3, 95% confidence interval [CI] = 4.4–19.7, P < 0.0001), and use of mosquito coils, bed net ownership, and house construction were non-significant, potentially indicating that malaria exposure during rural travel comprises an important element of risk. Control of severe malaria in an urban setting may be complicated by Plasmodium infections acquired elsewhere. Epidemiologic studies of urban malaria in low transmission settings should take travel history into account.
Author Notes
Financial support: This research was supported by CDC/KEMRI and by the University of Michigan through the Rackham Graduate School, the Center for Research on Ethnicity, Culture and Health, and the Global Health Program.
Disclaimer: This manuscript was published with the approval of the Director of the Kenya Medical Research Institute. The findings and conclusions in this report are those of the author(s) and do not necessarily represent the views of the Centers for Disease Control and Prevention.
Authors' addresses: Jose G. Siri, Health and Global Change Project, International Institute for Systems Analysis, Laxenburg, Austria. Mark L. Wilson, Department of Epidemiology, School of Public Health, University of Michigan, Ann Arbor, MI. Susan Murray, Department of Biostatistics, School of Public Health, University of Michigan, Ann Arbor, MI. Daniel H. Rosen and Laurence Slutsker, Division of Parasitic Diseases, National Center for Zoonotic, Vector-Borne and Enteric Diseases, Centers for Disease Control and Prevention, Atlanta, GA. John M. Vulule, Centre for Vector Biology and Control Research, Kenya Medical Research Institute, Kisumu, Kenya. Kim A. Lindblade, Centers for Diseases Control and Prevention Regional Office for Central America and Panama, Unit 3190, DPO AA.
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EndNote
-
1.
Snow RW, Guerra CA, Noor AM, Myint HY, Hay SI, 2005. The global distribution of clinical episodes of Plasmodium falciparum malaria. Nature 434: 214–217.
-
2.
Murphy SC, Breman JG, 2001. Gaps in the childhood malaria burden in Africa: cerebral malaria, neurological sequelae, anemia, respiratory distress, hypoglycemia, and complications of pregnancy. Am J Trop Med Hyg 64: 57–67.
-
3.
Maitland K, Marsh K, 2004. Pathophysiology of severe malaria in children. Acta Trop 90: 131–140.
-
4.
Clark IA, Cowden WB, 2003. The pathophysiology of falciparum malaria. Pharmacol Ther 99: 221–260.
-
5.
Mackintosh CL, Beeson JG, Marsh K, 2004. Clinical features and pathogenesis of severe malaria. Trends Parasitol 20: 597–603.
-
6.
Marsh K, Snow RW, 1999. Malaria transmission and morbidity. Parassitologia 41: 241–246.
-
7.
Greenwood BM, 1997. The epidemiology of malaria. Ann Trop Med Parasitol 91: 763–769.
-
8.
Reyburn H, Mbatia R, Drakeley C, Bruce J, Carneiro I, Olomi R, Cox J, Nkya WM, Lemnge M, Greenwood BM, Riley EM, 2005. Association of transmission intensity and age with clinical manifestations and case fatality of severe Plasmodium falciparum malaria. JAMA 293: 1461–1470.
-
9.
Snow RW, Omumbo JA, Lowe B, Molyneux CS, Obiero JO, Palmer A, Weber MW, Pinder M, Nahlen B, Obonyo C, Newbold C, Gupta S, Marsh K, 1997. Relation between severe malaria morbidity in children and level of Plasmodium falciparum transmission in Africa. Lancet 349: 1650–1654.
-
10.
Koram KA, Bennett S, Adiamah JH, Greenwood BM, 1995. Socio-economic determinants are not major risk factors for severe malaria in Gambian children. Trans R Soc Trop Med Hyg 89: 151–154.
-
11.
Mbogo CN, Kabiru EW, Glass GE, Forster D, Snow RW, Khamala CP, Ouma JH, Githure JI, Marsh K, Beier JC, 1999. Vector-related case-control study of severe malaria in Kilifi District, Kenya. Am J Trop Med Hyg 60: 781–785.
-
12.
Snow RW, Peshu N, Forster D, Bomu G, Mitsanze E, Ngumbao E, Chisengwa R, Schellenberg JR, Hayes RJ, Newbold CI, Marsh K, 1998. Environmental and entomological risk factors for the development of clinical malaria among children on the Kenyan coast. Trans R Soc Trop Med Hyg 92: 381–385.
-
13.
Ong'echa JM, Keller CC, Were T, Ouma C, Otieno RO, Landis-Lewis Z, Ochiel D, Slingluff JL, Mogere S, Ogonji GA, Orago AS, Vulule JM, Kaplan SS, Day RD, Perkins DJ, 2006. Parasitemia, anemia, and malarial anemia in infants and young children in a rural holoendemic Plasmodium falciparum transmission area. Am J Trop Med Hyg 74: 376–385.
-
14.
Luckner D, Lell B, Greve B, Lehman LG, Schmidt-Ott RJ, Matousek P, Herbich K, Schmid D, Mba R, Kremsner PG, 1998. No influence of socioeconomic factors on severe malarial anaemia, hyperparasitaemia or reinfection. Trans R Soc Trop Med Hyg 92: 478–481.
-
15.
Carme B, Plassart H, Senga P, Nzingoula S, 1994. Cerebral malaria in African children: socioeconomic risk factors in Brazzaville, Congo. Am J Trop Med Hyg 50: 131–136.
-
16.
Kahigwa E, Schellenberg D, Sanz S, Aponte JJ, Wigayi J, Mshinda H, Alonso P, Menendez C, 2002. Risk factors for presentation to hospital with severe anaemia in Tanzanian children: a case-control study. Trop Med Int Health 7: 823–830.
-
17.
D'Alessandro U, Olaleye BO, McGuire W, Langerock P, Bennett S, Aikins MK, Thomson MC, Cham MK, Cham BA, Greenwood BM, 1995. Mortality and morbidity from malaria in Gambian children after introduction of an impregnated bednet programme. Lancet 345: 479–483.
-
18.
Nevill CG, Some ES, Mung'ala VO, Mutemi W, New L, Marsh K, Lengeler C, Snow RW, 1996. Insecticide-treated bednets reduce mortality and severe morbidity from malaria among children on the Kenyan coast. Trop Med Int Health 1: 139–146.
-
19.
Holtz TH, Marum LH, Mkandala C, Chizani N, Roberts JM, Macheso A, Parise ME, Kachur SP, 2002. Insecticide-treated bednet use, anaemia, and malaria parasitaemia in Blantyre District, Malawi. Trop Med Int Health 7: 220–230.
-
20.
ter Kuile FO, Terlouw DJ, Kariuki SK, Phillips-Howard PA, Mirel LB, Hawley WA, Friedman JF, Shi YP, Kolczak MS, Lal AA, Vulule JM, Nahlen BL, 2003. Impact of permethrin-treated bed nets on malaria, anemia, and growth in infants in an area of intense perennial malaria transmission in western Kenya. Am J Trop Med Hyg 68: 68–77.
-
21.
Mathanga DP, Campbell CH, Taylor TE, Barlow R, Wilson ML, 2005. Reduction of childhood malaria by social marketing of insecticide-treated nets: a case-control study of effectiveness in Malawi. Am J Trop Med Hyg 73: 622–625.
-
22.
UNFPA, 2008. World Urbanization Prospects: The 2007 Revision. United Nations Population Division. Available at: http://esa.un.org/unup/.
-
23.
Trape JF, Lefebvre-Zante E, Legros F, Ndiaye G, Bouganali H, Druilhe P, Salem G, 1992. Vector density gradients and the epidemiology of urban malaria in Dakar, Senegal. Am J Trop Med Hyg 47: 181–189.
-
24.
Afolabi BM, Salako LA, Mafe AG, Ovwigho UB, Rabiu KA, Sanyaolu NO, Ibrahim MM, 2001. Malaria in the first 6 months of life in urban African infants with anemia. Am J Trop Med Hyg 65: 822–827.
-
25.
Modiano D, Sirima BS, Sawadogo A, Sanou I, Pare J, Konate A, Pagnoni F, 1998. Severe malaria in Burkina Faso: influence of age and transmission level on clinical presentation. Am J Trop Med Hyg 59: 539–542.
-
26.
Trape JF, 1997. Which strategy for malaria control in Africa? Parasitol Today 13: 125–126.
-
27.
Gay-Andrieu F, Adehossi E, Lacroix V, Gagara M, Ibrahim ML, Kourna H, Boureima H, 2005. Epidemiological, clinical and biological features of malaria among children in Niamey, Niger. Malar J 4: 10.
-
28.
Klinkenberg E, McCall PJ, Wilson MD, Akoto AO, Amerasinghe FP, Bates I, Verhoeff FH, Barnish G, Donnelly MJ, 2006. Urban malaria and anaemia in children: a cross-sectional survey in two cities of Ghana. Trop Med Int Health 11: 578–588.
-
29.
Nieto T, Mendez F, Carrasquilla G, 1999. Knowledge, beliefs and practices relevant for malaria control in an endemic urban area of the Colombian Pacific. Soc Sci Med 49: 601–609.
-
30.
Snow RW, Peshu N, Forster D, Mwenesi H, Marsh K, 1992. The role of shops in the treatment and prevention of childhood malaria on the coast of Kenya. Trans R Soc Trop Med Hyg 86: 237–239.
-
31.
Molyneux CS, Mung'ala-Odera V, Harpham T, Snow RW, 1999. Maternal responses to childhood fevers: a comparison of rural and urban residents in coastal Kenya. Trop Med Int Health 4: 836–845.
-
32.
Olano V, Carrasquilla G, Mendez F, 1997. Transmission of urban malaria in Buenaventrua, Colombia: entomological features [in Spanish]. Rev Panam Salud Publica 1: 287–294.
-
33.
El Sayed BB, Arnot DE, Mukhtar MM, Baraka OZ, Dafalla AA, Elnaiem DE, Nugud AH, 2000. A study of the urban malaria transmission problem in Khartoum. Acta Trop 75: 163–171.
-
34.
Thompson R, Begtrup K, Cuamba N, Dgedge M, Mendis C, Gamage-Mendis A, Enosse SM, Barreto J, Sinden RE, Hogh B, 1997. The Matola malaria project: a temporal and spatial study of malaria transmission and disease in a suburban area of Maputo, Mozambique. Am J Trop Med Hyg 57: 550–559.
-
35.
Ronald LA, Kenny SL, Klinkenberg E, Akoto AO, Boakye I, Barnish G, Donnelly MJ, 2006. Malaria and anaemia among children in two communities of Kumasi, Ghana: a cross-sectional survey. Malar J 5: 105.
-
36.
Central Bureau of Statistics, Ministry of Finance and Planning, 2000. 1999 Population and Housing Census, Volume I. Nairobi: Kenya.
-
37.
Githeko AK, Service MW, Mbogo CM, Atieli FK, Juma FO, 1993. Plasmodium falciparum sporozoite and entomological inoculation rates at the Ahero rice irrigation scheme and the Miwani sugar-belt in western Kenya. Ann Trop Med Parasitol 87: 379–391.
-
38.
Beier JC, Perkins PV, Onyango FK, Gargan TP, Oster CN, Whitmire RE, Koech DK, Roberts CR, 1990. Characterization of malaria transmission by Anopheles (Diptera: Culicidae) in western Kenya in preparation for malaria vaccine trials. J Med Entomol 27: 570–577.
-
39.
Siri JG, Lindblade KA, Rosen DH, Onyango B, Vulule J, Slutsker L, Wilson ML, 2008. Quantitative urban classification for malaria epidemiology in sub-Saharan Africa. Malar J 7: 34.
-
40.
Siri JG, Lindblade KA, Rosen DH, Onyango B, Vulule JM, Slutsker L, Wilson ML, 2008. A census-weighted, spatially-stratified household sampling strategy for urban malaria epidemiology. Malar J 7: 39.
-
41.
Alonso PL, Smith T, Schellenberg JR, Masanja H, Mwankusye S, Urassa H, Bastos de Azevedo I, Chongela J, Kobero S, Menendez C, 1994. Randomised trial of efficacy of SPf66 vaccine against Plasmodium falciparum malaria in children in southern Tanzania. Lancet 344: 1175–1181.
-
42.
Filmer D, Pritchett LH, 2001. Estimating wealth effects without expenditure data–or tears: an application to educational enrollments in states of India. Demography 38: 115–132.
-
43.
Eisele TP, Keating J, Swalm C, Mbogo CM, Githeko AK, Regens JL, Githure JI, Andrews L, Beier JC, 2003. Linking field-based ecological data with remotely sensed data using a geographic information system in two malaria endemic urban areas of Kenya. Malar J 2: 44.
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