1921
Volume 91, Issue 1
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645

Abstract

Abstract.

Although malnutrition and malaria co-occur among individuals and populations globally, effects of nutritional status on risk for parasitemia and clinical illness remain poorly understood. We investigated associations between infection, nutrition, and food security in a cross-sectional survey of 365 Batwa pygmies in Kanungu District, Uganda in January of 2013. We identified 4.1% parasite prevalence among individuals over 5 years old. Severe food insecurity was associated with increased risk for positive rapid immunochromatographic test outcome (adjusted relative risk [ARR] = 13.09; 95% confidence interval [95% CI] = 2.23–76.79). High age/sex-adjusted mid-upper arm circumference was associated with decreased risk for positive test among individuals who were not severely food-insecure (ARR = 0.37; 95% CI = 0.19–0.69). Within Batwa pygmy communities, where malnutrition and food insecurity are common, individuals who are particularly undernourished or severely food-insecure may have elevated risk for parasitemia. This finding may motivate integrated control of malaria and malnutrition in low-transmission settings.

[open-access] This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Loading

Article metrics loading...

/content/journals/10.4269/ajtmh.13-0422
2014-07-02
2017-09-25
Loading full text...

Full text loading...

/deliver/fulltext/14761645/91/1/39.html?itemId=/content/journals/10.4269/ajtmh.13-0422&mimeType=html&fmt=ahah

References

  1. Shankar AH, , 2008. Malaria and nutrition. Nutrition and Health in Developing Countries. Totowa, NJ: Springer, 229274.[Crossref]
  2. Crawley J, , 2004. Reducing the burden of anemia in infants and young children in malaria-endemic countries of Africa: from evidence to action. Am J Trop Med Hyg 71: 2534.
  3. Shankar AH, , 2000. Nutritional modulation of malaria morbidity and mortality. J Infect Dis 182: S37S53.[Crossref]
  4. Oppenheimer SJ, , 2001. Iron and its relation to immunity and infectious disease. J Nutr 131: 616S635S.
  5. Paaijmans KP, Blanford S, Bell AS, Blanford JI, Read AF, Thomas MB, , 2010. Influence of climate on malaria transmission depends on daily temperature variation. Proc Natl Acad Sci USA 107: 1513515139.[Crossref]
  6. Lindsay S, Martens W, , 1998. Malaria in the African highlands: past, present and future. Bull World Health Organ 76: 33.
  7. Pascual M, Ahumada J, Chaves L, Rodo X, Bouma M, , 2006. Malaria resurgence in the East African highlands: temperature trends revisited. Proc Natl Acad Sci USA 103: 58295834.[Crossref]
  8. Small J, Goetz SJ, Hay SI, , 2003. Climatic suitability for malaria transmission in Africa, 1911–1995. Proc Natl Acad Sci USA 100: 1534115345.[Crossref]
  9. Graves PM, Osgood DE, Thomson MC, Sereke K, Araia A, Zerom M, Ceccato P, Bell M, Del Corral J, Ghebreselassie S, Brantly EP, Ghebremeskel T, , 2008. Effectiveness of malaria control during changing climate conditions in Eritrea, 1998–2003. Trop Med Int Health 13: 218228.[Crossref]
  10. Hay SI, Cox J, Rogers DJ, Randolph SE, Stern DI, Shanks GD, Myers MF, Snow RW, , 2002. Climate change and the resurgence of malaria in the East African highlands. Nature 415: 905909.[Crossref]
  11. Van Lieshout M, Kovats R, Livermore M, Martens P, , 2004. Climate change and malaria: analysis of the SRES climate and socio-economic scenarios. Glob Environ Change 14: 8799.[Crossref]
  12. 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: 263274.[Crossref]
  13. Doolan DL, Dobano C, Baird JK, , 2009. Acquired immunity to malaria. Clin Microbiol Rev 22: 1336.[Crossref]
  14. Drakeley C, Corran P, Coleman P, Tongren J, McDonald S, Carneiro I, Malima R, Lusingu J, Manjurano A, Nkya W, , 2005. Estimating medium-and long-term trends in malaria transmission by using serological markers of malaria exposure. Proc Natl Acad Sci USA 102: 51085113.[Crossref]
  15. Langhorne J, Ndungu FM, Sponaas A-M, Marsh K, , 2008. Immunity to malaria: more questions than answers. Nat Immunol 9: 725732.[Crossref]
  16. Valle D, Clark JS, Zhao K, , 2011. Enhanced understanding of infectious diseases by fusing multiple datasets: a case study on malaria in the Western Brazilian Amazon region. PLoS ONE 6: e27462.[Crossref]
  17. Katsuragawa TH, Gil LHS, Tada MS, Silva Ad A, Costa JDAN, da Silva Araújo M, Escobar AL, da Silva LHP, , 2010. The dynamics of transmission and spatial distribution of malaria in riverside areas of Porto Velho, Rondônia, in the Amazon region of Brazil. PLoS ONE 5: e9245.[Crossref]
  18. Pates H, Curtis C, , 2005. Mosquito behavior and vector control. Annu Rev Entomol 50: 5370.[Crossref]
  19. Pérez-Escamilla R, Dessalines M, Finnigan M, Pachón H, Hromi-Fiedler A, Gupta N, , 2009. Household food insecurity is associated with childhood malaria in rural Haiti. J Nutr 139: 21322138.[Crossref]
  20. Tshikuka JG, Gray DK, Scott M, Olela KN, , 1997. Relationship of childhood protein—energy malnutrition and parasite infections in an urban African setting. Trop Med Int Health 2: 374382.[Crossref]
  21. El Samani FZ, Willett W, Ware J, , 1987. Nutritional and socio-demographic risk indicators of malaria in children under five: a cross-sectional study in a Sudanese rural community. J Trop Med Hyg 90: 6978.
  22. Berkley JA, Bejon P, Mwangi T, Gwer S, Maitland K, Williams TN, Mohammed S, Osier F, Kinyanjui S, Fegan G, , 2009. HIV infection, malnutrition, and invasive bacterial infection among children with severe malaria. Clin Infect Dis 49: 336343.[Crossref]
  23. Gera T, Sachdev H, , 2002. Effect of iron supplementation on incidence of infectious illness in children: systematic review. BMJ 325: 1142.[Crossref]
  24. Nyakeriga AM, Troye-Blomberg M, Dorfman JR, Alexander ND, Bäck R, Kortok M, Chemtai AK, Marsh K, Williams TN, , 2004. Iron deficiency and malaria among children living on the coast of Kenya. J Infect Dis 190: 439444.[Crossref]
  25. Jonker FA, Calis JC, van Hensbroek MB, Phiri K, Geskus RB, Brabin BJ, Leenstra T, , 2012. Iron status predicts malaria risk in malawian preschool children. PLoS ONE 7: e42670.[Crossref]
  26. Sazawal S, Black RE, Ramsan M, Chwaya HM, Stoltzfus RJ, Dutta A, Dhingra U, Kabole I, Deb S, Othman MK, , 2006. Effects of routine prophylactic supplementation with iron and folic acid on admission to hospital and mortality in preschool children in a high malaria transmission setting: community-based, randomised, placebo-controlled trial. Lancet 367: 133143.[Crossref]
  27. Kiszewski AE, Teklehaimanot A, , 2004. A review of the clinical and epidemiologic burdens of epidemic malaria. Am J Trop Med Hyg 71: 128135.
  28. Awah NW, Kaneko A, , 2012. Iron deficiency and severe Plasmodium falciparum malaria. Clin Infect Dis 54: 11451147.[Crossref]
  29. Gwamaka M, Kurtis JD, Sorensen BE, Holte S, Morrison R, Mutabingwa TK, Fried M, Duffy PE, , 2012. Iron deficiency protects against severe Plasmodium falciparum malaria and death in young children. Clin Infect Dis 54: 11371144.[Crossref]
  30. Roth DE, Black RE, Ojukwu JU, Okebe JU, Yahav D, Paul M, , 2010. Commentary on ‘Oral iron supplementation for preventing or treating anaemia among children in malaria-endemic areas’ with a response from the review authors. Evid Based Child Health 5: 11861188.[Crossref]
  31. Okebe JU, Yahav D, Shbita R, Paul M, , 2011. Oral iron supplements for children in malaria-endemic areas. Cochrane Database Syst Rev 10.
  32. Berger J, Dyck JL, Galan P, Aplogan A, Schneider D, Traissac P, Hercberg S, , 2000. Effect of daily iron supplementation on iron status, cell-mediated immunity, and incidence of infections in 6–36 month old Togolese children. Eur J Clin Nutr 54: 2935.[Crossref]
  33. Hunt JM, , 2005. The potential impact of reducing global malnutrition on poverty reduction and economic development. Asia Pac J Clin Nutr 14: 1038.
  34. Randolph T, Schelling E, Grace D, Nicholson CF, Leroy J, Cole D, Demment M, Omore A, Zinsstag J, Ruel M, , 2007. Invited review: role of livestock in human nutrition and health for poverty reduction in developing countries. J Anim Sci 85: 27882800.[Crossref]
  35. Atinmo T, Mirmiran P, Oyewole OE, Belahsen R, Serra‐Majem L, , 2009. Breaking the poverty/malnutrition cycle in Africa and the Middle East. Nutr Rev 67: S40S46.[Crossref]
  36. Sachs J, Malaney P, , 2002. The economic and social burden of malaria. Nature 415: 680685.[Crossref]
  37. Barrett CB, , 2010. Measuring food insecurity. Science 327: 825828.[Crossref]
  38. Thompson B, Cohen MJ, Meerman J, , 2012. World Food Insecurity and Malnutrition: Scope, Trends, Causes and Consequences. The Impact of Climate Change and Bioenergy on Nutrition. New York, NY: Springer, 2141.[Crossref]
  39. Pinstrup-Andersen P, , 2010. The African Food System and Its Interaction with Human Health and Nutrition. Ithaca, NY: Cornell University Press.
  40. Washington R, Downing TE, , 1999. Seasonal forecasting of African rainfall: prediction, responses and household food security. Geogr J 165: 255274.[Crossref]
  41. Battisti DS, Naylor RL, , 2009. Historical warnings of future food insecurity with unprecedented seasonal heat. Science 323: 240244.[Crossref]
  42. Nord M, Romig K, , 2006. Hunger in the summer: seasonal food insecurity and the National School Lunch and Summer Food Service programs. J Child Poverty 12: 141158.[Crossref]
  43. Maxwell DG, , 1996. Measuring food insecurity: the frequency and severity of “coping strategies.” Food Policy 21: 291303.[Crossref]
  44. Skalicky A, Meyers AF, Adams WG, Yang Z, Frank DA, , 2006. Child food insecurity and iron deficiency anemia in low-income infants and toddlers in the United States. Matern Child Health J 10: 177185.[Crossref]
  45. Tontisirin K, Nantel G, Bhattacharjee L, , 2002. Food-based strategies to meet the challenges of micronutrient malnutrition in the developing world. Proc Nutr Soc 61: 243250.[Crossref]
  46. Oldewage-Theron WH, Dicks EG, Napier CE, , 2006. Poverty, household food insecurity and nutrition: coping strategies in an informal settlement in the Vaal Triangle, South Africa. Public Health 120: 795804.[Crossref]
  47. Sorsdahl K, Slopen N, Siefert K, Seedat S, Stein DJ, Williams DR, , 2011. Household food insufficiency and mental health in South Africa. J Epidemiol Community Health 65: 426431.[Crossref]
  48. Hadley C, Tegegn A, Tessema F, Asefa M, Galea S, , 2008. Parental symptoms of common mental disorders and children's social, motor, and language development in sub-Saharan Africa. Ann Hum Biol 35: 259275.[Crossref]
  49. Weinreb L, Wehler C, Perloff J, Scott R, Hosmer D, Sagor L, Gundersen C, , 2002. Hunger: its impact on children's health and mental health. Pediatrics 110: e41.[Crossref]
  50. Borghetti P, Saleri R, Mocchegiani E, Corradi A, Martelli P, , 2009. Infection, immunity and the neuroendocrine response. Vet Immunol Immunopathol 130: 141162.[Crossref]
  51. McDade TW, , 2005. The ecologies of human immune function. Annu Rev Anthropol 34: 495521.[Crossref]
  52. Uscátegui Peñuela RM, Pérez Tamayo EM, Corrales Agudelo LV, Correa Botero A, Estrada Restrepo A, Carmona Fonseca J, , 2009. Relationship between malaria, malnutrition, food insecurity and low socio-economical conditions in children of Turbo, Colombia. Perspectivas en Nutrición Humana 11: 153164.
  53. Rodríguez JCP, Uribe GÁ, Araújo RM, Narváez PC, Valencia SH, , 2011. Epidemiology and control of malaria in Colombia. Mem Inst Oswaldo Cruz 106: 114122.[Crossref]
  54. Eisele TP, Keating J, Bennett A, Londono B, Johnson D, Lafontant C, Krogstad DJ, , 2007. Prevalence of Plasmodium falciparum infection in rainy season, Artibonite Valley, Haiti, 2006. Emerg Infect Dis 13: 1494.[Crossref]
  55. Hay SI, Noor AM, Simba M, Busolo M, Guyatt HL, Ochola SA, Snow RW, Hay S, Noor A, Simba M, , 2002. Clinical epidemiology of malaria in the highlands of western Kenya. Emerg Infect Dis 8: 543.[Crossref]
  56. Berrang-Ford L, Dingle K, Ford JD, Lee C, Lwasa S, Namanya DB, Henderson J, Llanos A, Carcamo C, Edge V, , 2012. Vulnerability of indigenous health to climate change: a case study of Uganda's Batwa Pygmies. Soc Sci Med 75: 10671077.[Crossref]
  57. Ford JD, Vanderbilt W, Berrang-Ford L, , 2012. Authorship in IPCC AR5 and its implications for content: climate change and Indigenous populations in WGII. Clim Change 113: 201213.[Crossref]
  58. Ford JD, , 2012. Indigenous health and climate change. Am J Public Health 102: 12601266.[Crossref]
  59. Pearce T, Ford JD, Caron A, Kudlak BP, , 2012. Climate change adaptation planning in remote, resource-dependent communities: an Arctic example. Reg Environ Change 12: 825837.[Crossref]
  60. Bukirwa H, Yau V, Kigozi R, Filler S, Quick L, Lugemwa M, Dissanayake G, Kamya M, Wabwire-Mangen F, Dorsey G, , 2009. Short report: assessing the impact of indoor residual spraying on malaria morbidity using a sentinel site surveillance system in western Uganda. Am J Trop Med Hyg 81: 611614.[Crossref]
  61. Yeka A, Gasasira A, Mpimbaza A, Achan J, Nankabirwa J, Nsobya S, Staedke SG, Donnelly MJ, Wabwire-Mangen F, Talisuna A, , 2012. Malaria in Uganda: challenges to control on the long road to elimination: I. Epidemiology and current control efforts. Acta Trop 121: 184195.[Crossref]
  62. Sherman M, Berrang-Ford L, Ford J, Lardeau M-P, Hofmeijer I, Cortijo CZ, , 2012. Balancing indigenous principles and institutional research guidelines for informed consent: a case study from the Peruvian Amazon. Am J Bioeth Primary Res 3: 5368.
  63. Pearce TD, Ford JD, Laidler GJ, Smit B, Duerden F, Allarut M, Andrachuk M, Baryluk S, Dialla A, Elee P, , 2009. Community collaboration and climate change research in the Canadian Arctic. Polar Res 28: 1027.[Crossref]
  64. Bwindi Community Hospital, 2013. Batwa and Byumba. Available at: http://www.bwindihospital.com. Accessed May 15, 2013.
  65. Bickel G, Nord M, Price C, Hamilton W, Cook J, , 2000. Guide to Measuring Household Food Security. Alexandria, VA: Department of Agriculture Food and Nutrition Service.
  66. Radimer KL, , 2002. Measurement of household food security in the USA and other industrialised countries. Public Health Nutr 5: 859864.[Crossref]
  67. Melgar-Quinonez HR, Nord M, Perez-Escamilla R, Segall-Correa AM, , 2007. Psychometric properties of a modified US-household food security survey module in Campinas, Brazil. Eur J Clin Nutr 62: 665673.[Crossref]
  68. Powell-Tuck J, Hennessy EM, , 2003. A comparison of mid upper arm circumference, body mass index and weight loss as indices of undernutrition in acutely hospitalized patients. Clin Nutr 22: 307312.[Crossref]
  69. Jenike MR, , 1995. Variation in body fat and muscle mass: responses to seasonal hunger among tropical horticulturists, Zaire. Ecol Food Nutr 34: 227249.[Crossref]
  70. De Souza RG, , 2006. Body size and growth: the significance of chronic malnutrition among the Casiguran Agta. Ann Hum Biol 33: 604619.[Crossref]
  71. Adhikari A, Sen A, Brumbaugh RC, Schwartz J, , 2011. Altered growth patterns of a mountain Ok population of Papua New Guinea over 25 years of change. Am J Hum Biol 23: 325332.[Crossref]
  72. Bisai S, Bose K, , 2009. Undernutrition in the Kora Mudi tribal population, West Bengal, India: a comparison of body mass index and mid-upper-arm circumference. Food Nutr Bull 30: 6367.[Crossref]
  73. Benefice E, Malina R, , 1996. Body size, body composition and motor performances of mild-to-moderately undernourished Senegalese children. Ann Hum Biol 23: 307321.[Crossref]
  74. Muthayya S, Kurpad AV, Duggan CP, Bosch RJ, Dwarkanath P, Mhaskar A, Mhaskar R, Thomas A, Vaz M, Bhat S, , 2006. Low maternal vitamin B12 status is associated with intrauterine growth retardation in urban South Indians. Eur J Clin Nutr 60: 791801.[Crossref]
  75. Gernaat HB, Dechering WH, Voorhoeve HW, , 1996. Absolute values or Z scores of mid-upper arm circumference to identify wasting? Evaluation in a community as well as a clinical sample of under fives from Nchelenge, Zambia. J Trop Pediatr 42: 2733.[Crossref]
  76. Rodrigues VC, Rao RS, Lena A, , 1994. Utility of arm circumference as a screening instrument to identify women at nutritional risk. Trop Doct 24: 164.[Crossref]
  77. Hakewill PA, Moren A, , 1991. Monitoring and evaluation of relief programmes. Trop Doct 21: 2428.[Crossref]
  78. Olukoya AA, , 1990. Identification of underweight women by measurement of the arm circumference. Int J Gynaecol Obstet 31: 231235.[Crossref]
  79. Collins S, , 1996. Using middle upper arm circumference to assess severe adult malnutrition during famine. JAMA 276: 391395.[Crossref]
  80. James WP, Mascie-Taylor GC, Norgan NG, Bistrian BR, Shetty PS, Ferro-Luzzi A, , 1994. The value of arm circumference measurements in assessing chronic energy deficiency in Third World adults. Eur J Clin Nutr 48: 883.
  81. Abeku TA, Kristan M, Jones C, Beard J, Mueller DH, Okia M, Rapuoda B, Greenwood B, Cox J, , 2008. Determinants of the accuracy of rapid diagnostic tests in malaria case management: evidence from low and moderate transmission settings in the East African highlands. Malar J 7: 202.[Crossref]
  82. Hopkins H, Bebell L, Kambale W, Dokomajilar C, Rosenthal PJ, Dorsey G, , 2008. Rapid diagnostic tests for malaria at sites of varying transmission intensity in Uganda. J Infect Dis 197: 510518.[Crossref]
  83. Nicastri E, Bevilacqua N, Schepisi MS, Paglia MG, Meschi S, Ame SM, Mohamed JA, Mangi S, Fumakule R, Di Caro A, , 2009. Accuracy of malaria diagnosis by microscopy, rapid diagnostic test, and PCR methods and evidence of antimalarial overprescription in non-severe febrile patients in two Tanzanian hospitals. Am J Trop Med Hyg 80: 712717.
  84. Bell DR, Wilson DW, Martin LB, , 2005. False-positive results of a Plasmodium falciparum histidine-rich protein 2-detecting malaria rapid diagnostic test due to high sensitivity in a community with fluctuating low parasite density. Am J Trop Med Hyg 73: 199203.
  85. Harris I, Sharrock WW, Bain LM, Gray K-A, Bobogare A, Boaz L, Lilley K, Krause D, Vallely A, Johnson M-L, , 2010. A large proportion of asymptomatic Plasmodium infections with low and sub-microscopic parasite densities in the low transmission setting of Temotu Province, Solomon Islands: challenges for malaria diagnostics in an elimination setting. Malar J 9: 29.[Crossref]
  86. Berk KN, , 1978. Comparing subset regression procedures. Technometrics 20: 16.[Crossref]
  87. Calcagno V, de Mazancourt C, , 2010. glmulti: an R package for easy automated model selection with (generalized) linear models. J Stat Softw 34: 29.[Crossref]
  88. Zeileis A, Hothorn T, Hornik K, , 2008. Model-based recursive partitioning. J Comput Graph Stat 17: 492514.
  89. Maas CJ, Hox JJ, , 2004. Robustness issues in multilevel regression analysis. Stat Neerl 58: 127137.[Crossref]
  90. Petersen MA, , 2009. Estimating standard errors in finance panel data sets: Comparing approaches. Rev Financ Stud 22: 435480.[Crossref]
  91. Hay SI, Smith DL, Snow RW, , 2008. Measuring malaria endemicity from intense to interrupted transmission. Lancet Infect Dis 8: 369378.[Crossref]
  92. Guyatt HL, Snow RW, , 2004. The management of fevers in Kenyan children and adults in an area of seasonal malaria transmission. Trans R Soc Trop Med Hyg 98: 111115.[Crossref]
  93. Filmer D, , 2005. Fever and its treatment among the more and less poor in sub-Saharan Africa. Health Policy Plan 20: 337346.[Crossref]
  94. Yekutiel P, , 1960. Problems of epidemiology in malaria eradication. Bull World Health Organ 22: 669.
  95. Ghesquiere J, Karvonen M, , 1981. Some anthropometric and functional dimensions of the pygmy (Kivu Twa). Ann Hum Biol 8: 119134.[Crossref]
  96. Pagezy H, , 1984. Seasonal hunger as experienced by the Oto and the Twa women of a Ntomba village in the equatorial forest (Lake Tumba, Zaire). Ecol Food Nutr 15: 1327.[Crossref]
  97. Mathers CD, Sadana R, Salomon JA, Murray CJ, Lopez AD, , 2001. Healthy life expectancy in 191 countries, 1999. Lancet 357: 16851691.[Crossref]
  98. Kikafunda JK, Walker AF, Collett D, Tumwine JK, , 1998. Risk factors for early childhood malnutrition in Uganda. Pediatrics 104: e45.[Crossref]
  99. Caicedo O, Villamor E, Forero Y, Ziade J, Perez P, Quinones F, Arevalo-Herrera M, Herrera S, , 2010. Relation between vitamin B12 and folate status, and hemoglobin concentration and parasitemia during acute malaria infections in Colombia. Acta Trop 114: 1721.[Crossref]
  100. Friedman JF, Kwena AM, Mirel LB, Kariuki SK, Terlouw DJ, Phillips-Howard PA, Hawley WA, Nahlen BL, Ping Shi Y, Ter Kuile FO, , 2005. Malaria and nutritional status among pre-school children: results from cross-sectional surveys in western Kenya. Am J Trop Med Hyg 73: 698704.
  101. Verret WJ, Arinaitwe E, Wanzira H, Bigira V, Kakuru A, Kamya M, Tappero JW, Sandison T, Dorsey G, , 2011. Effect of nutritional status on response to treatment with artemisinin-based combination therapy in young Ugandan children with malaria. Antimicrob Agents Chemother 55: 26292635.[Crossref]
  102. Davidenko O, Darcel N, Fromentin G, Tomé D, , 2013. Control of protein and energy intake—brain mechanisms. Eur J Clin Nutr 67: 455461.[Crossref]
  103. Steyn NP, Nel JH, Nantel G, Kennedy G, Labadarios D, , 2006. Food variety and dietary diversity scores in children: are they good indicators of dietary adequacy? Public Health Nutr 9: 644650.[Crossref]
  104. Schaible UE, Stefan HE, , 2007. Malnutrition and infection: complex mechanisms and global impacts. PLoS Med 4: e115.[Crossref]
  105. Garenne M, Willie D, Maire B, Fontaine O, Eeckels R, Briend A, van den Broeck J, , 2009. Incidence and duration of severe wasting in two African populations. Public Health Nutr 12: 19741982.[Crossref]
  106. Villamor E, Misegades L, Fataki MR, Mbise RL, Fawzi WW, , 2005. Child mortality in relation to HIV infection, nutritional status, and socio-economic background. Int J Epidemiol 34: 6168.[Crossref]
  107. Shafer LA, Biraro S, Nakiyingi-Miiro J, Kamali A, Ssematimba D, Ouma J, Ojwiya A, Hughes P, Van der Paal L, Whitworth J, Opio A, Grosskurth H, , 2008. HIV prevalence and incidence are no longer falling in southwest Uganda: evidence from a rural population cohort 1989–2005. AIDS 22: 16411649.[Crossref]
  108. Cook JT, Frank DA, Berkowitz C, Black MM, Casey PH, Cutts DB, Meyers AF, Zaldivar N, Skalicky A, Levenson S, Heeren T, Nord M, , 2004. Food insecurity is associated with adverse health outcomes among human infants and toddlers. J Nutr 134: 14321438.
  109. Stuff JE, Casey PH, Szeto KL, Gossett JM, Robbins JM, Simpson PM, Connell C, Bogle ML, , 2004. Household food insecurity is associated with adult health status. J Nutr 134: 23302335.
  110. World Health Organization, 2007. Conclusions and recommendations of the WHO Consultation on prevention and control of iron deficiency in infants and young children in malaria-endemic areas. Food Nutr Bull 28: S621S627.[Crossref]
  111. Mbugi EV, Meijerink M, Veenemans J, Jeurink PV, McCall M, Olomi RM, Shao JF, Verhoef H, Savelkoul HF, , 2010. Alterations in early cytokine-mediated immune responses to Plasmodium falciparum infection in Tanzanian children with mineral element deficiencies: a cross-sectional survey. Malar J 9: 130.[Crossref]
  112. Veenemans J, Milligan P, Prentice AM, Schouten LR, Inja N, van der Heijden AC, de Boer LC, Jansen EJ, Koopmans AE, Enthoven WT, , 2011. Effect of supplementation with zinc and other micronutrients on malaria in Tanzanian children: a randomised trial. PLoS Med 8: e1001125.[Crossref]
  113. Zeba AN, Sorgho H, Rouamba N, Zongo I, Rouamba J, Guiguemde RT, Hamer DH, Mokhtar N, Ouedraogo JB, , 2008. Major reduction of malaria morbidity with combined vitamin A and zinc supplementation in young children in Burkina Faso: a randomized double blind trial. Nutr J 7: 7.[Crossref]
  114. Richard SA, Zavaleta N, Caulfield LE, Black RE, Witzig RS, Shankar AH, , 2006. Zinc and iron supplementation and malaria, diarrhea, and respiratory infections in children in the Peruvian Amazon. Am J Trop Med Hyg 75: 126132.
  115. Shankar AH, Genton B, Baisor M, Paino J, Tamja S, Adiguma T, Wu L, Rare L, Bannon D, Tielsch JM, West KP, Alpers MP, , 2000. The influence of zinc supplementation on morbidity due to Plasmodium falciparum: a randomized trial in preschool children in Papua New Guinea. Am J Trop Med Hyg 62: 663669.
  116. Shankar AH, Genton B, Semba RD, Baisor M, Paino J, Tamja S, Adiguma T, Wu L, Rare L, Tielsch JM, Alpers MP, West KP, , 1999. Effect of vitamin A supplementation on morbidity due to Plasmodium falciparum in young children in Papua New Guinea: a randomised trial. Lancet 354: 203209.[Crossref]
  117. Cusick SE, Tielsch JM, Ramsan M, Jape JK, Sazawal S, Black RE, Stoltzfus RJ, , 2005. Short-term effects of vitamin A and antimalarial treatment on erythropoiesis in severely anemic Zanzibari preschool children. Am J Clin Nutr 82: 406412.
  118. Binka F, Ross D, Morris S, , 1995. Vitamin A supplementation and chilhood malaria in northern Ghana. Am J Clin Nutr 61: 853859.
  119. Reuben R, , 1993. Women and malaria—special risks and appropriate control strategy. Soc Sci Med 37: 473480.[Crossref]
  120. Guerra CA, Snow RW, Hay SI, , 2006. A global assessment of closed forests, deforestation and malaria risk. Ann Trop Med Parasitol 100: 189.[Crossref]
  121. Geissbühler Y, Chaki P, Emidi B, Govella NJ, Shirima R, Mayagaya V, Mtasiwa D, Mshinda H, Fillinger U, Lindsay SW, , 2007. Interdependence of domestic malaria prevention measures and mosquito-human interactions in urban Dar es Salaam, Tanzania. Malar J 6: 126.[Crossref]
  122. Stevenson J, Laurent BS, Lobo NF, Cooke MK, Kahindi SC, Oriango RM, Harbach RE, Cox J, Drakeley C, , 2012. Novel vectors of malaria parasite in the western highlands of Kenya. Emerg Infect Dis 18: 1547.[Crossref]
  123. White G, , 1973. Comparative studies on sibling species of Anopheles gambiae Giles complex (Dipt. Culicidae). III. The distribution, ecology, behaviour and vectorial importance of species D in Bwamba County, Uganda, with analysis of biological, ecological, morphological and cytogenetical relationships of Ugandan species D. Bull Entomol Res 63: 6597.[Crossref]
  124. Okumu FO, Moore SJ, Okumu F, Moore S, , 2011. Combining indoor residual spraying and insecticide-treated nets for malaria control in Africa: a review of possible outcomes and an outline of suggestions for the future. Malar J 10: 208.[Crossref]
  125. Perez-Escamilla R, Segall-Correa AM, Kurdian Maranha L, Sampaio Md M de F, Marin-Leon L, Panigassi G, , 2004. An adapted version of the U.S. Department of Agriculture Food Insecurity module is a valid tool for assessing household food insecurity in Campinas, Brazil. J Nutr 134: 19231928.
  126. Perez-Escamilla R, Segall-Correa AM, , 2008. Food security measurement and indicators. Rev Nutr 21: S15S26.[Crossref]
http://instance.metastore.ingenta.com/content/journals/10.4269/ajtmh.13-0422
Loading
/content/journals/10.4269/ajtmh.13-0422
Loading

Data & Media loading...

  • Received : 13 Jul 2013
  • Accepted : 24 Feb 2014

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error