1921
Volume 77, Issue 1
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645

Abstract

The highest prevalence of anemia exists in the developing world where its causes are multi-factorial. Anemia is responsible for significant morbidity and mortality, particularly in less developed countries (LDCs). Understanding causes of anemia and potential mechanisms are crucial to our ability to intervene to reduce this burden. In the past decade, our understanding of the etiology and mechanisms of anemia in LDCs has advanced significantly. This review will focus on recent advances in our understanding of the burden of anemia in specific sub-groups, the causes and mechanisms of anemia, and consequences of anemia for the human host.

Loading

Article metrics loading...

/content/journals/10.4269/ajtmh.2007.77.44
2007-07-01
2017-11-21
Loading full text...

Full text loading...

/deliver/fulltext/14761645/77/1/0770044.html?itemId=/content/journals/10.4269/ajtmh.2007.77.44&mimeType=html&fmt=ahah

References

  1. Yip R, Ramakrishnan U, 2002. Experiences and challenges in developing countries. J Nutr 132 : 827S–830S.
  2. Administrative Committee on Coordination/Standing Committee on Nutrition, ACC/SCN, 2000. Fourth Report on the World Nutrition Situation. New York: United Nations.
  3. Haas JD, Brownlie TT, 2001. Iron deficiency and reduced work capacity: a critical review of the research to determine a causal relationship. J Nutr 131 : 676S–688S.
  4. Sabbatini P, 2000. The relationship between anemia and quality of life in cancer patients. Oncologist 5 (Suppl 2): 19–23.
  5. Allen LH, 2000. Anemia and iron deficiency: effects on pregnancy outcome. Am J Clin Nutr 71 : 1280S–1284S.
  6. Stivelman JC, 2000. Benefits of anaemia treatment on cognitive function. Nephrol Dial Transplant 15 (Suppl 3): 29–35.
  7. Nelson M, 1996. Anaemia in adolescent girls: effects on cognitive function and activity. Proc Nutr Soc 55 : 359–367.
  8. World Health Organization, 2001. Iron Deficiency Anaemia: Assessment, Prevention and Control. Geneva: World Health Organization.
  9. Bruner AB, Joffe A, Duggan AK, Casella JF, Brandt J, 1996. Randomised study of cognitive effects of iron supplementation in non-anaemic iron-deficient adolescent girls. Lancet 348 : 992–996.
  10. Trowbridge F, Martorell R, 2002. Forging effective strategies to combat iron deficiency. Summary and recommendations. J Nutr 132 : 875S–879S.
  11. Levy JE, Jin O, Fujiwara Y, Kuo F, Andrews NC, 1999. Trans-ferrin receptor is necessary for development of erythrocytes and the nervous system. Nat Genet 21 : 396–399.
  12. Gambling L, Danzeisen R, Fosset C, Andersen HS, Dunford S, Srai SK, McArdle HJ, 2003. Iron and copper interactions in development and the effect on pregnancy outcome. J Nutr 133 : 1554S–1556S.
  13. Rao R, Georgieff MK, 2002. Perinatal aspects of iron metabolism. Acta Paediatr Suppl 91 : 124–129.
  14. Verhoeff FH, Brabin BJ, van Buuren S, Chimsuku L, Kazembe P, Wit JM, Broadhead RL, 2001. An analysis of intra-uterine growth retardation in rural Malawi. Eur J Clin Nutr 55 : 682–689.
  15. Allen LH, 2001. Biological mechanisms that might underlie iron’s effects on fetal growth and preterm birth. J Nutr 131 : 581S–589S.
  16. Rasmussen K, 2001. Is there a causal relationship between iron deficiency or iron-deficiency anemia and weight at birth, length of gestation and perinatal mortality? J Nutr 131 : 590S–601S.
  17. Cogswell ME, Parvanta I, Ickes L, Yip R, Brittenham GM, 2003. Iron supplementation during pregnancy, anemia, and birth weight: a randomized controlled trial. Am J Clin Nutr 78 : 773–781.
  18. Christian P, Khatry SK, Katz J, Pradhan EK, LeClerq SC, Shrestha SR, Adhikari RK, Sommer A, West KP Jr, 2003. Effects of alternative maternal micronutrient supplements on low birth weight in rural Nepal: double blind randomised community trial. BMJ 326 : 571.
  19. Rasmussen KM, Stoltzfus RJ, 2003. New evidence that iron supplementation during pregnancy improves birth weight: new scientific questions. Am J Clin Nutr 78 : 673–674.
  20. Tamura T, Picciano MF, 2006. Folate and human reproduction. Am J Clin Nutr 83 : 993–1016.
  21. Metz J, Zalusky R, Herbert V, 1968. Folic acid binding by serum and milk. Am J Clin Nutr 21 : 289–297.
  22. van den Broek NR, Letsky EA, 2000. Etiology of anemia in pregnancy in south Malawi. Am J Clin Nutr 72 : 247S–256S.
  23. Menendez C, Fleming AF, Alonso PL, 2000. Malaria-related anaemia. Parasitol Today 16 : 469–476.
  24. Fleming AF, 1989. Tropical obstetrics and gynaecology. 1. Anaemia in pregnancy in tropical Africa. Trans R Soc Trop Med Hyg 83 : 441–448.
  25. Fleming AF, Warrell DA, Dickmeiss H, 1974. Letter: Co-trimoxazole and the blood. Lancet 2 : 284–285.
  26. Weksler B, 1993. Hematology. Andreoli T, Bennett J, Carpentter C, Plum F, Smith L, eds. Cecil Essentials of Medicine. Philadelphia: W.B. Saunders Company, 351–416.
  27. Siekmann JH, Allen LH, Bwibo NO, Demment MW, Murphy SP, Neumann CG, 2003. Kenyan school children have multiple micronutrient deficiencies, but increased plasma vitamin B-12 is the only detectable micronutrient response to meat or milk supplementation. J Nutr 133 : 3972S–3980S.
  28. Allen LH, 2004. Folate and vitamin B12 status in the Americas. Nutr Rev 62 : S29–S33.
  29. Fishman SM, Christian P, West KP, 2000. The role of vitamins in the prevention and control of anaemia. Public Health Nutr 3 : 125–150.
  30. Wolbach S, Howe P, 1925. Tissue changes following deprivation of fat soluble A vitamin. J Exp Med 42 : 753–777.
  31. Findlay G, Mackenzie R, 1922. The bone marrow in deficiency diseases. J Pathol 25 : 402–403.
  32. Koessler KK, Maurer S, Loughlin R, 1926. The relation of anaemia, primary and secondary, to vitamin A deficiency. JAMA 87 : 476–482.
  33. Bloem MW, Wedel M, Egger RJ, Speek AJ, Schrijver J, Saowakontha S, Schreurs WH, 1989. Iron metabolism and vitamin A deficiency in children in northeast Thailand. Am J Clin Nutr 50 : 332–338.
  34. Olivares M, Walter T, Hertrampf E, Pizarro F, 1999. Anaemia and iron deficiency disease in children. Br Med Bull 55 : 534–543.
  35. Garcia-Casal MN, Layrisse M, Solano L, Baron MA, Arguello F, Llovera D, Ramirez J, Leets I, Tropper E, 1998. Vitamin A and beta-carotene can improve nonheme iron absorption from rice, wheat and corn by humans. J Nutr 128 : 646–650.
  36. Bloem MW, Wedel M, van Agtmaal EJ, Speek AJ, Saowakontha S, Schreurs WH, 1990. Vitamin A intervention: short-term effects of a single, oral, massive dose on iron metabolism. Am J Clin Nutr 51 : 76–79.
  37. Muhilal X, Permeisih D, Idjradinata YR, Muherdiyantiningsih X, Karyadi D, 1988. Vitamin A-fortified monosodium glutamate and health, growth, and survival of children: a controlled field trial. Am J Clin Nutr 48 : 1271–1276.
  38. Smith JC, Makdani D, Hegar A, Rao D, Douglass LW, 1999. Vitamin A and zinc supplementation of preschool children. J Am Coll Nutr 18 : 213–222.
  39. Mejia LA, Chew F, 1988. Hematological effect of supplementing anemic children with vitamin A alone and in combination with iron. Am J Clin Nutr 48 : 595–600.
  40. Suharno D, West CE, Muhilal, Karyadi D, Hautvast JG, 1993. Supplementation with vitamin A and iron for nutritional anaemia in pregnant women in West Java, Indonesia. Lancet 342 : 1325–1328.
  41. Panth M, Shatrugna V, Yasodhara P, Sivakumar B, 1990. Effect of vitamin A supplementation on haemoglobin and vitamin A levels during pregnancy. Br J Nutr 64 : 351–358.
  42. van den Broek NR, White SA, Flowers C, Cook JD, Letsky EA, Tanumihardjo SA, Mhango C, Molyneux M, Neilson JP, 2006. Randomised trial of vitamin A supplementation in pregnant women in rural Malawi found to be anaemic on screening by HemoCue. BJOG 113 : 569–576.
  43. Fawzi WW, Msamanga GI, Spiegelman D, Urassa EJ, McGrath N, Mwakagile D, Antelman G, Mbise R, Herrera G, Kapiga S, Willett W, Hunter DJ, 1998. Randomised trial of effects of vitamin supplements on pregnancy outcomes and T cell counts in HIV-1-infected women in Tanzania. Lancet 351 : 1477–1482.
  44. Sullivan PS, Hanson DL, Chu SY, Jones JL, Ward JW, 1998. Epidemiology of anemia in human immunodeficiency virus (HIV)-infected persons: results from the multistate adult and adolescent spectrum of HIV disease surveillance project. Blood 91 : 301–308.
  45. Mocroft A, Kirk O, Barton SE, Dietrich M, Proenca R, Colebunders R, Pradier C, dArminio Monforte A, Ledergerber B, Lundgren JD, 1999. Anaemia is an independent predictive marker for clinical prognosis in HIV-infected patients from across Europe. EuroSIDA study group. AIDS 13 : 943–950.
  46. Moore RD, Keruly JC, Chaisson RE, 1998. Anemia and survival in HIV infection. J Acquir Immune Defic Syndr Hum Retrovirol 19 : 29–33.
  47. O’Brien ME, Kupka R, Msamanga GI, Saathoff E, Hunter DJ, Fawzi WW, 2005. Anemia is an independent predictor of mortality and immunologic progression of disease among women with HIV in Tanzania. J Acquir Immune Defic Syndr 40 : 219– 225.
  48. Belperio PS, Rhew DC, 2004. Prevalence and outcomes of anemia in individuals with human immunodeficiency virus: a systematic review of the literature. Am J Med 116 (Suppl 7A): 27S–43S.
  49. Wilson IB, Cleary PD, 1996. Clinical predictors of functioning in persons with acquired immunodeficiency syndrome. Med Care 34 : 610–623.
  50. Revicki DA, Brown RE, Henry DH, McNeill MV, Rios A, Watson T, 1994. Recombinant human erythropoietin and health-related quality of life of AIDS patients with anemia. J Acquir Immune Defic Syndr 7 : 474–484.
  51. Henry DH, Beall GN, Benson CA, Carey J, Cone LA, Eron LJ, Fiala M, Fischl MA, Gabin SJ, Gottlieb MS, 1992. Recombinant human erythropoietin in the treatment of anemia associated with human immunodeficiency virus (HIV) infection and zidovudine therapy. Overview of four clinical trials. Ann Intern Med 117 : 739–748.
  52. Ganz T, 2002. The role of hepcidin in iron sequestration during infections and in the pathogenesis of anemia of chronic disease. Isr Med Assoc J 4 : 1043–1045.
  53. Ganz T, 2003. Hepcidin, a key regulator of iron metabolism and mediator of anemia of inflammation. Blood 102 : 783–788.
  54. Means RT Jr, 2000. The anaemia of infection. Baillieres Best Pract Res Clin Haematol 13 : 151–162.
  55. Totin D, Ndugwa C, Mmiro F, Perry RT, Jackson JB, Semba RD, 2002. Iron deficiency anemia is highly prevalent among human immunodeficiency virus-infected and uninfected infants in Uganda. J Nutr 132 : 423–429.
  56. Eley BS, Sive AA, Shuttleworth M, Hussey GD, 2002. A prospective, cross-sectional study of anaemia and peripheral iron status in antiretroviral naive, HIV-1 infected children in Cape Town, South Africa. BMC Infect Dis 2 : 3.
  57. Antelman G, Msamanga GI, Spiegelman D, Urassa EJ, Narh R, Hunter DJ, Fawzi WW, 2000. Nutritional factors and infectious disease contribute to anemia among pregnant women with human immunodeficiency virus in Tanzania. J Nutr 130 : 1950–1957.
  58. Meda N, Dao B, Ouangre A, 1998. HIV, maternal anemia and perinatal intervention using zidovudine. DITRAME Study Group (ANRS 049 Clinical Trial). Int J Gynaecol Obstet 61 : 65–66.
  59. Ramon R, Sawadogo D, Koko FS, Noba V, Likikouet R, Gourvellec G, Viho I, Mandelbrot L, Dabis F, Ekra CW, Msellati P, 1999. Haematological characteristics and HIV status of pregnant women in Abidjan, Côte d’Ivoire, 1995–96. Trans R Soc Trop Med Hyg 93 : 419–422.
  60. Patnaik P, Jere CS, Miller WC, Hoffman IF, Wirima J, Pendame R, Meshnick SR, Taylor TE, Molyneux ME, Kublin JG, 2005. Effects of HIV-1 serostatus, HIV-1 RNA concentration, and CD4 cell count on the incidence of malaria infection in a cohort of adults in rural Malawi. J Infect Dis 192 : 984–991.
  61. Cohen C, Karstaedt A, Frean J, Thomas J, Govender N, Prentice E, Dini L, Galpin J, Crewe-Brown H, 2005. Increased prevalence of severe malaria in HIV-infected adults in South Africa. Clin Infect Dis 41 : 1631–1637.
  62. Kamya MR, Gasasira AF, Yeka A, Bakyaita N, Nsobya SL, Francis D, Rosenthal PJ, Dorsey G, Havlir D, 2006. Effect of HIV-1 infection on antimalarial treatment outcomes in Uganda: a population-based study. J Infect Dis 193 : 9–15.
  63. de Silva NR, Brooker S, Hotez PJ, Montresor A, Engels D, Savioli L, 2003. Soil-transmitted helminth infections: updating the global picture. Trends Parasitol 19 : 547–551.
  64. Loukas A, Constant SL, Bethony JM, 2005. Immunobiology of hookworm infection. FEMS Immunol Med Microbiol 43 : 115–124.
  65. Albonico M, Stoltzfus RJ, Savioli L, Tielsch JM, Chwaya HM, Ercole E, Cancrini G, 1998. Epidemiological evidence for a differential effect of hookworm species, Ancylostoma duodenale or Necator americanus, on iron status of children. Int J Epidemiol 27 : 530–537.
  66. Steketee RW, 2003. Pregnancy, nutrition and parasitic diseases. J Nutr 133 : 1661S–1667S.
  67. Crompton DW, 2000. The public health importance of hookworm disease. Parasitology 121 (Suppl): S39–S50.
  68. Stephenson LS, 1994. Helminth parasites, a major factor in malnutrition. World Health Forum 15 : 169–172.
  69. Hotez PJ, Brooker S, Bethony JM, Bottazzi ME, Loukas A, Xiao S, 2004. Hookworm infection. N Engl J Med 351 : 799–807.
  70. Lozoff B, Jimenez E, Hagen J, Mollen E, Wolf AW, 2000. Poorer behavioral and developmental outcome more than 10 years after treatment for iron deficiency in infancy. Pediatrics 105 : E51.
  71. Dickson R, Awasthi S, Williamson P, Demellweek C, Garner P, 2000. Effects of treatment for intestinal helminth infection on growth and cognitive performance in children: systematic review of randomised trials. BMJ 320 : 1697–1701.
  72. Bhargava A, 2000. Treatment for intestinal helminth infection. Conclusions should have been based on broader considerations. BMJ 321 : 1225; author reply 1226–1227.
  73. Cooper E, 2000. Treatment for intestinal helminth infection. Message does not follow from systematic review’s findings. BMJ 321 : 1225–1226; author reply 1226–1227.
  74. Michael E, 2000. Treatment for intestinal helminth infection. Contrary to authors’ comments, meta-analysis supports global helminth control initiatives. BMJ 321 : 1224–1225; author reply 1226–1227.
  75. Savioli L, Neira M, Albonico M, Beach MJ, Chwaya HM, Crompton DW, Dunne J, Ehrenberg JP, Gyorkos T, Kvalsvig J, Taylor MG, Urbani C, Zheng F, 2000. Treatment for intestinal helminth infection. Review needed to take account of all relevant evidence, not only effects on growth and cognitive performance. BMJ 321 : 1226–1227.
  76. Bethony J, Chen J, Lin S, Xiao S, Zhan B, Li S, Xue H, Xing F, Humphries D, Yan W, Chen G, Foster V, Hawdon JM, Hotez PJ, 2002. Emerging patterns of hookworm infection: influence of aging on the intensity of Necator infection in Hainan Province, People’s Republic of China. Clin Infect Dis 35 : 1336–1344.
  77. Geiger SM, Massara CL, Bethony J, Soboslay PT, Correa-Oliveira R, 2004. Cellular responses and cytokine production in post-treatment hookworm patients from an endemic area in Brazil. Clin Exp Immunol 136 : 334–340.
  78. Lopez AD, Mathers CD, Ezzati M, Jamison DT, Murray CJ, 2006. Global and regional burden of disease and risk factors, 2001: systematic analysis of population health data. Lancet 367 : 1747–1757.
  79. Nussenblatt V, Semba RD, 2002. Micronutrient malnutrition and the pathogenesis of malarial anemia. Acta Trop 82 : 321–337.
  80. 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 : 25–34.
  81. Casals-Pascual C, Roberts DJ, 2006. Severe malarial anaemia. Curr Mol Med 6 : 155–168.
  82. Roberts DJ, Casals-Pascual C, Weatherall DJ, 2005. The clinical and pathophysiological features of malarial anaemia. Curr Top Microbiol Immunol 295 : 137–167.
  83. Phillips RE, Pasvol G, 1992. Anaemia of Plasmodium falciparum malaria. Baillieres Clin Haematol 5 : 315–330.
  84. Fleming A, 1996. Haematological diseases in the tropics. Cook GC, ed. Manson’s Tropical Disease. Philadelphia: W.B. Saunders, 101–173.
  85. Dondorp AM, Angus BJ, Chotivanich K, Silamut K, Ruangveerayuth R, Hardeman MR, Kager PA, Vreeken J, White NJ, 1999. Red blood cell deformability as a predictor of anemia in severe falciparum malaria. Am J Trop Med Hyg 60 : 733–737.
  86. Davis TM, Krishna S, Looareesuwan S, Supanaranond W, Pukrittayakamee S, Attatamsoonthorn K, White NJ, 1990. Erythrocyte sequestration and anemia in severe falciparum malaria. Analysis of acute changes in venous hematocrit using a simple mathematical model. J Clin Invest 86 : 793–800.
  87. Clark IA, Chaudhri G, 1988. Tumour necrosis factor may contribute to the anaemia of malaria by causing dyserythropoiesis and erythrophagocytosis. Br J Haematol 70 : 99–103.
  88. McGuire W, Knight JC, Hill AV, Allsopp CE, Greenwood BM, Kwiatkowski D, 1999. Severe malarial anemia and cerebral malaria are associated with different tumor necrosis factor promoter alleles. J Infect Dis 179 : 287–290.
  89. Burgmann H, Looareesuwan S, Kapiotis S, Viravan C, Vanijanonta S, Hollenstein U, Wiesinger E, Presterl E, Winkler S, Graninger W, 1996. Serum levels of erythropoietin in acute Plasmodium falciparum malaria. Am J Trop Med Hyg 54 : 280–283.
  90. el Hassan AM, Saeed AM, Fandrey J, Jelkmann W, 1997. Decreased erythropoietin response in Plasmodium falciparum malaria-associated anaemia. Eur J Haematol 59 : 299–304.
  91. Kurtzhals JA, Adabayeri V, Goka BQ, Akanmori BD, Oliver-Commey JO, Nkrumah FK, Behr C, Hviid L, 1998. Low plasma concentrations of interleukin 10 in severe malarial anaemia compared with cerebral and uncomplicated malaria. Lancet 351 : 1768–1772.
  92. Shankar AH, Genton B, Semba RD, Baisor M, Paino J, Tamja S, Adiguma T, Wu L, Rare L, Tielsch JM, Alpers MP, West KP Jr, 1999. Effect of vitamin A supplementation on morbidity due to Plasmodium falciparum in young children in Papua New Guinea: a randomised trial. Lancet 354 : 203–209.
  93. Prual A, Daouda H, Develoux M, Sellin B, Galan P, Hercberg S, 1992. Consequences of Schistosoma haematobium infection on the iron status of schoolchildren in Niger. Am J Trop Med Hyg 47 : 291–297.
  94. Mansour MM, Francis WM, Farid Z, 1985. Prevalence of latent iron deficiency in patients with chronic S. mansoni infection. Trop Geogr Med 37 : 124–128.
  95. Yuesgeng L, Dongbao Y, Yi L, Yang X, Meng X, 1992. Morbidity and Health Impact of Schistosomiasis japonica in Dongting Lake Area. A Final Report. Geneva: World Health Organization Collaborating Center for Research and Control on Schistosomiasisis in Lake Region.
  96. Tatala S, Svanberg U, Mduma B, 1998. Low dietary iron availability is a major cause of anemia: a nutrition survey in the Lindi District of Tanzania. Am J Clin Nutr 68 : 171–178.
  97. Friedman JF, Kanzaria HK, Acosta LP, Langdon GC, Manalo DL, Wu H, Olveda RM, McGarvey ST, Kurtis JD, 2005. Relationship between Schistosoma japonicum and nutritional status among children and young adults in Leyte, the Philippines. Am J Trop Med Hyg 72 : 527–533.
  98. Kanzaria HK, Acosta LP, Langdon GC, Manalo DL, Olveda RM, McGarvey ST, Kurtis JD, Friedman JF, 2005. Schistosoma japonicum and occult blood loss in endemic villages in Leyte, the Philippines. Am J Trop Med Hyg 72 : 115–118.
  99. Friedman JF, Kanzaria HK, McGarvey ST, 2005. Human schistosomiasis and anemia: the relationship and potential mechanisms. Trends Parasitol 21 : 386–392.
  100. Leenstra T, Acosta LP, Langdon GC, Manalo DL, Su L, Olveda RM, McGarvey ST, Kurtis JD, Friedman JF, 2006. Schistosomiasis japonica, anemia, and iron status in children, adolescents, and young adults in Leyte, Philippines 1. Am J Clin Nutr 83 : 371–379.
  101. Friis H, Mwaniki D, Omondi B, Muniu E, Thiong’o F, Ouma J, Magnussen P, Geissler PW, Michaelsen KF, 2003. Effects on haemoglobin of multi-micronutrient supplementation and multi-helminth chemotherapy: a randomized, controlled trial in Kenyan school children. Eur J Clin Nutr 57 : 573–579.
  102. Olds GR, King C, Hewlett J, Olveda R, Wu G, Ouma J, Peters P, McGarvey S, Odhiambo O, Koech D, Liu CY, Aligui G, Gachihi G, Kombe Y, Parraga I, Ramirez B, Whalen C, Horton RJ, Reeve P, 1999. Double-blind placebo-controlled study of concurrent administration of albendazole and praziquantel in schoolchildren with schistosomiasis and geohelminths. J Infect Dis 179 : 996–1003.
  103. Taylor M, Jinabhai CC, Couper I, Kleinschmidt I, Jogessar VB, 2001. The effect of different anthelmintic treatment regimens combined with iron supplementation on the nutritional status of schoolchildren in KwaZulu-Natal, South Africa: a randomized controlled trial. Trans R Soc Trop Med Hyg 95 : 211–216.
  104. Beasley NM, Tomkins AM, Hall A, Kihamia CM, Lorri W, Nduma B, Issae W, Nokes C, Bundy DA, 1999. The impact of population level deworming on the haemoglobin levels of schoolchildren in Tanga, Tanzania. Trop Med Int Health 4 : 744–750.
  105. Stephenson LS, Latham MC, Kurz KM, Kinoti SN, Oduori ML, Crompton DW, 1985. Relationships of Schistosoma hematobium, hookworm and malarial infections and metrifonate treatment to hemoglobin level in Kenyan school children. Am J Trop Med Hyg 34 : 519–528.
  106. Stephenson LS, Kinoti SN, Latham MC, Kurz KM, Kyobe J, 1989. Single dose metrifonate or praziquantel treatment in Kenyan children. I. Effects on Schistosoma haematobium, hookworm, hemoglobin levels, splenomegaly, and hepatomegaly. Am J Trop Med Hyg 41 : 436–444.
  107. McGarvey ST, Aligui G, Graham KK, Peters P, Olds GR, Olveda R, 1996. Schistosomiasis japonica and childhood nutritional status in northeastern Leyte, the Philippines: a randomized trial of praziquantel versus placebo. Am J Trop Med Hyg 54 : 498–502.
  108. Warren KS, Su DL, Xu ZY, Yuan HC, Peters PA, Cook JA, Mott KE, Houser HB, 1983. Morbidity in schistosomiasis japonica in relation to intensity of infection. A study of two rural brigades in Anhui Province, China. N Engl J Med 309 : 1533–1539.
  109. Coutinho HM, McGarvey ST, Acosta LP, Manalo DL, Langdon GC, Leenstra T, Kanzaria HK, Solomon J, Wu H, Olveda RM, Kurtis JD, Friedman JF, 2005. Nutritional status and serum cytokine profiles in children, adolescents, and young adults with Schistosoma japonicum-associated hepatic fibrosis, in Leyte, Philippines. J Infect Dis 192 : 528–536.
  110. Stephenson LS, Holland CV, Cooper ES, 2000. The public health significance of Trichuris trichiura. Parasitology 121 (Suppl): S73–S95.
  111. Ramdath DD, Simeon DT, Wong MS, Grantham-McGregor SM, 1995. Iron status of schoolchildren with varying intensities of Trichuris trichiura infection. Parasitology 110 : 347–351.
  112. Robertson LJ, Crompton DW, Sanjur D, Nesheim MC, 1992. Haemoglobin concentrations and concomitant infections of hookworm and Trichuris trichiura in Panamanian primary schoolchildren. Trans R Soc Trop Med Hyg 86 : 654–656.
  113. Duff EM, Anderson NM, Cooper ES, 1999. Plasma insulin-like growth factor-1, type 1 procollagen, and serum tumor necrosis factor alpha in children recovering from Trichuris dysentery syndrome. Pediatrics 103 : e69.
  114. Raj SM, 1999. Fecal occult blood testing on Trichuris-infected primary school children in northeastern peninsular Malaysia. Am J Trop Med Hyg 60 : 165–166.
  115. Mentzer WC, Kan YW, 2001. Prospects for research in hematologic disorders: sickle cell disease and thalassemia. JAMA 285 : 640–642.
  116. Williams TN, Mwangi TW, Roberts DJ, Alexander ND, Weatherall DJ, Wambua S, Kortok M, Snow RW, Marsh K, 2005. An immune basis for malaria protection by the sickle cell trait. PLoS Med 2 : e128.
  117. Cabrera G, Cot M, Migot-Nabias F, Kremsner PG, Deloron P, Luty AJ, 2005. The sickle cell trait is associated with enhanced immunoglobulin G antibody responses to Plasmodium falciparum variant surface antigens. J Infect Dis 191 : 1631–1638.
  118. Williams TN, Mwangi TW, Wambua S, Alexander ND, Kortok M, Snow RW, Marsh K, 2005. Sickle cell trait and the risk of Plasmodium falciparum malaria and other childhood diseases. J Infect Dis 192 : 178–186.
  119. Parikh S, Dorsey G, Rosenthal PJ, 2004. Host polymorphisms and the incidence of malaria in Ugandan children. Am J Trop Med Hyg 71 : 750–753.
  120. Olivieri NF, 1999. The beta-thalassemias. N Engl J Med 341 : 99–109.
  121. Greenberg PL, Gordeuk V, Issaragrisil S, Siritanaratkul N, Fucharoen S, Ribeiro RC, 2001. Major hematologic diseases in the developing world- new aspects of diagnosis and management of thalassemia, malarial anemia, and acute leukemia. Hematology (Am Soc Hematol Educ Program) : 479–498.
http://instance.metastore.ingenta.com/content/journals/10.4269/ajtmh.2007.77.44
Loading
  • Received : 26 Jul 2006
  • Accepted : 13 Apr 2007

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