The iron trap: iron, malaria and anemia at the mother-child interface

Microbes and Infection

Volumn 11, Issue 4, 2009, Pages 460-466

  Friedman, Jennifer F ^a,b   Kurtis, Jonathan D ^b,c   Kabyemela, Edward R ^d,e   Fried, Michal ^e,f   Duffy, Patrick E ^e,f  

^a BROWN UNIVERSITY   (United States)

^b RHODE ISLAND HOSPITAL   (United States)

^c BROWN UNIVERSITY   (United States)

^d MUHIMBILI UNIVERSITY OF HEALTH AND ALLIED SCIENCES   (Tanzania)

^e SEATTLE BIOMEDICAL RESEARCH INSTITUTE   (United States)

^f UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Anemia; Iron; Malaria; Plasmodium

Indexed keywords

C REACTIVE PROTEIN; FERROPORTIN; FOLIC ACID; HEMOGLOBIN; HEPCIDIN; IRON; TRANSFERRIN RECEPTOR;

CLINICAL TRIAL; CYTOKINE PRODUCTION; DISEASE ASSOCIATION; ETHNICITY; FERRITIN BLOOD LEVEL; FETUS; HEMOGLOBIN BLOOD LEVEL; HIGH RISK POPULATION; HOMEOSTASIS; HORMONE SYNTHESIS; HUMAN; INFECTION RISK; INFECTION SENSITIVITY; INFLAMMATION; IRON ABSORPTION; IRON DEFICIENCY; IRON DEFICIENCY ANEMIA; IRON METABOLISM; IRON STORAGE; IRON THERAPY; IRON TRANSPORT; MALARIA; MALARIA CONTROL; MORBIDITY; MORTALITY; PLACENTAL TRANSFER; PREGNANCY; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; RISK ASSESSMENT; RISK REDUCTION; SHORT SURVEY; TREATMENT OUTCOME;

ANEMIA; FEMALE; HUMANS; IRON; MALARIA; PREGNANCY;

EID: 64649102137     PISSN: 12864579     EISSN: 1769714X     Source Type: Journal    
DOI: 10.1016/j.micinf.2009.02.006     Document Type: Short Survey

References (76)

1. Oppenheimer S.J., Macfarlane S.B., Moody J.B., and Harrison C. Total dose iron infusion, malaria and pregnancy in Papua New Guinea. Trans. R. Soc. Trop. Med. Hyg. 80 (1986) 818-822
2. Menendez C., Todd J., Alonso P.L., Francis N., Lulat S., Ceesay S., M'Boge B., and Greenwood B.M. The effects of iron supplementation during pregnancy, given by traditional birth attendants, on the prevalence of anaemia and malaria. Trans. R. Soc. Trop. Med. Hyg. 88 (1994) 590-593
3. Nacher M., McGready R., Stepniewska K., Cho T., Looareesuwan S., White N.J., and Nosten F. Haematinic treatment of anaemia increases the risk of Plasmodium vivax malaria in pregnancy. Trans. R. Soc. Trop. Med. Hyg. 97 (2003) 273-276
4. Kabyemela E.R., Fried M., Kurtis J.D., Mutabingwa T.K., and Duffy P.E. Decreased susceptibility to Plasmodium falciparum infection in pregnant women with iron deficiency. J. Infect. Dis. 198 (2008) 163-166
5. Nyakeriga A.M., Troye-Blomberg M., Dorfman J.R., Alexander N.D., Back R., Kortok M., Chemtai A.K., Marsh K., and Williams T.N. Iron deficiency and malaria among children living on the coast of Kenya. J. Infect. Dis. 190 (2004) 439-447
6. Verhoef H., West C.E., Nzyuko S.M., de Vogel S., van der Valk R., Wanga M.A., Kuijsten A., Veenemans J., and Kok F.J. Intermittent administration of iron and sulfadoxine-pyrimethamine to control anaemia in Kenyan children: a randomised controlled trial. Lancet 360 (2002) 908-914
7. Oppenheimer S.J., Gibson F.D., Macfarlane S.B., Moody J.B., Harrison C., Spencer A., and Bunari O. Iron supplementation increases prevalence and effects of malaria: report on clinical studies in Papua New Guinea. Trans. R. Soc. Trop. Med. Hyg. 80 (1986) 603-612
8. Sazawal S., Black R.E., Ramsan M., Chwaya H.M., Stoltzfus R.J., Dutta A., Dhingra U., Kabole I., Deb S., Othman M.K., and Kabole F.M. 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 (2006) 133-143
9. Ellman R., Maxwell C., Finch R., and Shayo D. Malaria and anaemia at different altitudes in the Muheza district of Tanzania: childhood morbidity in relation to level of exposure to infection. Ann. Trop. Med. Parasitol. 92 (1998) 741-753
10. Coutinho H.M., McGarvey S.T., Acosta L.P., Manalo D.L., Langdon G.C., Leenstra T., Kanzaria H.K., Solomon J., Wu H., Olveda R.M., Kurtis J.D., and Friedman J.F. 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 (2005) 528-536
11. Leenstra T., Coutinho H.M., Acosta L.P., Langdon G.C., Su L., Olveda R.M., McGarvey S.T., Kurtis J.D., and Friedman J.F. Schistosoma japonicum reinfection after praziquantel treatment causes anemia associated with inflammation. Infect. Immun. 74 (2006) 6398-6407
12. Weiss G., Werner-Felmayer G., Werner E.R., Grunewald K., Wachter H., and Hentze M.W. Iron regulates nitric oxide synthase activity by controlling nuclear transcription. J. Exp. Med. 180 (1994) 969-976
13. Guidotti R.J. Anaemia in pregnancy in developing countries. BJOG 107 (2000) 437-438
14. Levy A., Fraser D., Katz M., Mazor M., and Sheiner E. Maternal anemia during pregnancy is an independent risk factor for low birthweight and preterm delivery. European journal of obstetrics, gynecology, and reproductive biology 122 (2005) 182-186
15. Murphy S.C., and Breman J.G. 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 (2001) 57-67
16. Brabin B. Fetal anaemia in malarious areas: its causes and significance. Ann. Trop. Paediatr. 12 (1992) 303-310
17. le Cessie S., Verhoeff F.H., Mengistie G., Kazembe P., Broadhead R., and Brabin B.J. Changes in haemoglobin levels in infants in Malawi: effect of low birth weight and fetal anaemia. Arch. Dis. Child Fetal Neonatal Ed. 86 (2002) F182-F187
18. van Eijk A.M., Ayisi J.G., Ter Kuile F.O., Slutsker L., Shi Y.P., Udhayakumar V., Otieno J.A., Kager P.A., Lal R.B., Steketee R.W., and Nahlen B.L. HIV, malaria, and infant anemia as risk factors for postneonatal infant mortality among HIV-seropositive women in Kisumu, Kenya. J. Infect. Dis. 196 (2007) 30-37
19. Brabin B.J., Kalanda B.F., Verhoeff F.H., Chimsuku L.H., and Broadhead R.L. Risk factors for fetal anaemia in a malarious area of Malawi. Ann. Trop. Paediatr. 24 (2004) 311-321
20. Abrams E.T., Kwiek J.J., Mwapasa V., Kamwendo D.D., Tadesse E., Lema V.M., Molyneux M.E., Rogerson S.J., and Meshnick S.R. Malaria during pregnancy and foetal haematological status in Blantyre, Malawi. Malar. J. 4 (2005) 39
21. Bodnar L.M., Siega-Riz A.M., Arab L., Chantala K., and McDonald T. Predictors of pregnancy and postpartum haemoglobin concentrations in low-income women. Publ. Health Nutr. 7 (2004) 701-711
22. Massawe S.N., Urassa E.N., Mmari M., Ronquist G., Lindmark G., and Nystrom L. The complexity of pregnancy anemia in Dar-es-Salaam. Gynecol. Obstet Investig. 47 (1999) 76-82
23. Atkinson S.H., Rockett K.A., Morgan G., Bejon P.A., Sirugo G., O'Connell M.A., Hanchard N., Kwiatkowski D., and Prentice A.M. Tumor necrosis factor SNP haplotypes are associated with iron deficiency anemia in West African children. Blood (2008)
24. Jaime-Perez J.C., Herrera-Garza J.L., and Gomez-Almaguer D. Sub-optimal fetal iron acquisition under a maternal environment. Arch. Med. Res. 36 (2005) 598-602
25. Ganz T. Hepcidin, a key regulator of iron metabolism and mediator of anemia of inflammation. Blood 102 (2003) 783-788
26. De Domenico I., Nemeth E., Nelson J.M., Phillips J.D., Ajioka R.S., Kay M.S., Kushner J.P., Ganz T., Ward D.M., and Kaplan J. The hepcidin-binding site on ferroportin is evolutionarily conserved. Cell. Metab. 8 (2008) 146-156
27. Nemeth E., Tuttle M.S., Powelson J., Vaughn M.B., Donovan A., Ward D.M., Ganz T., and Kaplan J. Hepcidin regulates cellular iron efflux by binding to ferroportin and inducing its internalization. Science 306 (2004) 2090-2093
28. Martin M.E., Nicolas G., Hetet G., Vaulont S., Grandchamp B., and Beaumont C. Transferrin receptor 1 mRNA is downregulated in placenta of hepcidin transgenic embryos. FEBS Lett. 574 (2004) 187-191
29. Andrews N.C. Forging a field: the golden age of iron biology. Blood 112 (2008) 219-230
30. Ganz T. The role of hepcidin in iron sequestration during infections and in the pathogenesis of anemia of chronic disease. Isr. Med. Assoc. J. 4 (2002) 1043-1045
31. Means Jr. R.T. The anaemia of infection. Baillieres Best Pract. Res. Clin. Haematol. 13 (2000) 151-162
32. el Hassan A.M., Saeed A.M., Fandrey J., and Jelkmann W. Decreased erythropoietin response in Plasmodium falciparum malaria-associated anaemia. Eur. J. Haematol. 59 (1997) 299-304
33. Baer A.N., Dessypris E.N., Goldwasser E., and Krantz S.B. Blunted erythropoietin response to anaemia in rheumatoid arthritis. Br. J. Haematol. 66 (1987) 559-564
34. Miller C.B., Jones R.J., Piantadosi S., Abeloff M.D., and Spivak J.L. Decreased erythropoietin response in patients with the anemia of cancer. N. Engl. J. Med. 322 (1990) 1689-1692
35. Means Jr. R.T., Dessypris E.N., and Krantz S.B. Inhibition of human colony-forming-unit erythroid by tumor necrosis factor requires accessory cells. J. Clin. Invest. 86 (1990) 538-541
36. Means Jr. R.T., and Krantz S.B. Inhibition of human erythroid colony-forming units by tumor necrosis factor requires beta interferon. J. Clin. Invest. 91 (1993) 416-419
37. Roodman G.D., Johnson R.A., and Clibon U. Tumor necrosis factor alpha and the anemia of chronic disease: effects of chronic exposure to TNF on erythropoiesis in vivo. Adv. Exp. Med. Biol. 271 (1989) 185-196
38. Konijn A., and Heschko C. The anaemia of inflammation and chronic disease. In: DeSousa M., and Brock J.H. (Eds). Iron in Immunity, Cancer, and Inflammation (1989), John Wiley and Sons, Chichester, UK 111-143
39. Nemeth E., Rivera S., Gabayan V., Keller C., Taudorf S., Pedersen B.K., and Ganz T. IL-6 mediates hypoferremia of inflammation by inducing the synthesis of the iron regulatory hormone hepcidin. J. Clin. Invest. 113 (2004) 1271-1276
40. Nicolas G., Chauvet C., Viatte L., Danan J.L., Bigard X., Devaux I., Beaumont C., Kahn A., and Vaulont S. The gene encoding the iron regulatory peptide hepcidin is regulated by anemia, hypoxia, and inflammation. J. Clin. Invest. 110 (2002) 1037-1044
41. Beguin Y., Huebers H.A., Weber G., Eng M., and Finch C.A. Hepatocyte iron release in rats. J. Lab. Clin. Med. 113 (1989) 346-354
42. Hershko C., Cook J.D., and Finch C.A. Storage iron kinetics VI. The effect of inflammation on iron exchange in the rat. Br. J. Haematol. 28 (1974) 67-75
43. Nicolas G., Bennoun M., Porteu A., Mativet S., Beaumont C., Grandchamp B., Sirito M., Sawadogo M., Kahn A., and Vaulont S. Severe iron deficiency anemia in transgenic mice expressing liver hepcidin. Proc. Natl. Acad. Sci. U S A 99 (2002) 4596-4601
44. Ganz T. Hepcidin and its role in regulating systemic iron metabolism, Hematology. Am. Soc. Hematol. Educ. Program. 29-35 (2006) 507
45. Muehlenbachs A., Fried M., Lachowitzer J., Mutabingwa T.K., and Duffy P.E. Genome-wide expression analysis of placental malaria reveals features of lymphoid neogenesis during chronic infection. J. Immunol. 179 (2007) 557-565
46. Howard C.T., McKakpo U.S., Quakyi I.A., Bosompem K.M., Addison E.A., Sun K., Sullivan D., and Semba R.D. Relationship of hepcidin with parasitemia and anemia among patients with uncomplicated Plasmodium falciparum malaria in Ghana. Am. J. Trop. Med. Hyg. 77 (2007) 623-626
47. Levy J.E., Jin O., Fujiwara Y., Kuo F., and Andrews N.C. Transferrin receptor is necessary for development of erythrocytes and the nervous system. Nat. Genet. 21 (1999) 396-399
48. Gambling L., Danzeisen R., Fosset C., Andersen H.S., Dunford S., Srai S.K., and McArdle H.J. Iron and copper interactions in development and the effect on pregnancy outcome. J. Nutr. 133 (2003) 1554S-1556S
49. Allen L.H. Anemia and iron deficiency: effects on pregnancy outcome. Am. J. Clin. Nutr. 71 (2000) 1280S-1284S
50. Rao R., and Georgieff M.K. Perinatal aspects of iron metabolism. Acta. Paediatr. Suppl. 91 (2002) 124-129
51. Verhoeff F.H., Brabin B.J., van Buuren S., Chimsuku L., Kazembe P., Wit J.M., and Broadhead R.L. An analysis of intra-uterine growth retardation in rural Malawi. Eur. J. Clin. Nutr. 55 (2001) 682-689
52. Allen L.H. Biological mechanisms that might underlie iron's effects on fetal growth and preterm birth. J. Nutr. 131 (2001) 581S-589S
53. Bastin J., Drakesmith H., Rees M., Sargent I., and Townsend A. Localisation of proteins of iron metabolism in the human placenta and liver. Br. J. Haematol. 134 (2006) 532-543
54. Fuchs R., and Ellinger I. Endocytic and transcytotic processes in villous syncytiotrophoblast: role in nutrient transport to the human fetus. Traffic 5 (2004) 725-738
55. Ganti A.K., Moazzam N., Laroia S., Tendulkar K., Potti A., and Mehdi S.A. Predictive value of absent bone marrow iron stores in the clinical diagnosis of iron deficiency anemia. In vivo (Athens, Greece) 17 (2003) 389-392
56. Hughes D.A., Stuart-Smith S.E., and Bain B.J. How should stainable iron in bone marrow films be assessed?. J. Clin. Pathol. 57 (2004) 1038-1040
57. Barron B.A., Hoyer J.D., and Tefferi A. A bone marrow report of absent stainable iron is not diagnostic of iron deficiency. Ann. Hematol. 80 (2001) 166-169
58. Finch C.A., Bellotti V., Stray S., Lipschitz D.A., Cook J.D., Pippard M.J., and Huebers H.A. Plasma ferritin determination as a diagnostic tool. West J. Med. 145 (1986) 657-663
59. Ferguson B.J., Skikne B.S., Simpson K.M., Baynes R.D., and Cook J.D. Serum transferrin receptor distinguishes the anemia of chronic disease from iron deficiency anemia. J. Lab. Clin. Med. 119 (1992) 385-390
60. Menendez C., Quinto L.L., Kahigwa E., Alvarez L., Fernandez R., Gimenez N., Schellenberg D., Aponte J.J., Tanner M., and Alonso P.L. Effect of malaria on soluble transferrin receptor levels in Tanzanian infants. Am. J. Trop. Med. Hyg. 65 (2001) 138-142
61. Siddappa A.M., Rao R., Long J.D., Widness J.A., and Georgieff M.K. The assessment of newborn iron stores at birth: a review of the literature and standards for ferritin concentrations. Neonatology 92 (2007) 73-82
62. Allen J., Backstrom K.R., Cooper J.A., Cooper M.C., Detwiler T.C., Essex D.W., Fritz R.P., Means Jr. R.T., Meier P.B., Pearlman S.R., Roitman-Johnson B., and Seligman P.A. Measurement of soluble transferrin receptor in serum of healthy adults. Clin. Chem. 44 (1998) 35-39
63. Zimmermann M.B., Molinari L., Staubli-Asobayire F., Hess S.Y., Chaouki N., Adou P., and Hurrell R.F. Serum transferrin receptor and zinc protoporphyrin as indicators of iron status in African children. Am. J. Clin. Nutr. 81 (2005) 615-623
64. Perry G.S., Byers T., Yip R., and Margen S. Iron nutrition does not account for the hemoglobin differences between blacks and whites. J. Nutr. 122 (1992) 1417-1424
65. Johnson-Spear M.A., and Yip R. Hemoglobin difference between black and white women with comparable iron status: justification for race-specific anemia criteria. Am. J. Clin. Nutr. 60 (1994) 117-121
66. Baumann-Blackmore N.L., Goetz E., Blohowiak S.E., Zaka O., and Kling P.J. Cord blood zinc protoporphyrin/heme ratio in minority neonates at risk for iron deficiency. J. Pediatr. 153 (2008) 133-136
67. Georgieff M.K., Wewerka S.W., Nelson C.A., and Deregnier R.A. Iron status at 9 months of infants with low iron stores at birth. J. Pediatr. 141 (2002) 405-409
68. Rettmer R.L., Carlson T.H., Origenes M.L., Jack R.M., and Labb R.F. Zinc protoporphyrin/heme ratio for diagnosis of preanemic iron deficiency. Pediatrics 104 (1999) e37
69. Cook J.D. Diagnosis and management of iron-deficiency anaemia. Best Pract. Res. Clin. Haematol. 18 (2005) 319-332
70. Labbe R.F., Rettmer R.L., Shah A.G., and Turnlund J.R. Zinc protoporphyrin. Past, present, and future. Ann. NY Acad. Sci. 514 (1987) 7-14
71. Labbe R.F., Vreman H.J., and Stevenson D.K. Zinc protoporphyrin: a metabolite with a mission. Clin. Chem. 45 (1999) 2060-2072
72. Labbe R.F., and Dewanji A. Iron assessment tests: transferrin receptor vis-a-vis zinc protoporphyrin. Clin. Biochem. 37 (2004) 165-174
73. Miller S.M., McPherson R.J., and Juul S.E. Iron sulfate supplementation decreases zinc protoporphyrin to heme ratio in premature infants. J. Pediatr. 148 (2006) 44-48
74. Juul S.E., Zerzan J.C., Strandjord T.P., and Woodrum D.E. Zinc protoporphyrin/heme as an indicator of iron status in NICU patients. J. Pediatr. 142 (2003) 273-278
75. Lott D.G., Zimmerman M.B., Labbe R.F., Kling P.J., and Widness J.A. Erythrocyte zinc protoporphyrin is elevated with prematurity and fetal hypoxemia. Pediatrics 116 (2005) 414-422
76. Stoltzfus R.J., Chwaya H.M., Albonico M., Schulze K.J., Savioli L., and Tielsch J.M. Serum ferritin, erythrocyte protoporphyrin and hemoglobin are valid indicators of iron status of school children in a malaria-holoendemic population. J. Nutr. 127 (1997) 293-298