ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
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1.
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-
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-
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Nemeth E, Rivera S, Gabayan V, Keller C, Taudorf S, Pedersen BK, Ganz T, 2004. IL-6 mediates hypoferremia of inflammation by inducing the synthesis of the iron regulatory hormone hepcidin. J Clin Invest 113: 1271–1276.
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Nemeth E, Tuttle MS, Powelson J, Vaughn MB, Donovan A, Ward DM, Ganz T, Kaplan J, 2004. Hepcidin regulates cellular iron efflux by binding to ferroportin and inducing its internalization. Science 306: 2090–2093.
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7.
Rodriguez R, Jung CL, Gabayan V, Deng JC, Ganz T, Nemeth E, Bulut Y, 2014. Hepcidin induction by pathogens and pathogen-derived molecules is strongly dependent on interleukin-6. Infect Immun 82: 745–752.
-
8.
Kemna E, Pickkers P, Nemeth E, van der Hoeven H, Swinkels D, 2005. Time-course analysis of hepcidin, serum iron, and plasma cytokine levels in humans injected with LPS. Blood 106: 1864–1866.
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Doherty CP, Cox SE, Fulford AJ, Austin S, Hilmers DC, Abrams SA, Prentice AM, 2008. Iron incorporation and post-malaria anaemia. PLoS One 3: e2133.
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Clark MA, Goheen MM, Fulford A, Prentice AM, Elnagheeb MA, Patel J, Fisher N, Taylor SM, Kasthuri RS, Cerami C, 2014. Host iron status and iron supplementation mediate susceptibility to erythrocytic stage Plasmodium falciparum. Nat Commun 5: 4446.
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Portugal S, Carret C, Recker M, Armitage AE, Goncalves LA, Epiphanio S, Sullivan D, Roy C, Newbold CI, Drakesmith H, Mota MM, 2011. Host-mediated regulation of superinfection in malaria. Nat Med 17: 732–737.
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Nyakeriga AM, Troye-Blomberg M, Dorfman JR, Alexander ND, Back 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: 439–447.
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Kabyemela ER, Fried M, Kurtis JD, Mutabingwa TK, Duffy PE, 2008. Decreased susceptibility to Plasmodium falciparum infection in pregnant women with iron deficiency. J Infect Dis 198: 163–166.
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Senga EL, Harper G, Koshy G, Kazembe PN, Brabin BJ, 2011. Reduced risk for placental malaria in iron deficient women. Malar J 10: 47.
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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: 1137–1144.
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18.
Sangare L, van Eijk AM, Ter Kuile FO, Walson J, Stergachis A, 2014. The association between malaria and iron status or supplementation in pregnancy: a systematic review and meta-analysis. PLoS One 9: e87743.
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Sazawal S, Black RE, Ramsan M, Chwaya HM, Stoltzfus RJ, Dutta A, Dhingra U, Kabole I, Deb S, Othman MK, Kabole FM, 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: 133–143.
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Veenemans J, Milligan P, Prentice AM, Schouten LR, Inja N, van der Heijden AC, de Boer LC, Jansen EJ, Koopmans AE, Enthoven WT, Kraaijenhagen RJ, Demir AY, Uges DR, Mbugi EV, Savelkoul HF, Verhoef H, 2011. Effect of supplementation with zinc and other micronutrients on malaria in Tanzanian children: a randomised trial. PLoS Med 8: e1001125.
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Drakesmith H, Prentice AM, 2012. Hepcidin and the iron-infection axis. Science 338: 768–772.
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Kabyemela E, Goncalves BP, Prevots DR, Morrison R, Harrington W, Gwamaka M, Kurtis JD, Fried M, Duffy PE, 2013. Cytokine profiles at birth predict malaria severity during infancy. PLoS One 8: e77214.
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Prentice AM, Doherty CP, Abrams SA, Cox SE, Atkinson SH, Verhoef H, Armitage AE, Drakesmith H, 2012. Hepcidin is the major predictor of erythrocyte iron incorporation in anemic African children. Blood 119: 1922–1928.
-
25.
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.
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Chong SS, Boehm CD, Higgs DR, Cutting GR, 2000. Single-tube multiplex-PCR screen for common deletional determinants of α-thalassemia. Blood 95: 360–362.
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Fibrinogen Studies Collaboration, Kaptoge S, White IR, Thompson SG, Wood AM, Lewington S, Lowe GD, Danesh J, 2007. Associations of plasma fibrinogen levels with established cardiovascular disease risk factors, inflammatory markers, and other characteristics: individual participant meta-analysis of 154,211 adults in 31 prospective studies: the Fibrinogen Studies Collaboration. Am J Epidemiol 166: 867–879.
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de Mast Q, Nadjm B, Reyburn H, Kemna EH, Amos B, Laarakkers CM, Silalye S, Verhoef H, Sauerwein RW, Swinkels DW, van der Ven AJ, 2009. Assessment of urinary concentrations of hepcidin provides novel insight into disturbances in iron homeostasis during malarial infection. J Infect Dis 199: 253–262.
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Cord Blood Hepcidin: Cross-Sectional Correlates and Associations with Anemia, Malaria, and Mortality in a Tanzanian Birth Cohort Study
Elizabeth B. Brickley
Elizabeth B. Brickley
Laboratory of Malaria Immunology and Vaccinology, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, Maryland.
Department of Public Health and Primary Care, University of Cambridge, Cambridge, United Kingdom.
Department of Epidemiology, Geisel School of Medicine at Dartmouth, Lebanon, New Hampshire.
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Natasha Spottiswoode
Natasha Spottiswoode
Laboratory of Malaria Immunology and Vaccinology, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, Maryland.
Weatherall Institute of Molecular Medicine, University of Oxford, Oxford, United Kingdom.
Department of Microbiology and Immunology, Columbia University College of Physicians and Surgeons, New York, New York.
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Edward Kabyemela
Edward Kabyemela
Muheza Designated District Hospital, Muheza, Tanzania.
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Robert Morrison
Robert Morrison
Laboratory of Malaria Immunology and Vaccinology, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, Maryland.
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Jonathan D. Kurtis
Jonathan D. Kurtis
Rhode Island Hospital, Department of Pathology and Laboratory Medicine, Brown University Medical School, Providence, Rhode Island.
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Angela M. Wood
Angela M. Wood
Department of Public Health and Primary Care, University of Cambridge, Cambridge, United Kingdom.
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Hal Drakesmith
Hal Drakesmith
Weatherall Institute of Molecular Medicine, University of Oxford, Oxford, United Kingdom.
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Michal Fried
Michal Fried
Laboratory of Malaria Immunology and Vaccinology, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, Maryland.
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Patrick E. Duffy
Patrick E. Duffy
Laboratory of Malaria Immunology and Vaccinology, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, Maryland.
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Hepcidin, the master regulator of bioavailable iron, is a key mediator of anemia and also plays a central role in host defense against infection. We hypothesized that measuring hepcidin levels in cord blood could provide an early indication of interindividual differences in iron regulation with quantifiable implications for anemia, malaria, and mortality-related risk. Hepcidin concentrations were measured in cord plasma from a birth cohort (N = 710), which was followed for up to 4 years in a region of perennial malaria transmission in Muheza, Tanzania (2002–2006). At the time of delivery, cord hepcidin levels were correlated with inflammatory mediators, iron markers, and maternal health conditions. Hepcidin levels were 30% (95% confidence interval [CI]: 12%, 44%) lower in children born to anemic mothers and 48% (95% CI: 11%, 97%) higher in placental malaria–exposed children. Relative to children in the lowest third, children in the highest third of cord hepcidin had on average 2.5 g/L (95% CI: 0.1, 4.8) lower hemoglobin levels over the duration of follow-up, increased risk of anemia and severe anemia (adjusted hazard ratio [HR] [95% CI]: 1.18 [1.03, 1.36] and 1.34 [1.08, 1.66], respectively), and decreased risk of malaria and all-cause mortality (adjusted HR [95% CI]: 0.78 [0.67, 0.91] and 0.34 [0.14, 0.84], respectively). Although longitudinal measurements of hepcidin and iron stores are required to strengthen causal inference, these results suggest that hepcidin may have utility as a biomarker indicating children's susceptibility to anemia and infection in early life.
Author Notes
Financial support: This work was supported by the Intramural Research Program of the National Institute of Allergy and Infectious Diseases, National Institutes of Health (http://www.niaid.nih.gov/), the Bill & Melinda Gates Foundation (grant number 29202, http://www.gatesfoundation.org/), the Grand Challenges in Global Health Initiative (grant number 1364, http://grandchallenges.org/), the National Institutes of Health Fogarty International Center (grant number D43 TW005509, http://www.fic.nih.gov/), and the National Institutes of Health (grant number R01A152059 to Patrick E. Duffy). During the duration of study, Elizabeth B. Brickley and Natasha Spottiswoode were supported by the National Institutes of Health Oxford Cambridge Scholars Program (http://oxcam.gpp.nih.gov/). Hal Drakesmith is supported by the Medical Research Council, United Kingdom (http://www.mrc.ac.uk/).
Authors' addresses: Elizabeth B. Brickley, Laboratory of Malaria Immunology and Vaccinology, National Institute of Allergy and Infectious Diseases, Bethesda, MD, Department of Public Health and Primary Care, University of Cambridge, Cambridge, United Kingdom, and Department of Epidemiology, Dartmouth College Geisel School of Medicine, Lebanon, NH, E-mail: elizabeth.b.brickley@dartmouth.edu. Natasha Spottiswoode, Laboratory of Malaria Immunology and Vaccinology, National Institute of Allergy and Infectious Diseases, Bethesda, MD, Weatherall Institute of Molecular Medicine, University of Oxford, Oxford, United Kingdom, and Department of Microbiology and Immunology, Columbia University College of Physicians and Surgeons, New York, NY, E-mail: nns2115@cumc.columbia.edu. Edward Kabyemela, Mother-Offspring Malaria Studies Project, Muheza Designated District Hospital, Muheza, Tanzania, E-mail: earkabyemela@yahoo.com. Robert Morrison, Michal Fried, and Patrick E. Duffy, Laboratory of Malaria Immunology and Vaccinology, National Institute of Allergy and Infectious Diseases, Bethesda, MD, E-mails: bob.morrison@cidresearch.org, michal.fried@nih.gov, and patrick.duffy@nih.gov. Jonathan D. Kurtis, Center for International Health Research, Rhode Island Hospital, Providence, RI, E-mail: jonathan_kurtis@brown.edu. Angela M. Wood, Public Health and Primary Care, University of Cambridge, Cambridge, United Kingdom, E-mail: amw79@medschl.cam.ac.uk. Hal Drakesmith, Weatherall Institute of Molecular Medicine, University of Oxford, Oxford, United Kingdom, E-mail: alexander.drakesmith@ndm.ox.ac.uk.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Grantham-McGregor S, Ani C, 2001. A review of studies on the effect of iron deficiency on cognitive development in children. J Nutr 131: 649S–666S; discussion 666S–668S.
-
2.
Burke RM, Leon JS, Suchdev PS, 2014. Identification, prevention and treatment of iron deficiency during the first 1,000 days. Nutrients 6: 4093–4114.
-
3.
Roca-Feltrer A, Carneiro I, Smith L, Schellenberg JR, Greenwood B, Schellenberg D, 2010. The age patterns of severe malaria syndromes in sub-Saharan Africa across a range of transmission intensities and seasonality settings. Malar J 9: 282.
-
4.
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.
-
5.
Nemeth E, Rivera S, Gabayan V, Keller C, Taudorf S, Pedersen BK, Ganz T, 2004. IL-6 mediates hypoferremia of inflammation by inducing the synthesis of the iron regulatory hormone hepcidin. J Clin Invest 113: 1271–1276.
-
6.
Nemeth E, Tuttle MS, Powelson J, Vaughn MB, Donovan A, Ward DM, Ganz T, Kaplan J, 2004. Hepcidin regulates cellular iron efflux by binding to ferroportin and inducing its internalization. Science 306: 2090–2093.
-
7.
Rodriguez R, Jung CL, Gabayan V, Deng JC, Ganz T, Nemeth E, Bulut Y, 2014. Hepcidin induction by pathogens and pathogen-derived molecules is strongly dependent on interleukin-6. Infect Immun 82: 745–752.
-
8.
Kemna E, Pickkers P, Nemeth E, van der Hoeven H, Swinkels D, 2005. Time-course analysis of hepcidin, serum iron, and plasma cytokine levels in humans injected with LPS. Blood 106: 1864–1866.
-
9.
Doherty CP, Cox SE, Fulford AJ, Austin S, Hilmers DC, Abrams SA, Prentice AM, 2008. Iron incorporation and post-malaria anaemia. PLoS One 3: e2133.
-
10.
Cercamondi CI, Egli IM, Ahouandjinou E, Dossa R, Zeder C, Salami L, Tjalsma H, Wiegerinck E, Tanno T, Hurrell RF, Hounhouigan J, Zimmermann MB, 2010. Afebrile Plasmodium falciparum parasitemia decreases absorption of fortification iron but does not affect systemic iron utilization: a double stable-isotope study in young Beninese women. Am J Clin Nutr 92: 1385–1392.
-
11.
Mabeza GF, Loyevsky M, Gordeuk VR, Weiss G, 1999. Iron chelation therapy for malaria: a review. Pharmacol Ther 81: 53–75.
-
12.
Clark MA, Goheen MM, Fulford A, Prentice AM, Elnagheeb MA, Patel J, Fisher N, Taylor SM, Kasthuri RS, Cerami C, 2014. Host iron status and iron supplementation mediate susceptibility to erythrocytic stage Plasmodium falciparum. Nat Commun 5: 4446.
-
13.
Portugal S, Carret C, Recker M, Armitage AE, Goncalves LA, Epiphanio S, Sullivan D, Roy C, Newbold CI, Drakesmith H, Mota MM, 2011. Host-mediated regulation of superinfection in malaria. Nat Med 17: 732–737.
-
14.
Nyakeriga AM, Troye-Blomberg M, Dorfman JR, Alexander ND, Back 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: 439–447.
-
15.
Kabyemela ER, Fried M, Kurtis JD, Mutabingwa TK, Duffy PE, 2008. Decreased susceptibility to Plasmodium falciparum infection in pregnant women with iron deficiency. J Infect Dis 198: 163–166.
-
16.
Senga EL, Harper G, Koshy G, Kazembe PN, Brabin BJ, 2011. Reduced risk for placental malaria in iron deficient women. Malar J 10: 47.
-
17.
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: 1137–1144.
-
18.
Sangare L, van Eijk AM, Ter Kuile FO, Walson J, Stergachis A, 2014. The association between malaria and iron status or supplementation in pregnancy: a systematic review and meta-analysis. PLoS One 9: e87743.
-
19.
Sazawal S, Black RE, Ramsan M, Chwaya HM, Stoltzfus RJ, Dutta A, Dhingra U, Kabole I, Deb S, Othman MK, Kabole FM, 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: 133–143.
-
20.
Veenemans J, Milligan P, Prentice AM, Schouten LR, Inja N, van der Heijden AC, de Boer LC, Jansen EJ, Koopmans AE, Enthoven WT, Kraaijenhagen RJ, Demir AY, Uges DR, Mbugi EV, Savelkoul HF, Verhoef H, 2011. Effect of supplementation with zinc and other micronutrients on malaria in Tanzanian children: a randomised trial. PLoS Med 8: e1001125.
-
21.
Drakesmith H, Prentice AM, 2012. Hepcidin and the iron-infection axis. Science 338: 768–772.
-
22.
Kabyemela E, Goncalves BP, Prevots DR, Morrison R, Harrington W, Gwamaka M, Kurtis JD, Fried M, Duffy PE, 2013. Cytokine profiles at birth predict malaria severity during infancy. PLoS One 8: e77214.
-
23.
World Health Organization, Department of Nutrition for Health and Development, 2001. Iron Deficiency Anaemia: Assessment, Prevention and Control: A Guide for Programme Managers. Geneva, Switzerland: World Health Organization.
-
24.
Prentice AM, Doherty CP, Abrams SA, Cox SE, Atkinson SH, Verhoef H, Armitage AE, Drakesmith H, 2012. Hepcidin is the major predictor of erythrocyte iron incorporation in anemic African children. Blood 119: 1922–1928.
-
25.
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.
-
26.
Chong SS, Boehm CD, Higgs DR, Cutting GR, 2000. Single-tube multiplex-PCR screen for common deletional determinants of α-thalassemia. Blood 95: 360–362.
-
27.
Fibrinogen Studies Collaboration, Kaptoge S, White IR, Thompson SG, Wood AM, Lewington S, Lowe GD, Danesh J, 2007. Associations of plasma fibrinogen levels with established cardiovascular disease risk factors, inflammatory markers, and other characteristics: individual participant meta-analysis of 154,211 adults in 31 prospective studies: the Fibrinogen Studies Collaboration. Am J Epidemiol 166: 867–879.
-
28.
Easton DF, Peto J, Babiker AG, 1991. Floating absolute risk: an alternative to relative risk in survival and case-control analysis avoiding an arbitrary reference group. Stat Med 10: 1025–1035.
-
29.
Nweneka CV, Doherty CP, Cox S, Prentice A, 2010. Iron delocalisation in the pathogenesis of malarial anaemia. Trans R Soc Trop Med Hyg 104: 175–184.
-
30.
de Mast Q, Nadjm B, Reyburn H, Kemna EH, Amos B, Laarakkers CM, Silalye S, Verhoef H, Sauerwein RW, Swinkels DW, van der Ven AJ, 2009. Assessment of urinary concentrations of hepcidin provides novel insight into disturbances in iron homeostasis during malarial infection. J Infect Dis 199: 253–262.
-
31.
de Mast Q, Syafruddin D, Keijmel S, Riekerink TO, Deky O, Asih PB, Swinkels DW, van der Ven AJ, 2010. Increased serum hepcidin and alterations in blood iron parameters associated with asymptomatic P. falciparum and P. vivax malaria. Haematologica 95: 1068–1074.
-
32.
Howard CT, McKakpo US, Quakyi IA, Bosompem KM, Addison EA, Sun K, Sullivan D, Semba RD, 2007. Relationship of hepcidin with parasitemia and anemia among patients with uncomplicated Plasmodium falciparum malaria in Ghana. Am J Trop Med Hyg 77: 623–626.
-
33.
Casals-Pascual C, Huang H, Lakhal-Littleton S, Thezenas ML, Kai O, Newton CR, Roberts DJ, 2012. Hepcidin demonstrates a biphasic association with anemia in acute Plasmodium falciparum malaria. Haematologica 97: 1695–1698.
-
34.
Burte F, Brown BJ, Orimadegun AE, Ajetunmobi WA, Afolabi NK, Akinkunmi F, Kowobari O, Omokhodion S, Osinusi K, Akinbami FO, Shokunbi WA, Sodeinde O, Fernandez-Reyes D, 2013. Circulatory hepcidin is associated with the anti-inflammatory response but not with iron or anemic status in childhood malaria. Blood 121: 3016–3022.
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