The science and practice of micronutrient supplementations in nutritional anemia: An evidence-based review

Journal of Parenteral and Enteral Nutrition

Volumn 38, Issue 6, 2014, Pages 656-672

  Chan, Lingtak Neander ^a   Mike, Leigh Ann ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

adult life cycle; cobalamin; copper; folate; geriatrics life cycle; iron; minerals trace elements; nutrition anemia; nutrition vitamins; zinc

Indexed keywords

COBALAMIN; COPPER; FOLIC ACID; IRON; ZINC; CYANOCOBALAMIN; IRON INTAKE; TRACE ELEMENT;

ANEMIA; BIOAVAILABILITY; CLINICAL ASSESSMENT; CLINICAL PRACTICE; COBALAMIN DEFICIENCY; COPPER DEFICIENCY; DIET SUPPLEMENTATION; EVIDENCE BASED MEDICINE; FOLIC ACID DEFICIENCY; GASTROINTESTINAL TRACT; HEMOGLOBIN DETERMINATION; HOMEOSTASIS; HUMAN; INTESTINE ABSORPTION; IRON ABSORPTION; IRON DEFICIENCY ANEMIA; NUTRITIONAL ANEMIA; NUTRITIONAL ASSESSMENT; NUTRITIONAL DEFICIENCY; NUTRITIONAL SCIENCE; NUTRITIONAL STATUS; PATIENT MONITORING; PRIORITY JOURNAL; REVIEW; TREATMENT PLANNING; TREATMENT RESPONSE; TURNOVER TIME; ADMINISTRATION AND DOSAGE; BLOOD; DEFICIENCY; DRUG EFFECTS; IRON INTAKE; PHARMACOKINETICS;

ANEMIA; COPPER; DIETARY SUPPLEMENTS; EVIDENCE-BASED MEDICINE; FOLIC ACID; HUMANS; INTESTINAL ABSORPTION; IRON, DIETARY; MICRONUTRIENTS; VITAMIN B 12; ZINC;

EID: 84904509384     PISSN: 01486071     EISSN: 19412444     Source Type: Journal    
DOI: 10.1177/0148607114533726     Document Type: Review

References (132)

1. Butler CC, Vidal-Alaball J, Cannings-John R, et al. Oral vitamin B12 versus intramuscular vitamin B12 for vitamin B12 deficiency: a systematic review of randomized controlled trials. Fam Pract. 2006 ; 23: 279-285
2. Chen M, Krishnamurthy A, Mohamed AR, Green R. Hematological disorders following gastric bypass surgery: emerging concepts of the interplay between nutritional deficiency and inflammation. Biomed Res Int. 2013 ; 2013: 205467
3. Chung M, Balk EM, Ip S, et al Nutrition Research Series. Rockville, MD: Agency for Healthcare Research and Quality ; 2009 :
4. Knovich MA, Il'yasova D, Ivanova A, Molnár I. The association between serum copper and anaemia in the adult Second National Health and Nutrition Examination Survey (NHANES II) population. Br J Nutr. 2008 ; 99: 1226-1229
5. Lee TW, Kolber MR, Fedorak RN, van Zanten SV. Iron replacement therapy in inflammatory bowel disease patients with iron deficiency anemia: a systematic review and meta-analysis. J Crohns Colitis. 2012 ; 6: 267-275
6. Ruz M, Carrasco F, Rojas P, et al. Heme- and nonheme-iron absorption and iron status 12 mo after sleeve gastrectomy and Roux-en-Y gastric bypass in morbidly obese women. Am J Clin Nutr. 2012 ; 96: 810-817
7. Stabler SP. Vitamin B12 deficiency. N Engl J Med. 2013 ; 368: 149-160
8. Zhao N, Zhang AS, Enns CA. Iron regulation by hepcidin. J Clin Invest. 2013 ; 123: 2337-2343
9. Beutler E, Waalen J. The definition of anemia: what is the lower limit of normal of the blood hemoglobin concentration?. Blood. 2006 ; 107 (5). 1747-1750 (Pubitemid 43289347)
10. Nutritional Anaemias. Geneva, Switzerland: WHO ; 1968: 405.
11. World Health Organization. Haemoglobin concentrations for the diagnosis of anaemia and assessment of severity. http://www.who.int/vmnis/indicators/ haemoglobin.pdf. Accessed April 28, 2014.
12. Worldwide Prevalence of Anaemia 1993-2005. McLean E Cogswell M Egli I Wojdyla D de Benoist B, ed. WHO Global Database on Anaemia. Geneva, Switzerland: World Health Organization ; 2008 :
13. Guralnik J, Eisenstaedt R, Ferrucci L, et al. Prevalence of anemia in persons 65 years and older in the United States: evidence for a high rate of unexplained anemia. Blood. 2004 ; 104: 2263-2268 (Pubitemid 39331821)
14. World Health Organization. Vitamin and Mineral Nutrition Information System (VMNIS). http://who.int/vmnis/anaemia/data/database/countries/usa-ida. pdf. Accessed April 28, 2014.
15. Hodges VM, Rainey S, Lappin TR, Maxwell AP. Pathophysiology of anemia and erythrocytosis. Crit Rev Oncol Hematol. 2007 ; 64: 139-158 (Pubitemid 47488895)
16. Zheng J, Kitajima K, Sakai E, et al. Differential effects of GATA-1 on proliferation and differentiation of erythroid lineage cells. Blood. 2006 ; 107 (2). 520-527 (Pubitemid 43076374)
17. Cantor AB, Orkin SH. Transcriptional regulation of erythropoiesis: an affair involving multiple partners. Oncogene. 2002 ; 21 (21). 3368-3376 (Pubitemid 34587709)
18. Saleque S, Cameron S, Orkin SH. The zinc-finger proto-oncogene Gfi-1b is essential for development of the erythroid and megakaryocytic lineages. Genes Dev. 2002 ; 16 (3). 301-306 (Pubitemid 34111410)
19. Bustos RI, Jensen EL, Ruiz LM, et al. Copper deficiency alters cell bioenergetics and induces mitochondrial fusion through up-regulation of MFN2 and OPA1 in erythropoietic cells. Biochem Biophys Res Commun. 2013 ; 437 (3). 426-432
20. Sarkar J, Seshadri V, Tripoulas NA, Ketterer ME, Fox PL. Role of ceruloplasmin in macrophage iron efflux during hypoxia. J Biol Chem. 2003 ; 278 (45). 44018-44024 (Pubitemid 37377141)
21. Anderson GJ, Frazer DM, McKie AT, Vulpe CD. The ceruloplasmin homolog hephaestin and the control of intestinal iron absorption. Blood Cells Mol Dis. 2002 ; 29 (3). 367-375
22. Petrak J, Vyoral D. Hephaestin - a ferroxidase of cellular iron export. Int J Biochem Cell Biol. 2005 ; 37 (6). 1173-1178 (Pubitemid 40381194)
23. Power HJ. Riboflavin (vitamin B-2) and health. Am J Clin Nutr. 2003 ; 77 (6). 1352-1360
24. Ajayi OA, Okike OC, Yusuf Y. Haematological response to supplements of riboflavin and ascorbic acid in Nigerian young adults. Eur J Haematol. 1990 ; 44 (4). 209-212 (Pubitemid 20203061)
25. Semba RD, Ferrucci L, Cappola AR, et al. Low serum selenium is associated with anemia among older women living in the community: the Women's Health and Aging Studies I and II. Biol Trace Elem Res. 2006 ; 112 (2). 97-107
26. Semba RD, Ricks MO, Ferrucci L, Xue QL, Guralnik JM, Fried LP. Low serum selenium is associated with anemia among older adults in the United States. Eur J Clin Nutr. 2009 ; 63 (1). 93-99
27. Roy CN, Semba RD, Sun K, et al. Circulating selenium and carboxymethyl-lysine, an advanced glycation endproduct, are independent predictors of anemia in older community-dwelling adults. Nutrition. 2012 ; 28 (7-8). 762-766
28. Koury MJ, Rhodes M. How to approach chronic anemia. Hematol Am Soc Hematol Educ Prog. 2012 ; 2012: 183-190
29. Pang WW, Schrier SL. Anemia in the elderly. Curr Opin Hematol. 2012 ; 19 (3). 133-140
30. Cullis J. Anaemia of chronic disease. Clin Med. 2013 ; 13 (2). 193-196
31. Andrews NC. Disorders of iron metabolism. N Engl J Med. 1999 ; 341: 1986-1995 (Pubitemid 30010408)
32. Blachier F, Vaugelade P, Robert V, et al. Comparative capacities of the pig colon and duodenum for luminal iron absorption. Can J Physiol Pharmacol. 2007 ; 85 (2). 185-192 (Pubitemid 46846429)
33. Geisser P, Burckhardt S. The pharmacokinetics and pharmacodynamics of iron preparation. Pharmaceutics. 2011 ; 3: 12-33
34. von Drygalski A, Andris DA. Anemia after bariatric surgery: more than just iron deficiency. Nutr Clin Pract. 2009 ; 24 (2). 217-226
35. Thankachan P, Walczyk T, Muthayya S, Kurpad AV, Hurrell RF. Iron absorption in young Indian women: the interaction of iron status with the influence of tea and ascorbic acid. Am J Clin Nutr. 2008 ; 87 (4). 881-886 (Pubitemid 351549232)
36. Thankachan P, Kalasuramath S, Hill AL, Thomas T, Bhat K, Kurpad AV. A mathematical model for the hemoglobin response to iron intake, based on iron absorption measurements from habitually consumed Indian meals. Eur J Clin Nutr. 2012 ; 66: 481-487
37. Taylor P, Martínez-Torres C, Leets I, Ramirez J, Garcia-Casal MN, Layrisse M. Relationships among iron absorption, percent saturation of plasma transferrin and serum ferritin concentration in humans. J Nutr. 1988 ; 118: 1110-1115
38. Thurnham DI. Interactions between nutrition and immune function: using inflammation biomarkers to interpret micronutrient status. Proc Nutr Soc. 2014 ; 73 (1). 1-8
39. Goddard AF, James MW, McIntyre AS, Scott BB. Guidelines for the management of iron deficiency anaemia. Gut. 2011 ; 60 (10). 1309-1316
40. Beshara S, Lundqvist H, Sundin J, et al. Pharmacokinetics and red cell utilization of iron(III)-hydroxidesucrose complex in anaemic patients: a study using positron emission tomography. Br J Haematol. 1999 ; 104: 296-302 (Pubitemid 29083337)
41. Casgrain A, Collings R, Harvey LJ, Hooper L, Fairweather-Tait SJ. Effect of iron intake on iron status: a systematic review and meta-analysis of randomized controlled trials. Am J Clin Nutr. 2012 ; 96 (4). 768-780
42. Bernhart FE, Skeggs L. The iron content of crystalline human hemoglobin. J Biol Chem. 1943 ; 147: 19-22
43. Charoenlarp P, Dhanamitta S, Kaewvichit R, et al. A WHO collaborative study on iron supplementation in Burma and in Thailand. Am J Clin Nutr. 1988 ; 47 (2). 280-297 (Pubitemid 18091578)
44. Fogelholm M, Suominen M, Rita H. Effects of low-dose iron supplementation in women with low serum ferritin concentration. Eur J Clin Nutr. 1994 ; 48 (10). 753-756 (Pubitemid 24315322)
45. Fernández-Gaxiola AC, De-Regil LM. Intermittent iron supplementation for reducing anaemia and its associated impairments in menstruating women. Cochrane Database Syst Rev. 2011 ; (12). CD009218
46. Gilgen D, Mascie-Taylor CG. The effect of weekly iron supplementation on anaemia and on iron deficiency among female tea pluckers in Bangladesh. J Hum Nutr Diet. 2001 ; 14: 185-190 (Pubitemid 32536822)
47. Petry N, Egli I, Zeder C, Walczyk T, Hurrell R. Polyphenols and phytic acid contribute to the low iron bioavailability from common beans in young women. J Nutr. 2010 ; 140 (11). 1977-1982
48. Hurrell R, Egli I. Iron bioavailability and dietary reference values. Am J Clin Nutr. 2010 ; 91 (5). 1461S - 1467S
49. Motoya T, Miyashita M, Kawachi A, Yamada K. Effects of ascorbic acid on interactions between ciprofloxacin and ferrous sulphate, sodium ferrous citrate or ferric pyrophosphate, in mice. J Pharm Pharmacol. 2000 ; 52 (4). 397-401 (Pubitemid 30223681)
50. Troesch B, Egli I, Zeder C, Hurrell RF, Zimmermann MB. Fortification iron as ferrous sulfate plus ascorbic acid is more rapidly absorbed than as sodium iron EDTA but neither increases serum nontransferrin-bound iron in women. J Nutr. 2011 ; 141: 822-827
51. Mehdad A, Siqueira EM, Arruda SF. Effect of vitamin A deficiency on iron bioavailability. Ann Nutr Metab. 2010 ; 57: 35-39
52. Michelazzo FB, Oliveira JM, Stefanello J, Luzia LA, Rondó PH. The influence of vitamin A supplementation on iron status. Nutrients. 2013 ; 5: 4399-4413
53. Thomas CE, Gaffney-Stomberg E, Sun BH, O'Brien KO, Kerstetter JE, Insogna KL. Increasing dietary protein acutely augments intestinal iron transporter expression and significantly increases iron absorption in rats. FASEB J. 2013 ; 27: 2476-2483
54. Recommendations to prevent and control iron deficiency in the United States. MMWR Recomm Rep. 1998 ; 47: 1-29
55. Gomollón F, Gisbert JP. Current management of iron deficiency anemia in inflammatory bowel diseases: a practical guide. Drugs. 2013 ; 73 (16). 1761-1770
56. Rimon E, Kagansky N, Kagansky M, et al. Are we giving too much iron? Low-dose iron therapy is effective in octogenarians. Am J Med. 2005 ; 118 (10). 1142-1147 (Pubitemid 41363767)
57. Stabler SP. Vitamin B12 deficiency. N Engl J Med. 2013 ; 368: 149-160
58. Scott JM. Folate and vitamin B12. Proc Nutr Soc. 1999 ; 58: 441-448
59. Doets EL, In 't, Veld PH, Szczecińska A, et al. Systematic review on daily vitamin B12 losses and bioavailability for deriving recommendations on vitamin B12 intake with the factorial approach. Ann Nutr Metab. 2013 ; 62 (4). 311-322
60. Bose S, Kalra S, Yammani RR, Ahuja R, Seetharam B. Plasma membrane delivery, endocytosis and turnover of transcobalamin receptor in polarized human intestinal epithelial cells. J Physiol. 2007 ; 581 (pt 2). 457-466 (Pubitemid 46831749)
61. Seetharam B, Yammani RR. Cobalamin transport proteins and their cell-surface receptors. Expert Rev Mol Med. 2003 ; 5 (18). 1-18
62. Heyssel RM, Bozian RC, Darby WJ, Bell MC. Vitamin B12 turnover in man: the assimilation of vitamin B12 from natural foodstuff by man and estimates of minimal daily requirements. Am J Clin Nutr. 1966 ; 18: 176-184
63. Carmel R Modern Nutrition in Health and Disease. 12 ). In: RossACCaballeroBCousinsRJTuckerKIZieglerTB, eds. Modern Nutrition in Health and Disease. 11th ed.Philadelphia, PA: Lippincott Williams & Wilkins; 2014:369-389. Ross AC Caballero B Cousins RJ Tucker KI Ziegler TB, ed. Philadelphia, PA: Lippincott Williams & Wilkins ; 369-389.
64. Berlin H, Berlin R, Brante G. Oral treatment of pernicious anemia with high doses of vitamin B12 without intrinsic factor. Acta Med Scand. 1968 ; 184 (4). 247-258
65. Berlin R, Berlin H, Brante G, Pilbrant A. Vitamin B12 body stores during oral and parenteral treatment of pernicious anaemia. Acta Med Scand. 1978 ; 204 (1-2). 81-84 (Pubitemid 8406949)
66. Savage DG, Lindenbaum J, Stabler SP, Allen RH. Sensitivity of serum methylmalonic acid and total homocysteine determinations for diagnosing cobalamin and folate deficiencies. Am J Med. 1994 ; 96: 239-246 (Pubitemid 24099223)
67. Lindenbaum J, Healton EB, Savage DG, et al. Neuropsychiatric disorders cause by cobalamin deficiency in the absence of anemia or macrocytosis. N Engl J Med. 1988 ; 318: 1720-1728
68. Carmel R. Biomarkers of cobalamin (vitamin B-12) status in the epidemiologic setting: a critical overview of context, applications, and performance characteristics of cobalamin, methylmalonic acid, and holotranscobalamin II. Am J Clin Nutr. 2011 ; 94 (1). 348S - 358S
69. Carmel R. Diagnosis and management of clinical and subclinical cobalamin deficiencies: why controversies persist in the age of sensitive metabolic testing. Biochimie. 2013 ; 95: 1047-1055
70. Delpre G, Stark P, Niv Y. Sublingual therapy for cobalamin deficiency as an alternative to oral and parenteral cobalamin supplementation. Lancet. 1999 ; 354: 740-741 (Pubitemid 29405791)
71. Bodamer OAF, Scaglia F. Sublingual therapy for cobalamin deficiency. Lancet. 1999 1562 ; 354 :
72. Sharabi A, Cohen E, Sulkes J, Garty M. Replacement therapy for vitamin B12 deficiency: comparison between the sublingual and oral route. Br J Clin Pharmacol. 2003 ; 56: 635-638 (Pubitemid 37491715)
73. Solomon LR. Disorders of cobalamin (vitamin B12) metabolism: emerging concepts in pathophysiology, diagnosis and treatment. Blood Rev. 2007 ; 21 (3). 113-130 (Pubitemid 46529054)
74. Andrès E, Dali-Youcef N, Vogel T, Serraj K, Zimmer J. Oral cobalamin (vitamin B(12)) treatment: an update. Int J Lab Hematol. 2009 ; 31 (1). 1-8
75. Andrès E, Fothergill H, Mecili M. Efficacy of oral cobalamin (vitamin B12) therapy. Expert Opin Pharmacother. 2010 ; 11 (2). 249-256
76. Rhode BM, Arseneau P, Cooper BA, Katz M, Gilfix BM, MacLean LD. Vitamin B-12 deficiency after gastric surgery for obesity. Am J Clin Nutr. 1996 ; 63 (1). 103-109 (Pubitemid 26005733)
77. Spring Valley, NY: Par Pharmaceutical Companies, Inc ; 2011 :
78. Zhao R, Matherly LH, Goldman ID. Membrane transporters and folate homeostasis: intestinal absorption and transport into systemic compartments and tissues. Expert Rev Mol Med. 2009 ; 11: e4
79. Koury MJ, Ponka P. New insights into erythropoiesis: the roles of folate, vitamin B12, and iron. Annu Rev Nutr. 2004 ; 24: 105-131 (Pubitemid 38938788)
80. Hoppner K, Lampi B. Folate levels in human liver from autopsies in Canada. Am J Clin Nutr. 1980 ; 33: 862-864 (Pubitemid 10077675)
81. Stites TE, Bailey LB, Scott KC, Toth JP, Fisher WP, Gregory JF. Kinetic modeling of folate metabolism through use of chronic administration of deuterium-labeled folic acid in men. Am J Clin Nutr. 1997 ; 65 (1). 53-60 (Pubitemid 27020459)
82. Dietary Reference Intakes for Thiamin, Riboflavin, Niacin, Vitamin B6, Folate, Vitamin B12, Pantothenic Acid, Biotin and Choline. Washington, DC: National Academies Press ; 1998 :
83. Zhao R, Goldman ID. Folate and thiamine transporters mediated by facilitative carriers (SLC19A1-3 and SLC46A1) and folate receptors. Mol Aspects Med. 2013 ; 34: 373-385
84. Maki KC, Ndife LI, Kelley KM, et al. Absorption of folic acid from a softgel capsule compared to a standard tablet. J Acad Nutr Diet. 2012 ; 112 (7). 1062-1067
85. Bailey RL, Mills JL, Yetley EA, et al. Unmetabolized serum folic acid and its relation to folic acid intake from diet and supplements in a nationally representative sample of adults aged ≥60 years in the United States. Am J Clin Nutr. 2010 ; 92: 383-389
86. Carter B, Monsivais P, Drewnowski A. Absorption of folic acid and ascorbic acid from nutrient comparable beverages. J Food Sci. 2010 ; 75 (9). H289 - H293
87. Wu A, Chanarin I, Slavin G, Levi AJ. Folate deficiency in the alcoholic - its relationship to clinical and haematological abnormalities, liver disease and folate stores. Br J Haematol. 1975 ; 29 (3). 469-478
88. Butterworth CE, Tamura T. Folic acid safety and toxicity: a brief review. Am J Clin Nutr. 1989 ; 50: 353-358 (Pubitemid 19208755)
89. Joseph B, Ramesh N. Weekly dose of iron-folate supplementation with vitamin-C in the workplace can prevent anaemia in women employees. Pak J Med Sci. 2013 ; 29 (1). 47-52
90. Robscheit-Robbins FS, Whipple GH. Copper and cobalt-related hemoglobin production in experimental anemia. J Exp Med. 1942 ; 75 (5). 481-487
91. Guggenheim K. The role of zinc, copper and calcium in the etiology of the "meat anemia.". Blood. 1964: 786-794
92. Cartwright GE, Wintrobe MM. The question of copper deficiency in man. Am J Clin Nutr. 1964 ; 15: 94-110
93. Butterworth CE, Gubler CJ, Cartwright GE, Wintrobe MM. Studies on copper metabolism, XXVI: plasma copper in patients with tropical sprue. Proc Soc Exper Biol Med. 1958 ; 98: 594
94. Halfdanarson TR, Kumar N, Li CY, Phyliky RL, Hogan WJ. Hematological manifestations of copper deficiency: a retrospective review. Eur J Haematol. 2008 ; 80 (6). 523-531 (Pubitemid 351677455)
95. Gletsu-Miller N, Broderius M, Frediani JK, et al. Incidence and prevalence of copper deficiency following roux-en-y gastric bypass surgery. Int J Obes (Lond). 2012 ; 36 (3). 328-335
96. Griffith DP, Liff DA, Ziegler TR, Esper GJ, Winton EF. Acquired copper deficiency: a potentially serious and preventable complication following gastric bypass surgery. Obesity (Silver Spring). 2009 ; 17 (4). 827-831
97. Vulpe CD, Kuo YM, Murphy TL, et al. Hephaestin, a ceruloplasmin homologue implicated in intestinal iron transport, is defective in the sla mouse. Nat Genet. 1999 ; 21 (2). 195-199 (Pubitemid 29070366)
98. Prohaska JR. Impact of copper limitation on expression and function of multicopper oxidases (ferroxidases). Adv Nutr. 2011 ; 2 (2). 89-95
99. Collins JF Modern Nutrition in Health and Disease. 11 th ed.Philadelphia, PA: Lippincott Williams & Wilkins; 2014:206-216. Ross AC Caballero B Cousins RJ Tucker KI Ziegler TB, ed. Philadelphia, PA: Lippincott Williams & Wilkins ; 206-216.
100. Wapnir RA. Copper absorption and bioavailability. Am J Clin Nutr. 1998 ; 67: 1054S - 1060S (Pubitemid 28198832)
101. Turnlund JR, Keyes WR, Anderson HL, Acord LL. Copper absorption and retention in young men at three levels of dietary copper by use of the stable isotope 65Cu. Am J Clin Nutr. 1989 ; 49: 870-878 (Pubitemid 19139791)
102. Crisponia G, Nurchia VM, Fanni D, Gerosa C, Nemolato S, Faa G. Copper-related diseases: from chemistry to molecular pathology. Coordination Chem Rev. 2010 ; 254: 876-889
103. Rowin J, Lewis SL. Copper deficiency myeloneuropathy and pancytopenia secondary to overuse of zinc supplementation. J Neurol Neurosurg Psychiatry. 2005 ; 76 (5). 750-751 (Pubitemid 40569695)
104. Greger JL, Snedeker SM. Effect of dietary protein and phosphorus levels on the utilization of zinc, copper and manganese by adult males. J Nutr. 1980 ; 110: 2243-2253 (Pubitemid 11172684)
105. Harvey LJ, McArdle HJ. Biomarkers of copper status: a brief update. Br J Nutr. 2008 ; 99: S10 - S13
106. Gabreyes AA, Abbasi HN, Forbes KP, McQuaker G, Duncan A, Morrison I. Hypocupremia associated cytopenia and myelopathy: a national retrospective review. Eur J Haematol. 2013 ; 90 (1). 1-9
107. Bo S, Durazzo M, Gambino R, et al. Associations of dietary and serum copper with inflammation, oxidative stress, and metabolic variables in adults. J Nutr. 2008 ; 138: 305-310 (Pubitemid 351213644)
108. Malek F, Jiresova E, Dohnalova A, Koprivova H, Spacek R. Serum copper as a marker of inflammation in prediction of short term outcome in high risk patients with chronic heart failure. Int J Cardiol. 2006 ; 113 (2). e51 - e53
109. Mirastschijski U, Martin A, Jorgensen LN, Sampson B, Ågren MS. Zinc, copper, and selenium tissue levels and their relation to subcutaneous abscess, minor surgery, and wound healing in humans. Biol Trace Elem Res. 2013 ; 153 (1-3). 76-83
110. Bui VQ, Stein AD, DiGirolamo AM, et al. Associations between serum C-reactive protein and serum zinc, ferritin, and copper in Guatemalan school children. Biol Trace Elem Res. 2012 ; 148 (2). 154-160
111. Oakes EJ, Lyon TD, Duncan A, Gray A, Talwar D, O'Reilly DS. Acute inflammatory response does not affect erythrocyte concentrations of copper, zinc and selenium. Clin Nutr. 2008 ; 27 (1). 115-120 (Pubitemid 351201858)
112. Btaiche IF, Yeh AY, Wu IJ, Khalidi N. Neurological dysfunction and pancytopenia secondary to acquired copper deficiency following duodenal switch: case report and review of the literature. Nutr Clin Pract. 2011 ; 26: 583-592
113. Hayton BA, Broome HE, Lilenbaum RC. Copper deficiency-induced anemia and neutropenia secondary to intestinal malabsorption. Am J Hematol. 1995 ; 48: 45-47
114. Schleper B, Stuerenburg HJ. Copper deficiency-associated myelopathy in a 46-year-old woman. J Neurol. 2001 ; 248 (8). 705-706 (Pubitemid 32695869)
115. Choi ER, Strum W. Hypocupremia-related myeloneuropathy following gastrojejunal bypass surgery. Ann Nutr Metab. 2010 ; 57: 190-192
116. King JC, Cousins RJ Modern Nutrition in Health and Disease. 11 th ed.Philadelphia, PA: Lippincott Williams & Wilkins; 2014:189-205. Ross AC Caballero B Cousins RJ Tucker KI Ziegler TB, ed. Philadelphia, PA: Lippincott Williams & Wilkins ; 189-205.
117. King JC. Zinc: an essential but elusive nutrient. Am J Clin Nutr. 2011 ; 94 (2). 679S - 684S
118. Chasapis CT, Loutsidou AC, Spiliopoulou CA, Stefanidou ME. Zinc and human health: an update. Arch Toxicol. 2012 ; 86 (4). 521-534
119. Roohani N, Hurrell R, Kelishadi R, Schulin R. Zinc and its importance for human health: an integrative review. J Res Med Sci. 2013 ; 18 (2). 144-157
120. Hinks LJ, Clayton BE, Lloyd RS. Zinc and copper concentrations in leucocytes and erythrocytes in healthy adults and the effect of oral contraceptives. J Clin Pathol. 1983 ; 36 (9). 1016-1021 (Pubitemid 13042035)
121. Naber TH, van den Hamer CJ, van den Broek WJ, Roelofs H. Zinc exchange by blood cells in nearly physiologic standard conditions. Biol Trace Elem Res. 1994 ; 46: 29-50 (Pubitemid 24381964)
122. Lichten LA, Cousins RJ. Mammalian zinc transporters: nutritional and physiologic regulation. Annu Rev Nutr. 2009 ; 29: 153-176
123. Wang X, Zhou B. Dietary zinc absorption: a play of Zips and ZnTs in the gut. IUBMB Life. 2010 ; 62 (3). 176-182
124. Cousins RJ. Gastrointestinal factors influencing zinc absorption and homeostasis. Int J Vitam Nutr Res. 2010 ; 80 (4-5). 243-248
125. Ghayour-Mobarhan M, Taylor A, New SA, Lamb DJ, Ferns GA. Determinants of serum copper, zinc and selenium in healthy subjects. Ann Clin Biochem. 2005 ; 42 (pt 5). 364-375 (Pubitemid 41354398)
126. Duggan C, MacLeod WB, Krebs NF, et al. Plasma zinc concentrations are depressed during the acute phase response in children with falciparum malaria. J Nutr. 2005 ; 135 (4). 802-807 (Pubitemid 40464108)
127. Chan L-N, Sethi P, Mike LA, Lee JK, Farver KL, Reilly DF. Comparison of clinical characteristics and outcomes in medically ill ICU (MICU) patients according to serum zinc profile on admission [abstract]. JPEN J Parenter Enteral Nutr. 2008 ; 32 (3). 308
128. Henderson LM, Brewer GJ, Dressman JB, et al. Use of zinc tolerance test and 24-hour urinary zinc content to assess oral zinc absorption. J Am Coll Nutr. 1996 ; 15 (1). 79-83 (Pubitemid 26042478)
129. Sieniawska CE, Jung LC, Olufadi R, Walker V. Twenty-four-hour urinary trace element excretion: reference intervals and interpretive issues. Ann Clin Biochem. 2012 ; 49 (pt 4). 341-351
130. Meadows NJ, Grainger SL, Ruse W, Keeling PWN, Thompson RPH. Oral iron and the bioavailability of zinc. BMJ. 1983 ; 287: 1013-1014 (Pubitemid 13009244)
131. Solomon NW, Jacob RA. Studies on the bioavailability of zinc in humans: effect of heme and nonheme iron on the absorption of zinc. Am J Clin Nutr. 1981 ; 34: 475-482 (Pubitemid 11068263)
132. Lee TW, Kolber MR, Fedorak RN, van Zanten SV. Iron replacement therapy in inflammatory bowel disease patients with iron deficiency anemia: a systematic review and meta-analysis. J Crohns Colitis. 2012 ; 6: 267-275