Trace element status in hemodialysis patients

Seminars in Dialysis

Volumn 23, Issue 4, 2010, Pages 389-395

  Rucker, Diana ^a   Thadhani, Ravi ^b   Tonelli, Marcello ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIALYSIS FLUID; TRACE ELEMENT;

CHEMISTRY; CHRONIC KIDNEY FAILURE; HUMAN; METABOLISM; RENAL REPLACEMENT THERAPY; REVIEW; RISK FACTOR;

DIALYSIS SOLUTIONS; HUMANS; KIDNEY FAILURE, CHRONIC; RENAL DIALYSIS; RISK FACTORS; TRACE ELEMENTS;

EID: 77955246054     PISSN: 08940959     EISSN: 1525139X     Source Type: Journal    
DOI: 10.1111/j.1525-139X.2010.00746.x     Document Type: Review

References (132)

1. Chan S, Gerson B, Reitz RE, Sadjadi SA. Technical and clinical aspects of spectrometric analysis of trace elements in clinical samples. Clin Lab Med 1998, 18:615-629.
2. Alfrey AC. Dialysis encephalopathy syndrome. Annu Rev Med 1978, 29:93-98.
3. Alfrey AC, LeGendre GR, Kaehny WD. The dialysis encephalopathy syndrome. Possible aluminum intoxication. N Engl J Med 1976, 294:184-188.
4. Altmann P, Al-Salihi F, Butter K. Serum aluminum levels and erythrocyte dihydropteridine reductase activity in patients on hemodialysis. N Engl J Med 1987, 317:80-84.
5. Kerr DN, Ward MK, Ellis HA, Simpson W, Parkinson IS. Aluminium intoxication in renal disease. Ciba Found Symp 1992, 169:123-135. discussion 35-41
6. Wills MR, Savory J. Aluminum and chronic renal failure: sources, absorption, transport, and toxicity. Crit Rev Clin Lab Sci 1989, 27:59-107.
7. D'Haese PC, De Broe ME. Adequacy of dialysis: trace elements in dialysis fluids. Nephrol Dial Transplant 1996, 11(Suppl. 2):92-97.
8. Zima T, Mestek O, Nemecek K. Trace elements in hemodialysis and continuous ambulatory peritoneal dialysis patients. Blood Purif 1998, 16:253-260.
9. Zima T, Tesar V, Mestek O, Nemecek K. Trace elements in end-stage renal disease. 2. Clinical implication of trace elements. Blood Purif 1999, 17:187-198.
10. Tonelli M, Wiebe N, Hemmelgarn B. Trace elements in hemodialysis patients: a systematic review and meta-analysis. BMC Med 2009, 7:25.
11. Shrimpton R, Gross R, Hill I, Young M. Zinc deficiency: what are the most appropriate interventions? BMJ 2005, 330:347-349.
12. Dvornik S, Cuk M, Racki S, Zaputovic L. Serum zinc concentrations in the maintenance hemodialysis patients. Coll Antropol 2006, 30:125-129.
13. Foote JW, Hinks LJ. Zinc absorption in haemodialysis patients. Ann Clin Biochem 1988, 25(Pt 4):398-402.
14. Briefel RR, Bialostosky K, Kennedy-Stephenson J, McDowell MA, Ervin RB, Wright JD. Zinc intake of the U.S. population: findings from the third National Health and Nutrition Examination Survey, 1988-1994. J Nutr 2000, 130:1367S-1373S.
15. King JC. Assessment of techniques for determining human zinc requirements. J Am Diet Assoc 1986, 86:1523-1528.
16. Weigand E. Absorption of trace elements: zinc. Int J Vitam Nutr Res Suppl 1983, 25:67-81.
17. Cousins R. Present Knowledge in Nutrition 1996, Washington, DC, ILSI Press
18. Hambidge K, Casey C, Krebs N. Zinc in trace elements. Human and Animal Nutrition 1986, 1. Mertz W, ed, 5th edn, Orlando, Academic Press
19. Hambidge KM, Krebs NF. Zinc deficiency: a special challenge. J Nutr 2007, 137:1101-1105.
20. Prasad AS. Clinical, endocrinological and biochemical effects of zinc deficiency. Clin Endocrinol Metab 1985, 14:567-589.
21. Mahajan SK, Abbasi AA, Prasad AS, Rabbani P, Briggs WA, McDonald FD. Effect of oral zinc therapy on gonadal function in hemodialysis patients. A double-blind study. Ann Intern Med 1982, 97:357-361.
22. Kay RG, Tasman-Jones C. Acute zinc deficency in man during intravenous alimentation. Aust N Z J Surg 1975, 45:325-330.
23. Prasad AS. Zinc in growth and development and spectrum of human zinc deficiency. J Am Coll Nutr 1988, 7:377-384.
24. Rink L, Gabriel P. Zinc and the immune system. Proc Nutr Soc 2000, 59:541-552.
25. Shankar AH, Prasad AS. Zinc and immune function: the biological basis of altered resistance to infection. Am J Clin Nutr 1998, 68:447S-463S.
26. Halliwell B. Ascorbic acid, iron overload, and desferrioxamine. Br Med J (Clin Res Ed) 1982, 285:296.
27. Markovits PM, Sankey AW, James DK, McCabe R, Mahomed K, Golding J. Zinc taste test and postnatal depression. Br J Psychiatry 1990, 156:451-452.
28. Ortega RM, Requejo AM, Andres P. Dietary intake and cognitive function in a group of elderly people. Am J Clin Nutr 1997, 66:803-809.
29. Sandstead HH, Penland JG, Alcock NW. Effects of repletion with zinc and other micronutrients on neuropsychologic performance and growth of Chinese children. Am J Clin Nutr 1998, 68:470S-475S.
30. Okuyama S, Mishina H, Hasegawa K, Nakano N, Ise K. Probable atherogenic role of zinc and copper as studied in chronic hemodialysis patients. Tohoku J Exp Med 1982, 138:227-229.
31. Fang YZ, Yang S, Wu G. Free radicals, antioxidants, and nutrition. Nutrition 2002, 18:872-879.
32. Powell SR. The antioxidant properties of zinc. J Nutr 2000, 130:1447S-1454S.
33. Prasad AS, Cossack ZT. Zinc supplementation and growth in sickle cell disease. Ann Intern Med 1984, 100:367-371.
34. Wood RJ. Assessment of marginal zinc status in humans. J Nutr 2000, 130:1350S-1354S.
35. Subar AF, Krebs-Smith SM, Cook A, Kahle LL. Dietary sources of nutrients among US children, 1989-1991. Pediatrics 1998, 102:913-923.
36. Bobat R, Coovadia H, Stephen C. Safety and efficacy of zinc supplementation for children with HIV-1 infection in South Africa: a randomised double-blind placebo-controlled trial. Lancet 2005, 366:1862-1867.
37. Field CJ, Johnson IR, Schley PD. Nutrients and their role in host resistance to infection. J Leukoc Biol 2002, 71:16-32.
38. Girodon F, Galan P, Monget AL. Impact of trace elements and vitamin supplementation on immunity and infections in institutionalized elderly patients: a randomized controlled trial. MIN. VIT. AOX. geriatric network. Arch Intern Med 1999, 159:748-754.
39. McElroy BH, Miller SP. An open-label, single-center, phase IV clinical study of the effectiveness of zinc gluconate glycine lozenges (Cold-Eeze) in reducing the duration and symptoms of the common cold in school-aged subjects. Am J Ther 2003, 10:324-329.
40. Prasad AS, Fitzgerald JT, Bao B, Beck FW, Chandrasekar PH. Duration of symptoms and plasma cytokine levels in patients with the common cold treated with zinc acetate. A randomized, double-blind, placebo-controlled trial. Ann Intern Med 2000, 133:245-252.
41. Antoniou LD, Shalhoub RJ, Schechter GP. The effect of zinc on cellular immunity in chronic uremia. Am J Clin Nutr 1981, 34:1912-1917.
42. Skarupskiene I, Kuzminskis V, Abdrachmanovas O, Ryselis S, Smalinskiene A. Zinc and aluminum concentrations in blood of hemodialysis patients and its impact on the frequency of infections. Medicina (Kaunas) 2005, 41(Suppl. 1):65-68.
43. Burk RF, Levander OA, Shils ME. Selenium. Modern Nutrition in Health and Disease 2005, 312-323. Shils ME, Shike M, eds, Philadelphia, Lippincott Williams and Wilkins
44. Levander O, Burk R. Selenium. Present Knowledge in Nutrition 1996, 320. Ziegler E, Filer LJ. eds, Washington, DC, ILSI Press
45. Burk RF. Selenium in nutrition. World Rev Nutr Diet 1978, 30:88-106.
46. Ge K, Xue A, Bai J, Wang S. Keshan disease-an endemic cardiomyopathy in China. Virchows Arch A Pathol Anat Histopathol 1983, 401:1-15.
47. Moore JA, Noiva R, Wells IC. Selenium concentrations in plasma of patients with arteriographically defined coronary atherosclerosis. Clin Chem 1984, 30:1171-1173.
48. Salonen JT, Alfthan G, Huttunen JK, Pikkarainen J, Puska P. Association between cardiovascular death and myocardial infarction and serum selenium in a matched-pair longitudinal study. Lancet 1982, 2:175-179.
49. Suadicani P, Hein HO, Gyntelberg F. Serum selenium concentration and risk of ischaemic heart disease in a prospective cohort study of 3000 males. Atherosclerosis 1992, 96:33-42.
50. Salvini S, Hennekens CH, Morris JS, Willett WC, Stampfer MJ. Plasma levels of the antioxidant selenium and risk of myocardial infarction among U.S. physicians. Am J Cardiol 1995, 76:1218-1221.
51. Klotz LO, Kroncke KD, Buchczyk DP, Sies H. Role of copper, zinc, selenium and tellurium in the cellular defense against oxidative and nitrosative stress. J Nutr 2003, 133:1448S-1451S.
52. Rayman MP. The argument for increasing selenium intake. Proc Nutr Soc 2002, 61:203-215.
53. Stenvinkel P. Interactions between inflammation, oxidative stress, and endothelial dysfunction in end-stage renal disease. J Ren Nutr 2003, 13:144-148.
54. Ward RA, McLeish KR. Oxidant stress in hemodialysis patients: what are the determining factors? Artif Organs 2003, 27:230-236.
55. Hays GL, Bullock Q, Lazzari EP, Puente ES. Salivary pH while dissolving vitamin C-containing tablets. Am J Dent 1992, 5:269-271.
56. Girelli D, Olivieri O, Stanzial AM. Low platelet glutathione peroxidase activity and serum selenium concentration in patients with chronic renal failure: relations to dialysis treatments, diet and cardiovascular complications. Clin Sci (Lond) 1993, 84:611-617.
57. Hampel G, Schaller KH, Rosenmuller M, Oefele C. Selenium-deficiency as contributing factor to anemia and thrombocytopenia in dialysis patients. Life Support Syst 1985, 3(Suppl. 1):36-40.
58. Longnecker MP, Taylor PR, Levander OA. Selenium in diet, blood, and toenails in relation to human health in a seleniferous area. Am J Clin Nutr 1991, 53:1288-1294.
59. Rayman MP. The importance of selenium to human health. Lancet 2000, 356:233-241.
60. Yang GQ, Wang SZ, Zhou RH, Sun SZ. Endemic selenium intoxication of humans in China. Am J Clin Nutr 1983, 37:872-881.
61. Laclaustra M, Navas-Acien A, Stranges S, Ordovas JM, Guallar E. Serum selenium concentrations and diabetes in U.S. adults: National Health and Nutrition Examination Survey (NHANES) 2003-2004. Environ Health Perspect 2009, 117:1409-1413.
62. Lippman SM, Klein EA, Goodman PJ. Effect of selenium and vitamin E on risk of prostate cancer and other cancers: the Selenium and Vitamin E Cancer Prevention Trial (SELECT). JAMA 2009, 301:39-51.
63. Duffield-Lillico AJ, Reid ME, Turnbull BW. Baseline characteristics and the effect of selenium supplementation on cancer incidence in a randomized clinical trial: a summary report of the Nutritional Prevention of Cancer Trial. Cancer Epidemiol Biomarkers Prev 2002, 11:630-639.
64. Aschner JL, Aschner M. Nutritional aspects of manganese homeostasis. Mol Aspects Med 2005, 26:353-362.
65. Greger JL. Nutrition versus toxicology of manganese in humans: evaluation of potential biomarkers. Neurotoxicology 1999, 20:205-212.
66. Faraci FM, Didion SP. Vascular protection: superoxide dismutase isoforms in the vessel wall. Arterioscler Thromb Vasc Biol 2004, 24:1367-1373.
67. Horsburgh MJ, Wharton SJ, Karavolos M, Foster SJ. Manganese: elemental defence for a life with oxygen. Trends Microbiol 2002, 10:496-501.
68. Kinnula VL, Crapo JD. Superoxide dismutases in the lung and human lung diseases. Am J Respir Crit Care Med 2003, 167:1600-1619.
69. Paynter DI. Changes in activity of the manganese superoxide dismutase enzyme in tissues of the rat with changes in dietary manganese. J Nutr 1980, 110:437-447.
70. Himmelfarb J. Linking oxidative stress and inflammation in kidney disease: which is the chicken and which is the egg? Semin Dial 2004, 17:449-454.
71. Himmelfarb J, Stenvinkel P, Ikizler TA, Hakim RM. The elephant in uremia: oxidant stress as a unifying concept of cardiovascular disease in uremia. Kidney Int 2002, 62:1524-1538.
72. Keen C, Zidenburg-Cherr S. Encyclopedia of Food Science, Food Technology, and Nutrition 1993, London, Academic Press
73. Hardy IJ, Gillanders L, Hardy G. Is manganese an essential supplement for parenteral nutrition? Curr Opin Clin Nutr Metab Care 2008, 11:289-296.
74. Fischbein A, Hu H. Occupational and environmental exposure to lead. Environmental and Occupational Medicine 2007, 958. Rom W, Markowitz S. eds, Philadelphia, Wolters Kluwer/Lippincott Williams & Wilkins
75. Jarup L. Hazards of heavy metal contamination. Br Med Bull 2003, 68:167-182.
76. Krantz A, Dorevitch S. Metal exposure and common chronic diseases: a guide for the clinician. Dis Mon 2004, 50:220-262.
77. Feldman RG. Urban lead mining: lead intoxication among deleaders. N Engl J Med 1978, 298:1143-1145.
78. Cullen MR, Robins JM, Eskenazi B. Adult inorganic lead intoxication: presentation of 31 new cases and a review of recent advances in the literature. Medicine (Baltimore) 1983, 62:221-247.
79. Thomson RM, Parry GJ. Neuropathies associated with excessive exposure to lead. Muscle Nerve 2006, 33:732-741.
80. Ekong EB, Jaar BG, Weaver VM. Lead-related nephrotoxicity: a review of the epidemiologic evidence. Kidney Int 2006, 70:2074-2084.
81. Needleman H. Lead poisoning. Annu Rev Med 2004, 55:209-222.
82. Bleecker ML, Lindgren KN, Ford DP. Differential contribution of current and cumulative indices of lead dose to neuropsychological performance by age. Neurology 1997, 48:639-645.
83. Schwartz BS, Bolla KI, Stewart W, Ford DP, Agnew J, Frumkin H. Decrements in neurobehavioral performance associated with mixed exposure to organic and inorganic lead. Am J Epidemiol 1993, 137:1006-1021.
84. Nawrot TS, Thijs L, Den Hond EM, Roels HA, Staessen JA. An epidemiological re-appraisal of the association between blood pressure and blood lead: a meta-analysis. J Hum Hypertens 2002, 16:123-131.
85. Schwartz J. Lead, blood pressure, and cardiovascular disease in men. Arch Environ Health 1995, 50:31-37.
86. Kim R, Rotnitsky A, Sparrow D, Weiss S, Wager C, Hu H. A longitudinal study of low-level lead exposure and impairment of renal function. The Normative Aging Study. JAMA 1996, 275:1177-1181.
87. Malcolm D, Barnett HA. A mortality study of lead workers 1925-76. Br J Ind Med 1982, 39:404-410.
88. Pirkle JL, Schwartz J, Landis JR, Harlan WR. The relationship between blood lead levels and blood pressure and its cardiovascular risk implications. Am J Epidemiol 1985, 121:246-258.
89. Taylor L, Jones RL, Ashley K, Deddens JA, Kwan L. Comparison of capillary earlobe and venous blood monitoring for occupational lead surveillance. J Lab Clin Med 2004, 143:217-224.
90. Barbosa F, Tanus-Santos JE, Gerlach RF, Parsons PJ. A critical review of biomarkers used for monitoring human exposure to lead: advantages, limitations, and future needs. Environ Health Perspect 2005, 113:1669-1674.
91. Hu H, Rabinowitz M, Smith D. Bone lead as a biological marker in epidemiologic studies of chronic toxicity: conceptual paradigms. Environ Health Perspect 1998, 106:1-8.
92. Chowdhury UK, Biswas BK, Chowdhury TR. Groundwater arsenic contamination in Bangladesh and West Bengal, India. Environ Health Perspect 2000, 108:393-397.
93. Eisler R. Arsenic hazards to humans, plants, and animals from gold mining. Rev Environ Contam Toxicol 2004, 180:133-165.
94. Toxicological Profile for Arsenic 2007, http://www.atsdr.cdc.gov/toxprofiles/tp2.html, U.S. Department of Health & Human Services, Public Health Service, Agency for Toxic Substances and Disease Registry, Available at
95. Lasky T, Sun W, Kadry A, Hoffman MK. Mean total arsenic concentrations in chicken 1989-2000 and estimated exposures for consumers of chicken. Environ Health Perspect 2004, 112:18-21.
96. Saper RB, Phillips RS, Sehgal A. Lead, mercury, and arsenic in US- and Indian-manufactured Ayurvedic medicines sold via the Internet. JAMA 2008, 300:915-923.
97. Ford M. Arsenic. Goldfrank's Toxicological Emergencies 2002, 1183-1199. Goldfrank LFlomenbaum NLewin NHowland MHoffman RNelson L. eds, New York, McGraw-Hill
98. Eckhert CD. Other trace elements. Modern Nutrition in Health and Disease 2005, 338-349. Shils MEShike MRoss ACCaballero BCousins RJ. eds, Philadelphia, Lippincott Williams and Wilkins
99. Schoen A, Beck B, Sharma R, Dube E. Arsenic toxicity at low doses: epidemiological and mode of action considerations. Toxicol Appl Pharmacol 2004, 198:253-267.
100. Huang C, Ke Q, Costa M, Shi X. Molecular mechanisms of arsenic carcinogenesis. Mol Cell Biochem 2004, 255:57-66.
101. Kitchin KT, Ahmad S. Oxidative stress as a possible mode of action for arsenic carcinogenesis. Toxicol Lett 2003, 137:3-13.
102. Zhao CQ, Young MR, Diwan BA, Coogan TP, Waalkes MP. Association of arsenic-induced malignant transformation with DNA hypomethylation and aberrant gene expression. Proc Natl Acad Sci USA 1997, 94:10907-10912.
103. Hei TK, Liu SX, Waldren C. Mutagenicity of arsenic in mammalian cells: role of reactive oxygen species. Proc Natl Acad Sci USA 1998, 95:8103-8107.
104. Reigart J, Roberts J. Arsenical pesticides. Recognition and Management of Pesticide Poisonings 1999, http://www.epa.gov/oppfead121/safety/healthcare/handbook/handbook.htm, 5th edn, Washington, U.S. Environmental Protection Agency, Available at, accessed April 24, 2010
105. Windebank A. Arsenic. Experimental and Clinical Neurotoxicology 2000, 203-207. Spencer PSchaumburg H. eds, New York, Oxford University Press
106. Morton WE, Caron GA. Encephalopathy: an uncommon manifestation of workplace arsenic poisoning? Am J Ind Med 1989, 15:1-5.
107. Chakraborti D, Mukherjee SC, Pati S. Arsenic groundwater contamination in Middle Ganga Plain, Bihar, India: a future danger? Environ Health Perspect 2003, 111:1194-1201.
108. Chiou HY, Hsueh YM, Liaw KF. Incidence of internal cancers and ingested inorganic arsenic: a seven-year follow-up study in Taiwan. Cancer Res 1995, 55:1296-1300.
109. Tseng CH. Blackfoot disease and arsenic: a never-ending story. J Environ Sci Health C Environ Carcinog Ecotoxicol Rev 2005, 23:55-74.
110. Yu HS, Lee CH, Chen GS. Peripheral vascular diseases resulting from chronic arsenical poisoning. J Dermatol 2002, 29:123-130.
111. Tseng CH, Tai TY, Chong CK. Long-term arsenic exposure and incidence of non-insulin-dependent diabetes mellitus: a cohort study in arseniasis-hyperendemic villages in Taiwan. Environ Health Perspect 2000, 108:847-851.
112. Biswas S, Talukder G, Sharma A. Prevention of cytotoxic effects of arsenic by short-term dietary supplementation with selenium in mice in vivo. Mutat Res 1999, 441:155-160.
113. Sim M. Case studies in the use of toxicological measures in epidemiological studies. Toxicology 2002, 181-182:405-409.
114. Clarkson TW, Magos L, Myers GJ. The toxicology of mercury-current exposures and clinical manifestations. N Engl J Med 2003, 349:1731-1737.
115. Agner E, Jans H. Mercury poisoning and nephrotic syndrome in two young siblings. Lancet 1978, 2:951.
116. Inorganic Mercury. Environmental Health Criteria 118 1991, Geneva, World Health Organization
117. Virtanen JK, Rissanen TH, Voutilainen S, Tuomainen TP. Mercury as a risk factor for cardiovascular diseases. J Nutr Biochem 2006, 18:75-85.
118. Nuttall KL. Interpreting mercury in blood and urine of individual patients. Ann Clin Lab Sci 2004, 34:235-250.
119. Risher JF, Amler SN. Mercury exposure: evaluation and intervention the inappropriate use of chelating agents in the diagnosis and treatment of putative mercury poisoning. Neurotoxicology 2005, 26:691-699.
120. Guallar E, Sanz-Gallardo MI, van't VP. Mercury, fish oils, and the risk of myocardial infarction. N Engl J Med 2002, 347:1747-1754.
121. Hallgren CG, Hallmans G, Jansson JH. Markers of high fish intake are associated with decreased risk of a first myocardial infarction. Br J Nutr 2001, 86:397-404.
122. Salonen JT, nen K, Lakka TA, Salonen R, Kaplan GA. Mercury accumulation and accelerated progression of carotid atherosclerosis: a population-based prospective 4-year follow-up study in men in eastern Finland. Atherosclerosis 2000, 148:265-273.
123. Salonen JT, Seppanen K, Nyyssonen K. Intake of mercury from fish, lipid peroxidation, and the risk of myocardial infarction and coronary, cardiovascular, and any death in Eastern Finnish men. Circulation 1995, 91:645-655.
124. Yoshizawa K, Rimm EB, Morris JS. Mercury and the risk of coronary heart disease in men. N Engl J Med 2002, 347:1755-1760.
125. Elinder C, Friberg L, Kjellstrom T, Nordberg G, Oberdoerster G. Biological monitoring of metals. Chemical safety monographs. International Program of Chemical Safety 1994, 1-88. http://whqlibdoc.who.int/hq/1994/WHO_EHG_1994.2.pdf, Available at, accessed April 24, 2010
126. Dietary Reference Intakes: The Essential Guide to Nutrient Requirements 2006, 530-541. Otten JJHellwig JPMeyers LD. eds, Washington, DC, The National Academies Press
127. Hambidge KM, Casey CE, Krebs NF. Introduction. Trace Elements in Human and Animal Nutrition 1986, 1-37. Mertz W, ed, Orlando, FL, Academic Press
128. Prasad AS, Brewer GJ, Schoomaker EB, Rabbani P. Hypocupremia induced by zinc therapy in adults. JAMA 1978, 240:2166-2168.
129. Scottish Trace Element and Micronutrient Reference Laboratory. http://www.trace-elements.org.uk/Selenium.htm, Available at
130. Barceloux DG. Manganese. J Toxicol Clin Toxicol 1999, 37:293-307.
131. Dietary Reference Intakes for Vitamin A, Vitamin K, Arsenic, Boron, Chromium, Copper, Iodine, Iron, Manganese, Molybdenum, Nickel, Silicon, Vanadium, and Zinc. 2001, http://www.nap.edu/books/0309072794/html/, Available at
132. Kosnett MJ, Wedeen RP, Rothenberg SJ. Recommendations for medical management of adult lead exposure. Environ Health Perspect 2007, 115:463-471.