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Journal of Nutritional & Environmental Medicine Volume 12, 2002 - Issue 1
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Research Article

Nutritional Components Modify Metal Absorption, Toxic Response and Chelation Therapy

S. J. S. Flora Division of Pharmacology and Toxicology, Defence Research and Development Establishment, Jhansi Road, Gwalior 474 002, India
Pages 53-67 | Published online: 13 Jul 2009

  • lyaniwura TT. Dietary factors in mammalian toxicity of chemicals. Vet Human Toxicol 1990; 32: 106-9.
  • Gumer H, Ercal N. Can antioxidant be beneficial in the treatment of lead poisoning? Free Rad Biol Med 2000; 29: 927-45.
  • Goyer RA. Toxic and essential metal intoxication. Ann Rev Nutr 1997; 17: 37-50.
  • Rabinowitz MB, Koppe JD, Wetherill GW. Effect of food intake and fasting on gastrointestinal lead absorption in humans. Am J Clin Nutr 1980; 33: 1784-8.
  • Blake KCH, Mann M. Effect of calcium and phosphorus on the gastrointestinal absorption of Fb in man. Environ Res 1983; 30: 188-94.
  • Sullivan MF, Ruemmler PS. Effect of excess iron on cadmium or lead absorption by rats. J Toxicol Environ Health 1987; 22: 131-9.
  • Mahaffey KR. Nutrition and lead: strategies for public health. Environ Health Prespect 1995; 103: 191-6.
  • Mahaffey KR, Gortside PS, Glueck CJ. Blood lead levels and dietary calcium intake in 1 to 11 year old children at the second national health and nutrition survey. Pediatric 1980; 78: 257-62.
  • Pound JG, Long GJ, Rosen JF. Cellular and molecular toxicity of lead bone. Environ Health Perspect 1991; 91: 17-24.
  • Aungst BJ, Pung HJ. The effect of dietary calcium and phosphorus absorption, distribution and elimination kinetics in rats. Toxicol Environ Health 1985; 16: 147-59.
  • Mahaffey-Six MK, Goyer RA. The influence of iron deficiency on tissue content and toxicity of ingested lead in the rat. J Lab Clin Med 1972; 79: 128-36.
  • Quarterman J, Morrison JM, Humphries WR. The influence of high dietary calcium and phosphate on lead uptake and release. Environ Res 1978; 17: 60-7.
  • Sorrell M, Rosen JF. Interaction of lead, calcium, vitamin D and nutrition in lead burdened children. Arch Environ Health 1977; 32: 160-4.
  • Sflbergeld EK, Shwartz J, Mahaffey KR. Lead and osteoporosis: mobilisation of lead from bone in postmenopausal women. Environ Res 1988; 47: 79-84.
  • Kostial K, Dekanic D, Telisman S et al. Dietary calcium and blood levels in women. Biol Trace Elem Res 1991; 28: 181-5.
  • Fullmer CS. Lead-calcium interaction: involvement of 1,25-dihydrox y vitamin D. Environ Res 1997; 72: 45-55.
  • Barton JC, Conrad ME, Harrison L, Nuby S. Effect of calcium on the absorption and retention of lead. J Lab Clin Med 1978; 91: 366-76.
  • Wang C, Bhattacharya MH. Effect of cadmium on bone calcium and 45Ca in non-pregnant mice on calcium deficient diet: evidence of direct effect of cadmium on bone. Toxicol Appl Pharmacol 1993; 120: 228-39.
  • Goyer RA. Nutrition and metal toxicity. Am J Clin Nutr 1995; 61 (Suppl.): 646S-50S.
  • Fullmer CS, Oku T, Wasserman H. Effect of cadmium administration on intestinal calcium absorption and vitamin D dependent calcium binding protein. Environ Res 1980; 22: 386-91.
  • Baynes RD, Bothwell TH. Iron deficiency. Ann Rev Nutr 1990; 10: 133-48.
  • McCormick CC. The tissue specific accumulation of hepatic ne metallothionein following parental iron load. Proc Soc Exp Biol Med 1984; 176: 392-402.
  • Mahaffey KR. Environmental lead toxicity: nutrition as a component of intervention. Environ Health Perspect 1990; 89: 75-8.
  • Mahaffey KR. Nutrient lead interaction. In: Singhal RL, Thomas JA (eds) Lead Toxicity. Baltimore: Urbam and Schwarzenberg, 1980; 452-60.
  • Hamilton DL. Interrelationship of lead and iron retention in iron-deficiency mice. Toxicol Appl Pharmacol 1978; 46: 651-66.
  • Flanagan PR. Mechanism and regulation of intestinal uptake and transfer of iron. Acta Paediatr Scand Suppl 1989; 361:21-30.
  • Lozoff B, Brittenham GM, Viteri FE, Wolf AW, Urrufta JJ. The effect of short-term oral iron therapy on developmental deficits in iron deficient anaemic infants. J Pediat 1982; 100: 351-7.
  • Oski FA, Honig AS, HeIy B, Howanitz P. Effects of iron therapy on behaviour performance in non-anaemic, iron deficient infants. Pediatrics 1983; 71: 877-80.
  • Piomelli S, Seaman C, Kapoor S. Lead induced abnormalities of porphyrin metabolism: the relationship with iron deficiency. Ann NY Acad Sei 1987; 514: 278-88.
  • Goering PL. Lead-protein interactions as a basis for lead toxicity. Neurotoxicology 1993; 14: 45-50.
  • Berglund M, Akesson A, Nermell B, Vahter M. Intestinal absorption of dietary cadmium in woman is dependent on body iron stores and fiber intake. Environ Health Perspect 1994; 102: 1058-66.
  • Fox MRS. Nutritional influence on metal toxicity: cadmium as a model toxic element. Environ Health Perspect 1979; 29: 95-100.
  • Flora SJS, Kumar D, Das Gupta S. Interaction of zinc, methionine or their combination with lead at gastrointestinal or post-absorptive level in rats Pharmacol Toxicol 1991; 68: 3-7.
  • Flora SJS, Singh S, Tandon SK. Thiamin and zinc in prevention or therapy of lead intoxication. J Int Med Res 1989; 17: 68-75.
  • Sakai T, Yanagihara S, Ushio K. Restoration of lead-inhibited 5-aminolevulenate dehydratese activity in whole blood by heat, zinc ion and (or) dithiothreitol. Clin Chem 1980; 26: 625-31.
  • Cerklewski FL. Post absorptive effect at increased dietary zinc on toxicity and removal of tissue lead in rats. J Nutr 1984; 114: 550-4.
  • Victery W, Miller CR, Goyer RA. Essential trace metal excretion from rats with lead exposure and during chelation therapy. J Lab Clin Med 1986; 107: 129-35.
  • Ashraf MH, Fosmire GJ. Effects of marginal zinc deficiency on sub-clinical lead toxicity in the rat neonate. J Nutr 1985; 115: 334-46.
  • United States Department of Agriculture Human Nutrition Informative Service. CSFN Natowide Food Consumption Survey: Continuing Survey of Food Intakes by Individuals, 1985.
  • Miller GD, Massaro TF, Massaro El. Interaction between lead and essential elements: a review. Neurotoxicology 1990; 11: 99-120.
  • Border EA, Cantrell AC, Kilroes-Smith TA. The in vitro effect of zinc on the inhibition of human d-aminolevulinic acid dehydratese by lead. Br I Indust Med 1976; 33; 85-7.
  • Bremner I. Cadmium toxicity : nutritional influences and the role of metallothionein. World Rev Nutr Diet 1978; 32: 165-97.
  • Paraza MA, Ayala-Fierro F, Barber DS, Casarez E, Rael LT. Effect of micronutrients on metal toxicity. Environ Health Perspect 1998; 106 (Suppl. 1): 203-16.
  • Coyle P, Niezing G, Shelton TL, Philcox IC, Rote AM. Tolerance to cadmium hepatotoxicity by metallothionein and zinc: in vivo and in vitro studies with MT-null mice. Toxicology 2000; 150: 53-67.
  • Chowdhury BA, Chandra RK. Effect of zinc administration on cadmium induced suppression of natural killer cell activity in mice. Immunol Lett 1989; 22: 287-92.
  • Maitani T, Saito N, Abe M, Uchiyama S, Saito Y. Chemical form-dependent induction of hepatic zinc-thionein by arsenic administration and effect of co-administrated selenium in mice. Toxicol Lett 1987; 39: 63-70.
  • Kreppel H, Liu I, Liu Y, Reicht FX, Klaassen CD. Zinc-induced arsenite tolerance in mice. Fund Appl Toxicol 1994; 23: 32-7.
  • Funkino H, Hirai M, Hsueh YM, Moriyasu S, Yamane Y. Mechanism of protection by zinc against mercuric chloride toxicity in rats: effect of zinc and mercury on glutathionine metabolism. I Toxico Environ Health 1986; 19: 75-89.
  • Gale TF. The amelioration of mercury-induced embryotoxic effect by simultaneous treatment with zinc. Environ Res 1984; 35: 405-12.
  • Cerklewski FL, Forbes RM. Influence of dietary zinc on lead toxicity in rats. I Nutr 1976; 106: 689-96.
  • Rastogi SC, Clausen I, Srivastava KC. Selenium and lead mutual detoxifying effects. Toxicology 1976; 6: 377-8.
  • Flora SIS, Singh S, Tandon SK. Role of selenium in protection against lead intoxication. Acta Pharmacol Toxicol 1983; 53: 28-32.
  • Othman AI, El-Missiry MA. Role of selenium against lead toxicity in male rats. I Biochem MoI Toxicol 1998; 12: 345-9.
  • Christensen M, Rugby I, Morgensen SC. Effect of selenium on toxicity and ultrastructure localization of mercury in cultured murine macrophages. Toxicol Lett 1989; 47: 259-70.
  • Ganther HE. Modification of methyl mercury toxicity and metabolism by selenium and vitamin E: possible mechanisms. Environ Health Perspect 1978; 25: 71-6.
  • Chen IS, Goetchius MP, Campbell CT, Combs GF. Effects of dietary selenium and vitamin E on hepatic mixed-function oxidase and in vivo covalent binding of aflatoxin BI in rats. I Nutr 1982; 112: 324-31.
  • Maines MD. Heme oxygenase: function, multiplicity, regulatory mechanism and clinical applications. FASEB I 1988; 2: 2557-68.
  • Magos L, Clarkson TW, Sparrow S, Hudson AR. Comparison of protection given by selenite, selenomethionine and biological selenium against the renotoxicity of mercury. Arch Toxicol 1987; 60: 422-6.
  • Drasch G, Wanghofer E, Roider G, Strobach S. Correlation of mercury and selenium in the human kidneys. I Trace Elem Med Biol 1996; 10: 251-4.
  • Zloch Z. The antioxidative role of selenium in cadmium chronic intoxication. In: Neve et al. (eds) Therapeutic Uses of Trace Elements. New York: Plenum Press, 1996, 225-8.
  • Flora SIS, Kantian GM, Kumar P. Selenium effects on gallium arsenide induced biochemical and immunotoxicological changes in rats. Chem Biol Interact 1999; 122: 1-13.
  • Magos L, Berg GG. Selenium. In: Clarkson TW, Friberg L, Nordberg GF, Sager PR (eds) Biological Monitoring of Toxic Metals. New York: Plenum Press, 1988, 383.
  • Gregus A, Gyurasics A, Koszorus L. Interactions between selenium and group Va-metalloids (arsenic, antimony and bismuth) in the biliary excretion. Environ Toxicol Pharmacol 1998; 5: 89-99.
  • Glattre E, Mravcova A, Lener I, Vobecky M, Egertova E, Mysliveckova M. Study of distribution and interaction of arsenic and selenium in rat thyroid. Biol Trace Elem Res 1995; 49: 177-86.
  • Badiello R, Feroci G, Fini A. Interaction between trace elements: selenium and cadmium ions. I Trace Elem Med Biol 1996; 10: 156-62.
  • Pike RL, Brown ML. Nutrition: an Integrated Approach, 3rd ed. New York: Marcel Dekker, 1984, 167-200.
  • O'Dell BL. Copper. In: Present Knowledge in Nutrition, 5th edn. Washington: The Nutrition Foundation, 1984; 506-18.
  • Klauder DS, Petering HG. Protective value of dietary copper and iron against some toxic effects of lead in rats. Environ Health Perspect 1975; 12: 77-80.
  • Cerklewski FL, Forbes RM. Influence of dietary zinc on lead toxicity in the rat. I Nutr 1977; 106: 686-96.
  • Flora SJS, Behari JR, Tandon SK. Protective role of trace metals in lead intoxication. Toxicol Lett 1982; 13: 51-6.
  • Mills CF, Dalgarno AC. Copper and zinc status of ewes and lambs receiving increased concentrations of cadmium. Nature 1972; 239: 171-3.
  • Peraza MA, Ayala-Fierro F, Barber DS, Casarez E, Raei LT. Effect of micronutrients on metal toxicity. Environ Health Perspect 1990; 106: 203-16.
  • Funk AE, Day FA, Brady FC. Displacement of zinc and copper-induce d metallothionei n by cadmium and by mercury: in vivo and in vitro studies. Comp Biochem Physiol C Pharmacol Toxicol 1987; 86: 1-6.
  • Bratton GR, Zmudzki J, Bell MC, Wamock LC. Thaimin (vitamin BI) effects on lead intoxication and deposition of lead in tissues: therapeutic potential. Toxicol Appl Pharmacol 1981; 59: 164-71.
  • Sasser LB, Hall GG, Bratton GR, Zmudzki J. Absorption and tissue distribution of lead in thiamin-replete and thiamin-defident rats. J Nutr 1984; 114: 1816-25.
  • Flora SJS, Sharma RP. Influence of dietary supplemental" n with thiamin on lead intoxication in rats. Bio Trace Elem Res 1986; 10: 137-44.
  • Cheong JH, Seo DO, yu JR et al. Lead induced thiamine deficiency in the brain decreased the threshold of electroshock in rat. Toxicology 1999; 133: 105-113.
  • Ghazaly KS. Influence of thiamin on lead intoxication, lead deposition in tissues and lead haematological response of Tilapia Zillii. Comp Biochem Physiol 1991 ; 100C: 417-21.
  • Ito Y, Sasaki M, Ohka Y, Shimohara T, Ishiguro I. Effect of thiamin on lead excretions into the bfle using rat perfusion experiment. Japan J Clin Chem 1986; 10: 185-9.
  • Ito Y, Niiya Y, Otani M, Shima S. Effect of thiamin on the excretion of subcutaneous! y ingested lead in rat. Toxicol Lett 1987; 37: 221-8.
  • Fischer AB, Hess C, Neubauer T, Eikmann T. Testing of chelating agents and vitamins against lead toxicity using mammalian cell cultures. Analyst 1998; 123: 55-8.
  • Dally S, Girre C, Hispard E, Thomas G, Fournier L. High blood levels in alcoholics: wine vs beer. Drug Alcohol Depend 1989; 23: 45-8.
  • Flora SJS, Tandon SK. Prevention and therapeutic effects of thiamin, ascorbic acid and their combination in lead intoxication. Acta Pharmacol Toxicol 1986; 58: 374-8.
  • Lauwerys R, Roels H, Buchet JP. The influence of orally administered vitamin C or zinc on the absorption of and the biological response to lead. J Occup Med 1983; 25: 668-78.
  • Sohler A, Kruesi M, Pfeiffer CC. Blood lead levels in psychiatric outpatients reduced by zinc and vitamin C. Orthololcul Psychiatr 1977; 6: 272-6.
  • Simon JA, Hudes ES. Relationship of ascorbic acid to blood lead levels. J Am Med Assoc 1999; 281 : 2289-93.
  • Vijayalakshmi K, Bapu C, Sood PP. Differential effects of methyl mercury, thiols and vitamins on galactosidase of nervous and non-nervous tissue. Bull Environ Contain Toxicol 1992; 49: 71-7.
  • Prasad KN, Ramanjujam M. Vitamin E and vitamin C alter the effect of methyl mercuric chloride on neuroblastoma and glioma cells in culture. Environ Res 1980; 21: 343-9.
  • Dhawan M, Flora SJS, Tandon SK. Preventive and therapeutic role of vitamin E in chronic plumbism. Biomed Environ Sei 1989; 2: 335-41.
  • Shukla GS, Chandra SV. Cadmium toxicity and bioantioxidants status of vitamin E and ascorbic acid of selected organs in rats. J Appl Toxicol 1989; 9: 119-22.
  • Murthy RC, Gupta A, Gupta A, Anand M, Chandra SV. Peripheral neurotoxicity of cadmium in growing rats: preventive role of vitamin E. Toxicol Environ Chem 1991; 29: 267-73.
  • Tandon SK, Singh S, Dhawan M. Preventive effects of vitamin E in cadmium intoxication. Biome Environ Sei 1992; 5: 39-45.
  • Weber P, Bendich A, Machlin LJ. Vitamin E and human health: rationale for determining recommended intake levels. Nutrition 1997; 13: 450-60.
  • Machlin LJ, Brin M. Vitamin E. In: Alfin-Slater RB, Kritchevsky D (eds) Human Nutrition, a Comprehensive Treatise, Nutrition and the Adult Micronutrients. New York: Plenum Press, 1980, 245.
  • Shukla GS, Hussain T, Chandra SV. Protective effect of vitamin E on cadmium induced alterations in lipofuscin and Superoxide dismutase in rat brain regions. Pharmacol Toxicol 1988; 63: 305-6.
  • Welsh SO, Sores JH Jr. The protective effect of vitamin E and selenium against methylmercury toxicity in the Japanese quail. Nutr Rep Int 1978; 13: 43.
  • Lee TC, Ho IC. Modulation of cellular antioxidant defense activities by sodium arsenite in human fibroblasts. Arch Toxicol 1994; 69: 498-504.
  • Chang LW, Gilbert M, Sprecher J. Modification of methyl mercury neurotoxicity by vitamin E. Environ Res 1978; 17: 356-66.
  • Mehta A, Flora SJS. Possible role of metal redistribution, hepatotoxicity and oxidative stress in chelating agents induced hepatic and renal metallothionei n in rats. Food Chem Toxicol 2001; 39: 1029-38.
  • Thomas DJ, Chisolm Jr JJ. Lead zinc and copper decorporation during treatment of lead-poisoned children with calcium disodium ethylenediamineteraacetate . lexicologist 1986; 6: 49 (abstract 191).
  • Flora SJS, Behari JR, Ashquin M, Tandon SK. Time dependent protective effects of selenium against cadmium induced nephrotoxicity and hepatotoxicity. Chem Biol Interact 1982; 42: 345-51.
  • Ibim SEM, Trotman J, Nusey FI, Semafuko WEB. Depletion of essential elements by calcium disodium EDTA treatment in the dog. Toxicology 1992; 72: 229-37.
  • Flora SJS, Gubrelay U, Kaiman GM, Mathur R. Effect of zinc supplementation during dictating agent administration in cadmium intoxication in rats. J Appl Toxicol 1998; 18: 357-62.
  • Flora SJS, Tandon SK. Beneficial effects of zinc supplementation during dictation treatment of lead intoxication in rats. Toxicology 1990; 60: 129-39.
  • Flora SJS, Bhattacharya R, Sachan SRS. Dose dependent effects of zinc supplementation during chelation treatment of lead intoxication in rats. Pharmacol Toxicol 1994; 74: 330-3.
  • Flora SJS, Bhattachary a R, Vijayaraghava n R. Combined therapeuti c potential of meso 2,3-dimercap tosuccinic add and calcium disodium edetate on the mobilisation and distribution of lead in experimental lead intoxication in rats. Fund Appl Toxicol 1995; 25: 233-41.
  • Cory-Slechta DA, Weiss B, Cox C. Mobilisatio n and redistributio n of lead over the course of calcium disodium ethylenediamine tetraacetate chelation therapy. J Pharmacol Exp Therap 1987; 243: 804-13.
  • Flora SJS, Kumar P. Biochemical and immunotoxicological evaluation of metal dictating drugs. Drug Invest 1993; 5: 269-73.
  • Finelli VN, Lerner S, Hong C, Lohiya C. Effect of zinc supplementation during chelation therapy in phimbism. Med Lav 1980; 2: 149-56.
  • Flora SJS. Influence of simultaneous supplementation of zinc and copper during chelation of lead in rats. Hum Exp Toxicol 1991; 10: 331-6.
  • [Ill] Tandon SK, Singh S, Flora SJS. Influence of methionine-zinc supplementation during chelation of lead in rats. J Trace Elem Electrol Health Dis 1994; 8: 75-8.
  • Flora SJS, Dhawan M, Tandon SK. Influence of copper supplementation during chelation of lead. Clin Chem Enzymol Commun 1990; 3: 97-105.
  • Haust HL, Inwoo M, Spence JD, Poona HC, Peter F. Intramuscular administration of iron during long-term chelation therapy with 2,3-dimercaptosuccini c add in a man with severe lead poisoning. Clin Biodiem 1989; 22: 189-96.
  • Jones SG, Jones MM, Holscher MA, Vaughn WK. Effect of zinc on the dithiocarbamates induced mobilization of cadmium deposits in mice. J Toxicol Environ Health 1988; 23: 91-101.
  • Flora SJS, Tandon SK. Adjuvants for therapeutic chelating drugs in lead ntoxication. Trace Elem Electr 1995; 12: 131-40.
  • Flora SJS, Singh S, Tandon SK. Chelation in metal intoxication XVIE: combined effects of thiamin and calcium disodium versenate on lead toxicity. Life Sei 1986; 38: 67-71.
  • Flora SJS, Pant SC, Sachan AS. Mobilisation and distribution of lead over the course of combined treatment with thiamin and meso 2,3-dimercaptosuccini c acid or 2,3-dimercaptopropan e 1 -sulfonate in experimental lead intoxication in rats. Clin Chem Enzymol Commun 1994; 6: 207-16.
  • Kim JS, Crichlow EC, Blaldey BR, Rousseaux CG. The effects of thiamin on the neurophysiological alterations induced by lead. Vet Hum Toxicol 1990; 32: 101-5.
  • Tandon SK, Flora SJS, Singh S. Chelation in metal intoxication XXIV: influence of various components of vitamin B complex on therapeutic efficacy of di-sodium calcium versenate in lead intoxication. Pharmacol Toxicol 1987; 60: 62-5.
  • Dhawan M, Kachru DN, Tandon SK. Influence of thiamin and ascorbic add supplementation on antidotal efficacy of thiol chelators in lead intoxication. Arch Toxicol 1988; 62: 301-4.
  • Kumar BD, Khan MM, Krishnaswamy K. Therapeutic potential of thiamin in lead toxicity. Ind J Pharmacol 1994; 26: 277-81.
  • Tandon SK, Prasad S. Effect of thiamine on the cadmium chelating capacity of thiol compounds. Human Exp Toxicol 2000; 19: 523-8.
  • Houston DKN, Johnson MA. Does vitamin C intake protect against lead toxicity? Nutr Rev 2000; 58: 73-9.
  • Goyer RA, Cherian MG. Ascorbic acid-EDTA treatment of lead toxicity in rats. Life Sei 1979; 24: 433-8.
  • Paredes SR, Kozicki PA, Del AM, Battle C. S-adenosyl L-methionine: a counter to lead intoxication? Comp Biochem Physiol B 1985; 82: 751-7.
  • Flora GJS, Seth PK. Beneficial effects of S-adenosyl L-methionine on aminolevulinic add dehydratase, glutathione and lipid peroxidation during acute lead-ethanol administration in mice. Alcohol 1999; 18: 103-8.
  • Gubrelay U, Mathur R, Kannan GM, Flora SJS. Role of S-adenosyl L-methionine in potentiating cadmium mobilization by diethylenetriamin e penta acetic acid in mice. Cytobios 2001 ; 104: 99-105.
  • Pande M, Mehta A, Pant BP, Flora SJS. Combined administration of a chelating agent and an antioxidant in the prevention and treatment of acute lead intoxication in rats. Environ Toxicol Pharmacol 2001; 9: 173-84.
  • Flora SJS. Arsenic induced oxidative stress and its reversibility following combined administration of n-acetylcysteine and meso 2,3-dimercaptosuccini c acid in rats. Clin Exp Pharmacol Physiol 1999; 26: 865-9.
  • El-Gazzar RM, Finneli VN, Boinano J, Petering HG. Influence of dietary zinc on lead toxicity in rats. Toxicol Lett 1978; 1: 227-34.
  • Wahba ZZ, Coogan TP, Rhodes SW, Waalkes MP. Protective effects of selenium on cadmium toxicity in rats: role of altered toxicokinetic and metallothionein. J Toxicol Environ Health 1993; 38: 171-82.
  • Cikrt M, Bencko V. Mercury-selenium interaction: distribution and excretion of 203 Hg in rats after simultaneous administration of selenite or selenate. Toxicol Lett 1989; 48: 159-64.

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