The Role of Copper and Zinc in Cholesterol Metabolism

  • Leslie M. Klevay
Part of the Advances in Nutritional Research book series (volume 1)

Abstract

Ischemic heart disease is the leading cause of death in the United States (Anonymous, 1974a). Previously termed coronary heart disease (Anonymous, 1969), this disease causes about 35% of deaths, twice as many as are caused by malignant neoplasms or cancer. In the United States, risk of ischemic heart disease is higher among men than among women, among smokers of cigarettes than among nonsmokers, among diabetics and among those with certain abnormalities of the electrocardiogram. Risk also increases with age, with blood pressure, and with the concentration of cholesterol in serum (Insull, 1973). The predictive utility of the concentration of cholesterol in serum or plasma (Fredrickson and Levy, 1972) and the identification of many dietary components that can alter these concentrations have been the sources of most interest among nutritionists in the metabolism of cholesterol.

Keywords

Nickel Sucrose Magnesium Zirconium Cadmium 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Albanese, A. A., Edelson, A. H., Woodhull, M. L., Lorenze, E. J., Jr., Wein, E. H., and Orto, L. A., 1973, Effects of a calcium supplement on serum cholesterol, calcium, phosphorus and bone density of “normal, healthy” elderly females, Nutr. Rep. Int 8: 119.Google Scholar
  2. Allen, K. G. D., and Klevay, L. M., 1976, Hypercholesterolemia in rats caused by copper deficiency, J. Nutr 106 (7): X XII.Google Scholar
  3. Anderson, J. T., Grande, F., and Keys, A., 1958, Dietary ascorbic acid and serum cholesterol, Fed. Proc 17: 468.Google Scholar
  4. Anderson, J. T., Grande, F., and Keys, A., 1973, Cholesterol-lowering diets, J. Am. Dieter. Assoc 62: 133.Google Scholar
  5. Anon., 1969, Vital Statistics of the United States 1967. Mortality, Vol. 2, Part A, Table 1–7, Washington, D.C., U.S. Department of Health, Education and Welfare.Google Scholar
  6. Anon., 1974a, Vital Statistics of the United States 1970. Mortality, Vol. 2, Part A, Table 1–7, Washington, D.C., U.S. Department of Health, Education and Welfare.Google Scholar
  7. Anon., I974b, Recommended Dietary Allowances, Food and Nutrition Board, National Research Council, National Academy of Sciences, Washington, D.C., pp. 92–96.Google Scholar
  8. Anon., 1976, The herbs and the heart, Nutr. Rev 34: 43.Google Scholar
  9. Barboriak, J. J., Krehl, W. A., Cowgill, G. R., and Whedon, A. D., 1958, Influence of high-fat diets on growth and development of obesity in the albino rat, J. Nutr 64: 241.Google Scholar
  10. Birenbaum, M. L., Fleischman, A. I., and Raichelson, R. I., 1972, Long term human studies on the lipid effects of oral calcium, Lipids 7: 202.CrossRefGoogle Scholar
  11. Brown, E. D., Howard, M. P., and Smith, J. C., Jr., 1977, The copper content of regular, vegetarian, and renal diets, Fed. Proc, 36: 1122.Google Scholar
  12. Burch, R. E., Williams, R. V., Hahn, H. K. J., Jetton, M. M., and Sullivan, J. F., 1975, Serum and tissue enzyme activity and trace-element content in response to zinc deficiency in the pig, Clin. Chem 21: 568.Google Scholar
  13. Burgoon, C. F., Jr., 1975, The skin, in Nelson’s Textbook of Pediatrics ( V. C. Vaughan III, R. J. McKay, and W. E. Nelson, eds.), 10th ed., pp. 1514–1568, W. B. Saunders, Philadelphia.Google Scholar
  14. Butler, L. C., and Daniel, J. M., 1973, Copper metabolism in young women fed two levels of copper and two protein sources, Am. J. Clin. Nutr 26: 744.Google Scholar
  15. Call, D. L., and Sanchez, A. M., 1967, Trends in fat disappearance in the United States 1909–65, J. Nutr$193 (Suppl. 1) Part II, 1.Google Scholar
  16. Carlson, L. A., Olsson, A. G., Orb, L., and Rössner, S., 1971, Effects of oral calcium upon serum cholesterol and triglycerides in patients with hyperlipidemia, Atherosclerosis 14: 391.CrossRefGoogle Scholar
  17. Cartwright, G. E., 1950, Copper metabolism in human subjects, in Copper Metabolism ( W. D. McElroy and B. Glass, eds.), pp. 274–314, Johns Hopkins Press, Baltimore.Google Scholar
  18. Cartwright, G. E., and Wintrobe, M. M., 1964, The question of copper deficiency in man, Am. J. Clin. Nutr 15: 94.Google Scholar
  19. Cartwright, G. E., Hodges, R. E., Gubler, C. J., Mahoney, J. P., Daum, K., Wintrobe, M. M., and Bean, W. B., 1954, Studies on copper metabolism. XIII. Hepatolenticular degeneration, J. Clin. Invest 33: 1487.CrossRefGoogle Scholar
  20. Crawford, M. D., Gardner, M. J., and Morris, J. N., 1968, Mortality and hardness of local water supplies, Lancet 1: 827.CrossRefGoogle Scholar
  21. Curren, G. L., Azarnoff, D. L., and Bolinger, R. E., 1959, Effect of cholesterol synthesis inhibition in normocholesteremic young men, J. Clin. Invest 38: 1251.CrossRefGoogle Scholar
  22. Dahl, L. K., 1960, Effects of chronic excess salt feeding. Elevation of plasma cholesterol in rats and dogs, J. Exp. Med 112: 635.CrossRefGoogle Scholar
  23. Darby, W. J., Friberg, L., Mills, C. F., Parizek, J., Ramalingaswami, V., Ronaghy, H. A., Sandstead, H. H., Underwood, E. J., Rao, N. M., Par, R., Bengoa, J. M., DeMaeyer, E. M., and Mertz, W., 1973, Trace Elements in Human Nutrition, Report of a WHO expert committee. World Health Organization Technical Report Series, No. 532 World Health Organization, Geneva, pp. 15–19.Google Scholar
  24. Dayton, S., Pearce, M. L., Hashimoto, S., Dixon, W. J., and Tomiyasu, U., 1969, A controlled clinical trial of a diet high in unsaturated fat, Circulation 39, 40 (Suppl. II): 1.Google Scholar
  25. Doisy, E. A., Jr., 1973, Micronutrient controls on biosynthesis of clotting proteins and cholesterol, in Trace Substances in Environmental Health. VI ( D. D. Hemphill, ed.), pp. 193–199, Univ. of Missouri Press, Columbia.Google Scholar
  26. Dietschy, J. M., and Wilson, J. D., 1970, Regulation of cholesterol metabolism, New Engl. J. Med 282: 1128.CrossRefGoogle Scholar
  27. Durfor, C. N., and Becker, E., 1964, Public water supplies of the 100 largest cities in the United States, 1962, Washington, D.C., U.S. Geological Survey, Water-Supply Paper 1812.Google Scholar
  28. Erdman, J. W., Jr., and Lachance, P. S., 1974, Effect of salt mixture and cholesterol upon rat serum and liver zinc, vitamin A, and cholesterol, Nutr. Rep. Int. 9: 319.Google Scholar
  29. Evans, G. W., 1973, Copper homeostasis in the mammalian system, Physiol. Rev 53: 535.Google Scholar
  30. Fillies, L. C., and Mann, G. F., 1954, Influence of sulfur amino acid deficiency on cholesterol metabolism, Metabolism 3: 16.Google Scholar
  31. Follis, R. H., and Van Itallie, T. B., 1974, Pellagra, in Harrison’s Principles of Internal Medicine (M. M. Wintrobe, G. W. Thorn, R. D. Adams E Braunwald, K. J. Isselbacher, and R. G. Petersdorf, eds.), pp. 427–430, McGraw-Hill, New York.Google Scholar
  32. Fredrickson, D. S., and Levy, R. I., 1972, Familial hyperlipoproteinemia, in The Metabolic Basis of Inherited Disease (J. B. Stanbury, J. B. Wyngaarden, and D. S. Fredrickson, eds.), 3rd ed., pp. 545–614. McGraw-Hill, New York.Google Scholar
  33. Friedberg, C. K., 1966, Diseases of the Heart, 3rd ed., pp. 652, 669, W. B. Saunders, Philadelphia.Google Scholar
  34. Gipp, W. F., Pond, W. G., Kallfelz, F. A., Tasker, J. B., Van Campen, D. R., Krook, L., and Visek, W. V., 1974, Effect of dietary copper, iron, and ascorbic acid levels on hematology, blood and tissue copper, iron and zinc concentrations and “Cu and 59Fe metabolism in young pigs, J. Nutr 104: 532.Google Scholar
  35. Hambidge, K. M., Hambidge, C., Jacobs, M., and Baum, J. D., 1972, Low levels of zinc in hair, anorexia, poor growth, and hypogeusia in children, Pediat. Res 6: 868.CrossRefGoogle Scholar
  36. Hambidge, K. M., Walravens, P. A., Brown, R. M., Webster, J., White, S., Anthony, M., and Roth, M. L., 1976, Zinc nutrition of preschool children in the Denver Head Start program, Am. J. Clin. Nutr 29: 734.Google Scholar
  37. Hartley, T. F., Dawson, J. B., and Hodgkinson, A., 1974, Simultaneous measurement of Na, K, Ca, Mg, Cu, and Zn balances in man, Clin. Chim. Acta 52: 321.CrossRefGoogle Scholar
  38. Haslewood, G. A. D., 1963, Bile salts, in Sterols, Bile Acids and Steroids ( M. Florkin and E. H. Stotz, eds.), Vol. 10, pp. 23–31, Elsevier, Amsterdam.Google Scholar
  39. Hegsted, D. M., et al,1942–1976, Nutr. Rev 1-34(8).Google Scholar
  40. Hellerstein, E. E., Nakamura, M., Hegsted, D. M., and Vitale, J. J., 1960, Studies on the interrelationships between dietary magnesium, quality and quantity of fat, hypercholesterolemia and lipidosis, J. Nutr 71: 339.Google Scholar
  41. Hodges, R. E., Hood, J., Canham, J. E., Sauberlich, H. E., and Baker, E. M., 1971, Clinical manifestations of ascorbic acid deficiency in man, Am. J. Clin. Nutr 24: 432.Google Scholar
  42. Hopkins, L. L., and Mohr, H. E., 1974, Vanadium as an essential nutrient, Fed. Proc 33: 1773.Google Scholar
  43. Iacono, J. M., 1974, Effect of varying the dietary level of calcium on plasma and tissue lipids ofGoogle Scholar
  44. rabbits, J. Nutr 104:1165.Google Scholar
  45. Ingbar, S. H., and Woeber, K. A., 1974, The thyroid gland, in Textbook of Endocrinology (R. H. Williams, ed.), 5th ed., pp. 95–232, W.B. Saunders, Philadelphia.Google Scholar
  46. Insull, W., Jr., 1973, Coronary Risk Handbook, p. 3, American Heart Association, New York. Jacob, R. A., Klevay, L. M., and Thacker, E. J., 1975, Hypercholesterolemia due to meat anemia, Fed Proc 34: 899.Google Scholar
  47. Kahn, H. A., 1970, Change in serum cholesterol associated with changes in the United States civilian diet, 1909–1965, Am. J. Clin. Nutr 23: 879.Google Scholar
  48. Kayden, H. J., and Cox, R. P., 1973, Evidence for normal metabolism and interconversions of unusual fatty acids in acrodermatitis enteropathica, J. Pediat 83: 993.CrossRefGoogle Scholar
  49. Klevay, L. M., 1970a, Hair as a biopsy material. I. Assessment of zinc nutriture. Am. J. Clin. Nutr 23: 284.Google Scholar
  50. Klevay, L. M., I970b, Hair as a biopsy material. II. Assessment of copper nutriture. Am. J. Clin. Nutr 23: 1194.Google Scholar
  51. Klevay, L. M., 1973, Hypercholesterolemia in rats produced by an increase in the ratio of zinc to copper ingested, Am. J. Clin. Nutr 26: 1060.Google Scholar
  52. Klevay, L. M., 1974a, An association between the amount of fat and the ratio of zinc to copper in 71 foods: Inferences about the epidemiology of coronary heart disease, Nutr. Rep. Int 9: 393.Google Scholar
  53. Klevay, L. M., 1974b, Lard diets (56.6%) don’t produce hypercholesterolemia in rats unless zinc/copper metabolism is altered, Clin. Res 22: 629A.Google Scholar
  54. Klevay, L. M., 1974c, Coronary heart disease and dietary fiber, Am. J. Clin. Nutr 27: 1202.Google Scholar
  55. Klevay, L. M., 1974d, Interactions among dietary copper, zinc, and the metabolism of cholesterol and phospholipids, in Trace Element Metabolism in Animals (W. G. Hoekstra, J. W. Suttie, H. E. Ganther, and W. Mertz, eds.), Vol. 2, pp. 553–556, University Park Press, Baltimore.Google Scholar
  56. Klevay, L. M., 1975a, The ratio of zinc to copper of diets in the United States, Nutr. Rep. Int 11: 237.Google Scholar
  57. Klevay, L. M., 1975b, The ratio of zinc to copper in milk and mortality due to coronary heart disease: An association, in Trace Substances in Environmental Health. VIII ( D. D. Hemphill, ed.), p. 9, Univ. of Missouri Press, Columbia.Google Scholar
  58. Klevay, L. M., 1975c, Coronary heart disease: The zinc/copper hypothesis, Am. J. Clin. Nutr. 28: 764.Google Scholar
  59. Klevay, L. M., 1976a, Hypercholesterolemia due to ascorbic acid, Proc. Soc. Exp. Biol. Med 151: 579.Google Scholar
  60. Klevay, L. M., 1976b, Elements of ischemic heart disease, Perspect. Biol. Med 20: 186.Google Scholar
  61. Klevay, L. M., 1976c, Ischemic heart disease: The fiber hypothesis, Proceedings of the Miles Symposium, Nutrition Society of Canada (in press).Google Scholar
  62. Klevay, L. M., and Forbush, J., 1976, Copper metabolism and the epidemiology of coronary heart disease, Nutr. Rep. Int 14: 221.Google Scholar
  63. Klevay, L. M., Evans, G. W., and Sandstead, H. H., 1975, Zinc/copper hypercholesterolemia: The effect of sodium phytate, Clin. Res 23: 460A.Google Scholar
  64. Klevay, L. M., Petering, H. G., and Stemmer, K. L., 1971, A controlled environment for trace metal experiments on animals, Environ. Sci. Technol 5: 1196.CrossRefGoogle Scholar
  65. Klevay, L. M., Vo-Khactu, K. P., and Jacob, R. A., 1976, The ratio of zinc to copper of cholesterol-lowering diets, in Trace Substances in Environmental Health. IX ( D. D. Hemphill, ed.), pp. 131–138, Univ. of Missouri Press, Columbia.Google Scholar
  66. Klevay, L. M., Reck, S., and Barcome, D. F., 1977, United States diets and the copper requirement, Fed. Proc, 36: 1175.Google Scholar
  67. Lei, K. Y., 1977, Dietary copper deficiency: Effects on cholesterol metabolism in the rat. Fed. Proc 36: 1151.Google Scholar
  68. Leren, P., 1966, The effect of plasma cholesterol lowering diet in male survivors of myocardial infarction, Acta Med. Scand. Suppl 446: 1.Google Scholar
  69. Leren, P., 1970, The Oslo diet-heart study, eleven-year report, Circulation 42: 935.CrossRefGoogle Scholar
  70. Leverton, R. M., and Binkley, E. S., 1944, The copper metabolism and requirement of young women, J. Nutr 27: 43.Google Scholar
  71. Looney, M. A., Lei, K. Y., and Kilgore, L. T., 1977, Effects of dietary fiber, zinc, and copper on serum and liver cholesterol levels in the rat, Fed. Proc, 36: 1134.Google Scholar
  72. Lorenz, K. Z., 1974, Analogy as a source of knowledge, Science 185: 229.CrossRefGoogle Scholar
  73. Maibach, E., 1967, Die Beeinflussung des Gesamtcholesterins der /3-Lipoproteide und Gesamtlipide des Serums durch orale und parenterale Calciumzufuhr, Schweiz med. Woch 97: 418.Google Scholar
  74. Maibach, E., 1969, Uber die Beeinflussung des Gesamtocholesterins und der Gesamtlipide im Serum des Menschen durch orale Kalziumzufuhr, Wien. med. Woch 118: 1059.Google Scholar
  75. Mann, G. V., Andrus, S. B., McNally, A., and Stare, F. J., 1953, Experimental atherosclerosis in Cebus monkeys J. Exp. Med. 98:195Google Scholar
  76. McPherson, W. J., 1976, Nickel Catalyst Scavenging Process, Technical Data Sheet No. 2625, Chicago, Illinois, Wurster and Sanger.Google Scholar
  77. Meneely, G. R., and Ball, C. O. T., 1958, Experimental epidemiology of chronic sodium chloride toxicity and the protective effect of potassium chloride, Am. J. Med 25: 713.CrossRefGoogle Scholar
  78. Miettinen, M., Turpeinen, O., Karvonen, M. J., Elosuo, R., and Paavilainen, E., 1972, Effect of cholesterol-lowering diet on mortality from coronary heart-disease and other causes, Lancet 2: 835.CrossRefGoogle Scholar
  79. Moynahan, E. J., 1974, Acrodermatitis enteropathica: a lethal inherited human zinc-deficiency disorder, Lancet 2: 399.CrossRefGoogle Scholar
  80. Neldner, K. H., Hagler, L., Wise, W. R., Stifel, F. B., Lufkin, E. G., and Herman, R. H., 1974, Acrodermatitis enteropathica, Arch. Dermatol. 110: 711.Google Scholar
  81. Neldner, K. H., and Hambidge, K. M., 1975, Zinc therapy of acrodermatitis enteropathica, New Engl. J. Med 292: 879.CrossRefGoogle Scholar
  82. Nielsen, F. H., Myron, D. R., Givand, S. H., Zimmerman, T. J., and O11erich, D. A., 1975, Nickel deficiency in rats, J. Nutr 105: 1620.Google Scholar
  83. O’Neal, R. M., Abrahams, O. G., Paulsen, D. S., Lorah, E. J., Eklund, D. L., and Dowdy, R. P., 1977, The relationships of hair zinc to copper ratios with serum cholesterol and triglyceride levels, Fed. Proc, 36: 1122.Google Scholar
  84. Osborn, G. R., 1968, Stages in development of coronary disease observed from 1500 young subjects. Relationship of hypotension and infant feeding to aetiology, in Le rôle de la paroi artérielle dans l’athérogénèse, (M. J. Lenègre, L. Scebat and J. Renais, Eds.), pp. 93–139, Centre National de la Recherche Scientifique, Paris.Google Scholar
  85. Page, L. B., Damon, A., Moellering, R. C., 1974, Antecedents of cardiovascular disease in six Solomon Islands societies, Circulation 49: 1132.CrossRefGoogle Scholar
  86. Patel, P. B., Chung, R. A., and Lu, J. Y., 1975, Effect of zinc deficiency on serum and liver cholesterol in the female rat, Nutr. Rep. Int 12: 205.Google Scholar
  87. Pond, W. G., and Walker, E. F., Jr., 1975, Effect of dietary Ca and Cd level of pregnant rats on reproduction and on dam and progeny tissue mineral concentrations, Proc. Soc. Exp. Biol. Med 148: 665.Google Scholar
  88. Portnoy, B., and Molokhia, M., 1974, Zinc in acrodermatitis enteropathica, Lancet 2: 663.CrossRefGoogle Scholar
  89. Reinhold, J. G., Faradji, B., Abadi, P., and Ismail-Beigi, F., 1976, Binding of zinc to fiber and other solids of whole meal bread, in Trace Elements in Human Health and Disease ( A. S. Prasad and D. Oberleas, eds.), Vol. 1, pp. 163–180, Academic Press, New York.Google Scholar
  90. Rizek, R. L., Friend, B., and Page, L., 1974, Fat in today’s food supply—Level of use and sources, J. Am. Oil Chem. Soc 51: 244.CrossRefGoogle Scholar
  91. Roe, D. A., 1973, A Plague of Corn, Cornell Univ. Press, Ithaca, N.Y.Google Scholar
  92. Sandstead, H. H., 1973, Zinc nutrition in the United States, Am. J. Clin. Nutr 26: 1251.Google Scholar
  93. Sandstead, H. H., 1974, Macroelement and trace element deficiencies, in Harrison’s Principles of Internal Medicine ( M. M. Wintrobe, G. W. Thorn, R. D. Adams, E. Braunwald, K. J. Isselbacher, and R. G. Petersdorf, eds.), pp. 441–443, McGraw-Hill, New York.Google Scholar
  94. Scheinberg, I. H., and Sternlieb, I., 1960, Copper metabolism, Pharmacol. Rev. 12:355. Schroeder, H. A., 1968, Serum cholesterol levels in rats fed thirteen trace elements, J. Nutr 94: 475.Google Scholar
  95. Schroeder, H. A., 1969, Serum cholesterol and glucose levels in rats fed refined and less refined sugars and chromium, J. Nutr 97: 237.Google Scholar
  96. Schroeder, H. A., and Balassa, J. J., 1965, Influence of chromium, cadmium, and lead on rat aortic lipids and circulating cholesterol, Am. J. Physiol 209: 433.Google Scholar
  97. Schroeder, H. A., Nason, A. P., Tipton, I. H., and Balassa, J. J., 1966, Essential trace metals in man: Copper, J. Chron. Dis 19: 1007.CrossRefGoogle Scholar
  98. Selye, H., 1964, From Dream to Discovery, p. 104, McGraw-Hill, New York.Google Scholar
  99. Selye, H., 1970, Experimental Cardiovascular Diseases, p. 308. Springer-Verlag, New York.CrossRefGoogle Scholar
  100. Sharrett, A. R., and Feinleib, M., 1975, Water constituents and trace elements in relation to cardiovascular disease, Prey. Med 4: 20.CrossRefGoogle Scholar
  101. Stamler, J., Pick, R., and Katz, L. M., 1958, Effects of dietary proteins, methionine and vitamins on plasma lipids and atherogenesis in cholesterol fed cockerels, Circ. Res 6: 442.CrossRefGoogle Scholar
  102. Staub, H. W., Reussner, G., and Thiessen, R., Jr., 1969, Serum cholesterol reduction by chromium in hypercholesterolemic rats, Science 166: 746.CrossRefGoogle Scholar
  103. Terris, M., ed., 1964, Goldberger on Pellagra, Louisiana State Univ. Press, Baton Rouge.Google Scholar
  104. Trowell, H., 1976, Definition of dietary fiber and hypotheses that it is a protective factor in certain diseases, Am. J. Clin. Nutr 29: 417.Google Scholar
  105. Tsai, C. M. E., and Evans, J. L., 1976, Influence of dietary ascorbic acid and copper on tissue trace elements, cholesterol, and hemoglobin, in Trace Substances in Environmental Health. IX ( D. D. Hemphill, ed.), pp. 441–449, Univ. of Missouri Press, Columbia.Google Scholar
  106. Turpeinen, O., Miettinen, M., Karvonen, M. J., Roione, P., Pekkarinen, M., Lehtosuo, E. J., and Alivirten, P., 1968, Dietary prevention of coronary heart disease: Long-term experiment, Am. J. Clin. Nutr 21: 225.Google Scholar
  107. Vitale, J. J., Velez, H., Guzman, C., and Correa, P., 1963, Magnesium deficiency in the Cebus monkey, Circ. Res 12: 642.CrossRefGoogle Scholar
  108. Walravens, P. A., and Hambidge, K. M., 1976, Growth of infants fed a zinc supplemented formula, Am. J. Clin. Nutr 29: 1114.Google Scholar
  109. Whanger, P. D., and Weswig, P. H., 1975, Effects of selenium, chromium, and antioxidants on growth, eye cataracts, plasma cholesterol, and blood glucose in selenium deficient, vitamin E supplemented rats, Nutr. Rep. Int 12: 345.Google Scholar
  110. Wolf, W. R., Holden, J., and Green, F. E., 1977, Daily intake of zinc and copper from self-selected diets, Fed. Proc, 36: 1175.Google Scholar
  111. Yacowitz, H., Fleischman, A. I., and Bierenbaum, M. L., 1965, Effects of oral calcium upon serum lipids in man, Br. Med. J 1: 1352.CrossRefGoogle Scholar
  112. Yudkin, J., 1974, Sugar and coronary disease, in Controversy in Internal Medicine. II ( F. J. Ingelfinger, R. V. Ebert, M. Finland, and A. S. Reiman, eds.), pp. 199–207, W. B. Saunders, Philadelphia.Google Scholar
  113. Zaidman, J. L., Julsary, A., Kook, A. I., Szeinberg, A., Wallis, K., and Azizi, E., 1971, Abetalipoproteinemia in acrodermatitis enteropathica, New Engl. J. Med 284: 1387.Google Scholar

Copyright information

© Plenum Press, New York 1977

Authors and Affiliations

  • Leslie M. Klevay
    • 1
  1. 1.Agricultural Research ServiceHuman Nutrition Laboratory, United States Department of AgricultureGrand ForksUSA

Personalised recommendations