Biological Trace Element Research

, Volume 32, Issue 1–3, pp 363–382 | Cite as

The role of zinc in reproduction

Hormonal mechanisms
  • Alain Emile Favier
Part 2: Trace elements in endocrinology Section 5: Reproduction, Growth, and Immunity

Abstract

Zinc is a very important element in the reproductive cycle of species. In humans, it is necessary for the formation and maturation of spermatozoa, for ovulation, and for fertilization. During pregnancy, zinc deficiency causes a number of anomalies: spontaneous abortion, pregnancy-related toxemia, extended pregnancy or prematurity, malformations, and retarded growth. Delivery is adversely affected by deficiency. These different effects of zinc can be explained by its multiple action on the metabolism of androgen hormones, estrogen and progesterone, together with the prostaglandins. Nuclear receptors for steroids are all zinc finger proteins. Zinc supplementation has already proven beneficial in male sterility and in reducing complications during pregnancy. However, it would be worth conducting larger-scale trials to confirm these beneficial effects.

Index Entries

Zinc hypogonadism sterility spermatozoon testosterone estrogens ovulation fertilization pregnancy toxemia abortion prematurity prostaglandins malformation 

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References

  1. 1.
    A. A. Abbassi, A. S. Prasad, J. Ortega, E. Congco, and D. Oberleas,Ann. Int. Med. 85, 601–605 (1976).Google Scholar
  2. 2.
    A. A. Abbassi, A. S. Prasad, and P. Rabbani,Trans. Ass. Am. Ph. 92, 292–302 (1979).Google Scholar
  3. 3.
    A. A. Abbassi, A. S. Prasad, P. Rabbani, and E. Dumouchelle,J. Lab. Clin. Med. 96, 544–550 (1980).Google Scholar
  4. 4.
    F. A. Adeniyi,Act. Obst. Gynecol. Scand. 66, 579–582 (1987).CrossRefGoogle Scholar
  5. 5.
    P. J. Aggett and R. K. Chandra,Trace Elements in Nutrition of Children, R. K. Chandra, ed., Nestlé Nutrition, Raven, New York, 1985, pp. 137.Google Scholar
  6. 6.
    K. Antoniou, M. Vassulaki-Grimani, D. Lolis, and A. P. Grimanis,J. Radioanal. Chem. 70, 77–84 (1982).Google Scholar
  7. 7.
    L. D. Antoniou, R. Shalhoub, T. Sudhakar, and J. C. Smith,Lancet 29 Oct., 895–898 (1977).CrossRefGoogle Scholar
  8. 8.
    J. Apgar,Ann. Rev. Nutr. 5, 43–68 (1985).CrossRefGoogle Scholar
  9. 9.
    S. Arver,J. Trace Elem. Electrolytes Health Dis. 1, 45–47 (1987).PubMedGoogle Scholar
  10. 10.
    F. K. Assadi and M. Ziai,Ped. Res. 19, 167A (1985).Google Scholar
  11. 11.
    B. A. Bassiouni, A. I. Foda, and A. A. Rafei,Europ. J. Obst. Gynec. Reprod. Biol. 9, 75 (1979).CrossRefGoogle Scholar
  12. 12.
    R. S. Beach, M. E. Gershwin, and L. S. Hurley,Am. J. Clin. Nutr. 38, 579–590 (1983).PubMedGoogle Scholar
  13. 13.
    K. E. Bergman, D. Makopsch, and K. H. Tews,Am. J. Clin. Nutr. 33, 2145–2150 (1980).Google Scholar
  14. 14.
    J. M. Brandes, A. Lightman, J. Itskovitz, and O. Zinder,Biol. Neonate 38, 66–70 (1980).PubMedCrossRefGoogle Scholar
  15. 15.
    M. W. Breskin, B. Worthington-Roberts, R. Knopp, Z. Brown, B. Plovie, K. Mottet, and J. Mills,Am. J. Clin. Nutr. 38, 943–953 (1983).PubMedGoogle Scholar
  16. 16.
    M. H. Briggs, M. Griggs, and A. Watakama,Experientia 28, 406 (1972).PubMedCrossRefGoogle Scholar
  17. 17.
    M. H. Brophy, N. F. Harris, and I. L. Crawford,Clin. Chim. Acta 107–112 (1985).Google Scholar
  18. 18.
    M. H. Brophy,Biol. Psychiatry 21, 702–707 (1986).CrossRefGoogle Scholar
  19. 19.
    P. K. Buamah and M. Russell,Brit. J. Obst. Gyn. 91, 788–790 (1984).Google Scholar
  20. 20.
    G. P. Budzik, J. M. Hutson, H. Ikawa, and P. K. Donahoe,Endocrinology 110, 1521–1525 (1982).PubMedCrossRefGoogle Scholar
  21. 21.
    G. E. Bunce, G. R. Wilson, C. F. Mills, and A. Klopper,Biochem. J. 210, 761–767 (1983).PubMedGoogle Scholar
  22. 22.
    G. E. Bunce, and M. Vessal,J. Steroid Biochem. 26, 303–308 (1987).PubMedCrossRefGoogle Scholar
  23. 23.
    A. A. Caldamone, M. K. Freytag, and A. T. Cockett,Urology 13, 280–281 (1979).PubMedCrossRefGoogle Scholar
  24. 24.
    M. Campbell-Brown, R. J. Ward, A. P. Haines, W. R. S. North, R. Abraham, and I. R. Mc Fayden,Br. J. of Obst. Gyn. 92, 875–885 (1985).Google Scholar
  25. 25.
    M. Castro-Magana, P. J. Collipp, S. Y. Chen, T. Cheruvansky, and V. Maddiah,Am. J. Dis. Child. 135, 322–325 (1981).PubMedGoogle Scholar
  26. 26.
    A. O. Cavdar, A. Arcassoy, S. Cin, and H. Gumus,Hematologica 65, 403–408 (1980).Google Scholar
  27. 27.
    A. O. Cavdar, A. Arcassoy, S. Cin, E. Babacar, and S. Gozdasaglu,Zinc Deficiency in Human Subjects, Alan R. Liss, New York, 1983, p. 71.Google Scholar
  28. 28.
    A. O. Cavdar, E. Babacan, A. Arcasoy, and U. Ertem,Am. J. Clin. Nutr. 33, 542–544 (1980).PubMedGoogle Scholar
  29. 29.
    A. O. Cavdar, M. Bahceci, N. Akar, J. Erten, G. Bahceci, E. Babacan, A. Arcasoy, and H. Yavuz,J. Trace Elem. Electrolytes Health Dis. 2, 9–19 (1988).PubMedGoogle Scholar
  30. 30.
    F. F. Cherry, E. A. Bennett, G. S. Bazzano, L. K. Johnson, G. J. Fosmire, and H. K. Bortson,Am. J. Clin. Nutr. 34, 2367 (1981).PubMedGoogle Scholar
  31. 31.
    F. Cherry, H. Sandstead, P. Rojas, L. Johnson, H. Batson, and X. Wang,Am. J. Clin. Nutr. 50, 945–954 (1989).PubMedGoogle Scholar
  32. 32.
    D. S. Colvar and E. M. Wilson,Biochemistry 23, 3471–3478 (1984).CrossRefGoogle Scholar
  33. 33.
    S. Cunnane, E. Majid, J. Senior, and C. F. Mills,Life Science 32, 2471–2478 (1983).CrossRefGoogle Scholar
  34. 34.
    A. Dib and J. P. Carreau,Ann. Nutr. Metab. 31, 312–319 (1987).PubMedGoogle Scholar
  35. 35.
    I. E. Dreosti,Clinical Applications of Recent Advances in Zinc Metabolism, Alan R. Liss, New York, 1982, p. 19.Google Scholar
  36. 36.
    I. E. Dreosti and R. M. Smith,Neurobiology of the Trace Elements, vols. 1 and 2, Humana, Clifton, New Jersey (1983).Google Scholar
  37. 37.
    U. J. Erickson,J. Nutr. 114, 477–484 (1984).Google Scholar
  38. 38.
    P. Faure, A. M. Roussel, A. Favier, and S. Halimi (1990),Diabete et Metabolisme, in press.Google Scholar
  39. 39.
    A. Favier, (1981) Mise au point de microdosages des oligoéléments Fe, Cu, Zn, Mn, par absorption atomique sans flamme. Rôle de ces éléments dans la gestation. Thèse d'Etat ès Sciences, Grenoble.Google Scholar
  40. 40.
    A. Favier, D. Ruffieux, G. Decoux, and J. Arnaud,J. Inh. Metab. Dis. 6, supl 2, 93–94 (1983).CrossRefGoogle Scholar
  41. 41.
    M. Favier, A. Favier, E. Robert, M. Guignier, and Y. Malinas,Rev Fr. Gyn. Obst. 82, 575–587 (1987).PubMedGoogle Scholar
  42. 42.
    A. Favier, B. Dardelet, M. J. Richard, and J. Arnaud,Trace Elements in Man and Animals, Plenum, New York, 1988, p. 609.Google Scholar
  43. 43.
    D. Fehily, K. Keohane, F. Cremin, and D. M. Jenkins,TEMA 6, Asilomar (1987).Google Scholar
  44. 44.
    D. Fehily, A. Kiswani, D. M. Jenkins, and F. M. Gremin,J. Trace Elem. Electrolytes Health Dis. 1, 63–68 (1987).PubMedGoogle Scholar
  45. 45.
    J. H. Fishman and J. Fishman,Biochem. Biophys. Res. Com. 144, 505–511 (1987).PubMedCrossRefGoogle Scholar
  46. 46.
    A. Flynn, S. S. Martin, R. J. Sokol, S. Miller, N. Golden, and B. Del Villano,The Lancet 14 572–574 (1981).CrossRefGoogle Scholar
  47. 47.
    R. H. Follis, H. G. Day, and E. V. McCollum,J. Nutr. 22, 223–237 (1941).Google Scholar
  48. 48.
    G. J. Fosmire, Y. Y. Al Ubaidi, and H. H. Sandstead,Ped. Res. 9, 89–93 (1975).Google Scholar
  49. 49.
    D. Gallaher and L. S. Hurley,J. Nutr. 110, 591–593 (1980).PubMedGoogle Scholar
  50. 50.
    S. Z. Ghavani-Maibodi, P. J. Colipp, M. Castro-Magana, C. Stewart, and S. Y. Chen,Ann. Nutr. Metab. 27, 214–219 (1983).Google Scholar
  51. 51.
    F. K. Ghishan and H. L. Green,Ped. Res. 17, 529–531 (1983).Google Scholar
  52. 52.
    A. Ghosh, L. Y. Y. Fong, C. W. Wan, S. T. Liang, J. S. K. Woo, and V. Wong,Br. J. Obst. Gyn. 92, 886–891 (1985).Google Scholar
  53. 53.
    M. S. Golub, M. E. Gershwin, L. S. Hurley, D. Baly, and A. G. Hendrickx,Am. J. Clin. Nutr. 39, 265–280 (1984).PubMedGoogle Scholar
  54. 54.
    M. Golub, E. Gershwin, L. Hurley, D. Baly, and A. Hendrickx,Am. J. Clin. Nutr. 39, 879–887 (1984).PubMedGoogle Scholar
  55. 55.
    R. M. Hackman and L. S. Hurley,Teratology 28, 355–368 (1983).PubMedCrossRefGoogle Scholar
  56. 56.
    N. Hahn and C. Fuchs,Zbl. Gynak. 96, 1520–1523 (1974).Google Scholar
  57. 57.
    E. S. Halas and H. H. Sandstead,Pediat. Res. 9, 94–97 (1975).PubMedCrossRefGoogle Scholar
  58. 58.
    E. S. Halas and H. H. Standstead,Fed. Proc. 41, 781 (1982).Google Scholar
  59. 59.
    J. A. Halsted, H. A. Ronaghy, P. Abadi, M. Haghshenass, G. H. Amirhakemi, R. M. Barakat, and J. G. Rheinbold,Am. J. Med. 53, 277–284 (1972).PubMedCrossRefGoogle Scholar
  60. 60.
    K. M. Hambidge and W. Droegemueller,Obst. Gyn. 44, 666–672 (1974).Google Scholar
  61. 61.
    K. M. Hambidge, K. H. Nelder, and P. A. Walravens,Lancet 1, 577, 578 (1975).CrossRefGoogle Scholar
  62. 62.
    K. M. Hambidge, N. F. Krebs, M. A. Jacobs, A. Favier, L. Guyette, and D. N. Ike,Am. J. Clin. 37, 429–442 (1983).Google Scholar
  63. 63.
    R. J. Hartoma, K. Naboul, and A. Netter,Lancet II, 1125–1126 (1977).CrossRefGoogle Scholar
  64. 64.
    N. Helbecque and J. P. Henichart,Médecine et Sciences 4, 624–628 (1988).Google Scholar
  65. 65.
    R. I. Henkin, J. R. Marshall, and S. Meret,Am. J. Obst. Gynecol. 110, 131–134 (1971).Google Scholar
  66. 66.
    J. E. Hesketh,J. Comp. Path. 99, 239–247 (1982).CrossRefGoogle Scholar
  67. 67.
    J. L. Hinks, A. Ogilvy-Stuart, K. M. Hambidge, and V. Walker,Br. J. Obst. Gyn. 96, 61–66 (1989).Google Scholar
  68. 68.
    K. S. Hirsch and L. S. Hurley,Teratology 17, 303–314 (1978).PubMedCrossRefGoogle Scholar
  69. 69.
    I. F. Hunt, N. J. Murphy, A. Cleaver, B. Faraji, M. Swendseid, A. Coulson, V. Clark, B. Browdy, M. T. Cabalum, and J. C. Smith,Am. J. Clin. Nutr. 40, 508–521 (1984).PubMedGoogle Scholar
  70. 70.
    I. F. Hunt, N. J. Murphy, P. Martiner Hewes, B. Faraji, M. Swendseid, R. Reynolds, A. Sanchez, and A. Muja,Am. J. Clin. Nutr. 46, 563–569 (1987).PubMedGoogle Scholar
  71. 71.
    L. S. Hurley and D. L. Baly,Clinical, Biochemical, and Nutritional Aspects of Trace Elements, Alan R. Liss, New York, 1982, p. 145.Google Scholar
  72. 72.
    A. J. Jackson and H. J. Schumacher,Teratology 19, 341–344 (1979).PubMedCrossRefGoogle Scholar
  73. 73.
    S. Jameson, (1976) Effects of zinc deficiency in human reproduction. Thèse de l'Université de Linkoping, Suède.Google Scholar
  74. 74.
    S. Jameson,Acta Med. Scand. 593 (Suppl), 3–89 (1976).Google Scholar
  75. 75.
    S. Jameson,Clinical Applications of Recent Advances in Zinc Metabolism, Alan R. Liss, New York, 1982, p. 39.Google Scholar
  76. 76.
    S. Jameson,Zinc Deficiency in Human Subjects, Alan R. Liss, New York, (1983), p. 53.Google Scholar
  77. 77.
    J. Joven, C. Villabona, J. Rubies-Prat, E. Espinel, and E. Galard,Clin. Chim. Acta 148, 239–245 (1985).PubMedCrossRefGoogle Scholar
  78. 78.
    C. L. Keen, M. S. Clegg, B. Lonnerdal, and L. S. Hurley,Trace Elements in Man and Animals, vol. 6, Plenum, New York, 1988, p. 203.Google Scholar
  79. 79.
    C. L. Keen and L. S. Hurley,Zinc in Human Biology, eds., Springer-Verlag, 1989, p. 183.Google Scholar
  80. 80.
    S. Kellokumpu and H. Rajamiemi,Biol. Reprod. 24, 298–305 (1981).PubMedCrossRefGoogle Scholar
  81. 81.
    L. D. Keppen, T. Pysher, and O. M. Rennert,Ped. Res. 19, 944–947 (1985).CrossRefGoogle Scholar
  82. 82.
    P. Kiilholma, R. Paul, P. Pakarinen, and M. Gronroos,Acta. Obstet. Gynecol. Scand. 63, 629–631 (1984).PubMedGoogle Scholar
  83. 83.
    C. A. Kimmel, R. E. Butcher, and H. J. Schummacher,Anat. Res. 172, 345 (1972).Google Scholar
  84. 84.
    J. C. King and J. R. Turnlund,Zinc in Human Biology, Springer-Verlag, Londres, 1988, p. 336.Google Scholar
  85. 85.
    N. F. Krebs, K. M. Hambidge, M. A. Jacobs, and J. O. Rasbash,Am. J. Clin. Nutr. 41, 560–570 (1985).PubMedGoogle Scholar
  86. 86.
    A. Krust, S. Green, and P. Argos,EMBO J. 5, 891–897 (1986).PubMedGoogle Scholar
  87. 87.
    S. Kumar,Nutr. Rep. Int. 13, 33–36 (1976).Google Scholar
  88. 88.
    J. L. Lafond, B. Sele, and A. Favier,J. Trace Elem. Electrolytes Health Dis. 2, 19–22 (1988).PubMedGoogle Scholar
  89. 89.
    R. Laitinen, A. S. Siimes, E. Vuori, and S. Salmela,Biol. Trace El. Res. 6, 415–421 (1984).CrossRefGoogle Scholar
  90. 90.
    N. Lazebnik, B. R. Kuhnert, P. M. Kuhnert, and K. Thompson,Trace Elements in Man and Animals, vol. 6, L. S. Hurley, ed., New York, 1988, p. 605.Google Scholar
  91. 91.
    A. Leake, G. D. Chisholm, and F. K. Halib,J. Steroid Biochem. 20, 651–655 (1984).PubMedCrossRefGoogle Scholar
  92. 92.
    D. Lentz and M. E. Gershwin,Developmental and Comparative Immunology 8, 1–5 (1984).PubMedCrossRefGoogle Scholar
  93. 93.
    P. H. Lohmar and D. O. Toft,Biochem. Biophys. Res. Com. 67, 8–15 (1975).PubMedCrossRefGoogle Scholar
  94. 94.
    C. J. MacClain, J. S. Gavaler, and D. H. Van Thiel,J. Lab. Clin. Med. 104, 1007–1015 (1984).Google Scholar
  95. 95.
    S. Mahajan, A. Abbasi, A. S. Prasad, P. Rabbani, W. Briggs, and F. McDonald,Ann. Int. Med. 97, 357–361 (1982).PubMedGoogle Scholar
  96. 96.
    K. Mahomed, D. K. James, and K. McCabe,Brit. Med. J. 299, 826–830 (1989).PubMedGoogle Scholar
  97. 97.
    J. Marmar, S. Katz, D. E. Praiss, and T. J. De Benedictis,Fertil Steril. 26, 1057–1063 (1975).PubMedGoogle Scholar
  98. 98.
    R. J. Matusik, C. Kreis, and P. Mc Nicol,Biochem. Cell. Biol. 64, 601–607 (1986).PubMedGoogle Scholar
  99. 99.
    N. J. Meadows, W. Ruse, M. Smith, P. W. N. Keeling, D. Bloxam, J. Day, J. W. Scopes, and R. P. Thompson,Lancet,ii, 1135–1137 (1981).CrossRefGoogle Scholar
  100. 100.
    N. J. Meadows, S. C. Cunnane, P. W. N. Keeling, and R. P. H. Thompson,Zinc Deficiency in Human Subjects, Alan R. Liss, New York, 1983, p. 139.Google Scholar
  101. 101.
    G. D. Mieden, C. L. Keen, L. S. Hurley, and N. W. Klein,J. Nutr. 116, 2424–2431 (1986).PubMedGoogle Scholar
  102. 102.
    M. Mukherjee, H. H. Sandstead, M. Ratnaparklir, L. Johnson, D. Milne, and H. Stelling,Am. J. Clin. Nutr. 40, 496–507 (1984).PubMedGoogle Scholar
  103. 103.
    P. B. Mutch, and L. S. Hurley,Am. J. Physiol. 238, E26-E31 (1980).PubMedGoogle Scholar
  104. 104.
    A. Netter, R. Hartoma, and K. Naboul,Arch of Andrology 7, 69–73 (1981).CrossRefGoogle Scholar
  105. 105.
    Y. Nishi, S. Hatano, K. Aimara, H. Okahata, H. Karvamura, K. Tanaka, Y. Miyachi, and T. Usui,Pediatric Research 18, 232 (1984).PubMedCrossRefGoogle Scholar
  106. 106.
    Y. Nishi, S. Hatano, K. Aihara, A. Fujie, and M. Kihara,J. Am. Coll. Nutr. 8, 93–97 (1989).PubMedGoogle Scholar
  107. 107.
    P. I. Oteiza, C. L. Keen, B. Lonnerdal, and L. S. Hurley,Trace Elements in Man and Animals, L. S. Hurley, ed., Plenum, New York, 1988, p. 631.Google Scholar
  108. 108.
    A. S. Prasad, ed.,Ann. Rev. Toxicol. 20, 393 (1979).Google Scholar
  109. 109.
    A. S. Prasad and Z. T. Cossak,Ann. Intern. Med. 100, 367–371 (1984).PubMedGoogle Scholar
  110. 110.
    I. Qvist, M. Abdulla, M. Jagestad, and S. Swensson,Acta Obstet. Gynecol. Scand. 65, 12–22 (1986).CrossRefGoogle Scholar
  111. 111.
    K. Raja, P. Leach, G. Smith, D. McCarthy, and T. Peters,Clin. Chim. Acta 123, 19–26 (1982).PubMedCrossRefGoogle Scholar
  112. 112.
    I. R. Record,Neurotoxicology 8, 369–378 (1987).PubMedGoogle Scholar
  113. 113.
    A. W. Root, G. Duckett, M. Sweetland, and E. O. Reiter,J. Nutr. 109, 958–964 (1979).PubMedGoogle Scholar
  114. 114.
    U. Rosick, E. Rosick, and P. Bratter,J. Clin. Chem. Biochem. 21, 363–372 (1983).Google Scholar
  115. 115.
    L. S. Sever and I. Emanual,Teratology 7, 117 (1973).PubMedCrossRefGoogle Scholar
  116. 116.
    N. A. Shaw, H. C. Dickey, H. M. Brugman, D. L. Blamberg, and J. F. Witter,Lab. Anim. 8, 1–7 (1974).PubMedCrossRefGoogle Scholar
  117. 117.
    J. C. L. Shaw,Am. J. Dis. Child. 133, 1260–1268 (1979).PubMedGoogle Scholar
  118. 118.
    G. Shymala and Y. F. Yeh,Biochem. Biophys. Res. Com. 64, 408–415 (1975).CrossRefGoogle Scholar
  119. 119.
    K. Simmer, N. Punchard, G. Murphy, and R. P. Thompson,Ped. Res. 19, 697–700 (1985).CrossRefGoogle Scholar
  120. 120.
    K. Simmer and R. P. Thompson,Clin. Sci. 68, 395–399 (1985).PubMedGoogle Scholar
  121. 121.
    M. H. Soltan and D. M. Jenkins,Brit. J. Obstet. Gynecol. 89, 56–58 (1982).Google Scholar
  122. 122.
    M. H. Soltan and D. M. Jenkins,Br. J. Obst. Gyne. 90, 457–459 (1983).Google Scholar
  123. 123.
    M. K. Song and N. F. Adham,Am. J. Clin. Nutr. 41, 1201–1209 (1985).PubMedGoogle Scholar
  124. 124.
    S. Southon, C. M. Williams, and S. J. Fairweather-Tait,Trace Elements in Man and Animals, Plenum, New York, 1988, p. 601.Google Scholar
  125. 125.
    K. B. Spenger, J. Schmitz, D. Hetzel, D. Bundshu, and H. E. Franz,Coutr. Nephrol. 38, 119–125 (1984).Google Scholar
  126. 126.
    M. Statter, Z. Schumert, N. Linder, J. S. Younis, Y. Servadio, and D. Weinstein,Trace Elements in Medicine,5, 137–138 (1988).Google Scholar
  127. 127.
    C. A. Swanson and J. C. King,Fed. Proc. 42, 3, 390 (1983).Google Scholar
  128. 128.
    H. Swenerton and L. S. Hurley,J. Nutr. 95, 8–18 (1968).PubMedGoogle Scholar
  129. 129.
    H. Swenerton and L. S. Hurley,J. Nutr. 110, 575–583 (1980).PubMedGoogle Scholar
  130. 130.
    J. Taper, J. Olivia, and S. J. Ritchey,Am. J. Clin. Nutr. 41, 1184–1192 (1985).PubMedGoogle Scholar
  131. 131.
    J. R. Turnlund,Stable Isotopes in Nutrition, 3–52 (1984).Google Scholar
  132. 132.
    J. Y. Uriu-Hare, J. S. Stern, and C. L. Keen,Fed. Proc. 46, 495 (1987).Google Scholar
  133. 133.
    S. C. Vir, A. H. Love, and W. Thompson,Am. J. Clin. Nutr. 34, 2800–2807 (1981).PubMedGoogle Scholar
  134. 134.
    J. Vorman, V. Hollgriegl, H. J. Merker, and T. Gunther,Biol. Trace El. Res. 10, 25–35 (1986).Google Scholar
  135. 135.
    T. Wanatabe, F. Sato, and A. Endo,Yamagata Med. J. 1, 13–20 (1983).Google Scholar
  136. 136.
    S. Zidenberg-Chen, J. Rosenbaum, and C.L. Keen,Trace Elements in Man and Animals, vol. 6, L. S. Hurley, ed., Plenum, New York, 1988, p. 613.Google Scholar
  137. 137.
    A. W. Zimmerman, B. S. Dunham, D. J. Nochimson, B. Kaplan, J. M. Clive, and S. L. Kunkel,Am. J. Obst. Gynecol. 149, 523–529 (1984).Google Scholar
  138. 138.
    A. W. Zimmerman,Neurology 34, 443–450 (1984).PubMedGoogle Scholar

Copyright information

© Humana Press Inc. 1992

Authors and Affiliations

  • Alain Emile Favier
    • 1
  1. 1.Laboratoire de Biochimie des Intéractions Micronutriments-Radicaux LibresUniversité J. Fourier-Faculté de PharmacieL. TroncheFrance

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