DOI QR코드

DOI QR Code

Role of Dietary Zinc as a Nutritional Immunomodulator

  • Goswami, T.K. (Section of Immunology, Indian Veterinary Research, Institute) ;
  • Bhar, R. (Division of Animal Nutrition, Indian Veterinary Research Institute) ;
  • Jadhav, S.E. (Division of Animal Nutrition, Indian Veterinary Research Institute) ;
  • Joardar, S.N. (West Bengal University of Animal and Fishery Sciences) ;
  • Ram, G.C. (In-charge, Section of Immunology, Indian Veterinary Research Institute)
  • Received : 2004.01.10
  • Accepted : 2004.08.04
  • Published : 2005.03.01

Abstract

Zinc is ubiquitous in all living cells. Structural and catalytic properties of cellular enzymes are zinc dependent. Zinc deficiency leads to a variety of pathological abnormalities with immune impairment. It is an established fact that nutritional status contributes to overall immune response of individuals. Outcome of zinc deficiency on immune system is so drastic that it is difficult to conceive at the first instance. Zinc supplementation has been advocated to prevent diarrheal disease in children with poor nutritional status. The bioavailability of zinc depends upon its sources. Moreover it varies between monogastrics and ruminants. Controversy still prevails between inorganic and organic sources of zinc with respect to their superiority in bioavailability. Zinc exerts immunostimulatory effects in various laboratory and farm animals. Animals having congenital zinc deficiency diseases like A46 lethal trait usually die due to impairment of the immune system unless treated with zinc. The immune mechanism of zinc and its effect on animals and man are discussed. Zinc has been considered as extremely safe at higher therapeutic doses, but does not provide any beneficial effect but rather may cause immunosuppression. More recently, zinc has been prescribed for immunodeficient hosts, to modulate the immune system so that to a certain extent it can combat against opportunistic pathogens.

Keywords

References

  1. AAFC. 1998. (Association of American Feed Control Officials). Official Publication, USA.
  2. Acda, S. P. and B. J. Choe. 2002. Effects of organic trace minerals supplementation on sows reproductive and neonate’s growth performance through 2nd week post weaning. Asian-Aust. J. Anim. Sci. 15:1312-1318.
  3. Aggett, P. J. and J. G. Comerford. 1995. Zinc and human health. Nutr. Rev. 53:S16-S22.
  4. Agricultural Research Council. 1980. The nutrient requirements of ruminant livestock. Commonwealth Agric. Bureaux..
  5. Alleyne, G. A. and V. H. Young. 1967. Adrenocortical function in children with severe protein calorie malnutrition. Clin. Sci. 33:189-200.
  6. Andresen, E., A. Basse, E. Brummmerstedt and T. Flagstad. 1974. Lethal trait A-46 in cattle. Additional genetic investigations. Nord. Veternaermed. 26:273-278.
  7. Arrayet, J. L., A. M. Oberbauer, T. R. Famula, I. Garnett, J. W. Oltjen, J. Imhoof, M. E. Kehrli and W. T. Grahm. 2002. Growth of Holestein calves from birth to 90 days: the influence of dietary zinc and BLAD status. J. Anim. Sci. 80:545-552.
  8. Bernatchez, C., R. Al-Daccak, P. E. Mayer, K. Mehindate, L. Rink, S. Mecheri and W. Mourad. 1997. Functional analysis of micoplasma arthritidis-derived mitogen interaction with Class II molecules. Infect. Immu. 65:200-205.
  9. Bhar, R., S. K. Maiti, T. K. Goswami, A. K. Garg, A. Chabra and Satyapal. 2001. Effect of Vitamin C and zinc as feed supplement on wound healing, antibody response and productivity in swine. In: 8th Annual Conference of Indian Association for Advancement of Veterinary Research, Ludhiana, India. p. 27.
  10. Bhar, R., S. K. Maiti, T. K. Goswami, R. C. Patra, A. K. Garg and A. K. Chabra. 2003. Effect of dietary vitamin C and zinc supplementation on wound healing, immune-response in swine. Ind. J. Anim. Sci. 73:674-677.
  11. Bone, R. C. 1991. The pathogenesis of sepsis. Ann. Intern. Med. 115:457-469 https://doi.org/10.7326/0003-4819-115-6-457
  12. Bosi, P. 2000. Modulation of immune response and barrier function in the piglets gut by dietary means. Asian-Aust. J. Anim. Sci. 13(Supp):278-293.
  13. Bosi, P., C. Gremo Kolini and P. Trevisi. 2003. Dietary regulation of the intestinal barrier functions at weaning. Asian-Aust. J. Anim. Sci. 16:596-608.
  14. Braunschweig, C. L., M. Sowers, D. S. Kovacevich, G. M. Hill and D. A. August. 1997. Parenteral zinc supplementation in adult human during the acute phase response increases the febrile response. J. Nut. 122:70-74.
  15. Brummerstedt, E., E. Andresen, A..Basse and T. Flagstad. 1974. Lethal trait A-46 in cattle. Immunological investigations. Nord. Veternaermed. 26:279-293.
  16. Burns, R. B. 1983. Antibody production suppressed in the domestic fowl by zinc deficiency. Avian. Pathol. 12:141-146. https://doi.org/10.1080/03079458308436156
  17. Carlson, M. S., G. M. Hill and J. E. Link. 1999. Early-and traditionally weaned nursery pigs benefit from phase feeding pharmacological concentration of zinc oxide; effect on metallothionein and mineral concentrations. J. Anim. Sci. 77:1199-1207.
  18. Caulfield, L. E., N. Zavateta and A. Figueroa. 1999. Adding zinc to prenatal iron and folate supplements improve maternal and neonatal zinc status in a peruvian population. Am. J. Clin. Nutr. 69:1257-1263.
  19. Chandra, R. K. 1984. Excessive intake of zinc impairs immune responses. J. Am. Med. Assoc. 252:1443-1446. https://doi.org/10.1001/jama.252.11.1443
  20. Chandra, R. K and P. Newberne. 1977. Nutrition immunity and infection. Plenum Press. New. York.
  21. Chesters, J. K., L. Patrie and K. Lipson. 1993. Two zinc dependant steps during G1 to S phase transition. J. Cell. Physiol. 155:445-451.
  22. Chesters, J. K. 1997. Zinc. In: Hand Book of Nutritionally Essential Mineral Elements (Ed. B. L. O’Dell and R. A. Sunde) Marcel Dekker Inc. New York. pp. 185-230.
  23. Chirase, N. K., D. P. Hutcheson, G. B. Thompson and J. W. Spears. 1994. Recovery rate and plasma zinc and copper concentration of steer calves fed organic and inorganic zinc and manganese source with or without injectable copper and challenged with infectious bovine rhinotracheitis virus. J. Anim. Sci. 72:212-219.
  24. Cohen, J. J. and R. C. Duke. 1984. Glucocorticoid activation of calcium dependant endonucleases in thymocyte nuclei leads to cell death. J. Immunol. 132:38-42.
  25. Coleman, J. E. 1992. Zinc proteins: enzymes, storage proteins, transcription factors and replication proteins. Annu. Rev. Biochem. 16:897-946.
  26. Cook-Mills, J. and P. J. Fraker. 1993. Functional capacity of residual lymphocytes from zinc-deficient adult mice. Br. J. Nutr. 69:835-848.
  27. Corah, L. R., D. A. Dargatz and C. W. Peters. 1996. NAHMS forage Survey. Trace mineral analysis of 352 forage samples collected in 18 states. J. Anim. Sci. 74(Suppl 1):202 (Abstr.).
  28. Coto, J. A., E. M. Hadden, M. Sauro, N. Zom and J. W. Hadden. 1992. Interleukin-1 regulate secretion of zinc-thymulin by human thymic epithelial cells and its action on T lymphocyte proliferation and nuclear protein kinase C. Proc. Natl. Acad. Sci. USA. 89:7752-7758.
  29. Cousins, R. J. and R. J. McMahon. 2000. Integrative aspects of zinc transporters. J. Nutr. 130 (Suppl):1384-1387.
  30. Cui, H., F. Jing and P. Xi. 2003: pathology of the thymus, spleen and bursa of Fabricius in zinc deficient ducklings. Avian Pathol. 32(3):259-264.
  31. Cunningham-Rundles, S., R. S. Bockman, A. Lin, P. V. Giardina, M. W. Hilgartner, D. Caldwell-Brown and D. M. Carter. 1980. Physiological and pharmacological effects of zinc on immuneresponse., Ann. NY. Acad. Sci. 1980, 587, 113-122.
  32. Dardenne, M., J. M. Pleau, B. Nabarra, P. Lefancier, M. Derrien, J. Choay and J. E. Bach. 1982. Contribution of zinc and other metals to the biological activity of serum thymic factor. Proc. Natl. Acad. Sci. USA. 79:5370-5373.
  33. Donmezz, H. H., M. A. Karsli, I. Meral, N. Donmez and N. Simsek. 2002. Effects of increasing zinc supplementation in drinking water on growth and thyroid gland function and histology in broiler chicks. Deutsche Tierarztliche Wochenschrift 109(10):438-442.
  34. Dorke, E. A. and J. W. Spears. 1993: In vitro and in vivo immunological measurements in growing lambs fed diets deficient, marginal or adequate in zinc. J. Nutr. Immunol. 2:71.
  35. Dorke, E. A., G. P. Gengelbach and J. W. Spears. 1998. Influence of level and source (inorganic versus organic) of zinc supplementation on immune function in growing lambs. Asian-Aust. J. Anim. Sci. 11:139-144 https://doi.org/10.5713/ajas.1998.139
  36. Dowd, P. S., J. Kelher and P. J. Guillou. 1986. T-lymphocytes subsets and interleukin-2 production in zinc deficient rats. Br. J. Nutr. 55:59-69.
  37. Driessen, C., K. Hirv, L. Rink and H. Kirchner. 1994. Induction of cytokines by zinc ions in human peripheral blood mononuclear cells and separated monocytes. Lymphokine Cytokine Res. 13:15-20.
  38. Driessen, C., K. Hirv, H. Kirchner and L. Rink. 1995a. Zinc regulates cytokines induction by super antigens and lipopolysaccharides, Immunology. 84:272-277
  39. Driessen, C., K. Hirv, H. Kirchner and L. Rink. 1995b. Divergent effects of zinc on different bacterial pathogenic agents. J. Infect. Dis. 171:486-489 https://doi.org/10.1093/infdis/171.2.486
  40. Edwards, H. M. and D. H. Baker. 1999. Bioavailability of zinc in several sources of zinc oxide, zincs sulfate, and zinc metal. J. Anim. Sci. 77:2730-2735 https://doi.org/10.2527/1999.77102730x
  41. Endre, L., F. Beck and A. Prasad. 1990. The role of zinc in human health. J. Trace Elem. Exp. Med. 3:337.
  42. Feng, J. and J. Cheng. 1993: Effect of zinc on the function of immune cells in vitro. Acta. Nutriment Sincia. 15:275-279.
  43. Fenwick, P. K., P. J. Aggett, D. Macdonald C. Hubber and D. Wakelin 1990a. Zinc deficiency and zinc repletion: effect on the response of rat to infection with Trichinella spiralis. Am. J. Clin. Nutr. 52:166-172.
  44. Fenwick, P.K., P. J. Aggett, D. Macdonald, C. Hubber and D. Wakelin. 1990b. Zinc deprivation and zinc repletion: effect on the response of rats to infection with Strongyloides ratii. Am. J. Clin. Nutr. 52:173-177.
  45. Flagstad, T. 1976. Lethal trait A-46 in cattle. Intestinal zinc absorption. Nord. Veternaermed. 28:160-169.
  46. Fosmire, G. J. 1990. Zinc toxicity. Am. J. Clin. Nutr. 51:225-227.
  47. Fraker, P. J., M. E. Gershwin, R. A. Good and A. Prasad. 1986. Interrelationships between zinc and immune functions. Fed. Proc. 45:1474-1479.
  48. Fraker, P. J., L. King, B. Garvy and C. Medina. 1993. Immunopathology of zinc deficiency: a role for apoptosis In: Human Nutrition: A comprehensive Treatise (Ed. D. Klurfeld). Plenum Press. New York. pp. 267-283.
  49. Fraker, P. J. and W. Telford. 1997. A reappraisal of the role of zinc in the life and death decisions of life. Proc. Soc. Expt. Med. 215:229-236.
  50. Fraser, J. D., R. G. Urban, J. L. Strominger and H. Robinson. 1992. Zinc regulates the functionof two super antigens. Proc. Natl. Acad. Sci. USA. 89:5507-5511.
  51. Garvy, B., L. King, W. Telford, L. Morford and P. J. Fraker. 1993. Chronic level of corticosterone reduces the number of cycling cells of the B lineage in murine bone marrow and induces apoptsis. Immunology 80:587-592.
  52. GfE (Gesellschaft fur Errnahrungsphysiologie) Ausschu$\beta$ fur Bedarfsnormen. 1987. Empfehlungen zur Energie-und Nahrstoffversorgung der Schweine DLG-Verlag, Frankfurt (Main).
  53. GfE (Gesellschaft fur Errnahrungsphysiologie) Ausschu$\beta$ fur Bedarfsnormen. 1999. Empfehlungen zur Energie-und Nahrstoffversorgung der Legehennen und Masthuhnerr (broiler). DLG Verlag Frankfurt (Main).
  54. GfE (Gesellschaft fur Errnahrungsphysiologie) Ausschu$\beta$ fur Bedarfsnormen. 2001. Empfehlungen zur Energie-und Nahrstoffversorgung der Mastrinder DLG-Verlag, Frankfurt am (Main).
  55. GfE (Gesellschaft fur Errnahrungsphysiologie)Ausschu$\beta$ fur Bedarfsnormen. 2003. Empfehlungen zur Energie-und Nahrstoffversorgung der Mastputen DLG Verlag, Frankfurt (Main).
  56. Goldenberg, R. L., T. Tamura, Y. Neggers, R. L. Copper, K. E. Johnson, M. B. Dubard and J. C. Hauth. 1995. The effect of zinc supplementation on pregnancy outcome, J. Am. Med. Assoc. 274:463-468.
  57. Goswami, T. K., G. C. Ram and D. K. Singh. 2002. Influence of zinc on the immune system. Pashudhan, 17:4,8.
  58. Greene, L. W., D. K. Lunt, F. M. Byers, N. K. Chirase, C. E. Richmond, R. E. Knutson and G. T. Schelling. 1988. Performance and carcass quality of steers supplemented with zinc oxide and zinc methionine. J. Anim. Sci. 66:1818-1823.
  59. Greskas, D., P. Alivanis, N. Kotzadamis, M. Kiriazopoulos and A. Tourkantonis. 1992. Influenza vaccination in chronic haemodialysis patients. The effect of zinc supplementation. Renal Failuure. 14:575-578.
  60. Hadden, J. W. 1995. The treatment of zinc as immunotherapy. Int. J. Immunopharmacol. 17:697-701. https://doi.org/10.1016/0192-0561(95)00062-7
  61. Hambidge, K. M., C. E. Casey and N. F. Krebs. 1986. Zinc. In: Trace elements in human and animal nutrition, Vo.2 (Ed. W. Mertz) Academic Press, San Diego. pp. 1-37.
  62. Hambidge, K. M. and P. A. Walravens. 1982. Disorders of mineral metabolism. Clin. Gastroenterol. 11:87-118.
  63. Hatfield, P. G., B. L. Robinson, D. L. Minikheim, R. W. Kott, N. I. Roth, J. T. Daniels and C. K. Swenson. 2002. J. Anim. Sci. 80:1329-1334.
  64. Hempe, J. M. and R. J. Cousins. 1989: Effects of EDTA and zinc methionin complex on zinc absorption by rat intestine. J. Nutr. 119:1179-1187.
  65. Humphery-Smith, I. and W. Blackstock. 1997. Proteome analysis: genomic via the out put rather than input code. J. Prot. Chem. 16:537-544.
  66. Keen, C. and M. Gershwin. 1990. Zinc deficiency and immune function. Ann. Rev. Nutr. 10:415-431.
  67. Kehrli, M. E., Jr., M. R. Ackermann, D. E. Shuster, M. J. Van Der Maaten, F. C. Schmalstieg, D. C. Anderson and B. J. Hughes. 1992. Animal model of human disease: Bovine leucosis adhesion deficiency: B2 integrin deficiency in young Holstein cattle. Am. J. Pathol. 140:1489-1492.
  68. Kelin, D. and T. Mann. 1939. Carbonic anhydrase. Nature 144:442-443.
  69. Kidd, M. T., M. A. Qureshi, P. R. Ferkett and L. N. Thomas. 1994a. Blood clearance of Escherichia coli and evaluation of mononuclear phagocytic system as influenced by supplemental dietary zinc-methionine in young turkeys. Poult. Sci. 73:1381-1389.
  70. Kidd, M. T., M. A. Qureshi, P. R. Ferkett and L. N. Thomas. 1994b. Dietary zinc-methionine enhances mononuclear phagocytic function in young turkeys. Biol. Trace. Elmt. Res. 42:217-229.
  71. Kim, J., R. G. Urban, J. L. Strominger and D. C. Wiley. 1994. Toxic shock syndrome toxin-1 complexed with a Class-II major histocompatibility molecule HLA-DR-I. Science 266:1870-1878.
  72. Kincaid, R. L., B. P. Chew and J. D. Cronrath. 1997. Zinc oxide and amino acids as source of dietary zinc for calves: Effects on uptake and immunity. J. Dairy. Sci. 80:1381-1388.
  73. King, J. C. 1990. Assessment of zinc status. J. Nutr. 120 (Suppl): 1474-1479. https://doi.org/10.1093/jn/120.suppl_11.1474
  74. Kirchner, H. and H. Ruhl. 1970. Stimulation of human peripheral lymphocytes by $Zn^{2+}$ in vitro. Exp. Cell. Res. 61:229-230.
  75. Klingman, D. and D. C. Hilt. 1988. The S-100 protein family. TIBS. 13:437.
  76. Klosterhalfen, B., C. Tons, S. Hauptmann, L. Tietze, F. A. Offner, W. Kupper and C. J. Kirpatrick. 1996. Influence of heat shock protein 70 and metallothioneins induction by zinc-bis (DLhydrogenaspartate) on the release of inflammatory mediators in a porcine model of recurrent endotoxemia. Biochem. Pharmacol. 52:1201-1210.
  77. Kraehenbuhl, J. P. and M. R. Neutra. 2000. Epithelial M cells: differentiation and function. Ann. Rev. Cell. Devp. Biol. 16:301-332.
  78. Kriegesmann, B., S. Jansen, B. Baumgartner and B. Brening. 1997. Partial genomic structure of bovine CD 18 gene and the refinement of test for bovine leukocyte adhesion deficiency. J. Dairy. Sci. 80(10):2547-2549.
  79. Kroneman, J., G. J. W. Van de Mey and A. Helder. 1975. Hereditary zinc deficiency in Dutch Frisian cattle. Zentrabl. Veterinaermed. Reihe A. 22:201-208.
  80. Lachance, P. A. 1998. International perspective: Basis need and application of RDA. Nutr. Rev. 56(4):S2-S4.
  81. Lee, S. H.., S. C. Choi, B. J. Chae, S. P. Acda and Y. K. Han. 2001a. Effects of feeding different chelated copper and zinc sources on growth performance and fecal excretion of weaning pigs. Asian-Aust. J. Anim. Sci. 14:1616-1620.
  82. Lee, S. H., S. C. Choi, B. J. Chae, J. K. Lee and S. P. Acda. 2001b. Evaluation of metal amino acid chelates and complexes at various levels of copper and zinc in weanling pigs and broilers chicks. Asian-Aust. J. Anim. Sci. 14:1734-1740.
  83. Lim, H. S. and I. K. Paik. 2003. Effects of supplementing minerals methionine chelates (Zn, Cu, Mn) on the performance and eggshell quality of laying hens. Asian-Aust. J. Anim. Sci. 16:1804-1808.
  84. Mavromichalis, I., C. M. Peter, T. M. Parr, D. Ganessunker and D. H. Baker. 2000: Growth promoting efficacy in young pigs of two sources of zinc oxide having either a high or a low bioavailability of zinc. J. Anim. Sci. 78:2896-2902.
  85. Mavromichalis, I., D. M. Webel, E. N. Parr and D. H. Baker. 2001. Growth promoting efficacy of pharmacological doses of tetrabasic zinc chloride in diets for nursery pigs. Can. J. Anim. Sci. 81:367-391.
  86. Mc Cance, R. A. and E. M. Widdowson. 1942. The absorption and excretion of zinc. Biochem. J. 36:692-696.
  87. Mignotte, B. and J. Vayssier. 1998. Mitochondria and apoptosis. Eur. J. Biochem. 252:1-15.
  88. Milne, D. B., N. V. Ralston and J. C. Wallwork. 1985. Zinc content of blood cellular components and lymphnode and spleen lymphocytes in severely zinc deficient rats. J. Nutr. 115:1073-1078.
  89. Moochegiani, E., L. Santareilli, M. Muzzioli and N. Fabris. 1995. Reversibility of the thymic involution and of age related peripheral immune dysfunction by zinc supplementation in old mice. Int. J. Immunopharmacol. 17:703-718.
  90. Murthy, A. R. K., R. I. Lehrer, S. S. L. Harwig and K. T. Miyasaki. 1993. Invitro candidastatic properties of the human neutrophil calprotectin complex. J. Immunol. 151:6291-6301.
  91. Naresh, R., S. K. Dwivedi, S. Dey and D. Swarup. 2001. Zinc, Copper and cobalt concentration in blood during inflammation of the mammary gland in dairy cow. Asian-Aust. J. Anim. Sci. 14:564-566.
  92. National Research Council. 1981. Nutrient requirements of Goats; Angora, Dairy and Meat goats in temperate and tropical countries. 5th Ed. National Academy Press, Washington, DC.
  93. National Research Council. 1985. Nutrient requirements of sheep. 6th Ed. National Academy Press. Washington, DC.
  94. National research Council. 1989a. Recommended Dietary Allowances, 10th Ed. National Academy Press. Washington, DC.
  95. National research Council. 1989b. Nutrient Requirements of dairy cattle. 6th Ed. National Academy Press. Washington, DC.
  96. National Research Council. 2001. Nutrient Requirements of dairy cattle. 7th revised Ed. National Academy Press, Washington, DC.
  97. O’Quinn, P. R., J. R. Bergstorm, J. L. Nelssen, M. D. Tokach, S. S. Dritz and R. D. Goodband. 1997. The interactive effects between diet complexity, zinc oxide and feed grade antibiotics on performance of segregated early weaned pigs. J. Anim. Sci. 75 (Suppl):192 (Abstr.).
  98. Origino, C. and G. Yang. 1978. Requirement of rainbow trout for dietary zinc. Bull. Jpn. Soc. Sci. Fish 44:1015-1018.
  99. Park, J. H., C. J. Grandjean, D. L. Antoson and J. A. Vander hoof. 1986. Effects of isolated zinc deficiency on the composition of skeletal muscles, liver and bone during growth in rats. J. Nutr. 116:610-617.
  100. Perryman, L. E., D. R. Leach, W. C. Davis, W. D. Mikelsen, S. R. Heller, H. D. Ochs, J. A. Ellis and E. Brummerstedt. 1989. Lymphocyte alterations in zinc deficient calves with lethal trait A 46. Vet. Immuunol. Immunopathol. 21:239-248.
  101. Pimentel, J. L., M. E. Cook and J. L. Gregor. 1991. Immuneresponse of chicks fed various level of zinc. Poult. Sc. 70:947.
  102. Poulsen, H. D. 1995. Zinc oxide for weanling pigs. Acta. Agric. Scandinavica Sect. A 45:159-167.
  103. Poulsen, R. D. and D. Carlson. 2001. Bioavailabality of zinc from different zinc sources. In: proc. 52nd Annual Meeting of European Association of Animal Production, Budapest, Hungary. EAAP publication. p. 123 (Abstr).
  104. Prasad, A. S., J. A. Halsted and M. Nadimi. 1961. Syndrome of iron deficiency anemia, hepato spleenomegaly, hypogonadism, dwarfism and geophagia. Am. J. Med. 31:532.
  105. Prasad, A. S. 1983. Clinical, biochemical and nutritional spectrum of zinc deficiency in human subjects an update. Nutr. Rev. 41:197-208. https://doi.org/10.1111/j.1753-4887.1983.tb07155.x
  106. Prasad, A. S. 1995. Zinc: An overview. Nutr. 11:93-99.
  107. Price, J. and D. A. Wood. 1982. Zinc responsive parakeratosis and ill thrift in Friesian cattle. Vet. Rec.110:478.
  108. Rajagopalan, S., C. C. Winter, N. Waghman and E. O. Lung. 1995. The immunoglobulin related killer cell inhibitory receptor binds zinc and require zinc for recognition on HLA-C on target T cells. J. Immunol. 155:4143-4146.
  109. Raulin, J. 1869. Etudes chimique sur Ia vegetation (Chemical studies on plants). Annales des Sciences Naturrelles Botanique at Biologie Vegetale 11:293-299.
  110. Rawer, P., W. R. Willems, T. Breidenbach, W. Guttmann, W. Pabst and G. Schutterle. 1987. Seroconverson rate of hepatitis B vaccination, haemodialysis and zinc supplementation. Kidney. Intn. 22S:149-152.
  111. Rink, L. and P. Gabriel. 2000. Zinc and immune system. Proc. Nutr. Soc. 59:541-552.
  112. Roberts, E. S., E. VanHeugten, K. Lloyd, G. W. Almond and J. W. Spears. 2002. Dietary zinc effects on growth performance and immune response of endotoxemic growing pigs. Asian-Aust. J. Anim. Sci. 15:1496-1501.
  113. Rucker, R. B., B. Lonnerdal and J. L. Keen. 1994. Intestinal absorption of nutritionally important trace minerals. In: Physiology of the intestinal tract, 3rd Ed. (Ed. L. R. Johnson) Raven Press, New York. pp. 2183-2202.
  114. Sazawal, S., R. E. Black, S. Jalla, S. Mazumdar, A. Sinha and M. K. Bhann. 1998. Zinc supplementation reduces the incidence of acute lower respiratory infection in infants and preschool children: a double blind control trial. Pediatrics. 102:1-4.
  115. Schwartzman, R. and J. Cidlowski. 1993. Apoptosis the biochemistry and molecular biology of programmed cell death. Endicr. Rev. 14:133-151.
  116. Scott, M. E. and K. G. Koski. 2000. Zinc deficiency impairs immune response against parasitic nematode infections at intestinal and systemic sites. J. Nutr. 130 (Suppl):1412 S-1420 S.
  117. Sharma, M. C. and C. Joshi. 2002. Serum mineral and hematological profile of microfilaria infected cattle in India. Its effects on production and therapy. Asian-Aust. J. Anim. Sci. 15:357-367.
  118. Shi, H. N., M. E. Scott, M. M. Stevenson and K. G. Koski. 1994. Zinc deficiency impairs T cell function in mice with primary infection of Heligmosomoides polygyrus. Parasite Immunol. 16:339-350.
  119. Shi, H. N., M. E. Scott, K. G. Koski and M. M. Stevenson. 1995. Energy restriction and severe zinc deficiency influence growth survival and reproduction of Heligmosomoides polygyrus Parasitology 100:599-609.
  120. Shi, H. N., M. E. Scott, M. M. Stevenson and K. G. Koski. 1998. Energy restriction and zinc deficiency impair the function of murine T cells and antigen presenting cells during gastrointestinal nematode infection. J. Nutr. 128:20-27.
  121. Simkin, P. A. J. 1997. Zinc, Again. Rheumatol. 24:626-628.
  122. Singh, C. and S. P. S. Singha. 2002. Effect of dexamethasone stress on concentration of zinc in blood plasma and subcellular fraction of various tissues of neonatal buffalo calves. Asian-Aust. J. Anim. Sci. 15:1022-1025.
  123. Smeyers-Verbeke, J., C. May, P. Drochmans and D. L. Massart. 1977. The determination of Cu, Zn. and Mn in subcellular rat liver fractions. Anal. Biochem. 83:746-753.
  124. Sobociniski, P. J., W. J. Canterbury Jr. and M. C. Powanda. 1977. Differential effect of parenteral zinc on the course of various bacterial infections. Proc. Soc. Exp. Biol. Med. 156:334-339.
  125. Sohnle, P. G., C. Collins-Lech and J. H. Wiessner. 1991. The zinc reversible antimicrobial activity of neutrophil lysates and abscess fluid supernatants. J. Infct. Dis. 164:137-142.
  126. Sorderberg, T. A., B. Sunzel, S. Holm, T. Elmros, G. Hallman and S. Sjoberg. 1990. Antibacterial effect of zinc oxide in vitro. Scand. J. Plast. Reconstr. Surg. Hand. Surg. 24:193-197.
  127. Spears, J. W. 1989. Zinc methionine for ruminants: Relative bioavailability of zinc in lambs and effects of growth and performance of growing heifers. J. Anim. Sci. 67:835-843. https://doi.org/10.2527/jas1989.673835x
  128. Spears, J. W. and E. B. Kegley. 2002. Effect of zinc source (zinc oxide vs. zinc proteinate) and level on performance carcass characteristics, and immune response of growing and finishing steers. J. Anim. Sci. 80:2747-2752.
  129. Spears, J. W., R. W. Harvey and T. T. Brown. 1991. Effect of zinc methionine and zinc oxide on performance, blood characteristics, and antibody titre response to viral vaccination in stressed feeder calves. J. Am. Vet. Med. Assoc. 199:1731-1733.
  130. Stahl, J. L., M. E. Cook, M. L. Sunde and J. L. Greeger. 1989. Enhanced humoral immunity in progeny chicks from hens fed practical diets supplemented with zinc. Appl. Agric. Res. 4(2):86-89
  131. Sandstead, H. H. 1994. Understanding zinc: recent observation and interpretation. J. Lab. Clin. Med. 124:322-327.
  132. Sundstrom, M., L. Abrahamsen, P. Antonsson, K. Mehindate, W. Mourad and M. Dohlsten. 1996. The crystal structure of staphylococcal enterotoxin type D reveals $zinc^{2+}$ mediated homodimerization. EMBO. J. 15:6832-6840.
  133. Svetic, A., K. B. Madden, Z. di zhou, P. Lu, I. M. Katona, F. D. Finkelman, J. F. Urban and W. C. Gause. 1993. A primary intestinal helminthic infection rapidly induces a gut-associated elevation of Th-2 associated cytokines and IL-3. J. Immunol. 150:3434-3441.
  134. Tanaka, Y., S. Shiozawa, I. Morimoto and T. Fujita. 1989. Zinc inhibit pokeweed mitogen-induced development of immunoglobulin-secreting cells through augmentation of both CD4 and CD8 cells. Int. J. Immunopharmacol. 11:673-679.
  135. Thiers, R. E. and B. L. Vallee. 1957. Distribution of metals in subcellular fractions of rat liver. J. Biol. Chem. 226:911-920.
  136. Tilden, W. P., E. C. Arthur and S. L. Roberts. 1990. The macro minerals In: feeds and feeding. Prentice Hall, New Jersey. pp. 114-116.
  137. Todd, W. R., C. A. Elvehejem and E. B. Harrt. 1934. Zinc in the nutrition of the rat. Am. J. Physiol. 107:146-156.
  138. Tucker, H. F. and W. D. Salmon. 1955. Parakeratosis or zinc deficiency disease in the pig. Proc. Soc. Exp. Biol. Med. 88:613-616.
  139. Turk, S., S. Bozfakioglu, S. T. Ecder, T. Kahraman, N. Gurel, N. Aysuna, A. Turkmen, N. Bekiroglu and E. Ark. 1998. Effects of zinc supplementation on the immune system and on antibody response to multivalent influenza vaccine in haemodialysis patients. Int. J. Artif. Org. 21:274-278.
  140. Urban, J. F., I. M. Katona, W. E. Paul and F. D. Frinkelman. 1991. Interleukin-4 is important in protective immunity in gastrointestinal nematodes of mice. Proc. Natl. Acad. Sci. USA. 88:3513-3517.
  141. Vallee, B. L. 1955. Zinc and metalloenzymes. Adv. Protein. Chem. 10:317-325. https://doi.org/10.1016/S0065-3233(08)60108-4
  142. Vallee, B. L. and J. G. Gibson. 1948. The content of normal human whole blood plasma leukocytes and erythrocytes. J. Biol. Chem. 176:445-457.
  143. Vierboom, M. M., T. E. Engle and C. V. Kimberling. 2003. Effect of gestational status on apparent absorption and retention of copper and zinc in mature Angus cows and suffolk ewes. Asian-Aust. J. Anim. Sci. 16:515-518.
  144. Wellinghausen, N., A. B. Schromm, U. Seydel, K. Brandenburg, J. Luhm, H. Kirchner and L. Rink. 1996a. Zinc enhances lipopolysaccharides induced monokines secretion by a fluidity change of lipopolysaccharides. J. Immunol. 157:3139-3145.
  145. Wellinghausen, N., A. Fischer, H. Kirchner and L. Rink. 1996b. Interaction of zinc ions with human peripheral blood mononuclear cells. Cell. Immunol. 171:255-261.
  146. Wellinghausen, N., H. Kirchner and L. Rink. 1997a. The immunobiology of zinc. Immunol. Today. 18:519-521.
  147. Wellinghausen, N., M. Martin and L. Rink. 1997b. Zinc inhibit IL-1 dependant T cell stimulation. Eur. J. Immunol. 27:2529-2535.
  148. Wellinghausen, N., M. Martin and L. Rink. 1999. Zinc status in patients with alveolar echinococcus is related to disease progression. Parasit. Imm. 21:237-241.
  149. Wight, P. A. L., W. A. Dewar and G. M. Mackenzie. 1980. Monocytes in experimental zinc deficiency of domestic birds. Avian. Pathol. 9:61-66.
  150. Wirth, J. J., P. Praker and F. Kierszenbaum. 1989. Zinc requirement for macrophage function: effect of zinc deficiency on uptake and killing of a protozoan parasite. Immunology. 68:114-119.
  151. Wu, J., J. He and D. Xu. 1998. Effect of zinc deficiency on thymus development and its mechanism in rats. Acta. Nutriment Sincia. 20:303-306.
  152. Zhang, R. and Y. Zhou. 1998. The effect of zinc on immune function in animals. Anim. Sci. Abroad. 25:3-8.
  153. Zhang, R., Y. Zhou, Y. Huang and H. Yang. 1999. The modulation effects of zinc on immune organs development and function in broiler. Acta Veterinaria Zootechnia Sinica. 30:504-512.
  154. Zhou, P. and J. Wu. 1995. The effect of zinc deficiency on T cellular immunity in mice. Acta Nutriment Sincia 17:78-81.

Cited by

  1. Effect of dose and source of supplemental zinc on immune response and oxidative enzymes in lambs vol.33, pp.7, 2009, https://doi.org/10.1007/s11259-009-9212-9
  2. Case-Control Study of a Multistate Equine Herpesvirus Myeloencephalopathy Outbreak vol.27, pp.2, 2013, https://doi.org/10.1111/jvim.12051
  3. Effects of zinc supplementation on catch-up growth in children with failure to thrive vol.11, pp.6, 2017, https://doi.org/10.4162/nrp.2017.11.6.487
  4. Immunomodulatory basis of antioxidant therapy and its future prospects: an appraisal vol.25, pp.5, 2017, https://doi.org/10.1007/s10787-017-0393-5
  5. Evaluation of immunomodulatory activity of Glycyrhiza glabra L roots in combination with zing vol.2, pp.1, 2012, https://doi.org/10.1016/S2221-1691(12)60122-1
  6. Relative availability of zinc in ground beef and soybean protein for young swine compared with zinc carbonate as the standard1 vol.92, pp.6, 2014, https://doi.org/10.2527/jas.2013-6921
  7. Mineral Status of Soils and Forages in Southwestern Punjab-Pakistan: Micro-minerals vol.19, pp.8, 2006, https://doi.org/10.5713/ajas.2006.1139
  8. Effects of Trace Mineral Supplementation and Source, 30 Days Post-weaning and 28 Days Post Receiving, on Performance and Health of Feeder Cattle vol.19, pp.10, 2006, https://doi.org/10.5713/ajas.2006.1450
  9. Studies on Vitamin Mineral Interactions in Relation to Passive Transfer of Immunoglobulins in Buffalo Calves vol.19, pp.6, 2005, https://doi.org/10.5713/ajas.2006.825
  10. Effects of Supplementing with Single or Multiple Trace Minerals on Growth Performance, Fecal Mineral Excretion and Nutrient Utilization in Pullets from 1 to 18 Weeks of Age vol.20, pp.6, 2005, https://doi.org/10.5713/ajas.2007.976
  11. Effects of Varying Dietary Zinc Levels and Environmental Temperatures on the Growth Performance, Feathering Score and Feather Mineral Concentrations of Broiler Chicks vol.23, pp.7, 2005, https://doi.org/10.5713/ajas.2010.90495
  12. Phosphorus, calcium, and magnesium contents of pasture and their effect on body condition scores and body mass of communal cattle depending on natural pasture of Mogosane Village, of the North-West Pr vol.51, pp.7, 2005, https://doi.org/10.1007/s11250-019-01908-z
  13. Micronutrients as immunomodulatory tools for COVID-19 management vol.220, pp.None, 2020, https://doi.org/10.1016/j.clim.2020.108545
  14. Pityriasis capitis: Causes, pathophysiology, current modalities, and future approach vol.20, pp.1, 2005, https://doi.org/10.1111/jocd.13488