The Journal of Nutritional Biochemistry
Volume 18, Issue 12 , Pages 813-819 , December 2007

Moderate zinc deficiency negatively affects biomechanical properties of rat tibiae independently of body composition

  • Angus G. Scrimgeour

      Affiliations

    • Military Nutrition Division, U.S. Army Research Institute of Environmental Medicine, Natick, MA 01760-5007, USA
    • Corresponding Author InformationCorresponding author. Tel.: +1 508 233 5155; fax: +1 508 233 4869.
  • ,
  • Chad H. Stahl

      Affiliations

    • Animal Science Department, Iowa State University, Ames, IA 50011-3150, USA
  • ,
  • James P. McClung

      Affiliations

    • Military Nutrition Division, U.S. Army Research Institute of Environmental Medicine, Natick, MA 01760-5007, USA
  • ,
  • Louis J. Marchitelli

      Affiliations

    • Military Nutrition Division, U.S. Army Research Institute of Environmental Medicine, Natick, MA 01760-5007, USA
  • ,
  • Andrew J. Young, PhD

      Affiliations

    • Military Nutrition Division, U.S. Army Research Institute of Environmental Medicine, Natick, MA 01760-5007, USA

Received 6 July 2006 ,Revised 20 November 2006 ,Accepted 28 December 2006.

References 

  1. Calhoun NR, Smith JC, Becker KL. The role of zinc in bone metabolism. Clin Orthop. 1974;103:212–234
  2. Suwarnasarn A, Wallwork JC, Lykken GI, Low FN, Sandstead HH. Epiphyseal plate development in the zinc-deficient rat. J Nutr. 1982;112(7):1320–1328
  3. Bougle DL, Sabatier JP, Guaydier-Souquieres G, Guillon-Metz F, Laroche D, Jauzac P, et al. Zinc status and bone mineralisation in adolescent girls. J Trace Elem Med Biol. 2004;18(1):17–21
  4. Doherty CP, Crofton PM, Sarkar MA, Shakur MS, Wade JC, Kelnar CJ, et al. Malnutrition, zinc supplementation and catch-up growth: changes in insulin-like growth factor I, its binding proteins, bone formation and collagen turnover. Clin Endocrinol. 2002;57(3):391–399
  5. Elmstahl S, Gullberg B, Janzon L, Johnell O, Elmstahl B. Increased incidence of fractures in middle-aged and elderly men with low intakes of phosphorus and zinc. Osteoporos Int. 1998;8(4):333–340
  6. Hyun TH, Barrett-Connor E, Milne DB. Zinc intakes and plasma concentrations in men with osteoporosis: the Rancho Bernardo Study. Am J Clin Nutr. 2004;80(3):715–721
  7. Peretz A, Papadopoulos T, Willems D, Hotimsky A, Michiels N, Siderova V, et al. Zinc supplementation increases bone alkaline phosphatase in healthy men. J Trace Elem Med Biol. 2001;15(2–3):175–178
  8. Eberle J, Schmidmayer S, Erben RG, Stangassinger M, Roth HP. Skeletal effects of zinc deficiency in growing rats. J Trace Elem Med Biol. 1999;13(1–2):21–26
  9. Hosea HJ, Taylor CG, Wood T, Mollard R, Weiler HA. Zinc-deficient rats have more limited bone recovery during repletion than diet-restricted rats. Exp Biol Med. 2004;229(4):303–311
  10. Ovesen J, Moller-Madsen B, Thomsen JS, Danscher G, Mosekilde L. The positive effects of zinc on skeletal strength in growing rats. Bone. 2001;29:565–570
  11. Rossi L, Migliaccio S, Corsi A, Marzia M, Bianco P, Teti A, et al. Reduced growth and skeletal changes in zinc-deficient growing rats are due to impaired growth plate activity and inanition. J Nutr. 2001;131(4):1142–1146
  12. Seco C, Revilla M, Hernández ER, Gervás J, González-Riola J, Villa LF, et al. Effects of zinc supplementation on vertebral and femoral bone mass in rats on strenuous treadmill training exercise. J Bone Miner Res. 1998;13(3):508–512
  13. Angus RM, Sambrook PN, Pocock NA, Eisman JA. Dietary intake and bone mineral density. Bone Miner. 1988;4(3):265–277
  14. New SA, Bolton-Smith C, Grubb DA, Reid DM. Nutritional influences on bone mineral density: a cross-sectional study in premenopausal women. Am J Clin Nutr. 1997;65(6):1831–1839
  15. Relea P, Revilla M, Ripoll E, Arribas I, Villa LF, Rico H. Zinc, biochemical markers of nutrition, and type I osteoporosis. Age Ageing. 1995;24(4):303–307
  16. Otsuka M, Ohshita Y, Marunaka S, Matsuda Y, Ito A, Ichinose N, et al. Effect of controlled zinc release on bone mineral density from injectable Zn-containing beta-tricalcium phosphate suspension in zinc-deficient diseased rats. J Biomed Mater Res. 2004;69A(3):552–560
  17. Yamaguchi M, Yamaguchi R. Action of zinc on bone metabolism in rats. Increases in alkaline phosphatase activity and DNA content. Biochem Pharmacol. 1986;35(5):773–777
  18. Yamaguchi M, Oishi H, Suketa Y. Zinc stimulation of bone protein synthesis in tissue culture. Activation of aminoacyl-tRNA synthetase. Biochem Pharmacol. 1988;37(21):4075–4080
  19. Matsui T, Yamaguchi M. Zinc modulation of insulin-like growth factor's effect in osteoblastic MC3T3-E1 cells. Peptides. 1995;16(6):1063–1068
  20. Moonga BS, Dempster DW. Zinc is a potent inhibitor of osteoclastic bone resorption in vitro. J Bone Miner Res. 1995;10(3):453–457
  21. Holloway WR, Collier FM, Herbst RE, Hodge JM, Nicholson GC. Osteoblast-mediated effects of zinc on isolated rat osteoclasts: inhibition of bone resorption and enhancement of osteoclast number. Bone. 1996;19(2):137–142
  22. Freudenheim JL, Johnson NE, Smith EL. Relationships between usual nutrient intake and bone-mineral content of women 35–65 years of age: longitudinal and cross-sectional analysis. Am J Clin Nutr. 1986;44(6):863–876
  23. DeRuisseau KC, Cheuvront SN, Haymes EM, Sharp RG. Sweat iron and zinc losses during prolonged exercise. Int J Sport Nutr Exerc Metab. 2002;12(4):428–437
  24. King JC, Shames DM, Woodhouse LR. Zinc homeostasis in humans. J Nutr. 2000;130(5S Suppl):1360S–1366S
  25. Herzberg M, Foldes J, Steinberg R, Menczel J. Zinc excretion in osteoporotic women. J Bone Miner Res. 1990;5(3):251–257
  26. Rico H, Villa LF. Zinc, a new coherent therapy for osteoporosis?. Calcif Tissue Int. 2000;67(5):422–423
  27. Gur A, Colpan L, Nas K, Cevik R, Sarac J, Erdogan F, et al. The role of trace minerals in the pathogenesis of postmenopausal osteoporosis and a new effect of calcitonin. J Bone Miner Metab. 2002;20(1):39–43
  28. Yamaguchi M, Ehara Y. Zinc decrease and bone metabolism in the femoral–metaphyseal tissues of rats with skeletal unloading. Calcif Tissue Int. 1995;57(3):218–223
  29. Nakamura T, Nishiyama S, Futagoishi-Suginohara Y, Matsuda I, Higashi A. Mild to moderate zinc deficiency in short children: effect of zinc supplementation on linear growth velocity. J Pediatr. 1993;123(1):65–69
  30. Hunt JR, Johnson LK. Dietary protein, as egg albumen: effects on bone composition, zinc bioavailability and zinc requirements of rats, assessed by a modified broken-line model. J Nutr. 1992;122(1):161–169
  31. Hambidge KM, Hambidge C, Jacobs M, Baum JD. Low levels of zinc in hair, anorexia, poor growth, and hypogeusia in children. Pediatr Res. 1972;6(12):868–874
  32. Gibson RS, Vanderkooy PD, MacDonald AC, Goldman A, Ryan BA, Berry M. A growth-limiting, mild zinc-deficiency syndrome in some southern Ontario boys with low height percentiles. Am J Clin Nutr. 1989;49(6):1266–1273
  33. Reeves PG, Nielsen FH, Fahey GC. AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J Nutr. 1993;123(11):1939–1951
  34. McClung JP, Stahl CH, Marchitelli LJ, Morales-Martinez N, Makin KM, Young AJ, et al. Effects of dietary phytase on body weight gain, body composition, and bone biomechanics in growing rats fed a low zinc diet. J Nutr Biochem. 2006;170:190–196
  35. Van Wouwe JP, Veldhuizen M. Growth characteristics in laboratory animals fed zinc-deficient, copper-deficient, of histidine-supplemented diets. Biol Trace Elem Res. 1996;55(1–2):71–77
  36. Fernandez-Madrid F, Prasad AS, Oberleas D. Effect of zinc deficiency on nucleic acids, collagen, and noncollagenous protein of the connective tissue. J Lab Clin Med. 1973;82(6):951–961
  37. Harada S, Rodan GA. Control of osteoblast function and regulation of bone mass. Nature. 2003;423(6937):349–355
  38. Parfitt AM. What is the normal rate of bone remodeling?. Bone. 2004;35(1):1–3
  39. Ahlborg HG, Johnell O, Turner CH, Rannevik G, Karlsson MK. Bone loss and bone size after menopause. N Engl J Med. 2003;349(4):327–334
  40. Bennell K, Matheson G, Meeuwisse W, Brukner P. Risk factors for stress fractures. Sports Med. 1999;28(2):91–122
  41. Salgueiro MJ, Torti H, Meseri E, Weill R, Orlandini J, Urriza R, et al. Dietary zinc effects on zinc, calcium, and magnesium content in bones of growing rats. Biol Trace Elem Res. 2006;110(1):73–78
  42. Leek JC, Keen CL, Vogler JB, Golub MS, Hurley LS, Hendrickx AG, et al. Long-term marginal zinc deprivation in rhesus monkeys. IV. Effects on skeletal growth and mineralization. Am J Clin Nutr. 1988;47(5):889–895
  43. Golub MS, Keen CL, Gershwin ME, Styne DM, Takeuchi PT, Ontell F, et al. Adolescent growth and maturation in zinc-deprived rhesus monkeys. Am J Clin Nutr. 1996;64(3):274–282
  44. Seeman E. The structural basis of bone fragility in men. Bone. 1999;25(1):143–147
  45. Jamieson JA, Taylor CG, Weiler HA. Marginal zinc deficiency exacerbates bone lead accumulation and high dietary zinc attenuates lead accumulation at the expense of bone density in growing rats. Toxicol Sci. 2006;92(1):286–294
  46. Hill T, Meunier N, Andriollo-Sanchez M, Ciarapica D, Hininger-Favier I, Polito A, et al. The relationship between the zinc nutritive status and biochemical markers of bone turnover in older European adults: the ZENITH study. Eur J Clin Nutr. 2005;59(Suppl 2):S73–S78
  47. Nielsen FH, Milne DB. A moderately high intake compared to a low intake of zinc depresses magnesium balance and alters indices of bone turnover in postmenopausal women. Eur J Clin Nutr. 2004;58(5):703–710
  48. Bauer DC. Biochemical markers of bone turnover: the study of osteoporotic fracture. In:  Eastell R editors. Bone markers: biochemical and clinical perspectives. London: Martin Dunitz; 2001;p. 219–223
  49. Tanimoto H, Lau KH, Nishimoto SK, Wergedal JE, Baylink DJ. Evaluation of the usefulness of serum phosphatases and osteocalcin as serum markers in a calcium depletion–repletion rat model. Calcif Tissue Int. 1991;48(2):101–110
  50. Rath NC, Huff GR, Huff WE, Balog JM. Factors regulating bone maturity and strength in poultry. Poult Sci. 2000;79(7):1024–1032

 This study was funded by the U.S. Army MRMC. The opinions or assertions contained herein are the private views of the authors and are not to be construed as official or as reflecting the views of the Army or the Department of Defense.

PII: S0955-2863(07)00044-7

doi: 10.1016/j.jnutbio.2006.12.018

The Journal of Nutritional Biochemistry
Volume 18, Issue 12 , Pages 813-819 , December 2007