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Osteoporosis International

, Volume 20, Issue 11, pp 1853–1861 | Cite as

Protective effect of total and supplemental vitamin C intake on the risk of hip fracture—a 17-year follow-up from the Framingham Osteoporosis Study

  • S. Sahni
  • M. T. Hannan
  • D. Gagnon
  • J. Blumberg
  • L. A. Cupples
  • D. P. Kiel
  • K. L. TuckerEmail author
Original Article

Abstract

Summary

Vitamin C may play a role in bone health. In the Framingham Study, subjects with higher total or supplemental vitamin C intake had fewer hip fractures and non-vertebral fractures as compared to subjects with lower intakes. Therefore, vitamin C may have a protective effect on bone health in older adults.

Introduction

Dietary antioxidants such as vitamin C may play a role in bone health. We evaluated associations of vitamin C intake (total, dietary, and supplemental) with incident hip fracture and non-vertebral osteoporotic fracture, over a 15- to 17-year follow-up, in the Framingham Osteoporosis Study.

Methods

Three hundred and sixty-six men and 592 women (mean age 75 ± 5 years) completed a food frequency questionnaire (FFQ) in 1988–1989 and were followed for non-vertebral fracture until 2003 and hip fracture until 2005. Tertiles of vitamin C intake were created from estimates obtained using the Willett FFQ, after adjusting for total energy (residual method). Hazard ratios were estimated using Cox-proportional hazards regression, adjusting for covariates.

Results

Over follow-up 100 hip fractures occurred. Subjects in the highest tertile of total vitamin C intake had significantly fewer hip fractures (P trend = 0.04) and non-vertebral fractures (P trend = 0.05) compared to subjects in the lowest tertile of intake. Subjects in the highest category of supplemental vitamin C intake had significantly fewer hip fractures (P trend = 0.02) and non-vertebral fractures (P trend = 0.07) compared to non-supplement users. Dietary vitamin C intake was not associated with fracture risk (all P > 0.22).

Conclusion

These results suggest a possible protective effect of vitamin C on bone health in older adults.

Keywords

Ageing Bone Fracture Nutrition Population studies Vitamin C 

Notes

Funding sources

This study was supported by the United States Department of Agriculture, Agriculture Research Services agreement number 58-1950-7-707; Framingham Osteoporosis grant number R01 AR/AG 41398; and the NHLBI’s Framingham study contract grant number N01-HC-25195.

Conflicts of interest

None.

References

  1. 1.
    Riggs BL, Melton LJ 3rd (1995) The worldwide problem of osteoporosis: insights afforded by epidemiology. Bone 17:505S–511SCrossRefPubMedGoogle Scholar
  2. 2.
    Ray NF, Chan JK, Thamer M, Melton LJ 3rd (1997) Medical expenditures for the treatment of osteoporotic fractures in the United States in 1995: report from the National Osteoporosis Foundation. J Bone Miner Res 12:24–35CrossRefPubMedGoogle Scholar
  3. 3.
    Cummings SR, Melton LJ (2002) Epidemiology and outcomes of osteoporotic fractures. Lancet 359:1761–1767CrossRefPubMedGoogle Scholar
  4. 4.
    WHO Scientific Group (2003) Prevention and management of osteoporosis. World Health Organ Tech Rep Ser 921:1–164, back coverGoogle Scholar
  5. 5.
    Macdonald HM, New SA, Golden MH, Campbell MK, Reid DM (2004) Nutritional associations with bone loss during the menopausal transition: evidence of a beneficial effect of calcium, alcohol, and fruit and vegetable nutrients and of a detrimental effect of fatty acids. Am J Clin Nutr 79:155–165PubMedGoogle Scholar
  6. 6.
    Tucker KL, Hannan MT, Kiel DP (2001) The acid–base hypothesis: diet and bone in the Framingham Osteoporosis Study. Eur J Nutr 40:231–237CrossRefPubMedGoogle Scholar
  7. 7.
    Prynne CJ, Mishra GD, O'Connell MA, Muniz G, Laskey MA, Yan L, Prentice A, Ginty F (2006) Fruit and vegetable intakes and bone mineral status: a cross sectional study in 5 age and sex cohorts. Am J Clin Nutr 83:1420–1428PubMedGoogle Scholar
  8. 8.
    Tucker KL, Chen H, Hannan MT, Cupples LA, Wilson PW, Felson D, Kiel DP (2002) Bone mineral density and dietary patterns in older adults: the Framingham Osteoporosis Study. Am J Clin Nutr 76:245–252PubMedGoogle Scholar
  9. 9.
    Tucker KL, Hannan MT, Chen H, Cupples LA, Wilson PW, Kiel DP (1999) Potassium, magnesium, and fruit and vegetable intakes are associated with greater bone mineral density in elderly men and women. Am J Clin Nutr 69:727–736PubMedGoogle Scholar
  10. 10.
    New SA, Robins SP, Campbell MK, Martin JC, Garton MJ, Bolton-Smith C, Grubb DA, Lee SJ, Reid DM (2000) Dietary influences on bone mass and bone metabolism: further evidence of a positive link between fruit and vegetable consumption and bone health? Am J Clin Nutr 71:142–151PubMedGoogle Scholar
  11. 11.
    Garrett IR, Boyce BF, Oreffo RO, Bonewald L, Poser J, Mundy GR (1990) Oxygen-derived free radicals stimulate osteoclastic bone resorption in rodent bone in vitro and in vivo. J Clin Invest 85:632–639CrossRefPubMedGoogle Scholar
  12. 12.
    Key LL Jr, Ries WL, Taylor RG, Hays BD, Pitzer BL (1990) Oxygen derived free radicals in osteoclasts: the specificity and location of the nitroblue tetrazolium reaction. Bone 11:115–119CrossRefPubMedGoogle Scholar
  13. 13.
    Ries WL, Key LL Jr, Rodriguiz RM (1992) Nitroblue tetrazolium reduction and bone resorption by osteoclasts in vitro inhibited by a manganese-based superoxide dismutase mimic. J Bone Miner Res 7:931–939PubMedCrossRefGoogle Scholar
  14. 14.
    Basu S, Michaelsson K, Olofsson H, Johansson S, Melhus H (2001) Association between oxidative stress and bone mineral density. Biochem Biophys Res Commun 288:275–279CrossRefPubMedGoogle Scholar
  15. 15.
    Conner EM, Grisham MB (1996) Inflammation, free radicals, and antioxidants. Nutrition 12:274–277CrossRefPubMedGoogle Scholar
  16. 16.
    Termine JD (1990) Bone matrix proteins and the mineralization process. American Society for Bone and Mineral Research, KelseyvilleGoogle Scholar
  17. 17.
    Peterkofsky B (1991) Ascorbate requirement for hydroxylation and secretion of procollagen: relationship to inhibition of collagen synthesis in scurvy. Am J Clin Nutr 54:1135S–1140SPubMedGoogle Scholar
  18. 18.
    Poal-Manresa J, Little K, Trueta J (1970) Some observations on the effects of vitamin C deficiency on bone. Br J Exp Pathol 51:372–378PubMedGoogle Scholar
  19. 19.
    Kipp DE, McElvain M, Kimmel DB, Akhter MP, Robinson RG, Lukert BP (1996) Scurvy results in decreased collagen synthesis and bone density in the guinea pig animal model. Bone 18:281–288CrossRefPubMedGoogle Scholar
  20. 20.
    Melhus H, Michaelsson K, Holmberg L, Wolk A, Ljunghall S (1999) Smoking, antioxidant vitamins, and the risk of hip fracture. J Bone Miner Res 14:129–135CrossRefPubMedGoogle Scholar
  21. 21.
    Zhang J, Munger RG, West NA, Cutler DR, Wengreen HJ, Corcoran CD (2006) Antioxidant intake and risk of osteoporotic hip fracture in Utah: an effect modified by smoking status. Am J Epidemiol 163:9–17CrossRefPubMedGoogle Scholar
  22. 22.
    Sahni S, Hannan MT, Gagnon D, Blumberg J, Cupples LA, Kiel DP, Tucker KL (2008) High vitamin C intake is associated with lower 4-year bone loss in elderly men. J Nutr 138:1931–1938PubMedGoogle Scholar
  23. 23.
    Dawber TR, Meadors GF, Moore FE Jr (1951) Epidemiological approaches to heart disease: the Framingham Study. Am J Public Health 41:279–281CrossRefGoogle Scholar
  24. 24.
    Rimm EB, Giovannucci EL, Stampfer MJ, Colditz GA, Litin LB, Willett WC (1992) Reproducibility and validity of an expanded self-administered semiquantitative food frequency questionnaire among male health professionals. Am J Epidemiol 135:1114–1126 discussion 1127–1136PubMedGoogle Scholar
  25. 25.
    Willett W, Stampfer MJ (1986) Total energy intake: implications for epidemiologic analyses. Am J Epidemiol 124:17–27PubMedGoogle Scholar
  26. 26.
    Ascherio A, Stampfer MJ, Colditz GA, Rimm EB, Litin L, Willett WC (1992) Correlations of vitamin A and E intakes with the plasma concentrations of carotenoids and tocopherols among American men and women. J Nutr 122:1792–1801PubMedGoogle Scholar
  27. 27.
    Jacques PF, Sulsky SI, Sadowski JA, Phillips JC, Rush D, Willett WC (1993) Comparison of micronutrient intake measured by a dietary questionnaire and biochemical indicators of micronutrient status. Am J Clin Nutr 57:182–189PubMedGoogle Scholar
  28. 28.
    U.S. Department of Health and Human Services and U.S. Department of Agriculture (2005) Dietary Guidelines for Americans. U.S. Government Printing Office, Washington, DCGoogle Scholar
  29. 29.
    Panel on Dietary Antioxidants and Related Compounds, Subcommittees on Upper Reference Levels of Nutrients and Interpretation and Uses of DRIs, Standing Committee on the Scientific Evaluation of Dietary Reference Intakes, Food and Nutrition Board, Institute of Medicine (2000) Dietary reference intakes for vitamin C, vitamin E, selenium, and carotenoids. National Academy Press, Washington, DCGoogle Scholar
  30. 30.
    Kiel DP, Felson DT, Anderson JJ, Wilson PW, Moskowitz MA (1987) Hip fracture and the use of estrogens in postmenopausal women. The Framingham Study. N Engl J Med 317:1169–1174PubMedGoogle Scholar
  31. 31.
    Nevitt MC, Cummings SR, Browner WS, Seeley DG, Cauley JA, Vogt TM, Black DM (1992) The accuracy of self-report of fractures in elderly women: evidence from a prospective study. Am J Epidemiol 135:490–499PubMedGoogle Scholar
  32. 32.
    Hannan MT, Felson DT, Dawson-Hughes B, Tucker KL, Cupples LA, Wilson PW, Kiel DP (2000) Risk factors for longitudinal bone loss in elderly men and women: the Framingham Osteoporosis Study. J Bone Miner Res 15:710–720CrossRefPubMedGoogle Scholar
  33. 33.
    Asomaning K, Bertone-Johnson ER, Nasca PC, Hooven F, Pekow PS (2006) The association between body mass index and osteoporosis in patients referred for a bone mineral density examination. J Womens Health (Larchmt) 15:1028–1034CrossRefGoogle Scholar
  34. 34.
    Kiel DP, Zhang Y, Hannan MT, Anderson JJ, Baron JA, Felson DT (1996) The effect of smoking at different life stages on bone mineral density in elderly men and women. Osteoporos Int 6:240–248CrossRefPubMedGoogle Scholar
  35. 35.
    Kiel DP, Felson DT, Hannan MT, Anderson JJ, Wilson PW (1990) Caffeine and the risk of hip fracture: the Framingham Study. Am J Epidemiol 132:675–684PubMedGoogle Scholar
  36. 36.
    Felson DT, Zhang Y, Hannan MT, Kannel WB, Kiel DP (1995) Alcohol intake and bone mineral density in elderly men and women. The Framingham Study. Am J Epidemiol 142:485–492PubMedGoogle Scholar
  37. 37.
    Bakhireva LN, Barrett-Connor E, Kritz-Silverstein D, Morton DJ (2004) Modifiable predictors of bone loss in older men: a prospective study. Am J Prev Med 26:436–442CrossRefPubMedGoogle Scholar
  38. 38.
    Dawson-Hughes B, Harris SS, Krall EA, Dallal GE (1997) Effect of calcium and vitamin D supplementation on bone density in men and women 65 years of age or older. N Engl J Med 337:670–676CrossRefPubMedGoogle Scholar
  39. 39.
    Cauley JA, Seeley DG, Ensrud K, Ettinger B, Black D, Cummings SR (1995) Estrogen replacement therapy and fractures in older women. Study of Osteoporotic Fractures Research Group. Ann Intern Med 122:9–16PubMedGoogle Scholar
  40. 40.
    Willett WC, Howe GR, Kushi LH (1997) Adjustment for total energy intake in epidemiologic studies. Am J Clin Nutr 65:1220S–1228S discussion 1229S–1231SPubMedGoogle Scholar
  41. 41.
    Maggio D, Barabani M, Pierandrei M, Polidori MC, Catani M, Mecocci P, Senin U, Pacifici R, Cherubini A (2003) Marked decrease in plasma antioxidants in aged osteoporotic women: results of a cross-sectional study. J Clin Endocrinol Metab 88:1523–1527CrossRefPubMedGoogle Scholar
  42. 42.
    Simon JA, Hudes ES (2001) Relation of ascorbic acid to bone mineral density and self-reported fractures among US adults. Am J Epidemiol 154:427–433CrossRefPubMedGoogle Scholar
  43. 43.
    Lanham-New SA (2008) The balance of bone health: tipping the scales in favor of potassium-rich, bicarbonate-rich foods. J Nutr 138:172S–177SPubMedGoogle Scholar
  44. 44.
    Pasco JA, Henry MJ, Wilkinson LK, Nicholson GC, Schneider HG, Kotowicz MA (2006) Antioxidant vitamin supplements and markers of bone turnover in a community sample of nonsmoking women. J Womens Health (Larchmt) 15:295–300CrossRefGoogle Scholar
  45. 45.
    Iotsova V, Caamano J, Loy J, Yang Y, Lewin A, Bravo R (1997) Osteopetrosis in mice lacking NF-kappaB1 and NF-kappaB2. Nat Med 3:1285–1289CrossRefPubMedGoogle Scholar
  46. 46.
    Schreck R, Albermann K, Baeuerle PA (1992) Nuclear factor kappa B: an oxidative stress-responsive transcription factor of eukaryotic cells (a review). Free Radic Res Commun 17:221–237CrossRefPubMedGoogle Scholar
  47. 47.
    Sen CK, Packer L (1996) Antioxidant and redox regulation of gene transcription. Faseb J 10:709–720PubMedGoogle Scholar
  48. 48.
    Sarisozen B, Durak K, Dincer G, Bilgen OF (2002) The effects of vitamins E and C on fracture healing in rats. J Int Med Res 30:309–313PubMedGoogle Scholar
  49. 49.
    Yilmaz C, Erdemli E, Selek H, Kinik H, Arikan M, Erdemli B (2001) The contribution of vitamin C to healing of experimental fractures. Arch Orthop Trauma Surg 121:426–428CrossRefPubMedGoogle Scholar
  50. 50.
    Garnero P, Borel O, Gineyts E, Duboeuf F, Solberg H, Bouxsein ML, Christiansen C, Delmas PD (2006) Extracellular post-translational modifications of collagen are major determinants of biomechanical properties of fetal bovine cortical bone. Bone 38:300–309CrossRefPubMedGoogle Scholar

Copyright information

© International Osteoporosis Foundation and National Osteoporosis Foundation 2009

Authors and Affiliations

  • S. Sahni
    • 1
  • M. T. Hannan
    • 2
  • D. Gagnon
    • 3
  • J. Blumberg
    • 4
  • L. A. Cupples
    • 3
  • D. P. Kiel
    • 2
  • K. L. Tucker
    • 1
    • 5
    Email author
  1. 1.Dietary Assessment and Epidemiology Research Program, Jean Mayer USDA Human Nutrition Research Center on Aging (HNRCA) and Friedman School of Nutrition Science and Policy (FSNSP)Tufts UniversityBostonUSA
  2. 2.Institute for Aging ResearchHebrew SeniorLife and Harvard Medical SchoolBostonUSA
  3. 3.Department of BiostatisticsBoston University School of Public HealthBostonUSA
  4. 4.Antioxidants Research Laboratory, HNRCA and FSNSPTufts UniversityBostonUSA
  5. 5.Dietary Assessment and Epidemiology Research Program, Jean Mayer USDA HNRCATufts UniversityBostonUSA

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