Skip to main content

Association of urinary sodium/creatinine ratio with bone mineral density in postmenopausal women: KNHANES 2008–2011

Endocrine volume 49, pages 791–799 (2015)Cite this article

Abstract

Accumulating evidence shows that high sodium chloride intake increases urinary calcium excretion and may be a risk factor for osteoporosis. However, the effect of oral sodium chloride intake on bone mineral density (BMD) and risk of osteoporosis has been inadequately researched. The aim of the present study was to determine whether urinary sodium excretion (reflecting oral sodium chloride intake) associates with BMD and prevalence of osteoporosis in postmenopausal women. This cross-sectional study involved a nationally representative sample consisting of 2,779 postmenopausal women who participated in the Korea National Health and Nutritional Examination Surveys in 2008–2011. The association of urinary sodium/creatinine ratio with BMD and other osteoporosis risk factors was assessed. In addition, the prevalence of osteoporosis was assessed in four groups with different urinary sodium/creatinine ratios. Participants with osteoporosis had significantly higher urinary sodium/creatinine ratios than the participants without osteoporosis. After adjusting for multiple confounding factors, urinary sodium/creatinine ratio correlated inversely with lumbar spine BMD (P = 0.001). Similarly, when participants were divided into quartile groups according to urinary sodium/creatinine ratio, the average BMD dropped as the urinary sodium/creatinine ratio increased. Multiple logistic regression analysis revealed that compared to quartile 1, quartile 4 had a significantly increased prevalence of lumbar spine osteoporosis (odds ratios 1.346, P for trend = 0.044). High urinary sodium excretion was significantly associated with low BMD and high prevalence of osteoporosis in lumbar spine. These results suggest that high sodium chloride intake decreases lumbar spine BMD and increases the risk of osteoporosis in postmenopausal women.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1

References

  1. L.G. Raisz, Pathogenesis of osteoporosis: concepts, conflicts, and prospects. J. Clin. Investig. 115(12), 3318–3325 (2005). doi:10.1172/jci27071

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  2. B.L. Riggs, The mechanisms of estrogen regulation of bone resorption. J. Clin. Investig. 106(10), 1203–1204 (2000). doi:10.1172/jci11468

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  3. M. Gass, B. Dawson-Hughes, Preventing osteoporosis-related fractures: an overview. Am. J. Med. 119(4 Suppl 1), S3–S11 (2006). doi:10.1016/j.amjmed.2005.12.017

    PubMed  Article  Google Scholar 

  4. A. Prentice, Diet, nutrition and the prevention of osteoporosis. Public Health Nutr. 7(1a), 227–243 (2004)

    CAS  PubMed  Article  Google Scholar 

  5. D. Bonaiuti, B. Shea, R. Iovine, S. Negrini, V. Robinson, H.C. Kemper, G. Wells, P. Tugwell, A. Cranney, Exercise for preventing and treating osteoporosis in postmenopausal women. Cochrane Database Syst. Rev. 3, Cd000333 (2002). doi:10.1002/14651858.cd000333

  6. T.V. Nguyen, P.N. Sambrook, J.A. Eisman, Bone loss, physical activity, and weight change in elderly women: the Dubbo Osteoporosis Epidemiology Study. J. Bone Miner. Res. 13(9), 1458–1467 (1998). doi:10.1359/jbmr.1998.13.9.1458

    CAS  PubMed  Article  Google Scholar 

  7. R.P. Heaney, Role of dietary sodium in osteoporosis. J. Am. Coll. Nutr. 25(3 Suppl), 271s–276s (2006)

    CAS  PubMed  Article  Google Scholar 

  8. A.G. Need, H.A. Morris, D.B. Cleghorn, D. De Nichilo, M. Horowitz, B.E. Nordin, Effect of salt restriction on urine hydroxyproline excretion in postmenopausal women. Arch. Intern. Med. 151(4), 757–759 (1991)

    CAS  PubMed  Article  Google Scholar 

  9. N.A. Breslau, K. Sakhaee, C.Y. Pak, Impaired adaptation to salt-induced urinary calcium losses in postmenopausal osteoporosis. Trans. Assoc. Am. Phys. 98, 107–115 (1985)

    CAS  PubMed  Google Scholar 

  10. B.E. Nordin, A.G. Need, H.A. Morris, M. Horowitz, The nature and significance of the relationship between urinary sodium and urinary calcium in women. J. Nutr. 123(9), 1615–1622 (1993)

    CAS  PubMed  Google Scholar 

  11. F.S. Wright, K. Bomsztyk, Calcium transport by the proximal tubule. Adv. Exp. Med. Biol. 208, 165–170 (1986)

    CAS  PubMed  Article  Google Scholar 

  12. P.A. Friedman, Mechanisms of renal calcium transport. Exp. Nephrol. 8(6), 343–350 (2000)

    CAS  PubMed  Article  Google Scholar 

  13. P.A. Friedman, Codependence of renal calcium and sodium transport. Annu. Rev. Physiol. 60, 179–197 (1998). doi:10.1146/annurev.physiol.60.1.179

    CAS  PubMed  Article  Google Scholar 

  14. C. Nagata, N. Takatsuka, N. Shimizu, H. Shimizu, Sodium intake and risk of death from stroke in Japanese men and women. Stroke 35(7), 1543–1547 (2004). doi:10.1161/01.STR.0000130425.50441.b0

    PubMed  Article  Google Scholar 

  15. T. Buclin, M. Cosma, M. Appenzeller, A.F. Jacquet, L.A. Decosterd, J. Biollaz, P. Burckhardt, Diet acids and alkalis influence calcium retention in bone. Osteoporosis 12(6), 493–499 (2001). doi:10.1007/s001980170095

    CAS  Article  Google Scholar 

  16. D.E. Sellmeyer, K.L. Stone, A. Sebastian, S.R. Cummings, A high ratio of dietary animal to vegetable protein increases the rate of bone loss and the risk of fracture in postmenopausal women. Study of Osteoporotic Fractures Research Group. Am. J. Clin. Nutr. 73(1), 118–122 (2001)

    CAS  PubMed  Google Scholar 

  17. D.A. McCarron, L.I. Rankin, W.M. Bennett, S. Krutzik, M.R. McClung, F.C. Luft, Urinary calcium excretion at extremes of sodium intake in normal man. Am. J. Nephrol. 1(2), 84–90 (1981)

    CAS  PubMed  Article  Google Scholar 

  18. M. Audran, E. Legrand, Hypercalciuria. Joint Bone Spine 67(6), 509–515 (2000)

    CAS  PubMed  Article  Google Scholar 

  19. M. Zarkadas, R. Gougeon-Reyburn, E.B. Marliss, E. Block, M. Alton-Mackey, Sodium chloride supplementation and urinary calcium excretion in postmenopausal women. Am. J. Clin. Nutr. 50(5), 1088–1094 (1989)

    CAS  PubMed  Google Scholar 

  20. B. Teucher, S. Fairweather-Tait, Dietary sodium as a risk factor for osteoporosis: where is the evidence? Proc. Nutr. Soc. 62(4), 859–866 (2003). doi:10.1079/pns2003300

    CAS  PubMed  Article  Google Scholar 

  21. S.M. Park, J. Jee, J.Y. Joung, Y.Y. Cho, S.Y. Sohn, S.M. Jin, K.Y. Hur, J.H. Kim, S.W. Kim, J.H. Chung, M.K. Lee, Y.K. Min, High dietary sodium intake assessed by 24-hour urine specimen increase urinary calcium excretion and bone resorption marker. J. Bone Metab. 21(3), 189–194 (2014). doi:10.11005/jbm.2014.21.3.189

    PubMed Central  PubMed  Article  Google Scholar 

  22. L.D. Carbone, A.J. Bush, K.D. Barrow, A.H. Kang, The relationship of sodium intake to calcium and sodium excretion and bone mineral density of the hip in postmenopausal African-American and Caucasian women. J. Bone Miner. Metab. 21(6), 415–420 (2003). doi:10.1007/s00774-003-0437-3

    CAS  PubMed  Article  Google Scholar 

  23. A. Devine, R.A. Criddle, I.M. Dick, D.A. Kerr, R.L. Prince, A longitudinal study of the effect of sodium and calcium intakes on regional bone density in postmenopausal women. Am J Clin. Nutr. 62(4), 740–745 (1995)

    CAS  PubMed  Google Scholar 

  24. G.A. Greendale, E. Barrett-Connor, S. Edelstein, S. Ingles, R. Haile, Dietary sodium and bone mineral density: results of a 16-year follow-up study. J. Am. Geriatr. Soc. 42(10), 1050–1055 (1994)

    CAS  PubMed  Article  Google Scholar 

  25. I.R. Reid, R.W. Ames, M.C. Evans, S.J. Sharpe, G.D. Gamble, Determinants of the rate of bone loss in normal postmenopausal women. J. Clin. Endocrinol. Metab. 79(4), 950–954 (1994). doi:10.1210/jcem.79.4.7962303

    CAS  PubMed  Google Scholar 

  26. B.E. Nordin, K.J. Polley, Metabolic consequences of the menopause. A cross-sectional, longitudinal, and intervention study on 557 normal postmenopausal women. Calcif. Tissue Int. 41(Suppl 1), S1–S59 (1987)

    PubMed  Google Scholar 

  27. G. Jones, T. Beard, V. Parameswaran, T. Greenaway, R. von Witt, A population-based study of the relationship between salt intake, bone resorption and bone mass. Eur. J. Clin. Nutr. 51(8), 561–565 (1997)

    CAS  PubMed  Article  Google Scholar 

  28. H.S. Koo, Y.C. Kim, S.Y. Ahn, S.W. Oh, S. Kim, H.J. Chin, J.H. Park, Estimating 24-hour urine sodium level with spot urine sodium and creatinine. J. Korean Med. Sci. 29(Suppl 2), S97–S102 (2014). doi:10.3346/jkms.2014.29.S2.S97

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  29. A.V. Chobanian, G.L. Bakris, H.R. Black, W.C. Cushman, L.A. Green, J.L. Izzo Jr, D.W. Jones, B.J. Materson, S. Oparil, J.T. Wright Jr, E.J. Roccella, The seventh report of the joint national committee on prevention, detection, evaluation, and treatment of high blood pressure: the JNC 7 report. JAMA 289(19), 2560–2572 (2003). doi:10.1001/jama.289.19.2560

    CAS  PubMed  Article  Google Scholar 

  30. D.A. Schoeller, F.A. Tylavsky, D.J. Baer, W.C. Chumlea, C.P. Earthman, T. Fuerst, T.B. Harris, S.B. Heymsfield, M. Horlick, T.G. Lohman, H.C. Lukaski, J. Shepherd, R.M. Siervogel, L.G. Borrud, QDR 4500A dual-energy X-ray absorptiometer underestimates fat mass in comparison with criterion methods in adults. Am. J. Clin. Nutr. 81(5), 1018–1025 (2005)

    CAS  PubMed  Google Scholar 

  31. T.L. Kelly, K.E. Wilson, S.B. Heymsfield, Dual energy X-Ray absorptiometry body composition reference values from NHANES. PLoS One 4(9), e7038 (2009). doi:10.1371/journal.pone.0007038

    PubMed Central  PubMed  Article  Google Scholar 

  32. Assessment of fracture risk and its application to screening for postmenopausal osteoporosis. Report of a WHO Study Group. World Health Organization technical report series 843, 1–129 (1994)

  33. A.J. Cohen, F.J. Roe, Review of risk factors for osteoporosis with particular reference to a possible aetiological role of dietary salt. Food Chem. Toxicol. 38(2–3), 237–253 (2000)

    CAS  PubMed  Article  Google Scholar 

  34. A. Goulding, E. Gold, Effects of dietary sodium chloride loading on parathyroid function, 1,25-dihydroxyvitamin D, calcium balance, and bone metabolism in female rats during chronic prednisolone administration. Endocrinology 119(5), 2148–2154 (1986). doi:10.1210/endo-119-5-2148

    CAS  PubMed  Article  Google Scholar 

  35. N.A. Breslau, J.L. McGuire, J.E. Zerwekh, C.Y. Pak, The role of dietary sodium on renal excretion and intestinal absorption of calcium and on vitamin D metabolism. J Clin. Endocrinol. Metab. 55(2), 369–373 (1982). doi:10.1210/jcem-55-2-369

    CAS  PubMed  Article  Google Scholar 

  36. R.P. Heaney, R.R. Recker, M.R. Stegman, A.J. Moy, Calcium absorption in women: relationships to calcium intake, estrogen status, and age. J. Bone Miner. Res. 4(4), 469–475 (1989). doi:10.1002/jbmr.5650040404

    CAS  PubMed  Article  Google Scholar 

  37. S. Pattanaungkul, B.L. Riggs, A.L. Yergey, N.E. Vieira, W.M. O’Fallon, S. Khosla, Relationship of intestinal calcium absorption to 1,25-dihydroxyvitamin D [1,25(OH)2D] levels in young versus elderly women: evidence for age-related intestinal resistance to 1,25(OH)2D action. J. Clin. Endocrinol. Metab. 85(11), 4023–4027 (2000). doi:10.1210/jcem.85.11.6938

    CAS  PubMed  Google Scholar 

  38. H.A. Morris, A.G. Need, M. Horowitz, P.D. O’Loughlin, B.E. Nordin, Calcium absorption in normal and osteoporotic postmenopausal women. Calcif. Tissue Int. 49(4), 240–243 (1991)

    CAS  PubMed  Article  Google Scholar 

  39. B.E. Nordin, Calcium and osteoporosis. Nutrition (Burbank, Los Angeles County, Calif.) 13(7–8), 664–686 (1997)

  40. K.I. Kim, H.J. Chang, Y.S. Cho, T.J. Youn, W.Y. Chung, I.H. Chae, D.J. Choi, C.H. Kim, Current status and characteristics of hypertension control in community resident elderly Korean people: data from a Korean longitudinal study on health and aging (KLoSHa study). Hypertens. Res. 31(1), 97–105 (2008). doi:10.1291/hypres.31.97

    CAS  PubMed  Article  Google Scholar 

Download references

Acknowledgments

We thank all participants for enthusiastically participating in this study. This work was supported by grants from the National Research Foundation of Korea (2012R1A2A2A01043867) funded by the Ministry of Science, ICT and Future Planning, and a grant from the Korea Health Technology R&D Project, Ministry of Health and Welfare, Republic of Korea (A111345).

Disclosure

The authors have nothing to disclose.

Author information

Affiliations

  1. Division of Endocrinology and Metabolism, Department of Internal Medicine, Kyungpook National University School of Medicine, 130 Dongdeok-ro, Jung-gu, Daegu, 700-721, South Korea

    Sung-Woo Kim, Jae-Han Jeon, Yeon-Kyung Choi, In-Ryang Hwang, Jung-Guk Kim, In-Kyu Lee & Keun-Gyu Park

  2. Department of Preventive Medicine, Kyungpook National University School of Medicine, Daegu, South Korea

    Won-Kee Lee

Authors
  1. Sung-Woo Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jae-Han Jeon
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yeon-Kyung Choi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Won-Kee Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. In-Ryang Hwang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jung-Guk Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. In-Kyu Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Keun-Gyu Park
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Keun-Gyu Park.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Kim, SW., Jeon, JH., Choi, YK. et al. Association of urinary sodium/creatinine ratio with bone mineral density in postmenopausal women: KNHANES 2008–2011. Endocrine 49, 791–799 (2015). https://doi.org/10.1007/s12020-015-0532-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12020-015-0532-y

Keywords

  • Urinary sodium excretion
  • Osteoporosis
  • Bone mineral density
  • Postmenopausal women