Skip to main content

Advertisement

Log in

Nonlinear association between bone mineral density and all-cause mortality: the Dong-gu study

  • Original Article
  • Published:
Osteoporosis International Aims and scope Submit manuscript

Abstract

Summary

There was a U-shaped association between hip BMD and all-cause mortality, with the lowest mortality in the 90th percentile in males. However, there was an inverse linear relationship in females. In contrast, the association between lumbar spine BMD and mortality was less evident in males, with no association in females.

Introduction

Bone mineral density (BMD) is reported inversely associated with mortality. Although some previous studies provided evidence for nonlinear associations, these were not adequately assessed in most previous works.

Methods

We evaluated the nonlinear relationship between BMD and mortality in Asians. Our study involved 8629 participants in the Dong-gu study from 2007 to 2010. Cox proportional hazard regression was used to calculate hazard ratios (HRs) according to BMD categories after adjusting for potential confounders. During a follow-up of 6.7 ± 1.4 years, 712 participants died.

Results

There was a U-shaped association between hip BMD and all-cause mortality, with the lowest mortality in the 90th percentile in males. However, there was an inverse linear relationship in females. In males, compared with the 75th to 95th percentile group, the < 2.5th percentile group had a 3.89 (95% CI 2.41–6.28)-fold higher risk and the 2.5th to 5th percentile group had a 2.51 (95% CI 1.25–5.04)-fold higher risk. The HR was 2.51 (95% CI 1.25, 5.04) in the > 97.5th percentile group. In females, compared with that in the 75th to 95th percentile group, the HR was 2.33 (95% CI 1.24, 4.39) in the < 2.5th percentile group. In contrast, the association between lumbar spine BMD and mortality was less evident in males, with no association in females.

Conclusion

In conclusion, this study shows that the association between BMD and mortality varies by gender and that high and low BMD are predictors of all-cause mortality in males.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  1. Burge R, Dawson-Hughes B, Solomon DH, Wong JB, King A, Tosteson A (2007) Incidence and economic burden of osteoporosis-related fractures in the United States, 2005–2025. J Bone Miner Res 22:465–475. https://doi.org/10.1359/jbmr.061113

    Article  PubMed  Google Scholar 

  2. Teng GG, Curtis JR, Saag KG (2008) Mortality and osteoporotic fractures: is the link causal, and is it modifiable? Clin Exp Rheumatol 26:S125–S137

    PubMed  PubMed Central  CAS  Google Scholar 

  3. Johnell O, Kanis JA, Oden A, Johansson H, de Laet C, Delmas P, Eisman JA, Fujiwara S, Kroger H, Mellstrom D, Meunier PJ, Melton LJ III, O'Neill T, Pols H, Reeve J, Silman A, Tenenhouse A (2005) Predictive value of BMD for hip and other fractures. J Bone Miner Res 20:1185–1194. https://doi.org/10.1359/JBMR.050304

    Article  PubMed  Google Scholar 

  4. Arden NK, Baker J, Hogg C, Baan K, Spector TD (1996) The heritability of bone mineral density, ultrasound of the calcaneus and hip axis length: a study of postmenopausal twins. J Bone Miner Res 11:530–534. https://doi.org/10.1002/jbmr.5650110414

    Article  PubMed  CAS  Google Scholar 

  5. Richards JB, Zheng H-F, Spector TD (2012) Genetics of osteoporosis from genome-wide association studies: advances and challenges. Nat Rev Genet 13:576–588. https://doi.org/10.1038/nrg3228

    Article  PubMed  CAS  Google Scholar 

  6. Liang B, Feng Y (2012) The association of low bone mineral density with systemic inflammation in clinically stable COPD. Endocrine 42:190–195. https://doi.org/10.1007/s12020-011-9583-x

    Article  PubMed  CAS  Google Scholar 

  7. Drake MT (2013) Osteoporosis and cancer. Current Osteoporosis Reports 11:163–170. https://doi.org/10.1007/s11914-013-0154-3

    Article  PubMed  PubMed Central  Google Scholar 

  8. Sennerby U, Farahmand B, Ahlbom A, Ljunghall S, Michaëlsson K (2007) Cardiovascular diseases and future risk of hip fracture in women. Osteoporosis Int 18:1355–1362. https://doi.org/10.1007/s00198-007-0386-0

    Article  CAS  Google Scholar 

  9. Johansson H, Oden A, Kanis J et al (2011) Low bone mineral density is associated with increased mortality in elderly men: MrOS Sweden. Osteoporosis Int 22:1411–1418. https://doi.org/10.1007/s00198-010-1331-1

    Article  CAS  Google Scholar 

  10. Trivedi DP, Khaw KT (2001) Bone mineral density at the hip predicts mortality in elderly men. Osteoporosis Int 12:259–265. https://doi.org/10.1007/s001980170114

    Article  CAS  Google Scholar 

  11. Nguyen ND, Center JR, Eisman JA, Nguyen TV (2007) Bone loss, weight loss, and weight fluctuation predict mortality risk in elderly men and women. J Bone Miner Res 22:1147–1154. https://doi.org/10.1359/jbmr.070412

    Article  PubMed  Google Scholar 

  12. Pinheiro MM, Castro CM, Szejnfeld VL (2006) Low femoral bone mineral density and quantitative ultrasound are risk factors for new osteoporotic fracture and total and cardiovascular mortality: a 5-year population-based study of Brazilian elderly women. J Gerontol A Biol Sci Med Sci 61:196–203

    Article  PubMed  Google Scholar 

  13. Suzuki T, Yoshida H (2010) Low bone mineral density at femoral neck is a predictor of increased mortality in elderly Japanese women. Osteoporosis Int 21:71–79. https://doi.org/10.1007/s00198-009-0970-6

    Article  CAS  Google Scholar 

  14. Van Der Klift M, Pols HAP, Geleijnse JM et al (2002) Bone mineral density and mortality in elderly men and women: the Rotterdam Study. Bone 30:643–648

    Article  Google Scholar 

  15. Domiciano DS, Machado LG, Lopes JB, Figueiredo CP, Caparbo VF, Oliveira RM, Scazufca M, McClung MR, Pereira RMR (2016) Bone mineral density and parathyroid hormone as independent risk factors for mortality in community-dwelling older adults: a population-based prospective cohort study in Brazil. The SAo Paulo Ageing & Health (SPAH) study. J Bone Miner Res 31:1146–1157. https://doi.org/10.1002/jbmr.2795

    Article  PubMed  CAS  Google Scholar 

  16. Mussolino ME, Madans JH, Gillum RF (2003) Bone mineral density and mortality in women and men: the NHANES I epidemiologic follow-up study. Ann Epidemiol 13:692–697

    Article  PubMed  Google Scholar 

  17. Qu X, Huang X, Jin F, Wang H, Hao Y, Tang T, Dai K (2013) Bone mineral density and all-cause, cardiovascular and stroke mortality: a meta-analysis of prospective cohort studies. Int J Cardiol 166:385–393. https://doi.org/10.1016/j.ijcard.2011.10.114

    Article  PubMed  Google Scholar 

  18. Choi YJ, Oh HJ, Kim DJ, Lee Y, Chung YS (2012) The prevalence of osteoporosis in Korean adults aged 50 years or older and the higher diagnosis rates in women who were beneficiaries of a national screening program: the Korea National Health and Nutrition Examination Survey 2008–2009. J Bone Miner Res 27:1879–1886. https://doi.org/10.1002/jbmr.1635

    Article  PubMed  Google Scholar 

  19. Kweon S-S, Shin M-H, Jeong S-K, Nam HS, Lee YH, Park KS, Ryu SY, Choi SW, Kim BH, Rhee JA, Zheng W, Choi JS (2014) Cohort profile: the Namwon Study and the Dong-gu Study. Int J Epidemiol 43:558–567. https://doi.org/10.1093/ije/dys244

    Article  PubMed  Google Scholar 

  20. Hurvich CM, Simonoff JS, Tsai C-L (2002) Smoothing parameter selection in nonparametric regression using an improved Akaike information criterion. Journal of the Royal Statistical Society: Series B (Statistical Methodology) 60:271–293. https://doi.org/10.1111/1467-9868.00125

    Article  Google Scholar 

  21. Eilers PHC, Marx BD (1996) Flexible smoothing with B-splines and penalties. Stat Sci 11:89–121. https://doi.org/10.1214/ss/1038425655

    Article  Google Scholar 

  22. Campos-Obando N, Castano-Betancourt MC, Oei L, Franco OH, Stricker BHC, Brusselle GG, Lahousse L, Hofman A, Tiemeier H, Rivadeneira F, Uitterlinden AG, Zillikens MC (2014) Bone mineral density and chronic lung disease mortality: the Rotterdam study. J Clin Endocrinol Metab 99:1834–1842. https://doi.org/10.1210/jc.2013-3819

    Article  PubMed  CAS  Google Scholar 

  23. Johansson C, Black D, Johnell O, Odén A, Mellström D (1998) Bone mineral density is a predictor of survival. Calcif Tissue Int 63:190–196

    Article  PubMed  CAS  Google Scholar 

  24. Zhao LP, Kolonel LN (1992) Efficiency loss from categorizing quantitative exposures into qualitative exposures in case-control studies. Am J Epidemiol 136:464–474. https://doi.org/10.1093/oxfordjournals.aje.a116520

    Article  PubMed  CAS  Google Scholar 

  25. Greenland S (1995) Avoiding power loss associated with categorization and ordinal scores in dose-response and trend analysis. Epidemiology 6:450–454. https://doi.org/10.1097/00001648-199507000-00025

    Article  PubMed  CAS  Google Scholar 

  26. Rand T, Seidl G, Kainberger F, Resch A, Hittmair K, Schneider B, Glüer CC, Imhof H (1997) Impact of spinal degenerative changes on the evaluation of bone mineral density with dual energy X-ray absorptiometry (DXA). Calcif Tissue Int 60:430–433

    Article  PubMed  CAS  Google Scholar 

  27. Reid IR, Evans MC, Ames R, Wattie DJ (1991) The influence of osteophytes and aortic calcification on spinal mineral density in postmenopausal women. Journal of Clinical Endocrinology & Metabolism 72:1372–1374. https://doi.org/10.1210/jcem-72-6-1372

    Article  CAS  Google Scholar 

  28. Drinka PJ, DeSmet AA, Bauwens SF, Rogot A (1992) The effect of overlying calcification on lumbar bone densitometry. Calcif Tissue Int 50:507–510

    Article  PubMed  CAS  Google Scholar 

  29. Ward KD, Klesges RC (2001) A meta-analysis of the effects of cigarette smoking on bone mineral density. Calcif Tissue Int 68:259–270. https://doi.org/10.1007/BF02390832

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  30. McFarlane SI, Muniyappa R, Shin JJ et al (2004) Osteoporosis and cardiovascular disease: brittle bones and boned arteries, is there a link? Endocrine 23:1–10. https://doi.org/10.1385/ENDO:23:1:01

    Article  PubMed  CAS  Google Scholar 

  31. Uzzan B, Cohen R, Nicolas P, Cucherat M, Perret GY (2007) Effects of statins on bone mineral density: a meta-analysis of clinical studies. Bone 40:1581–1587. https://doi.org/10.1016/j.bone.2007.02.019

    Article  PubMed  CAS  Google Scholar 

  32. Bolland MJ, Grey AB, Gamble GD, Reid IR (2010) Effect of osteoporosis treatment on mortality: a meta-analysis. J Clin Endocrinol Metab 95:1174–1181. https://doi.org/10.1210/jc.2009-0852

    Article  PubMed  CAS  Google Scholar 

  33. Van Wesenbeeck L, Cleiren E, Gram J et al (2003) Six novel missense mutations in the LDL receptor-related protein 5 (LRP5) gene in different conditions with an increased bone density. Am J Hum Genet 72:763–771. https://doi.org/10.1086/368277

    Article  PubMed  PubMed Central  Google Scholar 

  34. Balemans W, Ebeling M, Patel N, van Hul E, Olson P, Dioszegi M, Lacza C, Wuyts W, van den Ende J, Willems P, Paes-Alves AF, Hill S, Bueno M, Ramos FJ, Tacconi P, Dikkers FG, Stratakis C, Lindpaintner K, Vickery B, Foernzler D, van Hul W (2001) Increased bone density in sclerosteosis is due to the deficiency of a novel secreted protein (SOST). Hum Mol Genet 10:537–543

    Article  PubMed  CAS  Google Scholar 

  35. Shapiro F (1993) Osteopetrosis. Current clinical considerations. Clin Orthop Relat Res:34–44

  36. Steward CG (2003) Neurological aspects of osteopetrosis. Neuropathol Appl Neurobiol 29:87–97

    Article  PubMed  CAS  Google Scholar 

  37. Chaganti RK, Parimi N, Lang T et al (2010) Bone mineral density and prevalent osteoarthritis of the hip in older men for the Osteoporotic Fractures in Men (MrOS) Study Group. Osteoporos Int 21:1307–1316. https://doi.org/10.1007/s00198-009-1105-9

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  38. Cooper C, Harvey NC, Dennison EM, van Staa TP (2006) Update on the epidemiology of Paget’s disease of bone. J Bone Miner Res 21:P3–P8. https://doi.org/10.1359/jbmr.06s201

    Article  PubMed  Google Scholar 

  39. Narváez JA, Narváez J, Clavaguera MT, Juanola X, Valls C, Fiter J (1998) Bone and skeletal muscle metastases from gastric adenocarcinoma: unusual radiographic, CT and scintigraphic features. Eur Radiol 8:1366–1369. https://doi.org/10.1007/s003300050554

    Article  PubMed  Google Scholar 

  40. Evans CE, Ward C, Braidman IP (1991) Breast carcinomas synthesize factors which influence osteoblast-like cells independently of osteoclasts in vitro. J Endocrinol 128:R5–R8. https://doi.org/10.1677/joe.0.128R005

    Article  PubMed  CAS  Google Scholar 

  41. Kotzmann H, Bernecker P, Hübsch P, Pietschmann P, Woloszczuk W, Svoboda T, Geyer G, Luger A (1993) Bone mineral density and parameters of bone metabolism in patients with acromegaly. J Bone Miner Res 8:459–465. https://doi.org/10.1002/jbmr.5650080410

    Article  PubMed  CAS  Google Scholar 

  42. Vedi S, Purdie DW, Ballard P, Bord S, Cooper AC, Compston JE (1999) Bone remodeling and structure in postmenopausal women treated with long-term, high-dose estrogen therapy. Osteoporosis Int 10:52–58. https://doi.org/10.1007/s001980050194

    Article  CAS  Google Scholar 

  43. Felson DT, Zhang Y, Hannan MT, Anderson JJ (1993) Effects of weight and body mass index on bone mineral density in men and women: the Framingham study. J Bone Miner Res 8:567–573. https://doi.org/10.1002/jbmr.5650080507

    Article  PubMed  CAS  Google Scholar 

Download references

Funding

This study was supported by a grant (CRI13904-21) Chonnam National University Hospital Biomedical Research Institute.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to M. -H. Shin.

Ethics declarations

Conflicts of interest

None.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Choi, C.K., Kweon, S.S., Lee, Y.H. et al. Nonlinear association between bone mineral density and all-cause mortality: the Dong-gu study. Osteoporos Int 29, 2011–2020 (2018). https://doi.org/10.1007/s00198-018-4386-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00198-018-4386-z

Keywords

Navigation