Skip to main content

Advertisement

SpringerLink
Log in

Socioeconomic status, race, and bone turnover in the Midlife in the US Study

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

Abstract

Summary

Among a group of 940 US adults, economic adversity and minority race status were associated with higher serum levels of markers of bone turnover. These results suggest that higher levels of social stress may increase bone turnover.

Introduction

To determine socioeconomic status (SES) and race differences in levels of bone turnover.

Methods

Using data from the Biomarker Substudy of the Midlife in the US (MIDUS) study (491 men, 449 women), we examined cross-sectional associations of SES and race with serum levels of bone turnover markers (bone-specific alkaline phosphatase [BSAP], procollagen type I N-terminal propeptide [PINP], and N-telopeptide [Ntx]) separately in men and women. Linear multivariable regression was used to control for body weight, menopausal transition stage, and age.

Results

Among men, low family poverty-to-income ratio (FPIR) was associated with higher turnover, but neither education nor race was associated with turnover. Men with FPIR <3 had 1.808 nM BCE higher Ntx (P = 0.05), 3.366 U/L higher BSAP (P = 0.02), and 7.066 higher PINP (P = 0.02). Among women, neither education nor FPIR was associated with bone turnover, but Black women had 3.688 nM BCE higher Ntx (P = 0.001), 5.267 U/L higher BSAP (P = 0.005), and 11.906 μg/L higher PINP (P = 0.008) compared with non-Black women.

Conclusions

Economic adversity was associated with higher bone turnover in men, and minority race status was associated with higher bone turnover in women, consistent with the hypothesis that higher levels of social stresses cause increased bone turnover. The magnitude of these associations was comparable to the effects of some osteoporosis medications on levels of turnover.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Seeman T, Epel E, Gruenewald T, Karlamangla A, McEwen BS (2010) Socio-economic differentials in peripheral biology: cumulative allostatic load. Ann N Y Acad Sci 1186:223–239

    Article  PubMed  Google Scholar 

  2. Szulc P, Delmas PD (2008) Biochemical markers of bone turnover in osteoporosis. In: Rosen CJ (ed) Primer on the Metabolic Bone Diseases and Disorders of Mineral Metabolism, 7th edn. The American Society for Bone and Mineral Research, Washington

    Google Scholar 

  3. Civitelli RA-VR, Napoli N (2009) Bone turnover markers: understanding their value in clinical trials and clinical practice. Osteoporosis Int 20:843–851

    Article  CAS  Google Scholar 

  4. Garnero P, Sornay-Rendu E, Claustrat B, Delmas PD (2000) Biochemical markers of bone turnover, endogenous hormones and the risk of fractures in postmenopausal women: the OFELY study. J Bone Miner Res 15:1526–1536

    Article  PubMed  CAS  Google Scholar 

  5. Garnero P, Hausherr E, Chapuy MC, Marcelli C, Grandjean H, Muller C, Cormier C, Breart G, Meunier PJ, Delmas PD (1996) Markers of bone resorption predict hip fracture in elderly women: the EPIDOS Prospective Study. J Bone Miner Res 11:1531–1538

    Article  PubMed  CAS  Google Scholar 

  6. van Daele PL, Seibel MJ, Burger H, Hofman A, Grobbee DE, van Leeuwen JP, Birkenhager JC, Pols HA (1996) Case-control analysis of bone resorption markers, disability, and hip fracture risk: the Rotterdam study. BMJ 312:482–483

    Article  PubMed  Google Scholar 

  7. Ross PD, Kress BC, Parson RE, Wasnich RD, Armour KA, Mizrahi IA (2000) Serum bone alkaline phosphatase and calcaneus bone density predict fractures: a prospective study. Osteoporos Int 11:76–82

    Article  PubMed  CAS  Google Scholar 

  8. Krieger N, Rowley DL, Herman AA, Avery B, Phillips MT (1993) Racism, sexism, and social class: implications for studies of health, disease, and well-being. Am J Prev Med 9:82–122

    PubMed  CAS  Google Scholar 

  9. Williams DR (1996) Race/ethnicity and socioeconomic status: measurement and methodological issues. Int J Health Serv 26:483–505

    Article  PubMed  CAS  Google Scholar 

  10. Kaufman JS, Cooper RS, McGee DL (1997) Socioeconomic status and health in blacks and whites: the problem of residual confounding and the resiliency of race. Epidemiology 8:621–628

    PubMed  CAS  Google Scholar 

  11. Williams DR, Collins C (2001) Racial residential segregation: a fundamental cause of racial disparities in health. Public Health Rep 116:404–416

    PubMed  CAS  Google Scholar 

  12. Willhelm SM (1986) The economic demise of blacks in America: a prelude to genocide? J Black Stud 17:201–254

    Article  PubMed  CAS  Google Scholar 

  13. Dienberg Love G, Seeman TE, Weinstein M, Ryff CD (2010) Bioindicators in the MIDUS National Study: protocol, measures, sample, and comparative context. J Aging Health 22:1059–1080

    Article  PubMed  Google Scholar 

  14. Brim OG, Ryff CD, Kessler RC (2004) How healthy are we?: a national study of well-being at midlife. University of Chicago Press, Chicago

    Google Scholar 

  15. Radler BT, Ryff CD (2010) Who participates? Accounting for longitudinal retention in the MIDUS National Study of Health and Well-Being. J Aging Health 22:307–331

    Article  PubMed  Google Scholar 

  16. Ainsworth BE, Haskell WL, Leon AS, Jacobs DR Jr, Montoye HJ, Sallis JF, Paffenbarger RS Jr (1993) Compendium of physical activities: classification of energy costs of human physical activities. Med Sci Sports Exerc 25:71–80

    Article  PubMed  CAS  Google Scholar 

  17. Godin G, Shephard RJ (1985) A simple method to assess exercise behavior in the community. Can J Appl Sport Sci 10:141–146

    PubMed  CAS  Google Scholar 

  18. Brown JP, Albert C, Nassar BA et al (2009) Bone turnover markers in the management of postmenopausal osteoporosis. Clin Biochem 42:929–942

    Article  PubMed  CAS  Google Scholar 

  19. Seibel MJ (2005) Biochemical markers of bone turnover: part I: biochemistry and variability. Clin Biochem Rev 26:97–122

    PubMed  Google Scholar 

  20. Gerdhem P, Isaksson A, Akesson K, Obrant KJ (2005) Increased bone density and decreased bone turnover, but no evident alteration of fracture susceptibility in elderly women with diabetes mellitus. Osteoporos Int 16:1506–1512

    Article  PubMed  CAS  Google Scholar 

  21. Dobnig H, Piswanger-Solkner JC, Roth M, Obermayer-Pietsch B, Tiran A, Strele A, Maier E, Maritschnegg P, Sieberer C, Fahrleitner-Pammer A (2006) Type 2 diabetes mellitus in nursing home patients: effects on bone turnover, bone mass, and fracture risk. J Clin Endocrinol Metab 91:3355–3363

    Article  PubMed  CAS  Google Scholar 

  22. Yaturu S (2009) Diabetes and skeletal health. J Diabetes 1:246–254

    Article  PubMed  CAS  Google Scholar 

  23. Compston J (2009) Monitoring osteoporosis treatment. Best Pract Res Clin Rheumatol 23:781–788

    Article  PubMed  Google Scholar 

  24. Hochberg MC, Greenspan S, Wasnich RD, Miller P, Thompson DE, Ross PD (2002) Changes in bone density and turnover explain the reductions in incidence of nonvertebral fractures that occur during treatment with antiresorptive agents. J Clin Endocrinol Metab 87:1586–1592

    Article  PubMed  CAS  Google Scholar 

  25. Pearce MS, Relton CL, Groom A, Peaston RT, Francis RM (2010) A lifecourse study of bone resorption in men ages 49–51 years: the Newcastle Thousand Families cohort study. Bone 46:952–956

    Article  PubMed  CAS  Google Scholar 

  26. Karlamangla AS, Merkin SS, Crimmins EM, Seeman TE (2010) Socioeconomic and ethnic disparities in cardiovascular risk in the United States, 2001–2006. Ann Epidemiol 20:617–628

    Article  PubMed  Google Scholar 

  27. Karlamangla AS, Singer BH, Williams DR, Schwartz JE, Matthews KA, Kiefe CI, Seeman TE (2005) Impact of socioeconomic status on longitudinal accumulation of cardiovascular risk in young adults: the CARDIA Study (USA). Soc Sci Med 60:999–1015

    Article  PubMed  Google Scholar 

  28. MacIntyre S, Hunt K (1997) Socio-economic position, gender and health: how do they interact? J Health Psych Special Issue Health Socio-econo Position 2:315–334

    CAS  Google Scholar 

  29. Taylor SE, Klein LC, Lewis BP, Gruenewald TL, Gurung RA, Updegraff JA (2000) Biobehavioral responses to stress in females: tend-and-befriend, not fight-or-flight. Psychol Rev 107:411–429

    Article  PubMed  CAS  Google Scholar 

  30. Matsuoka LY, Wortsman J, Haddad JG, Kolm P, Hollis BW (1991) Racial pigmentation and the cutaneous synthesis of vitamin D. Arch Dermatol 127:536–538

    Article  PubMed  CAS  Google Scholar 

  31. Aloia JF (2008) African Americans, 25-hydroxyvitamin D, and osteoporosis: a paradox. Am J Clin Nutr 88:545S–550S

    PubMed  CAS  Google Scholar 

  32. Rosen CJ (2011) Clinical practice. Vitamin D insufficiency. N Engl J Med 364:248–254

    Article  PubMed  CAS  Google Scholar 

  33. Clemens TL, Adams JS, Henderson SL, Holick MF (1982) Increased skin pigment reduces the capacity of skin to synthesise vitamin D3. Lancet 1:74–76

    Article  PubMed  CAS  Google Scholar 

  34. Looker AC, Dawson-Hughes B, Calvo MS, Gunter EW, Sahyoun NR (2002) Serum 25-hydroxyvitamin D status of adolescents and adults in two seasonal subpopulations from NHANES III. Bone 30:771–777

    Article  PubMed  CAS  Google Scholar 

  35. Parisien M, Cosman F, Morgan D et al (1997) Histomorphometric assessment of bone mass, structure, and remodeling: a comparison between healthy black and white premenopausal women. J Bone Miner Res 12:948–957

    Article  PubMed  CAS  Google Scholar 

  36. Lips P (2001) Vitamin D deficiency and secondary hyperparathyroidism in the elderly: consequences for bone loss and fractures and therapeutic implications. Endocr Rev 22:477–501

    Article  PubMed  CAS  Google Scholar 

  37. Lips P (2006) Vitamin D physiology. Prog Biophys Mol Biol 92:4–8

    Article  PubMed  CAS  Google Scholar 

  38. Cosman F, Morgan DC, Nieves JW, Shen V, Luckey MM, Dempster DW, Lindsay R, Parisien M (1997) Resistance to bone resorbing effects of PTH in black women. J Bone Miner Res 12:958–966

    Article  PubMed  CAS  Google Scholar 

  39. Bikle DD, Ettinger B, Sidney S, Tekawa IS, Tolan K (1999) Differences in calcium metabolism between black and white men and women. Miner Electrolyte Metab 25:178–184

    Article  PubMed  CAS  Google Scholar 

  40. Harris SS, Soteriades E, Coolidge JA, Mudgal S, Dawson-Hughes B (2000) Vitamin D insufficiency and hyperparathyroidism in a low income, multiracial, elderly population. J Clin Endocrinol Metab 85:4125–4130

    Article  PubMed  CAS  Google Scholar 

  41. Kleerekoper M, Nelson DA, Peterson EL, Flynn MJ, Pawluszka AS, Jacobsen G, Wilson P (1994) Reference data for bone mass, calciotropic hormones, and biochemical markers of bone remodeling in older (55–75) postmenopausal white and black women. J Bone Miner Res 9:1267–1276

    Article  PubMed  CAS  Google Scholar 

  42. Bell NH, Epstein S, Greene A, Shary J, Oexmann MJ, Shaw S (1985) Evidence for alteration of the vitamin D-endocrine system in obese subjects. J Clin Invest 76:370–373

    Article  PubMed  CAS  Google Scholar 

  43. Harris SS, Soteriades E, Dawson-Hughes B (2001) Secondary hyperparathyroidism and bone turnover in elderly blacks and whites. J Clin Endocrinol Metab 86:3801–3804

    Article  PubMed  CAS  Google Scholar 

  44. Aloia JF, Mikhail M, Pagan CD, Arunachalam A, Yeh JK, Flaster E (1998) Biochemical and hormonal variables in black and white women matched for age and weight. J Lab Clin Med 132:383–389

    Article  PubMed  CAS  Google Scholar 

  45. Aloia JF, Vaswani A, Yeh JK, Flaster E (1996) Risk for osteoporosis in black women. Calcif Tissue Int 59:415–423

    Article  PubMed  CAS  Google Scholar 

  46. Hannon R, Eastell R (2000) Preanalytical variability of biochemical markers of bone turnover. Osteoporos Int 11(Suppl 6):S30–S44

    Article  PubMed  Google Scholar 

  47. Finkelstein JS, Sowers M, Greendale GA, Lee ML, Neer RM, Cauley JA, Ettinger B (2002) Ethnic variation in bone turnover in pre- and early perimenopausal women: effects of anthropometric and lifestyle factors. J Clin Endocrinol Metab 87:3051–3056

    Article  PubMed  CAS  Google Scholar 

  48. Cosman F, Nieves J, Morgan D, Shen V, Sherwood D, Parisien M, Lindsay R (1999) Parathyroid hormone secretory response to EDTA-induced hypocalcemia in black and white premenopausal women. Calcif Tissue Int 65:257–261

    Article  PubMed  CAS  Google Scholar 

  49. Henry YM, Eastell R (2000) Ethnic and gender differences in bone mineral density and bone turnover in young adults: effect of bone size. Osteoporos Int 11:512–517

    Article  PubMed  CAS  Google Scholar 

  50. Bryant RJ, Wastney ME, Martin BR, Wood O, McCabe GP, Morshidi M, Smith DL, Peacock M, Weaver CM (2003) Racial differences in bone turnover and calcium metabolism in adolescent females. J Clin Endocrinol Metab 88:1043–1047

    Article  PubMed  CAS  Google Scholar 

  51. Dawson-Hughes B, Harris SS, Finneran S, Rasmussen HM (1995) Calcium absorption responses to calcitriol in black and white premenopausal women. J Clin Endocrinol Metab 80:3068–3072

    Article  PubMed  CAS  Google Scholar 

  52. Perry HM 3rd, Horowitz M, Morley JE, Fleming S, Jensen J, Caccione P, Miller DK, Kaiser FE, Sundarum M (1996) Aging and bone metabolism in African American and Caucasian women. J Clin Endocrinol Metab 81:1108–1117

    Article  PubMed  CAS  Google Scholar 

  53. Bell NH, Greene A, Epstein S, Oexmann MJ, Shaw S, Shary J (1985) Evidence for alteration of the vitamin D-endocrine system in blacks. J Clin Invest 76:470–473

    Article  PubMed  CAS  Google Scholar 

  54. Gundberg CM, Looker AC, Nieman SD, Calvo MS (2002) Patterns of osteocalcin and bone specific alkaline phosphatase by age, gender, and race or ethnicity. Bone 31:703–708

    Article  PubMed  CAS  Google Scholar 

  55. Leder BZ, Araujo AB, Travison TG, McKinlay JB (2007) Racial and ethnic differences in bone turnover markers in men. J Clin Endocrinol Metab 92:3453–3457

    Article  PubMed  CAS  Google Scholar 

  56. Meier DE, Luckey MM, Wallenstein S, Lapinski RH, Catherwood B (1992) Racial differences in pre- and postmenopausal bone homeostasis: association with bone density. J Bone Miner Res 7:1181–1189

    Article  PubMed  CAS  Google Scholar 

  57. Travison TG, Chiu GR, McKinlay JB, Araujo AB (2011) Accounting for racial/ethnic variation in bone mineral content and density: the competing influences of socioeconomic factors, body composition, health and lifestyle, and circulating androgens and estrogens. Osteoporos Int

  58. Williams LJ, Pasco JA, Jacka FN, Henry MJ, Dodd S, Berk M (2009) Depression and bone metabolism. A review. Psychother Psychosom 78:16–25

    Article  PubMed  Google Scholar 

  59. Petronijevic M, Petronijevic N, Ivkovic M, Stefanovic D, Radonjic N, Glisic B, Ristic G, Damjanovic A, Paunovic V (2008) Low bone mineral density and high bone metabolism turnover in premenopausal women with unipolar depression. Bone 42:582–590

    Article  PubMed  CAS  Google Scholar 

  60. Herran A, Amado JA, Garcia-Unzueta MT, Vazquez-Barquero JL, Perera L, Gonzalez-Macias J (2000) Increased bone remodeling in first-episode major depressive disorder. Psychosom Med 62:779–782

    PubMed  CAS  Google Scholar 

  61. Cizza G, Marques AH, Eskandari F, Christie IC, Torvik S, Silverman MN, Phillips TM, Sternberg EM (2008) Elevated neuroimmune biomarkers in sweat patches and plasma of premenopausal women with major depressive disorder in remission: the POWER study. Biol Psychiatry 64:907–911

    Article  PubMed  CAS  Google Scholar 

  62. Cizza G, Eskandari F, Coyle M, Krishnamurthy P, Wright EC, Mistry S, Csako G (2009) Plasma CRP levels in premenopausal women with major depression: a 12-month controlled study. Horm Metab Res 41:641–648

    Article  PubMed  CAS  Google Scholar 

  63. Connor TJ, Leonard BE (1998) Depression, stress and immunological activation: the role of cytokines in depressive disorders. Life Sci 62:583–606

    Article  PubMed  CAS  Google Scholar 

  64. Carroll BJ, Curtis GC, Davies BM, Mendels J, Sugerman AA (1976) Urinary free cortisol excretion in depression. Psychol Med 6:43–50

    Article  PubMed  CAS  Google Scholar 

  65. Gold PW, Goodwin FK, Chrousos GP (1988) Clinical and biochemical manifestations of depression. Relation to the neurobiology of stress (2). N Engl J Med 319:413–420

    Article  PubMed  CAS  Google Scholar 

  66. Halbreich U, Asnis GM, Zumoff B, Nathan RS, Shindledecker R (1984) Effect of age and sex on cortisol secretion in depressives and normals. Psychiatry Res 13:221–229

    Article  PubMed  CAS  Google Scholar 

  67. Black PH (2003) The inflammatory response is an integral part of the stress response: Implications for atherosclerosis, insulin resistance, type II diabetes and metabolic syndrome X. Brain Behav Immun 17:350–364

    Article  PubMed  CAS  Google Scholar 

  68. Owen N, Poulton T, Hay FC, Mohamed-Ali V, Steptoe A (2003) Socioeconomic status, C-reactive protein, immune factors, and responses to acute mental stress. Brain Behav Immun 17:286–295

    Article  PubMed  CAS  Google Scholar 

  69. Steptoe A, Owen N, Kunz-Ebrecht S, Mohamed-Ali V (2002) Inflammatory cytokines, socioeconomic status, and acute stress responsivity. Brain Behav Immun 16:774–784

    Article  PubMed  CAS  Google Scholar 

  70. Maes M, Song C, Lin A et al (1998) The effects of psychological stress on humans: increased production of pro-inflammatory cytokines and a Th1-like response in stress-induced anxiety. Cytokine 10:313–318

    Article  PubMed  CAS  Google Scholar 

  71. Evans GW, English K (2002) The environment of poverty: multiple stressor exposure, psychophysiological stress, and socioemotional adjustment. Child Dev 73:1238–1248

    Article  PubMed  Google Scholar 

  72. Evans GW, Kim P (2007) Childhood poverty and health: cumulative risk exposure and stress dysregulation. Psychol Sci 18:953–957

    Article  PubMed  Google Scholar 

  73. Cohen S, Schwartz JE, Epel E, Kirschbaum C, Sidney S, Seeman T (2006) Socioeconomic status, race, and diurnal cortisol decline in the Coronary Artery Risk Development in Young Adults (CARDIA) Study. Psychosom Med 68:41–50

    Article  PubMed  Google Scholar 

  74. Li L, Power C, Kelly S, Kirschbaum C, Hertzman C (2007) Life-time socio-economic position and cortisol patterns in mid-life. Psychoneuroendocrinology 32:824–833

    Article  PubMed  CAS  Google Scholar 

  75. Steptoe A, Kunz-Ebrecht S, Owen N, Feldman PJ, Willemsen G, Kirschbaum C, Marmot M (2003) Socioeconomic status and stress-related biological responses over the working day. Psychosom Med 65:461–470

    Article  PubMed  Google Scholar 

  76. Manolagas SC, Bellido T, Jilka RL (1995) New insights into the cellular, biochemical, and molecular basis of postmenopausal and senile osteoporosis: roles of IL-6 and gp130. Int J Immunopharmacol 17:109–116

    Article  PubMed  CAS  Google Scholar 

  77. Ginaldi L, Di Benedetto MC, De Martinis M (2005) Osteoporosis, inflammation and ageing. Immun Ageing 2:14

    Article  PubMed  Google Scholar 

  78. Yun AJ, Lee PY (2004) Maldaptation of the link between inflammation and bone turnover may be a key determinant of osteoporosis. Med Hypotheses 63:532–537

    Article  PubMed  Google Scholar 

  79. Pereira RM, Delany AM, Canalis E (2001) Cortisol inhibits the differentiation and apoptosis of osteoblasts in culture. Bone 28:484–490

    Article  PubMed  CAS  Google Scholar 

  80. Cooper MS, Syddall HE, Fall CH, Wood PJ, Stewart PM, Cooper C, Dennison EM (2005) Circulating cortisone levels are associated with biochemical markers of bone formation and lumbar spine BMD: the Hertfordshire Cohort Study. Clin Endocrinol (Oxf) 62:692–697

    Article  CAS  Google Scholar 

  81. Prior L (1999) Socioeconomic status and health chartbook. Health, United States, 1998. Sociology Health Illn 21:851–852

    Google Scholar 

  82. Lewiecki EM (2010) Benefits and limitations of bone mineral density and bone turnover markers to monitor patients treated for osteoporosis. Curr Osteoporos Rep 8:15–22

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This research was supported by National Institutes of Health grant numbers 1R01AG033067, R01-AG-032271, and P01-AG-020166. The UCLA GCRC helped support this study (UCLA GCRC Grant #M01-RR000865).

Conflicts of interest

None

Author information

Authors and Affiliations

  1. Division of General Internal Medicine, David Geffen School of Medicine at University of California, Los Angeles, USA

    C. J. Crandall

  2. Division of Geriatrics, David Geffen School of Medicine at University of California, Los Angeles, USA

    D. Miller-Martinez, G. A. Greendale, T. E. Seeman & A. S. Karlamangla

  3. University of Wisconsin-Madison Osteoporosis Clinical Center and Research Program, Madison, WI, USA

    N. Binkley

  4. David Geffen School of Medicine at University of California, Los Angeles, UCLA Medicine/GIM, 911 Broxton Ave., 1st floor, Los Angeles, CA, 90024, USA

    C. J. Crandall

Authors
  1. C. J. Crandall
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. D. Miller-Martinez
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. G. A. Greendale
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. N. Binkley
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. T. E. Seeman
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. A. S. Karlamangla
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to C. J. Crandall.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Crandall, C.J., Miller-Martinez, D., Greendale, G.A. et al. Socioeconomic status, race, and bone turnover in the Midlife in the US Study. Osteoporos Int 23, 1503–1512 (2012). https://doi.org/10.1007/s00198-011-1736-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00198-011-1736-5

Keywords

Search

Navigation