Osteoporosis International

, Volume 23, Issue 5, pp 1503–1512 | Cite as

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

  • C. J. CrandallEmail author
  • D. Miller-Martinez
  • G. A. Greendale
  • N. Binkley
  • T. E. Seeman
  • A. S. Karlamangla
Original Article



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.


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


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.


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.


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.


Bone resorption Bone turnover Bone-specific alkaline phosphatase BSAP Income N-telopeptide Ntx PINP Poverty Procollagen type I N-terminal propeptide SES Socioeconomic status 



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



  1. 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 1186:223–239PubMedCrossRefGoogle Scholar
  2. 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, WashingtonGoogle Scholar
  3. 3.
    Civitelli RA-VR, Napoli N (2009) Bone turnover markers: understanding their value in clinical trials and clinical practice. Osteoporosis Int 20:843–851CrossRefGoogle Scholar
  4. 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 15:1526–1536PubMedCrossRefGoogle Scholar
  5. 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 11:1531–1538PubMedCrossRefGoogle Scholar
  6. 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 312:482–483PubMedCrossRefGoogle Scholar
  7. 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 11:76–82PubMedCrossRefGoogle Scholar
  8. 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 9:82–122PubMedGoogle Scholar
  9. 9.
    Williams DR (1996) Race/ethnicity and socioeconomic status: measurement and methodological issues. Int J Health Serv 26:483–505PubMedCrossRefGoogle Scholar
  10. 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 8:621–628PubMedGoogle Scholar
  11. 11.
    Williams DR, Collins C (2001) Racial residential segregation: a fundamental cause of racial disparities in health. Public Health Rep 116:404–416PubMedGoogle Scholar
  12. 12.
    Willhelm SM (1986) The economic demise of blacks in America: a prelude to genocide? J Black Stud 17:201–254PubMedCrossRefGoogle Scholar
  13. 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 22:1059–1080PubMedCrossRefGoogle Scholar
  14. 14.
    Brim OG, Ryff CD, Kessler RC (2004) How healthy are we?: a national study of well-being at midlife. University of Chicago Press, ChicagoGoogle Scholar
  15. 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 22:307–331PubMedCrossRefGoogle Scholar
  16. 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 25:71–80PubMedCrossRefGoogle Scholar
  17. 17.
    Godin G, Shephard RJ (1985) A simple method to assess exercise behavior in the community. Can J Appl Sport Sci 10:141–146PubMedGoogle Scholar
  18. 18.
    Brown JP, Albert C, Nassar BA et al (2009) Bone turnover markers in the management of postmenopausal osteoporosis. Clin Biochem 42:929–942PubMedCrossRefGoogle Scholar
  19. 19.
    Seibel MJ (2005) Biochemical markers of bone turnover: part I: biochemistry and variability. Clin Biochem Rev 26:97–122PubMedGoogle Scholar
  20. 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 16:1506–1512PubMedCrossRefGoogle Scholar
  21. 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 91:3355–3363PubMedCrossRefGoogle Scholar
  22. 22.
    Yaturu S (2009) Diabetes and skeletal health. J Diabetes 1:246–254PubMedCrossRefGoogle Scholar
  23. 23.
    Compston J (2009) Monitoring osteoporosis treatment. Best Pract Res Clin Rheumatol 23:781–788PubMedCrossRefGoogle Scholar
  24. 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 87:1586–1592PubMedCrossRefGoogle Scholar
  25. 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 46:952–956PubMedCrossRefGoogle Scholar
  26. 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 20:617–628PubMedCrossRefGoogle Scholar
  27. 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 60:999–1015PubMedCrossRefGoogle Scholar
  28. 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 2:315–334Google Scholar
  29. 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 107:411–429PubMedCrossRefGoogle Scholar
  30. 30.
    Matsuoka LY, Wortsman J, Haddad JG, Kolm P, Hollis BW (1991) Racial pigmentation and the cutaneous synthesis of vitamin D. Arch Dermatol 127:536–538PubMedCrossRefGoogle Scholar
  31. 31.
    Aloia JF (2008) African Americans, 25-hydroxyvitamin D, and osteoporosis: a paradox. Am J Clin Nutr 88:545S–550SPubMedGoogle Scholar
  32. 32.
    Rosen CJ (2011) Clinical practice. Vitamin D insufficiency. N Engl J Med 364:248–254PubMedCrossRefGoogle Scholar
  33. 33.
    Clemens TL, Adams JS, Henderson SL, Holick MF (1982) Increased skin pigment reduces the capacity of skin to synthesise vitamin D3. Lancet 1:74–76PubMedCrossRefGoogle Scholar
  34. 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 30:771–777PubMedCrossRefGoogle Scholar
  35. 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 12:948–957PubMedCrossRefGoogle Scholar
  36. 36.
    Lips P (2001) Vitamin D deficiency and secondary hyperparathyroidism in the elderly: consequences for bone loss and fractures and therapeutic implications. Endocr Rev 22:477–501PubMedCrossRefGoogle Scholar
  37. 37.
    Lips P (2006) Vitamin D physiology. Prog Biophys Mol Biol 92:4–8PubMedCrossRefGoogle Scholar
  38. 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 12:958–966PubMedCrossRefGoogle Scholar
  39. 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 25:178–184PubMedCrossRefGoogle Scholar
  40. 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 85:4125–4130PubMedCrossRefGoogle Scholar
  41. 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 9:1267–1276PubMedCrossRefGoogle Scholar
  42. 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 76:370–373PubMedCrossRefGoogle Scholar
  43. 43.
    Harris SS, Soteriades E, Dawson-Hughes B (2001) Secondary hyperparathyroidism and bone turnover in elderly blacks and whites. J Clin Endocrinol Metab 86:3801–3804PubMedCrossRefGoogle Scholar
  44. 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 132:383–389PubMedCrossRefGoogle Scholar
  45. 45.
    Aloia JF, Vaswani A, Yeh JK, Flaster E (1996) Risk for osteoporosis in black women. Calcif Tissue Int 59:415–423PubMedCrossRefGoogle Scholar
  46. 46.
    Hannon R, Eastell R (2000) Preanalytical variability of biochemical markers of bone turnover. Osteoporos Int 11(Suppl 6):S30–S44PubMedCrossRefGoogle Scholar
  47. 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 87:3051–3056PubMedCrossRefGoogle Scholar
  48. 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 65:257–261PubMedCrossRefGoogle Scholar
  49. 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 11:512–517PubMedCrossRefGoogle Scholar
  50. 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 88:1043–1047PubMedCrossRefGoogle Scholar
  51. 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 80:3068–3072PubMedCrossRefGoogle Scholar
  52. 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 81:1108–1117PubMedCrossRefGoogle Scholar
  53. 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 76:470–473PubMedCrossRefGoogle Scholar
  54. 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 31:703–708PubMedCrossRefGoogle Scholar
  55. 55.
    Leder BZ, Araujo AB, Travison TG, McKinlay JB (2007) Racial and ethnic differences in bone turnover markers in men. J Clin Endocrinol Metab 92:3453–3457PubMedCrossRefGoogle Scholar
  56. 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 7:1181–1189PubMedCrossRefGoogle Scholar
  57. 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 IntGoogle Scholar
  58. 58.
    Williams LJ, Pasco JA, Jacka FN, Henry MJ, Dodd S, Berk M (2009) Depression and bone metabolism. A review. Psychother Psychosom 78:16–25PubMedCrossRefGoogle Scholar
  59. 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 42:582–590PubMedCrossRefGoogle Scholar
  60. 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 62:779–782PubMedGoogle Scholar
  61. 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 64:907–911PubMedCrossRefGoogle Scholar
  62. 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 41:641–648PubMedCrossRefGoogle Scholar
  63. 63.
    Connor TJ, Leonard BE (1998) Depression, stress and immunological activation: the role of cytokines in depressive disorders. Life Sci 62:583–606PubMedCrossRefGoogle Scholar
  64. 64.
    Carroll BJ, Curtis GC, Davies BM, Mendels J, Sugerman AA (1976) Urinary free cortisol excretion in depression. Psychol Med 6:43–50PubMedCrossRefGoogle Scholar
  65. 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 319:413–420PubMedCrossRefGoogle Scholar
  66. 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 13:221–229PubMedCrossRefGoogle Scholar
  67. 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 17:350–364PubMedCrossRefGoogle Scholar
  68. 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 17:286–295PubMedCrossRefGoogle Scholar
  69. 69.
    Steptoe A, Owen N, Kunz-Ebrecht S, Mohamed-Ali V (2002) Inflammatory cytokines, socioeconomic status, and acute stress responsivity. Brain Behav Immun 16:774–784PubMedCrossRefGoogle Scholar
  70. 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 10:313–318PubMedCrossRefGoogle Scholar
  71. 71.
    Evans GW, English K (2002) The environment of poverty: multiple stressor exposure, psychophysiological stress, and socioemotional adjustment. Child Dev 73:1238–1248PubMedCrossRefGoogle Scholar
  72. 72.
    Evans GW, Kim P (2007) Childhood poverty and health: cumulative risk exposure and stress dysregulation. Psychol Sci 18:953–957PubMedCrossRefGoogle Scholar
  73. 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 68:41–50PubMedCrossRefGoogle Scholar
  74. 74.
    Li L, Power C, Kelly S, Kirschbaum C, Hertzman C (2007) Life-time socio-economic position and cortisol patterns in mid-life. Psychoneuroendocrinology 32:824–833PubMedCrossRefGoogle Scholar
  75. 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 65:461–470PubMedCrossRefGoogle Scholar
  76. 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 17:109–116PubMedCrossRefGoogle Scholar
  77. 77.
    Ginaldi L, Di Benedetto MC, De Martinis M (2005) Osteoporosis, inflammation and ageing. Immun Ageing 2:14PubMedCrossRefGoogle Scholar
  78. 78.
    Yun AJ, Lee PY (2004) Maldaptation of the link between inflammation and bone turnover may be a key determinant of osteoporosis. Med Hypotheses 63:532–537PubMedCrossRefGoogle Scholar
  79. 79.
    Pereira RM, Delany AM, Canalis E (2001) Cortisol inhibits the differentiation and apoptosis of osteoblasts in culture. Bone 28:484–490PubMedCrossRefGoogle Scholar
  80. 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) 62:692–697CrossRefGoogle Scholar
  81. 81.
    Prior L (1999) Socioeconomic status and health chartbook. Health, United States, 1998. Sociology Health Illn 21:851–852Google Scholar
  82. 82.
    Lewiecki EM (2010) Benefits and limitations of bone mineral density and bone turnover markers to monitor patients treated for osteoporosis. Curr Osteoporos Rep 8:15–22PubMedCrossRefGoogle Scholar

Copyright information

© International Osteoporosis Foundation and National Osteoporosis Foundation 2011

Authors and Affiliations

  • C. J. Crandall
    • 1
    • 4
    Email author
  • D. Miller-Martinez
    • 2
  • G. A. Greendale
    • 2
  • N. Binkley
    • 3
  • T. E. Seeman
    • 2
  • A. S. Karlamangla
    • 2
  1. 1.Division of General Internal MedicineDavid Geffen School of Medicine at University of CaliforniaLos AngelesUSA
  2. 2.Division of GeriatricsDavid Geffen School of Medicine at University of CaliforniaLos AngelesUSA
  3. 3.University of Wisconsin-Madison Osteoporosis Clinical Center and Research ProgramMadisonUSA
  4. 4.David Geffen School of Medicine at University of California, Los Angeles, UCLA Medicine/GIMLos AngelesUSA

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