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

Osteoporosis International

Volumn 23, Issue 5, 2012, Pages 1503-1512

  Crandall, C J ^a   Miller Martinez, D ^a   Greendale, G A ^a   Binkley, N ^b   Seeman, T E ^a   Karlamangla, A S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

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

Indexed keywords

ALKALINE PHOSPHATASE BONE ISOENZYME; AMINO TERMINAL TELOPEPTIDE; PROCOLLAGEN TYPE I N TERMINAL PROPEPTIDE; PROTEIN PRECURSOR; UNCLASSIFIED DRUG;

ADULT; AFRICAN AMERICAN; AGE; ALKALINE PHOSPHATASE BLOOD LEVEL; ARTICLE; BODY WEIGHT; BONE TURNOVER; CONTROLLED STUDY; EDUCATIONAL STATUS; FEMALE; HUMAN; INCOME; MALE; MENOPAUSE; POVERTY; PRIORITY JOURNAL; RACE DIFFERENCE; SOCIAL STATUS; UNITED STATES;

ADULT; AFRICAN AMERICANS; AGED; ALKALINE PHOSPHATASE; BIOLOGICAL MARKERS; BONE REMODELING; BONE RESORPTION; COLLAGEN TYPE I; CROSS-SECTIONAL STUDIES; FEMALE; HUMANS; MALE; MIDDLE AGED; PEPTIDE FRAGMENTS; PEPTIDES; POVERTY; PROCOLLAGEN; SEX CHARACTERISTICS; SOCIAL CLASS; SOCIOECONOMIC FACTORS; STRESS, PSYCHOLOGICAL; UNITED STATES;

EID: 84863610570     PISSN: 0937941X     EISSN: 14332965     Source Type: Journal    
DOI: 10.1007/s00198-011-1736-5     Document Type: Article

References (81)

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
2. Civitelli RA-VR, Napoli N (2009) Bone turnover markers: understanding their value in clinical trials and clinical practice. Osteoporosis Int 20:843-851
3. 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 (Pubitemid 30484522)
4. 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 (Pubitemid 26331009)
5. 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 (Pubitemid 26061239)
6. 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 (Pubitemid 30099514)
7. 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 (Pubitemid 24026404)
8. Williams DR (1996) Race/ethnicity and socioeconomic status: measurement and methodological issues. Int J Health Serv 26:483-505 (Pubitemid 26257182)
9. 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 (Pubitemid 27449492)
10. Williams DR, Collins C (2001) Racial residential segregation: a fundamental cause of racial disparities in health. Public Health Rep 116:404-416 (Pubitemid 34579067)
11. Willhelm SM (1986) The economic demise of blacks in America: a prelude to genocide? J Black Stud 17:201-254
12. 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
13. Brim OG, Ryff CD, Kessler RC (2004) How healthy are we?: a national study of well-being at midlife. University of Chicago Press, Chicago
14. 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
15. 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 (Pubitemid 23027685)
16. Godin G, Shephard RJ (1985) A simple method to assess exercise behavior in the community. Can J Appl Sport Sci 10:141-146
17. Brown JP, Albert C, Nassar BA et al (2009) Bone turnover markers in the management of postmenopausal osteoporosis. Clin Biochem 42:929-942
18. Seibel MJ (2005) Biochemical markers of bone turnover: part I: biochemistry and variability. Clin Biochem Rev 26:97-122
19. Gerdhem P, Isaksson A, Akesson K, Obrant KJ (2005) Increased bone density and decreased bone turnover, but no evidentalteration of fracture susceptibility in elderly women with diabetes mellitus. Osteoporos Int 16:1506-1512 (Pubitemid 41790853)
20. 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 (Pubitemid 44402104)
21. Yaturu S (2009) Diabetes and skeletal health. J Diabetes 1:246-254
22. Compston J (2009) Monitoring osteoporosis treatment. Best Pract Res Clin Rheumatol 23:781-788
23. 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 (Pubitemid 34615244)
24. 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
25. 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
26. 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 (Pubitemid 39612374)
27. 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 (Pubitemid 27365697)
28. 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
29. 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
30. Aloia JF (2008) African Americans, 25-hydroxyvitamin D, and osteoporosis: a paradox. Am J Clin Nutr 88:545S-550S
31. Rosen CJ (2011) Clinical practice. Vitamin D insufficiency. N Engl J Med 364:248-254
32. 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 (Pubitemid 12248649)
33. 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 (Pubitemid 34468001)
34. 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 (Pubitemid 27225006)
35. 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 (Pubitemid 32762324)
36. Lips P (2006) Vitamin D physiology. Prog Biophys Mol Biol 92:4-8 (Pubitemid 43831956)
37. 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 (Pubitemid 27225007)
38. 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 (Pubitemid 29339752)
39. 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 (Pubitemid 32055363)
40. 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 (Pubitemid 24238358)
41. 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 (Pubitemid 15243466)
42. 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 (Pubitemid 32755979)
43. 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 (Pubitemid 28552096)
44. Aloia JF, Vaswani A, Yeh JK, Flaster E (1996) Risk for osteoporosis in black women. Calcif Tissue Int 59:415-423 (Pubitemid 26397158)
45. Hannon R, Eastell R (2000) Preanalytical variability of biochemical markers of bone turnover. Osteoporos Int 11(SUPPL. 6):S30-S44 (Pubitemid 32039511)
46. 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 (Pubitemid 34816344)
47. 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 (Pubitemid 29471003)
48. 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
49. 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 (Pubitemid 36337754)
50. 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
51. 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 (Pubitemid 26083978)
52. 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 (Pubitemid 15227507)
53. 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 (Pubitemid 36092094)
54. 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 (Pubitemid 47435319)
55. 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
56. 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
57. Williams LJ, Pasco JA, Jacka FN, Henry MJ, Dodd S, Berk M (2009) Depression and bone metabolism. A review. Psychother Psychosom 78:16-25
58. 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
59. 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 (Pubitemid 32009083)
60. 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
61. 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
62. Connor TJ, Leonard BE (1998) Depression, stress and immunological activation: the role of cytokines in depressive disorders. Life Sci 62:583-606 (Pubitemid 28045567)
63. Carroll BJ, Curtis GC, Davies BM, Mendels J, Sugerman AA (1976) Urinary free cortisol excretion in depression. Psychol Med 6:43-50
64. 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
65. 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 (Pubitemid 15224202)
66. 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 (Pubitemid 36999842)
67. 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 (Pubitemid 36794149)
68. 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 (Pubitemid 36027067)
69. 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 (Pubitemid 28227076)
70. Evans GW, English K (2002) The environment of poverty: multiple stressor exposure, psychophysiological stress, and socioemotional adjustment. Child Dev 73:1238-1248 (Pubitemid 41692425)
71. Evans GW, Kim P (2007) Childhood poverty and health: cumulative risk exposure and stress dysregulation. Psychol Sci 18:953-957
72. 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 (Pubitemid 43803214)
73. Li L, Power C, Kelly S, Kirschbaum C, Hertzman C (2007) Lifetime socio-economic position and cortisol patterns in mid-life. Psychoneuroendocrinology 32:824-833 (Pubitemid 47189731)
74. 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 (Pubitemid 36628900)
75. 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
76. Ginaldi L, Di Benedetto MC, De Martinis M (2005) Osteoporosis, inflammation and ageing. Immun Ageing 2:14
77. 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 (Pubitemid 38993626)
78. Pereira RM, Delany AM, Canalis E (2001) Cortisol inhibits the differentiation and apoptosis of osteoblasts in culture. Bone 28:484-490 (Pubitemid 32409999)
79. 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 (Pubitemid 40825939)
80. Prior L (1999) Socioeconomic status and health chartbook. Health, United States, 1998. Sociology Health Illn 21:851-852
81. 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