Inflammatory Markers and the Risk of Hip and Vertebral Fractures in Men: the Osteoporotic Fractures in Men (MrOS)

Journal of Bone and Mineral Research

Volumn 31, Issue 12, 2016, Pages 2129-2138

  Cauley, Jane A ^a   Barbour, Kamil E ^b   Harrison, Stephanie L ^c   Cloonan, Yona K ^a   Danielson, Michelle E ^a   Ensrud, Kristine E ^d,e,f   Fink, Howard A ^e,f   Orwoll, Eric S ^g   Boudreau, Robert ^a  

^a UNIVERSITY OF PITTSBURGH GRADUATE SCHOOL OF PUBLIC HEALTH   (United States)

^b CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

^c CALIFORNIA PACIFIC MEDICAL CENTER   (United States)

^d UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^e UNIVERSITY OF MINNESOTA   (United States)

^f VETERANS AFFAIRS MEDICAL CENTER   (United States)

^g OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

AGING; CYTOKINES; FRACTURE RISK ASSESSMENT; GENERAL POPULATION STUDIES; OSTEOPOROSIS

Indexed keywords

BIOLOGICAL MARKER; C REACTIVE PROTEIN; INTERLEUKIN 10; INTERLEUKIN 6; INTERLEUKIN 6 RECEPTOR; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR ALPHA RECEPTOR; TUMOR NECROSIS FACTOR ALPHA SR1; TUMOR NECROSIS FACTOR ALPHA SR2; UNCLASSIFIED DRUG; CYTOKINE;

AGED; APPENDICULAR LEAN MASS; ARTICLE; BONE DENSITY; COHORT ANALYSIS; DISABILITY; FOLLOW UP; FRAGILITY FRACTURE; HIGH RISK POPULATION; HIP FRACTURE; HUMAN; INFLAMMATION; LEAN BODY WEIGHT; MAJOR CLINICAL STUDY; MALE; RISK ASSESSMENT; SPINE FRACTURE; BLOOD; COMPLICATION; INCIDENCE; METABOLISM; OSTEOLYSIS; PROPORTIONAL HAZARDS MODEL; RISK FACTOR;

BIOMARKERS; BONE RESORPTION; C-REACTIVE PROTEIN; CYTOKINES; HIP FRACTURES; HUMANS; INCIDENCE; INFLAMMATION; MALE; OSTEOPOROTIC FRACTURES; PROPORTIONAL HAZARDS MODELS; RISK FACTORS; SPINAL FRACTURES;

EID: 84994440967     PISSN: 08840431     EISSN: 15234681     Source Type: Journal    
DOI: 10.1002/jbmr.2905     Document Type: Article

References (52)

1. Kimble RB, Matayoshi AB, Vannice JL, Kung VT, Williams C, Pacifici R. Simultaneous block of interleukin-1 and tumor necrosis factor is required to completely prevent bone loss in the early postovariectomy period. Endocrinology. 1995; 136(7):3054–61.
2. Weitzmann MN, Cenci S, Rifas L, Haug J, Dipersio J, Pacifici R. T cell activation induces human osteoclast formation via receptor activator of nuclear factor kappaB ligand-dependent and -independent mechanisms. J Bone Miner Res. 2001; 16(2):328–37.
3. Kawaguchi H, Pilbeam CC, Vargas SJ, Morse EE, Lorenzo JA, Raisz LG. Ovariectomy enhances and estrogen replacement inhibits the activity of bone marrow factors that stimulate prostaglandin production in cultured mouse calvariae. J Clin Invest. 1995; 96(1):539–48.
4. Zupan J, Jeras M, Marc J. Osteoimmunology and the influence of pro-inflammatory cytokines on osteoclasts. Biochem Med (Zagreb). 2013; 23(1):43–63.
5. Cauley JA, Danielson ME, Boudreau RM, et al. Inflammatory markers and incident fracture risk in older men and women: the health aging and body composition study. J Bone Miner Res. 2007; 22(7):1088–95.
6. Barbour KE, Boudreau R, Danielson ME, et al. Inflammatory markers and the risk of hip fracture: the Women's Health Initiative. J Bone Miner Res. 2012; 27(5):1167–76.
7. Barbour KE, Lui LY, Ensrud KE, et al. Inflammatory markers and risk of hip fracture in older white women: the study of osteoporotic fractures. J Bone Miner Res. 2014; 29(9):2057–64.
8. Ing SW, Orchard TS, Lu B, et al. TNF receptors predict hip fracture risk in the WHI study and fatty acid intake does not modify this association. J Clin Endocrinol Metab. 2015; 100(9):3380–7.
9. Ding C, Parameswaran V, Udayan R, Burgess J, Jones G. Circulating levels of inflammatory markers predict change in bone mineral density and resorption in older adults: a longitudinal study. J Clin Endocrinol Metab. 2008; 93(5):1952–8.
10. Gertz ER, Silverman NE, Wise KS, et al. Contribution of serum inflammatory markers to changes in bone mineral content and density in postmenopausal women: a 1-year investigation. J Clin Densitom. 2010; 13(3):277–82.
11. Scheidt-Nave C, Bismar H, Leidig-Bruckner G, et al. Serum interleukin 6 is a major predictor of bone loss in women specific to the first decade past menopause. J Clin Endocrinol Metab. 2001; 86(5):2032–42.
12. Schett G, Kiechl S, Weger S, et al. High-sensitivity C-reactive protein and risk of nontraumatic fractures in the Bruneck study. Arch Intern Med. 2006; 166(22):2495–501.
13. Dahl K, Ahmed LA, Joakimsen RM, et al. High-sensitivity C-reactive protein is an independent risk factor for non-vertebral fractures in women and men: the Tromso Study. Bone. 2015; 72:65–70.
14. Orwoll E, Blank JB, Barrett-Connor E, et al. Design and baseline characteristics of the osteoporotic fractures in men (MrOS) study—a large observational study of the determinants of fracture in older men. Contemp Clin Trials. 2005; 26(5):569–85.
15. Blank JB, Cawthon PM, Carrion-Petersen ML, et al. Overview of recruitment for the Osteoporotic Fractures in Men Study (MrOS). Contemp Clin Trials. 2005; 26(5):557–68.
16. Prentice R. A case-cohort design for epidemiologic cohort studies and disease prevention trials. Biometricka. 1986; 73:1–11.
17. Genant HK, Wu CY, van Kuijk C, Nevitt MC. Vertebral fracture assessment using a semiquantitative technique. J Bone Miner Res. 1993; 8(9):1137–48.
18. Penninx BW, Kritchevsky SB, Newman AB, et al. Inflammatory markers and incident mobility limitation in the elderly. J Am Geriatr Soc. 2004; 52(7):1105–13.
19. Cauley JA, Cawthon PM, Peters KE, et al. Risk factors for hip fracture in older men: the Osteoporotic Fractures in Men Study (MrOS). J Bone Miner Res. Epub 2016 Mar 14.
20. Pahor M, Chrischilles EA, Guralnik JM, Brown SL, Wallace RB, Carbonin P. Drug data coding and analysis in epidemiologic studies. Eur J Epidemiol. 1994; 10(4):405–11.
21. Washburn RA, Smith KW, Jette AM, Janney CA. The Physical Activity Scale for the Elderly (PASE): development and evaluation. J Clin Epidemiol. 1993; 46(2):153–62.
22. Cawthon PM, Ewing SK, McCulloch CE, et al. Loss of hip BMD in older men: the Osteoporotic Fractures in Men (MrOS) study. J Bone Miner Res. 2009; 24(10):1728–35.
23. Cummings SR, Bates D, Black DM. Clinical use of bone densitometry: scientific review. JAMA. 2002; 288(15):1889–97.
24. Hochberg Y, Benjamini Y. More powerful procedures for multiple significance testing. Stat Med. 1990; 9(7):811–8.
25. Visser M, Simonsick EM, Colbert LH, et al. Type and intensity of activity and risk of mobility limitation: the mediating role of muscle parameters. J Am Geriatr Soc. 2005; 53(5):762–70.
26. Bertolini DR, Nedwin GE, Bringman TS, Smith DD, Mundy GR. Stimulation of bone resorption and inhibition of bone formation in vitro by human tumour necrosis factors. Nature. 1986; 319(6053):516–8.
27. Johnson RA, Boyce BF, Mundy GR, Roodman GD. Tumors producing human tumor necrosis factor induced hypercalcemia and osteoclastic bone resorption in nude mice. Endocrinology. 1989; 124(3):1424–7.
28. Kostenuik PJ, Shalhoub V. Osteoprotegerin: a physiological and pharmacological inhibitor of bone resorption. Curr Pharm Des. 2001; 7(8):613–35.
29. Clowes JA, Riggs BL, Khosla S. The role of the immune system in the pathophysiology of osteoporosis. Immunol Rev. 2005; 208:207–27.
30. Visser M, Pahor M, Taaffe DR, et al. Relationship of interleukin-6 and tumor necrosis factor-alpha with muscle mass and muscle strength in elderly men and women: the Health ABC Study. J Gerontol A Biol Sci Med Sci. 2002; 57(5):M326–32.
31. Schaap LA, Pluijm SM, Deeg DJ, Visser M. Inflammatory markers and loss of muscle mass (sarcopenia) and strength. Am J Med. 2006; 119(6):526 e9–17.
32. Wannamethee SG, Whincup PH, Lennon L, Papacosta O, Lowe GD. Associations between fibrin D-dimer, markers of inflammation, incident self-reported mobility limitation, and all-cause mortality in older men. J Am Geriatr Soc. 2014; 62(12):2357–62.
33. Brinkley TE, Leng X, Miller ME, et al. Chronic inflammation is associated with low physical function in older adults across multiple comorbidities. J Gerontol A Biol Sci Med Sci. 2009; 64(4):455–61.
34. Ferrucci L, Penninx BW, Volpato S, et al. Change in muscle strength explains accelerated decline of physical function in older women with high interleukin-6 serum levels. J Am Geriatr Soc. 2002; 50(12):1947–54.
35. Schaap LA, Pluijm SM, Deeg DJ, et al. Higher inflammatory marker levels in older persons: associations with 5-year change in muscle mass and muscle strength. J Gerontol A Biol Sci Med Sci. 2009; 64(11):1183–9.
36. Janssen SP, Gayan-Ramirez G, Van den Bergh A, et al. Interleukin-6 causes myocardial failure and skeletal muscle atrophy in rats. Circulation. 2005; 111(8):996–1005.
37. Li YP, Schwartz RJ, Waddell ID, Holloway BR, Reid MB. Skeletal muscle myocytes undergo protein loss and reactive oxygen-mediated NF-kappaB activation in response to tumor necrosis factor alpha. FASEB J. 1998; 12(10):871–80.
38. Li X, Moody MR, Engel D, et al. Cardiac-specific overexpression of tumor necrosis factor-alpha causes oxidative stress and contractile dysfunction in mouse diaphragm. Circulation. 2000; 102(14):1690–6.
39. Mohamed-Ali V, Pinkney JH, Coppack SW. Adipose tissue as an endocrine and paracrine organ. Int J Obes Relat Metab Disord. 1998; 22(12):1145–58.
40. Visser M, Bouter LM, McQuillan GM, Wener MH, Harris TB. Elevated C-reactive protein levels in overweight and obese adults. JAMA. 1999; 282(22):2131–5.
41. Fried SK, Bunkin DA, Greenberg AS. Omental and subcutaneous adipose tissues of obese subjects release interleukin-6: depot difference and regulation by glucocorticoid. J Clin Endocrinol Metab. 1998; 83(3):847–50.
42. Fain JN, Madan AK, Hiler ML, Cheema P, Bahouth SW. Comparison of the release of adipokines by adipose tissue, adipose tissue matrix, and adipocytes from visceral and subcutaneous abdominal adipose tissues of obese humans. Endocrinology. 2004; 145(5):2273–82.
43. de Vries JE. Immunosuppressive and anti-inflammatory properties of interleukin 10. Ann Med. 1995; 27(5):537–41.
44. Morita Y, Yamamura M, Kashihara N, Makino H. Increased production of interleukin-10 and inflammatory cytokines in blood monocytes of hemodialysis patients. Res Commun Mol Pathol Pharmacol. 1997; 98(1):19–33.
45. Dresner-Pollak R, Parker RA, Poku M, Thompson J, Seibel MJ, Greenspan SL. Biochemical markers of bone turnover reflect femoral bone loss in elderly women. Calcif Tissue Int. 1996; 59(5):328–33.
46. Saraiva M, O'Garra A. The regulation of IL-10 production by immune cells. Nat Rev Immunol. 2010; 10(3):170–81.
47. Pasco JA, Kotowicz MA, Henry MJ, et al. High-sensitivity C-reactive protein and fracture risk in elderly women. JAMA. 2006; 296(11):1353–5.
48. Ishii S, Cauley JA, Greendale GA, et al. C-reactive protein, bone strength, and nine-year fracture risk: data from the Study of Women's Health Across the Nation (SWAN). J Bone Miner Res. 2013; 28(7):1688–98.
49. Nakamura K, Saito T, Kobayashi R, et al. C-reactive protein predicts incident fracture in community-dwelling elderly Japanese women: the Muramatsu study. Osteoporos Int. 2011; 22(7):2145–50.
50. Ganesan K, Teklehaimanot S, Tran TH, Asuncion M, Norris K. Relationship of C-reactive protein and bone mineral density in community-dwelling elderly females. J Natl Med Assoc. 2005; 97(3):329–33.
51. Koh JM, Khang YH, Jung CH, et al. Higher circulating hsCRP levels are associated with lower bone mineral density in healthy pre- and postmenopausal women: evidence for a link between systemic inflammation and osteoporosis. Osteoporos Int. 2005; 16(10):1263–71.
52. Kim BJ, Yu YM, Kim EN, Chung YE, Koh JM, Kim GS. Relationship between serum hsCRP concentration and biochemical bone turnover markers in healthy pre- and postmenopausal women. Clin Endocrinol (Oxf). 2007; 67(1):152–8.