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ORIGINAL RESEARCH

Associations Between Inflammatory Mediators and Bone Outcomes in Postmenopausal Women: A Cross-Sectional Analysis of Baseline Data from the Prune Study

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Pages 639-663 | Received 16 Nov 2022, Accepted 27 Jan 2023, Published online: 15 Feb 2023

References

  • Kanis JA, Melton LJ, Christiansen C, Johnston CC, Khaltaev N. The diagnosis of osteoporosis. J Bone Miner Res. 2009;9(8):1137–1141. doi:10.1002/jbmr.5650090802
  • NIH Consensus Development Panel on Osteoporosis Prevention, Diagnosis, and Therapy. Osteoporosis prevention, diagnosis, and therapy. JAMA. 2001;285(6):785–795.
  • Compston JE, McClung MR, Leslie WD. Osteoporosis. Lancet. 2019;393(10169):364–376.
  • Johnell O, Kanis JA. An estimate of the worldwide prevalence and disability associated with osteoporotic fractures. Osteoporos Int. 2006;17(12):1726–1733.
  • Kanis JA. Assessment of fracture risk and its application to screening for postmenopausal osteoporosis: synopsis of a WHO report. WHO Study Group. Osteoporos Int. 1994;4(6):368–381.
  • Xiao PL, Cui AY, Hsu CJ, et al. Global, regional prevalence, and risk factors of osteoporosis according to the World Health Organization diagnostic criteria: a systematic review and meta-analysis. Osteoporos Int. 2022;33(10):2137–2153.
  • Sarafrazi N, Wambogo EA, Shepherd JA. Osteoporosis or low bone mass in older adults: United States, 2017–2018. NCHS Data Brief. 2021;405:1–8.
  • Burge R, Dawson-Hughes B, Solomon DH, Wong JB, King A, Tosteson A. Incidence and economic burden of osteoporosis-related fractures in the United States, 2005–2025. J Bone Miner Res. 2007;22(3):465–475.
  • Wright NC, Looker AC, Saag KG, et al. The recent prevalence of osteoporosis and low bone mass in the United States based on bone mineral density at the femoral neck or lumbar spine. J Bone Miner Res. 2014;29(11):2520–2526.
  • Singer A, Exuzides A, Spangler L, et al. Burden of illness for osteoporotic fractures compared with other serious diseases among postmenopausal women in the United States. Mayo Clin Proc. 2015;90(1):53–62. doi:10.1016/j.mayocp.2014.09.011
  • Cauley JA, Thompson DE, Ensrud KC, Scott JC, Black D. Risk of mortality following clinical fractures. Osteoporos Int. 2000;11(7):556–561.
  • Johnell O, Kanis JA, Odén A, et al. Mortality after osteoporotic fractures. Osteoporos Int. 2004;15(1):38–42.
  • Brauer CA, Coca-Perraillon M, Cutler DM, Rosen AB. Incidence and mortality of Hip fractures in the United States. JAMA. 2009;302(14):1573–1579.
  • Lorentzon M, Johansson H, Harvey NC, et al. Osteoporosis and fractures in women: the burden of disease. Climacteric. 2022;25(1):4–10.
  • Office of the Surgeon General (US). Bone Health and Osteoporosis: A Report of the Surgeon General. Rockville (MD): Office of the Surgeon General (US); 2004.
  • Blake J, Cosman FA, Lewiecki EM, et al. Management of osteoporosis in postmenopausal women: the 2021 position statement of The North American Menopause Society. Menopause. 2021;28(9):973–997.
  • Hannan MT, Felson DT, Dawson-Hughes B, et al. Risk factors for longitudinal bone loss in elderly men and women: the Framingham Osteoporosis Study. J Bone Miner Res. 2010;15(4):710–720.
  • Khosla S, Oursler MJ, Monroe DG. Estrogen and the skeleton. Trends Endocrinol Metab. 2012;23(11):576–581.
  • Manolagas SC, Jilka RL. Bone marrow, cytokines, and bone remodeling. Emerging insights into the pathophysiology of osteoporosis. N Engl J Med. 1995;332(5):305–311.
  • Pfeilschifter J. Role of cytokines in postmenopausal bone loss. Curr Osteoporos Rep. 2003;1(2):53–58.
  • Pacifici R. Estrogen, cytokines, and pathogenesis of postmenopausal osteoporosis. J Bone Miner Res. 1996;11(8):1043–1051.
  • Ginaldi L, Di Benedetto MC, De Martinis M. Osteoporosis, inflammation and ageing. Immun Ageing. 2005;2(1):14.
  • Mundy GR. Osteoporosis and inflammation. Nutr Rev. 2007;65(12 Pt 2):S147–S151.
  • Franceschi C, Campisi J. Chronic inflammation (inflammaging) and its potential contribution to age-associated diseases. J Gerontol a Biol Sci Med Sci. 2014;69(Suppl 1):S4–S9.
  • Rea IM, Gibson DS, McGilligan V, McNerlan SE, Alexander HD, Ross OA. Age and age-related diseases: role of inflammation triggers and cytokines. Front Immunol. 2018;9:586.
  • Gregor MF, Hotamisligil GS. Inflammatory mechanisms in obesity. Annu Rev Immunol. 2011;29(1):415–445.
  • Cao JJ. Effects of obesity on bone metabolism. J Orthop Surg Res. 2011;6(1):30.
  • Sponholtz TR, Zhang X, Fontes JD, et al. Association between inflammatory biomarkers and bone mineral density in a community-based cohort of men and women. Arthritis Care Res. 2014;66(8):1233–1240.
  • 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):1688–1698.
  • Greendale GA, Jackson NJ, Han W, et al.. Increase in C-reactive protein predicts increase in rate of bone mineral density loss: the study of women’s health across the nation. JBMR Plus. 2021;5(4):e10480.
  • Jackson RD, Donepudi S, Mysiw WJ. Epidemiology of fracture risk in the Women’s Health Initiative. Curr Osteoporos Rep. 2008;6(4):155–161.
  • Bailey RL, Sahni S, Chocano-Bedoya P, et al. Best practices for conducting observational research to assess the relation between nutrition and bone: an International Working Group Summary. Adv Nutr. 2019;10(3):391–409.
  • Varela A, Jolette J. Bone Toolbox: biomarkers, Imaging Tools, Biomechanics, and Histomorphometry. Toxicol Pathol. 2018;46(5):511–529.
  • Lacroix AZ, Beck TJ, Cauley JA, et al. Hip structural geometry and incidence of Hip fracture in postmenopausal women: what does it add to conventional bone mineral density? Osteoporos Int. 2010;21(6):919–929.
  • Cheung AM, Frame H, Ho M, Mackinnon ES, Brown JP. Bone strength and management of postmenopausal fracture risk with antiresorptive therapies: considerations for women’s health practice. Int J Womens Health. 2016;8:537–547.
  • Chen H, Zhou X, Fujita H, Onozuka M, Kubo KY. Age-related changes in trabecular and cortical bone microstructure. Int J Endocrinol. 2013;213234:1–9.
  • De Souza MJ, Strock NCA, Rogers CJ, et al. Rationale and study design of randomized controlled trial of dietary supplementation with prune (dried plums) on bone density, geometry, and estimated bone strength in postmenopausal women: the Prune study. Contemp Clin Trials Commun. 2022;28:100941.
  • De Souza MJ, Strock NCA, Williams NI, et al. Prunes preserve Hip bone mineral density in a 12-month randomized controlled trial in postmenopausal women: the Prune Study. Am J Clin Nutr. 2022;116(4):897–910.
  • Centers for Disease Control and Prevention (CDC). National Health and Nutrition Examination Survey (NHANES) 2017–2018 Procedure Manuals, National Center for Health Statistics. Rockville (MD): Department of Health and Human Services; 2017.
  • Yang YJ, Martin BR, Boushey CJ. Development and evaluation of a brief calcium assessment tool for adolescents. J Am Diet Assoc. 2010;110(1):111–115.
  • Kanis JA, McCloskey EV, Johansson H, Oden A, Ström O, Borgström F. Development and use of FRAX in osteoporosis. Osteoporos Int. 2010;21:407–413.
  • McCloskey EV, Oden A, Harvey NC, et al. A meta-analysis of trabecular bone score in fracture risk prediction and its relationship to FRAX. J Bone Miner Res. 2016;31(5):940–948.
  • Yoshikawa T, Turner CH, Peacock M, et al. Geometric structure of the femoral neck measured using dual-energy x-ray absorptiometry. J Bone Miner Res. 1994;9(7):1053–1064.
  • Beck TJ, Ruff CB, Warden KE, Scott WW, Rao GU. Predicting femoral neck strength from bone mineral data. A structural approach. Invest Radiol. 1990;25(1):6–18.
  • Morin S, Tsang JF, Leslie WD. Weight and body mass index predict bone mineral density and fractures in women aged 40 to 59 years. Osteoporos Int. 2009;20(3):363–370.
  • Gallagher JC. Effect of early menopause on bone mineral density and fractures. Menopause. 2007;14(3 Pt 2):567–571.
  • Harlow SD, Gass M, Hall JE, et al. Executive summary of the Stages of Reproductive Aging Workshop +10: addressing the unfinished agenda of staging reproductive aging. Climacteric. 2012;15(2):105–114.
  • Perry CD, Alekel DL, Ritland LM, et al. Centrally located body fat is related to inflammatory markers in healthy postmenopausal women. Menopause. 2008;15(4 Pt 1):619–627.
  • Ilesanmi-Oyelere BL, Schollum L, Kuhn-Sherlock B, et al. Inflammatory markers and bone health in postmenopausal women: a cross-sectional overview. Immun Ageing. 2019;16(1):15.
  • Cohen E, Margalit I, Shochat T, Goldberg E, Krause I. Markers of chronic inflammation in overweight and obese individuals and the role of gender: a cross-sectional study of a large cohort. J Inflamm Res. 2021;14:567–573.
  • 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):2495–2501.
  • Pasco JA, Kotowicz MA, Henry MJ, et al. High-sensitivity C-reactive protein and fracture risk in elderly women. JAMA. 2006;296(11):1353–1355.
  • 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):1088–1095.
  • Cauley JA, Barbour KE, Harrison SL, et al. Inflammatory markers and the risk of hip and vertebral fractures in men: the Osteoporotic Fractures in Men (MrOS). J Bone Miner Res. 2016;31(12):2129–2138.
  • 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):1167–1176.
  • 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):2057–2064.
  • 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):1263–1271.
  • Lee Y, Kim M, Choi K, et al. Relationship between inflammation biomarkers, antioxidant vitamins, and bone mineral density in patients with metabolic syndrome. Nutr Res Pract. 2011;5(2):150–156.
  • De Martinis M, Sirufo MM, Nocelli C, Fontanella L, Ginaldi L. Hyperhomocysteinemia is associated with inflammation, bone resorption, vitamin B12 and folate deficiency and MTHFR C677T polymorphism in postmenopausal women with decreased bone mineral density. Int J Environ Res Public Health. 2020;17(12):4260.
  • Khinda R, Valecha S, Kumar N, et al. Prevalence and predictors of osteoporosis and osteopenia in postmenopausal women of Punjab, India. Int J Environ Res Public Health. 2022;19(5):2999.
  • Khosla S, Peterson JM, Egan K, Jones JD, Riggs BL. Circulating cytokine levels in osteoporotic and normal women. J Clin Endocrinol Metab. 1994;79(3):707–711.
  • Al-Daghri NM, Yakout S, Al-Shehri E, Al-Fawaz H, Aljohani N, Al-Saleh Y. Inflammatory and bone turnover markers in relation to PTH and vitamin D status among Saudi postmenopausal women with and without osteoporosis. Int J Clin Exp Med. 2014;7(9):2812–2819.
  • Al-Daghri NM, Aziz I, Yakout S, et al. Inflammation as a contributing factor among postmenopausal Saudi women with osteoporosis. Medicine. 2017;96(4):e5780.
  • Murad R, Shezad Z, Ahmed S, Ashraf M, Qadir M, Rehman R. Serum tumour necrosis factor alpha in osteopenic and osteoporotic postmenopausal females: a cross-sectional study in Pakistan. J Pak Med Assoc. 2018;68(3):428–431.
  • Gunn CA, Weber JL, Kruger MC. Diet, weight, cytokines and bone health in postmenopausal women. J Nutr Health Aging. 2014;18(5):479–486.
  • Cervellati C, Bonaccorsi G, Bergamini CM, et al. Association between circulatory levels of adipokines and bone mineral density in postmenopausal women. Menopause. 2016;23(9):984–992.
  • Azizieh FY, Shehab D, Al Jarallah K, Mojiminiyi O, Gupta R, Raghupathy R. Circulatory pattern of cytokines, adipokines and bone markers in postmenopausal women with low BMD. J Inflamm Res. 2019;12:99–108.
  • Zhang Y, Huang X, Sun K, et al. The potential role of serum IGF-1 and leptin as biomarkers: towards screening for and diagnosing postmenopausal osteoporosis. J Inflamm Res. 2022;15:533–543.
  • Tworoger SS, Hankinson SE. Collection, processing, and storage of biological samples in epidemiologic studies: sex hormones, carotenoids, inflammatory markers, and proteomics as examples. Cancer Epidemiol Biomarkers Prev. 2006;15(9):1578–1581.
  • Burska A, Boissinot M, Ponchel F. Cytokines as biomarkers in rheumatoid arthritis. Mediators Inflamm. 2014;545493:1–24.
  • Azizieh F, Raghupathy R, Shehab D, Al-Jarallah K, Gupta R. Cytokine profiles in osteoporosis suggest a proresorptive bias. Menopause. 2017;24(9):1057–1064.
  • Azizieh FY, Al Jarallah K, Shehab D, Gupta R, Dingle K, Raghupathy R. Patterns of circulatory and peripheral blood mononuclear cytokines in rheumatoid arthritis. Rheumatol Int. 2017;37(10):1727–1734.
  • Dingle K, Azizieh F. Multivariate comparison of cytokine profiles for normal- and low-bone-density subjects. Diagnostics. 2019;9(4):134.
  • Pietschmann P, Mechtcheriakova D, Meshcheryakova A, Föger-Samwald U, Ellinger I. Immunology of osteoporosis: a mini-review. Gerontology. 2016;62(2):128–137.
  • Hlaing TT, Compston JE. Biochemical markers of bone turnover - uses and limitations. Ann Clin Biochem. 2014;51(Pt 2):189–202.
  • 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):329–333.
  • Bhupathiraju SN, Alekel DL, Stewart JW, et al. Relationship of circulating total homocysteine and C-reactive protein to trabecular bone in postmenopausal women. J Clin Densitom. 2007;10(4):395–403.
  • Nabipour I, Larijani B, Vahdat K, et al. Relationships among serum receptor of nuclear factor-kappaB ligand, osteoprotegerin, high-sensitivity C-reactive protein, and bone mineral density in postmenopausal women: osteoimmunity versus osteoinflammatory. Menopause. 2009;16(5):950–955.
  • Papadopoulos NG, Georganas K, Skoutellas V, Konstantellos E, Lyritis GP. Correlation of interleukin-6 serum levels with bone density in postmenopausal women. Clin Rheumatol. 1997;16(2):162–165.
  • Silva BC, Leslie WD, Resch H, et al. Trabecular bone score: a noninvasive analytical method based upon the DXA image. J Bone Miner Res. 2014;29(3):518–530.
  • Khosla S, Pacifici R. Estrogen deficiency, postmenopausal osteoporosis, and age-related bone loss. In: Marcus R, Feldman D, David WD, editors. Osteoporosis. 4th ed. San Diego: Academic Press; 2013:1113–1136.
  • Ridker PM, Hennekens CH, Rifai N, Buring JE, Manson JE. Hormone replacement therapy and increased plasma concentration of C-reactive protein. Circulation. 1999;100(7):713–716.
  • Pradhan AD, Manson JE, Rossouw JE, et al. Inflammatory biomarkers, hormone replacement therapy, and incident coronary heart disease: prospective analysis from the Women’s Health Initiative observational study. JAMA. 2002;288(8):980–987.
  • 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):1952–1958.
  • 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):277–282.
  • 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):2032–2042.
  • Zupan J, Komadina R, Marc J. The relationship between osteoclastogenic and anti-osteoclastogenic pro-inflammatory cytokines differs in human osteoporotic and osteoarthritic bone tissues. J Biomed Sci. 2012;19(1):28.
  • Seeman E. Age- and menopause-related bone loss compromise cortical and trabecular microstructure. J Gerontol a Biol Sci Med Sci. 2013;68(10):1218–1225.
  • Bjørnerem Å, Wang X, Bui M, et al. Menopause-related appendicular bone loss is mainly cortical and results in increased cortical porosity. J Bone Miner Res. 2018;33(4):598–605.
  • Chapurlat R, Bui M, Sornay‐Rendu E, et al. Deterioration of cortical and trabecular microstructure identifies women with osteopenia or normal bone mineral density at imminent and long‐term risk for fragility fracture: a prospective study. J Bone Miner Res. 2020;35(5):833–844.
  • Lauretani F, Bandinelli S, Russo CR, et al. Correlates of bone quality in older persons. Bone. 2006;39(4):915–921.
  • Zhu TY, Griffith JF, Qin L, et al. Alterations of bone density, microstructure, and strength of the distal radius in male patients with rheumatoid arthritis: a case-control study with HR-pQCT. J Bone Miner Res. 2014;29(9):2118–2129.
  • Hou JHC, He W, Yang M, Luo X, Li C. Obesity and bone health: a complex link. Front Cell Dev Biol. 2020;8:600181.
  • Fassio A, Idolazzi L, Rossini M, et al. The obesity paradox and osteoporosis. Eat Weight Disord. 2018;23(3):293–302.
  • Demirkol ME, Bilgin S, Kahveci G, et al. C-reactive protein-to-lymphocyte ratio is a reliable marker in patients with COVID-19 infection: the CLEAR COVID study. Cir Cir. 2022;90(5):596–601.
  • Demirkol ME, Aktas G, Bilgin S, et al. C-reactive protein to lymphocyte count ratio is a promising novel marker in hepatitis C infection: the clear hep-c study. Rev Assoc Med Bras. 2022;68(6):838–841.
  • Furman D, Campisi J, Verdin E, et al. Chronic inflammation in the etiology of disease across the life span. Nat Med. 2019;25(12):1822–1832.
  • Bilgin S, Kurtkulagi O, Atak Tel BM, et al. Does C-reactive protein to serum Albumin Ratio correlate with diabEtic nephropathy in patients with Type 2 dIabetes MEllitus? The CARE TIME study. Prim Care Diabetes. 2021;15(6):1071–1074.
  • Demirkol ME, Aktas G. C‐reactive protein to LymphocytE count ratio could be a reliable mArkeR of thyroiditis; the CLEAR‐T study. Precis Med Sci. 2022;11:31–34.
  • Weitzmann MN. Estrogen deficiency and bone loss: an inflammatory tale. J Clin Invest. 2006;116(5):1186–1194. doi:10.1172/JCI28550
  • Wu D, Cline-Smith A, Shashkova E, Perla A, Katyal A, Aurora R. T-cell mediated inflammation in postmenopausal osteoporosis. Front Immunol. 2021;12:687551.
  • Zupan J, Jeras M, Marc J. Osteoimmunology and the influence of pro-inflammatory cytokines on osteoclasts. Biochem Med. 2013;23(1):43–63.