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Lower Lean Mass Measured by Dual-Energy X-ray Absorptiometry (DXA) is Not Associated with Increased Risk of Hip Fracture in Women: The Framingham Osteoporosis Study

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Abstract

Although muscle mass influences strength in older adults, it is unclear whether low lean mass measured by dual-energy X-ray absorptiometry (DXA) is an independent risk factor for hip fracture. Our objective was to determine the association between DXA lean mass and incident hip fracture risk among 1978 women aged 50 years and older participating in the Framingham Study Original and Offspring cohorts. Leg and total body lean mass (kg) were assessed from whole-body DXA scans collected in 1992–2001. Hip fracture follow-up extended from DXA assessment to the occurrence of fracture, death, drop-out, or end of follow-up in 2007. Cox proportional hazards regression was used to calculate hazard ratios (HR) and 95% confidence intervals (CI) estimating the relative risk of hip fracture associated with a 1-kg increase in baseline lean mass. Mean age was 66 years (range 50–93). Over a median of 8 years of follow-up, 99 hip fractures occurred. In models adjusted for age, height, study cohort, and percent total body fat, neither leg (HR 1.11; 95% CI 0.94, 1.31) nor total body (HR 1.06; 95% CI 0.99, 1.13) lean mass were associated with hip fracture. After further adjustment for femoral neck bone mineral density, leg lean mass results were similar (HR 1.10; 95% CI 0.93, 1.30). In contrast, 1 kg greater total body lean mass was associated with 9% higher hip fracture risk (HR 1.09; 95% CI 1.02, 1.18). Our findings suggest that in women, lower lean mass measured by DXA is not associated with increased risk of hip fracture.

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References

  1. Johnell O, Kanis JA, Oden A, Johansson H, De Laet C, Delmas P, Eisman JA, Fujiwara S, Kroger H, Mellstrom D, Meunier PJ, Melton LJ, O’Neill T, Pols H, Reeve J, Silman A, Tenenhouse A (2005) Predictive value of BMD for hip and other fractures. J Bone Miner Res 20:1185–1194

    Article  PubMed  Google Scholar 

  2. Nguyen ND, Eisman JA, Center JR, Nguyen TV (2007) Risk factors for fracture in nonosteoporotic men and women. J Clin Endocrinol Metab 92:955–962

    Article  PubMed  CAS  Google Scholar 

  3. Wainwright SA, Marshall LM, Ensrud KE, Cauley JA, Black DM, Hillier TA, Hochberg MC, Vogt MT, Orwoll ES, Study of Osteoporotic Fractures Research Group (2005) Hip fracture in women without osteoporosis. J Clin Endocrinol Metab 90:2787–2793

    Article  PubMed  CAS  Google Scholar 

  4. Cummings SR, Nevitt MC, Browner WS, Stone K, Fox KM, Ensrud KE, Cauley J, Black D, Vogt TM (1995) Risk factors for hip fracture in white women. Study of osteoporotic fractures research group. N Engl J Med 332:767–773

    Article  PubMed  CAS  Google Scholar 

  5. Cauley JA, Cawthon PM, Peters KE, Cummings SR, Ensrud KE, Bauer DC, Taylor BC, Shikany JM, Hoffman AR, Lane NE, Kado DM, Stefanick ML, Orwoll ES, Osteoporotic Fractures in Men Study Research Group (2016) Risk factors for hip fracture in older men: the osteoporotic fractures in men study (MrOS). J Bone Miner Res 31:1810–1819

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  6. Proctor DN, Melton LJ, Khosla S, Crowson CS, O’Connor MK, Riggs BL (2000) Relative influence of physical activity, muscle mass and strength on bone density. Osteoporos Int 11:944–952

    Article  PubMed  CAS  Google Scholar 

  7. Khosla S, Atkinson EJ, Riggs BL, Melton LJ (1996) Relationship between body composition and bone mass in women. J Bone Miner Res 11:857–863

    Article  PubMed  CAS  Google Scholar 

  8. Tinetti ME, Doucette JT, Claus E, Marottoli R (1995) Risk factors for serious injury during falls by older persons in the community. J Am Geriatr Soc 43:1214–1221

    Article  PubMed  CAS  Google Scholar 

  9. Chen Z, Wang Z, Lohman T, Heymsfield SB, Outwater E, Nicholas JS, Bassford T, LaCroix A, Sherrill D, Punyanitya M, Wu G, Going S (2007) Dual-energy X-ray absorptiometry is a valid tool for assessing skeletal muscle mass in older women. J Nutr 137:2775–2780

    Article  PubMed  CAS  Google Scholar 

  10. Cawthon PM (2015) Assessment of Lean Mass and Physical Performance in Sarcopenia. J Clin Densitom 18:467–471

    Article  PubMed  Google Scholar 

  11. Fiatarone MA, O’Neill EF, Ryan ND, Clements KM, Solares GR, Nelson ME, Roberts SB, Kehayias JJ, Lipsitz LA, Evans WJ (1994) Exercise training and nutritional supplementation for physical frailty in very elderly people. N Engl J Med 330:1769–1775

    Article  PubMed  CAS  Google Scholar 

  12. Kukuljan S, Nowson CA, Sanders K, Daly RM (2009) Effects of resistance exercise and fortified milk on skeletal muscle mass, muscle size, and functional performance in middle-aged and older men: an 18-mo randomized controlled trial. J Appl Physiol 107:1864–1873

    Article  PubMed  CAS  Google Scholar 

  13. Verdijk LB, Jonkers RA, Gleeson BG, Beelen M, Meijer K, Savelberg HH, Wodzig WK, Dendale P, van Loon LJ (2009) Protein supplementation before and after exercise does not further augment skeletal muscle hypertrophy after resistance training in elderly men. Am J Clin Nutr 89:608–616

    Article  PubMed  CAS  Google Scholar 

  14. Visser M, Harris TB, Fox KM, Hawkes W, Hebel JR, Yahiro JY, Michael R, Zimmerman SI, Magaziner J (2000) Change in muscle mass and muscle strength after a hip fracture: relationship to mobility recovery. J Gerontol A 55:M434–M440

    Article  CAS  Google Scholar 

  15. Fox KM, Magaziner J, Hawkes WG, Yu-Yahiro J, Hebel JR, Zimmerman SI, Holder L, Michael R (2000) Loss of bone density and lean body mass after hip fracture. Osteoporos Int 11:31–35

    Article  PubMed  CAS  Google Scholar 

  16. Wehren LE, Hawkes WG, Hebel JR, Orwig DL, Magaziner J (2005) Bone mineral density, soft tissue body composition, strength, and functioning after hip fracture. J Gerontol A 60:80–84

    Article  Google Scholar 

  17. Schott AM, Cormier C, Hans D, Favier F, Hausherr E, Dargent-Molina P, Delmas PD, Ribot C, Sebert JL, Breart G, Meunier PJ (1998) How hip and whole-body bone mineral density predict hip fracture in elderly women: the EPIDOS Prospective Study. Osteoporos Int 8:247–254

    Article  PubMed  CAS  Google Scholar 

  18. Malkov S, Cawthon PM, Peters KW, Cauley JA, Murphy RA, Visser M, Wilson JP, Harris T, Satterfield S, Cummings S, Shepherd JA, Health ABCS. (2015) Hip fractures risk in older men and women associated with DXA-derived measures of thigh subcutaneous fat thickness, cross-sectional muscle area, and muscle density. J Bone Miner Res 30:1414–1421

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  19. Cawthon PM, Blackwell TL, Cauley J, Kado DM, Barrett-Connor E, Lee CG, Hoffman AR, Nevitt M, Stefanick ML, Lane NE, Ensrud KE, Cummings SR, Orwoll ES (2015) Evaluation of the usefulness of consensus definitions of Sarcopenia in older men: results from the observational osteoporotic fractures in men cohort study. J Am Geriatr Soc 63:2247–2259

    Article  PubMed  PubMed Central  Google Scholar 

  20. Zaslavsky O, Li W, Going S, Datta M, Snetselaar L, Zelber-Sagi S (2016) Association between body composition and hip fractures in older women with physical frailty. Geriatr Gerontol Int. https://doi.org/10.1111/ggi.12798

    Article  PubMed  PubMed Central  Google Scholar 

  21. Dawber TR, Meadors GF, Moore FEJ (1951) Epidemiological approaches to heart disease: the Framingham Study. Am J Public Health 41:279–286

    Article  CAS  Google Scholar 

  22. Kannel WB, Feinleib M, McNamara PM, Garrison RJ, Castelli WP (1979) An investigation of coronary heart disease in families. The Framingham offspring study. Am J Epidemiol 110:281–290

    Article  PubMed  CAS  Google Scholar 

  23. Visser M, Harris TB, Langlois J, Hannan MT, Roubenoff R, Felson DT, Wilson PW, Kiel DP (1998) Body fat and skeletal muscle mass in relation to physical disability in very old men and women of the Framingham Heart Study. J Gerontol A 53:M214–M221

    Article  CAS  Google Scholar 

  24. Kiel DP, Felson DT, Anderson JJ, Wilson PW, Moskowitz MA (1987) Hip fracture and the use of estrogens in postmenopausal women. The Framingham Study. N Engl J Med 317:1169–1174

    Article  PubMed  CAS  Google Scholar 

  25. Nevitt MC, Cummings SR, Browner WS, Seeley DG, Cauley JA, Vogt TM, Black DM (1992) The accuracy of self-report of fractures in elderly women: evidence from a prospective study. Am J Epidemiol 135:490–499

    Article  PubMed  CAS  Google Scholar 

  26. Schuit AJ, Schouten EG, Westerterp KR, Saris WH (1997) Validity of the Physical Activity Scale for the Elderly (PASE): according to energy expenditure assessed by the doubly labeled water method. J Clin Epidemiol 50:541–546

    Article  PubMed  CAS  Google Scholar 

  27. Graafmans WC, Ooms ME, Hofstee HM, Bezemer PD, Bouter LM, Lips P (1996) Falls in the elderly: a prospective study of risk factors and risk profiles. Am J Epidemiol 143:1129–1136

    Article  PubMed  CAS  Google Scholar 

  28. Tinetti ME, Speechley M, Ginter SF (1988) Risk factors for falls among elderly persons living in the community. N Engl J Med 319:1701–1707

    Article  PubMed  CAS  Google Scholar 

  29. O’Loughlin JL, Robitaille Y, Boivin JF, Suissa S (1993) Incidence of and risk factors for falls and injurious falls among the community-dwelling elderly. Am J Epidemiol 137:342–354

    Article  PubMed  Google Scholar 

  30. Moayyeri A, Besson H, Luben RN, Wareham NJ, Khaw KT (2010) The association between physical activity in different domains of life and risk of osteoporotic fractures. Bone 47:693–700

    Article  PubMed  Google Scholar 

  31. Hannan MT, Felson DT, Dawson-Hughes B, Tucker KL, Cupples LA, Wilson PW, Kiel DP (2000) Risk factors for longitudinal bone loss in elderly men and women: the Framingham Osteoporosis Study. J Bone Miner Res 15:710–720

    Article  PubMed  CAS  Google Scholar 

  32. Cupples LA, Gagnon DR, Ramaswamy R, D’Agostino RB (1995) Age-adjusted survival curves with application in the Framingham Study. Stat Med 14:1731–1744

    Article  PubMed  CAS  Google Scholar 

  33. Rubin D (1987) Multiple imputation for non response in surveys. Wiley, New York

    Book  Google Scholar 

  34. Rubin DB (1996) Multiple imputation after 18+ years. J Am Stat Assoc 91:473–489

    Article  Google Scholar 

  35. Kohl M, Plischke M, Leffondre K, Heinze G (2015) PSHREG: a SAS macro for proportional and nonproportional subdistribution hazards regression. Comput Methods Progr Biomed 118:218–233

    Article  Google Scholar 

  36. Fine JP, Gray RJ (1999) A proportional hazards model for the subdistribution of a competing risk. J Am Stat Assoc 94:496–509

    Article  Google Scholar 

  37. Nielson CM, Srikanth P, Orwoll ES (2012) Obesity and fracture in men and women: an epidemiologic perspective. J Bone Miner Res 27:1–10

    Article  PubMed  Google Scholar 

  38. Manini TM, Clark BC (2012) Dynapenia and aging: an update. J Gerontol A 67:28–40

    Article  Google Scholar 

  39. Goodpaster BH, Park SW, Harris TB, Kritchevsky SB, Nevitt M, Schwartz AV, Simonsick EM, Tylavsky FA, Visser M, Newman AB (2006) The loss of skeletal muscle strength, mass, and quality in older adults: the health, aging and body composition study. J Gerontol A 61:1059–1064

    Article  Google Scholar 

  40. Vandervoort AA (2002) Aging of the human neuromuscular system. Muscle Nerve 25:17–25

    Article  PubMed  CAS  Google Scholar 

  41. Goodpaster BH, Carlson CL, Visser M, Kelley DE, Scherzinger A, Harris TB, Stamm E, Newman AB (2001) Attenuation of skeletal muscle and strength in the elderly: the health ABC study. J Appl Physiol (1985) 90:2157–2165

    Article  CAS  Google Scholar 

  42. Lang T, Cauley JA, Tylavsky F, Bauer D, Cummings S, Harris TB (2010) Computed tomographic measurements of thigh muscle cross-sectional area and attenuation coefficient predict hip fracture: the health, aging, and body composition study. J Bone Miner Res 25:513–519

    Article  PubMed  Google Scholar 

  43. Washburn RA, Smith KW, Jette AM, Janney CA (1993) The Physical Activity Scale for the Elderly (PASE): development and evaluation. J Clin Epidemiol 46:153–162

    Article  PubMed  CAS  Google Scholar 

  44. Prince SA, Adamo KB, Hamel ME, Hardt J, Connor Gorber S, Tremblay M (2008) A comparison of direct versus self-report measures for assessing physical activity in adults: a systematic review. Int J Behav Nutr Phys Act 5:56

    Article  PubMed  PubMed Central  Google Scholar 

  45. Washburn RA, Ficker JL (1999) Physical Activity Scale for the Elderly (PASE): the relationship with activity measured by a portable accelerometer. J Sports Med Phys Fit 39:336–340

    CAS  Google Scholar 

  46. Bernardi M, Rosponi A, Castellano V, Rodio A, Traballesi M, Delussu AS, Marchetti M (2004) Determinants of sit-to-stand capability in the motor impaired elderly. J Electromyogr Kinesiol 14:401–410

    Article  PubMed  CAS  Google Scholar 

  47. Bohannon RW, Magasi SR, Bubela DJ, Wang YC, Gershon RC (2012) Grip and knee extension muscle strength reflect a common construct among adults. Muscle Nerve 46:555–558

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

Research reported in this publication was supported by the National Institute of Arthritis and Musculoskeletal and Skin Diseases and the National Institute on Aging of the National Institutes of Health under award number R01AR/AG41398 and the National Heart, Lung and Blood Institute’s Framingham Heart Study (Contract No. HHSN268201500001I). The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

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Authors and Affiliations

  1. Institute for Aging Research, Hebrew SeniorLife, 1200 Centre Street, Boston, MA, 02131, USA

    Robert R. McLean, Douglas P. Kiel, Sarah D. Berry, Kerry E. Broe, Xiaochun Zhang & Marian T. Hannan

  2. Department of Medicine, Beth Israel Deaconess Medical Center, Boston, MA, USA

    Robert R. McLean, Douglas P. Kiel, Sarah D. Berry & Marian T. Hannan

  3. Harvard Medical School, Boston, MA, USA

    Robert R. McLean, Douglas P. Kiel, Sarah D. Berry & Marian T. Hannan

  4. Biostatistics Department, Boston University School of Public Health, Boston, MA, USA

    L. Adrienne Cupples

  5. The National Heart Lung and Blood Institute’s Framingham Heart Study, Framingham, MA, USA

    L. Adrienne Cupples

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  1. Robert R. McLean
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Contributions

DPK is the guarantor. DPK, LAC, and MTH designed the study. RRM prepared the first draft of the paper. RRM, DPK, SDB, KEB, and MTH contributed to the data collection. RRM, KEB and XZ were responsible for statistical analysis of the data. All authors revised the paper critically for intellectual content and approved the final version. All authors agree to be accountable for the work and to ensure that any questions relating to the accuracy and integrity of the paper are investigated and properly resolved.

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Correspondence to Douglas P. Kiel.

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Conflict of interest

Douglas P. Kiel has received grants from Eli Lilly, Amgen, Merck Sharp and Dohme, and has served on scientific advisory boards for Eli Lilly, Amgen, Novartis, and Merck Sharp and Dohme. Sarah D. Berry has received grant funding from Amgen. Robert R. McLean, Kerry E. Broe, Xiaochun Zhang, L. Adrienne Cupples, and Marian T. Hannan declare that they have no conflict of interest.

Human and Animal Rights and Informed Consent

This study was approved by the institutional review board at Hebrew SeniorLife and written informed consent was obtained for all participants included in the study.

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McLean, R.R., Kiel, D.P., Berry, S.D. et al. Lower Lean Mass Measured by Dual-Energy X-ray Absorptiometry (DXA) is Not Associated with Increased Risk of Hip Fracture in Women: The Framingham Osteoporosis Study. Calcif Tissue Int 103, 16–23 (2018). https://doi.org/10.1007/s00223-017-0384-y

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