Skip to main content
Top
Published in: BMC Geriatrics 1/2020

Open Access 01-12-2020 | Research article

Individual and joint trajectories of change in bone, lean mass and physical performance in older men

Authors: Peggy M. Cawthon, Neeta Parimi, Lisa Langsetmo, Jane A. Cauley, Kristine E. Ensrud, Steven R. Cummings, Nancy E. Lane, Andrew R. Hoffman, Jodi Lapidus, Thomas M. Gill, Charles E. McCulloch, Marcia L. Stefanick, Deborah M. Kado, Rebecca Drieling, Eric S. Orwoll

Published in: BMC Geriatrics | Issue 1/2020

Login to get access

Abstract

Background

Declines in bone, muscle and physical performance are associated with adverse health outcomes in older adults. However, few studies have described concurrent age-related patterns of change in these factors. The purpose of this study was to characterize change in four properties of muscle, physical performance, and bone in a prospective cohort study of older men.

Methods

Using repeated longitudinal data from up to four visits across 6.9 years from up to 4681 men (mean age at baseline 72.7 yrs. ±5.3) participating in the Osteoporotic Fractures in Men (MrOS) Study, we used group-based trajectory models (PROC TRAJ in SAS) to identify age-related patterns of change in four properties of muscle, physical performance, and bone: total hip bone mineral (BMD) density (g/m2) and appendicular lean mass/ht2 (kg/m2), by DXA; grip strength (kg), by hand dynamometry; and walking speed (m/s), by usual walking pace over 6 m. We also described joint trajectories in all pair-wise combinations of these measures. Mean posterior probabilities of placement in each trajectory (or joint membership in latent groups) were used to assess internal reliability of the model. The number of trajectories for each individual factor was limited to three, to ensure that the pair-wise determination of joint trajectories would yield a tractable number of groups as well as model fit considerations.

Results

The patterns of change identified were generally similar for all measures, with three district groups declining over time at roughly similar rates; joint trajectories revealed similar patterns with no cross-over or convergence between groups. Mean posterior probabilities for all trajectories were similar and consistently above 0.8 indicating reasonable model fit to the data.

Conclusions

Our description of trajectories of change with age in bone mineral density, grip strength, walking speed and appendicular lean mass found that groups identified by these methods appeared to have little crossover or convergence of change with age, even when considering joint trajectories of change in these factors.
Appendix
Available only for authorised users
Literature
1.
go back to reference Cooper R, Kuh D, Hardy R. Objectively measured physical capability levels and mortality: systematic review and meta-analysis. Bmj. 2010;341:c4467.CrossRef Cooper R, Kuh D, Hardy R. Objectively measured physical capability levels and mortality: systematic review and meta-analysis. Bmj. 2010;341:c4467.CrossRef
2.
go back to reference 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.CrossRef 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.CrossRef
3.
go back to reference Guralnik JM, Seeman TE, Tinetti ME, Nevitt MC, Berkman LF. Validation and use of performance measures of functioning in a non-disabled older population: MacArthur studies of successful aging. Aging (Milan, Italy). 1994;6(6):410–9. Guralnik JM, Seeman TE, Tinetti ME, Nevitt MC, Berkman LF. Validation and use of performance measures of functioning in a non-disabled older population: MacArthur studies of successful aging. Aging (Milan, Italy). 1994;6(6):410–9.
4.
go back to reference Visser M, Goodpaster BH, Kritchevsky SB, et al. Muscle mass, muscle strength, and muscle fat infiltration as predictors of incident mobility limitations in well-functioning older persons. J Gerontol A Biol Sci Med Sci. 2005;60(3):324–33.CrossRef Visser M, Goodpaster BH, Kritchevsky SB, et al. Muscle mass, muscle strength, and muscle fat infiltration as predictors of incident mobility limitations in well-functioning older persons. J Gerontol A Biol Sci Med Sci. 2005;60(3):324–33.CrossRef
5.
go back to reference Gill TM, Murphy TE, Barry LC, Allore HG. Risk factors for disability subtypes in older persons. J Am Geriatr Soc. 2009;57(10):1850–5.CrossRef Gill TM, Murphy TE, Barry LC, Allore HG. Risk factors for disability subtypes in older persons. J Am Geriatr Soc. 2009;57(10):1850–5.CrossRef
6.
go back to reference Tas U, Verhagen AP, Bierma-Zeinstra SM, et al. Incidence and risk factors of disability in the elderly: the Rotterdam study. Prev Med. 2007;44(3):272–8.CrossRef Tas U, Verhagen AP, Bierma-Zeinstra SM, et al. Incidence and risk factors of disability in the elderly: the Rotterdam study. Prev Med. 2007;44(3):272–8.CrossRef
7.
go back to reference Visser M, Deeg DJ, Lips P, Harris TB, Bouter LM. Skeletal muscle mass and muscle strength in relation to lower-extremity performance in older men and women. J Am Geriatr Soc. 2000;48(4):381–6.CrossRef Visser M, Deeg DJ, Lips P, Harris TB, Bouter LM. Skeletal muscle mass and muscle strength in relation to lower-extremity performance in older men and women. J Am Geriatr Soc. 2000;48(4):381–6.CrossRef
8.
go back to reference Chan BK, Marshall LM, Winters KM, Faulkner KA, Schwartz AV, Orwoll ES. Incident fall risk and physical activity and physical performance among older men: the osteoporotic fractures in men study. Am J Epidemiol. 2007;165(6):696–703.CrossRef Chan BK, Marshall LM, Winters KM, Faulkner KA, Schwartz AV, Orwoll ES. Incident fall risk and physical activity and physical performance among older men: the osteoporotic fractures in men study. Am J Epidemiol. 2007;165(6):696–703.CrossRef
9.
go back to reference Cawthon PM, Fullman RL, Marshall L, et al. Physical performance and risk of hip fractures in older men. J Bone Miner Res. 2008;23(7):1037–44.CrossRef Cawthon PM, Fullman RL, Marshall L, et al. Physical performance and risk of hip fractures in older men. J Bone Miner Res. 2008;23(7):1037–44.CrossRef
10.
go back to reference Leibson CL, Tosteson AN, Gabriel SE, Ransom JE, Melton LJ. Mortality, disability, and nursing home use for persons with and without hip fracture: a population-based study. J Am Geriatr Soc. 2002;50(10):1644–50.CrossRef Leibson CL, Tosteson AN, Gabriel SE, Ransom JE, Melton LJ. Mortality, disability, and nursing home use for persons with and without hip fracture: a population-based study. J Am Geriatr Soc. 2002;50(10):1644–50.CrossRef
11.
go back to reference Magaziner J, Hawkes W, Hebel JR, et al. Recovery from hip fracture in eight areas of function. J Gerontol A Biol Sci Med Sci. 2000;55(9):M498–507.CrossRef Magaziner J, Hawkes W, Hebel JR, et al. Recovery from hip fracture in eight areas of function. J Gerontol A Biol Sci Med Sci. 2000;55(9):M498–507.CrossRef
12.
go back to reference Marks R, Allegrante JP, Ronald MacKenzie C, Lane JM. Hip fractures among the elderly: causes, consequences and control. Ageing Res Rev. 2003;2(1):57–93.CrossRef Marks R, Allegrante JP, Ronald MacKenzie C, Lane JM. Hip fractures among the elderly: causes, consequences and control. Ageing Res Rev. 2003;2(1):57–93.CrossRef
13.
go back to reference Lang T, Streeper T, Cawthon P, Baldwin K, Taaffe DR, Harris TB. Sarcopenia: etiology, clinical consequences, intervention, and assessment. Osteoporos Int. 2010;21(4):543–59.CrossRef Lang T, Streeper T, Cawthon P, Baldwin K, Taaffe DR, Harris TB. Sarcopenia: etiology, clinical consequences, intervention, and assessment. Osteoporos Int. 2010;21(4):543–59.CrossRef
14.
go back to reference Cawthon PM, Ewing SK, Mackey DC, et al. Change in hip bone mineral density and risk of subsequent fractures in older men. J Bone Miner Res. 2012;27(10):2179–88.CrossRef Cawthon PM, Ewing SK, Mackey DC, et al. Change in hip bone mineral density and risk of subsequent fractures in older men. J Bone Miner Res. 2012;27(10):2179–88.CrossRef
15.
go back to reference Cawthon PM, Patel S, Ewing SK, et al. Bone loss at the hip and subsequent mortality in older men: the osteoporotic fractures in men (MrOS) study. JBMR plus. 2017;1(1):31–5.CrossRef Cawthon PM, Patel S, Ewing SK, et al. Bone loss at the hip and subsequent mortality in older men: the osteoporotic fractures in men (MrOS) study. JBMR plus. 2017;1(1):31–5.CrossRef
16.
go back to reference Barbour KE, Lui LY, McCulloch CE, et al. Trajectories of lower extremity physical performance: effects on fractures and mortality in older women. J Gerontol A Biol Sci Med Sci. 2016;71(12):1609–15.CrossRef Barbour KE, Lui LY, McCulloch CE, et al. Trajectories of lower extremity physical performance: effects on fractures and mortality in older women. J Gerontol A Biol Sci Med Sci. 2016;71(12):1609–15.CrossRef
17.
go back to reference White DK, Neogi T, Nevitt MC, et al. Trajectories of gait speed predict mortality in well-functioning older adults: the health, aging and body composition study. J Gerontol A Biol Sci Med Sci. 2013;68(4):456–64.CrossRef White DK, Neogi T, Nevitt MC, et al. Trajectories of gait speed predict mortality in well-functioning older adults: the health, aging and body composition study. J Gerontol A Biol Sci Med Sci. 2013;68(4):456–64.CrossRef
18.
go back to reference Barbour KE, Lui LY, McCulloch CE, Ensrud KE, Cawthon PM, Yaffe K, Barnes DE, Fredman L, Newman AB, Cummings SR, Cauley JA. Study of Osteoporotic Fractures. Trajectories of Lower Extremity Physical Performance: Effects on Fractures and Mortality in Older Women. J Gerontol A Biol Sci Med Sci. 2016;71(12):1609-15. Epub 2016 Apr 15. PubMed PMID: 27084313; PubMed Central PMCID: PMC5106858. Barbour KE, Lui LY, McCulloch CE, Ensrud KE, Cawthon PM, Yaffe K, Barnes DE, Fredman L, Newman AB, Cummings SR, Cauley JA. Study of Osteoporotic Fractures. Trajectories of Lower Extremity Physical Performance: Effects on Fractures and Mortality in Older Women. J Gerontol A Biol Sci Med Sci. 2016;71(12):1609-15. Epub 2016 Apr 15. PubMed PMID: 27084313; PubMed Central PMCID: PMC5106858.
19.
go back to reference Goodpaster BH, Park SW, Harris TB, et al. The loss of skeletal muscle strength, mass, and quality in older adults: the health, aging and body composition study. J Gerontol A Biol Sci Med Sci. 2006;61(10):1059–64.CrossRef Goodpaster BH, Park SW, Harris TB, et al. The loss of skeletal muscle strength, mass, and quality in older adults: the health, aging and body composition study. J Gerontol A Biol Sci Med Sci. 2006;61(10):1059–64.CrossRef
20.
go back to reference Karasik D, Kiel DP. Evidence for pleiotropic factors in genetics of the musculoskeletal system. Bone. 2010;46(5):1226–37.CrossRef Karasik D, Kiel DP. Evidence for pleiotropic factors in genetics of the musculoskeletal system. Bone. 2010;46(5):1226–37.CrossRef
21.
go back to reference Cruz-Jentoft AJ, Bahat G, Bauer J, Boirie Y, Bruyère O, Cederholm T, Cooper C, Landi F, Rolland Y, Sayer AA, Schneider SM, Sieber CC, Topinkova E, Vandewoude M, Visser M, Zamboni M. Writing Group for the European Working Group on Sarcopenia in Older People 2 (EWGSOP2), and the Extended Group for EWGSOP2. Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing. 2019;48(1):16-31. https://doi.org/10.1093/ageing/afy169. Erratum in: Age Ageing. 2019;48(4):601. PubMed PMID: 30312372; PubMed Central PMCID: PMC6322506. Cruz-Jentoft AJ, Bahat G, Bauer J, Boirie Y, Bruyère O, Cederholm T, Cooper C, Landi F, Rolland Y, Sayer AA, Schneider SM, Sieber CC, Topinkova E, Vandewoude M, Visser M, Zamboni M. Writing Group for the European Working Group on Sarcopenia in Older People 2 (EWGSOP2), and the Extended Group for EWGSOP2. Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing. 2019;48(1):16-31. https://​doi.​org/​10.​1093/​ageing/​afy169. Erratum in: Age Ageing. 2019;48(4):601. PubMed PMID: 30312372; PubMed Central PMCID: PMC6322506.
22.
go back to reference Fielding RA, Vellas B, Evans WJ, et al. Sarcopenia: an undiagnosed condition in older adults. Current consensus definition: prevalence, etiology, and consequences. International working group on sarcopenia. J Am Med Dir Assoc. 2011;12(4):249–56.CrossRef Fielding RA, Vellas B, Evans WJ, et al. Sarcopenia: an undiagnosed condition in older adults. Current consensus definition: prevalence, etiology, and consequences. International working group on sarcopenia. J Am Med Dir Assoc. 2011;12(4):249–56.CrossRef
23.
go back to reference Studenski SA, Peters KW, Alley DE, et al. The FNIH sarcopenia project: rationale, study description, conference recommendations, and final estimates. J Gerontol A Biol Sci Med Sci. 2014;69(5):547–58.CrossRef Studenski SA, Peters KW, Alley DE, et al. The FNIH sarcopenia project: rationale, study description, conference recommendations, and final estimates. J Gerontol A Biol Sci Med Sci. 2014;69(5):547–58.CrossRef
24.
go back to reference Studenski S, Perera S, Patel K, et al. Gait speed and survival in older adults. Jama. 2011;305(1):50–8.CrossRef Studenski S, Perera S, Patel K, et al. Gait speed and survival in older adults. Jama. 2011;305(1):50–8.CrossRef
25.
go back to reference Rantanen T, Guralnik JM, Foley D, et al. Midlife hand grip strength as a predictor of old age disability. Jama. 1999;281(6):558–60.CrossRef Rantanen T, Guralnik JM, Foley D, et al. Midlife hand grip strength as a predictor of old age disability. Jama. 1999;281(6):558–60.CrossRef
26.
go back to reference Baumgartner RN, Koehler KM, Gallagher D, et al. Epidemiology of sarcopenia among the elderly in New Mexico. Am J Epidemiol. 1998;147(8):755–63.CrossRef Baumgartner RN, Koehler KM, Gallagher D, et al. Epidemiology of sarcopenia among the elderly in New Mexico. Am J Epidemiol. 1998;147(8):755–63.CrossRef
27.
go back to reference 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.CrossRef 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.CrossRef
28.
go back to reference 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.CrossRef 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.CrossRef
29.
go back to reference Harkonen R, Harju R, Alaranta H. Accuracy of the Jamar dynamometer. J Hand Ther. 1993;6(4):259–62.CrossRef Harkonen R, Harju R, Alaranta H. Accuracy of the Jamar dynamometer. J Hand Ther. 1993;6(4):259–62.CrossRef
30.
go back to reference Washburn RA, Smith KW, Jette AM, Janney CA. The physical activity scale for the elderly (PASE): development and evaluation. J ClinEpidemiol. 1993;46:153–62. Washburn RA, Smith KW, Jette AM, Janney CA. The physical activity scale for the elderly (PASE): development and evaluation. J ClinEpidemiol. 1993;46:153–62.
31.
go back to reference Jones BL, Nagin DS, Roeder K. A SAS Procedure Based on Mixture Models for Estimating Developmental Trajectories 1177/0049124101029003005. Sociol Method Res. 2001;29(3):374–93.CrossRef Jones BL, Nagin DS, Roeder K. A SAS Procedure Based on Mixture Models for Estimating Developmental Trajectories 1177/0049124101029003005. Sociol Method Res. 2001;29(3):374–93.CrossRef
32.
go back to reference Nagin DS, Odgers CL. Group-based trajectory modeling in clinical research. Annu Rev Clin Psychol. 2010;6:109–38.CrossRef Nagin DS, Odgers CL. Group-based trajectory modeling in clinical research. Annu Rev Clin Psychol. 2010;6:109–38.CrossRef
33.
go back to reference Paul HCE, Marx BD. Flexible smoothing with $B$-splines and penalties. Stat Sci. 1996;11(2):89–102.CrossRef Paul HCE, Marx BD. Flexible smoothing with $B$-splines and penalties. Stat Sci. 1996;11(2):89–102.CrossRef
34.
go back to reference Kallman DA, Plato CC, Tobin JD. The role of muscle loss in the age-related decline of grip strength: cross-sectional and longitudinal perspectives. J Gerontol. 1990;45(3):M82–8.CrossRef Kallman DA, Plato CC, Tobin JD. The role of muscle loss in the age-related decline of grip strength: cross-sectional and longitudinal perspectives. J Gerontol. 1990;45(3):M82–8.CrossRef
35.
go back to reference Rantanen T, Masaki K, Foley D, Izmirlian G, White L, Guralnik JM. Grip strength changes over 27 yr in Japanese-American men. J Appl Physiol. 1998;85(6):2047–53.CrossRef Rantanen T, Masaki K, Foley D, Izmirlian G, White L, Guralnik JM. Grip strength changes over 27 yr in Japanese-American men. J Appl Physiol. 1998;85(6):2047–53.CrossRef
36.
go back to reference Gill TM, Gahbauer EA, Han L, Allore HG. Trajectories of disability in the last year of life. N Engl J Med. 2010;362(13):1173–80.CrossRef Gill TM, Gahbauer EA, Han L, Allore HG. Trajectories of disability in the last year of life. N Engl J Med. 2010;362(13):1173–80.CrossRef
37.
go back to reference Clark BC, Tavoian D, Goodpaster BH, Cawthon PM, Hansen RD, Manini TM. Comment on: "pitfalls in the measurement of muscle mass: a need for a reference standard" by Buckinx et al. J Cachexia Sarcopenia Muscle. 2018;9(7):1269–71.CrossRef Clark BC, Tavoian D, Goodpaster BH, Cawthon PM, Hansen RD, Manini TM. Comment on: "pitfalls in the measurement of muscle mass: a need for a reference standard" by Buckinx et al. J Cachexia Sarcopenia Muscle. 2018;9(7):1269–71.CrossRef
38.
go back to reference Buckinx F, Landi F, Cesari M, Fielding RA, Visser M, Engelke K, Maggi S, Dennison E, Al-Daghri NM, Allepaerts S, Bauer J, Bautmans I, Brandi ML, Bruyère O, Cederholm T, Cerreta F, Cherubini A, Cooper C, Cruz-Jentoft A, McCloskey E, Dawson-Hughes B, Kaufman JM, Laslop A, Petermans J, Reginster JY, Rizzoli R, Robinson S, Rolland Y, Rueda R, Vellas B, Kanis JA. Pitfalls in the measurement of muscle mass: a need for a reference standard. J Cachexia Sarcopenia Muscle. 2018;9(2):269-78. https://doi.org/10.1002/jcsm.12268. Epub 2018 Jan 19. PubMed PMID: 29349935; PubMed Central PMCID: PMC5879987. Buckinx F, Landi F, Cesari M, Fielding RA, Visser M, Engelke K, Maggi S, Dennison E, Al-Daghri NM, Allepaerts S, Bauer J, Bautmans I, Brandi ML, Bruyère O, Cederholm T, Cerreta F, Cherubini A, Cooper C, Cruz-Jentoft A, McCloskey E, Dawson-Hughes B, Kaufman JM, Laslop A, Petermans J, Reginster JY, Rizzoli R, Robinson S, Rolland Y, Rueda R, Vellas B, Kanis JA. Pitfalls in the measurement of muscle mass: a need for a reference standard. J Cachexia Sarcopenia Muscle. 2018;9(2):269-78. https://​doi.​org/​10.​1002/​jcsm.​12268. Epub 2018 Jan 19. PubMed PMID: 29349935; PubMed Central PMCID: PMC5879987.
39.
go back to reference Cawthon PM, Orwoll ES, Peters KE, et al. Strong relation between muscle mass determined by D3-creatine dilution, physical performance, and incidence of falls and mobility limitations in a prospective cohort of older men. J Gerontol A Biol Sci Med Sci. 2019;74(6):844–52.CrossRef Cawthon PM, Orwoll ES, Peters KE, et al. Strong relation between muscle mass determined by D3-creatine dilution, physical performance, and incidence of falls and mobility limitations in a prospective cohort of older men. J Gerontol A Biol Sci Med Sci. 2019;74(6):844–52.CrossRef
40.
go back to reference Duchowny KA, Peters KE, Cummings SR, et al. Association of change in muscle mass assessed by D3 -creatine dilution with changes in grip strength and walking speed. J Cachexia Sarcopenia Muscle. 2020;11(1):55–61.CrossRef Duchowny KA, Peters KE, Cummings SR, et al. Association of change in muscle mass assessed by D3 -creatine dilution with changes in grip strength and walking speed. J Cachexia Sarcopenia Muscle. 2020;11(1):55–61.CrossRef
Metadata
Title
Individual and joint trajectories of change in bone, lean mass and physical performance in older men
Authors
Peggy M. Cawthon
Neeta Parimi
Lisa Langsetmo
Jane A. Cauley
Kristine E. Ensrud
Steven R. Cummings
Nancy E. Lane
Andrew R. Hoffman
Jodi Lapidus
Thomas M. Gill
Charles E. McCulloch
Marcia L. Stefanick
Deborah M. Kado
Rebecca Drieling
Eric S. Orwoll
Publication date
01-12-2020
Publisher
BioMed Central
Published in
BMC Geriatrics / Issue 1/2020
Electronic ISSN: 1471-2318
DOI
https://doi.org/10.1186/s12877-020-01560-5

Other articles of this Issue 1/2020

BMC Geriatrics 1/2020 Go to the issue