Top

Published in:

01-10-2013 | Original Article

Diagnostic measures for sarcopenia and bone mineral density

Authors: A. Y. Bijlsma, M. C. G. Meskers, M. Molendijk, R. G. J. Westendorp, S. Sipilä, L. Stenroth, E. Sillanpää, J. S. McPhee, D. A. Jones, M. Narici, H. Gapeyeva, M. Pääsuke, E. Seppet, T. Voit, Y. Barnouin, J. Y. Hogrel, G. Butler-Browne, A. B. Maier

Published in: Osteoporosis International | Issue 10/2013

Abstract

Summary

Currently used diagnostic measures for sarcopenia utilize different measures of muscle mass, muscle strength, and physical performance. These diagnostic measures associate differently to bone mineral density (BMD), as an example of muscle-related clinical outcome. These differences should be taken into account when studying sarcopenia.

Introduction

Diagnostic measures for sarcopenia utilize different measures of muscle mass, muscle strength, and physical performance. To understand differences between these measures, we determined the association with respect to whole body BMD, as an example of muscle-related clinical outcome.

Methods

In the European cross-sectional study MYOAGE, 178 young (18–30 years) and 274 healthy old participants (69–81 years) were recruited. Body composition and BMD were evaluated using dual-energy X-ray densitometry. Diagnostic measures for sarcopenia were composed of lean mass as percentage of body mass, appendicular lean mass (ALM) as percentage of body mass, ALM divided by height squared (ALM/height²), knee extension torque, grip strength, walking speed, and Timed Up and Go test (TUG). Linear regression models were stratified for sex and age and adjusted for age and country, and body composition in separate models.

Results

Lean mass and ALM/height² were positively associated with BMD (P < 0.001). Significance remained in all sex and age subgroups after further adjustment for fat mass, except in old women. Lean mass percentage and ALM percentage were inversely associated with BMD in old women (P < 0.001). These inverse associations disappeared after adjustment for body mass. Knee extension torque and handgrip strength were positively associated with BMD in all subgroups (P < 0.01), except in old women. Walking speed and TUG were not related to BMD.

Conclusions

The associations between diagnostic measures of sarcopenia and BMD as an example of muscle-related outcome vary widely. Differences between diagnostic measures should be taken into account when studying sarcopenia.

Buford TW, Anton SD, Judge AR, Marzetti E, Wohlgemuth SE, Carter CS, Leeuwenburgh C, Pahor M, Manini TM (2010) Models of accelerated sarcopenia: critical pieces for solving the puzzle of age-related muscle atrophy. Ageing Res Rev 9:369–383PubMedCrossRef

Rosenberg IH (1997) Sarcopenia: origins and clinical relevance. J Nutr 127:990S–991SPubMed

Cruz-Jentoft AJ, Baeyens JP, Bauer JM, Boirie Y, Cederholm T, Landi F, Martin FC, Michel JP, Rolland Y, Schneider SM, Topinkova E, Vandewoude M, Zamboni M (2010) Sarcopenia: European consensus on definition and diagnosis: report of the European Working Group on Sarcopenia in Older People. Age Ageing 39:412–423PubMedCrossRef

Fielding RA, Vellas B, Evans WJ, Bhasin S, Morley JE, Newman AB, van Abellan KG, Andrieu S, Bauer J, Breuille D, Cederholm T, Chandler J, De MC, Donini L, Harris T, Kannt A, Keime GF, Onder G, Papanicolaou D, Rolland Y, Rooks D, Sieber C, Souhami E, Verlaan S, Zamboni M (2011) Sarcopenia: an undiagnosed condition in older adults. Current consensus definition: prevalence, etiology, and consequences. International working group on sarcopenia. J Am Med Dir Assoc 12:249–256PubMedCrossRef

Baumgartner RN, Koehler KM, Gallagher D, Romero L, Heymsfield SB, Ross RR, Garry PJ, Lindeman RD (1998) Epidemiology of sarcopenia among the elderly in New Mexico. Am J Epidemiol 147:755–763PubMedCrossRef

Delmonico MJ, Harris TB, Lee JS, Visser M, Nevitt M, Kritchevsky SB, Tylavsky FA, Newman AB (2007) Alternative definitions of sarcopenia, lower extremity performance, and functional impairment with aging in older men and women. J Am Geriatr Soc 55:769–774PubMedCrossRef

Estrada M, Kleppinger A, Judge JO, Walsh SJ, Kuchel GA (2007) Functional impact of relative versus absolute sarcopenia in healthy older women. J Am Geriatr Soc 55:1712–1719PubMedCrossRef

Bijlsma AY, Meskers CG, Ling CH, Narici M, Kurrle SE, Cameron ID, Westendorp RG, Maier AB (2012). Defining sarcopenia: the impact of different diagnostic criteria on the prevalence of sarcopenia in a large middle aged cohort. Age (Dordr)

Kalyani RR, Metter EJ, Ramachandran R, Chia CW, Saudek CD, Ferrucci L (2012) Glucose and insulin measurements from the oral glucose tolerance test and relationship to muscle mass. J Gerontol A Biol Sci Med Sci 67:74–81PubMedCrossRef

10.

Bijlsma A.Y., Meskers CG, van Heemst D., Westendorp RG, Craen AJM, Maier AB (2012) Definitions of sarcopenia relate differently to insulin resistance. Submitted

11.

Morgan DJ, Bray KM (1994) Lean body mass as a predictor of drug dosage. Implications for drug therapy. Clin Pharmacokinet 26:292–307PubMedCrossRef

12.

Englesbe MJ, Patel SP, He K, Lynch RJ, Schaubel DE, Harbaugh C, Holcombe SA, Wang SC, Segev DL, Sonnenday CJ (2010) Sarcopenia and mortality after liver transplantation. J Am Coll Surg 211:271–278PubMedCrossRef

13.

van Vledder MG, Levolger S, Ayez N, Verhoef C, Tran TC, Ijzermans JN (2012) Body composition and outcome in patients undergoing resection of colorectal liver metastases. Br J Surg 99:550–557PubMedCrossRef

14.

Cheng Q, Zhu YX, Zhang MX, Li LH, Du PY, Zhu MH (2012) Age and sex effects on the association between body composition and bone mineral density in healthy Chinese men and women. Menopause 19:448–455PubMedCrossRef

15.

Park JH, Song YM, Sung J, Lee K, Kim YS, Kim T, Cho SI (2012) The association between fat and lean mass and bone mineral density: the Healthy Twin Study. Bone 50:1006–1011PubMedCrossRef

16.

Verschueren S, Gielen E, O'Neill TW, Pye SR, Adams JE, Ward KA, Wu FC, Szulc P, Laurent M, Claessens F, Vanderschueren D, Boonen S (2012) Sarcopenia and its relationship with bone mineral density in middle-aged and elderly European men. Osteoporos Int

17.

Rochefort GY, Pallu S, Benhamou CL (2010) Osteocyte: the unrecognized side of bone tissue. Osteoporos Int 21:1457–1469PubMedCrossRef

18.

Lima RM, Bezerra LM, Rabelo HT, Silva MA, Silva AJ, Bottaro M, de Oliveira RJ (2009) Fat-free mass, strength, and sarcopenia are related to bone mineral density in older women. J Clin Densitom 12:35–41PubMedCrossRef

19.

Marin RV, Pedrosa MA, Moreira-Pfrimer LD, Matsudo SM, Lazaretti-Castro M (2010) Association between lean mass and handgrip strength with bone mineral density in physically active postmenopausal women. J Clin Densitom 13:96–101PubMedCrossRef

20.

Lindsey C, Brownbill RA, Bohannon RA, Ilich JZ (2005) Association of physical performance measures with bone mineral density in postmenopausal women. Arch Phys Med Rehabil 86:1102–1107PubMedCrossRef

21.

Palombaro KM, Hack LM, Mangione KK, Barr AE, Newton RA, Magri F, Speziale T (2009) Gait variability detects women in early postmenopause with low bone mineral density. Phys Ther 89:1315–1326PubMedCrossRef

22.

Faulkner KG, Roberts LA, McClung MR (1996) Discrepancies in normative data between Lunar and Hologic DXA systems. Osteoporos Int 6:432–436PubMedCrossRef

23.

Janssen I, Heymsfield SB, Ross R (2002) Low relative skeletal muscle mass (sarcopenia) in older persons is associated with functional impairment and physical disability. J Am Geriatr Soc 50:889–896PubMedCrossRef

24.

Reid IR (2010) Fat and bone. Arch Biochem Biophys 503:20–27PubMedCrossRef

25.

Sternfeld B, Ngo L, Satariano WA, Tager IB (2002) Associations of body composition with physical performance and self-reported functional limitation in elderly men and women. Am J Epidemiol 156:110–121PubMedCrossRef

26.

Lauretani F, Russo CR, Bandinelli S, Bartali B, Cavazzini C, Di IA, Corsi AM, Rantanen T, Guralnik JM, Ferrucci L (2003) Age-associated changes in skeletal muscles and their effect on mobility: an operational diagnosis of sarcopenia. J Appl Physiol 95:1851–1860PubMed

27.

Narici MV, Maffulli N (2010) Sarcopenia: characteristics, mechanisms and functional significance. Br Med Bull 95:139–159PubMedCrossRef

28.

Rantanen T, Avlund K, Suominen H, Schroll M, Frandin K, Pertti E (2002) Muscle strength as a predictor of onset of ADL dependence in people aged 75 years. Aging Clin Exp Res 14:10–15PubMed

29.

Clark BC, Manini TM (2008) Sarcopenia =/= dynapenia. J Gerontol A Biol Sci Med Sci 63:829–834PubMedCrossRef

30.

Mitchell WK, Williams J, Atherton P, Larvin M, Lund J, Narici M (2012) Sarcopenia, dynapenia, and the impact of advancing age on human skeletal muscle size and strength; a quantitative review. Front Physiol 3:260PubMedCrossRef

31.

Genaro PS, Pereira GA, Pinheiro MM, Szejnfeld VL, Martini LA (2010) Influence of body composition on bone mass in postmenopausal osteoporotic women. Arch Gerontol Geriatr 51:295–298PubMedCrossRef

32.

Taaffe DR, Cauley JA, Danielson M, Nevitt MC, Lang TF, Bauer DC, Harris TB (2001) Race and sex effects on the association between muscle strength, soft tissue, and bone mineral density in healthy elders: the Health, Aging, and Body Composition Study. J Bone Miner Res 16:1343–1352PubMedCrossRef

33.

Taes YE, Lapauw B, Vanbillemont G, Bogaert V, De BD, Zmierczak H, Goemaere S, Kaufman JM (2009) Fat mass is negatively associated with cortical bone size in young healthy male siblings. J Clin Endocrinol Metab 94:2325–2331PubMedCrossRef

34.

Wang MC, Bachrach LK, Van LM, Hudes M, Flegal KM, Crawford PB (2005) The relative contributions of lean tissue mass and fat mass to bone density in young women. Bone 37:474–481PubMedCrossRef

35.

Szulc P, Beck TJ, Marchand F, Delmas PD (2005) Low skeletal muscle mass is associated with poor structural parameters of bone and impaired balance in elderly men—the MINOS study. J Bone Miner Res 20:721–729PubMedCrossRef

36.

Di MM, Vallero F, Di MR, Tappero R, Cavanna A (2007) Skeletal muscle mass, fat mass, and hip bone mineral density in elderly women with hip fracture. J Bone Miner Metab 25:237–242CrossRef

37.

Blain H, Vuillemin A, Teissier A, Hanesse B, Guillemin F, Jeandel C (2001) Influence of muscle strength and body weight and composition on regional bone mineral density in healthy women aged 60 years and over. Gerontology 47:207–212PubMedCrossRef

38.

Bayramoglu M, Sozay S, Karatas M, Kilinc S (2005) Relationships between muscle strength and bone mineral density of three body regions in sedentary postmenopausal women. Rheumatol Int 25:513–517PubMedCrossRef

39.

Dixon WG, Lunt M, Pye SR, Reeve J, Felsenberg D, Silman AJ, O'Neill TW (2005) Low grip strength is associated with bone mineral density and vertebral fracture in women. Rheumatology (Oxford) 44:642–646CrossRef

40.

Shin H, Panton LB, Dutton GR, Ilich JZ (2011) Relationship of physical performance with body composition and bone mineral density in individuals over 60 years of age: a systematic review. J Aging Res 2011:191896PubMed

41.

Tom SE, Adachi JD, Anderson FA, Jr., Boonen S, Chapurlat RD, Compston JE, Cooper C, Gehlbach SH, Greenspan SL, Hooven FH, Nieves JW, Pfeilschifter J, Roux C, Silverman S, Wyman A, Lacroix AZ (2013) Frailty and fracture, disability, and falls: a multiple country study from the Global Longitudinal Study of Osteoporosis in Women. J Am Geriatr Soc

42.

Woods NF, Lacroix AZ, Gray SL, Aragaki A, Cochrane BB, Brunner RL, Masaki K, Murray A, Newman AB (2005) Frailty: emergence and consequences in women aged 65 and older in the Women's Health Initiative Observational Study. J Am Geriatr Soc 53:1321–1330PubMedCrossRef

43.

Ensrud KE, Ewing SK, Taylor BC, Fink HA, Cawthon PM, Stone KL, Hillier TA, Cauley JA, Hochberg MC, Rodondi N, Tracy JK, Cummings SR (2008) Comparison of 2 frailty indexes for prediction of falls, disability, fractures, and death in older women. Arch Intern Med 168:382–389PubMedCrossRef

44.

Bocalini DS, Serra AJ, Dos SL (2010) Moderate resistive training maintains bone mineral density and improves functional fitness in postmenopausal women. J Aging Res 2010:760818PubMed

45.

Karsenty G, Ferron M (2012) The contribution of bone to whole-organism physiology. Nature 481:314–320PubMedCrossRef

46.

Cornish J, Callon KE, Bava U, Lin C, Naot D, Hill BL, Grey AB, Broom N, Myers DE, Nicholson GC, Reid IR (2002) Leptin directly regulates bone cell function in vitro and reduces bone fragility in vivo. J Endocrinol 175:405–415PubMedCrossRef

47.

Peppa M, Koliaki C, Nikolopoulos P, Raptis SA (2010) Skeletal muscle insulin resistance in endocrine disease. J Biomed Biotechnol 2010:527850PubMedCrossRef

48.

Bostrom P, Wu J, Jedrychowski MP, Korde A, Ye L, Lo JC, Rasbach KA, Bostrom EA, Choi JH, Long JZ, Kajimura S, Zingaretti MC, Vind BF, Tu H, Cinti S, Hojlund K, Gygi SP, Spiegelman BM (2012) A PGC1-alpha-dependent myokine that drives brown-fat-like development of white fat and thermogenesis. Nature 481:463–468PubMedCrossRef

49.

Yu Z, Zhu Z, Tang T, Dai K, Qiu S (2009) Effect of body fat stores on total and regional bone mineral density in perimenopausal Chinese women. J Bone Miner Metab 27:341–346PubMedCrossRef

50.

Douchi T, Yamamoto S, Oki T, Maruta K, Kuwahata R, Nagata Y (2000) Relationship between body fat distribution and bone mineral density in premenopausal Japanese women. Obstet Gynecol 95:722–725PubMedCrossRef

Title: Diagnostic measures for sarcopenia and bone mineral density
Authors: A. Y. Bijlsma
M. C. G. Meskers
M. Molendijk
R. G. J. Westendorp
S. Sipilä
L. Stenroth
E. Sillanpää
J. S. McPhee
D. A. Jones
M. Narici
H. Gapeyeva
M. Pääsuke
E. Seppet
T. Voit
Y. Barnouin
J. Y. Hogrel
G. Butler-Browne
A. B. Maier
Publication date: 01-10-2013
Publisher: Springer London
Published in: Osteoporosis International / Issue 10/2013
Print ISSN: 0937-941X
Electronic ISSN: 1433-2965
DOI: https://doi.org/10.1007/s00198-013-2376-8

At a glance: The STEP trials

Springer Medicine

Diagnostic measures for sarcopenia and bone mineral density

Abstract

Summary

Introduction

Methods

Results

Conclusions

At a glance: The STEP trials

Springer Medicine

Abstract

Summary

Introduction

Methods

Results

Conclusions

Please log in to get access to this content

Other articles of this Issue 10/2013

Micro-morphological properties of osteons reveal changes in cortical bone stability during aging, osteoporosis, and bisphosphonate treatment in women

Correlation between 25-hydroxyvitamin D levels and latitude in Brazilian postmenopausal women: from the Arzoxifene Generations Trial

Can bone loss in rheumatoid arthritis be prevented?

The risk of falls on initiation of antihypertensive drugs in the elderly

Failure after osteosynthesis of trochanteric fractures. Where is the limit of osteoporosis?

Changes in bone mineral density in men starting androgen deprivation therapy and the protective role of vitamin D