Skip to main content

Muscle Mass, Quality, and Composition Changes During Atrophy and Sarcopenia

  • Chapter
  • First Online:

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 1088))

Abstract

Skeletal muscle mass (SMM) and muscle strengh reach their peak in 20s to 40s of age in human life and then decrease with advancing age. The decrease rate of muscle strength or power was twice to four times as large as that of the SMM. Thus, the normalized muscle force (muscle strength divided by SMM) also decreases in aging. It depends on the number of factors in skeletal muscle tissues and neuromuscular system. In human study, SMM cannot be measured directly without dissection so that all of the methodologies are indirect methods to assess SMM, even computing tomography or magnetic resonance imaging. Dual-energy X-ray absorptiometry, ultrasonography, anthropometry, and bioelectrical impedance analysis (BIA) are used as secondary indirect methods to estimate SMM. Recent researches show muscle composition changes in aging, and in particular, the ratio of muscle cell mass (MCM) against SMM decrease and relative expansion of extracellular water (ECW) and extracellular space is observed with advancing age and/or decrease of physical function. The intracellular water (ICW) and ECW estimated by segmental bioelectrical impedance spectroscopy or multifrequency BIA are good biomarkers of the ratio of MCM against SMM in limbs. The BIS and other state-of-the-art technology for assessment of muscle mass, quality, and composition are useful to fully understand the muscle atrophy in a living organism.

This is a preview of subscription content, log in via an institution.

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   189.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD   249.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  1. Allen TH, Anderson EC, Langham WH (1960) Total body potassium and gross body composition in relation to age. J Gerontol 15:348–357

    Article  CAS  Google Scholar 

  2. Yamada Y (2015) Assessment of skeletal muscle mass, strength and frailty. In: Shimada H (ed) Prevention and rehabilitation of the frailty (FUREILU NO YOBOU TO RIHABIRITESHON). Ishiyaku Publishers, Inc., Tokyo

    Google Scholar 

  3. Janssen I, Heymsfield SB, Wang ZM, Ross R (2000) Skeletal muscle mass and distribution in 468 men and women aged 18–88 year. J Appl Physiol (1985) 89(1):81–88

    Article  CAS  Google Scholar 

  4. 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 3:260. https://doi.org/10.3389/fphys.2012.00260

    Article  PubMed  PubMed Central  Google Scholar 

  5. Ferrucci L, de Cabo R, Knuth ND, Studenski S (2012) Of Greek heroes, wiggling worms, mighty mice, and old body builders. J Gerontol A Biol Sci Med Sci 67(1):13–16. https://doi.org/10.1093/gerona/glr046

    Article  PubMed  Google Scholar 

  6. 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 Ser A Biol Med Sci 61(10):1059–1064

    Article  Google Scholar 

  7. Lauretani F, Russo CR, Bandinelli S, Bartali B, Cavazzini C, Di Iorio A, 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(5):1851–1860. https://doi.org/10.1152/japplphysiol.00246.2003

    Article  PubMed  Google Scholar 

  8. Newman AB, Kupelian V, Visser M, Simonsick EM, Goodpaster BH, Kritchevsky SB, Tylavsky FA, Rubin SM, Harris TB (2006) Strength, but not muscle mass, is associated with mortality in the health, aging and body composition study cohort. J Gerontol A Biol Sci Med Sci 61(1):72–77 doi:61/1/72 [pii]

    Article  Google Scholar 

  9. Visser M, Goodpaster BH, Kritchevsky SB, Newman AB, Nevitt M, Rubin SM, Simonsick EM, Harris TB (2005) 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 60(3):324–333 doi:60/3/324 [pii]

    Article  Google Scholar 

  10. Clark BC, Manini TM (2008) Sarcopenia =/= dynapenia. J Gerontol A Biol Sci Med Sci 63(8):829–834

    Article  Google Scholar 

  11. Manini TM, Clark BC (2012) Dynapenia and aging: an update. J Gerontol A Biol Sci Med Sci 67(1):28–40. https://doi.org/10.1093/gerona/glr010

    Article  PubMed  Google Scholar 

  12. Rosenberg IH (1989) Summary comments for the meeting of epidemiologic and methodologic problems in determining nutritional status of older persons. Am J Clin Nutr 50(5):1231–1233. https://doi.org/10.1093/ajcn/50.5.1231

    Article  Google Scholar 

  13. Garry PJ, Hunt WC, VanderJagt DJ, Rhyne RL (1989) Clinical chemistry reference intervals for healthy elderly subjects. Am J Clin Nutr 50 (5 Suppl):1219–1230; discussion 1231-1215. https://doi.org/10.1093/ajcn/50.5.1219

    Article  CAS  Google Scholar 

  14. Goodwin JS (1989) Social, psychological and physical factors affecting the nutritional status of elderly subjects: separating cause and effect. Am J Clin Nutr 50 (5 Suppl):1201–1209; discussion 1231-1205. https://doi.org/10.1093/ajcn/50.5.1201

    Article  CAS  Google Scholar 

  15. Harris T, Woteki C, Briefel RR, Kleinman JC (1989) NHANES III for older persons: nutrition content and methodological considerations. Am J Clin Nutr 50 (5 Suppl):1145–1149; discussion 1231-1145. https://doi.org/10.1093/ajcn/50.5.1145

    Article  CAS  Google Scholar 

  16. Hegsted DM (1989) Recommended dietary intakes of elderly subjects. Am J Clin Nutr 50 (5 Suppl):1190–1194; discussion 1231-1195. https://doi.org/10.1093/ajcn/50.5.1190

    Article  CAS  Google Scholar 

  17. Samet JM (1989) Surrogate measures of dietary intake. Am J Clin Nutr 50 (5 Suppl):1139–1144; discussion 1231-1135. https://doi.org/10.1093/ajcn/50.5.1139

    Article  CAS  Google Scholar 

  18. Kuczmarski RJ (1989) Need for body composition information in elderly subjects. Am J Clin Nutr 50 (5 Suppl):1150–1157; discussion 1231-1155. https://doi.org/10.1093/ajcn/50.5.1150

    Article  CAS  Google Scholar 

  19. Chumlea WC, Baumgartner RN (1989) Status of anthropometry and body composition data in elderly subjects. Am J Clin Nutr 50 (5 Suppl):1158–1166; discussion 1231-1155. https://doi.org/10.1093/ajcn/50.5.1158

    Article  CAS  Google Scholar 

  20. Heymsfield SB, Wang J, Lichtman S, Kamen Y, Kehayias J, Pierson RN, Jr. (1989) Body composition in elderly subjects: a critical appraisal of clinical methodology. Am J Clin Nutr 50 (5 Suppl):1167–1175; discussion 1231-1165. https://doi.org/10.1093/ajcn/50.5.1167

    Article  CAS  Google Scholar 

  21. Schoeller DA (1989) Changes in total body water with age. Am J Clin Nutr 50 (5 Suppl):1176–1181; discussion 1231-1175. https://doi.org/10.1093/ajcn/50.5.1176

    Article  CAS  Google Scholar 

  22. Cruz-Jentoft AJ, Baeyens JP, Bauer JM, Boirie Y, Cederholm T, Landi F, Martin FC, Michel J-P, 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 39:412–423. https://doi.org/10.1093/ageing/afq034

    Article  Google Scholar 

  23. Fielding RA, Vellas B, Evans WJ, Bhasin S, Morley JE, Newman AB, Abellan van Kan G, Andrieu S, Bauer J, Breuille D, Cederholm T, Chandler J, De Meynard C, Donini L, Harris T, Kannt A, Keime Guibert F, 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(4):249–256. https://doi.org/10.1016/j.jamda.2011.01.003

    Article  PubMed  Google Scholar 

  24. Chen LK, Liu LK, Woo J, Assantachai P, Auyeung TW, Bahyah KS, Chou MY, Chen LY, Hsu PS, Krairit O, Lee JS, Lee WJ, Lee Y, Liang CK, Limpawattana P, Lin CS, Peng LN, Satake S, Suzuki T, Won CW, Wu CH, Wu SN, Zhang T, Zeng P, Akishita M, Arai H (2014) Sarcopenia in Asia: consensus report of the Asian working Group for Sarcopenia. J Am Med Dir Assoc 15(2):95–101. https://doi.org/10.1016/j.jamda.2013.11.025

    Article  PubMed  Google Scholar 

  25. Studenski SA, Peters KW, Alley DE, Cawthon PM, McLean RR, Harris TB, Ferrucci L, Guralnik JM, Fragala MS, Kenny AM, Kiel DP, Kritchevsky SB, Shardell MD, Dam TT, Vassileva MT (2014) The FNIH sarcopenia project: rationale, study description, conference recommendations, and final estimates. J Gerontol A Biol Sci Med Sci 69(5):547–558. https://doi.org/10.1093/gerona/glu010

    Article  PubMed  PubMed Central  Google Scholar 

  26. Cruz-Jentoft AJ, Landi F, Schneider SM, Zuniga C, Arai H, Boirie Y, Chen LK, Fielding RA, Martin FC, Michel JP, Sieber C, Stout JR, Studenski SA, Vellas B, Woo J, Zamboni M, Cederholm T (2014) Prevalence of and interventions for sarcopenia in ageing adults: a systematic review. Report of the International Sarcopenia Initiative (EWGSOP and IWGS). Age Ageing 43(6):748–759. https://doi.org/10.1093/ageing/afu115

    Article  PubMed  PubMed Central  Google Scholar 

  27. Cesari M, Fielding RA, Pahor M, Goodpaster B, Hellerstein M, van Kan GA, Anker SD, Rutkove S, Vrijbloed JW, Isaac M, Rolland Y, M’Rini C, Aubertin-Leheudre M, Cedarbaum JM, Zamboni M, Sieber CC, Laurent D, Evans WJ, Roubenoff R, Morley JE, Vellas B (2012) Biomarkers of sarcopenia in clinical trials-recommendations from the International Working Group on Sarcopenia. J Cachexia Sarcopenia Muscle 3(3):181–190. https://doi.org/10.1007/s13539-012-0078-2

    Article  PubMed  PubMed Central  Google Scholar 

  28. Alley DE, Shardell MD, Peters KW, McLean RR, Dam T-TL, Kenny AM, Fragala MS, Harris TB, Kiel DP, Guralnik JM, Ferrucci L, Kritchevsky SB, Studenski SA, Vassileva MT, Cawthon PM (2014) Grip strength Cutpoints for the identification of clinically relevant weakness. J Gerontol Ser A Biol Med Sci 69(5):559–566. https://doi.org/10.1093/gerona/glu011

    Article  Google Scholar 

  29. Cawthon PM, Peters KW, Shardell MD, McLean RR, Dam T-TL, Kenny AM, Fragala MS, Harris TB, Kiel DP, Guralnik JM, Ferrucci L, Kritchevsky SB, Vassileva MT, Studenski SA, Alley DE (2014) Cutpoints for low appendicular lean mass that identify older adults with clinically significant weakness. J Gerontol Ser A Biol Med Sci 69(5):567–575. https://doi.org/10.1093/gerona/glu023

    Article  Google Scholar 

  30. Dam T-T, Peters KW, Fragala M, Cawthon PM, Harris TB, McLean R, Shardell M, Alley DE, Kenny A, Ferrucci L, Guralnik J, Kiel DP, Kritchevsky S, Vassileva MT, Studenski S (2014) An evidence-based comparison of operational criteria for the presence of sarcopenia. J Gerontol Ser A Biol Med Sci 69(5):584–590. https://doi.org/10.1093/gerona/glu013

    Article  Google Scholar 

  31. McLean RR, Shardell MD, Alley DE, Cawthon PM, Fragala MS, Harris TB, Kenny AM, Peters KW, Ferrucci L, Guralnik JM, Kritchevsky SB, Kiel DP, Vassileva MT, Xue Q-L, Perera S, Studenski SA, Dam T-TL (2014) Criteria for clinically relevant weakness and low lean mass and their longitudinal association with incident mobility impairment and mortality: the Foundation for the National Institutes of Health (FNIH) sarcopenia project. J Gerontol Ser A Biol Med Sci 69(5):576–583. https://doi.org/10.1093/gerona/glu012

    Article  Google Scholar 

  32. Yamada Y (2015) New approach focused on muscle cell mass and muscle composition for the definition of skeletal muscle mass and sarcopenia. Jpn J Phys Fitness Sports Med (TAIRYOKUKAGAKU) 64(4):461–472 in Japanese

    Article  Google Scholar 

  33. Heymsfield SB, Lohman TG, Wang ZW, Going SB (2005) Human Body Composition, second edition

    Google Scholar 

  34. Ikai M, Fukunaga T (1968) Calculation of muscle strength per unit cross-sectional area of human muscle by means of ultrasonic measurement. Int Z Angew Physiol 26(1):26–32

    CAS  PubMed  Google Scholar 

  35. Heymsfield SB, Smith R, Aulet M, Bensen B, Lichtman S, Wang J, Pierson RN, Jr. (1990) Appendicular skeletal muscle mass: measurement by dual-photon absorptiometry. Am J Clin Nutr 52 (2):214–218

    Article  CAS  Google Scholar 

  36. Heymsfield SB, Gallagher D, Visser M, Nunez C, Wang ZM (1995) Measurement of skeletal muscle: laboratory and epidemiological methods. J Gerontol A Biol Sci Med Sci 50 Spec No:23–29

    Google Scholar 

  37. Wang ZM, Gallagher D, Nelson ME, Matthews DE, Heymsfield SB (1996) Total-body skeletal muscle mass: evaluation of 24-h urinary creatinine excretion by computerized axial tomography. Am J Clin Nutr 63(6):863–869

    Article  CAS  Google Scholar 

  38. Wang ZM, Visser M, Ma R, Baumgartner RN, Kotler D, Gallagher D, Heymsfield SB (1996) Skeletal muscle mass: evaluation of neutron activation and dual-energy X-ray absorptiometry methods. J Appl Physiol (1985) 80(3):824–831

    Article  CAS  Google Scholar 

  39. Mitsiopoulos N, Baumgartner RN, Heymsfield SB, Lyons W, Gallagher D, Ross R (1998) Cadaver validation of skeletal muscle measurement by magnetic resonance imaging and computerized tomography. J Appl Physiol (1985) 85(1):115–122

    Article  CAS  Google Scholar 

  40. Pietrobelli A, Morini P, Battistini N, Chiumello G, Nunez C, Heymsfield SB (1998) Appendicular skeletal muscle mass: prediction from multiple frequency segmental bioimpedance analysis. Eur J Clin Nutr 52(7):507–511

    Article  CAS  Google Scholar 

  41. Moritani T, deVries HA (1979) Neural factors versus hypertrophy in the time course of muscle strength gain. Am J Phys Med 58(3):115–130

    CAS  PubMed  Google Scholar 

  42. Abe T, Loenneke JP, Thiebaud RS, Fukunaga T (2014) Age-related site-specific muscle wasting of upper and lower extremities and trunk in Japanese men and women. Age (Dordr) 36(2):813–821. https://doi.org/10.1007/s11357-013-9600-5

    Article  Google Scholar 

  43. Abe T, Sakamaki M, Yasuda T, Bemben MG, Kondo M, Kawakami Y, Fukunaga T (2011) Age-related, site-specific muscle loss in 1507 Japanese men and women aged 20 to 95 years. J Sports Sci Med 10(1):145–150

    PubMed  PubMed Central  Google Scholar 

  44. Sanada K, Kearns CF, Midorikawa T, Abe T (2006) Prediction and validation of total and regional skeletal muscle mass by ultrasound in Japanese adults. Eur J Appl Physiol 96(1):24–31. https://doi.org/10.1007/s00421-005-0061-0

    Article  PubMed  Google Scholar 

  45. Snyder WS, Cook MJ, Nasset ES, Karhansen LR, Howells GP, Tipton IH (1975) Report of the task group on reference men. Pergamon Press, Oxford

    Google Scholar 

  46. Kim J, Wang Z, Heymsfield SB, Baumgartner RN, Gallagher D (2002) Total-body skeletal muscle mass: estimation by a new dual-energy X-ray absorptiometry method. Am J Clin Nutr 76(2):378–383

    Article  CAS  Google Scholar 

  47. Ikezoe T, Mori N, Nakamura M, Ichihashi N (2012) Effects of age and inactivity due to prolonged bed rest on atrophy of trunk muscles. Eur J Appl Physiol 112(1):43–48. https://doi.org/10.1007/s00421-011-1952-x

    Article  PubMed  Google Scholar 

  48. Abe T, Loenneke JP, Young KC, Thiebaud RS, Nahar VK, Hollaway KM, Stover CD, Ford MA, Bass MA, Loftin M (2015) Validity of ultrasound prediction equations for total and regional muscularity in middle-aged and older men and women. Ultrasound Med Biol 41(2):557–564. https://doi.org/10.1016/j.ultrasmedbio.2014.09.007

    Article  PubMed  Google Scholar 

  49. Miyatani M, Kanehisa H, Fukunaga T (2000) Validity of bioelectrical impedance and ultrasonographic methods for estimating the muscle volume of the upper arm. Eur J Appl Physiol 82(5–6):391–396

    Article  CAS  Google Scholar 

  50. Ohata K, Tsuboyama T, Ichihashi N, Minami S (2006) Measurement of muscle thickness as quantitative muscle evaluation for adults with severe cerebral palsy. Phys Ther 86(9):1231–1239. https://doi.org/10.2522/ptj.20050189

    Article  PubMed  Google Scholar 

  51. Masaki M, Ikezoe T, Fukumoto Y, Minami S, Tsukagoshi R, Sakuma K, Ibuki S, Yamada Y, Kimura M, Ichihashi N (2015) Association of sagittal spinal alignment with thickness and echo intensity of lumbar back muscles in middle-aged and elderly women. Arch Gerontol Geriatr 61:197. https://doi.org/10.1016/j.archger.2015.05.010

    Article  PubMed  Google Scholar 

  52. Fukumoto Y, Ikezoe T, Yamada Y, Tsukagoshi R, Nakamura M, Takagi Y, Kimura M, Ichihashi N (2015) Age-related ultrasound changes in muscle quantity and quality in women. Ultrasound Med Biol 41(11):3013–3017. https://doi.org/10.1016/j.ultrasmedbio.2015.06.017

    Article  PubMed  Google Scholar 

  53. Midorikawa T, Sanada K, Yoshitomi A, Abe T (2009) Is the use of ultrasound-derived prediction equations for adults useful for estimating total and regional skeletal muscle mass in Japanese children? Br J Nutr 101(1):72–78 S000711450899440X [pii]10.1017/S000711450899440X [doi]

    Article  CAS  Google Scholar 

  54. Loenneke JP, Thiebaud RS, Abe T (2014) Estimating site-specific muscle loss: a valuable tool for early sarcopenia detection? Rejuvenation Res 17(6):496–498. https://doi.org/10.1089/rej.2014.1611

    Article  PubMed  Google Scholar 

  55. Miyatani M, Kanehisa H, Azuma K, Kuno S, Fukunaga T (2003) Site-related differences in muscle loss with aging. “A cross-sectional survey on the muscle thickness in Japanese men aged 20 to 79 years.”. Int J Sport Health Sci 1:34–40

    Article  Google Scholar 

  56. Lexell J, Taylor CC, Sjostrom M (1988) What is the cause of the ageing atrophy? Total number, size and proportion of different fiber types studied in whole vastus lateralis muscle from 15- to 83-year-old men. J Neurol Sci 84(2–3):275–294

    Article  CAS  Google Scholar 

  57. Yamada Y (2014) Assessment methods of skeletal muscle mass and strength. J Clin Exp Med (IGAKU NO AYUMI) 248(9):670–678 in Japanese

    Google Scholar 

  58. Yamada Y (2014) Current issue of body composition research: Tissue, organ, cell level approach from fat to muscle. J Health Phys Educ Recreat (TAIIKU NO KAGAKU) 64 (3):149–155

    Google Scholar 

  59. Mingrone G, Bertuzzi A, Capristo E, Greco AV, Manco M, Pietrobelli A, Salinari S, Heymsfield SB (2001) Unreliable use of standard muscle hydration value in. Obesity 280, 2

    Google Scholar 

  60. Yamada Y, Watanabe Y, Ikenaga M, Yokoyama K, Yoshida T, Morimoto T, Kimura M (2013) Comparison of single- or multifrequency bioelectrical impedance analysis and spectroscopy for assessment of appendicular skeletal muscle in the elderly. J Appl Physiol (Bethesda, Md : 1985) 115(6):812–818. https://doi.org/10.1152/japplphysiol.00010.2013

    Article  Google Scholar 

  61. Yamada Y, Buehring B, Krueger D, Anderson RM, Schoeller DA, Binkley N (2017) Electrical properties assessed by bioelectrical impedance spectroscopy as biomarkers of age-related loss of skeletal muscle quantity and quality. J Gerontol Ser A Biol Med Sci 72(9):1180–1186. https://doi.org/10.1093/gerona/glw225

    Article  Google Scholar 

  62. Yamada Y, Yamagata E, Kimura M (2012) Frailty, sarcopenia, and long-term care prevention. J Kyoto Prefectural Univ Med 121(10):535–547 in Japanese with English abstract

    Google Scholar 

  63. Segal KR, Burastero S, Chun A, Coronel P, Pierson RN Jr, Wang J (1991) Estimation of extracellular and total body water by multiple-frequency bioelectrical-impedance measurement. Am J Clin Nutr 54(1):26–29

    Article  CAS  Google Scholar 

  64. Gudivaka R, Schoeller DA, Kushner RF, Bolt MJG (1999) Single- and multifrequency models for bioelectrical impedance analysis of body water compartments. J Appl Physiol 87(3):1087–1096

    Article  CAS  Google Scholar 

  65. Miyatani M, Kanehisa H, Masuo Y, Ito M, Fukunaga T (2001) Validity of estimating limb muscle volume by bioelectrical impedance. J Appl Physiol 91(1):386–394

    Article  CAS  Google Scholar 

  66. Tanaka NI, Miyatani M, Masuo Y, Fukunaga T, Kanehisa H (2007) Applicability of a segmental bioelectrical impedance analysis for predicting the whole body skeletal muscle volume. J Appl Physiol 103:1688–1695. https://doi.org/10.1152/japplphysiol.00255.2007

    Article  PubMed  Google Scholar 

  67. Yamada Y, Schoeller DA, Nakamura E, Morimoto T, Kimura M, Oda S (2010) Extracellular water may mask actual muscle atrophy during aging. J Gerontol Ser A Biol Med Sci 65A(5):510–516

    Article  Google Scholar 

  68. Yamada Y, Ikenaga M, Takeda N, Morimura K, Miyoshi N, Kiyonaga A, Kimura M, Higaki Y, Tanaka H (2014) Estimation of thigh muscle cross-sectional area by single- and multi-frequency segmental bioelectrical impedance analysis in elderly. J Appl Physiol 116(2):176–182

    Article  Google Scholar 

  69. Yamada Y, Yoshida T, Yokoyama K, Watanabe Y, Miyake M, Yamagata E, Yamada M, Kimura M (2017) The extracellular to intracellular water ratio in upper legs is negatively associated with skeletal muscle strength and gait speed in older people. J Gerontology Ser A Biol Sci Med Sci 72(3):293–298. https://doi.org/10.1093/gerona/glw125

    Article  Google Scholar 

  70. Deurenberg P, Schouten FJ (1992) Loss of total body water and extracellular water assessed by multifrequency impedance. Eur J Clin Nutr 46(4):247–255

    CAS  PubMed  Google Scholar 

  71. Cole KS (1972) Membranes, ions and impulses: a chapter of classical biophysics. University of California Press, Berkeley

    Google Scholar 

  72. De Lorenzo A, Andreoli A, Matthie J, Withers P (1997) Predicting body cell mass with bioimpedance by using theoretical methods: a technological review. J Appl Physiol 96:161–166

    Google Scholar 

  73. Hanai T (1968) Electrical properties of emulsions. In: Sherman PH (ed) Emulsion science. Academic Press Inc, London, pp 354–477

    Google Scholar 

  74. Piccoli A, Rossi B, Pillon L, Bucciante G (1994) A new method for monitoring body fluid variation by bioimpedance analysis: the RXc graph. Kidney Int 46(2):534–539

    Article  CAS  Google Scholar 

  75. Piccoli A, Piazza P, Noventa D, Pillon L, Zaccaria M (1996) A new method for monitoring hydration at high altitude by bioimpedance analysis. Med Sci Sports Exerc 28(12):1517–1522

    Article  CAS  Google Scholar 

  76. Siglinsky E, Buehring B, Krueger D, Binkley N, Yamada Y (2018) Could bioelectric impedance spectroscopy (BIS) measured appendicular intracellular water serve as a lean mass measurement in sarcopenia definitions? A pilot study. Osteoporos Int 29:1653–1657. https://doi.org/10.1007/s00198-018-4475-z

    Article  CAS  Google Scholar 

  77. Yamada Y, Matsuda K, Bjorkman MP, Kimura M (2014) Application of segmental bioelectrical impedance spectroscopy to the assessment of skeletal muscle cell mass in elderly men. Geriatr Gerontol Int 14(Suppl 1):129–134. https://doi.org/10.1111/ggi.12212

    Article  PubMed  Google Scholar 

  78. Wang Z, St-Onge MP, Lecumberri B, Pi-Sunyer FX, Heshka S, Wang J, Kotler DP, Gallagher D, Wielopolski L, Pierson RN Jr, Heymsfield SB (2004) Body cell mass: model development and validation at the cellular level of body composition. Am J Physiol Endocrinol Metab 286(1):E123–E128. https://doi.org/10.1152/ajpendo.00227.2003

    Article  CAS  PubMed  Google Scholar 

  79. Lustyik G (1986) Age-dependent alterations of the intracellular water and electrolyte content of heart and muscle cells. Arch Gerontol Geriatr 5(4):291–296

    Article  CAS  Google Scholar 

  80. Shiose K, Yamada Y, Motonaga K, Takahashi H (2018) Muscle glycogen depletion does not alter segmental extracellular and intracellular water distribution measured using bioimpedance spectroscopy. J Appl Physiol (Bethesda, Md : 1985). https://doi.org/10.1152/japplphysiol.00666.2017

    Article  Google Scholar 

  81. Shiose K, Yamada Y, Motonaga K, Sagayama H, Higaki Y, Tanaka H, Takahashi H (2016) Segmental extracellular and intracellular water distribution and muscle glycogen after 72-h carbohydrate loading using spectroscopic techniques. J Appl Physiol (1985) 121(1):205–211. https://doi.org/10.1152/japplphysiol.00126.2016

    Article  CAS  Google Scholar 

  82. Shiose K, Yamada Y, Motonaga K, Takahashi H (2017) Circadian variation of extracellular and intracellular resistance of the leg, arm, and trunk in healthy humans: a segmental bioimpedance spectroscopy study. Biomed Phys Eng Express 3(6):065007. https://doi.org/10.1088/2057-1976/aa87c0

    Article  Google Scholar 

  83. Zhang C, Gao Y (2014) Effects of aging on the lateral transmission of force in rat skeletal muscle. J Biomech 47(5):944–948. https://doi.org/10.1016/j.jbiomech.2014.01.026

    Article  PubMed  PubMed Central  Google Scholar 

  84. Heymsfield SB, Gonzalez MC, Lu J, Jia G, Zheng J (2015) Skeletal muscle mass and quality: evolution of modern measurement concepts in the context of sarcopenia. Proc Nutr Soc 74:1–12. https://doi.org/10.1017/s0029665115000129

    Article  Google Scholar 

  85. 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 90(6):2157–2165

    Article  CAS  Google Scholar 

  86. Goodpaster BH, Kelley DE, Thaete FL, He J, Ross R (2000) Skeletal muscle attenuation determined by computed tomography is associated with skeletal muscle lipid content. J Appl Physiol 89(1):104–110

    Article  CAS  Google Scholar 

  87. Kent-Braun JA, Ng AV, Young K (2000) Skeletal muscle contractile and noncontractile components in young and older women and men. J Appl Physiol 88(2):662–668

    Article  CAS  Google Scholar 

  88. Galban CJ, Maderwald S, Stock F, Ladd ME (2007) Age-related changes in skeletal muscle as detected by diffusion tensor magnetic resonance imaging. J Gerontol A Biol Sci Med Sci 62(4):453–458

    Article  Google Scholar 

  89. Ploutz-Snyder LL, Yackel-Giamis EL, Rosenbaum AE, Formikell M (2000) Use of muscle functional magnetic resonance imaging with older individuals. J Gerontol A Biol Sci Med Sci 55(10):B504–B511

    Article  CAS  Google Scholar 

  90. Watanabe Y, Yamada Y, Fukumoto Y, Ishihara T, Yokoyama K, Yoshida T, Miyake M, Yamagata E, Kimura M (2013) Echo intensity obtained from ultrasonography images reflecting muscle strength in elderly men. Clin Interv Aging 8:993–998. https://doi.org/10.2147/CIA.S47263

    Article  PubMed  PubMed Central  Google Scholar 

  91. Fukumoto Y, Ikezoe T, Yamada Y, Tsukagoshi R, Nakamura M, Mori N, Kimura M, Ichihashi N (2012) Skeletal muscle quality assessed from echo intensity is associated with muscle strength of middle-aged and elderly persons. Eur J Appl Physiol 112(4):1519–1525. doi. https://doi.org/10.1007/s00421-011-2099-5

    Article  PubMed  Google Scholar 

  92. Akagi R, Suzuki M, Kawaguchi E, Miyamoto N, Yamada Y, Ema R (2018) Muscle size-strength relationship including ultrasonographic echo intensity and voluntary activation level of a muscle group. Arch Gerontol Geriatr 75:185–190. https://doi.org/10.1016/j.archger.2017.12.012

    Article  PubMed  Google Scholar 

  93. Taniguchi M, Yamada Y, Fukumoto Y, Sawano S, Minami S, Ikezoe T, Watanabe Y, Kimura M, Ichihashi N (2017) Increase in echo intensity and extracellular-to-intracellular water ratio is independently associated with muscle weakness in elderly women. Eur J Appl Physiol 117(10):2001–2007. https://doi.org/10.1007/s00421-017-3686-x

    Article  PubMed  Google Scholar 

  94. Narici MV, Maganaris CN, Reeves ND, Capodaglio P (2003) Effect of aging on human muscle architecture. J Appl Physiol (1985) 95(6):2229–2234. https://doi.org/10.1152/japplphysiol.00433.2003

    Article  CAS  Google Scholar 

  95. Nishimura T, Ojima K, Hattori A, Takahashi K (1997) Developmental expression of extracellular matrix components in intramuscular connective tissue of bovine semitendinosus muscle. Histochem Cell Biol 107(3):215–221

    Article  CAS  Google Scholar 

  96. Kadi F, Charifi N, Denis C, Lexell J (2004) Satellite cells and myonuclei in young and elderly women and men. Muscle Nerve 29(1):120–127. https://doi.org/10.1002/mus.10510

    Article  PubMed  Google Scholar 

  97. Klitgaard H, Zhou M, Schiaffino S, Betto R, Salviati G, Saltin B (1990) Ageing alters the myosin heavy chain composition of single fibres from human skeletal muscle. Acta Physiol Scand 140(1):55–62. https://doi.org/10.1111/j.1748-1716.1990.tb08975.x

    Article  CAS  PubMed  Google Scholar 

  98. Cristea A, Qaisar R, Edlund PK, Lindblad J, Bengtsson E, Larsson L (2010) Effects of aging and gender on the spatial organization of nuclei in single human skeletal muscle cells. Aging Cell 9(5):685–697. https://doi.org/10.1111/j.1474-9726.2010.00594.x

    Article  CAS  PubMed  Google Scholar 

  99. Delbono O, O’Rourke KS, Ettinger WH (1995) Excitation-calcium release uncoupling in aged single human skeletal muscle fibers. J Membr Biol 148(3):211–222

    Article  CAS  Google Scholar 

  100. Kubo K, Ishida Y, Komuro T, Tsunoda N, Kanehisa H, Fukunaga T (2007) Age-related differences in the force generation capabilities and tendon extensibilities of knee extensors and plantar flexors in men. J Gerontol A Biol Sci Med Sci 62(11):1252–1258

    Article  Google Scholar 

  101. Luff AR (1998) Age-associated changes in the innervation of muscle fibers and changes in the mechanical properties of motor units. Ann N Y Acad Sci 854:92–101

    Article  CAS  Google Scholar 

  102. Moritani T, deVries HA (1980) Potential for gross muscle hypertrophy in older men. J Gerontol 35(5):672–682

    Article  CAS  Google Scholar 

  103. Kamen G (2005) Aging, resistance training, and motor unit discharge behavior. Can J Appl Physiol 30(3):341–351

    Article  Google Scholar 

  104. Kido A, Tanaka N, Stein RB (2004) Spinal excitation and inhibition decrease as humans age. Can J Physiol Pharmacol 82(4):238–248. https://doi.org/10.1139/y04-017

    Article  CAS  PubMed  Google Scholar 

  105. Oliviero A, Profice P, Tonali PA, Pilato F, Saturno E, Dileone M, Ranieri F, Di Lazzaro V (2006) Effects of aging on motor cortex excitability. Neurosci Res 55(1):74–77. https://doi.org/10.1016/j.neures.2006.02.002

    Article  CAS  PubMed  Google Scholar 

  106. Lauretani F, Bandinelli S, Bartali B, Di Iorio A, Giacomini V, Corsi AM, Guralnik JM, Ferrucci L (2006) Axonal degeneration affects muscle density in older men and women. Neurobiol Aging 27(8):1145–1154. https://doi.org/10.1016/j.neurobiolaging.2005.06.009

    Article  PubMed  Google Scholar 

  107. Klein CS, Rice CL, Marsh GD (2001) Normalized force, activation, and coactivation in the arm muscles of young and old men. J Appl Physiol (1985) 91(3):1341–1349

    Article  CAS  Google Scholar 

  108. Shinohara M, Latash ML, Zatsiorsky VM (2003) Age effects on force produced by intrinsic and extrinsic hand muscles and finger interaction during MVC tasks. J Appl Physiol (1985) 95(4):1361–1369. https://doi.org/10.1152/japplphysiol.00070.2003

    Article  Google Scholar 

  109. Billot M, Duclay J, Simoneau-Buessinger EM, Ballay Y, Martin A (2014) Is co-contraction responsible for the decline in maximal knee joint torque in older males? Age (Dordr) 36(2):899–910. https://doi.org/10.1007/s11357-014-9616-5

    Article  Google Scholar 

  110. Ikenaga M, Yamada Y, Mihara R, Yoshida T, Fujii K, Morimura K, Hirano M, Enishi K, Shindo M, Kiyonaga A (2012) Effects of slightly-weighted shoe intervention on lower limb muscle mass and gait patterns in the elderly. Jpn J Phys Fitness Sports Med (TAIRYOKUKAGAKU) 61(5):469–477 (in Japanese with English abstract)

    Article  Google Scholar 

  111. Ikenaga M, Yamada Y, Kose Y, Morimura K, Higaki Y, Kiyonaga A, Tanaka H (2017) Effects of a 12-week, short-interval, intermittent, low-intensity, slow-jogging program on skeletal muscle, fat infiltration, and fitness in older adults: randomized controlled trial. Eur J Appl Physiol 117(1):7–15. https://doi.org/10.1007/s00421-016-3493-9

    Article  PubMed  Google Scholar 

  112. Yamada Y, Nanri H, Watanabe Y, Yoshida T, Yokoyama K, Itoi A, Date H, Yamaguchi M, Miyake M, Yamagata E, Tamiya H, Nishimura M, Fujibayashi M, Ebine N, Yoshida M, Kikutani T, Yoshimura E, Ishikawa-Takata K, Yamada M, Nakaya T, Yoshinaka Y, Fujiwara Y, Arai H, Kimura M (2017) Prevalence of frailty assessed by fried and Kihon checklist indexes in a prospective cohort study: design and demographics of the Kyoto-Kameoka longitudinal study. J Am Med Dir Assoc 18:733.e7. https://doi.org/10.1016/j.jamda.2017.02.022

    Article  Google Scholar 

  113. Fried LP, Tangen CM, Walston J, Newman AB, Hirsch C, Gottdiener J, Seeman T, Tracy R, Kop WJ, Burke G, McBurnie MA (2001) Frailty in older adults: evidence for a phenotype. J Gerontol A Biol Sci Med Sci 56(3):M146–M156

    Article  CAS  Google Scholar 

  114. Xue QL, Bandeen-Roche K, Varadhan R, Zhou J, Fried LP (2008) Initial manifestations of frailty criteria and the development of frailty phenotype in the Women’s health and aging study II. J Gerontol A Biol Sci Med Sci 63(9):984–990

    Article  Google Scholar 

  115. Rockwood K, Andrew M, Mitnitski A (2007) A comparison of two approaches to measuring frailty in elderly people. J Gerontol A Biol Sci Med Sci 62(7):738–743

    Article  Google Scholar 

  116. Arai H, Satake S (2015) English translation of the Kihon checklist. Geriatr Gerontol Int 15(4):518–519. https://doi.org/10.1111/ggi.12397

    Article  PubMed  Google Scholar 

  117. Satake S, Senda K, Hong YJ, Miura H, Endo H, Sakurai T, Kondo I, Toba K (2016) Validity of the Kihon checklist for assessing frailty status. Geriatr Gerontol Int 16(6):709–715. https://doi.org/10.1111/ggi.12543

    Article  PubMed  Google Scholar 

  118. Arum O, Rasche ZA, Rickman DJ, Bartke A (2013) Prevention of neuromusculoskeletal frailty in slow-aging ames dwarf mice: longitudinal investigation of interaction of longevity genes and caloric restriction. PLoS One 8(10):e72255. https://doi.org/10.1371/journal.pone.0072255

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Feridooni HA, Sun MH, Rockwood K, Howlett SE (2015) Reliability of a frailty index based on the clinical assessment of health deficits in male C57BL/6J mice. J Gerontol A Biol Sci Med Sci 70(6):686–693. https://doi.org/10.1093/gerona/glu161

    Article  PubMed  Google Scholar 

  120. Kane AE, Hilmer SN, Boyer D, Gavin K, Nines D, Howlett SE, de Cabo R, Mitchell SJ (2016) Impact of longevity interventions on a validated mouse clinical frailty index. J Gerontol A Biol Sci Med Sci 71(3):333–339. https://doi.org/10.1093/gerona/glu315

    Article  CAS  PubMed  Google Scholar 

  121. Liu H, Graber TG, Ferguson-Stegall L, Thompson LV (2014) Clinically relevant frailty index for mice. J Gerontol A Biol Sci Med Sci 69(12):1485–1491. https://doi.org/10.1093/gerona/glt188

    Article  PubMed  Google Scholar 

  122. Whitehead JC, Hildebrand BA, Sun M, Rockwood MR, Rose RA, Rockwood K, Howlett SE (2014) A clinical frailty index in aging mice: comparisons with frailty index data in humans. J Gerontol A Biol Sci Med Sci 69(6):621–632. https://doi.org/10.1093/gerona/glt136

    Article  PubMed  Google Scholar 

  123. Yamada Y, Kemnitz JW, Weindruch R, Anderson RM, Schoeller DA, Colman RJ (2018) Caloric restriction and healthy life span: frail phenotype of nonhuman primates in the Wisconsin National Primate Research Center Caloric Restriction Study. J Gerontol A Biol Sci Med Sci 73(3):273–278. https://doi.org/10.1093/gerona/glx059

    Article  PubMed  Google Scholar 

  124. Mitnitski A, Rockwood K (2015) The rate of aging: the rate of deficit accumulation does not change over the adult life span. Biogerontology 17:199. https://doi.org/10.1007/s10522-015-9583-y

    Article  PubMed  Google Scholar 

  125. Mitnitski A, Song X, Rockwood K (2013) Assessing biological aging: the origin of deficit accumulation. Biogerontology 14(6):709–717. https://doi.org/10.1007/s10522-013-9446-3

    Article  PubMed  PubMed Central  Google Scholar 

  126. Studenski SA, Peters KW, Alley DE, Cawthon PM, McLean RR, Harris TB, Ferrucci L, Guralnik JM, Fragala MS, Kenny AM, Kiel DP, Kritchevsky SB, Shardell MD, Dam T-TL, Vassileva MT (2014) The FNIH sarcopenia project: rationale, study description, conference recommendations, and final estimates. J Gerontol Ser A Biol Med Sci 69(5):547–558. https://doi.org/10.1093/gerona/glu010

    Article  Google Scholar 

  127. Evans WJ (2010) Skeletal muscle loss: cachexia, sarcopenia, and inactivity. Am J Clin Nutr 91(4):1123s–1127s. https://doi.org/10.3945/ajcn.2010.28608A

    Article  CAS  PubMed  Google Scholar 

  128. Fearon K, Strasser F, Anker SD, Bosaeus I, Bruera E, Fainsinger RL, Jatoi A, Loprinzi C, MacDonald N, Mantovani G, Davis M, Muscaritoli M, Ottery F, Radbruch L, Ravasco P, Walsh D, Wilcock A, Kaasa S, Baracos VE (2011) Definition and classification of cancer cachexia: an international consensus. Lancet Oncol 12(5):489–495. https://doi.org/10.1016/s1470-2045(10)70218-7

    Article  PubMed  Google Scholar 

  129. Muscaritoli M, Anker SD, Argiles J, Aversa Z, Bauer JM, Biolo G, Boirie Y, Bosaeus I, Cederholm T, Costelli P, Fearon KC, Laviano A, Maggio M, Rossi Fanelli F, Schneider SM, Schols A, Sieber CC (2010) Consensus definition of sarcopenia, cachexia and pre-cachexia: joint document elaborated by Special Interest Groups (SIG) “cachexia-anorexia in chronic wasting diseases” and “nutrition in geriatrics”. Clin Nutr 29(2):154–159. https://doi.org/10.1016/j.clnu.2009.12.004

    Article  CAS  PubMed  Google Scholar 

  130. Yamada Y (2017) Assessment and definition of sarcopenia: general concept and importance at digestive surgery. Gastroenterol Surg (SHOKAKIGEKA) 40(7):1009–1024 in Japanese

    Google Scholar 

  131. Lee WJ, Liu LK, Peng LN, Lin MH, Chen LK (2013) Comparisons of sarcopenia defined by IWGS and EWGSOP criteria among older people: results from the I-Lan longitudinal aging study. J Am Med Dir Assoc 14(7):528 e521–528 e527. https://doi.org/10.1016/j.jamda.2013.03.019

    Article  Google Scholar 

  132. Cooper R, Bann D, Wloch EG, Adams JE, Kuh D (2015) “Skeletal muscle function deficit” in a nationally representative British birth cohort in early old age. J Gerontol A Biol Sci Med Sci 70(5):604–607. https://doi.org/10.1093/gerona/glu214

    Article  CAS  PubMed  Google Scholar 

  133. Wen X, An P, Chen WC, Lv Y, Fu Q (2015) Comparisons of sarcopenia prevalence based on different diagnostic criteria in chinese older adults. J Nutr Health Aging 19(3):342–347. https://doi.org/10.1007/s12603-014-0561-x

    Article  CAS  PubMed  Google Scholar 

  134. Buehring B, Siglinsky E, Krueger D, Evans W, Hellerstein M, Yamada Y, Binkley N (2017) Comparison of muscle/lean mass measurement methods: correlation with functional and biochemical testing. Osteoporos Int 29(3):675–683. https://doi.org/10.1007/s00198-017-4315-6

    Article  Google Scholar 

  135. Yamada Y, Nishizawa M, Uchiyama T, Kasahara Y, Shindo M, Miyachi M, Tanaka S (2017) Developing and validating an age-independent equation using multi-frequency bioelectrical impedance analysis for estimation of appendicular skeletal muscle mass and establishing a cutoff for sarcopenia. Int J Environ Res Public Health 14(7). https://doi.org/10.3390/ijerph14070809

    Article  Google Scholar 

  136. Yamada M, Yamada Y, Arai H (2016) Comparability of two representative devices for bioelectrical impedance data acquisition. Geriatr Gerontol Int 16(9):1087–1088. https://doi.org/10.1111/ggi.12647

    Article  PubMed  Google Scholar 

  137. Fukumoto Y, Yamada Y, Ikezoe T, Watanabe Y, Taniguchi M, Sawano S, Minami S, Asai T, Kimura M, Ichihashi N (2018) Association of physical activity with age-related changes in muscle echo intensity in older adults: a 4-year longitudinal study. J Appl Physiol [Epub ahead of print]. https://doi.org/10.1152/japplphysiol.00317.2018

  138. Nanri H, Yamada Y, Yoshida T, Okabe Y, Nozawa Y, Itoi A, Yoshimura E, Watanabe Y, Yamaguchi M, Yokoyama K, Ishikawa-Takata K, Kobayashi H, Kimura M, Kyoto-Kameoka Study Group (2018) Sex difference in the association between protein intake and frailty: assessed using the Kihon checklist indexes among older adults. J Am Med Dir Assoc 19(9):801–805. https://doi.org/10.1016/j.jamda.2018.04.005

    Article  Google Scholar 

Download references

Acknowledgments

This work was supported by the grants from Japan Agency for Medical Research and Development (AMED) Grant Number 17dk0310064h0102 and 17dk0310074h0202 and Japan Society for the Promotion of Science (JSPS) KAKENHI Grant Number 15H05363, 26560354, and 18H03164. The author has been supported by Ajinomoto Co., Inc., for the large cohort study.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yosuke Yamada .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer Nature Singapore Pte Ltd.

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Yamada, Y. (2018). Muscle Mass, Quality, and Composition Changes During Atrophy and Sarcopenia. In: Xiao, J. (eds) Muscle Atrophy. Advances in Experimental Medicine and Biology, vol 1088. Springer, Singapore. https://doi.org/10.1007/978-981-13-1435-3_3

Download citation

Publish with us

Policies and ethics