Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Physiology and biochemistry

Full characterisation of knee extensors’ function in ageing: effect of sex and obesity

Abstract

Background/Objectives

Muscle function is a marker of current and prospective health/independence throughout life. The effects of sex and obesity (OB) on the loss of muscle function in ageing remain unresolved, with important implications for the diagnosis/monitoring of sarcopenia. To characterise in vivo knee extensors’ function, we compared muscles torque and power with isometric and isokinetic tests in older men (M) and women (W), with normal range (NW) of body mass index (BMI) and OB.

Subjects/Methods

In 70 sedentary older M and W (69 ± 5 years), NW and OB (i.e. BMI < 30 kg m−2 and ≥30 kg m−2, respectively) we tested the right knee’s extensor: (i) isometric torque at 30°, 60°, 75° and 90° knee angles, and (ii) isokinetic concentric torque at 60, 90, 150, 180 and 210° s−1 angular speeds. Maximal isometric T–angle, maximal isokinetic knee-extensor torque–velocity, theoretical maximal shortening velocity, maximal power, optimal torque and velocity were determined in absolute units, normalised by body mass (BM) and right leg lean mass (LLMR) and compared over sex, BMI categories and angle or angular speeds by three-way ANOVA.

Results

In absolute units, relative to BM and LLMR, sex differences were found in favour of M for all parameters of muscle function (main effect for sex, p < 0.05). OB did not affect either absolute or relative to LLMR isometric and isokinetic muscle function (main effect for BMI, p > 0.05); however, muscle function indices, when adjusted for BM, were lower in both M and W with OB compared to NW counterparts (p < 0.05).

Conclusions

We confirmed sex differences in absolute, relative to BM and LLMR muscle function in favour of men. While overall muscle function and muscle contractile quality is conserved in individuals with class I OB, muscle function normalised for BM, which defines the ability to perform independently and safely the activities of daily living, is impaired in comparison with physiological ageing.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Knee extensors’ function curves.
Fig. 2: Isometric and isokinetic values in absolute units.
Fig. 3: Isometric and isokinetic values relative to body mass.
Fig. 4: Isometric and isokinetic values relative to lean mass.

Similar content being viewed by others

References

  1. Macaluso A, De Vito G. Muscle strength, power and adaptations to resistance training in older people. Eur J Appl Physiol. 2004;91:450–72.

    Article  PubMed  Google Scholar 

  2. Landi F, Liperoti R, Russo A, Giovannini S, Tosato M, Capoluongo E, et al. Sarcopenia as a risk factor for falls in elderly individuals: results from the ilSIRENTE study. Clin Nutr. 2012;31:652–8.

    Article  PubMed  Google Scholar 

  3. Harris-Love MO, Benson K, Leasure E, Adams B, McIntosh V. The influence of upper and lower extremity strength on performance-based sarcopenia assessment tests. J Funct Morphol Kinesiol. 2018;3:53.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Keller K, Engelhardt M. Strength and muscle mass loss with aging process. Age and strength loss. Muscles, Ligaments Tendons J. 2013;3:346.

    Article  Google Scholar 

  5. Skelton DA, Greig CA, Davies JM, Young A. Strength, power and related functional ability of healthy people aged 65–89 years. Age Ageing. 1994;23:371–7.

    Article  CAS  PubMed  Google Scholar 

  6. Cruz-Jentoft AJ, Landi F, Topinková E, Michel J-P. Understanding sarcopenia as a geriatric syndrome. Curr Opin Clin Nutr Metab Care. 2010;13:1–7.

    Article  PubMed  Google Scholar 

  7. Cooper C, Fielding R, Visser M, Van Loon L, Rolland Y, Orwoll E, et al. Tools in the assessment of sarcopenia. Calcif Tissue Int. 2013;93:201–10.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Narici MV, Maffulli N. Sarcopenia: characteristics, mechanisms and functional significance. Brit Med Bull. 2010;95:139–59.

    Article  CAS  PubMed  Google Scholar 

  9. Zamboni M, Mazzali G, Fantin F, Rossi A, Di Francesco V. Sarcopenic obesity: a new category of obesity in the elderly. Nutr, Metab Cardiovasc Dis. 2008;18:388–95.

    Article  CAS  Google Scholar 

  10. Delmonico MJ, Harris TB, Visser M, Park SW, Conroy MB, Velasquez-Mieyer P, et al. Longitudinal study of muscle strength, quality, and adipose tissue infiltration. Am J Clin Nutr. 2009;90:1579.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Tomlinson DJ, Erskine RM, Morse CI, Winwood K, Onambélé-Pearson G. The impact of obesity on skeletal muscle strength and structure through adolescence to old age. Biogerontology. 2016;17:467–83.

    Article  CAS  PubMed  Google Scholar 

  12. Tallis J, James RS, Seebacher F. The effects of obesity on skeletal muscle contractile function. J Exp Biol. 2018;221:jeb163840.

    Article  PubMed  Google Scholar 

  13. Bollinger LM. Potential contributions of skeletal muscle contractile dysfunction to altered biomechanics in obesity. Gait Posture. 2017;56:100–7.

    Article  PubMed  Google Scholar 

  14. Valenzuela PL, Maffiuletti NA, Tringali G, De Col A, Sartorio A. Obesity-associated poor muscle quality: prevalence and association with age, sex, and body mass index. BMC Musculoskelet Disord. 2020;21:1–8.

    Article  Google Scholar 

  15. Tomlinson D, Erskine R, Morse C, Winwood K, Onambele-Pearson G. Combined effects of body composition and ageing on joint torque, muscle activation and co-contraction in sedentary women. Age. 2014;36:9652.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Zoico E, Di Francesco V, Guralnik J, Mazzali G, Bortolani A, Guariento S, et al. Physical disability and muscular strength in relation to obesity and different body composition indexes in a sample of healthy elderly women. Int J Obes. 2004;28:234–41.

    Article  CAS  Google Scholar 

  17. Buckinx F, Aubertin-Leheudre M. Relevance to assess and preserve muscle strength in aging field. Prog Neuro-Psychopharmacol Biol Psychiatry. 2019;94:109663.

  18. Thompson BJ, Whitson M, Sobolewski EJ, Stock MS. The influence of age, joint angle, and muscle group on strength production characteristics at the knee joint. J Gerontol: Ser A. 2018;73:603–7.

    Article  Google Scholar 

  19. Lanza IR, Towse TF, Caldwell GE, Wigmore D, Kent-Braun JA. Effects of age on human muscle torque, velocity, and power in two muscle groups. J Appl Physiol. 2003;95:2361–9.

    Article  CAS  PubMed  Google Scholar 

  20. Maffiuletti NA, Ratel S, Sartorio A, Martin V. The impact of obesity on in vivo human skeletal muscle function. Curr Obes Rep. 2013;2:251–60.

    Article  Google Scholar 

  21. Barbat-Artigas S, Rolland Y, Zamboni M, Aubertin-Leheudre M. How to assess functional status: a new muscle quality index. J Nutr Health Aging. 2012;16:67–77.

    Article  CAS  PubMed  Google Scholar 

  22. Raj IS, Bird SR, Shield AJ. Aging and the force–velocity relationship of muscles. Exp Gerontol. 2010;45:81–90.

    Article  CAS  PubMed  Google Scholar 

  23. Fragala MS, Fukuda DH, Stout JR, Townsend JR, Emerson NS, Boone CH, et al. Muscle quality index improves with resistance exercise training in older adults. Exp Gerontol. 2014;53:1–6.

    Article  PubMed  Google Scholar 

  24. Alcazar J, Rodriguez-Lopez C, Ara I, Alfaro-Acha A, Rodríguez-Gómez I, Navarro-Cruz R, et al. Force-velocity profiling in older adults: an adequate tool for the management of functional trajectories with aging. Exp Gerontol. 2018;108:1–6.

    Article  PubMed  Google Scholar 

  25. Lee PH, Macfarlane DJ, Lam T, Stewart SM. Validity of the international physical activity questionnaire short form (IPAQ-SF): a systematic review. Int J Behav Nutr Phys Act. 2011;8:115.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Visser M, Fuerst T, Lang T, Salamone L, Harris TB, Health FT, et al. Validity of fan-beam dual-energy X-ray absorptiometry for measuring fat-free mass and leg muscle mass. J Appl Physiol. 1999;87:1513–20.

    Article  CAS  PubMed  Google Scholar 

  27. Skalsky AJ, Han JJ, Abresch RT, Shin CS, McDonald CM. Assessment of regional body composition with dual-energy X-ray absorptiometry in Duchenne muscular dystrophy: correlation of regional lean mass and quantitative strength. Muscle Nerve. 2009;39:647–51.

    Article  PubMed  Google Scholar 

  28. Cruz-Jentoft AJ, Bahat G, Bauer J, Boirie Y, Bruyère O, Cederholm T, et al. Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing. 2019;48:16–31.

    Article  PubMed  Google Scholar 

  29. Mullineaux DR, Bartlett RM, Bennett S. Research design and statistics in biomechanics and motor control. J Sports Sci. 2001;19:739–60.

    Article  CAS  PubMed  Google Scholar 

  30. Lee C, Dierickx E. Defining sarcopenia using muscle quality index. J Aging Res Clin Pract. 2018;7:55–9.

  31. Coleman TF, Li Y. An interior trust region approach for nonlinear minimization subject to bounds. SIAM J Optim. 1996;6:418–45.

    Article  Google Scholar 

  32. Ferri A, Scaglioni G, Pousson M, Capodaglio P, Van Hoecke J, Narici M. Strength and power changes of the human plantar flexors and knee extensors in response to resistance training in old age. Acta Physiol Scand. 2003;177:69–78.

    Article  CAS  PubMed  Google Scholar 

  33. Hill A. The heat of shortening and the dynamic constants of muscle. Proc R Soc Lond Ser B, Biol Sci. 1938;126:136–95.

  34. Ogden CL, Fakhouri TH, Carroll MD, Hales CM, Fryar CD, Li X, et al. Prevalence of obesity among adults, by household income and education—United States, 2011–2014. Morbid Mortal Wkly Rep. 2017;66:1369.

    Article  Google Scholar 

  35. Marques A, Peralta M, Naia A, Loureiro N, de Matos MG. Prevalence of adult overweight and obesity in 20 European countries, 2014. Eur J Public Health. 2018;28:295–300.

    Article  PubMed  Google Scholar 

  36. Stoklossa CAJ, Sharma AM, Forhan M, Siervo M, Padwal RS, Prado CM. Prevalence of sarcopenic obesity in adults with class II/III obesity using different diagnostic criteria. J Nutr Metabol. 2017;2017:1–11.

  37. Perna S, Peroni G, Faliva MA, Bartolo A, Naso M, Miccono A, et al. Sarcopenia and sarcopenic obesity in comparison: prevalence, metabolic profile, and key differences. A cross-sectional study in Italian hospitalized elderly. Aging Clin Exp Res. 2017;29:1249–58.

    Article  PubMed  Google Scholar 

  38. Lafortuna C, Maffiuletti N, Agosti F, Sartorio A. Gender variations of body composition, muscle strength and power output in morbid obesity. Int J Obes. 2005;29:833–41.

    Article  CAS  Google Scholar 

  39. McLeod M, Breen L, Hamilton DL, Philp A. Live strong and prosper: the importance of skeletal muscle strength for healthy ageing. Biogerontology. 2016;17:497–510.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Barbat-Artigas S, Plouffe S, Pion CH, Aubertin-Leheudre M. Toward a sex-specific relationship between muscle strength and appendicular lean body mass index? J Cachexia, Sarcopenia Muscle. 2013;4:137–44.

    Article  Google Scholar 

  41. Miyatake N, Fujii M, Nishikawa H, Wada J, Shikata K, Makino H, et al. Clinical evaluation of muscle strength in 20–79-years-old obese Japanese. Diabetes Res Clin Pract. 2000;48:15–21.

    Article  CAS  PubMed  Google Scholar 

  42. Maffiuletti NA, Jubeau M, Agosti F, De Col A, Sartorio A. Quadriceps muscle function characteristics in severely obese and nonobese adolescents. Eur J Appl Physiol. 2008;103:481–4.

    Article  PubMed  Google Scholar 

  43. Naugle KM, Higgins TJ, Manini TM. Obesity and use of compensatory strategies to perform common daily activities in pre-clinically disabled older adults. Arch Gerontol Geriatr. 2012;54:e134–8.

    Article  PubMed  Google Scholar 

  44. Leblanc A, Taylor BA, Thompson PD, Capizzi JA, Clarkson PM, White CM, et al. Relationships between physical activity and muscular strength among healthy adults across the lifespan. SpringerPlus. 2015;4:557.

    Article  PubMed  PubMed Central  Google Scholar 

  45. Villareal DT, Banks M, Siener C, Sinacore DR, Klein S. Physical frailty and body composition in obese elderly men and women. Obes Res. 2004;12:913–20.

    Article  PubMed  Google Scholar 

  46. Kowalk DL, Duncan JA, Vaughan CL. Abduction-adduction moments at the knee during stair ascent and descent. J Biomech. 1996;29:383–8.

    Article  CAS  PubMed  Google Scholar 

  47. Hortobágyi T, Mizelle C, Beam S, DeVita P. Old adults perform activities of daily living near their maximal capabilities. J Gerontol Ser A: Biol Sci Med Sci. 2003;58:M453–60.

    Article  Google Scholar 

  48. Startzell JK, Owens DA, Mulfinger LM, Cavanagh PR. Stair negotiation in older people: a review. J Am Geriatr Soc. 2000;48:567–80.

    Article  CAS  PubMed  Google Scholar 

  49. Pai Y-C, Rogers M. Speed variation and resultant joint torques during sit-to-stand. Arch Phys Med Rehabil. 1991;72:881–5.

    Article  CAS  PubMed  Google Scholar 

  50. Hughes VA, Frontera WR, Wood M, Evans WJ, Dallal GE, Roubenoff R, et al. Longitudinal muscle strength changes in older adults: influence of muscle mass, physical activity, and health. J Gerontol Ser A: Biol Sci Med Sci. 2001;56:B209–17.

    Article  CAS  Google Scholar 

  51. Maffiuletti NA, Jubeau M, Munzinger U, Bizzini M, Agosti F, De Col A, et al. Differences in quadriceps muscle strength and fatigue between lean and obese subjects. Eur J Appl Physiol. 2007;101:51–9.

    Article  PubMed  Google Scholar 

  52. Han L, Yang F. Strength or power, which is more important to prevent slip-related falls? Hum Mov Sci. 2015;44:192–200.

    Article  PubMed  Google Scholar 

  53. McGregor RA, Cameron-Smith D, Poppitt SD. It is not just muscle mass: a review of muscle quality, composition and metabolism during ageing as determinants of muscle function and mobility in later life. Longev Healthspan. 2014;3:9.

    Article  PubMed  PubMed Central  Google Scholar 

  54. Poggiogalle E, Lubrano C, Gnessi L, Mariani S, Di Martino M, Catalano C, et al. The decline in muscle strength and muscle quality in relation to metabolic derangements in adult women with obesity. Clin Nutr. 2019;38:2430–5.

    Article  PubMed  Google Scholar 

  55. Barbat-Artigas S, Filion M-E, Plouffe S, Aubertin-Leheudre M. Muscle quality as a potential explanation of the metabolically healthy but obese and sarcopenic obese paradoxes. Metabol Syndr Relat Disord. 2012;10:117–22.

    Article  Google Scholar 

  56. Hulens M, Vansant G, Lysens R, Claessens A, Muls E, Brumagne S. Study of differences in peripheral muscle strength of lean versus obese women: an allometric approach. Int J Obes. 2001;25:676–81.

    Article  CAS  Google Scholar 

  57. Erlandson M, Lorbergs A, Mathur S, Cheung A. Muscle analysis using pQCT, DXA and MRI. Eur J Radiol. 2016;85:1505–11.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors are grateful to all the participants.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Silvia Pogliaghi.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Muollo, V., Rossi, A.P., Zignoli, A. et al. Full characterisation of knee extensors’ function in ageing: effect of sex and obesity. Int J Obes 45, 895–905 (2021). https://doi.org/10.1038/s41366-021-00755-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41366-021-00755-z

This article is cited by

Search

Quick links