Skip to main content

Advertisement

Log in

Association of skeletal muscle oxidative capacity with muscle function, sarcopenia-related exercise performance, and intramuscular adipose tissue in older adults

  • ORIGINAL ARTICLE
  • Published:
GeroScience Aims and scope Submit manuscript

Abstract

Muscle function and exercise performance measures, such as muscle endurance capacity, maximal strength, chair stand score, gait speed, and Timed Up and Go score, are evaluated to diagnose sarcopenia and frailty in older individuals. Furthermore, intramuscular adipose tissue (IntraMAT) content increases with age. Skeletal muscle oxidative capacity determines muscle metabolism and maintains muscle performance. This study aimed to investigate the association of skeletal muscle oxidative capacity with muscle function, exercise performance, and IntraMAT content in older individuals. Thirteen older men and women participated in this study. Skeletal muscle oxidative capacity was assessed by the recovery speed of muscle oxygen saturation after exercise using near-infrared spectroscopy from the medial gastrocnemius. We assessed two muscle functions, peak torque and time to task failure, and four sarcopenia-related exercise performances: handgrip strength, gait speed, 30-s chair stand, and Timed Up and Go. The IntraMAT content was measured using axial magnetic resonance imaging. The results showed a relationship between skeletal muscle oxidative capacity and gait speed but not with muscle functions and other exercise performance measures. Skeletal muscle oxidative capacity was not related to IntraMAT content. Skeletal muscle oxidative capacity, which may be indicative of the capacity of muscle energy production in the mitochondria, is related to locomotive functions but not to other functional parameters or skeletal fat infiltration.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data availability

Data will be provided by the corresponding author upon request.

References

  1. 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 

  2. St-Jean-Pelletier F, Pion CH, Leduc-Gaudet JP, Sgarioto N, Zovile I, Barbat-Artigas S, et al. The impact of ageing, physical activity, and pre-frailty on skeletal muscle phenotype, mitochondrial content, and intramyocellular lipids in men. J Cachexia Sarcopenia Muscle. 2016;8:213–28.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Petersen KF, Befroy D, Dufour S, Dziura J, Ariyan C, Rothman DL, et al. Mitochondrial dysfunction in the elderly: possible role in insulin resistance. Science. 2003;300:1140–2.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Coen PM, Jubrias SA, Distefano G, Amati F, Mackey DC, Glynn NW, et al. Skeletal muscle mitochondrial energetics are associated with maximal aerobic capacity and walking speed in older adults. J Gerontol A Biol Sci Med Sci. 2013;68:447–55.

    Article  PubMed  Google Scholar 

  5. Santanasto AJ, Glynn NW, Jubrias SA, Conley KE, Boudreau RM, Amati F, et al. Skeletal muscle mitochondrial function and fatigability in older adults. J Gerontol A Biol Sci Med Sci. 2015;70:1379–85.

    Article  CAS  PubMed  Google Scholar 

  6. Brizendine JT, Ryan TE, Larson RD, McCully KK. Skeletal muscle metabolism in endurance athletes with near-infrared spectroscopy. Med Sci Sports Exerc. 2013;45:869–75.

    Article  CAS  PubMed  Google Scholar 

  7. Hunter SK, Griffith EE, Schlachter KM, Kufahl TD. Sex differences in time to task failure and blood flow for an intermittent isometric fatiguing contraction. Muscle Nerve. 2009;39:42–53.

    Article  PubMed  Google Scholar 

  8. Kent-Braun JA. Skeletal muscle fatigue in old age: whose advantage? Exerc Sport Sci Rev. 2009;37:3–9.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Mota JA, Stock MS. Rectus femoris echo intensity correlates with muscle strength, but not endurance, in younger and older men. Ultrasound Med Biol. 2017;43:1651–7.

    Article  PubMed  Google Scholar 

  10. Zane AC, Reiter DA, Shardell M, Cameron D, Simonsick EM, Fishbein KW, et al. Muscle strength mediates the relationship between mitochondrial energetics and walking performance. Aging Cell. 2017;16:461–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Newman AB, Kupelian V, Visser M, Simonsick EM, Goodpaster BH, Kritchevsky SB, et al. 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. 2006;61:72–7.

    Article  PubMed  Google Scholar 

  12. Moro C, Bajpeyi S, Smith SR. Determinants of intramyocellular triglyceride turnover: implications for insulin sensitivity. Am J Physiol Endocrinol Metab. 2008;294:E203–13.

    Article  CAS  PubMed  Google Scholar 

  13. Ryan AS, Nicklas BJ. Age-related changes in fat deposition in mid-thigh muscle in women: relationships with metabolic cardiovascular disease risk factors. Int J Obes Relat Metab Disord. 1999;23:126–32.

    Article  CAS  PubMed  Google Scholar 

  14. Goodpaster BH, Carlson CL, Visser M, Kelley DE, Scherzinger A, Harris TB, et al. Attenuation of skeletal muscle and strength in the elderly: the health ABC study. J Appl Physiol. 2001;90:2157–65.

    Article  CAS  PubMed  Google Scholar 

  15. Goodpaster BH, Thaete FL, Kelley DE. Thigh adipose tissue distribution is associated with insulin resistance in obesity and in type 2 diabetes mellitus. Am J Clin Nutr. 2000;71:885–92.

    Article  CAS  PubMed  Google Scholar 

  16. Choi SJ, Files DC, Zhang T, Wang ZM, Messi ML, Gregory H, et al. Intramyocellular lipid and impaired myofiber contraction in normal weight and obese older adults. J Gerontol A Biol Sci Med Sci. 2016;71:557–64.

    Article  PubMed  Google Scholar 

  17. Lanza IR, Bhagra S, Nair KS, Port JD. Measurement of human skeletal muscle oxidative capacity by 31P-MR spectroscopy: a cross-validation with in vitro measurements. J Magn Reson Imaging. 2011;34:1143–50.

    Article  PubMed  PubMed Central  Google Scholar 

  18. McCully KK, Fielding RA, Evans WJ, Leigh JS Jr, Posner JD. Relationships between in vivo and in vitro measurements of metabolism in young and old human calf muscles. J Appl Physiol. 1993;75:813–9.

    Article  CAS  PubMed  Google Scholar 

  19. Ryan TE, Brophy P, Lin CT, Hickner RC, Neufer PD. Assessment of in vivo skeletal muscle mitochondrial respiratory capacity in humans by near-infrared spectroscopy: a comparison with in situ measurements. J Physiol. 2014;592:3231–41.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Ryan TE, Southern WM, Reynolds MA, McCully KK. A cross-validation of near-infrared spectroscopy measurements of skeletal muscle oxidative capacity with phosphorus magnetic resonance spectroscopy. J Appl Physiol. 2013;115:1757–66.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Lagerwaard B, Nieuwenhuizen AG, de Boer VCJ, Keijer J. In vivo assessment of mitochondrial capacity using NIRS in locomotor muscles of young and elderly males with similar physical activity levels. Geroscience. 2020;42:299–310.

    Article  PubMed  Google Scholar 

  22. Niwayama M, Lin L, Shao J, Kudo N, Yamamoto K. Quantitative measurement of muscle hemoglobin oxygenation using near-infrared spectroscopy with correction for the influence of a subcutaneous fat layer. Rev Sci Instrument. 2000;71:4571–5.

    Article  CAS  Google Scholar 

  23. Jones CJ, Rikli RE, Beam WC. A 30-s chair-stand test as a measure of lower body strength in community-residing older adults. Res Q Exer Sport. 1999;70:113–9.

    Article  CAS  Google Scholar 

  24. Akima H, Hioki M, Yoshiko A, Koike T, Sakakibara H, Takahashi H, et al. Intramuscular adipose tissue determined by T1-weighted MRI at 3 T primarily reflects extramyocellular lipids. Magn Reson Imaging. 2016;34:397–403.

    Article  CAS  PubMed  Google Scholar 

  25. Kent-Braun JA, Ng AV, Young K. Skeletal muscle contractile and noncontractile components in young and older women and men. J Appl Physiol. 2000;88:662–8.

    Article  CAS  PubMed  Google Scholar 

  26. Sezgin M, Sankur B. Survey over image thresholding techniques and quantitative performance evaluation. J Electron Imaging. 2004;13:146–65.

    Article  Google Scholar 

  27. Chung S, Rosenberry R, Ryan TE, Munson M, Dombrowsky T, Park S, et al. Near-infrared spectroscopy detects age-related differences in skeletal muscle oxidative function: promising implications for geroscience. Phys Reports. 2018;6: e13588.

    Article  Google Scholar 

  28. Southern WM, Ryan TE, Kepple K, Murrow JR, Nilsson KR, McCully KK. Reduced skeletal muscle oxidative capacity and impaired training adaptations in heart failure. Phys Reports. 2015;3: e12353.

    Article  Google Scholar 

  29. Lagerwaard B, Keijer J, McCully KK, de Boer VCJ, Nieuwenhuizen AG. In vivo assessment of muscle mitochondrial function in healthy, young males in relation to parameters of aerobic fitness. Eur J Appl Physiol. 2019;119:1799–808.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Hunter SK, Yoon T, Farinella J, Griffith EE, Ng AV. Time to task failure and muscle activation vary with load type for a submaximal fatiguing contraction with the lower leg. J Appl Physiol. 2008;105:463–72.

    Article  PubMed  Google Scholar 

  31. Rudroff T, Justice JN, Holmes MR, Matthews SD, Enoka RM. Muscle activity and time to task failure differ with load compliance and target force for elbow flexor muscles. J Appl Physiol. 2011;110:125–36.

    Article  PubMed  Google Scholar 

  32. Senefeld J, Yoon T, Hunter SK. Age differences in dynamic fatigability and variability of arm and leg muscles: associations with physical function. Exp Gerontol. 2017;87:74–83.

    Article  PubMed  Google Scholar 

  33. Kunz HE, Port JD, Kaufman KR, Jatoi A, Hart CR, Gries KJ, et al. Skeletal muscle mitochondrial dysfunction and muscle and whole body functional deficits in cancer patients with weight loss. J Appl Physiol. 2022;132:388–401.

    Article  CAS  PubMed  Google Scholar 

  34. Frontera WR, Ochala J. Skeletal muscle: a brief review of structure and function. Calcif Tissue Int. 2015;96:183–95.

    Article  CAS  PubMed  Google Scholar 

  35. Porter C, Reidy PT, Bhattarai N, Sidossis LS, Rasmussen BB. Resistance exercise training alters mitochondrial function in human skeletal muscle. Med Sci Sports Exerc. 2015;47:1922–31.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Irving BA, Lanza IR, Henderson GC, Rao RR, Spiegelman BM, Nair KS. Combined training enhances skeletal muscle mitochondrial oxidative capacity independent of age. J Clin Endocriol Metab. 2015;100:1654–63.

    Article  CAS  Google Scholar 

  37. Shumway-Cook A, Brauer S, Woollacott M. Predicting the probability for falls in community-dwelling older adults using the Timed Up & Go Test. Phys Ther. 2000;80:896–903.

    Article  CAS  PubMed  Google Scholar 

  38. Ryan TE, Erickson ML, Verma A, Chavez J, Rivner MH, McCully KK. Skeletal muscle oxidative capacity in amyotrophic lateral sclerosis. Muscle Nerve. 2014;50:767–74.

    Article  CAS  PubMed  Google Scholar 

  39. Erickson ML, Ryan TE, Young H-J, McCully KK. Near-infrared assessments of skeletal muscle oxidative capacity in persons with spinal cord injury. Eur J Appl Physiol. 2013;113:2275–83.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Goodpaster BH, He J, Watkins S, Kelley DE. Skeletal muscle lipid content and insulin resistance: evidence for a paradox in endurance-trained athletes. J Clin Endocrinol Metab. 2001;86:5755–61.

    Article  CAS  PubMed  Google Scholar 

  41. Yoshiko A, Maeda H, Takahashi H, Koike T, Tanaka N, Akima H. Importance of skeletal muscle lipid levels for muscle function and physical function in older individuals. Appl Physiol Nutr Metab. 2022;47:649–58.

    Article  PubMed  Google Scholar 

  42. Gorgey AS, Dudley GA. Skeletal muscle atrophy and increased intramuscular fat after incomplete spinal cord injury. Spinal Cord. 2007;45:304–9.

    Article  CAS  PubMed  Google Scholar 

  43. Salvadego D, Domenis R, Lazzer S, Porcelli S, Rittweger J, Rizzo G, et al. Skeletal muscle oxidative function in vivo and ex vivo in athletes with marked hypertrophy from resistance training. J Appl Physiol. 2013;114:1527–35.

    Article  CAS  PubMed  Google Scholar 

  44. Berg OK, Kwon OS, Hureau TJ, Clifton HL, Thurston TS, Le Fur Y, et al. Skeletal muscle mitochondrial adaptations to maximal strength training in older adults. J Gerontol A Biol Sci Med Sci. 2020;75:2269–77.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Jubrias SA, Esselman PC, Price LB, Cress ME, Conley KE. Large energetic adaptations of elderly muscle to resistance and endurance training. J Appl Physiol. 2001;90:1663–70.

    Article  CAS  PubMed  Google Scholar 

  46. Hart CR, Layec G, Trinity JD, Liu X, Kim SE, Groot HJ, et al. Evidence of preserved oxidative capacity and oxygen delivery in the plantar flexor muscles with age. J Gerontol A Biol Sci Med Sci. 2015;70:1067–76.

    Article  CAS  PubMed  Google Scholar 

  47. Kemp GJ, Roberts N, Bimson WE, Bakran A, Harris PL, Gilling-Smith GL, et al. Mitochondrial function and oxygen supply in normal and in chronically ischemic muscle: a combined 31P magnetic resonance spectroscopy and near infrared spectroscopy study in vivo. J Vasc Surg. 2001;34:1103–10.

    Article  CAS  PubMed  Google Scholar 

  48. Southern WM, Ryan TE, Reynolds MA, McCully K. Reproducibility of near-infrared spectroscopy measurements of oxidative function and postexercise recovery kinetics in the medial gastrocnemius muscle. Appl Physiol Nutr Metab. 2014;39:521–9.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors thank all volunteers for their participation. The authors are also grateful to those who assisted with the MR data collection: Dr. Haruo Isoda and Mr. Akira Ishizuka (Brain & Mind Research Center, Nagoya University).

Funding

This work was supported by JSPS KAKENHI, Grant Number 20K19691, awarded to A.Y.

Author information

Authors and Affiliations

Authors

Contributions

Akito Yoshiko: conceptualization, data curation, formal analysis, investigation, methodology, writing—original draft preparation. Kana Shiozawa: data curation, writing, review and editing. Shiori Niwa: data curation, writing, reviewing, and editing. Hideyuki Takahashi: data curation, writing, reviewing, and editing. Teruhiko Koike: conceptualization, writing, reviewing, and editing. Kohei Watanabe: conceptualization, writing, review and editing. Keisho Katayama: conceptualization, methodology, writing, review and editing. Hiroshi Akima: conceptualization, methodology, writing, review and editing.

Corresponding author

Correspondence to Akito Yoshiko.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher's Note

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

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yoshiko, A., Shiozawa, K., Niwa, S. et al. Association of skeletal muscle oxidative capacity with muscle function, sarcopenia-related exercise performance, and intramuscular adipose tissue in older adults. GeroScience 46, 2715–2727 (2024). https://doi.org/10.1007/s11357-023-01043-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11357-023-01043-6

Keywords

Navigation