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Effects of post-fracture non-weight-bearing immobilization on muscle atrophy, intramuscular and intermuscular adipose tissues in the thigh and calf

Skeletal Radiology volume 47, pages 1541–1549 (2018)Cite this article

Abstract

Objective

Disuse and/or a non-weight-bearing condition changes muscle composition, with decreased skeletal muscle tissue and increased fat within (intramuscular adipose tissue, IntraMAT) and between (intermuscular adipose tissue, InterMAT) given muscles. Excessive adipose tissue contributes to dysfunctional and metabolically impaired muscle. How these adipose tissues change during orthopedic treatment (e.g., cast immobilization, daily use of crutches) is not well documented. This study aimed to quantify changes in IntraMAT, InterMAT, and thigh and calf muscle tissue during orthopedic treatment.

Materials and methods

We studied 8 patients with fifth metatarsal bone or fibular fractures. The ankle joint involved underwent plaster casting for approximately 4 weeks, with crutches used during that time. Axial T1-weighted MRI at the mid-thigh and a 30% proximal site at the calf were obtained to measure IntraMAT and InterMAT cross-sectional areas (CSAs) and skeletal muscle tissue CSA before treatment and 4 weeks afterward.

Results

Thigh and calf muscle tissue CSAs were significantly decreased from before to after treatment: thigh, 85.8 ± 7.6 to 77.1 ± 7.3 cm2; calf, 53.3 ± 5.5 to 48.9 ± 5.0 cm2 (p < 0.05). None of the IntraMAT or InterMAT changes was statistically significant. There was a relation between the percentage change of thigh IntraMAT CSA and muscle tissue CSA (rs = −0.86, p < 0.01).

Conclusions

The 4 weeks of treatment primarily induced skeletal muscle atrophy with less of an effect on IntraMAT or InterMAT. There is a risk of increasing IntraMAT relatively by decreasing skeletal muscle tissue size during orthopedic treatment.

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References

  1. Shaffer MA, Okereke E, Esterhai JL Jr, Elliott MA, Walker GA, Yim SH, et al. Effects of immobilization on plantar-flexion torque, fatigue resistance, and functional ability following an ankle fracture. Phys Ther. 2000;80(8):769–80.

    CAS  PubMed  Google Scholar 

  2. Stevens JE, Walter GA, Okereke E, Scarborough MT, Esterhai JL, George SZ, et al. Muscle adaptations with immobilization and rehabilitation after ankle fracture. Med Sci Sports Exerc. 2004;36(10):1695–701.

    Article  PubMed  Google Scholar 

  3. Berg HE, Dudley GA, Haggmark T, Ohlsen H, Tesch PA. Effects of lower limb unloading on skeletal muscle mass and function in humans. J Appl Physiol. 1991;70(4):1882–5.

    CAS  Article  PubMed  Google Scholar 

  4. Hather BM, Adams GR, Tesch PA, Dudley GA. Skeletal muscle responses to lower limb suspension in humans. J Appl Physiol. 1992;72(4):1493–8.

    CAS  Article  PubMed  Google Scholar 

  5. Schulze K, Gallagher P, Trappe S. Resistance training preserves skeletal muscle function during unloading in humans. Med Sci Sports Exerc. 2002;34(2):303–13.

    Article  PubMed  Google Scholar 

  6. Akima H, Hotta N, Sato K, Ishida K, Koike T, Katayama K. Cycle ergometer exercise to counteract muscle atrophy during unilateral lower limb suspension. Aviat Space Environ Med. 2009;80(7):652–6.

    Article  PubMed  Google Scholar 

  7. Heath GW, Gavin JR 3rd, Hinderliter JM, Hagberg JM, Bloomfield SA, Holloszy JO. Effects of exercise and lack of exercise on glucose tolerance and insulin sensitivity. J Appl Physiol. 1983;55(2):512–7.

    CAS  Article  PubMed  Google Scholar 

  8. Stein TP, Wade CE. Metabolic consequences of muscle disuse atrophy. J Nutr. 2005;135(7):1824S–8S.

    CAS  Article  PubMed  Google Scholar 

  9. Ryan AS, Dobrovolny CL, Smith GV, Silver KH, Macko RF. Hemiparetic muscle atrophy and increased intramuscular fat in stroke patients. Arch Phys Med Rehabil. 2002;83(12):1703–7.

    Article  PubMed  Google Scholar 

  10. Gorgey AS, Dudley GA. Skeletal muscle atrophy and increased intramuscular fat after incomplete spinal cord injury. Spinal Cord. 2007;45(4):304–9.

    CAS  Article  PubMed  Google Scholar 

  11. Ramsay JW, Barrance PJ, Buchanan TS, Higginson JS. Paretic muscle atrophy and non-contractile tissue content in individual muscles of the post-stroke lower extremity. J Biomech. 2011;44(16):2741–6.

    Article  PubMed  PubMed Central  Google Scholar 

  12. 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(6):2157–65.

    CAS  Article  PubMed  Google Scholar 

  13. Ruan XY, Gallagher D, Harris T, Albu J, Heymsfield S, Kuznia P, et al. Estimating whole body intermuscular adipose tissue from single cross-sectional magnetic resonance images. J Appl Physiol. 2007;102(2):748–54.

    Article  PubMed  Google Scholar 

  14. Marcus RL, Addison O, Dibble LE, Foreman KB, Morrell G, Lastayo P. Intramuscular adipose tissue, sarcopenia, and mobility function in older individuals. J Aging Res. 2012;2012:629637.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Hausman GJ, Basu U, Du M, Fernyhough-Culver M, Dodson MV. Intermuscular and intramuscular adipose tissues: bad vs. good adipose tissues. Adipocytes. 2014;3(4):242–55.

    CAS  Article  Google Scholar 

  16. Hilton TN, Tuttle LJ, Bohnert KL, Mueller MJ, Sinacore DR. Excessive adipose tissue infiltration in skeletal muscle in individuals with obesity, diabetes mellitus, and peripheral neuropathy: association with performance and function. Phys Ther. 2008;88(11):1336–44.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Goodpaster BH, Thaete FL, Simoneau JA, Kelley DE. Subcutaneous abdominal fat and thigh muscle composition predict insulin sensitivity independently of visceral fat. Diabetes. 1997;46(10):1579–85.

    CAS  Article  PubMed  Google Scholar 

  18. Elder CP, Apple DF, Bickel CS, Meyer RA, Dudley GA. Intramuscular fat and glucose tolerance after spinal cord injury—a cross-sectional study. Spinal Cord. 2004;42(12):711–6.

    CAS  Article  PubMed  Google Scholar 

  19. Akima H, Yoshiko A, Hioki M, Kanehira N, Shimaoka K, Koike T, et al. Skeletal muscle size is a major predictor of intramuscular fat content regardless of age. Eur J Appl Physiol. 2015;115(8):1627–35.

    CAS  Article  PubMed  Google Scholar 

  20. Yoshiko A, Hioki M, Kanehira N, Shimaoka K, Koike T, Sakakibara H, et al. Three-dimensional comparison of intramuscular fat content between young and old adults. BMC Med Imaging. 2017;17(1):12.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Sled JG, Zijdenbos AP, Evans ACA. Nonparametric method for automatic correction of intensity nonuniformity in MRI data. IEEE Trans Med Imaging. 1998;17(1):87–97.

    CAS  Article  PubMed  Google Scholar 

  22. Sezgin M, Sankur B. Survey over image thresholding techniques and quantitative performance evaluation. J Electron Imaging. 2004;13(1):146–65.

    Article  Google Scholar 

  23. Cook SB, Brown KA, Deruisseau K, Kanaley JA, Ploutz-Snyder LL. Skeletal muscle adaptations following blood flow-restricted training during 30 days of muscular unloading. J Appl Physiol. 2010;109(2):341–9.

    Article  PubMed  Google Scholar 

  24. Prado-Medeiros CL, Silva MP, Lessi GC, Alves MZ, Tannus A, Lindquist AR, et al. Muscle atrophy and functional deficits of knee extensors and flexors in people with chronic stroke. Phys Ther. 2012;92(3):429–39.

    Article  PubMed  Google Scholar 

  25. Dirks ML, Wall BT, Snijders T, Ottenbros CL, Verdijk LB, van Loon LJ. Neuromuscular electrical stimulation prevents muscle disuse atrophy during leg immobilization in humans. Acta Physiol. 2014;210(3):628–41.

    CAS  Article  Google Scholar 

  26. Boettcher M, Machann J, Stefan N, Thamer C, Haring HU, Claussen CD, et al. Intermuscular adipose tissue (IMAT): association with other adipose tissue compartments and insulin sensitivity. J Magn Reson Imaging. 2009;29(6):1340–5.

    Article  PubMed  Google Scholar 

  27. Manini TM, Clark BC, Nalls MA, Goodpaster BH, Ploutz-Snyder LL, Harris TB. Reduced physical activity increases intermuscular adipose tissue in healthy young adults. Am J Clin Nutr. 2007;85(2):377–84.

    CAS  Article  PubMed  Google Scholar 

  28. Ryan AS, Buscemi A, Forrester L, Hafer-Macko CE, Atrophy IFM. Intramuscular fat in specific muscles of the thigh: associated weakness and hyperinsulinemia in stroke survivors. Neurorehabil Neural Repair. 2011;25(9):865–72.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Addison O, Marcus RL, Lastayo PC, Ryan AS. Intermuscular fat: a review of the consequences and causes. Int J Endocrinol. 2014;2014:309570.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  30. Akima H, Kubo K, Imai M, Kanehisa H, Suzuki Y, Gunji A, et al. Inactivity and muscle: effect of resistance training during bed rest on muscle size in the lower limb. Acta Physiol Scand. 2001;172(4):269–78.

    CAS  Article  PubMed  Google Scholar 

  31. Akima H, Ushiyama J, Kubo J, Fukuoka H, Kanehisa H, Fukunaga T. Effect of unloading on muscle volume with and without resistance training. Acta Astronaut. 2007;60(8–9):728–36.

    Article  Google Scholar 

  32. Vandenborne K, Elliott MA, Walter GA, Abdus S, Okereke E, Shaffer M, et al. Longitudinal study of skeletal muscle adaptations during immobilization and rehabilitation. Muscle Nerve. 1998;21(8):1006–12.

    CAS  Article  PubMed  Google Scholar 

  33. Grosset J-F, Onambele-Pearson G. Effect of foot and ankle immobilization on leg and thigh muscles’ volume and morphology: a case study using magnetic resonance imaging. Anat Rec. 2008;291(12):1673–83.

    Article  Google Scholar 

  34. Goodpaster BH, Theriault R, Watkins SC, Kelley DE. Intramuscular lipid content is increased in obesity and decreased by weight loss. Metabolism. 2000;49(4):467–72.

    CAS  Article  PubMed  Google Scholar 

  35. De Boer MD, Maganaris CN, Seynnes OR, Rennie MJ, Narici MV. Time course of muscular, neural and tendinous adaptations to 23 day unilateral lower-limb suspension in young men. J Physiol. 2007;583(3):1079–91.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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Acknowledgements

The authors gratefully thank the volunteers for their participation and the staff of the Department of Radiology in Akita Hospital.

Funding

This research did not receive any specific grants from funding agencies in the public, commercial, or not-for-profit sectors.

Author information

Affiliations

  1. Graduate School of Medicine, Nagoya University, Nagoya, Japan

    Akito Yoshiko, Koun Yamauchi, Koji Ishida, Teruhiko Koike & Yoshiharu Oshida

  2. Department of Orthopedic Surgery, Akita Hospital, Chiryu, Japan

    Koun Yamauchi & Takayuki Kato

  3. Research Center of Health, Physical Fitness & Sports, Nagoya University, Nagoya, Japan

    Koji Ishida, Teruhiko Koike, Yoshiharu Oshida & Hiroshi Akima

  4. Graduate School of Education and Human Development, Nagoya University, Nagoya, Japan

    Hiroshi Akima

Authors
  1. Akito Yoshiko
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  2. Koun Yamauchi
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  3. Takayuki Kato
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Correspondence to Akito Yoshiko.

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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Declaration of Helsinki and its later amendments or comparable ethical standards.

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Yoshiko, A., Yamauchi, K., Kato, T. et al. Effects of post-fracture non-weight-bearing immobilization on muscle atrophy, intramuscular and intermuscular adipose tissues in the thigh and calf. Skeletal Radiol 47, 1541–1549 (2018). https://doi.org/10.1007/s00256-018-2985-6

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  • DOI: https://doi.org/10.1007/s00256-018-2985-6

Keywords

  • Cast immobilization
  • Non-weight-bearing
  • Muscle atrophy
  • Intramuscular adipose tissue
  • Intermuscular adipose tissue