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Skeletal muscle size is a major predictor of intramuscular fat content regardless of age

European Journal of Applied Physiology volume 115, pages 1627–1635 (2015)Cite this article

Abstract

Purpose

Skeletal muscles of older individuals have a larger amount of intramuscular adipose tissue (IntraMAT) than those of younger individuals. It is not understood how aging affects the IntraMAT content of individual muscles of the thigh. We assessed the relationship between IntraMAT content and skeletal muscle cross-sectional area (CSA), subcutaneous adipose tissue CSA, biochemical blood profiles, and physical activity.

Methods

Fifteen older (70.7 ± 3.8 years) and 15 younger (20.9 ± 0.3 years) men and women participated in this study. Magnetic resonance imaging of the right thigh was taken to measure IntraMAT content and skeletal muscle CSA for the quadriceps femoris (QF), hamstrings (HM), adductor (AD) muscle groups and subcutaneous adipose tissue CSA of the thigh. Fasting blood samples were collected to measure plasma lipids, adiponectin, and HbA1c levels.

Results

IntraMAT content in QF, HM, and AD for the Older group was significantly higher than in the Younger group. However, skeletal muscle CSA normalized by body weight (skeletal muscle CSA/bw) in the QF (P < 0.001) and total thigh (P < 0.01) were significantly lower in the Older group compared with the Younger group.There were no significant differences in HM and AD. Stepwise regression analysis with IntraMAT content as a dependent variable revealed that skeletal muscle CSA/bw of the thigh was the only predictive variable for IntraMAT content in Older and Younger groups.

Conclusion

These results suggest that skeletal muscle size could be a major determinant of IntraMAT content regardless of age.

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Abbreviations

AD:

Hip adductor

AL:

Adductor longus

AM:

Adductor magnus

ANOVA:

Analysis of variance

BFl:

Biceps femoris-long head

CSA:

Cross-sectional area

FFA:

Free fatty acids

Gr:

Gracilis

HDL-C:

High-density lipoprotein-cholesterol

HM:

Hamstrings

IntraMAT:

Intramuscular adipose tissue

LDL-C:

Low-density lipoprotein-cholesterol

MRI:

Magnetic resonance imaging

QF:

Quadriceps femoris

RF:

Rectus femoris

ROI:

Region-of-interest

Sar:

Sartorius

SM:

Semimembranosus

ST:

Semitendinosus

TG:

Triglycerides

Total-C:

Total cholesterol

VI:

Vastus intermedius

VL:

Vastus lateralis

VM:

Vastus medialis

References

  • Akima H, Kano Y, Enomoto Y, Ishizu M, Okada M, Oishi Y, Katsuta S, Kuno S (2001) Muscle function in 164 men and women aged 20–84 yrs. Med Sci Sports Exerc 33:220–226

    CAS  PubMed  Article  Google Scholar 

  • Akima H, Lott D, Senesac C, Deol J, Gemain S, Arpan I, Bendixen R, Sweeney HL, Walter G, Vandenborne K (2012) Relationships of thigh muscle contractile and non-contractile tissue with function, strength, and age in boys with Duchenne muscular dystrophy. Neuromuscul Disord 22:16–25

    PubMed Central  PubMed  Article  Google Scholar 

  • Ayabe M, Kumahara H, Morimura K, Sakane N, Ishii K, Tanaka H (2013) Accumulation of short bouts of non-exercise daily physical activity is associated with lower visceral fat in Japanese female adults. Int J Sports Med 34:62–67

    CAS  PubMed  Google Scholar 

  • Boettcher M, Machann J, Stefan N, Thamer C, Haring H-U, Claussen CD, Fritsche A, Schick F (2009) Intermuscular adipose tissue (IMAT): association with other adipose tissue compartments and insulin sensitivity. J Magn Reson Imaging 29:1340–1345

    PubMed  Article  Google Scholar 

  • Crane JD, Devries MC, Safdar A, Hamadeh MJ, Tarnopolsky MA (2010) The effect of aging on human skeletal muscle mitochondrial and intramyocellular lipid ultrastructure. J Gerontol A Bio Sci Med Sci 65A:119–128

    Article  Google Scholar 

  • DeNino WF, Ades PA, Tchernof A, Sites CK, Dionne IJ, Poehlman ET, Toth MJ (2001) Contribution of abdominal adiposity to age-related differences in insulin sensitivity and plasma lipids in healthy nonobese women. Diabetes Care 24:925–932

    CAS  PubMed  Article  Google Scholar 

  • Fukunaga T, Miyatani M, Tachi M, Kouzaki M, Kawakami Y, Kanehisa H (2001) Muscle volume is a major determinant of joint torque in humans. Acta Physiol Scand 172:249–255

    CAS  PubMed  Article  Google Scholar 

  • Gallagher D, Kuznia P, Heshka S, Aibu H, Heymsfield SB, Goodpaster B, Visse M, Harris TB (2005) Adipose tissue in muscle: a novel depot similar in size to visceral adipose tissue. Am J Clin Nutrit 81:903–910

    CAS  PubMed Central  PubMed  Google Scholar 

  • Goodpaster BH, Thaete FL, Kelley DE (2000) Thigh adipose tissue distribution is associated with insulin resistance in obesity and in type 2 diabetes mellitus. Am J Clin Nutrit 71:885–892

    CAS  PubMed  Google Scholar 

  • Goodpaster BH, Krishnaswami S, Resnick DE, Haggerty C, Harris TB, Schwartz AV, Kritchevsky S, Newman AB (2003) Assoication between regional adipose tissue distribution and both type 2 diabetes and impaired glucose tolerance in elderly men and women. Diabetes Care 26:372–379

    PubMed  Article  Google Scholar 

  • Janssen I, Fortier A, Hudson R, Ross RR (2002) Effects of an energy-restrictive diet with or without exercise on abdominal fat, intermuscular fat, and metabolic risk factors in obese women. Diabetes Care 25:431–438

    PubMed  Article  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Kumahara H, Schutz Y, Ayabe M, Yoshioka M, Yoshitake Y, Shindo M, Ishii K, Tanaka H (2004) The use of uniaxial accelerometer for the assessment of physical-activity-related energy expenditure: a validation study against whole-body indirect calorimetry. Br J Nutr 91:235–243

    CAS  PubMed  Article  Google Scholar 

  • Lihn AS, Pedersen SB, Richelsen B (2005) Adiponectin: action, regulation and association to insulin sensitivity. Obes Rev 6:13–21

    CAS  PubMed  Article  Google Scholar 

  • Manini TM, Clark BC, Goodpaster BH, Ploutz-Snyder LL, Harris TB (2007) Reduced physical activity increases intermuscular adipose tissue in health young adults. Am J Nutrit 85:377–384

    CAS  Google Scholar 

  • Marcus RL, Addison O, Dibble LE, Foreman KB, Morrell G, LaStayo P (2012) Intramuscular adipose tissue, sarcopenia, and mobility function in older individuals. J Aging Res 2012:1–6

    Article  Google Scholar 

  • Maughan RJ, Watson JS, Weir J (1983) Strength and cross-sectional area of human skeletal muscle. J Physiol (London) 338:37–49

    CAS  Article  Google Scholar 

  • Overend TJ, Cunningham DA, Kramer JF, Lefcoe MS, Paterson DH (1992) Knee extensor and knee flexor stremgth:cross-sectional area ratios in young and elderly men. J Gerontol A Biol Sci Med Sci 47:M204–M210

    CAS  Article  Google Scholar 

  • Popadic Gacesa JZ, Dusko KB, Grujic NG (2011) Triceps brachii strength and regional body composition changes after detraining quantified by MRI. J Magn Reson Imaging 33:1114–1120

    PubMed  Article  Google Scholar 

  • Ramsey JW, Barrance PJ, Buchanan TS, Higginson JS (2011) Paretic muscle atrophy and non-contractile tissue content in individual muscles of the post-stroke lower limb extremity. J Biomech 44:2741–2746

    Article  Google Scholar 

  • Rossi A, Zoico E, Goodpaster B, Sepe A, Di Francesco V, Fantin F, Pizzini F, Corzato F, Vitali A, Micciolo R, Harris TB, Cinti S, Zamboni M (2010) Quantification of intermuscular adipose tissue in the erector spinae muscle by MRI: agreement with histology evaluation. Obesity 18:2379–2384

    PubMed  Article  Google Scholar 

  • Ryan AS, Nicklas BJ (1999) Age-related changes in fat deposition in mid-thigh muscle in women: relationships with metabolic cardiovascular disease risk factors. Int J Obes 23:126–132

    CAS  Article  Google Scholar 

  • Ryan AS, Nicklas BJ, Berman DM (2002) Racial differences in insulin resistance and mid-thigh fat deposition in postmenopausal women. Obes Res 10:336–344

    PubMed  Article  Google Scholar 

  • Ryan AS, Buscemi A, Forrester L, Hafer-Macko CE, Ivey FM (2011) Atrophy and intramuscular fat in specific muscles of the thigh: associated weakness and hyperinsulinemia in stroke survivors. Neurorehabil Neural Repair 25:865–872

    PubMed Central  PubMed  Article  Google Scholar 

  • Schwenzer NF, Martirosian P, Machann J, Schraml C, Steidle G, Claussen CD, Schick F (2009) Aging effects on human calf muscle properties assessed by MRI at 3 tesla. J Magn Reson Imaging 29:1346–1354

    PubMed  Article  Google Scholar 

  • Sezgin M, Sankur B (2004) Survey over image thresholding techniques and quantitative performance evaluation. J Electron Imaging 13:146–165

    Article  Google Scholar 

  • Sled JG, Zijdenbos AP (1998) A nonparametric method for automatic correction of intensity nonuniformity in MRI data. IEEE Trans Med Imaging 17:87–97

    CAS  PubMed  Article  Google Scholar 

  • Song MY, Ruts E, Kim J, Janumala I, Heymsfield S, Gallagher D (2001) Sarcopenia and increased adipose tissue infiltration of muscle in elderly African American women. Am J Clin Nutrit 79:874–880

    Google Scholar 

  • Taaffe DR, Henwood TR, Nalls MA, Walker DG, Lang TF, Harris TB (2009) Alterations in muscle attenuation following detraining and retraining in resistance-trained older adults. Gerontology 55:217–223

    PubMed Central  PubMed  Article  Google Scholar 

  • Tuttle LJ, Sinacore DR, Mueller MJ (2012) Intermuscular adipose tissue is muscle specific and associated with poor functional performance. J Aging Res 2012:1–7

    Article  Google Scholar 

  • Visser M, Kritchevsky SB, Goodpaster BH, Newman AB, Nevitt M, Stamm E, Harris TB (2002) Leg muscle mass and composition in relation to lower extremity performance in men and women aged 70–79: the health, aging and body composition study. J Am Geriatr Soc 50:897–904

    PubMed  Article  Google Scholar 

  • Zoico E, Rossi A, Di Francesco V, Sepe A, Olioso D, Pizzini F, Fantin F, Bosello O, Cominacini L, Harris TB, Zamboni M (2010) Adipose tissue infiltration in skeletal muscle of healthy elderly men: relationships with body composition, insulin resistance, and inflammation at the systemic and tissue level. J Gerontol A Biol Sci Med Sci 65A:295–299

    PubMed Central  Article  Google Scholar 

Download references

Acknowledgments

The authors gratefully thank the volunteers for participation as well as Drs Haruo Isoda and Atsushi Fukuyama and Radiologic technologist Mr. Akira Ishizuka, Graduate School of Medicine, Nagoya University. This study was supported in part by a Grant-in-Aid for challenging Exploratory Research from the Ministry of Education, Culture, Sports and Science and Technology Grant (#23650432) to HA.

Conflict of interest

The authors declare no conflict of interest.

Author information

Affiliations

  1. Research Center of Health, Physical Fitness and Sports, Nagoya University, Furo, Chikusa, Nagoya, 4648601, Aichi, Japan

    Hiroshi Akima, Teruhiko Koike & Yoshiharu Oshida

  2. Graduate School of Education and Human Development, Nagoya University, Furo, Chikusa, Nagoya, 4648601, Aichi, Japan

    Hiroshi Akima

  3. Graduate School of Medicine, Nagoya University, Tsurumai, Showa, Nagoya, 4668550, Aichi, Japan

    Akito Yoshiko, Maya Hioki, Teruhiko Koike & Yoshiharu Oshida

  4. Graduate School of Medicine, Nagoya University, 1-1-20 Daiko-minami, Higashi, Nagoya, 4618673, Aichi, Japan

    Hisataka Sakakibara

  5. Faculty of Human Wellness and Nutrition, Tokaigakuen University, Nishinohora 21-233, Fukutani, Miyoshi, 4700207, Aichi, Japan

    Nana Kanehira

  6. Faculty of Human Wellness, Tokaigakuen University, Nishinohora 21-233, Fukutani, Miyoshi, 4700207, Aichi, Japan

    Kiyoshi Shimaoka

Authors
  1. Hiroshi Akima
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  2. Akito Yoshiko
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  3. Maya Hioki
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  4. Nana Kanehira
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  5. Kiyoshi Shimaoka
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  6. Teruhiko Koike
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  7. Hisataka Sakakibara
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  8. Yoshiharu Oshida
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Corresponding author

Correspondence to Hiroshi Akima.

Additional information

Communicated by William J. Kraemer.

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Akima, H., Yoshiko, A., Hioki, M. et al. Skeletal muscle size is a major predictor of intramuscular fat content regardless of age. Eur J Appl Physiol 115, 1627–1635 (2015). https://doi.org/10.1007/s00421-015-3148-2

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  • DOI: https://doi.org/10.1007/s00421-015-3148-2

Keywords

  • Skeletal muscle
  • Sarcopenia
  • Magnetic resonance imaging
  • Blood lipids