Ultrasonic assessment of exercise-induced change in skeletal muscle glycogen content

David C Nieman, R Andrew Shanely, Kevin A Zwetsloot, Mary Pat Meaney, Gerald E Farris, David C Nieman, R Andrew Shanely, Kevin A Zwetsloot, Mary Pat Meaney, Gerald E Farris

Abstract

Background: Ultrasound imaging is a valuable tool in exercise and sport science research, and has been used to visualize and track real-time movement of muscles and tendons, estimate hydration status in body tissues, and most recently, quantify skeletal muscle glycogen content. In this validation study, direct glycogen quantification from pre-and post-exercise muscle biopsy samples was compared with glycogen content estimates made through a portable, diagnostic high-frequency ultrasound and cloud-based software system (MuscleSound®, Denver, CO).

Methods: Well-trained cyclists (N = 20, age 38.4 ± 6.0 y, 351 ± 57.6 wattsmax) participated in a 75-km cycling time trial on their own bicycles using CompuTrainer Pro Model 8001 trainers (RacerMate, Seattle, WA). Muscle biopsy samples and ultrasound measurements were acquired pre- and post-exercise. Specific locations on the vastus lateralis were marked, and a trained technician used a 12 MHz linear transducer and a standard diagnostic high resolution GE LOGIQ-e ultrasound machine (GE Healthcare, Milwaukee, WI) to make three ultrasound measurements. Ultrasound images were pre-processed to isolate the muscle area under analysis, with the mean pixel intensity averaged from the three scans and scaled (0 to 100 scale) to create the glycogen score. Pre- and post-exercise muscle biopsy samples were acquired at the vastus lateralis location (2 cm apart) using the suction-modified percutaneous needle biopsy procedure, and analyzed for glycogen content.

Results: The 20 cyclists completed the 75-km cycling time trial in 168 ± 26.0 minutes at a power output of 193 ± 57.8 watts (54.2 ± 9.6% wattsmax). Muscle glycogen decreased 77.2 ± 17.4%, with an absolute change of 71.4 ± 23.1 mmol glycogen per kilogram of muscle. The MuscleSound® change score at the vastus lateralis site correlated highly with change in measured muscle glycogen content (R = 0.92, P < 0.001).

Conclusions: MuscleSound® change scores acquired from an average of three ultrasound scans at the vastus lateralis site correlated significantly with change in vastus lateralis muscle glycogen content. These data support the use of the MuscleSound® system for accurately and non-invasively estimating exercise-induced decreases in vastus lateralis skeletal muscle glycogen content.

Keywords: Cycling; Muscle biopsy; Skeletal muscle; Sonography; Vastus lateralis.

Figures

Figure 1
Figure 1
Ultrasonic scan from a subject with the rectangle area representing where images were segmented to isolate the muscle area under analysis using a center crop within the muscle section 25 mm from the top of the muscle sheath.
Figure 2
Figure 2
Pre-exercise muscle with high glycogen stores display darker pixel intensities.
Figure 3
Figure 3
Post-exercise muscle with lower glycogen stores display brighter pixel intensities.
Figure 4
Figure 4
The pixel intensity of the muscle fibers was measured to quantify the amount of glycogen stores within the region of interest. The mean pixel intensity was averaged from the three cropped and segmented scans, and scaled (0 to 100 scale) to create the glycogen score with MuscleSound® software.
Figure 5
Figure 5
Vastus lateralis muscle glycogen content data pre- and post-exercise, indicating a 77.2 ± 17.4% decrease and an absolute change of 71.4 ± 23.1 mmol glycogen per kilogram of muscle (P 

Figure 6

Correlation of the change in…

Figure 6

Correlation of the change in vastus lateralis MuscleSound® glycogen score with change in…

Figure 6
Correlation of the change in vastus lateralis MuscleSound® glycogen score with change in vastus lateralis muscle glycogen content (r = 0.92, P 

Figure 7

Correlation of pre-exercise vastus lateralis…

Figure 7

Correlation of pre-exercise vastus lateralis MuscleSound® scores and vastus lateralis muscle glycogen content…

Figure 7
Correlation of pre-exercise vastus lateralis MuscleSound® scores and vastus lateralis muscle glycogen content (r = 0.92, P 

Figure 8

Correlation of post-exercise vastus lateralis…

Figure 8

Correlation of post-exercise vastus lateralis MuscleSound® scores and vastus lateralis muscle glycogen content…

Figure 8
Correlation of post-exercise vastus lateralis MuscleSound® scores and vastus lateralis muscle glycogen content (r = 0.90, P 
All figures (8)
Similar articles
Cited by
References
    1. Conlee RK. Muscle glycogen and exercise endurance: a twenty-year perspective. Exerc Sport Sci Rev. 1987;15:1–28. doi: 10.1249/00003677-198700150-00004. - DOI - PubMed
    1. Nieman DC, Davis JM, Henson DA, Gross SJ, Dumke CL, Utter AC, et al. Muscle cytokine mRNA changes after 2.5 h of cycling: influence of carbohydrate. Med Sci Sports Exerc. 2005;37:1283–1290. doi: 10.1249/01.mss.0000175054.99588.b1. - DOI - PubMed
    1. Nieman DC, Davis JM, Henson DA, Walberg-Rankin J, Shute M, Dumke CL, et al. Carbohydrate ingestion influences skeletal muscle cytokine mRNA and plasma cytokine levels after a 3-h run. J Appl Physiol. 2003;94:1917–1925. doi: 10.1152/japplphysiol.01130.2002. - DOI - PubMed
    1. Avison MJ, Rothman DL, Nadel E, Shulman RG. Detection of human muscle glycogen by natural abundance 13C NMR. Proc Natl Acad Sci U S A. 1988;85:1634–1636. doi: 10.1073/pnas.85.5.1634. - DOI - PMC - PubMed
    1. Van Zijl PC, Jones CK, Ren J, Malloy CR, Sherry AD. MRI detection of glycogen in vivo by using chemical exchange saturation transfer imaging (glycoCEST) Proc Natl Acad Sci U S A. 2007;104:4359–4364. doi: 10.1073/pnas.0700281104. - DOI - PMC - PubMed
Show all 19 references
LinkOut - more resources
[x]
Cite
Copy Download .nbib
Format: AMA APA MLA NLM

NCBI Literature Resources

MeSH PMC Bookshelf Disclaimer

The PubMed wordmark and PubMed logo are registered trademarks of the U.S. Department of Health and Human Services (HHS). Unauthorized use of these marks is strictly prohibited.

Follow NCBI
Figure 6
Figure 6
Correlation of the change in vastus lateralis MuscleSound® glycogen score with change in vastus lateralis muscle glycogen content (r = 0.92, P 

Figure 7

Correlation of pre-exercise vastus lateralis…

Figure 7

Correlation of pre-exercise vastus lateralis MuscleSound® scores and vastus lateralis muscle glycogen content…

Figure 7
Correlation of pre-exercise vastus lateralis MuscleSound® scores and vastus lateralis muscle glycogen content (r = 0.92, P 

Figure 8

Correlation of post-exercise vastus lateralis…

Figure 8

Correlation of post-exercise vastus lateralis MuscleSound® scores and vastus lateralis muscle glycogen content…

Figure 8
Correlation of post-exercise vastus lateralis MuscleSound® scores and vastus lateralis muscle glycogen content (r = 0.90, P 
All figures (8)
Similar articles
Cited by
References
    1. Conlee RK. Muscle glycogen and exercise endurance: a twenty-year perspective. Exerc Sport Sci Rev. 1987;15:1–28. doi: 10.1249/00003677-198700150-00004. - DOI - PubMed
    1. Nieman DC, Davis JM, Henson DA, Gross SJ, Dumke CL, Utter AC, et al. Muscle cytokine mRNA changes after 2.5 h of cycling: influence of carbohydrate. Med Sci Sports Exerc. 2005;37:1283–1290. doi: 10.1249/01.mss.0000175054.99588.b1. - DOI - PubMed
    1. Nieman DC, Davis JM, Henson DA, Walberg-Rankin J, Shute M, Dumke CL, et al. Carbohydrate ingestion influences skeletal muscle cytokine mRNA and plasma cytokine levels after a 3-h run. J Appl Physiol. 2003;94:1917–1925. doi: 10.1152/japplphysiol.01130.2002. - DOI - PubMed
    1. Avison MJ, Rothman DL, Nadel E, Shulman RG. Detection of human muscle glycogen by natural abundance 13C NMR. Proc Natl Acad Sci U S A. 1988;85:1634–1636. doi: 10.1073/pnas.85.5.1634. - DOI - PMC - PubMed
    1. Van Zijl PC, Jones CK, Ren J, Malloy CR, Sherry AD. MRI detection of glycogen in vivo by using chemical exchange saturation transfer imaging (glycoCEST) Proc Natl Acad Sci U S A. 2007;104:4359–4364. doi: 10.1073/pnas.0700281104. - DOI - PMC - PubMed
Show all 19 references
LinkOut - more resources
[x]
Cite
Copy Download .nbib
Format: AMA APA MLA NLM

NCBI Literature Resources

MeSH PMC Bookshelf Disclaimer

The PubMed wordmark and PubMed logo are registered trademarks of the U.S. Department of Health and Human Services (HHS). Unauthorized use of these marks is strictly prohibited.

Follow NCBI
Figure 7
Figure 7
Correlation of pre-exercise vastus lateralis MuscleSound® scores and vastus lateralis muscle glycogen content (r = 0.92, P 

Figure 8

Correlation of post-exercise vastus lateralis…

Figure 8

Correlation of post-exercise vastus lateralis MuscleSound® scores and vastus lateralis muscle glycogen content…

Figure 8
Correlation of post-exercise vastus lateralis MuscleSound® scores and vastus lateralis muscle glycogen content (r = 0.90, P 
All figures (8)
Similar articles
Cited by
References
    1. Conlee RK. Muscle glycogen and exercise endurance: a twenty-year perspective. Exerc Sport Sci Rev. 1987;15:1–28. doi: 10.1249/00003677-198700150-00004. - DOI - PubMed
    1. Nieman DC, Davis JM, Henson DA, Gross SJ, Dumke CL, Utter AC, et al. Muscle cytokine mRNA changes after 2.5 h of cycling: influence of carbohydrate. Med Sci Sports Exerc. 2005;37:1283–1290. doi: 10.1249/01.mss.0000175054.99588.b1. - DOI - PubMed
    1. Nieman DC, Davis JM, Henson DA, Walberg-Rankin J, Shute M, Dumke CL, et al. Carbohydrate ingestion influences skeletal muscle cytokine mRNA and plasma cytokine levels after a 3-h run. J Appl Physiol. 2003;94:1917–1925. doi: 10.1152/japplphysiol.01130.2002. - DOI - PubMed
    1. Avison MJ, Rothman DL, Nadel E, Shulman RG. Detection of human muscle glycogen by natural abundance 13C NMR. Proc Natl Acad Sci U S A. 1988;85:1634–1636. doi: 10.1073/pnas.85.5.1634. - DOI - PMC - PubMed
    1. Van Zijl PC, Jones CK, Ren J, Malloy CR, Sherry AD. MRI detection of glycogen in vivo by using chemical exchange saturation transfer imaging (glycoCEST) Proc Natl Acad Sci U S A. 2007;104:4359–4364. doi: 10.1073/pnas.0700281104. - DOI - PMC - PubMed
Show all 19 references
LinkOut - more resources
[x]
Cite
Copy Download .nbib
Format: AMA APA MLA NLM
Figure 8
Figure 8
Correlation of post-exercise vastus lateralis MuscleSound® scores and vastus lateralis muscle glycogen content (r = 0.90, P 
All figures (8)

References

    1. Conlee RK. Muscle glycogen and exercise endurance: a twenty-year perspective. Exerc Sport Sci Rev. 1987;15:1–28. doi: 10.1249/00003677-198700150-00004.
    1. Nieman DC, Davis JM, Henson DA, Gross SJ, Dumke CL, Utter AC, et al. Muscle cytokine mRNA changes after 2.5 h of cycling: influence of carbohydrate. Med Sci Sports Exerc. 2005;37:1283–1290. doi: 10.1249/01.mss.0000175054.99588.b1.
    1. Nieman DC, Davis JM, Henson DA, Walberg-Rankin J, Shute M, Dumke CL, et al. Carbohydrate ingestion influences skeletal muscle cytokine mRNA and plasma cytokine levels after a 3-h run. J Appl Physiol. 2003;94:1917–1925. doi: 10.1152/japplphysiol.01130.2002.
    1. Avison MJ, Rothman DL, Nadel E, Shulman RG. Detection of human muscle glycogen by natural abundance 13C NMR. Proc Natl Acad Sci U S A. 1988;85:1634–1636. doi: 10.1073/pnas.85.5.1634.
    1. Van Zijl PC, Jones CK, Ren J, Malloy CR, Sherry AD. MRI detection of glycogen in vivo by using chemical exchange saturation transfer imaging (glycoCEST) Proc Natl Acad Sci U S A. 2007;104:4359–4364. doi: 10.1073/pnas.0700281104.
    1. Kogan F, Hariharan H, Reddy R. Chemical Exchange Saturation Transfer (CEST) Imaging: Description of technique and potential clinical applications. Curr Radiol Rep. 2013;1:102–114. doi: 10.1007/s40134-013-0010-3.
    1. Sikdar S, Wei Q, Cortes N. Dynamic ultrasound imaging applications to quantify musculoskeletal function. Exerc Sport Sci Rev. 2014;42:126–135. doi: 10.1249/JES.0000000000000015.
    1. Yim ES, Corrado G. Ultrasound in sports medicine: relevance of emerging techniques to clinical care of athletes. Sports Med. 2012;42:665–680. doi: 10.1007/BF03262287.
    1. Lopata RG, van Dijk JP, Pillen S, Nillesen MM, Maas H, Thijssen JM, et al. Dynamic imaging of skeletal muscle contraction in three orthogonal directions. J Appl Physiol. 2010;109:906–915. doi: 10.1152/japplphysiol.00092.2010.
    1. Sarvazyan A, Tatarinov A, Sarvazyan N. Ultrasonic assessment of tissue hydration status. Ultrasonics. 2005;43:661–671. doi: 10.1016/j.ultras.2005.03.005.
    1. Topchyan A, Tatarinov A, Sarvazyan N, Sarvazyan A. Ultrasound velocity in human muscle in vivo: perspective for edema studies. Ultrasonics. 2006;44:259–264. doi: 10.1016/j.ultras.2006.02.003.
    1. Arts IM, Pillen S, Schelhaas HJ, Overeem S, Zwarts MJ. Normal values for quantitative muscle ultrasonography in adults. Muscle Nerve. 2010;41:32–41. doi: 10.1002/mus.21458.
    1. Hill JC, Millán IS. Validation of musculoskeletal ultrasound to assess and quantify muscle glycogen content. A novel approach Phys Sportsmed. 2014;42(3):45–52. doi: 10.3810/psm.2014.09.2075.
    1. Shanely RA, Zwetsloot KA, Triplett NT, Meaney MP, Farris GE, Nieman DC. Human skeletal muscle biopsy procedures using the modified Bergström technique. J Vis Exp. 2014: (91). doi: 10.3791/51812
    1. Kim CK, Bangsbo J, Strange S, Karpakka J, Saltin B. Metabolic response and muscle glycogen depletion pattern during prolonged electrically induced dynamic exercise in man. Scand J Rehabil Med. 1995;27:51–58.
    1. Sherman WM, Doyle JA, Lamb DR, Strauss RH. Dietary carbohydrate, muscle glycogen, and exercise performance during 7 d of training. Am J Clin Nutr. 1993;57:27–31.
    1. Duhamel TA, Green HJ, Stewart RD, Foley KP, Smith IC, Ouyang J. Muscle metabolic, SR Ca(2+) -cycling responses to prolonged cycling, with and without glucose supplementation. J Appl Physiol. 2007;103:1986–1998. doi: 10.1152/japplphysiol.01440.2006.
    1. Lewis SF, Haller RG. The pathophysiology of McArdle’s disease: clues to regulation in exercise and fatigue. J Appl Physiol. 1986;61:391–401.
    1. Utter AC, McAnulty SR, Sarvazyan A, Query MC, Landram MJ. Evaluation of ultrasound velocity to assess the hydration status of wrestlers. J Strength Cond Res. 2010;24:1451–1457. doi: 10.1519/JSC.0b013e3181d82d26.

Source: PubMed

Подписаться