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Dynamic DTI (dDTI) shows differing temporal activation patterns in post-exercise skeletal muscles

  • Conrad Rockel
  • Alireza Akbari
  • Dinesh A. Kumbhare
  • Michael D. NoseworthyEmail author
Research Article

Abstract

Object

To assess post-exercise recovery of human calf muscles using dynamic diffusion tensor imaging (dDTI).

Materials and methods

DTI data (6 directions, b = 0 and 400 s/mm2) were acquired every 35 s from seven healthy men using a 3T MRI, prior to (4 volumes) and immediately following exercise (13 volumes, ~7.5 min). Exercise consisted of 5-min in-bore repetitive dorsiflexion-eversion foot motion with 0.78 kg resistance. Diffusion tensors calculated at each time point produced maps of mean diffusivity (MD), fractional anisotropy (FA), radial diffusivity (RD), and signal at b = 0 s/mm2 (S0). Region-of-interest (ROI) analysis was performed on five calf muscles: tibialis anterior (ATIB), extensor digitorum longus (EDL) peroneus longus (PER), soleus (SOL), and lateral gastrocnemius (LG).

Results

Active muscles (ATIB, EDL, PER) showed significantly elevated initial MD post-exercise, while predicted inactive muscles (SOL, LG) did not (p < 0.0001). The EDL showed a greater initial increase in MD (1.90 × 10−4mm2/s) than ATIB (1.03 × 10−4mm2/s) or PER (8.79 × 10−5 mm2/s) (p = 7.40 × 10−4), and remained significantly elevated across more time points than ATIB or PER. Significant increases were observed in post-exercise EDL S0 relative to other muscles across the majority of time points (p < 0.01 to p < 0.001).

Conclusions

dDTI can be used to differentiate exercise-induced changes between muscles. These differences are suggested to be related to differences in fiber composition.

Keywords

DTI Skeletal muscle Exercise Recovery Time course Human 

Notes

Acknowledgments

Funding was provided to CR in the form of a Natural Sciences and Engineering Research Council (NSERC) of Canada CGS-D PhD scholarship. The research was funded through an NSERC Discovery grant to MDN.

Compliance with ethical standards

Conflict of interest

No author has any potential conflict of interest with respect to the work described and performed in this current manuscript. Dr. Michael Noseworthy has received a one-time lecture honorarium from GE Healthcare (Canada) for two 50-min lectures delivered in September 2015 to MRI technologists. These lectures were not in any way related to the current work.

Research involving human participants and/or animals

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.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Supplementary material

10334_2016_587_MOESM1_ESM.docx (107 kb)
Supplementary material 1 (DOCX 106 kb)

References

  1. 1.
    Cleveland GG, Chang DC, Hazlewood CF, Rorschach HE (1976) Nuclear magnetic resonance measurement of skeletal muscle. Biophys J 16:1043–1053CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Van Donkelaar CC, Kretzers LJ, Bovendeerd PH, Lataster LM, Nicolay K, Janssen JD, Drost MR (1999) Diffusion tensor imaging in biomechanical studies of skeletal muscle function. J Anat 194:79–88CrossRefPubMedGoogle Scholar
  3. 3.
    Kermarrec E, Budzik JF, Khalil C, Le Thuc V, Hancart-Destee C, Cotton A (2010) In vivo diffusion tensor imaging and tractography of human thigh muscles in healthy subjects. Am J Roentgenol 195:W352–W356CrossRefGoogle Scholar
  4. 4.
    Galban CJ, Maderwald S, Uffman K, de Greiff A, Ladd ME (2004) Diffusive sensitivity to muscle architecture: a magnetic resonance diffusion tensor imaging study of the human calf. Eur J Appl Physiol 93:253–262CrossRefPubMedGoogle Scholar
  5. 5.
    Sinha S, Sinha U, Edgerton VR (2006) In vivo diffusion tensor imaging of the human calf muscle. J Magn Reson Imaging 24:182–190CrossRefPubMedGoogle Scholar
  6. 6.
    Deux JF, Malzy P, Paragios N, Bassez G, Luciani A, Zerbib P, Roudot-Thoraval F, Vignaud A, Kobeiter H, Rahmouni A (2008) Assessment of calf muscle contraction by diffusion tensor imaging. Eur Radiol 18:2303–2310CrossRefPubMedGoogle Scholar
  7. 7.
    Hatakenaka M, Yabuuchi H, Sunami S, Kamitani T, Takayama Y, Nishikawa K, Honda H (2010) Joint position affects muscle proton diffusion: evaluation with a 3-T MR system. Am J Roent 194:W208–W211CrossRefGoogle Scholar
  8. 8.
    Okamoto Y, Mori S, Kujiraoka Y, Katsuhiro N, Hirano Y, Minami M (2012) Diffusion property differences of the lower leg musculature between athletes and non-athletes using 1.5T MRI. Magn Reson Mater Phy (MAGMA) 25:277–284CrossRefGoogle Scholar
  9. 9.
    Nakai R, Azuma T, Sudo M, Urayama S, Takizawa O, Tsutsumi S (2008) MRI analysis of structural changes in skeletal muscles and surrounding tissues following long-term walking exercise with training equipment. J Appl Physiol 105:958–963CrossRefPubMedGoogle Scholar
  10. 10.
    Morvan D, Leroy-Willig A (1995) Simultaneous measurements of diffusion and transverse relaxation in exercising skeletal muscle. Magn Reson Imaging 13:943–948CrossRefPubMedGoogle Scholar
  11. 11.
    Nygren AT, Kaijser L (2002) Water exchange induced by unilateral exercise in active and inactive skeletal muscles. J Appl Physiol 93:1716–1722CrossRefPubMedGoogle Scholar
  12. 12.
    Ababneh ZQ, Ababneh R, Maier SE, Winalski CS, Oshio K, Ababneh AM, Mulkern RV (2008) On the correlation between T2 and tissue diffusion coefficients in exercised muscle: quantitative measurements at 3T within the tibialis anterior. Magn Reson Mater Phy (MAGMA) 21:273–278CrossRefGoogle Scholar
  13. 13.
    Morvan D (1995) In vivo measurement of diffusion and pseudo-diffusion in skeletal muscle at rest and after exercise. Magn Reson Imaging 13:193–199CrossRefPubMedGoogle Scholar
  14. 14.
    Sigmund EE, Novikov DS, Sui D, Ukpebor O, Baete S, Babb JS, Liu K, Feiweier T, Kwon J, McGorty K, Bencardino J, Fieremans E (2014) Time-dependent diffusion in skeletal muscle with the random permeable barrier model (RPBM): application to normal controls and chronic exertional compartment syndrome patients. NMR Biomed 27:519–528CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Okamoto Y, Kunimatsu A, Miki S, Shindo M, Niitsu M, Minami M (2008) Fraction anisotropy values of calf muscles in normative state after exercise: preliminary results. Magn Reson Med Sci 7:157–162CrossRefPubMedGoogle Scholar
  16. 16.
    Cermak NM, Noseworthy MD, Bourgeois JM, Tarnopolsky MA, Gibala MJ (2012) Diffusion tensor MRI to assess skeletal muscle disruption following eccentric exercise. Muscle Nerv 46:42–50CrossRefGoogle Scholar
  17. 17.
    Yangisawa O, Kurihara T, Koayashi N, Fukubayashi T (2011) Strenuous resistance exercise effects on magnetic resonance diffusion parameters and muscle-tendon function in human skeletal muscle. J Magn Reson Imaging 34:887–894CrossRefGoogle Scholar
  18. 18.
    Froeling M, Oudeman J, Strijkers GJ, Maas M, Drost MR, Nicolay K, Nederveen AJ (2015) Muscle changes detected with diffusion-tensor imaging after long distance running. Radiology 274:548–562CrossRefPubMedGoogle Scholar
  19. 19.
    Baete SH, Cho GY, Sigmund EE (2015) Dynamic diffusion-tensor measurements in muscle tissue using the single-line multiple-echo diffusion-tensor acquisition technique at 3T. NMR Biomed 28:667–678CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Polgar J, Johnson MA, Weightman D, Appleton D (1973) Data on fibre size in thirty six human muscles: an autopsy study. J Neurol Sci 19:307–318CrossRefPubMedGoogle Scholar
  21. 21.
    Basmajian JV, De Luca CJ (1985) Muscles alive: their functions revealed by electromyography hardcover, 5th edn. Williams & Wilkins, New York, p 561Google Scholar
  22. 22.
    Andersen P, Kroese AJ (1978) Capillary supply in soleus and gastrocnemius muscles of man. Pflug Arch 375:245–249CrossRefGoogle Scholar
  23. 23.
    Johnson MA, Polgar J, Weightman D, Appleton D (1973) Data on the distribution of fibre types in thirty-six human muscles: an autopsy study. J Neurol Sci 18:111–129CrossRefPubMedGoogle Scholar
  24. 24.
    Snell RS (2012) Clinical anatomy by regions, 9th edn. Lippincott Williams & Wilkens, PhiladelphiaGoogle Scholar
  25. 25.
    Rockel C, Davis A, Wells G, Noseworthy MD (2012) Monitoring exercise-induced muscle changes using diffusion tensor imaging. In: Proceedings of the 20th scientific meeting, International Society for Magnetic Resonance in Medicine, Melbourne, Australia, p 1425Google Scholar
  26. 26.
    Elzibak AH, Noseworthy MD (2014) Assessment of diffusion tensor imaging indices in calf muscles following postural change from standing to supine position. Magn Reson Mater Phy (MAGMA) 27:387–395CrossRefGoogle Scholar
  27. 27.
    Jenkinson M, Beckmann CF, Behrens TE, Woolrich MW, Smith SM (2012) FSL. NeuroImage 62:782–790CrossRefPubMedGoogle Scholar
  28. 28.
    Damon BM, Gregory CD, Hall KL, Stark HJ, Gulani V, Dawson MJ (2002) Intracellular acidification and volume increases explain R2 decreases in exercising muscle. Magn Reson Med 47:14–23CrossRefPubMedGoogle Scholar
  29. 29.
    Rockel C, Noseworthy MD (2016) An exploration of diffusion tensor eigenvector variability within human calf muscles. J Magn Reson Imaging 43:190–202CrossRefPubMedGoogle Scholar
  30. 30.
    Dietrich O, Raya JG, Reeder SB, Reiser MF, Schoenberg SO (2007) Measurement of signal-to-noise ratios in MR images: influence of multichannel coils, parallel imaging, and reconstruction filters. J Magn Reson Imaging 26:375–385CrossRefPubMedGoogle Scholar
  31. 31.
    Rockel C, Noseworthy MD (2015) Modification of signal-to-noise calculation for use in spatial mapping. In: Proceedings of the 29th scientific meeting, European Society for Magnetic Resonance in Medicine and Biology, Edinburgh, Scotland, p 646Google Scholar
  32. 32.
    Lundvall J, Mellander S, Westling H, White T (1972) Fluid transfers between blood and tissues during exercise. Acta Physiol Scand 85:258–269CrossRefPubMedGoogle Scholar
  33. 33.
    Saab G, Thompson RT, Marsh GD (2000) Effects of exercise on muscle transverse relaxation determined by MR imaging and in vivo relaxometry. J Appl Physiol 88:226–233PubMedGoogle Scholar
  34. 34.
    Okamoto Y, Kunimatsu A, Kono T, Nasu K, Sonobe J, Minami M (2010) Changes in MR diffusion properties during active muscle contraction in the calf. Magn Reson Med Sci 9:1–8CrossRefPubMedGoogle Scholar
  35. 35.
    Scheel M, von Roth P, Winkler T, Arampatzis A, Prokscha T, Hamm B, Diederichs G (2013) Fiber type characterization in skeletal muscle by diffusion tensor imaging. NMR Biomed 26:1220–1224CrossRefPubMedGoogle Scholar
  36. 36.
    Fitts RH, Widrick JJ (1995) Muscle mechanics: adaptations with exercise-training. Exerc Sport Sci Rev 24:427–474Google Scholar
  37. 37.
    Edgarton VR, Smith JL, Simpson DR (1975) Muscle fibre type populations of human leg muscles. Histochem J 7:259–266CrossRefGoogle Scholar
  38. 38.
    Houmard JA, Smith R, Jenrasiak GL (1995) Relationship between MRI relaxation time and muscle fiber composition. J Appl Physiol 78:807–809PubMedGoogle Scholar
  39. 39.
    Le Bihan D, Breton E, Lallemand D, Aubin ML, Vignaud J, Laval-Jeantet M (1988) Separation of diffusion and perfusion in intravoxel incoherent motion MR imaging. Radiology 168:497–505CrossRefPubMedGoogle Scholar
  40. 40.
    Noseworthy MD, Kim JK, Stainsby JA, Stanisz GJ, Wright GA (1999) Tracking oxygen effects on MR signal in blood and skeletal muscle during hyperoxia exposure. J Magn Reson Imaging 9:814–820CrossRefPubMedGoogle Scholar
  41. 41.
    Fleckenstein JL, Canby RC, Parkey RW, Peshock RM (1988) Acute effects of exercise on MR imaging of skeletal muscle in normal volunteers. Am J Radiol 151:231–237Google Scholar
  42. 42.
    Fisher MJ, Meyer RA, Adams GR, Foley JM, Potchen EJ (1990) Direct relationship between proton T2 and exercise intensity in skeletal muscle MR images. Invest Radiol 25:480–485CrossRefPubMedGoogle Scholar
  43. 43.
    Adams GR, Duvoisin MR, Dudlet GA (1992) Magnetic resonance imaging and electromyography as indexes of muscle function. J Appl Physiol 73:1578–1583PubMedGoogle Scholar
  44. 44.
    Price TB, Kamen G, Damon BM, Knight CA, Applegate B, Gore JC, Eward K, Signorile JF (2003) Comparison of MRI with EMG to study muscle activity associated with dynamic plantar flexion. Magn Reson Imaging 21:853–861CrossRefPubMedGoogle Scholar
  45. 45.
    Prior BM, Ploutz-Snyder LL, Cooper TG, Meyer RA (2001) Fiber type and metabolic dependence of T2 increases in stimulated rat muscles. J Appl Physiol 90:615–623PubMedGoogle Scholar
  46. 46.
    Tesch PA, Karlsson J (1985) Muscle fiber types and size in trained and untrained muscles of elite athletes. J Appl Physiol 59:1716–1720PubMedGoogle Scholar

Copyright information

© ESMRMB 2016

Authors and Affiliations

  • Conrad Rockel
    • 1
    • 2
  • Alireza Akbari
    • 1
    • 2
  • Dinesh A. Kumbhare
    • 1
    • 5
  • Michael D. Noseworthy
    • 1
    • 2
    • 3
    • 4
    • 6
    Email author
  1. 1.McMaster School of Biomedical EngineeringMcMaster UniversityHamiltonCanada
  2. 2.Imaging Research CentreSt. Joseph’s HealthcareHamiltonCanada
  3. 3.Medical Physics and Applied Radiation SciencesMcMaster UniversityHamiltonCanada
  4. 4.Department of RadiologyMcMaster UniversityHamiltonCanada
  5. 5.Division of Physical Medicine and Rehabilitation, Department of MedicineUniversity of TorontoTorontoCanada
  6. 6.Department of Electrical and Computer EngineeringMcMaster UniversityHamiltonCanada

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