Skip to main content
SpringerLink
Log in

Myofiber Ellipticity as an Explanation for Transverse Asymmetry of Skeletal Muscle Diffusion MRI In Vivo Signal

  • Published:
Annals of Biomedical Engineering Aims and scope Submit manuscript

Abstract

Due to its unique non-invasive microstructure probing capabilities, diffusion tensor imaging (DTI) constitutes a valuable tool in the study of fiber orientation in skeletal muscles. By implementing a DTI sequence with judiciously chosen directional encoding to quantify in vivo the microarchitectural properties in the calf muscles of three healthy volunteers at rest, we report that the secondary eigenvalue is significantly higher than the tertiary eigenvalue, a phenomenon corroborated by prior DTI findings. Toward a physics-based explanation of this phenomenon, we propose a composite medium model that accounts for water diffusion in the space within the muscle fiber and the extracellular space. The muscle fibers are abstracted as cylinders of infinite length with an elliptical cross section, the latter closely approximating microstructural features well documented in prior histological studies of excised muscle. The range of values of fiber ellipticity predicted by our model agrees with these studies, and the spatial orientation of the cross-sectional ellipses is consistent with local muscle strain fields and the putative direction of lateral transmission of stress between fibers in certain regions in three antigravity muscles (Tibialis Anterior, Soleus, and Gastrocnemius), as well as independent measurements of deformation in active calf muscles. As a metric, fiber cross-sectional ellipticity may be useful for quantifying morphological changes in skeletal muscle fibers with aging, hypertrophy, or sarcopenia.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6

Similar content being viewed by others

References

  1. Agur, A. M., V. Ng-Thow-Hing, K. A. Ball, E. Fiume, and N. H. McKee. Documentation and three-dimensional modelling of human soleus muscle architecture. Clin. Anat. 16:285–293, 2003.

    Article  PubMed  Google Scholar 

  2. Andersen, J. L. Muscle fibre type adaptation in the elderly human muscle. Scand. J. Med. Sci. Sports 13:42–47, 2003.

    Article  Google Scholar 

  3. Anderson, A. W. Theoretical analysis of the effects of noise on diffusion tensor imaging. Magn. Reson. Med. 46:1174–1188, 2001.

    Article  CAS  PubMed  Google Scholar 

  4. Aquin, L., A. J. Lechner, A. H. Sillau, and N. Banchero. Analysis of shape changes of muscle fiber cross sections in guinea pigs raised at 22 °C and 5 °C. Pfuegers Arch. 385:223–228, 1980.

    Article  CAS  Google Scholar 

  5. Basser, P. J., J. Mattiello, and D. Le Bihan. MR diffusion tensor spectroscopy and imaging. Biophys. J. 66:259–267, 1994.

    Article  CAS  PubMed  Google Scholar 

  6. Behan, W. M., D. W. Cossar, H. A. Madden, and I. C. McKay. Validation of a simple, rapid, and economical technique for distinguishing type 1 and 2 fibres in fixed and frozen skeletal muscle. J. Clin. Pathol. 55:375–380, 2002.

    CAS  PubMed  Google Scholar 

  7. Blemker, S. S., and S. L. Delp. Rectus femoris and vastus intermedius fiber excursions predicted by three-dimensional muscle models. J. Biomech. 39:1383–1391, 2006.

    Article  PubMed  Google Scholar 

  8. Blemker, S. S., P. M. Pinsky, and S. L. Delp. A 3D model of muscle reveals the causes of nonuniform strains in the biceps brachii. J. Biomech. 38:657–665, 2005.

    Article  PubMed  Google Scholar 

  9. Bojsen-Møller, J., H. P. Per Aagaard, U. Svantesson, M. Kjaer, and S. P. Magnusson. Differential displacement of the human soleus and medial gastrocnemius aponeuroses during isometric plantar flexor contractions in vivo. J. Appl. Physiol. 197:1908–1914, 2004.

    Article  Google Scholar 

  10. Campos, G. E., T. J. Luecke, H. K. Wendeln, K. Toma, F. C. Hagerman, T. F. Murray, K. E. Ragg, N. A. Ratamess, W. J. Kraemer, and R. S. Staron. Muscular adaptations in response to three different resistance-training regimens: specificity of repetition maximum training zones. Eur. J. Appl. Physiol. 85:50–60, 2002.

    Article  Google Scholar 

  11. Chin, C. L., F. W. Wehrli, C. N. Hwang, M. Takahashi, and D. B. Hackney. Biexponential diffusion attenuation in the rat spinal cord: computer simulations based on anatomic images of axonal architecture. Magn. Reson. Med. 47:455–460, 2002.

    Article  PubMed  Google Scholar 

  12. Cleveland, G. G., D. C. Chang, C. F. Hazlewood, and H. E. Rorschach. Nuclear magnetic resonance measurement of skeletal muscle anisotropy of the diffusion coefficient of the intracellular water. Biophys. J. 16:1043–1053, 1976.

    Article  CAS  PubMed  Google Scholar 

  13. Damon, B. M. Effects of image noise in muscle diffusion tensor (DT)-MRI assessed using numerical simulations. Magn. Reson. Med. 60:934–944, 2008.

    Article  PubMed  Google Scholar 

  14. Damon, B. M., Z. Ding, A. W. Anderson, A. S. Freyer, and J. C. Gore. Validation of diffusion tensor MRI-based muscle fiber tracking. Magn. Reson. Med. 48:97–104, 2002.

    Article  PubMed  Google Scholar 

  15. Delp, S. L., and J. P. Loan. A computational framework for simulating and analyzing human and animal movement. Comput. Sci. Eng. 2:46–55, 2000.

    Article  Google Scholar 

  16. Deux, J. F., P. Malzy, N. Paragios, G. Bassez, A. Luciani, P. Zerbib, F. Roudot-Thoraval, A. Vignaud, H. Kobeiter, and A. Rahnmouni. Assessment of calf muscle contraction by diffusion tensor imaging. Eur. Radiol. 18:2303–2310, 2008.

    Article  CAS  PubMed  Google Scholar 

  17. Galban, C. J., S. Maderwald, K. Uffmann, A. de Greiff, and M. E. Ladd. Diffusive sensitivity to muscle architecture: a magnetic resonance diffusion tensor imaging study of the human calf. Eur. J. Appl. Physiol. 93:253–262, 2004.

    Article  PubMed  Google Scholar 

  18. Galban, C. J., S. Maderwald, K. Uffmann, and M. E. Ladd. A diffusion tensor imaging analysis of gender differences in water diffusivity within human skeletal muscle. NMR Biomed. 18:489–498, 2005.

    Article  PubMed  Google Scholar 

  19. Gerdes, A. M., S. E. Kellerman, K. B. Malec, and D. D. Schocken. Transverse shape characteristics of cardiac myocytes from rats and humans. Cardioscience 5:31–36, 1994.

    CAS  PubMed  Google Scholar 

  20. Hatakenaka, M., Y. Matsuo, T. Setoguchi, H. Yabuuchi, T. Okafuji, T. Kamitani, K. Nishikawa, and H. Honda. Alteration of proton diffusivity associated with passive muscle extension and contraction. J. Magn. Reson. Imag. 27:932–937, 2008.

    Article  Google Scholar 

  21. Heemskerk, A. M., T. K. Sinha, K. J. Wilson, and B. M. Damon. Change in water diffusion properties with altered muscle architecture. In: Proceedings of the Int. Soc. Magn. Reson. Med., Toronto, Canada, 2008, p. 1787.

  22. Heemskerk, A. M., G. J. Strijkers, M. R. Drost, G. S. van Bochove, and K. Nikolay. Skeletal muscle degeneration and regeneration after femoral artery ligation in mice: monitoring with diffusion MR imaging. Radiology 243:414–421, 2007.

    Article  Google Scholar 

  23. Hodgson, J. A., T. Finni, A. M. Lai, V. R. Edgerton, and S. Sinha. Influence of structure on the tissue dynamics of the human soleus muscle observed in MRI studies during isometric contractions. J. Morphol. 267:584–601, 2006.

    Article  PubMed  Google Scholar 

  24. Karampinos, D. C., K. F. King, B. P. Sutton, and J. G. Georgiadis. In vivo study of cross-sectional skeletal muscle fiber asymmetry with diffusion-weighted MRI. In: Proceedings of the IEEE-EMBS, Lyon, France, 2007, pp. 327–330.

  25. Karampinos, D. C., K. F. King, B. P. Sutton, and J. G. Georgiadis. Mapping cross-sectional skeletal muscle asymmetry via high angular resolution diffusion imaging. In: Proceedings of the Int. Soc. Magn. Reson. Med., Hawaii, USA, 2009, p. 1928.

  26. Kärger, J., H. Pfeifer, and W. Heink. Principles and applications of self diffusion measurements by nuclear magnetic resonance. Adv. Magn. Reson. 12:1–89, 1988.

    Google Scholar 

  27. Kjaer, M. Role of extracellular matrix in adaptation of tendon and skeletal muscle to mechanical loading. Physiol. Rev. 84:649–698, 2004.

    Article  CAS  PubMed  Google Scholar 

  28. Landis, C. L., X. Li, F. W. Telang, P. Molina, I. Palyka, G. Vetek, and C. S. Spinger. Equilibrium transcytolemmal water-exchange kinetics in skeletal muscle in vivo. Magn. Reson. Med. 42:467–478, 1999.

    Article  CAS  PubMed  Google Scholar 

  29. Lansdown, D. A., Z. Ding, M. Wadington, J. L. Hornberger, and B. M. Damon. Quantitative diffusion tensor MRI-based fiber tracking of human skeletal muscle. J. Appl. Physiol. 48:97–104, 2002.

    Google Scholar 

  30. LeGrice, I. J., Y. Takayama, and J. W. Covell. Transverse shear along myocardial cleavage planes provides a mechanism for normal systolic wall thickening. Circ. Res. 77:182–193, 1995.

    CAS  PubMed  Google Scholar 

  31. Merboldt, K. D., W. Hanicke, and J. Frahm. Self-diffusion NMR imaging using stimulated echoes. J. Magn. Reson. 64:479–486, 1995.

    Google Scholar 

  32. Nagarsekar, G., J. Hodgson, D. Shin, and S. Sinha. Development of a spin tag sequence with spiral acquisition for elucidating shear at the deep gastrocnemius aponeurosis and other dynamics of the musculoskeletal elements of the leg. In: Proceedings of the Int. Soc. Magn. Reson. Med., Hawaii, USA, 2009, p. 549.

  33. Napadow, V. J., Q. Chen, V. Mai, P. T. C. So, and R. J. Gilbert. Quantitative analysis of three-dimensional-resolved fiber architecture in heterogeneous skeletal muscle tissue using NMR and optical imaging methods. Biophys. J. 80:2968–2975, 2001.

    Article  CAS  PubMed  Google Scholar 

  34. Pappas, G. P., D. S. Asakawa, S. L. Delp, F. E. Zajac, and J. E. Drace. Nonuniform shortening in the biceps brachii during elbow flexion. J. Appl. Physiol. 92:2381–2389, 2002.

    PubMed  Google Scholar 

  35. Passerieux, E., R. Rossignol, A. Chopard, A. Carnino, J. F. Marini, T. Letellier, and J. P. Delage. Structural organization of the perimysium in bovine skeletal muscle: junctional plates and associated intracellular subdomains. J. Struct. Biol. 154:206–216, 2006.

    Article  CAS  PubMed  Google Scholar 

  36. Purslow, P. P. The structure and functional significance of variations in the connective tissue within muscle. Comp. Biochem. Physiol. A 133:947–966, 2002.

    Article  Google Scholar 

  37. Saab, G., T. R. Thompson, and G. D. Marsh. Multicomponent T2 relaxation of in vivo skeletal muscle. Magn. Reson. Med. 42:150–157, 1999.

    Article  CAS  PubMed  Google Scholar 

  38. Saab, G., T. R. Thompson, G. D. Marsh, P. A. Picot, and G. R. Moran. Two-dimensional time correlation relaxometry of skeletal muscle in vivo at 3 Tesla. Magn. Reson. Med. 46:1093–1098, 2001.

    Article  CAS  PubMed  Google Scholar 

  39. Saotome, T., M. Sekino, F. Eto, and S. Ueno. Evaluation of diffusional anisotropy and microscopic structure in skeletal muscles using magnetic resonance. Magn. Reson. Imag. 24:19–25, 2006.

    Article  Google Scholar 

  40. Sen, P. N., C. Scala, and M. H. Cohen. A self-similar model for sedimentary rocks with application to the dielectric constant of fused glass beads. Geophysics 46:781–795, 1981.

    Article  Google Scholar 

  41. Sinha, S., U. Sinha, and V. R. Edgerton. In vivo diffusion tensor imaging of the human calf muscle. J. Magn. Reson. Imag. 24:182–190, 2006.

    Article  Google Scholar 

  42. Sinha, U., and L. Yao. In vivo diffusion tensor imaging of human calf muscle. J. Magn. Reson. Imag. 15:87–95, 2002.

    Article  Google Scholar 

  43. Song, S. K., N. Shimada, and P. J. Anderson. Orthogonal diameters in the analysis of muscle fiber and form. Nature 200:1220–1221, 1963.

    Article  CAS  PubMed  Google Scholar 

  44. Stanisz, G. J., A. Szafer, G. A. Wright, and R. M. Henkelman. An analytical model of restricted diffusion in bovine optic nerve. Magn. Reson. Med. 37:103–111, 1997.

    Article  CAS  PubMed  Google Scholar 

  45. Staron, R. S., W. J. Kraemer, R. S. Hikida, A. C. Fry, J. D. Murray, and G. E. Campos. Fibre type composition of four hindlimb muscles of adult Fisher 344 rats. Histochem. Cell Biol. 111:117–123, 1999.

    Article  CAS  PubMed  Google Scholar 

  46. Steidle, G., and F. Schick. Echoplanar diffusion tensor imaging of the lower leg musculature using eddy current nulled stimulated echo preparation. Magn. Reson. Med. 55:541–548, 2006.

    Article  CAS  PubMed  Google Scholar 

  47. Trotter, J. A. Dynamic shape of tapered skeletal muscle fibers. J. Morphol. 207:221–223, 1991.

    Article  Google Scholar 

  48. Trotter, J. A., and P. P. Purslow. Functional morphology of the endomysium in series fibered muscles. J. Morphol. 212:109–122, 1992.

    Article  CAS  PubMed  Google Scholar 

  49. Tseng, W. Y., V. J. Weeden, T. G. Reese, R. N. Smith, and E. F. Halpern. Diffusion tensor MRI of myocardial fibers and sheets: correspondence with visible cut-face texture. J. Magn. Reson. Imag. 17:31–42, 2003.

    Article  Google Scholar 

  50. van Donkelaar, C. C., P. J. B. Willems, A. M. M. Muijtjens, and M. R. Drost. Skeletal muscle transverse strain during isometric contraction at different lengths. J. Biomech. 32:755–762, 1999.

    Article  PubMed  Google Scholar 

  51. Venema, H. M., and J. Overweg. Analysis of the size and shape of cross-sections of muscle fibers. Med. Biol. Eng. 12:681–692, 1974.

    Article  CAS  PubMed  Google Scholar 

  52. Vincensini, D., V. Dedieu, J. P. Renou, P. Otal, and F. Joffre. Measurements of extracellular volume fraction and capillary permeability in tissues using dynamic spin–lattice relaxometry: studies in rabbit muscles. Magn. Reson. Imag. 21:85–93, 2003.

    Article  CAS  Google Scholar 

  53. Wedeen, V. J., T. G. Reese, V. J. Napadow, and R. J. Gilbert. Demonstration of primary and secondary muscle fiber architecture of the bovine tongue by diffusion tensor magnetic resonance imaging. Biophys. J. 80:1024–1028, 2001.

    Article  CAS  PubMed  Google Scholar 

  54. Zimmerman, S. D., J. Criscione, and J. W. Covell. Remodeling in myocardium adjacent to an infarction in the pig left ventricle. Am. J. Physiol. Heart Circ. Physiol. 287:H2697–H2704, 2004.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The present work was supported by the National Institutes of Health (grant R21HL090455), the Beckman Institute at the University of Illinois at Urbana-Champaign, IL, and the Applied Science Laboratory of GE Healthcare, Waukesha, WI, USA. DCK and JGG also thank Dr. Bruce Damon for a stimulating discussion regarding the possible role of the sarcoplasmic reticulum in diffusion, and Ms. Elise Corbin for her artwork.

Author information

Authors and Affiliations

  1. Department of Mechanical Science & Engineering, University of Illinois at Urbana-Champaign, Urbana, IL, USA

    Dimitrios C. Karampinos & John G. Georgiadis

  2. Department of Bioengineering, University of Illinois at Urbana-Champaign, Urbana, IL, USA

    Bradley P. Sutton

  3. Beckman Institute for Advanced Science and Technology, University of Illinois at Urbana-Champaign, Urbana, IL, USA

    Dimitrios C. Karampinos, Bradley P. Sutton & John G. Georgiadis

  4. Applied Science Laboratory, GE Healthcare, Waukesha, WI, USA

    Kevin F. King

  5. 2144 Mechanical Engineering Laboratory, 1206 West Green Street, MC-244, Urbana, IL, 61801, USA

    John G. Georgiadis

Authors
  1. Dimitrios C. Karampinos
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kevin F. King
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bradley P. Sutton
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. John G. Georgiadis
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to John G. Georgiadis.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Karampinos, D.C., King, K.F., Sutton, B.P. et al. Myofiber Ellipticity as an Explanation for Transverse Asymmetry of Skeletal Muscle Diffusion MRI In Vivo Signal. Ann Biomed Eng 37, 2532–2546 (2009). https://doi.org/10.1007/s10439-009-9783-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10439-009-9783-1

Keywords

Search

Navigation