Myofiber ellipticity as an explanation for transverse asymmetry of skeletal muscle diffusion MRI in vivo signal

Annals of Biomedical Engineering

Volumn 37, Issue 12, 2009, Pages 2532-2546

  Karampinos, Dimitrios C ^a   King, Kevin F ^c   Sutton, Bradley P ^a,b   Georgiadis, John G ^a,b  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b University of Illinois at Urbana Champaign   (United States)

^c GE HEALTHCARE   (United States)

Author keywords

Diffusion tensor imaging; Gastrocnemius; Myocytes; Myofiber ellipticity; Skeletal muscle; Soleus

Indexed keywords

ANTI-GRAVITY MUSCLES; CALF MUSCLE; COMPOSITE MEDIUM; DIFFUSION TENSOR IMAGING; EIGEN-VALUE; ELLIPTICAL CROSS SECTION; EXTRACELLULAR SPACE; FIBER ORIENTATIONS; GASTROCNEMIUS; IN-VIVO; INDEPENDENT MEASUREMENT; MICROSTRUCTURAL FEATURES; MORPHOLOGICAL CHANGES; MUSCLE FIBER; MUSCLE STRAIN; MYOCYTES; NON-INVASIVE; PHYSICS-BASED; SARCOPENIA; SECTIONAL ELLIPSIS; SKELETAL MUSCLE; SKELETAL MUSCLE FIBERS; SPATIAL ORIENTATIONS; TIBIALIS ANTERIOR; WATER DIFFUSION;

DIFFUSION; EIGENVALUES AND EIGENFUNCTIONS; FIBERS; MICROSTRUCTURAL EVOLUTION; TENSORS;

MUSCLE;

ALGORITHM; ANISOTROPY; ARTICLE; AUDIOVISUAL EQUIPMENT; BIOLOGICAL MODEL; COMPUTER ASSISTED DIAGNOSIS; COMPUTER SIMULATION; CYTOLOGY; DIFFUSION WEIGHTED IMAGING; IMAGE ENHANCEMENT; METHODOLOGY; PHYSIOLOGY; REPRODUCIBILITY; SENSITIVITY AND SPECIFICITY; SKELETAL MUSCLE;

ALGORITHMS; ANISOTROPY; COMPUTER SIMULATION; DIFFUSION MAGNETIC RESONANCE IMAGING; IMAGE ENHANCEMENT; IMAGE INTERPRETATION, COMPUTER-ASSISTED; MODELS, ANATOMIC; MODELS, BIOLOGICAL; MUSCLE FIBERS, SKELETAL; REPRODUCIBILITY OF RESULTS; SENSITIVITY AND SPECIFICITY;

EID: 70450253112     PISSN: 00906964     EISSN: 15739686     Source Type: Journal    
DOI: 10.1007/s10439-009-9783-1     Document Type: Article

References (54)

1. AM Agur V Ng-Thow-Hing KA Ball E Fiume NH McKee 2003 Documentation and three-dimensional modelling of human soleus muscle architecture Clin. Anat. 16 285 293 10.1002/ca.10112 12794910 (Pubitemid 36753669)
2. JL Andersen 2003 Muscle fibre type adaptation in the elderly human muscle Scand. J. Med. Sci. Sports 13 42 47 10.1034/j.1600-0838.2003.00299.x (Pubitemid 37463578)
3. AW Anderson 2001 Theoretical analysis of the effects of noise on diffusion tensor imaging Magn. Reson. Med. 46 1174 1188 10.1002/mrm.1315 1:STN:280:DC%2BD3Mnps12gsA%3D%3D 11746585 (Pubitemid 33104306)
4. L Aquin AJ Lechner AH Sillau N Banchero 1980 Analysis of shape changes of muscle fiber cross sections in guinea pigs raised at 22 C and 5 C Pfuegers Arch. 385 223 228 10.1007/BF00647461 1:STN:280:DyaL3c3lsFyrtA%3D%3D
5. PJ Basser J Mattiello D Le Bihan 1994 MR diffusion tensor spectroscopy and imaging Biophys. J. 66 259 267 10.1016/S0006-3495(94)80775-1 1:STN:280:DyaK2c7ns1Kgtw%3D%3D 8130344
6. WM Behan DW Cossar HA Madden IC McKay 2002 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 1:STN:280: DC%2BD383ot1OmsQ%3D%3D 11986345
7. SS Blemker SL Delp 2006 Rectus femoris and vastus intermedius fiber excursions predicted by three-dimensional muscle models J. Biomech. 39 1383 1391 10.1016/j.jbiomech.2005.04.012 15972213 (Pubitemid 44262075)
8. SS Blemker PM Pinsky SL Delp 2005 A 3D model of muscle reveals the causes of nonuniform strains in the biceps brachii J. Biomech. 38 657 665 10.1016/j.jbiomech.2004.04.009 15713285 (Pubitemid 40248451)
9. J Bojsen-Møller HP Per Aagaard U Svantesson M Kjaer SP Magnusson 2004 Differential displacement of the human soleus and medial gastrocnemius aponeuroses during isometric plantar flexor contractions in vivo J. Appl. Physiol. 197 1908 1914 10.1152/japplphysiol.00084.2004 (Pubitemid 39426010)
10. GE Campos TJ Luecke HK Wendeln K Toma FC Hagerman TF Murray KE Ragg NA Ratamess WJ Kraemer RS Staron 2002 Muscular adaptations in response to three different resistance-training regimens: specificity of repetition maximum training zones Eur. J. Appl. Physiol. 85 50 60 10.1007/s00421-002-0681-6 (Pubitemid 40826308)
11. CL Chin FW Wehrli CN Hwang M Takahashi DB Hackney 2002 Biexponential diffusion attenuation in the rat spinal cord: computer simulations based on anatomic images of axonal architecture Magn. Reson. Med. 47 455 460 10.1002/mrm.10078 11870831 (Pubitemid 34193999)
12. GG Cleveland DC Chang CF Hazlewood HE Rorschach 1976 Nuclear magnetic resonance measurement of skeletal muscle anisotropy of the diffusion coefficient of the intracellular water Biophys. J. 16 1043 1053 10.1016/S0006-3495(76) 85754-2 1:CAS:528:DyaE28XlslCrtr0%3D 963204
13. BM Damon 2008 Effects of image noise in muscle diffusion tensor (DT)-MRI assessed using numerical simulations Magn. Reson. Med. 60 934 944 10.1002/mrm.21707 18816814
14. BM Damon Z Ding AW Anderson AS Freyer JC Gore 2002 Validation of diffusion tensor MRI-based muscle fiber tracking Magn. Reson. Med. 48 97 104 10.1002/mrm.10198 12111936 (Pubitemid 34721592)
15. SL Delp JP Loan 2000 A computational framework for simulating and analyzing human and animal movement Comput. Sci. Eng. 2 46 55 10.1109/5992.877394
16. JF Deux P Malzy N Paragios G Bassez A Luciani P Zerbib F Roudot-Thoraval A Vignaud H Kobeiter A Rahnmouni 2008 Assessment of calf muscle contraction by diffusion tensor imaging Eur. Radiol. 18 2303 2310 10.1007/s00330-008-1012-z 1:STN:280:DC%2BD1crpsFSnsw%3D%3D 18463875
17. CJ Galban S Maderwald K Uffmann A de Greiff ME Ladd 2004 Diffusive sensitivity to muscle architecture: a magnetic resonance diffusion tensor imaging study of the human calf Eur. J. Appl. Physiol. 93 253 262 10.1007/s00421-004-1186-2 15322853 (Pubitemid 39534628)
18. CJ Galban S Maderwald K Uffmann ME Ladd 2005 A diffusion tensor imaging analysis of gender differences in water diffusivity within human skeletal muscle NMR Biomed. 18 489 498 10.1002/nbm.975 16075414 (Pubitemid 43013889)
19. AM Gerdes SE Kellerman KB Malec DD Schocken 1994 Transverse shape characteristics of cardiac myocytes from rats and humans Cardioscience 5 31 36 1:STN:280:DyaK2c3msVajtA%3D%3D 8204795
20. M Hatakenaka Y Matsuo T Setoguchi H Yabuuchi T Okafuji T Kamitani K Nishikawa H Honda 2008 Alteration of proton diffusivity associated with passive muscle extension and contraction J. Magn. Reson. Imag. 27 932 937 10.1002/jmri.21302
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. AM Heemskerk GJ Strijkers MR Drost GS van Bochove K Nikolay 2007 Skeletal muscle degeneration and regeneration after femoral artery ligation in mice: monitoring with diffusion MR imaging Radiology 243 414 421 10.1148/radiol. 2432060491 (Pubitemid 46649696)
23. JA Hodgson T Finni AM Lai VR Edgerton S Sinha 2006 Influence of structure on the tissue dynamics of the human soleus muscle observed in MRI studies during isometric contractions J. Morphol. 267 584 601 10.1002/jmor.10421 16453292 (Pubitemid 43666487)
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. J Kärger H Pfeifer W Heink 1988 Principles and applications of self diffusion measurements by nuclear magnetic resonance Adv. Magn. Reson. 12 1 89
27. M Kjaer 2004 Role of extracellular matrix in adaptation of tendon and skeletal muscle to mechanical loading Physiol. Rev. 84 649 698 10.1152/physrev.00031.2003 1:CAS:528:DC%2BD2cXjtlCktb4%3D 15044685 (Pubitemid 38365495)
28. CL Landis X Li FW Telang P Molina I Palyka G Vetek CS Spinger 1999 Equilibrium transcytolemmal water-exchange kinetics in skeletal muscle in vivo Magn. Reson. Med. 42 467 478 10.1002/(SICI)1522-2594(199909)42:3<467::AID- MRM9>3.0.CO;2-0 1:STN:280:DyaK1MzpvVGmuw%3D%3D 10467291 (Pubitemid 29416208)
29. DA Lansdown Z Ding M Wadington JL Hornberger BM Damon 2002 Quantitative diffusion tensor MRI-based fiber tracking of human skeletal muscle J. Appl. Physiol. 48 97 104
30. IJ LeGrice Y Takayama JW Covell 1995 Transverse shear along myocardial cleavage planes provides a mechanism for normal systolic wall thickening Circ. Res. 77 182 193 1:CAS:528:DyaK2MXmsFersbk%3D 7788876
31. KD Merboldt W Hanicke J Frahm 1995 Self-diffusion NMR imaging using stimulated echoes J. Magn. Reson. 64 479 486
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. VJ Napadow Q Chen V Mai PTC So RJ Gilbert 2001 Quantitative analysis of three-dimensional-resolved fiber architecture in heterogeneous skeletal muscle tissue using NMR and optical imaging methods Biophys. J. 80 2968 2975 10.1016/S0006-3495(01)76262-5 1:CAS:528:DC%2BD3MXkvFSqt7o%3D 11371469
34. GP Pappas DS Asakawa SL Delp FE Zajac JE Drace 2002 Nonuniform shortening in the biceps brachii during elbow flexion J. Appl. Physiol. 92 2381 2389 12015351
35. E Passerieux R Rossignol A Chopard A Carnino JF Marini T Letellier JP Delage 2006 Structural organization of the perimysium in bovine skeletal muscle: junctional plates and associated intracellular subdomains J. Struct. Biol. 154 206 216 10.1016/j.jsb.2006.01.002 1:STN:280:DC%2BD283isV2isw%3D%3D 16503167
36. PP Purslow 2002 The structure and functional significance of variations in the connective tissue within muscle Comp. Biochem. Physiol. A 133 947 966 10.1016/S1095-6433(02)00141-1 (Pubitemid 35463155)
37. G Saab TR Thompson GD Marsh 1999 Multicomponent T2 relaxation of in vivo skeletal muscle Magn. Reson. Med. 42 150 157 10.1002/(SICI)1522-2594(199907)42: 1<150::AID-MRM20>3.0.CO;2-5 1:STN:280:DyaK1MzjsVCksw%3D%3D 10398961 (Pubitemid 29325624)
38. G Saab TR Thompson GD Marsh PA Picot GR Moran 2001 Two-dimensional time correlation relaxometry of skeletal muscle in vivo at 3 Tesla Magn. Reson. Med. 46 1093 1098 10.1002/mrm.1304 1:STN:280:DC%2BD3Mnps12hsw%3D%3D 11746574 (Pubitemid 33104297)
39. T Saotome M Sekino F Eto S Ueno 2006 Evaluation of diffusional anisotropy and microscopic structure in skeletal muscles using magnetic resonance Magn. Reson. Imag. 24 19 25 10.1016/j.mri.2005.09.009 (Pubitemid 43061199)
40. PN Sen C Scala MH Cohen 2006 A self-similar model for sedimentary rocks with application to the dielectric constant of fused glass beads Geophysics 46 781 795 10.1190/1.1441215
41. S Sinha U Sinha VR Edgerton 2006 In vivo diffusion tensor imaging of the human calf muscle J. Magn. Reson. Imag. 24 182 190 10.1002/jmri.20593
42. U Sinha L Yao 2002 In vivo diffusion tensor imaging of human calf muscle J. Magn. Reson. Imag. 15 87 95 10.1002/jmri.10035 (Pubitemid 34008151)
43. SK Song N Shimada PJ Anderson 1963 Orthogonal diameters in the analysis of muscle fiber and form Nature 200 1220 1221 10.1038/2001220a0 1:STN:280:DyaF2c%2FkslGqtQ%3D%3D 14089928
44. GJ Stanisz A Szafer GA Wright RM Henkelman 1997 An analytical model of restricted diffusion in bovine optic nerve Magn. Reson. Med. 37 103 111 10.1002/mrm.1910370115 1:STN:280:DyaK2s7jtlansw%3D%3D 8978638 (Pubitemid 27008836)
45. RS Staron WJ Kraemer RS Hikida AC Fry JD Murray GE Campos 1999 Fibre type composition of four hindlimb muscles of adult Fisher 344 rats Histochem. Cell Biol. 111 117 123 10.1007/s004180050341 1:CAS:528:DyaK1MXlvVWqtw%3D%3D 10090572 (Pubitemid 29148251)
46. G Steidle F Schick 2006 Echoplanar diffusion tensor imaging of the lower leg musculature using eddy current nulled stimulated echo preparation Magn. Reson. Med. 55 541 548 10.1002/mrm.20780 1:STN:280:DC%2BD287gvFamsQ%3D%3D 16450364 (Pubitemid 43352552)
47. JA Trotter 1991 Dynamic shape of tapered skeletal muscle fibers J. Morphol. 207 221 223 10.1002/jmor.1052070212
48. JA Trotter PP Purslow 1992 Functional morphology of the endomysium in series fibered muscles J. Morphol. 212 109 122 10.1002/jmor.1052120203 1:STN:280:DyaK38zgtVOksA%3D%3D 1608046
49. WY Tseng VJ Weeden TG Reese RN Smith EF Halpern 2003 Diffusion tensor MRI of myocardial fibers and sheets: correspondence with visible cut-face texture J. Magn. Reson. Imag. 17 31 42 10.1002/jmri.10223 (Pubitemid 36034133)
50. CC van Donkelaar PJB Willems AMM Muijtjens MR Drost 1999 Skeletal muscle transverse strain during isometric contraction at different lengths J. Biomech. 32 755 762 10.1016/S0021-9290(99)00073-1 10433416 (Pubitemid 29287096)
51. HM Venema J Overweg 1974 Analysis of the size and shape of cross-sections of muscle fibers Med. Biol. Eng. 12 681 692 10.1007/BF02477231 1:STN:280:DyaE28%2FgvFWrtg%3D%3D 4465590
52. D Vincensini V Dedieu JP Renou P Otal F Joffre 2003 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 10.1016/S0730-725X(02)00638-0 1:STN:280:DC%2BD3s7lsFSktA%3D%3D (Pubitemid 36418726)
53. VJ Wedeen TG Reese VJ Napadow RJ Gilbert 2001 Demonstration of primary and secondary muscle fiber architecture of the bovine tongue by diffusion tensor magnetic resonance imaging Biophys. J. 80 1024 1028 10.1016/S0006-3495(01) 76081-X 1:CAS:528:DC%2BD3MXkvFSqsrc%3D 11159469
54. SD Zimmerman J Criscione JW Covell 2004 Remodeling in myocardium adjacent to an infarction in the pig left ventricle Am. J. Physiol. Heart Circ. Physiol. 287 H2697 H2704 10.1152/ajpheart.00160.2004 1:CAS:528:DC%2BD2cXhtVOmurbE 15319211 (Pubitemid 39557142)