Time-dependent diffusion in skeletal muscle with the random permeable barrier model (RPBM): Application to normal controls and chronic exertional compartment syndrome patients

NMR in Biomedicine

Volumn 27, Issue 5, 2014, Pages 519-528

  Sigmund, Eric E ^a   Novikov, Dmitry S ^a   Sui, Dabang ^a,b   Ukpebor, Obehi ^a,c   Baete, Steven ^a   Babb, James S ^a   Liu, Kecheng ^d   Feiweier, Thorsten ^e   Kwon, Jane ^a   Mcgorty, Kellyanne ^a,f   Bencardino, Jenny ^a   Fieremans, Els ^a  

^a NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

^b Shanghai Tongyue Leasing Co Ltd   (China)

^c CITY COLLEGE OF NEW YORK   (United States)

^d SIEMENS CORPORATE RESEARCH   (United States)

^e SIEMENS AG   (Germany)

^f Department of Orthopaedic Surgery   (United States)

Author keywords

Chronic exertional compartment syndrome; DTI; Exercise; Random permeable barrier model; Skeletal muscle; Stimulated echo; Time dependent diffusion

Indexed keywords

DIFFUSION TENSOR IMAGING; ESTIMATION; FIBERS; MAGNETIC RESONANCE IMAGING; MUSCLE; TENSORS;

COMPARTMENT SYNDROMES; DTI; EXERCISE; PERMEABLE BARRIER; SKELETAL MUSCLE; STIMULATED ECHOS; TIME-DEPENDENT DIFFUSION;

DIFFUSION BARRIERS;

ADOLESCENT; ADULT; ARTICLE; AUTOPSY; BIOPHYSICS; CHRONIC DISEASE; CHRONIC EXERTIONAL COMPARTMENT SYNDROME; CLINICAL ARTICLE; COMPARTMENT SYNDROME; CONTROLLED STUDY; DIFFUSION; DIFFUSION TENSOR IMAGING; ECHO PLANAR IMAGING; FEMALE; GASTROCNEMIUS MUSCLE; HUMAN; HUMAN TISSUE; IMAGING PHANTOM; MALE; MODEL; MUSCLE CELL; NUCLEAR MAGNETIC RESONANCE SCANNER; PERMEABILITY BARRIER; PRIORITY JOURNAL; RANDOM PERMEABLE BARRIER MODEL; REDUCTION; SIGNAL NOISE RATIO; SURFACE PROPERTY; TIME; TREADMILL EXERCISE; BIOLOGICAL MODEL; CASE CONTROL STUDY; CLINICAL TRIAL; EXERCISE; IMAGE QUALITY; PATHOLOGY; PERMEABILITY; SKELETAL MUSCLE; YOUNG ADULT;

ADOLESCENT; ADULT; CASE-CONTROL STUDIES; CHRONIC DISEASE; COMPARTMENT SYNDROMES; DIFFUSION; FEMALE; HUMANS; MALE; MODELS, BIOLOGICAL; MUSCLE, SKELETAL; PERMEABILITY; PHANTOMS, IMAGING; PHYSICAL EXERTION; SIGNAL-TO-NOISE RATIO; TIME FACTORS; YOUNG ADULT;

EID: 84897964765     PISSN: 09523480     EISSN: 10991492     Source Type: Journal    
DOI: 10.1002/nbm.3087     Document Type: Article

References (55)

1. Sinha S, Sinha U, Edgerton VR. In vivo diffusion tensor imaging of the human calf muscle. J. Magn. Reson. Imaging 2006; 24(1): 182-190.
2. Galban CJ, Maderwald S, Uffmann K, de Greiff A, Ladd ME. Diffusive sensitivity to muscle architecture: a magnetic resonance diffusion tensor imaging study of the human calf. Eur. J. Appl. Physiol. 2004; 93(3): 253-262.
3. Heemskerk AM, Drost MR, van Bochove GS, van Oosterhout MFM, Nicolay K, Strijkers GJ. DTI-based assessment of ischemia-reperfusion in mouse skeletal muscle. Magn. Reson. Med. 2006; 56(2): 272-281.
4. Zaraiskaya T, Kumbhare D, Noseworthy MD. Diffusion tensor imaging in evaluation of human skeletal muscle injury. J. Magn. Reson. Imaging 2006; 24(2): 402-408.
5. Blackman PG. A review of chronic exertional compartment syndrome in the lower leg. Med. Sci. Sports Exerc. 2000; 32(3): S4-S10.
6. Kiuru MJ, Mantysaari MJ, Pihlajamaki HK, Ahovuo JA. Evaluation of stress-related anterior lower leg pain with magnetic resonance imaging and intracompartmental pressure measurement. Milit. Med. 2003; 168(1): 48-52.
7. Litwiller D, Amrami K, Dahm D, Smith J, Laskowski E, Stuart M, Felmlee J. Chronic exertional compartment syndrome of the lower extremities: improved screening using a novel dual birdcage coil and in-scanner exercise protocol. Skeletal Radiol. 2007; 36(11): 1067-1075.
8. Andreisek G, White LM, Sussman MS, Langer DL, Patel C, Su JWS, Haider MA, Stainsby JA. T2*-weighted and arterial spin labeling MRI of calf muscles in healthy volunteers and patients with chronic exertional compartment syndrome: preliminary experience. Am. J. Roentgenol. 2009; 193(4): W327-W333.
9. Saab G, Thompson RT, Marsh GD. Multicomponent T2 relaxation of in vivo skeletal muscle. Magn. Reson. Med. 1999; 42(1): 150-157.
10. 2 relaxation decay curves in a rat muscle edema model: decay curve components and water compartments. Magn. Reson. Med. 2005; 54(3): 524-531.
11. 2-weighted imaging in chronic exertional compartment syndrome of the lower leg muscles. J. Magn. Reson. Imaging 2013; 38(5): 1073-1082.
12. Fordham EJ, Gibbs SJ, Hall LD. Partially restricted diffusion in a permeable sandstone: observations by stimulated echo PFG NMR. Magn. Reson. Imaging 1994; 12: 279-284.
13. Latour LL, Mitra PP, Kleinberg RL, Sotak CH. Time-dependent diffusion coefficient of fluids in porous media as a probe of surface-to-volume ratio. J. Magn. Reson. A 1993; 101: 342-346.
14. Sen PN, Schwartz LM, Mitra PP, Halperin BI. Surface relaxation and the long-time diffusion coefficient in porous media: periodic geometries. Phys. Rev. B 1994; 49: 215.
15. Sen PN. Time-dependent diffusion coefficient as a probe of geometry. Concepts Magn. Reson. A 2004; 23A(1): 1-21.
16. Hurlimann MD, Helmer KG, Latour LL, Sotak CH. Restricted diffusion in sedimentary rocks. Determination of surface-to-volume ratio and surface relaxivity. J. Magn. Reson. A 1994; 111: 169-178.
17. Sigmund EE, Cho H, Chen P, Byrnes S, Song Y-Q, Guo XE, Brown TR. Diffusion-based MR methods for bone structure and evolution. Magn. Reson. Med. 2008; 59(1): 28-39.
18. Mair RW, Sen MN, Hurlimann MD, Patz S, Cory DG, Walsworth RL. The narrow pulse approximation and long length scale determination in xenon gas diffusion NMR studies of model porous media. J. Magn. Reson. 2002; 156(2): 202-212.
19. Helmer KG, Dardzinski BJ, Sotak CH. The application of porous-media theory to the investigation of time-dependent diffusion in in vivo systems. NMR Biomed. 1995; 8: 297-306.
20. Latour LL, Svoboda K, Mitra PP, Sotak CH. Time-dependent diffusion of water in a biological model system. Proc. Natl. Acad. Sci. U. S. A. 1994; 91(4): 1229-1233.
21. Wang CB, Miller GW, Altes TA, de Lange EE, Cates GD, Mugler JP. Time dependence of He-3 diffusion in the human lung: measurement in the long-time regime using stimulated echoes. Magn. Reson. Med. 2006; 56(2): 296-309.
22. Peled S, Tseng CH, Sodickson AA, Mair RW, Walsworth RL, Cory DG. Single-shot diffusion measurement in laser-polarized gas. J. Magn. Reson. 1999; 140: 320-324.
23. Woods JC, Choong CK, Yablonskiy DA, Bentley J, Wong J, Pierce JA, Cooper JD, Macklem PT, Conradi MS, Hogg JC. Hyperpolarized He-3 diffusion MRI and histology in pulmonary emphysema. Magn. Reson. Med. 2006; 56(6): 1293-1300.
24. Kim S, Chi-Fishman G, Barnett AS, Pierpaoli C. Dependence on diffusion time of apparent diffusion tensor of ex vivo calf tongue and heart. Magn. Reson. Med. 2005; 54(6): 1387-1396.
25. Tanner JE. Self diffusion of water in frog muscle. Biophys. J. 1979; 28(1): 107-116.
26. Gabr RE, El-Sharkawy AM, Schar M, Weiss RG, Bottomley PA. High-energy phosphate transfer in human muscle: diffusion of phosphocreatine. Am. J. Physiol. Cell Physiol. 2011; 301(1): C234-241.
27. Schwenzer NF, Steidle G, Martirosian P, Schraml C, Springer F, Claussen CD, Schick F. Diffusion tensor imaging of the human calf muscle: distinct changes in fractional anisotropy and mean diffusion due to passive muscle shortening and stretching. NMR Biomed. 2009; 22(10): 1047-1053.
28. Steidle G, Schick F. Echoplanar diffusion tensor imaging of the lower leg musculature using eddy current nulled stimulated echo preparation. Magn. Reson. Med. 2006; 55(3): 541-548.
29. Fieremans E, Lemberskiy G, Jensen JH, Novikov DS. Observation of muscle fiber diameter increase with exercise using time-dependent diffusion. In: Proceedings of Scientific Meeting of International Society of Magnetic Resonance in Medicine, Salt Lake City, ISMRM, Berkeley, CA, USA, 2013; p. 489.
30. Novikov DS, Fieremans E, Jensen JH, Helpern JA. Random walks with barriers. Nat. Phys. 2011; 7(6): 508-514.
31. Mescher AL. Junqueira's Basic Histology. McGraw-Hill: New York; 2013.
32. Novikov DS, Jensen JH, Helpern JA, Fieremans E. Characterizing microstructure of living tissues with time-dependent diffusion. Proc. Nat. Acad. Sci. 2014, in press. Preprint available at arXiv:1210.3014; 2012.
33. Fieremans E, Novikov DS, Sigmund EE, Liu K, Jensen JH, Helpern JA. In vivo measurement of membrane permeability and fiber size in calf muscle using time-dependent DWI. In: Proceedings of Scientific Meeting, International Society for Magnetic Resonance in Medicine, Montreal, ISMRM, Berkeley, CA, USA, 2011; p. 1153,
34. Heemskerk AM, Sinha TK, Wilson KJ, Ding Z, Damon BM. Repeatability of DTI-based skeletal muscle fiber tracking. NMR Biomed. 2010; 23(3): 294-303.
35. Sinha S, Sinha U. Reproducibility analysis of diffusion tensor indices and fiber architecture of human calf muscles in vivo at 1.5 Tesla in neutral and plantarflexed ankle positions at rest. J. Magn. Reson. Imaging 2011; 34(1): 107-119.
36. Deux JF, Malzy P, Paragios N, Bassez G, Luciani A, Zerbib P, Roudot-Thoraval F, Vignaud A, Kobeiter H, Rahmouni A. Assessment of calf muscle contraction by diffusion tensor imaging. Eur. Radiol. 2008; 18(10): 2303-2310.
37. Karampinos DC, King KF, Sutton BP, Georgiadis JG. Myofiber ellipticity as an explanation for transverse asymmetry of skeletal muscle diffusion MRI in vivo signal. Ann. Biomed. Eng. 2009; 37(12): 2532-2546.
38. Karampinos DC, Banerjee S, King KF, Link TM, Majumdar S. Considerations in high-resolution skeletal muscle diffusion tensor imaging using single-shot echo planar imaging with stimulated-echo preparation and sensitivity encoding. NMR Biomed. 2012; 25(5): 766-778.
39. Basser PJ, Mattiello J, Lebihan D. Estimation of the effective self-diffusion tensor from the NMR spin-echo. J. Magn. Reson. B 1994; 103(3): 247-254.
40. Mattiello J, Basser PJ, LeBihan D. The b matrix in diffusion tensor echo-planar imaging. Magn. Reson. Med. 1997; 37(2): 292-300.
41. Kingsley PB. Introduction to diffusion tensor imaging mathematics: part II. Anisotropy, diffusion-weighting factors, and gradient encoding schemes. Concepts Magn. Reson. A 2006; 28A(2): 123-154.
42. Haacke EM, Brown RW, Thompson MR, Venkatesan R. Magnetic Resonance Imaging: Physical Principles and Sequence Design. Wiley: New York; 1999.
43. Polgar J, Johnson MA, Weightma D, Appleton D. Data on fiber size in 36 human muscles - autopsy study. J. Neurol. Sci. 1973; 19(3): 307-318.
44. Yanagisawa O, Kurihara T, Kobayashi N, Fukubayashi T. Strenuous resistance exercise effects on magnetic resonance diffusion parameters and muscle-tendon function in human skeletal muscle. J. Magn. Reson. Imaging 2011; 34(4): 887-894.
45. Morvan D, Leroy-Willig A. Simultaneous measurements of diffusion and transverse relaxation in exercising skeletal muscle. Magn. Reson. Imaging 1995; 13(7): 943-948.
46. Okamoto Y, Kunimatsu A, Kono T, Nasu K, Sonobe J, Minami M. Changes in MR diffusion properties during active muscle contraction in the calf. Magn. Reson. Med. Sci. 2010; 9(1): 1-8.
47. Hakkinen K, Pakarinen A, Kraemer WJ, Hakkinen A, Valkeinen H, Alen M. Selective muscle hypertrophy, changes in EMG and force, and serum hormones during strength training in older women. J. Appl. Physiol. 2001; 91(2): 569-580.
48. Ivey FM, Tracy BL, Lemmer JT, NessAiver M, Metter EJ, Fozard JL, Hurley BF. Effects of strength training and detraining on muscle quality: age and gender comparisons. J. Gerontol. A 2000; 55(3): B152-157; discussion B158-159.
49. Mero AA, Hulmi JJ, Salmijarvi H, Katajavuori M, Haverinen M, Holviala J, Ridanpaa T, Hakkinen K, Kovanen V, Ahtiainen JP, Selanne H. Resistance training induced increase in muscle fiber size in young and older men. Eur. J. Appl. Physiol. 2013; 113(3): 641-650.
50. Sinha-Hikim I, Artaza J, Woodhouse L, Gonzalez-Cadavid N, Singh AB, Lee MI, Storer TW, Casaburi R, Shen R, Bhasin S. Testosterone-induced increase in muscle size in healthy young men is associated with muscle fiber hypertrophy. Am. J. Physiol. Endocrinol. Metab. 2002; 283(1): E154-164.
51. Lundberg IE, Nader GA. Molecular effects of exercise in patients with inflammatory rheumatic disease. Nature Clin. Pract. Rheumatol. 2008; 4(11): 597-604.
52. Dastmalchi M, Alexanderson H, Loell I, Stahlberg M, Borg K, Lundberg IE, Esbjornsson M. Effect of physical training on the proportion of slow-twitch type I muscle fibers, a novel nonimmune-mediated mechanism for muscle impairment in polymyositis or dermatomyositis. Arthritis Rheum. 2007; 57(7): 1303-1310.
53. Hatakenaka M, Matsuo Y, Setoguchi T, Yabuuchi H, Okafuji T, Kamitani T, Nishikawa K, Honda H. Alteration of proton diffusivity associated with passive muscle extension and contraction. J. Magn. Reson. Imaging 2008; 27(4): 932-937.
54. Heemskerk AM, Sinha TK, Wilson KJ, Damon BM. Change in water diffusion properties with altered muscle architecture. In: Proceedings of Scientific Meeting, International Society for Magnetic Resonance in Medicine, Toronto, ISMRM, Berkeley, CA, USA, 2008; p. 1787.
55. Rominger MB, Lukosch CJ, Bachmann GF. MR imaging of compartment syndrome of the lower leg: a case control study. Eur. Radiol. 2004; 14(8): 1432-1439.