Diffusion Tensor Imaging and Diffusion Modeling: Application to Monitoring Changes in the Medial Gastrocnemius in Disuse Atrophy Induced by Unilateral Limb Suspension

Overview

Journal J Magn Reson Imaging

Date 2018 Dec 21

PMID 30569482

Citations 13

Authors

Vadim Malis

Usha Sinha

Robert Csapo

Marco Narici

Edward Smitaman

Shantanu Sinha

Affiliations

Soon will be listed here.

Abstract

Background: Diffusion tensor imaging (DTI) assesses underlying tissue microstructure, and has been applied to studying skeletal muscle. Unloading of the lower leg causes decreases in muscle force, mass, and muscle protein synthesis as well as changes in muscle architecture.

Purpose: To monitor the change in DTI indices in the medial gastrocnemius (MG) after 4-week unilateral limb suspension (ULLS) and to explore the feasibility of extracting tissue microstructural parameters based on a two-compartment diffusion model.

Study Type: Prospective cohort study.

Subjects: Seven moderately active subjects (29.1 ± 5.7 years).

Field Strength/sequence: 3T, single-shot fat-suppressed echo planar spin echo sequence.

Assessment: Suspension-related changes in the DTI indices (eigenvalues: λ , λ , λ , fractional anisotropy; coefficient of planarity) were statistically analyzed. Changes in model-derived tissue parameters (muscle fiber circularity and diameter, intracellular volume fraction, and residence time) after suspension are qualitatively discussed.

Statistical Tests: Changes in the DTI indices of the MG between pre- and postsuspension were assessed using repeated-measures two-way analysis of variance (ANOVA).

Results: All the eigenvalues (λ : P = 0.025, λ : P = 0.035, λ : P = 0.049) as well as anisotropic diffusion coefficient (P = 0.029) were significantly smaller post-ULLS. Diffusion modeling revealed that fibers were more circular (circularity index increased from 0.55 to 0.95) with a smaller diameter (diameter decreased from 82-60 μm) postsuspension.

Data Conclusion: We have shown that DTI indices change with disuse and modeling can relate these voxel level changes to changes in the tissue microarchitecture.

Level Of Evidence: 2 Technical Efficacy: Stage 1 J. Magn. Reson. Imaging 2018.

Citing Articles

Magnetic Resonance Imaging Biomarkers of Muscle.

Sinha U, Sinha S Tomography. 2024; 10(9):1411-1438.

PMID: 39330752 PMC: 11436019. DOI: 10.3390/tomography10090106.

Impact of Deep Learning Denoising Algorithm on Diffusion Tensor Imaging of the Growth Plate on Different Spatial Resolutions.

Santos L, Hsu H, Nelson Jr R, Sullivan B, Shin J, Fung M Tomography. 2024; 10(4):504-519.

PMID: 38668397 PMC: 11054892. DOI: 10.3390/tomography10040039.

Compositional and Functional MRI of Skeletal Muscle: A Review.

Hooijmans M, Schlaffke L, Bolsterlee B, Schlaeger S, Marty B, Mazzoli V J Magn Reson Imaging. 2023; 60(3):860-877.

PMID: 37929681 PMC: 11070452. DOI: 10.1002/jmri.29091.

Impact of different ground-based microgravity models on human sensorimotor system.

Saveko A, Bekreneva M, Ponomarev I, Zelenskaya I, Riabova A, Shigueva T Front Physiol. 2023; 14:1085545.

PMID: 36875039 PMC: 9974674. DOI: 10.3389/fphys.2023.1085545.

Association of vastus lateralis diffusion properties with in vivo quadriceps contractile function in premenopausal women.

Carpenter R, Samaan M, Clasey J, Butterfield T, Gao F, Hardy P Scand J Med Sci Sports. 2022; 33(3):213-223.

PMID: 36337008 PMC: 9928607. DOI: 10.1111/sms.14266.

References

Saab G, Thompson R, Marsh G . Multicomponent T2 relaxation of in vivo skeletal muscle. Magn Reson Med. 1999; 42(1):150-7. DOI: 10.1002/(sici)1522-2594(199907)42:1<150::aid-mrm20>3.0.co;2-5. View

Riley D, Bain J, Thompson J, Fitts R, Widrick J, Trappe S . Decreased thin filament density and length in human atrophic soleus muscle fibers after spaceflight. J Appl Physiol (1985). 2000; 88(2):567-72. DOI: 10.1152/jappl.2000.88.2.567. View

Behan W, Cossar D, Madden H, McKay I . Validation of a simple, rapid, and economical technique for distinguishing type 1 and 2 fibres in fixed and frozen skeletal muscle. J Clin Pathol. 2002; 55(5):375-80. PMC: 1769641. DOI: 10.1136/jcp.55.5.375. View

Ohira Y, Yoshinaga T, Nomura T, Kawano F, Ishihara A, Nonaka I . Gravitational unloading effects on muscle fiber size, phenotype and myonuclear number. Adv Space Res. 2003; 30(4):777-81. DOI: 10.1016/s0273-1177(02)00395-2. View

Rolland Y, Lauwers-Cances V, Cournot M, Nourhashemi F, Reynish W, Riviere D . Sarcopenia, calf circumference, and physical function of elderly women: a cross-sectional study. J Am Geriatr Soc. 2003; 51(8):1120-4. DOI: 10.1046/j.1532-5415.2003.51362.x. View

Trappe S, Trappe T, Gallagher P, Harber M, Alkner B, Tesch P . Human single muscle fibre function with 84 day bed-rest and resistance exercise. J Physiol. 2004; 557(Pt 2):501-13. PMC: 1665105. DOI: 10.1113/jphysiol.2004.062166. View

Rosset A, Spadola L, Ratib O . OsiriX: an open-source software for navigating in multidimensional DICOM images. J Digit Imaging. 2004; 17(3):205-16. PMC: 3046608. DOI: 10.1007/s10278-004-1014-6. View

Galban C, Maderwald S, Uffmann K, Ladd M . A diffusion tensor imaging analysis of gender differences in water diffusivity within human skeletal muscle. NMR Biomed. 2005; 18(8):489-98. DOI: 10.1002/nbm.975. View

de Boer M, Maganaris C, Seynnes O, Rennie M, Narici M . Time course of muscular, neural and tendinous adaptations to 23 day unilateral lower-limb suspension in young men. J Physiol. 2007; 583(Pt 3):1079-91. PMC: 2277190. DOI: 10.1113/jphysiol.2007.135392. View

10.

Seynnes O, Maganaris C, de Boer M, di Prampero P, Narici M . Early structural adaptations to unloading in the human calf muscles. Acta Physiol (Oxf). 2008; 193(3):265-74. DOI: 10.1111/j.1748-1716.2008.01842.x. View

11.

Assaf Y, Blumenfeld-Katzir T, Yovel Y, Basser P . AxCaliber: a method for measuring axon diameter distribution from diffusion MRI. Magn Reson Med. 2008; 59(6):1347-54. PMC: 4667732. DOI: 10.1002/mrm.21577. View

12.

Zhang J, Zhang G, Morrison B, Mori S, Sheikh K . Magnetic resonance imaging of mouse skeletal muscle to measure denervation atrophy. Exp Neurol. 2008; 212(2):448-57. PMC: 2532826. DOI: 10.1016/j.expneurol.2008.04.033. View

13.

Aja-Fernandez S, Niethammer M, Kubicki M, Shenton M, Westin C . Restoration of DWI data using a Rician LMMSE estimator. IEEE Trans Med Imaging. 2008; 27(10):1389-403. PMC: 2756835. DOI: 10.1109/TMI.2008.920609. View

14.

Tristan-Vega A, Aja-Fernandez S . Joint LMMSE estimation of DWI data for DTI processing. Med Image Comput Comput Assist Interv. 2008; 11(Pt 2):27-34. DOI: 10.1007/978-3-540-85990-1_4. View

15.

Karampinos D, King K, Sutton B, Georgiadis J . Myofiber ellipticity as an explanation for transverse asymmetry of skeletal muscle diffusion MRI in vivo signal. Ann Biomed Eng. 2009; 37(12):2532-46. PMC: 6617521. DOI: 10.1007/s10439-009-9783-1. View

16.

Englund E, Elder C, Xu Q, Ding Z, Damon B . Combined diffusion and strain tensor MRI reveals a heterogeneous, planar pattern of strain development during isometric muscle contraction. Am J Physiol Regul Integr Comp Physiol. 2011; 300(5):R1079-90. PMC: 3094039. DOI: 10.1152/ajpregu.00474.2010. View

17.

Horstman A, de Ruiter C, van Duijnhoven N, Hopman M, de Haan A . Changes in muscle contractile characteristics and jump height following 24 days of unilateral lower limb suspension. Eur J Appl Physiol. 2011; 112(1):135-44. PMC: 3253280. DOI: 10.1007/s00421-011-1958-4. View

18.

Jenkinson M, Beckmann C, Behrens T, Woolrich M, Smith S . FSL. Neuroimage. 2011; 62(2):782-90. DOI: 10.1016/j.neuroimage.2011.09.015. View

19.

Buford T, Lott D, Marzetti E, Wohlgemuth S, Vandenborne K, Pahor M . Age-related differences in lower extremity tissue compartments and associations with physical function in older adults. Exp Gerontol. 2011; 47(1):38-44. PMC: 3245356. DOI: 10.1016/j.exger.2011.10.001. View

20.

Sigmund E, Sui D, Ukpebor O, Baete S, Fieremans E, Babb J . Stimulated echo diffusion tensor imaging and SPAIR T2 -weighted imaging in chronic exertional compartment syndrome of the lower leg muscles. J Magn Reson Imaging. 2013; 38(5):1073-82. PMC: 3664655. DOI: 10.1002/jmri.24060. View