Cyril Tous, PhD1, Alexandre Jodoin, MD2, Detlev Grabs, MD, PhD3, Elijah Van Houten, PhD4, and Nathalie J Bureau, MD MSc FRCP(C)1,2
1Radiology, Centre de recherche du Centre hospitalier de l’Université de Montréal, Montreal, QC, Canada, 2Radiology, Centre hospitalier de l’Université de Montréal, Montréal, QC, Canada, 3Anatomy, Université du Québec à Trois-Rivières, Trois-Rivières, QC, Canada, 4Mechanical Engineering, Université de Sherbrooke, Sherbrooke, QC, Canada
Synopsis
Surgical planning of rotator cuff tears does not benefit from
quantitative measurement of muscles stiffness and microstructure leading to
retears in the following years. Since stiffness is dependent on anisotropy,
Diffusion Tensor Imaging can simplify the inversion algorithm of Magnetic
resonance elastography. Repeatability of DTI metrics from three scans
in six shoulders of six asymptomatic volunteers was achieved (coefficient of
variance <10%) for the fractional anisotropy, mean diffusivity, mode and
eigenvalues. Clear convergence of myocytes to the tendons was observed with
tractography in the supraspinatus as known in dissection. This MRI protocol is
promising for developing biomarkers for surgical planning.
Introduction
Surgical planning of rotator cuff tears does not benefit from
quantitative measurement of muscles stiffness and microstructure leading to
retears in the following years. Since stiffness is dependent on anisotropy,
Diffusion Tensor Imaging can simplify the inversion algorithm of Magnetic
resonance elastography. Repeatability of DTI metrics from three scans
in six shoulders of six asymptomatic volunteers was achieved (coefficient of
variance <10%) for the fractional anisotropy, mean diffusivity, mode and
eigenvalues. Clear convergence of myocytes to the tendons was observed with
tractography in the supraspinatus as
known in dissection. This MRI protocol is promising for developing biomarkers
for surgical planning. Methods
Six shoulders of six volunteers (median=41, IQR=13 years)
were scanned at 3T with DTI at b=0s/mm²
(2averages), 12 diffusion-encoding gradients at b=500 s/mm² (2averages), b=800
s/mm² (4averages), TR=5.8s, TE=57ms, slices=46, voxel size=3x3x3 mm3, resolution=106,
FOV read=318. The supraspinatus (SSP) and infraspinatus (ISP) segmented from T1 vibe DIXON (TE=2.46ms,
TR=5.76ms, voxel=1x1x1mm3 and FOV=320) were rigidly
coregistered with MrTrix3[7]. One way analysis of variance (ANOVA), pairwise comparison of
distribution, coefficient of variance (CV) and Bland-Altman analysis were used
to assess the repeatability within subjects of the three tensors eigenvalues (λ1,λ2,λ3) the fractional
anisotropy (FA), the mode and the apparent diffusion coefficient (ADC). Results
Across 6 volunteers, the ADC was higher in ISP than SSP with a CV inferior to 11% (Table 1). Mean FA was between
0.42 and 0.45 in SSP and ISP, with a CV inferior to 12%. One individual had CVADC and CVFA levels over 18% in 2/3 of tests. Bias and limit of
agreement in FA was 0 ± 0.071 and 0.005 ± 0.157 x10-3 mm2/s in ADC (Figure 1 and 2).
Pairwise comparison of repeated tests (1-2, 1-3, 2-3) of
eigenvalues showed nonsignificant difference (p>0.05) in 3/6 volunteers for the SSP and 5/6 volunteers between test 2 and 3. Pairwise comparison of
eigenvalues demonstrates significant difference and between the ISP and SSP. Thus, tractography could be achieved in the ISP and the SSP showing interleaved tracks
in the ISP and organized tracks in the SSP (Figure 3 and 4). The mean λ1 is in average 2.80±0.63 times higher in the ISP than
in the SSP across volunteers and tests.
Discussion
Our results are
consistent with other inter and intra scanner studies performing DTI in muscles[8,9,10]. Single scanner study on myocardial DTI reported CVADC of 19% and 7.2% for CVFA [8,9], while in the upper
leg had CVADC reported at 4.5% and CVFA at 15.2% [10]. DTI metrics in the
ISP are reproducible according to the bias and level of agreement in the
Bland-Altman plot, and from CV values based
on the mean and standard deviation, but reproducibility fails for ANOVA of the
DTI metric in the ISP. The SSP has a “fishbone” like structure where the
insertion angle between the myocytes and the bundle separation is consistent (Figure 4)
while the ISP has a more complex microstructure with interleaved myocytes (low
FA at 0.45) (Figure 3) and inhomogeneity proximal to the lungs which may
explain the lower repeatability of the eigenvalues in this muscle.Conclusion
The bland-Altman analysis showed good
repeatability (CV<10%) of ADC and FA which is promising for establishing DTI
biomarkers across volunteers and scanners that will allow the identification of
structural characteristics of RC tears.Acknowledgements
Québec Bio-Imaging Network Pilot Project #35450References
1.Gladstone, J. N., J. Y. Bishop,
I. K. Y. Lo, and E. L. Flatow. Fatty Infiltration and Atrophy of the Rotator
Cuff do not Improve after Rotator Cuff Repair and Correlate with Poor
Functional Outcome. Am. J. Sports Med. 35:719–728, 2007.
2. Karampinos, D. C., C. Holwein,
S. Buchmann, T. Baum, S. Ruschke, A. S. Gersing, R. Sutter, A. B. Imhoff, E. J.
Rummeny, and P. M. Jungmann. Proton Density Fat-Fraction of Rotator Cuff
Muscles Is Associated With Isometric Strength 10 Years After Rotator Cuff
Repair: A Quantitative Magnetic Resonance Imaging Study of the Shoulder. Am. J.
Sports Med. 45:1990–1999, 2017.
3.
Lee, S., R. M. Lucas, D. A. Lansdown, L. Nardo, A. Lai, T. M. Link, R. Krug,
and C. B. Ma. Magnetic resonance rotator cuff fat fraction and its
relationship with tendon tear severity and subject characteristics. J. Shoulder
Elb. Surg. 24:1442–1451, 2015.
4. Colvin, A. C., N. Egorova, A. K. Harrison, A. Moskowitz, and E.
L. Flatow. National trends in rotator cuff repair. J. Bone Joint Surg. Am.
94:227–33, 2012.
5. McElvany, M. D., E. McGoldrick, A. O. Gee, M. B. Neradilek, and
F. A. Matsen. Rotator cuff repair: published evidence on factors associated
with repair integrity and clinical outcome. Am. J. Sports Med. 43:491–500,
2015.
6. Anderson, A. T., E. E. W. Van Houten, M. D. J. McGarry, K. D.
Paulsen, J. L. Holtrop, B. P. Sutton, J. G. Georgiadis, and C. L. Johnson.
Observation of direction-dependent mechanical properties in the human brain
with multi-excitation MR elastography. J. Mech. Behav. Biomed. Mater.
59:538–546, 2016.
7.
Tournier, J.-D., R. Smith, D. Raffelt, R. Tabbara, T. Dhollander, M. Pietsch,
D. Christiaens, B. Jeurissen, C.-H. Yeh, and A. Connelly. MRtrix3: A fast,
flexible and open software framework for medical image processing and visualisation.
, 2019.doi:10.1016/j.neuroimage.2019.116137
8. Grech‐Sollars, M., P. W. Hales, K. Miyazaki, F. Raschke, D.
Rodriguez, M. Wilson, S. K. Gill, T. Banks, D. E. Saunders, J. D. Clayden, M.
N. Gwilliam, T. R. Barrick, P. S. Morgan, N. P. Davies, J. Rossiter, D. P.
Auer, R. Grundy, M. O. Leach, F. A. Howe, A. C. Peet, and C. A. Clark.
Multi‐centre reproducibility of diffusion MRI parameters for clinical sequences
in the brain. NMR Biomed. 28:468–485, 2015.
9. McGill, L.-A., T. F. Ismail, S. Nielles-Vallespin, P. Ferreira,
A. D. Scott, M. Roughton, P. J. Kilner, S. Y. Ho, K. P. McCarthy, P. D.
Gatehouse, R. de Silva, P. Speier, T. Feiweier, C. Mekkaoui, D. E. Sosnovik, S.
K. Prasad, D. N. Firmin, and D. J. Pennell. Reproducibility of in-vivo
diffusion tensor cardiovascular magnetic resonance in hypertrophic
cardiomyopathy. J. Cardiovasc. Magn. Reson. 14:86, 2012.
10. Monte, J. R., M. T. Hooijmans, M. Froeling, J. Oudeman, J. L.
Tol, M. Maas, G. J. Strijkers, and A. J. Nederveen. The repeatability of
bilateral diffusion tensor imaging (DTI) in the upper leg muscles of healthy
adults. Eur. Radiol. 30:1709–1718, 2020.