Nian Wang1, Gary Cofer1, Louis E. DeFrate2, Abigail Holt2, Amy L. McNulty2, Yi Qi1, Charles E. Spritzer1, and G. Allan Johnson1
1Department of Radiology, Duke University, Durham, NC, United States, 2Department of Orthopaedic Surgery, Duke University, Durham, NC, United States
Synopsis
Application of diffusion magnetic resonance
imaging (dMRI) to map the complex collagen fibril structures of meniscus is
still challenging, due to the short T2/T2* values, low fractional anisotropy (FA)
values, and relatively low signal-to-noise (SNR). In this study, we imaged the porcine
menisci in a preclinical 7 T system with relatively short echo time (TE ~ 11 ms). A 3D
diffusion-weighted spin-echo pulse sequence was used for whole meniscus
tractography at 125 µm isotropic resolution.
Purpose
To evaluate the
complex collagen fiber distributions of porcine meniscus using diffusion magnetic
resonance imaging (dMRI) at high angular resolution. Introduction
The
meniscus, a fibrocartilaginous cartilage, has a unique collagen structure
orientation with three different layers (superficial, the lamellar, and deep
layer)1. Both superficial
layer and lamellar layer contain randomly orientated collagen fibers, while the
deep layer consists of both circumferentially and randomly oriented fibers1. There are numerous crossing fibers
existing in all the layers of meniscus. This high-ordered structure has been
well studied using scanning electron microscopy and polarized light microscopy (PLM)2-3. Although these methods afford higher
spatial resolution than MRI, they are destructive and the images are often
presented in 2D instead of 3D. Alternatively, dMRI allows one to observe the
tissue microstructure nondestructively leveraging the
unique water molecular diffusion properties4. Revealing the complex crossing fiber network
may improve our understanding its intrinsic functions
for shock absorption, force transmission, and stability within the knee joint3,5.Methods
Two medial menisci were harvested from
skeletally mature porcine knee joints obtained from a local abattoir. Scan were
performed using a 3D Stejskal-Tanner diffusion-weighted spin-echo pulse
sequence at 7.0 T with parameters as follows: matrix size = 192 × 120 × 80, FOV
= 48 × 30× 20 mm3, TE = 10.9 ms, TR = 100 ms, 81 unique diffusion
directions with a b value of 1000 s/mm2 and 8 non-diffusion-weighted
(b0) measurements. All
the diffusion-weighted images (DWIs) were registered to the baseline images
(b0) to correct for eddy currents. The DTI model was used to characterize the
primary diffusion direction of the fiber in meniscus. The scalar indices
including FA and MD (mean diffusivity) were also calculated. The model-free
generalized q-sampling imaging method (GQI) was used to quantify the diffusing
water at different orientations6.
Both DTI and GQI were used for resolving fiber orientations and the whole
meniscus tractography was generated using GQI method.Results
Figure 1 shows the representative b0 (a), FA (b),
Color-FA (c), MD (d), and diffusion weighted images (DWI, e) at 125
µm isotropic resolution. The image intensity variation of meniscus is apparent
in b0 image (red and green arrows, a), MD image (d), and DWI image (e). The FA
values also vary at different part of the meniscus, probably due to the fiber
orientations and fiber densities. The fiber direction can be distinguished in
the Color-FA image by different colors (c). Figure 2 shows the FA (a)
and MD (b) values at different regions of meniscus. These values are derived
from the ROIs delineated in b0 images (a) by different colors. The FA values
vary from 0.05 to 0.40, while the MD values vary from 0.63 to 1.26 x 10-3
mm2/s. Figure 3 demonstrates the fiber orientation images of
meniscus resolved by DTI (a-d) and GQI (e-h). Compared
to DTI, there are numerous crossing fibers existing in meniscus using GQI.
Crossing fibers are shown in all the 3 ROIs (green boxes, e), while region 3 is
dominated by the crossing fibers. Figure 4 illustrates the whole meniscus
tractography with complex fiber distributions, where the radial fibers,
circumferential fibers, and cross fibers can be resolved by GQI method.Discussion and Conclusion
This study demonstrates that both FA and MD
values exhibit strong inhomogeneity in different regions of meniscus. The lower
FA regions may be related to the complex fiber distributions. High angular
resolution dMRI can nondestructively characterize the complex collagen fiber
orientations and architectures of meniscus. The diffusion tractography further
helps to visualize the ultrastructure and quantifying integrity of fibril
collagen network. The dMRI may help
visualize complex meniscal tears that are challenging with conventional imaging
and this
capacity can provide unique insight in animal studies of degenerative joint
disease.Acknowledgements
This work was supported
by NIH/NIBIB P41 EB015897, NIH
1R01NS096720-01A1, NIH AR073221, Orthopaedic Research and
Education Foundation Grant with Funding Provided by the Musculoskeletal
Transplant Foundation, and Charles
E. Putman MD Vision Award of the Department of Radiology, Duke University
School of Medicine. References
1. Petersen W, Tillmann B. Collagenous fibril texture of the
human knee joint menisci. Anat Embryol (Berl) 1998;197(4):317-324.
2. Steele JAM, McCullen SD, Callanan A, Autefage H, Accardi MA,
Dini D, Stevens MM. Combinatorial scaffold morphologies for zonal articular
cartilage engineering. Acta Biomater 2014;10(5):2065-2075.
3. Li Q, Qu FN, Han B, Wang C, Li H, Mauck RL, Han L.
Micromechanical anisotropy and heterogeneity of the meniscus extracellular
matrix. Acta Biomater 2017;54:356-366.
4. Wang N, Mirando AJ, Cofer G, Qi Y, Hilton MJ, Johnson GA.
Diffusion tractography of the rat knee at microscopic resolution. Magnetic
resonance in medicine 2019;81(6):3775-3786.Sweigart MA, Athanasiou KA. Toward
tissue engineering of the knee meniscus. Tissue Eng 2001;7(2):111-129.
5. Sweigart MA, Athanasiou KA. Toward tissue engineering of the
knee meniscus. Tissue Eng 2001;7(2):111-129.
6. Yeh
FC, Wedeen VJ, Tseng WY. Generalized q-sampling imaging. IEEE Trans Med Imaging
2010;29(9):1626-1635.