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Research Papers

Collagen Organization in Facet Capsular Ligaments Varies With Spinal Region and With Ligament Deformation

[+] Author and Article Information
Ehsan Ban

Department of Materials
Science and Engineering,
University of Pennsylvania,
211 LRSM,
3231 Walnut Street,
Philadelphia, PA 19104
e-mail: ehsan.ban@gmail.com

Sijia Zhang

Department of Bioengineering,
University of Pennsylvania,
240 Skirkanich Hall,
210 S. 33rd Street,
Philadelphia, PA 19104
e-mail: sijiaz@seas.upenn.edu

Vahhab Zarei

Department of Mechanical Engineering,
University of Minnesota—Twin Cities,
7-105 Nils Hasselmo Hall,
312 Church Street SE,
Minneapolis, MN 55455
e-mail: zarei004@umn.edu

Victor H. Barocas

Department of Biomedical Engineering,
University of Minnesota—Twin Cities,
7-105 Nils Hasselmo Hall,
312 Church Street SE,
Minneapolis, MN 55455
e-mail: baroc001@umn.edu

Beth A. Winkelstein

Departments of Bioengineering and Neurosurgery,
University of Pennsylvania,
240 Skirkanich Hall,
210 South 33rd Street,
Philadelphia, PA 19104
e-mail: winkelst@seas.upenn.edu

Catalin R. Picu

Department of Mechanical, Aerospace, and
Nuclear Engineering,
Rensselaer Polytechnic Institute,
2048 Jonsson Engineering Center,
110 8th Street,
Troy, NY 12180
e-mail: picuc@rpi.edu

1E. Ban, S. Zhang, and V. Zarei contributed equally to this work.

2Corresponding author.

Manuscript received December 15, 2016; final manuscript received February 1, 2017; published online June 6, 2017. Associate Editor: Kristen Billiar.

J Biomech Eng 139(7), 071009 (Jun 06, 2017) (9 pages) Paper No: BIO-16-1517; doi: 10.1115/1.4036019 History: Received December 15, 2016; Revised February 01, 2017

The spinal facet capsular ligament (FCL) is primarily comprised of heterogeneous arrangements of collagen fibers. This complex fibrous structure and its evolution under loading play a critical role in determining the mechanical behavior of the FCL. A lack of analytical tools to characterize the spatial anisotropy and heterogeneity of the FCL's microstructure has limited the current understanding of its structure–function relationships. Here, the collagen organization was characterized using spatial correlation analysis of the FCL's optically obtained fiber orientation field. FCLs from the cervical and lumbar spinal regions were characterized in terms of their structure, as was the reorganization of collagen in stretched cervical FCLs. Higher degrees of intra- and intersample heterogeneity were found in cervical FCLs than in lumbar specimens. In the cervical FCLs, heterogeneity was manifested in the form of curvy patterns formed by collections of collagen fibers or fiber bundles. Tensile stretch, a common injury mechanism for the cervical FCL, significantly increased the spatial correlation length in the stretch direction, indicating an elongation of the observed structural features. Finally, an affine estimation for the change of correlation length under loading was performed which gave predictions very similar to the actual values. These findings provide structural insights for multiscale mechanical analyses of the FCLs from various spinal regions and also suggest methods for quantitative characterization of complex tissue patterns.

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Figures

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Fig. 1

Anatomy and imaging of FCLs in the cervical and lumbar spinal regions. (a) Schematics showing the lateral view of the spine and vertebrae to demonstrate the overall anatomy of the cervical and lumbar facet joints and the location of the FCL in each spinal region. (b) The relevant anatomical and loading directions are labeled on the grayscale images of isolated cervical and lumbar FCLs positioned on the mechanical testing devices. (c) Orientation angles showing collagen alignment measurements using the quantitative polarized light imaging (QPLI) and polarization-sensitive optical coherence tomography (PS-OCT) for cervical and lumbar FCLs, respectively. TP: transverse process; SP: spinous process; IVD: intervertebral disk; VB: vertebral body; and SC: spinal cord.

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Fig. 2

Image-based spatial correlation analysis of collagen orientation in the facet capsular ligaments. (a) A representative vector plot showing the derived spatial collagen alignment from polarized light images (orientation and length of lines indicate the direction and strength of alignment) and relevant anatomical and loading directions for the spatial correlation calculation. (b) Isotropic (angle averaged) and ((c) and (d)) directional (along θ) correlations of orientation α were evaluated by averaging over pairs of points separated by δ. (e) Correlation length, c, was extracted by fitting an exponential function to the calculated autocorrelation.

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Fig. 3

Collagen fiber orientation in cervical FCLs. (a) Fiber orientation distribution and representative fiber alignment maps (from samples (b) C1, (c) C2, and (d) C7) demonstrate highly heterogeneous structures and large variability between different specimens. The single line arrows indicate directions across the joint. The orientation distribution functions in (a) were computed relative to the horizontal direction marked by 0.

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Fig. 4

Collagen fiber orientation in lumbar FCLs. Fiber orientation distribution (a) and representative fiber alignment maps (for samples L2 (b) and L5 (c)) show that the dominant fiber alignment is along the medial–lateral direction with varied local orientations. The single line arrows indicate the across-joint direction. The orientation distribution functions in (a) were computed relative to the horizontal direction marked by 0.

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Fig. 5

Spatial correlation of orientation in cervical and lumbar FCLs in the prestressed resting configuration. Representative autocorrelation curves are shown for (a) a cervical FCL (sample C2) and (b) a lumbar FCL (sample L3) in the across-joint direction, in the transverse direction, and averaged over all directions. Spatial correlation in both cervical and lumbar FCLs exhibits an initial drop within 1 mm. In the cervical region, correlations vanish beyond this distance, while in the lumbar samples correlations are longer ranged. (c) Comparison between correlation length, c, shows an overall significant difference due to anatomical region of the FCLs (p = 0.037). The correlation length in the cervical FCL is significantly smaller than that in the lumbar region in the average and transverse directions (*p < 0.022), indicating higher heterogeneity in the cervical FCLs compared with lumbar FCLs. Error bars indicate standard deviations.

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Fig. 6

Representative collagen fiber reorganization in a cervical FCL sample (C1) under uniaxial tension (applied in the vertical direction in this figure). (a) Representative regional fiber alignment maps show nonuniform fiber realignment with increasing deformation and a preferred re-orientation direction along the applied loading. (b) Representative correlation curves show more reorganization during stretch along the loading direction as compared to the horizontal direction or isotropic measurements.

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Fig. 7

Evolution of correlation lengths with the deformation of cervical FCLs. (a) Correlation length in the vertical direction at 3 mm displacement (1.55 stretch ratio on average) is significantly higher than both the vertical correlation length in the prestressed resting configuration (*p < 0.050) and horizontal correlation length of the deformed sample at same strain (#p < 0.006). Error bars indicate standard deviations. (b) Correlation length in the horizontal direction shows high sample-to-sample variability and no definite trend as the applied strain increases, whereas (c) vertical correlation length of all samples tends to increase with increasing macroscopic strain.

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Fig. 8

Comparison of the experimental correlation length with the prediction of the affine deformation model. The affine model assumes that the strains at each point inside the sample are identical to the macroscale, applied strains. The local reorientation was computed based on this assumption. A good agreement is observed with the measured data in the vertical direction. Error bars indicate standard deviations.

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