Detection of Altered Collagen Fiber Alignment in the Cervical Facet Capsule After Whiplash-Like Joint Retraction

The cervical facet joint has been identified as the source of pain in patients with whiplash-associated disorders, but most clinical studies report no radiographic evidence of tissue injury in these disorders. The goal of this study was to utilize quantitative polarized light imaging to assess the potential for altered collagen fiber alignment in human cadaveric cervical facet capsule specimens (n = 8) during and after a joint retraction simulating whiplash exposure. Although no evidence of ligament damage was detected during whiplash-like retraction, mechanical and microstructural changes were identified after loading. Retraction produced significant decreases in ligament stiffness (p = 0.0186) and increases in laxity (p = 0.0065). In addition, image analysis indicated that 21.1 ± 17.1% of the capsule sustained principal strains that were unrecovered immediately after retraction. Altered collagen fiber alignment was detected in 32.7 ± 22.9% of the capsule after retraction. The capsule regions with unrecovered strain and altered fiber alignment after retraction were significantly co-localized with each other (p < 0.0001), suggesting the altered mechanical function may relate to a change in the tissue’s fiber organization. The identification of altered fiber alignment in this ligament following retraction without any tears implicates the whiplash kinematic as a potential cause of microstructural damage that is not detectable using standard clinical imaging techniques.

[1]  Y. Toyama,et al.  Cervical curvature in acute whiplash injuries: prospective comparative study with asymptomatic subjects. , 1998, Injury.

[2]  Kathryn E. Lee,et al.  Joint distraction magnitude is associated with different behavioral outcomes and substance P levels for cervical facet joint loading in the rat. , 2009, The journal of pain : official journal of the American Pain Society.

[3]  M. Hull,et al.  A method for quantifying the anterior load-displacement behavior of the human knee in both the low and high stiffness regions. , 2001, Journal of biomechanics.

[4]  Martin B. Davis,et al.  Mechanical Evidence of Cervical Facet Capsule Injury During Whiplash: A Cadaveric Study Using Combined Shear, Compression, and Extension Loading , 2001, Spine.

[5]  Ronald P. McCabe,et al.  Cervical Stability After Sequential Capsule Resection , 1993, Spine.

[6]  Erik J. Carlson,et al.  Whiplash causes increased laxity of cervical capsular ligament. , 2008, Clinical biomechanics.

[7]  Nikolai Bogduk,et al.  Chapter 2 – Biomechanics of the Cervical Spine , 2002 .

[8]  M. Gadala,et al.  A Three-Dimensional Finite Element Model of the Cervical Spine with Spinal Cord: An Investigation of Three Injury Mechanisms , 2008, Annals of Biomedical Engineering.

[9]  A. Silman,et al.  Risk factors for neck pain: a longitudinal study in the general population , 2001, Pain.

[10]  B. Myers,et al.  The cervical facet capsule and its role in whiplash injury: a biomechanical investigation. , 2000, Spine.

[11]  N Yoganandan,et al.  Cervical spine vertebral and facet joint kinematics under whiplash. , 1998, Journal of biomechanical engineering.

[12]  Kathryn E. Lee,et al.  Structural changes in the cervical facet capsular ligament: potential contributions to pain following subfailure loading. , 2007, Stapp car crash journal.

[13]  Beth A Winkelstein,et al.  Vector correlation technique for pixel-wise detection of collagen fiber realignment during injurious tensile loading. , 2009, Journal of biomedical optics.

[14]  S. Tashman,et al.  Kinematics of human cadaver cervical spine during low speed rear-end impacts. , 2000, Stapp car crash journal.

[15]  V. Wright,et al.  The straight cervical spine: does it indicate muscle spasm? , 1994, The Journal of bone and joint surgery. British volume.

[16]  G. Bannister,et al.  The rate of recovery following whiplash injury , 2005, European Spine Journal.

[17]  P. Canham,et al.  Demonstration of quantitative fabric analysis of tendon collagen using two-dimensional polarized light microscopy. , 1991, Matrix.

[18]  M. Panjabi,et al.  Facet Joint Kinematics and Injury Mechanisms During Simulated Whiplash , 2004, Spine.

[19]  Chaoyang Chen,et al.  Neural response of cervical facet joint capsule to stretch: a study of whiplash pain mechanism. , 2005, Stapp car crash journal.

[20]  E. Teo,et al.  Evaluation of the role of ligaments, facets and disc nucleus in lower cervical spine under compression and sagittal moments using finite element method. , 2001, Medical engineering & physics.

[21]  Victor H Barocas,et al.  Image-based multiscale modeling predicts tissue-level and network-level fiber reorganization in stretched cell-compacted collagen gels , 2009, Proceedings of the National Academy of Sciences.

[22]  Theodore T. Tower,et al.  Fiber Alignment Imaging During Mechanical Testing of Soft Tissues , 2002, Annals of Biomedical Engineering.

[23]  Narayan Yoganandan,et al.  Validation of a Finite Element Model of the Young Normal Lower Cervical Spine , 2008, Annals of Biomedical Engineering.

[24]  Beth A Winkelstein,et al.  Capsular ligament involvement in the development of mechanical hyperalgesia after facet joint loading: behavioral and inflammatory outcomes in a rodent model of pain. , 2008, Journal of neurotrauma.

[25]  M. Nordin,et al.  Clinical practice implications of the Bone and Joint Decade 2000-2010 Task Force on Neck Pain and Its Associated Disorders: from concepts and findings to recommendations. , 2009, Journal of manipulative and physiological therapeutics.

[26]  Beth A Winkelstein,et al.  Full field strain measurements of collagenous tissue by tracking fiber alignment through vector correlation. , 2010, Journal of biomechanics.

[27]  K. Hayashi,et al.  Motion analysis of cervical vertebrae during whiplash loading. , 1999, Spine.

[28]  C. Franke,et al.  Acute whiplash injury: is there a role for MR imaging?--a prospective study of 100 patients. , 1996, Radiology.

[29]  B. Winkelstein,et al.  Cytokine Antagonism Reduces Pain and Modulates Spinal Astrocytic Reactivity After Cervical Nerve Root Compression , 2010, Annals of Biomedical Engineering.

[30]  Development of a computer model to predict strains in the individual fibers of a ligament across the ligamentous occipito-atlanto-axial (C0-C1-C2) complex , 2006, Annals of Biomedical Engineering.

[31]  Raj D. Rao,et al.  Whiplash Injury Determination With Conventional Spine Imaging and Cryomicrotomy , 2001, Spine.

[32]  J. Iatridis,et al.  Mechanical damage to the intervertebral disc annulus fibrosus subjected to tensile loading. , 2005, Journal of biomechanics.

[33]  Scott Tashman,et al.  Effect of Head-Neck Position on Cervical Facet Stretch of Post Mortem Human Subjects during Low Speed Rear End Impacts. , 2004, Stapp car crash journal.

[34]  L. Soslowsky,et al.  Effect of fiber distribution and realignment on the nonlinear and inhomogeneous mechanical properties of human supraspinatus tendon under longitudinal tensile loading , 2009, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[35]  M. Fagerlund,et al.  Disc pathology after whiplash injury. A prospective magnetic resonance imaging and clinical investigation. , 1997, Spine.

[36]  Raymond P. Molloy,et al.  In vivo multiphoton microscopy of deep brain tissue. , 2004, Journal of neurophysiology.

[37]  N Yoganandan,et al.  Biomechanics of the cervical spine Part 3: minor injuries. , 2001, Clinical Biomechanics.

[38]  G. Bannister,et al.  Whiplash injury. , 2009, The Journal of bone and joint surgery. British volume.