0
Research Papers

Repeated High Rate Facet Capsular Stretch at Strains That are Below the Pain Threshold Induces Pain and Spinal Inflammation With Decreased Ligament Strength in the Rat

[+] Author and Article Information
Sonia Kartha

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

Ben A. Bulka

Department of Bioengineering,
University of Pennsylvania,
Suite 240 Skirkanich Hall,
210 South 33rd Street,
Philadelphia, PA 19104
e-mail: benbulka8591@gmail.com

Nick S. Stiansen

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

Harrison R. Troche

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

Beth A. Winkelstein

Fellow ASME
Department of Bioengineering,
University of Pennsylvania,
Suite 240 Skirkanich Hall 210,
South 33rd Street,
Philadelphia, PA 19104
e-mail: winlest@seas.upenn.edu

1Corresponding author.

Manuscript received December 3, 2017; final manuscript received April 12, 2018; published online May 24, 2018. Assoc. Editor: Spencer P. Lake.

J Biomech Eng 140(8), 081002 (May 24, 2018) (8 pages) Paper No: BIO-17-1569; doi: 10.1115/1.4040023 History: Received December 03, 2017; Revised April 12, 2018

Repeated loading of ligamentous tissues during repetitive occupational and physical tasks even within physiological ranges of motion has been implicated in the development of pain and joint instability. The pathophysiological mechanisms of pain after repetitive joint loading are not understood. Within the cervical spine, excessive stretch of the facet joint and its capsular ligament has been implicated in the development of pain. Although a single facet joint distraction (FJD) at magnitudes simulating physiologic strains is insufficient to induce pain, it is unknown whether repeated stretching of the facet joint and ligament may produce pain. This study evaluated if repeated loading of the facet at physiologic nonpainful strains alters the capsular ligament's mechanical response and induces pain. Male rats underwent either two subthreshold facet joint distractions (STFJDs) or sham surgeries each separated by 2 days. Pain was measured before the procedure and for 7 days; capsular mechanics were measured during each distraction and under tension at tissue failure. Spinal glial activation was also assessed to probe potential pathophysiologic mechanisms responsible for pain. Capsular displacement significantly increased (p = 0.019) and capsular stiffness decreased (p = 0.008) during the second distraction compared to the first. Pain was also induced after the second distraction and was sustained at day 7 (p < 0.048). Repeated loading weakened the capsular ligament with lower vertebral displacement (p = 0.041) and peak force (p = 0.014) at tissue rupture. Spinal glial activation was also induced after repeated loading. Together, these mechanical, physiological, and neurological findings demonstrate that repeated loading of the facet joint even within physiologic ranges of motion can be sufficient to induce pain, spinal inflammation, and alter capsular mechanics similar to a more injurious loading exposure.

FIGURES IN THIS ARTICLE
<>
Copyright © 2018 by ASME
Your Session has timed out. Please sign back in to continue.

References

King, K. , Davidson, B. , Zhou, B. H. , Lu, Y. , and Solomonow, M. , “ High Magnitude Cyclic Load Triggers Inflammatory Response in Lumbar Ligaments,” Clin. Biomech., 24(10), pp. 792–798. [CrossRef]
Pollock, R. G. , Wang, V. M. , Bucchieri, J. S. , Cohen, N. P. , Huang, C. Y. , Pawluk, R. J. , Flatow, E. L. , Bigliani, L. U. , and Mow, V. C. , 2000, “ Effects of Repetitive Subfailure Strains on the Mechanical Behavior of the Inferior Glenohumeral Ligament,” J. Shoulder Elbow Surg., 9(5), pp. 427–435. [CrossRef] [PubMed]
Yassi, A. , 1997, “ Repetitive Strain Injuries,” Lancet, 349(9056), pp. 943–947. [CrossRef] [PubMed]
Cole, D. C. , Ibrahim, S. , and Shannon, H. S. , 2005, “ Predictors of Work-Related Repetitive Strain Injuries in a Population Cohort,” Am. J. Public Health, 95(7), pp. 1233–1237. [CrossRef] [PubMed]
van Rijn, R. M. , Huisstede, B. M. , Koes, B. W. , and Burdorf, A. , 2010, “ Associations Between Work-Related Factors and Specific Disorders of the Shoulder—A Systematic Review of the Literature,” Scand. J. Work Environ. Health, 36(3), pp. 189–201. [CrossRef] [PubMed]
Le, P. , Solomonow, M. , Zhou, B.-H. , Lu, Y. , and Patel, V. , “ Cyclic Load Magnitude is a Risk Factor for a Cumulative Lower Back Disorder,” J. Occup. Environ. Med., 49(4), pp. 375–387. [CrossRef] [PubMed]
Solomonow, M. , Baratta, R. V. , Zhou, B.-H. , Burger, E. , Zieske, A. , and Gedalia, A. , 2003, “ Muscular Dysfunction Elicited by Creep of Lumbar Viscoelastic Tissue,” J. Electromyogr. Kinesiol., 13(4), pp. 381–396. [CrossRef] [PubMed]
Sbriccoli, P. , Yousuf, K. , Kupershtein, I. , Solomonow, M. , Zhou, B.-H. , Zhu, P. , and Lu, Y. , 2004, “ Static Load Repetition is a Risk Factor in the Development of Lumbar Cumulative Musculoskeletal Disorder,” Spine (Phila. Pa. 1976), 29(23), pp. 2643–2653. [CrossRef] [PubMed]
Navar, D. , Zhou, B.-H. , Lu, Y. , and Solomonow, M. , 2006, “ High-Repetition Cyclic Loading is a Risk Factor for a Lumbar Disorder,” Muscle Nerve, 34(5), pp. 614–622. [CrossRef] [PubMed]
Olson, M. W. , Li, L. , and Solomonow, M. , 2009, “ Interaction of Viscoelastic Tissue Compliance With Lumbar Muscles During Passive Cyclic Flexion-Extension,” J. Electromyogr. Kinesiol., 19(1), pp. 30–38. [CrossRef] [PubMed]
Pearson, A. M. , Ivancic, P. C. , Ito, S. , and Panjabi, M. M. , 2004, “ Facet Joint Kinematics and Injury Mechanisms During Simulated Whiplash,” Spine (Phila. Pa. 1976), 29(4), pp. 390–397. [CrossRef] [PubMed]
Kaneoka, K. , Ono, K. , Inami, S. , and Hayashi, K. , 1999, “ Motion Analysis of Cervical Vertebrae During Whiplash Loading,” Spine (Phila. Pa. 1976), 24(8), pp. 763–769; discussion 770. [CrossRef] [PubMed]
Stemper, B. D. , Yoganandan, N. , Gennarelli, T. A. , and Pintar, F. A. , 2005, “ Localized Cervical Facet Joint Kinematics Under Physiological and Whiplash Loading,” J. Neurosurg. Spine, 3(6), pp. 471–476. [CrossRef] [PubMed]
Dong, L. , Quindlen, J. C. , Lipschutz, D. E. , and Winkelstein, B. A. , 2012, “ Whiplash-Like Facet Joint Loading Initiates Glutamatergic Responses in the DRG and Spinal Cord Associated With Behavioral Hypersensitivity,” Brain Res, 1461, pp. 51–63. [CrossRef] [PubMed]
Panjabi, M. M. , Cholewicki, J. , Nibu, K. , Grauer, J. , and Vahldiek, M. , 1998, “ Capsular Ligament Stretches During In Vivo Whiplash Simulations,” J. Spinal Disord., 11(3), pp. 227–232. [CrossRef] [PubMed]
Lee, K. E. , and Winkelstein, B. A. , 2009, “ Joint Distraction Magnitude is Associated With Different Behavioral Outcomes and Substance P Levels for Cervical Facet Joint Loading in the Rat,” J. Pain, 10(4), pp. 436–445. [CrossRef] [PubMed]
Kras, J. V. , Dong, L. , and Winkelstein, B. A. , 2013, “ The Prostaglandin E2 Receptor, EP2, is Upregulated in the Dorsal Root Ganglion After Painful Cervical Facet Joint Injury in the Rat,” Spine (Phila. Pa. 1976), 38(3), pp. 217–222. [CrossRef] [PubMed]
Dong, L. , Crosby, N. D. , and Winkelstein, B. A. , 2013, “ Gabapentin Alleviates Facet-Mediated Pain in the Rat Through Reduced Neuronal Hyperexcitability and Astrocytic Activation in the Spinal Cord,” J. Pain, 14(12), pp. 1564–1572. [CrossRef] [PubMed]
Crosby, N. D. , Gilliland, T. M. , and Winkelstein, B. A. , 2014, “ Early Afferent Activity From the Facet Joint After Painful Trauma to Its Capsule Potentiates Neuronal Excitability and Glutamate Signaling in the Spinal Cord,” Pain, 155(9), pp. 1878–1887. [CrossRef] [PubMed]
Bonner, T. J. , Newell, N. , Karunaratne, A. , Pullen, A. D. , Amis, A. A. , Bull, A. M. J. , and Masouros, S. D. , 2015, “ Strain-Rate Sensitivity of the Lateral Collateral Ligament of the Knee,” J. Mech. Behav. Biomed. Mater., 41, pp. 261–270. [CrossRef] [PubMed]
Malik-Hall, M. , Dina, O. A. , and Levine, J. D. , 2005, “ Primary Afferent Nociceptor Mechanisms Mediating NGF-Induced Mechanical Hyperalgesia,” Eur. J. Neurosci., 21(12), pp. 3387–3394. [CrossRef] [PubMed]
Woo, S. L. , Debski, R. E. , Withrow, J. D. , and Janaushek, M. A. , “ Biomechanics of Knee Ligaments Multiple Degrees of Freedom of Joint Motion,” Am. J. Sports Med., 27(4), pp. 533–543. [CrossRef] [PubMed]
Crowninshield, R. D. , and Pope, M. H. , 1976, “ The Strength and Failure Characteristics of Rat Medial Collateral Ligaments,” J. Trauma, 16(2), pp. 99–105. [CrossRef] [PubMed]
Mattucci, S. F. E. , Moulton, J. A. , Chandrashekar, N. , and Cronin, D. S. , 2012, “ Strain Rate Dependent Properties of Younger Human Cervical Spine Ligaments,” J. Mech. Behav. Biomed. Mater., 10, pp. 216–226. [CrossRef] [PubMed]
Quinn, K. P. , Lee, K. E. , Ahaghotu, C. C. , and Winkelstein, B. A. , 2007, “ Structural Changes in the Cervical Facet Capsular Ligament: Potential Contributions to Pain Following Subfailure Loading,” Stapp Car Crash J., 51, pp. 169–187. [PubMed]
Panjabi, M. M. , May, P. , Oxland, T. R. , and Cholewicki, J. , 1999, “ Subfailure Injury Affects the Relaxation Behavior of Rabbit ACL,” Clin. Biomech, 14(1), pp. 24–31. [CrossRef]
Lee, K. E. , Thinnes, J. H. , Gokhin, D. S. , and Winkelstein, B. A. , 2004, “ A Novel Rodent Neck Pain Model of Facet-Mediated Behavioral Hypersensitivity: Implications for Persistent Pain and Whiplash Injury,” J. Neurosci. Methods, 137(2), pp. 151–159. [CrossRef] [PubMed]
Ita, M. E. , Zhang, S. , Holsgrove, T. P. , Kartha, S. , and Winkelstein, B. A. , 2017, “ The Physiological Basis of Cervical Facet-Mediated Persistent Pain: Basic Science and Clinical Challenges,” J. Orthop. Sports Phys. Ther., 47(7), pp. 450–461. [CrossRef] [PubMed]
Curatolo, M. , Bogduk, N. , Ivancic, P. C. , McLean, S. A. , Siegmund, G. P. , and Winkelstein, B. A. , 2011, “ The Role of Tissue Damage in Whiplash-Associated Disorders,” Spine (Phila. Pa. 1976), 36(Suppl. 25), pp. S309–S315. [CrossRef] [PubMed]
Dong, L. , and Winkelstein, B. A. , 2010, “ Simulated Whiplash Modulates Expression of the Glutamatergic System in the Spinal Cord Suggesting Spinal Plasticity is Associated With Painful Dynamic Cervical Facet Loading,” J. Neurotrauma, 27(1), pp. 163–174. [CrossRef] [PubMed]
Lu, Y. , Chen, C. , Kallakuri, S. , Patwardhan, A. , and Cavanaugh, J. M. , 2005, “ Neural Response of Cervical Facet Joint Capsule to Stretch: A Study of Whiplash Pain Mechanism,” Stapp Car Crash J., 49, pp. 49–65. [PubMed]
Cavanaugh, J. M. , Lu, Y. , Chen, C. , and Kallakuri, S. , 2006, “ Pain Generation in Lumbar and Cervical Facet Joints,” J. Bone Jt. Surg. Am., 88(Suppl. 2), pp. 63–67.
Chen, C. , Lu, Y. , Kallakuri, S. , Patwardhan, A. , and Cavanaugh, J. M. , 2006, “ Distribution of a-Delta and C-Fiber Receptors in the Cervical Facet Joint Capsule and Their Response to Stretch,” J. Bone Jt. Surg. Am., 88(8), pp. 1807–1816. [CrossRef]
Quinn, K. P. , Dong, L. , Golder, F. J. , and Winkelstein, B. A. , 2010, “ Neuronal Hyperexcitability in the Dorsal Horn After Painful Facet Joint Injury,” Pain, 151(2), pp. 414–421. [CrossRef] [PubMed]
Lee, K. E. , Franklin, A. N. , Davis, M. B. , and Winkelstein, B. A. , 2006, “ Tensile Cervical Facet Capsule Ligament Mechanics: Failure and Subfailure Responses in the Rat,” J. Biomech., 39(7), pp. 1256–1264. [CrossRef] [PubMed]
Lee, K. E. , Davis, M. B. , and Winkelstein, B. A. , 2008, “ Capsular Ligament Involvement in the Development of Mechanical Hyperalgesia After Facet Joint Loading: Behavioral and Inflammatory Outcomes in a Rodent Model of Pain,” J. Neurotrauma, 25(11), pp. 1383–1393. [CrossRef] [PubMed]
Winkelstein, B. A. , and DeLeo, J. A. , 2002, “ Nerve Root Injury Severity Differentially Modulates Spinal Glial Activation in a Rat Lumbar Radiculopathy Model: Considerations for Persistent Pain,” Brain Res., 956(2), pp. 294–301. [CrossRef] [PubMed]
Ji, R.-R. , Chamessian, A. , and Zhang, Y.-Q. , 2016, “ Pain Regulation by Non-Neuronal Cells and Inflammation,” Science, 354(6312), pp. 572–577. [CrossRef] [PubMed]
Quinn, K. P. , and Winkelstein, B. A. , 2009, “ Vector Correlation Technique for Pixel-Wise Detection of Collagen Fiber Realignment During Injurious Tensile Loading,” J. Biomed. Opt., 14(5), p. 54010. [CrossRef]
Zhang, S. , Cao, X. , Stablow, A. M. , Shenoy, V. B. , and Winkelstein, B. A. , 2016, “ Tissue Strain Reorganizes Collagen With a Switchlike Response That Regulates Neuronal Extracellular Signal-Regulated Kinase Phosphorylation In Vivo: Implications for Ligamentous Injury and Mechanotransduction,” ASME J. Biomech. Eng., 138(2), p. 021013. [CrossRef]
Burgess, P. R. , and Perl, E. R. , 1967, “ Myelinated Afferent Fibres Responding Specifically to Noxious Stimulation of the Skin,” J. Physiol., 190(3), pp. 541–562. [CrossRef] [PubMed]
Zimmermann, M. , 1983, “ Ethical Guidelines for Investigations of Experimental Pain in Conscious Animals,” Pain, 16(2), pp. 109–110. [CrossRef] [PubMed]
Crosby, N. D. , Zaucke, F. , Kras, J. V. , Dong, L. , Luo, Z. D. , and Winkelstein, B. A. , 2015, “ Thrombospondin-4 and Excitatory Synaptogenesis Promote Spinal Sensitization After Painful Mechanical Joint Injury,” Exp. Neurol., 264, pp. 111–120. [CrossRef] [PubMed]
Dong, L. , Guarino, B. B. , Jordan-Sciutto, K. L. , and Winkelstein, B. A. , 2011, “ Activating Transcription Factor 4, a Mediator of the Integrated Stress Response, is Increased in the Dorsal Root Ganglia Following Painful Facet Joint Distraction,” Neuroscience, 193, pp. 377–386. [CrossRef] [PubMed]
Kras, J. V. , Dong, L. , and Winkelstein, B. A. , 2014, “ Increased Interleukin-1α and Prostaglandin E2 Expression in the Spinal Cord at 1 Day After Painful Facet Joint Injury: Evidence of Early Spinal Inflammation,” Spine (Phila. Pa. 1976), 39(3), pp. 207–212. [CrossRef] [PubMed]
Dong, L. , Odeleye, A. O. , Jordan-Sciutto, K. L. , and Winkelstein, B. A. , 2008, “ Painful Facet Joint Injury Induces Neuronal Stress Activation in the DRG: Implications for Cellular Mechanisms of Pain,” Neurosci. Lett., 443(2), pp. 90–94. [CrossRef] [PubMed]
Chaplan, S. R. , Bach, F. W. , Pogrel, J. W. , Chung, J. M. , and Yaksh, T. L. , 1994, “ Quantitative Assessment of Tactile Allodynia in the Rat Paw,” J. Neurosci. Methods, 53(1), pp. 55–63. [CrossRef] [PubMed]
Kras, J. V. , Kartha, S. , and Winkelstein, B. A. , 2015, “ Intra-Articular Nerve Growth Factor Regulates Development, but Not Maintenance, of Injury-Induced Facet Joint Pain and Spinal Neuronal Hypersensitivity,” Osteoarthritis Cartilage, 23(11), pp. 1999–2008. [CrossRef] [PubMed]
Quinn, K. P. , and Winkelstein, B. A. , 2007, “ Cervical Facet Capsular Ligament Yield Defines the Threshold for Injury and Persistent Joint-Mediated Neck Pain,” J. Biomech., 40(10), pp. 2299–2306. [CrossRef] [PubMed]
Dong, L. , Smith, J. R. , and Winkelstein, B. A. , 2013, “ Ketorolac Reduces Spinal Astrocytic Activation and PAR1 Expression Associated With Attenuation of Pain After Facet Joint Injury,” J. Neurotrauma, 30(10), pp. 818–825. [CrossRef] [PubMed]
Winkelstein, B. A. , and Santos, D. G. , 2008, “ An Intact Facet Capsular Ligament Modulates Behavioral Sensitivity and Spinal Glial Activation Produced by Cervical Facet Joint Tension,” Spine (Phila. Pa. 1976), 33(8), pp. 856–862. [CrossRef] [PubMed]
Zhang, G. , 2005, “ Evaluating the Viscoelastic Properties of Biological Tissues in a New Way,” J. Musculoskeletal Neuronal Interact., 5(1), pp. 85–90.
Mattei, G. , Tirella, A. , Gallone, G. , and Ahluwalia, A. , 2014, “ Viscoelastic Characterisation of Pig Liver in Unconfined Compression,” J. Biomech., 47(11), pp. 2641–2646. [CrossRef] [PubMed]
Winkelstein, B. A. , Nightingale, R. W. , Richardson, W. J. , and Myers, B. S. , 2000, “ The Cervical Facet Capsule and Its Role in Whiplash Injury: A Biomechanical Investigation,” Spine (Phila. Pa. 1976), 25(10), pp. 1238–1246. [CrossRef] [PubMed]
Ban, E. , Zhang, S. , Zarei, V. , Barocas, V. H. , Winkelstein, B. A. , and Picu, C. R. , 2017, “ Collagen Organization in Facet Capsular Ligaments Varies With Spinal Region and With Ligament Deformation,” ASME J. Biomech. Eng., 139(7), p. 071009. [CrossRef]
Zarei, V. , Zhang, S. , Winkelstein, B. A. , and Barocas, V. H. , 2017, “ Tissue Loading and Microstructure Regulate the Deformation of Embedded Nerve Fibres: Predictions From Single-Scale and Multiscale Simulations,” J. R. Soc. Interface, 14(135), p. 20170326. [CrossRef] [PubMed]
Quindlen, J. C. , Lai, V. K. , and Barocas, V. H. , 2015, “ Multiscale Mechanical Model of the Pacinian Corpuscle Shows Depth and Anisotropy Contribute to the Receptor's Characteristic Response to Indentation,” PLOS Comput. Biol., 11(9), p. e1004370. [CrossRef] [PubMed]
Lake, S. P. , Miller, K. S. , Elliott, D. M. , and Soslowsky, L. J. , 2009, “ Effect of Fiber Distribution and Realignment on the Nonlinear and Inhomogeneous Mechanical Properties of Human Supraspinatus Tendon Under Longitudinal Tensile Loading,” J. Orthop. Res., 27(12), pp. 1596–1602. [CrossRef] [PubMed]
Sugita, S. , and Matsumoto, T. , 2013, “ Heterogeneity of Deformation of Aortic Wall at the Microscopic Level: Contribution of Heterogeneous Distribution of Collagen Fibers in the Wall,” Biomed. Mater. Eng., 23(6), pp. 447–461. [PubMed]
Zeeman, M. E. , Kartha, S. , and Winkelstein, B. A. , 2016, “ Whole-Body Vibration Induces Pain and Lumbar Spinal Inflammation Responses in the Rat That Vary With the Vibration Profile,” J. Orthop. Res., 34(8), pp. 1439–1446. [CrossRef] [PubMed]
Zeeman, M. E. , Kartha, S. , Jaumard, N. V. , Baig, H. A. , Stablow, A. M. , Lee, J. , Guarino, B. B. , and Winkelstein, B. A. , 2015, “ Whole-Body Vibration at Thoracic Resonance Induces Sustained Pain and Widespread Cervical Neuroinflammation in the Rat,” Clin. Orthop. Relat. Res., 473(9), pp. 2936–2947. [CrossRef] [PubMed]
Baig, H. A. , Guarino, B. B. , Lipschutz, D. , and Winkelstein, B. A. , 2013, “ Whole Body Vibration Induces Forepaw and Hind Paw Behavioral Sensitivity in the Rat,” J. Orthop. Res., 31(11), pp. 1739–1744. [PubMed]
Azar, N. R. , Kallakuri, S. , Chen, C. , Lu, Y. , and Cavanaugh, J. M. , 2009, “ Strain and Load Thresholds for Cervical Muscle Recruitment in Response to Quasi-Static Tensile Stretch of the Caprine C5-C6 Facet Joint Capsule,” J. Electromyogr. Kinesiol., 19(6), pp. e387–e394. [CrossRef] [PubMed]

Figures

Grahic Jump Location
Fig. 1

(a) A STFJD1 or sham control (SHAM1) procedure was performed on day 0 and repeated 2 days later day 2 (STFJD2, SHAM2). Behavioral sensitivity was measured on day 0 before procedures and on days 1, 2, 3, and 7. (b) For the FJD, microforceps were affixed to the C6 and C7 vertebrae to distract the C6/C7 FCL. Markers on the FCL were used to measure the capsule's displacement, MPS, peak force, and stiffness during FJD. (c) In a separate set of rats, spinal columns were harvested to measure mechanical properties under tensile failure of the right FCL; displacements, MPS, peak force, and stiffness were measured in the right FCL at first failure and rupture. (d) On day 7 in the remaining subset of rats, spinal cord tissue was harvested for immunohistochemistry labeling for the glial markers Iba1 and GFAP.

Grahic Jump Location
Fig. 2

After a single STFJD1, withdrawal thresholds were not different from baseline for either day 1 or day 2. However, after the second STFJD2, the threshold measured on day 3 was significantly lower than baseline and days 1 and 2 (#p < 0.035) and remained lower also at day 7, which was significantly different than baseline, day 1 and day 2 (#p < 0.048). Although on days 0, 1, and 2 there was no difference between thresholds for the STFJD1 and SHAM1 groups, thresholds after STFJD2 were significantly lower than after a second sham procedure (SHAM2) on both days 3 and 7 (*p < 0.001).

Grahic Jump Location
Fig. 4

At day 7, increased expression of both GFAP (green) and Iba1 (red) was evident after repeated subthreshold loading in the spinal cord dorsal horn (dashed line). GFAP significantly increased in the superficial dorsal horn (white box) of the STFJDX2 group over both the SHAMX2 (*p = 0.007) and normal (*p = 0.0001) groups. Similarly, Iba1 expression significantly increased in the superficial dorsal horn after repeated subthreshold loading over both the SHAMX2 (*p = 0.013) and normal (*p = 0.0004) groups. Representative images indicate the greatest GFAP and Iba1 labeling occurs in the superficial dorsal horn of the STFJDX2 group.

Grahic Jump Location
Fig. 3

At the first failure, only the peak force was significantly altered, with a significant reduction in peak force in the STFJDX2 group (*p = 0.028) compared to the SHAMX2 group. There were no differences detected in any other biomechanical metric measured at first failure. At tissue rupture, the vertebral displacement was also significantly lower (*p = 0.041) in the STFJDX2 group compared to the SHAMX2 group; peak force remained significantly decreased at tissue rupture (*p = 0.014) following repeated STFJDs.

Tables

Errata

Some tools below are only available to our subscribers or users with an online account.

Related Content

Customize your page view by dragging and repositioning the boxes below.

Related Journal Articles
Related eBook Content
Topic Collections

Sorry! You do not have access to this content. For assistance or to subscribe, please contact us:

  • TELEPHONE: 1-800-843-2763 (Toll-free in the USA)
  • EMAIL: asmedigitalcollection@asme.org
Sign In