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.

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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. 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.

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.



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