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Effects of Unilateral Facet Fixation and Facetectomy on Muscle Spindle Responsiveness During Simulated Spinal Manipulation in an Animal Model

Published:October 25, 2013DOI:https://doi.org/10.1016/j.jmpt.2013.08.007

      Abstract

      Objectives

      Manual therapy practitioners commonly assess lumbar intervertebral mobility before deciding treatment regimens. Changes in mechanoreceptor activity during the manipulative thrust are theorized to be an underlying mechanism of spinal manipulation (SM) efficacy. The objective of this study was to determine if facet fixation or facetectomy at a single lumbar level alters muscle spindle activity during 5 SM thrust durations in an animal model.

      Methods

      Spinal stiffness was determined using the slope of a force-displacement curve. Changes in the mean instantaneous frequency of spindle discharge were measured during simulated SM of the L6 vertebra in the same 20 afferents for laminectomy-only and 19 laminectomy and facet screw conditions; only 5 also had data for the laminectomy and facetectomy condition. Neural responses were compared across conditions and 5 thrust durations (≤250 milliseconds) using linear-mixed models.

      Results

      Significant decreases in afferent activity between the laminectomy-only and laminectomy and facet screw conditions were seen during 75-millisecond (P < .001), 100-millisecond (P = .04), and 150-millisecond (P = .02) SM thrust durations. Significant increases in spindle activity between the laminectomy-only and laminectomy and facetectomy conditions were seen during the 75-millisecond (P < .001) and 100-millisecond (P < .001) thrust durations.

      Conclusion

      Intervertebral mobility at a single segmental level alters paraspinal sensory response during clinically relevant high-velocity, low-amplitude SM thrust durations (≤150 milliseconds). The relationship between intervertebral joint mobility and alterations of primary afferent activity during and after various manual therapy interventions may be used to help to identify patient subpopulations who respond to different types of manual therapy and better inform practitioners (eg, chiropractic and osteopathic) delivering the therapeutic intervention.

      Key Indexing Terms

      Intervertebral hypomobility can be described as an increase in spinal stiffness or a reduction in motion between adjacent spinal segments. Conversely, intervertebral hypermobility represents decreased spinal stiffness and increased intervertebral motion. Clinical diagnoses associated with spinal joint hypomobility include degenerative joint disease including facet degeneration, osteophyte formation, or increased tears in the innervated outer rim of the intervertebral disks that are often associated with low back pain (LBP).
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      In a randomized clinical trial, Fritz et al
      • Fritz JM
      • Whitman JM
      • Childs JD
      Lumbar spine segmental mobility assessment: an examination of validity for determining intervention strategies in patients with low back pain.
      categorized 131 patients with LBP with respect to the clinical determination of spinal joint hypomobility and hypermobility and found that spinal manipulation produced higher therapeutic success rates in participants with spinal joint hypomobility compared with those with spinal joint hypermobility. Participants with spinal joint hypomobility had treatment success rates of 74% after receiving spinal manipulation combined with stabilization exercises vs 25.6% after receiving stabilization exercises alone. In contrast, participants with spinal joint hypermobility had success rates of only 16.7% with spinal manipulation combined with stabilization exercises but 77.8% with stabilization exercises alone. The mechanisms responsible for this treatment effect are unknown, but alterations in sensorimotor processing due to intervertebral joint dysfunction may be a contributing factor.
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      Neurophysiological effects of spinal manipulation.
      Patients with LBP have shown a variety of sensorimotor abnormalities including abnormal reflex responses indicated by reduced reflex gain and slowed reaction latencies,
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      Inefficient muscular stabilization of the lumbar spine associated with low back pain: a motor control evaluation of transversus abdominis.
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      One-footed and externally distributed two-footed postural control in patients with chronic low back pain and healthy control subjects, a controlled study with follow-up.
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      Altered trunk muscle recruitment in people with low back pain with upper limb movement at different speeds.
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      Moving differently in pain: a new theory to explain the adaptation to pain.
      impaired lumbosacral proprioceptive acuity,
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      altered postural balance strategies,
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      and higher spinal loads during highly controlled exertions.
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      Many of these abnormalities are consistent with alterations in sensory feedback from the paraspinal tissues. Spindles in paraspinal muscles provide the central nervous system with sensory information regarding changes in muscle length and shortening velocity and thus are the proprioceptors most likely reporting changes in intervertebral position and aberrant vertebra movement. Pickar and Kang
      • Pickar JG
      • Kang YM
      Paraspinal muscle spindle responses to the duration of a spinal manipulation under force control.
      • Ge W
      • Pickar JG
      The decreased responsiveness of lumbar muscle spindles to a prior history of spinal muscle lengthening is graded with the magnitude of change in vertebral position.
      and Ge and Pickar
      • Pickar JG
      • Kang YM
      Paraspinal muscle spindle responses to the duration of a spinal manipulation under force control.
      • Ge W
      • Pickar JG
      The decreased responsiveness of lumbar muscle spindles to a prior history of spinal muscle lengthening is graded with the magnitude of change in vertebral position.
      have shown that very small displacements (0.5-1.0 mm) of lumbar vertebra evoke muscle spindle discharge from paraspinal muscles and that sustained vertebral positions can affect the accuracy of proprioceptive signaling.
      The apparent relationship between intervertebral joint mobility and the clinical success of spinal manipulation for LBP, combined with increasing evidence for proprioceptive-related changes in individuals with LBP, led us to undertake a basic science investigation to determine the relationship between changes in lumbar spinal stiffness and mechanoreceptor activity from muscle spindles in the low back during a simulated high-velocity, low-amplitude spinal manipulation (HVLA-SM) in an animal preparation. The purpose of this study was to determine whether relative increases vs decreases in spinal stiffness can impact paraspinal sensory responses for 5 thrust durations of HVLA-SM directed at the same level as the dysfunction. This study aims to be an important first step in concurrently examining the effects of intervertebral dysfunction and peripheral afferent signaling during a commonly used and effective therapeutic intervention for LBP.

      Methods

      All experiments were reviewed and approved by our Institutional Animal Care and Use Committee. Electrophysiological activity in single primary afferent fibers from muscle spindles was obtained during HVLA-SM of the lumbar spine in 23 male cats weighing an average (SD) of 4.46 (0.31) kg. One afferent was investigated per cat because of the irreversible nature of the L5/6 facetectomy surgical procedure.

      General Procedures

      The surgical procedures and device used to apply simulated spinal manipulations have previously been described in detail.
      • Pickar JG
      • Wheeler JD
      Response of muscle proprioceptors to spinal manipulative-like loads in the anesthetized cat.
      • Reed WR
      • Cao DY
      • Long CR
      • Kawchuk GN
      • Pickar JG
      Relationship between biomechanical characteristics of spinal manipulation and neural responses in an animal model: effect of linear control of thrust displacement versus force, thrust amplitude, thrust duration and thrust rate.
      Briefly, anesthesia was induced using isoflurane and catheters placed in a carotid artery and an external jugular vein to monitor blood pressure and introduce fluids respectively. Deep anesthesia was then maintained throughout the experiment with nembutal (35 mg/kg, intravenously). The trachea was intubated, and the cat was ventilated mechanically. Arterial pH, Pco2, and Po2 were monitored and maintained within the reference range (pH 7.32-7.43; Pco2, 32-37 mm Hg; Po2, >85 mm Hg). The right sciatic nerve was cut to reduce afferent input from the hindlimb. The lumbar spine was mechanically secured at the L4 spinous process and the iliac crests using a Kopf spinal unit (David Kopf Instruments, Tujunga, CA). The L5 laminae and caudal half of the L4 laminae were removed to expose the L6 dorsal rootlets. All intervertebral disks and facet joints remained intact. The dura mater was incised, and the L6 dorsal root was cut close to the spinal cord. Thin filaments from the cut proximal dorsal rootlets were teased using forceps until impulse activity from a single afferent was identified. The L6 spinal nerve innervates the fascicles of the multifidus and longissimus muscles attaching to the L6 vertebra.
      • Bogduk N
      The lumbosacral dorsal rami in the cat.
      Action potentials were recorded using a PC-based data acquisition system (Spike 2; Cambridge Electronic Design, Cambridge, UK).
      Calibrated nylon monofilaments (Stoelting, Wood Dale, IL) were applied to the exposed back muscle (longissimus or multifidus) to verify the location of the most sensitive portion of the afferent's receptive field. Afferents were identified as muscle spindles based on their increased discharge to succinylcholine (100-400 mg/kg; Butler Schein, Dublin, OH), decreased discharge to electrically induced muscle contraction, and sustained response to a fast vibratory stimulus.
      • Brown MC
      • Engberg I
      • Matthews PB
      The relative sensitivity to vibration of muscle receptors of the cat.
      • Pickar JG
      An in vivo preparation for investigating neural responses to controlled loading of a lumbar vertebra in the anesthetized cat.
      • Cao DY
      • Reed WR
      • Long CR
      • Kawchuk GN
      • Pickar JG
      Effects of thrust amplitude and duration of high-velocity, low-amplitude spinal manipulation on lumbar muscle spindle responses to vertebral position and movement.
      Animals were euthanized at the end of the experiment by an intravenous overdose of pentobarbital.

      Determination of Spinal Stiffness

      Changes in spinal stiffness relative to a laminectomy-only control condition were created by unilateral (left) L5/6 facet-fixation (to increase intervertebral stiffness) or L5/6 facetectomy (to decrease intervertebral stiffness). A previous study using a similar feline model showed that the average spinal stiffness did not differ significantly before and after the laminectomy procedure itself.
      • Pickar JG
      • Sung PS
      • Kang YM
      • Ge W
      Response of lumbar paraspinal muscles spindles is greater to spinal manipulative loading compared with slower loading under length control.
      Stiffness testing was done under the same conditions for which the neural recordings were obtained, namely, in the necessary presence of a laminectomy. To fixate the left L5/6 facet joint, a single 10-mm titanium endosteally anchored miniscrew (tomas-pin; Dentaurum, Ispringen, Germany) was inserted through the articular pillars of the L5/6 facet joint (Fig 1). For the facetectomy, the left L5 inferior facet and left L6 superior facet were completely removed using bone rongeurs (Fig 1). Muscle spindle responsiveness during the thrust of the HVLA-SM was tested in each of these 3 spinal joint conditions in the same animal. The testing order was always the same (laminectomy-only, laminectomy and facet screw, laminectomy and facetectomy) because of the irreversible nature of the facetectomy (Fig 2).
      Figure thumbnail gr1
      Fig 1Photos showing the L5/6 facet-fixation with the facet screw (A), forceps rigidly attached to the L6 spinous process (B), and the cut L6 dorsal nerve rootlets (C) along with an x-ray showing an inserted L5/6 facet-screw (D), and a L5/6 facetectomy (E).
      Figure thumbnail gr2
      Fig 2Diagram showing the anatomical location and sequence of surgical procedures (laminectomy-only, laminectomy and facet screw condition, and laminectomy and facetectomy condition) performed in the same animal while maintaining a primary afferent recording. Lam., represents the extent of surgical laminectomy performed; NR, neural recording. n = number of comparisons made to laminectomy-only condition that met the inclusion criteria.
      Spinal joint stiffness was determined for each of the 3 spinal joint conditions using a 1-mm ramp movement applied in the dorsal-ventral direction at the L6 vertebra. Ramp movements were applied 5 minutes before delivery of the HVLA-SM thrusts. A feedback-controlled motor (Aurora Scientific, Lever System Model 310; Aurora, Ontario, Canada) induced vertebral movement at a rate of 0.5 mm/s through a pair of rigid forceps attached to the L6 spinous process. This device and rate have been used in previous studies to assess stiffness in a feline preparation.
      • Vaillant M
      • Edgecombe T
      • Long CR
      • Pickar JG
      • Kawchuk GN
      The effect of duration and amplitude of spinal manipulative therapy (SMT) on spinal stiffness.
      • Vaillant M
      • Pickar JG
      • Kawchuk GN
      Performance and reliability of a variable rate, force/displacement application system.
      Forces and displacements applied at the L6 spinous process were simultaneously measured from outputs of the control system. The slope of the most linear portion of the force-displacement curve (between 2.16 and 8.83 N) was calculated and represented premanipulation spinal joint stiffness for each condition. Preconditioning was not performed to minimize the total number of facet screw/bone engagements. Preliminary testing indicated that spinal joint stiffness created by insertion of the facet screw remained unchanged through a minimum of 16 manipulative procedures, which was more than 3× the number performed after screw insertion in the present study. To confirm that during the manipulation thrust itself, the screw maintained the increase in stiffness and that the facetectomy decreased it relative to laminectomy-only, spinal stiffness was also determined during each manipulative thrust. Stiffness during the thrust was obtained from the slope of the force-displacement curves from thrust onset to peak thrust amplitude for each condition.
      Twenty-three animals were used in this study. In the laminectomy and facet screw condition, the screw failed to increase the 1mm ramp stiffness by at least 2% in 4 animals. Therefore, only 19 laminectomy and facet screw conditions were compared with the laminectomy-only condition (Fig 2). In the laminectomy and facetectomy condition, facetectomy failed to decrease the 1-mm ramp stiffness by at least 2% in 8 animals. In addition, owing to surgically associated bleeding during the facetectomy procedure (performed after removal of the facet screw), the neural signal was lost in another 10 laminectomy and facetectomy conditions. Therefore, only 5 laminectomy and facetectomy conditions were compared with the laminectomy-only condition (Fig 2).

      HVLA Spinal Manipulation

      Mechanical loading profiles measured during a clinically delivered HVLA-SM indicate that the thrust phase of a spinal manipulation can be likened to the up-ramp of a triangle wave.
      • Hessell BW
      • Herzog W
      • Conway PJW
      • McEwen MC
      Experimental measurement of the force exerted during spinal manipulation using the Thompson technique.
      • Herzog W
      • Conway PJ
      • Kawchuk GN
      • Zhang Y
      • Hasler EM
      Forces exerted during spinal manipulative therapy.
      • Triano JJ
      Biomechanics of spinal manipulative therapy.
      Peak manipulative forces during clinical treatment of the lumbosacral region can range from 200 to 1600 N, with a time to peak force being less than 150 milliseconds.
      • Hessell BW
      • Herzog W
      • Conway PJW
      • McEwen MC
      Experimental measurement of the force exerted during spinal manipulation using the Thompson technique.
      • Triano JJ
      Biomechanics of spinal manipulative therapy.
      • Conway PJW
      • Herzog W
      • Zhang Y
      • Hasler EM
      • Ladly K
      Forces required to cause cavitation during spinal manipulation of the thoracic spine.
      • Triano J
      • Schultz AB
      Loads transmitted during lumbosacral spinal manipulative therapy.
      • Herzog W
      The biomechanics of spinal manipulation.
      Simulated HVLA-SM thrusts were applied at the L6 spinous process using the same feedback motor control system and toothed forceps used for stiffness determination. Peak manipulative forces of 55% of an average cat body weight (3.95 kg as determined in previous studies
      • Reed WR
      • Cao DY
      • Long CR
      • Kawchuk GN
      • Pickar JG
      Relationship between biomechanical characteristics of spinal manipulation and neural responses in an animal model: effect of linear control of thrust displacement versus force, thrust amplitude, thrust duration and thrust rate.
      • Cao DY
      • Reed WR
      • Long CR
      • Kawchuk GN
      • Pickar JG
      Effects of thrust amplitude and duration of high-velocity, low-amplitude spinal manipulation on lumbar muscle spindle responses to vertebral position and movement.
      ) were applied in a dorsal-ventral direction (ie, from the cat's posterior toward its anterior) under force control. Forces were applied for 5 thrust durations (0-time control, 75, 100, 150, and 250 milliseconds). The time-control (0 milliseconds duration) represents a nonthrust testing protocol from which potential changes in discharge frequency related to surgical procedures could be determined. The range of thrust durations encompassed those used clinically with non–instrument-assisted HVLA-SMs.
      • Hessell BW
      • Herzog W
      • Conway PJW
      • McEwen MC
      Experimental measurement of the force exerted during spinal manipulation using the Thompson technique.
      • Triano JJ
      Biomechanics of spinal manipulative therapy.
      Spinal manipulations were separated by 5 minutes,
      • Cao DY
      • Reed WR
      • Long CR
      • Kawchuk GN
      • Pickar JG
      Effects of thrust amplitude and duration of high-velocity, low-amplitude spinal manipulation on lumbar muscle spindle responses to vertebral position and movement.
      and order was randomized within each of the 3 types of joint conditions (Fig 2).

      Data Analysis

      Muscle spindle activity was converted to instantaneous frequency (IF) by taking the reciprocal of the time interval between successive action potentials. Neural activity arising from HVLA-SM activation of muscle spindles was determined during the 2 seconds that immediately preceded each HVLA-SM thrust (baseline) and during the HVLA-SM's thrust phase. Mean IF (MIF) was calculated for baseline and the thrust phase. As in previous studies, the change in MIF resulting from the HVLA-SM (∆MIF) constituted the response measure.
      • Reed WR
      • Cao DY
      • Long CR
      • Kawchuk GN
      • Pickar JG
      Relationship between biomechanical characteristics of spinal manipulation and neural responses in an animal model: effect of linear control of thrust displacement versus force, thrust amplitude, thrust duration and thrust rate.
      • Cao DY
      • Reed WR
      • Long CR
      • Kawchuk GN
      • Pickar JG
      Effects of thrust amplitude and duration of high-velocity, low-amplitude spinal manipulation on lumbar muscle spindle responses to vertebral position and movement.
      All neural activities are reported in impulses per second (imp/s).
      The study was a split-plot design
      • Jones B
      • Nachtsheim CJ
      Split-plot designs: what, why, and how?.
      where the whole-plot factor, thrust duration, was a randomized complete block design and the subplot factor, spinal joint condition, was a repeated measures design. The data were analyzed with Proc Mixed in SAS System for Windows (Release 9.2; SAS Institute Inc, Cary, NC). Linear-mixed models of both lumbar stiffness and neural response were fit with terms for thrust duration, spinal joint condition, and their interaction, modeling within-block correlation over the 3 conditions as unstructured. Twenty afferents were included in the analysis; 4 had data for all 3 conditions (laminectomy-only, laminectomy and facet screw, laminectomy and facetectomy), 15 had data for the laminectomy-only and laminectomy and facet screw conditions, and 1 had data for the laminectomy-only and laminectomy and facetectomy conditions. Residual plots were used to confirm model assumptions. Comparisons between durations and among conditions were tested using linear contrasts. Statistical significance was set at .05. Adjusted means and 95% confidence intervals based on the above model are reported unless otherwise noted.

      Results

      Single-unit recordings were obtained from afferents that were responsive to dorsal-ventral movement of the L6 vertebra. The receptive field for each of the 20 afferents was located in either the L6 longissimus (n = 17) or multifidus (n = 3) paraspinal muscle. Succinylcholine injection (100-400 mg/kg, intra-arterially) induced high-frequency and long-lasting discharge in all afferents and each afferent exhibited a sustained response to a vibratory stimulus. In addition, all afferents were unloaded by bipolar muscle stimulation (amplitude 0.1-0.3 mA: 50 microseconds).

      Effect of Facet-Fixation and Facetectomy on Baseline Spinal Stiffness

      In the laminectomy-only condition, the premanipulation 1-mm ramp mean spinal stiffness measured at L6 was 11.51 N/mm (range, 6.39-18.23 N/mm). Compared with the laminectomy-only preparation, the mean increase in premanipulation spinal stiffness resulting from the laminectomy and facet screw was 4.02 N/mm (range, 1.08-7.75 N/mm). Mean premanipulation spinal stiffness resulting from the laminectomy and facetectomy decreased to 1.18 N/mm (range of −0.69 to −2.26 N/mm).
      The thrust duration by joint condition interaction (F6,89 = 0.56, P = .76) and differences among thrust duration (F3,56, = 0.06, P = .98) for lumbar stiffness were not significant. Compared with the laminectomy-only condition, the laminectomy and facet screw significantly increased mean spinal thrust stiffness by 4.8 N/mm (P < .001), whereas the laminectomy and facetectomy significantly decreased mean spinal thrust stiffness by 0.4 N/mm (P = .01). Compared with the laminectomy and facet screw condition, the mean change (−5.2 N/mm) in spinal stiffness due to the laminectomy and facetectomy was also significant (P < .001).

      Effect of Spinal Joint Condition on Neural Discharge

      There was a significant thrust duration by joint condition interaction (F8,110 = 3.64, P < .001). Therefore, thrust duration and joint condition could not be interpreted separately. Adjusted means and 95% confidence intervals of afferent activity between thrust durations for each facet joint condition are shown in Figure 3. Regardless of condition, significant differences in ∆MIF were found between the shortest thrust duration (75 milliseconds) and the 2 longest thrust durations of 150 and 250 milliseconds.
      Figure thumbnail gr3
      Fig 3Comparisons between mean change in MIF (∆MIF) during 5 manipulative thrust durations applied in each of 3 spinal joint conditions. Time-control represents a nonthrust or 0-millisecond thrust duration. Data reported as adjusted means and 95% confidence intervals with significance. Lam., laminectomy MIF, mean instantaneous frequency.
      Figure 4A shows the differences in afferent activity during each of the 5 L6 thrust durations (0-time control, 75, 100, 150, and 250 milliseconds) between the laminectomy-only condition and the laminectomy and facet screw condition. The laminectomy and facet screw condition produced a significantly larger decrease in adjusted mean ∆MIF during the thrust durations of 75 milliseconds (P < .001), 100 milliseconds (P = .04), and 150 milliseconds (P = .02) when compared with the laminectomy-only condition. The largest mean difference in afferent activity occurred at the shortest thrust duration of 75 milliseconds (Fig 4A). No differences in ∆MIF were seen either in the time-control or at the longest thrust duration of 250 milliseconds. The lack of changes within the time-control indicates the inherent stability of baseline afferent discharge over the duration of the experiments despite multiple manipulations and procedures having been performed.
      Figure thumbnail gr4
      Fig 4Comparisons of the mean change in MIF (∆MIF) during 5 manipulative thrust durations between the laminectomy-only and the laminectomy and facet screw conditions (A) and the laminectomy-only and the laminectomy and facetectomy conditions (B). Data reported as adjusted means and 95% confidence intervals. Time-control represents a nonthrust or 0-millisecond thrust duration. Lam., laminectomy; MIF, mean instantaneous frequency.
      In contrast to the decrease in spindle discharge during the HVLA-SM thrust caused by increasing intervertebral stiffness via the laminectomy and facet screw, spindle discharge increased during the HVLA-SM thrust when stiffness was decreased by the laminectomy and facetectomy (Fig 4B). Comparing differences in afferent activity between the laminectomy-only conditions and laminectomy and facetectomy condition, significantly larger increases in mean spindle discharge occurred during the 2 shortest thrust durations, 75 and 100 milliseconds (P < .001; Fig 4B). Unlike in the laminectomy and facet screw condition, mean ∆MIF in the laminectomy and facetectomy condition was not significant for either the 150- and 250-millisecond thrust durations in the laminectomy and facetectomy condition (Fig 4). There was no change in the time-control afferent discharge between the laminectomy-only and laminectomy and facetectomy conditions.

      Discussion

      This study indicates that biomechanical dysfunction at a single facet joint impacts how mechanoreceptive afferents respond to delivery of an HVLA spinal manipulative thrust. Whereas increased spinal stiffness decreased muscle spindle responses, decreased spinal stiffness increased it during clinically relevant HVLA-SM thrust durations (≤150 milliseconds). Because spinal stiffness had a little effect on spindle responses during HVLA-SM when its thrust duration was longer than that typically used clinically (ie, at the 250-millisecond thrust duration), sensory input from paraspinal muscle spindles during slower manual therapeutic interventions (≥250 milliseconds) may not be impacted by facet joint dysfunction (at a single joint level at least).
      These findings may have implications for clinical decision making if maximizing sensory input from segmental paraspinal tissues is important for optimizing manual therapy's therapeutic benefit. Knowledge of spinal stiffness
      • Fritz JM
      • Koppenhaver SL
      • Kawchuk GN
      • Teyhen DS
      • Hebert JJ
      • Childs JD
      Preliminary investigation of the mechanisms underlying the effects of manipulation.
      and manipulative dosage
      • Reed WR
      • Cao DY
      • Long CR
      • Kawchuk GN
      • Pickar JG
      Relationship between biomechanical characteristics of spinal manipulation and neural responses in an animal model: effect of linear control of thrust displacement versus force, thrust amplitude, thrust duration and thrust rate.
      • Gudavalli MR
      • DeVocht JW
      • Tayh A
      • Xia T
      Effect of sampling rates on the quantification of forces, durations, and rates of loading of simulated side posture high-velocity, low-amplitude lumbar spine manipulation.
      (eg, the magnitude of thrust duration and peak thrust amplitude) may be critical factors for determining the most effective manual therapy treatment regimens. Based on the results from a single facet fixation, one could speculate that in clinical conditions where intervertebral mobility is decreased such as advanced degenerative disk or joint disease, clinicians may need to alter their treatment approach to create greater levels of “afferent barrage” from paraspinal mechanoreceptors if this is indeed an essential component of the mechanisms underlying the efficacy of spinal manipulation as has been theorized.
      • Pickar JG
      Neurophysiological effects of spinal manipulation.
      • Korr IM
      Proprioceptors and somatic dysfunction.
      The general relationship between HVLA-SM thrust duration in the laminectomy-only condition and changes in muscle spindle activity in the present study was similar to that previously reported in the same animal model.
      • Pickar JG
      • Wheeler JD
      Response of muscle proprioceptors to spinal manipulative-like loads in the anesthetized cat.
      • Reed WR
      • Cao DY
      • Long CR
      • Kawchuk GN
      • Pickar JG
      Relationship between biomechanical characteristics of spinal manipulation and neural responses in an animal model: effect of linear control of thrust displacement versus force, thrust amplitude, thrust duration and thrust rate.
      Overall, as thrust durations became shorter, muscle spindle discharge frequency increased (Fig 3). This relationship was presumably caused primarily by a muscle spindle's inherent sensitivity to the rate change in muscle length. Intervertebral joint dysfunction (at a single facet joint) did not alter this inherent sensitivity.

      Implications for Clinical Practice

      In clinical practice, practitioners of manual therapy typically consider segmental levels with increased stiffness as being in need of manipulation.
      • Fritz JM
      • Whitman JM
      • Childs JD
      Lumbar spine segmental mobility assessment: an examination of validity for determining intervention strategies in patients with low back pain.
      • Abbott JH
      • Flynn TW
      • Fritz JM
      • Hing WA
      • Reid D
      • Whitman JM
      Manual physical assessment of spinal segmental motion: intent and validity.
      • Murphy DR
      • Morris C
      Manual examination of the patient.
      Reducing facet joint hypomobility itself has been hypothesized as an underlying mechanism of the beneficial effect of HVLA-SM.
      • Cramer GD
      • Cambron J
      • Cantu JA
      • et al.
      Magnetic resonance imaging zygapophyseal joint space changes (gapping) in low back pain patients following spinal manipulation and side-posture positioning: a randomized controlled mechanisms trial with blinding.
      • Evans DW
      Mechanisms and effects of spinal high-velocity, low amplitude thrust manipulation: previous theories.
      • Henderson CN
      The basis for spinal manipulation: chiropractic perspective of indications and theory.
      This study indicates that relative increases vs decreases in spinal stiffness caused by intervertebral dysfunction at a single facet joint can impact paraspinal sensory responses during clinically relevant HVLA-SM thrust durations (≤150 milliseconds) directed at the same segmental level as the dysfunction. More specifically, the laminectomy and facet screw condition significantly decreased paraspinal muscle spindle discharge during thrust durations of 75, 100, and 150 milliseconds, whereas the laminectomy and facetectomy condition significantly increased paraspinal muscle spindle discharge at 75 and 100 milliseconds. The relationship between intervertebral joint mobility and alterations of primary afferent activity during and after these shorter duration manual therapy interventions may provide (at least in part) an explanation for clinical prediction rules that successfully use intervertebral joint dysfunction to identify patient subpopulations who respond to different types of manual therapy.

      Limitations

      The present study was limited to the effects of intervertebral dysfunction at a single spinal joint. In a clinical setting, patients with acute and chronic LBP are often assessed as having dysfunctional joints at multiple segmental levels with additional confounding factors such as advanced facet and/or disk degeneration, muscle spasm, pain, and/or joint inflammation. The animal model used in the current study is an attempt to investigate the effects of the simplest degree of intervertebral joint dysfunction on paraspinal sensory input. Although the method used to create segmental fixation was invasive, it produced a lesser degree of total spinal joint dysfunction than the more aggressive intervertebral body fixation techniques incorporating instrumentation such as steel rods and/or intervertebral cages. By not anteriorly fixating the lumbar vertebral bodies, the current facet joint dysfunction model may provide greater similarity to the total degree of segmental dysfunction (at a given vertebral level) commonly observed in clinical manual therapy settings. That said, future studies should investigate greater degrees of joint dysfunction (multiple facet joints at the same or adjacent segmental levels) and/or the effect of degenerative/inflammatory processes on paraspinal mechanoreceptor activity during and after manual therapy interventions.
      Although most spinal manipulative maneuvers include a posterior-anterior component, rotary and/or other non–posterior-anterior thrust vectors are often used in clinical settings and their use should be considered in future studies. A rotary component was not part of the current study because of the increased risk it posed to tearing the afferent fiber off the recording electrode.
      Although the HVLA-SM procedure causes relatively small movements between the manipulated and surrounding vertebrae (between 0.4- and 2.6-mm translation and 0.4° and 3.5° rotation)
      • Nathan M
      • Keller TS
      Measurement and analysis of the in vivo posteroanterior impulse response of the human thoracolumbar spine: a feasibility study.
      • Gal J
      • Herzog W
      • Kawchuk G
      • Conway PJ
      • Zhang YT
      Movements of vertebrae during manipulative thrusts to unembalmed human cadavers.
      • Ianuzzi A
      • Khalsa PS
      Comparison of human lumbar facet joint capsule strains during simulated high-velocity, low-amplitude spinal manipulation versus physiological motions.
      ; ramp displacements that exceed 1 mm for determining premanipulation spinal joint stiffness may provide a better estimate of initial spinal stiffness particularly due to the inherent flexibility of the cat spine.
      • Ianuzzi A
      • Pickar JG
      • Khalsa PS
      Determination of torque-limits for human and cat lumbar spine specimens during displacement-controlled physiological motions.
      • Ianuzzi A
      • Pickar JG
      • Khalsa PS
      Validation of the cat as a model for the human lumbar spine during simulated high-velocity, low-amplitude spinal manipulation.
      However, the mean premanipulation spinal stiffness of 11.51 N/mm in the laminectomy-only condition was similar to that previously reported in the intact cat lumbar spine (6.07-12.14 N/mm
      • Vaillant M
      • Edgecombe T
      • Long CR
      • Pickar JG
      • Kawchuk GN
      The effect of duration and amplitude of spinal manipulative therapy (SMT) on spinal stiffness.
      ), the rat lumbar spine (14.52 N/mm
      • Henderson CN
      • Cramer GD
      • Zhang Q
      • DeVocht JW
      • Fournier JT
      Introducing the external link model for studying spine fixation and misalignment: part 2. Biomechanical features.
      ) and the lumbar spine of healthy human volunteers (~11-17 N/mm
      • Lee M
      • Liversidge K
      Posteroanterior stiffness at three locations in the lumbar spine.
      and 14.05-16.41 N/mm
      • Viner A
      • Lee M
      • Adams R
      Posteroanterior stiffness in the lumbosacral spine, the correlation between adjacent vertebral levels.
      ).
      Failure to create a minimal change (2%) in stiffness several preparations was likely the result of a combination of factors including but not limited to inadequate placement of the facet screw, partial splintering of the facet joint, incomplete facetectomy, the greater inherent flexibility of the feline spinal column, and/or biomechanical testing in the dorsal-ventral direction only as opposed to including lateral and/or rotary-type movements for which the facet joints play a greater role. Attempts should be made in future studies to eliminate as many of these factors as possible. Although the resulting number of preparations was small in the laminectomy and facetectomy condition, the statistical analysis indicated significant changes at the 2 shorter thrust durations; these findings should be confirmed in a powered study with minimal loss of preparations within the laminectomy and facetectomy condition.
      The effects spinal joint dysfunction have on muscle spindle discharge during HVLA-SM thrust durations of less than 10 milliseconds such as those associated with instrument-delivered HVLA-SM
      • Colloca CJ
      • Keller TS
      • Black P
      • Normand MC
      • Harrison DE
      • Harrison DD
      Comparison of mechanical force of manually assisted chiropractic adjusting instruments.
      were not determined in the current study. However, in a laminectomy-only preparation, we recently reported that spindle discharge became asymptotic with increasing thrust rate and suggested the presence of threshold range of thrust rates (200-500 N/s), after which faster rates would provide little additional effect on the neural response compared with the shortest thrust duration of 75 milliseconds.
      • Reed WR
      • Cao DY
      • Long CR
      • Kawchuk GN
      • Pickar JG
      Relationship between biomechanical characteristics of spinal manipulation and neural responses in an animal model: effect of linear control of thrust displacement versus force, thrust amplitude, thrust duration and thrust rate.

      Conclusion

      The findings of this study showed that relative increases vs decreases in spinal stiffness caused by intervertebral dysfunction at a single facet joint can impact paraspinal sensory responses during clinically relevant HVLA-SM thrust durations (≤150 milliseconds) directed at the same segmental level as the dysfunction.
      The relationship between intervertebral joint mobility and alterations of primary afferent activity during and after various manual therapy interventions may be used to help to identify patient subpopulations who respond to different types of manual therapy and better inform practitioners delivering the therapeutic intervention.

      Practical Applications

      • This study found that intervertebral dysfunction at a single facet joint can alter paraspinal sensory input from mechanoreceptors during clinically relevant durations of HVLA-SM.
      • This may become important to patient care if future studies show that a critical threshold of paraspinal sensory input is required to obtain positive clinical outcomes.
      • Findings are limited to simulated dorsal-ventral HVLA-SM manipulative thrusts in otherwise healthy animals. Confounding factors such as degenerative and/or inflammatory joint changes as well as rotary thrust components such as common in clinical settings may alter these findings.

      Funding Sources and Potential Conflicts of Interest

      This study was funded by K01AT005935 (to WRR) and was conducted in a facility constructed with support from Research Facilities Improvement Grant No. C06 RR15433 from the NCRR (National Center for Research Resources), National Institutes of Health. No conflicts of interest were reported for this study.

      Contributorship Information

      • Concept development (provided idea for the research): WRR, JGP.
      • Design (planned the methods to generate the results): WRR, JGP.
      • Supervision (provided oversight, responsible for organization and implementation, writing of the manuscript): WRR, JGP.
      • Data collection/processing (responsible for experiments, patient management, organization, or reporting data): WRR, JGP, CRL.
      • Analysis/interpretation (responsible for statistical analysis, evaluation, and presentation of the results): WRR, JGP, CRL.
      • Literature search (performed the literature search): WRR.
      • Writing (responsible for writing a substantive part of the manuscript): WRR.
      • Critical review (revised manuscript for intellectual content, this does not relate to spelling and grammar checking): WRR, JGP, CRL.

      Acknowledgments

      The authors thank Randall Sozio for technical support and Dr Robert Vining for radiology assistance. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

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