William R. Reed1*, Michael A.K. Liebschner2-4, Randall S. Sozio1, Joel G. Pickar1 and Maruti R. Gudavalli1
1Palmer Center for Chiropractic Research, Davenport, IA, USA
2Department of Neurosurgery, Baylor College of Medicine, Houston, TX, USA
3Research Service Line, Michael E. DeBakey VA Medical Center, Houston, TX, USA
4Exponent Failure Analysis, Houston, TX, USA
Received: 03 March, 2015; Accepted: 04 April, 2015; Published: 06 April, 2015
William R. Reed DC, PhD; Associate Professor, Palmer Center for Chiropractic Research, 741 Brady Street, Davenport, IA 52803, Tel: (563) 884-5145, Fax: (563) 884-5227; Email:
Reed WR, Liebschner MAK, Sozio RS, Pickar JG, Gudavalli MR (2015) Neural Response During a Mechanically Assisted Spinal Manipulation in an Animal Model: A Pilot Study. J Nov Physiother Phys Rehabil 2(1): 020-027. DOI: 10.17352/2455-5487.000021
© 2015 Reed WR, et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Spinal manipulation; Muscle spindle; Neurons afferent; Neurophysiology; Zygapophyseal joint; Spinal fixation; Manual therapy; Cat
Introduction: Mechanoreceptor stimulation is theorized to contribute to the therapeutic efficacy of spinal manipulation. Use of mechanically-assisted spinal manipulation (MA-SM) devices is increasing among manual therapy clinicians worldwide. The purpose of this pilot study is to determine the feasibility of recording in vivo muscle spindle responses during a MA-SM in an intervertebral fixated animal model.
Methods: Intervertebral fixation was created by inserting facet screws through the left L5-6 and L6-7 facet joints of a cat spine. Three L6 muscle spindle afferents with receptive fields in back muscles were isolated. Recordings were made during MA-SM thrusts delivered to the L7 spinous process using an instrumented Activator IV clinical device.
Results: Nine MA-SM thrusts were delivered with peak forces ranging from 68-122N and with thrust durations of less than 5ms. High frequency muscle spindle discharge occurred during MA-SM. Following the MA-SM, muscle spindle responses included returning to pre-manipulation levels, slightly decreasing for a short window of time, and greatly decreasing for more than 40s.
Conclusion: This study demonstrates that recording in vivo muscle spindle response using clinical MA-SM devices in an animal model is feasible. Extremely short duration MA-SM thrusts (<5ms) can have an immediate and/or a prolonged (> 40s) effect on muscle spindle discharge. Greater peak forces during MA-SM thrusts may not necessarily yield greater muscle spindle responses. Determining peripheral response during and following spinal manipulation may be an important step in optimizing its' clinical efficacy. Future studies may investigate the effect of thrust dosage and magnitude.
Spinal manipulation is a form of manual therapy commonly used by clinicians and therapists for conservative treatment of musculoskeletal complaints. Spinal manipulation is typically distinguished from spinal mobilization by the presence of a short duration mechanical thrust applied to the spinal column using either direct hand contact (≤150ms) or one of several commercially available mechanical devices (≤10ms) [1 Colloca CJ, Keller TS, Black P, Normand MC, Harrison DE, et al. (2005) Comparison of mechanical force of manually assisted chiropractic adjusting instruments. J Manipulative Physiol Ther 28: 414-422.-4 Keller TS, Colloca CJ, Moore RJ, Gunzburg R, Harrison DE, et al. (2006) Three-dimensional vertebral motions produced by mechanical force spinal manipulation. J Manipulative Physiol Ther 29: 425-436.]. Among chiropractic clinicians, use of mechanically-assisted spinal manipulation (MA-SM) is growing rapidly with reports that 40-60% of practitioners in the United States, Britain, Belgium, Canada, Australia, and New Zealand use MA-SM in some capacity of patient care [5 National Board of Chiropractic Examiners, Job Analysis of Chiropractic: a project report, survey analysis and summary of the practice of chiropractic in the United States, Greeley, Colorado, USA. National Board of Chiropractic Examiners; 2005.-10 Gleberzon BJ (2002) Chiropractic name techniques in Canada: A continued look at demographic trends and their impact on issues of jurisprudence. J Can Chiropr Assoc 46: 241-256.].
Spinal manipulation has been shown to be effective in the treatment of neck and low back pain and is recommended by clinical guidelines and evidence reports [11Bronfort G, Haas M, Evans R, Kawchuk G, Dagenais S (2008) Evidence-informed management of chronic low back pain with spinal manipulation and mobilization. Spine J 8: 213-225.-16Dagenais S, Tricco AC, Halderman S (2010) Synthesis of recommendations for the assessment and management of low back pain from recent clinical practice guidelines. Spine J 10: 514-529.]. Several reviews regarding the clinical efficacy, safety, usage, and mechanical effects of MA-SM have recently been published [17Fuhr AW, Menke JM (2005) Status of activator methods chiropractic technique, theory, and practice. J Manipulative Physiol Ther 28: e1-e20.-20Taylor SH, Arnold ND, Biggs L, Colloca CJ, Mierau DR, et al. (2004) A review of the literature pertaining to the efficacy, safety, educational requirements, uses and usage of mechanical adjusting devices: Part 2 of 2. J Can Chiropr Assoc 48: 152-161.]. A majority of the MA-SM reviews have noted study weaknesses such as small sample size, non-randomization, and/or lack of a placebo or control group. Despite these limitations, great strides have recently been made in determining the mechanical characteristics and/or biological effects of MA-SM [1 Colloca CJ, Keller TS, Black P, Normand MC, Harrison DE, et al. (2005) Comparison of mechanical force of manually assisted chiropractic adjusting instruments. J Manipulative Physiol Ther 28: 414-422.-4 Keller TS, Colloca CJ, Moore RJ, Gunzburg R, Harrison DE, et al. (2006) Three-dimensional vertebral motions produced by mechanical force spinal manipulation. J Manipulative Physiol Ther 29: 425-436.,21 Colloca CJ, Keller TS, Gunzburg R, Vandeputte K, Fuhr AW (2000) Neurophysiologic response to intraoperative lumbosacral spinal manipulation. J Manipulative Physiol Ther 23: 447-457.-31Colloca CJ, Keller TS, Moore RJ, Gunzburg R, Harrison DE. (2007) Intervertebral disc degeneration reduces vertebral motion responses. Spine 32: E544-E550.]. These studies may provide a foundation for larger randomly controlled trials of MA-SM therapy. One distinct advantage MA-SM offers over manually delivered manipulative thrusts in a research setting is that the thrust velocity and thrust magnitude can be standardized. This feature is of particular importance in efficacy and mechanistic studies investigating the biomechanical and/or neurophysiological effects of spinal manipulation. In addition, MA-SM devices can be mechanically altered to provide an adequate sham spinal manipulation (no force delivered) which is more difficult to accomplish with manually delivered manipulative thrusts.
Spinal manipulation by its very nature is a mechanical stimulus typically applied at clinically identified sites of intervertebral joint fixation or joint hypomobility. Theorized mechanisms for its therapeutic effects include breaking of joint adhesions and/or alteration of sensory input from primary afferents of paraspinal tissues which subsequently act to influence spinal cord reflexes and/or other central neural mechanisms [32Bialosky JE, Bishop MD, Price DD, Robinson ME, George SZ. (2009) The mechanisms of manual therapy in the treatment of musculoskeletal pain: a comprehensive model. Man Ther 14: 531-538.,33Pickar JG (2002) Neurophysiological effects of spinal manipulation. Spine J 2: 357-371.]. MA-SM has been shown to result in oscillatory intervertebral movements [4Keller TS, Colloca CJ, Moore RJ, Gunzburg R, Harrison DE, et al. (2006) Three-dimensional vertebral motions produced by mechanical force spinal manipulation. J Manipulative Physiol Ther 29: 425-436.,24Colloca CJ, Keller TS, Harrison DE, Moore RJ, Gunzburg R et al. (2006) Spinal manipulation force and duration affect vertebral movement and neuromuscular responses. Clin Biomech 21: 254-262.,29Colloca CJ, Keller TS, Gunzburg R. (2004) Biomechanical and neurophysiological responses to spinal manipulation in patients with lumbar radiculopathy. J Manipulative Physiol Ther 27: 1-15.,34Keller TS, Colloca CJ, Gunzburg R (2003) Neuromechanical characterization of in vivo lumbar spinal manipulation. Part I. Vertebral motion. J Manipulative Physiol Ther 26: 567-578.,35Nathan M, Keller TS (1994) Measurement and analysis of the in vivo posteroanterior impulse response of the human thoracolumbar spine: a feasibility study. J Manipulative Physiol Ther 17: 431-441.] and neurophysiological responses in the form of bilateral compound action potentials in both in vivo animal [24Colloca CJ, Keller TS, Harrison DE, Moore RJ, Gunzburg R et al. (2006) Spinal manipulation force and duration affect vertebral movement and neuromuscular responses. Clin Biomech 21: 254-262.,36Smith DB, Fuhr AW, Davis BP. (1989) Skin accelerometer displacement and relative bone movement of adjacent vertebrae in response to chiropractic percussion thrusts. J Manipulative Physiol Ther 12: 26-37.] and human [21Colloca CJ, Keller TS, Gunzburg R, Vandeputte K, Fuhr AW (2000) Neurophysiologic response to intraoperative lumbosacral spinal manipulation. J Manipulative Physiol Ther 23: 447-457.,23Colloca CJ, Keller TS, Gunzburg R (2003) Neuromechanical characterization of in vivo lumbar spinal manipulation. Part II. Neurophysiological response. J Manipulative Physiol Ther 26: 579-591.,29Colloca CJ, Keller TS, Gunzburg R. (2004) Biomechanical and neurophysiological responses to spinal manipulation in patients with lumbar radiculopathy. J Manipulative Physiol Ther 27: 1-15.] studies. The compound action potentials from spinal nerve roots have been attributed to the simultaneous activation of mechano-sensitive afferents innervating viscoelastic spinal tissues such as muscles, ligaments, facet joints, and discs, but the exact sources of neural activity were not identified [23Colloca CJ, Keller TS, Gunzburg R (2003) Neuromechanical characterization of in vivo lumbar spinal manipulation. Part II. Neurophysiological response. J Manipulative Physiol Ther 26: 579-591.,29Colloca CJ, Keller TS, Gunzburg R. (2004) Biomechanical and neurophysiological responses to spinal manipulation in patients with lumbar radiculopathy. J Manipulative Physiol Ther 27: 1-15.,37Colloca CJ, Keller TS, Gunzburg R, Vandeputte K, Fuhr AW. (2000) Neurophysiologic response to intraoperative lumbosacral spinal manipulation. J Manipulative Physiol Ther 23: 447-457.]. Muscle spindles are likely among the mechanoreceptors stimulated by MA-SM. They provide the central nervous system with sensory information regarding both changes in muscle length and the velocity at which those length changes occur. Using a feedback motor control system, we have previously shown that manipulative thrust durations between 25 and 150ms elicit high frequency discharge from paraspinal muscle spindles [38Pickar JG, Sung PS, Kang YM, Ge W. (2007) Response of lumbar paraspinal muscles spindles is greater to spinal manipulative loading compared with slower loading under length control. Spine J 7: 583-595.-40Reed WR, Long CR, Pickar JG. (2013) Effects of unilateral facet fixation and facetectomy on muscle spindle responsiveness during simulated spinal manipulation in an animal model. J Manipulative Physiol Ther 36: 585-594.]. However to our knowledge, recordings of muscle spindle response associated with short manipulative thrust durations (≤10ms) as generated with clinical MA-SM devices, have never been recorded. It is unclear whether the noise artifact or high frequency mechanical perturbation associated with use of short thrust duration MA-SM devices would prohibit, obscure, or otherwise interfere with dorsal root recordings in a cat preparation. Therefore, the primary goal of this pilot study was to determine the feasibility of recording primary afferent muscle spindle responses in dorsal rootlets using a commercially available MA-SM device in an in vivo feline model of intervertebral joint fixation.
Materials and Methods
The experimental preparation and procedures used in this study have been described in greater detail elsewhere [39Reed WR, Cao DY, Long CR, Kawchuk GN, Pickar JG. (2013) 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. Evid Based Complement Alternat Med eCAM 2013: 492039.-42Reed WR, Long CR, Kawchuk GN, Pickar JG (2014) Neural responses to the mechanical parameters of a high velocity. low amplitude spinal manipulation: Effect of preload parameters. J Manipulative Physiol Ther 37: 68-78.] and are therefore presented here only briefly. Electrophysiological recordings were made from 3 back muscle spindle afferents traveling in the dorsal roots of a single Nembutal-anesthetized (35 mg/kg, iv; Oak Pharmaceuticals, Lake Forest, IL) adult male cat (4.5 kg). All experimental procedures were approved by the Institutional Animal Care and Use Committee (#20120601). This pilot data using a MA-SM device was collected from an experimental preparation associated with a separate study investigating the relationship between intervertebral fixation and L6 spinal manipulation delivered by a computer controlled feedback motor.
Catheters were placed in the common carotid artery and external jugular vein to monitor blood pressure, introduce fluids and/or supplemental anesthesia if the arterial pressure rose above 120mm Hg or if a withdrawal reflex became present. The trachea was intubated and the cat was artificially ventilated. Since our focus was on back afferents, the right sciatic nerve was cut to reduce afferent input from the hindlimb. An L5 laminectomy was performed exposing the right L6 dorsal rootlets which were cut close to their entrance to the spinal cord and placed on a platform. Thin filaments were teased with fine forceps until action potentials from a single neuron were identified that responded to both mechanical pressure applied directly to the paraspinal back muscles (multifidus or longissimus) and a fast vibratory stimulus (~70 Hz; mini-therapeutic massage vibrator; North Coast Medical, Morgan Hill CA, USA). Afferent fibers remained positioned on the recording electrode while facet screws (10mm titanium endosteally anchored miniscrews; Dentaurum, Ispringen, Germany) were inserted through the left articular pillars of L5-6 and L6-7 vertebra in similar fashion to that previously described [40Reed WR, Long CR, Pickar JG. (2013) Effects of unilateral facet fixation and facetectomy on muscle spindle responsiveness during simulated spinal manipulation in an animal model. J Manipulative Physiol Ther 36: 585-594.]. An x-ray of the L5-6 and L6-7 facet fixation is shown in Figure 1. Neural activity was passed through a high-impedance probe (HIP511, Grass, West Warwick, RI), amplified (P511 K, Grass) and recorded using a CED 1401 interface and Spike 2 data acquisition software (Cambridge Electronic Design, Cambridge, England).
The Activator IV (Activator IV, Activator Methods Int. Ltd., Phoenix, AZ) is a hand-held clinical device comprised of a rubber-tipped spring-loaded hammer with 4 device settings that produce relative increases in thrust magnitude. Its thrust duration is <10ms and can deliver a maximum force of 212N when tested directly on a load cell [1Colloca CJ, Keller TS, Black P, Normand MC, Harrison DE, et al. (2005) Comparison of mechanical force of manually assisted chiropractic adjusting instruments. J Manipulative Physiol Ther 28: 414-422.]. For the current study, the device was modified by attaching an impedance head under the rubber tip (Figure 1). The impedance head included a dynamic load cell (Model 208C04; PCB, NY) and a tri-axial accelerometer (Model 356A01, PCB, NY).