Christopher J Colloca, DC, Tony S Keller, PhD, Robert Gunzburg, MD, PhD
State of the Art Chiropractic Center,
Pheonix, AZ, USA.
OBJECTIVE: To simultaneously quantify vertebral motions and neuromuscular and spinal nerve root responses to mechanical force, manually assisted, short-lever spinal manipulative thrusts.
METHODS: Four patients underwent lumbar laminarthrectomy to decompress the central spinal canal and neuroforamina, as clinically indicated. Prior to decompression, finely threaded, 1.8-mm diameter intraosseous pins were rigidly fixed to the lumbar spinous process (L1 or L3) using fluoroscopic guidance, and a high-frequency, low-noise, 10-g, triaxial accelerometer was mounted to the pin. Following decompression, 4 needle electromyographic (nEMG) electrodes were inserted into the multifidus musculature adjacent to the pin mount bilaterally, and 2 bipolar platinum electrodes were cradled around the left and right S1 spinal nerve roots. With the spine exposed, spinal manipulative thrusts were delivered internally to the lumbosacral spinous processes and facet joints and externally by contacting the skin overlying the respective spinal landmarks using 2 force settings ( approximately 30 N, < 5 milliseconds (ms); approximately 150 N, < 5 ms) and 2 force vectors (posteroanterior and superior; posteroanterior and inferior).
RESULTS: Spinal manipulative thrusts resulted in positive electromyographic (EMG) and compound action potential (CAP) responses that were typically characterized by a single voltage potential change lasting several milliseconds in duration. However, multiple EMG and CAP discharges were observed in numerous cases. The temporal relationship between the initiation of the mechanical thrust and the neurophysiologic response to internal and external spinal manipulative therapy (SMT) thrusts ranged from 2.4 to 18.1 ms and 2.4 to 28.6 ms for EMG and CAP responses, respectively. Neurophysiologic responses varied substantially between patients.
CONCLUSIONS: Vertebral motions and resulting spinal nerve root and neuromuscular reflex responses appear to be temporally related to the applied force during SMT. These findings suggest that intersegmental motions produced by spinal manipulation may play a prominent role in eliciting physiologic responses.
From the Full-Text Article:
In the understanding of musculoskeletal pain and the treatment of spinal disorders, basic science research has revealed a variety of pain generators in spinal tissues. The presence of mechanosensitive and nociceptive afferent fibers in spinal tissues (disk, facet, ligaments, and muscles) [1-5] and the subsequent neurophysiologic research demonstrating the role of such afferent stimulation in pain production6, [7, 8] and coordinated neuromuscular stabilization of the spine [9-14] provide a theoretical framework to investigate the mechanisms of chiropractic adjustments or spinal manipulative therapy (SMT). The mechanical and physiologic influence of SMT on the targeted spinal tissues has recently begun to be quantified experimentally. An important first step in validating chiropractic theories is to quantify the mechanical and neurophysiologic responses that occur during chiropractic adjustments.
Previous experimental and clinical work has identified certain neurophysiologic and biomechanical (neuromechanical) factors to be of central importance to understanding the underlying mechanistic nature of chiropractic. However, this work has been limited to animal models, noninvasive procedures, or minimally invasive procedures. For example, Pickar and McLain  measured afferent unit discharge to facet manipulation and muscle spindle and Golgi tendon organ responses to spinal manipulative-like loads in the feline. Basic animal research has now demonstrated the existence of neural discharge during spinal manipulative-like loads,  but the results are not easily extrapolated in humans. Moreover, only limited research has been conducted to investigate the vertebral motions that occur during spinal manipulative therapy. [17-19]
Intraoperative monitoring techniques have proven beneficial for monitoring neurophysiologic events during spinal surgery, but such techniques have only recently been used to study responses of spinal manipulation. Colloca et al  recently completed an investigation of spinal nerve root action potentials in response to intraoperative lumbosacral spinal manipulation. Spinal nerve root responses were found to be related to segmental contact point, and applied force vector and similarities were observed between internal and external thrusts. Due to the limitations of the study design, only 1 subject was investigated, nerve root measurements were unilateral, and the temporal relationships of the SMTs and nerve root response could not be studied. Nevertheless, such research assists in the understanding of the neuromechanical mechanisms of spinal manipulation.
To our knowledge, no other study has simultaneously recorded spinal motions and physiological responses from spinal nerve roots and paraspinal muscles during spinal manipulation. Building on our earlier work,  we performed a series of in vivo intraoperative neuromechanical experiments in human subjects. The objective of these experiments was to simultaneously quantify vertebral motions and bilateral neuromuscular and spinal nerve root responses to spinal manipulative thrusts.
Several findings emerge from this study, the most important of which is the confirmation that SMT can induce spinal motion and subsequent spinal nerve root and neuromuscular reflex responses in the adjacent musculature. This appears to be the first study to simultaneously measure vertebral movements, nerve root responses, and neuromuscular reflexes during SMT in human subjects. Such neuromechanical responses may be related to the therapeutic benefits associated with spinal manipulation as administered in routine clinical practice.
We hypothesized that mechanical stimulation of viscoelastic structures during SMT would result in physiologic responses in human subjects based on the knowledge of the presence of mechanosensitive afferents in the discoligamentous and muscular spinal tissues. [2, 3, 6] Despite the fact that preliminary work had demonstrated relationships between mechanical and electrical stimulation of spinal articulations resulting in neurophysiologic and neuromuscular responses, such research has mostly been limited to the laboratory utilizing animal models. [13, 16, 26] Intraoperative monitoring techniques are commonly used in spinal surgery and offer promise for evaluating neurophysiologic responses during SMT. [27-31] Thus, the objective of the current study was to measure intraoperative neuromechancial responses with a commonly used conservative therapeutic approach, SMT.
Because our measurements were taken just adjacent to the dorsal root ganglion, it is likely that the CAPs observed in the S1 spinal nerve roots were afferent traffic resulting from the stimulation of mechanosensitive afferent fibers in the viscoelastic spinal tissues during the spinal manipulative thrusts. Sensory receptors within a tissue, such as spinal ligaments, facets, disks, and muscles, can initiate neural outflow to the spinal cord during application of various mechanical stimuli (eg, pressure, elongation, vibration, friction, tissue crushing) and application of chemical stimulants.  Due to the participation of human subjects, we were not able to directly ascertain the exact source of the neurophysiologic responses, as is routinely performed in animal studies. [32, 33] This study, however, building on our previous work,  enabled the intraoperative monitoring of compound action potentials, which in this case represent the algebraic sum of action potentials arising from respective mechanosensitive axons passing through the epineuria of the dorsal spinal nerve roots. Because the CAP represents many axons with differing thresholds of excitation, the CAP response is graded, and the magnitude is proportional to the intensity of stimulation. In the current study, spinal manipulative thrusts were associated with CAP responses of different amplitudes. The presence (or absence) and amplitude of CAP and EMG responses may not only be related to the neurologic status of the patient, as discussed above, but also to the intensity of the mechanical stimulus. In this study, the stimulus was the spinal manipulative thrust using 2 force-time settings (˜ 30 N, < 5 ms and ˜ 150 N, < 5 ms). Based on our previous work investigating neuromuscular reflex responses, we set the threshold of a “positive” response at 2.5 × baseline, which represents a moderate neurophysiological response (1.5 × baseline = very weak, 5 × baseline = very strong).  We reported that the 2.5 × baseline increase corresponded to a relative mean EMG response of Seroussi and Pope,  equivalent to 3.5% of the prone-lying trunk extension EMG response, which was deemed to be a significant EMG response. This same criteria was applied to the motor unit action potential (MUAP) responses in the current study. It may be likely that larger force magnitudes, as delivered in other forms of SMT, may indeed cause more frequent and larger amplitude neurophysiologic and neuromuscular responses.  Further investigation into the effects of force-time profiles on neuromechanical responses is warranted.
Mean time durations from the mechanical stimulus of the SMT and EMG and CAP responses in this study ranged from 5.5 to 18.3 ms and 8.2 to 10.7 ms, respectively. The finding that in most cases the CAP response preceded the EMG response leads us to believe that the CAP response represents afferent traffic from multiple mechanosensitive units in the muscular and discoligamentous soft tissues and the EMG response may indeed be a reflex. Simply stated, the CAP and EMG responses measured in the current study are suggestive of, but do not provide direct evidence for, the reflexive nature of the paraspinal EMG activity. Later duration responses are normally delayed due to the reflex duration from the time it takes for the stimulus to travel along the Ia fibers, through the dorsal root ganglion, and across the spinal cord to the anterior horn cell, which then propagates the impulse along the alpha motor axon to the muscle. Alternatively, at times when the EMG response preceded the CAP response, it is likely that this may represent a direct local motor response analogous to an M-wave during H-reflex testing. Such a local muscle response may be from tissue preload prior to the delivery of the SMT. Alternatively, early EMG responses could represent a stimulus artifact. Noteworthy, however, are the time durations recorded in the current study being consistent with those measured in animal models and in humans. Other researchers have used electrical stimulation to measure reflexogenic activity in the adjacent spinal musculature. Indahl et al [13, 26] reported time durations of 4 to 8 ms in a porcine model on stimulating the intervertebral disk and sacroiliac joint. Kang et al  also reported similar stimulus-to-response times of about 10 ms in feline preparations. In addition, Solomonow et al  measured stimulus-to-response time durations of 5 to 10 ms in human subjects on electrical stimulation of the supraspinous ligament. Stimulus-to-response times in the current study corroborate these time durations in our human subjects. Neurologic deficits inherent in the patient population of the current study are likely to be responsible for delays in stimulus-to-response times or the absence of said positive responses in certain instances.
Limitations inherent in this study may help to explain some of the experimental results obtained. For example, a significant number of spinal thrusts did not elicit positive neurophysiological responses. Since the subject population in this study was patients with spinal disorders serious enough to undergo spinal surgery, it would not be uncommon to expect neurologic deficits from damaged tissues. Three fourths of patients in this study had radiculopathy in the left lower extremity. Such clinical presentation might help to explain the greater number of right-sided S1 compound action potential responses, as opposed to those measured from the left S1 spinal nerve root. Solomonow et al  reported similar problems (absence of EMG response) when performing intraoperative experiments in human subjects on measuring multifidus EMG responses during stimulation of the supraspinous ligament. Nevertheless, neurological deficit among patients could be a possible explanation for the decreased number of positive neurophysiologic responses to SMT. The number of positive responses in the current study is related to the threshold level of 2.5 × baseline that we set in the data analysis from our previous work,  and a substantially greater number of positive responses were observed at lower thresholds but were not counted as “positive.” The clinical relevance of CAP and EMG threshold should be further clarified experimentally.
Of further interest were the findings in the current study that spinal deformations were smaller than those reported in part I of this article. Spinal manipulative thrusts were delivered to the L5 and S1 spinal segments in the current experimental protocol, while the pin mount placement was located several segments cephalad at L3 (2 patients) and L1 (2 patients). Thus, measuring spinal motions 2 to 4 spinal segments away from the segmental contact point would explain the smaller spinal deformations as compared with thrusts made closer to the pin placement. These results also corroborate those previously noted by Nathan and Keller  in regard to the relationship between segmental contact point and adjacent segment spinal motions.
In addition, the less frequent nature of positive EMG responses as opposed to CAP responses may also be attributed to the segmental contact points and recording electrode locations. In this study, the nEMG electrodes were placed adjacent to the pin placement at L1 and L3, while the NR electrodes were placed at the level of the S1 spinal nerve roots. The experimental protocol did not allow for nEMG placement any closer to the segmental contact points due to space constraints. Because spinal manipulative thrusts were delivered to the L5-S1 facet joints and the sacral base, it might be expected that the largest responses would be recorded at the level being thrusted on as opposed to 2 to 4 segments cephalad. There are several explanations for the EMG responses at distant sites, which include the multiple segmental innervated nature of the lumbar spine [36, 37] and the fact that spinal manipulative thrusts create spinal motions (and therefore cause deformations in the viscoelastic tissues which contain mechanosensitive afferents) at multiple levels adjacent to the segmental contact point.  Such distally recorded EMG responses and the measurement of contralateral responses support the fact that such neuromuscular and neurophysiologic responses are not simply stimulus artifacts.
An inherent limitation in this study is the small sample size (n = 4). The addition of subjects in this line of investigation will assist in clarifying the experimental results obtained in regard to the neuromechanical effects of SMT, including the effects of directional sensitivity of the SMT on neuromechanical response. Further investigation of different force-time profiles, as commonly used in traditional SMT procedures,  should serve to better describe the neuromechanical responses of SMT. Neurophysiologic models theorize that SMT may stimulate or modulate the somatosensory system and subsequently may evoke neuromuscular reflexes. [15, 39-41] Such reflexes are thought to inhibit hyperactive musculature, inhibit nociceptive traffic, and improve spinal function. This line of investigation assists in understanding the relationships between the mechanical stimulation as delivered in SMT and the concomitant physiological responses. In attempting to understand such neuromechanical relationships, the clinical status of the patient is often overlooked. The highly individualized neuromechanical response characteristics among patients in this study serves to highlight the need to clinically correlate the neuromechanical response characteristics with patient clinical status. The clinical relevance of how SMT may be related to inhibition or stimulation of the central nervous system in modulating nociception in humans awaits clarification. Our current work and the work of others aim to investigate such issues. [42-44]
Spinal manipulation results in measurable biomechanical and neurophysiologic responses, which appear to be individualized among patients. The vertebral motions that occur (rotations and translations) and resulting spinal nerve root and neuromuscular reflex responses appear to be temporally related to the applied force during SMT. These findings suggest that intersegmental motions produced by spinal manipulation may play a prominent role in eliciting physiologic responses. Further work is necessary in elucidating the clinical relevance of these findings. Knowledge of biomechanical and neurophysiologic events that occur during spinal adjustments assists in formulating a theoretical framework to understand the mechanisms of spinal manipulation.