J Manipulative Physiol Ther. 2003 (Nov); 26 (9): 567–578 ~ FULL TEXT
Tony S Keller, PhD, Christopher J Colloca, DC, Robert Gunzburg, MD, PhD
Department of Mechanical Engineering,
University of Vermont,
OBJECTIVE: To quantify in vivo spinal motions and coupling patterns occurring in human subjects in response to mechanical force, manually assisted, short-lever spinal manipulative thrusts (SMTs) applied to varying vertebral contact points and utilizing various excursion (force) settings.
METHODS: Triaxial accelerometers were attached to intraosseous pins rigidly fixed to the L1, L3, or L4 lumbar spinous process of 4 patients (2 male, 2 female) undergoing lumbar decompressive surgery. Lumbar spine acceleration responses were recorded during the application of 14 externally applied posteroanterior (PA) impulsive SMTs (4 force settings and 3 contact points) in each of the 4 subjects. Displacement time responses in the PA, axial (AX), and medial-lateral (ML) axes were obtained, as were intervertebral (L3-4) motion responses in 1 subject. Statistical analysis of the effects of facet joint (FJ) contact point and force magnitude on peak-to-peak displacements was performed. Motion coupling between the 3 coordinate axes of the vertebrae was examined using a least squares linear regression.
RESULTS: SMT forces ranged from 30 N (lowest setting) to 150 N (maximum setting). Peak-to-peak ML, PA, and AX vertebral displacements increased significantly with increasing applied force. For thrusts delivered over the FJs, pronounced coupling was observed between all axes (AX-ML, AX-PA, PA-ML) (linear regression, R(2) = 0.35-0.52, P <.001), whereas only the AX and PA axes showed a significant degree of coupling for thrusts delivered to the spinous processes (SPs) (linear regression, R(2) = 0.82, P <.001). The ML and PA motion responses were significantly (P <.05) greater than the AX response for all SMT force settings. PA vertebral displacements decreased significantly (P <.05) when the FJ contact point was caudal to the pin compared with FJ contact cranial to the pin. FJ contact at the level of the pin produced significantly greater ML vertebral displacements in comparison with contact above and below the pin. SMTs over the spinous processes produced significantly (P <.05) greater PA and AX displacements in comparison with ML displacements. The combined ML, PA, and AX peak-to-peak displacements for the 4 force settings and 2 contact points ranged from 0.15 to 0.66 mm, 0.15 to 0.81 mm, and 0.07 to 0.45 mm, respectively. Intervertebral motions were of similar amplitude as the vertebral motions.
CONCLUSIONS: In vivo kinematic measurements of the lumbar spine during the application of SMTs over the FJs and SPs corroborate previous spinous process measurements in human subjects. Our findings demonstrate that PA, ML, and AX spinal motions are coupled and dependent on applied force and contact point.
Keywords: Acceleration, Biomechanics, Chiropractic, Kinematics, Lumbar Spine, Manipulation
From the Full-Text Article:
As spinal manipulation (SM) and chiropractic adjustment continue to be investigated for their clinical outcomes, basic science research into the mechanisms of the interventions lag behind and remain poorly understood. Because spinal manipulation is a mechanical intervention, it is inherently logical to assume that its mechanisms of therapeutic benefit may lie in the mechanical properties of the applied force (mechanical mechanisms), the body's response to such force (mechanical or physiologic mechanisms), or a combination of these and other factors. Biomechanical investigations of the spine's response to SM, therefore, should assist researchers, educators, and clinicians to understand the mechanisms of SM, more fully develop SM techniques, better train clinicians, and ultimately minimize risks while achieving better results with patients.
A number of studies have characterized the forces and force-time histories associated with various spinal manipulation therapies. [1–9] Such studies provide important information concerning the loading history and forces transmitted to patients. The posteroanterior (PA) stiffness or PA load-displacement response of the prone lying subject during SM has also been investigated using static or low-frequency indentation types of techniques, including mobilization and other physiotherapy simulation devices. [10–15] These studies indicate that the thoracolumbar spine has a quasi-static PA structural stiffness of approximately 15 N/mm to 30 N/mm at loads up to about 100 N. Stiffness measurements capture the displacement response of the area under test (vertebrae, disks, and adjacent structures—skin, muscles, and fascia) but cannot easily distinguish the contribution and/or displacement of individual vertebral components. To precisely quantify relative and absolute movements of individual vertebrae, it is necessary to rigidly attach intraosseous pins to the spine. Due to the invasiveness of such procedures, however, these techniques have only been performed in human cadavers [16, 17] or in animals. [18, 19] Research of this nature in living humans is very rare. 
In 1994, Nathan and Keller  first reported sagittal plane bone movements of the lumbar spine of human subjects during mechanical force, manually-assisted, short-lever (MFMA) spinal manipulative thrusts (SMTs). In their study, forces were delivered to the spinous processes (SPs) of the thoracolumbar spine using a spring-loaded adjusting instrument (Activator Adjusting Instrument, or AAI). Intersegmental or intervertebral movements of adjacent lumbar vertebrae were quantified using an intervertebral motion device (IMD)  attached directly to intraosseous pins fixed to the spinous processes. They found that the peak-to-peak amplitude of intervertebral motions were up to 6–fold greater when the short duration (< 5 milliseconds [ms]) AAI thrusts were delivered over spinous processes closer to the IMD measurement site. They also found that PA–directed forces produced coupled axial and flexion-extension rotation movements of the vertebrae. The study by Nathan and Keller  was limited to a single force amplitude PA thrust applied over the spinous processes in 3 subjects, and only the relative movements of 2 adjacent vertebrae (intervertebral motion) were determined. To our knowledge, there are no data in the literature that characterize the in vivo vertebral and intervertebral coupled motion responses of the spine to varying force amplitudes and contact points mimicking normal clinical practice.
The objective of this study was to quantify vertebral and intervertebral lumbar spinal motions occurring during spinal manipulation in human subjects in vivo. Mechanical force, manually assisted spinal manipulative thrusts of varying force amplitude were applied to vertebral contact points overlying the facet joints and spinous processes, as they are in routine clinical practice. We hypothesized that the vertebral motion response of the spine to PA thrusts would be coupled in different axes and that the force setting and vertebral contact point would modulate the motion response of the lumbar spine.
This study characterizes the in vivo dynamic PA motion response of the lumbar spine during spinal manipulation in patients undergoing surgery. Spinal motions (L1 in 2 patients, L3 in 2 patients, and L4 in 1 patient) were measured in response to different excursion (force) settings and varying segmental contact points (spinous processes and facet joints) at the same spinal levels and adjacent to the pin placement (facet joints). To our knowledge, this marks the first study to report in vivo vertebral and intervertebral motion responses of humans during the application of PA forces in a manner consistent with spinal manipulative therapy.
Due to the invasiveness necessary to quantify spinal motions during spinal manipulation, previous research has typically been limited to cadaver studies. [1, 16, 17, 24] Gál et al  reported their work in measuring relative movements between vertebral bodies during PA thoracic SM. In this study, steel bone pins were embedded into the vertebral bodies of 2 unembalmed postrigor cadavers (each aged 77 years) at the levels of T10, T11, and T12. High-speed cinematography measured spinal motions during SM delivered at the level of T11. Preload and peak forces were approximately 80 and 525 N, respectively, in this study. The authors reported statistically significant mean relative translations and rotations ranged from 0.3 ± 0.2 mm to 0.6 ± 0.4 mm and 0.0 ± 0.3° to 1.9 ± 0.2°, respectively, between the 2 subjects. Similarly, Maigne and Guillon  measured relative lumbar spinal motions during lumbar spinal manipulation in 2 unembalmed cadavers (aged 49 and 71 years) by implanting accelerometers into the vertebral bodies. Using side-posture manipulation, the authors reported a maximum translation between the L4–5 functional spinal unit of 1.1 mm. While the work of Gál et al  and Maigne and Guillon  report similar magnitudes of relative vertebral movements, a number of factors make the research difficult to generalize to our results, such as subject differences, recording and sampling methodologies utilized, and differences in the force-time profiles of the techniques used in the research. Table 4 highlights the differences in methodology in these 3 studies.
The amplitude and time history of the intervertebral motion responses are generally of the same magnitude as previously reported in situ and in vivo relative or intervertebral motion studies. Noteworthy, Nathan and Keller  used a 3–degree-of-freedom spatial linkage displacement sensor attached to 2.4–mm–diameter pins to quantify the in vivo motion response of the lumbar spine of 1 normal subject and 2 patients with spinal disorders requiring surgery. Pin placement was performed using a local anesthetic. In response to an approximately 90 N peak-to-peak PA impulsive force applied over spinous processes superior to the spatial linkage sensor, they reported intervertebral peak-to-peak PA displacements and axial displacements of the L3–4 and L4–5 vertebrae ranging from 0.10 to 0.51 mm and 0.25 to 1.5 mm, respectively. Accounting for differences in force magnitude, the PA intervertebral motion response to impulsive thrusts reported in this study agree with that of Nathan and Keller.  Axial displacements, however, were substantially lower than that reported by Nathan and Keller. 
The lower amplitude axial motion response obtained in the current study compared with Nathan and Keller21 may reflect other factors, including the age and pathology of the patients. Patients in the Nathan and Keller  study were relatively young (36–53 years) and had minimal pathology (1 subject) or moderate lumbar degenerative disk disease (2 patients), in comparison with the patients in this study who were older (48–75 years) and who were undergoing decompressive spinal surgery for spinal canal stenosis. Other factors, notably the thrust force vector, segmental contact points in relation to the pin mount, posture during testing, and motion measurement method, may also have contributed to the observed differences. In the current study, thrusts were applied to the spinous process (and over the facet joints) in a manner consistent with clinical practice in contrast with Nathan and Keller,  who only examined thrusts over the spinous processes and who specifically applied vertically vectored forces with respect to the table on which the prone lying subjects were tested. In addition, the patients examined in the current study were given general anesthesia and were placed in a prone posture with their legs and hips slightly flexed, producing a more lordotic posture compared with the prone lying patients examined by Nathan and Keller. 
A limitation of the current study was the fact that we did not quantify the precise anterior-superior thrust angle and segmental contact points during the SMTs. Both of these factors may influence the motion response, but the surgical setting and the complexity of the motion and neurophysiological measurements performed precluded such measurements. Care was taken to perform the SMTs in a consistent and clinically relevant manner, namely anterior-superior angulations of 20° ± 5° and offset of 10 to 15 mm from the midline (thrusts over FJs). Indeed, our aim was to quantify the lumbar vertebral motion response associated with spinal manipulation as it is performed in routine clinical chiropractic practice. Recent studies, however, indicate that the sagittal plane PA and axial motion responses of the lumbar spine to impulsive forces are relatively insensitive to thrust angle/contact point variations of 20°/5 mm or less.  According to computer simulations performed by Keller and associates,  a 5° angulation difference (?15° versus ?20°) and 5–mm contact point offset are predicted to result in less than an 0.1 mm difference in the peak-to-peak PA and axial motion responses to impulsive forces. Given the specificity of the SMT force vector and contact points, we feel that the methodology was justified. While imaging technology is currently available to identify the underlying segmental contact points during biomechanical assessments, we do not believe that this specificity would have assisted our aim of quantifying vertebral motions during clinically applied SMT. Nevertheless, the influence of variations in force vector and contact point on the in vivo motion response deserves further consideration.
The MFMA instrument used for the SMTs produced a very short time duration (impulsive) force that induced a transient dynamic oscillatory motion response. For a given force amplitude, impulsive forces are associated with smaller displacements in comparison with longer duration nonperiodic forces such as that commonly applied during manual manipulation.  Consequently, high-precision, low-noise, dynamic accelerometers were used in this study to quantify the dynamic motion response of individual segments and adjacent vertebral segments. The posteroanterior, medial-lateral, and axial acceleration responses and displacements derived from the acceleration responses indicate that the method yields results comparable with other kinematic measurement methods, including the aforementioned spatial linkage sensor. Additional work is needed to determine the reproducibility of the acceleration-based vertebral motion analysis method.
In the current study, we did not transform the Cartesian components of acceleration (x, y, z) to account for rotations of the vertebral segments or to estimate the flexion-extension rotation and medial-lateral rotation of the segments. Such transformations require knowledge of the location of the rotation axes relative to the accelerometer axes, and although we obtained fluoroscopic images of the pin-accelerometer sites, the image quality and image coverage were insufficient to perform these measurements in a manner precise enough to warrant transformation. Given the small absolute x, y, z vertebral displacements measured (< 1 mm), vertebral rotations would be predicted to be extremely small and therefore the transformed vertebral motions would not be expected to vary appreciably from that reported in this study. The absolute intervertebral flexion-extension rotations (< 1°) reported by Nathan and Keller21 and vertebral and intervertebral flexion-extension rotations reported by Keller et al  support this assumption. A 6–degree-of-freedom motion measurement system (3 translations and 3 rotations) would provide a more precise description of vertebral displacements and could be used to obtain vertebral rotations.
Complex, force-dependent motion patterns were observed in response to the application of impulsive forces over the facet joints and the spinous processes. We found that SMTs applied over the facet joints tended to produce a more marked ML motion response, whereas thrusts applied over the spinous processes resulted in a greater posteroanterior and axial displacement response. We expected that vertebral motions would occur in each of the 3 orthogonal axes in response to thrusts delivered in primarily one axis; however, the significant off-axis motions or “coupling” response that was observed between all axes (AX–ML, AX–PA, PA–ML) was much more appreciable than we had originally hypothesized. Motion coupling may play a significant role in terms of the putative therapeutic response associated with spinal manipulative therapy. Also noteworthy was our finding that the vertebral motion response was modulated in proportion to the force amplitude. Namely, a 5–fold increase in the facet joint SMT force produced a significant increase in the ML (2.3×), PA (3.7×), and AX (2.5×) peak-to-peak displacements. Results obtained for the intervertebral motion response showed similar trends and were of similar amplitude to the vertebral motion response, but statistical analyses could not be performed since intervertebral motion responses were obtained in only one patient. Additional work is needed to quantify the effects of SMT force amplitude and contact point on in vivo intervertebral motion responses.
It is important to note that our results are presented for patients undergoing surgery for significant spinal disorders and therefore should not be considered “normal lumbar segment motion responses.” As previously noted, investigations into spinal motions during SM are in their infancy, so readily available data regarding spinal motions in normal subjects as opposed to subjects with spinal disorders are sparse.21 A number of studies indicate that it is likely that spinal motions are highly dependent on the force-time input of the directed thrust, [14, 26–28] as well as a variety of clinical factors such as pain, [7, 13, 29] spinal morphology,  the presence of degeneration, [31–33] and muscular stiffness. [34, 35] Therefore, vertebral motions observed in the spinal surgery patients are not expected to be representative of normal or asymptomatic subjects.
Recent work by Kaigle et al36 examined in vivo spinal motions and muscular responses in patients and asymptomatic subjects performing unresisted flexion-extension tasks. They found that intervertebral motions and trunk mobility were significantly lower in the patients than controls both in terms of range and pattern of motion. In addition, persistent muscle activation as noted from a lack of flexion-relaxation phenomena was observed in the patients as opposed to the asymptomatic subjects. Kaigle et al  concluded that such persistent muscular activity may be characteristic of low back pain patients where said etiology may act to restrict intervertebral motion to provide stability to help protect diseased passive spinal structures from movements that may cause pain. Still other factors such as intra-abdominal pressure,  cycle of breathing,  spinal level being tested, [21, 39] vector of applied force, [40–42] and spinal positioning during testing  have been found to be important variables of spinal motion. In the current study, we accounted for many of these variables by placing patients in the same position on the same frame, standardizing the segemental level, vector, and cycle of breathing during performance of the SMTs. Further work in this regard with respect to understanding spinal motion differences among patients and asymptomatic subjects is warranted.
The results obtained from this study provide basic biomechanical information that is useful to both clinicians and researchers. The dynamic motion response data, force dependence, and coupling characteristics of the spinal segments to PA thrusts reported in this study will also assist researchers in the development and validation of computer models that aim to simulate the static and dynamic motion response of the spine. [25, 44–47] Based on the results of this study, a recent model developed by Keller et al  is currently being refined to include motion coupling in each of the orthogonal axes of the spine.
Complex spinal motions occur during MFMA SMTs that are dependent on the applied posteroanterior force and segmental contact point. Our findings indicated the following:
Posteroanterior impulsive forces applied over the facet joints or spinous processes produce posteroanterior vertebral motions that are coupled in the axial (cranial-caudal) and medial-lateral axes.
Posteroanterior impulsive forces applied over the facet joints result in vertebral displacements that are greatest in the medial-lateral axis, followed by the posteroanterior axis and the axial axis.
Increases in the posteroanterior impulsive force applied over the facet joints result in a significant increase in the posteroanterior, medial-lateral, and axial vertebral displacement responses. Medial-lateral and posteroanterior motion responses were significantly greater than the axial response for all facet joint force settings.
Vertebral and intervertebral displacement responses were of similar amplitude. Additional studies of this nature, including other forms of spinal manipulation with varying force-time profiles, are needed in both normal subjects and patients. From such studies, one may be able to identify motion patterns that can be linked to specific pathological musculoskeletal conditions. Further, more work in this area may assist in identifying thrust force/acceleration time profiles and vectors that may maximize the putative aspects of chiropractic adjustments or spinal manipulative therapy.
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