The Journal of Bone & Joint Surgery

The Journal of Bone & Joint Surgery, Volume 89, Issue 5

Scientific Articles | May 01, 2007

Level-Dependent Coronal and Axial Moment-Rotation Corridors of Degeneration-Free Cervical Spines in Lateral Flexion

Narayan Yoganandan, PhD¹; Frank A. Pintar, PhD¹; Brian D. Stemper, PhD¹; Christopher E. Wolfla, MD¹; Barry S. Shender, PhD²; Glenn Paskoff, MS³

¹ Department of Neurosurgery, Medical College of Wisconsin, 9200 West Wisconsin Avenue, Milwaukee, WI 53226. E-mail address for N. Yoganandan: yoga@mcw.edu
² Human Systems Department, NAVAIR, Code 4656, Building 2187, Suite 2280, 48110 Shaw Road, Unit 5, Patuxent River, MD 20670-1906
³ NAVAIR, Code 4.6.2.1, Building 2187, Suite 1280, 48110 Shaw Road, Unit 5, Patuxent River, MD 20670-1906

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Disclosure: In support of their research for or preparation of this work, one or more of the authors received, in any one year, outside funding or grants in excess of $10,000 from the Office of Naval Research (contract N00421-02-C-3005) and Veterans Affairs Medical Research. Neither they nor a member of their immediate families received payments or other benefits or a commitment or agreement to provide such benefits from a commercial entity. No commercial entity paid or directed, or agreed to pay or direct, any benefits to any research fund, foundation, division, center, clinical practice, or other charitable or nonprofit organization with which the authors, or a member of their immediate families, are affiliated or associated.

Investigation performed at the Department of Neurosurgery, Medical College of Wisconsin, Milwaukee, Wisconsin

The Journal of Bone and Joint Surgery, Incorporated

J Bone Joint Surg Am, 2007 May 01;89(5):1066-1074. doi: 10.2106/JBJS.F.00200

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Abstract

Background: Aging, trauma, or degeneration can affect intervertebral kinematics. While in vivo studies can determine motions, moments are not easily quantified. Previous in vitro studies on the cervical spine have largely used specimens from older individuals with varying levels of degeneration and have shown that moment-rotation responses under lateral bending do not vary significantly by spinal level. The objective of the present in vitro biomechanical study was, therefore, to determine the coronal and axial moment-rotation responses of degeneration-free, normal, intact human cadaveric cervicothoracic spinal columns under the lateral bending mode.

Methods: Nine human cadaveric cervical columns from C2 to T1 were fixed at both ends. The donors had ranged from twenty-three to forty-four years old (mean, thirty-four years) at the time of death. Retroreflective targets were inserted into each vertebra to obtain rotational kinematics in the coronal and axial planes. The specimens were subjected to pure lateral bending moment with use of established techniques. The range-of-motion and neutral zone metrics for the coronal and axial rotation components were determined at each level of the spinal column and were evaluated statistically.

Results: Statistical analysis indicated that the two metrics were level-dependent (p < 0.05). Coronal motions were significantly greater (p < 0.05) than axial motions. Moment-rotation responses were nonlinear for both coronal and axial rotation components under lateral bending moments. Each segmental curve for both rotation components was well represented by a logarithmic function (R² > 0.95).

Conclusions: Range-of-motion metrics compared favorably with those of in vivo investigations. Coronal and axial motions of degeneration-free cervical spinal columns under lateral bending showed substantially different level-dependent responses. The presentation of moment-rotation corridors for both metrics forms a normative dataset for the degeneration-free cervical spines.

Clinical Relevance: While clinical studies provide some information on spinal motions, laboratory-driven experimental biomechanical studies allow controlled load application, document motion magnitudes, and provide a critical dataset of moment-rotation responses. Because these data are derived from degeneration-free spines, validation efforts with use of this dataset will greatly improve model predictabilities while studying the effects of pathological processes, trauma, or instrumentation on spinal kinetics and, hence, stability.

Figures in this Article

It is well known that three-dimensional motions occur in the human vertebral column, especially in the cervical spine¹. Motion in the same plane as the applied load or moment is termed the principal motion, and motion in another plane is termed the secondary motion. The complex spinal geometry induces off-axis motions with pure-axis loading. Anatomical features of cervical spine joints contribute to these motions under external loads. Saddle-shaped vertebrae and uncovertebral joints play a role in kinematics^2-4. Two loading modes are of particular importance in the cervical spine because of its unique anatomy. Under axial rotation, motions occur in coronal and axial planes, with the former being the secondary component and the latter the principal component. Under lateral bending, coronal and axial rotations are, respectively, the principal and secondary components of motion. Accurate knowledge of coronal and axial moment-rotation responses of degeneration-free intact cervical spines may assist in treating spinal disorders. This is because trauma, aging, or degeneration can affect spinal motion and lead to instability^1,5.

Although investigators have attempted to quantify cervical moment-rotation responses, to our knowledge, no study has described level-dependent coronal and axial motion corridors from nondegenerated intact cervical spinal columns^6-24. The objective of the present in vitro biomechanical study was, therefore, to determine coronal and axial moment-rotation responses of degeneration-free, normal, intact human cadaveric cervicothoracic spinal columns under the lateral bending mode.

Materials and Methods

Materials and Methods | Results | Discussion | References

Specimen Preparation

Fresh intact human cadaveric cervical spinal columns (from C2 to T1) that were free of hepatitis A, B, and C and human immunodeficiency virus were used. Ligamentous columns were excised following removal of musculature and were deep-frozen until use, as this method has been shown not to affect the biomechanical responses of bone, ligament, and intervertebral disc^25-28. Lateral and anteroposterior radiographs were made. Specimen quality was determined on the basis of a scale of 0 to 3 (Table I)²⁹. The superior half of the axis and the inferior half of the caudad vertebra were embedded in polymethylmethacrylate. This was accomplished by placing the two cervical vertebrae in metal cylinders and inserting Steinmann pins in the two bodies through predrilled holes in the cylinders. The specimen was unconstrained between fixations, and no axial preload was applied. The specimens were attached to an inferiorly placed load cell (model 3803; Robert A. Denton, Rochester Hills, Michigan) that was capable of recording on-axis and off-axis moments and forces in the three planes (Fig. 1). Three retroreflective targets were inserted into each vertebra to obtain three-dimensional spinal motions from a motion analysis system (Vicon; Oxford Metrics, Oxford, England). The accuracy of locating the spatial reflective target position in the typical field of view was 0.1°.

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TABLE I Specimen Quality*

Specimen No.	C2-C3	C3-C4	C4-C5	C5-C6	C6-C7	C7-T1
1	0	0	0	0	0	0
2	0	0	0	0	0	0
3	0	0	0	0	0	0
4	2	0	0	0	0	0
5	1	1	1	0	0	0
6	0	0	0	0	0	0
7	0	0	0	0	0	0
8	0	0	0	0	0	0
9	0	0	0	0	0	0

A rating of 0 indicates normal findings; 0.5, minimal disc narrowing; 1.0, minimal disc narrowing and early osteophyte; 1.5, mild-to-moderate disc narrowing and osteophyte; 2.0, moderate disc narrowing and anterior osteophyte; 2.5, moderate disc narrowing and anterior and posterior osteophytes; and 3.0, severe disc narrowing, facet arthrosis, and osteophyte bridging.

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TABLE I Specimen Quality*

Specimen No.	C2-C3	C3-C4	C4-C5	C5-C6	C6-C7	C7-T1
1	0	0	0	0	0	0
2	0	0	0	0	0	0
3	0	0	0	0	0	0
4	2	0	0	0	0	0
5	1	1	1	0	0	0
6	0	0	0	0	0	0
7	0	0	0	0	0	0
8	0	0	0	0	0	0
9	0	0	0	0	0	0

Specimen Loading

Physiological equal and opposite forces were applied to the superior vertebra with use of a loading frame that created pure moment loading in right and left lateral bending modes (Fig. 1). All specimens were preconditioned by loading and unloading to 2.0 Nm for three cycles, and biomechanical data (loads and motions of the retroreflective targets) were gathered in the subsequent cycle³⁰. Preconditioning and data recording were performed unilaterally, followed by repeating the process contralaterally. The applied load was held constant for thirty seconds prior to acquiring data. Off-axis moments were monitored to ensure the purity of the applied lateral bending moment to the spinal column.

Data Analysis

Spinal responses were obtained as rotations in coronal and axial planes, and rotations were based on the initial undeformed spinal axis. Range-of-motion and neutral zone metrics were used to characterize biomechanics for each segment. The range of motion was defined as the angulation at maximum moment, and the neutral zone was defined as the angular rotation at zero load, measured from the neutral position³⁰. Statistical analyses were conducted with use of analysis of variance techniques. Initially, factorial analysis of variance was used to determine significant differences in metrics on the basis of the segmental level, side of bending moment application, and relevant interactions. The Fisher least-significant-difference post hoc test was used to determine differences (p < 0.05) between the levels in coronal and axial ranges of motion and neutral zones. Moment-rotation responses at each spinal level for both coronal and axial rotational components were described by fitting experimental data with use of the nonlinear logarithmic function: ? = ? + a ln (ß M_x + 1), wherein ? is the coronal or axial rotation metric, M_x is the bending moment, ? is the intercept, and a and ß are constants²⁹. Spinal level-dependent coronal and axial rotations and moment-rotation response corridors are expressed as the mean ± 1 standard deviation.

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Fig. 1: Schematic of the experimental setup (left). Locations of the three retroreflective targets used in each vertebra (right).

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Fig. 2: Stacked bar chart illustrating the range of motion (ROM) and neutral zone (NZ) metrics for the coronal component from cervical spine lateral flexion tests. Stacking of the data was performed only for the mean values of the two components. Error bars indicate ±1 standard deviation limits for both biomechanical components.

Results

Materials and Methods | Results | Discussion | References

Nine specimens from four female and five male donors, who were a mean (and standard deviation) of 34 ± 6.8 years old (range, twenty-three to forty-four years) at the time of death, were tested. Axial and transverse shear loads were within 5 N. Axial moments ranged from —0.133 to 0.160 Nm (mean, —0.024 ± 0.069 Nm), and sagittal plane moments ranged from —0.164 to 0.101 Nm (mean, 0.016 ± 0.085 Nm). One disc at the C2-C3 level was graded as level 2 (Table I), and results from this level for this specimen were not included in the data analyses. Factorial analysis of variance indicated no significant interaction between bending side and spinal level. However, spinal level was found to be a significant factor for coronal and axial ranges of motion (p < 0.05). Therefore, further analyses were conducted by grouping the left and right side data.

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Fig. 3: Stacked bar chart illustrating the range of motion (ROM) and neutral zone (NZ) metrics for the axial component from cervical spine lateral flexion tests. Stacking of the data was performed only for the mean values of the two components. Error bars indicate ±1 standard deviation limits for both biomechanical components.

Coronal ranges of motion (Fig. 2) were significantly greater than axial ranges of motion (Fig. 3) for C2 to T1 levels (p < 0.05). Coronal ranges of motion decreased from cephalad to caudad (Fig. 2), while the greatest axial ranges of motion occurring from C3 to C5 levels showed cranial and caudal decreases (Fig. 3). The C2-C3 level responded with the greatest coronal ranges of motion, and the C7-T1 level responded with the least coronal ranges of motion. The Fisher least-significant difference statistical analysis revealed that coronal ranges of motion were significantly greater at the C2-C3 level than from the C4 to T1 levels (p < 0.05). Motions were also significantly greater at the C3-C4 level than at the C7-T1 level (p < 0.05). In contrast, axial range of motion at the C7-T1 level was significantly smaller than it was from the C2 to C6 levels (p < 0.05).

The coronal neutral zone at the C2-C3 level was significantly greater than the coronal neutral zones from the C5 to T1 levels (p < 0.05) (Fig. 2). At the C3-C4 level, the coronal neutral zone was significantly greater than at the levels from C5 to T1 (Fig. 2). The coronal neutral zone at the C4-C5 level was significantly greater than at the C7-T1 level (p < 0.05). The axial neutral zone at the C2-C3 level was significantly smaller than the axial neutral zone at the C3-C4 level (p < 0.05) (Fig. 3). The axial neutral zone at the C3-C4 level was significantly greater than at the levels from C4 to T1 (p < 0.05). The neutral zone at the C7-T1 level was significantly smaller than at the levels from C4 to C7 (p < 0.05) (Fig. 3).

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Fig. 4: Coronal motion moment-rotation corridors from cervical spine lateral flexion tests for C2-C3, C3-C4, C4-C5, C5-C6, C6-C7, and C7-T1 levels. Corridors are expressed as the mean ± 1 standard deviation. Coefficients representing the mean curves at each spinal level are included in Table II.

Both coronal and axial moment-rotation corridors (Figs. 4 and 5) at all cervical spinal levels were nonlinear, and R² values exceeded 0.95 for each curve at each level (Table II).

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TABLE II Coefficients Representing the Mean Curve of the Nonlinear Function for the Moment-Rotation Corridors

Spinal Level	Coronal Motion Parameters					Axial Motion Parameters
	a	ß	?	a	ß	?
C2-C3	1.13	36.61	2.92	0.44	79.17	0.93
C3-C4	0.97	26.87	2.86	0.41	175.81	1.73
C4-C5	0.86	47.04	1.95	0.48	160.21	1.26
C5-C6	1.36	6.25	1.73	0.60	28.80	1.02
C6-C7	0.98	17.63	1.77	0.69	8.54	0.93
C7-T1	1.98	2.00	0.95	0.82	1.47	0.34

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TABLE II Coefficients Representing the Mean Curve of the Nonlinear Function for the Moment-Rotation Corridors

Spinal Level	Coronal Motion Parameters					Axial Motion Parameters
	a	ß	?	a	ß	?
C2-C3	1.13	36.61	2.92	0.44	79.17	0.93
C3-C4	0.97	26.87	2.86	0.41	175.81	1.73
C4-C5	0.86	47.04	1.95	0.48	160.21	1.26
C5-C6	1.36	6.25	1.73	0.60	28.80	1.02
C6-C7	0.98	17.63	1.77	0.69	8.54	0.93
C7-T1	1.98	2.00	0.95	0.82	1.47	0.34

Discussion

Materials and Methods | Results | Discussion | References

The present study was based on a specific protocol designed to provide coronal and axial motions, a dataset not consistently reported in a majority of previous studies. Off-axis loads were monitored, minimized, and quantified so that coronal and axial kinematics were due to pure lateral flexion, a feature not previously reported in the literature, to the best of our knowledge. Presentations in the form of nonlinear mathematical expressions for both coronal and axial motions, and mean ± 1 standard deviation responses, are also unique to this study. Because moment-rotation corridors were derived with use of degeneration-free columns, the present results may serve as a first step in the understanding of healthy cervical spine responses, a dataset needed to develop devices such as an artificial disc.

Kinematics has been used as a hallmark for spinal instability since 1944³¹. In vitro studies have been designed to assist clinicians in the understanding of the mechanics of back pain³². Kinematics has been used in the prognosis of neck pain in motor vehicle crashes^33-35. From an instrumentation perspective, accurate determination of normal spinal kinematics is needed, as flexible systems for preserving or restoring motion across the affected segment are being developed to replace conventional rigid fixation systems. For example, normal motion patterns serve as limit envelopes for artificial discs^36,37. The importance, and lack, of normative data in defining surgical goals has been recognized for more established procedures such as total knee arthroplasty³⁸.

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Fig. 5: Axial motion moment-rotation corridors from cervical spine lateral flexion tests for C2-C3, C3-C4, C4-C5, C5-C6, C6-C7, and C7-T1 levels. Corridors are expressed as mean ± 1 standard deviation. Coefficients representing the mean curves at each spinal level are included in Table II.

Researchers have stressed the importance of determining material properties of healthy and nondegenerated spines and of quantitatively expressing nonlinearity in the responses^36,39. Our study provides biomechanical data on healthy spine segments. Clinical studies have underscored the need to examine motions under modes other than flexion-extension⁴⁰. The presentation of normative coronal and axial motions under lateral flexion from this study is a first step. The cervical spine shows little off-axis motions under sagittal plane moments, while off-axis motions occur under moments in other planes¹. Because the cervical spine sustains and responds to three-dimensional loads in vivo, it is important to understand the behavior in all loading modes, as out-of-plane responses may contribute to a higher share of age-related effects than the more frequently studied and less out-of-plane dependent flexion-extension. Mathematical models have become useful tools in the analysis of normal spinal function, disease states, and effects of surgical and nonsurgical interventions⁴¹. Current and future implants are increasingly subjected to stress-analysis modeling early in the design phase to predict and improve performance, prior to prototyping and clinical trials^36,42-44.

Several groups have reported motions from pure moment lateral bending tests with use of human cadavers, albeit with differing protocols. Peak moment magnitudes have ranged from 0.3 to 4.5 Nm^{8,12,13,23,24}. The spinal levels used have ranged from single-level functional units to multilevel columns^{12,13,16,18,20,22-24,45}. Specimen age and quality have also varied^{12,13,16,22-24,45}. Some authors have not provided information on these factors^18,20. Loading paradigms were different. Even when multiple levels were included, kinematics was not determined at all spinal levels. While underscoring the heterogeneity in experimental designs, coronal and axial rotations from the present study generally compare well with those studies. However, previous studies have failed to show significant differences in intersegmental coronal rotations based on level^16,20,21,46.

In addition to specimen selection, the purity of the applied moment may have contributed to the lack of level dependency. The majority of researchers using pure moment paradigms have not specifically addressed this issue and have assumed theoretical mechanics to be valid during complex spine testing^{8,12,13,17,19-21,23,24}. Researchers have recognized the importance of load control and have suggested the use of a multiaxis load-cell to record specimen reactions^47-49. In this study, because the off-axis moments were small (see Results), motions were considered to be a result of pure bending.

A potential limitation of cadaver data is in vivo translation. In this study, the coronal range of motion under unilateral bending for the entire column (Fig. 2) agreed with the findings in in vivo studies in the literature and, thus, was within the physiological range^50-56. Therefore, the applied moment level of 2 Nm is considered to replicate in vivo conditions.

The present in vitro study did not find differences between left and right side bending. Muscles play a role during in vivo motions. While the present ranges of motion are comparable with those from in vivo studies, it is difficult to compare neutral zones because they are a byproduct of a pure moment protocol that included preconditioning. Defined as the motion under no load, the neutral zone is a sensitive parameter and linked to instability⁵⁷. Ligaments stabilize intervertebral joints and seldom reach zero-load state even when the spine is in the neutral position. Indeed, the ligamentous cadaveric cervical spine is almost elastic when physiologically loaded without potting material. It is conceivable that the neutral zone is somewhat a function of the potting mass and testing protocol. Variations in neutral zone data in the literature likely reflect the specific laboratory protocol. Some authors have continued to eliminate or not report this metric while others have incorporated it routinely^{8,12,18,20,23,24,58}. Since in vivo neutral zones represent the behavior of the composite spine including musculature, it would not be appropriate to directly compare this metric with in vitro studies⁵⁰. Finite element modelers should be cautious in the interpretation of this metric. The current neutral zone results were obtained according to established protocols^57,59,60.

Any off-axis loading induces additional moments to the column, and this added loading results in motion. For example, off-axis torque produces axial and coronal rotations, and these components will be superimposed on the intended on-axis lateral bending moment-induced coronal and axial motions. In addition, the superposition effect on the motion from the off-axis loading depends on the magnitude and direction of the off-axis moment. If the off-axis loading produces a positive torque, motions from this torque will be added to the motions from the on-axis lateral flexion. In contrast, motions will be reduced if the off-axis torque is negative. The effects of off-axis motions on coronal and axial motions are not identical to the effects of such motions from on-axis loading. Without a quantified knowledge of off-axis loads and motions, it is difficult to compare current results with other studies. With acknowledgment of the differences in experimental designs, an evaluation of the motion results of this study with use of degeneration-free cervical spinal columns indicated greater flexibility than that seen in other studies with use of degenerated spines or a mix of degenerated with potentially normal spines. For example, at 0.67 Nm, ranges of motion from C2-C3 to C6-C7 levels from a previous study of 3.46°, 3.73°, 3.73°, 2.53°, and 2.13° were considerably lower than values of 6.57°, 5.71°, 4.94°, 3.96°, and 4.26°³². These data may have clinical implications, e.g., degenerative changes such as osteophytes limit spinal motion.

The nonlinear pattern of moment-rotation responses found in this study is typical of human cadaver spine materials^12,20,46. The unique representation will be of benefit to clinicians in understanding normal degeneration-free spinal behavior, and to mathematical modelers, as finite element-predicted responses can be validated over the entire loading range. Geometry, material property, loading and boundary conditions, and validation are important steps in obtaining a clinically relevant mathematical model^61,62. Because of difficulties in obtaining in-house experimental data, modelers have resorted to using data from the literature with little regard to wide variations in testing protocols⁶³. Validation has been primarily limited to comparing motions at specific moment values, often at the highest magnitude reported by the experiment. To better validate models, it is necessary to compare model responses with experimental results over the entire loading range, i.e., from single point to entire curve validation⁶⁴. Level-specific corridors of coronal and axial rotations along with nonlinear curves will assist mathematical modelers to achieve a higher degree of validation, leading to greater confidence and, hence, improved clinical applicability. The logarithmic function reasonably represented the moment-rotation responses as R² values for all levels were >0.95. Because these data are derived from degeneration-free spines, validation efforts with use of this dataset will greatly improve model predictabilities while studying the effects of pathological processes, trauma, or instrumentation on spinal kinetics and, hence, on stability. ?

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Materials and Methods | Results | Discussion | References

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Topics

range of motion ; spine ; cervical spine ; lateral flexion ; tissue degeneration

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Narayan Yoganandan, Frank A. Pintar, Brian D. Stemper, Christopher E. Wolfla, Barry S. Shender, Glenn Paskoff; Level-Dependent Coronal and Axial Moment-Rotation Corridors of Degeneration-Free Cervical Spines in Lateral Flexion. The Journal of Bone & Joint Surgery. 2007 May;89(5):1066-1074.

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