SPINE Volume 33, Number 23, pp E870 E876 2008, Lippincott Williams & Wilkins

Kinematic Analysis of the Relationship Between Sagittal Alignment and Disc Degeneration in the Cervical Spine
Masashi Miyazaki, MD,* Henry J. Hymanson, BS, Yuichiro Morishita, MD, PhD, Wubing He, MD, Haihong Zhang, MD, Guizhong Wu, MD, Min Ho Kong, MD, Hiroshi Tsumura, MD, PhD,* and Jeffrey C. Wang, MD
The cervical spine withstands the axial load of the head and is the most mobile region of the spine. Normal lordotic alignment is one of the most important factors contributing to effective motion and function of the cervical spine. The discs degenerate with age, and degeneration may ultimately affect the mechanical properties of spinal motion.1,2 On the other hand, it was reported that severe degenerative changes tend to produce less cervical lordosis.3 The loss of normal lordotic alignment may induce pathologic changes in the kinematics and may accelerate degeneration of the functional motion unit. Furthermore, it is well known that sagittal malalignment in cervical degenerative disorders causes spinal morbidities such as neck pain and deterioration of neurologic decit.4 6 However, the relationship of altered alignment on the kinematics and degeneration of the cervical spine has not been elucidated thus far. Kinetic magnetic resonance imaging (MRI) allows us to obtain images of patients in weight-bearing and exion-extension positions and eventually provides considerable information, which would have been unavailable if a conventional MRI were used.2,711 It may also help in understanding the true nature of spinal pathologies. In addition, it can demonstrate the mobility of each motion segment and nally, relate the mobility to the changes in sagittal alignment and disc degeneration. The aim of this study was to investigate the relationship between altered sagittal alignment of the cervical spine and the kinematics of the functional motion unit and disc degeneration by using the kinetic MRI technology. Materials and Methods Participants
From the *Department of Orthopaedic Surgery, Oita University, Oita, Japan. Department of Orthopaedic Surgery, University of California at Los Angeles, Los Angeles, CA; and Department of Neurosurgery, Seoul Medical Center, Seoul, Korea. Acknowledgment date: March 7, 2008. Revision date: April 23, 2008. Acceptance date: May 16, 2008. The manuscript submitted does not contain information about medical device(s)/drug(s). No funds were received in support of this work. No benets in any form have been or will be received from a commercial party related directly or indirectly to the subject of this manuscript. Address correspondence and reprint requests to Jeffrey C. Wang, MD, Chief, Orthopaedic Spine Service, UCLA Comprehensive Spine Center, 1250 16th Street, Suite 745, Santa Monica, CA 90404; E-mail: JWang@mednet.ucla.edu

Study Design. Retrospective analysis using kinetic magnetic resonance images (MRIs). Objective. To investigate the relationship of changes in the sagittal alignment of the cervical spine on the kinematics of the functional motion unit and disc degeneration. Summary of Background Data. Normal lordotic alignment is one of the most important factors contributing to effective motion and function of the cervical spine. Loss of normal lordotic alignment may induce pathologic changes in the kinematics and accelerate degeneration of the functional motion unit. However, the relationship of altered alignment on kinematics and degeneration has not been evaluated. Methods. Kinetic MRIs in exion, neutral, and extension were performed. Study participants were classied into 5 groups based on the C1C7 Cobb angle of sagittal alignmentGroup A: Kyphosis (n 19), Group B: Straight (n 29), Group C: Hypolordosis (n 38), Group D: Normal (n 63), and Group E: Hyperlordosis (n 52). Intervertebral disc degeneration was graded (Grades 15), and the kinematics of the functional spinal unit were obtained. Results. When the alignment shifted from normal to less lordotic, the translational motion and angular variation tended to decrease at all levels. The contribution of the C1C2, C2C3, and C3C4 levels to total angular mobility tended to be higher in Group C than Group D. However, the contribution of the C4 C5, C5C6, and C6 C7 levels tended to be lower in Group C than in Group D. The grade of disc degeneration associated with loss of lordosis tended to be higher than that associated with normal alignment at the C2C3 and C3C4 levels. Conclusion. The present study demonstrated that the changes in sagittal alignment of the cervical spine affect the kinematics. Consequently, it may cause changes in the segment subjected to maximum load for overall motion and accelerate its degeneration. Key words: kinematic analysis, sagittal alignment, disc degeneration, cervical spine, kinetic MRI. Spine 2008;33: E870 E876

From February 2006 to April 2007, kinetic MRI scans of the cervical spine were taken consecutively on 267 patients. Among these, 201 participants (90 men and 111 women) with mild symptomatic neck pain associated with movement, with/without radiculopathy or myelopathy, were included in this study. The mean age of the participants was 44 years (range, 19 93 years). Patients with recent trauma, rheumatoid arthritis, infectious spondylitis, spinal tumors, prior cervical fractures or dislocations, or prior cervical spine surgery were excluded from this study. Additionally participants with severe neck pain who were expected to aggravate their symptoms by moving their neck or who were unable to remain still during exion-extension kinetic MRI scans were excluded from this study.

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Kinematic Analysis of Cervical Sagittal Alignment With Degeneration Miyazaki et al E871 Figure 1. MRI positioning in neutral, exion, and extension positions. A, Neutral position. Participants were rst seated on a bench between the 2 magnets in a relaxed position, with their heads looking straight ahead and without angling the chin (0 neutral position). B, Flexion position. Participants were positioned with theirs chin angled toward their chests (40 exion). C, Extension position. Participants were positioned with their chins angled toward the ceiling (20 extension).

MRI Positioning
Participants were rst seated on a bench between the two magnets in the neutral position with their heads facing straight ahead without angling their chin up or down (0 neutral position) (Figure 1A). This positioning was used for the neutral images. Next, the participants were positioned with their chins angled toward their chests (40 exion) (Figure 1B). This positioning was used to obtain the exion images. Finally, the participants were positioned with their chins angled towards the ceiling (20 extension) (Figure 1C). This positioning was used to obtain the extension images. For each of these positions a exible cervical coil was placed around the participants necks and the front and back of their heads were supported and kept in place with a padded bar and a headrest. Their bodies were not restricted by any fastening straps. Kinetic MRIs were taken with both T1-weighted sagittal spin echo sequences and T2-weighted sagittal fast spin echo sequences in the neutral position and T2-weighted sagittal fast spin echo sequences at the cervical exion and extension positions. Each of these sequences took approximately 5 minutes to complete.

ingly, the neutral-position T2-weighted sagittal images of 1206 cervical intervertebral discs of the 201 subjects were classied into 5 grades (Table 1) by the primary author and were judged eligible for inclusion in the study.

Image Analysis
All radiologic MRI data were recorded using computerbased measurements, and all calculations were performed using an MRI Analyzer (Truemetric Corp., Bellower, CA), as described previously.2 Sagittal MR images were analyzed in 3 positionsexion, neutral, and extension. For digitization, 77 points were marked on each lm by spine surgeons. Specic points were chosen for occiput (Oc), C1, and C2. The anterior and posterior baselines were marked at the Oc. The anterior tubercle and the posterior margin of the atlas and the lowest end of the spinous process were marked at C1, and a point at the tip of the odontoid process was marked at C2; other points were marked accordingly from C3 to T1. For the typical cervical vertebrae from C3-T1, 4 points were marked for the vertebral body (anterior-inferior, anterior-superior, posterior-superior, and posterior-inferior junctions); 2 points were marked for the disc height (the middle of the endplate); and 2 points were marked for the pedicle and spinal cord diameters. Basic measurements included all the static intervertebral angular displacements and translations calculated in different postures. Subsequently, total exibility (motion segment integrity, translational motion, and angular variation) at each vertebral level was calculated from the difference between the exion and extension positions. Translational motion was measured for each segment at 5 cervical intervertebral disc levels, namely, C2C3, C3C4, C4 C5, C5C6, and C6 C7 by determining the anteroposterior motion of 1 vertebra over the other vertebra; a positive value implies anterior translation (antelisthesis), whereas a negative value implies posterior translation (retrolisthesis). The sagittal angular variation was measured for each segment at 5 cervical intervertebral disc levels, namely, C2C3, C3C4, C4 C5, C5C6, and C6 C7. For calculating angular variation, lines were drawn from the inferior borders of the 2 vertebral bodies at a particular level. The lordotic angle was dened as negative, whereas the kyphotic angle was dened as positive. In addition, the angular variation at the C1C2 level was calculated from the C1C7 Cobb angle and each individual angular variation. To elucidate the mechanism underlying the changes in the role of each cervical spine unit in exion-extension motion depending

MRI Technique
MRI of the cervical spine was performed using a 0.6 Tesla MRI scanner (UPRIGHT Multi-Position; Fonar Corp., NY, NY). In the MR unit, 2 doughnut-shaped magnets placed 18 inches apart are vertically oriented, and this enables the scanning of a patient in an upright axially loaded position. Images were obtained using a exible surface coil. We examined the T1weighted sagittal spin echo images [repetition time, 671 milliseconds; echo time, 17 milliseconds; thickness, 3.0 mm; eld of view, 24 cm; matrix, 256 200; and number of excitations (NEX), 2] and T2-weighted sagittal fast spin echo images (repetition time, 3432 milliseconds; echo time, 160 milliseconds; thickness, 3.0 mm; eld of view, 24 cm; matrix, 256 224; and NEX, 2) of each patient.

Study Groups Formed According to Sagittal Alignment

The participants were classied into 5 groups based on the C1C7 Cobb angle of sagittal alignment observed on upright neutral T2-imagesGroup A: Kyphosis (Cobb angle, 0; n 19); Group B: Straight (Cobb angle, 0to 15; n 29); Group C: Hypolordosis (Cobb angle, 15to 30; n 38); Group D: Normal (Cobb angle, 30to 45; n 63); Group E: Hyperlordosis (Cobb angle, 45; n 52) (Figure 2).

Grades of Cervical Disc Degeneration

A comprehensive grading system for cervical disc degeneration was obtained using a previously reported system.2 Accord-

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Figure 2. Study Groups according to sagittal alignment. A , Group A: Kyphosis (Cobb angle, 0). B, Group B: Straight (Cobb angle, 0 to 15). C, Group C: Hypolordosis (Cobb angle, 15to 30). D, Group D: Normal (Cobb angle, 30 to 45). E, Group E: Hyperlordosis (Cobb angle, 45). on the changes in sagittal alignment, we calculated the contribution of each level to the total angular mobility. The total sagittal motion of the cervical spine was dened as the absolute total of the individual sagittal angular variations (C1C2 C2C3 C3C4 C4 C5 C5C6 C6 C7) in degrees. The contribution of each segment to the total angular mobility of the cervical spine between exion and extension was dened as percentage segmental mobility, which was calculated as follows: (the sagittal angular variation of each segment in degrees)/(total sagittal angular motion in degrees) 100.

Table 1. Grading System for Cervical Intervertebral Disc Degeneration

Grade I II III IV V Nucleus Signal Intensity Hyperintense Hyperintense Intermediate Hypointense Hypointense Nucleus Structure Homogenous, white Inhomogenous with horizontal band, white Inhomogenous, gray to black Inhomogenous, gray to black Inhomogenous, gray to black Distinction of Nucleus and Annulus Clear Clear Unclear Lost Lost Disc Height Normal Normal Normal to decreased Normal to decreased Collapsed

Kinematic Analysis of Cervical Sagittal Alignment With Degeneration Miyazaki et al E873

Table 2. Comparison of Each Group in the Study Population

(Group) No. Sex (female/male) Age A: Kyphosis 19 13/6 46.0 13.6 B: Straight 29 14/15 41.0 12.0 C: Hypolordosis 38 24/14 42.6 11.4 D: Normal 63 35/28 43.2 9.3 E: Hyperlordosis 52 25/27 45.4 14.4

Statistical Analysis
The SPSS software (version 13; SPSS, Chicago, IL) was used, and the values are represented as mean standard deviation (SD). Student t test was used for statistical analysis. A signicance level of 0.05 was adopted.

motion decreased in participants with hyperlordotic alignments. Additionally, the grade of disc degeneration at the upper levels was lower in participants with hyperlordotic alignment when compared with participants with normal lordotic alignment. The Correlation Between the Sagittal Alignment and the Degree of Cervical Disc Degeneration The grades of disc degeneration in each group are shown in Figure 3. In all the groups, maximum degeneration was noted at the intervertebral disc at the C5C6 level followed by that at the C4 C5 level. At the C3C4 level, the grade of disc degeneration was higher in Group B than in Group D and was lower in Group E than in Group D. Further, at the C2C3 level, the grade of disc degeneration in Group E was significantly lower than that in Group D (P 0.05). Interestingly, the grade of disc degeneration at the C5C6 level in Group A was signicantly higher than that in Group D (P 0.05). Translational Motion of Each Cervical Unit Figure 4 presents the graphs of translational motion of each cervical unit. At the C4 C5 and C5C6 levels, the translational motion in Group E tended to be higher than that in Group D; however, the translational motion was lower in Group C and Group B than in Group D, whereas it was lower in Group B than in Group C. At the C2C3 and C3C4 levels, the translational motion in Group E tended to be lower than that in Group D. There were signicant differences between Group E and Group D at the C2C3 and C5C6 levels (P 0.05). At all the levels, the translational motion in Group C and Group B was lower than that

Results Comparison of Each Group in the Study Population The number, gender distribution, and age of the participants are shown in Table 2. There were no statistical differences among the groups. General Trends in Results When normal lordotic alignment progressed to hypolordotic alignment and straight alignment, all levels of the cervical spine tended to have decreased translational motion and angular variation. Although angular variation decreased at all levels, the percent contribution to total angular variation of the upper (C2C3, C3 C4) levels tended to increase. In contrast, the percent contribution to total angular variation of the middle (C4 C5, C5C6) and low (C6 C7) levels tended to decrease. Additionally, this change in alignment was associated with increased grades of disc degeneration at the upper levels. However, there were no signicant associations observed between this alignment shift and the grade of disc degeneration at the middle and low levels. When alignment shifted from normal lordosis to hyperlordosis, translational motion, angular variation, and the percent contribution to total angular variation at the middle levels increased. However, these changes in mobility had no signicant effects on disc degeneration. At the upper levels, translational

Figure 3. The Correlation between the sagittal alignment and the degree of cervical disc degeneration. At the C3C4 level, the grade of disc degeneration was higher in Group B than in Group D and was lower in Group E than in Group D. Further, at the C2C3 level, the grade of disc degeneration in Group E was signicantly lower than that in Group D (P 0.05). The grade of disc degeneration at the C5C6 level in Group A was signicantly higher than that in Group D (P 0.05).

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Figure 4. Translational motion of each cervical unit. There were signicant differences between Group E and Group D at the C2C3 and C5C6 levels and between Group A and Group D at the C2C3 level (P 0.05).

in Group D. In Group A, the translational motion at the C5C6 level was the lowest, whereas that at the C3C4, C4 C5, and C6 C7 levels was denitely higher. There were signicant differences between Group A and Group D at the C2C3 level (P 0.05). Angular Variation of Each Cervical Unit Figure 5 shows the graphs of angular variation of each cervical unit. At the C4 C5 and C5C6 levels, the angular variation tended to be higher in Group E than in Group D. However, at the same level, the angular variation was lower in Groups C and B than in Group D and it was lower in Group B than in Group C. There were signicant differences between Group E and Group D with regard to the angular variation at the C5C6 level and between Group B and Group D with regard to the variation at the C4 C5 level (P 0.05).

Contribution of Each Level to Total Angular Mobility The contribution of each level to the total angular mobility is shown in Figure 6. The contribution of the C4 C5 and C5C6 levels to the total angular mobility tended to be higher in Group E than in Group D. However, at the C4 C5, C5C6, and C6 C7 levels, the total angular mobility in Group C and Group B was lower than that in Group D, whereas it was lower in Group B than in Group C. There were signicant differences between Group E and Group D at the C5C6 level (P 0.05). The contribution of the C1C2, C2C3, and C3C4 levels to the total angular mobility tended to be higher in Group C and Group B than in Group D, whereas it tended to be higher in Group B than in Group C. There were signicant differences between Group B and Group D at the C2C3 level (P 0.05).

Figure 5. Angular variation of each cervical unit. There were signicant differences between Group E and Group D with regard to the angular variation at the C5C6 level and between Group B and Group D with regard to the variation at the C4 C5 level (P 0.05).

Kinematic Analysis of Cervical Sagittal Alignment With Degeneration Miyazaki et al E875

Figure 6. Contribution of each level to total angular mobility. There were signicant differences between Group E and Group D at the C5C6 level and between Group B and Group D at the C2C3 level (P 0.05).

Discussion The cervical spine withstands substantial compressive axial load, which is approximately thrice the weight of the head because of muscle coactivation forces functioning to balance the head in the neutral position.12 The compressive force increases during exion and extension and other routine movements. Cervical lordosis is considered to decrease the internal compressive load and is essential for appropriate spinal coupling motion.1315 A major portion of this axial load is sustained by the intervertebral discs.16 During physiologic aging, degenerative changes are noted in many discs at around middle age. The changes usually occur gradually, and some individuals experience neck symptoms because of cervical degenerative disorders. The degeneration affects the motion units and the overall kinematics of the cervical spine,1,2 and axial loading is negatively affected. This may lead to the loss of normal cervical lordosis and considerable acceleration of the degeneration process. There are a few reports on the correlation of alignment and the kinematics of the cervical spine. Takeshima et al investigated the association between sagittal cervical kinematics and changes in the static alignment on upright cervical lordosis by using conventional lateral radiographs; they concluded that alterations in the static alignment of the cervical curvature causes alterations in the dynamic kinematics of the cervical spine during the exion-extension motion.17 However, they did not comment on the relationship of degeneration on the changes in kinematics. In the present study, we observed that the translational motion and angular variation in Group E was greater than that in Group D at the C4 C5 and C5C6 levels, which was the apex of the lordosis. Further, the contribution of each of these levels to the total angular mobility in Group E tended to be higher than that in Group D. Moreover, at the C2C3 level, the translational motion in Group E was lower than that in Group D. At the C2C3 and C3C4

levels, and disc degeneration in Group E was lower than that in Group D. It was assumed that a shift from normal lordosis to hyperlordosis renders the segment corresponding to the tip of lordosis more mobile and that this segment plays a major role in the total mobility during exionextension motions; moreover, such an alteration in alignment accelerates degeneration of this segment rather than that of other parts. Furthermore, translational motion and angular variation tended to decrease when normal lordotic alignment changed to loss of lordosis or straight alignment at all levels, i.e., when the cervical spine became more rigid. Disc degeneration was greater in Group B than in Group D at the C2C3 and C3C4 levels, and the contribution of C1C2, C2C3, and C3C4 levels in Group C and Group B tended to be higher than that in Group D. In contrast, the contribution of the C4 C5, C5C6, and C6 C7 levels in Group C and Group B tended to be lower than that in Group D. A limitation of our study was that we could not evaluate kyphotic or sigmoid (local kyphosis) cervical spines in detail because the number of participants with these alignments was less. Interestingly, we observed that the grade of disc degeneration at the C5C6 level in Group A was signicantly greater than that in Group D; the translational motion at the C5C6 level was the lowest among all functional motion units; and the translational motion at the C3C4, C4 C5, and C6 C7 levels was denitely higher than that at the C5C6 level. It was obvious that the kinematics in Group A lost the physiologic principle. Based on these results, it was assumed that the functional motion unit at the C5C6 level became more rigid and ankylosed, and the adjacent or 2 adjacent functional motion units became more mobile. The correlation between the cervical normal sagittal alignment and clinical symptoms is controversial because small segmental kyphotic regions have been detected in

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asymptomatic subjects.3,18,19 However, the incidence of segmental kyphosis is reported to be more than 4 times greater in patients with neck pain than in asymptomatic subjects.3,19,20 Further, we have experienced that maintenance of cervical lordosis after surgery is very important for preventing the recurrence of symptoms.4 6,21,22 However, the concept that the loss of cervical lordosis accelerates degeneration and causes symptoms has not yet been elucidated. Katsuura et al reported that degeneration of adjacent cervical levels was signicantly associated with the loss of physiologic cervical lordosis in a retrospective study of patients who had undergone anterior cervical discectomy and fusion.23 The present study demonstrated that the changes in the sagittal alignment of the cervical spine affects the kinematics and the contribution of each segment to the total angular mobility. Consequently, it may cause changes in the segment bearing the major load for overall motion and accelerate its degeneration. As inferred from a clinical case series study,23 we should consider physiologic lordotic reconstruction for preventing degeneration and symptomatic deterioration while planning cervical surgeries such as anterior cervical discectomy and fusion or articial disc replacement. In conclusion, the present study demonstrated a correlation between disc degeneration and static sagittal alignment of the cervical spine. We analyzed the changes in the kinematics of the functional motion unit according to the different types of cervical sagittal alignments. Our results suggest that a change in the sagittal alignment of the cervical spine affects the kinematics and the progress of degeneration in the cervical spine. Nevertheless, we investigated these analyses retrospectively and not prospectively. Therefore, further prospective researches are required to elucidate the details of the natural history of cervical spine degeneration. Further studies are required to provide with appropriate treatments for cervical degenerative disease. Key Points The present study investigated the correlation between disc degeneration and static sagittal alignment of the cervical spine and the changes in the kinematics of the functional motion unit according to different types of sagittal alignment. The present study demonstrated that the changes in sagittal alignment of the cervical spine affects the kinematics and the contribution of each segment to the total angular mobility. Consequently, it may cause changes in the segment subjected to maximum load for overall motion and accelerate its degeneration.

From the results of the present study, cervical surgery such as cervical discectomy and fusion or articial disc replacement should attempt to restore lordosis to prevent degeneration and symptomatic deteriorations.

References
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