Radiographic Changes in the Cervical Spine Following Anterior Arthrodesis: A Long-Term Analysis of 166 Patients

Rao, Raj D. MD; Gore, Donald R. MD; Tang, Shu-Jie MD; Rebholz, Brandon J. MD; Yoganandan, Narayan PhD; Wang, Mei PhD

Journal of Bone & Joint Surgery - American Volume:
doi: 10.2106/JBJS.15.01061
Scientific Articles
Abstract

Background: Adjacent segment degeneration frequently develops following anterior cervical discectomy and fusion. The objectives of the present study were to characterize the long-term evolution of degenerative radiographic changes at segments adjacent to anterior cervical fusion and to identify factors associated with the development of these changes, including the preoperative condition of the cervical spine and parameters related to arthrodeses.

Methods: One hundred and sixty-six patients who underwent anterior cervical discectomy and fusion for symptomatic cervical spondylosis or disc herniation were followed radiographically for a mean time of 12.7 years (range, 5 to 30 years). Radiographic changes representing degeneration at adjacent levels, including disc height loss, osteophyte formation, end-plate sclerosis, and facet arthrosis, along with changes in sagittal alignment of the fusion segment and cervical spine, were recorded preoperatively and at the time of the latest follow-up. Regression models were used to identify the parameters that affect these degenerative changes.

Results: More than 90% of patients had worsened anterior and posterior osteophytes at segments immediately adjacent to the fusion. Degenerative changes were significantly affected by the proximity of the level to the fusion and were inversely affected by the preoperative degenerative changes present at the segment (p < 0.0001). The time elapsed since the surgical procedure was a significant predictor of degenerative changes (p < 0.0001). However, the patient age, the number of levels fused, and the sagittal alignment of the fusion segment had no influence on the degenerative changes at adjacent segments.

Conclusions: Multiple factors likely contribute to adjacent segment degeneration following cervical arthrodesis. Although mechanical parameters associated with arthrodesis, such as length and alignment of the fusion, did not appear to play a role, the preoperative degenerative condition of the spine and inclusion of C5-C6 in the arthrodesis influenced the incidence of adjacent segment degeneration.

Level of Evidence: Prognostic Level III. See Instructions for Authors for a complete description of levels of evidence.

Author Information

1Department of Orthopaedic Surgery, George Washington University, Washington, DC

2Departments of Orthopaedic Surgery (D.R.G., S.-J.T., B.J.R., and M.W.) and Neurosurgery (N.Y.), Medical College of Wisconsin, Milwaukee, Wisconsin

E-mail address for M. Wang: meiwang@mcw.edu

Article Outline

Degenerative changes are common on radiographs of the cervical spine, in both symptomatic and asymptomatic adults1-4. In subjects with neck pain, Gore et al. found increases in every degenerative radiographic finding, in terms of both incidence and severity, over a 10 to 25-year period1. They did not find a correlation between progression of these radiographic findings and either the incidence or severity of neck pain in their patients. Other investigations of longitudinal and point prevalence of these degenerative radiographic features have attributed the progression to aging1,3,5-7 and to increased mobility present in the lower cervical motion segments3,5.

In patients with anterior cervical fusion, similar radiographic deterioration continues at motion segments adjacent to the fusion. These changes have been attributed to age-related progression of cervical spondylosis8-13, to increased stress at these segments resulting from loss of motion due to fusion14-16, and to a combination of these two etiologies17. Radiographic changes in the postoperative patient have been tenuously associated with development of recurrent symptoms18-20.

The evolution of radiographic changes in the cervical spine over the long term provides a measure of progression of degeneration. A study of 223 asymptomatic adults found natural progression of radiographic findings over a 10-year period in 84.8% (189) of these individuals, with significantly more frequent degenerative changes (with p values ranging from 0.001 to 0.05) in subjects ≥40 years of age4. Another long-term study showed a similar incidence of progression in several radiographic parameters in both symptomatic and asymptomatic age and sex-matched cohorts1. In an attempt to characterize the progression of degeneration in the cervical spine following a prior surgical procedure, in the present study, we conducted a long-term retrospective analysis of 166 patients with anterior cervical fusion. The goals were to characterize the evolution of degenerative radiographic changes at segments adjacent to the fusion and to determine whether these changes correlate with the preoperative condition of the cervical spine and factors related to the operation, such as fusion length, proximity to the fusion, and time elapsed since the arthrodesis.

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Materials and Methods

Patient Population

Between 1969 and 2000, 166 patients underwent anterior cervical discectomy and fusion by a single surgeon. There were 67 men and 99 women, with a mean age of 46.7 years (range, 25 to 74 years) at the time of the procedure. All patients had symptomatic cervical spondylosis or disc herniation that had failed nonoperative treatment. The selection of levels included was based on signs and symptoms and radiographs in all patients, on pantopaque myelography in some patients, and on discography and electromyography in selected patients.

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Operative Technique

All patients had noninstrumented anterior cervical discectomy and fusion. An anteromedial approach was used to remove disc and vertebral end-plate cartilage. Posterior osteophytes, if present, were not disturbed. Autologous corticocancellous bone graft from the ilium, tibia, or fibula was inserted in a manner similar to that described by Simmons and Bhalla21. In multilevel arthrodesis, a trough was cut into the interposed vertebral bodies to accommodate a single strut of bone graft, with contact between the graft and the cancellous bone of the intervening vertebral bodies.

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Radiographic Technique

A lateral radiograph obtained preoperatively and at varying intervals postoperatively, ranging from 5 to 30 years (mean, 12.7 years), was available for all patients (Fig. 1 and Fig. 2). Radiographs were obtained with the patient standing in a comfortable position looking straight ahead and with a tube-film distance of 103 cm. Preoperative and postoperative radiographs were scanned into a DICOM (Digital Imaging and Communications in Medicine) format. Digital images were analyzed by one orthopaedic surgeon using ImageJ (version 1.42; National Institutes of Health). Eighty-eight individual parameters were recorded on each radiograph made preoperatively and at the time of the latest follow-up. Measurements included sagittal alignments, disc heights, and scores for osteophyte formation around the disc, end-plate sclerosis, and facet arthrosis.

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Degenerative Grading

Anterior osteophytes, posterior osteophytes, and vertebral end-plate sclerosis were assessed at the superior and inferior corners separately using a 0-to-3 grading scale. Grading criteria for anterior osteophytes and posterior osteophytes were as follows: 0 indicated no osteophytes, 1 indicated a mild osteophyte (<10% of the anteroposterior diameter), 2 indicated a moderate osteophyte (10% to 25% of the anteroposterior diameter), and 3 indicated a severe osteophyte (>25% of the anteroposterior diameter). The grading criteria for vertebral end-plate sclerosis were as follows: 0 indicated no sclerosis, 1 indicated mild sclerosis, 2 indicated moderate sclerosis, and 3 indicated severe sclerosis with cystic changes. Facet joint arthrosis was assessed as follows: 0 indicated no sclerosis, 1 indicated mild sclerosis without loss of joint space, 2 indicated moderate sclerosis with loss of joint space, and 3 indicated severe sclerosis with osteophytes or facet fusion. An overall representation of degeneration at the motion segment was determined by the summation of these values, the summed degenerative score, which was scored on a 0-to-21 scale.

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Sagittal Alignment and Disc Heights

On each lateral radiograph, the sagittal alignment of the cervical spine was assessed as the angle between posterior tangent lines to the bodies of C2 and C7; the sagittal alignment of the fusion segment was assessed as the angle between posterior tangents of the most cephalad and the most caudad vertebrae involved in the fusion. Positive values indicate lordosis.

Anterior, intermediate, and posterior disc heights were measured at each cervical disc space. The effect of anterior or posterior osteophytes was mitigated by obtaining these measurements posterior to the anterior cortical margin of the vertebral bodies to take into account the anterior osteophytes and anterior to the posterior cortical margin of the vertebral bodies to take into account the posterior osteophytes. The mean of these three disc heights was normalized with respect to the anteroposterior diameter of the cephalad vertebral body (i.e., expressed as a percentage of the mean disc height) to minimize any effects of variations in image magnification.

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Measurement Reproducibility

In 20 randomly selected patients, degenerative assessments were conducted independently by two orthopaedic surgeons to evaluate interobserver reliability. In 10 randomly selected patients, assessments were conducted by the same surgeon on two separate occasions (10 days apart) to evaluate intraobserver reliability. The kappa score was calculated for the ordinal variables of degenerative grades, and the coefficient of variation and correlation coefficient were calculated from the continuous variables (disc heights and lordosis). A kappa score of ≥0.75 indicated excellent concordance, and a kappa score between 0.75 and 0.40 indicated good to fair concordance22. Coefficients of variation of <20% were considered acceptable, and those of <10% were considered excellent. Correlation coefficients (adjusted R2) that were >80% were considered acceptable.

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Statistical Analysis

Parameters of disc heights and degenerative scores at each disc level were coded to identify the disc location with reference to the fusion segment (1 level superior, 2 levels superior, 3 levels superior, and 1 level inferior). The changes in these scores from individuals’ preoperative to postoperative follow-up values and the incidence of degenerative progression at each adjacent level were calculated. The Wilcoxon signed rank test was performed to evaluate changes in the mean disc height (expressed as a percentage) and summed degenerative score and to compare differences among various adjacent levels. Significance was set at p < 0.05.

Preliminary analysis was performed to identify those covariates that likely contribute significantly to the changes in the primary degenerative scores. Covariates for the regression model included preoperative degenerative scores, age, sex, follow-up duration, number of levels fused, proximity to the fusion, and postoperative sagittal alignment of the fused segments. Regression models were built to study the effects of these variables on the summed degenerative score and the mean disc height. A random effects model was selected to account for multiple measurements at various levels within each patient.

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Results

Patient Population

Fifty-one patients had a 1-level fusion, 88 patients had a 2-level fusion, and 27 patients had a 3-level fusion. More than 87% of the fusion procedures involved the C5-C6 level, including 86 of the 88 2-level fusions, all 27 of the 3-level fusions, and 32 of the 51 1-level fusions.

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Progression of Degeneration

Interobserver and intraobserver reliability tests showed good to excellent results (Table I). The incidence of progression of anterior osteophytes was greatest at the two immediately adjacent levels (93% at 1 level inferior and 95% at 1 level superior) and decreased at the levels further away from fusion (79% at 2 levels superior and 61% at 3 levels superior) (Fig. 3). The incidences of posterior osteophyte and facet arthrosis progression were >91% at all assessed levels. The incidence of end-plate sclerosis was the lowest, from 67% at 1 level inferior to 20% at 3 levels superior. The overall degenerative changes at each motion segment (the summed degenerative score) are presented in Table II. The Wilcoxon signed rank test showed a significant increase in degeneration at all assessed levels (p < 0.0001), with 1 level superior and 1 level inferior to the fusions showing the greatest degenerative changes. Significant differences in the summed degenerative score were found between 1 level and the more distant levels (p ≤ 0.01) (Table III).

Regression analysis of the summed degenerative score revealed that level location, follow-up duration, preoperative degenerative score, and sex had significant effects on changes in the summed degenerative score (Table IV). Specifically, a longer duration since the surgical procedure was associated with greater degenerative changes at the time of follow-up (p < 0.0001), and the severity of the preoperative degenerative condition of the adjacent segments was inversely associated with the amount of degenerative progression seen at the time of follow-up at these levels (p < 0.0001). The further away the adjacent level was from the fusion segment, the smaller the changes in the summed degenerative score (p < 0.0001). Male patients had significantly greater degenerative changes than female patients (p < 0.0001). Neither the number of levels fused nor the fusion segment sagittal alignment had an effect on the adjacent-level degenerative score.

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Disc Heights

The mean disc height was significantly decreased at levels immediately adjacent to the fusion: by 18% at 1 level inferior (p = 0.008), by 11% at 1 level superior (p < 0.0001), and, to a lesser degree, at 2 levels superior at 7% (p = 0.0008) (Table V). The differences in the mean disc height reduction percentage between 1 level and the more distant levels were generally significant (p < 0.01) (Table VI).

The same covariates used in modeling ordinal summed degenerative scores were used to construct the model for the percentage of mean disc height change (Table VII). Results showed that the preoperative mean disc height percentage and proximity to the fusion were the only two factors that significantly influenced the mean disc height percentage change at the time of follow-up (p < 0.0001). The length of the fusion (p = 0.15) and the postoperative sagittal alignment of the fused segments (p = 0.56) had no significant impact on the mean disc height percentage change, and neither did follow-up duration (p = 0.60).

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Sagittal Alignments

The mean global lordosis decreased from 19.6° preoperatively to 13.6° at the time of follow-up (p < 0.001). A mean 8.1° of kyphosis developed at the fusion segments: 4.5° developed at 1 level away, 10.1° developed at 2 levels away, and 9.6° developed at 3 levels away. Classifying subjects into kyphotic and non-kyphotic groups based on postoperative fusion segment alignment, the mean global lordosis was 11.7° for the kyphotic group and 19.0° for the non-kyphotic group (p < 0.007).

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Discussion

Despite the conventional wisdom that radiographic changes in the cervical spine are generally asymptomatic, imaging findings can be associated with neck pain when studying patients over the longer term2,4. A 10-year study of 159 asymptomatic subjects showed that 15% (24 of 159 patients) developed neck pain at a mean onset of 4.9 years2. Subjects with initial degenerative findings at the C6-C7 level were 4 times more likely to develop pain than those without initial degenerative findings. In another longitudinal study of asymptomatic individuals, magnetic resonance imaging (MRI) scans were repeated over a 10-year period. Subjects who developed neck pain over this duration also developed more compression of the dura (12.4% compared with 5.8%; p = 0.015) and foraminal stenosis (25.0% compared with 8.4%; p = 0.04) on follow-up MRI scans4. Matsumoto et al.23 compared radiographic degeneration and neck pain between asymptomatic subjects and patients who had anterior cervical fusion. At the 10-year follow-up, the surgical group had more degenerative changes (posterior disc protrusion, disc narrowing and degeneration, foraminal stenosis) than asymptomatic subjects. Clinical symptoms at the time of follow-up were also higher in the surgical group, with more neck pain and numbness in the upper extremity. The present study carefully characterized the radiographic changes that occur in the cervical spine of subjects after arthrodesis, at a mean time of 12.7 years following the surgical procedure, and investigated factors that may contribute to these changes. We found a high incidence of radiographic degenerative progression at levels near previously fused segments. More than 90% of patients had worsening posterior osteophytes and facet arthrosis at all assessed adjacent levels and worsening anterior osteophytes at the immediately adjacent levels. This represents a higher incidence of degenerative progression than previously reported incidences over similar periods of time (70% and 65%) for non-surgical subjects1,4.

There has been debate over whether adjacent segment degeneration is a result of natural progression of spondylosis or whether the fused segments mechanically predispose the adjacent segments to faster deterioration9,14,15. In the present study, several findings from regression analysis support the theory that biomechanical effects play a role in the adjacent segment degeneration. First, the proximity of an adjacent level to the fused levels was a strong predictor for all categories of degenerative changes. The levels immediately adjacent to the fusion (more so at the inferior level) showed the most severe changes compared with levels further away from the fusion. Second, age was not a significant predictor for the progression of adjacent segment degeneration; instead, duration since the time of the surgical procedure was significantly correlated with the changes in the overall degenerative score. In a study of 181 patients who underwent anterior cervical discectomy and fusion, Goffin et al. also reported that, for 5 to 15.6 years following the surgical procedure, the increased degenerative scores were significantly correlated with the length of time after the surgical procedure but not with the patient age24. We found that a radiographically healthy disc adjacent to a contemplated fusion was not protection against adjacent segment degeneration. On the contrary, a strong inverse relationship was found between the preexisting degeneration at levels adjacent to the fusion and the severity of progression of degenerative changes at the time of follow-up. Matsumoto et al. reported similar findings in a 10-year follow-up MRI study of 64 patients who had undergone anterior cervical discectomy and fusion; in that study, the progression of degenerative change at the adjacent discs was much higher in patients without preexisting disc degeneration23. A comparable compensatory increase in motion was also seen at healthy discs adjacent to degenerative discs in human subjects25 and finite element models26. These findings suggest increased mechanical consequences at healthy discs adjacent to a fused segment.

In long-term studies of anterior cervical discectomy and fusion, some authors have reported a lower level of adjacent segment deterioration following multilevel cervical fusion27-29. Intuitively, a longer stiff segment should result in greater adjacent segment degeneration, and, given the absence of findings of increased severity27 or incidence28,29, those authors proposed that adjacent segment degeneration is less likely due to mechanical effects of the fusion and more likely a consequence of aging. The data in the current study also showed that the severity of adjacent segment degenerative changes did not increase with the number of levels fused. More specifically, patients who had C5-C6 included in the fusion (87% [145 of 166 patients]) had fewer degenerative changes than the group in whom C5-C6 was adjacent to the fusion (13% [21 of 166 patients]). The mean degenerative score change for anterior osteophytes was 1.56 in the C5-C6 included group compared with 1.88 in the C5-C6 adjacent group (p < 0.003); for end-plate sclerosis, 0.55 in the included group compared with 0.61 in the adjacent group (p < 0.02); and for posterior osteophytes, 1.78 in the included group compared with 1.93 in the adjacent group (p < 0.066). A subanalysis of patients with single-level fusion (n = 51) revealed a similar trend, with patients undergoing C5-C6 arthrodesis (n = 32) showing significantly fewer degenerative changes at adjacent levels than when C5-C6 was one of the adjacent segments. The mean degenerative score changes for anterior osteophytes was 1.36 for the included group compared with 2.00 for the adjacent group (p < 0.0001); for posterior osteophytes, 1.62 for the included group compared with 1.93 for the adjacent group (p < 0.004); and for facet arthrosis, 1.85 for the included group compared with 2.13 for the adjacent group (p < 0.03). We propose that data from multilevel fusion need to be carefully weighed, because most subjects with multilevel cervical fusion likely include the C5-C6 level. The inclusion of C5-C6, a level that is inherently predisposed to greater degeneration within the fusion segment, potentially skews the assessment of adjacent segment effects. A similar scenario may exist at the C6-C7 level, but the small sample size at that level did not allow for adequate analysis.

Prior investigations have shown mixed findings on whether degenerative changes in the cervical spine are predisposed to by sagittal alignment of the preoperative cervical spine or by kyphosis that frequently results in the year following the surgical procedure as settling occurs through the graft-vertebra interface17,18,30-32. Okada et al.30 studied MRI-based degenerative changes over a 10-year period in two groups of asymptomatic subjects: lordotic and non-lordotic. The non-lordotic group had a higher odds ratio of posterior disc protrusion (p = 0.033) than the lordotic group. Using a similar MRI grading system, Lundine et al.17 recorded degenerative findings in 106 symptomatic patients prior to the surgical procedure, and showed no correlation between cervical spine alignment and degeneration. In patients who had undergone arthrodesis, Katsuura et al.32 found a higher incidence of lordotic alignment of the cervical spine in patients who did not have adjacent level degeneration (86% [18 of 21 patients] compared with 43% [9 of 21 patients]; p = 0.0148), whereas Goffin et al.24, with a mean 8.3-year follow-up in 180 patients, found no correlation between the increase in the degenerative scores and the alignment of the fused segment (Spearman rs = 0.002; p = 0.983). Regression analysis from the present study demonstrated that, over the long term, sagittal alignment of both the global cervical spine and the fused segments did not affect the severity of adjacent segment degeneration.

The present study has several strengths. The incidence and severity of multiple radiographically relevant degenerative changes were carefully analyzed in a large group of subjects followed over the long term. Analysis of severity changes using regression models facilitated investigation of multiple potential covariates that may play a role in predisposing to degenerative changes at segments adjacent to a fusion. Labeling the location of adjacent segments with reference to their proximity to the fusion segment enabled the analysis to be conducted on the collective data of fusion procedures at different spinal level(s) to maximize the statistical power.

However, the retrospective nature of the study and the nonconsecutive inclusion of cohort cases were some inherent limitations. The radiographs were obtained for routine postoperative clinical evaluation, in the days before digital imaging. As such, several radiographs were suboptimal studies, in that not all levels, especially the inferior adjacent level, could be adequately assessed. This resulted in some variation in the number of disc levels available for evaluation. The absence of information on subject pain levels precluded us from drawing conclusions on clinical implications of the degenerative findings or sagittal alignment of the cervical spine. The absence of repeat surgical procedures in this subset of patients suggests that clinical manifestations were not substantial over the follow-up period.

In summary, we find that adjacent segment degeneration following cervical arthrodesis is likely a multifactorial process. The progression of these degenerative changes was significantly associated with proximity to the fusion and the time elapsed since the surgical procedure and was inversely associated with the preoperative degenerative condition of the disc. The C5-C6 level is most prone to degeneration and is also the most likely to show adjacent segment degeneration when not included in a fusion. Several other factors, including patient age, number of fusion levels, and lordosis of the fused segment, had no significant influence on the severity of degenerative progression at levels adjacent to prior fusion.

Investigation performed at the Department of Orthopaedic Surgery, Medical College of Wisconsin, Milwaukee, Wisconsin

A commentary by Ferhan A. Asghar, MD, is linked to the online version of this article at jbjs.org.

Disclosure: This study received no external funding. The Disclosure of Potential Conflicts of Interest forms are provided with the online version of the article.

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