Accelerated spondylotic changes adjacent to the fused segment following central cervical corpectomy: magnetic resonance imaging study evidence

See the Editorial and the Response in this issue, p 1. J Neurosurg (Spine 1) 100:2 6, 2004 Accelerated spondylotic changes adjacent to the fused segment following central cervical corpectomy: magnetic resonance imaging study evidence VAIJAYANTEE KULKARNI, M.CH. (NEURO), VEDANTAM RAJSHEKHAR, M.CH. (NEURO), AND LAKSHMINARAYAN RAGHURAM, D.N.B. (RADIOLOGY) Departments of Neurological Sciences and Radiodiagnosis, Christian Medical College Hospital, Vellore, India Object. The authors studied whether cervical spine motion segments adjacent to a fused segment exhibit accelerated degenerative changes on short-term follow-up magnetic resonance (MR) imaging. Methods. Preoperative and short-term follow-up (mean duration 17.5 months, range 10 48 months) cervical MR images obtained in 44 patients who had undergone one- or two-level corpectomy for cervical spondylotic myelopathy were evaluated qualitatively and quantitatively. The motion segment adjacent to the fused segment and a segment remote from the fused segment were evaluated for indentation of the thecal sac,, and sagittal functional diameter of the spinal canal on midsagittal T 2 -weighted MR images. Thecal sac indentations were classifed as mild, moderate, and severe. New indentations of the thecal sac of varying severity (mild in 17 patients [38.6%], moderate in 10 [22.7%], and severe in six [13.6%]) had developed at the adjacent segments in 33 (75%) of 44 patients. The degenerative changes were seen at the superior level in 11 patients, inferior level in 10 patients, and at both levels in 12 patients and resulted from both anterior and posterior element degeneration in the majority (23 [69.6%]) of patients. The remote segments showed mild thecal sac indentations in seven patients and moderate indentations in two patients (nine [20.5%] of 44). Compared with the changes at the remote segment, the was significantly decreased at the superior adjacent segment by 0.9 mm (p = 0.007). No patient sustained a new neurological deficit due to adjacent-segment changes. Conclusions. On short-term follow-up MR imaging, levels adjacent to the fused segment exhibited more pronounced degenerative changes (compared with remote levels) in 75% of patients who had undergone one- or two-level central corpectomy. KEY WORDS adjacent-segment disease corpectomy spondylosis cervical spine C Abbreviations used in this paper: ACF = anterior cervical fusion; CSM = cervical spondylotic myelopathy; MR = magnetic resonance imaging; PLL = posterior longitudinal ligament; VB = vertebral body. 2 ENTRAL corpectomy has been shown to be an effective method for the treatment of CSM. Fusion of the decompressed segments involving a bone graft with or without a cervical plate is an integral part of the surgical strategy. Fusion of cervical segments following decompression has been postulated to produce an acceleration of degenerative changes at adjacent segments. 4 The authors of previous studies involving long-term follow up in cervical fusion treated patients have documented evidence of adjacent-segment degeneration causing symptomatic radiculopathy and myelopathy; 2,3,5,12 however, the adjacent-segment disease was not conclusively proven to be the result of the fusion. It is possible that the spondylotic adjacent-segment changes in these patients were not hastened by the fusion but occurred at the natural rate. 12 Indeed, Emery, et al., 5 commented that it was impossible to determine whether symptomatic adjacent-segment changes developing in their patients after cervical corpectomy were due to normal progression of degenerative changes or an acceleration of changes induced by the fused segment. We performed this short-term follow-up study to address this concern in part because degenerative changes occurring at the adjacent segment soon after the surgery are likely to be due to an accelerated degenerative rather than a natural process. Clinical Material and Methods All patients who had undergone central corpectomy for CSM and in whom preoperative and early follow-up MR images were available were included in the study. Postoperative follow-up MR images were routinely acquired in patients presenting for follow-up examination to our hospital. Clinical records were reviewed and the details regarding preoperative and follow-up Nurick grade as well as levels of central corpectomy were noted. The MR images were obtained from the radiology departmental archives. Magnetic resonance images were evaluated to determine and functional canal diameter at the superior

Postcorpectomy adjacent-segment spondylosis and inferior levels adjacent to the fused segment. One level remote from the fused segment (superior or inferior) was used as a control segment. The and were measured in millimeters by assessing comparable preoperative and follow-up midsagittal T 2 -weighted MR images of the cervical spine. The anteroposterior functional canal diameter was measured as the minimum sagittal diameter at the level of the disc space. The presence and severity of indentation of anterior and posterior subarachnoid spaces at these levels were noted. The extent of disc and ligament encroachment on the spinal canal were graded as mild (indentation of the subarachnoid space not reaching the cord), moderate (indentation reaching the cord but not deforming it), and severe (indentation of the cord causing deformation). The mean change in and at the adjacent superior or inferior level and one remote level were calculated. The mean change at the adjacent level was compared with that at the remote level, which served as the intrinsic control. The sagittal alignment of the spine was studied on neutral lateral cervical radiographs acquired before surgery and at the follow-up visit. A line was drawn to join the posterior end of the inferior endplate of the C-2 VB and a similar point on the C-7 VB. If the intervening VBs were all ventral to this line, the spine was categorized as lordotic; if any VBs touched the line, then the spine was considered to be straight, and in a kyphotic spine one or more VBs would intersect the line. Forty-four patients (43 men and one woman) were included in the study. The mean age at presentation was 46 years (range 31 66 years). Seventeen patients presented with Nurick Grade 3, 13 with Grade 2, nine with Grade 4, three with Grade 5, and two with Grade 1 function. Thirty-three patients underwent two-level corpectomy (C5 6 in 21, C4 5 in nine, C6 7 in one, and skip corpectomies of C-4 and C-6 in two). Eleven patients underwent a single-level corpectomy (C-5 and C-6 in five each and C-4 in one). The adjacent and remote segments studied are shown in Table 1. The C3 4 and C7 T1 segments were the most common superior (59%) and inferior (65.9%) levels, respectively. The C2 3 level was the most commonly (61.4%) studied remote segment. The Student t-test was used to compare means, and the chi-square and Fisher exact tests were used to compare proportions. A probability value of 0.05 or less was considered to be significant. Results The mean follow-up duration was 17.5 months (range 10 48 months). Symptoms in all but one patient improved following surgery. No clinical deterioration was seen in any patient. Nurick grades in 41 patients improved from 0 to 2 by final follow up. Of the two patients with preoperative Nurick Grade 4, status in one improved to Grade 3 and in the other it remained Grade 4. One patient in whom status was Grade 5 preoperatively experienced clinical improvement to Grade 4. Qualitative Observations On follow-up MR images, adjacent-segment changes were noted both ventrally and dorsally (Table 2). There TABLE 1 Distribution of adjacent and remote segments in 44 patients with CSM Level No. of Cases superior adjacent segment C2 3 12 C3 4 26 C4 5 6 inferior adjacent segment C5 6 1 C6 7 13 C7 T1 29 T1 2 1 remote segment C2 3 27 C3 4 5 C6 7 1 C7 T1 9 T1 2 2 were varying degrees of indentation of the ventral subarachnoid space caused by the posterior anulus of the disc and the PLL. The dorsal subarachnoid space indentation was produced by hypertrophy and buckling of the ligamentum flavum. Overall, indentations of the ventral or dorsal subarachnoid space were seen in 33 patients (75%). The indentations were classified as mild in 17 patients (38.6%), moderate in 10 (22.7%), and severe in six (13.6%). The degenerative changes were visualized at the superior segment alone in 11, inferior segment alone in 10, and in both segments in 12 patients. Anterior canal changes were seen in four, posterior canal changes in six, and anterior and posterior canal changes in 23 patients. The changes were therefore almost uniformly distributed both cranially and caudally, and anteriorly and posteriorly (Figs. 1 and 2), although changes in the posterior elements of the superior segment were seen in more patients (20 of 44) than in the other regions. No significant changes in signal intensity of the adjacent intervertebral discs were seen, however. The posterior indentations observed at the level of the compression on the preoperative images were absent on follow-up images in nearly all patients (Fig. 1). Evaluation of the remote levels revealed mild degenerative changes with mild indentation of the subarachnoid spaces in seven patients and moderate indentations in two patients (total nine [20.5%]) (Fig. 1). Changes at the remote segment were seen in a proportionately smaller number of patients compared with those in whom indentations of the thecal sac developed at the adjacent segment (20.5 and 75%, respectively [p 0.001]). In all but one of the nine patients in whom remote segments exhibited degenerative changes, the adjacent segments also showed thecal sac indentations. In 35 patients the remote segments remained unchanged from preoperative status. Quantitative Observations The changes in the and the were calculated for the remote segment (Table 3) and then compared with those at the adjacent segment (Table 4). There was a significant decrease in at the superior level (mean 0.93 mm [p = 0.006]) and at the inferior level (mean 0.81 mm [p = 0.07]) (Table 4). The slight increase 3

V. Kulkarni, V. Rajshekhar, and L. Raghuram TABLE 2 Adjacent and remote segment changes demonstrated on follow-up MR images: qualitative analysis* Level (no. of cases) Superior Inferior Remote ant subarachnoid space mild indentation 12 11 2 moderate indentation 4 3 0 severe indentation 3 0 0 pst subarachnoid space mild indentation 10 7 5 moderate indentation 7 5 2 severe indentation 3 2 0 cord changes 1 0 0 * ant = anterior; pst = posterior. in at the superior adjacent level was not significant. When data were analyzed for two-level corpectomy alone (33 cases) (Table 4), the mean decrease in canal size at the superior level was 0.96 mm and was highly significant. Decreases in at the inferior level and increases in were not significant. When data for the 11 single-level corpectomies were analyzed (Table 4), the decrease in at both adjacent levels was significant, especially at the inferior level (p = 0.006). There was also statistically significant minimal increase in at the lower level. Sagittal Alignment FIG. 1. Preoperative (left) and 39-month follow-up (right) T 2 - weighted sagittal MR images of the cervical spine obtained in a 42- year-old man who underwent a C5 6 corpectomy. There is evidence of moderate anterior and posterior canal compromise at the superior adjacent segment (C3 4). No new degenerative changes are apparent at the inferior adjacent segment (C7 T1). Note the mild posterior indentation of the thecal sac at the C2 3 level. Postoperatively the posterior canal compression at the level of the corpectomy has resolved. FIG. 2. Preoperative (left) and 22-month follow-up (right) T 2 -weighted sagittal MR images of the cervical spine obtained in a 49-year-old man who underwent a C-5 corpectomy. The followup MR image reveals moderate canal indentation posteriorly and mild canal indentation anteriorly at the inferior adjacent segment (C6 7). No new degenerative changes are present at the superior adjacent segment and the remote segment (C2 3). The sagittal alignment of the cervical spine underwent a kyphotic alteration (defined as a lordotic spine becoming straight or kyphotic or a straight spine becoming kyphotic) in 17 patients, whereas in 27 patients the preoperative spinal alignment was maintained (24 patients) or was improved (three patients) (Table 5). The incidence of adjacent-segment spondylotic changes were compared in these two groups (with and without a kyphotic change). In 15 (88%) of 17 patients with kyphotic change and 18 (67%) of 27 without kyphotic change, adjacent-segment degenerative changes were present (p = 0.1, Fisher exact test). Discussion Plain Radiographic Studies Although the authors of most studies on plain radiography have shown progression of degenerative arthritis at adjacent levels following ACF, 1,5,12 some have reported contrary results. 9 The authors of studies on dynamic radiograpy have demonstrated increased motion above and below the level of cervical fusion. 1,6 In experimental studies on stresses on the adjacent segments and the motion at the adjacent segments following cervical fusion, investigators have also formed differing conclusions based on their findings. Maiman, et al., 13 reported that increased internal stress responses in the adjacent motion segments reflects the changes in the load sharing after ACF. Fuller, et al., 7 however, found a uniform increase in motion across the remaining open segments with no disproportionate motion-related increase in the segments adjacent to the fusion. Neuroimaging of Adjacent-Segment Disease The commonly observed MR imaging findings in patients with symptoms of adjacent-segment disease are intervertebral disc herniations and spinal malalignment in both superior and inferior directions, hypertrophy of yellow ligaments, and ossification of the PLL. 10 The rate of 4

Postcorpectomy adjacent-segment spondylosis TABLE 3 Quantitative changes occurring at the remote segment* TABLE 5 Sagittal alignment of the cervical spine Variable (no. of cases) Mean Change SD (mm) Follow-Up Position 1- or 2-level corpectomy (44) 0.07 0.96 0.27 1.12 1-level corpectomy (11) 0.25 0.87 0.48 1.06 2-level corpectomy (33) 0.49 1.01 0.35 1.06 * SD = standard deviation. symptomatic adjacent-segment disease following ACF ranges from 8 to 25%. 5,8,11 Hilibrand, et al., 11 reported that the incidence of adjacent-segment disease was lower in multilevel fusion compared with single-level fusion. This rate is similar to ours; in patients who had undergone single-level corpectomy, there were more significant adjacent-segment changes than those who had undergone twolevel corpectomy. Several reasons may account for this finding. A C5 6 corpectomy was the most common twolevel corpectomy performed in our series. The lower adjacent level (C7 T1), being inherently less prone to degeneration, did not show any degenerative changes. On the other hand, in patients who underwent single-level corpectomy, C6 7 was the most common adjacent segment, because it is prone to degeneration, and this segment showed a highly significant decrease in. Even in asymptomatic patients who have undergone ACF, early follow-up MR imaging studies have revealed an increased incidence of adjacent-segment disc herniations in a significant proportion of patients. 14 16 TABLE 4 Quantitative changes demonstrated at the adjacent segment* Variable (no. of cases) Mean Change SD (mm) p Value 1- or 2-level corpectomy (44) superior level 0.7 0.67 NS inferior level 0.23 0.92 NS superior level 0.93 0.95 0.006 inferior level 0.81 1.21 0.07 1-level corpectomy (11) superior level 0.02 0.5 0.13 inferior level 0.32 0.52 0.011 superior level 0.82 1.05 0.04 inferior level 0.95 0.9 0.006 2-level corpectomy (33) superior level 0.08 1.02 0.23 inferior level 0.2 0.71 0.86 superior level 0.97 0.93 0.05 inferior level 0.76 1.3 0.59 * NS = not significant. A negative value indicates a decrease in dimension, and a positive value reflects an increase in dimension. A statistically significant difference was found. Preop Position Lordotic Straight Kyphotic lordotic 14 15 1 straight 3 9 1 kyphotic 0 0 1 Present Findings The following are unique features in our study of patients without symptoms of adjacent-segment disease: 1) evaluation of MR imaging changes in a short-term followup period, which partially avoids the confounding effect of the natural degenerative changes; 2) use of remote control intervertebral segments; and 3) quantitative assessment of the degenerative changes determined by measuring the and spinal canal dimension. Previously investigators used age- and sex-matched controls to study adjacent-segment degenerative changes in patients who had undergone ACF. Degenerative changes in the cervical spine, however, are highly variable and dependent on several factors other than age and sex. Therefore, the degenerative changes in cervical spines of age- and sex-matched individuals may not be an ideal control for comparison. We chose to use internal control segments remote from the fusion, but even this approach is partially flawed because some of these control segments are inherently stable and do not normally show degenerative changes. Thus, it is almost impossible to distinguish categorically natural degenerative processes from those provoked by the fusion of the adjacent segment. 5 Some observations in our study, however, indicate that fusion does accelerate spondylotic changes at the adjacent segments. The C3 4 level was affected only when it was adjacent to the fused segment, not when it was remote. Subarachnoid space indentation was significant even at the C2 3 level (a level seldom affected in spondylotic disease) when it was the adjacent segment. Causes of Accelerated Degenerative Changes It is speculated that because cervical spinal fusion provokes degenerative arthritis due to functional overloading of the spaces adjacent to the fusion, it increases the biomechanical stresses at these levels. 4,13 Interestingly, no significant change was noted in disc height even at levels at which canal stenosis developed. This finding likely indicates that the compressive elements causing decrease in are the PLL and the ligamentum flavum, at least in the early stages of the disease. The hypertrophy of these ligaments may be a consequence of increase in sagittal motion at the adjacent segments resulting from the lack of motion at the fused segment, rather than an increase in axial loading strain that might be expected to alter the. Another possible cause of the adjacent-segment spondylotic changes might be the kyphotic alterations that occur in the cervical spine after ACF. The kyphotic sagittal alignment may provoke acceleration of the degenerative processes, especially adjacent to the fused segments, 5

V. Kulkarni, V. Rajshekhar, and L. Raghuram because the kyphotic tendency is maximal at the fused segment. Although our analysis did not reveal a statistically significant difference in the incidence of adjacentsegment disease in patients with and without kyphotic cervical changes, there was a trend toward a higher incidence in those with kyphotic changes postoperatively. Conclusions In the present study we found that central corpectomy for CSM leads to a statistically significant decrease in canal size at adjacent levels. New degenerative changes were demonstrated at the adjacent segments on follow-up MR images in 75% of the patients studied, and in some of these cases the changes were recorded in normally stable segments such as C2 3. References 1. Baba H, Furusawa N, Imura S, et al: Late radiographic findings after anterior cervical fusion for spondylotic myeloradiculopathy. Spine 18:2167 2173, 1993 2. Bohlman HH, Emery SE, Goodfellow DB, et al: Robinson anterior cervical discectomy and arthrodesis for cervical radiculopathy. Long term follow-up of one hundred and twenty-two patients. J Bone Joint Surg Am 75:1298 1307, 1993 3. Braunstein EM, Hunter LY, Bailey RW: Long term radiographic changes following anterior cervical fusion. Clin Radiol 31: 201 203, 1980 4. Cherubino P, Benazzo F, Borromeo U, et al: Degenerative arthritis of the adjacent spinal joints following anterior cervical spinal fusions: clinicoradiologic and statistical correlations. Ital J Orthop Traumatol 16:533 543, 1990 5. Emery SE, Bohlman HH, Bolesta MJ, et al: Anterior cervical decompression and arthrodesis for the treatment of cervical spondylotic myelopathy. Two to seventeen-year follow-up. J Bone Joint Surg Am 80:941 951, 1998 6. Fielding JW: Normal and selected abnormal motion of the cervical spine from the second cervical vertebra to the seventh cervical vertebra based on cineroentgenography. J Bone Joint Surg Am 46:1779 1781, 1964 7. Fuller DA, Kirkpatrick JS, Emery SE, et al: A kinematic study of the cervical spine before and after segmental arthrodesis. Spine 23:1649 1656, 1998 8. Garvey TA, Eismont FJ, Roberti LJ: Anterior decompression, structural bone grafting and Caspar plate stabilization for unstable cervical spine fractures and/or dislocations. Spine 17: S431 S435, 1992 9. Gore DR, Gardner GM, Sepic SB, et al: Roentgenographic findings following anterior cervical fusion. Skeletal Radiol 15: 556 559, 1986 10. Goto S, Mochizuki M, Watanabe T, et al: Long-term follow-up study of anterior surgery for cervical spondylotic myelopathy with special reference to the magnetic resonance imaging findings in 52 cases. Clin Orthop 291:142 153, 1993 11. Hilibrand AS, Carlson GD, Palumbo MA, et al: Radiculopathy and myelopathy at segments adjacent to the site of a previous anterior cervical arthrodesis. J Bone Joint Surg Am 81: 519 528, 1999 12. Hunter LY, Braunstein EM, Bailey RW: Radiographic changes following anterior cervical fusion. Spine 5:399 401, 1980 13. Maiman DJ, Kumaresan S, Yoganandan N, et al: Biomechanical effect of anterior cervical spine fusion on adjacent-segments. Biomed Mater Eng 9:27 38, 1999 14. Matsunaga S, Kabayama S, Yamamoto T, et al: Strain on intervertebral discs after anterior cervical decompression and fusion. Spine 24:670 675, 1999 15. Ross JS, Masaryk TJ, Modic MT: Postoperative cervical spine: MR assessment. J Comput Assist Tomogr 11:955 962, 1987 16. Wu W, Thuomas KA, Hedlund R, et al: Degenerative changes following anterior cervical discectomy and fusion evaluated by fast spin-echo MR imaging. Acta Radiol 37:614 617, 1996 Manuscript received February 25, 2003. Accepted in final form August 5, 2003. This study was funded by a Fluid Research Grant from the Christian Medical College, Vellore, India Address reprint requests to: Vedantam Rajshekhar, M.Ch.(Neuro), Department of Neurological Sciences, Christian Medical College Hospital, Vellore 632 004, India. email: rajshekhar@cmcvellore.ac.in. 6