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Non-mobile Adjacent Level Cervical Spondylolisthesis Does Not Always Require Fusion in Patients Undergoing ACDF

Segar, Anand H. MBChB, DPhil(Oxon), FRACS; Divi, Srikanth N. MD; Tarazona, Daniel MD; Fried, Tristan BS; Sandhu, Hanna BS; Kaye, Ian D. MD; Kepler, Christopher K. MD, MBA; Kurd, Mark F. MD; Woods, Barrett I. MD; Hilibrand, Alan S. MD; Radcliff, Kristen E. MD; Rihn, Jeffrey A. MD; Anderson, D. Greg MD; Vaccaro, Alexander R. MD, PhD, MBA; Schroeder, Gregory D. MD

doi: 10.1097/BRS.0000000000003070
CERVICAL SPINE
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Study Design. Retrospective review of a prospectively maintained database.

Objective. Compare outcomes following anterior cervical decompression and fusion (ACDF) between patients with no adjacent level spondylolisthesis (NAS) and adjacent level spondylolisthesis (AS).

Summary of Background Data. There are no prior studies evaluating the effect of preoperative adjacent-level cervical spondylolisthesis on outcomes following anterior cervical discectomy and fusion (ACDF).

Methods. A retrospective review of consecutive patients who underwent ACDF for degenerative cervical disease was performed. Adjacent level spondylolisthesis was defined on radiographs as anterior displacement (> 1 mm) of the vertebra in relation to an adjacent “to be fused” level. Patients were categorized as either AS or NAS. Preoperative and 1-year postoperative outcomes including Short Form-12 Physical and Mental Component Scores, Neck Disability Index, Visual Analog Score for arm and neck pain, and rate of revision surgery were compared between the two groups. Radiographic changes were also analyzed for patients with AS.

Results. A total of 264 patients met the inclusion criteria. There were 53 patients (20.1%) with AS and 211 patients (79.9%) with NAS. Both groups improved significantly from baseline with respect to all patient outcomes and there were no significant differences between the two groups. After accounting for confounding variables, the presence of an AS was not a predictor of any postoperative outcome. Revision rates did not differ between the two groups.

Conclusion. Patients with an AS had similar postoperative clinical outcomes compared with NAS. Furthermore, the presence of an AS was not a predictor of poorer clinical outcomes. This is the first study to investigate the effect of AS in patients undergoing ACDF and suggests that an adjacent-level spondylolisthesis does not need to be included in a fusion construct if it is not part of the primary symptom generating pathology.

Level of Evidence: 3

The optimal management of degenerative cervical spondylolisthesis adjacent to other cervical pathology is unclear. In patients undergoing ACDF, adjacent-level spondylolisthesis had similar postoperative clinical outcomes compared to those without one. Our findings suggest that adjacent-level spondylolistheses do not need to be included in the fusion construct if they do not contribute to the neurologic symptoms.

Rothman Institute at Thomas Jefferson University, Philadelphia, PA.

Address correspondence and reprint requests to Srikanth N. Divi, MD, Rothman Institute, Thomas Jefferson University Hospital, 925 Chestnut Street, 5th Floor, Philadelphia, PA 19107; E-mail: srikanth.divi@gmail.com

Received 9 November, 2018

Revised 18 February, 2019

Accepted 25 March, 2019

The manuscript submitted does not contain information about medical device(s)/drug(s).

No funds were received in support of this work.

Relevant financial activities outside the submitted work: board membership, consultancy, grants, royalties, stocks, travel/accommodations/meeting expenses.

Spondylolisthesis, slippage of one vertebra in relation to another, is commonly seen in the lumbar spine. However, degenerative cervical spondylolisthesis (DCS) is less well studied. Radiographically, these degenerate slips are accompanied by loss of disc height, facet arthrosis, and sometimes instability.1 Clinically, some authors have reported cervical spondylolistheses to be associated with significant neck pain and myelopathy.2,3

Anterior cervical discectomy and fusion is a safe and reliable procedure to achieve neural decompression. However, spine surgeons are often faced with patients who present with compression of the neural elements at one level and an adjacent level spondylolisthesis without significant neural compression. Routine fusion of a questionably symptomatic adjacent level could lead to increased short and long-term complications associated with fusing multiple levels.4 However, not fusing a level with radiographic signs of instability and degeneration may lead to poorer clinical outcomes and higher reoperation rates.

Currently, there is a paucity of data examining the long-term outcomes of patients undergoing anterior cervical discectomy and fusion (ACDF) with and without a preoperative adjacent-level cervical spondylolisthesis. The aim of this current study is to elucidate any differences in healthcare-related quality of life outcomes (HRQOL) between these two groups before and after surgery.

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MATERIAL AND METHODS

Patient Population

After obtaining institutional review board approval, a retrospective analysis was performed including patients who underwent a primary ACDF for degenerative cervical disease. Patients were identified from a large institutional database utilizing International Classification, Ninth Revision, Clinical Modification (ICD-9-CM) codes 723.4 and 721.1, and Current Procedural Terminology (CPT) 22551, 22552. All procedures were performed by fellowship-trained spine surgeons at a single, high-volume orthopedic practice. Patients who underwent surgery for trauma, infection, tumor, or planned anterior and posterior procedures were excluded. In addition, only patients with at least 1-year follow-up were included. Medical records for each patient were reviewed to confirm inclusion and exclusion criteria were met. Age, sex, body mass index (BMI), American Society of Anesthesiology (ASA) classification, Charlson Comorbidity Index, number of levels fused, and revision surgeries were also obtained.

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Radiographic Analysis

All radiographic measurements were made using Sectra Workstation IDS7 18.2 (Sectra AB; Linköping, Sweden). Adjacent level spondylolisthesis was defined as anterior displacement (1 mm or greater) of one vertebra in relation to an adjacent “to be fused” level on preoperative lateral, flexion, and extension radiographs. Based on these preoperative radiographs and the levels that were ultimately fused, patients were categorized as no adjacent spondylolisthesis (NAS), and adjacent spondylolisthesis (AS).

The magnitude of slip of the spondylolisthesis was obtained on lateral neutral radiographs. In addition, the motion of the spondylolisthesis was calculated as the change on flexion and extension lateral radiographs. Preoperative and postoperative cervical lordosis and sagittal vertical axis (SVA) were recorded for patients with AS. Cervical lordosis was measured as the angle formed by the inferior endplate of C2 and the superior endplate of C7. SVA was measured as the horizontal distance between a C2 plumb line and the posterior-superior corner of C7.

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Clinical Outcomes

Prospectively recorded preoperative and minimum 1-year postoperative HRQOL outcomes were obtained for all patients. HRQOL outcomes included Short Form-12 Physical Component Score (PCS), Mental Component Score (MCS), Neck Disability Index (NDI), and Visual Analog Score for neck and arm pain. Rates of revision surgery were also compared.

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Statistical Analysis

Preoperative and postoperative radiographic data were analyzed with paired sample t test and presented as mean and standard deviation. Continuous variables were compared between the two groups at the preoperative and postoperative time-points using a general linear model (ANOVA repeated measures) controlling for age, sex, and BMI. Categorical variables were analyzed using Fisher exact test for nominal data and Kruskal–Wallis test for ordinal data and results were presented as percentages. Multiple linear regression was used to determine if AS was an independent predictor of postoperative PCS, MCS, or NDI. Multiple logistic regression was used to determine if AS was an independent predictor of residual neck or arm pain. Statistical significance was assumed at P < 0.05. All analyses were performed using Statistical Package for the Social Sciences (SPSS) version 24 (IBM Corporation, Armonk, NY).

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RESULTS

Of the total 264 patients included there were 53 patients (20.1%) with AS and 211 patients (79.9%) with NAS. The average age for the overall cohort was 53.1 years (SD = 11.1 yrs), with 53% females and a mean of 2.12 levels fused (SD = 0.83 levels). Patient baseline characteristics are presented by group in Table 1. There was a baseline difference in mean age between the AS and NAS groups (58.2 vs. 51.8 yrs, respectively; P < 0.001) and also a higher proportion of females in the AS group (67.9% vs. 49.8%, respectively; P = 0.018). Patients were followed up on average for 19.8 months (SD = 6.4 mo, range 12.0–46.6 mo).

TABLE 1

TABLE 1

BMI and smoking status were not significantly different among all groups. Patients with AS had a mean BMI of 28.1 (SD = 6.0) versus those with NAS had 29.9 (SD = 6.0). There was a slightly higher proportion of current smokers in the NAS group (18.0% vs. 9.4%); however, this difference did not reach statistical significance. The proportion of patients that were ASA classification 1, 2, or 3 were similar between the two groups (P = 0.365). There were no patients with an ASA classification of four or five in either group. On average, patients with AS had 2.5 levels fused (SD = 1.2 levels) compared with those with NAS with 1.9 levels fused (SD = 1.3), P = 0.010.

Preoperative and postoperative radiographic data for the AS group are presented in Table 2. On average, the AS group had a 2.7 mm slip on preoperative neutral radiographs which significantly reduced to 1.7 mm postoperatively (P < 0.001). On flexion-extension films, there was an average of 1.29 mm of motion preoperatively which also reduced significantly to 0.62 mm postoperatively (P = 0.001). There was no significant change in cervical lordosis after surgery, however the SVA increased from 29.07 to 32.50 mm (P = 0.001).

TABLE 2

TABLE 2

There was a significant improvement from baseline in all HRQOL outcomes within both groups (Table 3). Comparing between the two groups, there were no differences in either preoperative or postoperative HRQOL and pain score outcomes (Figures 1–3). Similarly, after accounting for confounding variables, such as age, sex, BMI, smoking status, ASA, and number of levels fused, the presence of an AS was not a predictor of postoperative SF-12 PCS and MCS, NDI, or residual neck and arm pain (Table 3).

TABLE 3

TABLE 3

Figure 1

Figure 1

Figure 2

Figure 2

Figure 3

Figure 3

Out of the total cohort, 22 (8.3%) underwent revision surgery for pseudarthrosis, adjacent segment disease, or seroma. There was no difference in revision rates between the two groups, with three patients in the AS group (5.66%) and 19 patients in the NAS group (9.00%), P = 0.431 (Table 1). There was also no statistically significant difference in the reason for revision between the two groups, P = 0.149 (Table 4).

TABLE 4

TABLE 4

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DISCUSSION

This study found that patients who had a degenerative spondylolisthesis adjacent to anterior cervical fusions showed similar improvement in pain, disability, and function compared with those with no adjacent spondylolisthesis. Furthermore, there was no progression of the spondylolisthesis and no adverse change in cervical lordosis. This is one of the largest studies investigating degenerative cervical spondylolisthesis and the only one to investigate the effect of adjacent degenerative cervical spondylolisthesis (DCS) upon the outcomes of anterior cervical discectomy and fusion.

Only a few authors have studied DCS. In a systematic review of all DCS studies, Jiang et al5 showed that patients can present with mixed symptoms of pain and neurological compression although these symptoms did not correlate with the degree of slip. They also found that DCS was more common at C3–4 and C4–5, a finding confirmed by Jun et al.6 Kopacz and Connolly7 found the prevalence of DCS in asymptomatic patients was 5.2%, however this assessment was made only on static images. Using dynamic magnetic resonance imaging, Suzuki et al8 found that 20% of symptomatic patients with neck or arm pain had a DCS. Jun et al6 compared DCS patient to controls and found that patients with a DCS an increased T1 slope (3.7o). Patients with a higher T1 slope require a larger cervical lordosis, however patients with DCS had a similar cervical lordosis as controls and as such it is postulated the DCS could be a result of cervical sagittal imbalance.6,9

Lee et al1 characterized DCS radiographically as intervertebral disc degeneration, uncovertebral spurring, and facet arthrosis with articular mass thinning. Pellengahr et al10 further found that these motion segments had flatter, less angled, facet joints which predispose to anterolisthesis. Asymmetric facet hypertrophy is also associated with DCS, a finding Chaput et al described as analogous to facet gapping in the lumbar spine.11 Etiologically, DCS has been classified by Dean et al into two groups.12 The adjacent type, which occurs next to a stiff spondylotic segment and is due to the altered biomechanics and the spondylotic type, which occurs at an index level and is due to disc degeneration with height loss and facet arthrosis. The adjacent type was also described by Deburge et al and Lee et al.1,2 Interestingly, we found that fusion of the caudal level did not lead to further “compensatory subluxation” of the cephalad spondylolisthesis suggesting that AS may be more stable than thought.

The biomechanical effect of an ACDF on adjacent levels has been well studied. In a cadaveric model, Eck et al13 found an up to a 73% increase in intradiscal pressure at adjacent levels, suggesting greater load. Changes in load sharing were also noted by Maiman et al14 who found a similar increase in adjacent level stress. Hence, it was hypothesized that an ACDF would lead to progression of an adjacent DCS and thus poorer clinical outcomes.

This in vitro data is supported by radiographic analyses showing greater adjacent segment degeneration (ASD) after an ACDF. In the landmark study, Hilibrand et al15 showed a 2.9% annual incidence of adjacent degeneration and 17% rate of revision surgery. Similarly, at an average of 8.5 years, Baba et al16 showed a significantly increased segmental range of motion at adjacent fusion levels. Furthermore, they found a 15% incidence of a new onset adjacent anterolisthesis and an 11% retrolisthesis and only one of these patients with a retrolisthesis, required fusion for the slip. This would suggest that although there are biomechanical changes at adjacent levels, these may be of limited clinical significance.

Prior to the current study, the correlation between an adjacent level DCS and clinical outcomes following an ACDF was limited; however, Kieser et al17 found an adjacent DCS had no effect on the rate of ASD above a cervical disc replacement and this result was irrespective of the alignment and ROM of the replacement. Furthermore, in the laminoplasty literature, Suzuki et al found 28% patients undergoing laminoplasty for myelopathy had a DCS. After controlling for confounders, the authors found that the presence of a slip did not have an effect on neurological outcome or pain (neck and arm) with both groups showing equivalent improvement. Furthermore, similar to our study the magnitude of the slip did not progress postoperatively.18 In comparable populations, Shigematsu and Kawakami both showed that instability did not influence the surgical results of double-door laminoplasty.19,20

The findings in this study showed no changes in slip progression or cervical lordosis for the AS group but overall cervical SVA changed significantly from 29.07 to 32.50 mm (P = 0.001). While increasing SVA is a known predictor of pain and disability, patients in this study still showed improvement in all outcomes.21,22 It is possible that the limited effect of adjacent DCS on the outcomes of ACDF, cervical disc replacement and laminoplasty is due to DCS being more stable than the lumbar counterpart. As such, a similar approach to both problems may be inappropriate.

This study has many limitations including the retrospective nature of the study that allows for all biases associated with a retrospective study. Aside from these inherent limitations, the main limitation of our study is the duration of follow-up, as the average follow-up in this study was 19.8 months. Because of this, it is possible that there is a difference that would be identified with longer follow-up. However, Hilibrand et al showed that symptomatic ASD was seen at a similar annual incidence over a 10-year period, so in spite of the limited follow-up, if the difference was significant, one would expect to identify it. In addition, a post hoc power analysis showed that this study is underpowered to detect differences in revision rate given that only six patients underwent revision in the NAS group and none in the AS group. There is also selection bias in the treatment patients received. The patients who had an AS were evaluated by a fellowship trained spine surgeon, who determined that this was not the cause of the symptoms. This should not be interpreted that NAS should be included in the fusion. For instance, the motion on flexion/extension radiographs in the AS group was only 1.29 mm. It is possible in patients with a mobile AS that these results would be different.

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CONCLUSION

In patients undergoing ACDF, those with a nonmobile, adjacent spondylolisthesis that was not included in the fusion construct had similar postoperative clinical outcomes compared with those without an adjacent level spondylolisthesis. This is the first study to investigate the effect of adjacent spondylolisthesis in patients undergoing ACDF and the results suggest that in the short term, a stable spondylolisthesis without neural compression does not have to be included in a fusion construct.

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References

1. Lee C, Woodring JH, Rogers LF, et al. The radiographic distinction of degenerative slippage (spondylolisthesis and retrolisthesis) from traumatic slippage of the cervical spine. Skeletal Radiol 1986; 15:439–443.
2. Deburge A, Mazda K, Guigui P. Unstable degenerative spondylolisthesis of the cervical spine. J Bone Joint Surg Br 1995; 77:122–125.
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4. Veeravagu A, Cole T, Jiang B, et al. Revision rates and complication incidence in single- and multilevel anterior cervical discectomy and fusion procedures: an administrative database study. Spine J 2014; 14:1125–1131.
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12. Dean CL, Gabriel JP, Cassinelli EH, et al. Degenerative spondylolisthesis of the cervical spine: analysis of 58 patients treated with anterior cervical decompression and fusion. Spine J 2009; 9:439–446.
13. Eck JC, Humphreys SC, Lim T-H, et al. Biomechanical study on the effect of cervical spine fusion on adjacent-level intradiscal pressure and segmental motion. Spine (Phila Pa 1976) 2002; 27:2431–2434.
14. Maiman DJ, Kumaresan S, Yoganandan N, et al. Biomechanical effect of anterior cervical spine fusion on adjacent segments. Biomed Mater Eng 1999; 9:27–38.
15. 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 1999; 81:519–528.
16. Baba H, Furusawa N, Imura S, et al. Late radiographic findings after anterior cervical fusion for spondylotic myeloradiculopathy. Spine (Phila Pa 1976) 1993; 18:2167–2173.
17. Kieser DC, Cawley DT, Roscop C, et al. Spondylolisthesis adjacent to a cervical disc arthroplasty does not increase the risk of adjacent level degeneration. Eur Spine J 2018; 54:1–7.
18. Suzuki A, Tamai K, Terai H, et al. Clinical outcome of cervical laminoplasty and postoperative radiological change for cervical myelopathy with degenerative spondylolisthesis. Spine (Phila Pa 1976) 2016; 41:1808–1812.
19. Shigematsu H, Ueda Y, Takeshima T, et al. Degenerative spondylolisthesis does not influence surgical results of laminoplasty in elderly cervical spondylotic myelopathy patients. Eur Spine J 2010; 19:720–725.
20. Kawakami M, Tamaki T, Ando M, et al. Preoperative instability does not influence the clinical outcome in patients with cervical spondylotic myelopathy treated with expansive laminoplasty. J Spinal Disord Tech 2002; 15:277–283.
21. Tang JA, Scheer JK, Smith JS, et al. The impact of standing regional cervical sagittal alignment on outcomes in posterior cervical fusion surgery. Neurosurgery 2012; 71:662–669.
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Keywords:

ACDF; adjacent level spondylolisthesis; anterior cervical decompression and fusion; cervical spondylolisthesis; clinical outcomes; degenerative cervical disease

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