Segmental Motion of the Cervical Spine After Total Disc Replacement Using ActivC Versus Discectomy and Fusion Using Stand-alone Cage

Original Article

Segmental Motion of the Cervical Spine After Total Disc Replacement Using ActivC Versus Discectomy and Fusion Using Stand-alone Cage Bum-Joon Kim, Se-Hoon Kim, Seung-Hwan Lee, Sung-Kon Ha, Sang-Dae Kim, Dong-Jun Lim

OBJECTIVE: Anterior cervical discectomy and fusion (ACDF) has been a widely accepted procedure for the treatment of cervical disc diseases. However, due to several reports regarding postfusion exacerbation of adjacent segments, a motion-preserving prosthesis was developed. In the present retrospective analysis, total disc replacement (TDR) using ActivC (Aesculap AG, Tuttlingen, Germany) was compared with ACDF using a stand-alone cage.

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METHODS: Among patients diagnosed with cervical disc diseases, those who received either ACDF or TDR at a single level between C3 and C7 from January 2010 to December 2015 were reviewed. Clinical outcomes were assessed using the visual analogue scale for arm and neck pain and the neck disability index. Clinical scales, lateral neutral, and flexione extension radiographs were taken for all patients preoperatively and 2 months, 6 months, 1 year, and 2 years postoperatively. Global lordosis, C2eC7 Sagittal vertical axis, and T1 slope were measured on lateral neutral radiographs. The segmental range of motion (ROM) of the operated level, cranial adjacent level, and caudal adjacent level were defined as the difference between Cobb angles on flexione extension lateral radiographs.

outcome was excellent in both ACDF and TDR groups and was maintained until the 2-year follow-up. CONCLUSIONS: In the present study, TDR using ActivC showed successful motion preservation at the operated level and equivalent results were observed with ACDF based on clinical and radiologic results.

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RESULTS: A total of 53 patients (mean age 48.5 years) were reviewed. Thirty patients were treated with ACDF and the remaining 23 patients received TDR. At the 2-year follow-up, the segmental ROM of operated level was significantly preserved in the TDR group compared with the ACDF group (P [ 0.007). Conversely, no significant differences in the ROM at the adjacent segments were observed between the TDR and ACDF groups (P > 0.05). The clinical

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Key words Arthroplasty - Cervical vertebrae - Diskectomy - Intervertebral disc degeneration - Range of motion - Spinal fusion - Total disc replacement -

Abbreviations and Acronyms ACDF: Anterior cervical discectomy and fusion HO: Heterotopic ossification ROM: Range of motion SVA: Sagittal vertical axis

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INTRODUCTION

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nterior cervical fusion has been widely accepted as the gold standard procedure in cervical degenerative disc diseases. However, Goffin et al.1 and Hilibrand et al.2 reported degenerative changes in the adjacent segments of the fusion level on long-term follow-up. Biomechanical studies have shown fusion to increase intradiscal pressure and motion of adjacent segments,3,4 and in some reports, fusion surgery was suggested to actually increase segmental range of motion (ROM) at adjacent levels.5,6 In 1989, the ball-and-socket type artificial disc composed of stainless steel was introduced by Cummins7; subsequently, cervical motion preservation prostheses have been extensively studied for degenerative disc diseases.5-12 Although several authors suggest the long-term results of total disc replacement (TDR) are not inferior to anterior cervical discectomy and fusion (ACDF),12,13 whether TDR actually prevents degeneration in adjacent segments remains unclear.9 In addition, debate continues because many studies have failed to show statistically significant increase of the ROM of the adjacent segments.3,11,14,15 There are many different types of TDR, each with certain advantages and disadvantages. Because a new prosthesis has been TDR: Total disc replacement VAS: Visual analog scale Department of Neurosurgery, Korea University Ansan Hospital, Ansan, Korea To whom correspondence should be addressed: Se-Hoon Kim, M.D., Ph.D. [E-mail: [email protected]] Citation: World Neurosurg. (2019). https://doi.org/10.1016/j.wneu.2019.02.233 Journal homepage: www.journals.elsevier.com/world-neurosurgery Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2019 Elsevier Inc. All rights reserved.

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ADJACENT SEGMENT ROM AFTER TDR VERSUS ACDF

developed and improved, the evaluation of TDR conducted using data from previously performed TDRs may not be accurate. We presumed that recently developed artificial disc devices can provide better results compared with the early devices. The outcomes between TDR with artificial disc ActivC (Aesculap AG, Tuttlingen, Germany; Figure 1) and ACDF using a standalone cage performed in our hospital were compared. Although several studies on TDR have been previously conducted, studies on ActivC are lacking, thus, the present study provides valuable new evidence.

SVA was measured as the distance between a plumb line dropped from the center of C2 and the posterosuperior corner of the C7 vertebral body (Figure 2B). T1 slope was defined as the sagittal angle measured between the superior endplate of T1 and the horizontal line (Figure 2B). In addition, the segmental ROM of the operated, cranial adjacent, and caudal adjacent levels was defined as the difference between Cobb angles on lateral flexion and extension radiographs (Figure 2A). In cases where the endplate was invisible because of the shoulder, the ROM was defined as the difference between the flexioneextension angles measured from both superior endplates.

MATERIALS AND METHODS Ethics Statement Approval for this retrospective review was obtained from the institutional review board (number: 2018AS0054). The requirement for written informed consent was waived by the board. Patient Population Patients diagnosed with cervical disc diseases and who received either ACDF using stand-alone cage or TDR using ActivC at a single level from C3eC4 to C6eC7 from January 2010 to December 2015 were reviewed. Patient exclusion criteria were as follows: multilevel surgery; surgery combined with laminectomy, laminoplasty, or posterior screw fixation; vertebral anomaly of the adjacent level including block vertebra; traumatic injury such as fracture, posterior element injury, or cord injury, infection; and patients who did not complete the 2-year follow-up or did not have an adequate flexioneextension radiograph. Clinical and Radiologic Data Acquisition The clinical and radiologic data were collected in accordance with the regulations of the institutional review board at our hospital. Clinical outcomes were assessed using the visual analogue scale (VAS) for arm and neck pain and the neck disability index. Clinical scales, lateral neutral, and flexioneextension radiographs were taken for all patients preoperatively, and 2 months, 6 months, 1 year, and 2 years postoperatively. Global lordosis, C2eC7 sagittal vertical axis (SVA), and T1 slope were measured on lateral neutral radiographs. Global lordosis was measured from the Cobb angle between the lower endplate of C2 and C7 (Figure 2A). The C2eC7

Surgical Procedure The patient was placed in the supine position on the operating table under general anesthesia. A transverse linear incision was made along the skin crease on the anterior aspect of the sternocleidomastoid muscle. After dissection through the avascular plane to the anterior border of the cervical vertebral bodies medial to the carotid sheath, longus colli muscles were stripped out and 2 Caspar pins were inserted into the vertebral bodies. After incision of the annulus fibrosus, the intervertebral space was gently distracted using a Caspar distractor. Then, disc materials and posterior osteophytes were removed and the posterior longitudinal ligament was partially resected in most cases. At this stage, a polyetheretherketone cage with demineralized bone matrix was inserted in patients undergoing ACDF. For patients undergoing TDR, the guiding instrument was mounted and reaming of the keel groove was performed at the center of the superior endplate of the caudal vertebra. After size measurement using a trial implant, an ActivC prosthesis was inserted along the keel groove and correct position was confirmed using fluoroscopy. Statistical Analyses Statistical analyses and visualization were conducted using R version 3.3.2 (2016-10-31; R Foundation for Statistical Computing, Vienna, Austria) and ggplot2. Testing of normality was performed using ShapiroeWilk tests. The comparison between preoperative and postoperative parameters was performed using paired t tests and Wilcoxon signed rank tests. In addition, the comparison of parameters between ACDF and TDR groups was performed using the Student t tests and ManneWhitney U tests. A P value < 0.05 was considered statistically significant. RESULTS

Figure 1. ActivC cervical disc prosthesis. (used with permission by B. Braun Aesculap).

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A total of 53 patients (mean age 48.5 years) were reviewed. Thirty patients (22 males and 8 females) were treated with ACDF and the remaining 23 patients (15 males and 8 females) received TDR. As shown in Table 1, baseline characteristics were not different between the 2 groups. The most frequent operated level was C5eC6 in both groups (56.7% and 69.6%, respectively) followed by C4eC5 (20.0% and 13.0%, respectively). In addition, operative time or blood loss did not differ between the two groups (Table 1). The ROM in the operated segment was significantly different between the 2 groups from 2 months postoperatively (Figure 3), and the difference remained until 2 years after surgery (Table 2, P ¼ 0.007). The TDR group showed

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ORIGINAL ARTICLE BUM-JOON KIM ET AL.

ADJACENT SEGMENT ROM AFTER TDR VERSUS ACDF

Figure 2. Radiologic measurements. (A) Segmental range of motion and global lordosis. (B) C2eC7 sagittal vertical axis and T1 slope.

successful motion preservation at the operated level for the postoperative 2 years whereas the ACDF group decreased to <2 and was maintained for 2 years (Figure 3). However, for

Table 1. Patient Demographic Characteristics at Baseline Variable

ACDF (n [ 30)

TDR (n [ 23)

8 (26.7)

8 (34.8)

Sex, n (%) Female Male Age, years, mean  SD

P Value 0.737

22 (73.3)

15 (65.2)

50.6  9.4

45.9  8.4

Level, n (%)

0.064 0.702

3/4

2 (6.7)

2 (8.7)

4/5

6 (20.0)

3 (13.0)

5/6

17 (56.7)

16 (69.6)

6/7

5 (16.7)

2 (8.7)

23.1  3.9

22.6  4.1

0.637

Diabetes, n (%)

6 (20.0)

5 (21.7)

1.000

Smoking, n (%)

4 (13.3)

7 (30.4)

0.238

BMI, mean  SD

Operation time, minutes, mean  SD 77.3  15.4 74.5  10.8

0.471

Blood loss, mL, mean  SD

0.261

55.2  14.5 62.6  28.1

ACDF, anterior cervical discectomy and fusion; TDR, total disc replacement; SD, standard deviation; BMI, body mass index.

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the cranial and caudal adjacent levels, the ROM was not different during the 2 years of follow-up (Table 2 and Figure 3). Regarding clinical parameters, neck VAS, arm VAS, and neck disability index were not different between the groups (Figure 3). Both groups showed a significant improvement at 2 months postoperatively and slight improvement up to 2 years after surgery (Figure 3). At 2 years after surgery, the mean cranial and caudal segmental ROM was increased in patients who underwent ACDF and decreased in patients who underwent TDR (Table 2 and Figure 4). However, the changes reached statistical significance only at the operated level (Table 2 and Figure 4). Mean global lordosis was slightly improved in both groups compared with before surgery whereas mean C2eC7 SVA was decreased in both groups; however, no difference was observed between the ACDF and TDR groups (Table 2). In contrast, the changes in T1 slope were <2 in both groups (Table 2). The changes in ROM and global lordosis during the 2 years of follow-up based on the operated level are presented in Table 3. For the C5eC6 operated level, which occupied the largest number, ROM increased in both cranial and caudal segments in the ACDF group but decreased in the TDR group; however, statistical significance was not reached. DISCUSSION In many TDR clinical studies, motion preservation in the operative segments was reported as successful.5,6,8,10-12 In recent years, improvements in prosthesis maximized bone anchoring and minimized bone sacrifice while reproducing physiologic motion beyond simply preserving motion.16,17 A standard guideline based on the heterogeneity of artificial disc devices has yet to be established.9 ActivC (Figure 1) is a third-generation artificial disc

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ADJACENT SEGMENT ROM AFTER TDR VERSUS ACDF

Figure 3. Radiologic and clinical outcomes in anterior cervical discectomy and fusion (ACDF) and total disc replacement (TDR) groups. ROM, range of motion; VAS, visual analog scale.

prosthesis that has a dorsally located center of rotation.10 Because ActivC prosthesis has spikes on the superior plate and a relatively shallow single keel on the inferior plate, the insertion procedure is not time consuming compared with fusion surgery.18 On the surface of the end-plates, a plasmapore coating is applied to facilitate osteointegration.19 Based on our results, the same operation time and blood loss results were observed as with ACDF. No withdrawal or migration was observed in our series during the 2 years of follow-up. To prevent degenerative changes in adjacent segments is the most important issue when considering TDR as a replacement for ACDF, which has been regarded as the standard treatment. Numerous patients worldwide have undergone TDR surgery, and studies on long-term results are increasing; however, the prevention of degenerative changes in adjacent segments remains unclear.9,20 Unlike the results reported in several studies,4-6 a

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significantly increased ROM in the adjacent segments was not observed in patients in the fusion group in the present study. Despite the significant ROM difference at the operated level, patients in the ACDF and TDR groups did not show ROM differences in the adjacent segments for 2 years, possibly because the degeneration pathway does not have a constant influence on joint ROM. According to Fujiwara et al.,21 segmental motion increases with increasing disc degeneration but decreases with more advanced degeneration. Another reason is the 2-year follow-up period might have been too short to reveal a distinct difference in ROM changes in adjacent segments. In several studies, significant ROM differences in adjacent segments were not seen.3,11,14,15 Radcliff et al.22 suggested a selection bias may have existed that favored positive findings in previous TDR studies, pointing out that negative findings are equally noteworthy. Based on the ROM analysis results in the present study,

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ORIGINAL ARTICLE BUM-JOON KIM ET AL.

ADJACENT SEGMENT ROM AFTER TDR VERSUS ACDF

Table 2. Change of ROM at the Adjacent Levels and Sagittal Alignment Parameters During the 2 Years of Follow-Up ACDF (n [ 30)

TDR (n [ 23)

P Value

Operated level ROM  SD ( ) Pre

5.9  3.0

4.4  3.2

0.082

Final

2.4  2.8

4.8  3.4

0.007*

3.5  3.8

0.4  4.8

0.002*

6.8  4.4

0.451

Changes

Cranial adjacent-level ROM  SD ( ) 5.9  3.7

Pre Final

6.6  4.5

6.6  4.9

0.986

Changes

0.6  4.6

0.2  4.8

0.528

Caudal adjacent-level ROM  SD ( ) Pre

4.6  3.6

5.4  3.8

0.414

Final

6.0  4.5

5.4  3.7

0.626

Changes

1.4  4.8

0.0  3.9

0.261

Figure 4. Box plot of the degree of global lordosis and range of motion changes between anterior cervical discectomy and fusion (ACDF) and total disc replacement (TDR) groups.

Global lordosis  SD ( ) Pre

13.7  9.9

12.4  7.6

0.614

Final

14.8  11.6

13.3  6.4

0.562

1.1  6.3

0.9  6.5

0.909

26.7  9.5

0.320

23.3  10.6

0.190

Changes

C2eC7 SVA, mm  SD 23.6  12.2

Pre

19.6  9.2

Final

4.0  12.4

Changes

3.4  9.5

0.860



T1 slope  SD ( ) Pre

25.0  4.7

22.8  4.9

0.122

Final

23.4  6.5

23.4  5.3

0.990

1.6  4.6

0.6  3.9

0.080

Changes

ROM, range of motion; ACDF, anterior cervical discectomy and fusion; TDR, total disc replacement; SD, standard deviation; SVA, sagittal vertical axis. *Indicates statistically significant difference with P < 0.05.

monitoring degenerative changes to adjacent segments with changes in ROM within 2 years may not be effective. Cervical lordotic curvature often is considered associated with cervical degeneration or neck pain,23,24 although the reported normal value varies.23,25 Therefore, evaluating global lordotic angle improvement after surgery was evaluated in the present study and statistically significant change was not observed in either group (Table 2 and Figure 4). In particular, although a polyetheretherketone cage with lordotic angle was routinely inserted in patients in the ACDF group, change was not observed in global lordosis compared to before surgery. Recently, an increasing number of studies have suggested a relationship between cervical curvature and thoracolumbar deformity.23,26 Although not conducted in this study, further studies on whole spine curvature are needed to exclude the contribution of compensatory changes.

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The incidence of heterotopic ossification (HO) reported has varied widely between studies.27-31 Mehren et al.29 reported that HO was observed in up to 66.2% of patients undergoing TDR. Based on the hypothesis for HO formation that an extensive milling process for inserting an artificial disc device increases risks,28,31 a different incidence for each surgeon and for each device is expected. Leung et al.31 asserted the incidence was greater in males and older patients. Yi et al.32 suggested male sex and device type, and Suchomel et al.33 suggested the position of the device were related to HO generation. However, predisposing factors, mechanisms, and prevalence remain unclear. According to the grading system of McAfee and Mehren et al.,29,30 grade 3 or greater HO was observed in 4 patients (16.7%); in the present study, all had ROM <2 in the operated segment. All patients were male and the mean age was 48 years, which was greater than the mean age of 45.9 years in the TDR group. This is consistent with previous studies. Conversely, the fusion rate of the single-level ACDF using demineralized bone matrix has been reported to range from 52.6% to 97%.34,35 In this study, the overall fusion rate was 86.7%. Four of the 30 patients who underwent ACDF developed pseudarthrosis, and of those, 3 had severe osteoporosis. This study had some limitations because of the small population size and retrospective design. South Korea’s National Health Insurance limits the reimbursement for TDR in cervical disc diseases where meaningful osteophytes are observed. In addition, generally the total treatment for TDR costs approximately $3500 more than ACDF. For this reason, the possibility of selection bias may exist in South Korea, favoring more ACDF than TDR in patients with spur or foraminal stenosis or economically poor patients. Considering the patients in the ACDF group tended to have a slightly increased ROM in the adjacent segments compared with patients in the TDR group, further long-term and larger prospective studies of the latest artificial disc devices are needed in the future.

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ADJACENT SEGMENT ROM AFTER TDR VERSUS ACDF

Table 3. Mean Changes of ROM Based on Operated Cervical Level ACDF

Variables Operated level ROM  SD ( )

3/4 (n [ 2)

4/5 (n [ 6)

5/6 (n [ 17)

TDR 6/7 (n [ 5)

Total (n [ 30)

4.1  0.1 4.6  4.0 3.8  4.3 0.7  1.5 3.5  3.8

3/4 (n [ 2)

4/5 (n [ 3)

5/6 (n [ 16)

4.3  4.2 2.0  1.1 0.0  5.3

6/7 (n [ 2) 3.5  1.1

Total (n [ 23) 0.4  4.8

Cranial adjacent ROM 1.6  5.5

1.2  5.4

0.6  5.0

1.0  3.3

0.6  4.6

2.9  6.9

4.1  4.3 0.9  4.3 3.9  5.2 0.2  4.8

Caudal adjacent ROM 0.5  4.6

2.9  5.8

1.9  5.0 1.5  2.2

1.4  4.8

0.8  3.0

2.4  1.4 0.3  4.5 2.3  0.2 0.0  3.9

3.9  5.9

1.1  6.3 2.0  6.0

Global lordosis

7.1  0.4 3.8  4.5

0.7  4.7

3.3  7.3

0.7  7.0

1.7  3.5

0.9  6.5

ROM, range of motion; ACDF, anterior cervical discectomy and fusion; TDR, total disc replacement.

CONCLUSIONS Based on the results of the present study, the clinical outcomes for ACDF and TDR were equally favorable for 2 years after surgery. TDR using ActivC showed excellent motion preservation at the

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operated level during the 2 years of follow-up. Regarding segmental motion of the adjacent levels, both groups did not show significant differences. Considering the excellent motion preservation, the long-term results of TDR using ActivC are promising.

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with thoracolumbar deformity. Spine (Phila Pa 1976). 2014;39:E1001-E1009. 27. Brenke C, Scharf J, Schmieder K, Barth M. High prevalence of heterotopic ossification after cervical disc arthroplasty: outcome and intraoperative findings following explantation of 22 cervical disc prostheses. J Neurosurg Spine. 2012;17:141-146. 28. Suchomel P, Jurak L, Benes V 3rd, Brabec R, Bradac O, Elgawhary S. Clinical results and development of heterotopic ossification in total cervical disc replacement during a 4-year followup. Eur Spine J. 2010;19:307-315. 29. Mehren C, Suchomel P, Grochulla F, et al. Heterotopic ossification in total cervical artificial disc replacement. Spine (Phila Pa 1976). 2006;31: 2802-2806. 30. McAfee PC, Cunningham BW, Devine J, Williams E, Yu-Yahiro J. Classification of heterotopic ossification (HO) in artificial disk replacement. J Spinal Disord Tech. 2003;16:384-389.

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Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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Received 10 January 2019; accepted 25 February 2019 Citation: World Neurosurg. (2019). https://doi.org/10.1016/j.wneu.2019.02.233 Journal homepage: www.journals.elsevier.com/worldneurosurgery Available online: www.sciencedirect.com

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