Since 1958, anterior cervical discectomy and fusion (ACDF) have been widely performed for the surgical treatment of radiculopathy or myelopathy in degenerative cervical disease.1,2 After removal of the interval disk, autologous bone, and allograft bone, an interbody cage is used as a substitute. ACDF with an interbody cage is effective for the recovery of disk height. Cage subsidence, when it occurs, often leads to poor results. Cage subsidence in the vertebral body after ACDF reduces the foraminal height and cervical alignment. Many authors have suggested that the use of plates increases the fusion rate in ACDF.3–6 The rigid fixation of an anterior plate eliminates micromotion between the graft and body interface.7 However, postoperative dysphagia, adjacent segment degeneration, and other complications often occur.8–12 The current study attempts to investigate cage subsidence after ACDF using stand-alone cages.
A total of 136 patients 182 disks with degenerative disk disease underwent ACDF using stand-alone cages between February 2006 and October 2015 at our center. Seventy-eight (57.4%) (52 males, 26 females) of the 136 patients were included in this study (Table 1). Patients were followed regularly for at least 1 year after surgery. Inclusion criteria were: (1) myelopathy or radiculopathy diagnosed in the physical examination; (2) spinal cord or root compression visible in recent magnetic resonance imaging and/or computed tomography with myelogram (MCT) at single or multilevels; (3) no response to conservative treatment. Exclusion criteria were: (1) patients who needed anterior cervical plate fixation (fixation of >3 disks); (2) patients who needed posterior approach; (3) trauma; (4) infection. Of the 105 operated disks, 8 disks were C3/C4 level, 24 disks were C4/C5 level, 53 disks were C5/C6 level, 18 disks were C6/C7 level, and 2 disks were C7/Th1 level. There were 61 disks in the titanium cage group, 36 disks in the polyetheretherketone (PEEK) cage group, and 8 disks in the anchored cage group.
A left-sided Smith-Robinson anterior cervical approach was used in all cases. Vertebral bodies were distracted using a Casper distractor. There was minimum bone removal of the anterior bony spur for rear visibility and cage fitting. After microsurgical discectomy, posterior longitudinal ligaments with posterior bony spur were removed. Endplate cartilage was also removed using a curette avoiding additional damage to the endplates. Titanium interbody cages of the following types were used: Syncage-C (Depuy-Synthes, Raynham, MA), Cornerstone (Medtronic Sofamor Danek, Memphis, TN). PEEK cages of the following types were used: CeSpace PEEK (B.Braun Aesculap, Melsungen, Germany), Cornerstone PEEK (Medtronic Sofamor Danek, Memphis, TN), C-THRU (Zimmer-Biomet, Broomfield, CO), ACIS (Depuy-Synthes). Zero-profile anchored PEEK cages of the following types were used: Anchor-C (Stryker, Kalamazoo, MI), Solitaire-C (Zimmer-Biomet), PEEK PREVAIL(Medtronic Sofamor Danek) (Table 2). The mean cage height was 5.1 mm (4–7 mm). Interbody cages were packed with the harvested autologous cancellous bone from the anterior iliac crest via a 1-cm skin incision. All patients wore a cervical collar for 4 weeks after surgery.
The intervertebral height was assessed using radiographs taken preoperatively, at 1 week, and at 1, 3, 6, 12 months postoperatively. The intervertebral height was calculated as the height of the anterior border. Cage subsidence was calculated as the decrease in intervertebral height. Cervical lordosis was assessed using Cobb angle at levels C2–C7 preoperatively, at 1 week, and at 12 months postoperatively. The Cobb angle was formed by lines along the inferior endplate of C2 to the inferior endplate of C7 in a neutral position. Fusion was determined with dynamic radiographs to identify segment stability as a distance change of <2 mm between the tips of the spinous processes and/or the presence of bridging trabecular bone at the surgically treated level. Clinical results were evaluated using the Japanese Orthopedic Association Score System (JOA Score) preoperatively and at 12 months postoperatively.
For statistical analysis, the Spearman rank correlation coefficient or the Mann-Whitney U test were conducted to evaluate the radiologic and clinical outcomes for each group. The 2-tailed test results were considered significant when P-value <0.05. All statistical analyses were performed using statistical software for Windows (version13.0; SPSS Inc., Chicago, IL).
The radiologic outcomes are summarized in Figure 1. The anterior intervertebral height was 4.23±0.13 mm before surgery, 6.78±0.13 mm 1 week after surgery, 6.05±0.14 mm 1 month after surgery, 5.52±0.14 mm 3 months after surgery, 5.23±0.14 mm 6 months after surgery, and 4.80±0.13 mm 12 months after surgery. Cage subsidence was 1.97±0.13 mm at the final follow-up. The period exhibiting the most disk height decrease was 1 month postoperatively. There was no correlation seen in intervertebral height between the preoperative period and the 12 months postoperative period (P=0.149). In addition, there was no correlation seen between age and cage subsidence (P=0.288) (Fig. 2). However, there was a correlation between cage height and cage subsidence (P<0.01) (Fig. 3).
The mean height of the titanium and PEEK cages was 5.20±0.60 and 4.76±0.68 mm, respectively, indicating a significant difference between the 2 groups (P<0.01). The subsidence of the titanium and PEEK cages was 2.26±1.26 and 1.27±1.02 mm, respectively, also indicating a significant difference (P<0.01) (Fig. 4). However, when cage height was <5 mm, the subsidence of the titanium cages and PEEK cages was 1.85±0.96 and 1.21±0.97 mm, respectively, which did not indicate a significant difference (P=1.992) (Fig. 5). Large subsidence (>3 mm) was observed in 17 patients, 20 disks: titanium cages 14 disks, PEEK cages 3 disks, and anchored cages 3 disks. A continued decrease in disk height was observed in these patients from 1 month postoperatively to 12 months postoperatively (Fig. 6). The mean subsidence was 4.13 mm (3.00–7.00 mm). The mean cage height was 5.6 mm (4.5–7.0 mm). The disk levels involved were: C4/C5 level, 4 disks; C5/C6 level, 13 disks; C6/C7 level, 2 disks; and C7/Th1 level, 1 disk.
There were 39 smokers (51 disks) in this study: 26 current smokers (33 disks) and 13 former smokers (18 disks). The mean subsidence was 1.98 mm (0.36–6.18 mm) in nonsmokers, 1.71 mm (0–4.01 mm) in former smokers, and 2.11 mm (0.16–7 mm) in current smokers. There was no significant difference among the 3 groups.
The C2–C7 Cobb angle was 2.3±1.5 degrees before surgery, 6.8±1.2 degrees 1 week after surgery, and 5.2±1.2 degrees 12 months after surgery (Fig. 7). There was a significant difference between preoperative and postoperative Cobb angle (P<0.01). However, in large subsidence cases, the Cobb angle was 8.7±3.0 degrees before surgery, 9.4±1.8 degrees 1 week after surgery, and 11.6±1.6 degrees 12 months after surgery, which indicated no significant difference between preoperative and postoperative Cobb angle (P=0.688). The C2–C7 Cobb angle kept a good value in spite of large subsidence.
The segmental angle was −1.8±0.9 degrees before surgery, 4.1±0.8 degrees 1 week after surgery, and −1.1±0.8 degrees 12 months after surgery (Fig. 8). In large subsidence cases, the segmental angle was −2.3±1.9 degrees before surgery, 3.2±2.3 degrees after surgery and −3.5±1.9 degrees 12 months after surgery. No significant difference was observed in segmental angle preoperatively and at 12 months after surgery in either group (P=0.754 and 0.576).
Fusion rate was 80% (84/105). In large subsidence cases, the fusion rate was 65% (13/20). However, the fusion rate was affected by smoking status. Fusion rate in current smokers (26 cases, 33 disks), former smokers (13 cases, 33 disks) and nonsmokers (39 cases, 54 disks) was 60.6%, 88.9%, 87.0%, respectively.
The average JOA Score improved from 13.6 to 15.7 and the recovery rate was 15.4%. In large subsidence cases, the average JOA Score improved from 13.9 to 15.6 and the recovery rate was 12.2%. No significant difference was observed in the recovery rate between the 2 groups (P=0.629).
ACDF is a standard procedure for the surgical treatment of patients with radiculopathy and myelopathy. After surgery, subsidence is a frequent phenomenon. However, in some studies subsidence has not been reported as affecting clinical outcome.13–18 Our data also shows similar results. Parks et al19 reported that subsidence reduced the distance of foramina and segmental and overall cervical lordosis. In contrast, Lee and colleagues reported that the lack of correlation between bad clinical outcome and radiographic subsidence may be due to segmental kyphosis, preserved posterior height, and maintaining the global cervical angle.20 In this study, segmental angle did not show improvement at the final follow-up period. However, the C2–C7 Cobb angle and clinical outcome improved. Global cervical alignment is affected not only by segmental kyphosis but by other factors. The global and segmental angle measured preoperatively had no relation to subsidence in this study. We can safely say that a small degree of subsidence helps retain posterior height and maintain interbody stability. However, we must avoid cage subsidence since it is often the cause of cervical foraminal stenosis and cage displacement.
According to some previous articles, factors resulting in subsidence are site-specific bone mineral density, cage placement, and cage material.21–23 In the modulus, the elasticity of PEEK is similar to the elasticity of bone. The subsidence occurring in PEEK cages was smaller than that occurring in titanium cages. However, we cannot conclude that PEEK cages are superior to titanium cage in terms of the maintenance of intervertebral height in clinical situations. In cages with heights of <5 mm, there was no significant difference observed between PEEK cages and titanium cages. Truumees et al24 reported that significantly higher distractive and compressive forces were recorded with large grafts. These results indicate clearly that the greater the cage height, the greater the risk of cage subsidence.
In many cases, subsidence occurred in the first month after surgery (Fig. 1). When patients get out of bed in the initial days following surgery, great pressure is applied to the interbody. In this study, large subsidence cases (>3 mm) existed in 20 levels. In these cases, there were 5 levels in which a nonanatomic (flat shaped) cage was used. Nonanatomic interbody cages do not fit the underside endplate of the vertebral body, which easily results in subsidence. Anatomic (dome-shaped) interbody cages should be selected to avoid this result. If nonanatomic shaped cages are selected, we must level the endplate of the vertebral body to obtain a large contact area. Dai et al4 concluded that supplemented anterior plate fixation can increase fusion rate and prevent cage subsidence. However, a second surgery was necessary in 1 case in our study in which radiculopathy recurred 3 years after the initial operation. In contrast, postoperative dysphagia, adjacent segment degeneration, and other complications often occur. There were 2 cases among our patients which required the removal of the plate due to infection. Fountas et al9 reported a rare case of a screw extrusion into the gastrointestinal tract of a patient 16 months after ACDF. The use of plates should be considered only when absolutely necessary. If contact is not established between the cage and the endplate of the vertebral body, rigid plates, and anchored cages reduce the compression force. Increased space between the cage and endplate may result in the loosening of the screw or subsidence (Fig. 9).
In addition, it is important to increase the area of the contact surface. Kwon et al25 reported that interspinous motion decreased as the graft-area increased and that the necessary graft-area might be >100 mm2 for intragraft bone bridging. In general, the graft-area of commercial stand-alone cages is too small to achieve bone union. It is important to avoid cage subsidence in the first month after surgery by avoiding wide cages.
Cigarette smoking increases the risk of perioperative complications, nonunion and delayed union of fractures, infection, and soft-tissue and wound-healing complications.26–28 In ACDF, many studies have stated that smoking increases the risk of pseudarthrosis and other complications.29–33 Bishop et al29 reported that smokers had substantially higher delayed and failed fusion rates and greater interspace collapse and angulation following single and multilevel cervical interbody fusion than nonsmokers. This study also found a lower fusion rate in smokers. The known factor in cigarette smoking is nicotine. Nicotine has numerous physiological effects, including stimulating the sympathetic nervous system, causing vascular disturbances, and inducing cell death.34 Conversely, it is known that the terminal half-life of nicotine after smoking is ∼2 hours.35 Nonsmoking is beneficial to bone fusion. However, it does not affect the maintenance of disk height due to the amount of time needed to achieve bone fusion. Therefore, in our study, there was no significant difference between subsidence and smoking.
The greater the cage height, the greater the risk of cage subsidence in ACDF. PEEK cages are superior to titanium cages for the maintenance of intervertebral height in cases where cage height is >5.5 mm.
1. Smith GW, Robinson RA. The treatment of certain cervical-spine disorders by anterior removal of the intervertebral disc and interbody fusion. J Bone Joint Surg Am. 1958;40-A:607–624.
2. Cloward RB. The anterior approach for removal of ruptured cervical disks. J Neurosurg. 1958;15:602–617.
3. Jeffrey CW, Paul WM, Kevin E, et al. The effect of cervical plating on single-level anterior cervical discectomy and fusion. J Spinal Disord Tech. 1999;12:467–471.
4. Dai LY, Jiang LS. Anterior cervical fusion with interbody cage
containing β-tricalcium phosphate augmented with plate fixation: a prospective randomized study with 2-year follow-up. Eur Spine J. 2008;17:698–705.
5. Song KJ, Taghavi CE, Lee KB, et al. The efficacy of plate construct augmentation versus cage alone in anterior cervical fusion. Spine. 2009;34:2886–2892.
6. Lee CH, Hyun SJ, Kim MJ, et al. Comparative analysis of 3 different construct systems for single-level anterior cervical discectomy and fusion. Stand-alone cage, iliac graft plus plate augmentation, and cage plus plating. J Spinal Disord Tech. 2013;26:112–118.
7. Shimamoto N, Cunningham BW, Dmitriev AE, et al. Biomechanical evaluation of stand-alone interbody fusion cage in the cervical spine. Spine. 2001;26:E432–E436.
8. Lee MJ, Bazaa R, Furey CG, et al. Influence of anterior cervical plate design on dysphagia: a 2-year prospective longitudinal follow-up study. J Spinal Disord Tech. 2005;18:406–409.
9. Fountas KN, Kapsalaki EZ, Nikolakakos LG, et al. Anterior cervical discectomy and fusion associated complications. Spine. 2007;32:2310–2317.
10. Park JB, Cho YS, Riew KD, et al. Development of adjacent-level ossification in patients with an anterior cervical plate. J Bone Joint Surg Am. 2005;87A:558–563.
11. Geyer TE, Foy MA. Oral extrusion of a screw after anterior cervical spine plating. Spine. 2001;26:1814–1816.
12. Fujibayashi S, Shikata J, Kamiya N, et al. Missing anterior cervical plate and screws: a case report. Spine. 2000;25:2258–2261.
13. Tomé-Bermejo F, Morales-Valencia JA, Moreno-Pérez J, et al. Degenerative cervical disc disease: long-term changes in sagittal alignment and their clinical implications after cervical interbody fusion cage subsidence
. A prospective study with standalone lordotic tantalum cages. Clin Spine Surg. 2017;30:E648–E655.
14. Yson SC, Sembrano JN, Santos ER. Comparison of allograft and polyetheretherketone (PEEK) cage subsidence
rates in anterior cervical discectomy and fusion (ACDF). J Clin Neurosci. 2017;38:118–121.
15. Kim WB, Hyun SJ, Choi H, et al. Long-term follow-up results of anterior cervical inter-body fusion with stand-alone cages. J Korean Neurosurg Soc. 2016;59:385–391.
16. Kao TH, Wu CH, Chou YC, et al. Risk factors for subsidence
in anterior cervical fusion with stand-alone polyetheretherketone (PEEK) cages: a review of 82 cases and 182 levels. Arch Orthop Trauma Surg. 2014;134:1343–1351.
17. Yamagata T, Takami T, Uda T, et al. Outcome of contemporary use of rectangular titanium stand-alone cages in anterior cervical discectomy and fusion: cage subsidence
and cervical alignment. J Clin Neurosci. 2012;19:1673–1678.
18. Park JY, Choi KY, Moon BJ, et al. Subsidence
after single-level anterior cervical fusion with a stand-alone cage. J Clin Neurosci. 2016;33:83–88.
19. Park JH, Hyun SJ, Lee CH, et al. Efficacy of a short plate with an oblique screw trajectory for anterior cervical plating. A comparative study with a 2-year minimum follow-up. Clin Spine Surg. 2016;29:E43–E48.
20. Lee CH, Kim KJ, Hyun SJ, et al. Subsidence
as of 12 months after single-level anterior cervical inter-body fusion. Is it related to clinical outcomes? Acta Neurochir. 2015;157:1063–1068.
21. Brenke C, Dostal M, Scharf J, et al. Influence of cervical bone mineral density on cage subsidence
in patients following stand-alone anterior cervical discectomy and fusion. Eur Spine J. 2015;24:2832–2840.
22. Wu WJ, Jiang LS, Liang Y, et al. Cage subsidence
does not, but cervical lordosis improvement does affect the long-term results of anterior cervical fusion with stand-alone cage for degenerative cervical disc disease: a retrospective study. Eur Spine J. 2012;21:1374–1382.
23. Barsa P, Suchomel P. Factors affecting sagittal malalignment due to cage subsidence
in standalone cage assisted anterior cervical fusion. Eur Spine J. 2007;16:1395–1400.
24. Truumees E, Demetropoulos CK, Yang KH, et al. Effect of disc height and distractive forces on graft compression in an anterior cerivical discectomy model. Spine. 2002;27:2441–2445.
25. Kwon SW, Kim CH, Chung CK, et al. The formation of extragraft bone bridging after anterior cervical discectomy and fusion: a finite element analysis. J Korean Neurosug Soc. 2017;60:611–619.
26. Brown CW, Orme TJ, Richardson HD. The rate of pseudarthrosis (surgical nonunion) in patients who are smokers and in patients who are nonsmokers: a comparison study. Spine. 1986;11:942–943.
27. Moghaddam A, Zimmermann G, Hammer K, et al. Cigarette smoking influences the clinical and occupational outcome of patients with tibial shaft fractures. Injury. 2011;42:1435–1442.
28. Lau D, Chou D, Ziewacz JE, et al. The effects of smoking on perioperative outcomes and pseudarthrosis following anterior cervical corpectomy. J Neurosurg Spine. 2014;21:547–558.
29. Bishop RC, Moore KA, Hadley MN. Anterior cervical interbody fusion using autogeneic and allogeneic bone graft substrate: a prospective comparative analysis. J Neurosurg. 1996;85:206–210.
30. Hillbrand AS, Fye MA, Emery SE, et al. Impact of smoking on the outocome of anterior cervical arthrodesis with interbody or strut-grafting. J Bone Joint Surg Am. 2001;83-A:668–673.
31. Hermansen A, Hedlund R, Vavruchi L, et al. Positive predictive factors and subgroup analysis of clinically relevant improvement after anterior cervical decompression and fusion for cervical disc disease. A 10- to 13 follow-up of a prospective randomized study. J Neurosurg Spine. 2013;19:403–411.
32. Lee JC, Lee SH, Peters C, et al. Adjacent segment pathology requiring reoperation after anterior cervical arthrodesis: the influence of smoking, sex, and number of operated levels. Spine. 2015;40:E571–E577.
33. Tabaraee E, Ahn J, Bohl DD, et al. The impact of worker’s compensation claims on outcomes and costs following an anterior cervical discectomy and fusion. Spine. 2015;40:948–953.
34. Lee JJ, Patel R, Biermann JS, et al. Current concepts review: the musculoskeletal effects of cigarette smoking. J Bone Joint Surg Am. 2013;95:850–859.
35. Nakajima M, Yamaguchi S, Yamamoto H, et al. Deficient continine formation from nicotine is attributed to the whole deletion of the CRP2A6 gene in human. Clin Pharmacol Ther. 2000;67:57–69.