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Cage Subsidence and Fusion Rate in Extreme Lateral Interbody Fusion with and without Fixation
Original Article
Cage Subsidence and Fusion Rate in Extreme Lateral Interbody Fusion with and without Fixation Enliang Chen1,2, Junjie Xu1-3, Shanzhi Yang2,4, Qingshun Zhang2,3, Honglei Yi2,3, Daxuan Liang1,2, Sibin Lan5, Mingyang Duan4, Zenghui Wu1-3
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OBJECTIVE: To examine the subsidence rate in patients undergoing extreme lateral interbody fusion (XLIF) using data from a 2-year retrospective study to assess the effect of supplemental fixation on the stand-alone procedure.
BPS group compared with the other groups. At the last follow-up, high-grade subsidence was found in 26.89% of all cases, the fusion rate was 85.71%, and the VAS and JOA scores were significantly improved in all groups.
METHODS: Demographic and perioperative data for all patients who underwent XLIF for degenerative lumbar disorders between June 2012 and January 2016 were collected and divided into 4 groups: the stand-alone (SA), lateral fixation, unilateral pedicle screw, and bilateral pedicle screw (BPS) groups. The disk height (DH), lumbar lordotic (LL) angle, and segmental lordotic (SL) angle were measured preoperatively and 3 days, 3 months, 1 year, and 2 years postoperatively. Clinical outcomes were evaluated using Japanese Orthopaedic Association (JOA) and visual analog scale (VAS) scores. Fusion was defined according to computed tomography scan.
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RESULTS: There were 126 vertebrae in 107 patients treated. SL angle, LL angle, and DH significantly increased postoperatively in all groups. Although the preoperative and 2-year postoperative DHs in the SA group were similar, the other measures showed significant differences from baseline at each follow-up visit. No significant effects on SL angle or DH were found in any of the groups. A significant difference in the LL angle was found in the
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Key words Cage subsidence - Fusion - Internal fixation - XLIF -
Abbreviations and Acronyms ANOVA: Analysis of variance BMD: Bone mineral density BMI: Body mass index BPS: Bilateral pedicle screw CT: Computed tomography DH: Disk height JOA: Japanese Orthopaedic Association LF: Lateral fixation LL: Lumbar lordotic rh-BMP2: Recombinant human bone morphogenetic protein 2 SA: Stand-alone SL: Segmental lordotic
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CONCLUSIONS: Supplemental fixation did not significantly influence cage subsidence or SL angle. Only BPS fixation significantly improved the LL angle. The 2-year fusion rate was satisfactory.
INTRODUCTION
S
ince Ozgur et al.1 first described extreme lateral interbody fusion (XLIF) in 2006, the technique has become a less invasive alternative to conventional anterior and posterior approaches for interbody fusion.2 XLIF has been practiced at the Guangzhou General Hospital of People's Liberation Army, China, since 2008. As a minimally disruptive approach for spinal fusion, XLIF has been widely used to treat degenerative lumbar disease, such as low-grade spondylolisthesis (grades 1 and 2), spinal stenosis, degenerative lumbar scoliosis, and multilevel degenerative disk disease. Using a transpsoas approach, which is made via a tubular retractor system, the disk height (DH) and sagittal alignment can be restored by implanting a large cage
UPS: Unilateral pedicle screw VAS: Visual analog scale XLIF: Extreme lateral interbody fusion From the 1Southern Medical University, Guangzhou; 2Department of Orthopedics, Guangzhou General Hospital of Guangzhou Military Command, Guangzhou; 3Institute of Traumatic Orthopaedics of People’s Liberation Army, Guangzhou; 4Guangzhou University of Traditional Chinese Medicine, Guangzhou, People’s Republic of China; and 5The Third Affiliated Hospital of Guangzhou University of Chinese Medicine, Guangzhou, People’s Republic of China To whom correspondence should be addressed: Zenghui Wu, M.D., Ph.D. [E-mail: [email protected]] Enliang Chen and Junjie Xu are coefirst authors. Citation: World Neurosurg. (2018). https://doi.org/10.1016/j.wneu.2018.10.182 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2018 Elsevier Inc. All rights reserved.
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XLIF WITH AND WITHOUT FIXATION
Figure 1. Postoperative radiographs of the 4 groups: (A and B) stand-alone group, (C and D) lateral fixation group, (E and F) unilateral pedicle screw group, and (G and H) bilateral pedicle screw group.
without disrupting the back muscles, anterior and posterior longitudinal ligaments, or facet joints. Therefore, XLIF has been widely accepted because of its advantages, including reduced tissue trauma and postoperative pain, shorter hospital stays, and quicker recovery. However, XLIF also has the potential to cause psoas disruption and lumbar plexus injury. Such cages could potentially fail to restore the DH or maintain the segmental lordosis because of cage subsidence.3 Currently, 2 mm of cage settlement into the vertebral body is considered cage subsidence.4,5 Bocahut et al.6 reported a cage subsidence rate of 32%, with subsidence defined as 4 mm of cage settlement into the vertebral body. Several reports have described cage subsidence after the XLIF procedure, with an incidence ranging from 9.5% to 22%.3,7,8 However, with the lack of uniform methods for assessing the extent of subsidence, interpreting or comparing the results of such studies is difficult.8 Regarding the implant graft, autologous bone can be replaced with many types of bone substitutes, such as allograft bone, demineralized bone matrix, ceramics, and recombinant human bone morphogenetic protein 2 (rh-BMP2). The question is
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whether these alternatives exhibit the characteristics of an ideal graft, including those characteristics required for osteoconduction, osteoinduction, or osteogenesis. Our implant grafts consist of allograft bone mixed with autologous bone marrow.
Table 1. Main Indication Parameter
SA
LF
UPS
BPS
Lumbar disk herniation
10
11
8
11
40
Grade 1 or 2 spondylolisthesis
10
10
8
11
39
Lumbar spinal stenosis
6
10
6
2
24
Degenerative scoliosis
1
0
1
2
4
Total
27
31
23
26
107
Values are number of patients. SA, stand-alone; LF, lateral fixation; UPS, unilateral pedicle screw; BPS, bilateral pedicle screw.
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ORIGINAL ARTICLE ENLIANG CHEN ET AL.
XLIF WITH AND WITHOUT FIXATION
Table 2. Demographic, Clinical, and Surgical Data Group Parameter Number of levels Age (years) Male-to-female ratio BMI (kg/m2)
SA (n [ 27)
LF (n [ 31)
UPS (n [ 23)
BPS (n [ 26)
34
32
28
32
60.15 11.28
59.56 11.02
61.96 11.95
61.47 10.87
P Value
0.823*
19:15
16:16
9:19
9:23
0.067y
24.30 2.21
24.50 2.44
23.82 2.20
23.76 1.88
0.470*
e0.14 1.66
e0.38 1.30
e0.36 1.54
e0.29 1.45
0.909*
Preoperative VAS score
6.03 1.24
6.34 1.15
6.04 1.07
6.28 1.28
0.620*
Preoperative JOA score
13.00 2.59
12.75 3.00
12.00 2.93
13.03 2.91
0.480*
Preoperative SL angle
11.97 5.99
12.19 10.19
11.41 5.48
10.12 1.79
0.878*
Preoperative LL angle
32.68 10.66
31.40 8.40
30.05 9.86
37.50 10.34
0.104*
BMD
Preoperative DH
6.33 1.68
6.24 1.71
5.78 1.82
6.30 2.21
0.650*
Blood loss (mL)
37.16 8.15
43.75 15.14
81.79 15.71
102.03 37.80
< 0.001*
Surgery duration (minutes)
53.21 8.68
56.44 10.06
87.21 18.73
128.88 22.31
< 0.001*
Values are mean SD or as otherwise indicated. SA, stand-alone; LF, lateral fixation; UPS, unilateral pedicle screw; BPS, bilateral pedicle screw; BMI, body mass index; BMD, bone mineral density; VAS, visual analog scale; JOA, Japanese Orthopaedic Association; SL, segmental lordotic; LL, lumbar lordotic; DH, disk height. *One-way analysis of variance. yFisher exact test.
Therefore, the main goal of this study was to examine the subsidence rate after XLIF using data from a 2-year, retrospective, randomized study of the effects of supplemental lateral fixation (LF), unilateral pedicle screw (UPS) fixation, and bilateral pedicle screw (BPS) fixation on the stand-alone (SA) procedure. MATERIALS AND METHODS Patients and Indications This study examined 107 patients who underwent XLIF between June 2012 and January 2016. The indications for surgery were symptomatic single-level or multilevel lumbar degenerative disease from L1 to L5. Radiograph (anterior-posterior, lateral, flexion, and extension), computed tomography (CT) scan, and magnetic resonance imaging studies, and dual-energy x-ray absorptiometry studies to assess bone mineral density (BMD), were performed preoperatively for each patient. Postoperative data were collected at 3 days, 3 months, 1 year, and 2 years after the surgery. Surgical Techniques All procedures were performed by one spine surgeon with XLIF experience. Under general anesthesia, patients were placed in a true right lateral position, with the left hip and knee flexed. Adhesive plaster was used to appropriately fix the patient with the bed bent, therefore maximally extending the space between the iliac crest and lowest rib. Fluoroscopy was used to localize the index level. After a small incision was made across the target area, the surgeon reached the retroperitoneal space with a finger. Then, a blunt dilator was used to penetrate the psoas muscle. The target
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intervertebral disk area was located and exposed with a retractor, and diskectomy was performed. Autologous bone marrow was extracted from the vertebral body of the operated segment. Then, a polyetheretherketone cage filled with allograft bone and autologous bone marrow was implanted. The cancellous allograft bone was produced by Shanxi Aorui Biological Materials Co., Ltd., (Shanxi, People's Republic of China) using the Shanxi Medical
Table 3. Summary of Cage Size Variable
Number of Patients (%)
Cage width (number of levels) 18 mm
126 (100)
Cage height (number of levels) 8 mm
4 (3.17)
10 mm
54 (42.86)
12 mm
68 (53.97)
Cage length (number of levels) 45 mm
52 (41.27)
50 mm
63 (50.00)
55 mm
11 (8.73)
Cage lordotic angle (number of levels) 12
126 (100)
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Table 4. Segmental Lordotic and Lumbar Lordotic Correction Values Parameter
SA
LF
UPS
BPS
P Value*
Pre to post (3 days)
1.64 2.59
1.31 3.62
1.02 2.47
2.53 4.77
0.364
Pre to post (3 months)
1.51 3.41
2.16 4.37
1.61 2.22
2.18 3.88
0.815
P Valuey
SL
Pre to post (1 year)
1.53 2.96
1.75 4.63
1.44 3.16
0.948
1.96 3.98
Pre to post (2 years)
1.59 3.62
1.73 4.55
1.38 3.44
1.71 4.15
0.986
Pre to post (3 days)
2.25 3.49
2.55 3.38
2.44 3.67
2.50 7.89
0.043
Pre to post (3 months)
3.33 3.77
2.86 4.47
3.45 4.29
4.31 5.02
0.003
0.893
LL
Pre to post (1 year) Pre to post (2 years)
3.47 3.83 2.57 4.13
2.88 4.51 2.58 4.84
3.37 5.03 2.61 5.37
0.004
0.004
7.22 9.01 7.07 9.39
0.006
Values are mean SD or as otherwise indicated. SA, stand-alone; LF, lateral fixation; UPS, unilateral pedicle screw; BPS, bilateral pedicle screw; SL, segmental lordotic; Pre, preoperative; Post, postoperative; LL, lumbar lordotic. *P value comparison between the 4 surgical procedures at each time point. yP value the value of surgical procedures impacting the SL angle and LL angle.
Organization Database. The lateral dimension of the cage (40, 45, 50, or 55 mm) was determined preoperatively according to a measurement of the index level on lumbar CT scan, whereas the cage height (8, 10, or 12 mm) was determined intraoperatively by trials. All the cages were lordotic. In this study, dual-energy x-ray absorptiometry studies were performed preoperatively to assess the BMD, and neural and dynamic standing radiographic films were used to assess the position of the iliac crest in each patient. The surgeon decided to use different types of fixations according to the BMD, radiographs, and basic conditions of the patients. If the BMD T score of a patient was less than e2.5, then the surgeon would prefer to use BPSs for fixation. For L4-5 segments, even if the BMD was suitable for vertebral screw fixation, if the iliac crest obstructed supplementation with LF, then the surgeon would not choose LF. If a patient had both a high iliac crest and chronic disease, such as diabetes, cardiopathy, or hypertension, then the surgeon would prefer to use UPS fixation while not changing the true right lateral position of the patient. Finally, if the BMD T score of a patient was equal to or greater than e2.5, then the surgeon would select LF on principle. When performing the posterior lumbar surgery for supplementation with BPS fixation, bilateral facet joints were removed.
Radiologic Analysis Radiologic outcomes were assessed by radiograph (neutral and dynamic standing films), CT scan, and magnetic resonance imaging preoperatively and 3 days, 3 months, 1 year, and 2 years postoperatively by the authors. The segments were divided into 4 groups: the SA, LF, UPS, and BPS groups. The DH was measured as the average of the anterior and posterior margins of the internal space on the standing films. The lumbar lordotic (LL) angle was measured as the Cobb angle formed between the superior end plate of L1 and the upper end plate of S1. The segmental lordotic (SL) angle was measured as the angle between the upper end plate
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of the upper vertebra and the lower end plate of the lower vertebra at the corresponding level. Subsidence was evaluated at each postoperative visit (3 days, 3 months, 1 year, and 2 years) using the classification described by Marchi et al.8 Subsidence was measured and classified into 4 grades based on the amount of cage subsidence into the vertebral end plates on the standing neutral lateral radiographs: grade 0 (0%e24%), grade I (25%e49%), grade II (50%e74%), and grade III (75%e100%, indicating collapse of the level). Grades 0 and I were considered low-grade subsidence, whereas grades II and III were considered high-grade subsidence. Fusion was defined as the presence of bridging trabecular bone.9 Clinical Assessment Preoperatively and at the last postoperative visit (2 years), a self-assessment of disability and pain was performed using the Japanese Orthopaedic Association (JOA) and visual analog scale
Table 5. Complications Group Parameter
SA
LF
UPS
BPS
P Value*
Psoas weakness
3
2
1
2
0.828
Psoas hematoma
0
1
0
0
0.480
Left thigh numbness
9
6
6
5
0.570
Revision
2
1
0
0
0.316
Values are number of patients or as otherwise indicated. SA, stand-alone; LF, lateral fixation; UPS, unilateral pedicle screw; BPS, bilateral pedicle screw. *Fisher exact test.
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ORIGINAL ARTICLE ENLIANG CHEN ET AL.
XLIF WITH AND WITHOUT FIXATION
Table 6. Radiographic Results Group Parameter
Time Point
SA
SL angle
Preoperative
11.97 5.99
3 days
13.61 6.35
3 months
13.47 6.07
0.015
14.34 1.48
0.009
13.02 5.62
0.001
12.81 8.41
0.003
1 year
13.49 6.35
0.005
13.94 1.57
0.040
12.85 6.09
0.022
12.59 8.97
0.009
0.015
13.88 1.56
0.044
12.79 6.31
0.043
12.33 8.68
0.027
LL angle
DH
2 years
13.56 6.64
Preoperative
33.99 11.94
3 days
34.97 11.30
P Value*
LF
P Value*
12.19 1.80 0.001
13.50 1.59
33.44 7.62
P Value*
11.41 5.48 0.049
30.89 8.17 0.010
UPS
12.43 5.85
32.98 1.25
P Value*
10.62 10.12 0.037
30.54 1.16 0.034
BPS
13.15 7.57
0.005
34.96 12.77 0.004
37.47 10.41
0.039
3 months
35.38 10.88
0.005
33.76 8.43
0.041
33.99 1.38
0.001
39.27 10.57
< 0.001
1 year
35.64 11.00
0.002
33.77 8.36
0.041
33.90 1.52
0.004
42.17 12.03
< 0.001
0.001
33.47 6.95
0.045
33.15 1.58
0.029
42.03 11.25
0.001
2 years
35.33 11.27
Preoperative
6.33 0.29
3 days
9.34 0.19
< 0.001
3 months
8.46 0.28
< 0.001
8.87 1.48
< 0.001
8.87 1.56
< 0.001
8.75 1.95
< 0.001
1 year
7.74 0.31
0.001
8.23 1.77
< 0.001
8.18 2.02
< 0.001
8.12 1.85
< 0.001
2 years
6.91 0.38
0.179
7.77 2.01
< 0.001
7.40 2.34
0.001
7.80 1.86
< 0.001
6.24 1.71 9.60 1.36
5.78 1.82 < 0.001
9.42 1.54
6.30 2.21 < 0.001
9.46 1.88
< 0.001
Values are mean SD or as otherwise indicated. SA, stand-alone; LF, lateral fixation; UPS, unilateral pedicle screw; BPS, bilateral pedicle screw; SL, segmental lordotic; LL, lumbar lordotic; DH, disk height. *Repeated-measures analysis of variance, comparison with baseline.
(VAS) scores for back/leg symptoms. Any complications and reoperations were also recorded at each time point (3 days, 3 months, 1 year, and 2 years). Statistical Analysis Statistical analysis was performed using SPSS v19 (IBM, Armonk, New York, USA). Continuous variables are shown as mean SD, and discrete variables are shown as frequency (%). One-way analysis of variance (ANOVA) was used to determine differences among the respective groups. Repeated-measures ANOVA was used to determine differences in the subsidence and LL and SL angles among the 4 groups. Fisher exact test was used to compare the frequency of events between groups. Paired-samples t tests were used to compare the clinical outcomes; P < 0.05 was considered statistically significant.
Surgical Data In the SA group, a single level was treated in 23 patients (85.19%), and 2 levels were treated in 4 patients (14.81%). In the LF group, a single level was treated in 30 patients (96.77%), and 2 levels were treated in 1 patient (3.23%). In the UPS group, a single level was treated in 19 patients (82.61%), 2 levels were treated in 3 patients (13.04%), and 3 levels were treated in 1 patient (4.35%). In the BPS
RESULTS Demographic Data Of the 107 patients, 37.38% (n ¼ 40) had lumbar disk herniation, 36.45% (n ¼ 39) had grade 1 or 2 spondylolisthesis, 22.43% (n ¼ 24) had lumbar spinal stenosis, and 3.74% (n ¼ 4) had a mild coronal curve (less than 15 ). The SA, LF, UPS, and BPS groups contained 27, 31, 23 and 26 patients, respectively (Figure 1). The indications for surgery in the 4 groups are shown in Table 1. Other demographic data are shown in Table 2.
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Figure 2. Graph showing the incidence rate of subsidence grade (0eIII) at each time point.
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XLIF WITH AND WITHOUT FIXATION
Table 7. Demographic, Radiologic, and Clinical Data in Different Subsidence Grades Group
Figure 3. Graph showing the incidence rate of subsidence per surgical group at 1-year follow-up. BPS, bilateral pedicle screw; LF, lateral fixation; SA, stand-alone; UPS, unilateral pedicle screw.
group, a single level was treated in 21 patients (80.77%), 2 levels were treated in 4 patients (15.38%), and 3 levels were treated in 1 patient (3.85%). The mean operative time and blood loss volume in the 4 groups are also shown in Table 2. A summary of the cage size is shown in Table 3, whereas the SL and LL correction values are shown in Table 4. Complications included psoas weakness, psoas hematoma, left thigh numbness, and revision (Table 5). Two patients in the SA group and 1 patient in the LF group required reoperation because of sustained lower extremity symptoms. Other postoperative events were transient and relieved in 1 year. Radiologic Outcomes A comparison of lordosis (segmental and global lumbar) and DH among the 4 groups is provided in Table 6. No significant differences in the preoperative LL angle, SL angle, or DH were found among the 4 groups. The SL and LL angles and DH significantly increased in all 4 groups after the operation. In the SA group, compared with the preoperative value, the DH was not significantly different at the last follow-up. However, the values of other measures at each follow-up visit were significantly different from the corresponding preoperative values. Although
Figure 4. Graph showing the incidence rate of subsidence per surgical group at 2-year follow-up. BPS, bilateral pedicle screw; LF, lateral fixation; SA, stand-alone; UPS, unilateral pedicle screw.
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Parameter
Low-Grade Subsidence
High-Grade Subsidence
Age (years)
59.72 10.77
65.30 12.03
0.030*
BMI (kg/m2)
23.86 2.11
25.15 2.26
0.009*
BMD
P Value
0.06 1.34
e1.83 1.04
< 0.001*
Female sex (%)
52.43
82.61
0.008y
Fusion at last follow-up (%)
75.73
86.96
0.242y
Values are mean SD or as otherwise indicated. BMI, body mass index; BMD, bone mineral density. *Independent-sample t test. yc2 test.
none of the surgical procedures significantly impacted the SL angle or DH, as determined by repeated-measures ANOVA (P ¼ 0.893 and P ¼ 0.746, respectively), a significant difference in the LL angle was observed in the BPS group compared with the other groups (P ¼ 0.006). The overall subsidence rate at each time point is shown in Figure 2. Comparing the 1- and 2-year rates, the pattern changed because 11.14% (n ¼ 14) of the levels showed increased subsidence. The 1- and 2-year subsidence rates in each group are shown in Figures 3 and 4. No relationship between the surgical procedure and subsidence rate was found (P ¼ 0.961). Marchi et al.8 defined 50% or more cage settling (grade II or III) as high-grade subsidence. In the present study, high-grade subsidence was found in 26.89% of all cases at the last follow-up. Demographic data of the patients exhibiting high- and lowgrade subsidence are shown in Table 7. The mean age, body mass index (BMI), and BMD and the proportion of women in the high-grade subsidence group was 65.30 12.03, 25.15 2.26, e1.83 1.04 and 82.61%, whereas the corresponding values in the low-grade subsidence group were 59.72 10.77 (P ¼ 0.030), 23.86 2.11 (P ¼ 0.009), 0.06 1.34 (P < 0.001), and 52.43% (P ¼ 0.008), respectively. The total fusion rate, confirmed on high definition CT coronal images, progressed from 47.62% at 3 months to 74.60% at 1 year and 85.71% at 2 years (Figure 5). The fusion status of each group is shown in Table 8. No relationship between fusion and fixation was found at any time point (3 months: P ¼ 0.436, 1 year: P ¼ 0.461, 2 years: P ¼ 0.987). At the last follow-up, solid fusion was considered to have occurred in 20 patients (86.96%) in the high-grade subsidence group and 78 patients (75.73%) in the low-grade subsidence group. Additionally, no relationship between fusion and subsidence was found at the 2-year follow-up (P ¼ 0.242). Clinical Outcomes The preoperative VAS and JOA scores of the 4 groups did not show significant differences (P ¼ 0.620 and P ¼ 0.480, respectively) (Table 2). At the last follow-up, the VAS and JOA scores of the 4
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2018.10.182
ORIGINAL ARTICLE ENLIANG CHEN ET AL.
XLIF WITH AND WITHOUT FIXATION
Figure 5. Coronal and sagittal computed tomography scan showing solid arthrodesis: (A and B) 32-month follow-up and (C and D) 40-month follow-up.
groups were significantly increased (Table 9). Because of the complex mix of diseases, we did not compare the clinical outcomes between the low- and high-grade subsidence groups.
DISCUSSION During this surgery, DH and sagittal alignment can be restored by implanting a large cage to achieve the goal of indirect decompression. Preservation of the back muscles, anterior and posterior longitudinal ligaments, and facet joints makes SA LF possible. However, indirect decompression may fail if cage subsidence occurs. Subsidence, a radiographic phenomenon that manifests as the intervertebral spacer sinking into the adjacent vertebral end plates, results in increased stenosis and sagittal malalignment and has the potential to cause adjacent-segment disturbances.8 However, the correlation between cage subsidence and clinical outcomes remains unclear. Choi and Sung10 and Pawar et al.11 found no relationship between cage subsidence and symptom recurrence or clinical outcome scores. Because of the complex mix of diseases in this study, we did not examine the relationship between subsidence and clinical outcomes. We think subsidence affects various diseases differently. Therefore, we focused on the radiologic data. The classification of subsidence introduced by Marchi et al.8 uses a percentage format to represent the sinking of the cage; this uniform scale makes the classification and reporting of subsidence more efficient and reliable. Overall, studies reporting the role played by fixation type in subsidence are rare. Beutler and Peppelman12 and Schiffman et al.13 reported that the incidence of subsidence was generally observed at the
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3-month follow-up and that no incident or increased subsidence occurred after the 1-year follow-up. In the current study, only 1 segment was confirmed to have high-grade subsidence at 3 days postoperatively. The overall subsidence rate gradually increased over 1 year, and no significant difference was found between the 1and 2-year follow-ups. These results are in accordance with those of previous studies. The subsidence rates in the SA and UPS groups were similar at the 1- and 2-year follow-ups and were greater than those in the LF and BPS groups. Pimenta et al.14 found that the range of motion of functional spinal units dissected from fresh-frozen human spines was the smallest in the cage alone group, followed by the UPS and BPS groups. Fogel et al.15 reported that the flexion-extension range
Table 8. Fusion Rate Group Parameter
SA
LF
UPS
BPS
P Value*
3 months
44.12
46.88
39.29
59.38
0.436
1 year
70.59
75
67.86
84.38
0.461
2 years
85.29
84.38
85.71
87.5
0.987
Values are percentages or as otherwise indicated. SA, stand-alone; LF, lateral fixation; UPS, unilateral pedicle screw; BPS, bilateral pedicle screw. *Fisher exact test.
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Table 9. Clinical Outcome Group Parameter
SA
LF
UPS
BPS
P Value*
Preoperative
6.03 1.24
6.34 1.15
6.04 1.07
6.28 1.28
0.620
Postoperativey
2.15 1.28
2.59 1.19
2.11 1.26
2.75 1.46
0.132
<0.001
<0.001
<0.001
<0.001
Preoperative
13.00 2.59
12.75 3.00
12.00 2.93
13.03 2.91
0.480
Postoperativey
18.41 2.74
19.16 3.60
18.93 4.47
18.16 3.47
0.667
<0.001
<0.001
<0.001
<0.001
VAS score
P valuez JOA score
P valuez
Values are mean SD or as otherwise indicated. SA, stand-alone; LF, lateral fixation; UPS, unilateral pedicle screw; BPS, bilateral pedicle screw; VAS, visual analog scale; JOA, Japanese Orthopaedic Association. *One-way analysis of variance. yAt the last follow-up. zPaired-samples t test.
of motion of the BPS group (2.1 0.8) was less than that of the UPS group (4.8 1.9), lateral plate group (6.6 2.1), and cage alone group (6.6 2.4). These results are mainly because of the different supporting forces afforded by the various types of interbody fixation. In this study, if the BMD T score of a patient was less than e2.5, then the surgeon would supplement with BPS fixation. Additionally, no significant differences were found in the preoperative age, BMI, BMD, or male-to-female ratio among the 4 groups. In other words, because patients with osteoporosis are more likely to develop subsidence, the subsidence rates found in this study are consistent with the findings of previous studies showing that the supporting forces provided by BPSs are greater than those provided by LF, followed by UPSs and a cage alone. Despite the diversity of the forces provided by the different fixation types, a relationship between fixation and subsidence was not found. Therefore, we think these 4 types of fixation can all maintain the DH and sagittal alignment well. At the last follow-up, the low- and high-grade groups showed significant differences in age, BMI, BMD, and the proportion of women, indicating that women, older patients, and patients with a higher BMI or lower BMD T score were more likely to develop subsidence. Therefore, these patients should be treated with solid interbody fixation, such as BPS fixation or LF. Although autologous bone grafting is still considered the gold standard in bony defect repair, harvesting iliac crest bone grafts is associated with chronic donor site pain, infections, fractures, and hematomas.16 Over the last century, significant advances have occurred in the development of valid alternatives to natural bone, such as allograft bone, demineralized bone matrix, ceramics, bone morphogenetic proteins, and bone marrow aspirate. However, none of these alternatives exhibit all the properties of an ideal spine graft material, including those required for osteoinduction, osteoconduction, and most importantly, osteogenesis. Pimenta et al.16 and Karikari et al.17
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reported a fusion rate of 100% after treating different thoracolumbar pathologies using rh-BMP2. However, because bone morphogenetic protein receptors are expressed by cancer cells, there is concern about the potential for cancer after treatment with rh-BMP2. Kim et al.18 found that with epithelialmesenchymal transition and/or changes in cancer stem cell markers, bone morphogenetic protein 2 treatment induced the signal transducer and activator of transcription 3-mediated induction of colon cancer cell metastasis. Voorneveld et al.19 found that the loss of SMAD4 from colorectal cancer cells causes bone morphogenetic protein signaling to switch from tumor suppressive to metastasis promoting. Furthermore, rh-BMP2 could lead to uncontrolled bone formation, osteolysis, inflammation, and neurologic injury. In contrast, allograft bone is less expensive and easier to obtain than autologous bone. It can be collected from either living donors (patients undergoing total hip replacement surgery) or nonliving donors and must be processed within a bone tissue bank. Donor bone is osteoconductive but weakly osteoinductive, whereas autologous bone marrow is osteoinductive. Therefore, we routinely use allograft bone mixed with autologous bone marrow extracted from the vertebral body as a bone graft substitute in patients undergoing XLIF because the autologous bone alone cannot meet the demands of the large XLIF cage. Our total fusion rate was relatively high, demonstrating that our approach of applying allograft bone mixed with autologous bone marrow is feasible and safe. If solid fusion does not occur or the forces provided by the instrumentation are insufficient, the relative motion between the upper and lower vertebral bodies is more likely to lead to cage subsidence. However, this study found no significant relationship between fusion and fixation type. Several reports studying lumbar and segmental lordosis have presented varying results. Alimi et al.20 reported that the lumbar sagittal lordosis of 145 operative levels increased by 5.3 postoperatively (P < 0.0001) and by 2.9 at the latest follow-
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ORIGINAL ARTICLE ENLIANG CHEN ET AL.
XLIF WITH AND WITHOUT FIXATION
up. Afathi et al.21 found that the LL angle did not significantly change after SA anterior lumbar interbody fusion or lateral lumbar interbody fusion for low-grade isthmic spondylolisthesis or degenerative disk disease, whereas the segmental lordosis significantly improved. Sembrano et al.22 reported that the LL angle did not significantly change when using a lordotic or nonlordotic cage, but the SL angle improved significantly only in the lordotic cage group. Furthermore, Jagannathan et al.23 found that the transforaminal lumbar interbody fusion procedure is highly effective for restoring lumbar lordosis and attributed the improvement in lumbar lordosis to 2 factors: 1) bilateral facetectomies, which permitted improved lordosis intraoperatively via a method analogous to a chevron osteotomy; and 2) the use of a larger interbody graft, which acted as a fulcrum at the junction of the anterior third and middle third of the vertebral body. Our study found that compared with the preoperative values, the LL angle was improved in all groups at each follow-up; however, only BPS
REFERENCES 1. Ozgur BM, Aryan HE, Pimenta L, Taylor WR. Extreme lateral interbody fusion (XLIF): a novel surgical technique for anterior lumbar interbody fusion. Spine J. 2006;6:435-443. 2. Malham GM, Ellis NJ, Parker RM, Seex KA. Clinical outcome and fusion rates after the first 30 extreme lateral interbody fusions. ScientificWorldJournal. 2012;2012:246989. 3. Satake K, Kanemura T, Yamaguchi H, Segi N, Ouchida J. Predisposing factors for intraoperative endplate injury of extreme lateral interbody fusion. Asian Spine J. 2016;10:907-914. 4. Lang G, Navarro-Ramirez R, Gandevia L, Hussain I, Nakhla J, Zubkov M, et al. Elimination of subsidence with 26-mm-wide cages in extreme lateral interbody fusion. World Neurosurg. 2017;104: 644-652. 5. Tohmeh AG, Khorsand D, Watson B, Zielinski X. Radiographical and clinical evaluation of extreme lateral interbody fusion: effects of cage size and instrumentation type with a minimum of 1-year follow-up. Spine (Phila Pa 1976). 2014;39: E1582-E1591. 6. Bocahut N, Audureau E, Poignard A, Poignard A, Delambre J, Queinnec S, Flouzat Lachaniette CH, et al. Incidence and impact of implant subsidence after stand-alone lateral lumbar interbody fusion. Orthop Traumatol Surg Res. 2018;104:405-410. 7. Kim SJ, Lee YS, Kim YB, Park SW, Hung VT. Direct lateral lumbar interbody fusion : clinical and radiological outcomes. J Korean Neurosurg Soc. 2014;11:145-151. 8. Marchi L, Abdala N, Oliveira L, Amaral R, Coutinho E, Pimenta L. Radiographic and clinical evaluation of cage subsidence after stand-alone lateral interbody fusion. J Neurosurg Spine. 2013;19:110-118. 9. Williams AL, Gornet MF, Burkus JK, Al E. CT evaluation of lumbar interbody fusion: current concepts. Am J Neuroradiol. 2005;1:2057-2066.
fixation had a significant impact on the LL angle. We think bilateral facetectomy and compression on the pedicle screws would significantly increase the LL angle in the BPS group. Regarding the SL angle, it was also improved in all groups and well maintained, but no relationship between fixation type and the SL angle was found. In other words, we think the lordotic cage has a greater impact on the SL angle and LL angle than the type of surgical fixation, and supplementation with BPS fixation greatly improves the LL angle. CONCLUSIONS From this study, it can be concluded that the type of surgical fixation did not significantly influence cage subsidence. Only supplemental BPS fixation could significantly improve the LL angle, and none of the surgical procedures significantly affected the SL angle. The 2-year fusion rate was satisfactory with the use of allograft bone mixed with autologous bone marrow.
10. Choi JY, Sung KH. Subsidence after anterior lumbar interbody fusion using paired stand-alone rectangular cages. Eur Spine J. 2006;15:16-22. 11. Pawar AY, Hughes AP, Sama AA, Girardi FP, Lebl DR, Cammisa FP. A comparative study of lateral lumbar interbody fusion and posterior lumbar interbody fusion in degenerative lumbar spondylolisthesis. Asian Spine J. 2015;9:668-674. 12. Beutler WJ, Peppelman WC. Anterior lumbar fusion with paired BAK standard and paired BAK proximity cages: subsidence incidence, subsidence factors, and clinical outcome. Spine J. 2003; 3:289-293. 13. Schiffman M, Brau SA, Henderson R, Gimmestad G. Bilateral implantation of low-profile interbody fusion cages: subsidence, lordosis, and fusion analysis. Spine J. 2003;3:377-387. 14. Pimenta L, Turner AWL, Dooley ZA, Parikh RD, Peterson MD. Biomechanics of lateral interbody spacers: going wider for going stiffer. ScientificWorldJournal. 2012;2012:381814.
promoting colon cancer stemness through STAT3 activation. Tumor Biol. 2015:9475-9486. 19. Voorneveld PW, Kodach LL, Jacobs RJ, Liv N, Zonnevylle AC, Hoogenboom JP, et al. Loss of SMAD4 alters BMP signaling to promote colorectal cancer cell metastasis via activation of rho and ROCK. Gastroenterology. 2014;147:196-208.e13. 20. Alimi M, Hofstetter CP, Guang-Ting Cong BS, Tsiouris AJ, James AR, Danika Paulo BS, et al. Radiological and clinical outcomes following extreme lateral interbody fusion. J Neurosurg Spine. 2014;20:623-635. 21. Afathi M, Zairi F, Devos P, Allaoui M, Marinho P, Chopin D, et al. Anterior lumbar sagittal alignment after anterior or lateral interbody fusion. Orthop Traumatol Surg Res. 2017;103:1245-1250. 22. Sembrano JN, Horazdovsky RD, Sharma AK, Yson SC, Santos ERG, Polly DW. Do lordotic cages provide better segmental lordosis versus nonlordotic cages in lateral lumbar interbody fusion (LLIF)? Clin Spine Surg. 2017;30:E338-E343.
15. Fogel GR, Turner AWL, Dooley ZA, Cornwall GB. Biomechanical stability of lateral interbody implants and supplemental fixation in a cadaveric degenerative spondylolisthesis model. Spine (Phila Pa 1976). 2014;39:E1138-E1146.
23. Jagannathan J, Sansur CA, Oksouian RJ Jr, Fu KM, Shaffrey CI. Radiographic restoration of lumbar alignment after trans foraminal lumbar interbody fusion. Neurosurgery. 2009;64:955-964.
16. Pimenta L, Marchi L, Oliveira L, Coutinho E, Amaral R. A prospective, randomized, controlled trial comparing radiographic and clinical outcomes between stand-alone lateral interbody lumbar fusion with either silicate calcium phosphate or rh-BMP2. J Neurol Surg A Cent Eur Neurosurg. 2013;74:343-350.
Conflict of interest statement: Foundation funds were provided by the National Natural Science Foundation of China (81672178).
17. Karikari IO, Nimjee SM, Hardin CA, Hughes BD, Hodges TR, Mehta AI, et al. Extreme lateral interbody fusion approach for isolated thoracic and thoracolumbar spine diseases: initial clinical experience and early outcomes. J Spinal Disord Tech. 2011;24:368-375.
Journal homepage: www.WORLDNEUROSURGERY.org
Received 14 August 2018; accepted 27 October 2018 Citation: World Neurosurg. (2018). https://doi.org/10.1016/j.wneu.2018.10.182
Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2018 Elsevier Inc. All rights reserved.
18. Kim BR, Oh SC, Lee D, Kim JL, Lee SY, Kang MH, et al. BMP-2 induces motility and invasiveness by
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Cage Subsidence and Fusion Rate in Extreme Lateral Interbody Fusion with and without Fixation Enliang Chen1,2, Junjie Xu1-3, Shanzhi Yang2,4, Qingshun Zhang2,3, Honglei Yi2,3, Daxuan Liang1,2, Sibin Lan5, Mingyang Duan4, Zenghui Wu1-3
-
OBJECTIVE: To examine the subsidence rate in patients undergoing extreme lateral interbody fusion (XLIF) using data from a 2-year retrospective study to assess the effect of supplemental fixation on the stand-alone procedure.
BPS group compared with the other groups. At the last follow-up, high-grade subsidence was found in 26.89% of all cases, the fusion rate was 85.71%, and the VAS and JOA scores were significantly improved in all groups.
METHODS: Demographic and perioperative data for all patients who underwent XLIF for degenerative lumbar disorders between June 2012 and January 2016 were collected and divided into 4 groups: the stand-alone (SA), lateral fixation, unilateral pedicle screw, and bilateral pedicle screw (BPS) groups. The disk height (DH), lumbar lordotic (LL) angle, and segmental lordotic (SL) angle were measured preoperatively and 3 days, 3 months, 1 year, and 2 years postoperatively. Clinical outcomes were evaluated using Japanese Orthopaedic Association (JOA) and visual analog scale (VAS) scores. Fusion was defined according to computed tomography scan.
-
-
RESULTS: There were 126 vertebrae in 107 patients treated. SL angle, LL angle, and DH significantly increased postoperatively in all groups. Although the preoperative and 2-year postoperative DHs in the SA group were similar, the other measures showed significant differences from baseline at each follow-up visit. No significant effects on SL angle or DH were found in any of the groups. A significant difference in the LL angle was found in the
-
Key words Cage subsidence - Fusion - Internal fixation - XLIF -
Abbreviations and Acronyms ANOVA: Analysis of variance BMD: Bone mineral density BMI: Body mass index BPS: Bilateral pedicle screw CT: Computed tomography DH: Disk height JOA: Japanese Orthopaedic Association LF: Lateral fixation LL: Lumbar lordotic rh-BMP2: Recombinant human bone morphogenetic protein 2 SA: Stand-alone SL: Segmental lordotic
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CONCLUSIONS: Supplemental fixation did not significantly influence cage subsidence or SL angle. Only BPS fixation significantly improved the LL angle. The 2-year fusion rate was satisfactory.
INTRODUCTION
S
ince Ozgur et al.1 first described extreme lateral interbody fusion (XLIF) in 2006, the technique has become a less invasive alternative to conventional anterior and posterior approaches for interbody fusion.2 XLIF has been practiced at the Guangzhou General Hospital of People's Liberation Army, China, since 2008. As a minimally disruptive approach for spinal fusion, XLIF has been widely used to treat degenerative lumbar disease, such as low-grade spondylolisthesis (grades 1 and 2), spinal stenosis, degenerative lumbar scoliosis, and multilevel degenerative disk disease. Using a transpsoas approach, which is made via a tubular retractor system, the disk height (DH) and sagittal alignment can be restored by implanting a large cage
UPS: Unilateral pedicle screw VAS: Visual analog scale XLIF: Extreme lateral interbody fusion From the 1Southern Medical University, Guangzhou; 2Department of Orthopedics, Guangzhou General Hospital of Guangzhou Military Command, Guangzhou; 3Institute of Traumatic Orthopaedics of People’s Liberation Army, Guangzhou; 4Guangzhou University of Traditional Chinese Medicine, Guangzhou, People’s Republic of China; and 5The Third Affiliated Hospital of Guangzhou University of Chinese Medicine, Guangzhou, People’s Republic of China To whom correspondence should be addressed: Zenghui Wu, M.D., Ph.D. [E-mail: [email protected]] Enliang Chen and Junjie Xu are coefirst authors. Citation: World Neurosurg. (2018). https://doi.org/10.1016/j.wneu.2018.10.182 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2018 Elsevier Inc. All rights reserved.
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XLIF WITH AND WITHOUT FIXATION
Figure 1. Postoperative radiographs of the 4 groups: (A and B) stand-alone group, (C and D) lateral fixation group, (E and F) unilateral pedicle screw group, and (G and H) bilateral pedicle screw group.
without disrupting the back muscles, anterior and posterior longitudinal ligaments, or facet joints. Therefore, XLIF has been widely accepted because of its advantages, including reduced tissue trauma and postoperative pain, shorter hospital stays, and quicker recovery. However, XLIF also has the potential to cause psoas disruption and lumbar plexus injury. Such cages could potentially fail to restore the DH or maintain the segmental lordosis because of cage subsidence.3 Currently, 2 mm of cage settlement into the vertebral body is considered cage subsidence.4,5 Bocahut et al.6 reported a cage subsidence rate of 32%, with subsidence defined as 4 mm of cage settlement into the vertebral body. Several reports have described cage subsidence after the XLIF procedure, with an incidence ranging from 9.5% to 22%.3,7,8 However, with the lack of uniform methods for assessing the extent of subsidence, interpreting or comparing the results of such studies is difficult.8 Regarding the implant graft, autologous bone can be replaced with many types of bone substitutes, such as allograft bone, demineralized bone matrix, ceramics, and recombinant human bone morphogenetic protein 2 (rh-BMP2). The question is
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whether these alternatives exhibit the characteristics of an ideal graft, including those characteristics required for osteoconduction, osteoinduction, or osteogenesis. Our implant grafts consist of allograft bone mixed with autologous bone marrow.
Table 1. Main Indication Parameter
SA
LF
UPS
BPS
Lumbar disk herniation
10
11
8
11
40
Grade 1 or 2 spondylolisthesis
10
10
8
11
39
Lumbar spinal stenosis
6
10
6
2
24
Degenerative scoliosis
1
0
1
2
4
Total
27
31
23
26
107
Values are number of patients. SA, stand-alone; LF, lateral fixation; UPS, unilateral pedicle screw; BPS, bilateral pedicle screw.
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XLIF WITH AND WITHOUT FIXATION
Table 2. Demographic, Clinical, and Surgical Data Group Parameter Number of levels Age (years) Male-to-female ratio BMI (kg/m2)
SA (n [ 27)
LF (n [ 31)
UPS (n [ 23)
BPS (n [ 26)
34
32
28
32
60.15 11.28
59.56 11.02
61.96 11.95
61.47 10.87
P Value
0.823*
19:15
16:16
9:19
9:23
0.067y
24.30 2.21
24.50 2.44
23.82 2.20
23.76 1.88
0.470*
e0.14 1.66
e0.38 1.30
e0.36 1.54
e0.29 1.45
0.909*
Preoperative VAS score
6.03 1.24
6.34 1.15
6.04 1.07
6.28 1.28
0.620*
Preoperative JOA score
13.00 2.59
12.75 3.00
12.00 2.93
13.03 2.91
0.480*
Preoperative SL angle
11.97 5.99
12.19 10.19
11.41 5.48
10.12 1.79
0.878*
Preoperative LL angle
32.68 10.66
31.40 8.40
30.05 9.86
37.50 10.34
0.104*
BMD
Preoperative DH
6.33 1.68
6.24 1.71
5.78 1.82
6.30 2.21
0.650*
Blood loss (mL)
37.16 8.15
43.75 15.14
81.79 15.71
102.03 37.80
< 0.001*
Surgery duration (minutes)
53.21 8.68
56.44 10.06
87.21 18.73
128.88 22.31
< 0.001*
Values are mean SD or as otherwise indicated. SA, stand-alone; LF, lateral fixation; UPS, unilateral pedicle screw; BPS, bilateral pedicle screw; BMI, body mass index; BMD, bone mineral density; VAS, visual analog scale; JOA, Japanese Orthopaedic Association; SL, segmental lordotic; LL, lumbar lordotic; DH, disk height. *One-way analysis of variance. yFisher exact test.
Therefore, the main goal of this study was to examine the subsidence rate after XLIF using data from a 2-year, retrospective, randomized study of the effects of supplemental lateral fixation (LF), unilateral pedicle screw (UPS) fixation, and bilateral pedicle screw (BPS) fixation on the stand-alone (SA) procedure. MATERIALS AND METHODS Patients and Indications This study examined 107 patients who underwent XLIF between June 2012 and January 2016. The indications for surgery were symptomatic single-level or multilevel lumbar degenerative disease from L1 to L5. Radiograph (anterior-posterior, lateral, flexion, and extension), computed tomography (CT) scan, and magnetic resonance imaging studies, and dual-energy x-ray absorptiometry studies to assess bone mineral density (BMD), were performed preoperatively for each patient. Postoperative data were collected at 3 days, 3 months, 1 year, and 2 years after the surgery. Surgical Techniques All procedures were performed by one spine surgeon with XLIF experience. Under general anesthesia, patients were placed in a true right lateral position, with the left hip and knee flexed. Adhesive plaster was used to appropriately fix the patient with the bed bent, therefore maximally extending the space between the iliac crest and lowest rib. Fluoroscopy was used to localize the index level. After a small incision was made across the target area, the surgeon reached the retroperitoneal space with a finger. Then, a blunt dilator was used to penetrate the psoas muscle. The target
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intervertebral disk area was located and exposed with a retractor, and diskectomy was performed. Autologous bone marrow was extracted from the vertebral body of the operated segment. Then, a polyetheretherketone cage filled with allograft bone and autologous bone marrow was implanted. The cancellous allograft bone was produced by Shanxi Aorui Biological Materials Co., Ltd., (Shanxi, People's Republic of China) using the Shanxi Medical
Table 3. Summary of Cage Size Variable
Number of Patients (%)
Cage width (number of levels) 18 mm
126 (100)
Cage height (number of levels) 8 mm
4 (3.17)
10 mm
54 (42.86)
12 mm
68 (53.97)
Cage length (number of levels) 45 mm
52 (41.27)
50 mm
63 (50.00)
55 mm
11 (8.73)
Cage lordotic angle (number of levels) 12
126 (100)
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Table 4. Segmental Lordotic and Lumbar Lordotic Correction Values Parameter
SA
LF
UPS
BPS
P Value*
Pre to post (3 days)
1.64 2.59
1.31 3.62
1.02 2.47
2.53 4.77
0.364
Pre to post (3 months)
1.51 3.41
2.16 4.37
1.61 2.22
2.18 3.88
0.815
P Valuey
SL
Pre to post (1 year)
1.53 2.96
1.75 4.63
1.44 3.16
0.948
1.96 3.98
Pre to post (2 years)
1.59 3.62
1.73 4.55
1.38 3.44
1.71 4.15
0.986
Pre to post (3 days)
2.25 3.49
2.55 3.38
2.44 3.67
2.50 7.89
0.043
Pre to post (3 months)
3.33 3.77
2.86 4.47
3.45 4.29
4.31 5.02
0.003
0.893
LL
Pre to post (1 year) Pre to post (2 years)
3.47 3.83 2.57 4.13
2.88 4.51 2.58 4.84
3.37 5.03 2.61 5.37
0.004
0.004
7.22 9.01 7.07 9.39
0.006
Values are mean SD or as otherwise indicated. SA, stand-alone; LF, lateral fixation; UPS, unilateral pedicle screw; BPS, bilateral pedicle screw; SL, segmental lordotic; Pre, preoperative; Post, postoperative; LL, lumbar lordotic. *P value comparison between the 4 surgical procedures at each time point. yP value the value of surgical procedures impacting the SL angle and LL angle.
Organization Database. The lateral dimension of the cage (40, 45, 50, or 55 mm) was determined preoperatively according to a measurement of the index level on lumbar CT scan, whereas the cage height (8, 10, or 12 mm) was determined intraoperatively by trials. All the cages were lordotic. In this study, dual-energy x-ray absorptiometry studies were performed preoperatively to assess the BMD, and neural and dynamic standing radiographic films were used to assess the position of the iliac crest in each patient. The surgeon decided to use different types of fixations according to the BMD, radiographs, and basic conditions of the patients. If the BMD T score of a patient was less than e2.5, then the surgeon would prefer to use BPSs for fixation. For L4-5 segments, even if the BMD was suitable for vertebral screw fixation, if the iliac crest obstructed supplementation with LF, then the surgeon would not choose LF. If a patient had both a high iliac crest and chronic disease, such as diabetes, cardiopathy, or hypertension, then the surgeon would prefer to use UPS fixation while not changing the true right lateral position of the patient. Finally, if the BMD T score of a patient was equal to or greater than e2.5, then the surgeon would select LF on principle. When performing the posterior lumbar surgery for supplementation with BPS fixation, bilateral facet joints were removed.
Radiologic Analysis Radiologic outcomes were assessed by radiograph (neutral and dynamic standing films), CT scan, and magnetic resonance imaging preoperatively and 3 days, 3 months, 1 year, and 2 years postoperatively by the authors. The segments were divided into 4 groups: the SA, LF, UPS, and BPS groups. The DH was measured as the average of the anterior and posterior margins of the internal space on the standing films. The lumbar lordotic (LL) angle was measured as the Cobb angle formed between the superior end plate of L1 and the upper end plate of S1. The segmental lordotic (SL) angle was measured as the angle between the upper end plate
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of the upper vertebra and the lower end plate of the lower vertebra at the corresponding level. Subsidence was evaluated at each postoperative visit (3 days, 3 months, 1 year, and 2 years) using the classification described by Marchi et al.8 Subsidence was measured and classified into 4 grades based on the amount of cage subsidence into the vertebral end plates on the standing neutral lateral radiographs: grade 0 (0%e24%), grade I (25%e49%), grade II (50%e74%), and grade III (75%e100%, indicating collapse of the level). Grades 0 and I were considered low-grade subsidence, whereas grades II and III were considered high-grade subsidence. Fusion was defined as the presence of bridging trabecular bone.9 Clinical Assessment Preoperatively and at the last postoperative visit (2 years), a self-assessment of disability and pain was performed using the Japanese Orthopaedic Association (JOA) and visual analog scale
Table 5. Complications Group Parameter
SA
LF
UPS
BPS
P Value*
Psoas weakness
3
2
1
2
0.828
Psoas hematoma
0
1
0
0
0.480
Left thigh numbness
9
6
6
5
0.570
Revision
2
1
0
0
0.316
Values are number of patients or as otherwise indicated. SA, stand-alone; LF, lateral fixation; UPS, unilateral pedicle screw; BPS, bilateral pedicle screw. *Fisher exact test.
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Table 6. Radiographic Results Group Parameter
Time Point
SA
SL angle
Preoperative
11.97 5.99
3 days
13.61 6.35
3 months
13.47 6.07
0.015
14.34 1.48
0.009
13.02 5.62
0.001
12.81 8.41
0.003
1 year
13.49 6.35
0.005
13.94 1.57
0.040
12.85 6.09
0.022
12.59 8.97
0.009
0.015
13.88 1.56
0.044
12.79 6.31
0.043
12.33 8.68
0.027
LL angle
DH
2 years
13.56 6.64
Preoperative
33.99 11.94
3 days
34.97 11.30
P Value*
LF
P Value*
12.19 1.80 0.001
13.50 1.59
33.44 7.62
P Value*
11.41 5.48 0.049
30.89 8.17 0.010
UPS
12.43 5.85
32.98 1.25
P Value*
10.62 10.12 0.037
30.54 1.16 0.034
BPS
13.15 7.57
0.005
34.96 12.77 0.004
37.47 10.41
0.039
3 months
35.38 10.88
0.005
33.76 8.43
0.041
33.99 1.38
0.001
39.27 10.57
< 0.001
1 year
35.64 11.00
0.002
33.77 8.36
0.041
33.90 1.52
0.004
42.17 12.03
< 0.001
0.001
33.47 6.95
0.045
33.15 1.58
0.029
42.03 11.25
0.001
2 years
35.33 11.27
Preoperative
6.33 0.29
3 days
9.34 0.19
< 0.001
3 months
8.46 0.28
< 0.001
8.87 1.48
< 0.001
8.87 1.56
< 0.001
8.75 1.95
< 0.001
1 year
7.74 0.31
0.001
8.23 1.77
< 0.001
8.18 2.02
< 0.001
8.12 1.85
< 0.001
2 years
6.91 0.38
0.179
7.77 2.01
< 0.001
7.40 2.34
0.001
7.80 1.86
< 0.001
6.24 1.71 9.60 1.36
5.78 1.82 < 0.001
9.42 1.54
6.30 2.21 < 0.001
9.46 1.88
< 0.001
Values are mean SD or as otherwise indicated. SA, stand-alone; LF, lateral fixation; UPS, unilateral pedicle screw; BPS, bilateral pedicle screw; SL, segmental lordotic; LL, lumbar lordotic; DH, disk height. *Repeated-measures analysis of variance, comparison with baseline.
(VAS) scores for back/leg symptoms. Any complications and reoperations were also recorded at each time point (3 days, 3 months, 1 year, and 2 years). Statistical Analysis Statistical analysis was performed using SPSS v19 (IBM, Armonk, New York, USA). Continuous variables are shown as mean SD, and discrete variables are shown as frequency (%). One-way analysis of variance (ANOVA) was used to determine differences among the respective groups. Repeated-measures ANOVA was used to determine differences in the subsidence and LL and SL angles among the 4 groups. Fisher exact test was used to compare the frequency of events between groups. Paired-samples t tests were used to compare the clinical outcomes; P < 0.05 was considered statistically significant.
Surgical Data In the SA group, a single level was treated in 23 patients (85.19%), and 2 levels were treated in 4 patients (14.81%). In the LF group, a single level was treated in 30 patients (96.77%), and 2 levels were treated in 1 patient (3.23%). In the UPS group, a single level was treated in 19 patients (82.61%), 2 levels were treated in 3 patients (13.04%), and 3 levels were treated in 1 patient (4.35%). In the BPS
RESULTS Demographic Data Of the 107 patients, 37.38% (n ¼ 40) had lumbar disk herniation, 36.45% (n ¼ 39) had grade 1 or 2 spondylolisthesis, 22.43% (n ¼ 24) had lumbar spinal stenosis, and 3.74% (n ¼ 4) had a mild coronal curve (less than 15 ). The SA, LF, UPS, and BPS groups contained 27, 31, 23 and 26 patients, respectively (Figure 1). The indications for surgery in the 4 groups are shown in Table 1. Other demographic data are shown in Table 2.
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Figure 2. Graph showing the incidence rate of subsidence grade (0eIII) at each time point.
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Table 7. Demographic, Radiologic, and Clinical Data in Different Subsidence Grades Group
Figure 3. Graph showing the incidence rate of subsidence per surgical group at 1-year follow-up. BPS, bilateral pedicle screw; LF, lateral fixation; SA, stand-alone; UPS, unilateral pedicle screw.
group, a single level was treated in 21 patients (80.77%), 2 levels were treated in 4 patients (15.38%), and 3 levels were treated in 1 patient (3.85%). The mean operative time and blood loss volume in the 4 groups are also shown in Table 2. A summary of the cage size is shown in Table 3, whereas the SL and LL correction values are shown in Table 4. Complications included psoas weakness, psoas hematoma, left thigh numbness, and revision (Table 5). Two patients in the SA group and 1 patient in the LF group required reoperation because of sustained lower extremity symptoms. Other postoperative events were transient and relieved in 1 year. Radiologic Outcomes A comparison of lordosis (segmental and global lumbar) and DH among the 4 groups is provided in Table 6. No significant differences in the preoperative LL angle, SL angle, or DH were found among the 4 groups. The SL and LL angles and DH significantly increased in all 4 groups after the operation. In the SA group, compared with the preoperative value, the DH was not significantly different at the last follow-up. However, the values of other measures at each follow-up visit were significantly different from the corresponding preoperative values. Although
Figure 4. Graph showing the incidence rate of subsidence per surgical group at 2-year follow-up. BPS, bilateral pedicle screw; LF, lateral fixation; SA, stand-alone; UPS, unilateral pedicle screw.
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Parameter
Low-Grade Subsidence
High-Grade Subsidence
Age (years)
59.72 10.77
65.30 12.03
0.030*
BMI (kg/m2)
23.86 2.11
25.15 2.26
0.009*
BMD
P Value
0.06 1.34
e1.83 1.04
< 0.001*
Female sex (%)
52.43
82.61
0.008y
Fusion at last follow-up (%)
75.73
86.96
0.242y
Values are mean SD or as otherwise indicated. BMI, body mass index; BMD, bone mineral density. *Independent-sample t test. yc2 test.
none of the surgical procedures significantly impacted the SL angle or DH, as determined by repeated-measures ANOVA (P ¼ 0.893 and P ¼ 0.746, respectively), a significant difference in the LL angle was observed in the BPS group compared with the other groups (P ¼ 0.006). The overall subsidence rate at each time point is shown in Figure 2. Comparing the 1- and 2-year rates, the pattern changed because 11.14% (n ¼ 14) of the levels showed increased subsidence. The 1- and 2-year subsidence rates in each group are shown in Figures 3 and 4. No relationship between the surgical procedure and subsidence rate was found (P ¼ 0.961). Marchi et al.8 defined 50% or more cage settling (grade II or III) as high-grade subsidence. In the present study, high-grade subsidence was found in 26.89% of all cases at the last follow-up. Demographic data of the patients exhibiting high- and lowgrade subsidence are shown in Table 7. The mean age, body mass index (BMI), and BMD and the proportion of women in the high-grade subsidence group was 65.30 12.03, 25.15 2.26, e1.83 1.04 and 82.61%, whereas the corresponding values in the low-grade subsidence group were 59.72 10.77 (P ¼ 0.030), 23.86 2.11 (P ¼ 0.009), 0.06 1.34 (P < 0.001), and 52.43% (P ¼ 0.008), respectively. The total fusion rate, confirmed on high definition CT coronal images, progressed from 47.62% at 3 months to 74.60% at 1 year and 85.71% at 2 years (Figure 5). The fusion status of each group is shown in Table 8. No relationship between fusion and fixation was found at any time point (3 months: P ¼ 0.436, 1 year: P ¼ 0.461, 2 years: P ¼ 0.987). At the last follow-up, solid fusion was considered to have occurred in 20 patients (86.96%) in the high-grade subsidence group and 78 patients (75.73%) in the low-grade subsidence group. Additionally, no relationship between fusion and subsidence was found at the 2-year follow-up (P ¼ 0.242). Clinical Outcomes The preoperative VAS and JOA scores of the 4 groups did not show significant differences (P ¼ 0.620 and P ¼ 0.480, respectively) (Table 2). At the last follow-up, the VAS and JOA scores of the 4
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XLIF WITH AND WITHOUT FIXATION
Figure 5. Coronal and sagittal computed tomography scan showing solid arthrodesis: (A and B) 32-month follow-up and (C and D) 40-month follow-up.
groups were significantly increased (Table 9). Because of the complex mix of diseases, we did not compare the clinical outcomes between the low- and high-grade subsidence groups.
DISCUSSION During this surgery, DH and sagittal alignment can be restored by implanting a large cage to achieve the goal of indirect decompression. Preservation of the back muscles, anterior and posterior longitudinal ligaments, and facet joints makes SA LF possible. However, indirect decompression may fail if cage subsidence occurs. Subsidence, a radiographic phenomenon that manifests as the intervertebral spacer sinking into the adjacent vertebral end plates, results in increased stenosis and sagittal malalignment and has the potential to cause adjacent-segment disturbances.8 However, the correlation between cage subsidence and clinical outcomes remains unclear. Choi and Sung10 and Pawar et al.11 found no relationship between cage subsidence and symptom recurrence or clinical outcome scores. Because of the complex mix of diseases in this study, we did not examine the relationship between subsidence and clinical outcomes. We think subsidence affects various diseases differently. Therefore, we focused on the radiologic data. The classification of subsidence introduced by Marchi et al.8 uses a percentage format to represent the sinking of the cage; this uniform scale makes the classification and reporting of subsidence more efficient and reliable. Overall, studies reporting the role played by fixation type in subsidence are rare. Beutler and Peppelman12 and Schiffman et al.13 reported that the incidence of subsidence was generally observed at the
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3-month follow-up and that no incident or increased subsidence occurred after the 1-year follow-up. In the current study, only 1 segment was confirmed to have high-grade subsidence at 3 days postoperatively. The overall subsidence rate gradually increased over 1 year, and no significant difference was found between the 1and 2-year follow-ups. These results are in accordance with those of previous studies. The subsidence rates in the SA and UPS groups were similar at the 1- and 2-year follow-ups and were greater than those in the LF and BPS groups. Pimenta et al.14 found that the range of motion of functional spinal units dissected from fresh-frozen human spines was the smallest in the cage alone group, followed by the UPS and BPS groups. Fogel et al.15 reported that the flexion-extension range
Table 8. Fusion Rate Group Parameter
SA
LF
UPS
BPS
P Value*
3 months
44.12
46.88
39.29
59.38
0.436
1 year
70.59
75
67.86
84.38
0.461
2 years
85.29
84.38
85.71
87.5
0.987
Values are percentages or as otherwise indicated. SA, stand-alone; LF, lateral fixation; UPS, unilateral pedicle screw; BPS, bilateral pedicle screw. *Fisher exact test.
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Table 9. Clinical Outcome Group Parameter
SA
LF
UPS
BPS
P Value*
Preoperative
6.03 1.24
6.34 1.15
6.04 1.07
6.28 1.28
0.620
Postoperativey
2.15 1.28
2.59 1.19
2.11 1.26
2.75 1.46
0.132
<0.001
<0.001
<0.001
<0.001
Preoperative
13.00 2.59
12.75 3.00
12.00 2.93
13.03 2.91
0.480
Postoperativey
18.41 2.74
19.16 3.60
18.93 4.47
18.16 3.47
0.667
<0.001
<0.001
<0.001
<0.001
VAS score
P valuez JOA score
P valuez
Values are mean SD or as otherwise indicated. SA, stand-alone; LF, lateral fixation; UPS, unilateral pedicle screw; BPS, bilateral pedicle screw; VAS, visual analog scale; JOA, Japanese Orthopaedic Association. *One-way analysis of variance. yAt the last follow-up. zPaired-samples t test.
of motion of the BPS group (2.1 0.8) was less than that of the UPS group (4.8 1.9), lateral plate group (6.6 2.1), and cage alone group (6.6 2.4). These results are mainly because of the different supporting forces afforded by the various types of interbody fixation. In this study, if the BMD T score of a patient was less than e2.5, then the surgeon would supplement with BPS fixation. Additionally, no significant differences were found in the preoperative age, BMI, BMD, or male-to-female ratio among the 4 groups. In other words, because patients with osteoporosis are more likely to develop subsidence, the subsidence rates found in this study are consistent with the findings of previous studies showing that the supporting forces provided by BPSs are greater than those provided by LF, followed by UPSs and a cage alone. Despite the diversity of the forces provided by the different fixation types, a relationship between fixation and subsidence was not found. Therefore, we think these 4 types of fixation can all maintain the DH and sagittal alignment well. At the last follow-up, the low- and high-grade groups showed significant differences in age, BMI, BMD, and the proportion of women, indicating that women, older patients, and patients with a higher BMI or lower BMD T score were more likely to develop subsidence. Therefore, these patients should be treated with solid interbody fixation, such as BPS fixation or LF. Although autologous bone grafting is still considered the gold standard in bony defect repair, harvesting iliac crest bone grafts is associated with chronic donor site pain, infections, fractures, and hematomas.16 Over the last century, significant advances have occurred in the development of valid alternatives to natural bone, such as allograft bone, demineralized bone matrix, ceramics, bone morphogenetic proteins, and bone marrow aspirate. However, none of these alternatives exhibit all the properties of an ideal spine graft material, including those required for osteoinduction, osteoconduction, and most importantly, osteogenesis. Pimenta et al.16 and Karikari et al.17
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reported a fusion rate of 100% after treating different thoracolumbar pathologies using rh-BMP2. However, because bone morphogenetic protein receptors are expressed by cancer cells, there is concern about the potential for cancer after treatment with rh-BMP2. Kim et al.18 found that with epithelialmesenchymal transition and/or changes in cancer stem cell markers, bone morphogenetic protein 2 treatment induced the signal transducer and activator of transcription 3-mediated induction of colon cancer cell metastasis. Voorneveld et al.19 found that the loss of SMAD4 from colorectal cancer cells causes bone morphogenetic protein signaling to switch from tumor suppressive to metastasis promoting. Furthermore, rh-BMP2 could lead to uncontrolled bone formation, osteolysis, inflammation, and neurologic injury. In contrast, allograft bone is less expensive and easier to obtain than autologous bone. It can be collected from either living donors (patients undergoing total hip replacement surgery) or nonliving donors and must be processed within a bone tissue bank. Donor bone is osteoconductive but weakly osteoinductive, whereas autologous bone marrow is osteoinductive. Therefore, we routinely use allograft bone mixed with autologous bone marrow extracted from the vertebral body as a bone graft substitute in patients undergoing XLIF because the autologous bone alone cannot meet the demands of the large XLIF cage. Our total fusion rate was relatively high, demonstrating that our approach of applying allograft bone mixed with autologous bone marrow is feasible and safe. If solid fusion does not occur or the forces provided by the instrumentation are insufficient, the relative motion between the upper and lower vertebral bodies is more likely to lead to cage subsidence. However, this study found no significant relationship between fusion and fixation type. Several reports studying lumbar and segmental lordosis have presented varying results. Alimi et al.20 reported that the lumbar sagittal lordosis of 145 operative levels increased by 5.3 postoperatively (P < 0.0001) and by 2.9 at the latest follow-
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2018.10.182
ORIGINAL ARTICLE ENLIANG CHEN ET AL.
XLIF WITH AND WITHOUT FIXATION
up. Afathi et al.21 found that the LL angle did not significantly change after SA anterior lumbar interbody fusion or lateral lumbar interbody fusion for low-grade isthmic spondylolisthesis or degenerative disk disease, whereas the segmental lordosis significantly improved. Sembrano et al.22 reported that the LL angle did not significantly change when using a lordotic or nonlordotic cage, but the SL angle improved significantly only in the lordotic cage group. Furthermore, Jagannathan et al.23 found that the transforaminal lumbar interbody fusion procedure is highly effective for restoring lumbar lordosis and attributed the improvement in lumbar lordosis to 2 factors: 1) bilateral facetectomies, which permitted improved lordosis intraoperatively via a method analogous to a chevron osteotomy; and 2) the use of a larger interbody graft, which acted as a fulcrum at the junction of the anterior third and middle third of the vertebral body. Our study found that compared with the preoperative values, the LL angle was improved in all groups at each follow-up; however, only BPS
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fixation had a significant impact on the LL angle. We think bilateral facetectomy and compression on the pedicle screws would significantly increase the LL angle in the BPS group. Regarding the SL angle, it was also improved in all groups and well maintained, but no relationship between fixation type and the SL angle was found. In other words, we think the lordotic cage has a greater impact on the SL angle and LL angle than the type of surgical fixation, and supplementation with BPS fixation greatly improves the LL angle. CONCLUSIONS From this study, it can be concluded that the type of surgical fixation did not significantly influence cage subsidence. Only supplemental BPS fixation could significantly improve the LL angle, and none of the surgical procedures significantly affected the SL angle. The 2-year fusion rate was satisfactory with the use of allograft bone mixed with autologous bone marrow.
10. Choi JY, Sung KH. Subsidence after anterior lumbar interbody fusion using paired stand-alone rectangular cages. Eur Spine J. 2006;15:16-22. 11. Pawar AY, Hughes AP, Sama AA, Girardi FP, Lebl DR, Cammisa FP. A comparative study of lateral lumbar interbody fusion and posterior lumbar interbody fusion in degenerative lumbar spondylolisthesis. Asian Spine J. 2015;9:668-674. 12. Beutler WJ, Peppelman WC. Anterior lumbar fusion with paired BAK standard and paired BAK proximity cages: subsidence incidence, subsidence factors, and clinical outcome. Spine J. 2003; 3:289-293. 13. Schiffman M, Brau SA, Henderson R, Gimmestad G. Bilateral implantation of low-profile interbody fusion cages: subsidence, lordosis, and fusion analysis. Spine J. 2003;3:377-387. 14. Pimenta L, Turner AWL, Dooley ZA, Parikh RD, Peterson MD. Biomechanics of lateral interbody spacers: going wider for going stiffer. ScientificWorldJournal. 2012;2012:381814.
promoting colon cancer stemness through STAT3 activation. Tumor Biol. 2015:9475-9486. 19. Voorneveld PW, Kodach LL, Jacobs RJ, Liv N, Zonnevylle AC, Hoogenboom JP, et al. Loss of SMAD4 alters BMP signaling to promote colorectal cancer cell metastasis via activation of rho and ROCK. Gastroenterology. 2014;147:196-208.e13. 20. Alimi M, Hofstetter CP, Guang-Ting Cong BS, Tsiouris AJ, James AR, Danika Paulo BS, et al. Radiological and clinical outcomes following extreme lateral interbody fusion. J Neurosurg Spine. 2014;20:623-635. 21. Afathi M, Zairi F, Devos P, Allaoui M, Marinho P, Chopin D, et al. Anterior lumbar sagittal alignment after anterior or lateral interbody fusion. Orthop Traumatol Surg Res. 2017;103:1245-1250. 22. Sembrano JN, Horazdovsky RD, Sharma AK, Yson SC, Santos ERG, Polly DW. Do lordotic cages provide better segmental lordosis versus nonlordotic cages in lateral lumbar interbody fusion (LLIF)? Clin Spine Surg. 2017;30:E338-E343.
15. Fogel GR, Turner AWL, Dooley ZA, Cornwall GB. Biomechanical stability of lateral interbody implants and supplemental fixation in a cadaveric degenerative spondylolisthesis model. Spine (Phila Pa 1976). 2014;39:E1138-E1146.
23. Jagannathan J, Sansur CA, Oksouian RJ Jr, Fu KM, Shaffrey CI. Radiographic restoration of lumbar alignment after trans foraminal lumbar interbody fusion. Neurosurgery. 2009;64:955-964.
16. Pimenta L, Marchi L, Oliveira L, Coutinho E, Amaral R. A prospective, randomized, controlled trial comparing radiographic and clinical outcomes between stand-alone lateral interbody lumbar fusion with either silicate calcium phosphate or rh-BMP2. J Neurol Surg A Cent Eur Neurosurg. 2013;74:343-350.
Conflict of interest statement: Foundation funds were provided by the National Natural Science Foundation of China (81672178).
17. Karikari IO, Nimjee SM, Hardin CA, Hughes BD, Hodges TR, Mehta AI, et al. Extreme lateral interbody fusion approach for isolated thoracic and thoracolumbar spine diseases: initial clinical experience and early outcomes. J Spinal Disord Tech. 2011;24:368-375.
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Received 14 August 2018; accepted 27 October 2018 Citation: World Neurosurg. (2018). https://doi.org/10.1016/j.wneu.2018.10.182
Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2018 Elsevier Inc. All rights reserved.
18. Kim BR, Oh SC, Lee D, Kim JL, Lee SY, Kang MH, et al. BMP-2 induces motility and invasiveness by
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