Study Design:
Prospective cross-sectional cohort study.
Objectives:
The main purpose of this study was to evaluate the association between demographical, surgery-related and morphologic parameters, and the development or progress of adjacent segment degeneration (ASD) after short-segment lumbar fusions.
Summary of Background Data:
ASD is a major long-term complication after lumbar fusions. Possible risk factors are related to the patients’ demographics, spinopelvic anatomy, or preoperative lumbar intervertebral disk conditions, but the role of these parameters is still not clear.
Methods:
A prospective cross-sectional study of 100 patients who underwent 1- or 2-level open lumbar transforaminal interbody fusions due to a lumbar degenerative pathology was conducted. Demographical, radiologic findings, and magnetic resonance imaging features were analyzed to identify factors associated with ASD in 5-year follow-up.
Results:
ASD patients showed higher level of pain (P=0.004) and disability (P=0.020) at follow-up. In univariate analysis, older age (P=0.007), upper-level lumbar fusion (P=0.007), lower L4-S1 lordosis (P=0.039), pelvic incidence-lumbar lordosis mismatch (P=0.021), Pfirrmann grade III or higher disk degeneration (P=0.002), and the presence of disk bulge/protrusion (P=0.007) were associated with ASD. In multivariate analysis, the presence of major degenerative sign (disk degeneration and/or disk bulge) was the significant predictor for developing ASD (odds ratio: 3.85, P=0.006).
Conclusion:
By examining the role of different patient- and procedure-specific factors, we found that preoperative major degenerative signs at the adjacent segment increase the risk of ASD causing significantly worse outcome after short-segment lumbar fusion. On the basis of our results, adjacent disk conditions should be considered carefully during surgical planning.
Key Words: ASD, disk degeneration, spinopelvic parameters, risk factors, major degenerative signs, short-segment lumbar fusions
Spinal fusion has become the most frequent surgical method in the treatment of degenerative spinal instability.1,2 Although lumbar fusion provides segmental stability, it can change the physiology and biomechanics of the adjacent segments by increasing motion and altering load in the adjacent facet joints and disks.3 It can result in the deterioration of anatomic structures and consequently disk height reduction, disk bulging/herniation, spinal canal stenosis, spondylolisthesis, and abnormal motion either in sagittal or in coronal plane may develop.4 The prevalence of adjacent segment degeneration (ASD), defined as morphologic deterioration on x-ray varies between 4.8% and 100%. The rate of ASD-related clinical symptoms and/or subsequent surgeries are between 0% and 30.3%.5–7
Many factors are reported in association with ASD including age, female sex, body mass index, change in lumbar and segmental lordosis, high pelvic incidence (PI), sagittal malalignment, preoperative disk degeneration, and length of fusion.8–17 Some authors also discussed the possible role of preoperative lumbar degenerative signs and the features of the index surgery.7,18 Despite the multifactorial nature of the condition, most studies have investigated only 1 or few risk factors. Long lumbar-, thoracolumbar surgeries were studied extensively; however, only a few paper investigated the risk factors of developing ASD after short-segment lumbar fusions, which is the most frequent procedure to surgically treat lumbar degenerative conditions. The current literature lacks of well-designed prospective studies focusing on the multidimensional nature of the condition.
The aim of this study was to evaluate the association between demographical, surgery-related and morphologic parameters, and ASD after short-segment lumbar fusions up to a 5-year follow-up period.
MATERIALS AND METHODS
One hundred patients over 18 years of age operated with lumbar degenerative (L1 to S1) condition between January and May 2015 were enrolled into to this prospective cross-sectional study at a tertiary care spine referral center. Excluded pathologies were trauma, tumor, infection, and congenital deformities. Index surgeries were 1- or 2-level open transforaminal lumbar interbody fusions. Study endpoint was defined as the time of the ASD-related subsequent surgery (mean follow-up time in this subgroup was 2.69±2.04 y) and/or up to 5-year follow-up period (mean follow-up time was 5.01±0.45 y in this subgroup). Indication for adjacent-level surgeries were analyzed in details and presented in supplementary material (Supplementary Table 1, Supplemental Digital Content 1, http://links.lww.com/CLINSPINE/A238).
The study was approved by the Scientific and Research Ethics Committee of the Medical Research Council. Manuscript was built according to STROBE statement for cohort studies.19
Data Collection
Demographical data were collected from electronic health records before the index operation. Surgery-related parameters were the length of fusion (single-, or 2 levels), inclusion of the sacrum and the level of stabilization. The surgery was considered as lower lumbar fusion if the top instrumented vertebra was L4 or caudal; all other cases considered as upper lumbar fusion. Preoperative radiologic data [x-ray and magnetic resonance imaging (MRI)] were collected within 3 months before the index surgery, postoperative data (x-ray) were collected within 5 days after the index surgery and at end of the follow-up (endpoint x-ray). Follow-up lumbar MRI was performed only for patients with subsequent surgery, to identify the source of pain and disability. Patient-reported outcome questionnaires were completed by each subject before the index surgery and at the endpoint. Validated version of Oswestry Disability Index was used to measure disability and Visual Analogue Scale to assess pain (low back and leg pain).
Definition of ASD
ASD was defined as a radiologic changes between postoperative and endpoint x-rays or/and the need for subsequent surgical procedure due to degenerative pathology in the spinal segment adjacent to the index fusion.20,21 Radiologic ASD was defined if at least one of the following was found on standing x-rays: (1) onset of segmental change (either kyphotic or lordotic) equal or >5 degrees, (2) decrease in disk height by 50%, (3) anteroposterior translation ≥3 mm.22,23
Radiologic Measurements
Radiologic measurements were performed in Surgimap software (Surgimap ver. 2.3.2., New York, NY). Data were obtained from standing anteroposterior and lateral lumbar x-rays before and after the index surgery and at study endpoint. Spinopelvic [PI, sacral slope, pelvic tilt (PT), lumbar lordosis (LL), and L4-S1 lordosis] and segmental parameters (segmental lordosis in adjacent segment, anterior and posterior disk height, and anteroposterior translation) were measured. Anteroposterior translation in adjacent segment was measured as the distance between the posterior wall of the 2-adjacent vertebral bodies, where the inferior vertebra is considered as fix point. Segmental lordosis in fusion site measured as the angle between the upper endplate of the most cranial vertebra and the lower endplate of the most caudal vertebra of the fusion. If the fusion involved the sacrum, the sacral plateau considered as the lower plane.
Detailed MRI analysis was performed to identify the signs of degeneration in adjacent intervertebral disks on preoperative MRIs. Five main phenotypes were studied: (1) Disk degeneration: MRI signal intensity, disk structure, and distinctions among the nucleus pulposus and annulus fibrosus were classified according to 5-grade Pfirrmann system.24 (2) Disk bulge/protrusion: presence of disk material displacement was classified as bulgeing/protrusion or herniation in adjacent segments according to Fardon et al.25 (3) Endplate damage: a trackable marker of disk degeneration process, classified based on its severity. The 6-type classification could distinguish between healthy (Type I), ageing (Type II–III), and degenerated (Type IV–VI) conditions.26 (4) Annular fissure: avulsions of annular fibers and fluid tracking thought that annulus fibrosus fissure presented as high signal intensity in T2-WI sequences.27 (5) Modic change: classification of degenerative bone marrow changes were performed according to Modic et al.28 In our statistical analysis all measured MRI parameters were dichotomized: Pfirrmann grade III or higher disk degeneration, presence of disk bulge/protrusion or herniation, Type II or higher endplate defect, presence of annular fissure and any Modic type degeneration were also considered as degenerative conditions.28,29
Finally, Pfirrmann grade III or higher disk degeneration and/or presence of disk bulge/protrusion or herniation were considered as major degenerative sign.
Statistical Analysis
Differences in spinopelvic x-ray measurements between ASD and Non-ASD groups were assessed by Student t tests for parametric variables and Mann-Whitney U test for nonparametric variables. Normality of data was determined by Shapiro-Wilk test. For categorical variables χ2 or Fisher exact tests were applied. Multiple logistic regression models were built to identify risk factors for ASD. Parameters that were not distributed equally across groups were selected for stepwise backward conditional method to extract the final model. Multicollinearity was evaluated by Pearson rank correlation (r>0.8). Statistical analysis was performed using SPSS software (IBM Corp. released 2016. IBM SPSS Statistics, Version 24.0. Armonk, NY). P values <0.05 were considered as significant.
RESULTS
A total of hundred patients were recruited into the study. Fifteen subjects were excluded from the final analysis due to incomplete dataset (n=12) or surgical site infection (n=3). Total of 85 subjects were included in the present analysis, of those 62 underwent single- and 23 underwent 2-level open transforaminal lumbar interbody fusion. On the basis of our ASD definition (detailed in methods section) 31 of the 85 patients (36.4%, 21 female and 10 male) developed ASD. The incidence of subsequent surgery was 17.6% (15/85), timing of subsequent surgery was ranging between 6 months to 4 years.
Demographics and Surgery-related Factors
Age was significantly higher in ASD group (47.1±11.6 vs. 54.2±10.4, P=0.007). ASD patients reported higher pain preoperatively (6.8±2.2 vs. 7.8±1.7, P=0.048) and at follow-up (4.6±2.9 vs. 6.5±2.5, P=0.004). On the basis of Oswestry Disability Index increased disability was found in ASD group compared to non-ASD group at the endpoint (27.0±20.3 vs. 38.3±21.8, P=0.020). In regards of surgery-related factors, upper-level lumbar fusion was more frequent in ASD group (6% vs. 26%, χ2=3.99, P=0.007) (Table 1).
TABLE 1.
Demographic Characteristics and Surgical Details in the Study Cohort
| Demographics | Non-ASD n=54 | ASD n=31 | P |
|---|---|---|---|
| Age, y (mean±SD) | 47.1±11.6 | 54.2±10.4 | 0.007 |
| Sex (M/F) | 19/35 | 10/21 | 0.784 |
| BMI, kg/m2(mean±SD) | 27.3±5.1 | 28.5±4.8 | 0.264 |
| Pain (preoperative) | 6.8±2.2 | 7.8±1.7 | 0.048 |
| ODI (preoperative) | 44.4±18.1 | 48.1±14.3 | 0.326 |
| Pain (FU) | 4.6±2.9 | 6.5±2.5 | 0.004 |
| ODI (FU) | 27.0±20.3 | 38.4±21.8 | 0.020 |
| Surgical details | |||
| Length of fusion (1/2-level, %) | 41/13 (76%/24%) | 20/11 (65%/35%) | 0.261 |
| Upper/lower lumbar fusion (upper/lower, %) | 3/51 (6%/94%) | 8/23(26%/74%) | 0.007 |
| Inclusion of sacrum (yes/no, %) | 33/21 (61%/39%) | 16/15(51%/49%) | 0.394 |
Bold values represent significant P values <0.05. ASD indicates adjacent segment degeneration; BMI, body mass index; FU, follow-up; ODI, Oswestry disability index.
MRI Phenotypes, Intervertebral Disk Characteristics
Pfirrmann grade III or higher disk degeneration at the adjacent level before the index surgery was more frequent in ASD group (24% vs. 51%, χ2=9.70, P=0.002). The presence of disk bulge/protrusion was 3 times higher in ASD patients (11% vs. 35%, χ2=7.31, P=0.007). Major degenerative signs (Pfirrmann grade III or higher disk degeneration and/or presence of disk bulge/protrusion or herniation) were more common in ASD cases (30% vs. 64%, χ2=9.81, P=0.002) (Table 2).
TABLE 2.
Distribution of Preoperative MRI Phenotypes
| MRI Phenotype | Non-ASD n=54, n (%) | ASD n=31, n (%) | P |
|---|---|---|---|
| Disk degeneration | 13 (24) | 16 (51) | 0.002 |
| Disk bulge/protrusion | 6 (11) | 11 (35) | 0.007 |
| Endplate damage | 43 (80) | 26 (84) | 0.630 |
| Annular fissure | 1 (2) | 1 (3) | 0.116 |
| Modic change | 22 (41) | 18 (58) | 0.124 |
| Major degenerative sign | 16 (30) | 20 (64) | 0.002 |
Bold values represent significant P values <0.05. Pfirrmann grade III or higher disk degeneration and/or presence of disk bulge/protrusion or herniation were considered as major degenerative sign.
ASD indicates adjacent segment degeneration; MRI, magnetic resonance imaging.
In subjects requiring a subsequent surgery, MRI findings in the adjacent segments before the second operation were the followings: all cases showed advanced disk degeneration, 7 cases developed moderate to severe spinal canal stenosis (7/15, 46.6%), 9 patients showed large disk protrusion (9/15, 60%), and 3 cases developed disk extrusion (3/15, 20%) (Supplementary Table 1, Supplemental Digital Content 1, http://links.lww.com/CLINSPINE/A238). Regarding the MRI findings before the index surgery, 11 patients out of 15 (73.3%) had major degenerative signs at the adjacent disk whereas only 4 patients had good adjacent disk conditions.
Spinopelvic Parameters
Preoperative L4-S1, PI-LL mismatch, and PT showed difference between ASD and non-ASD groups. L4-S1lordosis was significantly lower in ASD group (32.9±8.8 degrees vs. 29.0±7.3 degrees, P=0.039). PI-LL mismatch was greater in ASD patients (−2.3±9.7 degrees vs. 3.2±11.5 degrees, P=0.021). PT was higher in ASD group, which showed a trend to significant difference (14.4±7.5 degrees vs. 17.7±7.9 degrees, P=0.056) (Table 3A). In contrast, postoperative spinopelvic parameters showed no significant differences between groups (Table 3B). Significant differences in spinopelvic parameters have exceeded the minimally detectable change of these radiologic measurements calculated from the previous work of the authors.30 minimally detectable change proved to be 2.8 degrees for segmental lordosis, 2.5 degrees for PI, and 4.5 degrees for LL measurements.
TABLE 3.
Comparison of Preoperative (A) and Postoperative (B) Spinopelvic Parameters
| Preoperative X-ray | Non-ASD n=54 | ASD n=31 | P |
|---|---|---|---|
| A. Preoperative | |||
| Pelvic incidence (deg) | 52.9±11.6 | 56.9±12.5 | 0.141 |
| Sacral slope (deg) | 38.2±8.9 | 39.6±9.6 | 0.493 |
| Pelvic tilt (deg) | 14.4±7.5 | 17.7±7.9 | 0.056 |
| Lumbar lordosis (deg) | 55.2±12.4 | 53.7±13.0 | 0.601 |
| L4-S1 lordosis (deg) | 32.9±8.8 | 29.0±7.3 | 0.039 |
| Segmental lordosis in fusion site (deg) | 12.8±7.2 | 10.9±6.4 | 0.215 |
| PI-LL mismatch | −2.3±9.7 | 3.2±11.5 | 0.021 |
| B. Postoperative | |||
| Pelvic incidence (deg) | 52.4±11.9 | 56.7±12.4 | 0.122 |
| Sacral slope (deg) | 35.2±8.9 | 38.1±8.6 | 0.163 |
| Pelvic tilt (deg) | 17.2±6.9 | 18.9±7.8 | 0.309 |
| Lumbar lordosis (deg) | 48.2±12.6 | 51.5±10.9 | 0.218 |
| L4-S1 lordosis (deg) | 31.6±9.4 | 28.3±9.2 | 0.130 |
| Segmental lordosis in fusion site (deg) | 13.0±6.9 | 13.7±6.4 | 0.647 |
| PI-LL mismatch | 4.3±9.3 | 5.2±8.9 | 0.657 |
Bold values represent significant P values <0.05. ASD indicates adjacent segment degeneration.
Multiparametric Model for ASD
Parameters that were not distributed equally across groups were entered into the multiple logistic regression model: age, upper or lower lumbar fusion, preoperative L4-S1 lordosis, preoperative PI-LL mismatch and preoperative PT, and the presence of major degenerative sign on preoperative MRI. After application of stepwise backward conditional method, the presence of major degenerative sign remained a significant predictor of developing ASD with an odds ratio of 3.85 (confidence interval 95%=1.43–10.37, P=0.006).
DISCUSSION
Most common spinal fusion procedures (1- or 2-level lumbar fusions) were analyzed in terms of the development of ADS. We found that presence of major degenerative signs in the adjacent segment before the index surgery increased the risk of developing ASD after controlling for age, surgery-related factors, spinopelvic parameters, and preoperative MRI findings. The impact of preoperative disk degeneration in adjacent segments was discussed in previous studies.16,31,32 In agreement with our findings, some authors also reported that Pfirrmann grade III or higher severe disk degeneration and presence of disk bulge/protrusion in adjacent segment increased the risk of developing ASD.8,20,31 Altered biomechanics in adjacent segments may have more profound effect on disks with higher grade degeneration and predispose patients to clinically significant ASD. In line with this observation, every patient who underwent subsequent surgery presented with severe degenerative changes and disk displacements on MRI and higher pain and disability on Patient-reported outcome questionnaires scores.
Aging is a reliable factor of disk degeneration, although being a slow process.29 In our study age was not an independent predictor of developing ASD, possibly due to the relative short follow-up period.
The current literature is controversial about the impact of instrumentation length and level of fusion as a risk factors leading to ASD.18,33,34 Patients with upper-level lumbar fusions more frequently developed ASD. The reason might be the difference in range of motions in lumbar segments. As Cook et al35 described, the range of motions of L1-L3 segments are less flexible and more rigid compared with lower segments. In upper lumbar fusions rigidity limits segmental compensatory mechanisms in adjacent segments and can lead to disk degeneration.
As a compensation, pelvic retroversion led to higher PT to maintain balance. Although higher PT can lead to increased pain and disability, PT was not proved to be a risk factor of ASD in the final model,36 supporting the current literature findings.18
The LL and its distribution are one of the main components in lumbar spine stabilization surgeries. Optimal distribution of L4-S1 lordosis was previously discussed by Yilgor at al.37 However, its role, it has never studied before in the development of ASD. Improper distribution of lordosis has a significant consequence on sagittal alignment and can influence the local biomechanics too.37 Preoperative L4-S1 lordosis was significantly lower in ASD group, but it was not a predictor of developing ASD in our multivariate regression model.
In current study LL and PI were not different between groups; however, only ASD patients showed moderate PI-LL mismatch preoperatively according to original classification by Schwab et al.38 The moderate mismatch combined with mild increase in PT could be reason of higher preoperative pain in ASD patients.39
Our study has some limitations, that should be taken into consideration. First, the relatively low number of participants in our homogenous study group could limit our analysis. In line with it, we could not analyze radiologic and clinical ASD separately due the low number of patients in subgroups. Second, only lumbar spine x-rays were carried out due to technical reasons, so we were not able to calculate global sagittal balance. One of the strengths of our work is the “multidimensional” analysis. A number of patient- and procedure specific data was collected and multivariable models were built to find the most important risk factors. Our radiologic analysis was also detailed, clear, and reproducible focusing not only on measurements of spinopelvic parameters and spinal motion segments but also on degenerative MRI phenotypes analysis, including Pfirrmann grade, disk bulge/protrusion, endplate defects, annular fissures, and Modic changes. According to our knowledge, this is the first paper considering the role of endplate defects, annular fissures, and Modic changes in ASD. However, the relatively low number of cases limit our analysis, but the clear methodology could support and aid further studies.
CONCLUSION
Despite the multitude of studies published, the causes of ASD are not understood completely and the literature is incomplete in multiparametric analysis on the most common—1- or 2-level—lumbar fusion patient-group. The role of spinopelvic parameters and other factors that influence, induce, or trigger changes in the adjacent mobile segments are not clear. We found that preoperative major degenerative sign was a strong, independent predictor of developing ASD. Consequently, adjacent disk conditions should be carefully analyzed during surgical planning. If major degenerative signs are present, the inclusion of the segment into the index fusion is considerable.
Supplementary Material
Footnotes
This manuscript was previously posted to Research Square: doi: 10.21203/rs.3.rs-898513/v1.
The study was approved by the National Institute of Pharmacy and Nutrition (Reference Number: OGYÉI/163-4/2019).
The project leading to the scientific results was supported by the Hungarian Scientific Research Fund Grant Budapest, Hungary (Award Number: OTKA FK123884).
The authors declare no conflict of interest.
Supplemental Digital Content is available for this article. Direct URL citations appear in the printed text and are provided in the HTML and PDF versions of this article on the journal's website, www.jspinaldisorders.com.
Contributor Information
Laszlo Kiss, Email: laszlo.kiss@bhc.hu.
Zsolt Szoverfi, Email: zsolt.szoverfi@bhc.hu.
Ferenc Bereczki, Email: ferenc.bereczki@bhc.hu.
Peter Endre Eltes, Email: peter.eltes@bhc.hu.
Balazs Szollosi, Email: balazs.szollosi@bhc.hu.
Julia Szita, Email: julia.szita@bhc.hu.
Zoltan Hoffer, Email: zoltan.hoffer@bhc.hu.
Aron Lazary, Email: aron.lazary@bhc.hu.
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Associated Data
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