Predicting factors of adjacent segment degeneration after long-segment spinal fusion: spinopelvic parameters analysis

Purpose We investigated whether spinopelvic parameters are important prognostic factors for adjacent segment degeneration after long instrumented spinal fusion for degenerative spinal disease. Methods This uncontrolled, randomized, single arm retrospective study included patients who underwent long instrumented lumbar fusion (fusion levels≥ 4) in the past 5 years with follow-up for at least 2 years. The inclusion criteria included adult patients (≥40 years of age) with a diagnosis of spinal degeneration who underwent instrumented corrective surgery. The exclusion criteria included preexisting adjacent disc degeneration, combined anterior reconstructive surgery, and distal ASD. Clinical and operative characters were evaluated. Lumbar lordotic angle (LLA), sacral slope angle (SSA), pelvic tilt angle (PTA) and pelvic incidence angle (PIA) were compared preoperatively, postoperatively and at the final follow-up. Results From 2009 to 2014, 60 patients (30 ASD and 30 non-ASD patients) were enrolled. The average age was 66.82 ± 7.48 years for the study group and 67.97 ± 7.81 years for the control group. There was no statistically significant difference in clinical and operative characteristics. Among all spinopelvic parameters, only pre-, post-operative and final follow-up PIA in ASD group (53.9±10.4, 54.6±14.0, 54.3±14.1) and non-ASD group (60.3±13.0, 61.8±11.3, 62.5±11.2) showed statistically significant differences (p<0.05). Conclusion This study confirms that preoperative, postoperative and final follow-up PIA is a significant factor contributing to the development of adjacent segment degeneration after long instrumented spinal fusion.


Introduction
Decompression and long segmental instrumented fusion are mainstay treatments for adult degenerative scoliosis patients who need a full correction of deformity [1]. The major long-term concern for long segmental spinal fusion is adjacent segment degeneration (ASD). Various studies have proposed risk factors for ASD for short segmental fusion, including the aging process, scarifying posterior ligament complex or overdecompression during surgery and poor sagittal balance after lumbar fusion [2][3]. Sagittal plane imbalance on reconstructive spine surgery has become popular and is an increasingly recognized cause of postoperative back pain [4][5][6][7]. The key concept is that normal sagittal alignment helps individuals remain in a stable posture with less energy consumption.
The fused spine of a locked position may cause a loss of lumbar lordosis, a forward shift of the upper trunk [12][13][14] and subsequent adjacent degeneration.
Various spinopelvic parameters have been proposed to evaluate sagittal balance, including pelvic incidence angle (PIA) [16], sacral slope angle (SSA) [15], and pelvic tilt angle (PTA) [17]. These parameters are common measurements used to assess the morphology of the pelvis with adequate intraobserver and interobserver reliability [18]. The most commonly used parameter is pelvic incidence (PI), which is defined as the angle between the line perpendicular to the sacral endplate at its midpoint and the line connecting the middle axis of the bilateral femoral head to the midpoint, and PI is calculated as the algebraic sum of the SSA and the PTA. Boulay et al. demonstrated excellent the intraobserver and interobserver reliability of these measurements [19]. The C7 plumb line is another measurement useful in evaluating sagittal balance [20][21][22]. The horizontal distance between the posterosuperior corner of the sacrum and the plumb line drawn from the center of the C7 vertebra (C7 plumb line) is recorded, and the sagittal balance is indicated by the distance [22][23][24]. The relations between ASD and the spinopelvic parameters of short segmental fusion have been studied [1,2,4,14]. Postoperative flat back, including decreased lumbar lordotic angle (LLA), SSA and increased PTA, may have a negative impact on the adjacent segment [4].
To our knowledge, no existing research has addressed the effect of spinopelvic parameters on proximal ASD of long segmental spinal fusion. Our study is the first retrospective controlled study to determine whether spinopelvic and associated parameters are important prognostic factors for proximal ASD after long segmental spinal fusion.

Materials And Methods
This study is a controlled, open-labeled, randomized, single center retrospective study. From August 2009 to July 2014, 5575 patients with degenerative lumbar scoliosis underwent surgery at our institution. The Chang Gung Medical Foundation Institutional Review Board approved this study (201600408B0) and waived the requirement for informed consent due to the retrospective nature of this study. The inclusion criteria included fusion levels≥4 and adult patients (≥40 years of age) with a diagnosis of spinal degeneration who underwent instrumented corrective surgery. The exclusion criteria included preexisting disc degeneration,spondylolisthesis or junctional kyphoscoliosis of the proximal adjacent segment, combined anterior reconstructive surgery, distal ASD and proximal adjacent level vertebral compression fracture.
Thirty ASD and 30 non-ASD patients were included with a minimal follow-up of 2 years. Pairwise, retrospective, case-control matching was performed between these two groups. Thirty patients from the ASD group were randomly selected as the study group. Another computer-generated thirty patients from the non-ASD group with potential matching criteria, including similar diagnosis, pathological levels (≤ 1 level difference), sex and age were included as the control group.
Clinical characteristics, including sex, age, duration of follow-up and the preoperative and postoperative Oswestry Disability Index (ODI) [14], were assessed. Operative data, including the number of levels fused and upper instrumented vertebrae (UIV) above T12, were also evaluated.

Radiographic evaluation
The investigator measured the LLA, SSA, PTA, and PIA preoperatively, postoperatively and at the final follow-up. Radiographic ASD was defined as follows: 1. adjacent segment spondylolisthesis≥4 mm, 2. adjacent segmental kyphosis≥10°, 3. complete collapse of adjacent disc space (Figure)

Statistical analysis
A statistical software program (SPSS for Windows, version 12.0; SPSS Inc., Chicago, IL) was used to analyze the preoperative and postoperative parameters in both groups. All data are presented as the mean ± standard deviation. The differences between the study and control groups in spinopelvic parameters and lumbar lordosis were evaluated using Fisher's exact test and the Mann-Whitney U test. We compared the clinical and spinopelvic parameters at the preoperative, postoperative, and follow-up periods. The statistical significance for all tests was set at a p value of less than 0.05.

Results
The clinical and operative characteristics of both groups are shown in Table 1. A total of 60 patients were analyzed in this study (53 females and 7 males), of which the 30 patients who developed ASD during follow-up were included in the study group and the other 30 patients were included in the control group. The average age was 66.82 ± 7.48 years for the study group and 67.97 ± 7.81 years for the control group. All patients received clinical and radiographic follow-up for a minimum of 24 months, with an average follow-up of 48 ±22 months in the ASD group and 52 ±26 months in the non-ASD group. No statistically significant differences were detected with respect to age, sex, followup period, mean pre-and postoperative ODI, number of levels fused and UIV above T12.
The details of these radiographic spinopelvic parameters are listed in Table 2 Table 3. There was no statistically significant difference in other parameters between the groups. The value of corrected PIA was less than 5 degrees, which was in the range of interobserver mistakes.

Discussion
The most common long-term complication of adult degenerative scoliosis patients who receive corrective surgery is ASD. According to previous studies, the reasons and risk factors for ASD after long segmental spinal surgery remain controversial. Some reports have indicated that aging and mechanical and biomechanical changes in the fused segment were risk factors [14,25,26], but unrandomized controlled patient characteristics, preoperative surgical data, and mixed short and long segmental spinal fusions generated doubtful results.
Whether the possibility of ASD increases as more motion segments are included in spinal fusion remains unclear. Dehnokhalaji et al. [27] found that the length of fusion was not significant in developing ASD, but only the distal intervertebral disc was discussed. Bassani et al. [28] proposed that patients with single-level fusions were more likely to have clinical ASD than those with multilevel fusions [29]. Gillet et al. included patients with 5 or more fusion levels and found that the risk of ASD was not increased [30]. However, in our studies, no significant difference in the number of fusion levels suggested that the adjacent degeneration was not affected by the fusion levels.
The rib cage provides a stabilizing effect and may balance the detrimental effect of long-level fusion in the development of ASD. These findings may be attributed to the bracing effect of the rib cage.
Thus, the recommended length of fusion should be extended to the thoracic area when treating patients with ASD proximal to a prior fusion [30]. In our study, extending the fusion level to the thoracic spine did not increase the risk of ASD (p>0.05); thus, "rib cage protection" had no effect because sagittal alignment has a more profound influence than structural anatomical protection.
PI is a morphological parameter that plays a key role in the regulation of positional pelvic and spinal factors [14,31]. The potential for variations in spinal curves is associated with variations in pelvic positional parameters. For the same PI, SS and PT can vary, with the following relation among them: PI (morphological) = SS (positional) + PT (positional) [14]. PI creates different lordosis values to allow conditions conducive to standing posture and gait, according to the principle of biomechanical economy [14]. In contrast, we found that lower PIA patients may be a contributing factor to the development of ASD after long spinal fusion (Table 2). Many studies [32][33][34][35][36][37][38] have focused on how to correct the sagittal profile, including increased LLA, reduced normal C7 plumb line and PTA, but our results show that there was no significant significant difference between the incidence of ASD with preoperative and postoperative spinopelvic parameters, except for PIA. The PI, or pelvic base angle, is a useful descriptive terminology and an extremely important parameter for determining the global spinal balance of an individual [39,40]. The PI thus determines the relative position of the sacral plate with respect to the femoral head and the amount of lumbar lordosis required to maintain an erect posture [39][40][41][42]. In summary, higher PIA was always accompanied by higher LLA due to higher SSA, which decreased the adjacent segment facet pressure and reduced the energetic consumption of erect muscle. The accepted postoperative sagittal profile did not indicate proper preservation of an erect back muscle. One study [43] found significant geometrical reductions of erector spinae by approximately 26 and 14% at the L5-S1 and L4-L5 levels, respectively, after posterior lumbar surgery.
Another study [44] found that fusion generated a 12% reduction in the total multifidus muscle force during erect standing, and 10.5% reductions were produced during 20° flexion In our study, muscle weakness may be one of the major causes of adjacent level degeneration.
Although the PIA is an anatomical indicator of sagittal balance and is simple to estimate, the correlation between the PIA and ASD has not been determined. Our study revealed that the lower The Chang Gung Medical Foundation Institutional Review Board approved this study (201600408B0) and waived the requirement for informed consent due to the retrospective nature of this study.

Availability of data and materials
The data supporting the findings of this study are available from Chang Gung Memorial Hospital, but restrictions apply to the availability of these data, which were used under license for the current study, and so are not publicly available. However, the data are available from the corresponding author upon reasonable request and with permission from Chang Gung Memorial Hospital.  All data are given as the mean ± SD unless otherwise indicated.
*Statistical significance was defined as p<0.05.

Supplementary Files
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