Abstract
Study Design
Retrospective observational study.
Purpose
To comprehensively evaluate skeletal-muscle characteristics in patients with degenerative spondylolisthesis (DS), clarify the association between sarcopenia and DS, and determine the impact of sarcopenia on surgical outcomes.
Overview of Literature
In lumbar spinal stenosis (LSS), factors such as spinal alignment, facet-joint orientation, and trunk muscle atrophy and fatty degeneration contribute to DS development. However, the role of sarcopenia in surgical outcomes in DS remains unclear.
Methods
A cross-sectional analysis of 1,415 patients with LSS and L4–L5 stenosis (mean age 75.2±8.7 years; 703 males and 712 females) was performed to identify factors associated with Meyerding grade I or greater spondylolisthesis using sex-adjusted analysis of covariance and logistic regression. A longitudinal analysis of 373 patients who underwent surgery for LSS (mean age, 72.1±8.8 years; 200 males and 173 females) was conducted using the Asian Working Group for Sarcopenia algorithm to evaluate the effect of sarcopenia on 1-year postoperative outcomes.
Results
Logistic regression analysis identified female sex, greater lumbar lordosis, lower skeletal-muscle mass index, smaller lumbar-multifidus (LM) cross-sectional area, smaller facet-joint angle, disc degeneration, smaller L4–L5 dural-sac area, and low flavum-canal ratio as significant variables associated with DS. No significant differences in the surgical outcomes were observed in LSS patients with and without DS, and no significant intergroup differences were noted in limb skeletal-muscle mass. However, both LM and erector spinae exhibited significantly more postoperative decreases in the DS group than in the non-DS group. No significant differences in skeletal-muscle mass change or surgical outcomes were observed according to sarcopenia status among DS patients.
Conclusions
Sarcopenia is associated with DS, trunk muscle atrophy, and fatty degeneration. However, surgical treatment of patients with DS and sarcopenia yields favorable clinical outcomes because adequate decompression and stabilization may mitigate the impact of reduced skeletal-muscle mass.
Keywords: Spondylolisthesis, Lumbar spinal stenosis, Sarcopenia, Multifidus, Surgery
Graphical Abstract
Introduction
Lumbar spinal stenosis (LSS) is characterized by low back pain, leg pain, and/or numbness that impairs ambulation owing to compression of the nerve roots and cauda equina by the disc, facet joint, and supporting structures, including the ligamentum flavum. Degenerative spondylolisthesis (DS), a common cause of LSS, results from vertical shear forces between adjacent vertebrae and frequently leads to symptomatic spinal stenosis requiring surgical treatment. Surgical management has been shown to provide substantially greater improvement in pain and function than nonsurgical treatment [1]. The optimal surgical treatment for DS remains controversial, particularly regarding the choice between decompression alone and decompression combined with fusion. Fusion surgery is often performed because it can restore the spinal mechanical stability and prevent further vertebral slippage; however, its higher complication risk and cost of fusion must be weighed against its potential clinical benefits, and the indications for fusion in patients with concomitant spondylolisthesis remain uncertain [2]. Therefore, preventing slippage is crucial, and many studies have identified the risk factors for DS development. A 2023 review identified several factors contributing to DS development, including anatomical characteristics that predispose to vertebral slippage, such as facet-joint sagittalization, pelvic tilt (PT), pelvic incidence, sacral slope (SS), and lumbar lordosis (LL), as well as demographic factors such as advanced age, female sex, higher body mass index (BMI), and ethnicity [3]. However, preventive measures targeting these age-related spinal factors at disease onset primarily rely on lifestyle modifications and early initiation of physical therapy, which may be difficult to implement in clinical practice.
Recently, increasing attention has been directed toward sarcopenia [4], the age-related decline in skeletal-muscle mass and function, highlighting the need for therapeutic strategies targeting skeletal muscle in geriatric medicine. Although anatomical factors contributing to degeneration of the intervertebral discs and facet joints are considered the primary basis for DS onset, the surrounding skeletal muscles (particularly the paraspinal muscles) also play a critical role in maintaining spinal stability. Previous studies have reported atrophy and fatty infiltration of the multifidus muscle in patients with DS [5,6]. As the multifidus is a deep muscle essential for segmental spinal stability, it is plausible that its functional decline contributes to instability, thereby promoting the development or progression of vertebral slippage. However, limited evidence exists regarding whether atrophy and fatty degeneration of the trunk muscles, including those affecting the multifidus muscle, share the same etiology as age-related generalized skeletal-muscle loss or instead represent a distinct form of spine-specific sarcopenia [7]. Given the unclear relationship between generalized sarcopenia and paraspinal muscle atrophy, along with insufficient previous research reports, it is essential to evaluate them separately because of the differing characteristics of these skeletal-muscle groups. Furthermore, despite ongoing debate regarding whether DS should be considered a sarcopenia-related disease, analysis using established global criteria for sarcopenia is necessary; however, few studies have investigated this question using these criteria, although some have assessed skeletal-muscle mass using the skeletal-muscle mass index (SMI). Clarifying the impact of generalized sarcopenia on DS and its surgical outcomes is therefore important for managing patients with LSS.
This study employed cross-sectional and longitudinal analyses to evaluate the skeletal muscle in patients with DS among individuals undergoing treatment for LSS, clarify the association between sarcopenia and DS, and determine the impact of sarcopenia, a systemic age-related condition, on surgical outcomes.
Materials and Methods
Ethics statement
The observational study protocol was approved by the National Center for Geriatrics and Gerontology Ethics Committee (approval number: 1102) and was conducted in accordance with the principles of the Declaration of Helsinki. All participants were informed of the study objectives and provided written informed consent.
Participants
This single-center retrospective study analyzed prospectively collected data from patients who underwent treatment for LSS, including DS, between 2013 and 2023. Among 1,704 patients diagnosed with LSS during the study period, 1,415 with L4–L5 stenosis (mean age, 75.2±8.7 years; 703 males, 712 females) were included in the analysis. LSS diagnosis was based on neurogenic claudication, regardless of low back pain, and was confirmed by two board-certified spine surgeons in Japan using magnetic resonance imaging (MRI) findings and neurological examination. Patients with a history of LS surgery or systemic diseases, including rheumatoid arthritis, infections, malignant tumors, or dementia, and those who could not provide patient-reported outcomes were excluded.
Questionnaires
Pain intensity was evaluated using a Visual Analog Scale (VAS; 0–10 mm) for both lower back pain and leg pain. Activities of daily living (ADLs) were evaluated using the Roland Morris Disability Questionnaire (RDQ; 0–24 points) [8] and the European Quality of Life-5 Dimensions (EQ-5D; 0–1) questionnaire [9]. The RDQ assesses disability related to low back pain, whereas the EQ-5D, the most widely used generic patient-reported outcome measure, assesses health-related quality of life. Locomotive function status was assessed using the Locomo-25 score (0–100), a self-administered questionnaire including four questions on pain, 16 on ADLs, three on social function, and two on mental health, all referring to the preceding month [10]; higher scores indicate poorer locomotive function.
Physical function
Muscle strength was assessed using grip, lower-extremity, and back extension strength. Grip strength was measured in each hand using a Jamar-type dynamometer (SH5001; Sakai Medical Co. Ltd., Tokyo, Japan); the average value on both sides was considered for the analysis. Back muscle strength was evaluated as the maximum isometric strength of the trunk muscles in a sitting posture with 30° lumbar extension using a digital muscle strength meter (Isoforce GT-300, 310; OG GIKEN Co. Ltd., Okayama, Japan). Quadriceps femoris strength was measured for each leg using a handheld dynamometer (#Tas F-1; Anima Co. Ltd., Tokyo, Japan) with the hips and knees flexed at 90° in the initial posture; the average value of both sides was used for analysis. Mobility was objectively assessed using the Timed Up and Go test [11], which measures the time required to rise from a chair, walk 3 m, turn, return, and sit down for dynamic balance evaluation. Gait speed (m/sec) was measured over a 10-m distance at the usual walking pace. The participants were provided with an additional 3-m acceleration phase before the test distance and a 3-m deceleration phase afterward. Two trials were performed, and the faster gait speed (m/sec) was used for analysis.
Blood-sample analysis
Venous blood samples were collected before LSS treatment using standard venipuncture techniques. We analyzed complete blood cell counts, albumin, creatine phosphokinase, hemoglobin A1c, C-reactive protein, estimated glomerular filtration rate, and vitamin D (25-hydroxyvitamin D [25(OH)D]) levels in peripheral blood. Serum 25(OH)D levels were measured using an electrochemiluminescence immunoassay.
Radiographic findings
Whole-spine radiographs were obtained with participants standing naturally with their forearms crossed over their chest. The following parameters were measured on standing lateral whole-spine radiographs: scoliosis Cobb angle (L1–S1), LL (L1–S1), SS, lumbar range of motion (L1–S1), sagittal vertical axis, thoracic kyphosis, PT, and pelvic incidence minus LL. Spondylolisthesis was defined as vertebral slippage of Meyerding grade I or more [12]. We compared clinical symptoms, imaging findings, body composition, and blood test results between patients with and without DS.
MRI findings
To evaluate paraspinal muscle morphology, cross-sectional areas of the bilateral lumbar-multifidus (LM) and erector spinae (ES) muscles were measured at the L4–L5 level. The facet-joint angle is defined as the angle between the facet-joint and planum medianum of the vertebrae [13], was measured bilaterally, and the average value was used for analysis. For LM fatty degeneration, the classification by Kjaer et al. [14] was applied to T1-weighted axial MR images, with grade I or higher considered indicative of fatty degeneration. Intervertebral disc degeneration was graded on T2-weighted midsagittal MRI using the Pfirrmann classification, and grade IV or higher was defined as disc degeneration [15]. Stenosis severity was assessed by measuring the dural canal area at the L4–L5 level. Ligamentum flavum hypertrophy was evaluated using the flavum-canal ratio (FCR) [16], which was obtained by dividing the combined area of the ligamentum flavum on both sides at the L4–L5 level by the L4–L5 spinal canal area. All CSA measurements were made using image analysis software (SYNAPSE; Fujifilm Medical, Tokyo, Japan).
Body composition analysis
Body composition was assessed using dual-energy X-ray absorptiometry (DXA) (Lunar iDXA; GE Healthcare, Chicago, IL, USA). Bone mineral density (g/cm2) was measured at the lumbar vertebrae (L2–4). Appendicular muscle mass was determined from the upper and lower extremities, and the SMI was calculated as appendicular muscle mass divided by height squared. Sarcopenia was diagnosed according to the Asian Working Group for Sarcopenia (AWGS) 2019 algorithm, which incorporates muscle strength, appendicular skeletal-muscle mass, and physical performance [17]. Body fat percentage was calculated as the total body fat mass divided by body weight.
Surgical outcome
Among the 1,415 enrolled patients with LSS, the relationship between DS and postoperative outcomes was examined in 373 patients (mean age, 72.1±8.8 years; 200 males, 173 females) who underwent surgical treatment and had complete 1-year follow-up data (Fig. 1). We compared the VAS scores for low back and leg pain, as well as the RDQ and EQ-5D scores, before surgery and 1 year later in patients with and without DS. To evaluate changes in skeletal-muscle mass, we compared preoperative and postoperative limb skeletal-muscle mass measured by DXA and CSAs of the multifidus and ES muscles at the L4–L5 level on MRI.
Fig. 1.
Schematic diagram for the enrollment of patients with lumbar spinal stenosis (LSS) and their 1-year postoperative follow-up. This study comprised a cross-sectional analysis of 1,415 cases involving surgical and conservative treatments for degenerative spondylolisthesis and a longitudinal analysis of 373 patients who underwent surgical treatment for degenerative spondylolisthesis.
Statistical analysis
Power analyses were conducted using G*Power ver. 3.1.9.2 (Heinrich-Heine-Universität, Düsseldorf, Germany). We employed z tests for logistic regression with two-sided testing, odds ratio=1.3, Pr (Y=1| X=1) H0=0.2, α error probability=0.01, power (1–β error probability)=0.9, R2 other X=0, with X following a normal distribution, x parm μ=0, and x parm σ=1. The minimum required sample size was 1,365.
Statistical analyses were performed using EZR software (Saitama Medical Center, Jichi Medical University, Saitama, Japan). Proportions and means with standard deviations were calculated for demographic and clinical variables. Categorical variables were expressed as frequencies or percentages. Chi-square or Fisher’s exact tests were used to evaluate differences in categorical variables, whereas mean values were compared using sex-adjusted analysis of covariance (ANCOVA). A p-value <0.05 was considered statistically significant. For multivariate analysis, logistic regression was performed to identify risk factors for spondylolisthesis; explanatory variables with p<0.05 in the comparison between patients with and without spondylolisthesis were considered. Multicollinearity was assessed using variance inflation factors (VIFs), with a VIF of >5 considered indicative of multicollinearity.
Repeated-measures analysis of variance was used to compare preoperative and postoperative outcomes based on the presence or absence of spondylolisthesis.
Results
Cross-sectional analysis for DS
Among the 1,415 registered patients with LSS, 610 (43.1%) had DS and 805 did not. DS was more prevalent in females. Therefore, in comparisons between the DS and non-DS groups, continuous variables were analyzed using sex-adjusted ANCOVA, whereas nominal variables were analyzed separately for males and females. Comparisons of the clinical and radiographic findings between the two groups is presented in Table 1. In the DS group, sex-adjusted two-group comparisons demonstrated significantly higher EQ-5D scores. However, SMI was significantly lower, lumbar spinal cord CSA exhibited atrophy, and back muscle strength was significantly reduced. The FCR at the L4–L5 level was significantly lower in the DS group. No significant differences in sarcopenia, as defined by the AWGS criteria, were observed between the two groups. Regarding spinal alignment, the DS group demonstrated significantly greater LL and SS values. Comparison of MRI findings revealed significantly smaller facet-joint angles, more severe disc degeneration according to the Pfirrmann classification, and a significantly reduced dural canal area at the L4–L5 level in the DS group.
Table 1.
Comparison between the spondylolisthesis and non-spondylolisthesis groups
| Variable | Spondylolisthesis (+) (n=610) | Spondylolisthesis (−) (n=805) | 95% CI | p-valuea) | Effect size |
|---|---|---|---|---|---|
| Age (yr) | 75.82±8.26 | 74.69±9.03 | 0.210 to 2.044 | 0.6667 | 0.13 |
| Female | 67.87 | 37.02 | NA | <0.0001 | NA |
| Body mass index (kg/cm2) | 24.51±3.69 | 24.41±3.52 | −0.285 to 0.473 | 0.0838 | 0.03 |
| Diabetes mellitus | |||||
| Male | 21.43 | 19.01 | NA | 0.2490 | NA |
| Female | 13.29 | 18.00 | NA | 0.0920 | NA |
| ASCVD | |||||
| Male | 22.96 | 19.21 | NA | 0.4110 | NA |
| Female | 18.12 | 18.33 | NA | 0.9999 | NA |
| Affected periods (day) | 196.97±356.66 | 200.91±410.34 | −45.697 to 37.811 | 0.8519 | 0.01 |
| VAS (LBP) | 5.33±2.99 | 5.07±3.02 | −0.057 to 0.589 | 0.4182 | 0.09 |
| VAS (leg pain) | 6.61±2.72 | 6.34±2.85 | −0.035 to 0.567 | 0.5925 | 0.10 |
| RDQ | 12.68±5.47 | 12.58±5.76 | −0.809 to 0.404 | 0.1122 | 0.02 |
| EQ5D | 0.55±0.15 | 0.54±0.17 | −0.007 to 0.028 | 0.0194 | 0.06 |
| Locomo-25 score | 39.51±19.66 | 40.32±20.61 | −4.049 to 2.426 | 0.0893 | 0.04 |
| Grip power (kg) | 21.78±8.48 | 26.91±9.41 | −6.590 to −3.681 | 0.6380 | 0.57 |
| Back muscle strength (N) | 113.78±47.82 | 131.04±50.38 | −22.565 to −11.949 | 0.0316 | 0.35 |
| QF strength (N) | 23.60±11.94 | 26.54±14.22 | −5.273 to −0.614 | 0.1675 | 0.22 |
| TUG (sec) | 10.80±3.89 | 10.78±4.93 | −0.746 to 0.780 | 0.5133 | 0.00 |
| Gait speed (m/sec) | 1.78±1.88 | 1.31±2.34 | 0.120 to 0.828 | 0.0585 | 0.22 |
| Hemoglobin (g/dL) | 12.79±1.59 | 13.37±1.66 | −0.747 to −0.402 | 0.1827 | 0.36 |
| Albumin (g/dL) | 4.11±0.39 | 4.11±0.41 | −0.047 to 0.038 | 0.7453 | 0.00 |
| CPK (U/L) | 138.37±173.05 | 133.23±163.97 | −12.548 to 22.834 | 0.5685 | 0.03 |
| HbA1c (%) | 6.06±0.67 | 6.12±0.81 | −0.141 to 0.017 | 0.1767 | 0.06 |
| CRP (mg/dL) | 0.22±0.66 | 0.30±1.11 | −0.180 to 0.019 | 0.2743 | 0.08 |
| eGFR (mL/min/1.73 m2) | 65.55±17.94 | 66.92±19.21 | −3.342 to 0.592 | 0.3322 | 0.07 |
| 25(OH)D (ng/mL) | 17.75±8.11 | 20.00±8.89 | −3.281 to −1.220 | 0.2495 | 0.26 |
| Scoliotic angle (°) | 6.59±6.29 | 6.19±6.76 | −0.284 to 1.098 | 0.2495 | 0.06 |
| LL (°) | 32.36±12.63 | 27.87±13.15 | 3.125 to 5.850 | 0.0392 | 0.35 |
| SS (°) | 26.57±8.78 | 23.86±9.11 | 1.768 to 3.656 | <0.0001 | 0.30 |
| L-ROM (°) | 27.24±10.31 | 27.71±11.18 | −1.615 to 0.664 | 0.7276 | 0.04 |
| SVA (mm) | 68.39±45.85 | 68.32±44.60 | −5.000 to 5.173 | 0.8952 | 0.00 |
| TK (°) | 34.56±10.76 | 34.64±11.94 | −1.363 to 1.218 | 0.4567 | 0.01 |
| PT (°) | 25.19±10.28 | 22.86±9.95 | 1.189 to 3.470 | 0.2080 | 0.23 |
| PI–LL | 19.52±14.89 | 18.90±13.84 | −0.999 to 2.238 | 0.6545 | 0.04 |
| LM CSA (mm2) | 688.75±353.20 | 875.06±370.84 | −224.572 to −148.051 | <0.0001 | 0.51 |
| ES CSA (mm2) | 1,572.78±594.08 | 1,658.62±567.77 | −359.004 to −185.317 | 0.1899 | 0.15 |
| Facet joint angle (°) | 41.34±9.84 | 44.93±12.03 | −4.762 to −2.414 | <0.0001 | 0.32 |
| LM fat infiltration | 71.97 | 60.87 | NA | <0.0001 | NA |
| Disc degeneration | |||||
| Male | 84.18 | 76.04 | NA | 0.0189 | NA |
| Female | 87.68 | 78.00 | NA | 0.0007 | NA |
| Dural sac CSA (mm2) | 100.91±54.97 | 114.42±57.35 | −19.489 to −7.534 | 0.0010 | 0.24 |
| L4/5 FCR | 0.41±0.21 | 0.44±0.22 | −0.048 to −0.003 | 0.0377 | 0.14 |
| L-spine BMD (g/cm2) | 1.14±0.25 | 1.22±0.30 | −0.116 to −0.058 | 0.8851 | 0.29 |
| SMI (kg/m2) | 6.46±1.03 | 6.70±1.05 | −0.351 to −0.131 | 0.0133 | 0.23 |
| Sarcopenia (AWGS) | |||||
| Male | 36.60 | 44.71 | NA | 0.0598 | NA |
| Female | 20.82 | 25.08 | NA | 0.2040 | NA |
| Body fat ratio (%) | 34.55±8.29 | 31.88±7.97 | 1.816 to 3.527 | 0.0229 | 0.33 |
Values are presented as mean±standard deviation, %, or 95% CI unless otherwise stated.
CI, confidence interval; NA, not applicable; ASCVD, atherosclerotic cardiovascular disease; VAS, Visual Analog Scale; LBP, low back pain; RDQ, Roland Morris Disability Questionnaire; EQ5D, European Quality of life-5 Dimensions; QF, quadriceps femoris; TUG, Timed Up and Go Test; CPK, creatine phosphokinase; HbA1c, hemoglobin A1c; eGFR, estimated glomerular filtration rate; 25(OH)D, 25-hydroxyvitamin D; LL, lumbar lordosis; SS, sacral slope; L-ROM, lumbar range of motion; SVA, sagittal vertical axis; TK, thoracic kyphosis; PT, pelvic tilt; PI–LL, pelvic incident minus lumbar lordosis; LM, lumbar multifidus; ES, erector spinae; CSA, cross sectional area; FCR, flavum canal ratio; BMD, bone mineral density; SMI, skeletal-muscle mass index; AGWS, Asian working group for sarcopenia.
Sex-adjusted analysis of covariance.
Logistic regression analysis with stepwise variable selection based on the Akaike information criterion (AIC), including explanatory variables with p-values <0.05 in the two-group comparison according to DS status, identified female sex, high LL, low SMI, smaller multifidus muscle area, smaller facet-joint angle, disc degeneration, lower L4–L5 dural canal area, and low FCR as significant factors associated with DS (AIC=1,483.70) (Table 2).
Table 2.
Logistic regression analysis for spondylolisthesis
| Variable | Regression coefficient | SE | p-value | OR (95% CI) | VIF |
|---|---|---|---|---|---|
| Age | 0.009 | 0.009 | 0.3045 | 1.010 (0.992–1.430) | 1.432 |
| Sex (female) | −1.018 | 0.191 | <0.0001 | 0.361 (0.249–0.526) | 2.227 |
| EQ5D | −0.501 | 0.421 | 0.2346 | 0.606 (0.265–1.380) | 1.601 |
| Back muscle strength | 0.002 | 0.002 | 0.2163 | 1.000 (0.999–1.010) | 1.738 |
| LL | −0.030 | 0.008 | 0.0003 | 0.971 (0.956–0.986) | 1.297 |
| SS | −0.013 | 0.011 | 0.2346 | 0.987 (0.965–1.010) | 2.602 |
| LM CSA | 0.001 | 0.002 | <0.0001 | 1.000 (1.001–1.002) | 2.524 |
| Facet joint angle | 0.036 | 0.007 | <0.0001 | 1.040 (1.020–1.050) | 1.068 |
| Disc degeneration (+) | −0.753 | 0.174 | <0.0001 | 0.471 (0.335–0.562) | 1.086 |
| LM fat infiltration | 0.262 | 0.155 | 0.0918 | 1.300 (0.958–1.760) | 1.057 |
| Dural sac CSA | 0.007 | 0.002 | 0.0002 | 1.010 (1.000–1.010) | 2.000 |
| L4/5 FCR | 1.536 | 0.501 | 0.0021 | 4.690 (1.763–12.476) | 2.621 |
| SMI | −0.179 | 0.079 | 0.0233 | 0.836 (0.717–0.976) | 2.841 |
| Body fat ratio | −0.004 | 0.009 | 0.6777 | 0.996 (0.979–1.010) | 1.350 |
Akaike information criterion=1,488.17.
SE, standard error; OR, odds ratio; CI, confidence interval; VIF, variance inflation factor; EQ5D, European Quality of life-5 Dimensions; LL, lumbar lordosis; SS, sacral slope; LM, lumbar multifidus; CSA, cross-sectional area; FCR, flavum canal ratio; SMI, skeletal muscle mass index.
Longitudinal analysis of surgical patients with LSS
Among the 1,415 registered patients with LSS, 373 of the 595 surgically treated patients completed the 1-year follow-up and underwent repeat imaging evaluation. We investigated whether postoperative changes in skeletal-muscle mass differed according to the presence of DS. Surgical procedures included posterior lumbar interbody fusion (PLIF) in 171 patients and decompression of the stenotic segment in 201. In the DS group, PLIF was performed in 89.6% of cases, whereas decompression surgery was performed in 81.7% of cases in the non-DS group. Table 3 presents the changes in pain, ADL scores, and body composition before and after surgery. Clinical outcomes assessed using the VAS, RDQ, and EQ5D demonstrated favorable postoperative results in both the DS and non-DS groups, with no significant differences in the magnitude of improvement between the two groups. Moreover, no significant changes in appendicular muscle mass were observed between the groups. However, LM and ES measurements revealed a significant postoperative decrease in the DS group (LM: p=0.0176; ES: p<0.0001). Comparing postoperative outcomes between 110 cases with sarcopenia according to the AWGS criteria and 263 cases without sarcopenia, the sarcopenia group was significantly older and had a higher proportion of males (p<0.0001). PLIF was performed in 38.2% of patients in the sarcopenia group, with no significant difference compared with the non-sarcopenia group. Clinical outcomes were favorable in both groups, with no significant between-group differences. Although a significant postoperative decrease in appendicular skeletal-muscle mass was observed in the sarcopenia group (p=0.0371), no significant difference in postoperative trunk muscle atrophy was noted compared with the non-sarcopenia group (Table 4).
Table 3.
Comparison of operative outcomes between the spondylolisthesis and non-spondylolisthesis groups
| Variable | Spondylolisthesis (+) (n=144) | Spondylolisthesis (−) (n=229) | 95% CI | p-valuea) | Effect size | p-valueb) |
|---|---|---|---|---|---|---|
| Age (yr) | 72.59±7.79 | 71.78±9.40 | −1.030 to 2.656 | 0.3863 | 0.09 | NA |
| Female | 63.19 | 35.81 | NA | <0.0001 | NA | NA |
| PLIF | 89.58 | 18.34 | NA | <0.0001 | NA | NA |
| VAS (LBP) | 0.8641 | |||||
| Baseline | 4.93±2.87 | 5.04±3.06 | −0.739 to 0.517 | 0.7379 | 0.04 | |
| Postop | 2.30±2.68 | 2.52±2.80 | −0.797 to 0.354 | 0.1147 | 0.08 | |
| VAS (leg pain) | 0.0764 | |||||
| Baseline | 6.55±2.50 | 6.15±2.90 | −0.180 to 0.978 | 0.1766 | 0.15 | |
| Postop | 2.57±2.94 | 2.88±3.16 | −0.955 to 0.332 | 0.3414 | 0.10 | |
| RDQ | 0.6915 | |||||
| Baseline | 12.32±5.24 | 12.45±5.63 | −1.283 to 1.024 | 0.8250 | 0.02 | |
| Postop | 6.41±5.62 | 6.23±5.91 | −1.031 to 1.396 | 0.5354 | 0.03 | |
| EQ5D | 0.8001 | |||||
| Baseline | 0.57±0.13 | 0.56±0.15 | −0.021 to 0.041 | 0.5305 | 0.07 | |
| Postop | 0.73±0.17 | 0.71±0.22 | −0.029 to 0.056 | 0.5329 | 0.10 | |
| L-spine BMD | 0.1341 | |||||
| Baseline | 1.15±0.24 | 1.13±0.28 | −0.111 to −0.002 | 0.4273 | 0.08 | |
| Postop | 1.13±0.23 | 1.20±0.30 | −0.133 to −0.011 | 0.9382 | 0.25 | |
| Muscle mass | 0.7101 | |||||
| Baseline | 15.67±3.63 | 17.44±4.17 | −2.600 to −0.938 | 0.8570 | 0.45 | |
| Postop | 15.31±3.44 | 17.03±4.19 | −2.603 to −0.844 | 0.4869 | 0.44 | |
| Fat mass | 0.3251 | |||||
| Baseline | 7.07±2.63 | 6.69±2.54 | −0.166 to 0.918 | 0.7868 | 0.15 | |
| Postop | 7.27±2.49 | 6.95±2.45 | −0.229 to 0.875 | 0.2503 | 0.13 | |
| LM CSA | 0.0176 | |||||
| Baseline | 826.79±385.52 | 1,039.78±373.10 | −292.034 to −133.957 | 0.0007 | 0.56 | |
| Postop | 509.48±348.64 | 782.53±351.94 | −346.990 to −199.102 | <0.0001 | 0.78 | |
| ES CSA | <0.0001 | |||||
| Baseline | 1,772.59±599.34 | 1,812.45±578.19 | −162.502 to 82.783 | 0.2379 | 0.07 | |
| Postop | 1,388.54±631.64 | 1,686.26±609.52 | −428.040 to −167.390 | 0.0047 | 0.48 |
Values are presented as mean±standard deviation, %, or 95% CI unless otherwise stated.
CI, confidence interval; NA, not applicable; PLIF, posterior lumbar interbody fusion; VAS, Visual Analog Scale; LBP, low back pain; Postop, postoperative; RDQ, Roland-Morris Disability Questionnaire, EQ5D: European Quality of life-5 Dimensions, LM, lumbar multifidus; ES, erector spinae; CSA, cross-sectional area.
Sex-adjusted analysis of covariance.
Repeated-measures analysis of variance.
Table 4.
Comparison of operative outcomes between the sarcopenia and non-sarcopenia groups
| Variable | Sarcopenia (+) (n=110) | Sarcopenia (−) (n=263) | 95% CI | p-valuea) | Effect size | p-valueb) |
|---|---|---|---|---|---|---|
| Age (yr) | 74.93±7.09 | 71.04±9.40 | −1.030 to 2.656 | <0.0001 | 0.44 | NA |
| Female | 24.77 | 55.73 | NA | <0.0001 | NA | NA |
| PLIF | 38.18 | 49.05 | NA | 0.0863 | NA | NA |
| VAS (LBP) | 0.4190 | |||||
| Baseline | 5.19±3.01 | 4.92±2.94 | −0.401 to 0.942 | 0.4499 | 0.09 | |
| Postop | 2.42±2.88 | 2.46±2.71 | −0.662 to 0.575 | 0.4988 | 0.01 | |
| VAS (leg pain) | 0.7594 | |||||
| Baseline | 6.08±2.82 | 6.38±2.73 | −0.916 to 0.324 | 0.7972 | 0.11 | |
| Postop | 2.44±2.88 | 2.89±3.15 | −1.129 to 0.248 | 0.7445 | 0.15 | |
| RDQ | 0.3493 | |||||
| Baseline | 12.68±5.79 | 12.32±5.35 | −0.875 to 1.590 | 0.4986 | 0.07 | |
| Postop | 6.10±5.97 | 6.40±5.74 | −1.598 to 1.006 | 0.5940 | 0.05 | |
| EQ5D | 0.2571 | |||||
| Baseline | 0.54±0.16 | 0.57±0.15 | −0.058 to 0.008 | 0.1396 | 0.20 | |
| Postop | 0.72±0.21 | 0.72±0.20 | −0.042 to 0.049 | 0.3352 | 0.00 | |
| L-spine BMD | 0.3304 | |||||
| Baseline | 1.17±0.25 | 1.19±0.27 | −0.075 to 0.043 | <0.0001 | 0.08 | |
| Postop | 1.18±0.27 | 1.17±0.28 | −0.057 to 0.075 | 0.0061 | 0.04 | |
| Muscle mass | 0.0371 | |||||
| Baseline | 16.68±3.15 | 17.18±4.31 | −2.402 to −0.606 | 0.0101 | 0.12 | |
| Postop | 15.55±3.30 | 16.71±4.23 | −2.112 to −0.209 | <0.0001 | 0.29 | |
| Fat mass | 0.4540 | |||||
| Baseline | 5.73±1.99 | 7.30±2.68 | −2.131 to −1.011 | <0.0001 | 0.63 | |
| Postop | 5.97±1.97 | 7.54±2.51 | −2.133 to −1.002 | <0.0001 | 0.68 | |
| LM CSA | 0.1407 | |||||
| Baseline | 939.04±390.88 | 965.76±393.01 | −114.662 to 61.229 | <0.0001 | 0.07 | |
| Postop | 690 55±365.05 | 671.72±380.28 | −66.122 to 103.783 | 0.0579 | 0.05 | |
| ES CSA | 0.0557 | |||||
| Baseline | 1,664.57±510.24 | 1,851.62±608.74 | −316.415 to −55.689 | <0.0001 | 0.32 | |
| Postop | 1,524.83±626.69 | 1,591.88±638.97 | −210.650 to 76.550 | 0.0005 | 0.11 |
Values are presented as mean±standard deviation, %, or 95% CI unless otherwise stated.
CI, confidence interval; NA, not applicable; PLIF, posterior lumbar interbody fusion; VAS, Visual Analog Scale; LBP, low back pain; Postop, postoperative; RDQ, Roland-Morris Disability Questionnaire, EQ5D: European Quality of life-5 Dimensions, LM, lumbar multifidus; ES, erector spinae; CSA, cross-sectional area.
Sex-adjusted analysis of covariance.
Repeated-measures analysis of variance.
A subgroup analysis of postoperative outcomes in 144 patients with DS who completed the 1-year follow-up was performed, comparing 36 and 108 cases with and without sarcopenia, respectively. No significant differences were observed in clinical outcomes or postoperative changes in skeletal-muscle mass based on the presence of sarcopenia (Table 5).
Table 5.
Comparison of operative outcomes in spondylolisthesis between the sarcopenia and non-sarcopenia groups
| Variable | Sarcopenia (+) (n=36) | Sarcopenia (−) (n=108) | 95% CI | p-valuea) | Effect size | p-valueb) |
|---|---|---|---|---|---|---|
| Age (yr) | 75.44±6.78 | 71.64±7.98 | 0.901 to 6.711 | 0.0111 | 0.49 | NA |
| Female | 47.22 | 68.52 | NA | 0.0283 | NA | NA |
| PLIF | 91.67 | 90.74 | NA | 0.9999 | NA | NA |
| VAS (LBP) | 0.9926 | |||||
| Baseline | 4.07±2.77 | 5.00±2.91 | −1.395 to 0.800 | 0.5901 | 0.32 | |
| Postop | 2.30±2.68 | 2.52±2.80 | −0.797 to 0.354 | 0.7859 | 0.08 | |
| VAS (leg pain) | 0.5066 | |||||
| Baseline | 5.78±1.98 | 6.73±2.65 | −1.839 to 0.010 | 0.0523 | 0.38 | |
| Postop | 2.14±2.62 | 2.71±3.04 | −1.168 to 0.555 | 0.3246 | 0.19 | |
| RDQ | 0.6937 | |||||
| Baseline | 11.83±5.03 | 12.49±5.32 | −2.658 to 1.344 | 0.5360 | 0.13 | |
| Postop | 6.33±5.99 | 6.44±5.52 | −2.248 to 2.045 | 0.8161 | 0.02 | |
| EQ5D | 0.7434 | |||||
| Baseline | 0.57±0.10 | 0.57±0.14 | −0.052 to 0.049 | 0.9741 | 0.00 | |
| Postop | 0.72±0.20 | 0.73±0.16 | −0.079 to 0.052 | 0.5590 | 0.06 | |
| L-spine BMD | 0.4325 | |||||
| Baseline | 1.14±0.23 | 1.15±0.24 | −0.098 to 0.083 | 0.0476 | 0.04 | |
| Postop | 1.16±0.25 | 1.12±0.23 | −0.058 to 0.129 | 0.3497 | 0.17 | |
| Muscle mass | 0.2854 | |||||
| Baseline | 14.21±3.00 | 16.15±3.70 | −3.294 to −0.601 | <0.0001 | 0.55 | |
| Postop | 14.14±3.14 | 15.72±3.46 | −2.933 to −0.950 | <0.0001 | 0.47 | |
| Fat mass | 0.2786 | |||||
| Baseline | 5.72±2.17 | 7.52±2.63 | −2.762 to −0.843 | 0.0018 | 0.71 | |
| Postop | 5.87±1.98 | 7.78±2.47 | −2.838 to −0.950 | 0.0013 | 0.76 | |
| LM CSA | 0.0559 | |||||
| Baseline | 718.23±272.94 | 862.97±411.06 | −289.953 to 0.463 | 0.0033 | 0.64 | |
| Postop | 469.91±276.20 | 524.32±368.41 | −188.488 to 79.661 | 0.0063 | 0.16 | |
| ES CSA | 0.1941 | |||||
| Baseline | 1,595.72±427.37 | 1,831.55±637.40 | −461.270 to −10.385 | <0.0001 | 0.40 | |
| Postop | 1,290.55±575.98 | 1,424.37±346.22 | −376.305 to 108.377 | <0.0001 | 0.32 |
Values are presented as mean±standard deviation, %, or 95% CI unless otherwise stated.
CI, confidence interval; NA, not applicable; PLIF, posterior lumbar interbody fusion; VAS, Visual Analog Scale; LBP, low back pain; Postop, postoperative; RDQ, Roland-Morris Disability Questionnaire, EQ5D: European Quality of life-5 Dimensions, LM, lumbar multifidus; ES, erector spinae; CSA, cross-sectional area.
Sex-adjusted analysis of covariance.
Repeated-measures analysis of variance.
Discussion
To our knowledge, this study is the first to evaluate the risk factors for DS in patients with LSS using multivariate analysis and to longitudinally investigate the influence of sarcopenia on surgical outcomes in DS based on diagnostic criteria incorporating a low SMI. DS has been reported to be more common in females [3], and our findings are consistent with this observation. Moreover, Jacobsen et al. [18] reported that DS is more prevalent in females with a higher BMI. They suggested that the combination of increased LL and BMI may impose additional stress on adjacent spinal ligaments and lumbar intervertebral discs in postmenopausal women, potentially contributing to the multifaceted biomechanical pathogenesis of DS. Although BMI was relatively high in the present cohort, it was not identified as a significant factor in DS occurrence. However, comparisons between patients with and without DS revealed that a lower SMI and a higher body fat percentage were significant factors. These findings suggest that sarcopenic obesity may contribute to DS development. Although several studies have evaluated obesity using BMI, analyses that simultaneously account for skeletal muscle and fat mass may have yielded results comparable to those of the present study.
In this study, spinal anatomical factors identified as significant in the multivariate analysis and considered to influence the occurrence of L4 vertebral anterior slippage included lumbar hyperlordosis, sagittalization of the facet-joint angle, and advanced disc degeneration, consistent with previous reports [3,11]. Particularly, facet-joint orientation plays a crucial role in lumbar biomechanics. Facet joints primarily share load during lumbar compression and extension, and a more sagittal orientation of the joint reduces resistance to anterior shear forces, thereby leading to anterior vertebral gliding [19]. However, whether these abnormalities determine the predisposition to slippage or are secondary remodeling changes from existing degenerative changes remains unclear, and their role is limited to radiographic descriptions of instability [3]. Preventing degenerative changes in the aging-associated spine is challenging. If DS defines anatomical features related to instability based on spinal degeneration as a risk factor, spinal balance can be viewed as the equilibrium between external forces acting on the spine and the compensatory trunk muscle response [20]. The skeletal muscle, which is affected by aging, is subject to a wide range of factors, including not only the systemic mechanisms of sarcopenia but also denervation associated with lumbar neuropathy and disuse resulting from aging. Therefore, a comprehensive investigation of the pathological processes contributing to this skeletal-muscle loss is essential to better understand the association between DS and sarcopenia.
Numerous studies investigating the relationship between DS and skeletal muscles have reported that degeneration of the paraspinal muscles, particularly the LM, impairs segmental stability and is associated with the development and progression of vertebral slippage [5,6,14]. LM degeneration is characterized by muscle atrophy and increased fatty infiltration. Zhang et al. [21] reported that LM atrophy is especially pronounced in the DS-affected segment, whereas Virk et al. [5] reported that greater slip severity is associated with increased paralumbar muscle atrophy and fatty degeneration. The pathophysiological hallmark of sarcopenia is the loss of skeletal-muscle mass due to intramuscular and intermuscular fat infiltration known as myosteatosis [6]. Muscle weakness occurs concurrently with or may even precede this process. It is believed that a similar pathophysiological process occurs in the paraspinal muscle, whereby the multifidus muscle is progressively replaced by fat, leading to reduced muscle strength and impaired spinal stability.
Denervation due to compression of the medial branch of the segmental nerve in both DS and LM induces subsequent LM atrophy within the affected myotome. While paraspinal muscles are reportedly associated with DS, sarcopenia is primarily characterized by an age-related decrease in skeletal-muscle mass that predominantly affects Type II muscle fibers. Consequently, clinical diagnostic systems for sarcopenia have largely been based on appendicular skeletal-muscle mass, as limb muscles predominantly contain Type II fibers [4]. Age-related reduction in trunk muscles rich in Type II muscle fibers has been reported to occur after reductions in appendicular muscles rich in Type I muscle fibers [22]. Among the trunk muscles where Type I fibers predominate, the ES functions as a global muscle with a higher proportion of Type II fibers, whereas the LM is relatively rich in Type I fibers and contributes to spinal segmental stability [23]. Therefore, if age-related loss of LM muscle mass contributes to DS onset, a corresponding reduction in appendicular muscle mass would also be expected. However, few studies have comprehensively examined the relationship between appendicular skeletal-muscle mass (a key diagnostic component of sarcopenia) and DS.
To our knowledge, only three clinical studies have examined the relationship between DS and appendicular skeletal-muscle mass. Matsuo et al. [24] evaluated 178 patients with LSS and reported that the percentage of vertebral slip was higher in sarcopenia patients, which was identified in 19.7% of cases using the AWGS criteria based on muscle mass measurements via bioelectrical impedance analysis (BIA). Similarly, Feng et al. [25] diagnosed sarcopenia in 161 patients with DS at the L4–L5 level using the AWGS criteria based on muscle mass measurements obtained via DXA and reported that severe functional impairment in DS patients is closely associated with sarcopenia. Conversely, Arita et al. [26] measured muscle mass using BIA in 1,522 individuals from the general population and reported that in 17.4% of DS patients, the appendicular lean mass was significantly lower than that in non-slipped cases; however, it lost its statistical significance in multivariate analysis. Notably, this study observed posterior slippage, which differs pathophysiologically from DS, in 13.9% of cases. Because this study surveyed community-dwelling individuals with healthier lifestyles rather than patients with LSS, the findings may not accurately reflect the physical impairment associated with DS. To date, no study has specifically evaluated sarcopenia, particularly appendicular skeletal-muscle mass, in patients with both DS and LSS. Consequently, the precise etiological factors underlying LM atrophy in LSS and their causal relationship with age-related LM degeneration, which is strongly associated with DS, remain incompletely understood [20]. The present cross-sectional study, which investigated the relationship between DS and limb and trunk muscles in a sufficiently large cohort, demonstrated that reduced appendicular skeletal-muscle mass and significant atrophy and fatty degeneration of the LM at the L4–L5 level were important factors linked to DS. Vertebral slippage is thought to result primarily from the loss of spinal segmental stability due to LM atrophy [6]. However, when considering strategies to prevent vertebral slippage before the onset of LM atrophy, it is important to focus not only on LSS-caused neuropathy but also on the age-related decline in appendicular skeletal muscle, which may precede the decrease in trunk muscle mass.
Research on the role of the ligamentum flavum in DS is limited, and many aspects remain unclear. In this study, ligamentum flavum thickening was significantly less prevalent in DS patients. In a study by Feng et al. [25] involving 161 patients with L4–L5 level DS, significant flavum hypertrophy was associated with sarcopenia, whereas Hung et al. [27] reported no such association. The lumbar ligamentum flavum can be considered to be in a pathological state, in which its stabilizing function is impaired due to spinal instability [16]. Slippage is thought to develop and progress when ligament thickening is impeded by an as-of-yet uncharacterized mechanism, allowing instability to persist. However, elucidating this pathology will require long-term longitudinal studies evaluating the occurrence of slippage and progression of ligamentum flavum thickening.
Surgical treatment for DS frequently involves fusion procedures; in our study, PLIF was performed in 90% of cases. The impact of fixation surgery on the posterior spinal muscles was reflected by the significant postoperative muscle strength reduction in the LM and ES groups in the DS group compared with that in the non-DS group; nevertheless, the clinical outcomes were favorable. This study was not designed to evaluate the advantages and disadvantages of the selected surgical procedure for DS. However, controlling segmental instability appeared to resolve trunk muscle atrophy and improve neurological deficits. Consistent findings regarding the effect of sarcopenia on LSS surgical outcomes have yet to be established. Some reports suggest that muscle mass correlates with postoperative outcomes [28], whereas others have demonstrated favorable outcomes even in patients with sarcopenia [29]. In this study, which included 43% of patients with sarcopenia, postoperative outcomes in these patients were not inferior, although follow-up was limited to 1 year. Discrepancies among previous reports may be attributed to the differences in assessment methods, including skeletal-muscle mass and diagnostic criteria, as well as the higher prevalence of DS in females and sarcopenia in males. Therefore, a comparison of the surgical outcomes requires rigorous prospective controlled trials. PLIF was performed in 90% of patients with DS, regardless of the sarcopenia status. In patients with sarcopenia, both the LM and ES demonstrated significant preoperative atrophy; nevertheless, outcomes were favorable, and no significant difference in skeletal-muscle mass reduction was noted in comparison to the non-sarcopenia group during the 1-year follow-up. While previous studies have suggested that atrophy and fatty degeneration of trunk muscles following surgery for DS cause postoperative disability [30], the present study is the first to evaluate DS surgical outcomes based on sarcopenia diagnosis using appendicular skeletal-muscle strength as a criterion. ADL improvement following LSS treatment and the resolution of spinal instability may have contributed to favorable outcomes in sarcopenia patients. For patients with LSS involving slippage and sarcopenia, surgery targeting trunk muscle atrophy at the vertebral slippage level may be crucial. However, validating this aspect requires prospective studies comparing spinal stabilization to non-fusion surgery in terms of postoperative skeletal-muscle mass changes.
This study has several limitations. First, the evaluation of skeletal-muscle involvement in DS was cross-sectional and did not longitudinally assess the occurrence and progression of slippage. Therefore, the causal relationship between skeletal-muscle mass reduction and slippage remains unclear. Second, because this study was conducted at a single institution, section bias in the identification of patients with LSS may be present, potentially limiting the generalizability of the findings. Regarding the comparison of surgical outcomes, this was not a prospective controlled study, and the choice of surgical procedure reflected the attending surgeon’s judgment, resulting in the inclusion of different surgical techniques. In addition, postoperative complications and reoperations were not evaluated; therefore, it cannot be inferred that sarcopenia patients experienced equivalent surgical outcomes as compared to those without sarcopenia. Furthermore, factors that may influence postoperative changes in skeletal-muscle mass, including the differences in rehabilitation protocols and the use of osteoporosis medications, were not evaluated. Finally, the postoperative follow-up period was limited to 1 year, precluding evaluation of long-term outcomes. Thus, data on changes in appendicular and trunk muscle mass remains limited.
Conclusions
In patients with LSS, DS was associated with female sex, LL, facet-joint angle, disc degeneration, severe spinal canal stenosis, reduced limb muscle mass, multifidus muscle atrophy, and fatty degeneration. Despite the impact of both DS and sarcopenia on LSS, favorable postoperative outcomes were achieved following fusion surgery. Patients with concomitant DS and sarcopenia also experienced satisfactory outcomes fusion procedures, and postoperative improvements in ADLs may help prevent postoperative muscle atrophy.
Key Points.
Degenerative L4–L5 spondylolisthesis in lumbar stenosis is associated with sarcopenia.
Multifidus and erector spinae atrophy occurred following surgery for spondylolisthesis.
Surgical outcomes for degenerative spondylolisthesis with sarcopenia are favorable.
Postoperative muscle atrophy in spondylolisthesis with sarcopenia is comparable to that in controls.
Funding Statement
This study was supported by the National Centre for Geriatrics and Gerontology (23-8).
Footnotes
Conflict of Interest
No potential conflict of interest relevant to this article was reported.
Data Availability
The data that support the findings of this study are not publicly available as they contained information that could compromise the privacy of the research participants; however, they are available from the corresponding author (Yoshihito Sakai) upon reasonable request.
Acknowledgments
We are grateful to all patients who agreed to participate in the study, the staff who delivered the intervention, and the surgeons who helped with patient recruitment. We appreciate the administrative assistance provided by Junko Suzuki, Miki Morita, and Reina Yamamoto.
Funding
This study was supported by the National Centre for Geriatrics and Gerontology (23-8). The funders were not involved in the design or conduct of the study; collection, management, analysis, or interpretation of the data; nor in the preparation, review, or approval of the manuscript.
AI Use Disclosure
During the preparation of this work, the corresponding author, whose native language is Japanese, used DeepL Translate to assist in translating short passages of the text. After using this tool, the authors reviewed and edited the content as needed and take full responsibility for the content of the publication.
Author Contributions
Conceptualization: YS. Data acquisition: YT, TW, HM, YA, KU. Formal analysis: YS. Investigation: YT. KU. Supervision: YS. Writing–original draft: YT. Writing–review & editing: YS, TW, HM, YA, RS, KU. Final approval of the manuscript: all authors.
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