Paraspinal muscle degeneration patterns in degenerative spinal deformity: a histological, morphological, and muscle functional comparison

Introduction

Degenerative spinal deformity (DSD) is a comprehensive term that encompasses age-related spinal deformities, which affect 13.3% of the Chinese population aged >40 years (1). DSD frequently results in disability, neurological impairment, and significantly diminishing health-related quality of life (2,3). Furthermore, most patients with DSD require spinal arthrodesis to restore spinal alignment, which imposes a socioeconomic burden of >US$1.65 billion in medical treatment per year (4,5). However, postoperative mechanical complications accompanied more than 25% of patients with DSD, which is mainly because of the lack of individualized surgical planning. DSD presents with divergent subtypes involving single-plane curvatures, such as degenerative lumbar scoliosis (DLS) and kyphosis (DLK), or a combination of both (6,7). Given the heterogeneous curve behavior of DSD, surgical approaches and prognostic outcomes vary considerably. The poor understanding of the pathological features and intrinsic difference of each DSD subtype contributes significantly to the uncertainty of surgical outcomes.

The paraspinal muscle (PSM) plays a crucial role in controlling spinal locomotion and maintaining upright posture (8). Enormous studies have recognized PSM degeneration as a driving risk factor for DSD and post-operative surgical outcomes. However, due to lack of tailored intervention, significant variations in morbidity rates and surgical outcomes have been observed in patients with DSD across the literature. Preoperative PSM degeneration is closely associated with postoperative coronal balance transition in patients with DLS (9). Other studies have shown that PSM degeneration was highly implicated in sagittal mechanical complications in patients with DLK (10). To comprehensively assess the individual degenerative status, multidimensional evaluation is essential for clarification of intrinsic properties and functional features of PSM. Especially, a multi-modal assessment of the PSM is the key to depict the substantial changes such a complex of spinal deformities. The current focuses of degenerative muscle disease are not limited to indirect morphological analysis, but underscore the alterations in muscle strength and its histological properties. However, limited studies have investigated the histological features and functional difference of DSD, and controversial results have been reported regarding the morphological characteristics of PSM. Specifically, no study has never comprehensibly applied a multimodal approach to examine the similarity of PSM degeneration between DLS and DLK. Therefore, this study aimed to systematically explore the differences in the degenerative changes of PSM between DLS and DLK subtypes through histological, morphological, and functional comparison, and provide pathological references for clinical diagnosis and treatment. We present this article in accordance with the STROBE reporting checklist (available at https://qims.amegroups.com/article/view/10.21037/qims-2025-1878/rc).

Methods

Patient enrollment

Hospitalized patients with DLK, lumbar spinal stenosis (LSS), and DLS were prospectively recruited (Figure 1). This study was conducted following the Declaration of Helsinki and its subsequent amendments, and was approved by the Institutional Review Board (IRB) of Nanjing Drum Tower Hospital, Affiliated Hospital of Nanjing University Medical School (IRB No. 2021-389-01). Informed consent was obtained from all patients in this study for all procedures undertaken and all data obtained.

Figure 1 Workflow of this study. DLK, degenerative lumbar kyphosis; DLS, degenerative lumbar scoliosis; ET, endurance time; LSS, lumbar spinal stenosis; MVE, maximal voluntary exertion.

The inclusion criteria for DLK patients (11) were as follows: (I) patients aged >50 years; (II) regional kyphosis >30° or sagittal vertical axis >50 mm; (III) Cobb angle <10°.

The inclusion criteria for LSS patients were as follows: (I) age >50 years; (II) no spinal deformity on radiographs; (III) diagnosis made based on a combination of clinical history (such as lower extremity pain), physical examination (such as femoral nerve stretch test), and radiographic evidence of spinal canal stenosis (12,13), and the patients with upper lumbar spinal canal stenosis at the L1–L3 levels, in which the stenotic segment involved L2.

The inclusion criteria for DLS patients were as follows: (I) patients aged >50 years; (II) Cobb angle 10–60°; (III) regional kyphosis ≤10°; and sagittal vertical axis <50 mm.

In addition, basic demographic data, including gender, age, and body mass index (BMI), were also obtained.

The exclusion criteria for this study were as follows: (I) patients with kyphosis caused by trauma, tuberculosis, and Scheuermann’s disease; (II) acute or chronic back pain that could interfere with the evaluation of endurance and maximal voluntary exertion (MVE); (III) a Visual Analog Scale score of more than 6; (IV) any history of spinal surgery.

Radiological assessment

A comprehensive anteroposterior and lateral radiographic examination of the full spine was conducted for participants in this study. Radiographic parameters were assessed on X-ray films in accordance with the guidelines established by the Spine Deformity Study Group, encompassing both coronal and sagittal parameters (14). Coronal parameters included the Cobb angle of the main curve. In contrast, sagittal parameters comprised measurements such as the sagittal vertical axis, thoracic kyphosis, lumbar lordosis, regional kyphosis, pelvic incidence, pelvic tilt, and sacral slope. All measurements were obtained using Surgimap software (version 2.3.2.1, Nemaris Inc., New York, NY, USA), and were conducted following methodologies outlined in previous research (1,11,15).

• Sagittal vertical axis: the horizontal distance between a plumb line projected from the centroid of the C7 vertebra and a perpendicular line intersecting the posterior superior sacral endplate.
• Regional kyphosis: the angle formed between the superior endplate of the upper terminal vertebra and the inferior endplate of the lower terminal vertebra.
• Thoracic kyphosis: the angle formed between the superior endplate of T5 vertebra and the inferior endplate of the T12 vertebra.
• Lumbar lordosis: the angle between the superior endplate of the L1 vertebra and the superior endplate of S1.
• Sacral slope: the angle formed by the upper sacral endplate and a horizontal line.
• Pelvic incidence: the angle is defined by the intersection of a line perpendicular to the sacral endplate and a line connecting the centroid of the femoral head to the midpoint of the sacral endplate.
• Pelvic tilt: the angle is defined by the intersection of a line extending from the midpoint of the sacral end plate to the center of the femoral head with a vertical line passing through the center of the femoral head.

Evaluation of morphology of PSM

The magnetic resonance imaging (MRI) of enrolled patients was acquired on a 1.5-T sigma imaging system (Magetom Skyra, Siemens Healthcare, Erlangen, Germany). After scanning, the trans-axial and sagittal sequences of T2-weighted images were saved with Digital Imaging and Communications in Medicine (DICOM) format from the Picture Archiving and Communication System (PACS), (axial T2 parameters included repetition time 4,000, echo time 113, and slice thickness 3 mm). The sagittal MRI sequences can be used to identify the intervertebral discs and the inferior endplate of the vertebral body. The axial plane was set to ensure that the imaging line traversed the L2/3 intervertebral disc. An example of image displacement is shown in Figure S1.

For DLS and DLK, the apex vertebral position was selected for measurement data, whereas for LSS, the L2 level was chosen as the measurement segment for sample uniformity. Relative cross-sectional area (rCSA) of PSM was quantified by outlining thoracolumbar facial boundaries using ImageJ (Image J ver. 1.3; National Institutes of Health, Bethesda, MD, USA) (16,17), and calculated as: (CSA of the PSM on one side of the vertebra / CSA of the intervertebral disc) × 100. Percentage of fat infiltration area (%FIA) and functional cross-sectional area (fCSA; muscle area excluding FIA) were measured using this algorithm (18,19).

Evaluation of PSM function

The MVE of the PSM was assessed utilizing a calibrated hand-held dynamometer (Micro FET3, Hoggan Health Industries, South Salt Lake City, UT, USA). The measured values are expressed in newtons (N). The measurements were performed in a quiet room. Participants were positioned in a standardized prone posture, with hips and knees neutrally aligned, and arms extended. The dynamometer was positioned at the midline between the superior angles of the scapulae, then secured to the muscle strength testing apparatus (20). Participants executed maximal back extensions with scapular elevation, maintaining an isometric contraction for a duration of 3–5 seconds. The peak force values were recorded. Three measurements were recorded, with 60-second intervals between trials. If the final measurement exceeded previous results by more than 5%, an additional trial was conducted to ensure the capture of maximal effort. The protocol demonstrated satisfactory safety and reproducibility (17,21).

PSM endurance time (ET) was assessed in the unit of seconds (s). Participants were positioned in a prone posture with a pelvic cushion. The protocol required participants to maintain sternal elevation while maximizing cervical flexion and engaging gluteal contraction. Trials were concluded upon meeting one of the following cessation criteria: (I) an upper-trunk-to-surface angle of less than 5°; (II) three consecutive sternal contacts; or (III) participant-reported discomfort. A maximum duration of 5 minutes was allowed, with two trials conducted, separated by a 5-minute rest period between trials, and the best score was recorded. The protocol demonstrated favorable safety and test–retest reliability (17,21).

Histological assessment

All patients underwent posterior spinal surgery; the L2 level was selected as the standardized sampling site for histological quantification. After completing posterior exposure and confirming the spinal level, bilateral multifidus muscle (MF) samples at the L2 vertebral level were collected. A muscle sample of 1 cm × 1 cm in size was collected and the muscle tissues were snap-frozen in nitrogen-cooled isopentane-embedded Optimal Cutting Temperature compound (Tissue-Tek, 4583; Sakura Finetek, Torrance, CA, USA). Then, 10-micrometer sections were obtained from optimal cutting temperature compound-embedded frozen samples using a Leica (CM3050S, Buffalo Grove, IL, USA) cryostat. Hematoxylin and eosin (H&E) were used to visualize gross muscle morphology. Sirius Red staining and Oil Red O staining were used to respectively evaluate the degree of fibrosis and fat infiltration in the PSM (22). For Sirius Red staining, frozen PSM sections (10 µm) were fixed in 4% paraformaldehyde for 10 minutes, washed in phosphate-buffered saline (PBS) twice for 5 minutes each, and stained with Sirius Red solution (PH1098, Phygene, Shenzhen, China) for 30 minutes at room temperature. Sections were briefly rinsed in 0.5% acetic acid, dehydrated through graded ethanol, cleared in xylene, and mounted with a resinous medium (23). Microscopic images were acquired using an Olympus light microscope (Tokyo, Japan). Under bright-field microscopy, collagen fibers appeared red. For the quantitative analysis of staining, the red, green, and blue images were converted to an 8-bit grayscale image, and then the Image → Adjust → Threshold tool was used to set the threshold according to the experimental requirements (22).

Method reliability

To assess the reliability of radiological, histological, and functional measurements, all parameters were independently evaluated by two observers (Q.L. and M.W.), both of whom were blinded to the participants’ clinical information. Intra- and inter-observer agreement was assessed using the intraclass correlation coefficient (ICC). According to previously described semi-quantitative criteria, ICC values were interpreted as follows: excellent (ICC ≥0.90), good (0.70≤ ICC <0.90), acceptable (0.60≤ ICC <0.70), poor (0.50≤ ICC <0.60), and unreliable (ICC <0.50) (15,24).

Statistical analysis

The data was presented as means ± standard deviation. Statistical analyses were performed using the software SPSS 23.0 (IBM Corp., Armonk, NY, USA). Pearson correlation coefficient was used to examine the correlation between MVE/ET of PSM and morphological parameters. A P value <0.05 was considered statistically significant. Correlation was defined as follows: 0.2≤ |R| <0.4 mild correlation, 0.4≤ |R| <0.6 moderate correlation (25). Group differences were analyzed using one-way analysis of variance (ANOVA) with Bonferroni post hoc correction. Post hoc power analysis for the primary histological outcomes was performed using G*Power (version 3.1, Heinrich-Heine-University Düsseldorf, Germany) at a two-sided α of 0.05.

Results

Patient information

The demographic data of the patients and the parameters of the radiographical evaluations are summarized in (Table 1). A total of 62 patients with LSS, 65 patients with DLS, and 57 patients with DLK were enrolled in this study. The mean ages of the patients were 62.3±4.2, 63.6±5.5, and 62.9±5.0 years, respectively. The PSM biopsies for histological analysis were respectively obtained from 17, 21, and 19 patients in the LSS, DLS, and DLK groups. The intra- and inter-observer ICC for radiological, histological, and functional measurements ranged from 0.82 to 0.97, indicating good to excellent reliability between the two observers (Table S1). The DLK patients were featured by a much larger sagittal vertical axis, whereas DLS patients showed larger cobb angle (DLK: sagittal vertical axis: 89.5±34.2 or regional kyphosis: 40.6±6.1; DLS: cobb angle: 45.2±6.7). As most apex vertebrae were located at the L2 level in both patients with DLK and DLS, L2 level was selected to examine the morphological and histological change of PSM in three groups. A post hoc power analysis demonstrated adequate statistical power (>0.99) for the primary histological outcomes, and this sample size also provided sufficient statistical power to detect potential differences (Table S2).

Histological comparison of PSMs in patients with LSS, DLS, and DLK

In the LSS group, histological staining revealed normal muscle fiber integrity with mild fatty infiltration. For DLS patients, histological analysis revealed significant fatty infiltration on the concave side, with a higher degree than that observed on the convex side (concave vs. convex: 25.8%±2.5% vs. 13.5%±2.1%, P<0.05). Meanwhile, fibrosis was predominantly present on the convex side (concave vs. convex: 10.5%±2.2% vs. 26.5%±2.4%, P<0.05). In contrast, DLK patients also exhibited lower levels of fatty infiltration compared to the concave side of DLS (DLS vs. DLK: 25.8%±2.5% vs. 14.0%±1.4%, P<0.05). However, Sirius Red staining indicated a markedly higher degree of fibrosis in DLK than in the concave side of DLS (DLS vs. DLK: 10.5%±2.2% vs. 26.8%±2.2%, P<0.05). Moreover, histological staining further demonstrated that DLK patients and the convex side of DLS shared similar patterns of fatty and fibrotic infiltration (fatty infiltration: DLS vs. DLK: 13.5%±2.1% vs. 14.0%±1.4%; fibrotic infiltration: DLS vs. DLK: 26.5%±2.4% vs. 26.8%±2.2%) (Figure 2).

Figure 2 Histological comparison of paraspinal muscles in patients with LSS, DLS, and DLK. Upper panel: representative DR and MRI images of indicated groups at the L2 level. Lower panel: H&E, Sirius Red, and Oil Red O staining for multifidus muscle in the specified group. Quantitative images of tissues stained with Sirius Red and Oil Red O. *, P<0.05. DLK, degenerative lumbar kyphosis; DLS, degenerative lumbar scoliosis; DR, digital radiography; H&E, hematoxylin and eosin; LSS, lumbar spinal stenosis; MRI, magnetic resonance imaging.

Morphological comparison of bilateral PSMs in patients with LSS, DLS, and DLK

In patients with DLS, the rCSA on the convex side was significantly smaller than that on the concave side in the MF (concave vs. convex: 29.0±4.5 vs. 25.2±3.9 mm², P<0.05), ES (concave vs. convex: 97.4±14.0 vs. 74.2±11.8 mm², P<0.05) and total muscle (MF + ES). However, there was a significant difference in the %FIA between the concave and convex sides at the level of MF (concave vs. convex: 35.9%±6.7% vs. 25.0%±4.8%, P<0.05), ES (concave vs. convex: 28.9%±5.5% vs. 23.7%±4.4%, P<0.05), and total muscle, with a significant increase in %FIA on the concave side in the DLS. In the DLK and LSS group, the measurement outcomes for %FIA and rCSA exhibit no significant differences (Figure 3).

Figure 3 Morphological comparison of bilateral paraspinal muscles in patients with LSS, DLS, and DLK. *, P<0.05. Total: total muscle (MF + ES). DLK, degenerative lumbar kyphosis; DLS, degenerative lumbar scoliosis; ES, erector spinae; LSS, lumbar spinal stenosis; MF, multifidus muscle.

Morphological comparison of PSMs in patients with LSS, DLS, and DLK

Compared to patients with LSS, the patients with DLS demonstrated a significantly higher %FIA in both sides of MF, ES, and total muscle (P<0.05). Meanwhile, DLS patients demonstrated smaller rCSA of bilateral MF compared to patients with LSS (LSS vs. concave side of DLS: 36.3±4.9 vs. 29.0±4.5 mm², P<0.05), and the ES and total muscle at the concave of DLS were smaller compared to patients with LSS (ES: LSS vs. DLS: 109.3±16.1 vs. 97.4±14.0 mm², P<0.05). The rCSA of patients with DLK was smaller compared to that of those with LSS in the MF (LSS vs. DLK: 36.3±4.9 vs. 25.9±3.8 mm², P<0.05), ES (LSS vs. DLK: 109.3±16.1 vs. 70.4±11.2 mm², P<0.05), and total muscle (P<0.05). The %FIA of MF (LSS vs. DLK: 8.7%±3.4% vs. 23.9%±6.4%, P<0.05) and ES (LSS vs. DLK: 9.6%±4.2% vs. 27.2%±4.3%, P<0.05) were higher in the PSM of patients with DLK compared to the LSS (P<0.05).

The rCSA of patients with DLK showed significant atrophy compared to the concave side of DLS in the MF (DLS vs. DLK: 29.0±4.5 vs. 25.9±3.8 mm², P<0.05), ES (DLS vs. DLK: 97.4±14.0 vs. 70.4±11.2 mm², P<0.05), and total muscle (P<0.05), whereas the rCSA of DLK patients was similar to that of the convex side of DLS. The %FIA in MF in the concave side of DLS was much higher than that of DLK patients (DLS vs. DLK: 35.9%±6.7% vs. 23.9%±6.4%, P<0.05). Meanwhile, the %FIA of ES (DLK vs. DLS: 27.2%±4.3% vs. 23.7%±4.4%, P<0.05) and total muscle (DLK vs. DLS: 26.4%±3.9% vs. 24.0%±3.5%, P<0.05) of patients with DLK was higher than the convex side of the patients with DLS.

For the fCSA, compared with LSS patients, fCSA decreased in both DLS and DLK (P<0.05). In the PSM of MF, the study found no significant difference between the concave side of DLS patients and DLK patients, but the reduction of fCSA was more pronounced in the convex side of DLS patients (DLS vs. DLK: 17.9±3.0 vs. 19.7±2.9 mm², P<0.05). In addition, in the PSM of ES, compared with DLS patients, the fCSA of DLK patients also showed a significant decrease (DLK vs. concave or convex: 51.2±8.7 vs. 69.2±11.7 or 56.7±9.4 mm², P<0.05). For total muscle, the reduction of PSM fCSA in DLK patients is more significant than in DLS patients (DLK vs. concave or convex: 70.9±9.8 vs. 87.8±12.1 or 75.5±9.7 mm², P<0.05) (Figure 4).

Figure 4 Morphological comparison of paraspinal muscles in patients with LSS, DLS, and DLK. *, P<0.05. Total: total muscle (MF + ES). DLK, degenerative lumbar kyphosis; DLS, degenerative lumbar scoliosis; ES, erector spinae; LSS, lumbar spinal stenosis; MF, multifidus muscle.

Functional comparison of PSMs in patients with LSS, DLS, and DLK

The MVE and ET of DLS and DLK were much lower compared to those of LSS (MVE: LSS vs. DLS or DLK: 121.9±21.7 vs. 90.5±13.9 or 84.0±16.9 N, P<0.05; ET: LSS vs. DLS or DLK: 30.5±7.7 vs. 18.6±5.6 or 16.0±5.2 s, P<0.05). However, the MVE and ET of DLS were slightly higher than those of DLK (MVE: DLS vs. DLK: 90.5±13.9 vs. 84.0±16.9 N, P<0.05; ET: DLS vs. DLK: 18.6±5.6 vs. 16.0±5.2 s, P<0.05) (Figure 5).

Figure 5 Functional comparison of paraspinal muscles in patients with LSS, DLS, and DLK. *, P<0.05. DLK, degenerative lumbar kyphosis; DLS, degenerative lumbar scoliosis; ET, endurance time; LSS, lumbar spinal stenosis; MVE, maximal voluntary exertion.

Correlation between muscle morphological, muscle functional, and muscle histological parameters in patients with LSS, DLS, and DLK

In LSS patients, there was a moderate strength of correlation between MVE and rCSA of (MF + ES) (R=0.427). For the concave side and convex side of DLS, compared to the convex side of DLS, the rCSA of (MF + ES) and %FIA of (MF + ES) of concave side showed higher strength of correlation with MVE and ET. MVE and ET had moderate correlation with rCSA of (MF + ES) (MVE: R=0.463; ET: R=0.413). However, only ET showed a moderate strength of correlation with %FIA of (MF + ES) (R=–0.492). In DLK patients, there was a moderate strength of correlation between MVE and rCSA of (MF + ES) (R=0.432), and a mild strength of correlation between ET and %FIA of (MF + ES) (R=–0.384).

In LSS patients, a moderate correlation was observed between fCSA of (MF + ES) and MVE (R=0.446). In DLS patients, there was a moderate strength of correlation between MVE and fCSA of (MF + ES) on the concave side (R=0.403), and there was also a mild correlation between ET and fCSA of (MF + ES) (R=0.373), However, there was only a mild correlation between fCSA of (MF + ES) and MVE on the convex side of DLS patients (R=0.298). For DLK patients, there was a mild correlation between fCSA of (MF + ES) and MVE (R=0.372) (Table 2). In patients with DLS, a moderate correlation (R=0.48) between imaging parameters and histological indices was observed on the concave side of the PSM (Figure S2).

Discussion

Significant variations in morbidity rates and surgical outcomes have been observed in DSD across the literature. This may be due to the poor understanding of the intrinsic difference of each DSD subtype. PSM degeneration is a well-recognized risk factor for DSD and post-operative surgical outcomes, but it remains unknown how PSM properties and functions are shared or differ between DLK and DLS. In this study, we investigated differences in the degeneration patterns of the PSM in terms of histology, morphology, and functionality. Histologically, severe fatty infiltration was observed on the concave side of DLS patients, whereas prominent fibrotic deposition was observed on the convex side of DLS and in DLK patients. Morphologically, in patients with DLK, the ES and MF had a smaller cross-sectional area than in patients with DLS and LSS, with more pronounced atrophy being observed in the ES. Conversely, more significant atrophy and fat infiltration of the MF was observed in individuals with DLS than in those with DLK or LSS. Functionally, patients with DLK showed poor muscle strength and endurance compared to the ones with DLS. Together, the degeneration pattern was similar in the convex side of DLS and DLK, whereas a significant difference was found between the concave side of DLS and DLK, especially the ES. These findings may provide a novel insight to understanding the intrinsic difference of PSM and its role in the evolution of subtypes of DSD, and guiding individual surgical decision-making. In DLK patients, ES degeneration is more severe, therefore, appropriate extension of the fusion segment and timely postoperative muscle augmentation should be considered. In DLS patients, the treatment of MF of the convex side should be emphasized, and intraoperative damage should be reduced.

The PSM are crucial for spinal stability and posture maintenance (26,27). Atrophy and fatty infiltration are two major features of muscle degeneration (2). Multiple studies have reported that PSM affects the long-term clinical outcomes of lumbar spine degenerative diseases (28,29). Preoperative PSM is closely associated with postoperative coronal balance transition in patients with DLS. Other studies have also shown that PSM was highly implicated in sagittal mechanical complications in patients with DLK. However, significant variations in poor surgical outcomes were observed in DSD, perhaps due to its heterogenous nature. However, the similarity and difference between subtypes of DSD remains to be investigated. Multiple studies (30) have confirmed asymmetric PMS in patients with DLS, particularly in terms of fat infiltration, which is consistent with the current study. However, the degenerative pattern in patients with DLK remains controversial. Hyun et al. (31) reported higher fat infiltration in patients with DLK comparable to the controls, yet no significant difference in CSA. However, Ding et al. (16) reported that patients with DLK exhibited smaller CSA of the ES and MF than did those with LSS. The findings reported by Ding et al. are consistent with our observations. We also noted that the reduction in muscle mass, as indicated by a lower CSA was significantly more pronounced in patients with DLK who exhibited higher levels of fat infiltration than in those with LSS. This discrepancy may be attributed to differences in the patient population included in our study and the severity of their conditions.

Although patients with severe DLK and DLS exhibit elevated fat infiltration and a CSA area than do asymptomatic patients or those with LSS, few studies have discussed differences in PSM degeneration patterns in patients with DLK and DLS. In this study, we found that in patients with DLK, the ES and MF had smaller CSA than those on the concave side in patients with DLS. However, the CSA of the PSM on the convex side of the DLS was comparable with that of patients with DLK. This may be attributed to the nature of the spinal alignment, which causes different biomechanical changes in the PSM (32). Yagi et al. (30) explained the differences in bilateral PSM degeneration caused by asymmetrical biomechanical loading, which lead to muscle relaxation on the concave side while sustaining contraction on the convex side. In contrast, patients with DLK have a single-lane deformity that commonly presents with sagittal imbalance, leading to sustained contractions on both sides (33). The variation in biomechanical loading between the concave and convex sides of DLS may account for the observed differences in the degeneration patterns of the PSM of these two groups.

Furthermore, this study was the first to describe the difference of histological degenerative pattern in patients with DLS and DLK. Skeletal muscle atrophy is typically associated with adipose tissue infiltration, a reduction in muscle fibers, and fibrotic infiltration. Shafaq et al. (2) observed the loss of muscle nuclei and myofiber atrophy during histological evaluation of the bilateral PSM of patients with DLS. However, whether paraspinal morphological alterations are correlated with histological changes has been scarcely discussed. In the present study, we found more severe fat infiltration and fibrosis on both sides in patients with DLS and DLK than in those with LSS. This can be expected given that PSM degeneration is shown to be more severe in patients with deformities. Interestingly, PSM of the convex side of DLS and DLK showed prominent fibrosis with less adipocytes. This histological alternation coincides with their biomechanical loading pattern. Several studies have reported that chronic stretching of certain muscle leads to muscle atrophy and excessive extracellular matrix deposition (34,35). PSM at the convex side of both DLS and DLK underwent sustained muscle contraction due to the biomechanical overloading which may lead to similar histological degeneration. Meanwhile, the concave side of patients with DLS exhibited more pronounced fat infiltration, which was consistent with fat infiltration observed in MRI images. This may be correlated with disuse caused by sustained relaxed of PSM on the concave side of DLS. Unfortunately, owing to ethical constraints and the limited availability of adequate PSM biopsy specimens, the histological sample size remained relatively small. Therefore, although the findings are clinically informative, they should be interpreted with caution and further validated in larger studies. Furthermore, although biomechanical abnormalities are to some extent associated with histological alterations of the PSM, the causal relationship between these two dimensions remains to be further elucidated.

In addition, we observed lower muscle strength and endurance in patients with DLK than in those with DLS. The CSA reportedly correlates with muscle strength in healthy volunteers, and fatty replacement of myofibers disrupts the contractibility of trunk muscle (36,37). Previous studies have implicated this correlation in degenerative lumbar diseases, suggesting that reduced muscle CSA correlates with reduced strength (37). Others have found that the fat infiltration rate is highly correlated with the ET of the trunk muscle rather than its strength. Recently, Han et al. (38) revealed that patients with DLK had lower PSM endurance than those with LSS. Chen et al. (21) also found that MVE was significantly higher in patients with LSS than in those with DSD. Similar findings were also observed in the present study. Interestingly, we observed lower muscle strength and endurance in patients with DLK than in those with DLS. This may be attributed to the smaller ES and MF cross-sectional area in patients with DLK, despite similar fat infiltration in the PSM. In particular, the CSA of the ES was larger than that of the MF, and the ES mass was significantly reduced in patients with DLK. Correlation analysis also showed a stronger correlation between the CSA of the total muscle and muscle strength, indicating a synergetic loss of CSA and muscle strength. In contrast, the PSM of the DLK was replaced by non-contractible fibrotic tissue, which may underlie the significant loss of muscle strength and endurance. Patients with DLS had a larger muscle CSA than those with DLK, which may explain the slightly higher muscle strength in patients with DLS. However, it was difficult to ascertain which comes first—spinal deformity or pathological changes in the PSM. This requires further investigation in future studies.

Limitations

This study had several limitations. First, this was a single-center study with a relatively small sample size. Therefore, large-scale multicenter studies are warranted to further investigate the relationship between histological features and radiological findings. Second, patients with DLS and DLK could present with several different deformity patterns, which may have differing degrees of PSM degeneration (11,15). Since the sample size was limited, this was not addressed in the current study. Third, the PSM strength was not compared between the concave and convex sides of DLS due to restrictions imposed by the handheld dynamometer and the lack of a standard protocol.

Conclusions

PSM degeneration patterns vary among the DSD subtypes with respect to morphology, muscle function, and histological characteristics. Histologically, patients with DLS showed higher fat infiltration on the concave side of the scoliosis than on the convex side, while exhibiting a lower extent of fibrosis than that observed in patients with DLK and the convex side of DLS. In DLK patients, ES showed significant atrophy, whereas MF in DLS patients showed more severe degeneration. Considering that ES accounts for main extensor to maintain the spinal sagittal balance, the loss of ES may serve as a driver for development of DLK. Functionally, poor muscle function was found in DLK patients. These findings highlight that PSM patterns predispose distinct etiologies to the development of different DSD subtypes. Furthermore, this finding suggests that more attention should be paid to the protection and intervention of PSM after DLK surgery. However, further investigation is warranted to determine the causal relationship between spinal deformities and patterns of PSM degeneration.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://qims.amegroups.com/article/view/10.21037/qims-2025-1878/rc

Data Sharing Statement: Available at https://qims.amegroups.com/article/view/10.21037/qims-2025-1878/dss

Funding: This work was supported by the National Natural Science Foundation of China (NSFC) (No. 82272545), the Affiliated Drum Tower Hospital of the Nanjing University Medical School (No. HB2387202403), and the China Postdoctoral Science Foundation (No. 2024M751403).

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://qims.amegroups.com/article/view/10.21037/qims-2025-1878/coif). A.K. is supported by The Affiliated Drum Tower Hospital of Nanjing University Medical School (No. HB2387202403) and the China Postdoctoral Science Foundation (No. 2024M751403). Z.L. is supported by The National Natural Science Foundation of China (NSFC) (No. 82272545). The other authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. The study was conducted following the Declaration of Helsinki and its subsequent amendments, and was approved by the Institutional Review Board (IRB) of Nanjing Drum Tower Hospital, Affiliated Hospital of Nanjing University Medical School (IRB No. 2021-389-01). Informed consent was obtained from all patients in this study for all procedures undertaken and all data obtained.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

References

1. Ailon T, Smith JS, Shaffrey CI, Lenke LG, Brodke D, Harrop JS, Fehlings M, Ames CP. Degenerative Spinal Deformity. Neurosurgery 2015;77:S75-91. [Crossref] [PubMed]
2. Shafaq N, Suzuki A, Matsumura A, Terai H, Toyoda H, Yasuda H, Ibrahim M, Nakamura H. Asymmetric degeneration of paravertebral muscles in patients with degenerative lumbar scoliosis. Spine (Phila Pa 1976) 2012;37:1398-406. [Crossref] [PubMed]
3. Malakoutian M, Noonan AM, Dehghan-Hamani I, Yamamoto S, Fels S, Wilson D, Doroudi M, Schutz P, Lewis S, Ailon T, Street J, Brown SHM, Oxland TR. Dysfunctional paraspinal muscles in adult spinal deformity patients lead to increased spinal loading. Eur Spine J 2022;31:2383-98. [Crossref] [PubMed]
4. Chua M, Hochberg U, Regev G, Ophir D, Salame K, Lidar Z, Khashan M. Gender differences in multifidus fatty infiltration, sarcopenia and association with preoperative pain and functional disability in patients with lumbar spinal stenosis. Spine J 2022;22:58-63. [Crossref] [PubMed]
5. Deyo RA, Mirza SK, Martin BI, Kreuter W, Goodman DC, Jarvik JG. Trends, major medical complications, and charges associated with surgery for lumbar spinal stenosis in older adults. JAMA 2010;303:1259-65. [Crossref] [PubMed]
6. Schwab FJ, Smith VA, Biserni M, Gamez L, Farcy JP, Pagala M. Adult scoliosis: a quantitative radiographic and clinical analysis. Spine (Phila Pa 1976) 2002;27:387-92. [Crossref] [PubMed]
7. Jang JS, Lee SH, Min JH, Han KM. Lumbar degenerative kyphosis: radiologic analysis and classifications. Spine (Phila Pa 1976) 2007;32:2694-9. [Crossref] [PubMed]
8. Hodges PW, Danneels L. Changes in Structure and Function of the Back Muscles in Low Back Pain: Different Time Points, Observations, and Mechanisms. J Orthop Sports Phys Ther 2019;49:464-76. [Crossref] [PubMed]
9. Chen X, Xu R, Yuan S, Fu W, Zhang X, Zhang Y, Wang L, Liu X. The Role of Paraspinal Muscle in Postoperative Coronal Balance Transition in Degenerative Lumbar Scoliosis: A Two-Year Follow-Up Study. Spine (Phila Pa 1976) 2025;50:528-36. [Crossref] [PubMed]
10. Wang G, Li Y, Zhang C, Liu P, Sun J. Erector Spinae Atrophy Correlates with Global Sagittal Imbalance and Postoperative Proximal Junctional Kyphosis Incidence in Lumbar Degenerative Kyphosis. Asian Spine J 2024;18:50-7. [Crossref] [PubMed]
11. Li J, Tang Z, Hu Z, Xu Y, Liang B, Qiu Y, Zhu Z, Liu Z. Sagittal Imbalance in Degenerative Kyphosis: Prevalence and Implication on Postoperative Mechanical Failure. Neurosurgery 2024;95:1026-39. [Crossref] [PubMed]
12. Kreiner DS, Shaffer WO, Baisden JL, Gilbert TJ, Summers JT, Toton JF, Hwang SW, Mendel RC, Reitman CANorth American Spine Society. An evidence-based clinical guideline for the diagnosis and treatment of degenerative lumbar spinal stenosis (update). Spine J 2013;13:734-43. [Crossref] [PubMed]
13. Steurer J, Roner S, Gnannt R, Hodler J. LumbSten Research Collaboration. Quantitative radiologic criteria for the diagnosis of lumbar spinal stenosis: a systematic literature review. BMC Musculoskelet Disord 2011;12:175. [Crossref] [PubMed]
14. Kuklo TR, Potter BK, Polly DW Jr, O'Brien MF, Schroeder TM, Lenke LG. Reliability analysis for manual adolescent idiopathic scoliosis measurements. Spine (Phila Pa 1976) 2005;30:444-54. [Crossref] [PubMed]
15. Kiram A, Hu Z, Man GC, Ma H, Li J, Xu Y, Qian Z, Zhu Z, Liu Z, Qiu Y. The role of paraspinal muscle degeneration in coronal imbalance in patients with degenerative scoliosis. Quant Imaging Med Surg 2022;12:5101-13. [Crossref] [PubMed]
16. Ding JZ, Kong C, Li XY, Sun XY, Lu SB, Zhao GG. Different degeneration patterns of paraspinal muscles in degenerative lumbar diseases: a MRI analysis of 154 patients. Eur Spine J 2022;31:764-73. [Crossref] [PubMed]
17. Wang M, Kiram A, Li J, Xu Y, Hu J, Qin X, Wang Y, Qiao J, Shi B, Mao S, Zhu Z, Qiu Y, Liu Z. The Contribution of Paraspinal Sarcopenia on Sagittal Imbalance in Degenerative Kyphosis. Neurospine 2025;22:680-91. [Crossref] [PubMed]
18. Liu S, Reitmaier S, Mödl L, Yang D, Zhang T, Becker L, Hoehl B, Schönnagel L, Diekhoff T, Pumberger M, Schmidt H. Quality of lumbar paraspinal muscles in patients with chronic low back pain and its relationship to pain duration, pain intensity, and quality of life. Eur Radiol 2025;35:3652-60. [Crossref] [PubMed]
19. Wu AY, Hong TH, Rosenfeld A. Threshold selection using quadtrees. IEEE Trans Pattern Anal Mach Intell 1982;4:90-4. [Crossref] [PubMed]
20. Valentin G, Maribo T. Hand-held dynamometry fixated with a tripod is reliable for assessment of back extensor strength in women with osteoporosis. Osteoporos Int 2014;25:2143-9. [Crossref] [PubMed]
21. Chen C, Yang S, Tang Y, Yu X, Chen C, Zhang C, Luo F. Correlation between strength/endurance of paraspinal muscles and sagittal parameters in patients with degenerative spinal deformity. BMC Musculoskelet Disord 2023;24:643. [Crossref] [PubMed]
22. Mehlem A, Hagberg CE, Muhl L, Eriksson U, Falkevall A. Imaging of neutral lipids by oil red O for analyzing the metabolic status in health and disease. Nat Protoc 2013;8:1149-54. [Crossref] [PubMed]
23. Rittié L. Method for Picrosirius Red-Polarization Detection of Collagen Fibers in Tissue Sections. Methods Mol Biol 2017;1627:395-407. [Crossref] [PubMed]
24. Dong LB, Wei YZ, Lan GP, Chen JT, Xu JJ, Qin J, An L, Tan HS, Huang YP. High resolution imaging and quantification of the nailfold microvasculature using optical coherence tomography angiography (OCTA) and capillaroscopy: a preliminary study in healthy subjects. Quant Imaging Med Surg 2022;12:1844-58. [Crossref] [PubMed]
25. Okabe K, Yaku K, Uchida Y, Fukamizu Y, Sato T, Sakurai T, Tobe K, Nakagawa T. Oral Administration of Nicotinamide Mononucleotide Is Safe and Efficiently Increases Blood Nicotinamide Adenine Dinucleotide Levels in Healthy Subjects. Front Nutr 2022;9:868640. [Crossref] [PubMed]
26. Ozenbas C, Ozturk CA, Altinok T. Quantitative MRI assessment of paraspinal muscles and the psoas: associations with low back pain. Quant Imaging Med Surg 2026;16:119. [Crossref] [PubMed]
27. Kokosova V, Krkoska P, Vlazna D, Dostal M, Ovesna P, Matulova K, Adamova B. Quantitative magnetic resonance imaging parameters of lumbar paraspinal muscles and their relationship to function and ageing in healthy subjects. Quant Imaging Med Surg 2025;15:6517-25. [Crossref] [PubMed]
28. Hyun SJ, Kim YJ, Rhim SC. Patients with proximal junctional kyphosis after stopping at thoracolumbar junction have lower muscularity, fatty degeneration at the thoracolumbar area. Spine J 2016;16:1095-101. [Crossref] [PubMed]
29. Tian Z, Li J, Xu H, Xu Y, Zhu Z, Qiu Y, Liu Z. Prediction of proximal junctional kyphosis and failure after corrective surgery for adult spinal deformity: an MRI-based model combining bone and paraspinal muscle quality metrics. Spine J 2024;24:2389-99. [Crossref] [PubMed]
30. Yagi M, Hosogane N, Watanabe K, Asazuma T, Matsumoto M. The paravertebral muscle and psoas for the maintenance of global spinal alignment in patient with degenerative lumbar scoliosis. Spine J 2016;16:451-8. [Crossref] [PubMed]
31. Hyun SJ, Bae CW, Lee SH, Rhim SC. Fatty Degeneration of the Paraspinal Muscle in Patients With Degenerative Lumbar Kyphosis: A New Evaluation Method of Quantitative Digital Analysis Using MRI and CT Scan. Clin Spine Surg 2016;29:441-7. [Crossref] [PubMed]
32. Kim H, Lee CK, Yeom JS, Lee JH, Cho JH, Shin SI, Lee HJ, Chang BS. Asymmetry of the cross-sectional area of paravertebral and psoas muscle in patients with degenerative scoliosis. Eur Spine J 2013;22:1332-8. [Crossref] [PubMed]
33. Boonyarom O, Inui K. Atrophy and hypertrophy of skeletal muscles: structural and functional aspects. Acta Physiol (Oxf) 2006;188:77-89. [Crossref] [PubMed]
34. Williams PE, Goldspink G. Changes in sarcomere length and physiological properties in immobilized muscle. J Anat 1978;127:459-68.
35. Gullbrand SE, Kiapour A, Barrett C, Fainor M, Orozco BS, Hilliard R, Mauck RL, Hast MW, Schaer TP, Smith HE. Restoration of physiologic loading after engineered disc implantation mitigates immobilization-induced facet joint and paraspinal muscle degeneration. Acta Biomater 2025;192:128-39. [Crossref] [PubMed]
36. Franchi MV, Longo S, Mallinson J, Quinlan JI, Taylor T, Greenhaff PL, Narici MV. Muscle thickness correlates to muscle cross-sectional area in the assessment of strength training-induced hypertrophy. Scand J Med Sci Sports 2018;28:846-53. [Crossref] [PubMed]
37. Jones EJ, Bishop PA, Woods AK, Green JM. Cross-sectional area and muscular strength: a brief review. Sports Med 2008;38:987-94. [Crossref] [PubMed]
38. Han G, Fan Z, Yue L, Zou D, Zhou S, Qiu W, Sun Z, Li W. Paraspinal muscle endurance and morphology (PMEM) score: a new method for prediction of postoperative mechanical complications after lumbar fusion. Spine J 2024;24:1900-9. [Crossref] [PubMed]