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Relationship between paraspinal muscle morphology and function in different directions in a healthy Chinese population at different ages: a cross-sectional study

Abstract

Background

Paraspinal muscle degeneration occurs with age; however, it is unknown whether strength and endurance change with muscle cross-sectional area (CSA) and fatty infiltration (FI) parameters in Chinese healthy individuals.

Methods

A total of 94 asymptomatic Chinese volunteers were enrolled in this study. The participants were divided into three groups: young (20–39 years old, n = 27), middle-aged (40–59 years old, n = 49), and elderly (≥ 60 years old, n = 18). CSA and FI of the psoas (PS), quadratus lumborum (QL), multifidus (MF), and erector spinae (ES) were measured using magnetic resonance imaging. The Bionix Sim3 Pro was used to evaluate the maximum isometric torque and the Ito test to evaluate endurance.

Results

The CSA of the PS and ES in the elderly group was smaller than those in the other groups, while the CSA of QL in the young group was larger than that in the other groups. There were differences in the MF and ES FI among the three groups. The maximum isometric torque and endurance test time decreased with increasing age; however, these differences were not statistically significant. Maximum isometric torque positively correlated with the average paraspinal muscle CSA and negatively correlated with the torque and FI of the MF and ES muscles. The endurance test was found to be positively correlated with the FCSA of the MF and to be negatively correlated with the FI of the MF and ES. PS and QL can predict the maximum isometric torque, and MF and PS can predict the endurance time.

Conclusion

MF and ES showed earlier degeneration than PS and QL. MF is the first paraspinal muscle to undergo functional area atrophy, and it plays an important role in the endurance test. The maximum moment of equal length in all directions of the lumbar spine is not completely symmetrical, but it is correlated with the imaging parameters of the paraspinal muscles. QL and PS were more activated in the lumbar activity.

Trial registration

The study was registered in Chinese Clinical Trial Registry and the registration number is ChiCTR2000039073 on 15/10/2020 (https://www.chictr.org.cn/showproj.html?proj=62785). Ethical Approval was obtained from the Peking University Third Hospital Medical Science Research Ethics Committee (IRB00006761-M2020305).

Peer Review reports

Introduction

Paraspinal muscles are critical in maintaining spinal stability and motor function. The active motor function unit of the spine consists of the muscles and ligaments of the paraspinal muscle [1]. At present, many studies have reported that paravertebral muscle degeneration is closely related to spinal degenerative diseases [2,3,4,5,6]. Magnetic resonance imaging (MRI) is mainly used to evaluate the degeneration of the paraspinal muscle, while cross-sectional area (CSA) and fat infiltration (FI) are commonly used to evaluate the paraspinal muscle [7,8,9]. However, imaging parameters, being static indicators, cannot measure the function of muscles in an active state. The CSA of the core muscles has been associated with the capacity of muscles to generate force [10], although the relationship is not perfectly linear. Therefore, functional evaluation of muscles is important for accessing paravertebral muscle function. The first measurement method of lumbar trunk muscle strength was proposed in 1964, which indirectly reflects muscle endurance by measuring the horizontal time of the upper body of volunteers [11]. Ito et al. [12] then proposed an improved endurance measurement method that has been widely used for the clinical evaluating patients with low back pain, but it is susceptible to psychological factors such as tester compliance and willpower. The evaluation methods for muscle function include isometric torque and isokinetic torque tests. Since isometric activity does not cause any motion, there is no need for the neuromusculoskeletal system to divert effort towards joint stability. Therefore, the isometric torque test can measure the maximum muscle strength produced by muscle contraction at a special joint angle [13, 14]. Previous studies have confirmed that the paraspinal muscle cross-sectional area is related to muscular strength in the flexion and extension direction [10, 15]; however this relationship remains unclear in other directions. This study aims to describe the imaging parameters of asymptomatic healthy Chinese individuals of different ages and to analyze the correlation among the cross-sectional area of paraspinal muscle, maximum isometric torque, and endurance.

Materials and methods

Patients

All volunteers underwent a detailed history taking before participating in the study. The inclusion criteria were as follows: (1) Age ≥ 20 years; (2) No low back pain in the previous six months; (3) No history of radicular symptoms; (4) No history of spinal scoliosis or surgery; (5) No coronal deformity or lumbar spondylolisthesis. General demographic information, such as height, weight, sex, and age, was documented for each participant.

Radiographic evaluation

Anteroposterior and lateral standing radiographs, particularly including the entire spine and pelvis, were obtained from all volunteers. Using the PACS system (Picture Archiving and Communication System, GE Healthcare, Mount Prospect, IL, USA), the following parameters were measured: Cobb angle, coronal vertical axis from the central sacrum vertical line (CSVL), thoracic kyphosis (TK, T5–T12), thoracolumbar kyphosis (TLK), lumbar lordosis (LL, L1–S1), lordosis of L4-S1, pelvic incidence (PI), pelvic tilt (PT), sacral slope (SS), sagittal vertical axis (SVA), T1-Pelvic angle (TPA), and global tile (GT).

Paraspinal muscle measurements

Magnetic resonance imaging (MRI) was performed on all participants using a 3.0 T system (Siemens, Germany or General Electric, USA) to measure muscle area and T2 signal intensity. Axial MRI images were aligned parallel to the middle of each disc at L2–L3, L3–L4, L4–L5, and L5–S1. The conditions of the psoas (PS), quadratus lumborum (QL), multifidus (MF), and erector spinae (ES) were analyzed using the cross-sectional area (CSA) and signal intensity (SI) from axial T2-weighted image. To reduced bias, the area of the muscles was divided by the intervertebral disc area at the same level and multiplied by 100 (muscle CSA/disc CSA × 100) to represent the lumbar muscularity in each individual. Similarly, the degree of fat change was estimated as the muscle-fat index at each level by multiplying the muscle–subcutaneous fat SI ratio by 100 [7]. The region of interest (ROI) of the lean muscle tissue area, excluding fatty infiltration, was drawn to determine the functional cross-sectional area (FCSA), the muscle–fat index of the lean muscle within the ROI was defined as the lean muscle–fat index (LMFI). The gross cross-sectional area (GCSA) was determined by drawing the outer perimeter of the muscle, including any areas of intramuscular fat, and its muscle-fat index was defined as the total muscle-fat index (TMFI). The GCSA was not measured in PS and QL because it was too difficult to distinguish their borders, and the T2 signal intensities of the PS and QL were measured using the FCSA instead [16].

Function test

Isometric testing of the paraspinal muscle was performed using the Bionix Sim3 Pro (Physiomed, Germany). The participants stood on the instrument, fixed their knees, pelvis, and shoulder joints, and crossed their hands over their chests (Fig. 1). Fixation in the anterior superior iliac spine has been confirmed to lead to accurate and reliable measurements of the back musculature in the standing position [17], and the sitting posture reduces possible compensatory mechanisms by hip flexors. Before the test, the subjects were warmed up with isokinetic movement at a 60°/s angle for 3–5 min and then instructed to perform rotation, flexion, extension, and lateral flexion. Participants were asked to perform isometric contracting for ten seconds in each direction after which the maximum isometric moment values of the subjects' movements in each direction were recorded.

Fig. 1
figure 1

Study setup of the Bionix 3D isokinetic Core Muscle Assessment Training system

The endurance test was performed according to the Ito test [12]. Participants were instructed to raise their upper body to an individually adjusted endpoint with the arms kept parallel to the body axis, the cervical spine held in a neutral position, and both feet on the examination table throughout the entire test. Task failure was defined as a drop in the trunk angle greater than 10° at any point. The test started with a trial for recognition, followed by a 5 min rest for baseline data, and then two recorded trials with a 5 min rest in between. The test result was identified as the best record of the two trials.

Statistical analysis

Data were analyzed using SPSS software version 24 (SPSS Inc, Chicago, IL, USA). Descriptive results are expressed as the mean and standard deviation (SD) for continuous variables with an approximately normal distribution. Categorical values were presented as frequencies and percentages. Based on the age data, the participants were divided into three groups, and the normality and homogeneity of variance of the relevant data were tested. Analysis of variance or the Mann–Whitney U test of independent samples was used to verify whether there were differences between the three groups. The relationship between the paraspinal muscle FCSA and FI, endurance test time and maximum isometric contraction torque was evaluated using Spearman’s correlation. Stepwise linear regression analysis was used to establish the predictive formulas for the maximum isometric contraction torque and the endurance test time of the volunteers in each direction based on the FCSA and LMFI at each level. Statistical significance was set at a p-value < 0.05.

Ethics approval and consent to participate

All volunteers gave informed written and oral consent. Written informed consent was obtained from each participant and the study was performed in accordance with the Declaration of Helsinki as revised in 2013. The study was registered in Chinese Clinical Trial Registry and the registration number is ChiCTR2000039073 on 15/10/2020. Ethical Approval was obtained from the Peking University Third Hospital Medical Science Research Ethics Committee (IRB00006761-M2020305).

Result

Patient and radiographic characteristics

In total, 104 asymptomatic volunteers were recruited for this study, and only 94 volunteers were finally included. There were 37 males and 57 females, with an average age of 46.8 years (range, 24–75 years). The subjects were divided into 3 groups according to their age including the young group (20–39 years old), the middle-aged group (40–59 years old), and the elderly group (≥ 60 years old). Their general demographic data and radiographic parameters are summarized in Table 1. There were no significant differences among the other parameters except for age and BMI; TK, LL, PT, SVA, TPA, and GT increased with age, whereas LL-TK decreased with age.

Table 1 Clinical characteristics and radiographic parameters of whole spine X-ray in the young, middle-aged and elderly groups

Paraspinal muscle characteristics

For the PS CSA, MF GCSA and ES FCSA, there was no significant difference between the young and middle-aged groups, and both were larger than those of the elderly group. However, the MF FCSA has a statistically significant difference among the three groups. The elderly group showed significantly lower ES GCSA at all levels except L4-5 compared to the young group. The young group had a greater QL CSA than the other two groups. (Table 2, Fig. 2).

Table 2 Lumbar muscularity (CSA of muscle-disc ratio*100) of the paraspinal muscles of the three groups using MRI
Fig. 2
figure 2

Comparison of cross-sectional area three groups

The LMFI of the PS and QL of the elderly and middle-aged groups were higher than those of the young group at the L2-3 and L3-4 levels, and the middle-aged group had a higher QL LMFI than the young group at the L4-5 level. There was no significant difference in PS LMFI among the three groups at L4-5 level, but the elderly group was higher than young group at L5-S1 level. For MF and ES, the LMFI and TMFI values in each group increase with age at all levels, and there are significant difference among three groups. (Table 3, Fig. 3).

Table 3 Degree of fatty change (mean signal intensity of muscle-subcutaneous fat ratio*100) of the paraspinal muscles of three groups using MRI
Fig. 3
figure 3

Comparison of muscle-fat index among three groups

Functional evaluation

The results of the maximum isometric torque and endurance tests are listed in Table 4. The torque in each direction of lumbar movement decreased with increasing age. Similarly, the endurance test time was progressively shorter among the three groups, but the difference was not statistically significant.

Table 4 Maximum isometric contraction torque in all directions and the endurance test time among the three groups

Correlation analyses showed that the maximum isometric torque in all directions positively correlated with the average paraspinal muscle CSA of L2-S1, and the correlation was stronger with PS and QL than with the posterior vertebral muscles. We also found a negative correlation between the torque and the LMFI of the MF and ES. The endurance of the paraspinal muscle was positively correlated with the MF FCSA and negatively correlated with the MF and ES LMFI. (Table 5).

Table 5 Spearman correlation coefficient between the mean values of the paraspinal muscle parameters from L1 to L5, HGS, maximum isometric contraction torque, and the Ito test

By incorporating paraspinal muscle CSA and MFI as independent variables into stepwise multiple linear regression analyses were performed to identify potential relationships between the maximum isometric and paraspinal muscle imaging parameters. The maximum isometric torque in all directions was corelated with the PS and QL FCSA, and in the rotation, flexion and lateral flexion to the left directions was corelated with MF and ES FCSA. For the endurance test time, although the R2 value was lower, it could still be predicted by the FCSA of the MF and PS (Table 6).

Table 6 Multiple linear regression analysis of the relationship between maximum isometric torque, endurance test time, and paraspinal muscle parameters

Discussion

In this study, we quantified the cross-sectional area (CSA) and fatty infiltration (FI) of the paraspinal muscles using MRI, and measured the maximum isometric torque of the lumbar region in all motion directions using the BIONIX 3D isokinetic Core Muscle Assessment Training system in 94 men and women aged 24–75 years-old. This study demonstrated that multifidus and erector spinae muscles exhibited earlier degeneration compared psoas and quadratus lumborum muscles in Chinese healthy population, and the MF was the earliest area to experience atrophy. QL and PS were found to be more activated during lumbar activity. Few studies have examined the relationship between the quantitative assessment of the paraspinal muscles on MRI and the maximum isometric muscle force torque.

We measured the coronal parameters (Cobb angle and CVA) among different age groups, and the coronal balance was good without significant deformity. Previous studies with large samples of Chinese people have shown [18, 19] that TK, PT, SVA, and TPA increase with age, whereas LL decreases with age. Our findings were consistent with these results. This suggests that within our study sample, there was no significant spinal degeneration, even in the elderly group. This decreases the likelihood of sampling errors arising from paraspinal muscle degeneration associated with changes in spinal bone structure.

Magnetic resonance imaging is the gold standard for estimating muscle mass among numerous other measuring techniques. We found an age-related decrease in functional cross-sectional area (FCSA) and an increase in the fatty infiltration (FI) of the paraspinal muscles at all levels. These findings are consistent with previous studies [20,21,22], but we found that different paraspinal muscles have different degenerative processes. For the psoas major muscle, the middle-aged group and young group maintained similar CSA, but their FI was comparable to that of the elderly group. This suggests that as age increases, paraspinal muscle fat infiltration occurs earlier than a reduction in the muscle's cross-sectional area. The CSA and LMFI of Psoas quadratus are similar between middle-age and elderly groups, suggesting that the regression of QL gradually slows down with age. For multifidus muscle, the GCSA and TMFI in the middle-aged group are similar to those of psoas major, but there are differences in FCSA and LMFI among the three group. This indicats that muscle atrophy and fat infiltration in the effective muscle units of MF occur earlier and worsen with age. The degeneration of MF is the earliest among all paraspinal muscles. A previous study on changes in the paraspinal muscles in patients with lumbar spinal stenosis [16] showed that the degeneration of the multifidus muscle was more obvious than that of the psoas major muscle. The erector spinae muscle FCSA in middle-aged group is similar to that of the young group, but the LMFI gradually increases among the three groups. This suggests that degeneration is primarily attributable to fat infiltration and occurs earlier than in the psoas major muscle. Considering the function of the paraspinal muscles [23], hypertrophy of the psoas may be the result of increased activity due to the degeneration of the multifidus as a stabilizer. Meanwhile, the PS functions as a flexor of the hip, and sufficient stimulus can be provided to reduce PS atrophy by hip flexion. QL acts in the coronal plane because of its lateral positioning; therefore, it is more easily activated during daily activities, such as walking. As older adults exhibit reduced coronal-plane trunk motion during everyday activities [24], resulting in lower mechanical demands, it is likely that insufficient stimulus contributes to slow muscle atrophy in the QL.

The paraspinal muscle cross-sectional area is a determinant of isometric trunk muscle strength [25]. Although there was no significant difference in torque among the three groups, muscle strength gradually decreased with age. Correlation analysis showed that, compared to MF and ES, the CSA of PS and QL had a stronger correlation with lumbar spine activity. According to the linear regression analysis model, the FCSAs of PS and QL more accurately predicted the maximum isometric torque of the lumbar spine in all directions.

Regarding rotation, Ng JK [26] et al. found that significant differences in the activity between right and left axial rotation were demonstrated in the external oblique, internal oblique, latissimus dorsi, and iliocostalis lumborum muscles, while no difference was observed in the rectus abdominis and multifidus muscles using electromyography. Our research found that the maximum torque in the left and right rotation directions related to the paraspinal muscles are not exactly the same. This reflects that the muscles mobilized in rotation directions are not completely symmetrical. It is expected that the larger quadratus lumborum contributes to the coronal movement of the lumbar spine. There is a study shows that, when compared with their untrained counterparts, male prepubescent tennis players had larger psoas and quadratus lumborum muscle volumes, but no significant difference in multifidus and erector spinae muscles [27], suggesting that QL and PS were more activated in the lumbar activity.

The expected corresponding roles of the erector spinae (ES) and multifidus (MF) in lumbar spine extension were not observed. By measuring the pennation angle and muscle thickness of L3-4 erector spinae muscles using ultrasound and electromyography, Cuesta-Vargas A [28, 29]et al. found that these factors had a moderate effect on torque changes during maximum isometric extension of the lumbar spine in a neutral position(R2 = 0.69). Schlaeger S [30] et al. found that the maximum isometric contraction moment measured in the sitting position was significantly and positively correlated with the CSA of the erector spinae and psoas major muscles, and ES muscle proton density fat fraction remained a statistically significant predictor of relative extensor strength (R2 = 0.34). We did not find the independent correlation between the ES and the lumbar extension, which may be due to the fact that our sample have larger average age compared to the above study, and the ES degeneration is more severe, so it could not play a sufficient role in stretching activities. Secondly, our study was conducted under the condition of maximum isometric contraction, the fiber length of ES is not limited to the lumbar segment, which cannot fully utilize the advantages brought by its long arm during isometric contraction. Finally, previous studies have found that the stabilization of joints while twisting is far more important to the lumbar spine than the production of large levels of axial torque [31]. Compared to the trunk muscles in front of the lumbar spine, the MF and ES positioned at the back play stabilizing roles during movement. Therefore, the maximum rorque correlation with the PS and MF is more pronounced. The Ito test was used to evaluate paraspinal endurance. The MF play a critical role in the dynamic stability of the lumbar spine [32],while the PS is located in front of the lumbar vertebrae and plays an antagonistic role in posterior extension activity. They maintain the stability of the lumbar together, which explain why their CSA can predict endurance function.

The present study had several limitations. Firstly, the study population may not be representative of the general population because the participants were from only one region of China and there were some differences in the sample sizes among the three groups. Secondly, the participants were unfamiliar with the isometric test process and could not exert maximum strength, which affected the results. To address this issue, we instructed them to be adequately warmed before performing the test and to perform isokinetic movements in all directions to familiarize themselves with the force pattern to reduce errors. Thirdly, our study did not include patients with lumbar degenerative diseases, so we were unable to investigate the effect of paraspinal muscle which under pathological conditions on the isometric torque. Finally, we did not measure the pinnation angle or degree of muscle activation, which may have affected the isometric torque. This needs to be refined with more diverse tests, such as ultrasonography or electromyography.

Conclusion

In conclusion, we measured the maximum isometric torque, FCSA, and FI of the paraspinal muscles in healthy Chinese populations across various agegroups using BioniX Sim3 Pro and MRI. This study offers valuable insights into paraspinal muscle function and morphology. The degeneration pattern of different paraspinal muscles is varies, the fat infiltration appearing earlier than muscle atrophy, and posterior muscles is earlier than anterior muscles. MF is the first paraspinal muscle to undergo functional area atrophy, but it plays an important role in endurance testing. PS and QL have a strong influence on the maximum isometric torque of the lumbar spine in all directions, indicating the importance of paying more attention to them in clinical practice.

Availability of data and materials

The datasets used and/or analysed during the current study available from the corresponding author on reasonable request.

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Acknowledgements

Not applicable

Funding

This study was supported by the National Natural Science Foundation of China (ID:82272540), Beijing Natural Science Fund Projects(L232127) and Key Clinical Projects of Peking University Third Hospital (No. BYSYZD2022028).

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Authors and Affiliations

Authors

Contributions

The investigations were by Yinhao Liu, Lei Yuan and Jiajun Ni and clinical data were collected by Yinhao Liu and Lei Yuan. The original draft was written by YH L. The funding was provided by Yan Zeng and Lei Yuan. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Yan Zeng.

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Ethics approval and consent to participate

All volunteers gave informed written and oral consent. Written informed consent was obtained from each participant and the study was performed in accordance with the Declaration of Helsinki as revised in 2013. The study was registered in Chinese Clinical Trial Registry and the registration number is ChiCTR2000039073 on 15/10/2020 (https://www.chictr.org.cn/showproj.html?proj=62785). Ethical Approval was obtained from the Peking University Third Hospital Medical Science Research Ethics Committee (IRB00006761-M2020305).

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Not applicable.

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The authors declare no competing interests.

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Liu, Y., Yuan, L., Zeng, Y. et al. Relationship between paraspinal muscle morphology and function in different directions in a healthy Chinese population at different ages: a cross-sectional study. BMC Musculoskelet Disord 25, 738 (2024). https://doi.org/10.1186/s12891-024-07842-y

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