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Preliminary investigation of spinal level and postural effects on thoracic muscle morphology with upright open MRI

Abstract Objective Spinal‐muscle morphological differences between weight‐bearing and supine postures have potential diagnostic, prognostic, and therapeutic applications. While the focus to date has been on cervical and lumbar regions, recent findings have associated spinal deformity with smaller paraspinal musculature in the thoracic region. We aim to quantitatively investigate the morphology of trapezius (TZ), erector spinae (ES) and transversospinalis (TS) muscles in upright postures with open upright MRI and also determine the effect of level and posture on the morphological measures. Methods Six healthy volunteers (age 26 ± 6 years) were imaged (0.5 T MROpen, Paramed, Genoa, Italy) in four postures (supine, standing, standing with 30° flexion, and sitting). Two regions of the thorax, middle (T4‐T5), and lower (T8‐T9), were scanned separately for each posture. 2D muscle parameters such as cross‐sectional area (CSA) and position (radius and angle) with respect to the vertebral body centroid were measured for the three muscles. Effect of spinal level and posture on muscle parameters was examined using 2‐way repeated measures ANOVA separately for T4‐T5 and T8‐T9 regions. Results The TZ CSA was smaller (40%, P = .0027) at T9 than at T8. The ES CSA was larger at T5 than at T4 (12%, P = .0048) and at T9 than at T8 (10%, P = .0018). TS CSA showed opposite trends at the two spinal regions with it being smaller (16%, P = .0047) at T5 than at T4 and larger (11%, P = .0009) at T9 than at T8. At T4‐T5, the TZ CSA increased (up to 23%), and the ES and TS CSA decreased (up to 10%) in upright postures compared to supine. Conclusion Geometrical parameters that describe muscle morphology in the thorax change with level and posture. The increase in TZ CSA in upright postures could result from greater activation while upright. The decrease in ES CSA in flexed positions likely represents passive stretching compared to neutral posture.


| INTRODUCTION
Spinal geometry in upright postures is different than in supine. [1][2][3] Most symptoms of spinal deformities are worse in a standing posture 4 and upright clinical measurements are important for better diagnosis and treatment outcomes. 5,6 For example, a study in people with lowback pain found that geometric parameters such as lumbosacral angle, lordosis, and disc height were significantly different in upright postures in 70% of patients when compared to their supine measurements. 6 Another study showed that the Cobb angle of the thoracolumbar major curve was significantly higher, and the lumbar lordosis was considerably lower while standing than when measured supine. 2 It is intuitive that with the change in spinal geometry in different postures, the overall morphometry, position, moment-arm and activation levels of the surrounding musculature 7 would also change.
Closed-bore magnetic resonance imaging (MRI) requires the subject to be in a supine or prone position. Our knowledge of muscle morphology is thus restricted to the non-upright postures. This poses a challenge in using the muscle data obtained from clinical imaging in the development of biomechanical spine models, and personalized treatment strategies. 8 Open and upright MRI allows subjects to be imaged in different weight-bearing postures and has shown some encouraging results in visualizing muscles in vivo. Upright imaging studies that focused on the lumbar spine have shown significant changes in muscle morphology between supine and upright postures [9][10][11][12][13] and differences between the flexed and extended positions. 14 In the cervical spine, it was shown that the position of the head and neck significantly affected area and location of the sternocleidomastoid and posterior neck muscles. 15 Almost all upright MRI studies have been on the cervical and lumbar spine. However, spinal extensor muscle strength is shown to be more important for muscular support of the thoracic spine 16,17 and is presumed to have the greater clinical significance with respect to thoracic spinal health. 18,19 Thoracic hyperkyphosis, an exaggerated anterior curvature of the thoracic spine, is known to affect 20% to 40% of older adults above the age of 60 years, 20 with an average cost of about 54 000 USD for principal diagnosis of spine curvature. 21,22 Previous research has reported that lower muscle density, 23 smaller muscle volume, 24 and reduced extensor muscle strength 16,[25][26][27] in the lumbar spine is associated with kyphosis 16,[25][26][27] . On the other hand, the findings of a recent longitudinal study suggested that smaller cross-sectional area (CSA) and lower density (muscle-to-fat ratio) of the thoracic muscles, especially those situated nearest to the kyphosis curvature was associated with kyphosis severity more than those in the lumbar region. 18 Some studies have assessed spinopelvic musculature in upright postures while trying to understand the fundamental morphological changes in healthy individuals. Shaikh et al assessed and quantified muscles at three lumbar levels 13 and in the pelvic region in different upright postures. This study follows a similar approach for investigating two paraspinal extensor muscles-erector spinae (ES) and transversospinalis (TS) and one posterior muscle-trapezius (TZ) in the thoracic spine. Although the TZ is mainly involved in stabilizing and controlling the scapula, it has been noted that correction of thoracic kyphosis should be included among exercises designed to achieve normal scapular alignment, which could imply that the TZ may be involved in development of hyperkyphosis. 28,29 In light of the high prevalence of adult spinal deformities, the incremental cost effectiveness ratio of correction surgery to nonsurgical management at 3 year follow-up was estimated as 375 000 USD. 22,30 Proximal junctional kyphosis (PJK) is a well-documented post-surgical clinical problem where understanding the thoracic muscle morphology is relevant. PJK often manifests as a kyphotic change in the disc space of vertebral body adjacent to the fusion. 31 PJK typically occurs in the thoracolumbar junction 32,33 or upper thoracic levels [33][34][35] and is found to be prevalent in about 17% to 39% of patients 36 who undergo a fusion surgery in the thoracolumbar spine.
PJK is attributed to the failure of the soft tissue at the back 22 such as loss of muscle CSA and density, 37 atrophy, 38,39 altered muscle activations, 40 and reduced muscle strength. 38,41 Furthermore, clinical studies by Yagi et al. 42 suggested that 41% of patients post lumbar degenerative scoliosis surgery, developed progressive global kyphosis in the thorax. Clearly, PJK is a multifactorial problem where the health of the surrounding musculature, especially those in the thoracic spine, is important. 43,44 Given that paraspinal musculature in the thorax plays a vital role in maintaining weight-bearing postures, onset and progression of adult spinal deformity, and post-surgical pathologies, there is a need to quantitatively investigate thoracic musculature in different postures in vivo. Thus, with an aim to fill this literature gap, our study had two objectives. The first objective was to quantitatively investigate the parameters such as CSA and position of muscles in the thoracic region. The second objective was to study the effect of spinal level and posture on these muscle parameters.
While our previous article 45 focused on outlining detailed segmentation guidelines and assessing segmentation repeatability on the thoracic muscle data, this study focuses on investigating the effect of upright, seated, and supine postures on thoracic muscle morphometry.

| Study participants
Six healthy participants were recruited (five male and one female, age 26 ± 6 years, height 177 ± 9 cm, and weight 75 ± 10 kg, BMI 24 ± 3 kg/m 2 with no history of spine conditions).

| Image acquisition
The imaging protocol for human-study was approved by the Clinical Research Ethics Board (CREB) of the University of British Columbia and the Vancouver Coastal Health Research Institute (H10-00942).
All the participants signed an informed and written consent along with permission for publishing their imaging data without disclosing any per- The volunteers were systematically repositioned twice in every posture, such that T4-T5 or T8-T9 regions were centered in the scanner. Images were obtained from a stack of continuous, parallel slices (typically 9 or 11 in number) with the middle slice aligned to the center of the intervertebral disc (T4-5 or T8-9) and parallel to it ( Figure 2A). The number of slices in a stack was varied in order to cover the entire length of the thoracic regions under consideration.
To accurately detect the required thoracic levels in each region

| Image analysis
Segmentation guidelines described previously 45 were used to manually segment regions of interest of TZ, ES, and TS in 3D Slicer (Version 4.10.12, http://www.slicer.org). 46 Magnitudes of CSA and positions (radius and angle) were computed as shown in Figure 2B in MATLAB (version R2019a, Natick, Massachusetts: The MathWorks Inc.). CSA (mm 2 ) was determined by manually tracing the outline of the muscle boundary on every slice, and the centroid was defined as its geometric center. Radius (mm) was measured as the absolute distance between the centroid of the muscle and the vertebral body. 15 Angle, A (degrees) was measured between the line connecting centroids of the muscle and the vertebral body, and the line connecting the centroids of vertebral body and the vertebral canal. Both the vertebral body and the vertebral canal were segmented as circles with constant radii for a given subject as shown in Figure 2B. The anterior-posterior (Radius × cosA) and medial-lateral (Radius × sinA) distances were then computed. Intra and inter-rater repeatability of segmentation for all muscles was generally good/excellent (average Intraclass Correlation Coefficient ICC [3, 1] = 0.9 with ranges of 0.56-0.98). 45

| RESULTS
The effects of level and posture, and any interactions on CSA, radius and angle are presented for each muscle at each thoracic region, with summative data presented in Figures 3, 4, and 5 and Table 1, Tables 2 and 3.
Note that posture effects for each thoracic region are presented as averaged across the two spinal levels (Tables 1 and 2), and the spinal level effects are presented as averaged across all four postures (Table 3).

| Trapezius
The CSA of TZ was found to be 40% (P = .0027) larger at T8 compared to T9 ( Figure 3A), while no significant level effect was observed between T4 and T5. Posture significantly (P = .0001) affected the CSA at T4-T5 region with an increase of approximately 10%, 12%, and 23% in standing, flexed and sitting postures when compared to supine (Figure 3A and

| Erector spinae
Significant level effects were observed for ES CSA across both the spinal regions. The CSA was larger by 12% (P = .0048) and 10% (P = .0018) at T5 than T4 and at T9 than T8, respectively ( Figure 3B).
For posture, no significant changes were detected at T8-T9 region. At T4-T5 region, the CSA decreased by 10% (P = .0508) in flexion when compared to supine ( Figure 3B and Figure 5). No interaction was detected between levels and postures at T4-T5, but significant interaction was detected at the lower thoracic region, T8-T9 (P = .0052).
Specifically, at level T8, there was 7%, 8%, and 7% decrease in CSA for supine, flexed and sitting compared to standing. At level T9, there was 3% increase, 4% and 6% decrease for standing, flexed and sitting respectively compared to supine, and a 7% and 9% decrease for flexion and sitting compared to standing.

| Transversospinalis
TS CSA showed opposite trends at the two regions under consideration. The CSA was 16% (P = .0047) smaller at T5 than the T4 level ( Figure 3C and Figure 5), but it was larger by about 11% (P = .0009) F I G U R E 3 Box plots of muscle CSA (averaged across all subjects) shown for each posture by spinal level. The median is marked by the horizontal line inside the box, the ends of the box are the upper and lower quartiles, and the whiskers are the two lines outside the box that extend to the highest and lowest observation. Outliers are represented by circular markers above or below each box. Post hoc significant marked by notations. * = significant from supine, $ = significant from standing, # = significant from flexion. CSA, cross-sectional area ( Figure 3C) at T9 than the T8 level. Although posture did not seem to have any effect on CSA at T8-T9, there was an 8% and 10% decrease in upright standing and flexion when compared to supine, a 2% decrease and 7% increase in standing and sitting compared to flexion at T4-T5 (P = .0019). The interactions between level and posture were found to be not significant for our data.
However, no significant difference was found between levels T8 and T9. On the other hand, the angular position was found to be consistent across T4 and T5 levels, while the angle was 18% (P = .0143, Friedman test) larger at T8 than at T9 ( Figure 4B). For postures, the radius at T4-T5 for standing, flexion and sitting was respectively 8%, 7% and 10% more than that in supine, and was 2% more in sitting than in flexion (P = .0005) Figure 4A). The angle at T8-T9 was 21%, 10%, and 16% smaller in standing, flexion and sitting compared to T A B L E 1 Average muscle crosssectional area (CSA in mm 2 ), radius (mm), and angle (degrees) for all subjects across different postures (averaged across levels T4 and T5). Significant results (P < .05) from Neuman Keuls post-hoc indicated by symbols in legend. The CSA value is the sum of right and left sides.

| Erector spinae
While there were no level-effects observed between T4 and T5 for both radius and angle, the ES radius at T9 was always found to be larger than at T8 (P = .0156), but the magnitude of difference was negligible (1%). While radius did not vary with posture at both spinal levels and the ANOVA showed no interaction between levels and posture for the given dataset, the angle decreased by about 12% at T8 and about 14% at T9 from supine to all upright postures. The angle between stand to sit significantly increased at T9, with a small difference in magnitude (4%) Figure 4B).

| Transversospinalis
No significant level-effects were noted in TS radius across both thoracic regions. However, the angles at T4 and T8 were larger by 3%

| DISCUSSION
The CSA and position of three muscles were quantitatively investigated at two levels in the thoracic spine. The effect of thoracic level and posture on the muscle parameters was also examined.

| Comparison with literature
The magnitudes of CSAs reported this study ( T A B L E 3 Average muscle cross-sectional area (CSA in mm 2 ), radius (mm), and angle (degrees) for all subjects across T4, T5, T8, and T9 levels (averaged for all postures). Significant results (P < .05) from Neuman Keuls post-hoc indicated by symbols in legend. The radius and angles measured in this study essentially give the anterior-posterior (A-P) and medial-lateral (M-L) distances from the vertebral body center, which is also a conventional approach for comparing relative position of a muscle in axial radiographs. 48

| Trends due to level and posture
Most observed changes in thoracic muscle CSA were expected due to the muscle anatomy. While, the large difference (40%) in CSA for TZ from T8 to T9 characterizes its tapering, 45,57 a large SD ( Table 2) is indicative of wide variation in insertion points along lower thoracic levels (T8 to T12). 45,58 In addition, paraspinal muscle (especially ES in the entire spinal column and multifidus in the thoracolumbar and lumbar region) size is known to typically increase caudally 45,58,59 and a similar trend was observed in our study (Table 3 and Figure 3B).
The increase (up to 23%) in TZ CSA at T4-T5 region in upright postures when compared to supine could be due to muscle activation in upright postures. Our results, however, showed a decrease (about 10%) in CSA during upright flexion compared to erect seated position, which is contrary to the findings in the literature, 60 where substantial activation was observed in the middle and lower TZ in the slouched sitting compared to sitting erect. While TZ is known to hyperactivate during slouching, we acknowledge the possibility of these muscles undergoing passive stretching during torso flexion. 61 Passive stretching is a concurrent effect of the lengthening of the muscles, a mechanical behavior of transverse contraction during longitudinal stretching, which is expected for any typical elastic material or tissue.
Furthermore, the head/neck posture was not controlled in our study and could also affect the CSA measures of TZ. Further investigation on the muscle activation levels in different postures is required to accurately validate our assertion.
O'Sullivan et al. 62 showed that the superficial lumbar multifidus and thoracic ES muscles are more active in maintaining optimally aligned, erect postures, than during the adoption of passive postures.
Although ES and TS are extensor muscles, which act to maintain more active extended postures, the decrease in CSA in upright standing (8% for TS at T8-T9) compared to supine or sitting could be due to the fact that the participants in our study may have adopted a slightly slouched and comfortable upright posture since they were not instructed to hold an active and erect trunk. Furthermore, the decrease in CSA at both regions going from neutral to flexed posture could be attributed to passive stretching, which aligns with the findings for lumbar ES and multifidus. 61 Moreover, the significant levelposture interaction suggests that activation may not be uniform throughout the length of the muscle and is level and posture dependent.
Thoracic spine position is known to significantly affect scapular kinematics, 29 where the scapula is more elevated and protracted in a

| Clinical implications
Paravertebral muscle size and health was found to have a crucial influence on standing and walking in adults, post-surgery for spinal deformity correction. 73

| Limitations of the study
Interpretation of the data presented in this study must acknowledge the study's limitations. The small sample size of six individuals may influence the observed level and postural trends on the muscle parameters. While thoracic hyperkyphosis is more common in elderly women, our data (healthy and male-dominated) might not be suitable to make direct comparisons with the deformity cohort. We also acknowledge the small sample size being a shortcoming for using our data as normative muscle data representing the healthy cohort. Furthermore, the subjects were asked to hold postures as naturally as possible without exerting load on the support bars and hence muscle activations were not controlled for or measured during this study.
Also, due to the restricted field of view of the imaging coil, the muscle could not be imaged along its entire length, which would give more

CONFLICT OF INTEREST
The authors declare that they have no conflict of interest.