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63 (); 29-34
doi:
10.1016/j.jor.2024.10.037

Relationship between the course of postoperative pelvic axis rotation and shoulder balance in patients with Lenke types 1 and 2 adolescent idiopathic scoliosis

Department of Orthopaedic Surgery, Faculty of Medicine, Oita University, 1-1 Idaigaoka, Hasama-machi, Yufu-shi, Oita, 879-5593, Japan

⁎Corresponding author: Masashi Miyazaki. masashim@oita-u.ac.jp

Disclaimer:
This article was originally published by Reed Elsevier India Pvt. Ltd. and was migrated to Scientific Scholar after the change of Publisher.

Abstract

Abstract

Posteroanterior radiographs of patients with adolescent idiopathic scoliosis (AIS) show bilateral differences in the iliac wings. This is due to pelvic axis rotation (PAR) associated with scoliosis. We often encounter cases wherein the PAR changes with surgery and postoperatively. We investigated the course of preoperative PAR and the relationship between PAR and shoulder balance in patients with Lenke 1,2 AIS.

In total, 28 patients with Lenke 1,2 AIS undergoing scoliosis correction were included. The PAR and shoulder parameters were measured on posteroanterior radiographs. The correlation between the measured parameters and the extent of changes in each parameter was also examined.

Eleven patients (39.3 %) underwent preoperative PAR. Six patients (21.4 %) showed a greater change in PAR from 1 week to 2 years postoperatively. The rotation did not change significantly from preoperatively to immediately postoperatively but changed during the first three months postoperatively. The rotation group had significantly more balanced shoulders at 2 years (P = 0.025). The rotation group had a greater change in shoulder balance in the postoperative course significantly (P < 0.05). The extent of change in pelvic rotation from 1 week to 2 years postoperatively correlated with the extent of change in shoulder balance.

The PAR in patients with Lenke 1,2 AIS significantly changed during 3 months postoperatively. Patients with Lenke 1,2 AIS with preoperative PAR can be expected to have postoperative shoulder rebalancing.

Keywords

Adolescent idiopathic scoliosis
Pelvic axis rotation
Shoulder balance
Surgery
1

1 Introduction

Adolescent idiopathic scoliosis (AIS) is a complex deformity of the spine and pelvis in which the trunk deviates from its normal plane of symmetry.1 Although it is primarily a spine deformity, the pelvis is considered the “pelvic vertebrae” and is also considered part of this deformity. Recently, it has been reported that global alignment, including the pelvis as well as the spine, affects clinical outcomes, and balance including the pelvis should be considered.2–4 Pelvic tilt has also been reported to affect trunk and shoulder balance in AIS.5,6

Similar to the spine, the pelvis shows three-dimensional changes not only in the sagittal and coronal planes but also in the axial plane; patients with AIS often show bilateral differences in the iliac wings on anterior radiographs. This has been reported in previous anatomical studies as pelvic axis rotation (PAR).7–9 Most of the rotation direction of PAR was the same as the main curve of the thoracic spine and is associated with trunk rotation8,10 Although changes in the sagittal and coronal planes of the pelvis have often been reported in AIS, there are few reports on the effect of rotation in the axial direction and its impact remains unclear.

In corrective scoliosis surgery, it is important to not only straighten the curved spine but also achieve balanced shoulders. The aesthetics of the shoulders play an important role in patient satisfaction with surgical outcomes. However, postoperative shoulder balance is relatively difficult to predict, with 55.4 % of patients still having unbalanced shoulders two years after surgery.11–14 Interestingly, it is also known that shoulder imbalance immediately after surgery can be restored in the postoperative course.15,16

Similarly, PAR has been reported to change over the course of the preoperative and postoperative periods.17,18 The pelvis is an important component of trunk and shoulder balance. Therefore, we hypothesised that pelvic rotation may influence shoulder balance, especially postoperative rebalance, and evaluated the relationship between shoulder balance and pelvic rotation.

2

2 Materials and methods

2.1

2.1 Patient population

Our institutional review board approved the study protocol. This study is a retrospective study conducted at an academic teaching facility. Because this study is retrospective and non-invasive, informed consent was obtained through opt-out, and our institutional ethics committee waived the need to obtain informed consent from individual patients.

This is a retrospective study consisting of records of 46 AIS patients consecutively retrieved from our database from August 2011 to December 2020. The inclusion criteria for this study were (1) Lenke type 1 or 2, (2) posterior corrective surgery, and (3) follow-up at least 24 months after surgery. The exclusion criteria were Chiari malformation and other symptomatic scoliosis types. Twenty-eight patients who met these criteria were recruited for the study. Four were men and 24 were women, with a mean age of 14.5 years at the time of surgery. Patient parameters are provided in Table 1.

Table 1 Patient parameters.
Lenke type(1:2) 21:7
age 14.54 ± 1.26
Hight(cm) 156.31 ± 6.77
Weight(kg) 45.04 ± 5.59
Preoperative main thoracic Cobb angle(°) 54.11 ± 12.04
Preoperative proximal thoracic Cobb angle(°) 48.02 ± 1.74
Postoperative main thoracic Cobb angle(°) 13.05 ± 6.08
Correction rate(%) 76.27 ± 10.18
Preoperative clavicle angle(°) −2.06 ± 0.60
Preoperative coracoid height difference(mm) −6.00 ± 2.18
Number of fixed vertebral 9.75 ± 1.96
PS density 0.89 ± 0.02
2.2

2.2 Surgical technique

All patients underwent posterior corrective surgery. Preoperative computed tomography (CT) was performed, surgery was planned, and pedicle screws were inserted as far as possible. When the pedicle was thin and screw insertion was difficult, a hook or sublaminar tape fixation was used. The surgeon determined the extent of fixation, following the report by Lenke et al..19,20 After facetectomy at the apical lesion, two titanium alloy rods were bent identically, 6.0 mm in diameter. The two rods were connected to screw heads and then rotated simultaneously. Compression was performed on the convex side and distraction was performed on the concave side. When residual vertebral rotation or additional correction was needed, direct vertebral rotation or additional bending was used. A soft corset was worn for 6 months postoperatively.

2.3

2.3 Measurement parameters

Full-spine posteroanterior radiographs were obtained. Each radiograph was obtained in the natural standing position with the eyes straight ahead. The patient was in a standing position so that the line connecting the toes of both feet was parallel to the x-ray cassette. The hands naturally droop in the anteroposterior position. Using posteroanterior radiographs at preoperative and at 1 week, 3 months, and 2 years postoperatively, the following parameters were measured. Clavicle angle (CA), coracoid height difference (CHD), and T1 tilt were measured to evaluate the shoulder balance. For the pelvis, the left-right ratio of the iliac width (L/R ratio) and pelvic obliquity (PO) of the right and left pelvis were measured. The CA was defined as the angle between the horizontal plane and the line connecting the highest point of each clavicle. The CHD was defined as the height difference in millimetres between the coracoid processes by drawing a horizontal line at the upper margin of each process. T1 tilt was defined as the angle between the upper endplate of T1 and the horizontal plane (Fig. 1A). The PO was defined as the angle between the horizontal plane and the line connecting the upper edges of both iliac ridges. The radiographic measurement of pelvic rotation was based on the report of Lucas et al.,21 in which the best-positioned and most reliable landmarks were the inferior iliac crest of the sacroiliac joint on the medial side and the anterior superior iliac spine on the lateral side; this distance was measured to determine the L/R ratio (Fig. 1B). The CA, CHD, T1 tilt, and PO were defined as positive values that increased toward the left. The extent of change in CA, CHD, and L/R ratio from 1 week postoperative to 2 years postoperative were calculated as ΔCA, ΔCHD, ΔT1 tilt, ΔPO and ΔL/R ratio. Each absolute value was described as |CA|, |CHD|, |ΔCA|, |ΔCHD|, |ΔT1 tilt|, |ΔPO|, and |ΔL/R ratio|. A CA≧2° and a CHD≧9 mm were defined as shoulder imbalance.22 Pelvic rotation was defined as a change in the L/R ratio of 0.1 or more.23 Patients were divided into two groups according to the presence of preoperative pelvic rotation or not (rotation group [pre L/R ratio≧0.1] and non-rotation group [pre ΔL/R ratio<0.1]). These two groups were examined to determine 1) whether they had balanced shoulders at 2 years postoperative and 2) whether their shoulder balance worsened during the postoperative course. Additionally, a comparative analysis was performed between the two groups. The correlation between the measured parameters and the extent of change in each parameter was also examined. Patients fixed to L2 or lower were defined as the lumbar spine fixation group, and those fixed up to L1 were defined as the non-fixation group. The effect on the relationship between PAR and shoulder balance was examined using partial correlation analysis.

Measurement of radiographic parameters A. Clavicle angle (CA) was defined as the angle between a line connecting the highest points of both clavicles and the horizontal plane. The coracoid height difference (CHD) was defined as the height difference in millimetres between the coracoid processes by drawing a horizontal line at the upper margin of each. T1 tilt was defined as the angle between the horizontal line and the line through the upper endplate of T1 B. Pelvic obliquity (PO) was defined as the angle between the line connecting the upper edges of both iliac ridges and the horizontal line. The medial side was the inferior iliac crest of the sacroiliac joint and the lateral side was the anterior superior iliac spine, and this distance was measured to obtain the left-right ratio of iliac width (L/R ratio).
Fig. 1 Measurement of radiographic parameters A. Clavicle angle (CA) was defined as the angle between a line connecting the highest points of both clavicles and the horizontal plane. The coracoid height difference (CHD) was defined as the height difference in millimetres between the coracoid processes by drawing a horizontal line at the upper margin of each. T1 tilt was defined as the angle between the horizontal line and the line through the upper endplate of T1 B. Pelvic obliquity (PO) was defined as the angle between the line connecting the upper edges of both iliac ridges and the horizontal line. The medial side was the inferior iliac crest of the sacroiliac joint and the lateral side was the anterior superior iliac spine, and this distance was measured to obtain the left-right ratio of iliac width (L/R ratio).

Each parameter was measured by three independent observers from images created using the DICOM viewer on a DICOM workstation. An electronic caliper was used for the measurements. All measurements were taken by three independent observers and averages were used. Inter- and intra-rater reliability was good (κ > 0.80).

2.4

2.4 Statistical analysis

All analyses were performed using SPSS Statistics for Windows version 13 (SPSS Inc.). Values are presented as means and standard deviations (SD). Statistical significance was set at P < 0.05. Normality was checked and Pearson's product-rate correlation and Spearman's rank correlation were used for correlation comparisons as appropriate. Each independent variable was compared between the two groups using independent t-tests for continuous variables and chi-square tests for categorical variables. Correlation analysis was evaluated using Spearman's rank correlation coefficient. Patients fixed to L2 or lower were defined as the lumbar spine fixation group, and those fixed up to L1 were defined as the non-fixation group. Partial correlation analysis was performed to examine the relationship between PAR and shoulder balance, controlling for potential confounding variables, while stratifying by the presence or absence of lumbar fusion. Lumbar fixation is recorded as a binary variable (0 = no fixation, 1 = fixation). This method allowed for the evaluation of the association between PAR and shoulder balance independent of other influencing factors, such as lumbar fusion.

3

3 Results

3.1

3.1 Participants

The mean Cobb angle for the 28 patients was 54.1° ± 2.28. The mean postoperative Cobb angle was 11.7° ± 1.12, and the correction rate was 76.3 % ± 1.92. The mean L/R ratio was 0.94 ± 0.01, and preoperative PAR was observed in 11 of 28 cases (39.3 %). The most extensive fixation was from T1 to L3, with an average fixation level of 9.75 vertebrae. Twelve patients were fixed to the lumbar spine below L2. Fig. 2 shows pre-to postoperative changes in the L/R ratio. There was no significant change in the PAR between the preoperative and immediate postoperative periods (1 week); however, a significant change was observed from 1 week to 3 months postoperatively, which remained stable until 2 years. During the 2-year postoperative course, pelvic rotation was observed in 6 cases (|ΔL/R ratio|≧0.1). Shoulder imbalance persisted for 2 years postoperatively in 16 of the 28 cases. There were 8 cases of worsening shoulder balance during the 2-year postoperative course.

Pre-to postoperative change in the left-right ratio of iliac width (L/R ratio) There was no significant change in pelvic axis rotation (PAR) between the preoperative and immediate postoperative periods; however, significant changes were observed at 1 week and 3 months postoperatively and remained stable until 2 years. NS: no significant; S: significant.
Fig. 2 Pre-to postoperative change in the left-right ratio of iliac width (L/R ratio) There was no significant change in pelvic axis rotation (PAR) between the preoperative and immediate postoperative periods; however, significant changes were observed at 1 week and 3 months postoperatively and remained stable until 2 years. NS: no significant; S: significant.
3.2

3.2 Comparison analysis

The rotation group had significantly more instances of balanced shoulders at 2 years postoperatively than the non-rotation group (Table 2a). In one patient, where the CHD was balanced but the CA was imbalanced, the comparison in CA did not show a significant difference between the two groups (Table 2b).

Table 2a Comparison of shoulder balance (|CHD|<9 mm) between the two groups at 2 years postoperatively.
Shoulder balance at 2 years postoperatively (|CHD|<9 mm)
balanced imbalanced total
rotation group 8 3 11
non-rotation group 5 12 17
total 13 15 28
Table 2b Comparison of shoulder balance (|CA|<2°) between the two groups at 2 years postoperatively.
Shoulder balance at 2 years postoperatively (|CA|<2°)
balanced imbalanced total
rotation group 7 4 11
non-rotation group 5 12 17
total 12 16 28

The rotation group had significantly greater ΔCHD and ΔCA than the non-rotation group. However, there was no significant difference in the extent of change in pelvic rotation between the two groups (Table 3).Most patients in the rotation group showed no deterioration of shoulder balance during the postoperative period (Table 4a, Table 4b). The ratio of shoulder balance to shoulder imbalance was the same for both CA and CHD. Of the six cases in whose pelvis rotated in the postoperative course, five had preoperative PAR.

Table 3 Comparison analysis between the rotation group and non-rotation group.
rotation group non-rotation group P value
2y CHD 6.76 ± 8.31 7.10 ± 11.86 0.934
|2y CHD| 8.62 ± 6.14 11.96 ± 6.51 0.186
2y CA 1.35 ± 1.89 1.22 ± 3.03 0.902
|2y CA| 1.89 ± 1.27 2.76 ± 1.64 0.149
2y T1tilt 4.51 ± 4.14 3.24 ± 6.04 0.547
|2y T1tilt| 4.93 ± 3.58 5.82 ± 3.41 0.511
2y L/R ratio 0.98 ± 0.10 0.98 ± 0.07 0.83
2y PO 0.155 ± 2.29 0.394 ± 1.75 0.757
|2y PO| 1.97 ± 0.99 1.27 ± 1.24 0.124
ΔCHD −7.91 ± 11.81 −4.57 ± 8.68 0.396
|ΔCHD| 12.42 ± 6.23 7.42 ± 6.24 0.048a
ΔCA −1.37 ± 3.27 −1.00 ± 1.97 0.709
|ΔCA| 2.97 ± 1.48 1.71 ± 1.36 0.041a
ΔT1 tilt −0.77 ± 3.02 −1.67 ± 3.25 0.470
|ΔT1 tilt| 2.63 ± 1.48 3.00 ± 1.99 0.600
ΔL/R ratio 0.07 ± 0.14 0.01 ± 0.09 0.184
|ΔL/R ratio| 0.11 ± 0.11 0.06 ± 0.07 0.224
ΔPO −0.51 ± 16.9 0.39 ± 1.12 0.100
|ΔPO| 1.29 ± 1.14 0.94 ± 0.70 0.314
P < 0.05; CHD: Coracoid height difference, CA: Clavicle angle.
Table 4a Relationships between shoulder balance (CHD) and the two groups at 2 years postoperatively.
Shoulder balance after surgery (CHD)
Improved Worsened total
rotation group 10 1 11
non-rotation group 11 6 17
total 21 7 28
Table 4b Relationships between shoulder balance (CA) and the two groups at 2 years postoperatively.
Shoulder balance after surgery (CA)
Improved Worsened total
rotation group 10 1 11
non-rotation group 11 6 17
total 21 7 28
3.3

3.3 Correlation analysis

The ΔL/R ratio was negatively correlated with ΔCHD, ΔCA, and ΔT1 tilt (r = −0.425, P = 0.024.; r = −0.457, P = −0.015.; r = −0.520, P = 0.005) (Table 5a, Table 6a). |ΔL/R ratio| was positively correlated with |ΔCHD| and |ΔCA| (r = 0.375, P = 0.049.; 0.388, P = 0.041.) (Table 5b). No correlation was observed between the values at 2 years postoperatively. The ΔPO did not correlate with the extent of change in shoulder parameters. PS density was not significantly correlated with any of the parameters. Partial correlation analysis was performed controlling for the presence or absence of lumbar fusion, but the correlation rate did not change significantly (Table 6a, Table 6b).

Table 5a Correlation analysis with ΔL/R ratio and ΔPO.
ΔCHD ΔCA Δ T1 tilt 2y CHD 2y CA
ΔL/R ratio −0.425∗ −0.457∗ −0.520 −0.125 −0.190
ΔPO −0.001 −0.001 −0.226 0.457 0.467
Fixation level −0.259 −0.289 0.189 −0.256 −0.322
PS density 0.195 0.206 −0.122 0.306 0.316
P < 0.05; CHD: Coracoid height difference, CA: Clavicle angle, PO: pelvic obliquity angle, PS: Pedicle screw.
Table 6a Partial correlation analysis with ΔL/R ratio and ΔPO, controlling for the effect of lumbar fixation.
ΔCHD ΔCA Δ T1 tilt 2y CHD 2y CA
ΔL/R ratio −0.415∗ −0.481∗ −0.450 −0.042 −0.021
ΔPO −0.085 −0.149 −0.317 0.449 0.438
P < 0.05; CHD: Coracoid height difference, CA: Clavicle angle, PO: pelvic obliquity angle.
Table 5b Correlation analysis with |ΔL/R ratio| and |ΔPO|.
|ΔCHD| |ΔCA| |Δ T1 tilt| |2y CHD| |2y CA|
|ΔL/R ratio| 0.379∗ 0.391∗ 0.263 −0.175 −0.206
|ΔPO| 0.208 0.163 0.137 −0.474 −0.495
Fixation level 0.228 0.248 −0.078 −0.204 −0.213
PS density −0.303 −0.346 0.044 0.288 0.273
P < 0.05; CHD: Coracoid height difference, CA: Clavicle angle, PO: pelvic obliquity angle, PS: Pedicle screw.
Table 6b Partial correlation analysis with |ΔL/R ratio| and |ΔPO|, controlling for the effect of lumbar fixation.
|ΔCHD| |ΔCA| |Δ T1 tilt| |2y CHD| |2y CA|
|ΔL/R ratio| 0.525∗ 0.429∗ 0.265 −0.305 −0.228
|ΔPO| 0.290 0.367 0.273 −0.410 −0.424
P < 0.05; CHD: Coracoid height difference, CA: Clavicle angle, PO: pelvic obliquity angle.
3.4

3.4 Representative case

A 15-year-old Lenke type 2 AIS male patient, a main thoracic spine Cobb angle of 70°, and preoperative and postoperative changes are shown. Preoperative pelvic axis rotation (PAR) was an L/R ratio of 0.85 (Fig. 3A). There was no change in PAR immediately postoperatively (L/R ratio = 0.83) (Fig. 3B); however, PAR changed during the postoperative course (L/R ratio = 1.16) (Fig. 3C). Shoulder balance also improved during the postoperative course (CHD: 22.83 mm to −2.38, CA: 3.9° to −1.6°, CA: 5.3°–0.8°).

Representative case A 15-year-old male patient, Lenke type 2 AIS, main thoracic spine Cobb 70°, showing preoperative and postoperative changes. A. Preoperative pelvic axis rotation (PAR) was defined as a left-right ratio of the iliac width (L/R ratio) = 0.85. B. Immediately postoperatively, there was no change in PAR (L/R ratio = 0.83). C. The PAR changed during the postoperative course (L/R ratio = 1.16). Shoulder balance also improved during the postoperative course (CHD: 22.83 mm to −2.38, CA: 3.9° to −1.6°, CA: 5.3°–0.8°). CA: Clavicle angle; CHD: Coracoid height difference.
Fig. 3 Representative case A 15-year-old male patient, Lenke type 2 AIS, main thoracic spine Cobb 70°, showing preoperative and postoperative changes. A. Preoperative pelvic axis rotation (PAR) was defined as a left-right ratio of the iliac width (L/R ratio) = 0.85. B. Immediately postoperatively, there was no change in PAR (L/R ratio = 0.83). C. The PAR changed during the postoperative course (L/R ratio = 1.16). Shoulder balance also improved during the postoperative course (CHD: 22.83 mm to −2.38, CA: 3.9° to −1.6°, CA: 5.3°–0.8°). CA: Clavicle angle; CHD: Coracoid height difference.
4

4 Discussion

In this study, we investigated the pre-and postoperative course of PAR and its relationship with shoulder balance in AIS patients. Gum et al. reported that most patients with AIS have their pelvis rotated in the same direction as the main thoracic curve.7 In our study, 10 of the 11 patients (90 %) with preoperative pelvic rotation had an L/R < 0.95, indicating right rotation in the same direction as the main thoracic curve. Other studies reported that most pelvic rotations are rightward.

PAR changes after surgery. Two studies reported progress before and after previous surgeries. Qui et al. evaluated 38 AIS patients with a main TL/L curve and showed that the pelvis shows active rebalancing within 3 months after corrective surgery.17 Asher et al. evaluated 17 patients with AIS with double curves and reported that 7 of 17 patients had a transverse plane pelvic rotation increase after surgery which resolved by up to 12 months.18 There have been no previous reports on the course of pre-and postoperative PAR limited to Lenke 1,2, and in this study, we have clarified this course of rotation. Specifically, pelvic rotation did not change significantly from preoperatively to postoperatively (L/R ratio 0.94 to 0.95) but changed over the 3-month postoperative period (L/R ratio 0.95 to 0.98). This indicates that PAR is more involved in postoperative rebalancing than in the effect of surgical curve correction. The difference from the report by Asher et al. may be because only the thoracic spine curve was involved in the present study and the lumbar spine was not directly corrected; therefore, the effect of surgery on the pelvis was small.

The pelvis is known to influence shoulder balance, and pelvic oblique and sacral slopes are factors that have been previously reported.6,24 The present study shows that patients with preoperative PAR may eventually achieve good shoulder balance. A correlation was observed between the extent of change in pelvic rotation and shoulder balance during the postoperative course, and the movements appeared to be linked (Fig. 2). Although the shoulder and pelvis are distant segments, it is thought that surgery to fix the vertebrae creates a link between the pelvis and shoulder movements. Furthermore, five of the six patients with pelvic rotation in the postoperative course showed preoperative PAR. These results suggest that patients with preoperative pelvic rotation have a better ability to adjust their body balance and may have more potential to correct shoulder balance in the postoperative course.

However, although there was a correlation between the extent of change, there was no correlation between the extent of pelvic change and the absolute value of shoulder balance 2 years postoperatively. As past studies have shown, we believe that closer factors such as the correction rate and extent of fixation have a greater impact on shoulder balance.25 Thus, we featured the extent of change rather than the absolute value of shoulder balance and confirmed its association with the pelvis. In terms of changes, pelvic rotation seems to affect shoulder balance more than pelvic tilt. No correlation was found for the extent of fixation with any of the shoulder balance parameters, and it does not appear to be related to postoperative shoulder balance.

This study had several limitations. The first is the possibility of a left-right difference in the pelvic morphology. Left-right morphological differences in some bones have been reported in patients with AIS.26–28 While Gum et al. and Qiu et al. reported no difference in pelvic morphology between the right and left sides, Georgios et al. and Dalleau et al. measured using the Flock of Bird system and reported that patients with AIS have a larger right pelvis than normal patients.29–31 However, even in the same patient, the radiographic appearance before and after surgery is very different and PAR definitely occurs. Similar to the pelvis, the shoulder can rotate in the axial plane. The evaluation of shoulder rotation on radiographs is difficult, and shoulder movement in the axial plane has not been evaluated. Wafa et al. investigated the preoperative shoulder horizontal plane rotation, which decreased after surgery.32 It is highly likely that the shoulder, like the pelvis, also moves in three dimensions, and three-dimensional evaluations such as CT and motion capture will be necessary. Second, the small sample size is a drawback of this study, and we intend to continue this study and report on a larger sample size in the near future. Third, we did not investigate whether PAR has a significant impact on cosmetic appearance. This is also an issue that needs to be addressed in the future.

5

5 Conclusion

The PAR in patients with Lenke 1,2 AIS significantly changed over the 3 months postoperatively. Patients with Lenke 1,2 AIS and preoperative PAR can be expected to have postoperative shoulder rebalance.

CRediT authorship contribution statement

Noriaki Sako: Analyze, Writing – original draft. Masashi Miyazaki: Conceptualization, Methodology, Writing – review & editing. Tetsutaro Abe: Validation, Data curation. Nobuhiro Kaku: Supervision, All authors have read and approved the final version to be published.

Ethical statement

This study was conducted following the ethical principles of the Declaration of Helsinki, and the study protocol for this retrospective and noninvasive study was approved by the institutional review board of Oita University. Informed consent was obtained in the form of an opt-out, and the need to obtain informed consent from individual patients was waived by the ethics committee of Oita University.

Funding statement

This research received no specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

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