INTRODUCTION

Parkinson’s disease (PD), a multisystem and multisymptomatic neurodegenerative disorder, is increasingly prevalent in aging populations [1]. PD patients can be categorized into the postural instability and gait difficulty (PIGD) subtype, the tremor-dominant (TD) subtype, and the mixed subtype based on clinical symptoms. The PIGD subtype is associated with quicker disease progression, more rapid motor dysfunction [2], and more pronounced spinopelvic alignment abnormalities [3]. Furthermore, a systematic review revealed that a higher PIGD score is a prognostic indicator of faster disability progression in patients with PD [4]. Consequently, individuals with the PIGD phenotype face more health challenges and are at greater risk of disability and functional impairment.

Shoulder dysfunction refers to changes in both the quality and quantity of shoulder movement, which can affect daily activities [5]. Previous studies have reported that PD patients experience shoulder complaints, frozen shoulders, and increased muscle stiffness more frequently than normal individuals do [6,7]. Abnormal ultrasonography findings, such as increased effusion in the biceps long head tendon sheath, rotator cuff tendinopathy, and tears, are common in the PD population [8]. However, there is a lack of research on the impact of different motor subtypes on shoulder dysfunction. Understanding changes in shoulder function in PD patients across motor subtypes and identifying contributing factors are crucial. This knowledge can help healthcare providers optimize patient care and enhance the quality of life for affected individuals.

Shoulder kinematics must be considered more comprehensively than just scapula-humeral motion [9]. PD patients often develop changes in scapula-humeral kinematics and increased muscle stiffness, which may lead to rotator cuff tendinopathy and impaired shoulder mobility [10,11]. Previous studies have hypothesized that postural modifications and rigidity in patients with PD may affect the kinematics of the upper trunk and scapulothoracic region, leading to shoulder pathology [12]. Paggou et al. [5] suggested that disease duration, rigidity, and tremor could contribute to shoulder dysfunction in patients with PD. Overall, there is increasing evidence of the multifactorial pathophysiology of shoulder dysfunction in PD patients. However, the effects of PD and spinopelvic alignment on shoulder dysfunction have not been thoroughly investigated and remain unclear.

In this study, we aimed to investigate whether PD patients with the PIGD subtype differ from those with the non-PIGD subtype in shoulder function, range of motion (ROM), and muscle stiffness. We also examined whether these two subgroups exhibit shoulder dysfunction compared with healthy subjects. Additionally, we explored the relationships between spinopelvic parameters and clinical factors in relation to shoulder parameters to identify the factors associated with shoulder dysfunction in patients with PD.

MATERIALS & METHODS

Study subjects

Patients with PD and healthy controls were consecutively recruited from the Neurology Unit of Kaohsiung Chang Gung Memorial Hospital between June 2022 and December 2023. All PD patients were over 20 years old and were clinically diagnosed with idiopathic PD according to the UK Brain Bank criteria [13]. The exclusion criteria included the following: 1) newly diagnosed PD or follow-up for less than 6 months, 2) atypical parkinsonism, such as progressive supranuclear palsy, corticobasal degeneration, or dementia with Lewy bodies, 3) presence of focal neurological signs, 4) history of shoulder or spinal surgery, 5) history of spondyloarthropathy, 6) comorbidities that precluded reliable study examination completion, and 7) pregnancy.

This prospective study was approved by the Kaohsiung Chang Gung Memorial Hospital ethics committee (protocol number: 202200096A3), and written informed consent was obtained from all participants.

Clinical assessment of PD

Descriptive data, including age, sex, disease duration, and levodopa equivalent daily dose (LEDD) [14], were recorded. The clinical severity of PD was assessed via the Unified Parkinson’s Disease Rating Scale (UPDRS) and the modified Hoehn and Yahr staging (H&Y) scale. The total UPDRS score was computed by summing the subscores of UPDRS parts I, II, and III. The tremor score was calculated by summing the baseline tremor score from the UPDRS part II and the tremor score from the UPDRS part III for the face, hands, feet, and action tremors in both hands. The PIGD score was determined by adding the baseline scores for falling (2.13), freezing (2.14), walking (2.15), gait (3.29), and postural stability (3.30) from the UPDRS parts II and III. Based on the ratio of the mean tremor score to the mean PIGD score, participants were classified into either the PIGD group (ratio ≤1) or the non-PIGD group (ratios >1, which includes both TD and indeterminate types). Both clinical evaluations and imaging tests were conducted during the “ON” state.

Clinical assessment of the shoulder

The shoulder condition was evaluated using active ROM and American Shoulder and Elbow Surgeons (ASES) score [15]. To minimize the influence of sports or overuse injuries, which typically affect the dominant side, the nondominant shoulders of all participants were examined. Each participant was instructed to achieve maximal shoulder ROM without assistance. The maximal angles of shoulder external rotation (ER), internal rotation (IR), abduction (AB), and forward flexion (FF) were measured with a universal goniometer, following the guidelines of the American Academy of Orthopedic Surgeons [16].

The ASES score is a widely accepted patient-reported outcome questionnaire used to assess shoulder pain and function; it consists of 18 items divided into three parts: pain, instability, and activities of daily living related to shoulder function. Among the 18 questions, subscores ranging from 0–50 are assigned to the functional dimension (10 items) and the pain dimension (1 item). The functional and pain subscores are combined to provide an overall ASES score on a 0–100 scale, with higher scores indicating better shoulder condition.

Sonographic assessment of the shoulder

Ultrasound examination of the nondominant shoulder was conducted by an experienced radiologist who was blinded to the clinical information and test results of the participants. To assess muscle stiffness, shear wave velocity (SWV) in the selected muscle was measured using an ACUSON Sequoia Ultrasound System with a 9L4 linear array probe (Siemens Medical Solutions). The participants were instructed to look ahead and sit in a relaxed position with their arms resting on their thighs. The muscles investigated included the supraspinatus (SSP), infraspinatus (ISP), upper trapezius (UT), and middle deltoid (MD). The ultrasound probe was placed on the skin with minimal pressure and oriented along the muscle fibers, with the region of interest set to a size of 10 mm. The scanning sites for SWV measurement were as follows: 1) SSP and ISP muscles, 2 cm above and below the midpoint between the acromial angle and the root of the spine of the scapula, respectively, 2) UT muscle, midway between the angle of the acromion and the spine of C7, and 3) MD muscle, midway between the deltoid tuberosity and the midpoint of the acromion. SWV acquisitions were repeated twice per muscle, and the mean SWV value was recorded in meters per second (m/s).

Imaging assessment of spinopelvic alignment

Spinopelvic alignment was evaluated using standing wholespine lateral and frontal radiographs following a standardized protocol (Supplementary Figure 1 in the online-only Data Supplement) [17]. For ethical reasons, radiographs were taken during the “ON” phase of therapy for PD patients. On frontal radiographs, the coronal spinal parameters were assessed, including the C7-central sacral vertical line (C7-CSVL), defined as the distance between the C7 plumb line and the central sacral vertical line, and the Cobb angle. On lateral radiographs, the sagittal spinal parameters were assessed, including: the C7 sagittal vertical axis (SVA), defined as the distance between the centroid of the C7 plumb line and the S1 posterior superior corner; the T1 slope, defined as the angle between the horizontal plane and the T1 superior endplate; thoracic kyphosis (TK), defined as the kyphotic angle between the T5 superior endplate and the T12 inferior endplate; lumbar lordosis (LL), defined as the lordotic angle between the L1 superior endplate and sacral plate; sacral slope (SS), defined as the angle between the horizontal plane and sacral plate; pelvic tilt (PT), defined as the angle between the line connecting the midpoint of the sacral plate to the bicoxofemoral axis and the vertical line from the bicoxofemoral axis; and pelvic incidence (PI), defined as the angle between the line perpendicular to the sacral plate and the line connecting the midpoint of the sacral plate to the bicoxofemoral axis. Negative values indicated lordosis in the radiographic parameters. All spinal radiological parameters were measured by an experienced radiologist who was blinded to the clinical information and shoulder sonography findings.

Statistical analysis

The Kolmogorov–Smirnov test was used to assess the normality of all continuous variables. To compare continuous variables, we employed the Kruskal–Wallis test or the Mann–Whitney U test, and the results are reported as the median (interquartile range). Categorical variables were analyzed via the χ² test or Fisher’s exact test. To account for sex and age in a nonparametric comparison of shoulder parameters among the three groups, we performed data transformation and employed a general linear model (GLM). Initially, logarithmic transformations were applied to the data to better approximate normality, thereby enabling parametric analysis. A GLM was subsequently fitted with the group variable treated as a factor while adjusting for covariates such as sex and age. This methodology facilitated the examination of group differences while controlling for these variables. Post hoc tests were conducted to investigate differences among specific groups. Additionally, after adjusting for age and sex, we performed a partial Spearman rank correlation to explore the relationships between shoulder dysfunction and various clinical factors, as well as spinopelvic alignment. All data analyses were conducted via IBM SPSS Statistics 25 (IBM Corp.), with a significance threshold set at p<0.05.

RESULTS

Participant demographic characteristics

One hundred and two participants were initially enrolled in this study, and five PD patients were excluded due to a history of shoulder or spinal surgery (n=3) and an inability to complete the examinations (n=2). In total, 62 PD patients (30 with the PIGD subtype and 32 with the non-PIGD subtype) and 35 healthy controls were eligible for the study and completed all clinical and imaging examinations.

Table 1 summarizes the demographic and clinical characteristics of the PIGD, non-PIGD, and healthy control groups. There were no significant differences among the three groups in terms of age (p=0.217) or sex (p=0.310). Patients of both PD subtypes were similar in terms of disease duration and disease severity, as evaluated by the total UPDRS score and the modified H&Y stage (all p>0.05). The mean LEDD was greater in the PIGD group than in the non-PIGD group. Consequently, the influence of possible confounding factors that might affect shoulder condition was substantially minimized.

Differences in spinopelvic alignment among groups

As shown in Table 1, spinopelvic alignment differed significantly among the three groups in terms of C2-C7 SVA (p=0.005), C7-S1 SVA (p=0.001), and C7-CSVL (p=0.003). Post hoc comparisons revealed that, compared with the controls, both PD groups presented increased distances in the C2‒C7 SVA, C7‒S1 SVA, and C7‒CSVL (all p<0.05).

Differences in shoulder ASES scores, ROM, and muscle stiffness among groups, adjusted for sex and age

Differences in shoulder ASES scores, ROM, and muscle stiffness between PD (PIGD and non-PIGD) patients and controls are presented in Table 2 and Figure 1. After adjustment for sex and age, a significant group effect was observed for the total ASES score (p=0.001), the ASES pain subscore (p=0.014) and the ASES functional subscore (p=0.004). Post hoc analysis revealed that the PIGD group had significantly lower total ASES scores (p<0.001), ASES pain subscores (p=0.011) and ASES functional subscores (p=0.002) than the control group did. There was no statistically significant difference in the ASES score between the PIGD and non-PIGD groups.

The analysis of the ROM revealed significant group effects for various measures: ER (p=0.003), AB (p=0.012), and FF (p<0.001). Post hoc comparisons indicated that the PIGD group had a significantly lower ER compared with both the non-PIGD group (p=0.015) and the control group (p=0.004). When the PD patient groups were compared with the control groups, both the PIGD and non-PIGD groups presented decreased angles of AB (PIGD versus controls: p=0.023; non-PIGD versus controls: p=0.045) and FF (PIGD versus controls: p<0.001; non-PIGD versus controls: p=0.008). There were no significant differences in AB, FF, or FE between the PIGD and non-PIGD groups.

In the analysis of shoulder muscle stiffness, a significant group effect was found for the ISP muscle (p=0.016). Post hoc analysis indicated that the PIGD group had a significantly greater SWV in the ISP muscle compared with the control group (p=0.012). No other comparisons reached statistical significance (Table 2).

Correlations among shoulder parameters, clinical factors, and spinopelvic alignment in 62 PD patients

The results of the correlation analysis are presented in Table 3 and Figure 2. Partial correlation analysis revealed significant associations between the overall ASES score and several clinical measures: the total UPDRS score (r=-0.495), UPDRS-I score (r=-0.273), UPDRS-II score (r=-0.538), UPDRS-III score (r=-0.282), H&Y stage (r=-0.356), and PIGD score (r=-0.415). The pain subscore was significantly associated with the total UPDRS score (r=-0.323), UPDRS-I score (r=-0.269), UPDRS-II score (r=-0.347), and H&Y stage (r=-0.300). The functional subscore was significantly associated with the total UPDRS score (r=-0.475), UPDRS-II score (r=-0.527), UPDRS-III score (r=-0.298), bradykinesia score (r=-0.255), and PIGD score (r=-0.405).

Additionally, the shoulder ROM angles were also associated with clinical severity and spinopelvic alignment. ER was significantly correlated with the PIGD score (r=-0.355), AB with LL (r=0.359) and SS (r=0.481), FF with the UPDRS-II score (r=-0.335), and FE with the tremor score (r=-0.256).

The SWV of the ISP was significantly positively correlated with the PIGD score (r=0.262). The SWV of the UT was significantly positively correlated with LL (r=0.312) and the SS (r=0.342). The SWV of the deltoid muscle was significantly negatively correlated with PI (r=-0.291) and PT (r=-0.345).

Correlations between shoulder parameters and spinopelvic alignment in healthy controls

The correlation analysis results are displayed in Table 4. Partial correlation analysis revealed a significant association between the overall ASES score and both the C7-S1 SVA (r=0.407) and Cobb angle (r=0.354). Similarly, the functional subscore was significantly correlated with the C7-S1 SVA (r=0.406) and Cobb angle (r=0.473). Additionally, the SWV of the ISP demonstrated a significant positive correlation with the C7-S1 SVA (r=0.525).

DISCUSSION

The present study examined shoulder function and muscle alterations in PD patients with different motor subtypes, considering aspects such as shoulder pain, function, ROM, and muscle stiffness. Compared with controls, both groups of PD patients presented poorer shoulder function and limited ROM. Notably, compared with non-PIGD patients and controls, those with the PIGD phenotype presented decreased ER. Correlation analysis revealed that shoulder condition was significantly associated with PD disease severity and the PIGD score, whereas muscle stiffness was linked to spinopelvic alignment and the PIGD score. Various clinical factors, including PD disease severity, the PIGD score, the tremor score, and spinopelvic alignment, were significantly correlated with shoulder ROM. These results highlighted the impact of PD motor subtype, disease severity, and spinopelvic alignment on shoulder condition, emphasizing the multifactorial nature of shoulder dysfunction pathophysiology in PD.

In our study, we are the first to demonstrate that PD patients with the PIGD phenotype experience worse shoulder conditions compared with those with the non-PIGD phenotype and healthy controls. PIGD is marked by an impaired ability to adjust posture in response to changing support conditions, alongside a Parkinsonian gait characterized by a stooped posture, reduced arm swing, and a shuffling walk. This subtype tends to have more severe motor symptoms, such as bradykinesia, freezing, rigidity, and postural instability, which are linked to disability and motor dysfunction [18,19]. These postural changes, diminished arm swing, and exacerbated motor symptoms likely contribute to the poorer shoulder condition observed in the PIGD subtype. Our study revealed that a higher PIGD score was correlated with a lower ASES score, reduced shoulder ROM (particularly in ER), and increased stiffness of the ISP muscle. Additionally, a higher bradykinesia score was weakly correlated with a lower ASES score. These findings underscore the significant impact of PIGD and its associated worsening of parkinsonism, especially bradykinesia, on various aspects of shoulder dysfunction.

Shoulder pathologies detected through imaging become more common in PD patients as UPDRS severity increases [20,21]. Consistent with previous studies, we found that a lower ASES score was linked to more severe PD, as measured by the UPDRS and H&Y stage. Specifically, the UPDRS II score was closely associated with the total ASES score. These findings suggest that motor abnormalities are crucial in the development of shoulder dysfunction. As the disease progresses, PD-affected shoulders exhibit muscle weakness and disrupted activation associated with bradykinesia and rigidity [22,23]. Shoulder pain, reduced arm swing, and limited ROM, observed as early symptoms or prodromal presentations of PD [24,25], indicate the early presence of these PD-related neuromuscular changes. Additionally, more severe shoulder disorders, such as frozen shoulder, rotator cuff tears, and fractures, occur as PD advances [8,26]. Taken together, the deterioration of the shoulder condition in PD patients may stem from these neuromuscular changes and shoulder pathologies.

Postural deformities linked to PD have been suggested to be significant contributors to shoulder disorders [12]. Our study revealed that certain spinopelvic parameters were weakly correlated with shoulder ROM and muscle stiffness but not significantly correlated with the ASES score. This finding indicates that spinopelvic alignment may indirectly affect shoulder function, even without any clinically evident shoulder impairment. Specifically, LL and SS exhibited a weak positive correlation with shoulder AB in PD patients, whereas the Cobbs angle and the C7-S1 SVA, which are associated with shoulder function in the healthy control group, did not show a similar correlation in PD patients. The relationship between postural alterations in PD and shoulder function may reflect a unique musculoskeletal interaction specific to this population. While previous studies have explored the interaction between the thoracic spine and scapulohumeral motion [27], the impact of lumbar and pelvic alignment on shoulder ROM remains underexplored. In PD patients, a decreased SS may indicate pelvic adaptations to primary postural alterations stemming from positive sagittal imbalance and reduced lordosis [28,29]. Based on our correlation analysis, we suggest that shoulder ROM may be compromised as a means of maintaining a compensated posture, although the precise mechanism remains uncertain. In this analysis, muscle stiffness was associated primarily with LL and pelvic parameters, supporting our hypothesis that compensatory changes in the spinopelvic region could contribute to restricted shoulder ROM in PD patients. Further investigation is necessary to examine the effects of these compensatory strategies on shoulder movement and to validate our hypothesis.

The increased stiffness of the shoulder muscles in the PD group aligns with previous studies showing greater muscle stiffness in both the upper and lower extremities [7,30]. In our study, the ISP muscles were primarily affected, which could be a source of chronic shoulder and scapular pain [31]. The increased muscle stiffness was likely due to changes related to altered neuromuscular drive and rigidity, which are key features of PD [32,33]. On the other hand, there were no significant differences in the SWV of the SSP, UT, or ISP muscles among the groups. These findings might be explained by different muscle structural modifications in response to parkinsonian rigidity in each muscle [34].

There are several limitations to this study. The complex mechanisms underlying shoulder dysfunction may be influenced by factors such as physical exercise and comorbidities, which were not thoroughly addressed in this study. Additionally, our study included a relatively high proportion of early-stage PD patients. Shoulder dysfunction or stiffness can appear early in the disease or as prodromal symptoms of PD [24,25]. Focusing on early-stage patients might clarify the relationships between shoulder dysfunction and clinical factors. Future longitudinal studies with larger sample sizes are needed to investigate the factors contributing to shoulder dysfunction in different stages of PD. Finally, spinopelvic alignment and shoulder ROM were measured under static conditions rather than during movement, which may not accurately reflect their relationship in real-life situations.

Conclusion

PD patients experienced shoulder dysfunction in several ways, such as a reduced ASES score, limited ROM, and increased shoulder muscle stiffness. Compared with the non-PIGD phenotype and controls, the PIGD phenotype, in particular, showed worse shoulder conditions. Our study also highlighted the links between PD motor subtype, disease severity, and spinopelvic alignment in relation to shoulder dysfunction. These findings suggest that different pathophysiological processes are involved in shoulder dysfunction among PD patients with different motor phenotypes. This study offered deeper insights into the underlying causes of shoulder dysfunction in PD patients, which could help in the development of targeted prevention and treatment strategies in the future.

Supplementary Materials

Notes

Conflicts of Interest

The authors have no financial conflicts of interest.

Funding Statement

This work was supported by Grant CMRPG8M0801, CMRPG8M0802 from Kaohsiung Chang Gung Memorial Hospital, Taiwan.

Acknowledgments

We would like to acknowledge Biostatistics Center, Kaohsiung Chang Gung Memorial Hospital for their support in the statistical analyses of this study.

Author Contributions

Conceptualization: Sieh Yang Lee, Cheng-Hsien Lu. Data curation: Lay San Lim, Yun-Ru Lai. Formal Analysis: Sieh Yang Lee, Lay San Lim. Funding acquisition: Sieh Yang Lee. Investigation: Yun-Ru Lai, Cheng-Hsien Lu. Methodology: Sieh Yang Lee, Cheng-Hsien Lu. Project administration: Sieh Yang Lee. Resources: Lay San Lim, Yun-Ru Lai. Software: Sieh Yang Lee, Cheng-Hsien Lu. Supervision: Cheng-Hsien Lu. Validation: Yun-Ru Lai, Cheng-Hsien Lu. Visualization: Sieh Yang Lee, Lay San Lim. Writing—original draft: Sieh Yang Lee. Writing—review & editing: Cheng-Hsien Lu.

Figure 1.

Comparisons of shoulder parameters between PIGD, non-PIGD, and control groups. Comparison of the ASES score (A), ROM (B), and muscl SWV (C) among patients in the PIGD, non-PIGD, and control groups, adjusted for sex and age. *indicates p<0.05; ^†indicates p<0.01; ^‡indicates p<0.001 in the post hoc comparisons. ns, no statistical significance; ASES, American Shoulder and Elbow Surgeons; SE, standard error; PIGD, postural instability and gait difficulty; ROM, range of motion; ER, external rotation; AB, abduction; FF, forward flexion; FE, forward extension; SWV, shear wave velocity.

Figure 2.

Scatter plots illustrate the relationships between shoulder parameters and clinical status/spinopelvic alignment in 62 patients with PD, adjusted for sex and age. The top row shows the total ASES score versus the UPDRS-II score (A), the total ASES score versus the total UPDRS score (B), and the abduction versus sacral slope (C). The bottom row shows a significant correlation between the PIGD score and shoulder parameters. (D): Total ASES score versus the PIGD score. (E): External rotation versus the PIGD score. (F): The SWV of the infraspinatus muscle versus the PIGD score. ASES, American Shoulder and Elbow Surgeons; UPDRS, Unified Parkinson’s Disease Rating Scale; PIGD, postural instability and gait difficulty; SWV, shear wave velocity; PD, Parkinson’s disease.

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