Abstract
[Purpose] To confirm the reliability and validity of the acromion-greater tuberosity (AGT) distance measured using ultrasound and to investigate its relationship with functional impairments inpatients with stroke. [Participants and Methods] Twenty-four patients with stroke admitted between May and September 2024 were evaluated. Physical function assessments included motor paralysis, spasticity, pain (numerical rating scale [NRS]), shoulder range of motion (ROM), sensory impairments, and shoulder subluxation using the fingerbreadth palpation method. Ultrasound was used to measure the AGT distance and the thickness of the long head of the biceps tendon. [Results] A significant correlation was found between the AGT distance and subluxation, measured using the fingerbreadth palpation method, confirming its validity. The AGT distance was positively correlated with spasticity, tendon thickness, and NRS during movement but negatively correlated with motor paralysis and shoulder ROM. These findings suggest that an increased AGT distance may be associated with severity of subluxation, reduced motor function, and a higher pain level during movement. [Conclusion] The AGT distance measured using ultrasound is a valid tool for assessing shoulder subluxation and related impairments in patients with stroke. Further studies are required to explore the causal relationship between pain and tendon inflammation to guidebetter clinical management strategies.
Keywords: Stroke, Subluxation, Ultrasound imaging equipment
INTRODUCTION
In post-stroke shoulder subluxation on the paralyzed side (hereinafter, subluxation) is a condition in which the glenohumeral joint is displaced due to relaxation of the supraspinatus and deltoid muscles due to paralysis, together with sustained downward traction from the weight of the upper limb1, 2). Subluxation is a common secondary complication, with incidence ranging from 15% to 81% depending on the timing of measurement3). While the exact impact of subluxation on shoulder pain and functional recovery of the upper limb remains unclear, it is considered one cause of shoulder pain4, 5). Several recent reviews focusing on shoulder pain have described subluxation management as a primary intervention for preventing shoulder pain6).
Against this backdrop, subluxation is a significant secondary complication for individuals with hemiplegia after stroke, yet its primary evaluation methods in physical therapy are limited to X-rays and the fingerbreadth palpation method. Measuring the distance between the acromion and the humeral head on X-rays is considered the best method for quantifying subluxation1). However, due to concerns such as radiation exposure, cost, and time, frequent measurements in the clinical setting are challenging, making it less feasible for routine evaluations aimed at determining the effectiveness of physical therapy.
In the fingerbreadth palpation method, the evaluation results are described as “1-fingerbreadth”, “2-fingerbreadth”, and so on, based on the examiner’s fingerbreadth. This method does not require specialized equipment and can be easily performed from the body surface, but it cannot follow detailed changes over time and is limited to binary (“present” or “absent”) assessments7). Since this method is almost the only evaluation method used routinely in physical therapy, there are few studies investigating the causal relationship between the degree of subluxation and the degree of functional impairment. This situation is likely one of the reasons why the relationship between subluxation and shoulder pain remains largely unknown.
In recent years, ultrasound imaging has increasingly been used in physical therapy. The key features of ultrasound include its non-invasiveness and the development of compact and portable devices. Additionally, unlike computed tomography or magnetic resonance imaging, it has the ability to capture images during joint movement, making it widely applicable for locomotor disorders8). Several studies on subluxation have used ultrasound to measure the distance between the edge of the acromion and the apex of the greater tuberosity (acromion-greater tuberosity, AGT), which demonstrated sufficient intra- and inter-rater reliability9,10,11). Moreover, it has been reported that a difference of 0.2 cm or more in AGT distance measured by ultrasound between the paralyzed and non-paralyzed sides suggests subluxation11). These findings indicate the potential of using ultrasound to evaluate subluxation in physical therapy settings.
The aims of this study were 1) to confirm the reliability and validity of AGT distance measured by ultrasound and 2) to statistically investigate the link between AGT distance and functional impairments caused by stroke.
PARTICIPANTS AND METHODS
The participants were 24 stroke patients admitted to our hospital between May and September 2024. We included first-time stroke patients undergoing inpatient treatment who were 1 to 5 months post-onset and exhibited motor paralysis of the upper limb on one side. The participants’ basic characteristics, including diagnosis, age, sex, height, weight, body mass index, and disease duration, was collected from the medical records.
Physical function assessment was performed by the attending physical or occupational therapist and involved evaluating motor paralysis using the Brunnstrom Recovery Stage (BRS) for the paralyzed upper limb and assessing spasticity using the Modified Ashworth Scale (MAS). For pain assessment associated with physical function, pain at rest and pain on movement were evaluated using a numerical rating scale (NRS)12). Shoulder range of motion (ROM) was assessed using passive flexion, abduction, and external rotation (first position).
Sensory impairment was evaluated using the sensory impairment component of the Stroke Impairment Assessment Set, assessing light touch and position on a 4-point scale (0–3). Upper limb light touch was initially tested on the non-paretic side (C5 dermatome) and then on the paretic side. Position was assessed by evaluating joint position sense using the thumb13).
Shoulder subluxation was measured using the fingerbreadth palpation method and ultrasound examination. For both palpation and ultrasound, the patient sat upright on a bed or chair with both feet on the ground, the forearms resting on the knees, and the elbows unsupported. Some patients with high muscle tone were unable to let the affected arm hang freely at their side2). For these patients, the shoulder was maintained in an internally rotated position with a slight bend in the elbow and the forearm resting on the knee.
Evaluation using the fingerbreadth palpation method involved measuring the space between the underside of the acromion and the top of the humeral head on the affected side. The measurement was categorized into a six-level ordinal scale: no subluxation, 0.5-fingerbreadth gap, 1-fingerbreadth gap, 1.5-fingerbreadth gap, 2-fingerbreadth gap, and 2.5-fingerbreadth gap.
Ultrasound examination was performed using an ultrasound scanner (LOGIQ P5, GE Healthcare Japan Corp., Tokyo, Japan) with a 11 L probe (GE Healthcare Japan Corp.) in B (Brightness) mode. A sufficient about of ultrasound gel (Pro Jelly, Jex Co., Ltd., Osaka, Japan) was used for imaging. Ultrasound examination measured the AGT distance and the long head biceps tendon thickness on the paretic side. For the AGT distance measurement, the probe was positioned to visualize the shortest distance between the lateral edge of the acromion and the apex of the greater tuberosity of the humerus10). The supraspinatus tendon was clearly visible as a thick band (high echogenicity image) at its attachment site, making it easy to identify the greater tuberosity (Fig. 1).
Fig. 1.
Measurement of acromion-greater tuberosity (AGT) distance between the lateral border of the acromion (AC) and the nearest superior margin of the greater tuberosity (GT).
The long head biceps tendon thickness on the paretic side was measured by positioning the probe at the level of coracoid process between the greater and lesser tuberosities in a short-axis view. The probe was then rotated 90° to visualize the long axis of the tendon14). To measure the tendon thickness, a line was drawn vertically at the most proximal end of the bicipital groove, and the distance from the superficial to the deep layer was measured. The captured image was imported into ImageJ image analysis software (National Institutes of Health, Bethesda, MD, USA) for distance measurement.
All measurements were performed by one physical therapist with 7 years of experience as a physical therapist and 3 years of experience using the ultrasound scanner.
For each participant, the AGT distance and long head biceps tendon thickness on the paretic side were measured once each on the same day. To confirm intra-rater and inter-rater reliability, all measurements were performed a second time within 7 days in 7 stroke patients, and the intraclass correlation coefficient (ICC) was calculated. The results for the evaluation items are expressed as mean ± standard deviation. For statistical analysis, Spearman’s rank correlation (ρ) was calculated for the AGT distance and the evaluation of subluxation using the fingerbreadth palpation method, as well as for the evaluation of functional impairment due to stroke. Intra-rater reliability was calculated as ICC(1, 1), and inter-rater reliability was calculated as ICC(2, 1). Statistical analysis was performed using JMP17.1 (SAS Institute Inc., Cary, NC, USA).
This study was conducted in accordance with the Declaration of Helsinki. The purpose of the study was explained to the participants, and written informed consent was obtained from either the participants themselves or their family members.
This study was conducted under the supervision and approval of the attending physician and was also approved by the Ethics Committee of Kaga City Medical Center (Approval No: R6-2).
RESULTS
Tables 1 show the results of intra-rater and inter-rater reliability. The AGT distance demonstrated high reliability, with values of 0.8 or higher for both the affected and unaffected sides. Table 2 presents the participants’ basic characteristics and the results of the physical function evaluation.
Table 1. Intra- and inter-rater reliability (ICC [1.1] and [2.1]).
| Paretic | Non-Paretic | ||||
| ICC (95% CI) | SEM (± cm) | ICC (95% CI) | SEM (± cm) | ||
| AGT distance | Rater 1 | 0.96 (0.79–0.99) | 0.1 | 0.98 (0.88–0.99) | 0.1 |
| Rater 2 | 0.89 (0.56–0.98) | 0.1 | 0.98 (0.93–0.99) | 0.1 | |
AGT: acromion–greater tuberosity; ICC: intraclass correlation coefficient; CI: confidence interva; SEM: standard error of measurement.
Table 2. Basic patient characteristics and physical function evaluation (N=24).
| Variables | Mean ± SD |
| Age (years) | 76.5 ± 12.7 |
| Height (m) | 157.0 ± 10.9 |
| Weight (kg) | 49.3 ± 11.2 |
| BMI (kg/m2) | 20.0 ± 3.4 |
| Time since stroke onset (days) | 62.9 ± 41.3 |
| Paretic shoulder ROM (°): | |
| Forward flexion | 124.3 ± 32.9 |
| Abduction | 111.2 ± 36.4 |
| External rotation | 31.6 ± 19.4 |
| NRS for shoulder pain at rest | 0.7 ± 1.5 |
| NRS for shoulder pain on movement | 2.4 ± 3.0 |
| Ultrasound method: | |
| Non-paretic AGT distance (cm) | 1.7 ± 0.4 |
| Paretic AGT distance (cm) | 1.9 ± 0.6 |
| Non-paretic long head biceps tendon thickness (cm) | 0.3 ± 0.1 |
| Paretic long head biceps tendon thickness (cm) | 0.4 ± 0.1 |
| Variables | n |
| Sex (men/women) | 10/14 |
| Ischemic/hemorrhagic/subarachnoid hemorrhage | 10/12/2 |
| UE BRS (I/II/III/IV/V/VI) | 2/2/3/5/8/4 |
| UE MAS (0/1/1+/2/3/4) | 16/2/2/2/2/0 |
| Sensory function: | |
| Touch (0/1/2/3) | 1/4/8/11 |
| Position (0/1/2/3) | 1/6/8/9 |
| Fingerbreadth palpation method (0/0.5/1/1.5/2/2.5) | 17/0/1/1/5/0 |
Data are presented as mean ± standard deviation or as the number.
BMI: body mass index; ROM: range of motion; NRS; numerical rating scale; AGT: acromion-greater tuberosity; BRS: Brunnstrom Recovery Stage; MAS: Modified Ashworth Scale; GHS: glenohumeral subluxation.
In the correlation between AGT distance and subluxation assessment using the fingerbreadth palpation method, a significant correlation of 0.65 was observed. Additionally, the correlation between AGT distance and functional impairment assessment due to stroke showed a positive correlation with the MAS, Paretic Biceps long head tendon thickness, and NRS during movement, while a negative correlation was found with the upper limb BRS and shoulder ROM (flexion, abduction, and external rotation) (Table 3).
Table 3. Correlation between AGT distance and functional impairment (N=24).
| Item | AGT distance |
| Time since stroke onset | 0.18 |
| UE BRS | −0.40* |
| UE MAS | 0.51** |
| Sensory function: | |
| Touch | −0.14 |
| Position | −0.34 |
| NRS: | |
| Rest | 0.06 |
| Movement | 0.51** |
| ROM: | |
| Forward flexion | −0.66** |
| Abduction | −0.64** |
| External rotation | −0.52** |
| Fingerbreadth palpation method | 0.65* |
| Paretic long head biceps tendon thickness | 0.45* |
*p<0.05 **p<0.01. ρ: correlation coefficient; AGT: acromion-greater tuberosity; ROM: range of motion; BRS: Brunnstrom; NRS: numerical rating scale; Recovery Stage; MAS: Modified Ashworth Scale.
DISCUSSION
The aims of this study were 1) to confirm the reliability of AGT distance measured by ultrasound, and 2) to statistically investigate the relationship between AGT distance and functional impairments caused by stroke.
We confirmed high intra- and inter-rater reliability for AGT distance measurements, with ICC values exceeding 0.8 for both the paralyzed and non-paralyzed sides. Generally, reproducibility issues are cited as a drawback of ultrasound evaluations; however, ultrasound evaluation of AGT distance demonstrated high intra- and inter-rater reliability in this study, showing no such issue in this context.
We also found a moderate correlation between AGT distance measured by ultrasound and the subluxation evaluation by the fingerbreadth palpation method, indicating that measuring AGT distance using ultrasound is valid. Moreover, AGT distance was found to be negatively correlated with motor paralysis (BRS) and positively correlated with spasticity (MAS), suggesting that greater AGT distances resulted in more severe functional impairments. As mentioned above, subluxation evaluations to date have relied heavily on the fingerbreadth palpation method, effectively resulting in binary “present” or “absent” assessments. This reliance has limited comparative research between subluxation severity and functional impairments7). Demonstrating correlations between AGT distance and multiple functional impairments in this study may offer a promising avenue for further elucidating the largely unresolved causal relationships between subluxation and shoulder pain1).
Regarding the relationship between subluxation and shoulder pain, a systematic review reported mixed findings from 14 studies: seven studies found a close association between hemiplegic shoulder pain and subluxation, while the other seven did not find a significant association15). In the present study, a positive correlation was observed between AGT distance and pain on movement or the biceps tendon thickness. Previous studies on post-stroke shoulder pain have suggested that the long head of the biceps tendon is a primary lesion site in painful post-stroke shoulders, with inflammation leading to tendon thickening16, 17). Therefore, our findings indicate that there may be a causal relationship between greater AGT distance and stronger pain during movement with inflammation of the biceps tendon. While further investigation is needed, comparisons with AGT distance are expected to lead to better understanding.
This study has several limitations. First, the cross-sectional design means that any considerations regarding causal relationships remain hypothetical. Future longitudinal analyses should be conducted to examine the impact of the amount of change in AGT distance on related factors. Second, this study was conducted at a single facility with a limited sample size, which may limit the applicability and generalizability of the results. Third, post-stroke shoulder pain can be broadly classified into mechanical pain and neurological pain, but this study did not distinguish between these types. Therefore, the link between subluxation and pain needs to be further investigated.
Fourth, in this study, functional impairment assessments were performed by the attending physical or occupational therapist, while ultrasound examinations were conducted by a single physical therapist with experience in using the ultrasound scanner. Although the assessments and ultrasound examinations were conducted separately, all procedures took place within the same ward, and thus, the study was not fully blinded.
At present, fingerbreadth palpation method, which is low objectivity, remains the primary means of assessment. However, measuring AGT distance using ultrasound may be a viable superior alternative for evaluating subluxation in stroke patients.
Conflict of interest
The authors declare no conflicts of interest.
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