Introduction: This study is a cross-sectional study that investigated the factors influencing shoulder mobility in terms of pain, grip strength, and supraspinatus muscle thickness in patients with impaired shoulder mobility during chemotherapy after radical breast cancer surgery. Methods: This study included 165 female patients with unilateral breast cancer who had shoulder joint mobility disorders during chemotherapy within 3 months after surgery. The clinical examination included the maximum active range of motion of the shoulder (flexion, extension, abduction, adduction, external rotation, and internal rotation), pain score (visual analog scale [VAS]), grip strength, and supraspinatus muscle thickness. Results: During shoulder abduction, supraspinatus muscle thickness was greatest at 90°, lowest at 0°, and higher at 60° than at 30° (p < 0.01). The factors influencing the active movement of shoulder flexion were the VAS score, body weight, grip strength, and supraspinatus contraction rate (R2 = 0.295), while the factors influencing active shoulder abduction were the VAS score, body weight, grip strength, supraspinatus muscle thickness (drooping position), and supraspinatus contraction rate (R2 = 0.295). Moreover, the factors influencing the active movement of shoulder external rotation were age, VAS score, body weight, grip strength, and supraspinatus muscle thickness (drooping position) (R2 = 0.258). There were no significant results from multiple linear regressions for shoulder extension, adduction, or internal rotation. Conclusion: Pain, weight, grip strength, supraspinatus muscle thickness, and supraspinatus distensibility are the main factors affecting shoulder flexion, abduction, and external rotation. In addition, supraspinatus muscle thickness and contraction rate may be a new index for assessing shoulder dysfunction.

The International Cancer Research Center of the World Health Organization estimates that 1.67 million new cases of breast cancer occur annually, with 525,000 deaths. It is the most common cancer among women and the second most common cancer worldwide after lung cancer [1]. The annual economic burden of cancer in China is approximately 970 million yuan [2]. Moreover, the incidence of breast cancer is high among female cancer patients, with a 5-year survival rate of 90% [3]. After breast cancer surgery, approximately 21–35% of patients have shoulder joint movement disorders, which seriously affects upper limb movement in daily life [4, 5].

Drug treatment for breast cancer has long-term sequelae that affect the upper limbs. The main sequelae include shoulder movement disorder, decreased muscle strength around the shoulder and scapula, rigidity of the pectoralis major and minor, pain in the shoulder and arm, and lymphedema [6]. Surgical treatment can cause damage to the tissues of the nerves, muscles, and blood vessels. The severity of shoulder pain and mobility restriction is related to mastectomy, lymphadenectomy, chemotherapy, and radiotherapy [7‒11]. According to previous studies, most patients with cancer will experience a certain degree of discomfort and functional limitation, and the incidence of cancer after breast cancer surgery varies depending on the surgical method. However, regardless of the surgical method, most patients with cancer will experience chronic arm or shoulder discomfort, which can last for up to 3 years after surgery [12, 13]. The sequelae caused by the clinical treatment of breast cancer may be related to the pathological development of the affected rotator cuff muscles [14]. A previous study that performed a follow-up evaluation at 6 months after surgery observed that the intensity of shoulder pain increased, shoulder function decreased, and symptoms significantly worsened throughout the follow-up period. At the same time, the quality of life of the postoperative patients also decreased, and the thickness of the supraspinatus muscle in the affected shoulder sleeve muscle group showed a decreasing trend. Early detection of these issues is of great significance for early or preventive treatment [15]. Therefore, we hypothesized that shoulder joint dysfunction after radical breast cancer surgery is related to supraspinatus muscle thickness. This study aimed to investigate the factors influencing shoulder mobility in terms of pain, grip strength, and supraspinatus muscle thickness in patients with impaired shoulder mobility during chemotherapy after radical breast cancer surgery.

We conducted a cross-sectional study between November 2020 and March 2022. This study included 165 female patients with unilateral breast cancer who had shoulder joint mobility disorders during chemotherapy within 3 months after surgery. Patients were interviewed regarding their age (years), body mass index, and side of surgery. The type of surgical treatment (modified radical mastectomy, breast-conserving surgery, sentinel lymph node biopsy, and axillary lymph node dissection) was recorded by inspecting the patient files. Body mass index was calculated as the weight in kilograms divided by the square of height in meters (kg/m2).

This study has been approved by the Ethics Committee of Beijing Chaoyang District Sanhuan Cancer Hospital in accordance with its regulations and guidelines. All participating patients or legal guardians have agreed to participate and signed an informed consent form.

A physical therapist conducted the clinical examination, which included the maximum active range of motion of the shoulder (flexion, extension, abduction, adduction, external rotation, and internal rotation), pain score (visual analog scale [VAS] score), grip strength, and supraspinatus muscle thickness. The above tests were performed twice, and the mean values were used for statistical analysis.

According to the guidelines of the American Medical Association, a goniometer is used to measure the maximum range of motion of the shoulder joint for abduction, adduction, flexion, extension, internal rotation, and external rotation [16]. The VAS score is used to evaluate shoulder pain. To determine the VAS score, a 10 cm line is drawn, with the leftmost end marked as “no pain” and the rightmost end marked as “the most severe pain experienced,” and participants were asked to mark the degree of pain on the scale before and after treatment and to measure the distance to the left end.

Supraspinatus muscle thickness measurement by ultrasound is a reliable method for muscle atrophy evaluation [17]; therefore, we measured the supraspinatus muscle thickness using ultrasound. A marker was placed with a magic marker at the 50% site above the scapular spine (linear distance from the acromial angle to the supra-scapular angle), the probe was applied perpendicular to the long axis of the muscle, and the longitudinal image was measured.

Ultrasound images were obtained with an echo jelly attached to the probe to obtain clear ultrasound images without compressing the superficial musculature. Supraspinatus muscle thickness was defined as the distance from the fascia at the border of the trapezius muscle to the scapula. At the start of the study, the therapist practiced operating the ultrasound machine under the supervision of a clinical ultrasound technician for approximately 1 month. The thickness of the supraspinatus muscle was measured at 0°, 30°, 60°, and 90° of active abduction of the shoulder on the affected side of the patient in a sitting position. The supraspinatus muscle thickness at 0° shoulder dips was used as a reference value to calculate the supraspinatus contraction rate at 90° of abduction. We used the following equation: supraspinatus contraction rate (%) = supraspinatus muscle thickness at 90° of active abduction/supraspinatus muscle thickness at 0° of abduction.

We selected the upper limb of the patient’s unimpaired side and tested grip strength as an indicator of whole-body endurance to assess physical strength and upper limb muscle strength [18]. Standard grip dynamometry was used to measure grip strength.

Statistical Analyses

The required number of samples was calculated using the G*Power software. The following method was used: “Linear multiple regression: Fixed model, R2 deviation from zero.” The sample size for this study was calculated by setting α = 0.05 and test efficacy 1-β = 0.8. With reference to the literature and previous case analysis, the minimum total sample size was calculated as 103 cases at a significance level of 0.05 bilaterally and an effect size of 0.15.

We used the Kolmogorov-Smirnov test to determine whether the variables conformed to a normal distribution. One-way analyses of variance (ANOVA) and multiple comparisons (Bonferroni test) were used to test for statistically significant differences in supraspinatus muscle thickness when the abduction angle was changed. In addition, a multiple linear regression analysis using shoulder joint mobility as a dependent variable was performed. The data were analyzed using SPSS version 23.0 for Windows. Statistical significance was set at p < 0.05.

Breast-conserving surgery and modified radical mastectomy were performed in 76 (46.1%) and 89 (53.9%) of the patients, respectively, and axillary lymph node dissection was performed in most patients (74.6%). The clinical characteristics of the patients are summarized in Table 1.

Table 1.

Clinical characteristics of the patients in the study

Age, years 51.0±12.5 
BMI 24.7±3.7 
Type of surgery 
 BCS (+SLNB) 29 (17.6) 
 BCS (+ALND) 47 (28.5) 
 MRM 89 (53.9) 
Type of lymph node dissection 
 SLNB 32 (19.4) 
 ALND 123 (74.6) 
Operation side 
 Right 88 (53.3) 
 Left 77 (46.7) 
Active ROM of the shoulder, ° 
 Flexion 125.0±28.4 
 Extension 41.9±8.8 
 Abduction 122.7±32.2 
 Adduction 38.2±8.3 
 External rotation 51.1±10.2 
 Internal rotation 54.8±15.2 
 Grip strength, kg 20.3±5.8 
 VAS 1.9±1.5 
Age, years 51.0±12.5 
BMI 24.7±3.7 
Type of surgery 
 BCS (+SLNB) 29 (17.6) 
 BCS (+ALND) 47 (28.5) 
 MRM 89 (53.9) 
Type of lymph node dissection 
 SLNB 32 (19.4) 
 ALND 123 (74.6) 
Operation side 
 Right 88 (53.3) 
 Left 77 (46.7) 
Active ROM of the shoulder, ° 
 Flexion 125.0±28.4 
 Extension 41.9±8.8 
 Abduction 122.7±32.2 
 Adduction 38.2±8.3 
 External rotation 51.1±10.2 
 Internal rotation 54.8±15.2 
 Grip strength, kg 20.3±5.8 
 VAS 1.9±1.5 

Values are presented as the mean ± standard deviation or n (%).

SLNB, sentinel lymph node biopsy; BMI, body mass index; MRM, modified radical mastectomy; BCS, breast-conserving surgery; ALND, axillary lymph node dissection; ROM, range of motion.

The results of the one-way ANOVA for supraspinatus muscle thickness showed that it was greatest at 90° of shoulder abduction, lowest at 0° of abduction, and higher at 60° than at 30° of abduction (p < 0.01) (Table 2). The results of multiple linear regression showed that the factors influencing the active movement of shoulder flexion were the VAS score, body weight, grip strength, and supraspinatus contraction rate (R2 = 0.295, adjusted R2 = 0.277) (Table 3). The factors influencing active shoulder abduction were the VAS score, body weight, grip strength, supraspinatus muscle thickness (drooping position), and supraspinatus contraction rate (R2 = 0.295, adjusted R2 = 0.273) (Table 4). The factors influencing active shoulder external rotation were age, VAS score, body weight, grip strength, and supraspinatus muscle thickness (drooping position) (R2 = 0.258, adjusted R2 = 0.235) (Table 5). There were no significant results from multiple linear regressions for shoulder extension, adduction, or internal rotation.

Table 2.

Results for supraspinatus muscle thickness and expansion rate (n = 165)

Shoulder joint abduction (°)p value
Supraspinatus muscle thickness, cm 0° 1.3±0.3 **30°>0°; 60°>0°, 30°; 90°>0°, 30°, 60° 
30° 1.5±0.3** 
60° 1.6±0.3** 
90° 1.7±0.3** 
Supraspinatus contraction rate (%)  135.5±30.6  
Shoulder joint abduction (°)p value
Supraspinatus muscle thickness, cm 0° 1.3±0.3 **30°>0°; 60°>0°, 30°; 90°>0°, 30°, 60° 
30° 1.5±0.3** 
60° 1.6±0.3** 
90° 1.7±0.3** 
Supraspinatus contraction rate (%)  135.5±30.6  

Values are means ± standard deviation. **p < 0.01.

Table 3.

Stepwise multiple linear regression analysis for shoulder active flexion movement of participants (n = 165)

VariablesBetatp value95% CIa
Constant  8.744 <0.01 115.240–182.482 
VASb −0.351 −4.874 <0.01 −9.152–−3.874 
Weight −0.330 −4.590 <0.01 −1.282–−0.511 
Grip strength 0.271 3.673 <0.01 0.617–2.051 
Supraspinatus contraction rate 0.153 2.275 <0.05 1.872–26.477 
VariablesBetatp value95% CIa
Constant  8.744 <0.01 115.240–182.482 
VASb −0.351 −4.874 <0.01 −9.152–−3.874 
Weight −0.330 −4.590 <0.01 −1.282–−0.511 
Grip strength 0.271 3.673 <0.01 0.617–2.051 
Supraspinatus contraction rate 0.153 2.275 <0.05 1.872–26.477 

The independent variables were as follows: VAS score, age, weight, height, grip strength, supraspinatus muscle thickness (drooping position), and supraspinatus contraction rate.

aCI, confidence interval.

bVAS, visual analog scale, pain severity score.

Table 4.

Stepwise multiple linear regression analysis for shoulder active abduction movement of participants (n = 165)

VariablesBetatp value95% CIa
Constant  3.241 <0.01 39.115–161.124 
VASb −0.302 −4.153 <0.01 −9.390–−3.337 
Weight −0.321 −4.327 <0.01 −1.442–−0.538 
Grip strength 0.275 3.668 <0.01 0.709–2.365 
Supraspinatus contraction rate 0.279 3.101 <0.01 10.654–48.021 
Supraspinatus muscle thickness 0.182 1.998 <0.05 0.243–41.998 
VariablesBetatp value95% CIa
Constant  3.241 <0.01 39.115–161.124 
VASb −0.302 −4.153 <0.01 −9.390–−3.337 
Weight −0.321 −4.327 <0.01 −1.442–−0.538 
Grip strength 0.275 3.668 <0.01 0.709–2.365 
Supraspinatus contraction rate 0.279 3.101 <0.01 10.654–48.021 
Supraspinatus muscle thickness 0.182 1.998 <0.05 0.243–41.998 

The independent variables were as follows: VAS score, age, weight, height, grip strength, supraspinatus muscle thickness (drooping position), and supraspinatus contraction rate.

aCI, confidence interval.

bVAS, visual analog scale, pain severity score.

Table 5.

Stepwise multiple linear regression analysis for shoulder active external rotation movement of participants (n = 165)

VariablesBetatp value95% CIa
Constant  13.261 <0.01 70.628–95.349 
Age −0.204 −2.801 <0.01 −0.285–−0.049 
VASb −0.226 −3.015 <0.01 −2.499–−0.521 
Supraspinatus muscle thickness −0.231 −3.241 <0.01 −13.707–−3.327 
Weight −0.248 −3.199 <0.01 −0.393–−0.093 
Grip strength 0.175 2.261 <0.05 0.039–0.582 
VariablesBetatp value95% CIa
Constant  13.261 <0.01 70.628–95.349 
Age −0.204 −2.801 <0.01 −0.285–−0.049 
VASb −0.226 −3.015 <0.01 −2.499–−0.521 
Supraspinatus muscle thickness −0.231 −3.241 <0.01 −13.707–−3.327 
Weight −0.248 −3.199 <0.01 −0.393–−0.093 
Grip strength 0.175 2.261 <0.05 0.039–0.582 

The independent variables were as follows: VAS score, age, weight, height, grip strength, supraspinatus muscle thickness (drooping position), and supraspinatus contraction rate.

aCI, confidence interval.

bVAS, visual analog scale, pain severity score.

This study investigated the factors influencing shoulder mobility in patients who underwent radical breast cancer surgery. Pain, weight, grip strength, supraspinatus muscle thickness, and supraspinatus distensibility were the main factors affecting shoulder flexion, abduction, and external rotation. Reasons for limited shoulder motion after radical breast cancer surgery include trauma, scarring, pain, and other factors. Acute postoperative pain, radiation therapy, and invasive surgery are risk factors for chronic pain [19, 20]. Acute postoperative pain is associated with patients with high levels of preoperative anxiety and is thus more likely to occur in such patients. These patients reduce their activity to protect their arms and treatment areas from further damage [21]. Therefore, preoperative rehabilitation education is particularly important.

The supraspinatus is an important component of the rotator cuff muscle group and is important for shoulder joint stability. The supraspinatus muscle is the most commonly torn muscle in the rotator cuff muscle group and has always been a research hotspot; however, further elucidation regarding this small but important muscle is required [22]. Supraspinatus dysfunction is present in cases of periarthritis, rotator cuff injury, and subluxation of the shoulder joint in patients with hemiplegia. Additionally, a decreasing trend was observed in the thickness of the supraspinatus tendon on the affected side [23]. Our study suggests that there is a tendency for supraspinatus hypofunction in patients with impaired shoulder joint mobility after radical breast cancer surgery. Promoting the recovery of supraspinatus function may be an important factor in improving shoulder mobility in patients after radical breast cancer surgery. Patients who undergo radical breast cancer surgery have a general fear of active shoulder movement due to the fear of pain and leakage in the treated shoulder, resulting in a long-term lack of movement of the affected upper extremity, supraspinatus muscle atrophy, decreased contractile function of the supraspinatus muscle, and other disuse syndromes.

In this study, supraspinatus muscle contraction rate was established as a new index for assessing shoulder dysfunction. The muscle contraction rate represents the muscle contraction function, elasticity, and activity, which are objective indicators for assessing muscle function. In our previous study, we used the transversus abdominis muscle contraction rate as an indicator of the intervention effect and effectively evaluated the effect of core strength gymnastics on female urinary incontinence [24]. As there may be individual differences in muscle thickness, muscle distensibility can be objectively compared between volunteers; in other words, the problem of individual differences is eliminated. In the clinical application, you can measure the supraspinatus muscle contraction rate of the patients before the operation, guide the supraspinatus rehabilitation exercise gymnastics for the patients with low supraspinatus muscle contraction rate, and carry out a stage evaluation to guide the rehabilitation training program after the operation. This altogether can precisely improve the shoulder joint function.

The absolute muscle strength of the deep muscle groups, including the inner muscle and rotator cuff muscle groups, is smaller than that of the outer muscle, and they play a greater role in the stability of the joints and trunk; therefore, as a method of assessing the function of the deep muscle groups, both the muscle strength and activity, such as the muscle contraction rate, should be included.

The results of this study indicate that individuals with weaker grip strength are prone to shoulder joint dysfunction. Grip strength, an indicator of endurance, predisposes patients to shoulder dysfunction when their physical strength and endurance decrease. In the future, targeted rehabilitation and exercise interventions should be actively carried out with preoperatively and postoperatively targeted rehabilitation exercise intervention, to prevent disuse syndrome.

Study Limitations

The main limitation of this study is that the coefficients of determination of the multivariate regressions were low. The coefficients of determination with active shoulder flexion, abduction, and external rotation as the dependent variables were 0.295, 0.295, and 0.258, respectively, implying that there are other factors influencing joint mobility disorders; therefore, future studies should increase the sample size and the number of independent variables.

The present study revealed that the main factors affecting shoulder flexion, abduction, and external rotation after radical breast cancer surgery were pain, weight, grip strength, supraspinatus muscle thickness, and supraspinatus distensibility. In addition, the supraspinatus muscle contraction rate may be a new index for assessing shoulder dysfunction.

This study has been approved by Beijing Chaoyang Sanhuan Cancer Hospital and registered under No. ZH-2020013. All participating patients or legal guardians have agreed to participate and signed an informed consent form.

The authors have no conflicts of interest to declare.

Not applicable.

All authors contributed to the study conception and design. Material preparation and data collection were performed by Xin Zhang, Jialin Fan, Chao Wang, and Ming Huo. Data analysis was performed by Hualong Xie and Shinichiro Murakami. The manuscript was written by Xin zhang, Ming Huo, and Hualong Xie. All authors read and approved the final version of the manuscript.

Additional Information

Xin Zhang, Chao Wang, and Jialin Fan contributed equally to this work.

The STROBE checklist is under online supplementary material (for all online suppl. material, see https://doi.org/101159/000535063). The data generated by this research can be obtained from the corresponding author within reasonable requirements.

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