Factors affecting upper limb function recovery after mastectomy with immediate breast reconstruction: a STROBE study

Abstract

Purpose

With improvements in surgical techniques, the number of immediate breast reconstructions (IBRs) after mastectomy is increasing. Based on reports regarding postoperative shoulder function, scapular alignment and strength recovery have been confirmed, while movement accuracy has deteriorated. As this might induce residual shoulder discomfort, proper rehabilitation may manage the situation. Along with the recommendation for early rehabilitation after breast cancer surgery, this study was designed to identify the relationship between shoulder function and acute postoperative breast cancer survivors (BrCS) after IBR.

Methods

In this prospective observational study, subjective and objective functions of 67 BrCS were observed over 4 months. Hierarchical regression and correlation studies were conducted to reveal the relationship between functional improvement.

Results

The improvement of the QuickDASH score was significantly explained by the improvement of six shoulder functions after adjusting for covariates (R² = 0.21, p = 0.01). Among the variables, the change in range of motion and neuropathic pain was statistically significant (p < 0.03). The BrCS with chemotherapy group showed deterioration of subjective shoulder function, compared with the BrCS without chemotherapy group (t = 2.97, p = 0.004). This might be owing to the difference in neuropathic pain score changes between the two groups. There was no major difference in functional improvement between the two IBR options.

Conclusion

Regular exercise focused on pectoral tightness may be effective in improving general shoulder flexibility. Given that neuropathic pain did not change, specific interventions may be required. In addition, rehabilitation should be differentiated based on the chemotherapy plan.

Introduction

Pectoral tightness, defined as the limitation of arm elevation and horizontal abduction without rotation limitation [1], is a common upper limb dysfunction in addition to pain, strength loss, and lymphedema after mastectomy [2]. Recently, the number of immediate breast reconstructions (IBRs) has increased [3, 4] as the bilateral mastectomy rate has risen [5]. However, research focused on shoulder function after IBR was not sufficient to understand overall shoulder function. While the abdominally-based approach or tissue expander/implant-based approach provides better upper limb function recovery [6, 7], studies have reported that breast expansion due to reconstruction might change the muscle force vector such that the movement quality becomes inaccurate [2, 8]. Given that recent rehabilitation studies insisted on including movement quality in important postoperative shoulder functions [9, 10], this might be more important than quantitative shoulder functions such as strength or range of motion. Moreover, previous research has focused on donor site morbidities, rather than upper limb function, in the abdominally-based approach [2]; subjective upper limb function is commonly measured by disabilities of the arm, shoulder, and hand (DASH) and Quick DASH (Q-DASH) [11, 12].

Given that current rehabilitation has shown that neuropathic pain [13] and working body schema (WBS) [14, 15] could be related to subjective upper limb dysfunction, investigating previously reported shoulder functions with common patient-reported outcome measures in this population would further the understanding of upper limb dysfunction after IBR. Therefore, we designed a 4-month prospective observational study of breast cancer survivors (BrCS) to understand upper limb function and its change during cancer therapy and postoperative rehabilitation; this study reports correlations between functional changes and reports the predictive value of shoulder function for subjective shoulder disability. We primarily hypothesized that improvement in six functions regarding upper limb disability (shoulder range of motion, shoulder strength, scapular alignment, shoulder proprioception, neuropathic pain, and WBS) would significantly explain the improvement in subjective function.

Methods

1. Study design

   This was a STROBE study for a 4-month prospective cohort (Registered at CRIS, KCT 0006501). Clinical observation was conducted in the Department of Rehabilitation Medicine of a tertiary hospital.

2. Ethical approval

   Ethical approval for this study was obtained from the Seoul National University Bundang Hospital Institutional Review Board (IRB No. B-2108-702-309). 

3. Surgical options

   IBR surgery options included transverse rectus abdominis myocutaneous (TRAM) flap and direct-to- implant or expander insertion (DoT). IBR was selected by the surgeon and patient after a thorough consultation [7]. 

4. Sample size

   Given the six variables used in the regression study, 60 participants were required by the statistical recommendation (sample size=variables × 10 [16]). Considering the 10% drop rate, we decided to enroll 67 BrCS.

5. Participants

   All BrCS who underwent IBR were included in the study. BrCS aged >18 years who were able to understand the Korean language and who underwent ipsilateral IBR using TRAM or DoT were included. Patients were screened at the first postoperative rehabilitation medicine clinic from August 2021 to February 2022. To avoid selection bias, we excluded patients with BrCS diagnosed with adhesive capsulitis [17], axillary web syndrome [18], rotator cuff disease [1], and severe arm lymphedema. Those with unhealed surgical sutures, bilateral surgery, and terminal cancer were also excluded to provide proper medical intervention as quickly as possible. After screening, 67 patients with BrCS following IBR provided written informed consent. A total of 60 participants completed the follow-up measurements. The overall procedure is illustrated in Figure 1. The demographic and cancer-related summary of the participants is provided in Table 1. 

6. Electronic medical record review

   Each participant’s age, height, weight, cancer-related information, and cancer treatment-related information were identified via electronic medical records at each visit. At the first visit, 21, 9, and 20 patients had undergone chemotherapy, radiation therapy, and hormonal therapy, respectively. At the second visit, 32, 17, and 39 BrCS had undergone or were undergoing the three cancer therapies, respectively. Tamoxifen was the most used hormonal therapy.

7. Functional assessments
   1. Shoulder range of motion (ROM): Range of the operated arm measures were taken three times using a smartphone application [19]. The sum of the mean ROM values was used for the main analysis [20, 21].
   2. Shoulder Strength: Peak torques of operated shoulder abduction, adduction, external rotation, and internal rotation were measured using a dynamometer (BTE PrimusRS™, BTE Technologies, Inc., Hanover, MD) with a 60-degree per second angular velocity [7]. The sum of the peak torque values was used for the main analysis [20].
   3. Resting scapular alignment: The distance between the coracoid process and the 4^th intercostal space was measured three times using a PALpation Meter (PALM; Performance Attainment Associates, St Paul, MN) [22]. The distance was then divided by height and multiplied by 100 [23] to represent the pectoralis minor length index (PMI). The mean PMI was used for the main analysis.
   4. Absolute angle error: A passive/active protocol for internal rotation was used to measure shoulder proprioception [15]. The average absolute differences were used for the analysis.
   5. Upper limb body schema: A hand left right judgement test (LRJT) was performed to examine the WBS of the upper limb [15, 24]. The average accuracy was used for the main analysis.
   6. Neuropathic pain score: The possibility of neuropathic pain was quantified using the Pain Detection Questionnaire (PDQ) [25]. The PDQ can be used to measure neuropathic pain in cancer survivors, including BrCS [26, 27], and the Korean version has been validated [28]. A higher score indicated a greater possibility of neuropathic pain.
8. Patient-reported outcome measures

   Upper limb disability was measured using the Korean version of the Q-DASH [29, 30]. A higher score represented more severe upper limb disability. Quality of life, various individual functions, and symptoms were also subjectively reported via the Korean version of European Organization for Research and Treatment of Cancer (EORTC) Core 30 (C30) and the Korean version of the breast cancer-specific quality of life questionnaire (BR23) [31-34]. C30 was administered to evaluate the participants’ quality of life (QoL), physical functioning (PF), role functioning (RF), emotional function (EF), cognitive functioning (CF), social functioning (SF), fatigue (FA), pain (PA), and insomnia (SL), while BR23 was used to evaluate the degree of systemic therapy side effects (ST), arm and breast symptoms (AS and BS), body image (BI), future perspective (FP), and sexual function (SEF) in BrCS. 

9. Rehabilitation intervention

   All participants were directed to practice specific exercise regularly. Exercise was instructed at the first visit, and the exercise adherence survey was conducted at the second visit (supplemental exercise description). Among the patients, 28 BrCS who underwent TRAM also received postoperative donor-site care education. Additionally, 43 participants were referred to the physical therapy unit. Exercise therapy was prescribed for 40 BrCS with pectoral tightness to repeat the instructed exercise two or three times. AK provided re-education for exercise consistency. Complex decongestive therapy was also prescribed for 13 BrCS who had risks of lymphedema to preventatively provide self-care education by a specialized physical therapist. As this variety could also affect improvement of upper limb disability and QoL, both the exercise adherence score and total number of visits to the physical therapy unit over the follow-up period were included in the covariate analysis.

10. Statistical analysis

    All procedures were performed using SPSS 26.0 (IBM, Armonk, NY, USA). Paired t-tests and non-parametric tests were used to summarize the follow-up results. For analysis, the improvement in each variable was calculated by subtracting the value at the first visit from that of the second visit. Improvements of some variables such as Q-DASH, PDQ, absolute angle error, LRJT reaction time, FA, PA, SL, ST, BS, and AS were inversely calculated, as the increase in the scores indicated worsening of the functions or symptoms. A per-protocol analysis was then performed.

    Covariate analysis was performed. Pearson’s correlation test and independent t-test were conducted to find covariates (p<0.1). When the tests reported multiple significance variables, only significant variable(s) via the multiple regression study (p<0.05) were selected as covariates.

    We then performed a hierarchical regression. Hierarchical regression analysis was conducted using the traditional method [16], and the covariates and independent variables were entered in the first and second blocks, respectively. Then, a simple linear regression study and analysis of variance (ANOVA) with Bonferroni’s test was conducted for deeper understanding.

    Independent t-tests were conducted to identify differences in each improvement between the BrCS who underwent TRAM and DoT and those with and without chemotherapy (CTx). Additional analysis was performed, and the results are described in supplementary statistical analysis. 

Results

Changes in the cohort

At the first visit, there were no differences in QoL, Q-DASH score, and the six shoulder functions between the BrCS with and without CTx and between those who underwent TRAM and DoT. At the second visit, the PDQ and Q-DASH scores were higher in patients with BrCS with CTx than in patients without CTx (t[58]=2.63, p=0.011; t[51.2]=3.3, p=0.002; respectively). During the follow-up, the shoulder ROM, shoulder peak torque, shoulder proprioception, scapular alignment, LRJT accuracy, and upper limb disability improved, while the LRJT reaction time and neuropathic pain score did not change. Both the objective and subjective examination results during the follow-up period are shown in Table 2. 

Covariate analysis

Pearson’s correlation test reported that the post-operative day (POD) at the first visit (the time from surgery to the commencement of rehabilitation exercise) and exercise adherence were related to the improvement of the Q-DASH score (r =-0.24, p = 0.07; r = 0.27, p = 0.04; respectively). The independent t-test also reported that the Q-DASH score improvement was different between the BrCS who received chemotherapy and those without a history of chemotherapy (t[58]=-2.97, p=0.004), and between the BrCS who underwent TRAM and those who underwent DoT (t[58]=1.81, p=0.08). The linear regression model significantly explained the Q-DASH score improvement (R²=0.33, F[4,55]=6.63, p=0.00), but only history of chemotherapy and reconstruction type were significant variables in the regression model (p<0.01). Therefore, we included these two variables as covariates in the hierarchical regression analysis.

The relationship between the Q-DASH improvement and functional outcomes improvement

The hierarchical regression model with improvement in six variables significantly explained the Q-DASH improvement during follow-up (adjusted R²=0.36, p<0.01). Among the six variables, both the increase in total ROM and the increase in PDQ score were significant variables in the model. As the partial correlation study (Supplementary Table S1) reported a stronger impact in abduction improvement (r=0.39) than that of total ROM (r=0.27), we performed a regression analysis including abduction instead of total ROM. Table 3 presents the results of the analyses. Post-hoc power analysis using G-power software showed 99% and 87% of power for crude analysis (f²=0.64) and increase of R² (R²=0.23), respectively. 

Explaining Q-DASH score improvement with individual functional outcomes

Simple regression analysis confirmed the hierarchical regression model (Table 4). While the PDQ improvement was significantly related to the Q-DASH score change in all groups (R²>0.24), except for the BrCS that did not undergo CTx (R²=0.09), ROM improvement was related only to Q-DASH improvement for the BrCS who underwent TRAM (R²=0.16). Interestingly, none of the functional improvements explained the upper limb disability resolution in BrCS who did not undergo CTx. In this group, the improvement in shoulder proprioception and external rotation seemed to be related to the upper limb disability change (R²<0.11), without statistical significance (p=0.07 and 0.10, respectively). 

No interaction effect of the reconstruction type and history of chemotherapy

Univariate ANOVA revealed a main effect for IBR options (F[1,56]=6.43, p<0.02) and history of chemotherapy (F[1,56]=10.67, p<0.01), with no interaction effect (F[1,56]=3.41, p=0.07). The estimated marginal means and 95% confidence intervals (CIs) for BrCS with CTx, BrCS without CTx, BrCS who underwent TRAM, and BrCS who underwent DoT were 0.91 (-4.08 5.90), 13.11 (7.53 18.68), 11.74 (5.96 17.53), and 2.27 (-2.47 7.02), respectively. Despite the lack of a significant interaction effect, we categorized them into four groups to compare changes in upper limb disability. ANOVA revealed a significant group difference (F[3, 56]=7.07, p=0.00). In the group comparison, the Q-DASH score deteriorated in BrCS who underwent DoT and CTx, while the Q-DASH score improved in the other three groups (p<0.012). The results are shown in Figure 2.

Discussion

This study aimed to report the relationship between changes in subjective shoulder disability and various shoulder functions. Although the variables regarding exercise and rehabilitation were excluded from the covariates, initiation of exercise should be considered as early as possible, and practice of stretching exercises should be continued for subjective improvement. When the effect of chemotherapy history and reconstruction type were statistically controlled, the abduction improvement and neuropathic pain decrease were significantly correlated with subjective improvements in upper limb functionality. Despite the lack of an interaction effect between them, a trend for interaction was observed (Figure 2). The present study reported no adverse effects of chemotherapy following IBR; however, subjective upper limb function might not improve. 

The analysis using this increase was different from the cross-sectional analysis (Supplementary Tables S3 and S5). The main result mostly agrees with a similar analysis [21], while it partially agrees with cross-sectional studies [13, 20]. Pectoral tightness was confirmed by observation. In this study, the mean shoulder ROM was a <150-degree elevation with a >80-degree rotation after surgery. Given that abduction requires adequate scapular adduction and humeral external rotation, the pectoralis major tightness appears to be key in the limitation of arm abduction. The improvement in muscle tightness is directly related to amelioration in upper limb disability and indirectly related to QoL improvement via PF, RF, and BS (Supplementary Table S2). Given that 10 PMI was regarded as normal in the resting position [35], the pectoralis minor length was not significantly shortened after IBR. As reported, the pectoralis minor was not severely shortened after surgery, and returned normal at 4 months postoperatively. Thus, pectoralis major tightness should be measured, and its acute rehabilitation should be prioritized after IBR, rather than that of the pectoralis minor.

The neuropathic pain score change was also the most significant variable for the Q-DASH score change, which agrees with a previous report that neuropathic pain was the sole significant variable explaining the DASH score. In this study, this score change correlation coefficient was slightly larger (r=0.49) than the correlation coefficient of the PA change from the EORTC C30 (r=0.47) to the improvement in the Q-DASH score, and the two pain score changes were moderately correlated with each other (r=0.46). The major finding of this study was that the improvement in the PDQ score was independent of the abduction and strength changes (Supplementary Table S1). A recent systematic review article [36] recommended the use of transcutaneous electrical nerve stimulation (TENS) and physiotherapy in conjunction with pharmaceutical or cognitive intervention, but there was no consensus on the appropriate physiotherapy. Given that manual therapy, including massage, has a positive effect on postoperative pain in BrCS [37], adequate physiotherapy might provide TENS and manual therapy. While until now rehabilitation programs have commonly aimed at ROM improvement, future rehabilitation programs will preferentially aim to manage the painful nature of the condition rather than the ROM. However, further research must be conducted to shed light on this issue.

The improvement in dynamic shoulder strength was not related to the improvement in other shoulder functions and subjective reports. Although the cross-sectional relationship between strength and the Q-DASH score (Supplementary Table S5) was similar to that reported by Harrington and colleagues [20], the increase in strength was not similar. Myung and colleagues [7] described that muscle continuity provided better exercise adherence for the full recovery of shoulder strength. Given the lack of a relationship between the ROM and strength increases, the shoulder strength increase seems to be a natural recovery rather than due to the muscle length change. However, the strength index can be used as a predictor. According to the prediction analysis (Supplementary Table S8), the early peak torque of rotation significantly predicted late upper-limb disability. Therefore, shoulder strengthening is not necessary for acute postoperative rehabilitation in this population, but the initial measurement could distinguish rehabilitation candidates.

Similarly, shoulder proprioception improvement was not related to upper limb disability. Given the possible relationship between movement accuracy and social function, this function should not be ignored. Considering that social function could be influenced by upper-limb disability, movement quality should be measured and targeted, especially in patients with BrCS who underwent breast reconstruction. A previous study reported that this surgery may alter the shoulder biomechanics [8]; hence, the movement quality was poorer than that of the BrCS who underwent mastectomy and controls. In addition, the present study reported a possible explanation value of shoulder proprioception improvement for the improvement in the upper limb disability score. Despite insignificance (p<0.07), the improvement in shoulder proprioception could explain 10% of the Q-DASH score change in the BrCS without CTx (Table 4). In a previous study, movement quality, pain intensity, and DASH score improved after rehabilitation, including pectoral muscle stretching [9]. In this study, the POD of the participants was approximately 18 months, and approximately 40% of the participants received chemotherapy. Considering that systemic therapy ends within a year after surgery, the negative effects of chemotherapy might decrease. Therefore, the results of the previous study may align with the results of the present one. When the BrCS were not administered chemotherapy after IBR, movement accuracy could be improved in the rehabilitation program to ameliorate upper limb disability.

As the accuracy of LRJT improved throughout the cohort, a positive relationship with upper limb disability change was expected. However, there was no relationship with upper limb disability. We only found a trend for a positive relationship between the improvement of body schema and the improvement of social function (Supplementary Table S2) and confirmed the predictive value of LRJT accuracy (Supplementary Table S8), as we reported previously [15]. Brain-targeted intervention, such as Graded Motor Imagery (GMI), to improve LRJT results has been recently studied in various pain conditions. In addition to studies that included participants with chronic regional pain syndrome, GMI was only applied to participants with chronic shoulder pain [38], frozen shoulder [39, 40], and knee osteoarthritis [41]. Only two studies implemented the LRJT [40, 41], but the effect of GMI was controversial between two results. Given this controversy, the present result could be explained by the fact that we provided a rehabilitation program without GMI. As the central mechanism for pain control was not manipulated by a specific regimen such as GMI, the degree of pain and disability was sustained in this study. Thus, improvement in WBS did not change upper limb disability or pain in this population. Along with neuropathic pain rehabilitation, this is a challenge to be addressed in the future.

This study reported both subjective and objective outcomes of BrCS who underwent IBR. Given the increasing importance of early rehabilitation after IBR, this study might help clinicians understand the physical characteristics and impact of subjective reports. In addition, we captured the real course of breast cancer treatment, in which systemic therapy or local therapy began after surgery, while early mobilization started as soon as possible.

However, this study should be interpreted with caution. First, the small sample size reduced the power of the analysis. Second, a few variables were not adequately changed. While the LRJT accuracy was statistically improved, the difference was lower than the previous minimal clinically important difference of 10%. Third, the measurement method may have decreased study quality. The length of the pectoralis minor was palpated rather than imaged by X-ray; the absolute angle error was modified from the standard position, and the test-retest reliability was approximately 0.7 [15]. Fourth, the data on non-protocol exercises such as yoga, which may have affected upper limb function, were not recorded. Fifth, the cause-effect relationship was not clear owing to differences in cancer therapy and rehabilitation therapy. Finally, there was no normative Q-DASH score for the BrCS, and we could not identify the normal value of each function regarding the Q-DASH score.

Conclusion

We observed shoulder function and subjective reports in BrCS after IBR. In the 4-month cohort, adverse effects of chemotherapy and DoT were reported, and the change in abduction ROM and the possibility of neuropathic pain affected the degree of upper limb disability. Rehabilitation focused on resolving muscle tightness could help decrease upper limb disability; however, it did not alleviate neuropathic pain. Considering the impact of neuropathic pain on life and various functions, acute rehabilitation may be a strategy for reducing this pain. Based on this study, we hope that an effective postoperative rehabilitation program will be investigated in the future.  

Declarations

Funding

The authors declare that no funds, grants, or other support were received during the preparation of this manuscript.”

Competing Interests

The authors have no relevant financial or non-financial interests to disclose.

Author Contributions

Asall Kim, Eun Joo Yang, and Chunghwi Yi contributed to the study conception and design. Material preparation, data collection and analysis were performed by Asall Kim, Myungki Ji, Jaewon Boem, Woochol Joseph Choi and Chunghwi Yi. The first draft of the manuscript was written by Asall Kim, and all authors commented on the subsequent manuscript versions. All authors read and approved the final manuscript.

Ethics Approval

This study was performed in line with the principles of the Declaration of Helsinki. Approval was granted by the Ethics Committee of Seoul National University Bundang Hospital (07/29/2021, IRB no. B-2108/702-309).

Consent to Participate

Informed consent was obtained from all individual participants included in the study.

Consent to Publish

There is no content that required consent to publish.

Acknowledgements

The devotion that all participants provided to us is unforgettable. We would also like to thank Editage for English language editing.

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Tables

Table 1. Participant age, cancer stage, and treatment information

Table 2. Results and mean differences of the follow-up

Table 3. The significant predictors for the quick DASH improvement

Table 4. Linear regression models using individual variable