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Protocol
Comparison of the effects of different functional exercise sequences on lymphedema in breast cancer: protocol for an exploratory randomised controlled cross-over trial
  1. Lin Qiu1,
  2. Jing Wu2,
  3. Yingying Huang3,
  4. Maodie Ye3,
  5. Lifang Song1,
  6. Haihong Huang1,
  7. Yongmei Jin4
  1. 1Department of Thyroid and Breast Surgery, Shanghai Seventh People's Hospital, Shanghai, Shanghai, China
  2. 2School of Nursing, Shanghai University of Traditional Chinese Medicine, Shanghai, Shanghai, China
  3. 3Department of Nursing, Seventh People's Hospital, Shanghai University of Traditional Chinese Medicine, Shanghai, Shanghai, China
  4. 4Department of Nursing, Shanghai Seventh People's Hospital, Shanghai, Shanghai, China
  1. Correspondence to Professor Yongmei Jin; 13795272016{at}163.com

Abstract

Introduction Breast cancer-related lymphedema (BCRL) is a common postoperative complication of breast cancer. It develops in a chronic and vicious cycle. Once lymphedema occurs, it cannot be cured and bring serious physiological, psychological, social and economic burden to patients. Upper limb functional exercises are an effective and convenient intervention for managing lymphedema. However, the optimal exercise sequence remains unclear. Therefore, we aim to compare the effects of exercise sequences under the guidance of commonly used exercise sequences and lymphatic flow theory.

Methods An exploratory randomised controlled cross-over trial will be conducted. 32 patients with BCRL are randomly allocated into two groups (group A and group B). Group A patients will perform functional exercise from wrist joint to shoulder joint, and the exercise direction of group B is opposite to that of group A, that is, from shoulder joint to wrist joint end. Exercise time is once a day, each 20–30 min, for 2 weeks. After 2 weeks of washout period, A and B groups of exchange exercise sequences (exercise frequency and duration unchanged). The primary outcome is upper limb circumference, and secondary outcomes are upper limb function and lymphedema symptoms.

Ethics and dissemination This study protocol is presented in accordance with the Standard Protocol Items: Recommendations for Interventional Trials guidelines. All participants will sign a written informed consent. The research ethics regional committee of Shanghai Seventh People’s Hospital has approved the study. Regardless of the outcome of this study, the results will be published in open-access journals to ensure public access.

Trial registration number ChiCTR2200066463.

  • Breast tumours
  • REHABILITATION MEDICINE
  • SPORTS MEDICINE
http://creativecommons.org/licenses/by-nc/4.0/

This is an open access article distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited, appropriate credit is given, any changes made indicated, and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/.

https://doi.org/10.1136/bmjopen-2023-076127

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Strengths and limitations of this study

  • This will be the first trial aiming to compare the effects of different sequences of functional exercises on patients with lymphedema.

  • To explore the effect of functional exercise in the home maintenance period of complex decongestive therapy and provide evidence-based basis for clinical practice.

  • Although there is a lack of objective indicators, we use the circumference measurement method to reflect the swelling changes of patients with lymphedema and evaluate the changes in patients’ functions and symptoms with related scales.

Background

Breast cancer-related lymphedema (BCRL) is the most common chronic, long-term and vicious circle complication after breast cancer surgery.1 Disorders in lymphatic circulation, which can be caused by breast cancer surgery, radiotherapy or tumour metastasis, may lead to obstruction or disruption of lymph reflux, resulting in abnormal accumulation of protein-rich interstitial fluid in a generalised or regional manner. Lymphedema mainly occurs within 3–5 years after breast cancer surgery and is estimated to affect between 20.3% and 30.2% of breast cancer survivors.2–4 With the increase of patients with breast cancer, the incidence of BCRL may further increase.5 6

BCRL can affect the individual, caregivers and society of patients in physiological, psychological and financial aspects. Physiologically, patients with lymphedema reported different symptoms, including heaviness, impaired shoulder mobility, seroma formation and breast swelling.7 8 Patients with BCRL were twice as likely to have lymphangitis or cellulitis,9 affecting limb activity and reducing daily function.10 Psychologically, nearly half (48.9%) of the patients with BCRL experienced moderate-to-severe psychological distress.11 The sexual function of patients with breast cancer is affected as they continue to face negative emotions such as inferiority and helplessness caused by unpleasant experiences.12 13 Financially, the costs associated with surgery, cancer drugs and various treatment modalities contribute to the financial burden experienced by patients with lymphedema, and lymphedema requires long-term treatment. In patients with breast cancer, the financial burden of patients with lymphedema within 10 years is estimated to be twice as high as that without lymphedema.9 14

The treatment of BCRL included surgical treatment, non-surgical treatment and related molecular therapy.15 However, once BCRL occurs, it cannot be cured, mainly to control the process of lymphedema and relieve symptoms. The effect is not lasting and requires long-term intervention.16 Complex decongestive therapy (CDT) is a recognised intervention for lymphedema. Standard CDT includes manual lymphatic drainage, pressure therapy, functional exercise and skin care.17 There is high-quality evidence reported in Rangon et al17 that CDT is more conducive to alleviating the total volume and pain of lymphedema on multimodal approaches. Functional exercise is a convenient, effective and economical intervention for patients. At present, few studies have explored the content of functional exercise in lymphedema. In terms of exercise, the main research is to study the effect of progressive resistance exercise or aerobic exercise on patients with BCRL. At the same time, Buchan et al18 have found that resistance training has the effect of preventing lymphedema and reducing upper arm volume, and functional exercises are simple and safe freehand resistance exercises that use their own weight to contract muscles. More evidence is still needed to support the effect of functional exercise on lymphedema.

There is no standard guideline for functional exercise in sequences. In general, the sequences of functional exercise for patients are from the distal to the proximal, including from the wrist, elbow to shoulder; according to the lymphatic drainage and related theory, should first activate lymph node function, exercise can be from the proximal to the distal, including from the shoulder joint, elbow to wrist.19 However, to our best knowledge, there is no relevant research and clear evidence to indicate the order of exercise in patients with BCRL. Therefore, this study aims to explore the effects of different functional exercise sequences on lymphedema through randomised controlled clinical cross-over trials to provide a basis and reference for clinical practice.

Hypothesis

We hypothesise that the proximal-to-distal movement of the upper limb function exercises can promote the return of lymphatic fluid. Thus, we expect that the intervention group, which exercised in order from shoulder to elbow to wrist, had better lymphedema maintenance or better oedema remission, that is, a smaller difference in circumference.

Methods

This study protocol is presented in accordance with the Standard Protocol Items: Recommendations for Interventional Trials guidelines. The trial was registered with ClinicalTrials.gov (ChiCTR2200066463).

Study design

This study is a randomised controlled exploratory clinical cross-over trial. 32 patients with postoperative lymphedema after breast cancer will be recruited and randomly assigned into two groups (group A and group B) to compare the effects of different modes of hand-functional exercise (figure 1). 16 patients in group A perform functional exercises from wrist joint to shoulder joint under the guidance of a specialist nurse, and the exercise direction of group B is opposite to that of group A, that is, from shoulder joint to wrist joint end. The duration of exercise is 20–30 min once a day for 2 weeks. The frequency and duration of the exercise remain unchanged, and the results of the evaluation indexes are statistically analysed. It began on 1 September 2022 and will end on 1 September 2024.

Figure 1
Figure 1

Study outline. Included patients are randomised to intervention for 14 days, followed by 2-week washout and crossover to 14 days intervention.

Participants

The diagnostic criteria are as follows: (1) breast cancer diagnostic criteria: breast cancer is diagnosed according to clinical pathology and (2) diagnostic criteria for BCRL: with reference to the 2021 edition of the Chinese Anti-Cancer Association Guidelines for the diagnosis and treatment of breast cancer and norms on breast cancer upper limb lymphedema moderate-to-severe clinical grading standards, mild: the circumference of the affected upper limb was less than 3 cm longer than that of the contralateral upper limb; moderate: comparing the most obvious parts of the circumference of the upper limbs, the affected limbs increased by about 3–5 cm compared with the healthy limbs; and severe: comparing the most obvious circumference of both upper limbs, the affected limb increased by >5 cm compared with the healthy limb.

Inclusion criteria include: (1) patients with unilateral BCRL who meet the diagnostic criteria for lymphedema, mild and above; (2) patients aged 35–65 years; (3) patients with breast cancer diagnosed by pathology after surgical treatment; and (4) Karnofsky Score no less than 60 points, the estimated survival time of more than 6 months.

Exclusion criteria include: (1) patients are undergoing chemotherapy, radiotherapy or a full course of chemotherapy, less than 3 months after radiotherapy; (2) pregnant and lactating women; (3) patients with tumour metastasis and lymph node metastasis after re-examination; (4) patients with severe primary diseases in the heart, liver, kidney or hematopoietic system or mental disorders; (5) patients with the limb local skin rash, papules, erythema, herpes, trauma, ulcers and infection; and (6) patients with upper limb vascular diseases such as arteriovenous thrombosis and arteriovenous sclerosis.

If the patient has the following conditions during the intervention, it is considered as sample shedding: (1) serious adverse events during treatment; (2) deterioration or serious complications (any disease or accident) during treatment; (3) receiving other BCRL-related treatments during the treatment (including the washout period); (4) who have poor compliance, in addition to the elution period of continuous treatment interval greater than 2 weeks; (5) who voluntarily withdraw from the trial; and (6) who did not withdraw from the trial but did not receive treatment for more than two consecutive times or more than four times.

Sample size

The required calculation of the sample size is performed by using PASS V.21. Based on the standard calculation formula, randomised cross-over test was used, choose ‘tests for the difference between two means in a 2×2 cross-over design’. The upper limb circumference was used as the main outcome evaluation index. The bilateral α=0.05, β=0.10, μα=1.282 and μβ=1.960 were taken. The sample size was calculated to be 24 participants based on previous relevant studies,20 with an increase of loss of follow-up rate of about 20%. The sample size was 32 cases, with 16 cases in each group.

Concealed randomisation

Prior to the study, non-intervention researchers conducted randomised grouping. 32 random numbers are randomly generated by SPSS V.25.0 and concealed in opaque envelopes. According to the enrolment time, 32 participants are randomly assigned to groups A and B, 16 cases each. At the same time, the researchers only know the patient’s enrolment on the day of enrolment. Due to the nature of the intervention, neither participants nor staff can be blinded to allocation.

Exercise intervention

The enrolled patients in two groups received face-to-face functional exercise instruction, and inform the main points and precautions, while lymphedema-related health education, the rest of the daily regular open line with the practice mode, and conduct video guidance every 3 or 4 days to correct the wrong movements. When you open another set of workouts after the end of 2 weeks, also instruct functional workouts offline for the first day.

Group A carries out its exercises in three parts, the first part is to dredge lymph nodes, respectively, by massaging supraclavicular, axillary and inguinal lymph nodes for 30 s. The second part is the abdominal breathing training, deep breathing exercises are performed before exercise. The hands are placed in the abdomen to feel the breathing changes. When the nose inhales, hands on the belly are raised; exhale with pursed lips, and hands on the belly should move down to its original position. the abdominal breathing training for 15 times. In the third part of the limb function exercise (details in online supplemental figure S1), each step is repeated 10–15 times, including (1) grasping activity: both upper limbs are raised simultaneously, with both hands forming fists and then relaxing the grip; (2) flexion/extension motion of wrist joint: both upper limbs are raised with palms facing forward and then moved backward; (3) forearm rotation: included forearm supination and forearm pronation, placing hands, shoulder-width apart, slowly rotating hands to a palms-up position, and then back to their original palms-down position; (4) flexion/extension motion of elbow joint: both upper limbs are raised, decreasing the angle between the forearm and the arm at the elbow joint during flexion and increasing the angle during extension; (5) shoulder rotation: place hands on the shoulders, palms facing downwards (or hands naturally down), and rotate them forward and backward in circular motions; (6) chest expansion: place arms in front of your chest. Close the hands into fists with thumbs on the inside. Inhale while taking the arms sideways and back as far as possible, keeping the elbows at shoulder level. Exhale while bringing the arms towards each other, maintaining muscular tension; (7) flexion motion of shoulder joint: slowly move the upper limbs forward and upwards along the coronal axis in the sagittal plane; and (8) abduction motion of shoulder joint: along the coronal axis in the sagittal plane, move the upper extremity away from the body.

Group B also carries out its exercises in three parts: dredging, abdominal breathing training and limb function exercise. Different from group A, the exercise sequences of limb function exercise is as follows (details in online supplemental figure S2): (1) shoulder rotation; (2) chest expansion; (3) flexion motion of shoulder joint; (4) abduction motion of shoulder joint; (5) flexion/extension motion of elbow joint; (6) forearm rotation; (7) flexion/extension motion of wrist joint; and (8) grasping activity.

Variables

Baseline observation indicators

Demographic characteristics include age, height and weight; related medical history: oedema-related medical history (oedema limb and time), surgery-related medical history (surgical method, time, number of lymph node dissection) and tumour-related medical history (tumour location, radiotherapy, chemotherapy, endocrine therapy); measurement of lymphedema-related symptoms (limb arm circumference, lymphedema symptom), and upper limb function.

Primary outcome

The primary outcome is circumference difference. It will be measured by the non-elastic soft ruler, measurement site selection included 6 (figure 2): (1) part of the hand between the thumb and the index finger; (2) upper limb wrist stripes; (3) wrist stripes on 10 cm; (4) elbow (elbow stripes); (5) 10 cm above the elbow stripe; and (6) underarm vertex; measurement of each point arm circumference measured two times, take the average. At present, there is no uniform standard for measuring the position of the arm circumference of the upper limb. Li et al21 and Wei et al22 used the middle of the palm, elbow, wrist and every 4 cm from the wrist to the axilla. Byun et al23 measured four positions of the metacarpal, wrist and 10 cm below and above the lateral epicondyle. We conducted the assessment using the ‘Prevention and care of lymphedema after breast cancer surgery’ published by the Chinese Nursing Association in 2021.24 The most consistent diagnostic criterion is that patients are classified as having lymphedema if the affected arm circumference is ≥2 cm.

Figure 2
Figure 2

Measuring point of circumference measurement. The figure was created by the authors of this paper.

Secondary outcomes for the proposed study will include the Chinese vision of disabilities of the arm, shoulder and hand (DASH) and Breast Cancer and Lymphedema Symptom Experience Index (BCLE-SEI). The DASH was developed by Beaton et al25 in 2001 and can be used to assess upper extremity dysfunction due to any disease. It consists of two parts to evaluate the ability to perform activities of daily living and upper extremity discomfort conditions and the degree of interference, with 30 entries, each scored according to a 5-point scale. The final score of the scale is equal to (total score-30)/1.2, the scores range from 0 to 100, with lower scores indicating better functioning. Lee et al26 sinicised the scale with intragroup correlation coefficient (ICC) and Cronbach’s α coefficients of 0.77 and 0.94, respectively, indicating good reliability and validity. Beaton et al27 simplified the scale. The content validity values of the Chinese version of the DASH (short form) for all items are 0.8 to 1. The Cronbach’s α coefficient for the whole scale is 0.911 and the ICC for the scale was 0.882, indicating that the validity and reliability of the short-form scale were good and the set items are suitable to evaluate the degree of upper limb dysfunction in patients with breast cancer.

BCLE-SEI was developed by Fu et al at the New York University School of Nursing and presented at the International Symposium on Supportive Care in Cancer in 2012 to measure symptoms of BCRL and their resulting distress.8 It has two parts: symptom appearance and symptom distress. The first part consists of 24 entries, including arm swelling, breast swelling, chest wall swelling, heaviness, stiffness and numbness. The second part consists of 32 entries, assessing symptom distress through six dimensions: functional, emotional, psychological, self-perception, sexual and sleep,8 28 with a Cronbach’s α coefficient of 0.92, indicating good internal consistency, and the correlation coefficients among the symptom distress dimensions ranged from 0.35 to 0.93.8 28 Shi et al28 sinicised their total questionnaire with a Cronbach’s α coefficient of 0.967, and the Cronbach’s α coefficients of parts I and II are 0.930 and 0.960, respectively, indicating good internal consistency; the reliability of retesting at a 1 week interval is 0.705. Content validity and structural validity showed that the Chinese version of the BCLE-SEI could reflect the symptoms and distress of BCRL in patients. An overview of the collected variables at each time point is given in table 1.

View this table:
Table 1

Procedures per time points, overview of study visits and items to be recorded

Adverse event

Observe for adverse events or serious adverse events and record the patient’s discomfort after exercise, such as muscle pain discomfort or others. If there is an adverse event, the cause of the disease needs to be addressed immediately and suspend the trial, follow-up continuously and evaluate whether to continue the trial by a rehabilitation therapist outside the study.

Patient and public involvement

Patients did not participate in the design of this study, and at the intervention stage in the research process are patients first involved in the research. We routinely carry out upper limb functional exercise training for patients with BCRL and follow up on self-management of functional exercise every month. Participants will get personal test results immediately after each assessment.

Statistical analysis

The original observation record data of each subject are entered into the case report form, and EpiData V.3.1 is used for data management. The method of double entry and mutual proofreading is used to ensure the accuracy of the entry. Handling missing data, including deletion method and single imputation method. All the results of this study are statistically analysed by SPSS, V.25.0, software, and the measurement data are described by mean±SD. For the statistical analysis of measurement data, if the data conform to the normal distribution and homogeneity of variance, the t-test is used, and if not, Wilcoxon’s paired signed rank test will be used. χ2 test or exact probability method is used for the statistical analysis of count data. First, testing the baseline 'residual effect' and 'sequential effect' of the data, if there is a ‘residual effect’ then discard the second phase of data, the first phase of the independent sample t-test or rank sum test.29 30 If there is no ‘residual effect’, then continue to test the ‘sequential effect’. If there is no difference in the test results, it indicates that the research programme is set up reasonably. If the results are different, the opposite number is used to correct the ‘sequential effect’ and then statistical analysis is carried out.

Discussion

Functional exercise is an essential component of CDT and has been shown to effectively alleviate lymphedema and related symptoms. For patients with breast cancer, functional exercise plays a vital role in rehabilitation after surgery. Early progressive functional exercise is necessary to improve blood and lymphatic circulation in the affected limb, reduce subcutaneous effusion, prevent lymphedema and restore upper limb function. For patients with lymphedema, there is a lymphatic circulation disorder, and the lymphatic drainage volume of the muscle is significantly higher than that of the subcutaneous tissue, which is the main source and drainage pathway of upper limb lymph.31 32 Exercise stimulates lymphatic contraction through alternating muscle contractions, thereby increasing venous and lymphatic drainage. Joint flexion and extension activities act as a ‘joint pump’ mechanism, which stimulates lymph nodes, enhances lymph node function and promotes lymphatic movement.33 The relationship between limb function and lymphedema is a positive cycle, where movement accelerates lymphatic transport through the double pump mechanism and facilitates lymphatic return. Fu et al19 34 35 developed the ‘Optimal Lymph Flow’ exercise program based on the theory of lymphatic flow. This program includes muscle-tightening deep breathing, muscle-tightening pumping, shoulder exercises and large muscle exercises. Studies have demonstrated that lymphatic drainage exercises can safely and effectively promote reduction of swelling in patients.

CDT is widely regarded as the most effective treatment for lymphedema. The main purpose of CDT is to promote the return of lymph, including the detumescence stage and maintenance stage. The detumescence stage is usually 5 times a week, a total of 20 times as a course of treatment; the maintenance stage focuses on home self-management. Considering that this study is a cross-controlled trial, to reduce the shedding of samples and maintain the comparability of sample baselines, we selected patients with lymphedema treated in the maintenance phase.34 Additionally, to ensure patient compliance and the quality of functional exercise during home intervention, it is important to implement measures that can effectively monitor and support patients. The study of Bluethmann et al,36 Abdin et al37 and Dorri et al38 showed that measures such as web-based mobile tools, face-to-face interviews and group interventions can effectively improve the exercise level of patients with breast cancer. Therefore, in this study, we plan to adopt face-to-face functional exercise intervention, distribution of educational materials and videos and group follow-up mode to effectively monitor exercise compliance and ensure exercise quality.

Currently, there is no standardised method for diagnosing lymphedema. The measurement methods include measurement tools and scales. Objective tools mainly include bioimpedance analysis (BIA), tissue dielectric constant (TDC) and lymphoscintigraphy.1 39 40 Currently, there is no standardised method for diagnosing lymphedema. The L-Dex Score, which is obtained through BIA, can be used to diagnose the occurrence of lymphedema if it is higher than the preoperative baseline measurement value of 10 or 7.1 in the absence of preoperative evaluation.39 However, BIA may not be able to capture tissue changes caused by fibrosis or fat infiltration in the later stages of lymphedema.41 Different from the overall detection of BIA, TDC can be used for the analysis of local tissue water composition. The dielectric constant obtained by measuring the local water content of the tissue is used to reflect the lymphedema. Koehler and Mayrovitz42 found that the TDC ratio of women with trunk lymphedema was higher than 1.2 as early as 2 weeks and remained high at 78 weeks through a prospective follow-up observation of 78 weeks. Study has shown that TDC measurement helps to detect changes in early lymphedema. In our study, we used circumference measurement to evaluate oedema in patients. Circumference measurement is a direct and commonly used method for diagnosing upper limb lymphedema after mastectomy. Hidding et al43 have shown that the circumference measurement method is highly consistent with the water volume method and perometry and has good reliability and effectiveness. Additionally, studies have shown that arm circumference measurement can better reflect patients’ self-reported outcomes than biological impedance.44 In future studies, it is important to apply convenient and effective objective tools to evaluate upper limb conditions after breast cancer surgery, in order to effectively monitor tissue changes and the occurrence of lymphedema.

Overall, the results of this study can increase the evidence of functional exercise intervention for lymphedema. In this randomised exploratory cross-over trial, the effects of different exercise sequences on lymphedema are explored to provide evidence-based exercise guidance for patients with lymphedema. For patients, evidence-based functional exercise promotes effective control of lymphedema; for healthcare workers, clarifying the effect of functional exercise can improve the attention and persuasion of healthcare workers on functional exercise education.

Ethics and dissemination

Participation in this study will be voluntary and informed consent was provided by the participants (online supplemental appendix 1). This study complies with the Declaration of Helsinki and has been reviewed and approved by the research ethics regional committee of Shanghai Seventh People’s Hospital (2022-7th-HIRB-055). All participants received oral and written information and signed written informed consent prior to inclusion. Because the study is a cross-over trial, each group of patients received the same intervention while mastering upper limb exercise techniques, and participants will know the results of their individual tests. The results of this study will be published in relevant journals to disseminate the research results.

Ethics statements

Patient consent for publication

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Supplementary materials

  • Supplementary Data

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Footnotes

  • Contributors LQ and JW were involved in study concept and design. The manuscript was drafted by LQ, MY and HH and was revised critically for important intellectual content by JW and YJ. HH, LS and YJ provided the study with analysis tools. All authors contributed with writing, revising and approving this manuscript.

  • Funding The study was funded by Hospital Management Research Fund of Shanghai Hospital Association (grant no. X2022058), Pudong New Area Health System Discipline Construction Project (grant no. PWZxk2022-06), Pudong New Area Health Committee Youth Science and Technology Project (grant no. PW2021B-04) and Pudong New Area Health Committee (grant no. PW2023A-15). This funding source had no effect in the design of this study and will not have any role during its execution, analyses, interpretation of the data, or decision to submit results.

  • Competing interests None declared.

  • Patient and public involvement Patients and/or the public were involved in the design, or conduct, or reporting, or dissemination plans of this research. Refer to the Methods section for further details.

  • Provenance and peer review Not commissioned; externally peer reviewed.

  • Supplemental material This content has been supplied by the author(s). It has not been vetted by BMJ Publishing Group Limited (BMJ) and may not have been peer-reviewed. Any opinions or recommendations discussed are solely those of the author(s) and are not endorsed by BMJ. BMJ disclaims all liability and responsibility arising from any reliance placed on the content. Where the content includes any translated material, BMJ does not warrant the accuracy and reliability of the translations (including but not limited to local regulations, clinical guidelines, terminology, drug names and drug dosages), and is not responsible for any error and/or omissions arising from translation and adaptation or otherwise.