The long-term effects of posttreatment exercise on pain in young women with breast cancer
Background Persistent pain after treatment has been identified in breast cancer populations, with prevalence rates ranging from 25%-60%. Age, surgical procedure, axillary node dissection, and radiation therapy have shown correlation with chronic pain development.
Objective To conduct a pilot randomized controlled trial targeting young breast cancer patients to determine the effectiveness of a 12-week exercise program on long-term levels of upper-limb pain, as measured by the Brief Pain Inventory-Short Form (BPI-SF), and pain measured by physical examination of specific shoulder movements.
Methods Young adults (18-45 years of age) recently diagnosed with breast cancer consenting to participate in this study were randomly allocated to intervention or control groups. The exercise intervention group participated in a 12-week exercise program starting 3-4 weeks after the cessation of radiation therapy, and the control group received standard care consisting of encouragement for an active lifestyle and pamphlets on the benefits of exercise. The location and severity of pain and its interference with daily life were recorded at the following 6 time points: postsurgery and preradiation (T1, baseline), postradiation and preintervention (T2), and 4 points during an 18-month period postradiation (T3-T6 at 3, 6, 12, and 18 months). In addition, clinical physical assessment of range of motion and pain on active shoulder movements were recorded at each time point.
Results 59 young breast cancer patients participated in the study (exercise group: n = 29; control group: n = 30). Over the course of the trial, there were no significant differences between study groups in the BPI-SF measures of pain interference and severity scores. Improvements in pain on shoulder movements were noted in the intervention group at 3 and 6 months postintervention (T3 and T4) but were not sustained over time (by T6, 18 months postradiation). Shoulder girdle-chest wall pain improved at 12 and 18 months postradiation in both groups but persisted despite exercise intervention. Recordings of shoulder pain on physical examination of range showed a distinct pattern of temporal improvement (T3-T5), followed by low levels of pain recurrence at 18 months postradiation (T6) in both groups.
Limitations Stringent exclusion criteria, including the absence of any shoulder pathology or pre-existent medical comorbidities impacting upper limb function, long-term follow-up, and the relatively small population of breast cancer patients in this age demographic, limited and prolonged recruitment for this study. In addition, the general activity levels of the young breast cancer survivors who agreed to participate in this exercise intervention study may have had an impact on the significance of results.
Conclusion Transient improvements in shoulder pain can be attributed to a 12-week exercise program, but they did not translate to long-term benefits. Moreover, the BPI-SF did not capture shoulder pain and limitations related to upper-limb disability in this study, in contrast with the findings on physical examination.
Funding This study was funded by Hope & Cope, a grant from the CURE Foundation, and grants from the Jewish General Hospital's Weekend to End Breast Cancer.
Accepted for publication May 15, 2018
Correspondence Mary-Ann Dalzell, MScxPT; madalzell5@gmail.com
Disclosures Thierry Muanza holds an intellectual property patent (United States Provisional Patent Application No. 62/359,918; Title: Adipose Mesenchymal Stromal Cells for Treating Radiation-Induced Oral Mucositis). Mary-Ann Dalzell, Richard Dalfen, Beatrice Fournier, Marize Ibrahim, Petr Kavan, Michael Palumbo, Warren Sateren, and Nadia Smirnow report no disclosures or conflicts of interest.
Citation JCSO 2018;16(3):e145-e151
©2018 Frontline Medical Communications
doi https://doi.org/10.12788/jcso.0395
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Clinical characteristics. We used standardized questions and chart review to document the participants’ clinical characteristics and to capture information on the following: the stage and subtype of breast cancer, hormonal and human epidermal growth factor receptors (HER2) (estrogen receptor, progesterone receptor, and HER2 status), extent of surgery (lumpectomy or total mastectomy), and other modalities of treatment (eg, chemotherapy, radiation therapy).
Pain assessment. The BPI-SF was used to assess participants’ cancer-related pain. Pain severity ranged from 0 (no pain), 1 to 4 (mild pain), 5 to 6 (moderate pain), to 7 to 10 (severe pain).18,19 The questionnaire also identifies the pain interference in daily activities using a Likert scale ranging from 0 (Does not interfere) to 10 (Completely interferes) in the following 7 domains or subscales: General Activity, Walking, Mood, Sleep, Work, Relations with Others, and Enjoyment of Life.16 For the purpose of this study, mean scores were tabulated using both pain intensity and interference scales.
Another important component of the BPI-SF instructs participants to localize pain by means of a body diagram. For purpose of analysis, 3 pain regions were established: shoulder girdle/chest wall on the affected side; neck and other upper extremity, including hand(s), forearm(s), wrist(s), and finger(s); and other regions, including abdominal discomfort, leg(s), hip(s), knee(s), ankle(s), lower back, and feet. In addition, pain levels on movement (Yes/No) were recorded for isolated shoulder flexion, abduction, and horizontal abduction (sitting and standing). The measurements were completed by a single physical therapist throughout the course of the study to minimize variance.
Procedure
The study protocol was approved by the Research Ethics Board at the Jewish General Hospital. Recruitment occurred from 2011 through 2015. The research was in accordance with the ethical standards of the responsible committee on human experimentation. Eligible women were recruited by the research coordinator who described the purpose, risks, and benefits of the study; advised on confidentiality, data collection, and intervention allocation procedures; and highlighted voluntary participation. The research coordinator addressed any concerns on the part of the participants before obtaining their written informed consent. Random allocation to the intervention and control groups was established using a web-based randomization plan generator (www.randomization.com). A single individual was responsible for the randomization process, and treatment assignments were revealed after each participant’s name had been entered. A physical therapist performed 6 sequential evaluations (T1-T6) at the time of participants’ medical follow-up appointments.
Intervention
The 12-week exercise intervention started 3 weeks postradiation and was composed of an initial 6-week program of low-level cardiovascular and resistance exercises that progressed to a set of more advanced exercises for the remaining 6 weeks. Participants were instructed to warm up for at least 10 minutes with a cardiovascular exercise of their choice (eg, a recumbent cross trainer, walking, or stairs) before doing a combined strength, endurance, and stretching exercise program for the upper body.20 The final portion of the exercise intervention included a period of light cool-down. Weight training resistance levels were based on a maximum 8 to 10 repetitions for strength and a maximum of 20 repetitions for endurance training exercises, which progressed gradually over the course of the 12-week exercise program to ensure participant safety.21,22 Participants in the intervention group were supervised at least once a week by an exercise physiologist at a center for oncology patients (Hope & Cope Wellness Centre), and patients were encouraged to perform the program at home 2 to 3 times a week. Those who were not able to exercise consistently at the center were provided with equipment and instructed on how to do the program safely at home.
By comparison, the control group received standard care, which included advice on the benefits of an active lifestyle, including exercise, but without a specific intervention. Participants were not restricted in their physical activity and/or sport participation levels, and their weekly activity levels were calculated using the Metabolic Equivalent of Task and recorded at each of the 6 time points.
Statistical analysis
Descriptive statistics were used to examine participant characteristics. The quantitative data collected through the BPI-SF measures were analyzed with JMP software (version 11.2; SAS Institute, Cary, NC). Continuous variables were tested for statistical significance (P ≤ .05) through the chi-square (categorical), analysis of variance, and nonparametric Wilcoxon tests. The analyses did not include missing data.
Results
A total of 59 young women were randomized into the intervention (n = 29) and control (n = 30) groups. Of those, 2 participants dropped out of the study because of family and time constraints, and 3 participants died, 2 from the control and 1 from the intervention group, after subsequently developing metastatic disease. Baseline data including comparative tumor characteristics, surgical interventions, and treatment interventions have been published in relation to other elements of this study.23,24 The participants had a mean age of 39.2 years (standard deviation [SD], 5.0). More than half of them had an invasive ductal carcinoma (69.5%) and were estrogen positive (78.0%), progesterone positive (74.6%), or HER2 positive (20.3%), whereas 10.2% were triple negative. Most of the participants had undergone breast-sparing procedures (86.4% lumpectomy), and 18.6% had a total mastectomy. By random chance, the intervention group had higher rates of total mastectomy (24.4% and 13.3%, respectively) and surgical reconstruction (12.2% and 6.7%, respectively) compared with the control group. Most of the women (71.2%) received chemotherapy, and all received radiation therapy. In the intervention group, 37.2% received radiation therapy localized to the axilla, and 88% received a boost of radiation to the surgical bed. Self-reported exercise diaries were returned by 15 of the 29 intervention participants, and training frequencies among them varied significantly (1-6 times a week).
