Journal of Exercise Medicine online

April 2018Volume 3 Number 2

Published by the American Society of Exercise

Physiologists

ISSN 2378-4083

JEMonline

Effects of a Translational Community-Based Multimodal Exercise Program on Sleep Quality in Breast Cancer Survivors: A Pilot Study

Michael P. Foley1, Scott M. Hasson2, Bryan M. Gee1

1Idaho State University, Department of Physical and Occupational Therapy, Pocatello, Idaho, USA, 2Augusta University, Department of Physical Therapy, Augusta, Georgia, USA

ABSTRACT

Foley MP, Hasson SM, Gee BM. Effects of a Translational Community-Based Multimodal Exercise Program on Sleep Quality in Breast Cancer Survivors: A Pilot Study. JEMonline 2018;3(2):1-14. The purpose of this single-arm pilot study was to examine the translational effects of a 12-wk community-based multimodal exercise program on sleep quality in breast cancer survivors (BCS). Thirty-nine female BCS participated in a twice weekly supervised 90-min multimodal exercise session (aerobic conditioning, resistance strengthening, and balance and flexibility training). The primary outcome measure for this study was global sleep quality from the Pittsburg Sleep Quality Index (PSQI). Pre- and post-exercise program global sleep quality and domains of PSQI were statistically analyzed for differences (P<0.05). The main results of this study were significant (P<0.05) improvements in post-exercise program global sleep quality (23%, effect size (ES) = 0.42), as well as significant improvements in: (a) sleep disturbance (12%, ES = 0.42); (b) sleep dysfunction (31%, ES = 0.41); and (c) sleep quality (37%, ES = 0.52). We found that the BCS were “poor sleepers” at baseline. After completing 12 wks of the community-based multimodal exercise, the BCS sleep quality was significantly improved, though they were still classified as “poor sleepers”. However, moderate effect size improvements in sleep quality were found. This study provides evidence that supports exercise physiology applications for front-line community-based exercise programming for cancer survivors.

Key Words: Breast Cancer Survivors, Exercise, Sleep Quality

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INTRODUCTION

Advances in science and medicine have resulted in earlier detection and improved treatment of breast cancer, which has greatly improved survival rates. According to the National Cancer Institute: Surveillance, Epidemiology, and End Results, the 5-yr survival rate for breast cancer is 89.4% (31). Consequently, cancer today is often considered a chronic disease. And yet, of all the chronic diseases, cancer and its treatment are viewed as the most distressing (16).

Cancer-related distress can adversely affect sleep quality, physical function, quality of life (QoL), and ultimately survival (36). In particular, the oncologic treatment can have significant negative effects on sleep quality (1). Research indicates that 30 to 90% of all patients with cancer report difficulties with sleeping, which is double or triple what is found in the general population (17,29). Decreased sleep quality in patients with cancer may be linked to diminished quality of life (3), high levels of fatigue (4,6,17), pain (4,17), and anxiety (4,17,37). Often, patients with cancer report a decrease in quality of life as a result of cancer-related fatigue that is believed to be associated with poor sleep quality (14,20,24).

Cancer survivors frequently experience sleep disorders (impaired sleep) as either an isolated complaint or part of cancer and oncologic treatment symptomology (13,22). Poor sleep quality has been linked to symptoms of pain intolerance, depression, decreased desire to participate in social activities, and increased susceptibility to infection (4,17). Unfortunately, cancer-related sleep impairments are often not addressed in cancer survivorship (19). Research also has shown that impairments in sleep quality in patients with cancer have been found prior to adjuvant chemotherapy (3,5) and persist during (33) and after treatment (25), which contribute to morbidity and mortality (36).

Furthermore, research shows a significant positive relationship between physical activity and sleep quality in individuals with cancer (12,18,27). Increased physical activity is positively correlated with improved quality of life, increased energy, and improved sleep quality (18). Physical activity and exercise are recommended for reducing fatigue and promoting better sleep. Yet, despite the level one evidence that supports the extensive benefits of exercise training for cancer survivors, most cancer survivors experience a decrease in physical activity. Moreover, they do not regain their pre-cancer physical activity levels, and they are no more likely to follow the physical activity guidelines than the general population (34,39).

Unfortunately, research translation from clinical trials to front-line community-based exercise programming has been limited in regards to sleep quality. There is an abundant need for establishing translational community-based exercise programming for cancer survivors so they can realize the many benefits of regular exercise (35). Hence, given the anticipated benefits, the purpose of this single-arm study was to examine the translational effects of a 12-wk community-based multimodal exercise program on global sleep quality, sleep duration, sleep disturbance, sleep latency, sleep daytime dysfunction, sleep efficiency, and sleep medication used in BCS.

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METHODS

Study DesignSleep quality was assessed pre- and post-participation in a 12-wk translational community-based multimodal exercise program for BCS.

Participant PopulationThis study was approved by (Augusta University) institutional review board and was administered by means of a community partnership (Savannah River Area LIVESTRONG at Y). Breast cancer survivors were besought by the researchers for voluntary participation in this study. The inclusion criteria for this study were: (a) consenting adult BCS; (b) signed physician approval for participation; and (c) BCS regardless of the treatment/recovery phase. Minors (<18 yrs of age) were excluded from participation in this study. Written informed consent was obtained from all the subjects, and all who participated were enrolled over a 17-month period. All BCS were female.

Description of the Multimodal Exercise ProgramThe translational cancer survivor community-based multimodal exercise program was a free voluntary program that met twice weekly for 90-min exercise classes for 12 wks. The subjects were also encouraged to exercise for at least one additional day each week. Each exercise class was divided into three 30-min components: (a) aerobic conditioning; (b) resistance exercise training (RET); and (c) balance and flexibility training. A maximum of 10 subjects participated in each exercise session in which two LIVESTRONG Foundation™ certified instructors, who were also trained YMCA fitness instructors, supervised the duration of each session. A licensed physical therapist, who was also a certified lymphedema therapist with several years of oncology rehabilitation experience, assisted in the program development, implementation, and assessment. Sleep quality was assessed by the researchers prior to beginning the exercise training program and post-exercise program completion.

Baseline characteristics and physical function measures were taken prior to beginning the exercise program to assist in the development of the individualized exercise programs. The American College of Sports Medicine (ACSM) exercise guidelines and position statements were used in the development of the individualized exercise prescriptions for each of the subjects (10,15,23,38). Initially, for 1 to 2 wks, the subjects completed aerobic conditioning exercises at an intensity of 70 to 85% of each subject’s calculated heart rate maximum (15)and a rated perceived exertion (RPE) value between 3 and 5 (moderate to strong) on the Borg scale (0 to 10) (8) for 10 to 20 min during treadmill walking. During the remaining 12 wks, the subjects increased the duration of the aerobic conditioning exercise from 10 to 20 min to 30 min. Also, the subjects were encouraged by the instructors to use other aerobic exercise machines if desired (e.g., cycle ergometer, elliptical trainer, and NuStep Recumbent Cross Trainer).

The RET component was designed to include 1 to 2 sets of 8 to 12 reps at 60 to 70% of the subject’s repetition maximum (1RM) (23) for the major muscle groups. Progression of the RET element consisted of approximately 5 to 10% increases in weight at which time the subject was capable of completing more than 12 reps for a given exercise (23). The third component of the program involved balance and flexibility training. This part of the program consisted primarily of stretching exercises as well as seated and standing static and dynamic

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balance exercises (e.g., balance ball exercises, ball and balloon tosses, reaches, bends, dance exercises, and yoga poses). Deep diaphragmatic breathing techniques were also part of the balance and flexibility component of the training sessions.

Outcome Measures

PSQI Outcome Measure The Pittsburgh Sleep Quality Index (PSQI) is a patient-reported outcome measure that assesses sleep quality over the previous month. The PSQI consists of 19 individual items that yield a composite or global sleep quality score, as well as sleep scores in seven sleep domains. The domains are: 1) sleep duration; 2) sleep disturbance; 3) sleep latency; 4) sleep daytime dysfunction; 5) sleep efficiency; 6) sleep quality; and 7) sleep medication use. The 19 items are grouped into seven domains, which are weighted equally on a scale from zero to three. The seven domains are also combined to yield a global sleep score, ranging from 0 to 21. Higher scores correlate to poor sleep quality (8). Buysee et al. (8) define sleep quality as the duration of sleep, sleep latency, number of arousals, as well as depth/restfulness of sleep. The PSQI was designed to measure sleep quality and sleep disturbances over the prior month and to discriminate between “good” (total PSQI score ≤5) and “bad” sleepers (total PSQI score >5).

The psychometrics of the PSQI are well established showing both validity and reliability for diagnosing sleep disorders in older populations (4,9) and cancer survivors (1). Internal consistency based on Cronbach’s alpha was shown as good (0.74(30) – 0.81(5)). Construct validity has also been shown as good (28,32). The PSQI possesses high diagnostic sensitivity (89.6%) and specificity (86.5%) in regards to the assessment of good and bad sleepers (4,8). Akman et al. (1) indicate that the PSQI is an appropriate and practical instrument to investigate sleep disorders in patients with cancer.

Data Analysis

The primary outcome measure for this study was global sleep quality via the PSQI. The secondary outcome measures were the domains of global sleep quality: 1) sleep duration; 2) sleep disturbance; 3) sleep latency; 4) sleep daytime dysfunction; 5) sleep efficiency; 6) sleep quality; and 7) sleep medication use. The analysis of sleep quality outcome was performed for all BCS who completed the exercise program and both the pre- and post- assessments. In some cases, the subjects did not complete a pre- or post-assessment and, thus they were excluded from analysis. Analyses were performed using SPSS® version 23.0. Sleep quality outcome measures were tested for skewness and kurtosis using z-tests, whereas a z-score was calculated by dividing the skew values and the kurtosis values by their respective standard errors (21). Z-scores for either skewness or kurtosis greater than 1.96 (0.05 alpha level) warranted rejection of the null hypothesis, and that the alternative hypotheses was accepted: the sample was not normally distributed (21). Results from this analysis revealed that some of the pre- or post-sleep domain scores were either skewed or kurtotic. Therefore, non-parametric related-samples Wilcoxon Signed Rank Tests were used for pre- and post- comparisons for the outcome measure that were considered not normally distributed (sleep duration, sleep disturbance, days of dysfunction, sleep efficiency, and sleep medication use). For the sleep outcome measures that were normally distributed (global sleep quality, sleep

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latency, and sleep quality), dependent t-tests were used to analyze the pre- post-differences. All data were tested for differences at an alpha level of 0.05.

The procedures described by Cohen were utilized in order to calculate and interpret effect sizes (ES), whereas 0.2 to 0.50 = “small to moderate”, 0.51 to 0.80 = “moderate to large”, and greater than 0.80 = “large” (11). Minimal clinically important differences (MCID) were calculated by multiplying the mean value of pre-assessment outcome measure by 15% (2).

RESULTS

Subject CharacteristicsRefer to Figure 1 for a graphic representation of the study flow. A total of 60 female BCS signed informed consent for the involvement in this study, but only 52 BCS completed the 12-wk multimodal exercise program (86.7%). Thirty-nine BCS subjects completed the PSQI both pre- and post-exercise program and were subsequently included in this investigation. Baseline demographic and anthropometric measures with comparative analysis (independent t-tests) for all BCS and the sub-sample BCS with completed pre- and post-PSQI outcome measures are presented in Table 1. The sub-set sample (N = 39) and total sample (N = 52) were not different in any participant characteristics (Table 1).

Figure 1. Study Flow Diagram.

Description of the medical treatment for the sub-set sample and the total sample are as follows: (a) all of the BCS in sub-set sample and all of the BCS in the total sample had surgery; (b) 82% of the BCS in the sub-set and 85% of the BCS in the total sample received chemotherapy; (c) 74% of the BCS in the sub-set and 75% of the BCS in the total sample

Eligible Breast Cancer Survivors Enrolled In Central Savannah River Area LIVESTRONG at Y

(n = 62)

Signed informed consents (n = 60)

Dropped out for various (e.g. family, work, scheduling etc) reasons (n = 8)

Analyzed with pre-post-outcomes available(n = 39)

Excluded no signed informed consent (n = 2)

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received radiation therapy; and (d) 38% of the BCS in the sub-set and 39% of the BCS in the total sample reported taking hormonal deprivation therapy.

Table 1. Baseline Demographic and Anthropometric Measures for all Breast Cancer Survivors (BCS) and the BCS with Completed pre- and post-PSQI Outcome Measures.

All BCS BCS with Completed Pre- and Post-PSQI

Comparison Analysis P Value (two tail)

t value

Mean ± SDRangeN

Mean ± SDRangeN

Age (yrs) 59.7 ± 10.446 – 8252

59.4 ± 10.536 – 8239

P = 0.8924  t = 0.1356

Weight (kg) 81.0 ± 16.176.7 – 127.144

77.5 ± 16.250.5 – 113.634

P = 0.3454 t = 0.9495

Height (cm) 164 ± 5152 – 178 44

163 ± 5152 – 17234

P = 0.3839 t = 0.8759

BMI (kg·m-2) 30 ± 329 – 4744

29 ± 328 – 3134

P = 0.1485 t = 1.4598

Resting Heart Rate(beats·min-1)

76 ± 9.160 – 10044

76 ± 9.960 - 10034

P = 1.0 t = 0.1498

Resting Systolic Blood Pressure (mmHg)

128 ± 15100 – 15844

128 ± 15100 – 15833

P = 0.5030 t = 0.6729

Resting Diastolic Blood Pressure (mmHg)

80 ± 860 – 9644

79 ± 863 – 9633

P = 0.5889 t = 0.5428

Years Since Medical Treatment

Average Attendance (%)

Exercise Level

4.96 ± 6.300 – 2452

82.9% ± 12.752

4.68 ± 5.780 – 2139

85.1% ± 12.439

P = 0.8342 t = 0.2100

P = 0.4110 t = 0.8260

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0.65 ± 0.8252

0.69 ± 0.7739

P = 0.8137 t = 0.2363

BMI = Body Mass Index; Comparison Analysis (independent t-tests); Medical Treatment (surgery, chemotherapy, and/or radiation therapy); Exercise Level (0 = No Regular Physical Exercise, 1 = Some Exercise (<2 times·wk-1), and 2 = Exercise Regularly (>3 times·wk-1)

Prior to the initiation of the exercise program, the subjects were asked about their current exercise activity. Their exercise levels were later categorized as 0 = no regular physical exercise, 1 = some exercise (<2 times·wk-1), and 2 = exercise regularly (>3 times·wk-1). Exercise level for the BCS in the sub-set sample was 0.69 ± 0.77 and exercise level for the BCS in the total sample was 0.65 ± 0.82.

The subjects were monitored throughout the exercise program for any signs and symptoms of exercise intolerance of which appropriate adjustments were made accordingly on an individualized basis. Although each subject was monitored for major adverse advents, no such outcome was reported.

Sleep Quality Outcome MeasuresThe mean baseline global sleep quality score was 7.9 which indicated the BCS were “poor” sleepers (>5) (8,40) prior to beginning the multimodal exercise program. Analysis of pre- post-exercise program sleep quality outcome measures revealed statistically significant improvements (P<0.05) in the following: global sleep quality; sleep quality; sleep disturbance; and days of dysfunction (Table 2).

Table 2. Comparison Analysis of Pre- and Post-PSQI Sleep Outcome Measures.

Pre- Post- P value (two tail)

Sleep DurationMean ± SD95% CIMedianRange

0.85 ± 1.100.5 - 1.200 - 3

0.69 ± 0.950.4 - 1.000 - 3

0.253Wilcoxon

Sleep DisturbanceMean ± SD95% CIMedianRange

1.64 ± 0.480.5 - 0.821 - 2

1.44 ± 0.501.3 - 1.611 - 2

0.021*Wilcoxon

Sleep LatencyMean ± SD95% CIMedianRange

1.28 ± 1.140.9 - 1.610 - 3

1.02 ± 1.010.7 - 1.310 - 3

0.058t = 1.96

Days of DysfunctionMean ± SD 1.0 ± 0.76 0.69 ± 0.61 0.014*

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95% CIMedianRange

0.8 - 1.210 - 3

0.5 - 0.910 - 3

Wilcoxon

Sleep EfficiencyMean ± SD95% CIMedianRange

1.10 ± 1.200.7 - 1.510 - 3

0.87 ± 1.100.5 - 1.21 0 - 3

0.206Wilcoxon

Sleep Quality Mean ± SD95% CIMedianRange

1.07 ± 0.770.8 - 1.310 - 3

0.67 ± 0.700.5 - 0.910 - 2

0.000*t = 4.02

Sleep Medication UseMean ± SD95% CIMedianRange

0.92 ± 1.260.5 - 1.300 - 3

0.74 ± 1.220.3 - 1.100 - 3

0.143Wilcoxon

Global Sleep QualityMean ± SD95% CIMedianRange

7.9 ± 4.306.5 - 9.271 - 17

6.1 ± 3.94.8 - 7.461 - 15

0.001*t = 3.79

SD = Standard Deviation; CI = Confidence Interval; * Statistical significance (P<0.05)

DISCUSSION

The primary findings in this study indicate that the BCS were “poor” sleepers at baseline and, yet they had significantly (P<0.05) improved global sleep quality (23%) after the program was completed. However, they were still “poor sleepers”. The secondary findings were that the post-exercise program sleep outcome measures of sleep disturbance (12%), days of dysfunction (31%), and sleep quality (37%) were significantly improved (P<0.05) compared to the pre-exercise program sleep quality measures. Although the BCS in this study showed improvement in these sleep quality outcome measures after participating in this community-based exercise program, careful interpretation of these results are necessary.

In this study, the baseline (pre-) mean global sleep quality was (7.9) which indicates that the BCS were “poor sleepers” (>5) (8,40) prior to participation. This finding is comparable with results reported by Garret et al. (17) for global sleep quality (7.3) in other BCS. Although the subjects’ global sleep quality in the present study had significantly improved (-1.8) post-exercise, they would still be classified as “poor sleepers” (6.1 >5). Hence, while global sleep quality may be improved after participating in multimodal exercise, the improvement (-1.8) may not be sufficient to make “poor sleepers” into “good sleepers”. The PSQI does not

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provide information regarding a clinically important magnitude of change, however, we determined a “small to moderate” ES (0.42) improvement in global sleep quality (Table 3). The present ES improvement in global sleep quality is similar to the ES improvement (0.40) in the global sleep quality improvement reported in two systematic reviews on exercise interventions and sleep quality in patients with cancer (26,27). Additionally, we calculated a MCID of 1.18 for global sleep quality (Table 3) and after comparing this to the mean difference for pre- post-global sleep quality (1.8), we believe that this improvement is clinically important.

In the two aforementioned systematic reviews, the ESs reported were for global sleep quality and not for the other sleep domains. However, we calculated and present the ESs and minimally clinically important differences for the domains of sleep quality in Table 3. “Small to moderate” ESs were noted for sleep disturbance (0.42), sleep latency (ES = 0.23), days of dysfunction (ES = 0.41), and PSQI total (0.42). As to whether these improvements in sleep domain are clinically important remains to be determined (refer to Table 3).

Table 3. Comparison of Clinimetric Data for PSQI Outcome Measures.

Outcome Measure Mean Difference

95% CI Effect Size MCID

Sleep Duration -0.16 -0.43 to -0.12 0.14 0.13

Sleep Disturbance -0.2 -0.37 to -0.04 0.42 0.25

Sleep Latency -0.26 -0.52 to -0.01 0.23 0.19

Days of Dysfunction -0.31 -0.54 to -0.07 0.41 0.15

Sleep Efficiency -0.23 -0.61 to -0.15 0.19 0.16

Sleep Quality -0.40 -0.62 to -0.20 0.52 0.16

Sleep Medication Use -0.18 -0.41 to -0.05 0.14 0.14

Global Sleep Quality -1.8 -2.67 to -0.81 0.42 1.18

CI = Confidence Interval; MCID = Minimal Clinically Important Difference; Bolded outcome measures were significantly different (P<0.05) pre- to post-

Improvements in days of dysfunction (mean difference = 0.31; MCID = 0.15) and sleep quality (mean difference = 0.40; MCID = 0.16) were all greater than the MCIDs, thus indicating that these improvements are clinically important. It is worth noting that even though sleep duration, sleep latency, sleep efficiency, and medicine induced sleep were not statistically (P>0.05) improved, the mean differences from pre- to post- were greater than the calculated MCIDs. This suggests that these improvements may be clinically important. A “Moderate to large” ES was noted for the domain sleep quality (0.52). This finding was also considered clinically important (mean difference = 0.40; MCID = 0.16).

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Direct comparison of the present findings with other research findings on the effects of multimodal community-based exercise programs on sleep quality in BCS is difficult due to limited translational studies at the community level and variety of exercise modalities. However, there is research evidence that supports exercise as an adjuvant therapy for cancer survivors and the improvement in their sleep quality (12,29,30). Courneya et al. (12) reported that high levels of aerobic exercise effectively contributed to sleep quality management. They reported that a high level of aerobic exercise (50 to 60 min 3 times·wk -1) or a combination of aerobic and resistance training (50 to 60 min 3 times·wk -1) can lead to improvement in sleep quality and sleep latency in individuals in comparison to the standard level (25 to 30 min) of aerobic exercise. They also reported the following mean differences in the high volume aerobic exercise training as compared to standard training: global sleep quality (-0.90), sleep quality (-0.18), and sleep latency (-0.16). These values compare to the results of the pre- post-mean differences in the present study for global sleep quality (-1.8) and sleep quality (-0.4). In the present study, we also found a trend towards improved sleep latency (-0.26).

In another investigation by Mustian et al. (30) on the effects of yoga training on sleep quality (PSQI), pre- post- mean differences were reported for significant improvements in global sleep quality (-0.79), daytime dysfunction (-0.38), sleep quality (-0.63), and sleep medication use (-0.56). Although the exercise modalities and parameters (yoga, 75 min, 2 times·wk -1 for 4 wks versus multimodal exercise, 90 min for 12 wks) were different, the improvements are comparable with our findings. Also, the results of the present study indicate a trend of decreased sleep medication use (-0.18).

In a systematic review (27) of exercise interventions on health-related quality of life for people during active cancer treatment it was reported that exercise interventions can lead to decreased sleep disturbance (mean difference -0.46). In comparison, this current study reports a pre- post-mean difference for sleep disturbance (-0.20).

Limitations in this Study

Due to this study being a translational community-based cancer survivor exercise program and the fact the study evaluated BCS who volunteered for the program and also that it did not have a control group for definitive comparison or randomization, time was the independent variable that may have played a role in the improvement found in global sleep quality and sleep domains. Therefore, no cause and effect conclusions can be made. We can only state that improvements were found after the pre- post-comparisons. Since we studied volunteer BCS who participated in the program, the sample of BCS may not represent BCS as a whole. Additionally, we did not assess potential covariates (e.g., race, ethnicity, income, and education); consequently, there is limited generalizability. Collectively, the BCS were “poor sleepers” and the effect of exercise on “poor sleepers may be different than the effect on “good sleepers”. Despite these limitations we believe this investigation has translation merit that suggests improved sleep quality may be another of the many the benefits of community-based exercise programs for BCS.

CONCLUSIONS and CLINICAL RELEVANCE

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Breast cancer survivors and cancer survivors in general are living longer and many have multisystem impairments that can adversely affect sleep quality and quality of life (1). Incidence of sleep impairments in cancer survivors are double or triple of what is found in the general population (17,29). We found that the BCS were “poor sleepers” at baseline and after completing 12 wks of a community-based multimodal exercise program, their sleep quality significantly improved (although they were still classified as “poor sleepers”). These findings are greater than the calculated minimum clinically significant differences. Thus, it is more than reasonable to conclude that the improvements in sleep quality are clinically important. Our findings are similar to clinically-based exercise studies for cancer survivors with regards to sleep quality. We believe this study promotes exercise as medicine for cancer survivors, while emphasizing translational application towards community-based exercise programming for cancer survivors.

ACKNOWLEDGMENTSSpecial thanks to all the breast cancer survivors who participated in this study.

Address for correspondence: Michael P. Foley, PhD, PT, Department of Physical and Occupational Therapy, Idaho State University, Campus Stop, 8045, Pocatello, Idaho, USA, 83209-8045. Email: folemich@isu.edu

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