Clinical Research

Safety and efficacy of resistance exercise in prostate cancer patients with bone metastases

An Erratum to this article was published on 12 May 2015

Abstract

Background:

Due to concerns of fragility fracture, exercise is a perceived contraindication for prostate cancer patients with bone metastases. These patients experience significant functional impairment and muscle atrophy, which may lead to an increased likelihood of skeletal complications (i.e., pathological fracture, bone pain) and/or falls. Safe resistance exercise prescription may counteract this effect. The aim of this feasibility trial was to determine the safety and efficacy of resistance exercise by prostate cancer survivors with bone metastatic disease.

Methods:

Twenty men with established bone metastases secondary to prostate cancer were randomly assigned to a 12-week resistance exercise program in which exercise prescription was based on the location of bone lesions (n=10) or usual care (n=10). Outcomes included safety and tolerance of the exercise program, physical function, physical activity level, body composition, fatigue, quality of life and psychological distress. Outcomes were compared between groups using analysis of covariance adjusted for baseline values.

Results:

Participants had significant disease load with 65% of participants presenting with two or more regions affected by bone metastases and an average Gleason score of 8.2±0.9. Five participants (exercise=2; usual care=3) did not complete the intervention, three of which were due to advancing disease (exercise=2; usual care=1). No adverse events or skeletal complications occurred during the supervised exercise sessions. The exercise program was well tolerated as evidenced by high attendance (83%) and compliance rates (93%), and the ability of the participants to exercise at an intensity within the target range for cancer survivors (rating of perceived exertion =13.8±1.5). The change in physical function (muscle strength 11%; submaximal aerobic exercise capacity 5% and ambulation 12%), physical activity level (24%) and lean mass (3%) differed significantly between groups following the intervention, with favorable changes in the exercise group compared with the usual care group. No significant between-group differences were observed for fatigue, quality of life or psychological distress.

Conclusions:

This initial evidence involving a small sample size suggests that appropriately designed and supervised resistance exercise may be safe and well tolerated by prostate cancer patients with bone metastatic disease and can lead to improvements in physical function, physical activity levels and lean mass. Future trials involving larger sample sizes are required to expand these preliminary findings.

Introduction

Bone metastatic disease is estimated to affect 65–75% of men with prostate cancer1 and involves sclerotic lesions that commonly occur in the axial skeleton and pelvis.2 Although the clinical course of bone metastatic disease secondary to prostate cancer is relatively long with an estimated 5-year survival rate of 30–46%,1, 3 it is associated with significant morbidity caused by skeletal complications.1, 4 As such, patients are likely to experience bone pain, pathological fractures, hypercalcaemia and spinal cord/nerve compressions over an extended period of time.1, 4, 5 These complications coupled with the extensive treatment-related adverse effects of long-term androgen-suppression therapy6, 7, 8, 9 and therapy for castration-resistance disease1, 10 result in considerable disease burden that has a profound impact on everyday function and quality of life.4, 11, 12 Consequently, strategies to reduce the burden of bone metastatic disease have a high degree of clinical importance.

Clinical trials have demonstrated exercise to be an effective medicine to counteract treatment-related adverse effects, leading to improved physical and psychological outcomes in men with localized prostate cancer.13, 14 The magnitude of effect observed in studies involving prostate cancer patients as well as patients with other cancer diagnoses (predominately breast cancer) has led the American Cancer Society to endorse international guidelines that advise all cancer survivors (including those with bone metastases) to avoid inactivity and engage in regular exercise including strength training exercises.15, 16 However, there is an absence of clinical trials examining whether exercise is safe and can be tolerated by patients with bone metastatic disease. In fact, all clinical trials to date investigating the safety and efficacy of exercise have excluded patients who had bone metastases or bone lesions deemed as unstable due to the potential increased risk of skeletal complications.17 Although reasonable given the relative paucity of research into the safety and efficacy of exercise in the general oncology setting, this situation is highly detrimental because patients with bone metastases are reducing their physical activity levels for fear of skeletal complications, a strategy that can only result in further declines in musculoskeletal structure and function, a greater risk of comorbid conditions and a reduced quality of life.5, 11, 18 Safe exercise prescription for prostate cancer patients with bone metastatic disease may provide clinically meaningful benefits to patients through improvements in musculoskeletal structure/function, which lead to enhanced functional abilities and potentially a reduced risk of skeletal complications. Despite the likely benefit of targeted exercise prescription for patients with bone metastatic disease, there is a clear lack of clinical and empirical data of implementing exercise in these advanced patients. The purpose of this trial was to provide initial experimental data on safety and efficacy of resistance exercise in prostate cancer survivors with bone-metastatic disease. To the authors’ knowledge, this is the first trial specifically designed to examine exercise in cancer patients with bone metastases.

Materials and methods

Participants

Twenty-seven men aged 57–83 years with bone metastatic disease secondary to prostate cancer were referred by oncologists and urologists in Perth, Western Australia from July 2011 through July 2012 and screened for participation in the study (Figure 1). Participants had a histological diagnosis of prostate cancer, established bone metastatic disease as determined by a whole-body bone scan and obtained written medical clearance from their physicians (general practitioner). Patients were excluded if they experienced moderate–severe bone pain that limited activities of daily living (i.e., National Cancer Institute’s Common Terminology Criteria for Adverse Events grade 2–3 bone pain19) or had musculoskeletal, cardiovascular and/or neurological disorders that could inhibit them from exercising (as determined by the patient’s physician). This protocol was approved by the University Human Research Ethics Committee and all participants provided written informed consent.

Figure 1
figure1

Flow of participants throughout the trial. RM, repetition maximum.

Experimental design

This pilot study involved a two-armed prospective randomized controlled trial design. Following familiarization and baseline testing sessions, participants were randomized into the two arms: exercise or usual care. Stratification for age (70>) was carried out and participants were randomized in an allocation ratio of 1:1 using a random assignment computer program. The project coordinator and exercise physiologists involved in assigning participants to groups were blinded to the allocation sequence. Participants randomized to the usual care group received no intervention but were offered the exercise program after the completion of the intervention period. All participants were instructed to maintain their customary activities, dietary and social patterns as well as their usual self-management regimen throughout the intervention period.

Exercise intervention

The exercise intervention involved twice-weekly resistance exercise sessions for 12 weeks in an exercise clinic. Sessions were conducted in small groups of one to five participants supervised by accredited exercise physiologists. The sessions were 60 min in duration, commencing with a 5-min warm-up period and ending with a 10-min cool-down period consisting of low-level aerobic exercise and stretching. The resistance exercise regime included eight exercises that target the major muscle groups of the upper and lower body. The selection of specific exercises was based on the location of bone metastases so that affected regions were not targeted and mechanical force was minimized (Table 1).20 Participants were instructed to perform the exercises using controlled, smooth movements at a set cadence of 1–2 s for both eccentric and concentric phases in order to minimize peak forces transmitted to the skeleton. The resistance exercise load progressed from 12–8 repetition maximum (RM) with two to four sets per exercise.16, 21 To ensure the progressive nature of the program, participants were encouraged to work past the specific RMs prescribed and if they exceeded the target then additional resistance was added for the next set and/or session. The prescribed target number of RM (i.e., 12–8 RM) and sets (i.e., 2–4) were progressed every 2 weeks, with the absolute load of each exercise progressed according to individual response. Although the intensity and volume of the resistance exercise program is in accordance with recommendations for cancer patients with localized disease,16 the modular approach to exercise selection involved with this program is novel and specialized for patients with bone metastatic disease.20 This approach is designed to minimize compressive and shear loads on affected skeletal sites to account for the reduced load-bearing capabilities of the bone because of metastatic disease in specific regions. Participants were encouraged to supplement the resistance exercise sessions with home-based aerobic exercise sessions involving walking and/or stationary cycling, with the aim of accumulating a total of at least 150 min of moderate-intensity aerobic exercise each week.16

Table 1 Systematic approach to resistance exercise selection for prostate cancer with bone metastases

Outcome measures

Outcome measures were assessed at baseline (0 weeks) and post intervention (12 weeks). Participants completed a familiarization session 7–10 days prior to baseline testing involving all physical function assessments.

Safety and tolerability of exercise

The safety of the exercise program was assessed by recording the incidence and severity of any adverse events and skeletal complications (including pain at known bone metastases sites and pathological skeletal fractures1) throughout the intervention. Any adverse event occurring during a supervised exercise session was recorded by the exercise physiologist and events occurring outside of the supervised sessions were recorded using a detailed log completed by the participant. Severity of bone pain was assessed using the Functional Assessment of Cancer Therapy Bone Pain questionnaire, with higher scores representing lesser bone pain and/or better quality of life,22, 23 as well as a visual analog scale (VAS)24 including severity ratings from no pain (VAS score=0) to very severe pain (VAS score=10). Additional measurements were taken during every exercise session. The level of bone pain participants were experiencing prior to the start of each exercise session was assessed using the VAS. Participants designated the location of any bone pain and whether this pain affected their ability to undertake usual activities of daily living since the previous exercise training session. Compliance to the prescribed exercise program was assessed as the rate of successfully completed exercise sessions compared with the number of sessions attended. Non-compliance to an exercise session was considered as any deviation from the prescribed number of exercises, sets or repetitions (for example, a session was classified as non-compliant if just one set of one exercise was not completed). Session rating of perceived exertion (RPE) was recorded immediately after the completion of each exercise session to assess the perceived intensity of the exercise.25 Participants were asked to rate the overall difficulty of the session (i.e., how hard/how much exertion was involved) on a scale of 6 (no exertion at all) to 20 (maximal exertion). A 7-point Likert scale was also administered after the completion of each exercise session to assess the perception of tolerance of the exercise session.26 Participants rated how much they agreed or disagreed to the statement “I have found the exercise session to be tolerable” on a scale of one (strongly disagree) to seven (strongly agree).

Physical function and physical activity levels

A series of standard tests were used to assess physical function that are as follows:21 (1) one RM in the leg extension (muscular strength), (2) 400-m walk (submaximal aerobic exercise capacity), (3) usual and fast pace 6-m walk (ambulation), (4) timed up and go (muscular power and ambulation) and (5) sensory organization test (balance) performed on the Neurocom Smart Balancemaster (NeuroCom, Clackamas, OR, USA). To minimize the potential risk of skeletal complications, participants with bone metastases affecting the femur did not perform the 400-m walk and leg extension 1RM assessments (exercise group n=3; usual care group n=1). Falls self-efficacy was also determined using the Activities-Specific Balance Confidence scale (ABC score; higher score represent greater balance confidence).27 Physical activity levels were assessed objectively over a 7-day period using a validated, reliable tri-axial accelerometer activity monitor (ActiGraph GT3X+).28 The assessment period occurred prior to baseline testing and after the completion of the post-intervention test (i.e., not contaminated by exercise sessions and/or testing sessions involved with the trial). Standard data processing was applied and the weekly duration of low, moderate and vigorous-intensity physical activity determined in accordance with established ranges.29 Self-reported physical activity was also assessed by the leisure score index from the Godin Leisure-Time Exercise Questionnaire.30, 31

Body composition

Regional and whole-body lean mass and fat mass were derived from whole-body dual-energy X-ray absorptiometry scans (Hologic Discovery A, Waltham, MA, USA). Appendicular lean mass, trunk adiposity and visceral fat mass were assessed using standard procedures.

Patient-reported outcomes

A series of questionnaires with sound psychometric properties were utilized to assess cancer-related fatigue, quality of life and psychological distress. The Multidimensional Fatigue Symptom Inventory-Short Form assessed general, physical, emotional, mental and total fatigue as well as vigor.32 The Medical Outcomes Study 36-Item Short-Form Health Survey (SF-36) was used to assess quality of life status across the following domains: physical function, role physical, body pain, general health, vitality, social function, role emotional and mental health.33 The Brief Symptom Inventory-18 was utilized to assess psychological distress across the domains of depression, anxiety, somatization and global distress severity.34

Statistical analyses

Sample size calculations were based on change in physical function. As the first exercise intervention trial involving patients with bone metastatic disease, we estimated the change in physical function based on results over the same intervention period in prostate cancer patients with localized disease.21 We anticipated a change of 10% with a s.d. of 8% for an effect size of 1.25. With an alpha level of 0.05 and a final sample of 20 patients, we achieved 75% statistical power to detect such a change.

Data were analyzed using SPSS Statistics 20. Analyses including standard descriptive statistics, independent t-tests, χ2 tests, analysis of covariance adjusted for baseline values. Measures of bone pain were also adjusted for use of pain medication. An intention-to-treat approach was utilized for all analyses using maximum likelihood imputation of missing values (expectation maximization). All tests were two-tailed, with statistical significance set at an alpha level of 0.05. Results are presented as mean±s.d. or number of participants (percentage of participants) for frequency data.

Results

The two groups were well balanced, with no significant differences in characteristics at baseline (Table 2). Furthermore, there were no significant differences between groups at baseline in any of the outcome measures assessed. Participants had significant disease load, with 65% of participants presenting with two or more regions affected by bone metastases and an average Gleason score of 8.2±0.9. Two participants from the exercise group discontinued the intervention because of advancing disease requiring further treatment with chemotherapy (n=1) and increased level of bone pain which occurred during a 2-week break from the exercise program over the Christmas holiday period (n=1; related to events outside of the intervention). Three participants from the usual care group were lost to follow-up because of advancing disease requiring further treatment with chemotherapy (n=1), travel constraints (n=1) and the need to commit to being a full-time carer for their spouse (n=1). There were no demographic or clinical differences between those who did and did not complete the intervention. Four participants from the usual care group completed the delayed exercise program after the intervention period and the outcomes were similar to those of the exercise group.

Table 2 Baseline characteristics of participants

Safety and tolerability of exercise

No adverse events or skeletal complications occurred during the exercise sessions (Table 3). One incident was reported outside of the exercise sessions, in which a participant in the exercise group fell while dressing at home and suffered a fractured rib. This occurred during week 10 of the intervention; however, he was able to continue the intervention with a modified exercise program for the remaining 2 weeks. There was no between-group difference in the total number of adverse events that occurred throughout the intervention period (exercise=3 (advancing disease requiring chemotherapy=1, increased bone pain=1 and fall=1); usual care=1 (advancing disease requiring chemotherapy); P=0.264). There was no change in the use of pain medication throughout the intervention. Exercise program attendance was high, with an average attendance of 20 sessions out of a possible 24 (83% attendance) and 70% of the participants completing all the 24 sessions. Compliance to the exercise prescription was 93.2±6.3% (i.e., 93% of attended sessions were successfully completed in full adherence with the prescribed program). Deviations from the prescribed program commonly involved not completing all the required sets for an exercise or not performing an exercise during the session. There were no significant group differences in the change in bone pain following the intervention (Table 4). The severity of bone pain reported at each exercise session was low, with an average of 0.6±0.7 on a scale of 0 (no pain) to 10 (very severe pain) and a maximum of 1.4±1.2 across all sessions (Table 3). The highest level of bone pain recorded throughout the exercise program was 3.3. There were no incidences in which a change in bone pain since the previous exercise session negatively affected the abilities to undertake normal daily activities (Table 3). Participants were able to exercise at an intensity within the target range for cancer survivors (i.e., moderate–high intensity; RPE=12–1616) with the average perceived intensity of 13.8±1.5 on the RPE scale. Furthermore, the exercise sessions were well tolerated as evidenced by an average perceived tolerance score of 6.1±0.7 out of a possible rating of 7 (Table 3).

Table 3 Safety and tolerability of the exercise intervention
Table 4 Bone pain, physical function, physical activity levels and body composition values and the group difference in change over the intervention

Physical function and physical activity levels

Change in maximal muscular strength (leg extension 1RM 11%; n=16), submaximal aerobic exercise capacity (400-m walk 5%; n=16) and ambulation (6-m walk—usual pace 12%) across the 12-week intervention differed significantly between groups, with favorable changes in physical function observed for the exercise group compared with the usual care group (Table 4). Trends towards greater improvement in the exercise group for 6-m walk—fast pace (7%)— and timed up and go (6%) performance were also observed. No significant between-group differences were observed for balance or balance confidence (Table 4). Change in low-intensity physical activity level across the 12-week intervention differed significantly between groups (24%), with the exercise program prompting favorable physical activity behavior compared with usual care (Table 4). A borderline group difference in the change in vigorous-intensity physical activity was also observed.

Body composition

Change in whole body and appendicular lean mass across the 12-week intervention differed significantly between groups (3 and 4% respectively; Table 4). Favorable changes were observed for the exercise group compared with the usual care group. No significant between-group differences were observed for fat mass (Table 4).

Patient-reported outcomes

No significant between-group differences were observed for fatigue, quality of life or psychological distress (Table 5).

Table 5 Absolute and change values for patient-reported outcomes of fatigue, quality of life and psychological distress

Discussion

This trial provides initial evidence that appropriately designed and supervised resistance exercise may be safe and effective in prostate cancer patients with bone metastatic disease. The primary findings were that appropriate resistance exercise prescription (1) was well tolerated and did not significantly increase skeletal complications and (2) resulted in improved physical function, physical activity levels and lean mass in the sample of prostate cancer patients with bone metastases involved in this trial.

International exercise guidelines for cancer survivors recommend an ‘altered’ program for patients with bone metastases due to increased risk of skeletal complications.16 However, no evidence has been available to support or refute this claim or to provide any guidance on the alterations in exercise prescription necessary for this patient population. This trial provides the first evidence to address this gap in knowledge. Specifically, appropriately supervised resistance exercise targeting areas unaffected by bone metastases was observed to be safe and well tolerated by this cohort of prostate cancer patients with bone metastatic disease. Despite the high disease load associated with the enrolled participants, no adverse events were observed during the exercise sessions and there were no between-group differences in the number of adverse events that occurred throughout the 12-week intervention period. Importantly, the patients involved in this trial were able to exercise at intensities required to realize health benefits (i.e., moderate–high intensity) consistently throughout the program.15, 16

Not only was the targeted resistance exercise program safe but was also effective, resulting in improvements to musculoskeletal structure and function in this sample of patients. Despite a relatively short intervention, the exercise program resulted in significant improvements in muscular strength (11%), submaximal aerobic exercise capacity (5%) and ambulation (12%), changes anticipated to have a considerable impact on functional ability in everyday life.35 Notably, the program protected against muscle atrophy with an 4% difference in the change in lean muscle mass observed between the exercise and usual care groups. Collectively, these improvements have a high degree of clinical significance, as they protect against falls and skeletal complications that cause significant morbidity and mortality36, 37, 38 as well as high treatment costs.39 Although fat mass was not reduced by this short-duration exercise intervention, the increase in skeletal muscle mass will likely result in considerable benefit by ameliorating metabolic disorders through improved insulin resistance and glucose homeostasis.40 Furthermore, the exercise intervention had a positive effect on objectively measured levels of physical activity (beyond the prescribed exercise intervention), prompting behavior change that led to a difference of 24% between exercisers and non-exercisers. This is another clinically meaningful outcome, given the association between physical activity and both all-cause and prostate cancer mortality.14

There are several unique features of this research that are worthy of comment. This trial was the first to specifically target patients with bone metastatic disease and involved older patients with high disease load; a cohort that is typically difficult to enroll in exercise trials. Furthermore, a thorough series of objective and self-reported measures were used to comprehensively examine the safety and efficacy of the intervention. However, limitations included the low number of participants involved with the trial, the relatively well-functioning status of the participants, the self-reporting approach to monitor the severity of bone pain and adverse events outside of supervised exercise sessions, as well as the lack of a follow-up assessment point. The number of participants restricted the power to detect significant changes in outcomes with small–moderate standardized effects (i.e., quality of life, psychological distress and fatigue). Further research involving larger sample sizes and the combination of resistance and aerobic exercise within the supervised exercise program is underway to expand these initial findings and also to determine whether exercise confers any beneficial effect on quality of life in patients with bone metastases.20 Despite their significant disease load, participants were relatively well-functioning individuals (i.e., average self-rated health reported as ‘good’; Table 2) who were mostly motivated to undertake the exercise study. Thus, they may not be representative of all prostate cancer patients with bone metastatic disease, and the results of this trial should be interpreted with this in mind. Furthermore, future trials involving long-term follow-ups are required to examine whether exercise has a protective effect against the risk of skeletal complications, disease progression and ultimately mortality.

Conclusions

Exercise programs for patients with bone metastases must be designed and executed with careful consideration of the location and severity of bone lesions and the associated skeletal complications. Initial evidence from this small randomized controlled trial suggests that appropriately designed and supervised resistance exercise targeting skeletal regions not affected by bone lesions may be safe and well tolerated by prostate cancer patients with bone metastatic disease and can lead to improved physical function, physical activity levels and lean mass. These changes are expected to have a positive impact on disease burden through delaying (or potentially preventing) skeletal complications, falls and functional decline, as well as reducing the risk of comorbid conditions. However, future trials involving larger sample sizes are required to expand these preliminary findings.

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Acknowledgements

This study was funded by the Cancer Council of Western Australia through the Early Career Investigator research grants program. PC is supported by the Cancer Council Western Australia Postdoctoral Research Fellowship. DAG is funded by a Movember New Directions Development Award obtained through the Prostate Cancer Foundation of Australia’s Research Program.

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Cormie, P., Newton, R., Spry, N. et al. Safety and efficacy of resistance exercise in prostate cancer patients with bone metastases. Prostate Cancer Prostatic Dis 16, 328–335 (2013). https://doi.org/10.1038/pcan.2013.22

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Keywords

  • bone metastatic disease
  • physical activity
  • advanced cancer
  • physical function

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