Exercise for people with cancer: a systematic review

Review Article


Exercise for people with cancer: a systematic review


R. Segal, MD*, C. Zwaal, MSc, E. Green, BScN, J.R. Tomasone, PhD§, A. Loblaw, MD MSc, T. Petrella, MD#, Exercise for People with Cancer Guideline Development Group


doi: https://doi.org/10.3747/co.24.3619


ABSTRACT

Background

This systematic review was completed by the Exercise for People with Cancer Guideline Development Group, a group organized by Cancer Care Ontario’s Program in Evidence-Based Care (pebc). It provides background and guidance for clinicians with respect to exercise for people living with cancer in active and post treatment. It focuses on the benefits of specific types of exercise, pre-screening requirements for new referrals, safety concerns, and delivery models.

Methods

Using the pebc’s standardized approach, medline and embase were systematically searched for existing guidelines, systematic reviews, and primary literature.

Results

The search identified two guidelines, eighteen systematic reviews, and twenty-nine randomized controlled trials with relevance to the topic. The present review provides conclusions about the duration, frequency, and intensity of exercise appropriate for people living with cancer.

Conclusions

The evidence shows that exercise is safe and provides benefit in quality of life and in muscular and aerobic fitness for people with cancer both during and after treatment. The evidence is sufficient to support the promotion of exercise for adults with cancer, and some evidence supports the promotion of exercise in group or supervised settings and for a long period of time to improve quality of life and muscular and aerobic fitness. Exercise at moderate intensities could also be sustainable for longer periods and could encourage exercise to be continued over an individual’s lifetime. It is important that a pre-screening assessment be conducted to evaluate the effects of disease, treatments, and comorbidities.

KEYWORDS: Exercise, systematic reviews

INTRODUCTION

The inclusion of exercise into an individual’s daily lifestyle is known to promote many health benefits; the same holds true for people with cancer. In addition to improving physical wellbeing, exercise can help in the management of treatment side effects, and its physiologic and psychological changes can drastically affect quality of life (qol).

The present systematic review explores the effects of exercise for people living with cancer with respect to qol, physical fitness, safety, adverse events or injuries, intensity levels, types of exercise, and delivery models. The exercise-specific recommendations are relevant for oncologists, exercise consultants, primary care providers, and other members of health care teams who work with people with cancer. Guidelines, systematic reviews, and primary literature are used as the evidence for the review, which was conducted for the purposes of preparing an evidence-based guideline by Cancer Care Ontario’s pebc in 2015.

METHODS

The pebc uses the methods of the practice guidelines development cycle1 to produce evidence-based and evidence-informed guidance documents. The process consists of conducting a systematic review, conducting a quality appraisal and interpretation of the evidence, drafting recommendations that undergo internal review, and conducting an external review.

Literature Search Strategy for Guidelines and Systematic Reviews

A search of medline, embase, and the Cochrane Database of Systematic Reviews (January 2005 to October 2013; updated to January 2014) was conducted for published guidelines and systematic reviews. The search terms “exercise guideline” and “exercise and cancer” were used in searches of the Standards and Guidelines Evidence Directory of Cancer Guidelines, the U.S. National Guideline Clearinghouse, and the Canadian Medical Association Infobase for existing evidence-based guidelines. Additional guidelines relevant to the present study were found in a general Internet search using the Google search engine. The agree ii instrument2 was used to evaluate the quality of guidelines that had relevant objectives and research questions. The amstar tool3 served a similar purpose for relevant systematic reviews. Two Cochrane reviews that covered all randomized controlled trials (rcts) until 2011 were identified. A systematic review of the primary literature was therefore conducted to update the Cochrane reviews.

Literature Search Strategy for Primary Studies

A search for primary studies in medline (September 2011 to April, week 1, 2015) and embase (September 2011 to April, week 2, 2015) used the mesh headings “exercise.mp” and “neoplasms.mp.” To be included, studies had to be rcts published in the English language between 2011 and 2015. The Cochrane Risk of Bias tool4 was used to assess rcts.

Study Selection Criteria: RCTs

Articles were considered for inclusion according to their study design and relevance to the research questions. Studies were included if they were rcts that

  • ■ considered adult individuals with cancer in active or post treatment,

  • ■ considered the effects of an exercise regimen compared with usual care,

  • ■ evaluated the outcomes of qol and aerobic capacity or muscular fitness,

  • ■ used an exercise regimen that included repetitive aerobic or resistance exercises,

  • ■ were not included in an identified systematic review,

  • ■ were published in the English language (because of unavailability of translation services), and

  • ■ were published in 2011 or later.

Studies were excluded if they

  • ■ compared exercise regimens,

  • ■ involved non-repetitive exercise regimens (that is, yoga),

  • ■ were observational studies, or

  • ■ evaluated outcomes other than qol or muscular or aerobic fitness.

Data Extraction and Assessment of Study Quality and Potential for Bias

Data extraction was conducted by one author (CZ) and was reviewed by a second independent individual using a data audit procedure. Disagreements were resolved by consensus. The data extracted from each relevant article were the authors, publication year, study population, number of participants, treatment phase, intervention characteristics, qol scores, fitness measures, adherence, and adverse events. All extracted data and information were audited by an independent auditor.

RESULTS

Overall Literature Search Results

The literature included in the review were 2 of the 11 identified guidelines, 18 of the 84 identified systematic reviews, and 29 of the 405 identified rcts.

Synthesizing the Evidence

Because of the clinical heterogeneity of the studies (for example, disease types, treatment status), the nature of the interventions (varying types of exercises), and the outcomes assessed (varying measures), a meta-analysis was not possible.

Outcomes

QOL and Exercise During Active or Post Treatment

A systematic review of evidence published between 2005 and 2013 identified two guidelines, eighteen systematic reviews, and twenty-nine rcts that examined topics concerning exercise, such as safety, qol, aerobic and muscular fitness, delivery models, and types of exercise (Figure 1, Table i). Much of the evidence supports an improvement in qol and physical fitness for patients participating in the interventions.

 


 

FIGURE 1 Flow diagram of study selection.

TABLE I Sources selected for inclusion

 

The evidence is of moderate quality (Tables iiiv). The guidelines scored well on the agree ii reporting instrument2. The systematic reviews had some issues with heterogeneity of outcomes, populations, and interventions. Issues with the rcts included active control groups who increased their voluntary exercise, variation in adherence rates or lack of adherence measurements, performance bias, and in some cases, use of questionnaires targeted to patients in active treatment that might not be applicable in a post-treatment population. The next few subsections examine evidence about the safety of exercise and whether, for people with cancer, exercise can be used as an intervention to improve qol as well as physical fitness—and, if so, what types of exercise accomplish that goal the best.

TABLE II AGREE II scores for the included guidelines

 

TABLE III AMSTAR results for the included systematic reviews

 

TABLE IV Risk-of-bias results for the included randomized controlled trials

 

QOL and Muscular and Aerobic Fitness

For most cancer types, the Belgian Health Care Knowledge Centre5 found no conclusive evidence about the benefits of exercise treatment for qol. Fourteen systematic reviews621 found an improvement in qol for people with cancer participating in an exercise intervention during the active treatment or post-treatment periods (Table v). Of the sixteen rcts involving patients in active treatment2237, seven reported significant differences between the intervention and control groups (Table vi)23,24,26,3133,36. In the thirteen post-treatment intervention studies3853, two reported significant qol improvement in the exercise groups41,42. In particular, patients with lymphedema experienced qol benefits, and aerobic and resistance exercises were both safe for women who had undergone breast and axillary surgery6,7,38,39,44.

TABLE V Systematic review data





 

TABLE VI Randomized controlled trial data












 

All systematic reviews621,48,49 found positive changes in both muscular and aerobic fitness (Table v). Of the sixteen rcts that measured muscular or aerobic fitness or both22,23,27,28,30,32,33,37,38,40,41,4347, twelve found significant positive changes in the exercise groups (Table vi)22,23,27,28,30,32,37,38,41,43,44,46. One systematic review14 found substantial increases in muscular strength and endurance with resistance training for patients on androgen deprivation therapy (Table v).

Safety, Adverse Events, or Injuries

The safety of exercise for adults living with cancer is a very important outcome. Safety outcomes include measures such as the frequencies and types of adverse events during exercise sessions or whether treatment delivery or cancer-specific outcomes were negatively affected.

Two guidelines5,43 concluded that exercise is safe for people with cancer both during active treatment and after treatment. The Belgian Health Care Knowledge Centre5 developed recommendations concerning the efficacy and safety of exercise treatment during cancer treatment. Based on data about the safety of exercise from a systematic literature review, no harmful effects of exercise during treatment were found. Thus, it was concluded that exercise is safe for patients undergoing treatment for cancer. The American College of Sports Medicine43 convened an expert panel to create a roundtable consensus statement about exercise for cancer survivors. After reviewing the literature, the panel concluded that exercise training is safe during and after cancer treatments. They recommended that exercises could be specifically adapted based on disease-and treatment-related adverse effects such as lymphedema. They also developed pre-exercise medical assessments to help ensure safety and to guide exercise specialists concerning exercise programs for people living with cancer.

In the systematic reviews and rcts, very few adverse events were attributable to exercise; most studies reported no adverse events at all that were attributable to exercise (Tables v and vi). Of the systematic reviews, nine69,13,15,16,19,21 made no mention of adverse events, two10,48 indicated that no adverse events were reported in the studies, and six12,14,17,18,20,49 indicated that adverse events had been reported in studies, but did not provide information about the events. One systematic review20 found that cardiopulmonary exercise testing was a safe, noninvasive method to measure cardiopulmonary fitness in people living with cancer, both during and after treatment.

Seventeen rcts2224,27,29,3033,37,39,42,45,47,5153 found that no adverse events or side effects were attributable to the exercise program. Seven26,28,34,35,40,46,50 did not report on adverse events at all. Three rcts25,41,44 reported adverse events that were deemed not to be related to the intervention; two36,38 reported events that were attributable to the intervention (3 patients experienced muscle soreness, and 2 experienced musculoskeletal injury).

Delivery Models and Supervised Settings

Four systematic reviews8,11,15,49 detected a greater and more consistent benefit of exercise for qol and muscular and aerobic fitness when the intervention was offered in a group or supervised setting compared with a home-based or unsupervised setting (Table v). Two rcts32,36 compared various settings for interventions and found that the beneficial effects were greater when exercise was supervised, either in groups or by telephone. One rct40 found a significant linear trend between an increase in weekly metabolic equivalents of task performed and an improved qol score for all patients in the study.

Intensity Levels and Types of Exercise

Intensity Levels:

Three systematic reviews6,11,18 studied exercise intensity levels and found that studies of longer length (more weeks) and those that included at least moderate-intensity exercise were associated with improved qol and muscular and aerobic fitness (Table v). Another systematic review19 that evaluated interventions with positive results for qol found that moderate-intensity aerobic exercise programs used in those interventions resulted in a benefit for qol (Table v). Two rcts33,39 compared various exercise intensity levels and found improvements in muscular endurance and aerobic capacity for the higher-intensity groups (Table vi). One rct40 found, for all participants, a significant linear trend between an increase in weekly energy expenditure or metabolic equivalents of task performed and an improved qol score (Table vi).

Resistance Training:

Focht et al.12 analyzed only resistance exercise interventions used in fifteen studies in both active-and post-treatment patients, finding a small and meaningful increase in effect size for qol (Cohen d = 0.25; range: –0.72 to 1.14). In a systematic review, Cramer et al.10 examined resistance training in three studies with colorectal cancer patients, finding that resistance training improved colorectal cancer–specific qol. Strasser et al.48 looked at both active-and post-treatment groups in four rcts that compared a resistance training group with a non-exercise group and that measured qol (five other rcts examined muscle strength): two rcts detected a significant effect of resistance training for qol (compared with usual care), and two rcts detected a trend for improved qol in the resistance training group.

Five rcts22,31,39,42,45 used resistance training alone for their exercise intervention. Winters-Stone et al.22 and Lonbro et al.42 both found a significant difference in qol for the exercise group (p < 0.01 and p < 0.05 respectively). Rogers et al.31 found a positive minimally important difference effect size of d = 0.52 at 6 weeks and d = 0.39 at 12 weeks. Cormie et al.39,45 did not find a significant difference between groups for qol in both of their rcts (p = 0.195, p = 0.475).

Aerobic Training:

Ferrer et al.11 found that aerobic activity intensity was a significant predictor of qol improvement as a quadratic trend (bivariate moderator analyses: β = 0.25, p = 0.03). Four rcts26,35,46,47 used only aerobic interventions. Three26,46,47 showed no significant differences between the intervention and control groups for qol, but in one35, paired pre–post t-tests showed a significant difference between groups on the Short Form-36 mental component summary (p ≤ 0.05).

Resistance Versus Aerobic Training:

Santa Mina et al.29 compared aerobic and resistance training programs, both moderate-to-vigorous intensity and home-based. No difference in qol was found between the training groups.

Pre-exercise Assessment for Evaluation of the Effects of Disease Treatments or Comorbidities:

The American College of Sports Medicine’s guideline expert panel developed recommendations for pre-exercise medical assessments to help ensure patient safety and to guide exercise specialists with respect to an exercise program for people living with cancer43. One systematic review in the panel’s literature review20 found that cardiopulmonary exercise testing is a safe, noninvasive method for measuring the cardiopulmonary fitness of people living with cancer, both during and after treatment. No rct in the literature review reported any adverse events during pre-screening or baseline assessments before initiation of the study intervention2242,4447,5053.

DISCUSSION

Safety, QOL, and Muscular and Aerobic Capacity

Outcomes of importance to the current guideline included safety, qol, and aerobic and muscular fitness. Numerous studies provide evidence that supports an improvement in qol for patients participating in the interventions. The published guidelines concluded that exercise is safe for people with cancer. Exercise is beneficial for enhancing qol and aerobic and muscular fitness. As with any exercise intervention in an adult population, harm or adverse events can occur, but a cancer diagnosis or its therapy does not exert a negative influence.

Exercising in Group or Supervised Setting

Studies detected a greater and more consistent benefit when the intervention occurred in a group compared with a home (individual) setting. Several systematic reviews assessed the components that were included in successful interventions, concluding that the positive changes in group settings and supervised interventions are substantial.

Almost every intervention started in a supervised setting. A supervised setting can provide not only motivation for an individual to perform exercise, but might also allow for an educational component—especially for individuals receiving resistance-type interventions. Safety and exercise options would then both be optimized. Supervision can also allow individuals who might prefer to exercise outside a group setting to learn about their options and can ensure that exercise professionals have the opportunity to review and instruct people on how to safely perform or use a specific exercise modality.

Exercising at Moderate Intensity and Length of Intervention

No studies directly compared various intensities or lengths of exercise interventions for people with cancer. The systematic reviews detected a benefit for increasing intensities up to a moderate level (3–6 metabolic equivalents of task), but greater amounts of exercise did not necessarily further improve outcomes, including qol.

Longer interventions (18 weeks and ongoing) detected a benefit for qol as well as for aerobic and muscular fitness. Compared with high intensities, moderate intensities of exercise might be sustainable for a longer period and might encourage exercise to be continued throughout a person’s life.

The rcts were not conducted for a period adequate to study the long-term effects of exercise. Study lengths were associated with the funding and time available to complete the study rather than with the feasibility or sustainability of an exercise regimen.

Pre-exercise Assessment for Evaluation of Effects of Disease Treatments or Comorbidities

It is a standard recommendation that healthy adults in the general population undergo a fitness assessment before initiating exercise; people living with cancer should therefore also participate in a pre-exercise fitness assessment. The assessment should evaluate comorbidities and any possible latent effects from treatment that might alter a person’s ability to safely engage in exercise. Such an assessment also allows the exercise consultant to modify an exercise program, individualizing it for the person and giving consideration to modifications of standard programs based on physical limitations or vulnerabilities.

The time and personnel required to perform a pre-exercise assessment are acknowledged. However, such assessments can allow clinicians and people living with cancer to feel more safe and secure before an exercise regimen commences. Assessments can also ensure that individuals are aware of potential vulnerabilities connected to their condition.

Implementation Considerations

Some of the issues identified here include concerns about the lack of exercise knowledge, funding, facilities, programs, qualified staff, and exercise specialists in cancer. Clinicians or health care professionals might be inexperienced with exercise regimens, and pre-exercise screening for all cancer survivors could be difficult to achieve, given the additional time and personnel requirements. The type of activity and exercise will depend on the individual patient and his or her preferences, and the choice should be promoted as a part of rehabilitative recovery or the survivorship phase of a treatment program.

Evidence Limitations

The present systematic review was conducted to provide a background and guidance for clinicians with respect to exercise for people living with cancer. It focuses on the benefits of specific types of exercise, pre-screening requirements for new referrals, safety concerns, and delivery models. It covers all cancer types; aerobic and resistance exercise; and qol, muscular, and aerobic outcomes. Other reviews were more specialized in their objectives. Unfortunately, evidence to create specific exercise regimens for specific types of cancer was not available to provide guidance for clinicians. In addition, evidence that met the inclusion criteria was insufficient to produce recommendations based on survival outcomes.

The evidence found in this review showed some weak-nesses. A systematic review was not undertaken to inform the guideline from the American College of Sports Medicine; that guideline depended on expert opinion for some topics (such as the pre-screening recommendation). Many of the systematic reviews had issues with heterogeneity in their analysis. Sources of heterogeneity included a population with varying cancer types; varied timing of the exercise intervention (during or after completion of therapy); varying interventions (aerobic compared with resistance training); various lengths of intervention (4–24 weeks); variable exercise intensities; varying frequencies of the intervention (daily to 2, 3, or 5 times per week); multiple measures of qol, aerobic capacity, and strength; varying use of individual or group sessions; and variable timing of the assessments.

The risk of bias in lifestyle trials is an acknowledged issue. Within the rcts reviewed, the following concerns were noted: participants could not be blinded; some assessments (especially qol) were subjective; many trials had performance bias; many trials did not measure exercise activity before entry into the study; adherence during the intervention was variable or not reported; and the exercise level of the control group quite often increased during the intervention, sometimes as much as it did in the exercise group. The lengths of the rcts were not sufficient to fully study a long-term exercise duration. The study lengths were connected to the money and time needed to complete a study rather than to the feasibility or sustainability of the exercise regimen.

CONCLUSIONS

Exercise is safe and can provide qol and fitness benefits for adults living with cancer, whether during active treatment or after treatment. During active treatment, systematic reviews examining patients with all cancers demonstrated a positive influence of exercise on qol. In rcts, benefits within and between groups were found for exercise interventions of moderate intensity. For the post-treatment period, systematic reviews found a positive influence for all exercise interventions. Thus, people living with cancer can be allowed to determine the type of exercise that they would prefer to do for aerobic and resistance training (for example, running, brisk walking, cycling, weight lifting, body weight or elastic band exercises), with similar benefits.

So far, studies have not been designed to determine more exact exercise programs for specific cancer types. Studies with a longer duration are also needed to determine the long-term effects of exercise, as are studies that compare various exercise intensities to determine any difference in benefit. In the present review, evidence that met the inclusion criteria was insufficient to provide recommendations based on survival outcomes. However, sufficient evidence is available to promote exercise to adults with cancer, and some evidence is available to promote exercise in a group or supervised setting and for a long period of time to improve qol and muscular and aerobic fitness. Exercise at a moderate intensity might be sustainable for longer periods and could potentially encourage continuation over a lifetime. It is important that a pre-screening assessment be conducted to evaluate for the effects of disease, treatments, or comorbidities. More research to help create more exact exercise programs for specific cancer types would be beneficial.

REVIEW AND UPDATE

Practice guidelines and literature reviews developed by the pebc are reviewed and updated regularly. For the full guideline and subsequent updates, please visit the Cancer Care Ontario Web site at https://www.cancercare.on.ca/toolbox/qualityguidelines/clin-program/psychonc/.

ACKNOWLEDGMENTS

The authors thank the members of the Exercise for People with Cancer Guideline Development Group for their contributions to the development of this practice guideline. The pebc is a provincial initiative of Cancer Care Ontario supported by the Ontario Ministry of Health and Long-Term Care (mohltc). All work produced by the pebc is editorially independent from the mohltc.

CONFLICT OF INTEREST DISCLOSURES

We have read and understood Current Oncology’s policy on disclosing conflicts of interest, and we declare that we have none.

AUTHOR AFFILIATIONS

*Medical Oncology, The Ottawa Hospital, Ottawa;,
McMaster University, Hamilton;,
Canadian Partnership Against Cancer, Toronto;,
§Queen’s University, Kingston;,
Odette Cancer Research Program, Sunnybrook Hospital, Toronto; and,
#Sunnybrook Hospital, Toronto, ON..

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Correspondence to: Caroline Zwaal, Program in Evidence-Based Care, Juravinski Hospital, 711 Concession Street, Hamilton, Ontario L8V 1C3. E-mail: zwaalc@mcmaster.ca

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Current Oncology, VOLUME 24, NUMBER 4, August 2017








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ISSN: 1198-0052 (Print) ISSN: 1718-7729 (Online)