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An Executive Summary of Reports From an International Multidisciplinary Roundtable on Exercise and Cancer

Evidence, Guidelines, and Implementation

Campbell, Kristin L. PT, PhD1; Winters-Stone, Kerri M. PhD2; Patel, Alpa V. PhD3; Gerber, Lynn H. MD4,5; Matthews, Charles E. PhD6,*; May, Anne M. PT, PhD7; Stuiver, Martijn M. PT, PhD8,9,10; Stout, Nicole L. DPT11,*; Schmitz, Kathryn H. PhD12; Morris, G. Stephen PT, PhD13

doi: 10.1097/01.REO.0000000000000186
CPG SUMMARY
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Physical activity can play an important role in cancer prevention and control, but there is a need to update the state of the science to best facilitate dissemination and implementation of evidence into practice. The American College of Sports Medicine convened an International Multidisciplinary Roundtable on Exercise and Cancer to update recommendations based on current evidence on the role of physical activity and exercise in cancer prevention and survivorship. There was strong evidence for a protective effect of physical activity against colon, breast, endometrial, kidney, bladder, esophagus, and stomach cancer; moderate evidence that pre-diagnosis physical activity may reduce risk of dying from breast and colon cancer; and, moderate evidence that higher levels of physical activity post-diagnosis are associated with lower risk of dying from colon, breast, and prostate cancer. For cancer survivors, an exercise prescription for moderate intensity aerobic and/or resistance exercise at least 3 times per week, 30 minutes/sessions, for at least 8-12 weeks may consistently improve common treatment-related symptoms and side effects. To implement this knowledge, an Exercise Is Medicine approach was adapted to the cancer context. Oncology clinicians are asked to: 1) assess current physical activity levels and safety to engage in exercise, 2) advise patients to increase physical activity if not currently reaching recommended levels, and 3) refer individuals to appropriate services. Exercise can play a vital role in prevention and management of cancer. The Roundtable update provides physical therapists with practical, evidence-based information for utilization of exercise as a treatment strategy and models for implementation.

1Department of Physical Therapy, Faculty of Medicine, University of British Columbia, Vancouver, Canada

2School of Nursing and Knight Cancer Institute, Oregon Health Sciences University, Portland, OR

3Behavioral and Epidemiology Research, American Cancer Society, Atlanta, GA

4Department of Medicine, Inova Fairfax Medical Campus, Falls Church, VA

5Center for the Study of Chronic Illness and Disability, George Mason University, Fairfax, VA

6Metabolic Epidemiology Branch, Division of Cancer Epidemiology and Genetics, National Cancer Institute, Rockville, MD*

7Julius Center for Health Sciences and Primary Care, University Medical Center Utrecht, Utrecht University, Utrecht, the Netherlands

8Center for Quality of Life, Netherlands Cancer Institute, Amsterdam, the Netherlands

9ACHIEVE, Faculty of Health, Amsterdam University of Applied Sciences, Amsterdam, the Netherlands

10Department of Clinical Epidemiology, Biostatistics and Bioinformatics, Amsterdam University Medical Center, University of Amsterdam, Amsterdam, the Netherlands

11Office of Strategic Research, Rehabilitation Medicine Department, National Institutes of Health, Bethesda, MD*

12Public Health Science, Penn State Cancer Institute, Penn State College of Medicine, Hershey, PA

13Department of Physical Therapy, Wingate University, Wingate, NC

Correspondence: Kerri M. Winters-Stone, PhD, School of Nursing and Knight Cancer Institute, Oregon Health Sciences University, Portland, OR 97239 (wintersk@ohsu.edu).

*Note for Nicole L. Stout and Charles E. Matthews: The opinions are the authors' own and do not reflect the official positions of the National Institutes of Health, the Department of Health and Human Services, nor the US government.

The authors declare no conflicts of interest.

Worldwide 18.1 million individuals will be diagnosed with cancer in 2018 and 9.6 million individuals will die from the disease—making cancer the second leading cause of mortality.1 There is a great need to understand how modifiable health behaviors like physical activity may help prevent and control cancer in the population. Furthermore, there are now more than 16.9 million cancer survivors in the United States—a figure that is expected to double by 2040.2 Improved prognosis has created a growing need to address the unique health issues facing cancer survivors that result from the disease, its treatment, and related comorbid conditions. The prevalence of cancer-related impairments and the underutilization of rehabilitation services, which have been shown to be efficacious, have been well documented.3,4 In addition, almost half of cancer survivors are older than 70 years, resulting in adverse synergistic effects of age, cancer treatment, and related sequelae, which increase the total burden of cancer-related morbidity for these cancer survivors.5

The American College of Sports Medicine (ACSM) convened an International Multidisciplinary Roundtable on Exercise and Cancer in March 2018 to bring together a group of exercise and rehabilitation professionals representing multiple disciplines, as well as key professional and stakeholder organizations, with the goal to update recommendations based on current evidence around the role of physical activity and exercise in cancer prevention and survivorship. Roundtable participants were charged with reviewing the state of the science, determining the goals of the Roundtable, and contributing to corresponding products. The Academy of Oncologic Physical Therapy of the APTA and the APTA were 2 of 19 organizations that supported the Roundtable meeting and sent a representative to attend the in-person meeting (Table 1).

TABLE 1

TABLE 1

The Roundtable focused on 3 specific goals: (1) evaluating and summarizing evidence for the role of exercise and activity in reducing risk of developing cancer and for improving survival after diagnosis of cancer; (2) reviewing the efficacy of exercise to improve cancer-related health outcomes (acute, late, and long-term effects) to inform evidence-based exercise prescriptions for cancer survivors; and (3) translating evidence into the clinical and community settings and providing recommendations for practice implementation in oncology. The outcome of the work done in achieving these goals resulted in 3 more detailed and separate publications, 2 of which were clinical practice recommendations.6–8 The 3 manuscripts were reviewed by the participating organizations prior to submission for publication to obtain their official endorsement, if applicable (Table 1). The purpose of this executive summary is to briefly describe the major findings of the 3 manuscripts resulting from the Roundtable and to then provide specific recommendations on how they may impact physical therapy practice.

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THE ROLE OF EXERCISE IN CANCER PREVENTION AND CONTROL

Published in the journal Medicine & Science in Sports & Exercise, this article reviewed the biologic and epidemiologic evidence for an association between physical activity and cancer risk and cancer survival.6 Evidence that physical activity may play an important role in cancer prevention and control has grown rapidly over the past decade. The review of evidence for cancer prevention included evaluation of existing systematic and meta-analysis reviews9–24 and a large pooled analysis of 1.44 million participants.25 The Roundtable review for cancer prevention was undertaken concurrently with other large review efforts by the Physical Activity Guidelines Advisory Committee (PAGAC)26 and the World Cancer Research Fund and summary results were reported considering whether or not there was agreement from the Roundtable with the conclusions of these review efforts. To derive conclusions for cancer survival, the Roundtable reviewed observational studies of pre- and postdiagnosis physical activity, as well as results from randomized controlled trials (RCTs) of exercise interventions conducted in cancer survivors and reached agreement on the level of evidence by consensus.

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Physical Activity and Risk of Developing Cancer

The Roundtable members concurred with the PAGAC for types of cancer with strong evidence for a protective effect of physical activity, including colon, breast, endometrial, kidney, bladder, esophagus (adenocarcinoma), stomach (cardia), a finding or moderate evidence for lung cancer, with strong potential for confounding by smoking, and limited evidence for a protective association for myeloma, hematological, head and neck, pancreas, prostate, and ovarian cancer (Table 2). The current evidence supporting biological mechanisms linking higher physical activity to lower risk for many cancers was also reviewed.

TABLE 2

TABLE 2

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Potential Impact of Type, Amount, or Intensity of Physical Activity and Cancer Prevention

The type, amount, and intensity of physical activity associated with lower risk were examined for cancers, with strong evidence that higher levels of physical activity are associated with lower risk. The number of studies available differed by cancer site, dimensions of physical activity examined (eg, leisure time and occupational). For type of activity, results were strongest for leisure-time and occupational physical activity, but different patterns of activity accumulation in these 2 domains of physical activity suggest that a broad range of activity types may confer a lower risk of some cancers, although more definitive evidence is needed. For intensity, the best available evidence from studies of leisure-time physical activity indicates that moderate- to vigorous-intensity physical activity is associated with reduced risk of many types of cancer, while evidence showing benefit individually for light, moderate, and vigorous-intensity activity is more limited. For the “amount” or total volume of physical activity (ie, metabolic equivalent hours/week), it was not possible to determine the minimum amount of leisure-time physical activity associated with lower risk of cancer, or to reliably characterize the shape of the dose-response curve due to wide variation in study methods used. In the absence of available evidence, the current physical activity guidelines of 150 to 300 minutes/week of moderate or an equivalent amount of vigorous-intensity aerobic activity (75-150 minutes/week) are recommended. Future research should consider these methodological gaps so that a more precise dose of exercise can be recommended.

The Roundtable members also considered the emerging evidence for the role of sedentary time on risk of developing cancer. Although the number of studies of this modifiable risk factor is much less than that for physical activity, a moderate level of evidence suggests that higher levels of daily sitting time and/or television viewing time are associated with increased risk of colon, endometrial, and lung cancer (Table 2).

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Effects of Physical Activity After a Cancer Diagnosis Impact All-Cause Mortality and Cancer-Specific Mortality

In the last decade an increasing number of studies have examined whether exercise prior to or after a cancer diagnosis is associated with improved cancer-specific survival among those diagnosed with colon, breast, and prostate cancer. A moderate level of evidence shows that prediagnosis physical activity may reduce risk of dying from breast and colon cancer among those diagnosed with these malignancies. Similarly, there is a moderate level of evidence showing that engaging in higher levels of physical activity before diagnosis is associated with lower risk of dying from colon, breast, and prostate cancer among these survivor populations. However, the exact dose of physical activity needed to reduce cancer-specific or all-cause mortality is not yet known since too few studies have been conducted that have sufficient data to determine the risk associations for specific doses of activity. There is also emerging evidence from exploratory analyses of 5 RCTs of exercise during and following cancer treatment on all-cause and cancer-specific mortality that are consistent with the observational studies of breast cancer. However, the original studies were not powered to test these hypotheses and will need to be interpreted accordingly. Clearly, more research is needed to provide a more granular and evidence-based recommendation on the type and amount of physical activity that improves cancer survival.

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THE EFFICACY OF EXERCISE TO IMPROVE CANCER-RELATED HEALTH OUTCOMES AND UPDATED EXERCISE GUIDELINES

Published in the journal Medicine & Science in Sports & Exercise, this article updated the evidence-based guidelines for exercise testing, prescription, and delivery in cancer survivors.7

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Efficacious Exercise Prescription

The exercise recommendations for cancer survivors published in 2010 were consistent with broader US public health activity guidelines.28 It was recognized, though, that this level of physical activity might be unachievable for all cancer survivors and that benefits may still be achieved from less exercise. Therefore, a goal of the 2018 Roundtable was to review the updated exercise literature to develop evidence-informed exercise prescriptions for positively impacting distinct cancer-related health outcomes (Table 3). To efficiently evaluate and provide a rich synthesis of the evidence, a review of published RCTs, systematic reviews, and meta-analyses for cancer-related health outcomes was conducted. For each outcome, the most recent, relevant, and high-quality publications that could facilitate evaluation of the state of science around efficacy of exercise for a particular outcome were reviewed by 2 team members. If no systematic reviews and meta-analyses were identified, the available RCTs were reviewed. Using a decision framework adapted from the Dutch Physical Activity Guidelines29 to determine strength of evidence, outcomes deemed to have strong evidence were considered sufficient to warrant an exercise prescription, while outcomes with moderate evidence received an emerging prescription that might change with future research (Table 3).

TABLE 3

TABLE 3

An efficacious exercise prescription that most consistently addresses health-related outcomes experienced due to a cancer diagnosis and cancer treatment includes moderate-intensity aerobic and/or resistance training at least 3 times per week, for at least 30 minutes, for at least 8 to 12 weeks. However, evidence is either insufficient or suggestive that resistance training alone may not be enough to reduce anxiety and depressive symptoms. Current evidence supports a greater effect for supervised exercise than unsupervised exercise on cancer-related health outcomes, although the reasons for these differences are debatable since it is not clear whether or not a higher dose of exercise may be better achieved with supervised training or from other attributes of this setting (ie, more attention, motivation, reinforcement, and selection bias). More research is needed to provide further detailed prescriptions according to cancer type, timing of treatment, and/or types of treatment.

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Key Elements for Delivery of Safe and Efficacious Exercise Programming

To best evaluate a cancer survivor's exercise tolerance and prescribe a safe and effective exercise program, it is necessary for the fitness professionals and rehabilitation specialists to:

  • Know about the type and extent (ie, stage) of cancer a person or has had.
  • Be familiar with the common treatment approaches to cancer, the side effects and symptoms these treatments can cause, and their subsequent impact on exercise tolerance.
  • Be prepared to create exercise programs that are feasible and help reach an individual's goals, taking into account exercise preferences.
  • Be aware of and respectful of the fact that individuals diagnosed with cancer frequently have many added concerns, such as life expectancy, employment and financial issues, and family matters that may limit prioritization of exercise in their lives.
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Approach to Medical Evaluation

The question of whether or not cancer survivors require a medical evaluation or medical clearance (eg, approval from a medical professional to engage in exercise) prior to starting an exercise program continues to evolve. Recently, the ACSM updated its preparticipation exercise guidelines for all persons, removing an earlier guideline that required medical clearance for individuals whose risk of an adverse cardiac event during exercise was low.30 The new recommendation includes exercise-naïve persons and was made in an attempt to reduce a recognized barrier to exercise prescription and participation. However, the ACSM preparticipation guidelines do not explicitly address risks for adverse events and/or injury during exercise that are specific to the common adverse effects of cancer treatment. The 2019 ACSM Guidelines adapted the National Comprehensive Cancer Network (NCCN) Survivorship Guidelines31 to provide guidance around safety concerns predicated on the disease and treatment-related side effects (Table 4).

TABLE 4

TABLE 4

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Approach to Exercise Testing

While it may be ideal for cancer survivors to undergo a comprehensive assessment of all components of health-related physical fitness (ie, cardiorespiratory fitness, muscle strength and endurance, body composition, and flexibility), requiring a comprehensive physical fitness assessment prior to starting an exercise program may create an unnecessary barrier to an individual starting to engage in physical activity. The following recommendations regarding preexercise assessments were made:

  • No assessments are required to start low-intensity aerobic training (ie, walking or cycling), resistance training with gradual progression, or a flexibility program in most survivors.
  • Medical evaluation clearance may still be indicated as previously described depending on the exercise and health history of an individual and presence of cardiovascular, pulmonary, renal, or metabolic symptoms.
  • For additional cancer-specific guidance for exercise testing, health professionals are referred to the original article for details.
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TRANSLATION OF EVIDENCE INTO THE CLINICAL AND COMMUNITY SETTINGS

This article, published in the journal CA: A Cancer Journal for Clinicians, identifies and uses elements from ACSM's Exercise Is Medicine (EIM) initiative to propose solutions to overcoming key barriers identified to moving the research evidence into practice.8 The authors of this article, which were a subset of participants from the Roundtable, used the EIM initiative and current evidence to develop a framework that would assist referring physicians in identifying patient needs for exercise and provide an approach to facilitate exercise referrals.

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Ask Oncology Clinicians to Assess, Advise, and Refer

The EIM approach considers the assessment of physical activity as a vital sign. The ACSM Roundtable Team adapted this approach to the cancer context. Using this approach, oncology clinicians are asked to follow a 3-step process to (1) assess, (2) advise, and (3) refer (Figure). In step 1, clinicians are asked to assess current physical activity levels and safety of patients to engage in exercise, using three standard questions. In step 2, clinicians can advise patients to increase physical activity if they are not currently reaching recommended activity levels (ie, ≥3 days per week of aerobic activity or ≥2 days per week of resistance activity) or encourage maintenance of activity in those meeting recommended levels. In step 3, clinicians can refer individuals to the appropriate services to increase or assistance with maintenance of current physical activity levels or for additional assessment to determine the appropriate setting for a client to safely engage in exercise.

Fig

Fig

Clinicians are also asked to follow up with assessment of progress (or lack thereof) at subsequent visits, which can serve as key transition points to change patients' behavior and impact their tolerance of or recovery from treatment. One key point to clarify is that all members of the oncology care team (ie, physicians, nurses, or other allied health providers) are not expected to give specifics of exercise prescriptions (eg, prescribe specific resistance training exercises, equipment, or progression of weights) or to do extensive screening and triaging to determine whether exercise needs to be done in a rehabilitative versus community setting as making such determinations are the role of health care providers (HCPs) for whom exercise and rehabilitation is their primary scope of practice (ie, physical and occupational therapists, physiatrists, and exercise professionals). All members of the oncology care team, however, play a vital role in telling the patient that it is important to exercise and pointing patients in the right direction to make that happen.

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Delineation of Types of Programming Available to Provide Exercise Programming for Cancer Survivors

The setting to which cancer survivors are referred may depend based on their medical complexity and the ability of the patients to self-manage their condition. Two distinct settings were outlined: (1) HCP-supervised exercise programs, at inpatient or outpatient ambulatory centers, in public and private practice, which are overseen by licensed health care providers, and (2) community or home-based settings, with specific local structured exercise programs in community or home settings in which individuals with cancer can participate. Individuals could be referred to either and move between the settings as dictated by their medical status. The ACSM registry of exercise programs for patients with cancer can help providers find programs that would be feasible, safe, and appropriate for patients (https://www.exerciseismedicine.org/movethruca). In an ideal scenario, a multidisciplinary team would work alongside oncology clinicians, assessing, triaging, and referring patients to appropriate exercise programming. Until such a system becomes commonplace, there is a need for simple systems, which facilitate referrals to the appropriate health care provider for further assessment and triage, much like what currently happens with psychosocial distress assessment and referrals. Further, it was highlighted that the availability of HCP-supervised exercise programs may be limited by workforce challenges and further workforce capacity building is needed. Using telemedicine or other distance-based approaches may help when HCP supervision is needed, but local programs do not exist.

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Key Considerations for Successful Behavior Change

Exercise is only effective in improving clinical outcomes if the patient “fills the script” (does the exercise program). Changing behavior is complex and depends on personal, social, and environmental factors, as well as individual and community resources. This article on translating evidence to practice reviewed the research evidence to provide recommendations around key considerations to successful behavior change and how these factors could be embedded in programming. A referral to an appropriate exercise specialist is important. The exercise specialist can assess these important factors and guide the patients to a program that best fits their needs and preferences so as to facilitate exercise adoption and reduce the time burden on the medical professional (eg, oncologist). The article also highlighted an update of a 2013 Cochrane review (23 studies, a total of 1372 patients treated for breast, prostate, colorectal, and lung cancer), which showed that programs with the best adherence to exercise guidelines used techniques of goal setting, setting graded exercise tasks and instructions on how to exercise.32 A synthesis of exercise programs that examined exercise maintenance (exercise assessed at least 3 months postprogram completion) reported that graded tasks, social support, and action planning were used in studies sustaining significant behavior change.33

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Exercise Is Medicine in Oncology: A Call to Action

Overcoming the above-noted barriers and making exercise assessment, advice, and referral a standard practice within clinical oncology will require action from multiple stakeholders:

  • Oncology care team clinicians and primary care providers. Assess physical activity for all patients at regular intervals, continuously along the cancer continuum; advise patients to move more and sit less; refer to local health care provider supervised and community or home programs as appropriate.
  • Policy makers. Develop policies, programs, and initiatives that facilitate the translation and funding (reimbursement) for implementation of clinical and community exercise programming across all cancer diagnoses and at all points on the cancer continuum. A drug with a similar benefit profile would likely be prescribed broadly.
  • Researchers. Adapt effective interventions for community and home-based settings. Conduct implementation science and health services research on clinical and community exercise during and after active cancer care to drive improvements in infrastructure, reimbursement, and other policies that will make exercise standard practice in oncology.
  • Clinical educators. Expand physical activity education in the training of all health care providers and social workers who are or will be a part of the oncology workforce. Develop the workforce for clinical and community exercise practitioners in oncology.
  • Rehabilitation and exercise health care providers (physical therapists and clinical exercise professionals). Seek additional training to meet the unique needs of patients with cancer and survivors. Demand new curriculum development to meet this unmet educational need.
  • Mainstream health and fitness industry. While LIVESTRONG at the YMCA (https://www.livestrong.org/ymca) and the MoveMore program (https://www.macmillan.org.uk/about-us/health-professionals/programmes-and-services/move-more-scotland.html#316048) provide successful models, by providing high-quality programming to a large number of cancer survivors worldwide. Expansion and support of these and similar programs could benefit industry, patients with cancer and survivors, as well as oncology clinicians.
  • Oncology patients and survivors. Oncology patients and survivors have a powerful voice in shaping oncology care. If patient advocates spoke with one voice about asking for exercise assessment, advice, and referral to be standard practice, it would facilitate forward motion toward this goal.
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CLINICAL SUMMARY

The triad of manuscripts emerging from 2018 International Multidisciplinary Roundtable on Exercise and Cancer represents a tremendous amount of thought and reflection on the part a large number of researchers and clinicians. Almost every sentence in these manuscripts provides the clinician with new insights and perspectives. Reducing this body of work to a clinical summary of this substantive work on “exercise oncology” is a daunting task, but doing so in the context of the broader field of physical therapy reveals 5 take-home messages.

First, given the poor exercise behaviors of the American public and the burgeoning number of cancer survivors, the findings that exercise training offers reductions in risk of developing or experiencing a recurrence of cancer impact virtually every physical therapist (PT) and physical therapist assistant (PTA) in this country. Screening all patients for their exercise behaviors and then acting appropriately on those findings as described in the last paper in this series could profoundly affect not only the incidence of cancer and cancer recurrence in this country but also the incidence of other chronic diseases known to be linked to poor exercise behaviors.

Second, patients with cancer can be complex patients. This work provides evidence-based exercise prescriptions that are safe and effective in positively impacting cancer-related health outcomes, including physical function. These guidelines should help allay fears clinicians have in using exercise interventions for their patients with a cancer history. Importantly, these guidelines are not intended to be a substitute for using good clinical judgment but rather as an adjunct to good clinical judgment. The pace and focus of exercise oncology research and increased rigor required in reporting the intervention details of exercise studies suggest that these guidelines will rapidly expand, providing greater precision and applicability of such exercise oncology guidelines.

Third, delivery of safe, effective, and affordable health care, including physical therapy services, is of ever increasing interest and concern. This work addresses programs in both clinical and community settings that have successfully delivered exercise oncology services to cancer survivors. For therapists interested in adding exercise oncology services to their practice or practice setting, the current work describes delivery care models that have done so in several different settings. Further, this work suggests that the EIM initiative provides a way of bringing exercise into the oncology setting. Similar to the guidelines, this work provides practical support and ideas for clinicians to pursue in their efforts to utilize exercise as a safe and effective therapeutic intervention.

Fourth, cancer survivors vary widely in their medical acuity and complexity, ranging from being fundamentally healthy to having serious comorbidities arising from their disease and/or its treatment. Furthermore, their acuity and complexity can vary widely, as they move along the trajectory of their disease. The current work reminds us that PTs and PTAs are not always required or are the most effective in delivering exercise services to the cancer survivor. Optimal care to this patient population is provided by an oncology care team, which can effectively address the many medical needs of these patients. Working in the context of such a team helps to insure that physical therapy services are provided to the appropriate patients when they are most needed. For those noncomplex patients requiring reconditioning, athletic trainers or certified exercise trainers may be the most appropriate team member to provide those services. For those patients requiring reconditioning services in the context of comorbidities, PTs and PTAs may be the most appropriate.

Lastly, while PTs and PTAs are very much interested in the physiologic improvements brought about by exercise, these rehabilitation professionals are more interested in the impact of these physiologic changes on the physical function of their patients. Sufficient evidence is now available to support the Roundtable's conclusion that moderate-intensity aerobic training, resistance training, or a combination of the 2, performed 3 times weekly for 8 to 12 weeks, can significantly improve self-reported physical function. Greater improvements can be seen if the exercise training component of the intervention is supervised. This conclusion gives therapists a stronger rationale for linking improvements in physical fitness (strength, endurance) to improvements in physical function, justifying the inclusion of exercise training in a treatment plan to patients, administrators, and third-party payers.

In conclusion, the collective work of the Roundtable provides clinicians with a great deal of practical information regarding the utilization of exercise as interventional treatment strategies and models that can help in implementing those services. Much work remains to be done in the area of exercise oncology, but if the rate of progress continues as it has over the past decade, the clinician can expect continued expansion of evidence-based exercise interventions to use with their cancer survivors.

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    Keywords:

    neoplasm; cancer prevention; survivorship; physical activity; rehabilitation

    Copyright 2019 © Academy of Oncology Physical Therapy, APTA