Exercise in clinical cancer care : a call to action and program development description

s?&vmview=abst_detail_view&confID=55&abstract ID=33601; cited April 6, 2012] 73. Joly F, Alibhai SM, Galica J, et al. Impact of androgen deprivation therapy on physical and cognitive function, as well as quality of life of patients with nonmetastatic prostate cancer. J Urol 2006;176:2443–7. 74. Hsing AW, Sakoda LC, Chua S Jr. Obesity, metabolic syndrome, and prostate cancer. Am J Clin Nutr 2007;86:s843–57. 75. Freedland SJ, Platz EA. Obesity and prostate cancer: making sense out of apparently conflicting data. Epidemiol Rev 2007;29:88–97. 76. Galvão DA, Nosaka K, Taaffe DR, et al. Resistance training and reduction of treatment side effects in prostate cancer patients. Med Sci Sports Exerc 2006;38:2045–52. 77. Galvão DA, Taaffe DR, Spry N, Joseph D, Newton RU. Combined resistance and aerobic exercise program reverses muscle loss in men undergoing androgen suppression therapy for prostate cancer without bone metastases: a randomized controlled trial. J Clin Oncol 2010;28:340–7. 78. Yellen SB, Cella DF, Webster K, Blendowski C, Kaplan E. Measuring fatigue and other anemia-related symptoms with the Functional Assessment of Cancer Therapy (fact) measurement system. J Pain Symptom Manage 1997;13:63–74. 79. Cella DF, Tulsky DS, Gray G, et al. The Functional Assessment of Cancer Therapy scale: development and validation of the general measure. J Clin Oncol 1993;11:570–9. 80. Courneya KS, Friedenreich CM, Quinney HA, Fields AL, Jones LW, Fairey AS. A randomized trial of exercise and quality of life in colorectal cancer survivors. Eur J Cancer Care (Engl) 2003;12:347–57. 81. Vallance JK, Courneya KS, Plotnikoff RC, Yasui Y, Mackey JR. Randomized controlled trial of the effects of print materials and step pedometers on physical activity and quality of life in breast cancer survivors. J Clin Oncol 2007;25:2352–9. 82. Demark–Wahnefried W. Print-to-practice: designing tailored print materials to improve cancer survivors’ dietary and exercise practices in the fresh start trial. Nutr Today

Responding to overwhelming scientific literature that describes the benefits of exercise for cancer survivors, evidence-based exercise guidelines were created for cancer prevention and for the treatment and post-treatment periods [47][48][49] .To implement those guidelines, clinical and academic organizations developed certification courses to train exercise professionals in the safe and effective training of cancer survivors (for example, http://www.unco.edu/rmcri/, http://certification.acsm.org/acsm-cancer-exercisetrainer).Unfortunately, the aggregate effect of clinical guidelines, qualified personnel, and research about the demands and preferences of cancer survivors for exercise programming has not been sufficient to yield widespread implementation.Thus, there appears to be a gap in translating knowledge about exercise and cancer research into practice in tertiary-care centres, and subsequently, lost patient benefit.
The slow maturation process from exercise research to clinically integrated cancer programming is similar to that experienced in cardiac rehabilitation.Despite initial resistance to the integration of exercise into coronary intervention, compelling evidence about the benefits of early postoperative exercise and the detriment of physical inactivity stimulated a paradigm shift in cardiac care 50 .An exercise-oriented approach to cardiac rehabilitation was implemented in the 1960s and has since become essential to post-treatment care [50][51][52][53] .Accordingly, cardiac rehabilitation specialists are now important allied health professionals in this field.A half century later, cancer exercise researchers and clinicians have compiled a body of empirical evidence and experience comparable to that achieved by the cardiac group and are now at the cusp of an integrated model.However, challenges to knowledge translation in this field persist and require strategic approaches to ensure that the benefits of exercise are more widely available to cancer survivors.Reasons for poor knowledge translation include • an impression among clinicians that exercise may increase the risk of injury, fatigue, and exacerbation of symptoms in the patient [54][55][56] .• overwhelmed and financially drained clinical programs.• physical space restrictions.
• overall lack of clinicians with relevant exercise and clinical education and experience.• lack of discussion between patient and physician about exercise 57 .
Despite obstacles to implementation, evidence from more than eighty controlled exercise trials demonstrates that the oncologic community must strive to include exercise in cancer care.The question of a benefit of exercise for cancer patients no longer predominates the literature; researchers are now examining the most beneficial types and delivery methods of exercise interventions (for example, Segal et al. and Newton et al. 58,59 ).At this stage of empirical maturity, it is the responsibility of oncology programs to start delivering exercise programming for cancer patients.In the sections that follow, we describe our exercise intervention and integration strategy, and we offer insights about the facilitators and barriers to exercise program implementation within oncology.

Guiding Principles
The mandate of the Survivorship Exercise Program (sep) is to improve the physical and psychosocial wellbeing of cancer survivors during and after cancer treatment through structured exercise.Linked with that mandate is the advancement of cancer and exercise research by systematic collection and analysis of participant outcomes, allowing for the most efficient use of clinical and research resources in the service of patient care.Finally, the program seeks to increase the number of experienced and qualified exercise physiologists and clinical researchers within exercise and cancer by providing meaningful learning opportunities to students interested in exercise and oncology.

Personnel and Staffing
The sep is a multidisciplinary program that includes exercise physiologists, physicians, clinical psychologists, researchers, nurses, and student interns.
The organizational structure starts with a medical director who oversees the health of the patients and a program director who manages the clinical and research agendas.Exercise programming is provided by certified exercise physiologists with oncologyspecific education and training-a preference identified by many patients 31,40,41,43,44,54 62 .Moreover, the convenience of exercise has been the root of preference on the part of many cancer survivors for homebased exercise 34,35,[41][42][43] .Because concerns about patient adherence to home-based exercise prescription in the absence of direct supervision are valid, the sep has implemented adherence-boosting strategies that are further discussed later in this article.

Institutional Support and Funding
Collegial support from the medical and patient support and education departments has been vital to the initiation, maintenance, and advancement of the sep.To facilitate that support, staff must be educated about the benefits of exercise and informed of new services that will support clinical care and improve the experience and health outcomes of cancer patients.The sep generated institutional support through interprofessional workshops and presentations at clinical rounds and departmental meetings.
Partial funding for the sep is provided by the hospital foundation and by fundraising initiatives that have financed basic overhead costs and pilot research projects.Pilot data from a small study funded by the hospital foundation formed the basis for national and international peer-reviewed research grant submissions.A cost-recovery model was also implemented to cover ongoing expenses associated with program delivery.The cost-recovery model includes donations from participants.The participants have generously supported the sep and have viewed the donation as nominal compared with the equipment (exercise bands, a stability ball, and a yoga mat) and services received in the sep.It should be noted that participants are not obligated to contribute any money and that they receive the exercise program and associated materials regardless of their donations.

Referrals and Assessments
The sep accepts ambulatory cancer patients undergoing any type of treatment.Participants may be self-referred or referred by in-house allied health professionals, attending physicians, and community affiliates.Community affiliates and external physicians that refer patients to the sep are required to submit a standard sep referral form and the Physical Activity Readiness-Medical Examination form (available for download at http://www.csep.ca/english/view.asp?x=698).This form is a 4-page checklist-style medical screening form completed by patients and their physicians that conveys clearance for physical activity.Upon referral, each participant is screened by the exercise physiologist or the medical director, or both.During the screening, a participant interview and detailed chart review are used to determine eligibility based on general and oncology-specific contraindications to exercise 63 .
Participants complete standardized assessments at program entry, and at 12, 24, and 48 weeks.Each assessment is conducted by the exercise physiologist and includes measurements consistently utilized in current literature and those recommended by active cancer exercise programs 28,29 .See Table i for a summary of the physical measures.For specific research projects, serum may be collected and stored for biomarker analysis.Physical assessments are complemented by cancer-specific measures of fatigue 78 and health-related quality of life 79 .

Program Components
Participants are offered a variety of exercise-related services depending on their needs assessment and interests.Participants can receive a consultation to discuss integration of exercise into their daily routine, including a discussion of basic physical activity and exercise principles.For participants who prefer more structured exercise, an individualized exercise prescription may be provided.The exercise prescriptions are based on the participant's fitness assessment and are accompanied by an exercise manual that details the aerobic or resistance exercises (with variations for beginner, intermediate followed by 30 minutes of class discussion based on Booster Sessions designed by Culos-Reed et al. 70,71 . Adherence to exercise is critical for the maintenance of benefit.Previous studies have shown that discontinuing exercise results in a return of cancer and treatment-related side effects 70,80 .The sep uses several features to promote compliance to the exercise prescription and long-term adherence.First, the training staff regularly communicates with participants (by telephone or e-mail) to address any specific barriers to exercise.Second, in addition to the home-based exercise equipment, participants are provided with an exercise manual that reinforces specific strategies for chronic behaviour change, including goal-setting, identification of facilitators and barriers to exercise, exercise preference lists, and detailed exercise instruction with pictures.Previous studies have shown that tailored print materials are effective in increasing exercise motivation in various cancer groups 81 .Third, home-based exercise is supported by weekly group-based exercise classes to encourage social support.Fourth, participants may consult with clinical psychologists and cognitive behavioural therapists who specialize in healthy behaviour change to address cognitive or emotional barriers to routine exercise.Finally, educational seminars on physical activity for cancer survivors are offered on a monthly basis to improve the understanding of the benefits of an active lifestyle.The foregoing program components accommodate the identified preferences of cancer survivors for access to a multifaceted approach to exercise, including flexibility in structure, social support, print educational material, home-based exercise equipment and instruction, and routine follow-up from the cancer exercise specialists 28,29,31,32,34,37,[40][41][42][43][44]82 .

Research
Research-through hypothesis generation and testing, and the provision of pilot data for research funding opportunities-is the driving force behind

Component Description Rationale
Aerobic capacity Cardiovascular fitness is assessed using the modified Bruce treadmill protocol 64,65 .Participants walk at progressively higher speed and incline until they can no longer continue.Peak volume (VO 2 ) is estimated using standard American College of Sports Medicine (acsm) metabolic equations 66 .The acsm Termination Criteria are used to discontinue tests before a participant reached maximum exertion 66 .
Cardiovascular fitness assessment provides important information about the participant's functional capacity and exercise prescription parameters.The modified Bruce treadmill protocol was selected because it uses a prolonged warm-up and walking (rather than running) combined with increases in grade (incline) to bring participants to maximum intensity and because it is used frequently in cancer populations 29 Grip strength Grip strength is measured using a Jamar dynamometer (Sammons Preston, Bolingbrook, IL, U.S.A.) according to the Canadian Society for Exercise Physiology protocol 67 .The dynamometer is held laterally away from the body and maximally squeezed for 3-5 s.
Grip strength is an independent predictor of mortality in older adults and may identify patients, including those with a high level of function, who are at risk of deteriorating health 68,69 .Grip strength has frequently been used as a measure of physical function in cancer patients [70][71][72][73] .

Height, weight, body mass index (bmi) waist circumference and skinfold measurements
Height is measured to the nearest half centimeter using a wall-mounted stadiometer.Weight is measured to the nearest 0.5 kg using an analog scale.The calculation for bmi is weight in kilograms divided by height in square metres.Waist circumference is measured using anthropometric tape according to protocols defined by the World Health Organization (tape placed horizontally mid-way between the bottom of the rib cage and the iliac crest 64 .Measurements are taken to the nearest 0.5 cm.Skinfolds are assessed using skinfold calipers (FitSystems, Calgary, AB) at various sites (sex-specific) and are used to calculate body density and body fat percentage.
Body composition changes are highly prevalent in patients receiving treatment and are associated with poor prognosis 74,75 .Beneficial augmentation of body composition with exercise has been demonstrated in cancer populations 70,71,76,77  the sep.Data from each assessment are collected and stored for longitudinal analyses.The intake of patients with a range of cancer diagnoses and treatments means that populations can be stratified into subgroups that allow for population-or treatmentspecific research.Moreover, the exercise assessment facility is comparable to those available in other cancer exercise research programs and can therefore function as a participating site in large, multicentre trials.Finally, the multidisciplinary nature of the program is conducive to examining outcomes from basic science to the behavioural and psychosocial implications of exercise throughout the cancer continuum.

Community Partners
Hospitals are a rich source of patients as well as of medical and research expertise, but they often lack the physical space, exercise equipment, and access to exercise specialists to deliver routine programming for cancer patients.By contrast, community-based survivorship programs often have greater geographic accessibility and more physical space, and they may even have access to qualified cancer exercise specialists, but they often lack the research capabilities and direct affiliations with physicians and patients.Thus, collaborations between hospital-based and community-based programs may offer an ideal opportunity for patients to transition into independent exercise.For example, a participant may receive an exercise consultation and fitness evaluation at the sep, transition to a community-based program for supervised exercise, and finally transition to homebased exercise.
The Wellspring Cancer Exercise Program (http:// www.wellspring.ca/Centre-of-Innovation/Centreof-Innovation-Programs/Cancer-Exercise.aspx) is an example of a community-based cancer exercise program that may function in an intermediary role.Wellspring uses a multidisciplinary rehabilitative approach led by physiotherapists and kinesiologists to provide a comprehensive exercise training program that is complemented, when needed, with manual therapy and assisted rehabilitation and education.Participants are assessed and receive an individualized, supervised exercise program that typically includes interval training, resistance training, stretching and balance exercises, twice weekly for 10 weeks, followed by once weekly for 20 weeks.Wellspring's Cancer Exercise Program is free to access, and participants are graduated to home-based training after safe levels of exercise education and fitness are reached.

DISCUSSION
Evidence demonstrating the benefits of exercise for cancer survivors has reached a pivotal point.At this time in empirical maturity, a more concerted effort toward knowledge translation in this field needs to be made by clinicians, health care administrations, and health policymakers.Although clinical trials examining exercise and cancer patients are abundant, theory-based knowledge translation strategies for the integration of exercise into oncologic care remain noticeably absent in the literature and should advance in priority for researchers.Furthermore, few approaches to implementing cancer rehabilitation programs have been published (for example, Segal et al., Schneider et al., Demark-Wahnefried, Grabois, and Schmidt 28,29,[82][83][84] ).
In the absence of extensive evidence for successful knowledge translation, simple strategies may assist in accelerating the availability of cancer exercise programs.First, oncologists and patients must be made aware of the extensive empirical evidence regarding the efficacy and safety of exercise during and after cancer treatment.National organizations that provide research overviews and exercise recommendations (for example, the American Cancer Society 49 and the National Comprehensive Cancer Network 85 ) can facilitate an awareness of benefits and joint discussion during clinical interaction.Joint discussion and oncologist recommendation are critical to patient participation in cancer exercise programs and ongoing physical activity 60 .Although the trend appears to be changing, few physicians capitalize on their motivational influence with respect to lifestyle intervention guidance, emphasizing the continual need for physician education regarding the benefits of exercise for their cancer patients 54,57,86 .Second, oncology programs must intensify their pursuit of funding to develop, implement, and maintain cancer exercise programs.Financial support may come from the government (in jurisdictions in which health care is publicly funded), national granting agencies, insurance companies, private donors, or corporate sponsors.Through successful grant applications, small amounts of research funding may be acquired for feasibility studies, followed by larger grants to support adequately powered randomized controlled trials.This approach will not only improve the body of evidence in cancer and exercise, but finance the capital equipment costs and generate institutional support for sustained cancer exercise programming.Third, partnership with private and community health-and-fitness clubs may be an option to provide facility space, exercise equipment, and in-kind professional support.Moreover, community survivorship or fitness clubs remove the barrier of distance and travel time associated with tertiary care centres, a known barrier to participation in physical activity 87 .
The sep represents one oncology institution's attempt at bridging the gap between cancer exercise research and clinical practice by making exercise assessment, prescription, and education a part of standard care.The physiologists, with cancer-specific training, under the guidance of oncologists and psychologists.Accordingly, the sep is well-suited to accommodate survivors coming from a variety of cancer diagnoses and treatment histories with various physical and psychosocial considerations.To facilitate participation, prescription compliance, and chronic behaviour change, the sep provides a comprehensive adherence maintenance program.Included in that program is the provision of a detailed exercise manual and exercise equipment for participants to do their exercises at home.This approach is sustainable with even nominal contributions from participants to cover the basic costs of the materials.Additionally, group exercise sessions encourage social support and opportunities for patients to discuss various barriers and facilitators in a welcoming environment.Finally, community partners provide an outlet for sep participants to exercise with additional support and fewer geographic and financial barriers.The transitional approach from hospital to community and ultimately to independent home-based exercise, is likely to promote chronic exercise and accommodate a variety of exercise preferences.
The sep also has several limitations.It is limited by a lack of in-hospital physical space and funding to conduct highly specialized fitness testing and training.The location of the sep (within an urban, oncologic institution) may be perceived as a strength in some ways (as noted earlier), but it can also be a barrier to participation.Anecdotal evidence from our experience echoes previous reports suggesting that some patients prefer not to come to the hospital to exercise because of negative associations formed with the hospital setting (for example, testing, diagnosis, treatments, and so on) 82 .Furthermore, the urban location presents commuting challenges: parking can be expensive, road congestion can increase travel time, and public transit can be intimidating.The sep is also ill-equipped to assist patients who are available only outside of regular business hours.
Many lessons have been learned in our pursuit of an integrated model of exercise and cancer care.The primary lesson learned is that it is essential to have the collegial support and commitment of oncologists to drive the development of this type of survivorship programming.The sep has benefitted from significant personal and professional investment by several oncologists and nurses-investments have lent gravity to the program within the administration.Equally important is the commitment of the exercise specialists to ensure that the delivery of the program is safe, effective, and enjoyable for the participants.The voice of the participants has proved to be the most effective marketing tool for the sep; positive reviews of the program have driven program growth.We have also found that survivors are more likely to be referred to the sep after diagnosis or when initiating primary or adjuvant treatments.That finding is consistent with previous reports of the response by cancer survivors to the "teachable moment" and their preference to start a lifestyle intervention after a diagnosis or shortly thereafter 54,88 .
Inevitably, the literature will grow, yielding new understandings of the benefits and risks of exercise for cancer patients.It is also important to review the cancer survivor's perspective of participating in cancer exercise programs to ensure that their needs are adequately addressed.Program evaluation may use efficacy metrics (that is, assessing changes in cancer-specific outcomes associated with exercise) or client satisfaction and participation assessments.Ideally, outcomes are examined concurrently in a way in which participants in randomized trials are also assessed for satisfaction, adverse events, and attendance or adherence.Participant satisfaction questionnaires could be accompanied by qualitative assessment to provide deeper insight regarding satisfaction and program preferences that have not previously been captured.
Ultimately, research in this field must extend beyond efficacy trials, addressing questions pertaining to effective and efficient intervention delivery models, strategies to boost exercise adherence, and systematic knowledge translation approaches at the institutional and health policy levels.Finally, a key research area that would stimulate health care investment would be strong evidence of cost-effectiveness of cancer exercise programs.Although research has demonstrated survival benefits for cancer survivors with exercise [24][25][26] , no evidence has, to our knowledge, described the cost savings that may result from reduced hospitalizations, treatment complication rates, or overall health care utilization.Assessing the potential savings associated with the improved health of cancer survivors will likely be key to establishing consistent implementation of cancer exercise programs.

CONCLUSIONS
Amid their acclaim as centres of excellence in oncology, many tertiary care institutions fail to adopt cancer exercise programming, which has proved to provide substantial benefit to cancer survivors.The barriers to implementation are numerous, but we urge the medical and research community to continue with high-quality cancer exercise research in the areas identified in this article and to forge ahead with the development and advancement of cancer rehabilitation and survivorship programs that incorporate exercise as a standard of care.The sep is merely one example of an approach to integrating exercise.Future publications on implementation approaches are required.
, and advanced exercisers to allow for progression within the program) and an exercise log.Participants are encouraged to follow their exercise program at home, and they are provided with the exercise equipment described earlier.Participants may also attend weekly 90-minute group exercise classes that include a 10-minute warm-up, 20 minutes of low-impact aerobic exercise, 20 minutes of resistance training, and 10 minutes of cool-down, e139 Current OnCOlOgy-VOlume 19, number 3, June 2012 Copyright © 2012 Multimed Inc.Following publication in Current Oncology, the full text of each article is available immediately and archived in PubMed Central (PMC).
sep has several strengths to highlight.The sep program is delivered by certified exercise Current OnCOlOgy-VOlume 19, number 3, June 2012 Copyright © 2012 Multimed Inc.Following publication in Current Oncology, the full text of each article is available immediately and archived in PubMed Central (PMC).

table i
.
Current OnCOlOgy-VOlume 19, number 3, June 2012Copyright © 2012 Multimed Inc.Following publication in Current Oncology, the full text of each article is available immediately and archived in PubMed Central (PMC).