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Evaluation of an Exercise-Based Phase Program as Part of a Standard Care Model for Cancer Survivors

Brown, Jessica Marlene; Shackelford, Daniel Yoon Kee; Hipp, Maria Lyn; Hayward, Reid

Translational Journal of the American College of Sports Medicine: April 1, 2019 - Volume 4 - Issue 7 - p 45–54
doi: 10.1249/TJX.0000000000000082
Original Investigation
Free
SDC

Exercise is a well-established method of alleviating cancer-related toxicities both during and after treatment. However, specific exercise prescription recommendations for patients at varying points along the cancer continuum are not fully developed. The Phase Program of cancer rehabilitation was created to address this issue.

Purpose This study aimed to evaluate the effectiveness of the Phase Program on cardiorespiratory fitness (V˙O2peak), muscular strength (MS), and fatigue in cancer survivors during and after treatment.

Methods A total of 183 cancer survivors were included in this study. The Phase Program consisted of four, 12-wk, sequential phases representing differing time points from diagnosis, and prescribed intensity, progression, and goals unique to each phase. Changes in V˙O2peak, leg press MS, chest press MS, and fatigue were measured during transitions from phase 1 to phase 2, phase 2 to phase 3, and phase 3 to phase 4.

Results Eighty-one patients completed the entire program with entry into phase 4, with 71% retention. V˙O2peak, leg press MS, chest press MS, and fatigue significantly improved from phase 1 to phase 2 by 13%, 13%, 18%, and −25%, and from phase 2 to phase 3 by 14%, 19%, 26%, and −27%, respectively (P < 0.05). V˙O2peak and chest press MS significantly improved from phase 3 to phase 4 by 4% and 7%, respectively (P < 0.05).

Conclusion Current exercise guidelines do not fully address the multifaceted needs of cancer survivors at different points along the cancer continuum, nor do most exercise programs properly adhere to the principles of exercise training necessary for a safe and effective intervention. The Phase Program expands on current exercise guidelines providing more precise exercise prescription. This study provides clear, reproducible, and empirical evidence of its effectiveness.

School of Sport and Exercise Science and the University of Northern Colorado Cancer Rehabilitation Institute, University of Northern Colorado, Greeley, CO

Address for correspondence: Reid Hayward, School of Sport and Exercise Science and the University of Northern Colorado Cancer Rehabilitation Institute, University of Northern Colorado, 913 19th Street, Greeley, CO 80639 (E-mail: reid.hayward@unco.edu).

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INTRODUCTION

Advancements in cancer treatments such as chemotherapy and radiation have increased survival rates but often result in many deleterious side effects during and after treatments. Cancer survivors can suffer from physiological toxicities affecting the cardiovascular, pulmonary, musculoskeletal, immune, gastrointestinal, hepatic, and neuroendocrine systems (1). In addition, many survivors will experience psychological decrements such as increased fatigue, increased depression, and decreased quality of life (QOL) (2,3), whereas exercise directly attenuates the toxicities and decrements of cancer and its concurrent treatments (4,5). The need to establish an exercise Standard of Care Model (SCM) has been recognized by many organizations. The American Cancer Society has established physical activity guidelines for cancer survivors (6), and the American College of Sports Medicine (ACSM) established exercise guidelines endorsed by the American Society of Clinical Oncology (7). In addition, the National Comprehensive Cancer Network added guidelines to their inclusive treatment recommendations (8). Exercise programming should be included in the survivorship plan as early as possible and should be considered as a foundational component to improve lifelong QOL (9). The addition of an SCM or, more specifically, a structured and empirically tested exercise intervention may increase patient benefit by reducing variations in practice and standardizing program implementation.

To derive the greatest benefit, exercise-based interventions must be comprehensive and address the multidimensional needs of cancer survivors during and after treatment. For this reason, a “one size fits all” approach to exercise interventions will not suffice (10). Survivors require prescriptive exercise that is specialized for each individual based on treatment status, comorbidities, and placement on the cancer continuum. At the University of Northern Colorado Cancer Rehabilitation Institute (UNCCRI), we have developed an SCM that includes physician referral, medical and cancer screening, initial physiological and psychological assessments, and an individualized exercise prescription and intervention using a Phase Program (Fig. 1). Numerous exercise studies have been conducted in cancer patients, most of which have focused primarily on breast cancer, with varying modes, intensities, and outcome measures making standardization and interpretation of results challenging (11). Furthermore, to date, virtually all exercise programs reported in the literature have failed to properly apply and adhere to the standard principles of exercise training: individuality, specificity, progressive overload, reversibility, and diminishing returns (12). ACSM has established exercise intensity guidelines for cancer patients; however, they are broad and have been adapted from recommendations for the apparently healthy population (7). Because of a lack of information in previous studies, these guidelines do not provide strict training intensities for exercise prescribed during and after treatment, and they recommend long-term goals that may be inappropriate for sedentary or debilitated patients. Likewise, a detailed medical history and direct patient referrals by an oncologist may be necessary to ensure safety and to individualize the exercise prescription for the patient’s specific needs. As a result, it is difficult for exercise professionals and clinicians to formulate exercise prescriptions for cancer patients at different points along the cancer continuum and does not specify why or when to modify exercise dosage to elicit optimal adaptations. It has been reported that 80% of oncology care providers are unaware of the availability of exercise guidelines and lack knowledge about when to implement them (13).

Figure 1

Figure 1

The Phase Program proposed here was created to address these concerns while providing a clear method of exercise prescription and intervention to alleviate treatment-related toxicities in cancer survivors. Therefore, the purpose of this study was to evaluate the effectiveness of the Phase Program on cardiovascular fitness (V˙O2peak), muscular strength (MS), and fatigue in a group of cancer survivors at each phase transition and in those who completed the entire program. We hypothesized that significant improvements would be made in V˙O2peak, MS, and fatigue after completion of the Phase Program, and that these improvements would be evident during each phase transition.

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METHODS

Participants

Patients were male and female (n = 183) cancer survivors 18 yr and older who were undergoing or had completed surgical intervention, chemotherapy, radiation therapy, immunotherapy, hormonal therapy, and/or other types of treatment. Inclusion criteria were as follows: 1) diagnosed with cancer, 2) at least 18 yr of age, and 3) medically cleared and referred to the program by the participant’s oncologist or physician. Clearance criteria were based on the discretion of the individual oncologist or physician. Exclusion criteria for all subjects included 1) history of congestive heart failure, 2) history of myocardial infarction, 3) chronic lung disease, 4) history of coughing up blood, 5) fainting, and 6) epilepsy. Upon entry into the program, every subject consented to dissemination and interpretation of their assessment values for research.

All participants were referred and cleared to participate in an exercise program by the supervising oncologist or primary care physician. A detailed medical and cancer history accompanied each referral and was screened before any testing was conducted (see Patient Summary, Supplemental Content 1, which documents all patient screening information compiled before data collection, http://links.lww.com/TJACSM/A31). Participants provided written informed consent, and all protocols were approved by the University of Northern Colorado’s Institutional Review Board.

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Data Collection

The Phase Program of cancer rehabilitation uses a four-phase system with assessments of physiological and psychological variables conducted at the beginning of each phase. Each reassessment marked the completion of the phase and subsequent entry into the next. The point of entry into the Phase Program was determined by patient treatment status. Patients currently undergoing chemotherapy and radiation treatment entered at phase 1, and all posttreatment patients, or those without chemotherapy or radiation treatment, entered at phase 2, which altered the length of the intervention depending on which phase the participant entered the Phase Program. Phases 1 through 3 are considered “true cancer rehabilitation” and are each composed of 12 wk of exercise-based rehabilitation. The program was marked as completed once the patient had entered phase 4 (Fig. 1).

Data were obtained from initial assessments occurring at entry into the program and subsequent reassessments every 12 wk (see Data Collection Sheet, Supplemental Content 2, which comprises all physical tests and data acquired during each assessment, http://links.lww.com/TJACSM/A32). At each assessment, fatigue was measured via the Piper Fatigue Inventory (14). Cardiovascular endurance was evaluated using the cancer-specific UNCCRI Treadmill Protocol, which yields V˙O2peak values (15). MS was assessed via an estimated one-repetition maximum protocol (EST 1-RM) using the Brzycki equation for chest press, lat pulldown, seated row, shoulder press, leg press, leg curl, and leg extension (16).

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Exercise Intervention

The Phase Program exercise intervention prescribed one-on-one sessions with trained Clinical Cancer Exercise Specialists (CCES) certified by UNCCRI. These clinicians had over 500 h of training and patient contact and were certified by a written examination and practical evaluation. All sessions for all participants were conducted at UNCCRI by a trained CCES.

Training frequency was three sessions per week for 12 wk, per phase. The duration of each exercise session was 60 min with 20 min designated for aerobic exercise, 30 min for resistance exercise, 10 min for flexibility training, and balance exercises incorporated throughout the session. Each CCES prescribed the mode of aerobic exercise based on the participants’ assessment results and desired goals in adherence to both the principles of individuality and specificity. The following modes were used for the aerobic portion of the exercise session: treadmill, cycle ergometer, NuStep, Aquaciser (underwater treadmill), and outdoor walking or jogging. During the resistance portion of each exercise session, the following muscle groups were targeted: chest (pectoralis major and minor), back (rhomboids and latissimus dorsi), lower body (quadriceps and hamstrings), and core (trunk stabilizers and pelvic floor). All resistance exercises included three sets of 10 repetitions of each exercise. Other muscle groups may have been included (deltoids, biceps, triceps, adductors, etc.) within the 30 min of strength training if time permitted. Modes of resistance training included Cybex® resistance machines, resistance bands, dumbbells, medicine balls, body weight, and resistance tubing. The resistance training regimen was designed to target all major muscle groups needed for activities of daily living and to limit single-joint exercises until larger, multijoint exercises were complete for efficiency in the sessions. With this in mind, the repetition and set range was set so that those less familiar with standard weight training could progress using only intensity (weight). The entirety of the exercise intervention has been designed for enhanced reproducibility with an individualized, but formulaic layout.

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The Phase Program

The intensity and the general purpose of the individualized exercise interventions were prescribed based on the standards of the Phase Program, the participants’ assigned phase, and dictated by the results of each assessment and subsequent reassessments (Fig. 2). Each phase represents a unique time point on the cancer continuum, and exercise is prescribed to adhere to goals and intensity ranges matched with the expected toxicities, limitations, and ability level. In addition to these predetermined objectives, our SCM follows the goals and objectives of exercise prescription set by the ACSM Roundtable (7). For exercise prescription, the assessment results, and specifically the classifications achieved by the participant during each assessment, were used for the selection of appropriate starting intensities and progression prescribed during the intervention. Higher assessment values resulted in the selection of greater starting intensities (overload), whereas lower functioning indicated the use of the lower ranges of intensity prescribed for each phase (see Patient Overview, Supplemental Content 3, which dictates the exercise prescription of intensity and progression for each patient in the Phase Program, http://links.lww.com/TJACSM/A33).

Figure 2

Figure 2

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Phase 1

Phase 1 is designed for cancer survivors still receiving chemotherapy and/or radiation treatments. Because of the fact that side effects are more prevalent during treatment, the goal of this phase is to maintain or slightly increase physiological and psychological parameters and prevent any decline in functional capacity. Phase 1 is specifically designed to adhere to the exercise training principles of individuality and specificity. Decrements below baseline values obtained at the onset of the program should not occur because this phase is designed to attenuate the toxicities of cancer treatment. In phase 1, the initial exercise intensity is categorized as low, ranging between 30% and 45% of heart rate reserve (HRR) and EST 1-RM (17). The rate of progression (i.e., how quickly overload is applied) is small representing only a 0%–5% and 10%–15% range of increase in aerobic and resistance exercise intensity, respectively, over the course of the intervention. Phase 1 is intended to last a total of 12 wk. However, participants remained in this phase for the duration of treatment regardless of its length, or for the full 12 wk if treatment was less than 12 wk.

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Phase 2

Phase 2 is designed for cancer survivors who have completed phase 1, or for survivors who have completed or are undergoing cancer treatment that is not categorized as chemotherapy or radiation therapy (e.g., hormonal therapy, immunotherapy, and stem cell transplant). Side effects of chemotherapy and radiation are fundamentally different from the side effects experienced during other forms of cancer treatment, which are generally less severe. As a result, the starting intensity of phase 2 is prescribed as low to moderate and ranges between 40% and 60% of HRR and EST 1-RM (17). The rate of progression is moderate to vigorous, representing a 10%–20% and a 30%–50% range for increases in aerobic and resistance exercise intensity, respectively, over 12 wk. This intensity serves as a natural progression for those completing phase 1, which prescribes lower intensity and aligns with the ACSM guidelines. Phase 2 is designed to continue adherence to the principles of individuality and specificity and to begin incorporating progressive overload based on physiological assessment results and treatment-related functional deficits. Therefore, the goal of phase 2 is to reduce the physical and functional limitations created by cancer treatment and to improve cardiovascular and muscular function. An additional focus of phase 2 is to build a foundational base using corrective and functional training with an emphasis on developing and stabilizing the core, pelvic floor, shoulder girdle, or any other joints or muscles affected by surgery, hormonal treatments, as well as the long-term effects of chemotherapy or radiotherapy. Stabilizer muscles such as the core, pelvic floor, and shoulder girdle may be prominently affected by cancer and its treatments (18). Strengthening these components will improve functional capacity, assist with activities of daily living, and enhance general movement patterns that are key to optimizing outcomes in subsequent phases.

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Phase 3

Phase 3 is designed for cancer survivors who have completed phase 2. This is the final phase of what is considered “true cancer rehabilitation” and allows the participant to transition to an exercise intervention prescribed for the apparently healthy population. As phase 3 represents the last phase of cancer rehabilitation, a major goal is to teach participants the specific skills necessary to implement and maintain an exercise program on their own. Participants should transition from phase 3 with the ability to perform exercises with self-efficacy, they should have an understanding of proper technique to avoid injury, and they should have a foundational grasp of exercise training principles to create progression. This goal exists to support the principles of diminishing returns and reversibility. Phase 3 also aims to improve physiological and psychological parameters beyond phase 2 and to incorporate the principle of progressive overload to the highest extent during cancer rehabilitation. At the completion of this phase, cancer survivors should achieve a categorical classification at or near apparently healthy status for all physiological assessment variables. Phase 3 training is classified as moderate to high, and intensities range between 60% and 85% of HRR and EST 1-RM. The rate of progression is modest, representing a 5%–15% and a 30%–50% range of increase in aerobic and resistance exercise intensity, respectively, over 12 wk. This range has been deemed appropriate for vigorous exercise in the cancer population (17) and can elicit overload.

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Phase 4

Phase 4 is designed for those who have completed phase 3. This phase has no time limits on its duration and is meant to assist cancer survivors in the maintenance of physical activity and a healthy lifestyle. The exercise intensity can vary between 65% and 95% of HRR and EST 1-RM during this phase and is dependent on the patient’s goals. Phase 4 can be conducted independently by the cancer survivor, one on one with a certified CCES, or in a group setting.

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Statistical Analysis

Individual paired-sample t-tests were used to determine whether significant differences occurred in cardiovascular endurance, MS, and fatigue during each phase transition. The statistical package G*Power (3.1.9.2) was used to calculate statistical power. Individual paired-sample t-tests were used to obtain a power of 0.95 with a medium effect size. According to the statistical program, to achieve a power of 0.95, each statistical test suggested an N of at least 47, which was met by all phase transitions. A Bonferroni adjustment was used to reduce the chance of committing type I error. The following dependent variables were measured: V˙O2peak, EST 1-RM of the leg press, EST 1-RM of the chest press, and fatigue. The following phase transitions (assessment vs reassessment) were evaluated: phase 1 to phase 2, phase 2 to phase 3, and phase 3 to phase 4. The statistical package G*Power (3.1.9.2) was used to calculate the power of the statistics. All data are presented as mean ± SD, and statistical analyses were performed using the Statistical Package for the Social Sciences software package (SPSS, Chicago, IL). All analyses were two-tailed, and an alpha level of 0.05 was used to define statistical significance.

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RESULTS

Table 1 displays the demographic characteristics of all participants. A total of 183 cancer survivors were included in the study (70 males and 113 females) with a mean age of 61 ± 13 yr. Breast cancer survivors represented 37% of participants, with similar numbers representing liquid (12%), prostate (10%), and lung cancers (10%). Cancer stages I, II, and III were represented near equally (24%, 25%, and 24%, respectively), and 16% were diagnosed as stage IV. Of the participants, 65% underwent chemotherapy and 25% received all three major treatment modalities (surgery, chemotherapy, and radiation). On average, patients entered this study 7.4 months after treatment was completed, whereas 38% entered this study during chemotherapy and/or radiation treatment.

TABLE 1

TABLE 1

Of the 183 program participants, 81 (44%) completed the entire Phase Program and entered phase 4. The mean attendance for all subjects was 80% ± 3.8%, and the average retention was 71% between each phase transition. Retention rate for phase 1 was 69% (i.e., 69% of the patients completing phase 1 entered phase 2). Of the 70 patients who entered the program at phase 1, 18 remained in treatment and completed a postassessment as phase 1 (i.e., phase 1 to 1 transition). Including those who remained in phase 1 for treatment continuation, total retention was 94%. The average retention rate for those who transitioned from phase 2 was 88%. Specifically, retention for those patients who entered the program at phase 2 was 83%, whereas retention was 100% in those who entered phase 2 after graduation from phase 1. Finally, retention rate for those completing phase 3 was 57% (Table 2).

TABLE 2

TABLE 2

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Changes in Peak Volume of Oxygen Consumption, MS, and Fatigue

Table 3 summarizes absolute values (pre- to posttreatment) for all phase transitions for V˙O2peak (mL·kg−1 ·min−1), leg press MS (kg), chest press MS (kg), and fatigue. Fig. 3 depicts mean percent change in V˙O2peak, leg press MS, chest press MS, and fatigue. Additional assessment data and results can be viewed online (Supplemental Content 4, http://links.lww.com/TJACSM/A34).

TABLE 3

TABLE 3

Figure 3

Figure 3

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Phase 1 to 2 Transition

Statistically significant improvements were observed in V˙O2peak (P < 0.001), leg press MS (P < 0.05), chest press MS (P < 0.001), and fatigue (P < 0.001) when comparing data obtained at entry into phase 1 versus data obtained after completion of phase 1 (i.e., entry into phase 2). Mean percent changes in V˙O2peak, leg press MS, and chest MS were 13%, 13%, and 18%, respectively. Mean values of fatigue decreased as a result of completing phase 1, lowering the fatigue classification from “moderate” to “mild” according to the Piper Fatigue Inventory.

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Phase 2 to 3 Transition

When comparing data obtained at entry into phase 2 versus data obtained after completion of phase 2 (i.e., entry into phase 3), significant improvements were observed in V˙O2peak (P < 0.001), leg press MS (P < 0.001), chest press MS (P < 0.001), and fatigue (P < 0.001). Mean percent changes in V˙O2peak, leg press MS, and chest MS were 14%, 19%, and 26%, respectively. Mean values of fatigue decreased, as a result of completing phase 2, lowering the fatigue classification from “moderate” to “mild.”

Initial assessment values for those entering the program at phase 2 who had undergone chemotherapy and/or radiation before starting the Phase Program were evaluated against those who graduated from phase 1 to determine whether the effectiveness of the phase 1 intervention was due to the exercise prescription or the spontaneous healing effect of time. For those patients entering the program at phase 2, mean values for V˙O2peak, leg press, chest press, and fatigue were 19.7 ± 7.0 mL·kg−1 ·min−1, 79.2 ± 34 kg, 30.1 ± 18 kg, and 4.8 ± 2.2, respectively. These values are significantly lower (P < 0.05) when compared with values observed in those who completed phase 1 and transitioned to phase 2. In addition, fatigue was significantly (P < 0.001) elevated in those entering as phase 2 after treatment.

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Phase 3 to 4 Transition

Significant improvements were observed in V˙O2peak (P < 0.05) and chest press MS (P < 0.05) when comparing data obtained at entry into phase 3 versus data obtained after completion of phase 3 (i.e., entry into phase 4). Mean percent change of V˙O2peak, leg press MS, and chest MS were 4%, 5%, and 7%, respectively. Mean values of fatigue decreased during this transition but remained at a “mild” Piper Fatigue Inventory classification.

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Changes in Patients Who Completed the Entire Phase Program (Entry to Phase 4)

In the 81 patients who completed the Phase Program and entered phase 4, significant improvements were observed in V˙O2peak (21.0 ± 6.8 to 26.1 ± 7.3 mL·kg−1 ·min−1; P < 0.001), leg press MS (78.6 ± 31 to 105.8 ± 41 kg; P < 0.001), chest press MS (26.3 ± 17 to 39.2 ± 19 kg; P < 0.001), and fatigue (4.9 ± 2.2 to 3.2 ± 2.2; P < 0.001). Total mean percent change for V˙O2peak, leg press MS, chest press MS, and fatigue were 24%, 35%, 49%, and −35%, respectively (Fig. 3). For those patients completing the Phase Program, mean values of fatigue decreased yielding a mild classification.

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DISCUSSION

Exercise-based interventions are widely considered a viable method of cancer rehabilitation because of the clear evidence that exercise improves functional capacity, reduces cardiovascular disease risk factors (19), decreases mortality (20), may limit the risk of cancer recurrence (21,22), and improves QOL (23). The Phase Program of our SCM for cancer rehabilitation elicited improvements in cardiovascular endurance, MS, and fatigue during all phase transitions, and only leg MS and fatigue resulted in nonsignificant improvement in those transitioning from phase 3 to phase 4. Substantial improvements occurred across each phase in those who completed the entire program, suggesting the effective use of progressive overload and individuality throughout the program.

The standardization and consistency of medical screening and assessments between each phase transition is critical for the successful use of the Phase Program. Although each phase prescribes an appropriate range for starting intensities and rates of progression, essentially governing the use of the principle of progressive overload, the clinician truly individualizes the exercise intervention. This is accomplished through the use and interpretation of the patients’ comprehensive assessment results and corresponding classifications. Higher levels of functioning will result in the creation of an exercise prescription that is more challenging than that created for a patient with lower levels, yet each participant’s exercise prescription will fall within the guidelines of the assigned phase when using the Phase Program. This method of exercise prescription adheres to the ACSM guidelines but establishes stricter intensity ranges and goals representative of differing time points on the cancer continuum, i.e., during (phase 1), immediately after (phase 2), and after treatment (phase 3). In addition, the program seeks to individualize progressive overload and specificity using medical information, assessment results, and patient goals. The exercise intervention is formulaic and prescribes frequency and duration similarly across patients for easy reproducibility, whereas the one-on-one clinician-to-patient ratio allows for a personalized approach.

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Phase 1

Participants who completed phase 1 experienced significant improvements in all variables after the 12-wk intervention. The goal of phase 1 is to offset cancer and cancer treatment-related negative side effects through the use of low-intensity, prescriptive exercise. The low intensity used for this phase did not only reduce the decline in function typically seen in cancer patients undergoing chemotherapy and radiation treatment, it significantly improved function. Participants who completed phase 1 improved lower (13%) and upper (18%) body MS and cardiovascular endurance (13%). Similar improvements in lower and upper body strength have been observed in patients undergoing treatment previously (24). Strength training increases protein synthesis, increases muscle mass, and may offset cancer-related cachexia. This may explain why survivors in phase 1 not only maintained MS levels but significantly improved beyond their initial baseline measurements. In addition, aerobic exercise and its associated cardioprotective effects may explain the improvements observed in cardiovascular endurance (25). Cancer-related fatigue decreased by 25% in patients transitioning from phase 1. This reduction is similar to previously observed results in studies using lower intensity exercise (26,27). Higher prescribed exercise intensities may not improve fatigue levels and may be detrimental. One study found that resistance training at a moderate to high intensity in breast cancer survivors undergoing treatment resulted in an overall increase in fatigue (28). Contrary to the belief that fatigue levels may be heightened for those exercising while undergoing treatment, the current study demonstrates that exercising at appropriate, low intensities can significantly reduce fatigue levels.

Modest improvements were expected because the exercise prescription dictated an initial low intensity and a small rate of progression, and the majority of patients underwent all major treatment modalities. The exercise intensity prescribed for patients in phase 1 was low due to the J-shaped curvilinear relationship between the risk of infection and the increasing exercise workloads, where vigorous- or heavy-intensity exercise may result in a higher than normal risk of infection (29). Infection is a significant cause of death in patients undergoing treatment (30), and exercise at lower intensities has been shown to preserve immune function and reduce the risk of adverse effects in patients undergoing treatment (31). Studies using high-intensity exercise interventions have been conducted in cancer patients during treatment with similar, positive results as observed in the current study (32). It should be noted that in some studies incorporating high-intensity exercise, blood draws were performed before each day of exercise, and the session was terminated if leukopenia, thrombocytopenia, or infection were detected. Although this methodology is sound and offers a solution for the implementation of high-intensity protocols, it is not feasible for exercise professionals to test and analyze immune function on each patient in perpetuity, and it may significantly limit the number of exercise sessions that can be performed by the participant. Increases in cardiorespiratory fitness similar to those of the Phase Program were observed in a demographically comparable group of breast cancer survivors undergoing treatment after a 12-wk high-intensity (60%–100% of V˙O2peak) aerobic exercise intervention (33). Although the research indicates that high-intensity exercise does yield significant improvements, our study demonstrates that similar benefits occur using a lower intensity. Given the equivalency of the outcomes resulting from both high- and low-intensity exercise interventions, the use of lower intensities provides optimal benefit and reduced risk to the patient.

The prescribed intensity and rate of progression of phase 1 was appropriate for those undergoing cancer treatment and was well tolerated by every participant. This addresses one of the most prevalent concerns that patients undergoing treatment may not be able or willing to participate in an exercise-based rehabilitation program and negates the premise that these patients only be prescribed in-patient physical therapy (4). Our results suggest that the Phase Program is well tolerated, as evidenced by the 94% retention rate, is capable of eliciting significant physiological and psychological improvements despite the limiting side effects of cancer treatment, and should be considered for use in patients undergoing treatment.

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Phase 2

Energy levels and functional capacity have been observed to increase after the completion of cancer treatment (34), which will increase exercise tolerance and enhance the positive effects of exercise (35). Because of this, the intensity and progression prescribed for phase 2 is higher than that of phase 1 and represents a moderate range. The exercise prescription was then individualized based on the patient’s improvements from phase 1 or the assessment at entry. In conjunction with an increased emphasis on the principle of progressive overload, phase 2 also prescribes correctional exercises (e.g., hamstring strengthening to offset anterior pelvic tilt) with the goal of attenuating functional and postural deviations that may be present in patients after treatment or surgical intervention. The prescription and rate of progressive overload allowed participants to achieve greater improvements in cardiovascular endurance, MS, and fatigue than what was observed in phase 1.

Levels of fatigue significantly decreased in patients transitioning from phase 2 to phase 3. This reduction resulted in an improvement in the fatigue classification from “moderate” to “mild.” Our findings demonstrate that significant declines in fatigue scores are possible during and immediately after treatment and are more profound than the reductions in fatigue seen in those farthest from treatment (i.e., those transitioning from phase 3 to phase 4). Interestingly, the improvements immediately after treatment were additive to the large, near identical, significant improvements previously observed in those during treatment (phase 1), suggesting that exercise attenuates cancer-related fatigue to the greatest extent during and immediately after treatment.

In the present study, MS improved significantly in subjects completing phase 2 by an average of 23%. Similar improvements in strength have been observed in several other studies in cancer survivors not undergoing treatment, many of which used higher exercise intensities (4,36). Cardiovascular endurance significantly increased by 14% in the transition from phase 2 to phase 3, which is similar to other interventions (37) and greater than improvements seen previously in earlier versions of our program (27).

A correlation may exist between time from treatment, exercise intensity, attendance, and adherence. Winters-Stone et al. (38) reported that after a 1-yr, moderate- to high-intensity resistance training intervention in breast cancer survivors (~1 yr from treatment), average MS significantly improved by 16%. Of note, strength gains were only observed in those who attended 50% or more of the prescribed exercise sessions, and withdrawal from the program occurred primarily in those closest to treatment (38). The vigorous nature of the exercise intervention may have been a deterrent for continued program participation, and it provides evidence that attendance and retention may be reduced in patients closest to treatment and affected by exercise intensity. It has been well documented that increased exercise intensity reduces adherence and attendance (39). In a study of sedentary adults randomly assigned to a moderate- or high-intensity exercise intervention, adherence was significantly greater in the moderate intensity group (40). The low to moderate intensity of phase 2 resulted in significantly improved physiological and psychological values in cancer survivors immediately after treatment, while maintaining an average attendance rate of 80% and a retention rate of 88%. This suggests that the intensity and progression prescribed in phase 2 not only improves function but may also positively affect program attendance and reduce attrition—aspects that must be considered during exercise prescription.

The average time from treatment in our study was 7.4 months. The majority of studies investigating the effects of exercise on cancer survivors after cancer therapy employ patients who are greater than 1 yr posttreatment (26,41), with some as great as 4 yr after treatment (4,26), and many which do not report the time, simply referring to the subject demographic as “posttreatment” (11,42,43). A similar 12-wk exercise program resulted in a 7.5% nonsignificant improvement in cardiovascular endurance (4). This smaller improvement may have been due to the use of a group model versus an individualized, one-on-one model, or it may be due to the characteristics of the study participants. The aforementioned study consisted of mainly female breast cancer survivors, with an average time from diagnosis of 2.36 yr. These subjects may not accurately represent the diverse demographic makeup of the cancer population as a whole, specifically in terms of cancer type, treatment modality, and treatment timetable. The term “posttreatment” is too broad for detailed exercise prescription and creates a disparity in the literature. Exercise guidelines and subsequent interventions must address the differing treatment time points and acknowledge that patient needs may differ at 1 month after treatment versus 2 yr. The use of the Phase Program, and specifically phase 2, creates a new time point that could be referred to as “immediately after” treatment. Future research regarding exercise-based rehabilitation should focus on patients who are in the period immediately after treatment (within 1–9 months), as it represents a common time point on the cancer continuum that is underrepresented in the literature.

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Phase 3

The transition from phase 3 marks the end of what is considered “true cancer rehabilitation” in the Phase Program. Further participation in phase 4 is considered maintenance and can be completed one on one, in a group, or independently. For this reason, a major goal of phase 3 is to prevent reversibility by educating participants and building self-efficacy to sustain the physical and mental adaptations for life. An individualized, one-on-one approach is uniquely suited to address behavior modification, to teach form and safety, and to instill motivation for future exercise prescription.

After the completion of phase 3, 65% of the participants improved to the “good” or above classifications for strength-to-weight ratio on the leg press and 53% of the subjects scored in the “excellent” or “superior” classification when using normative data for the apparently healthy population. Forty-three percent of the patients improved to the classification of “good” or above on strength-to-weight ratio for the chest press. Although fewer patients improved to the “good” classification for the chest press, it should be noted that 36% of the participants were breast cancer survivors, which provides a significant hurdle to improvements in upper body strength. Nevertheless, improvements in upper body MS were still significant for participants completing phase 3. Cardiovascular endurance as measured by V˙O2peak improved to a classification and percentile deemed “fit” in 59% of the participants. It has been demonstrated that sedentary men who were unfit at the initial examination, but who became fit at reassessment, had a 44% reduction in risk of mortality when compared with similar unfit men who did not improve (44). The Phase Program produced significant improvements in cardiovascular endurance during the transition from phases 1, 2, and 3. Improvements in cardiovascular endurance, regardless of population, are strongly correlated with a decrease in all cause and cardiovascular mortality (20). Considering the complex nature of cancer and cancer treatment-related toxicities, the continual decrease in risk of mortality at each reassessment during the Phase Program may improve patient prognosis, improve QOL, and reduce risk of recurrence (21,22).

The degree of improvement was attenuated in phase 3 for all variables assessed. This can be expected considering the significant improvements previously elicited in the program. For some individuals, this reduced improvement may be due to the principle of diminishing returns, particularly in those who achieved classifications above excellent by the end of this phase. For others, there may have been an unforeseen reduction in the ability to maintain adherence to the principle of overload as the frequency and duration of exercise sessions were capped in this study. Phase 3 was designed to adhere to the principle of progressive overload, as the intensity prescribed in this phase is considered “high.” This level of overload may be sufficient to elicit change in some individuals in phase 3, but as the side effects from cancer continue to lessen and one adapts to the stress of the exercise and improves fitness level, a greater exercise volume is necessary to elicit additional gains. The ability to increase session length, add additional sessions, or increase intensity may be required by some cancer survivors to realize even further increases in cardiovascular endurance and MS. However, because high-intensity exercise may negatively affect attendance and adherence, for most cancer survivors, it is recommended that this be accomplished by supplementing the structured Phase Program with longer sessions, additional weekly exercise sessions, and/or exercise homework.

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Retention and Safety

Retention, as defined as a patient completing a 12-wk exercise intervention (phase transition) with pre- and postassessments, was high in this study. The greatest retention was observed at earlier time points in the program (phases 1 and 2). Despite known barriers for attendance and program adherence for those in active treatment (e.g., treatment schedules, treatment symptoms, and transportation), overall program adherence in phase 1 was 94%. All of the participants who graduated from phase 1 subsequently completed phase 2 and entered phase 3, representing 100% retention. A major factor that may have enhanced program adherence was the individualized, one-on-one clinician-to-patient ratio. This personalized approach allowed for immediate adjustments in exercise intensity, correction of form and body mechanics, and constant motivation. It is hypothesized that retention decreased in phase 3 because of patients’ improved health and function and the return to work or other obligations. Those who remained in phase 3 may have desired the social support provided by the specialist or sought further increases in functional capacity. Over the past 5 yr of data collection at our facility, only 21 injuries or illnesses occurred as a result of our program, which represents only 0.19% of all prescribed exercise sessions. The consistent education and training of our CCES, in conjunction with the one-on-one approach, may have been key factors in improved safety and reduced patient risk.

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Limitations and Strengths

The current study had several limitations. This study did not contain a nonexercise control group. However, UNCCRI is an established exercise-based cancer rehabilitation program that receives referrals from oncologists for patients on a daily basis. The benefits of exercise are well known and are recommended for cancer survivors. Because of this, the researchers chose not to withhold a known stimulus from cancer survivors who were referred for exercise and sought to participate in the program. In a follow-up study, we will conduct pre- and postassessments on patients who do not wish to participate in an exercise program. Second, this manuscript does not report all data for nonstandard phase transitions. A nonstandard phase transition occurs when the patient remains in the same phase after a postassessment, for example, when cancer treatment continues after the completion of phase 1 or when severe functional deviations are not fully corrected after phase 2. Although we tracked and reported program attendance and adherence across each phase transition, we did not track attendance specific to each phase or adherence to each component of the exercise prescription. Our intervention was highly scripted; therefore, we hypothesize that the protocol and the exercise prescription were followed each session. However, future investigations should report acute, day-to-day modifications to further elucidate the exercise dose–response. We have reported anecdotal reasons for program withdrawal, but future studies could formally record this and further explore any barriers to retention and adherence.

To our knowledge, this the first proposal of an SCM including a method of individualized exercise prescription fully adhering to all principles of exercise training. In addition, the Phase Program adheres to the ACSM guidelines, which are endorsed by the American Society of Clinical Oncology. Our setting and population demographics closely reflect the cancer population and real-world clinics/fitness facilities, enhancing its efficacy and reproducibility. Another strength is that our model uses physician-initiated patient referrals and includes direct communication with oncologists and detailed medical screening needed for personalized exercise. Finally, the term rehabilitation means to restore back to normal, and this is a major intent of all rehabilitation programs. We evaluated our data using age and gender-matched norms with the goal of achieving at least average status when compared with the apparently healthy population. The Phase Program proposed here meets this standard, and we suggest that this be a method for evaluating the effectiveness of exercise-based rehabilitation.

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CONCLUSION

Despite the prevalence and abundance of exercise-based programs, standardization of both the methodology and anticipated outcomes does not exist currently. Specific recommendations regarding mode, intensity, frequency, and duration of exercise for cancer survivors is lacking because of the range of cancer types, varying treatments, and timeline of treatment, particularly in regard to exercise during and after treatment. As a result, numerous studies have failed to adhere to the principles of exercise training, which guide appropriate exercise intervention for this population. The Phase Program is an attempt to improve the clarity of exercise prescription for cancer survivors. Data from this study provide evidence in support of a structured, individualized, exercise-based intervention for cancer patients, which adheres to the principles of exercise training and relies on consistent and timely assessment to augment prescription accuracy. The Phase Program expands on guidelines created by ACSM, adding precision and modification of intensity, while establishing unique goals that address the multifaceted treatment timeline of cancer patients. It is scalable, it provides clinicians the flexibility to individualize exercise, while remaining clear and reproducible, and it is supported by empirical evidence demonstrating significant physiological and psychological improvements in cancer survivors.

The authors thank all members of UNCCRI who assisted with this study. They also recognize Dr. Carole Schneider, the founder and creator of UNCCRI. The authors did not receive funding for this study.

Authors have no professional relationships with companies or manufactures who will benefit from the results of the present study. The results of the present study do not constitute endorsement by the ACSM.

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REFERENCES

1. Schneider CM, Dennehy CA, Carter SD. Exercise and Cancer Recovery. Champaign (IL): Human Kinetics; 2003.
2. Dauchy S, Dolbeault S, Reich M. Depression in cancer patients. EJC Suppl. 2013;11(2):205–15.
3. Lee JI, Kim SH, Tan AH, et al. Decreased health-related quality of life in disease-free survivors of differentiated thyroid cancer in Korea. Health Qual Life Outcomes. 2010;8(1):101.
4. Dittus KL, Lakoski SG, Savage PD, et al. Exercise-based oncology rehabilitation: leveraging the cardiac rehabilitation model. J Cardiopulm Rehabil Prev. 2015;35(2):130.
5. Cormie P, Zopf EM, Zhang X, Schmitz KH. The impact of exercise on cancer mortality, recurrence, and treatment-related adverse effects. Epidemiol Rev. 2017;39(1):71–92.
6. Rock CL, Doyle C, Demark-Wahnefried W, et al. Nutrition and physical activity guidelines for cancer survivors. CA Cancer J Clin. 2012;62(4):43–74.
7. Schmitz KH, Courneya KS, Matthews C, et al. American College of Sports Medicine roundtable on exercise guidelines for cancer survivors. Med Sci Sports Exerc. 2010;42(7):1409–26.
8. Kimmel GT, Haas BK, Hermanns M. The role of exercise in cancer treatment: bridging the gap. Transl J Am Coll Sports Med. 2016;1(17):152–8.
9. Schwartz AL, De Heer HD, Bea JW. Initiating exercise interventions to promote wellness in cancer patients and survivors. Oncology (Williston Park). 2017;31(10):711–7.
10. Kirkham AA, Bonsignore A, Bland KA, et al. Exercise prescription and adherence for breast cancer: one size does not FITT all. Med Sci Sports Exerc. 2018;50(2):177–86.
11. Speck RM, Courneya KS, Mâsse LC, Duval S, Schmitz KH. An update of controlled physical activity trials in cancer survivors: a systematic review and meta-analysis. J Cancer Surviv. 2010;4(2):87–100.
12. Campbell KL, Neil SE, Winters-Stone KM. Review of exercise studies in breast cancer survivors: attention to principles of exercise training. Br J Sports Med. 2012;46(13):909–16.
13. Nadler M, Bainbridge D, Tomasone J, Cheifetz O, Juergens RA, Sussman J. Oncology care provider perspectives on exercise promotion in people with cancer: an examination of knowledge, practices, barriers, and facilitators. Support Care Cancer. 2017;25(7):2297–304.
14. Piper BF, Dibble SL, Dodd MJ, Weiss MC, Slaughter RE, Paul SM. The revised piper fatigue scale: psychometric evaluation in women with breast cancer. Oncol Nurs Forum. 1998;25(4):677–84.
15. Shackelford DYK, Brown JM, Peterson BM, Schaffer J, Hayward R. Validation of the University of Northern Colorado Cancer Rehabilitation Institute Treadmill Protocol. Int J Phys Med Rehabil. 2017;5(6):437.
16. Brzycki M. Strength testing—predicting a one-rep max from reps-to-fatigue. J Phys Educ Recreat Dance. 1993;64(1):88–90.
17. Kuehl R, Scharhag-Rosenberger F, Schommer K, et al. Exercise intensity classification in cancer patients undergoing allogeneic HCT. Med Sci Sports Exerc. 2015;47(5):889–95.
18. Swenson KK, Nissen MJ, Ceronsky C, Swenson L, Lee MW, Tuttle TM. Comparison of side effects between sentinel lymph node and axillary lymph node dissection for breast cancer. Ann Surg Oncol. 2002;9(8):745–53.
19. Sattelmair J, Pertman J, Ding EL, Kohl HW 3rd, Haskell W, Lee IM. Dose response between physical activity and risk of coronary heart disease. Circulation. 2011;124(7):789–95.
20. Blair SN, Kampert JB, Kohl HW 3rd, et al. Influences of cardiorespiratory fitness and other precursors on cardiovascular disease and all-cause mortality in men and women. JAMA. 1996;276(3):205–10.
21. Holmes MD, Chen WY, Feskanich D, Kroenke CH, Colditz GA. Physical activity and survival after breast cancer diagnosis. J Am Med Assoc. 2005;293(20):2479–86.
22. Meyerhardt JA, Heseltine D, Niedzwiecki D, et al. Impact of physical activity on cancer recurrence and survival in patients with stage III colon cancer: findings from CALGB 89803. J Clin Oncol. 2006;24(22):3535–41.
23. Schneider CM, Hsieh CC, Sprod LK, Carter SD, Hayward R. Cancer treatment-induced alterations in muscular fitness and quality of life: the role of exercise training. Ann Oncol. 2007;18(12):1957–62.
24. Lira FS, Neto JC, Seelaender M. Exercise training as treatment in cancer cachexia. Appl Physiol Nutr Metab. 2014;39(6):679–86.
25. Scott JM, Khakoo A, Mackey JR, Haykowsky MJ, Douglas PS, Jones LW. Modulation of anthracycline-induced cardiotoxicity by aerobic exercise in breast cancer. Circulation. 2011;124(5):642–50.
26. Puetz TW, Herring MP. Differential effects of exercise on cancer-related fatigue during and following treatment: a meta-analysis. Am J Prev Med. 2012;43(2):e1–24.
27. Schneider CM, Hsieh CC, Sprod LK, Carter SD, Hayward R. Effects of supervised exercise training on cardiopulmonary function and fatigue in breast cancer survivors during and after treatment. Cancer. 2007;110(4):918–25.
28. Schmidt ME, Wiskemann J, Armbrust P, Schneeweiss A, Ulrich CM, Steindorf K. Effects of resistance exercise on fatigue and quality of life in breast cancer patients undergoing adjuvant chemotherapy: a randomized controlled trial. Int J Cancer. 2015;137(2):471–80.
29. Nieman DC. Exercise, upper respiratory tract infection, and the immune system. Med Sci Sports Exerc. 1994;26(2):128–39.
30. Zaorsky NG, Churilla TM, Egleston BL, et al. Causes of death among cancer patients. Ann Oncol. 2017;28(2):400–7.
31. Baumann FT, Zimmer P, Finkenberg K, Hallek M, Bloch W, Elter T. Influence of endurance exercise on the risk of pneumonia and fever in leukemia and lymphoma patients undergoing high dose chemotherapy. A pilot study. J Sports Sci Med. 2012;11(4):638.
32. Quist M, Rorth M, Zacho M, et al. High-intensity resistance and cardiovascular training improve physical capacity in cancer patients undergoing chemotherapy. Scand J Med Sci Sports. 2006;16(5):349–57.
33. Hornsby WE, Douglas PS, West MJ, et al. Safety and efficacy of aerobic training in operable breast cancer patients receiving neoadjuvant chemotherapy: a phase II randomized trial. Acta Oncol. 2014;53(1):65–74.
34. Ganz PA, Kwan L, Stanton AL, Bower JE, Belin TR. Physical and psychosocial recovery in the year after primary treatment of breast cancer. J Clin Oncol. 2011;29(9):1101–9.
35. Pinto BM, Trunzo JJ, Reiss P, Shiu SY. Exercise participation after diagnosis of breast cancer: trends and effects on mood and quality of life. Psychooncology. 2002;11(5):389–400.
36. De Backer IC, Van Breda E, Vreugdenhil A, Nijziel MR, Kester AD, Schep G. High-intensity strength training improves quality of life in cancer survivors. Acta Oncol. 2007;46(8):1143–51.
37. Kampshoff CS, Chinapaw MJ, Brug J, et al. Randomized controlled trial of the effects of high intensity and low-to-moderate intensity exercise on physical fitness and fatigue in cancer survivors: results of the Resistance and Endurance exercise After ChemoTherapy (REACT) study. BMC Med. 2015;13:275.
38. Winters-Stone KM, Dobek J, Bennett JA, Nail LM, Leo MC, Schwartz A. The effect of resistance training on muscle strength and physical function in older, postmenopausal breast cancer survivors: a randomized controlled trial. J Cancer Surviv. 2012;6(2):189–99.
39. Cox KL, Burke V, Gorely TJ, Beilin LJ, Puddey IB. Controlled comparison of retention and adherence in home- vs center-initiated exercise interventions in women ages 40–65 years: the S.W.E.A.T. study (Sedentary Women Exercise Adherence Trial). Prev Med. 2003;36(1):17–29.
40. Perri MG, Anton SD, Durning PE, et al. Adherence to exercise prescriptions: effects of prescribing moderate versus higher levels of intensity and frequency. Health Psychol. 2002;21(5):452.
41. Cadmus LA, Salovey P, Yu H, Chung G, Kasl S, Irwin ML. Exercise and quality of life during and after treatment for breast cancer: results of two randomized controlled trials. Psychooncology. 2009;18(4):343–52.
42. Haas BK, Kimmel G. Model for a community-based exercise program for cancer survivors: taking patient care to the next level. J Oncol Pract. 2011;7(4):252–6.
43. Haas BK, Kimmel G, Hermanns M, Deal B. Community-based FitSTEPS for life exercise program for persons with cancer: 5-year evaluation. J Oncol Pract. 2012;8(6):320–4.
44. Farrell SW, Braun L, Barlow CE, Cheng YJ, Blair SN. The relation of body mass index, cardiorespiratory fitness, and all-cause mortality in women. Obes Res. 2002;10(6):417–23.

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