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Exercise Prescription and Adherence for Breast Cancer: One Size Does Not FITT All

KIRKHAM, AMY, A.1; BONSIGNORE, ALIS2; BLAND, KELCEY, A.3; MCKENZIE, DONALD, C.2; GELMON, KAREN, A.3; VAN PATTEN, CHERI, L.4; CAMPBELL, KRISTIN, L.1,5

Medicine & Science in Sports & Exercise: February 2018 - Volume 50 - Issue 2 - p 177–186
doi: 10.1249/MSS.0000000000001446
CLINICAL SCIENCES

Purpose To prospectively assess adherence to oncologist-referred, exercise programming consistent with current recommendations for cancer survivors among women with early breast cancer across the trajectory of adjuvant treatment.

Methods Sixty-eight women participated in supervised, hour-long, moderate-intensity, aerobic, and resistance exercise thrice per week during adjuvant chemotherapy ± radiation, with a step-down in frequency for 20 additional weeks. Adherence to exercise frequency (i.e., attendance), intensity, and time/duration, and barriers to adherence were tracked and compared during chemotherapy versus radiation, and during treatment (chemotherapy plus radiation, if received) versus after treatment.

Results Attendance decreased with cumulative chemotherapy dose (cycles 1–2 vs cycles 3–8, cycle 3 vs cycles 7–8, all P ≤ 0.05) and was lower during chemotherapy than radiation (64% ± 25% vs 71% ± 32%, P = 0.02) and after treatment than during treatment (P < 0.01). Adherence to exercise intensity trended toward being higher during chemotherapy than radiation (69% ± 23% vs 51% ± 38%, P = 0.06) and was higher during than after treatment (P = 0.01). Adherence to duration did not differ with treatment. Overall adherence to the resistance prescription was poor, but was higher during chemotherapy than radiation (57% ± 23% vs 34% ± 39%, P < 0.01) and was not different during than after treatment. The most common barriers to attendance during treatment were cancer-related (e.g., symptoms, appointments), and after treatment were life-related (e.g., vacation, work).

Conclusions Adherence to supervised exercise delivered in a real-world clinical setting varies among breast cancer patients and across the treatment trajectory. Behavioral strategies and individualization in exercise prescriptions to improve adherence are especially important for later chemotherapy cycles, after treatment, and for resistance exercise.

1Department of Rehabilitation Sciences, University of British Columbia, Vancouver, BC, CANADA; 2Department of Kinesiology, University of British Columbia, Vancouver, BC, CANADA; 3Department of Medical Oncology, British Columbia Cancer Agency, Vancouver, BC, CANADA; 4Department of Oncology Nutrition, British Columbia Cancer Agency, Vancouver, BC, CANADA; and 5Department of Physical Therapy, British Columbia Cancer Agency, Vancouver, BC, CANADA

Address for correspondence: Kristin Campbell, Ph.D., 212-2177 Wesbrook Mall, Vancouver, Canada V6T1Z3; E-mail: Kristin.Campbell@ubc.ca.

Submitted for publication June 2017.

Accepted for publication September 2017.

Supplemental digital content is available for this article. Direct URL citations appear in the printed text and are provided in the HTML and PDF versions of this article on the journal’s Web site (www.acsm-msse.org).

The American College of Sports Medicine (ACSM) published a roundtable consensus document on exercise guidelines for cancer survivors in 2010 (1). Similar to the physical activity guidelines for American adults, these guidelines report that benefits for health- and cancer-related side effects can be achieved by performing 150 min of moderate intensity, or 75 min of vigorous-intensity aerobic exercise per week, and resistance training for major muscle groups at least twice per week (1,2). Further published exercise recommendations for cancer survivors include an initial dose of three moderate-intensity, 20-min walking sessions per week with progression as tolerated (3), and an aerobic intensity prescription of 50% to 75% of HR reserve (HRR), or a rating of perceived exertion (RPE) of 11 to 14 (4). These guidelines are not specific with respect to exercise being performed during active cancer treatment or after completion of treatment. Given the wide variation in treatment symptoms and side effects, it seems prudent to incorporate flexibility into exercise prescriptions used during chemotherapy, in particular.

Accurate reporting of both the exercise prescription goal and the extent to which the behavior of exercise program participants correspond with the goal (i.e., adherence) is required to ensure that resulting health outcomes can be attributed to the intervention and to assist exercise professionals to translate research into clinical practice. The majority of published exercise intervention studies in breast cancer have incompletely reported the exercise prescription as well as adherence to each of the exercise prescription components (frequency, intensity, time/duration, type, progression) (5). Furthermore, the exercise prescriptions used and patterns of adherence achieved in efficacy trials of exercise during chemotherapy for breast cancer that have been published to-date are likely not a realistic representation of what might be expected for programming in a real-world setting.

The primary purpose of this study was to assess adherence of women with breast cancer to a supportive care exercise program that spanned the adjuvant treatment trajectory and is consistent with the recommended exercise prescription for cancer survivors; namely, to 1) describe and compare adherence to the prescribed frequency, intensity and duration during chemotherapy, during radiation, and after treatment completion; and 2) to describe barriers to adherence across the treatment trajectory. A secondary purpose was to describe and assess three novel methods of adjusting the exercise prescription to accommodate for individual variability and the dynamic nature of chemotherapy therapy.

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METHODS

Design and participants

The Nutrition and Exercise during adjuvant Treatment (NExT) study was a single-arm, oncologist-referred lifestyle program, consisting of supervised exercise and a single 2-h group nutrition information session offered free-of-charge as supportive care for women with stage I–III breast cancer who were scheduled to receive adjuvant chemotherapy with or without radiation. Participants had to enroll in the program within the first half of chemotherapy treatment, have a body mass index <40 kg·m−2, and speak English. The British Columbia Cancer Agency Research Ethics Board approved this study. Participants signed an informed consent. The primary study results have been previously reported (6).

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Exercise program and prescription

There were three distinct study phases with different exercise prescriptions (Table 1): 1) treatment phase (thrice per week for the length of chemotherapy, plus radiation, if received); 2) posttreatment phase (twice per week for the following 10 wk); 3) maintenance phase (once per week for an additional 10 wk). The supervised aerobic and resistance exercise program took place at a private research gym near the treatment center on Mondays, Wednesdays, and Fridays during normal business hours, excluding statutory holidays. Available equipment included treadmills, ellipticals, upright and recumbent cycle ergometers, resistance machines and dumbbells. Participants performed their individualized program at prespecified drop-in times with oversight by staff in a ratio of one staff to four participants. Staff included a paid exercise trainer and graduate and undergraduate students in kinesiology or a related program. Participants were also encouraged to perform aerobic exercise at home to work toward achieving a total of 150 min·wk−1 of moderate-intensity aerobic activity.

TABLE 1

TABLE 1

To accommodate for individual variability and the dynamic nature of chemotherapy, we tested the benefits of three approaches to exercise prescription. First, the HRR method was used to prescribe aerobic intensity based on our previous work, indicating that it is accurate in achieving the desired intensity in women with breast cancer both during and after chemotherapy treatment (8). In a previous exercise study in a similar population completed by members of our team (9), wide variations in resting HR (HRrest) and subjective assessment of intensity were noted when using the same target heart throughout adjuvant chemotherapy treatment. Thus, in an attempt to maintain a consistent exercise intensity, HRrest was measured approximately once per week during treatment and was used to calculate new HR targets for the supervised exercise. After treatment completion, HRrest was measured once every 5 wk. HRrest was measured as the lowest HR during the last 30 s of a 5-min period of quiet, seated rest, in a hard-backed chair with back against the chair, feet flat on the floor, and arms and legs uncrossed and relaxed (10). The age-predicted maximal HR (APMHR) was estimated via 206 – 0.88 × age (11). As a preliminary assessment of whether adjusting the HR target for chemotherapy-related changes in HRrest would maintain the desired relative exercise intensity level, we completed a separate substudy of 13 early stage breast cancer patients receiving doxorubicin and cyclophosphamide chemotherapy. They performed a 30-min treadmill session at 70% HRR using the same prescription method as above before starting treatment and again the day before the fourth treatment when HRrest might be expected to have changed. The target HR, average HR, %HRR, and RPE were compared between these two sessions.

Second, to accommodate for the dynamic nature of chemotherapy treatment symptoms, a standardized prescription adjustment method was used for the “bad days” when participants felt particularly unwell upon arrival to the gym. Based on our previous observation that aerobic intensity is often the more difficult aspect of the prescription for adherence with increased treatment symptoms, the standardized adjustment was chosen as a 10 percentage point reduction in the prescribed aerobic exercise intensity for that session only (e.g., planned intensity of 60%–65% HRR was reduced to 50%–55% HRR). Intensity was also reduced by 10 percentage points or more on a case-by-case basis for participants who were consistently unable to meet their HR target or after extended absences from the gym. In those cases, the intensity was gradually returned to the goal, as tolerated. For participants on ß-blockers, intensity was prescribed as a RPE of 13, which typically corresponded to 40% to 45% HRR. The adjustment approach was assessed by the proportion of sessions where the new HR target was met, as well as comparison of the average RPE between sessions with and without an adjusted prescription.

Third, participants who reported performing at least three 30-min sessions per week of moderate-intensity aerobic exercise in the month before enrollment started the program with an advanced exercise prescription, whereas all others received the standard prescription to individualize the initial prescription for recent exercise behavior (Table 1).

Regarding exercise prescription after completion of treatment, aerobic interval sessions were introduced to reduce monotony and maintain engagement for participants without a history of cardiovascular disease, or current heart medications, dyspnea/asthma issues, or injuries limiting exercise intensity (Table 1). The ACSM metabolic equation for treadmill walking (12) was used to prescribe the required treadmill grade to achieve the prescribed intensity at each participant’s preferred treadmill speed. The peak oxygen consumption used in this calculation was estimated from a modified Balke submaximal treadmill test performed at the end of the treatment and posttreatment phases. If the interval sessions were performed on the cycle ergometer or elliptical, the HRR method was used to prescribe HR zones (i.e., target HR corresponding to the two intensities ±3 bpm.)

The resistance exercise prescription consisted of one set of 10 to 12 repetitions at 50% of estimated one-repetition maximum (1-RM) for leg press and chest press (9,13) and a similar RPE for leg curls, calf raises, seated row, biceps curls, and triceps extensions in the first week, and two sets in the second week onward. Weight was increased every 4 wk by the smallest possible increment up to 75% of 1-RM. Two core-strengthening exercises were completed until fatigue or technique breakdown. After treatment completion, the resistance program remained the same except that weight progressions continued up to 75% of the new 1-RM assessed at the end of the treatment and posttreatment phases.

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Outcome measures

Demographics were collected at baseline with a short questionnaire and treatment and diagnosis characteristics were extracted from medical records. To determine adherence to frequency (i.e., attendance) and barriers to adherence, missed supervised exercise sessions were recorded, and a reason was collected from the participant by phone, email or at their next session. Attendance was calculated as: number of attended exercise sessions/total prescribed sessions. For aerobic exercise specifically, adherence to the prescribed intensity, duration, and progression was assessed. The completed duration and intensity (i.e., average HR) of each aerobic exercise session were recorded, and a reason was collected if that session’s target was not met. Adherence to intensity and duration were calculated as the percentage of sessions where the lower limit of the target was met or exceeded. The occurrences and reasons for adjustments in aerobic exercise intensity were recorded by the study staff. For resistance exercise, adherence to the prescribed exercise type, as well as the prescribed intensity (weight) and time (sets, repetitions) for each exercise, was assessed. Adherence to frequency, intensity, and duration were calculated for each phase and for chemotherapy and radiation separately. For simplicity, barriers to adherence and reasons for prescription adjustments were compiled for the treatment phase, and the posttreatment and maintenance phases combined only. Participants who withdrew before completing any exercise sessions were excluded.

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Statistics

Descriptive statistics, counts and frequencies were used to characterize the study participants and their adherence. Paired t tests were used to assess the changes in target HR, HRrest, %HRR, and RPE for the substudy. A generalized estimating equation (GEE) was used to compare adherence variables between chemotherapy and radiation, and between the treatment phase (chemotherapy ± radiation) and after treatment (posttreatment and maintenance phases combined). This model does not require normality or equal variances of the data and accounts for correlation of responses within subjects in longitudinal data sets (14). SPSS Version 24.0 (IBM Corporation, Armonk, NY) was used to fit the model with a Tweedie distribution (mixed distribution) and an identity link function. Time was used as a repeated and fixed factor. To assess the effect of treatment protocol and cycle number, attendance during the first four cycles of docetaxel and cyclophosphamide was compared with attendance during the first four cycles of doxorubicin and cyclophosphamide also using a GEE with a protocol by cycle number interaction, and protocol and cycle main effects. Attendance was also compared using a GEE among all eight cycles of those receiving four cycles of paclitaxel after doxorubicin and cyclophosphamide. Contrasts were used to interpret significant interactions or main effects. A P value ≤0.05 was considered significant. Sample size was planned as the number recruited within 12 months as a measure of yearly intake for a potential clinical program, but was later extended to 15 months upon securing additional funding.

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RESULTS

Participants

In total, 109 patients were referred, 93 were eligible, and 73 (88%) enrolled, but five withdrew before doing any exercise sessions and were excluded (Fig. 1). Baseline characteristics for the remaining 68 participants are described in Table 2. Another four withdrew during chemotherapy but were included in the chemotherapy and treatment phase attendance data with the primary withdrawal reason (Fig. 1) used as the barrier to attendance of the remaining sessions. The program length was 45 ± 8 wk. Table 3 shows the average adherence to frequency, intensity and duration across participants for chemotherapy, radiation, and each study phase.

TABLE 2

TABLE 2

TABLE 3

TABLE 3

FIGURE 1

FIGURE 1

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Adherence to overall program frequency

During the treatment phase (which includes the time between chemotherapy and radiation), 2779 exercise sessions were attended out of 4804 prescribed sessions (58%). During chemotherapy only, 1891 sessions were attended out of 3023 (63%) prescribed sessions. The effect of chemotherapy protocol on attendance did not differ across the first four cycles of treatment (P = 0.74). Chemotherapy protocol also did not significantly affect overall attendance (P = 0.50). Attendance did vary across the first four cycles among both treatment protocols, where it was significantly lower during cycles 3 and 4 than cycles 1 and 2 (all P ≤ 0.01) (Fig. 2A). For those receiving eight cycles of treatment (i.e., 4× doxorubicin + cyclophosphamide, then 4× paclitaxel), attendance during cycles 1 to 2 was significantly higher than cycles 3 to 8 (all P ≤ 0.01), cycles 3 to 6 did not differ from each other (all P > 0.05), and cycles 7 to 8 were also lower than cycle 3 (both P ≤ 0.05) (Fig. 2A). During radiation treatment only, the 56 participants who received radiation (and excluding one participant who moved away before starting radiation) attended 488 (70%) of 697 sessions prescribed. Attendance during radiation was significantly higher than during chemotherapy (P = 0.02).

FIGURE 2

FIGURE 2

During the posttreatment phase, 673 of 1209 (56%) prescribed sessions were attended, whereas during the maintenance phase, 320 prescribed sessions of 601 (53%) were attended. Attendance after treatment was significantly lower than during treatment (P < 0.01). The barriers to adherence are listed in Table 4.

TABLE 4

TABLE 4

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Adherence to aerobic exercise intensity and duration

The variation in weekly HRrest measurements is shown in figure form in the supplemental digital content to illustrate a basis for the recalculation of HRR for the aerobic exercise sessions during treatment (see Figure, Supplemental Digital Content 1, Variation in weekly measurements of resting HR, http://links.lww.com/MSS/B64). For the substudy, there was a significant increase in HRrest from prechemotherapy to the day before the fourth chemotherapy (71 ± 9 to 78 ± 13 bpm, P = 0.03). The target HR also increased significantly by 3 ± 2 bpm (min, 0; max, 10 bpm increase, P = 0.04), but average achieved %HRR did not change (P = 0.20). RPE was significantly reduced (13.7 ± 1.0 to 12.8 ± 1.4, P = 0.01).

Seven (10%) participants qualified for the advanced exercise prescription of intensity and duration, and the remaining 61 participants performed the standard prescription. For both prescriptions combined, there was a trend toward higher adherence to intensity during chemotherapy than radiation (P = 0.06), whereas adherence to duration did not differ (P = 0.30) (Table 3). Figures 2B and 2C show the percentage of sessions where the intensity and duration prescriptions were met for each step of the prescription progressions in the standard prescription group, whereas the same figure for the advanced prescription group is in Figure, Supplemental Digital Content 2, Adherence to (A) intensity and (B) duration for each step of progression over the first 12 wk of the study, http://links.lww.com/MSS/B65.

There were 449 interval sessions and 492 continuous intensity sessions performed in total during the posttreatment and maintenance phases. Adherence to the intensity prescription after treatment, whether interval or continuous, was significantly lower than during treatment (P = 0.01), whereas adherence to duration did not differ (P = 0.86).

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Aerobic intensity adjustments

During the treatment phase, there were aerobic intensity adjustments in 542 exercise sessions (20% of all sessions). Forty (59%) participants required at least one adjustment. The reasons for the adjustments included treatment symptoms (38%), use of ß-blockers (28%), the prescription being consistently too difficult (20%), asthma symptoms (7%), extended gym absence (5%), and other illness (2%). In 68% of all adjusted sessions, participants adhered to the new prescribed target. For those who received adjustments, their average RPE did not differ between adjusted (12.7 ± 1.0) and nonadjusted (12.7 ± 0.7, P = 0.97) sessions. In contrast, after treatment, there were no adjustments made for treatment symptoms, yet there were adjustments to the prescription in 169 exercise sessions (34% of all sessions) due to ß-blockers (43%), asthma, or other symptom threshold (18%), intensity consistently too difficult (15%), extended absence from the gym (14%), and cold, flu, or injury (6%).

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Adherence to resistance exercise intensity, time, and type

The descriptive statistics for overall adherence to the resistance program at the individual level are shown in Table 3, whereas adherence to each different exercise is shown in table format in Table, Supplemental Digital Content 3, Adherence rates to each resistance exercise type, http://links.lww.com/MSS/B66. Adherence was not different during versus after treatment (P = 0.63), but was higher during chemotherapy than radiation (57 ± 23 vs 34 ± 39, P < 0.01).

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DISCUSSION

This study provides comprehensive documentation of patterns of adherence to the frequency, intensity, duration/time, type, and progressions recommended for cancer survivors delivered via a supervised exercise program in a supportive care setting for a generalizable sample of women with early-stage breast cancer during and after adjuvant chemotherapy and radiation. An understanding of the feasibility of the recommended exercise prescription is important for designing future efficacy studies, for ensuring effectiveness in clinical or community-based programs, and in planning for additional behavioral support or supervision for particular exercise prescriptions or at particular time points during treatment where adherence is more challenging. Furthermore, this study assessed novel methods of prescription adjustment specifically for chemotherapy.

A key study finding was assessing the attendance that could be expected in a clinical program in comparison to a randomized control trial. The efficacy of exercise to attenuate the negative effects of chemotherapy on health-related physical fitness and quality of life for women with breast cancer has been primarily established by three large (n ≥ 230) randomized trials of supervised exercise in breast cancer patients during adjuvant chemotherapy (START (15), CARE (9), and PACES (16)). Average attendance for these aerobic (with or without resistance) exercise interventions were 72% ± 30% (17) and 73% ± 24% (18) for three times per week, or 71% (SD not reported) (16) for twice per week interventions. Reported attendance for other smaller randomized control trials of exercise during adjuvant chemotherapy and/or radiation therapy for breast cancer occurring twice to thrice per week ranges from 70% to 83%, typically with large SD (19–23). In comparison to these efficacy trials, the attendance reported in our single-arm effectiveness trial for chemotherapy only was marginally lower at 64% ± 25% to three weekly sessions. This is notable because our trial had more inclusive eligibility criteria and less emphasis on required adherence than those used in efficacy trials. Attendance was not statistically different among chemotherapy protocols but decreased with cumulative chemotherapy dose, which also likely corresponds with increasing symptoms, suggesting a greater need for behavioral support, more flexible gym schedules, or home-based programming during the later chemotherapy treatments to maintain exercise consistency throughout treatment. Attendance was higher (71% ± 32%) while receiving daily radiation treatments than during chemotherapy, which could be due to the shorter length of treatment and fewer side effects with radiation, as well as the close proximity (three to four blocks) of the gym to the radiation treatment center.

The barriers to attendance differed across the treatment trajectory. Consistent with the START trial (24), the top barrier during the treatment phase was treatment symptoms (33%). In the START trial, cancer-related barriers (e.g., treatment symptoms, appointments) accounted for 53% of the missed sessions in total (24), which is similar to the current study (59%). Life-related barriers (e.g., vacation, taking care of family members, visitors, work, transportation issues, and cold/flu) accounted for 34% of missed sessions in the START trial and 40% in the current study. In contrast, after treatment, life-related barriers (primarily vacation and work) accounted for the majority of missed sessions (60%). Other potential barriers to adherence during this time could include a reduction in social connections with the exercise trainers and other participants with reduced program frequency, and a lack of variation in the resistance prescription. Barriers to attendance would impede delivery of a specific dose of exercise that may be required to address treatment-related side effects in future studies. Expanding gym hours and allowing make-up sessions on alternate days could help improve attendance.

To our knowledge, adherence to the progressions in intensity or duration during chemotherapy has not been previously reported, whereas adherence to the prescribed intensity and duration of aerobic exercise sessions has either not been reported or incompletely reported (5). Nearly all participants adhered to the prescribed 20-min duration in the first week of the current study’s prescription. Adherence dropped to approximately 70% when the prescription was increased to 30 min in week 4, but between weeks 5 and 7, whereas the prescription remained at 30 min, adherence steadily increased. This observation indicates that 20 min is a feasible initial duration and that 30 min is feasible with the appropriate progression; adding an extra week or two to the progression may help with this transition. Secondary analysis of the aerobic arm of the START trial reported 69% ± 30% adherence to the prescribed duration that progressed to a maximum of 45 min (25). The current study’s average adherence of 82% ± 20% for chemotherapy was for a maximum duration of 30 min, which suggests that 30 min may be a more achievable target during adjuvant treatment.

Adherence to the prescribed intensity was lower than adherence to duration across the treatment trajectory. In the first 6 wk while the intensity was progressed from 50%–55% to 60%–65% HRR, participants adhered to the prescribed intensity in approximately 80% of sessions. From week 7 onward, where the intensity was 65% to 75% HRR, adherence was reduced to approximately 65%, indicating that intensities at or above 65% HRR are more challenging during chemotherapy. Secondary analysis of the aerobic arm of the START trial reported adherence to the prescribed intensity of 60%–80% of peak oxygen consumption (which would be slightly more intense than 60%–80% %HRR or %V˙O2R) as 63% ± 30% (25) compared with the average of 69% ± 23% in the current study. The higher adherence to intensity during chemotherapy in the START trial relative to the current study, as well as during treatment relative to posttreatment in the current study could be related to the prescription adjustments for changes in HRrest that were made weekly during treatment in the current study.

Although there is not a strong consensus as to the best method for prescribing aerobic exercise intensity in cancer survivors, especially during chemotherapy, members of our team have previously reported that the HRR method and the ACSM metabolic equation for treadmill walking were the most accurate for women with breast cancer in a cross-sectional study (8). The HRR method of prescription is based on the close matching between %HRR and % of volume of oxygen consumption reserve (V˙O2R) (e.g., 60% HRR is equivalent to 60% V˙O2R) (26). V˙O2R and HRR will both decrease with chemotherapy-related reductions in cardiorespiratory fitness and elevations in HRrest, but the relative change may not be equivalent. To our knowledge, there is no data to suggest that peak HR changes with chemotherapy treatment. The substudy within the current study examined the longitudinal influence of adjusting the target HR to account for the chemotherapy-related elevations in HRrest. Relative to the prechemotherapy exercise session, in the exercise session before the fourth chemotherapy treatment, participants were exercising at a significantly higher target HR (but same relative %HRR), and RPE was significantly reduced. This reduction in RPE could be partly attributed to familiarization, but the lack of increase in RPE with exercise performed at a higher absolute HR could also be indirect support that the reduction in HRR occurring during chemotherapy matches the reduction in V˙O2R. Empirical testing is required to objectively confirm that the chemotherapy-related changes in HRR correspond to changes in V˙O2R, but the required study design (i.e., multiple maximal incremental and steady state exercise tests) would be challenging to execute during chemotherapy treatment.

Other novel methods of tailoring the aerobic exercise prescription used in the current study included a standardized 10-percentage point intensity reduction to accommodate for treatment symptoms and using recent exercise levels to triage participants into different initial prescriptions. The prescribed intensity was reduced for 20% of all exercise sessions during the treatment phase. In over two thirds of adjusted sessions, the new target HR was met, and RPE was similar for adjusted sessions relative to unadjusted sessions, suggesting that the adjustment method was effective. It was reported that prescriptions in the CARE trial were modified based on participants’ exercise experience or treatment symptoms (18), but a standardized approach like that used in the current study was reported. Regarding our use of recent exercise levels to triage participants, the adherence of seven participants, who were eligible for the advanced stream of the exercise prescription ranged from 95%–100% and 76%–95% to the prescribed durations and intensities over each week of the study, suggests that a simple question regarding recent exercise behavior may be an effective standardized approach to individualize initial prescriptions.

In the current study, the most common barrier to adherence to the prescribed intensity or duration was that the prescription felt too difficult in the absence of any particular treatment symptom (27% during treatment, 58% after treatment). Potential reasons for this are that the APMHR overestimated actual peak HR or that the prescribed intensity was above these participants’ anaerobic thresholds. The second most common barrier during treatment was treatment symptoms (20%), which were also the major barriers to adherence in an randomized control trial of aerobic exercise training during neoadjuvant chemotherapy for breast cancer (23). In addition, technical challenges with HR monitors or staff members’ provision of prescriptions to participants affected adherence. Using watches with ongoing average HR indicators as well as one-on-one supervision by paid (vs volunteer) trainers could reduce these challenges, but would increase cost and reduce the social benefits of group-based exercise. Non–cancer-related injuries (e.g., plantar fasciitis, knee injuries) accounted for only 5% of barriers during treatment potentially due to the gradual prescription progression, and use of warm-ups/cool-downs. After treatment, injuries were a more prominent barrier (15%), potentially due to the long exercise program length.

The average overall adherence to the prescribed resistance exercises, sets, repetitions, and weights ranged from 50% to 56% across the treatment trajectory. These poor adherence statistics indicate that there is a need to largely individualize the resistance prescription to accommodate for the wide variation in physical limitations noted among women with breast cancer across the trajectory from diagnosis through recovery (27). During the treatment phase, the intensity, time, or format of each specific resistance exercise type had to be modified in 17% to 23% of sessions. Upper body exercises were performed the least and required the most modifications in the treatment phase, which was likely related to the primary surgery, or the secondary surgery that 44% of participants received after chemotherapy. Notably, modifications continued to be required for upper body exercises after treatment. Adherence to the resistance and aerobic intensity prescriptions were higher during chemotherapy than during radiation, potentially due to cumulative fatigue or skin irritation at the site of radiation. An injury was a much more common barrier to adherence to resistance exercise than aerobic exercise. Individualization of prescriptions, injury prevention and monitoring practices, and a referral system to health care providers, such as physical therapists, are recommended to optimize safety of longer-term aerobic and resistance exercise training programs for women with breast cancer.

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Strengths and limitations

To our knowledge, this study is the most comprehensive assessment of adherence to supervised exercise during or after chemotherapy and radiation for breast cancer, with data collected for over 6500 prescribed exercise sessions. Another strength is that our setting and population more closely resembles that of a real-world clinical program rather than a tightly controlled randomized trial setting. We also developed and assessed three novel methods of adjusting the exercise prescription for chemotherapy. A limitation to the assessment of adherence to exercise intensity is the use of APMHR rather than measured peak HR to calculate target HR. Maximal exercise testing was not performed, because it is currently not the standard oncological care. The APMHR equation used was developed from a cohort of women (11), which may improve specificity over the generic equations. Exercise adherence was assessed for a 45+ week-long supervised, group-based program in an urban setting requiring travel and parking costs, and therefore, these results may not be entirely generalizable to shorter programs, one-on-one supervised exercise, home-based exercise, or programs in more rural areas. Furthermore, our samples were relatively highly educated and younger than the average woman diagnosed with breast cancer, and these factors could play important roles in adherence.

In summary, adherence to an exercise prescription consistent with the current recommended exercise prescription for cancer survivors varies among breast cancer patients and across the breast cancer treatment trajectory. Addressing barriers that impact adherence to prescribed frequency, intensity, duration, and progressions is necessary to implement exercise programming to target specific chemotherapy side effects in a research or clinical setting. Within clinical exercise programming for breast cancer, behavioral supportive strategies and flexibility in exercise prescriptions are especially important for later chemotherapy cycles, after treatment completion, and resistance exercise prescriptions.

The authors acknowledge the contributions of the students who helped with exercise supervision and collection of adherence data, as well as our participants.

The BC Cancer Foundation funded this study. A. K. was funded by the Canadian Institute of Health Research.

There are no conflicts of interest to declare for any authors. The results of the present study do not constitute endorsement by ACSM. The results of the study are presented clearly, honestly, and without fabrication, falsification, or inappropriate data manipulation.

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    Keywords:

    CHEMOTHERAPY; RADIATION; HEART RATE RESERVE; EXERCISE TRAINING; RESISTANCE TRAINING

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