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Evaluation of an Exercise-Based Phase Program
as Part of a Standard Care Model for
Cancer Survivors
Jessica Marlene Brown, Daniel Yoon Kee Shackelford, Maria Lyn Hipp, and Reid Hayward
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 physio-
logical toxicities affecting the cardiovascu-
lar, 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 treat-
ments (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 sur-
vivors (6), and the American College of
Sports Medicine (ACSM) established ex-
ercise guidelines endorsed by the American
Society of Clinical Oncology (7). In addi-
tion, the National Comprehensive Cancer
Network added guidelines to their inclu-
sive treatment recommendations (8). Exer-
cise 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 stan-
dardizing 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 sta-
tus, 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 physi-
ological and psychological assessments, and an individualized
exercise prescription and intervention using a Phase Program
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).
2379-286 8/0407/0 045–0054
Translational Journal of the ACSM
Copyright © 2019 by the American College of Sports Medicine
ABSTRACT
Exercise is a well-established method of alleviating cancer-related toxicities both
during and after treatment. However, specific exercise prescription recommenda-
tions for patients at varying points along the cancer continuum are not fully devel-
oped. The Phase Program of cancer rehabilitation was created to address this
issue. Purpose: This study aimed to evaluate the effectiveness of the Phase Pro-
gram on cardiorespiratory fitness (V
˙
O
2peak
), muscular strength (MS), and fatigue in
cancer survivors during and after treatment. Methods: A total of 183 cancer survi-
vors were included in this study. The Phase Program consisted of four, 12-wk, se-
quential phases representing differing time points from diagnosis, and prescribed
intensity, progression, and goals unique to each phase. Changes in V
˙
O
2peak
,leg
press MS, chest press MS, and fatigue were measured during transitions from phase
1tophase2,phase2tophase3,andphase3tophase4.Results: Eighty-one
patients completed the entire program with entry into phase 4, with 71% retention.
V
˙
O
2peak
, 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
˙
O
2peak
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 mul-
tifaceted needs of cancer survivors at different points along the cancer contin-
uum, nor do most exercise programs properly adhere to the principles of
exercise training necessary for a safe and effective intervention. The Phase Pro-
gram expands on current exercise guidelines providing more precise exercise
prescription. This study provides clear, reproducible, and empirical evidence of
its effectiveness.
http://www.acsm-tj.org Translational Journal of the ACSM 45
Original Investigation
Copyright © 2019 by the American College of Sports Medicine. Unauthorized reproduction of this article is prohibited.
(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 challeng-
ing (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: individual-
ity, 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 intensi-
ties 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 med-
ical history and direct patient referrals by anoncologist may be
necessary toensure safety and to individualize the exercise pre-
scription for the patient’s specific needs. As a result, it is diffi-
cult 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 un-
aware of the availability of exercise guidelines and lack knowl-
edge about when to implement them (13).
The Phase Program proposed here was created to address
these concerns while providing a clear method of exercise pre-
scription and intervention to alleviate treatment-related toxic-
ities in cancer survivors. Therefore, the purpose of this study
was to evaluate the effectiveness of the Phase Program on car-
diovascular fitness (V
˙
O
2peak
), muscular strength (MS), and
fatigue in a group of cancer survivors at each phase transition
and in those who completed the entire program. We hy-
pothesized that significant improvements would be made in
V
˙
O
2peak
, MS, and fatigue after completion of the Phase
Program, and that these improvements would be evident dur-
ing each phase transition.
METHODS
Participants
Patients were male and female (n= 183) cancer survivors 18 yr
and older who were undergoing or had completed surgical inter-
vention, chemotherapy, radiation therapy, immunotherapy, hor-
monal 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 clearedand 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 con-
sented to dissemination and interpretation of their assessment
values for research.
All participants were referred and cleared to participate in an ex-
ercise program by the supervising oncologist or primary care physi-
cian. 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 Univer-
sity of Northern Colorado’s Institutional Review Board.
Data Collection
The Phase Program of cancer rehabilitation uses a four-phase
system with assessments of physiological and psychological vari-
ables conducted at the beginning of each phase. Each reassess-
ment marked the completion of the phase and subsequent entry
into the next. The point of entry into the Phase Program was de-
termined by patient treatment status. Patients currently undergo-
ing 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 partici-
pant entered the Phase Program. Phases 1 through 3 are consid-
ered “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 en-
durance was evaluated using the cancer-specific UNCCRI Tread-
mill Protocol, which yields V
˙
O
2peak
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).
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 con-
ducted 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
Figure 1: Overview of the UNCCRI SCM.
46 Volume 4 •Number 7 •April 1 2019 Phase Program for Can cer Survivors
Copyright © 2019 by the American College of Sports Medicine. Unauthorized reproduction of this article is prohibited.
20 min designated for aerobic exercise, 30 min for resistance exer-
cise, 10 min for flexibility training, and balance exercises incorpo-
rated 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 jog-
ging. 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 (del-
toids, 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, medi-
cine 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 exer-
cises 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.
The Phase Program
The intensity and the general purpose of the individualized ex-
ercise 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 in-
tensity 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 as-
sessment results, and specifically the classifications achieved by
the participant during each assessment, were used for the selection
of appropriate starting intensities and progression prescribed dur-
ing the intervention. Higher assessment values resulted in the se-
lection of greater starting intensities (overload), whereas lower
functioning indicated the use of the lower ranges of intensity pre-
scribed for each phase (see Patient Overview, Supplemental Con-
tent 3, which dictates the exercise prescription of intensity and
progression for each patient in the Phase Program, http://links.
lww.com/TJACSM/A33).
PHASE 1
Phase 1 is designed for cancer survivors still receiving chemo-
therapy 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, re-
spectively, 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.
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 radi-
ation 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
Figure 2: Overview of the Phase Program.
http://www.acsm-tj.org Translational Journal of the ACSM 47
Copyright © 2019 by the American College of Sports Medicine. Unauthorized reproduction of this article is prohibited.
the principles of individuality and specificity andto begin incorpo-
rating progressive overload based on physiological assessment re-
sults and treatment-related functional deficits. Therefore, the goal
of phase 2 is to reduce the physical and functional limitations cre-
ated by cancer treatment and to improve cardiovascular and mus-
cular 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 chemo-
therapy 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 im-
prove functional capacity, assist with activities of daily living,
and enhance general movement patterns that are key to optimiz-
ing outcomes in subsequent phases.
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 exer-
cise 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 per-
form exercises with self-efficacy, they should have an understanding
of proper technique to avoid injury, and they should have a founda-
tional 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 be-
tween 60% and 85% of HRR and EST 1-RM. The rate of progres-
sion 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.
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 can-
cer 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.
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. Individ-
ual paired-sample t-testswereusedtoobtainapowerof0.95witha
medium effect size. According to the statistical program, to achieve
a power of 0.95, each statistical test suggested an Nof 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 fol-
lowing dependent variables were measured: V
˙
O
2peak
,EST1-RM
of the leg press, EST 1-RM of the chest press, and fatigue. The
following phase transitions (assessment vs reassessment) were eval-
uated: 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
TABLE 1.
Participant Demographics and Treatment Characteristics.
Demographic Characteristics N=183
Male, n70 (38%)
Female, n11 3 ( 6 2 % )
Age, yr 61 ± 13
Height (cm) 167 ± 10
Weight (kg) 79 ± 20
Cancer types N(%)
Breast 67 (37%)
Liquid 21 (12%)
Prostate 18 (10%)
Lung 18 (10%)
Head and neck 15 (8%)
Colorectal 11 (7%)
Gynecological 10 (6%)
Other 23 (13%)
Cancer stage N(%)
I43(24%)
II 45 (25%)
III 44 (24%)
IV 30 (16%)
Unknown/not staged 21 (12%)
Treatment demographics N(%)
Surgery only 25 (14%)
Chemotherapy only 19 (10%)
Radiation only 6 (3%)
Surgery and chemotherapy only 49 (27%)
Surgery and radiation only 31 (17%)
Chemotherapy and radiation only 6 (3%)
Surgery, chemotherapy, and radiation 45 (25%)
No treatment 2 (1%)
Average months since treatment 7.4 ± 15
Data are presented as the mean and frequency (percent) or mean ± SD.
48 Volume 4 •Number 7 •April 1 2019 Phase Program for Can cer Survivors
Copyright © 2019 by the American College of Sports Medicine. Unauthorized reproduction of this article is prohibited.
the Social Sciences software package (SPSS, Chicago, IL). All anal-
yses were two-tailed, and an alpha level of 0.05 was used to define
statistical significance.
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 partic-
ipants, with similar numbers representing liquid (12%), pros-
tate (10%), and lung cancers (10%). Cancer stages I, II, and
III were represented near equally (24%, 25%, and 24%, re-
spectively), and 16% were diagnosed as stage IV. Of the partic-
ipants, 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.
Of the 183 program participants, 81 (44%) completed the
entire Phase Program and entered phase 4. The mean atten-
dance for all subjects was 80% ± 3.8%, and the average reten-
tion 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 contin-
uation, total retention was 94%. Theaverage 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).
Changes in Peak Volume of Oxygen Consumption, MS,
and Fatigue
Table 3 summarizes absolute values (pre- to posttreatment) for
all phase transitions for V
˙
O
2peak
(mL·kg
−1
·min
−1
), leg press MS
(kg), chest press MS (kg), and fatigue. Fig. 3 depicts mean percent
change in V
˙
O
2peak
, leg press MS, chest press MS, and fatigue. Ad-
ditional assessment data and results can be viewed online (Supple-
mental Content 4, http://links.lww.com/TJACSM/A34).
PHASE 1TO 2TRANSITION
Statistically significant improvements were observed in V
˙
O
2peak
(P< 0.001), leg press MS (P<0.05),chestpressMS(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
˙
O
2peak
, 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 fa-
tigue classification from “moderate”to “mild”according to the
Piper Fatigue Inventory.
PHASE 2TO 3TRANSITION
When comparing data obtained at entry into phase 2 versus data
obtained after completion of phase 2 (i.e., entry into phase 3), sig-
nificant improvements were observed in V
˙
O
2peak
(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
˙
O
2peak
, 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 grad-
uated 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
˙
O
2peak
, 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 signif-
icantly lower (P< 0.05) when compared with values observed in
those who completed phase 1 and transitioned to phase 2. In ad-
dition, fatigue was significantly (P< 0.001) elevated in those
entering as phase 2 after treatment.
PHASE 3TO 4TRANSITION
Significant improvements were observed in V
˙
O
2peak
(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
˙
O
2peak
,leg
press MS, and chest MS were 4%, 5%, and 7%, respectively.
Mean values of fatigue decreased during this transition but re-
mained at a “mild”Piper Fatigue Inventory classification.
Changes in Patients Who Completed the Entire Phase Program
(Entry to Phase 4)
In the 81 patients who completed the Phase Program and en-
tered phase 4, significant improvements were observed in V
˙
O
2peak
(21.0±6.8to26.1±7.3mL·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
˙
O
2peak
,legpress
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.
TABLE 2.
Retention between Phase Transitions.
Phase Transition
Entry
(n)
Completion
(n)
Retention
(%)
Phase 1 to phase 2 70 48 69
Phase 1 to 1 18 26
Phase 2 to phase 3 161 142 88
Phase 2 at entry 113 94 83
Phase 1 Graduates 48 48 100
Phase 3 to phase 4 142 81 57
Entry as phase 1 or 2 183 81 44
Phase 1 to 1: patients in phase 1 who completed a reassessment but re-
mained in phase 1 due to treatment continuation.
Phase 2 at entry: patients who did not participate in phase 1 and started
the program in phase 2 after treatment.
Phase 1 graduates: patients who started and completed the program in
phase 1 and then entered phase 2.
Entry as phase 1 or 2: patients who completed the entire Phase Program
by starting in phase 1 or 2.
http://www.acsm-tj.org Translational Journal of the ACSM 49
Copyright © 2019 by the American College of Sports Medicine. Unauthorized reproduction of this article is prohibited.
DISCUSSION
Exercise-based interventions are widely considered a via-
ble method of cancer rehabilitation because of the clear evi-
dence that exercise improves functional capacity, reduces
cardiovascular disease risk factors (19), decreases mortality
(20), may limit the risk of cancer recurrence (21,22), and im-
proves QOL (23). The Phase Program of our SCM for cancer
rehabilitation elicited improvements in cardiovascular endur-
ance, 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 im-
provements 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 princi-
ple of progressive overload, the clinician truly individualizes
the exercise intervention. This is accomplished through the
use and interpretation of the patients’comprehensive assess-
ment results and corresponding classifications. Higher levels
of functioning will result in the creation of an exercise prescrip-
tion 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 ad-
heres 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 pro-
gram seeks to individualize progressive overload and specific-
ity using medical information, assessment results, and patient
goals. The exercise intervention is formulaic and prescribes fre-
quency and duration similarly across patients for easy repro-
ducibility, whereas the one-on-one clinician-to-patient ratio
allows for a personalized approach.
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 mus-
cle mass, and may offset cancer-related cachexia. This may ex-
plain why survivors in phase 1 not only maintained MS levels
but significantly improved beyond their initial baseline measure-
ments. In addition, aerobic exercise and its associated cardio-
protective 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 inten-
sity 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
TABLE 3.
Improvements in Cardiovascular Endurance, Strength, and Fatigue at Each Phase Transition.
Phase Transition Phase 1 to Phase 2 Phase 2 to Phase 3 Phase 3 to Phase 4
n48 142 81
Pre Post Percent
Change
Pre Post Percent
Change
Pre Post Percent
Change
V
˙
O
2peak
(mL·kg
−1
·min
−1
) 20.9 ± 7.4 23.5 ± 7.9** 13 21.9 ± 7.3 24.8 ± 8.5** 14 25.1 ± 7.1 26.1 ± 7.3* 4
Leg press (kg) 81 ± 33 91 ± 42* 13 82 ± 31 98 ± 40** 19 100.9 ± 45.5 105.8 ± 41 5
Chest press (kg) 27 ± 16 32 ± 19** 18 31 ± 18 39 ± 20** 26 36.6 ± 17.8 39.2 ± 19* 7
Fatigue 5.1 ± 2.4 3.8 ± 2.0** −25 4.1 ± 2.2 3.0 ± 2.1** −27 3.3 ± 2.1 3.2 ± 2.2 −5
Values represent mean ± SD.
*Pvalue <0.05 between Pre and Post values.
** Pvalue <0.001 between Pre and Post values.
50 Volume 4 •Number 7 •April 1 2019 Phase Program for Can cer Survivors
Copyright © 2019 by the American College of Sports Medicine. Unauthorized reproduction of this article is prohibited.
breast cancer survivors undergoing treatment resulted in an over-
all increase in fatigue (28). Contrary to the belief that fatigue levels
may be heightened for those exercising while undergoing treat-
ment, the current study demonstrates that exercising at appropri-
ate, low intensities can significantly reduce fatigue levels.
Modest improvements were expected because the exercise pre-
scription dictated an initial low intensity and a small rate of pro-
gression, and the majority of patients underwent all major
treatment modalities. The exercise intensity prescribed for pa-
tients in phase 1 was low due to the J-shaped curvilinear relation-
ship 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 signif-
icant cause of death in patients undergoing treatment (30), and ex-
ercise at lower intensities has been shown to preserve immune
function and reduce therisk of adverse effectsin patients undergo-
ing treatment (31). Studies using high-intensity exercise interven-
tions 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 implementa-
tion of high-intensity protocols, it is not feasible for exercise pro-
fessionals 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 car-
diorespiratory 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
˙
O
2peak
) aerobic exercise intervention (33). Al-
though the research indicates that high-intensity exercise does
yield significant improvements, our study demonstrates that sim-
ilar benefits occur using a lower intensity. Given the equivalency
of the outcomes resulting from both high- and low-intensity exer-
cise 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 pre-
scribed in-patient physical therapy (4). Our results suggest that
the Phase Program is well tolerated, as evidenced by the 94% re-
tention 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.
Phase 2
Energy levels and functional capacity have been observed to in-
crease after the completion of cancer treatment (34), which will in-
crease 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 pro-
gressive 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 partici-
pants to achieve greater improvements in cardiovascular endur-
ance, 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 find-
ings demonstrate that significant declines in fatigue scores are pos-
sibleduringandimmediately 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). Inter-
estingly, the improvements immediately after treatment were
additive to the large, near identical, significant improvements pre-
viously observed in those during treatment (phase 1), suggesting
that exercise attenuates cancer-related fatigue to the greatest ex-
tent 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 improve-
ments 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) re-
ported that after a 1-yr, moderate- to high-intensity resistance
training intervention in breast cancer survivors (~1 yr from treat-
ment), 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 ev-
idence 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 adher-
ence 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
Figure 3: Mean percent change in V
˙
O
2peak
,legpressMS,chestpress
MS, and fatigue in patients completing phases 1 through 3. **Denotes
p value < 0.001 between pre and post values.
http://www.acsm-tj.org Translational Journal of the ACSM 51
Copyright © 2019 by the American College of Sports Medicine. Unauthorized reproduction of this article is prohibited.
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 can-
cer 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 re-
ferring to the subject demographic as “posttreatment”(11,42,43).
A similar 12-wk exercise program resulted in a 7.5% nonsignifi-
cant 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 char-
acteristics 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 popula-
tion as a whole, specifically in terms of cancer type, treatment mo-
dality, 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.
Phase 3
The transition from phase 3 marks the end of what is consid-
ered “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 rea-
son, 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 im-
proved 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 pa-
tients 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 significantfor participants completing phase 3. Car-
diovascular endurance as measured by V
˙
O
2peak
improved to a
classification and percentile deemed “fit”in 59% of the partici-
pants. It has been demonstrated that sedentary men who were unfit
at the initial examination, but who became fit at reassessment, had
a44%reductioninriskofmortalitywhencomparedwithsimilar
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). Consid-
ering the complex nature of cancer and cancer treatment-related
toxicities, the continual decrease in risk of mortality at each reas-
sessment during the Phase Program may improve patient progno-
sis, 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 signifi-
cant 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 classifi-
cations 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 dura-
tion of exercise sessions were capped in this study. Phase 3 was de-
signed 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 ses-
sions, or increase intensity may be required by some cancer survi-
vors 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.
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 bar-
riers 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 subse-
quently 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 adjust-
ments in exercise intensity, correction of form and body mechan-
ics, 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 bythe specialist orsought further increasesin 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.
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
52 Volume 4 •Number 7 •April 1 2019 Phase Program for Can cer Survivors
Copyright © 2019 by the American College of Sports Medicine. Unauthorized reproduction of this article is prohibited.
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 pro-
gram 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. How-
ever, future investigations should report acute, day-to-day modifi-
cations to further elucidate the exercise dose–response. We have
reported anecdotal reasons for program withdrawal, but future
studies could formally record this andfurther 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 popu-
lation demographics closely reflect the cancer population and
real-world clinics/fitness facilities, enhancing its efficacy and reproduc-
ibility. Another strength is that our model uses physician-initiated
patient referrals and includes direct communication with oncolo-
gists and detailed medical screening needed for personalized exer-
cise. 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.
CONCLUSION
Despite the prevalence and abundance of exercise-based
programs, standardization of both the methodology and antic-
ipated outcomes does not exist currently. Specific recommenda-
tions 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 prin-
ciples of exercise training, which guide appropriate exercise in-
tervention for this population. The Phase Program is an
attempt to improve the clarity of exercise prescription for can-
cer 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 train-
ing 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 cli-
nicians the flexibility to individualize exercise, while remaining
clear and reproducible, and it is supported by empirical evidence
demonstrating significant physiological and psychological im-
provements 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.
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 rehabilita-
tion: leveraging the cardiac rehabilitation model. JCardiopulmRehabilPrev.
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. Nutritionand 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, DeHeer HD, Bea JW. Initiating exercise interventionsto promote
wellness in cancer patients and survivors. Oncology (Williston Par k). 2017;
31(10):711–7.
10. Kirkham AA, Bonsignore A, Bland KA, et al. Exercise prescription and adher-
ence for breast cancer: one size does not FITT all. Med Sci Sports Exerc.
2018;50(2):177–86.
11. Speck RM, Courneya KS, MâsseLC, Duval S, Schmitz KH. An update ofcon-
trolled physical activity trials in cancer survivors: a systematic review and
meta-analysis. JCancerSurviv.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, DibbleSL, 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 Unive rsity of Nor thern Color ado Cancer Rehabilitation Ins titute Trea d-
mill 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, SchommerK, et al. Exercise intensity clas-
sification 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. Com-
parison 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 re-
sponse between physical activity and risk of coronary heart disease. Circula-
tion. 2011;124(7):789–95.
20. Blair SN, Kampert JB, Kohl HW 3rd, et al. Influences of cardiorespiratory fit-
ness 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, KroenkeCH, Colditz GA. Physical activ-
ity and survivalafter breast cancer diagnosis. JAmMedAssoc.2005;293(20):
2479–86.
22. Meyerhardt JA,Heseltine D, Niedzwiecki D, et al. Impactof 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 ca-
chexia. Appl Physiol Nutr Metab.2014;39(6):679–86.
http://www.acsm-tj.org Translational Journal of the ACSM 53
Copyright © 2019 by the American College of Sports Medicine. Unauthorized reproduction of this article is prohibited.
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 fa-
tigue 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 su-
pervised 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 sys-
tem. Med Sci Sports Exerc. 1994;26(2):12 8–39.
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, BlochW, Elter T. Influence of
endurance exercise on the risk of pneumonia and fever in leukemia and lym-
phoma patients undergoing high dose chemotherapy. A pilot study. JSports
Sci Med. 2012;11(4):638.
32. Quist M, Rorth M, ZachoM, et al. High-intensityresistance and cardiovascular
training improve physical capacity in cancer patients undergoing chemother-
apy. Scand J Med Sci Sports. 2006;16(5):349–57.
33. Hornsby WE, Douglas PS, West MJ, et al. Safety and efficacy of aerobic train-
ing in operablebreast cancer patients receiving neoadjuvantchemotherapy: a
phase II randomized trial. Acta Oncol.2014;53(1):65–74.
34. Ganz PA, Kwan L, Stanton AL, BowerJE, Belin TR. Physicaland psychosocial
recovery in the year after primary treatment of breast cancer. JClinOncol.
2011;29(9):1101–9.
35. Pinto BM, TrunzoJJ, Reiss P, Shiu SY. Exercise participationafter diagnosisof
breastcancer: trends andeffects on mood and quality of life. Psychoonco logy.
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 ofhigh intensity and low-to-moderate intensity exercise on physicalfit-
ness 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.
JCancerSurviv. 2012;6( 2):189–99.
39. Cox KL, Burke V,Gorely TJ, Beilin LJ,Puddey IB. Controlledcomparison of re-
tention 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, AntonSD, Durning PE, et al.Adherence to exercise prescriptions:ef-
fects 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, KaslS, 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. JOncol
Pract. 2012;8(6):320–4.
44. Farrell SW, BraunL, Barlow CE, Cheng YJ,Blair SN. The relationof body mass
index, cardiorespiratory fitness, and all-cause mortality in women. Obes Res.
2002;10(6):417–23.
54 Volume 4 •Number 7 •April 1 2019 Phase Program for Can cer Survivors
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