Cancer is considered a threat to public health and one of the leading causes of death worldwide.1 Among women, breast cancer is responsible for approximately 2 million cases each year, being the most frequent cancer-related cause of death.2 Breast cancer represents 29.7% of new cancer diagnoses in Brazil, accounting for 66,280 new cases only in 2020.3 Notwithstanding this, more women survive breast cancer due to medical advances and early detection of the disease.4 Still, there are considerable long-term side effects related to both cancer and its treatment, which impact aspects of daily living and the quality of life of these individuals. Improving interventions to counteract these health problems, therefore, is paramount.
Among the side effects related to cancer treatment, patients have marked impairments in muscle strength,5 power,6 and peak oxygen uptake (VO2peak),7,8 and an increase in fatigue9 often due to treatment toxicity. According to Berger et al,10 fatigue has been reported as one of the main factors leading to functional limitations in patients with a history of breast cancer. As a consequence, breast cancer survivors typically demonstrate lower functional capacity (ie, walking speed) when compared with women of the same age who have never undergone cancer therapy,6 a condition that has been previously associated with higher all-cause mortality risk in the former.10
Despite the clear negative impact breast cancer and its treatment has on breast cancer survivors’ health, the impact of rehabilitation physical exercise programs in this clinical population remains underexplored. Some studies11,12 have shown that combined training, herein defined as the inclusion of resistance and aerobic exercises in the same session, can improve VO2peak, muscle strength, cancer-related fatigue, and quality of life. These outcomes were found to mediate the improvements observed in functional capacity in breast cancer survivors.11,12 However, multiple-set (MS) resistance training protocols typically employed in these studies (ie, 3 sets, 8–12 repetitions with ≈80% of 1-repetition maximum [1RM]) may represent a challenge for breast cancer survivors due to their lower functional capacity compared with women who have never undergone cancer treatment.6,13
Given the numerous variables that can be manipulated to adequately prescribe a resistance training program, training volume has been shown as an important factor that can influence muscle hypertrophy, muscle strength, and functional capacity adaptations.14 Interventions using training volumes as low as 1 set per exercise (ie, single set [SS]) have shown muscle mass, muscle strength, and functional capacity improvements similar to those achieved using greater volumes (ie, MS) in healthy older women.15,16 Considering breast cancer survivors’ increased fatigue and reduced exercise capacity, it is reasonable to speculate that these patients could benefit from performing SS resistance training protocols. The literature, however, is scarce on studies comparing different resistance training volumes in oncology patients. Therefore, the present study aimed to investigate the effects of different resistance training volumes within combined training on physical (maximal strength, muscle thickness, and cardiorespiratory capacity) and perceptual (ie, cancer-related fatigue and quality of life) outcomes in breast cancer survivors. Given that the optimal resistance training volume to improve health-related outcomes in this population is not yet established, we hypothesized that the lower-volume resistance training protocol would achieve comparable physical and perceptual benefits compared with a protocol with greater volume.
Materials and Methods
Experimental Design
This study is a 2-armed randomized trial that compared the short-term (ie, 8 wk) effects of different resistance training volumes (ie, SS vs MS) within a combined training intervention in physical and perceptual outcomes in breast cancer survivors. The primary outcomes were maximal knee extension dynamic strength and cancer-related fatigue. Secondary outcomes were quadriceps muscle thickness, cardiorespiratory capacity, and quality of life. Standard procedures were established and repeated by the same evaluators (blinded to group allocation) preintervention (week 0) and postintervention (week 9). The outcomes were measured by the same training investigator blinded to participant allocation within 1 week in 3 separate sessions at baseline and 2 sessions postintervention to avoid accumulated fatigue. The interval was 48 hours between each session.
Participants
Participants were recruited through social media advertising and phone calls from a potential list of participants that finished the primary treatment for breast cancer provided by the Federal University of Pelotas’ Hospital. Inclusion criteria were defined as follows: women who completed their primary treatment for breast cancer (surgery, chemotherapy, and/or radiotherapy) within 3 months to 5 years before the study (volunteers could be undergoing hormonal therapy at the time of the study); diagnosed with stage I to III breast cancer, and 18 years of age or older. Exclusion criteria included the inability or unwillingness to give informed consent for participation or the presence of metastatic or active locoregional disease; cardiovascular disease history (except for hypertension); severe physical disabilities or psychological disorders, severe nausea, anorexia, or any condition that precluded physical exercise participation. Moreover, the volunteers could not have been engaged in regular physical exercise in the 3 months before eligibility. The participants were instructed to maintain eating and physical activity habits during the study period.
The recruitment process was conducted in 2 separate waves: first, 11 participants were recruited from a passive control group of a previous study from our laboratory and performed this intervention between January and July 2017, whereas 8 additional volunteers were recruited through different recruitment strategy (ie, through social media advertising and phone calls from a list of women that finished the primary treatment for breast cancer provided by the Federal University of Pelotas’ Hospital) between October 2019 and March 2020. Thus, a total of 19 women were included in the present study (SS: n = 10; MS: n = 9). All participants were informed about the possible benefits and risks of participating in the research and gave their written informed consent. This trial received ethical approval from the Universidade Federal de Pelotas Research Ethics Committee (CAAE: 59195516.9.0000.5313; protocol number: 1.977.039) and was conducted in accordance with the Declaration of Helsinki. All testing and exercise training sessions took place at the Universidade Federal de Pelotas exercise science laboratory.
Randomization Process
An external researcher with no involvement in the trial created a computer-generated random number list, 1:1 ratio, with blocks of participants stratified by breast cancer stage at the time of diagnosis (ie, I, II, or III). This conduct was chosen because treatment protocols may differ according to the stage in which patients are diagnosed. Thus, possible differences in adverse effects could interfere with the outcomes of this study. Allocation concealment was implemented by researchers in charge of participant’s enrollment, requesting that one of the blinded investigators who had access to the randomization list provide the participant’s identifier number. The participants were randomized to either the SS or MS group only after completing preintervention assessments.
Interventions
Training sessions were performed twice weekly over 8 weeks on preestablished and nonconsecutive days. They were all supervised by trained sports science students at a ratio of 2 participants to 1 instructor. The sessions began with a 5-minute lower-body warm-up in a cycle ergometer, followed by 3 stick mobility exercises to upper limb, and finished with a standardized stretching routine. Resistance exercises were performed before the aerobic exercise in all combined training sessions. The total time per session spent by SS and MS was approximately 1 hour and 1 hour 40 minutes, respectively. The progression of both resistance and aerobic exercises over the 8 weeks of intervention is shown in Table 1.
Progression of Resistance and Aerobic Training Over the 8 Weeks
| Weeks | Resistance training | Aerobic training | ||||
|---|---|---|---|---|---|---|
| Sets (SS/MS) | Reps | SS volumea | MS volumea | Intensity | Duration | |
| 1–2 | 1/3 | 18 RM | 198 reps | 594 reps | 80%–85% HRVT2 | 20 min |
| 3–4 | 1/3 | 15 RM | 165 reps | 495 reps | 85%–90% HRVT2 | 25 min |
| 5–6 | 1/3 | 12 RM | 132 reps | 396 reps | 90%–95% HRVT2 | 25 min |
| 7–8 | 1/3 | 9 RM | 99 reps | 297 reps | 2 min VVT2: 2 min VVT1 | 32 min |
Abbreviations: HRVT2, heart rate associated with the second ventilatory threshold; MS, multiple-set group; Reps, repetitions; RM, repetition maximum; SS, single-set group; VVT1, velocity associated with the first ventilatory threshold; VVT2, velocity associated with the second ventilatory threshold.
aRelative volume was calculated as follows: number of exercises × (number of sets × number of repetitions).
Resistance Training
The resistance training portion of the combined training session included 11 exercises, which were performed in the following order: leg press, chest press machine, crunches, hip adduction, leg extension, elbow flexion, lying leg curl, hip abduction, triceps pulley, seated row, and lower back extension. Exercise volume was prescribed according to the participant’s assigned group, that is, those assigned to SS performed 1 set per exercise, whereas those in the MS group performed 3 sets per exercise. All sets were performed to failure, and the intervention period was divided into four 2-week mesocycles in which exercise intensity increased after each new mesocycle (Figure 1). When subjects could easily perform the proposed number of repetitions in 2 consecutive sessions, the exercise load increased individually.
—Mean (SD) of maximal training load (percentage) relative to preintervention knee extensors 1-maximal repetition values during different mesocycles (M1, M2, M3, and M4) in SS and MS groups. MS indicates multiple set; SS, single set.
Citation: Journal of Physical Activity and Health 20, 3; 10.1123/jpah.2022-0097
—Mean (SD) of maximal training load (percentage) relative to preintervention knee extensors 1-maximal repetition values during different mesocycles (M1, M2, M3, and M4) in SS and MS groups. MS indicates multiple set; SS, single set.
Citation: Journal of Physical Activity and Health 20, 3; 10.1123/jpah.2022-0097
—Mean (SD) of maximal training load (percentage) relative to preintervention knee extensors 1-maximal repetition values during different mesocycles (M1, M2, M3, and M4) in SS and MS groups. MS indicates multiple set; SS, single set.
Citation: Journal of Physical Activity and Health 20, 3; 10.1123/jpah.2022-0097
Aerobic Training
Aerobic training was performed on a treadmill, and exercise intensity was prescribed based on the percentage of the heart rate (HR) associated with the second ventilatory threshold (HRVT2) during the first 3 mesocycles and on the velocity associated with the first (VT1) and second ventilatory threshold (VT2) in the last mesocycle, which was performed in an interval training fashion, as evidenced in Table 1. Exercise intensity was monitored telemetrically using codified heart rate monitors (FS1, Polar). The intensity and volume were increased throughout the intervention period, as shown in Table 1.
Measurements
After participants provided written consent to participate in the study, questionnaires were applied to gather tumor, treatment, lifestyle, and sociodemographic information. After the interview, another appointment was scheduled to explain the tests that would be performed and familiarize participants with their procedures. Cancer-related fatigue, quality of life, muscle thickness, and maximal dynamic strength were measured on the first day, whereas anthropometric measures to characterize the participants were performed on the second day at baseline. Cardiorespiratory outcomes were determined on a treadmill graded exercise test on the third day. The postintervention assessments started 72 hours after the last training session.
Maximal Knee Extension Dynamic Strength
The 1RM was used to assess maximal knee extension dynamic strength in a bilateral leg extension machine (New Fitness). The 1RM was considered the maximal load (in kilograms) participants could lift only once through a full range of motion. A 5-minute warm-up preceded the test in a cycle ergometer and submaximal repetitions in the leg extension machine, and the 1RM load was determined with no more than 5 attempts, with a 4-minute rest between them. If more than one complete repetition could be performed, the weight was readjusted (based on the Lombardi17) until no additional load could be lifted using proper technique. The cadence of each contraction phase (concentric and eccentric) lasted 2 seconds and was monitored using a metronome (MA-30, KORG).
Muscle Thickness
Muscle thickness (MT) was analyzed using B-mode ultrasound imaging (Toshiba—Tosbee/SSA-240A). Before testing, participants remained supine, with arms and legs extended and relaxed for 15 minutes to stabilize normal body fluids after which a linear transducer (wave frequency 7.5 MHz; 80 mm image depth; 90 dB general gain and time-gain compensation at neutral position) was placed perpendicular to the muscle of interest, using a water-soluble transmission gel that provided acoustic contact without depressing the skin surface. Measurements from the vastus lateralis, vastus medialis, vastus intermedius, and rectus femoris muscles were taken from the right thigh. Specifically, vastus lateralis MT was measured at the midpoint between the lateral condyle and the great trochanter of the femur.18 In contrast, vastus medialis MT was measured at 30% of the distance between the lateral condyle and the great trochanter of the femur.19 Vastus intermedius and rectus femoris MT images were taken at 2/3 of the length between the great trochanter and the lateral condyle of the femur and 3 cm laterally from the midline of the thigh.20 A map of the right thigh of each participant was created to ensure the same transductor position in all subsequent measurements by drawing references of anatomical points and marks on the skin in transparent plastic.21
The same experienced investigator obtained 3 images from each muscle which were digitized for further analysis using the Image J software (National Institute of Health, version 1.37). MT was determined in each image as the distance between the adipose tissue and the muscle interface for the rectus femoris, vastus lateralis, and vastus medialis muscles; and the distance between the femur and muscle interface for the vastus intermedius. The MT value of the 3 images from each muscle were averaged to obtain a final value for analysis. Finally, quadriceps femoris MT was determined as the sum of the 4 individual quadriceps muscles.
Anthropometric Measures
Body mass and height were measured on a digital scale with a stadiometer (WELMY), and body mass index was calculated. Skinfold thickness measures were taken on the right side of the body at the chest, axilla, triceps, subscapular, abdomen, suprailium, and thigh with a skinfold caliper (CESCORF) to estimate body density.22
Cardiorespiratory Capacity
A graded exercise test on a treadmill was used to measure peak oxygen uptake (VO2peak), time to exhaustion, oxygen uptake at VT2, and time to reach VT2. For this purpose, a 3-minute warm-up was performed in which treadmill speed was gradually increased up to 3 km·h−1. After that the test began at 3 km·h−1 and 1% incline, and 0.5 km·h−1 and 1% incline increments were applied every 1 and 2 minutes, respectively. The test was interrupted when the participant signaled exhaustion. The respiratory gases were collected through a portable gas analyzer (VO2000, MedGraphics), which was previously calibrated before each session in agreement with the manufacturer’s specifications.
The VO2peak value (in milliliters per kilograms per minute) obtained near exhaustion was considered as VO2peak. Additionally, time to exhaustion was analyzed considering the beginning of the test until its interruption. Both VT1 and VT2 were determined by the ventilation versus intensity course and confirmed by the O2 (VE/VO2) and CO2 (VE/VCO2) ventilatory equivalents, respectively.23 HRVT2 and the velocity at VT1 and VT2 were also determined and used to prescribe the aerobic exercise intensity, as previously explained. All cardiorespiratory tests were performed in the presence of a physician, and because of logistical issues, the postintervention assessor differed from baseline for 3 participants.
Cancer-Related Fatigue
The perception of fatigue was determined using the revised Piper Fatigue Scale through an interview. Its version translated to Portuguese is a reliable and valid instrument to measure fatigue in Brazilian cancer patients.24 The revised Piper Fatigue Scale consists of 22 items numerically scaled from 0 to 10 (with zero indicating “no fatigue”), measuring 4 dimensions of subjective fatigue and total fatigue. The behavioral fatigue subscale includes 6 questions and assesses the impact of fatigue on school or work, interacting with friends, and the overall interference in enjoyable activities. The affective fatigue subscale includes 5 questions and assesses the emotional meaning attributed to fatigue. The sensory fatigue subscale consists of 5 questions and assesses mental, physical, and emotional fatigue symptoms. The cognitive/mood fatigue subscale includes 6 questions and is used to determine the impact of fatigue on concentration, memory, and the ability to think clearly. To calculate the subscale score, the scores of the items on the specific subscales are summed and divided by the number of items in the subscale.25 All item scores are summed and divided by 22 to calculate the total fatigue score, with a high score indicating a high fatigue level.25 To classify the intensity of the fatigue based in the total score, 3 levels were defined: mild (score higher than 0 and lower than 4), moderate (score equal or higher than 4 and lower than 6), and severe (score equal or higher than 6 until 10).26
Quality of Life
The Functional Assessment of Cancer Therapy-Breast (FACT-B) questionnaire was applied in an interview. Its Portuguese-translated version is a valid and reliable instrument.27 The FACT-B subscales include physical well-being (7 items), functional (7 items), emotional (6 items), social or familiar (7 items), and a breast cancer (10 items) subscale. The sum of the 5 subscales scores determines the FACT-B score (all 37 items). Additionally, the Functional Assessment of Cancer Therapy-General (FACT-G; 28 items, excluding the breast cancer subscale) and trial outcome index (TOI; 23 items, composed of physical well-being and function and the breast cancer scale) are calculated. Higher total and/or subscale scores represent better quality of life.
Statistical Analysis
The sample size was calculated in G*Power (version 3.0.10) Windows version considering an α = 5%, 80% of power, and a .5 correlation coefficient. Previously published data from maximal dynamic knee extension strength (effect size f = 0.31) and cancer-related fatigue (effect size f = 0.74) data were utilized.28 As a result, it was determined that a sample size of 12 and 8 participants in each group (SS and MS) were required for the maximal knee extension dynamic strength and cancer-related fatigue outcomes, respectively. However, due to the COVID-19 pandemic, we could not achieve the estimated sample number (26 participants for knee extension dynamic strength).
The variables are described as mean (SD), absolute (no.), and/or relative frequency (%) as stated. The normality and homogeneity of variance of the sample characterization numerical outcomes were verified using the Shapiro–Wilk and Levene tests. Aiming to identify potential baseline differences between groups, the t-student test or Mann–Whitney to numerical variables independent samples, and the Pearson chi-squared to categorical variables were applied. Generalized estimating equations and Bonferroni post hoc were used for comparing time points (preintervention and postintervention) and groups (SS and MS), and also to investigate potential group × time point interactions. Comparisons between SS and MS were also conducted individually based on the difference between the preoutcomes and postoutcomes values. All randomized women were included in the analyses using an intention-to-treat approach. In addition, intragroup effect sizes were calculated using the Cohen d test,29 being classified as small (0.20 ≤ d < 0.50); medium (0.50 ≤ d < 0.80); and great (d ≥ 0.80). The significance level considered in this study was 5%, and all statistical analyses were conducted in the SPSS software (version 23.0).
Results
Descriptive characteristics of the participants at baseline are reported in Table 2. In addition, the study flowchart is presented in Figure 2. Of the 171 women who were contacted for participation, 19 were randomized and included in the intention to treat analysis (SS: n = 10; MS: n = 9). Fifteen participants completed the intervention (14 women performed all 16 sessions and 1 participant 15 sessions) and the preoutcomes and postoutcomes evaluations. Three participants were evaluated at baseline but could not start the intervention due to COVID-19 restrictions, whereas one participant give up after 2 training sessions due to a distant-metastasis diagnosis. Thus, 4 participants had an imputation of the post outcomes evaluations missing values.
Baseline Characteristics of Participants
| Characteristics | All (N = 19) | SS (n = 10) | MS (n = 9) | P |
|---|---|---|---|---|
| Demographic | ||||
| Age, y, mean (SD) | 53.89 (11.23) | 56.30 (9.91) | 51.22(12.57) | .339 |
| Body mass, kg, mean (SD) | 75.31 (13.49) | 82.15 (11.77) | 67.72 (11.42) | .015* |
| Height, cm, mean (SD) | 152.30 (7.30) | 153.78 (6.12) | .641 | |
| BMI, kg/m2 (%) | .066 | |||
| <25 | 3 (15.8%) | 0 (0%) | 3 (33.3%) | |
| 25 to <30 | 5 (26.3%) | 2 (20%) | 2 (22.2%) | |
| ≥30 | 11 (57.9%) | 8 (80%) | 4 (44.4%) | |
| Clinic | ||||
| Skinfold sum, mm, mean (SD) | 257.73 (73.16) | 282.45 (75.07) | 230.26 963.97) | .123 |
| Years since diagnosis, mean (SD) | 3.00 (2.00) | 3.00 (3.00) | 2.00 (2.00) | .079 |
| Stage, no. (%) | .153 | |||
| I | 6 (31.6%) | 3 (30.0%) | 3 (33.3%) | |
| II | 8 (42.1%) | 6 (60.0%) | 2 (22.2%) | |
| III | 5 (26.3%) | 1 (10.0%) | 4 (44.4%) | |
| Surgery, no. (%) | .463 | |||
| Mastectomy | 11 (57.9%) | 5 (50%) | 6 (66.7%) | |
| Quadrantectomy | 8 (42.1%) | 5 (50%) | 3 (33.3%) | |
| Treatment, no. (%) | ||||
| Radiation only | 5 (26.3%) | 2 (20.0%) | 3 (33.3%) | |
| Chemotherapy only | 3 (15.8%) | 3 (15.8%) | 0 (0%) | |
| Chemotherapy and radiation | 11 (57.9%) | 5 (50%) | 6 (66.7%) | |
| Hormonal therapy, no. (%) | 15 (78.9%) | 8 (80%) | 7 (77.8%) | .906 |
| Smoking, no. (%) | .751 | |||
| Nonsmoker | 11 (57.9%) | 6 (60.0%) | 5 (55.6%) | |
| Ex-smoker | 5 (26.3%) | 2 (20.0%) | 3 (33.3%) | |
| Smoker | 3 (15.8%) | 2 (20.0%) | 1 (11.1%) | |
| Diabetes, no. (%) | 5 (26.3%) | 5 (50.0%) | 0 (0%) | .013* |
| Hypertension, no. (%) | 10 (52.6%) | 7 (70.0%) | 3 (33.3%) | .110 |
Abbreviations: BMI, body mass index; MS, multiple-set group; no., number; SS, single-set group.
*Significant difference between groups.
—Participants’ flowchart. BC: breast cancer.
Citation: Journal of Physical Activity and Health 20, 3; 10.1123/jpah.2022-0097
—Participants’ flowchart. BC: breast cancer.
Citation: Journal of Physical Activity and Health 20, 3; 10.1123/jpah.2022-0097
—Participants’ flowchart. BC: breast cancer.
Citation: Journal of Physical Activity and Health 20, 3; 10.1123/jpah.2022-0097
Maximal Dynamic Strength and Muscle Thickness
Both knee extension maximal dynamic strength and quadriceps muscle thickness results are presented in Table 3. Both SS (29.8% [37.5%]) and MS (19.3% [11.8%]) increased knee extension 1RM after the combined training intervention (P < .001), with no difference between groups (P = .852). Lower-limb MT also improved posttraining (vastus lateralis [VL], vastus medialis [VM], and rectus femoris [RF]: P < .001; vastus intermedius (VI): P = .002; quadriceps femoris: P < .001) in both the SS (VL: 9.7% [8.8%]; VM: 9.9% [7.3%]; VI: 8.9% [12.9%]; rectus femoris (RF): 8.4% [4.7%]; quadriceps: 9.4% [4.1%]) and MS group (VL: 9.6% [9.7%]; VM: 9.1% [9.8%]; VI: 8.4% [13.3%]; RF: 8.5% 7.7%]; quadriceps: 8.9% [5.9%]), with no difference between them (VL: P = .172; VM: P = .671; VI: P = .848; quadriceps: P = .694). The only exception was for rectus femoris MT, in which a significant group factor (P = .035) indicated that the SS group had a greater rectus femoris MT regardless of the time point.
Maximal Dynamic Strength and MT Outcomes Pre and Post SS and MS Interventions
| Outcomes | n | Pre | Post | Cohen d |
|---|---|---|---|---|
| Mean (SD) | Mean (SD) | |||
| Knee extension 1RM, kg | ||||
| SS | 10 | 28.00 (11.83) | 32.86 (11.45)† | 0.42 |
| MS | 9 | 29.11 (12.42) | 33.86 (13.71)† | 0.36 |
| Vastus lateralis MT, mm | ||||
| SS | 10 | 15.89 (2.78) | 17.20 (2.43)† | 0.50 |
| MS | 9 | 17.66 (3.93) | 19.28 (3.12)† | 0.46 |
| Vastus medialis MT, mm | ||||
| SS | 10 | 18.69 (5.34) | 20.27 (5.44)† | 0.29 |
| MS | 9 | 17.63 (6.33) | 19.02 (6.45)† | 0.22 |
| Vastus intermedius MT, mm | ||||
| SS | 10 | 13.59 (3.10) | 14.58 (2.88)† | 0.33 |
| MS | 9 | 13.21 (4.86) | 14.25 (4.92)† | 0.21 |
| Rectus femoris MT, mm | ||||
| SS | 10 | 18.54 (3.42) | 19.94 (3.32)† | 0.42 |
| MS | 9 | 15.39 (3.66)§ | 16.52 (3.24)§,† | 0.33 |
| Quadriceps femoris MT, mm | ||||
| SS | 10 | 66.20 (10.75) | 72.01 (10.15)† | 0.56 |
| MS | 9 | 63.90 (17.70) | 69.14 (16.47)† | 0.31 |
Abbreviations: 1RM, 1-repetition maximum; MS, multiple set; MT, muscle thickness; SS, single set.
†Significant difference from preintervention values. §Significant difference from SS values.
Quality of Life and Cancer-Related Fatigue
Quality of life results are presented in Table 4. Both the FACT-B (P = .001), FACT-G (P = .002), TOI (P < .001), and physical well-being subscale (P = .019) improved after the intervention in the SS (FACT-B: 4.3% [6.3%]; FACT-G: 3.5% [5.9%]; TOI: 4.2% [7.9%]; physical well-being subscale: 2.1% [10.2%]) and MS group (FACT-B: 7.9% [8.9%]; FACT-G: 8.8% [10.5%]; TOI: 13.3% [13.6%]; physical well-being subscale: 19.8% [27.8%]), with no difference between them (FACT-B: P = .685; FACT-G: P = .439; TOI: P = .972; physical well-being subscale: P = .483). For all the other subscales, no difference was observed between the preintervention and postintervention time points for both the SS and MS groups (P > .05)(P > .05).
Quality of Life Outcomes Pre and Post SS and MS Interventions
| Outcomes | n | Pre | Post | Cohen d |
|---|---|---|---|---|
| Mean (SD) | Mean (SD) | |||
| FACT-B (0–148) | ||||
| SS | 10 | 112.20 (15.08) | 117.14 (18.25)† | 0.30 |
| MS | 9 | 113.11 (12.24) | 121.45 (12.84)† | 0.66 |
| FACT-G (0–108) | ||||
| SS | 10 | 86.10 (11.32) | 89.06 (13.06)† | 0.23 |
| MS | 9 | 87.44 (7.89) | 94.67 (8.91)† | 0.86 |
| TOI (0–96) | ||||
| SS | 10 | 70.30 (11.26) | 73.01 (11.42)† | 0.24 |
| MS | 9 | 67.89 (11.25) | 75.76 (9.69)† | 0.75 |
| Physical well-being (0–28) | ||||
| SS | 10 | 22.20 (4.74) | 22.65 (4.46)† | 0.10 |
| MS | 9 | 21.89 (4.95) | 25.07 (3.45)† | 0.75 |
| Emotional well-being (0–24) | ||||
| SS | 10 | 21.00 (3.51) | 20.47 (5.22) | −0.12 |
| MS | 9 | 22.67 (3.03) | 23.53 (2.34) | 0.32 |
| Functional well-being (0–28) | ||||
| SS | 10 | 19.30 (4.74) | 21.78 (3.19) | 0.61 |
| MS | 9 | 21.00 (1.89) | 21.36 (3.24) | 0.14 |
| Social/family well-being (0–28) | ||||
| SS | 10 | 23.10 (4.43) | 23.03 (3.16) | −0.02 |
| MS | 9 | 21.89 (3.48) | 24.31 (4.56) | 0.60 |
| Breast cancer subscale (0–40) | ||||
| SS | 10 | 26.90 (5.25) | 28.90 (5.44) | 0.37 |
| MS | 9 | 25.67 (5.31) | 26.79 (5.91) | 0.20 |
Abbreviations: FACT-B, Functional Assessment of Cancer Therapy-Breast; FACT-G, Functional Assessment of Cancer Therapy-General; MS, multiple set; SS, single set; TOI, trial outcome index.
†Significant difference from preintervention values.
Cancer-related fatigue outcomes are shown in Table 5. Affective meaning subscale score showed similar results between the preintervention and postintervention time points in SS and MS (P = .109), with no difference between the groups (P = .308). The behavioral/severity subscale score decreased preintervention to postintervention (P = .003) in SS (−0.5% [1.8%]) and MS (−2.3% [2.4%]), with no difference between the groups (P =.469). For all the other subscales, a group × time point interaction was observed (P < .05). Bonferroni post hoc indicated that only the MS group decreased its sensory (−2.5% [2.3%]; P = .001), cognitive/mood (−2.3% [1.9%]; P < .001) subscales and total fatigue (−2.1% [1.7%]; P < .001) scores. The SS group, on the other hand, showed similar results between the preintervention and postintervention time points for these outcomes (sensory subscale: P = .389; cognitive/mood subscale: P = .584; total fatigue score: P = .456). Moreover, for the sensory and cognitive/mood subscales, as well as for total fatigue, no differences were found between the groups both preintervention (P = .238; P = .258; P =.238, respectively) and postintervention (P = .700; P = .403; P =.970, respectively).
Cancer-Related Fatigue Outcomes Pre and Post SS and MS Interventions
| Outcomes | n | Pre | Post | Cohen d |
|---|---|---|---|---|
| Mean (SD) | Mean (SD) | |||
| Affective meaning (0–10) | ||||
| SS | 10 | 2.80 (3.00) | 2.38 (2.85) | −0.14 |
| MS | 9 | 4.67 (3.78) | 3.58 (3.87) | −0.28 |
| Behavioral/severity (0–10) | ||||
| SS | 10 | 2.92 (2.88) | 2.28 (2.15)† | −0.25 |
| MS | 9 | 4.52 (3.30) | 2.30 (2.04)† | −0.81 |
| Sensory (0–10) | ||||
| SS | 10 | 2.62 (2.66) | 2.20 (2.31) | −0.17 |
| MS | 9 | 4.22 (3.21) | 1.84 (1.74)† | −0.92 |
| Cognitive/mood (0–10) | ||||
| SS | 10 | 2.65 (2.47) | 2.40 (2.25) | −0.11 |
| MS | 9 | 3.96 (2.58) | 1.71 (1.29)† | −1.10 |
| Total fatigue scale (0–10) | ||||
| SS | 10 | 2.75 (2.72) | 2.35 (2.34) | −0.16 |
| MS | 9 | 4.32 (3.06) | 2.31 (1.98)† | −0.78 |
Abbreviations: MS, multiple set; SS, single set.
†Significant difference from preintervention values.
Cardiorespiratory Capacity Outcomes
The results of cardiorespiratory capacity outcomes are presented in Table 6. For VO2peak, both time (P = .125) and group × time point interaction (P = .078) factors were not significant. Conversely, the group factor was significant (P = .036), indicating that the MS group had a significantly higher VO2peak compared to the SS group regardless of time point. For the time to exhaustion outcome, there was a significant group × time point interaction (P = .037). Bonferroni post hoc showed that the MS group increased its time to exhaustion on the graded exercise test (21.3% [14.9%]; P < .001), but not the SS group (P = .722). No differences were found between the groups both pretraining (P = .898) and posttraining (P = .472).
Cardiorespiratory Capacity Outcomes Pre and Post SS and MS Interventions
| Outcomes | n | Pre | Post | Cohen d |
|---|---|---|---|---|
| Mean (SD) | Mean (SD) | |||
| VO2peak, mL·kg−1·min−1 | ||||
| SS | 10 | 21.97 (5.98) | 21.75 (6.01) | −0.04 |
| MS | 9 | 26.00 (6.78)§ | 29.01 (5.97)§ | 0.47 |
| VO2VT2, mL·kg−1·min−1 | ||||
| SS | 10 | 22.11 (5.41) | 21.69 (6.10) | −0.07 |
| MS | 9 | 19.54 (5.31) | 20.72 (4.95) | 0.23 |
| Time to exhaustion, min | ||||
| SS | 10 | 13.31 (5.47) | 13.60 (6.13) | 0.05 |
| MS | 9 | 13.00 (4.86) | 15.40 (4.74)† | 0.50 |
| Time at VT2, min | ||||
| SS | 10 | 9.29 (2.69) | 9.49 (2.91) | 0.07 |
| MS | 9 | 9.25 (4.11) | 10.54 (3.72) | 0.33 |
Abbreviations: MS, multiple set; SS, single set; VO2peak, peak oxygen uptake; VO2VT2, oxygen uptake at the second ventilatory threshold; VT2, second ventilatory threshold.
†Significant difference from preintervention values. §Significant difference from SS values.
The individual comparisons in both groups are shown in Figures 3–5. The knee extension 1RM (Figure 3, panels A and B), quality of life (measured by FACT-B questionnaire; Figure 4, panels A and B), and cancer-related fatigue (Figure 4, panels C and D) were measured preintervention and postintervention in 7 and 8 participants in SS and MS groups, respectively. The quadriceps MT was evaluated pre and post in 6 and 7 participants in SS (Figure 3, panel C) and MS (Figure 3, panel D) groups, respectively, while the time to exhaustion was measured in 7 participants in SS (Figure 5, panel A) and MS (Figure 5, panel B) groups.
—Mean (bars) and individual (lines) maximal dynamic strength (knee extension 1RM, panels A and B) and MT (quadriceps MT, panels C and D) in preintervention and postintervention for SS and MS interventions. Waterfall plot of the individual differences in maximal dynamic strength (knee extension 1RM, panel E) and MT (quadriceps MT, panel F) between SS (gray bars) and MS (white bars) groups. 1RM indicates 1-maximal repetition; MS, multiple set; MT, muscle thickness; SS, single set.
Citation: Journal of Physical Activity and Health 20, 3; 10.1123/jpah.2022-0097
—Mean (bars) and individual (lines) maximal dynamic strength (knee extension 1RM, panels A and B) and MT (quadriceps MT, panels C and D) in preintervention and postintervention for SS and MS interventions. Waterfall plot of the individual differences in maximal dynamic strength (knee extension 1RM, panel E) and MT (quadriceps MT, panel F) between SS (gray bars) and MS (white bars) groups. 1RM indicates 1-maximal repetition; MS, multiple set; MT, muscle thickness; SS, single set.
Citation: Journal of Physical Activity and Health 20, 3; 10.1123/jpah.2022-0097
—Mean (bars) and individual (lines) maximal dynamic strength (knee extension 1RM, panels A and B) and MT (quadriceps MT, panels C and D) in preintervention and postintervention for SS and MS interventions. Waterfall plot of the individual differences in maximal dynamic strength (knee extension 1RM, panel E) and MT (quadriceps MT, panel F) between SS (gray bars) and MS (white bars) groups. 1RM indicates 1-maximal repetition; MS, multiple set; MT, muscle thickness; SS, single set.
Citation: Journal of Physical Activity and Health 20, 3; 10.1123/jpah.2022-0097
—Mean (bars) and individual (lines) quality of life (FACT-B, panels A and B) and cancer-related fatigue (total fatigue, panels C and D) in preintervention and postintervention for SS and MS interventions. Waterfall plot of the individual differences in quality of life (FACT-B, panel E) and cancer-related fatigue (total fatigue, panel F) between SS (gray bars) and MS (white bars) groups. FACT-B indicates Functional Assessment of Cancer Therapy-Breast; MS, multiple set; SS, single set.
Citation: Journal of Physical Activity and Health 20, 3; 10.1123/jpah.2022-0097
—Mean (bars) and individual (lines) quality of life (FACT-B, panels A and B) and cancer-related fatigue (total fatigue, panels C and D) in preintervention and postintervention for SS and MS interventions. Waterfall plot of the individual differences in quality of life (FACT-B, panel E) and cancer-related fatigue (total fatigue, panel F) between SS (gray bars) and MS (white bars) groups. FACT-B indicates Functional Assessment of Cancer Therapy-Breast; MS, multiple set; SS, single set.
Citation: Journal of Physical Activity and Health 20, 3; 10.1123/jpah.2022-0097
—Mean (bars) and individual (lines) quality of life (FACT-B, panels A and B) and cancer-related fatigue (total fatigue, panels C and D) in preintervention and postintervention for SS and MS interventions. Waterfall plot of the individual differences in quality of life (FACT-B, panel E) and cancer-related fatigue (total fatigue, panel F) between SS (gray bars) and MS (white bars) groups. FACT-B indicates Functional Assessment of Cancer Therapy-Breast; MS, multiple set; SS, single set.
Citation: Journal of Physical Activity and Health 20, 3; 10.1123/jpah.2022-0097
—Mean (bars) and individual (lines) time to exhaustion in preintervention and postintervention for SS (panel A) and MS (panel B) interventions. Waterfall plot of the individual differences in time to exhaustion (panel C) between SS (gray bars) and MS (white bars) groups. MS indicates multiple set; SS, single set.
Citation: Journal of Physical Activity and Health 20, 3; 10.1123/jpah.2022-0097
—Mean (bars) and individual (lines) time to exhaustion in preintervention and postintervention for SS (panel A) and MS (panel B) interventions. Waterfall plot of the individual differences in time to exhaustion (panel C) between SS (gray bars) and MS (white bars) groups. MS indicates multiple set; SS, single set.
Citation: Journal of Physical Activity and Health 20, 3; 10.1123/jpah.2022-0097
—Mean (bars) and individual (lines) time to exhaustion in preintervention and postintervention for SS (panel A) and MS (panel B) interventions. Waterfall plot of the individual differences in time to exhaustion (panel C) between SS (gray bars) and MS (white bars) groups. MS indicates multiple set; SS, single set.
Citation: Journal of Physical Activity and Health 20, 3; 10.1123/jpah.2022-0097
Only one participant in the SS group did not modify the knee extension 1RM preintervention to postintervention (Figure 3, panel E). The quadriceps MT (Figure 3, panel F) in all participants increased in both groups. For FACT-B, 3 participants in the SS group presented a decrease in the score, while 4 participants presented positive gains. In the MS group, 2 participants presented a decrease in FACT-B score, one did not modify, and 5 presented positive gains after the intervention (Figure 4, panel E). Regarding cancer-related fatigue, 3 participants in the SS group presented zero fatigue scores at baseline, and at the end of the intervention, they continued to report no fatigue. One participant increased the fatigue score, and the other did not modify it. Two participants decreased their total fatigue score after the intervention. In the MS group, 2 participants presented zero fatigue score at baseline, and at the end of the intervention, they continued to report no fatigue, and the others (ie, 6 women) decreased the total fatigue score after intervention (Figure 4, panel F). For the time to exhaustion, 4 participants in the SS group presented a decrease in this outcome, while 3 participants presented positive gains. In the MS group, all the participants presented positive gains in time to exhaustion after the intervention (Figure 5, panel C).
Discussion
This study aimed to investigate the effects of different resistance training volumes within a combined training routine on physical and perceptual outcomes in breast cancer survivors. The main findings were that cancer-related fatigue and time to exhaustion on the graded exercise test improved only in the MS group after the intervention. On the other hand, similar improvements in maximal knee extension dynamic strength, knee extensors muscle thickness, and quality of life in breast cancer survivors, irrespective of the resistance training volume performed.
Our investigation is possibly the first experimental study to compare the effects of different resistance training volumes in breast cancer survivors. Lopez et al30 conducted a systematic review and meta-regression to examine the occurrence of a dose–response effect for both volume and intensity in breast cancer patients undergoing primary treatment that performed resistance training. Their results showed that resistance training weekly prescribed volume was inversely associated with increases in upper and lower body-muscle strength, although there was no relationship between resistance training intensity and strength gains. In the present study, we demonstrate that both SS and MS increased knee extension 1RM and quadriceps MT with no difference between the groups. These results follow those of previous studies that analyzed the effects of 6 to 13 weeks of resistance training interventions executed with 1 and/or 3 sets in older women.15,16
Muscle weakness is a common side effect of cancer treatment that is usually associated with loss of function.31,32 A study of breast cancer survivors that were assessed after primary chemotherapy showed that muscle strength was 20% to 30% lower in 7 different exercises in comparison to a control group with individuals that never had cancer.5 Several studies have reported improvement in maximal dynamic strength after resistance training programs performed by breast cancer survivors.33–39 These studies lasted between 12 and 24 weeks and included breast cancer survivors with a time since diagnosis of 4 to 94 months. Our study was executed during 8 weeks with breast cancer survivors diagnosed approximately 36 months before the enrolment in the study.
Moreover, irrespective of whether or not sarcopenia presents with or without weight change (gain or loss), adverse changes in body composition have been associated with greater morbidity (including strength and function impairments) and mortality.40 Studies that evaluated lean mass after resistance training programs in breast cancer survivors showed different results.34,41–44 Two studies reported significant improvement in lean mass after 16 weeks (3 sets of 10 repetitions) and 6 months (3 sets of 8–12 repetitions) of resistance training twice a week, respectively.34,42 Another study showed that those assigned to a passive control group significantly lost lean mass after 1 year. In contrast, the exercise group maintained its lean mass after 12 months of resistance training (3 sets of 10 repetitions) twice a week.41 Two additional studies reported that 1 year of resistance training (only 13 wk supervised; 3 sets of 10 repetitions) did not impact the lean mass of both exercise and nonexercise groups.43,44 These studies34,41–44 evaluated the lean mass with a dual-energy x-ray absorptiometry scan, whereas quadriceps muscle thickness in our study was measured using ultrasound measures. Our study suggests that breast cancer survivors’ quadriceps muscle thickness can be improved as early as 8 weeks, independent of the resistance training volume employed.
As for the perceptual outcomes, Lopez et al45 systematically reviewed the effects of resistance training in prostate cancer patients to determine the minimal dose of exercise components such as mode, duration, volume, and intensity on fatigue and quality of life. The researchers concluded that low-volume resistance exercise undertaken at a moderate to high intensity was sufficient to achieve significant fatigue and quality of life benefits in men with prostate cancer. On the other hand, our study found that cancer-related fatigue improved only in the MS group. But caution is needed to extrapolate this result because the SS and MS group’s fatigue scores differed at baseline. That is, while SS had only mild fatigue (2.8 points), MS showed moderate levels of fatigue (4.3 points).24 Thus, these different fatigue classifications may have influenced the intervention’s capacity to reduce fatigue in the former.
Fatigue is the most common side effect during cancer treatment. Over 90% of patients experience some level of fatigue during treatment, and in as much as 60% of survivors, fatigue will persist after treatment has ended.9 Cancer-related fatigue is distinct from the tiredness that the average person feels at the end of a workday or after a long exercise session and is described as the same as feeling “sick.”10 The experience of cancer-related fatigue has been associated with elevated cytokines; however, whether it is centrally or peripherally mediated remains unclear, and the precise mechanisms may vary across individuals, treatments, and treatment period.10 Research has demonstrated the benefits of aerobic and/or resistance training for reducing fatigue and showed that fatigue improves as the duration of training is lengthened to longer than 30 minutes per session; however, a cumulative dose beyond 150 minutes per week of aerobic exercise may not result in any greater reductions in fatigue.46
As previously mentioned, cancer treatment generates adverse psychological and physical symptoms, some of which include insomnia,47 depression,48 anxiety,49 and fatigue.9 These symptoms impact and impair patients’ social and physical functions, and, as a consequence, patients typically present a decrease in their overall quality of life. The improvements observed in the quality of life outcomes in the present study are, therefore, relevant, and even though cancer-related fatigue seemed to improve only in the MS group, quality of life improved similarly in both SS and MS. Combined moderate-intensity aerobic and resistance training improves health-related quality of life after treatment.50 Based on our results, it seems that a small dose of it is already enough to improve the quality of life in breast cancer survivors who were sedentary before the engagement in periodic and systematic training. Moreover, the benefits of combined aerobic and resistance training programs appear more potent than either aerobic or resistance training programs alone.50
Regarding cardiorespiratory capacity, there was no significant difference in VO2peak after the intervention. On the other hand, time to exhaustion improved, but only in the MS group. Survivors of some types of cancer have a significant increase in their risk of developing cardiovascular diseases because of the toxicity related to specific cancer treatments.7 In addition, low cardiorespiratory fitness has been implicated in the etiology of certain treatment-induced cardiovascular late effects and is a predictor of anthracycline- and trastuzumab-induced left ventricular dysfunction.7 This impact on cardiovascular function is relevant because reductions in cardiorespiratory fitness have been typically observed in response to cancer treatment. Fitness levels are estimated to be 30% below that of age- and sex-matched sedentary individuals without a history of cancer.8 Thus, efforts to prevent the decline or improve fitness following a cancer diagnosis, particularly for those with low fitness levels, are warranted. Our results suggest that the greater resistance training volume effectively improves breast cancer survivors’ time to exhaustion, but not VO2peak.
A possible limitation of the present study is its length. Longer intervention periods could bring more information regarding physiological and psychological adaptations in women who survived breast cancer. Another limitation is the absence of upper-body strength assessments. The shoulder function is often affected by breast cancer treatment, and therefore, it would have been important to assess bench press or shoulder press strength, for example. In addition, the final sample size was lower than that estimated on the sample size calculation, and, as a result, the results should be considered with caution. Another limitation is that we did not collect the participants’ eating and physical activity habits before and after the intervention. Finally, the present study included only breast cancer survivors who were not previously engaged in periodic and systematic training. Thus, caution is needed when extrapolating our results to other cancer-related populations.
Conclusions
Our results suggest that cancer-related fatigue and time to exhaustion improve only in those performing a MS resistance training volume, at least in the short term (ie, 8 wk). However, SS or MS resistance training volume configuration is sufficient to increase muscle strength and thickness and improve the quality of life of breast cancer survivors. From a practical standpoint, we found that performing even a low volume of muscle-strengthening exercises combined with aerobic activities might be a protective factor against breast cancer-related muscle wasting, enhancing muscle strength and thickness and improving breast cancer survivors’ quality of life.
Acknowledgments
The authors would like to thank the participants for contributing to this study. This work was supported by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brazil (CAPES, Finance Code 001).
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