Design and Procedures
Thirty-eight female patients who completed cancer treatment were enrolled. Patients were recruited through a state-wide referral network comprised of oncologists, radiologists, and surgeons. All participants received exercise clearance from their oncology-related medical provider and medical histories were provided. Inclusion criteria included being female, having been diagnosed with cancer, having completed clinical cancer treatments at least 3 months previously, being ambulatory, over the age of 18 years, received exercise clearance from their provider, literacy in English, and ability to attend exercise sessions for 12 weeks. Prior to participation, patients provided their verbal and written consent. Research activities were approved by the Institutional Review Board (IRB, #2018 − 00167).
Initial and final fitness testing took place in-person; final assessments were conducted during the pandemic using additional safety precautions as approved by the IRB. At the mid-point of the exercise intervention, the COVID-19 pandemic emerged, precluding in-person, individualized exercise training. All participants were given the option to continue their program virtually during the quarantine. Of the 38 patients, 16 completed the intervention (mean age±SD: 65±10 years). Twelve of these patients were new to the program and these novice exercisers received 3 exercise sessions per week (36 sessions total). Four patients were experienced exercisers, having completed a 12-week face-to-face exercise program prior to their current enrollment. In the current study, they received 2 exercise sessions per week (24 sessions total). Participants included those diagnosed with breast cancer (invasive ductal carcinoma and invasive lobular carcinoma in either the right or left breast, n = 14), endometrial carcinoma (n = 1) and Non-Hodgkin’s lymphoma (n = 1). Cancer treatments completed by breast cancer patients included breast lumpectomy or mastectomy (right, left or both sides, n = 13), conserving therapy (n = 1), reconstruction (n = 3), radiation (n = 7), chemotherapy (n = 6), and hormonal therapy (utilizing Herceptin, Anastrozole and/or Tamoxifen, n = 11).
Balance measures
Unipedal single leg stance (SLS) was used to measure static balance. Patients were instructed to balance on each bare foot, beginning with their dominant foot for as long as possible up to a maximum time of 45 seconds. This was performed with and without visual feedback, eyes open (EO) and eyes closed (EC), on both right (R) and left (L) feet. The best score out of 3 trials was recorded for EOR, EOL, ECR and ECL.
Dynamic balance was measured with the Bertec Balance Screener (Columbus, OH). Limits of Stability (LOS) were evaluated in the anterior-posterior and medio-lateral directions on a flat/firm surface with visual feedback. Patients were directed to sway in each direction including forward (F), back (B), right (R) and left (L) in order to approach the limits of their base of support while maintaining foot placement and complete foot contact with the force plate. The LOS values were normalized to their age- and height-predicted values and expressed as a percentage. The LOSF, LOSB, LOSR, LOSL and overall LOS percentile scores were recorded.
Postural measures
All postural measurements were qualitatively assessed. Subjective descriptions such as “mild” or “significant” variations in posture have used to describe the severity of an abnormality [15]. However, the use of this method is limited by subjective observations and therefore, the presence or absence of a deviation was recorded and frequencies of postural deviations were analyzed in each group.
Overhead Squat. The National Academy of Sports Medicine’s (NASM) overhead squat assessment was used to assess muscle imbalance and postural deviations during a dynamic squat [16]. Patients were asked to stand with their feet-distance apart, toes pointing forward, heels on the floor and arms extended overhead. Then, they were asked to slowly squat down to sit in a chair while evaluators noted upper and lower body anatomical deviations (i.e., forward head/arms/torso, knees and toes pointing inward/outward).
Plumb line Method. This method was used to assess posture deviations in a static position in anterior, sagittal and posterior views. Patients were asked to stand comfortably in the anatomical position with their feet shoulder width apart and arms hanging to the side while evaluators noted prominent deviations. In the sagittal view, the presence or absence of forward head, forward lean, scapular protraction/retraction, kyphosis, lordosis and posterior or anterior pelvic tilt was recorded. In the anterior view, the following deviations were notated: head tilt or rotation, shoulder elevation, high hip, valgus or varus knee, pronation or supination of feet and inward or outward pointing toes. The posterior view was used to detect weight shifts, hyperextension of the knees or elevation of hips.
Cardiorespiratory, body composition, flexibility, muscular fitness measures
Prior to physical fitness testing, resting vital measurements were used to verify that all subjects had normal blood pressure, oxygen saturation and sinus rhythm. Body composition, muscular strength, flexibility and cardiovascular endurance were measured pre- and post-intervention. These measures helped to identify baseline fitness characteristics as well as show changes in fitness. Body composition was measured with bioimpedance analysis (Omron, HMF306), waist circumference measurements, waist-to-hip ratios and body mass index. Lower body muscular strength was assessed using 1-repetition maximum (1-RM) tests using the horizontal leg press, seated leg extension and seated leg curl exercises. In cases where the 1-RM could not be achieved, a prediction equation was used to estimate 1-RM using the maximum weight lifted for 10 or less repetitions [17]. Hamstring flexibility was measured with the modified sit-and-reach test. Upper body flexibility was measured with the back scratch test with the right or left arm overhead with fingers of opposite hands reaching toward each other. A negative score indicates the fingers did not overlap while a positive score indicates overlapping of fingers. Cardiovascular endurance was measured with a treadmill protocol specific to the cancer population [18] where final speed and grade were used to estimate and maximal oxygen uptake (VO2peak) [19]. The test was terminated upon volitional fatigue, the patient’s request to stop or if contraindications to exercise were observed.
Exercise Training
Fifty percent of the exercise intervention was provided in person with the remaining 50% being provided virtually due to COVID-19 restrictions. The in-person training was led by an exercise specialist knowledgeable in cancer exercise rehabilitation principles. Exercise specialists were trained using a specialized curriculum [20]. Patients were led through 90-minute exercise sessions and at least 1 rest day was placed between training sessions. Specifically, patients completed 30 minutes of cardiovascular training and 5–7 resistance training exercises at a workload of 40–85% of the subject’s 1-repetition maximum (1-RM). Heart rate reserve (40–85% of HRR) [21] and Borg’s Rate of Perceived Exertion (RPE) were used to determine indices of physiological strains during cardiovascular training [22]. Heart rate (HR) was monitored throughout the session using a chest-based device that wirelessly connected to an external tablet (Polar H10, USA). Target RPE was 3–6 (on a scale of 0.5 to 10, where 0.5 corresponds to resting and 10 corresponds to maximal exertion). RPE was a necessary tool for patients who use pharmacological drugs that lower HR such as β-blockers, non-dihydropyridine calcium channel blockers and ivabradine [23]. RPE was reported after each exercise bout and helped to identify true physiological strain independent of HR response to exercise.
Balance was trained using foam pads, BOSU balls, stairs or other techniques to work on strengthening leg, foot and back muscles. Exercises that used tandem or split stances in resistance training exercises were used to train balance. With regard to postural training, exercise specialists used results of the NASM overhead squat assessment to identify specific muscles to stretch or strengthen with the goal of improving posture [24]. All exercise programs incorporated exercise training principles and followed recommendations of the ACSM for patients diagnosed with cancer, i.e., aerobic, resistance training, balance and flexibility training [19, 25]. Logbooks were used to document exercises and assure fidelity to the protocol.
Virtual programs followed the same guidelines listed above. Trainers provided the exercise program through email or Google Docs and patients reported their progress in the same manner or through phone or text messaging. Trainers utilized exercise equipment the patient had at home or outdoor activities (i.e., open water swimming, walking in the neighborhood) to create the exercise program. Trainers utilized online resources (i.e., videos which demonstrated the exercise) or shared videos of themselves performing the exercise. Trainers then relayed patient progress to administrators, and this correspondence was used to assure fidelity to the protocol.
Statistical analyses
Quantitative fitness data were analyzed with 2-way repeated measures ANOVAs with factors Time (pre, post) x Group (novice, experienced). Bonferroni’s posthoc multiple comparisons tests were used to detect differences between groups pre- to post-intervention; significance was set at P < .05 (GraphPad Prism, version 8.0.0 for Windows, San Diego, CA). Pilot data were used in power analyses to show that with 9 subjects, there would be a 95% chance of detecting improved static balance with a mean improvement of 5 seconds and incorporating 10 subjects would result in a 95% chance of detecting improved dynamic balance (power, 1-β = 0.8, one-tailed, SPSS ver. 27). Qualitative data for dynamic and static posture were organized into tables to show the frequencies of which a postural deviation was observed.