Swenson, Karen K. PhD, RN; Nissen, Mary Jo PhD, MPH; Knippenberg, Kathryn MPH; Sistermans, Annemiek PT; Spilde, Paul PT; Bell, Elaine M. RN, OCN; Nissen, Julia BA; Chen, Cathleen MD; Tsai, Michaela L. MD
There are now nearly 12 million cancer survivors in the United States.1 Because of the aging population and improvements in cancer diagnosis and treatment, this number is expected to continue to increase.2 Although life expectancy for those diagnosed with cancer has increased, adverse effects of cancer and cancer treatments continue to be detrimental to both physical and psychological health and contribute to declines in quality of life (QOL). These include, but are not limited to, fatigue, pain, anxiety, depression, and reduced physical capabilities.3 Cancer rehabilitation entails physical, social, psychological, and vocational services to promote maximum functional capacity for oncology patients.4 Although many cancer rehabilitation programs offer services for specific patient needs, such as lymphedema, upper-extremity functional impairment, gait, and balance dysfunction, few programs offer comprehensive physical conditioning and strengthening services for oncology patients.
The goal of our cancer rehabilitation program was to maximize each patient’s ability to remain independent and productive through strengthening and conditioning. The major advantages of a cancer rehabilitation program compared with a supervised exercise program were as follows: (1) the program was offered in a rehabilitation center within the healthcare setting so that physical therapists had access to review patient’s electronic medical records prior to appointments, charted in the electronic medical record, and communicated with the healthcare team; (2) services were ordered by the medical oncologists using International Classification of Disease, Ninth Revision (ICD-9) codes, so the services were billable to the patient’s insurance; and (3) careful monitoring was conducted for safety measures by the physical therapists including checking presession heart rate, blood pressure, and blood glucose levels (for diabetics) prior to starting, during, and at the completion of each session.
Regular exercise can greatly affect the symptom experience by increasing physical well-being, decreasing fatigue, providing a sense of control, and serving as a diversion from emotionally distressing factors.3,5 Aerobic activity increases QOL,6–9 decreases fatigue,10–12 and decreases length of hospital stay.13 Resistance training increases QOL,14 mobility, strength, and power15 and is particularly useful in increasing strength and endurance in the upper extremities.16 Cancer patients and oncologists have expressed a need for structured conditioning and strengthening programs for patients during and after cancer treatment. Many patients and oncologists also have a preference for supervised rehabilitation programs.17
A recent review of various rehabilitation methods found that while all studies indicated beneficial results of exercise programs for oncology patients, an overall increase in QOL was associated with the amount of aerobic activity and the length of intervention.6 Although both individual-based and group-based physical activity programs show positive outcomes, group programs may have additional benefits of providing structure, encouragement, and social support to enhance program participation, improve long-term adherence, and increase psychological well-being. Group programs can also positively affect attendance and improve psychological symptoms.18,19 Participants in the present program were offered an individual or small group program based on their needs, insurance coverage, and personal preference.
The Cancer Survivorship Model of Care was used as a guide our institution in developing the Cancer Rehabilitation Program. Our primary physical therapist (A.S.) attended a weeklong cancer rehabilitation training session for health professionals at the Rocky Mountain Cancer Rehabilitation Institute before opening our Cancer Rehabilitation Program. The training program focused on teaching professionals how to implement and manage cancer rehabilitation centers to improve QOL for cancer survivors through prescriptive rehabilitation. Cancer survivorship begins at diagnosis and continues throughout the cancer continuum. According to the American Cancer Society, cancer survivorship care includes several performance indicators: (1) healthy habits, (2) early detection/disease surveillance, (3) management of adverse effects (psychosocial and physical), and (4) healthcare professional communication. In this study, we addressed 2 components: (1) healthy habits (measured with outcomes of functional status and conditioning level) and (2) management of adverse effects (measured with the M. D. Anderson Symptom Inventory [MDASI]). Symptoms included fatigue, disturbed sleep, shortness of breath, sadness, and distress, which may be an acute or a late adverse effect of cancer and/or cancer treatment.
The purpose of this study was to determine if an outpatient, comprehensive, physical therapy–supervised cancer rehabilitation strengthening and conditioning program improved patient’s functional status, conditioning level, oncology symptoms, and QOL. Specific aims were to compare individual preprogram and postprogram measures of functional status, conditioning level, symptom severity, symptom interference with daily life, and QOL. Secondary aims were to evaluate if program benefits were continued with a 6-month maintenance program beyond the completion of the initial intensive program and to evaluate which patients benefited the most from the program based on demographic or clinical characteristics.
Eligible participants included all patients with cancer who were referred to the Cancer Rehabilitation Strengthening and Conditioning (CRSC) program by their medical oncologist during or after completion of cancer treatments. The medical oncologist completed and signed a CRSC program referral form with a checklist of referral reasons along with associated ICD-9 diagnosis codes. Referrals were made for oncology patients who had (1) fatigue/malaise due to treatment or malignancy, (2) balance difficulties due to malignancy or treatment, (3) muscle weakness, (4) steroid myopathy, (5) peripheral neuropathy, (6) low back pain, and/or (7) inability to independently regain pretreatment activities of daily living, stamina, or endurance. Referrals were made at any point along the disease trajectory from early cancer diagnosis, immediately following treatment completion, and during late-stage disease. At each patient’s initial evaluation in the CRSC program, they were invited to participate in the study, and if they agreed to participate, they were asked to sign a consent form. Eligibility criteria for the study included cancer diagnosis, referral to the CRSC program, ability to read and understand the consent form and questionnaires, and willingness to participate in the study. The study was reviewed and approved by the Park Nicollet Institute institutional review board.
The study methodology was a single-sample, preprogram-postprogram longitudinal design. A control group was not used for this study because medical oncologists wanted to offer the program to all of their eligible oncology patients. Other preliminary studies have shown beneficial effects from exercise and rehabilitation programs for oncology patients. Outcome variables were assessed at baseline (prior to program participation), at the end of the intensive phase of the program (at approximately 8 weeks), and at the end of the 6-month maintenance phase of the program. Demographic and clinical characteristics included age, gender, cancer type, extent of disease (metastatic vs nonmetastatic cancer diagnoses), treatment type, and Charlson Comorbidity Index20 score based on ICD-9 codes recorded in the medical record. The Charlson Comorbidity Index provided a valid method of estimating risk of death from comorbid diseases by assigning a numerical value of comorbidity level.20 Points are assigned (0-10) based on the participant’s other serious illnesses such as diabetes mellitus and/or liver, renal, cerebrovascular, and/or cardiovascular disease.
The CRSC program combined aerobic exercise and strength training supervised by a physical therapist. The program was designed and implemented to help cancer patients increase endurance, strength, and flexibility and decrease oncology-related symptoms. The first 2 sessions included an evaluation and a follow-up visit with a physical therapist. Through these 2 individual sessions, it was determined whether patients would participate in individual or group sessions. Patients who needed physical help when walking, transferring, or using any of the exercise equipment continued to attend 1-hour, individual sessions supervised by a physical therapist. Individual or group sessions were recommended based on the patient’s need for physical assistance during the sessions, insurance coverage for group sessions, patient’s scheduling needs, and personal preference. Patients who were more independent but needed strength and endurance training transitioned to the 90-minute group sessions in which there were up to 4 oncology patients attending.
The program was conducted in the Park Nicollet Heart and Vascular Fitness Center located adjacent to Methodist Hospital in Minneapolis, Minnesota.The facility contains treadmills, elliptical machines, upright and recumbent bikes, a Life-Fitness functional cable machine, and a walking track. Because the physical therapists were part of the healthcare team, they had access to the patient’s medical records, so that they could review the patient’s diagnosis, treatment, and comorbid health conditions prior to the initial evaluation. Physical therapists monitored participants’ heart rate, blood pressure, and oxygen saturation at baseline, after the 6-minute walk test (SMWT), and at the end of the session for safety. Session rigor and length were adjusted for participants according to individual physiological measures.
At the completion of the intensive CRSC program, patients were offered an opportunity to participate in a medically supervised exercise program in the same facility for an additional 6 months with all monthly fees waived. This provided participants with a setting to continue to improve or to maintain the strength and endurance they achieved in the intensive program.
Functional status was measured by the Physical Component Summary (PCS) of the Short Form 36 (SF-36), a self-administered 36-item survey.21 Four of the 8 scales of the SF-36 contribute to the PCS: physical functioning, role-physical, bodily pain, and general health. Results were expressed as a standardized score from 0 to 100 with a mean of 50 and an SD of 10. Very low scores are interpreted as having substantial limitations in self-care, and very high scores show no physical limitations and excellent health. Internal consistency across domains was found to be high, and criterion validity comparing functional status and well-being with overall health was high.22
Conditioning level was measured using an SMWT, a standardized procedure for determining the distance a person can walk during 6 minutes.23 Step-by-step protocol safety measures and guidelines for interpretation of results were followed as outlined by the American Thoracic Society.24 Data on resting and post-SMWT blood pressure, pulse, and oxygen saturation were obtained during the SMWT. Grip strength was measured in pounds of pressure using a handheld dynamometer. The maximum reading from 3 attempts using the patient’s dominant hand was recorded. Metabolic equivalent (MET) level, the level of intensity at which the participant performed physical activities, was recorded by the physical therapist. The MET rating is a measure of the energy expenditure of activities compared with the resting metabolic rate (MET of 1.0 = resting metabolic rate). “Time on treadmill” was the total time period that the patient could tolerate walking on the treadmill as recorded by the physical therapist.
Symptoms were assessed using the MDASI, a validated, reliable 19-item questionnaire that measures the severity and impact of common cancer-related symptoms such as nausea/vomiting, pain, fatigue, and sadness.25 This questionnaire is a self-rated measure of the severity of cancer-related symptoms on an 11-point scale from 0 (not present) to 10 (as bad as you can imagine). It also assesses how much symptoms interfere with general activity, mood, work, relations with others, walking, and enjoyment of life. The mean of responses to the first 13 items on the MDASI provides a measure of symptom severity, whereas the last 6 items on the MDASI provide a measure of how symptoms interfere with life.
Quality of life was measured using the Mental Component Summary (MCS) of the SF-36.21. The SF-36 is a widely used validated instrument for measuring patient-reported QOL. Four scales contributed to the MCS: vitality, social functioning, role-emotional, and mental health. Results were expressed as a standardized score from 0 to 100 with a mean of 50 and an SD of 10. Very low scores were interpreted as showing a high level of psychological distress and social/role disability due to emotional problems, whereas high scores reflect positive affect and excellent mental health. The MCS of the SF-36 has high sensitivity and specificity for diagnosing depressive disorders.21
For analytic purposes, patients were categorized as having completed the intensive CRSC program if baseline measurements and post–intensive measurements were both available for at least 1 outcome measure. Comparisons of demographic and clinical characteristics of patients who did versus did not complete the intensive program used χ2 or Fisher exact tests for categorical variables and t tests for continuous variables were performed. Chart review was used to confirm details of patients’ oncology treatment as well as comorbidities. The Charlson Comorbidity Index provided a numerical value of comorbidity level.20 Time since active treatment (surgery, chemotherapy, or radiation therapy) was calculated as number of months from the most recent treatment until the date on which the patient provided informed consent for the study.
Paired t tests compared baseline and post–intensive measurements on each outcome. For descriptive purposes, a difference score was also calculated on each outcome variable: result following the CRCS program minus result obtained at baseline. The mean, median, and range of differences were determined. Results on the SF-36 and MDASI obtained following the 6-month maintenance program were also compared with baseline data by paired t tests, and the mean, median, and range of difference scores were calculated as result following the maintenance program minus result at baseline.
Regression analyses were used to identify clinical or demographic characteristics that were predictive of change from baseline on outcome measures. For this purpose, the following potential predictor variables were evaluated: age, gender, type of cancer, cancer stage (metastatic vs nonmetastatic), time since end of active treatment (still in active treatment, <6 months, 6 to <12 months, >12 months), surgery (yes/no), chemotherapy (yes/no), radiation therapy (yes/no), hormone therapy (yes/no), comorbidity score (higher vs lower than median score), type of participation (group vs individual), number of sessions of participation, and baseline scores on the outcome measure.
All analyses were conducted using SAS version 9.2 (SAS Institute, Cary, North Carolina). All tests of significance were 2-sided with a P < .05.
One hundred fifteen patients were recruited for the study (Table 1). Consecutive patients who were referred to the CRSC program were recruited from May 2009 through September 2010. Forty patients did not complete the rehabilitation program for a variety of reasons, the most common of which were medical complications (n = 11) and noncompliance with attendance/scheduling of future appointments (n = 15). Demographic and clinical characteristics of patients who completed the intensive CRSC program versus those who did not differed on only 2 characteristics (Table 1): time since end of active treatment and group versus individual participation. Patients who did not complete the program were more likely to still be receiving active treatment (P = .001) and were less likely to have attended group sessions (P = .001). Table 2 contains baseline data for the outcome variables.
Results for the SMWT showed that, on average, patients were able to walk 186.4 ft farther at the end of the intensive program than at baseline (P < .0001) (Table 3). The average speed on the SMWT increased by 0.35 mph (P < .0001), and patients walked 3.5 minutes longer on the treadmill (P = .001). Patients also raised their MET level by 0.87 (P < .0001). Grip strength was not significantly greater at the end of the intensive phase of the program, although the average grip strength increased by 2.4 lb.
Functional Status/Quality of Life
Physical Component Summary scores on the SF-36 increased by 5.9 points (P < .0001) indicating a significant improvement in functional status. The MCS score increased by 4.8 points (P = .005). Among patients who completed the SF-36 following the 6-month maintenance program, the PCS score remained significantly improved relative to baseline (P < .0001), but the MCS score did not.
Symptom Severity and Interference With Daily Life
Results on the MDASI showed significant decreases in symptom severity (P < .0001), symptom interference (P < .0001), fatigue (P = .003), shortness of breath (P = .007), and feelings of sadness (P = .004). Results following the 6-month maintenance program showed significant decreases relative to baseline in symptom severity (P = .0004), symptom interference (P = .0017), fatigue (P = .0077), shortness of breath (P = .0005), and disturbed sleep (P = .045).
Predictors of Change From Baseline
The strongest predictor of improvement following the CRCS program was baseline performance: those who showed worse performance at baseline showed the greatest improvement. This was true for the MCS scale of the SF-36 (P = .0003): symptom severity (P = .005), symptom interference (P ≤ .0001), fatigue (P = .0003), disturbed sleep (P < .0001), shortness of breath (P < .0001), and feeling sad (P < .0001) on the MDASI; distance (P = .024) and speed (P = .043) on the SMWT; and time on treadmill (P < .0001).
In addition, patients still undergoing active treatment showed significantly less improvement on the MCS scale of the SF-36 after the CRCS program than those who had completed treatment (P = .001), and this difference was maintained after adjustment for baseline score. Other potential predictor variables were not significantly associated with amount of improvement.
This study included a heterogeneous group of oncology patients at all stages along the disease trajectory from initial diagnosis of early-stage nonsymptomatic cancer to metastatic symptomatic disease. Patients were referred to the program by their medical oncologist, and it is interesting to note that patients at all stages of disease were deemed appropriate for referral. The cancer rehabilitation program had beneficial effects on participants’ conditioning level, functional status, QOL, symptom severity, and symptom interference with daily life. The program was associated with significant improvements from baseline in conditioning level and functional status measured by the SMWT, MET level, time tolerated on the treadmill, and SF-36 PCS. This is consistent with other oncology-related exercise studies with improvements experienced in muscular strength, endurance, and physical functioning.26,27 Most notable are the significant improvements in overall symptom severity and interference with daily life, but also in specific symptoms including fatigue, shortness of breath, and sadness. These improvements were noted even though approximately one-third of participants had metastatic disease while they were enrolled in the program. These results concur with other conditioning and strengthening programs that were associated with improvements in pain, fatigue, bone health, and other emotionally distressing symptoms.3,5,11,12,28–30 Evidence is emerging that physical activity may even impact cancer recurrence and survival. A recent review of studies evaluating the impact of physical activity on breast cancer mortality found that being physically active provided a protective effect against breast cancer recurrence.31 More studies will be necessary to determine how physical activity affects recurrence and survival for other cancer diagnoses.
This study provides evidence that the program was most beneficial for patients who were more deconditioned at baseline; this group of patients showed the greatest improvement in their conditioning during the program. This is an interesting finding because many of those patients would not typically embark on an independent exercise program because of safety concerns. Other studies have shown that, with supervision, palliative cancer patients are willing and able to participate in physical activity interventions.32
Patients who attended the group sessions were more likely to complete the program. Patients reported anecdotally that they enjoyed participating in the group sessions because of the camaraderie that developed with other patients. When the CRSC program was developed, we envisioned that most participants would attend group sessions. However, many patients who were enrolled in the program were physically debilitated at baseline and required one-on-one attention with the physical therapist for safety reasons. Insurance coverage was provided for the CRSC program through the Centers for Medicare & Medicaid Services and/or patient’s private insurance. One of the private insurance carriers did not allow insurance coverage for group participation in the program, further limiting the number of patient participating in group sessions.
Study limitations include lack of control group. A single-sample, preprogram-postprogram design allows the possibility that the improvements noted with the program were related to recovery from treatment rather than program participation. Participants in the program were at all stages of the disease and treatment trajectory with approximately one-third of participants having metastatic disease during program participation. Other limitations include an unknown refusal rate for study participation and a relatively high dropout rate of 35% (40 of 115 participants enrolled). The program was open to all oncology patients regardless of disease and treatment status, so many of the enrollees were actively undergoing treatment during program participation.
Strengths of this program include that it was open to all patients with a cancer diagnosis regardless of cancer type, disease and treatment status, age, or gender. A finding from this study was that the greatest benefit from the program was experienced by participants who were the most debilitated at baseline. We also found the group setting to be acceptable and beneficial for those participants who were appropriate for a group cancer rehabilitation setting. Patients were enthusiastic about participating in the program, and 29 patients continued their participation in the 6-month extended program. These are important findings for clinical practice. Future research should focus on further testing a group setting for a cancer rehabilitation model and exploring a cancer rehabilitation model in patients who are receiving treatment for metastatic disease.
The authors would like to acknowledge Debi Lillegard posthumously for her contribution to development of the CRSC program at Park Nicollet Frauenshuh Cancer Center.
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