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Keywords:

  • stress management;
  • exercise;
  • cancer;
  • chemotherapy

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Method
  5. Results
  6. Discussion
  7. Acknowledgements
  8. REFERENCES

Although exercise may be used by some to decrease distress, little is known about how it may contribute to stress management (SM) among patients receiving chemotherapy. We evaluated whether exercise separately or in combination with SM training is effective at increasing perceived ability to manage stress. Patients receiving chemotherapy (N = 391) were randomized to receive usual care only (UCO), SM, exercise (EX), or stress management and exercise (SMEX). They completed the Measure of Current Status prior to receiving chemotherapy and 12 weeks after the first infusion. We hypothesized that participants randomized to an intervention condition would report improvements in relaxation, awareness of tension, getting needs met and coping confidence compared with those receiving UCO. Results indicated significant group-by-time interactions for the following: relaxation (UCO versus SM, p = 0.008), awareness of tension (UCO versus SMEX, p = 0.029 and UCO versus EX, p < 0.001), getting needs met (UCO versus SMEX, p = 0.020) and Measure of Current Status total score (UCO versus SMEX, p = 0.007 and UCO versus EX, p = 0.016). There were no group-by-time interactions for coping confidence (p-values >0.05). This study provides support for including an exercise component in SM interventions for cancer patients receiving chemotherapy (clinicaltrials.gov identifier: NCT00740038). Copyright © 2012 John Wiley & Sons, Ltd.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Method
  5. Results
  6. Discussion
  7. Acknowledgements
  8. REFERENCES

The diagnosis and treatment of cancer is stressful for many patients (Cordova et al., 1995). To address this issue, a number of stress management (SM) interventions have been developed and evaluated. Results of systematic reviews and meta-analyses of randomized controlled trials of interventions incorporating SM techniques show that they are effective in improving quality of life and relieving emotional distress in cancer patients undergoing treatment (e.g. Gorin et al., 2012; Jacobsen & Jim, 2008).

Mechanisms by which these interventions may yield improvements in quality of life and related domains in cancer patients are not well known. To date, attention has focused primarily on changes in patients' perceived ability to manage stress. Patients may experience improvements in quality of life domains after learning SM skills because they perceive themselves being better able to recognize tension and relax, more confident in their SM abilities and more confident about getting their needs met. Evidence in support of this view comes from studies that have used the self-report Measure of Current Status (MOCS; Carver, 2006) to assess cancer patients' perceptions of their SM skills (Antoni et al., 2006; Penedo et al., 2006). Confidence in SM skills is associated with better quality of life and less depression and anxiety in patients about to start chemotherapy treatment (Faul, Jim, Williams, Loftus, & Jacobsen, 2010). Among patients undergoing treatment for breast cancer (Antoni et al., 2006) and recovering from treatment for prostate cancer (Penedo et al., 2006), beneficial effects of group-based cognitive behavioural stress management (CBSM) interventions on quality of life outcomes have been explained by improvements in SM skills.

Another technique used to combat stress is exercise (Salmon, 2001). Although the group-based CBSM interventions described previously did not include exercise (Antoni et al., 2006; Penedo et al., 2006), recent meta-analyses found exercise interventions with cancer patients can have positive impacts on quality of life outcomes including anxiety (Speck, Courneya, Masse, Duval, & Schmitz, 2010) and depressive symptoms (Craft, VanIterson, Helenowski, Rademaker, & Courneya, 2012). To the best of our knowledge, there have been no studies evaluating whether cancer patients find exercise helpful in managing the stress of cancer treatment.

The purpose of the current study was to evaluate whether self-directed SM and/or home-based exercise training lead to improvements in specific SM skills. We previously found that a self-directed SM intervention is more efficacious and less expensive than a professionally administered intervention (Jacobsen et al., 2002). Furthermore, pilot data on the self-administered exercise and SM intervention demonstrated its feasibility, safety and effectiveness (Wilson, Taliaferro, & Jacobsen, 2006). The current randomized controlled trial was conducted in which patients receiving chemotherapy were randomized to one of four conditions [usual care only (UCO), SM, exercise (EX), stress management and exercise (SMEX)]. We recently reported that patients who received the combined intervention reported reduced anxiety and depression relative to patients who received UCO (Jacobsen et al., 2012). As part of the same study, patients completed the MOCS to measure their perceived ability to enact SM skills prior to initiating chemotherapy and approximately 12 weeks after their first infusion. We hypothesized that patients in the intervention groups would report improvements in relaxation, awareness of tension, getting needs met and coping confidence skills compared with those in the UCO condition. If more than one intervention condition was found to perform better than the usual care condition, additional analyses were performed to compare perceived SM ability among those groups.

Method

  1. Top of page
  2. Abstract
  3. Introduction
  4. Method
  5. Results
  6. Discussion
  7. Acknowledgements
  8. REFERENCES

Participants

Data for this report are drawn from a randomized controlled trial of the separate and combined effects of SMEX training on quality of life during chemotherapy (Jacobsen et al., 2012). Eligibility criteria were as follows: ≥18 years old, diagnosed with cancer, scheduled to receive chemotherapy for ≥9 weeks at the Moffitt Cancer Center (MCC), no chemotherapy treatment within the past 2 months, medically cleared for moderate intensity exercise (including ECOG performance status <2) and fluent in English.

Procedures

Patients were identified through medical record review and were recruited between June 2006 and December 2010. For those potentially eligible, clearance was obtained from their oncologists confirming the ability to engage in moderate intensity exercise. Before the first infusion and prior to randomization, patients signed an informed consent form approved by the University of South Florida Institutional Review Board and completed a baseline questionnaire. Participants were randomized using MCC's web-based clinical trials subject registration and randomization system. Randomization was stratified by gender, physical activity level (i.e. inactive, minimally active and active), chemotherapy administration schedule (i.e. Day 7/Day 14, Day 21/Day 28/Day 1 and Day 8) and concurrent radiotherapy (i.e. yes and no).

Intervention materials were distributed by a doctoral-level psychologist. Approximately 1 week later, the interventionist telephoned participants to ask if they had reviewed the materials and to address any questions. Participants completed a follow-up questionnaire that is the focus of this study approximately 12 weeks following their initial infusions. During scheduled clinic visits, research assistants handed participants follow-up questionnaires, which participants later completed in clinic or at home.

The UCO participants had access to the full range of psychosocial services provided to MCC patients. These included opportunities for free meetings with a social worker and support groups. Patients could also be referred or self-refer to in-house psychiatrists and psychologists on a fee-for-service basis. Specific to this condition, patients also met with the interventionist for approximately 5 min before the first infusion, at which time they received the booklet, ‘Chemotherapy and You’ (National Cancer Institute, 2007). This 62-page booklet includes information about chemotherapy and ways to manage side effects.

The SM participants met with the interventionist for approximately 10 min before the first infusion. As in our previous study (Jacobsen et al., 2002), they were provided with a 15-min video, 12-page booklet and 30-min audio recording titled, ‘Coping with Chemotherapy’. The video and booklet included information, demonstrations and instructions regarding paced breathing (Turk, Meichenbaum, & Genest, 1983), progressive muscle relaxation with guided imagery (Burish, Snyder, & Jenkins, 1991) and use of coping self-statements to manage stress (Meichenbaum, 1985). Participants were instructed to follow directions on how to learn and practise the techniques and use them during chemotherapy. Directions included listening to an audio recording, which led participants through an abbreviated form of progressive muscle relaxation training.

Exercise participants met with the interventionist for approximately 10 min before the first infusion. They were provided with a 12-min video and 14-page booklet titled, ‘Stepping Forward: A Guide to Exercise during Chemotherapy’ and an electronic pedometer (Digi-Walker SW-651-04). The video and booklet included information and instructions on engaging in regular exercise while undergoing chemotherapy. The emphasis was on walking, which is well suited to home-based exercise. Participants were advised to exercise 3–5 times per week for 20–30 min at approximately 50–75% of their estimated heart rate reserve, which is consistent with exercise recommendations for cancer patients (Courneya, Mackey, & Quinney, 2002).

The SMEX participants met with the interventionist for approximately 15 min before the first infusion. They were provided with a 20-min video and a 20-page booklet titled, ‘Stepping Forward: A Guide to Stress Management and Exercise during Chemotherapy’ that combined content from SM and EX videos and brochures. Participants also received the same audio recording provided to SM participants and pedometer provided to EX participants. Instructions for exercising and for learning, practising and using SM techniques mirrored those in the SM and EX conditions.

Measures

Demographic data were obtained at baseline through self-report. Medical information was obtained through review of patient records. Participants' current perceived ability to enact several SM skills was measured using Part A of the MOCS (Carver, 2006). Response options to the 13 items ranged from I cannot do this at all (1) to I can do this extremely well (5). Four factors were identified through principal-components analyses conducted by the measure's developers (Antoni et al., 2006): Relaxation is the average of two items (e.g. ‘I am able to use muscle relaxation techniques to reduce any tension I experience’); awareness of tension is the average of three items (e.g. ‘I can easily recognize situations that make me feel stressed or upset’); Getting needs met is the average of three items (e.g. ‘It's easy for me to go to people in my life for help or support when I need it’); Coping confidence is the average of five items (e.g. ‘It's easy for me to decide how to cope with whatever problems arise’). A total score was also generated by summing ratings for the 13 items. Prior work found MOCS associated with improvements in quality of life among cancer patients who received an SM intervention (Antoni et al., 2006; Penedo et al., 2006). Alpha reliability coefficients for the four MOCS components and total score were 0.62, 0.71, 0.85, 0.91 and 0.89, respectively.

Data analysis

In preliminary analyses, the demographic and clinical characteristics of participants based on randomization condition were compared using chi squares for categorical variables and one-way analyses of variance for continuous variables. To examine longitudinal changes in perceived ability to enact SM skills from baseline to 12-week follow-up, random effects models were applied using SAS Proc Mixed (SAS Institute, Cary, NC, USA), which uses all available data. Analyses focused on comparing each intervention condition separately with UCO. Initial analysis therefore consisted of three separate 2 (group comparison: UCO versus SM, UCO versus EX, UCO versus SMEX) by 2 (time: baseline, follow-up) analyses. Of principal interest was the significance of the group-by-time interaction, which would indicate differential improvement in perceived ability to implement SM skills as a function of intervention condition. In the case of significant interactions, the within-group time effects were examined to determine the direction and magnitude of change in each of the groups. Effect sizes were calculated using Cohen's d. An effect size of 0.2–0.3 is considered small; 0.5, medium; and ≥0.8, large (Cohen, 1988). If more than one group performed better than UCO, then similar interaction analyses were conducted comparing those groups. A p-value of 0.05 (two-tailed) was used for statistical significance. The study was powered at 0.80 to detect an effect size of f = 0.25 for the interaction between an intervention condition versus UCO and time, assuming a per group sample size of 80 and alpha = 0.05.

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Method
  5. Results
  6. Discussion
  7. Acknowledgements
  8. REFERENCES

Accrual data are presented in Figure 1. Of the 436 participants who received the intervention, 42 were enrolled before MOCS was added to the questionnaire. An additional three participants did not complete MOCS at baseline. Analyses are based on the 391 participants who completed MOCS baseline assessment.

image

Figure 1. CONSORT diagram

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Demographic and clinical characteristics are presented in Table 1. There were no differences across conditions for demographic or clinical characteristics, with the exception that Hispanic participants were more likely to receive UCO (χ2 = 10.26, p = 0.016). Because there were no group-by-ethnicity interactions for any MOCS components (p-values >0.05), ethnicity was not included as a control variable. Means and standard deviations of MOCS skills at baseline and follow-up are presented in Table 2.

Table 1. Characteristics of study participants, N = 391
 UCOSMEXSMEXpa
 (n = 98)(n = 101)(n = 90)(n = 102) 
  1. UCO: usual care only; SM: stress management; EX: exercise; SMEX: stress management + exercise; SCLC: small cell lung cancer.

  2. a

    p-values are based on chi square analyses for categorical variables and one-way analyses of variance for continuous variables.

Age (years)    0.186
Mean56.4057.3559.0559.60 
SD11.6511.5111.6911.56 
Gender    0.999
Males (%)34353434 
Females (%)66656666 
Education    0.389
College graduate (%)46363637 
Non-college graduate (%)54646463 
Race    0.617
White (%)92909494 
Non-white (%)81066 
Ethnicity    0.016
Hispanic (%)13374 
Non-Hispanic (%)87979396 
Relationship status    0.428
Married/partnered (%)64667274 
Not married/partnered (%)36342826 
Disease stage    0.955
Non-metastatic (%)62646666 
Stage I99710 
Stage II21222424 
Stage III31303231 
Limited SCLC1331 
Metastatic (%)38363434 
Stage IV36343431 
Extensive SCLC2203 
Cancer type    0.822
Breast (%)29292525 
Lung (%)27343530 
Other (%)44374045 
Bladder78410 
Cervical0100 
Colon3323 
Endometrial5335 
Esophageal1000 
Gastric1010 
Kidney1010 
Larynx1000 
Lip/oral1001 
Mesothelioma1284 
Nasal/sinus0001 
Oropharynx1101 
Ovarian12131015 
Prostate0022 
Rectal/anal0031 
Sarcoma3000 
Testicular2421 
Unknown4041 
Uterine1200 
Concurrent radiotherapy    0.873
Yes (%)9977 
No (%)91919393 
Previous chemotherapy    0.745
Yes (%)15202118 
No (%)85807982 
Table 2. Estimated means and standard deviations, N = 391
 RelaxationAwareness of tensionCoping confidenceGetting needs metMOCS total score
UCO     
  1. UCO: usual care only; SM: stress management; EX: exercise; SMEX: stress management + exercise.

Baseline2.71 (1.02)3.76 (0.74)3.65 (0.79)3.72 (0.99)46.11 (8.60)
Follow-up2.70 (1.10)3.47 (0.82)3.65 (0.87)3.66 (1.06)45.02 (9.25)
Cohen's d−0.01−0.370.00−0.06−0.12
SM     
Baseline2.73 (0.97)3.71 (0.78)3.75 (0.78)3.77 (0.96)46.63 (8.62)
Follow-up3.17 (1.12)3.66 (0.89)3.79 (0.88)3.84 (1.07)47.75 (9.80)
Cohen's d0.42−0.060.050.070.12
EX     
Baseline2.64 (1.14)3.57 (0.91)3.59 (0.87)3.70 (1.04)45.07 (9.92)
Follow-up2.81 (1.29)3.71 (1.02)3.79 (0.98)3.72 (1.19)46.93 (11.09)
Cohen's d0.140.140.220.020.18
SMEX     
Baseline2.72 (1.05)3.60 (0.86)3.73 (0.80)3.53 (1.08)45.49 (9.77)
Follow-up2.97 (1.24)3.59 (1.01)3.87 (0.88)3.79 (1.23)47.57 (10.94)
Cohen's d0.22−0.010.170.220.20

Analyses for the relaxation score yielded group-by-time interactions for UCO versus SM (p = 0.008) (Table 3). Evaluation of within-group time effects indicated perceived ability to relax increased over time in the SM (p = 0.002; Cohen's d = 0.42) but did not change in the UCO group (p = 0.899) (Figure 2a).

Table 3. Summary of analyses of interaction effects, N = 391
InteractionUCO versus SMpUCO versus EXpUCO versus SMEXp
FFF
  1. UCO: usual care only; SM: stress management; EX: exercise; SMEX: stress management + exercise.

Relaxation      
Group * time7.220.0081.590.2103.140.078
Awareness of tension      
Group * time3.720.05612.47<0.0014.860.029
Getting needs met      
Group * time0.870.3530.310.5795.510.020
Coping confidence      
Group * time0.150.7022.620.1081.750.188
Total score      
Group * time2.990.0865.990.0167.480.007
image

Figure 2. Change over time in skills

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Analyses for the awareness of tension score yielded group-by-time interactions for two comparisons: UCO versus SMEX (p = 0.029) and UCO versus EX (p < 0.001) (Table 3). Evaluation of within-group time effects indicated awareness of tension decreased in the UCO group (p < 0.001; Cohen's d = −0.37) while remaining stable in the SMEX (p = 0.921) and EX (p = 0.117) groups (Figure 2b). Group-by-time interactions for EX versus SMEX were non-significant (p = 0.322), suggesting changes in awareness of tension were comparable in these two groups.

Analyses for the getting needs met score yielded group-by-time interactions for UCO versus SMEX (p = 0.020) (Table 3). Evaluation of within-group time effects indicated perceived ability to get one's needs met increased over time in the SMEX group (p = 0.021; Cohen's d = 0.22) and did not change in the UCO group (p = 0.511) (Figure 2c).

Analyses for the coping confidence score did not yield any group-by-time interactions (p-values >0.05) (Table 3).

Analyses for the total score yielded group-by-time interactions for two comparisons: UCO versus SMEX (p = 0.007) and UCO versus EX (p = 0.016) (Table 3). Evaluation of the within-group time effects indicated perceived ability to use SM techniques increased in the SMEX group (p = 0.023; Cohen's d = 0.20) but did not change in the UCO group (p = 0.152) (Figure 2d). The increase in the EX group was not statistically significant (p = 0.059). Group-by-time interactions for EX versus SMEX were non-significant (p = 0.867), suggesting changes in perceived ability to use SM techniques were comparable in these two groups.

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Method
  5. Results
  6. Discussion
  7. Acknowledgements
  8. REFERENCES

We found that self-directed SM and home-based exercise interventions can produce changes in perceived ability to manage stress. Specifically, compared with participants in the usual care condition, participants in the SM condition reported an increase in ability to relax, those in both the exercise and combined SMEX conditions reported maintained awareness of tension, and those in the combined condition reported an increase in ability to get one's needs met. In contrast, coping confidence did not change as a function of intervention condition. Finally on a summary index, participants in the combined condition reported improved overall ability to manage stress.

Results in this study for self-directed SM training are consistent with prior research. Similar to prior research, we found that SM training produced an increase in perceived ability to relax (Antoni et al., 2006; Andersen, Shelby, & Golden-Kreutz, 2007); however, previous interventions consisted of intensive, group-based meetings over the course of 10 (Antoni et al., 2006; Penedo et al., 2006) or 26 (Andersen et al., 2007) sessions. In the current study, an effect was found using a brief, self-directed intervention where participants were instructed how to use SM skills during an initial visit then practised at home over the course of 12 weeks.

This study expands upon previous research by demonstrating that exercise contributes to improvements in overall SM skills. Moreover, we found an effect for exercise on awareness of tension, a skill for which a significant effect was not found among participants receiving a group-based CBSM intervention (Antoni et al., 2006). The current study revealed group-by-time interactions for usual care compared with both the exercise and combined interventions. Although awareness of tension did not increase in the intervention conditions, the interventions may have provided a protective effect against the decreased awareness of tension reported by those who received usual care.

The current study is among the first to explicitly test the effects of a combined stress management and exercise condition on SM skills. Of particular importance is the pattern of results showing that the combined intervention had broader effects on SM skills than either SM or exercise training alone. In addition to having a significant effect on overall skills similar to exercise alone and on awareness of tension similar to exercise alone, it was the only condition to produce a significant effect on getting needs met relative to usual care. The finding that the combined intervention affected participants feeling able to clearly express their needs in a way that provided them with the support they need was surprising. Although our intervention did not specifically address assertiveness, CBSM (which does include assertiveness training) did not have an effect on this component (Antoni et al., 2006). More work is needed to understand mechanisms behind this effect.

Coping confidence was the only SM skill assessed that did not vary as a function of intervention assignment. As some items assessing coping confidence asked about use of coping self-statements that were part of the SM condition (e.g. ‘I can easily stop and re-examine my thoughts to gain a new perspective’), others asked about one's ability to handle more general problems (e.g. ‘It's easy for me to decide how to cope with whatever problems arise’). More work is needed to understand how to assist patients increase their overall coping confidence, which may require interventions tailored to the needs and concerns of the participants.

Strengths of this study include the longitudinal design with a pre-chemotherapy baseline, comparison of three intervention conditions to standard care, and sample heterogeneity in terms of cancer diagnosis and disease stage. Other randomized studies of psychosocial interventions investigating SM skills have focused on breast (Andersen et al., 2004; Antoni et al., 2006) or prostate (Penedo et al., 2006) cancer patients and excluded patients with metastatic disease (Andersen et al., 2004; Antoni et al., 2006; Penedo et al., 2006). This study also has limitations. First, there is a lack of ethnic and racial diversity among participants. Additional work is currently underway by our group evaluating SM training for Latinas receiving chemotherapy. Second, the study relied on self-reported mastery of SM skills. Future research should look at biological indicators of SM (e.g. Phillips et al., 2008). Third, conducting analyses on MOCS subscales and total score may have inflated experimentwise error. Fourth, the reliability coefficient for the two-item MOCS relaxation component was small. Fifth, effect sizes were generally small suggesting limited clinical significance. However, the modest improvements should be balanced against the fact the intervention is easily implemented. Future research should evaluate whether a tailored intervention delivered via the internet can produce stronger effects. Finally, it was outside the scope of the current study to evaluate whether the intervention affected adherence to medical treatment, which should be considered in future research.

In summary, this study provides strong evidence that exercise training can enhance the ability of cancer patients to manage stress while undergoing chemotherapy. Findings also suggest that an intervention combining stress management and exercise training may have broader effects on abilities to manage stress than either stress management or exercise training alone. Findings support conducting additional research on exercise interventions and combined SMEX interventions to help patients manage the stress of cancer treatment.

Acknowledgements

  1. Top of page
  2. Abstract
  3. Introduction
  4. Method
  5. Results
  6. Discussion
  7. Acknowledgements
  8. REFERENCES

Contributions: K. M. P. delivered interventions, analysed and interpreted data, and wrote the manuscript; H. S. L. J. delivered interventions, interpreted data, critically reviewed and gave final approval of the manuscript; B. J. S. provided statistical consultation, interpreted data, critically reviewed and gave final approval of the manuscript; T. T. and W. S. R. referred patients to investigators, critically reviewed and gave final approval of the manuscript; and P. B. J. designed the study, interpreted data and wrote the manuscript. The authors would like to thank Leigh Ann Faul, PhD, Lora Thompson, PhD, Cathy Meade, PhD, RN, and Rick W. Wilson, PhD, PT. This research was supported by American Cancer Society Grant No. RSGPB-05-243-01 CPPB.

REFERENCES

  1. Top of page
  2. Abstract
  3. Introduction
  4. Method
  5. Results
  6. Discussion
  7. Acknowledgements
  8. REFERENCES