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Insights Into the Reluctance of Patients With Late-Stage Cancer to Adopt Exercise as a Means to Reduce Their Symptoms and Improve Their Function

      Abstract

      Context

      Exercise reduces cancer-related disablement and adverse symptoms, yet patients' attitudes toward exercise remain largely unexamined.

      Objectives

      This qualitative study sought to characterize the beliefs of patients with late-stage disease regarding exercise, its relationship to their symptoms, and their clinicians' roles in providing related counseling.

      Methods

      Semistructured interviews with 20 adults (half male and half aged 65 years or older) with Stage IIIB or IV nonsmall cell lung cancer were qualitatively analyzed. Participants were questioned about their levels of activity, the influence of their symptoms on their activities, perceived barriers and facilitators for exercise, and exercise-related instructions received from their professional caregivers.

      Results

      Participants overwhelmingly cited usual daily activities as their source of “exercise.” Symptoms, particularly treatment-related, discouraged participation, with fear of harm being a significant concern only among younger women. Exercise was recognized as important for physical and mental well-being but seldom as a means to mitigate symptoms. Weather, recalled levels of premorbid fitness, and exercise participation modulated current exercise behaviors. Although respondents preferred to receive guidance from their oncologist, none reported receiving more than general encouragement to “stay active.” A lack of direction was typically accepted as a sanction of their current activity levels. Participants appeared less receptive to guidance from ancillary health professionals.

      Conclusion

      Effective use of exercise and activity modification to ameliorate cancer-related symptoms appears to require a linkage to a patient's usual and past activities, proactive negotiation of potential barriers, education regarding symptoms and exercise, and the positive support of their oncologist.

      Key Words

      Introduction

      Exercise, even at surprisingly low intensities, is well established as an effective means of controlling the symptoms and improving the function of the frail and elderly, as well as those suffering from a variety of chronic and debilitating diseases.
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      Physical activity for the chronically ill and disabled.
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      American College of Sports Medicine position stand. Exercise and physical activity for older adults.
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      What is far less well known is that these benefits extend even to people in the advanced stages of terminal illness.
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      Rehabilitation for the terminal cancer patient.
      • Oldervoll L.M.
      • Loge J.H.
      • Paltiel H.
      • et al.
      The effect of a physical exercise program in palliative care: a phase II study.
      Unfortunately, although we know that activity levels in this group may be low, we have limited information about how these patients can be encouraged to adopt an exercise program or even perceive one's value.
      An obviously important consideration is that, despite the fact that people in the terminal stages of a disease can benefit from increasing their activity levels, they may feel that adopting a program would be either ludicrous, futile, or worsen their symptoms.
      • Oldervoll L.M.
      • Loge J.H.
      • Paltiel H.
      • et al.
      Are palliative cancer patients willing and able to participate in a physical exercise program?.
      In essence, however, any judgments that we can make about how patients with terminal illness will weigh the costs and benefits of exercise, and what factors may influence their assessments, remain speculative. This lack of knowledge limits the ability of clinicians to effectively address a potentially beneficial approach for their patients or, of equal importance, to overcome their own ambivalence about the role of exercise in the palliative setting.
      Patients in the later stages of lung cancer (LC) may serve as an ideal population in which to examine these issues. First, LC is highly prevalent and associated with a high level of morbidity.
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      Cancer statistics, 2010.
      Second, the limited survival of patients in this group highlights the palliative nature of their care and the need to identify treatments with the greatest likelihood of ameliorating symptoms and functional decline.
      • Molina J.R.
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      • Cassivi S.D.
      • Schild S.E.
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      Non-small cell lung cancer: epidemiology, risk factors, treatment, and survivorship.
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      Epidemiology of lung cancer prognosis: quantity and quality of life.
      Third, although patients with advanced LC have the highest symptom burden of any cancer population,
      • Doorenbos A.Z.
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      • Verbitsky N.
      Symptom experience in the last year of life among individuals with cancer.
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      • Gift A.G.
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      A cluster of symptoms over time in patients with lung cancer.
      roughly half will live for more than one year. Fourth, there are strong reasons to believe that their most prevalent and problematic symptoms, dyspnea and fatigue, may be particularly susceptible to mitigation by therapeutic exercise.
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      • Yang P.
      • Cassivi S.D.
      • Schild S.E.
      • Adjei A.A.
      Non-small cell lung cancer: epidemiology, risk factors, treatment, and survivorship.
      • Temel J.S.
      • Greer J.A.
      • Goldberg S.
      • et al.
      A structured exercise program for patients with advanced non-small cell lung cancer.
      Lastly, research suggests that preservation of aerobic fitness may actually lead to a prolongation and enhancement of their quality of life.
      • Jones L.W.
      • Watson D.
      • Herndon 2nd, J.E.
      • et al.
      Peak oxygen consumption and long-term all-cause mortality in nonsmall cell lung cancer.
      Evidence supporting exercise as a means of symptom control has been primarily studied in disease-free cancer survivors and patients with cardiac or respiratory failure.
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      Exercise for the management of cancer-related fatigue in adults.
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      • et al.
      Interval versus continuous training in individuals with chronic obstructive pulmonary disease–a systematic review.
      There are obvious differences between these groups. Nevertheless, a number of small trials suggest that patients with Stage IV cancer, including LC, may enjoy benefits similar to those obtained in debilitated noncancer populations.
      • Oldervoll L.M.
      • Loge J.H.
      • Paltiel H.
      • et al.
      The effect of a physical exercise program in palliative care: a phase II study.
      • Temel J.S.
      • Greer J.A.
      • Goldberg S.
      • et al.
      A structured exercise program for patients with advanced non-small cell lung cancer.
      • Culos-Reed S.N.
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      • Lau H.
      • et al.
      Physical activity for men receiving androgen deprivation therapy for prostate cancer: benefits from a 16-week intervention.
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      • Clark M.M.
      • et al.
      Therapeutic exercise during outpatient radiation therapy for advanced cancer: feasibility and impact on physical well-being.
      These findings, combined with our ever increasing recognition of the detrimental effects of immobility, make exercise an important consideration in provision of palliative as well as preventive and restorative care.
      • Halar E.
      • Bell K.R.
      Immobility and inactivity: physiological and functional changes, prevention, and treatment.
      Given the above, we conducted semistructured interviews with 20 patients with late-stage LC and performed a qualitative analysis to explore their beliefs regarding exercise, its relationship to their symptoms, and their clinicians' roles in providing related counseling.

      Methods

      Subjects

      This study was reviewed and approved by the Mayo Clinic's Institutional Review Board. Using a two-step process, 20 subjects were recruited from among 202 surviving members of a cohort of 311 patients with late-stage LC (Stage IIIB and IV non-small cell lung carcinoma) whose activity levels and physical function were being monitored with monthly telephone calls.
      • Cheville A.L.
      • Yost K.
      • Larson D.
      • et al.
      Performance of an item response theory-based computer adaptive test in identifying functional decline.
      First, during prescheduled monthly telephone calls, surviving members of the cohort were queried about their willingness to be interviewed. Second, cohort members who were willing to be interviewed were consecutively contacted during a follow-up telephone call—unrelated to the prospective cohort study—to schedule an interview time and place. Queries continued until the recruitment goal of 20 participants (10 men and 10 women) with half of each group being 65 years or older was met.

      Data Collection

      Clinical Data

      Data regarding participants' cancer treatment regimens, LC stage, metastasis locations, body mass indices, and medical comorbidities were obtained from the participants' electronic medical records.

      Interviews

      Interviews with those who agreed to be interviewed were scheduled on the basis of the date they indicated willingness to participate. Participants living less than 50 km (30 miles) from the Mayo Clinic were offered the opportunity of being interviewed either at the time of a scheduled oncology visit or in their homes. In all, 18 chose to be interviewed during a clinic visit and two in their homes. Interviews were conducted and audiorecorded after participant consent by an experienced qualitative nurse researcher (A. M. D. or L. M. R.). Interviews were scheduled to be 45 minutes in length and each began with the participant being asked what the term “exercise” meant to them. After their response, the investigator shared a definition of exercise as “a systematic way of stressing the body to increase flexibility, stamina, and strength” and proceeded to the rest of the interview. Interview lengths ranged from 20 to 50 minutes. Data were collected over a six-month time frame from June to November 2009.

      Analyses

      Quantitative Analysis

      The demographics of the study cohort, as well as its age- and gender-defined subgroups, were characterized with descriptive statistics. Comparisons between members of the target cohort who agreed or declined to be interviewed, as well as receptive patients who were and were not enrolled in the study, were performed with Chi-squared tests for categorical variables and Student's t-tests for continuous variables to examine potential biases in participant selection. All analyses were performed using STATA v9.0 (StataCorp LP, College Station, TX). Findings with an α0.05 were considered statistically significant.

      Qualitative Analysis

      Typed transcripts were verified for accuracy and then read in their entirety to gain an overall impression of the content. Content analysis methodologies
      • Graneheim U.H.
      • Lundman B.
      Qualitative content analysis in nursing research: concepts, procedures and measures to achieve trustworthiness.
      were used to analyze the text of each interview. The development of the coding scheme was incremental and iterative beginning with the first transcript. Categories, groups of content sharing common features, were created and abstraction of the text was accomplished by assigning category codes.
      • Graneheim U.H.
      • Lundman B.
      Qualitative content analysis in nursing research: concepts, procedures and measures to achieve trustworthiness.
      Subcategories were identified to further delineate the content. Finally, themes or ideas that cut across categories
      • Graneheim U.H.
      • Lundman B.
      Qualitative content analysis in nursing research: concepts, procedures and measures to achieve trustworthiness.
      were created. As new concepts emerged, they were defined and added to the coding scheme. Data saturation (no new concepts or categories) was reached after 16 interviews. Examples of the data abstraction process are listed in Table 1.
      Table 1Examples of the Sequential Data Abstraction Process
      Meaning UnitCondensed Meaning UnitCategory CodeSubcategory Code
      I was working and also I like to go out and do grocery shopping, to run errands. Oh, very independent. You know, run errands, going to the bank, you know, all those things—grocery shoppingRun errands, going to the bank, you know, all those things—grocery shoppingPast preferences and patternsUsual activity as exercise
      Well, I have a treadmill and I walk on it in the wintertime if I can't get to a gymnasium or … I prefer to walk in the gym as opposed to that but I do …I walk on it in the wintertime if I can't get to a gymnasiumExercise modifiersWeather
      Attention to measures of trustworthiness including credibility, dependability, and transferability was maintained throughout the analytic process. Credibility of the study data and processes was assured through: 1) the systematic use of an interview guide; 2) biweekly meetings to review field notes, category codes, and exemplars for category fit and discuss any new findings or observations; 3) coding in small units to capture unique concepts; 4) review of transcript codes by a second investigator; and 5) final verification of the coding scheme through the evaluation of the exemplar quotations associated with each category or subcategory. Dependability was a limited concern because of the single interview per subject design and the completion of data collection in a six-month interval. However, potential clinical practice changes that might influence study findings were monitored. According to Graneheim and Lundman,
      • Graneheim U.H.
      • Lundman B.
      Qualitative content analysis in nursing research: concepts, procedures and measures to achieve trustworthiness.
      decisions about transferability or generalizability of the study findings are ultimately up to the reader. Participants' demographic data and a description of the study setting are offered to aid readers in evaluating transferability.

      Results

      Subjects

      Among the 148 members in the recruitment cohort who were asked whether they would be willing to be interviewed, 110 were receptive. The first 20 from among this group who fulfilled our age and gender sampling requirements were contacted; all agreed to participate. Participant flow is outlined in Fig. 1.
      Figure thumbnail gr1
      Fig. 1Flow diagram illustrating the sequential enrollment process for the 20 study participants. NSCLC=non-small cell lung cancer; SCLC=small cell lung cancer.
      Demographic, clinical, and cancer characteristics of the participants are listed in Table 2. Study participants did not systematically differ from the target cohort (n=202), those who were queried on their willingness to be interviewed (n=148), those who agreed to be interviewed (n=110), or those who agreed to be interviewed but were not scheduled, aside from gender proportions and mean ages, which were skewed by purposive sampling.
      Table 2Participants' Demographic, Cancer, and Clinical Characteristics
      Subject NumberGenderAge (years)Stage of Initial LC DiagnosisMetastasesComorbid Medical Conditions
      BrainBoneCOPDCADConnective Tissue Disorder
      1F59IVX
      2F72IVXX
      3F84IVX
      4M72IVX
      5M79IIIBXXX
      6F61IV
      7F68IVXX
      8F53IVX
      9M56IVXX
      10M65IVX
      11F67IIIBX
      12F74IVXX
      13M57IVX
      14F55IVX
      15M58IV
      16M74IVX
      17M70IVX
      18M66IVXX
      19F56IVXX
      20M62IV
      LC=lung cancer; COPD=chronic obstructive pulmonary disease; CAD=coronary artery disease; F=female; M=male.
      Two participants had Stage IIIB and 18 had Stage IV non-small cell lung carcinoma, with all the Stage IV respondents having undergone at least one procedure to palliate symptomatic metastases. Twelve were receiving anticancer treatment: 11 systemic chemotherapy and one radiation therapy. None had histories of significant neurologic or psychiatric disorders. A minority had chronic obstructive pulmonary disease (n=3), coronary artery disease (n=4), or a connective tissue/musculoskeletal disorder (n=4).

      Qualitative Results

      A single overarching theme was supported by two categories and three subcategories. Most participants equated, and used, the term “physical activity” as a synonym for exercise.

      Primary Theme

      The overarching theme describing participants' views and preferences about exercise was that exercise is being active by engaging in usual activity. Both men and women described usual activities as a source of exercise. For many, housework, cooking, yard work, and other activities such as home maintenance and getting out of their home for social reasons were viewed as opportunities to engage in physical activity. Additionally, among the few participants with formal exercise programs, carrying out normal or usual activities was a priority.I do my own cooking, housekeeping or whatever … We have a small vegetable garden in the back and to me, that is an exercise in itself, just the up and the down and activity of the gardening. (Patient 10; female [F] older than 65 years)I try and do just what I normally was doing before. (Patient 08; F younger than 65 years)Well, if you include things like working in the trees, cutting trees down and cutting wood up and splitting wood and the garden and all of those things—pretty much daily, everyday … I'm lifting 50 lbs. and a log or something. (Patient 11; male [M] younger than 65 years)
      One man was still flying his airplane and riding a motorcycle. Like others, he articulated the physical benefits of activity and preference for usual activities over formal exercise programs.… flying moves your legs, your feet, your arms, your hands … like the hangar—I have one of these big old mops; I can mop the floor with water and get a push broom. … You have to push the airplane to the gas pump—it is exercise, but it is not like formal yuppie gym crap. (Patient 09; M younger than 65 years)
      Younger men in particular described a sense of satisfaction from performing physical activity. For example, one man described digging up his backyard patio over a period of days.… I knew I could do it, but it wasn't like I was looking forward to it because I knew it was going to hurt. But I wanted to see if I could do it. And I did it. And it made me feel good at the end that I could. (Patient 13; M younger than 65 years)
      Whereas most participants were retired or had not previously worked outside the home, those who were still employed included their employment as exercise. One man was a manager at a food production company, and two were farmers.I walk on my job but a lot of it is not physical. … I'm up and down stairs quite a bit. … go through the pilot plant so it takes me from one end to the other. (Patient 20; M younger than 65 years)Well, I live on a farm so we have got everyday chores and everyday things that need to go on there—if it is feeding cattle or getting on the tractor and planting corn or harvesting or making hay … (Patient 18; M older than 65 years)

      Activity Modifiers

      A number of factors appeared to affect the frequency and intensity of participants' activity levels. These influencers were subcategorized as symptoms, past preferences and patterns, and weather.

      Symptoms

      Participants consistently expressed the idea that their symptoms strongly influenced their activity. Not surprisingly, symptoms were most often described as interfering with the activity and dampening their desire to exercise. Fatigue was the most commonly cited problem, but nausea, malaise, and cold intolerance also were noted as activity limiting. Symptoms were frequently noted as being the most problematic in a period of about a week after a course of chemotherapy.You know the first week of chemo … I feel pretty yuck. After that, if I have to get anything done, it is usually in the morning because by afternoon I am usually pretty tired. (Patient 08; F younger than 65 years)I have had 15 rounds of chemo and the fatigue gets more and more every time, so you don't have as much energy. (Patient 09; M younger than 65 years)When I was taking chemo I felt like laying down and sleeping most of the time. (Patient 17; M older than 65 years)
      Many participants believed that LC was not the primary cause of the symptoms that limited their activities. Men were more likely to attribute activity-limiting symptoms to their comorbidities. Although some symptoms were related to LC metastasis or complications, patients did not directly connect these with their LC.I have had my knees replaced. I have got arthritis, also … It is hard to blame this [on] lung cancer or chemo or being 66 years old … I mean it is some of all three, I'm sure. (Patient 18; M older than 65 years)So the lung cancer part, that was not a bad deal at all. Other than it is a tough deal for the body. But, the continual brain ones, that's hard (Patient 11; M younger than 65 years)
      One potential difference across subgroups appeared to lie in a fear of exercise being harmful rather than beneficial. Only women younger than 65 years expressed concerns about whether symptoms experienced during exercise reflected bodily harm. Two described situations in which exercise-associated symptoms triggered intense fear and that education about what to expect during exercise may have eased this.I remember … (I) couldn't breathe … I was scared and I finally thought, wait a second, let's think through this … I guess information, so you know what to expect of like symptoms or whatever, radiation and that kind of thing. Like, where you are going to feel sore afterward, but things are going to be happening, but that it is still all right to go ahead and do these and that it will help. (Patient 14; F younger than 65 years)
      One woman recalled that shortness of breath while walking resulted in concerns about continuing walking as exercise. This woman consulted her physician.I guess my biggest thing, my biggest fear of lung cancer and exercise, like I say, is the shortness of breath. Am I sure it is from my lungs and not my heart? And, I think that's only because my mom—and she had it (heart disease) forever … when I would see her get short of breath and I think, oh, my God, I'm getting short of breath. But now, Dr. [name] has taken care of that as far as my walking—I'm fine with that, but I guess new exercises I am a little hesitant just because … (Patient 08; F younger than 65 years)
      The capacity of physical activity to help participants feel better and positively influence their symptoms emerged as a variation on the theme of symptoms as activity influencers. Participants noted both physical and mental symptom improvement with exercise.I notice if I don't exercise, I don't feel as well. The shortness of breath increases if I skip or if I have a particularly bad day and don't get up and around. So I know the value of the exercise … I feel that it is very valuable for me. (Patient 10; F older than 65 years)I pretty much always have to keep physically active or I start having more, I think, more mental problems. I think keeping the oxygen going, keeping the body exercising helps me with my headaches and things that are from the cancer operations. (Patient 11; M younger than 65 years)… I will get sort of sore, but when I go out and move I feel better. That is just like before, that is how it is. (Patient 14; F younger than 65 years)

      Past Preferences and Patterns

      Past preferences and patterns were described by participants as their guide not only for choosing what they did but also for evaluating their current abilities. Many, in fact, described being able to engage in their usual activities or exercise patterns as their personal barometer for acceptable activity levels.That is kind of a benchmark thing. “I used to be able to do that, I should be able to do that; can I do it?” But I found my ceiling. I can't do what I used to do … I can stay up all day, drive tractor as long as I don't have to lift heavy objects. (Patient 13; M younger than 65 years)I don't think I quite have the, uh, stamina that I did have. I feel like I'm probably a little weaker. I know that my golf game has suffered somewhat … I mean, I will wear down quicker than I used to. But … as far as physical strength for a short period of time, I think I'm still pretty close to as strong as I was. (Patient 17; M older than 65 years)
      Decisions to incorporate exercise into their lifestyles and to participate in formal exercise programs also were related to past preferences and patterns. Interestingly, many expressed the view that there are “exercise people” and “non-exercise people.” Those who had not previously engaged in exercise tended to prefer describing themselves and their exercise as staying active.Well, to say that I want to stay active kind of gives the impression that I'm going out of my way to do this, and that may not be the case. I mean, sure, it is something that I want to do, but I wanted to do that before I had cancer, also. I mean, I just haven't changed my lifestyle is what it amounts to. (Patient 17; M older than 65 years)And, I wasn't that organized exercise oriented. He [my doctor] was aware right away that I didn't want to join a Pilates class or anything. (Patient 10; F older than 65 years)

      Weather

      Many, consistent with the overall theme of usual activity as exercise, described walking as their preferred form of activity. Given this preference, and the direction from providers to walk as a primary form of activity, participants described winter weather as a barrier to activity. Concerns included fear of falling, the effects of cold on breathing, and a general dislike of cold.I was real afraid of the effect that winter was going to have on the lungs … the cold air did affect the breathing a lot when I went out. … So, yes, I was quite afraid, especially of exercise. Because you just didn't know. (Patient 10; F older than 65 years)I have to say that during winter I'm home almost all the time … because of the cold weather and even if I go out I have to be in the car. Also, if it is snowy, then being out, you know, increases the risk of falling … (Patient 01; F younger than 65 years)In the summertime I'm quite active outside. In the wintertime I get on the treadmill … But it is not a training session like it used to be. (Patient 20; M younger than 65 years)

      Clinicians' Role in Promoting Exercise

      Participants were asked about conversations with their oncologists concerning exercise. All stated that they would be comfortable discussing activity/exercise with their oncologists but few had done so. Conversations, if held, tended to generically focus on keeping active. In other cases, an assumption that the oncologist was knowledgeable about their activity/exercise habits appeared to be interpreted as tacit endorsement of their program.… he [oncologist] more or less said, you know, stay active. (Patient 17; M older than 65 years)Well, she [oncologist] knows what I do and doesn't have a problem with it. You know, they say to keep active in doing what you are doing, and so that's what I do. (Patient 18; M older than 65 years)He [oncologist] didn't really talk to me [about exercise]. He said it's best and I took it upon myself. (Patient 20; M younger than 65 years)Yes, it is just that he [oncologist] knows that I have been walking. I said, “Should I keep it up?” and he said absolutely! (Patient 12; F older than 65 years)
      Physician encouragement or prescription of exercise was described as a strong actuator to enhance physical activity.Well, if I'm told to do a certain exercise I'll go ahead and do it. I will do anything they want me to do. If the promise or the possibility of walking normally is the end result, even if it isn't, I'll still continue to do these. (Patient 04; M older than 65 years)
      When asked from whom they would seek advice about an exercise program, most participants indicated that they would seek advice from either a physician or a physical therapist. Most preferred guidance from their oncologist.I'd have to ask him [oncologist] first. Like if they had deep breathing exercises, something to help with the lungs. (Patient 19; F younger than 65 years)Well, first off, I would talk to my oncologist and just ask him what he would think if I wanted to do this. (Patient 13; M younger than 65 years)Yes, I think a physical therapist that is more medically inclined than just an ordinary trainer. (Patient 01; F younger than 65 years)
      Responses varied when participants were asked about how assistance from a physical therapist or nurse would be received. Many believed that they were not at a level of functional disability where such assistance was needed. Others expressed uncertainty about its benefits.I don't know. If it's good advice, fine. But I feel that I can do it [exercise] when I can do it … (Patient 03; F older than 65 years)I don't know. I think I know most of it now. I just want to get going again. (Patient 05; M older than 65 years)Oh, I don't know, it probably wouldn't be very necessary for me. Yeah, I would do it on my own, I would think. Like right now I'm doing a lot of sitting around, but I plan to be busier again. I just haven't felt good. (Patient 07; F older than 65 years)I don't think I need any help, but if my health turns worse it wouldn't hurt then to possibly have help if I needed it. (Patient 11; M younger than 65 years)
      For others, direction from a physical therapist was viewed as potentially beneficial, generally for support rather than to build strength and stamina. Again, for the younger women, the opportunity for guidance about exercise was viewed as a benefit.That would be fine. Yeah, if they can tell me what I can do and should be doing, that is great! (Patient 14; F younger than 65 years)I am guessing it [call from nurse or therapist] would be okay. Possibly good. I can't imagine why it would be bad. I don't really think it is necessary right now; I'm too busy. But if things changed in my health and things, sure, that might be a good idea. (Patient 11; M younger than 65 years)That would be good, I would have somebody to say, “Okaaay, come on.” (Patient 19; F younger than 65 years)

      Discussion

      This study represents, to the best of our knowledge, the first systematic examination of beliefs held by patients with advanced cancer about the interrelationships among their cancers, their symptoms, and exercise. This information is important because symptoms (or a fear of triggering symptoms) may result in an unnecessarily accelerated pattern of decreased activity, deconditioning, morbidity, and avoidable disability.
      • Dahele M.
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      Objective physical activity and self-reported quality of life in patients receiving palliative chemotherapy.
      • Kurtz M.E.
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      Symptomatology and loss of physical functioning among geriatric patients with lung cancer.
      • Dodd M.J.
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      These findings also are important in light of data that establish exercise and physical activity as among the most effective strategies for reducing fatigue and dyspnea, which are, in addition to being particularly problematic among patients with late-stage cancer, limitedly responsive to pharmacologic approaches.
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      Our findings reveal a number of themes and subcategories with potentially important implications for research and clinical care. Notably, far from confirming stereotypes of patients with advanced LC as being frail and debilitated, many study participants were robustly, and perhaps defiantly, active. In this regard, some respondents were unquestionably outliers with respect to their high levels of drive and functionality. Others, however, as noted in Table 1, were severely debilitated and died within months of their interviews. Reassuringly, saturation was reached during content analysis. It is, therefore, unlikely that important themes were overlooked as a result of sampling limitations and bias.
      The participants' often expressed view that usual activity served as their exercise suggests that highly structured, non-daily activity-oriented exercise programs will be unappealing and poorly accepted by this population without careful planning and implementation. This finding is supported by the difficulties of recruiting patients with advanced stage LC reported by two otherwise successful studies involving exercise-focused training programs.
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      Furthermore, adherence following discontinuation of supervised formal sessions will likely be low, in light of the fact that adherence rates of roughly 40% or lower at six to 12 months have been noted among cancer survivors with no evidence of disease.
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      Predictors of follow-up exercise behavior 6 months after a randomized trial of exercise training during breast cancer chemotherapy.

      Schmitz K. Adherence to resistance training following discontinuation of supervised sessions. 2010.

      The fact that respondents often noted that there are “exercise” and “non-exercise” people and that they frequently self-identified themselves as being “non-exercisers” suggests that even presenting loose activity recommendations as “exercise” may not be particularly helpful. In addition, weather may be a particularly refractory barrier. “Non-exercisers” are unlikely to have home exercise equipment and although our study took place in the Midwest where winter cold limits outside activities, similar ambivalence over weather-related discomfort is found in regions with high summer temperatures and humidities.
      • Tu W.
      • Stump T.E.
      • Damush T.M.
      • Clark D.O.
      The effects of health and environment on exercise-class participation in older, urban women.
      • Eves F.F.
      • Masters R.S.
      • McManus A.
      • et al.
      Contextual barriers to lifestyle physical activity interventions in Hong Kong.
      It became clear during analysis that participants conceptualize “exercise” with little appreciation of how specific activities can produce desirable benefits such as increased strength, endurance, and a lessened symptom burden. This lack of insight points to a need to engage with patients through education regarding symptoms and exercise and supports the importance of establishing an explicit connection between the performance of therapeutically based exercises and an improved ability to perform one's usual activities. Such efforts may include taking into consideration the patient's chemotherapy schedule, with a planned lessening of intensity in the week after treatment. The fact that patients appear to overestimate the level of physical exertion associated with their usual activities, for example, gardening and shopping, may point to an opportunity to increase beneficial levels of exertion by providing objective feedback through the use of accelerometers or pedometers.
      It is interesting that symptom aggravation, in distinction to the concern that aggravated symptoms might reflect physical harm, was not cited as a reason for avoiding exercise. This lack may result from the fact that patients self-regulated their activities to levels below those that triggered adverse symptomatology. Such patterns of activity avoidance, if persistent, will inevitably lead to deconditioning and its well-characterized adverse effects.
      • Allen C.
      • Glasziou P.
      • Del Mar C.
      Bed rest: a potentially harmful treatment needing more careful evaluation.
      • Bergel R.R.
      Disabling effects of inactivity and importance of physical conditioning. A historical perspective.
      The processes by which patients attribute activity-induced symptoms to cancer and noncancer sources and how these may impact their receptivity to exercise remain poorly understood. Our findings that these attributions may be inaccurate suggest that research into whether improved insight into the sources of activity-associated symptoms would be beneficial or potentially harmful is needed. A reluctance to attribute symptoms to cancer may reflect an adaptive coping mechanism.
      Benchmarking of current activity levels against recall of previous capabilities emerged as a common means by which patients gauged how they were doing. By and large, benchmarks were selected or interpreted in a nonthreatening manner that supported the acceptability of their current status. This process likely reflects a constructive coping mechanism. However, recall biases also may have served to falsely reassure the respondents that their functional status was stable, when it, in fact, was not. Longitudinal studies of physical function in advanced cancer suggest that meaningful decline begins more than one year before death and steadily worsens.
      • Lunney J.R.
      • Lynn J.
      • Foley D.J.
      • Lipson S.
      • Guralnik J.M.
      Patterns of functional decline at the end of life.
      Objective benchmarking via activity monitors or other performance measures may be a means to encourage patients to become engaged in preserving their functionality.
      A potentially important finding is that although participants reported wanting medically informed exercise, they seldom received specific recommendations. Input was particularly desired from their oncologists, with several participants asserting the equivalent of “if they tell me to, I will.” Receptivity to inquiries and advice about exercise behaviors from nonphysician health care workers appeared to be far lower. Disappointingly, even when exercise was discussed, oncologists' recommendations remained relatively generic and on the nonspecific “stay active” level. A failure to provide prescriptive recommendations appeared to be interpreted as tacit approval that the patients' current activities were sufficient and likely served as a disincentive toward doing anything more. This appears less than optimal as clear and concise exercise prescriptions formally delivered by clinicians have increased exercise behaviors in diverse clinical populations.
      • Elley C.R.
      • Kerse N.
      • Arroll B.
      • Robinson E.
      Effectiveness of counselling patients on physical activity in general practice: cluster randomised controlled trial.
      • Swinburn B.A.
      • Walter L.G.
      • Arroll B.
      • Tilyard M.W.
      • Russell D.G.
      The green prescription study: a randomized controlled trial of written exercise advice provided by general practitioners.

      Limitations

      The study's setting was not representative of the community practices where 85% of patients with cancer receive care.

      National Cancer Institute. NCI Community Cancer Centers Program Pilot: 2007-2010. Available from http://ncccp.cancer.gov/Media/FactSheet.htm. Accessed June 2, 2011.

      The study was conducted at a National Cancer Institute-designated comprehensive cancer center housed within a large quaternary medical center in the northern Midwest. Consequently, participants' characteristics and attitudes may not be representative of the broader target population of all patients with late Stage IV LC. Additionally, social acceptability bias may have influenced participants' responses leading to overreporting of physical activity and capacity.

      Conclusions

      People in the late stages of cancer appear to conceptualize the relationships among their exercise behaviors, cancer, symptoms, and overall well-being in ways that are largely uninformed by professional caregivers. Our findings suggest that the successful use of exercise to lessen symptoms and improve function will require 1) consideration of a patient's usual level of activities, 2) proactive addressing of potential barriers (e.g., weather), 3) education, and 4) engagement of oncologists to deliver encouragement and prescriptions. Home programs that incorporate the daily activities and those that patients enjoy may offer the greatest degree of acceptance.

      Disclosures and Acknowledgments

      This study was funded by a grant from the Fraternal Order of the Eagles.
      The authors declare no conflicts of interest.

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