Knowledge, barriers and facilitators of exercise in dialysis patients: a qualitative study of patients, staff and nephrologists

Background Despite growing evidence on benefits of increased physical activity in hemodialysis (HD) patients and safety of intra-dialytic exercise, it is not part of standard clinical care, resulting in a missed opportunity to improve clinical outcomes in these patients. To develop a successful exercise program for HD patients, it is critical to understand patients’, staff and nephrologists’ knowledge, barriers, motivators and preferences for patient exercise. Methods In-depth interviews were conducted with a purposive sample of HD patients, staff and nephrologists from 4 dialysis units. The data collection, analysis and interpretation followed Criteria for Reporting Qualitative Research guidelines. Using grounded theory, emergent themes were identified, discussed and organized into major themes and subthemes. Results We interviewed 16 in-center HD patients (mean age 60 years, 50% females, 63% blacks), 14 dialysis staff members (6 nurses, 3 technicians, 2 dietitians, 1 social worker, 2 unit administrators) and 6 nephrologists (50% females, 50% in private practice). Although majority of the participants viewed exercise as beneficial for overall health, most patients failed to recognize potential mental health benefits. Most commonly reported barriers to exercise were dialysis-related fatigue, comorbid health conditions and lack of motivation. Specifically for intra-dialytic exercise, participants expressed concern over safety and type of exercise, impact on staff workload and resistance to changing dialysis routine. One of the most important motivators identified was support from friends, family and health care providers. Specific recommendations for an intra-dialytic exercise program included building a culture of exercise in the dialysis unit, and providing an individualized engaging program that incorporates education and incentives for exercising. Conclusion Patients, staff and nephrologists perceive a number of barriers to exercise, some of which may be modifiable. Participants desired an individualized intra-dialytic exercise program which incorporates education and motivation, and they provided a number of recommendations that should be considered when implementing such a program.


Background
Of the 600,000 prevalent end-stage renal disease (ESRD) patients in the US, the vast majority suffer from fatigue, poor sleep, poor physical functioning and frailty [1][2][3][4]. These highly debilitating symptoms lead to falls, loss of independence, frequent hospitalizations, premature mortality as well as poor health-related quality of life (HRQOL) [5][6][7][8][9]. Exercise improves aerobic capacity, blood pressure and HRQOL in ESRD patients [10]. Compelling observational data also suggest that regular exercise may improve fatigue, sleep and mortality in hemodialysis (HD) patients [11,12]. However, <50% of HD patients in the US exercise at least once a week [12]. In fact, the vast majority of these patients often report very low levels of physical activity in general, which is associated with increased symptom burden, poor physical functioning and higher mortality [13,14].
International data suggest that patients from dialysis facilities that offer exercise programs are 38% more likely to exercise regularly [12]. Unfortunately, in the US, exercise is not part of "standard clinical care" and few facilities offer any kind of exercise program to the patients [12]. This is despite Kidney Disease Outcomes Quality Initiative (KDOQI) guidelines for increasing physical activity in ESRD patients almost a decade ago [15], and over 30 years of research demonstrating safety and benefits of intra-dialytic exercise [16]. Intra-dialytic is ideal as it can be implemented in a setting with rigorous clinical monitoring, does not involve additional time or travel, and may alleviate patient fear of injury [16,17]. The present challenge involves identification of strategies for translation of research findings into clinical practice [18,19]. A critical barrier has been the failure to identify an optimal exercise program that meets the needs and preferences of both patients and providers, and is sustainable within the limited resources of the clinical setting [18,19].
Since dialysis patients, staff and nephrologists are the key stakeholders in the implementation, acceptance and adherence for exercise, especially an intra-dialytic exercise program, it is critical to understand their knowledge, barriers, motivators and preferences. Prior survey-based studies have failed to provide in-depth exploration of participants' views [20][21][22][23]; and the limited qualitative work in this area has mainly focused on specific patient populations or single university-based dialysis units, thus limiting the transferability of results to the majority of dialysis patients and practices in the US [21,[24][25][26]. We are unaware of any prior qualitative studies that included nephrologists; assessed patients, staff and nephrologists congruently; or sought recommendations from these groups on how to best design an intra-dialytic exercise program.
In this qualitative study, we conducted in-depth interviews with HD patients that were heterogeneous with respect to age, gender and race; dialysis staff at different organizational hierarchy levels; and academic and private nephrologists. Given the recent increased emphasis in the physical activity field on the potential benefits of overall physical activity at any "dose", as well as emphasis on the benefits of formal exercise training [27], we described exercise as any kind of physical activity such as walking, climbing steps, etc. The primary aim was to elicit participants' knowledge, barriers and motivators for physical activity in general and specifically for intra-dialytic exercise. The overarching goal was to inform the development of a patient and provider preferred exercise program for HD patients.

Participant recruitment
We recruited ESRD patients ≥18 years on in-center HD 3 times/week for at least 3 months. We used purposive sampling to ensure a sample that reflected a range of important characteristics and ensured adequate number of patients in each of the 4 preidentified strataa) sex (men/women); b) ageyounger (18-49 years)/older(50-80 years); c) race (White/Black) and d) education level (high school or less/more than high school). Patients were recruited until "saturation", i.e., no new themes emerged in the interviews. Exclusion criteria included contraindication to exercise (e.g. unstable angina), refractory/untreated psychiatric disease, history of poor adherence to HD treatments, currently in an acute or chronic care facility, life expectancy less than 6 months. After screening the patients through medical chart review, the research team discussed with the dialysis nurse manager and/or social worker at each unit to confirm patient eligibility. Out of the 17 patients initially consented, 1 dropped out due to lack of time availability.
Similar strategies of purposive sampling and thematic saturation were used to recruit dialysis staff at different levels of organization and nephrologists from both academic and private practice setting. Since older nephrologists may be more likely to counsel patients about physical activity [28], we recruited an age-stratified sample [younger (<50 years)/older (≥50 years)]. All participants were recruited from 4 different out-patient Dialysis Clinic, Inc. (DCI) affiliated dialysis units in Western Pennsylvania and identified based on discussion with nurse manager at each dialysis unit. This study followed the Criteria for Reporting Qualitative Research guidelines for conducting and reporting qualitative research [29]. The study was approved by the University of Pittsburgh Institutional Review Board and all subjects provided informed consent.

Interviews
Members of the research team (MJ, MLM and MAD) developed an interview guide (see Appendix) for semistructured interviews and this was pretested with a dialysis patient (GI), dialysis unit nurse manager (AHa) and dialysis social worker (GF). The participants were asked to think about exercise as any kind of physical activity such as walking, climbing stairs, etc. MJ, a nephrologist with prior training in qualitative research conceptualized the study. The current literature in this area was extensively reviewed and lack of physical activity/exercise adoption was identified as a critical gap between the research recommendations and usual clinical practice. In order to develop and implement interventions aimed at increasing physical activity in HD patients, this study was conceptualized and designed to gain insights about patient, provider and system level factors involved. GI, a HD patient for 4 years was a key participant in the study design, data interpretation and analysis. All interviews were conducted by MLM (research coordinator) who was trained by MAD, an expert in qualitative analysis. Participants were probed to ensure rich details emerged. The interviews were conducted over the telephone, audiotaped and lasted approximately 20-40 min. They were transcribed verbatim and randomly audited to ensure accuracy.

Data analysis
Applying grounded theory framework [29], all transcribed interviews were independently coded by MJ and MLM. Initially, open coding was used, in which any and all themes generated were considered in an inductive manner without restricting the focus. The themes and codes that repeatedly emerged were examined to develop focused themes and sub-themes. Inter-coder consensus was established by cross checking, discussing and refining themes until consensus was achieved. In case of disagreement, the differences in coding were resolved through discussion among MJ, MLM and MAD and reviewed by GI. Under each theme, comments from patients, staff and physicians were organized together to evaluate similarities and differences among these groups. For each theme and subtheme, most descriptive representative statements were chosen after discussion among MJ, MLM and MAD and were reviewed by GI.

Results
We interviewed 16 in-center hemodialysis patients, 14 dialysis staff members and 6 nephrologists ( Table 1). The mean (SD) age of patients was 60.1 (17) years, 50% were females, 62.5% were blacks and 25% had high school degree or less. This is representative of the HD population in Pittsburgh area (mean age 64 years, 38% females, 41% blacks; data obtained from DCI, 2015). Dialysis staff included 6 nurses, 3 technicians, 2 dietitians, 1 social worker and 2 unit administrators. Nephrologists also represented a diverse group including one third over 50 years of age, 50% female gender and 50% academic nephrologists.
Major themes and subthemes Theme 1: Knowledge and perceived benefits of exercise: patients and staff view exercise as beneficial: "It gives me more energy…" As illustrated in Table 2, majority of the participants' comments reflected a view that a major benefit of exercise was improved overall perception of health and well-being. Physical health benefits such as improving cardiovascular health, energy level, muscular strength and balance emerged as a prominent sub-theme,  Abbreviation. yo years old especially in the patient interviews. Male patients seemed to focus more on the muscular strength benefits and females on cardio-protective benefits. Interestingly, only a few of the patients commented on the mental health benefits, such as reduced depression and stress, and an increased sense of accomplishment. We found that all but one patient (72 yo White female) and surprisingly one staff member (dialysis technician, 28 yo) reported no knowledge of benefits of exercise. Most patients were unaware or underestimated the recommended frequency and/or duration of exercise: "Probably couldn't be no more than maybe twice a week" [Interview 10, F, 54yo, Black] Theme 2: Reported barriers to exercise: dialysis makes exercise challenging: "When I come home from dialysis, I'm a little bit wiped out" We identified a number of patient-and system-related or logistic factors that are perceived as barriers (Table 3). Fatigue or lack of energy, especially post-dialysis fatigue was universally cited as the biggest barrier to exercise and was described as "drained", "just don't feel like doing anything after HD". Limitations on lifting weights due to fear of injuring the fistula, inability to do water exercises due to dialysis catheter and time constraints due to dialysis were other major dialysis-related barriers. Several participants commented on the poor overall health and comorbidities such as arthritis, amputations, leg weakness and blindness as common barriers. Fear of falling, lack of counselling by staff and lack of suitable exercise options were some of the other reported barriers.
As with adopting any lifestyle modification, lack of motivation is one of the biggest challengesand patients, staff and nephrologists readily recognized this. Patients reported that dealing with physical and mental challenges of having a chronic illness and being on dialysis made exercise a low priority for them. Providers felt most patients lacked the motivation to take care of their health and were thus not likely to care about exercising.
Theme 3: Reported barriers to intra-dialytic exercise: intra-dialytic exercise should be safe without disrupting usual care: "None of us want to stay there any longer than we have to" We identified several barriers related to type, safety and feasibility of intra-dialytic exercise ( Table 4). As expected, safety concerns regarding blood pressure stability, limitations due to inability to use the access arm, fear of needle dislodgement and infiltration and cramps due to exercise were commonly reported barriers. Only a few patients stated that exercising in front of others was a significant barrier. Several participants talked about limitations related to the ease of use, cost, and storage of exercise equipment. Some of them had prior experience using a stationary pedaling bike during HD and offered reasons for poor adherence -patients felt that the bike was boring, staff felt that it added to their workload. All participants felt that extensive staff involvement in any intra-dialytic exercise program would be impractical. An interesting barrier that emerged was patients' resistance to changing the routine of dialysis. Although patients described situational reasons for this (e.g., extending time spent at the dialysis center), providers viewed resistance in terms of patients' personal characteristics, describing some, especially long-term HD patients as "strong-willed", and introducing any change to dialysis routine as being "an uphill battle".
Theme 4: Motivators and facilitators for exercise: motivation for exercise comes from within and from the encouragement of others: "I'm 100% for exercise, I know first-hand that it is beneficial" A number of patients expressed self-motivation to exercise, arising from either experiencing positive benefits or from recognition of loss of physical fitness after starting dialysis (Table 5). Patients who had accepted dialysis as a lifestyle change seemed to overcome the psychosocial challenges of being more physically active. Participants also identified health incentives and achieving health goals as important motivators to exercise. We also identified a strong trusting relationship of patients with their doctors (primary care and nephrologists) and dialysis staff, and this was a key motivating factor, along with encouragement from family, friends and other dialysis patients. Although most nephrologists offered a number of thoughts on what would motivate patients for an intra-dialytic exercise program (as mentioned below), majority of them did not comment on motivators for overall physical activity.
Theme 5: Recommendations for intra-dialytic exercise: "It would be good for us mentally to have something else to do there while we are sitting in those chairs" Participants' thoughts on why, how and what kind of intra-dialytic exercise program they believed might work are shown in Table 6. A recurring theme was the convenience in terms of saving travel and precious non-dialysis time. Moreover, by adding distraction to the mundane routine of dialysis, participants felt that it would make the time go faster and add value to the dialysis time. They reiterated that since the dialysis unit is a social environment and if a culture of exercise is introduced, it is likely to be well accepted by the patients. However, an individualized engaging program with prior testing of individual's capabilities was important to the patients. A dialysis unit administrator described his experience with a  Abbreviation. yo years old pilot group physical therapy program in his unit involving an in-center physical therapist: "it was well tolerated, it was well accepted … was extremely positive from patients. The anecdotal patients' feedback was overwhelming, not just one or two, essentially all patients seemed to very much appreciate the attention, the diversion…. the patient response one after another after another totally was "This is fun, I like it, I love the person, I look forward to it". From our measurements of patient perception, participation, and their feedback, it was a wonderful success." [Interview 30, 54 yo, Administrator] Despite its initial success, the program failed due to lack of resources to support the in-center exercise staff, thus again emphasizing the need for a less resource intensive program.
Staff and nephrologists suggested offering patients incentives such as prizes or raffles as a way to motivate them to participate in exercise. Interestingly many patients identified positive health benefits and the ability to  Theme 6: Dialysis staff attitude towards promoting exercise: "I know it can be done and that it can be tolerated" Since dialysis staff -the nurses, technicians, social workers, dietitians and administrators -are the key front line staff involved in the successful implementation of any intra-dialytic exercise program, we elicited their attitude and willingness to support such a program and the extent of their participation that they thought would be feasible. Majority of staff members believed that intra-dialytic exercise was safe and feasible: "There's clearly a significant population of patients who could participate in some kind of planned exercise during a dialysis treatment, I know that to be possible. I know it can be done and that it can be tolerated" [Interview 30, 54 yo, Administrator] Although most of the staff members were supportive of an intra-dialytic exercise program, they strongly felt that their direct responsibility should be limited to patient encouragement, motivation and monitoring. Staff felt that a program that required minimal staff assistance could be easily accommodated and would not add to their workload.

Discussion
In this qualitative study, we identified the knowledge, barriers and motivators to exercise in dialysis patients by interviewing HD patients, dialysis staff and nephrologists. Although the need for promoting exercise participation in dialysis patients is widely recognized, as is evident by the National Kidney Foundation guidelines [15], the lack of an exercise routine in a majority of dialysis patients uncovers the critical need for understanding exercise-related barriers and preferences. Our study takes a novel approach of addressing these important questions by including a heterogeneous sample of all the key stakeholderspatients, dialysis staff and nephrologists. Additionally, by eliciting their recommendations for an intra-dialytic exercise program, it lays the foundation for developing a patient and provider preferred program that is more likely to have long term acceptability and adherence.
Most dialysis patients viewed exercise as beneficial, consistent with prior studies [20]. However we identified a critical gap in patients' knowledge of mental health benefits of exercise, thus providing a target for intervention. We found that patients unanimously underestimated the exercise goals, which per the KDOQI guidelines should be at least 30 min of moderate-intensity exercise on most, and preferably all days of the week [15]. This extends the findings of Painter et al. who found that even dialysis staff were largely unaware of these guidelines [26]. Although these guidelines imply the notion that quantification of exercise and reaching a critical threshold may be important as a key metric of efficacy, the recent focus in the physical fitness field has shifted to greater emphasis on overall physical activity in lieu of the burdensome sentiment that only 150 min/week can or will determine benefit [30,31]. It is especially important to impart this knowledge to dialysis patients and providers as many of our patients may be unable or unwilling to engage in higher doses or duration of exercise. More importantly, the emphasis should be on increasing overall physical activity rather than participating in formal exercise training program. Most HD patients may be unable or unwilling to participate in formal exercise training, but may be more inclined and able to modify their day to day routine so as to incorporate more physical activity and reduce their sedentary behavior. However, such a shift in focus not only needs revision of national guidelines, but also educational efforts to increase awareness among the health care providers so that they can appropriately counsel and motivate their patients.
Confirming findings from previous studies, a major barrier identified by patients and providers was fatigue [5,20,25]. At the same time, improvement in energy level was recognized as a benefit of exercise by all participants. Lack of energy due to the disease or the dialysis treatment itself may lead to low physical activity, which in turn may perpetuate fatigue and the vicious cycle of inactivity continues. Since the majority of dialysis patients value improvement in fatigue, even more than improvement in survival [32], more research is needed to find how and what kind of exercise may lessen the experience and impact of fatigue in these patients.
Although some prior studies have examined barriers to exercise [20,[24][25][26], an additional important focus of our study was identifying factors and behaviors that would motivate patients to participate and adhere to exercise. Self-awareness of benefits of exercise was a key element, similar to what Kontos et al. reported in a predominantly white Canadian cohort [25]. Accepting dialysis as part of life, starting slow, doing something rather than nothing, desire to achieve pre-dialysis physical health, experiencing positive benefits from exercise and achieving health goals were other motivators cited by the patients. Incorporating communication skills such as motivational interviewing can be useful to elicit these patient motivators to reinforce and encourage adherence to an exercise program, as has been shown in dialysis and non-dialysis patients [10,33]. However, how to incorporate such interventions in a clinical setting with minimal additional resources or costs remains a challenge.
As with any life-changing disease, patients relied heavily on their health-care providers and social network for support, encouragement and guidance for exercise. More importantly, it was evident that there is an interactive contextual influence of the provider and clinic setting on the patients' attitudes towards exercise. Patients who perceived the staff to be supportive, were more likely to have a positive attitude towards exercise "…I have a crew down there at the dialysis clinic that don't let you do that [sit around and mope]. They encourage it [exercise]…it's just a good environment." ( Table 5). Given that prior studies have shown that assessment of physical function is not part of routine practice [26], nor are dialysis staff or nephrologists confident in counseling patients about exercise [22,28], a major change in provider training and practice patterns is called for. Additionally, increased involvement of health professionals with specialized training in exercise prescription such as physical therapists may be needed.
Because so much of dialysis patients' lives revolve around the process of getting dialysis and non-dialysis time is precious, we wanted to explore what participants thought about doing exercise during dialysis. Almost all participants felt that an intra-dialytic exercise program would be preferred to exercising at other times, as well as feasible. Important barriers related to safety, limitations of type of exercise and impact on staff workload emerged. An intriguing set of barriers pertained to patients' apparent resistance to changing dialysis routine. However, both patients and professionals felt that building a culture of exercise and obtaining commitment from long-time dialysis patients may inspire others to follow. Novel approaches for building such social support systems within and across dialysis units by integrating technology, such as competitions and rewards based on number of steps using wearable accelerometers, should be explored in future studies.
An important consideration for long-term adherence was participants' desire for a multi-modal intra-dialytic exercise training program that incorporated exercise, educational and motivational components. It was viewed as very important to have an engaging exercise program which would incorporate elements that could be individualized to the patient's health status and ability. In general, dialysis staff had a supportive attitude towards intra-dialytic exercise, but it would be crucial to minimize their active responsibility and workload in such a program. Dietitians and technicians seemed most willing to advocate for such a program.
A limitation of our study may be that although we continued to conduct interviews until we reached what we saw as thematic saturation, we may have failed to capture additional thoughts and beliefs that might have emerged from more interviews. However, we used purposive sampling to select a heterogeneous group of participants with key characteristics in each group which is likely to be reflective of a broader population and thus would facilitate the capture of a wide range of relevant views, concerns and beliefs. Moreover, we incorporated feedback from a dialysis patient, unit nurse manager and social worker in developing the interview guide, thus including a broad-range of questions and probes. However, although the patients were representative of the Pittsburgh HD population, they were older, included more blacks and did not represent diverse ethnicity as compared to the United States HD population (mean age 54 years, 43% females, 31% blacks, 17% Hispanics) [34]; which may limit generalizability of our findings. Also, all participants were recruited from a single large dialysis organization (LDO, DCI) and may not represent the practices at other LDOs. The findings from our study may not be applicable to the home dialysis patients. However, in the US, more than 10 times as many ESRD patients receive HD treatments at a clinic as those who do peritoneal dialysis and home HD combined [34]. Thus, our findings are likely to be relevant to more than 90% of the ESRD patients in the US. Lastly, we did not include representatives of large dialysis organizations (LDOs) in the US in our study. We believe that the onus rests on the nephrology research and clinical community to devise innovative ways of increasing physical activity and delivering intra-dialytic exercise to HD patients, with minimal additional costs and resources. However, not involving LDOs as stakeholders may be a limitation of this study and is very important for future research.

Conclusion
Given the paucity of interventions to improve the HRQOL and physical well-being of patients on chronic HD and the promise of exercise therapy, there is a critical need to optimize exercise participation in these patients. Our study identifies important barriers to exercise, several of which may be modifiable, as well as factors that may motivate HD patients to exercise. Patients and providers favor a multi-modal program that includes individually-adaptable intra-dialytic exercises, education and motivation Understanding and incorporating the preferences and devising novel ways to incorporate these in a cost-and resource-effective manner is the key to successful implementation of such a program. Future research is needed to design such a program and evaluate its impact on patient outcomes.

What barriers do you see for implementing an
intra-dialytic exercise program?
Questions for nephrologists: