A qualitative stakeholder analysis of beliefs, facilitators, and barriers for a feasible prehabilitation program before lung cancer surgery

A qualitative interview study was performed to develop a feasible prehabilitation program, including physical exercise training, nutritional and psychological support, and/or coaching towards lifestyle changes for patients with operable NSCLC. Healthcare professionals, patients, and informal caregivers were interviewed to explore beliefs, facilitators, and barriers to prehabilitation. Included patients did not perform prehabilitation but had the experience of a perioperative period and could reflect on facilitating factors and barriers. In order to gain a respectable representation of beliefs, no exclusion criteria were set. This study was approved by the Medical Research Ethics Committee Zuyderland (reference number: 2021–2879). All participants were recruited between September 2021 and February 2022.

Data was collected through one-to-one semi-structured interviews at a time and place suited for each participant. Interviews with healthcare professionals were conducted via video consulting online. For patients and informal caregivers this was at their home or before or after a scheduled usual care appointment at the hospital. One researcher (MV) conducted the interviews with patients and informal caregivers separately. The other researcher (EB) conducted the interviews with healthcare professionals. The number of interviews intended to perform was based on inductive thematic saturation. Saturation was considered when interviews did not lead to new themes. It was expected that approximately ten interviews with healthcare professionals, fifteen interviews with patients, and fifteen with informal caregivers were required. Preoperative and postoperative patient characteristics were derived from the electronic patient files. When applicable, a patient’s postoperative complications were graded according to the Clavien-Dindo classification (Clavien et al. 2009) to provide insight into treatment characteristics and treatment outcomes of the patients.

The interviews were conducted based on a semi-structured interview guide (developed by MV, CS, BB, and MJ) using open-ended questions that initially defined the areas explored. Interview topics are shown in Table 1. These initial topics were chosen based on an existing behavior model. The capability, opportunity, motivation, and behavior (COM-B) model (Michie et al. 2011) guided the categories of questions regarding three types of behavior: (1) participating in multimodal prehabilitation, (2) referring to a prehab program, or (3) to support a loved one during prehab. The COM-B model (Michie et al. 2011) suggests that engagement in a behavior is determined by capability (e.g., physical skills, knowledge), opportunity (e.g., environment, social norms), and motivation (e.g., habits, beliefs, general attitude towards multimodal prehabilitation). Three test interviews were conducted for the study population, after which the topics and interview guides were optimized. The researchers (MV and EB) discussed changes in the interview guides.

Healthcare professionals were asked about the facilitators and barriers concerning their ability and available opportunities to refer patients to prehabilitation. Additionally, their opinion about which subgroup(s) of patients benefits the most from prehabilitation was asked. Information requested included patient characteristics, previous experiences with physical exercise training, nutritional advice, and smoking-cessation. Moreover, the occurrence of postoperative complications and their opinion about surgical delay to gain time for prehabilitation were questioned. Informal caregivers were interviewed about barriers and facilitators to support their loved ones to adhere to a prehabilitation program.

Data was collected according to the standards for reporting qualitative research checklist (O'Brien et al. 2014). All interviews were recorded and transcribed verbatim. These transcripts were fragmented and open coded in ATLAS.ti version 9 (ATLAS.ti Scientific Software Development GmbH) (N. V. 2020; Soratto et al. 2020). The open codes were divided into subthemes and themes using thematic analysis (Soratto et al. 2020). The first three interviews of each study population were independently fragmented, coded, and thematized by two researchers (MV and EB). Themes were discussed until consensus was reached. These themes were used as a base for coding the other transcripts.

A total of 45 interviews were conducted with twelve healthcare professionals, seventeen patients, and sixteen informal caregivers. Healthcare professionals involved in the treatment process of patients with NSCLC were two rehabilitation physicians, two pulmonologists, one surgeon, one psychologist, two dieticians, two physical therapists, and two case managers (Table 3). The median age of the healthcare professionals was 44 (range 24–64) years. Most healthcare professionals had more than five years of experience in the treatment of lung cancer, but some healthcare professionals mainly treated patients in general pulmonary rehabilitation. All patients and informal caregivers were interviewed at their homes. The median age of the patients was 65 (range 51–85) years, the median time between diagnosis and surgery was six (range 1–24) weeks, and the median length of hospital stay was four (range 2–11) days. Postoperative complications occurred in 69% of the interviewed patients, of which 64% were Clavien-Dindo grade I, 18% were Clavien-Dindo grade II, and 18% were Clavien-Dindo grade IIIa complications. Median age of the informal caregivers was 62 (range 21–84) years. The relationships of the informal caregivers with the patient were spouse (94%) or son (6%). All participant characteristics are summarized in Table 2. Final themes concerning prehabilitation were described and summarized on a code tree (Table 3) The themes from the interviews are summarized in the text below and in Table 4.

Healthcare professionals mentioned a need for consensus on a cut-off value for including or excluding patients with lung cancer for prehabilitation, as well as regarding the cost-effectiveness of prehabilitation. Healthcare professionals preferred that case managers screen patients on preoperative modifiable risk factors. They expected that prehabilitation would be most effective in patients with a poor preoperative physical fitness and/or a poor nutritional status.

“I would prefer that a case manager screens the patient, connecting patients with healthcare professionals, designing treatment plans, and making sure it all gets done on time.” Healthcare professional 3

According to all healthcare professionals, patients should be informed on how they can positively influence their health and functioning preoperatively. They mentioned the importance of providing similar and unambiguous information about a healthy lifestyle before surgery to patients, taking into account different cultures, beliefs, or language barriers. Healthcare professionals mentioned the short period between diagnosis and surgery as a barrier for prehabilitation, which might be too short to initiate an effective prehabilitation program. Nevertheless, most healthcare professionals reported that surgery could be delayed safely when the pulmonologist or surgeon decides that a delay of surgery is possible. They mentioned that referring patients to prehabilitation might be facilitated when multiple professionals within and between primary and secondary healthcare are involved in prehabilitation and have weekly time slots available to schedule patients quickly. Most healthcare professionals prefer prehabilitation to take place at the hospital because communication between healthcare professionals within the hospital is easier. Healthcare professionals share an electronic patient file which gives the opportunity for quick referrals to prehabilitation. Furthermore, they expressed more trust in the knowledge of physical therapists working in their own hospital.

“I have doubts about the knowledge and skills regarding prehabilitation by physical therapists in primary care. So, my preference is to offer prehabilitation in the hospital.” Healthcare professional 3

Healthcare professionals encouraged informal caregivers to be involved in prehabilitation as they can stimulate their loved ones and know how to motivate them. A barrier is that, currently, patients must pay the costs associated with preoperative preventive interventions themselves. Prehabilitation is not yet reimbursed by Dutch healthcare insurance companies.

“If patients become more fit preoperatively due to prehabilitation, there will be a faster recovery after surgery and therefore a shorter length of hospital stay. While prehabilitation is not yet standard care and is not reimbursed by the by Dutch healthcare insurance companies, I think this is very effective in lowering healthcare costs.” Healthcare professional 9

Most patients considered themselves sufficiently fit for surgery; they reported a healthy diet and felt no need for a prehabilitation program.

“My condition was sufficient because I cycled to work every day before the diagnosis. In addition, during the test (cardiopulmonary exercise test) before surgery, I did not have to make an effort to reach the level required to be operated on.” Patient 2

“I didn't need to get fit before surgery. I think the pulmonologist thought I was fit enough, because in that lung test (forced expiratory volume in one second) it turned out that I could miss a lung.” Patient 6

Patients did not know that a better preoperative physical fitness and nutritional status reduces the risk of postoperative complications. When the pulmonologist concluded that their physical fitness, according to the preoperative lung function tests, was sufficient to undergo surgery, patients indicated that they felt no need to prepare for surgery. When the patients received information about prehabilitation, they believed it facilitated postoperative recovery and mentioned that they would participate in prehabilitation if their physician recommended it. Patients said they would prefer to receive information about preparation for surgery, the surgery itself, and a healthy lifestyle before surgery and during the postoperative period.

“During the consultation at which I was diagnosed with lung cancer, the pulmonologist said that I needed to see a physical therapist to increase my endurance capacity. I was fine with it, but I was never referred and never heard from it again.” Patient 3

“The doctor asked what activities I did on a regular day. I replied: all household activities, cleaning, and grocery shopping. Hereafter she concluded: well, in that case preoperative physical exercise training is not necessary.” Patient 8

Patients indicated that they want to know what physical exercises would be practical for them and that an expert, such as a physical therapist or sports instructor, is the one to decide. A preoperative physical exercise training program, such as endurance training (e.g., walking, cycling, swimming) and resistance training, was most frequently mentioned as an intervention that patients would prefer. In contrast, patients felt no need for nutritional support from a dietician.

“A physical therapist is the best person to advise me what kind of exercises I should do; after all, he has learned for it.” Patient 1

Patients reported that they would prefer face-to-face guidance of a physical therapist or personal trainer to improve their preoperative physical fitness. Guidance of a dietician could be done by phone or via video-consulting. If a physician recommended prehabilitation, all patients reported that they felt capable to execute a physical exercise training session one to three times weekly and would change their diet when necessary. Most patients had enough time to participate and otherwise would have made time for prehabilitation. Patients indicated that they had many hospital appointments and medical examinations but that was not seen as a barrier to take part in a prehabilitation program. Some patients stated that they had a busy preoperative period because friends and family visited them at home, which was experienced as a barrier to take part in prehabilitation.

“Normally I walked every day, but in the last week before the operation I had so many visitors that I lost my walking rhythm, and I could not do anything about my fitness anymore.” Patient 3

The opportunity of having a direct communication with a healthcare professional was mentioned as a facilitator for patients to take part in a prehabilitation program. Patients preferred a physical exercise training program organized in primary care, because it fits better within their living context. Group-based exercises or having a training buddy were preferred by most patients, because of contact with other patients and motivational reasons. A long travel distance was seen as a barrier to participate in prehabilitation.

“I would have liked to do physical exercises in a group, because it allows you to talk to other patients and it helps to stay motivated.” Patient 9

Unsupervised prehabilitation at home was seen as a barrier for most patients, as they mentioned a lack of self-discipline. Patients felt they needed the support of their loved ones and preferred that they were able to join the appointments in a prehabilitation program. Some patients described that the intense and stressful period before surgery motivated them to be more physically active and to improve their health. Other patients indicated they were worried about the surgery and the outcomes and felt the need for a preoperative consultation by a psychologist, but this was not offered.

“I missed psychological support in the entire process. When the doctor said “we found a tumor in your lung”, I really would have liked to have a conversation with a psychologist, because your world is falling apart.” Patient 15

Patients would like to receive more information about the postoperative period during a prehabilitation program (e.g., what to expect, how to deal with side effects and complications, medication use, process emotions).

“They write in leaflets what you can and cannot do after surgery in case of fever, regarding medication, et cetera, but not about the preparation for surgery in terms of physical exercise training and nutritional support. I would consider that information about physical exercises is being of additional value.” Patient 4

“I would have liked information about physical preparation before surgery. I went to the rehabilitation center where I worked until the diagnosis NSCLC and asked if I can do something to improve my physical fitness before the operation, but they mentioned that they did not know what kind of physical exercises were good and safe.” Patient 15

Some patients suggested that smoking-cessation before surgery was difficult because of the stressful period before surgery. Furthermore, patients reported that healthcare professionals recommended that they could quit smoking after surgery to avoid an increase in the perceived level of stress before surgery.

“My wife wanted me to stop smoking right away, but the pulmonologist wanted to wait until after surgery to avoid stress before surgery. After surgery I went to the general practitioner myself and asked for help with quitting smoking.” Patient 5

Patients did not feel the need for smoking-cessation interventions during prehabilitation. Most patients mentioned that they could talk to their spouses and family about their feelings and felt supported. Some patients would not like a delay of their surgery in favor of prehabilitation; they indicated that they wanted their tumor to be removed as soon as possible, and postponing surgery would increase their anxiety. However, some patients said they would accept a delay of two to four weeks to improve their physical fitness preoperatively.

Most informal caregivers considered their loved ones to be adequately fit for surgery. Informal caregivers said smoking-cessation should be a part of a prehabilitation program merely when initiated by the patient instead of persuading the patient; otherwise, they considered it ineffective. Informal caregivers preferred prehabilitation for their loved ones to be organized in their own living context in primary care in order to be able to provide optimal support. Most informal caregivers indicated they were also willing to participate in a physical exercise training with their loved ones and to offer nutritional support.

“I think it is important to provide support. You just do that as a partner. It is… we have been together for so long for a reason.” Informal caregiver 4

Most informal caregivers reported that they wanted the tumor to be resected at the earliest convenience and did not prefer a delay of the surgery in favor of prehabilitation. Most informal caregivers were worried to lose their loved ones due to cancer but tried to remain positive and said they could talk to their loved ones about their feelings and concerns.

The results from this study provide valuable information to implement a prehabilitation program before lung surgery that considers the facilitators and barriers of healthcare professionals, patients, and informal caregivers. For developing a feasible prehabilitation program for patients to adhere, it is important that content and context is made as optimal as possible. This study shows that there are many facilitators to set up a feasible prehabilitation program. When prehabilitation becomes usual care, it is important that (1) health professionals know when to refer patients to prehabilitation and that there is a clear application procedure to enroll in a prehabilitation program (2) that patients receive a referral and recommendation for prehabilitation and that patients are adequately informed about the purpose and benefits of prehabilitation (e.g., leaflets, website of the hospital, improving the communication between healthcare professionals and patients). The current study shows that patients were motivated to participate when prehabilitation is recommended by a physician. Knowing the positive effects of prehabilitation before lung resection on postoperative complications, prehabilitation should be considered to become part of usual care.

Patients indicated that they would prefer group training sessions organized in their own living context. A previous study has shown that group-based postoperative physical exercise training for operable lung cancer had social benefits in addition to improved physical fitness in addition to improving exercise adherence, like good social relations with other patients and learning from each other’s experiences (Missel et al. 2019). Thereby, patients prefer a prehabilitation program supervised by a specialized healthcare professional with the possibility that their loved ones could interact as well. Contrary to the patients, most healthcare professionals preferred prehabilitation to take place in the hospital, because communication with other involved healthcare professionals is easier for them. Furthermore, multiple professionals within and between primary and secondary healthcare should be involved in the context of prehabilitation. However, the Dutch government recommends that 50% of care must take place in the living environment of the patient instead of in a healthcare institution by 2030 (Mission document Top sectors and Innovation policy. 2022).

The present study provides detailed qualitative data on beliefs, preferences, barriers, and facilitators of prehabilitation from the perspective of healthcare professionals, patients with operable NSCLC, and informal caregivers. Ascertaining what is meaningful to patients in the perioperative period in order to participate in a prehabilitation program may be challenging, but is fundamental to clinical patient care (DiGloia et al. 2016), as engagement of patients in their care has been associated with improved clinical outcomes and care experience (Carman et al. 2013). Limitations of the study should also be acknowledged. First, recruitment for healthcare professionals and scheduling interviews was difficult due to hectic periods in pulmonology departments in the medical centers because of the coronavirus disease 2019 pandemic. As such, not all healthcare professionals had extensive experience in the treatment of patients with lung cancer, but they did have experience in treatment of patients with other lung diseases. Second, both pulmonologists interviewed for this study were employed in the same medical center, with the same organization of care and information provision. This might have resulted in reduced richness of the data. Third, patients who participated in this study had not been offered to participate in a prehabilitation program. This means that future studies are needed to evaluate experiences with a prehabilitation program that can be developed with the results from the current study.

In order to facilitate healthcare professionals to refer patients to a prehabilitation program directly after the diagnosis of NSCLC, agreements about the preoperative screening, assessment, and enrollment in prehabilitation is needed. With sufficient time between diagnosis and surgery, prehabilitation could be organized in primary care and it is therefore essential to make workable agreements between healthcare professionals and negotiate with health insurance companies to reimburse prehabilitation. Furthermore, it is recommended to focus on the inclusion of high-risk patients with NSCLC prehabilitation as part of usual care because of the positive effects of prehabilitation on surgical outcomes (Beck et al. 2020).