Patient perspectives of multimodal prehabilitation for ovarian cancer with surgical intent: a multicentre qualitative evaluation of acceptability, barriers and facilitators for participation

Abstract

Objective

To carry out a qualitative evaluation of personalised, multimodal prehabilitation for patients with advanced ovarian cancer in the UK, to inform the design and implementation of future programmes worldwide.

Methods

A multicentre, qualitative exploration of patients with advanced (stage III–IV) ovarian cancer with a surgical intent to treatment, who had been referred to a UK National Health Service prehabilitation programme. Using a purposive, maximum variation sampling approach, patients were invited to complete a semi-structured interview about their views and experiences of multimodal prehabilitation (exercise, nutritional, psychological and medical optimisation interventions). The interview focused on acceptability, perceived usefulness of the service and barriers and facilitators to engagement and adherence. Interviews were conducted virtually. Audio recordings of interviews were transcribed verbatim. Data were analysed thematically.

Results

Interviews were completed with 21 patients, with a median age of 56.5 years (range 37–89 years). Four main themes were identified with associated subthemes as follows: (1) introduction to the programme (timing, volume and content of information), (2) perceived need (support system and mindset, psychological and physical health), (3) delivery of the programme (convenience of appointments, accessibility of staff, family involvement, individual components of the intervention; ie, physical, psychological, nutritional interventions and group work) and (4) future engagement (addressing postsurgical gynaecological health and closure).

Conclusion

Overall, prehabilitation was acceptable to patients with advanced ovarian cancer who had been referred to a multimodal prehabilitation programme. Perceived accessibility of staff and inclusion of patients’ social network facilitated engagement. Lack of perceived need for prehabilitation was a barrier to participation, particularly for those with a strong support system or self-confessed strong physical and psychological baseline fitness. Effective patient-centred communication about prehabilitation could support patients with making informed choices about engagement in prehabilitation as part of their care plan.

WHAT IS ALREADY KNOWN ON THIS TOPIC

• Multimodal prehabilitation programmes aim to improve the patient’s functional and metabolic reserve preoperatively, thereby improving perioperative recovery.

WHAT THIS STUDY ADDS

• There are limited data available on ovarian cancer patient perspectives of multimodal prehabilitation. Some qualitative studies have shown a general acceptance among patients with ovarian cancer; however, there remains a lack of perceived need.

• Accessibility of healthcare professionals, person-centred communication and inclusion of patients’ social networks in prehabilitation can facilitate participation, while patients’ lack of perceived need for prehabilitation can act as a barrier to engagement.

HOW THIS STUDY MIGHT AFFECT RESEARCH, PRACTICE OR POLICY

• To implement a truly personalised approach to multimodal prehabilitation in ovarian cancer, it is important to ensure that patients have opportunities for high-quality, person-centred communication with their healthcare teams, eliciting and discussing individual patient attitudes towards prehabilitation, and supporting inclusion of their informal support network.

Introduction

Background

Patients with ovarian cancer often present late, in advanced stages, and are frail as a result.^{1 2} Malnourishment is reported in up to 67% of patients with ovarian cancer,¹ with 30% reporting anxiety and depression.³ This results in a high-risk cohort of surgical patients⁴ with perioperative frailty in up to 60% of patients,⁵ irrespective of age.⁶ Multimodal prehabilitation includes physical, nutritional, psychological, medical optimisation and smoking cessation interventions.^{7 8} The aim of prehabilitation is to improve the patient’s functional and metabolic reserve preoperatively.⁹ Prehabilitation can reduce perioperative complications, length of stay (LOS) and improve quality of life for patients undergoing surgery.¹⁹,¹² IMPROVE-UK was the first major programme within the UK addressing the inequalities in care for patients with advanced ovarian cancer. As part of this, the IMPROV-UK prehabilitation collaborative included three multimodal prehabilitation programmes comprising six gynaecological oncology cancer centres.¹³ The results from these prehabilitation quality improvement initiatives have shown high rates of frailty,¹⁴,¹⁶ psychological distress¹⁵ and improved perioperative outcomes following the introduction of prehabilitation.¹³,¹⁶

Relevance of the subject of interest

Personalised prehabilitation is essential to increase engagement and reduce unnecessary stress when patients are already dealing with complex and emotive decisions.¹⁷,¹⁹ Across the UK, prehabilitation is not provided as standard of care for ovarian cancer in most cancer centres. Collaborative guidance from Macmillan, the Royal College of Anaesthetists and the National Institute of Healthcare Research states that prehabilitation “should be integral in the management and support of patients diagnosed with cancer”.²⁰ To successfully provide personalised prehabilitation, an in-depth understanding of patients’ perspectives is required.²¹ Qualitative research is vital in understanding how interventions are implemented and received.²²

Goals of the study

Qualitative studies of the views and experiences of patients in prehabilitation programmes have been conducted in Europe²³,²⁶ and the USA,²⁷ typically in groups with mixed cancer diagnoses. The perspectives of patients with ovarian cancer have been insufficiently studied, and due to their frequent deconditioning and frailty at presentation, understanding their perspectives is important.²⁸ A qualitative study of patients with advanced ovarian cancer who were referred to prehabilitation prior to primary debulking surgery (PDS) highlighted a lack of perceived need for prehabilitation.²⁹ The authors suggest that self-determination theory indicates that focusing on patients’ intrinsic motivation (ie, the activity is engaged in for an individual’s own interest and satisfaction) could improve engagement with prehabilitation in this context.²⁹ The aim of this qualitative evaluation was to investigate patient perspectives on acceptability, usefulness, barriers and facilitators to engagement with multimodal prehabilitation.

Methods

Study population

Patients were purposively sampled from the All-Wales Ovarian Cancer Prehabilitation Project (AWOCPP)¹⁴ and the Holistic Integrated Care in Ovarian Cancer (HICO) Service¹⁶ as part of the IMPROVE-UK prehabilitation collaborative^{13 30} from February 2023 to February 2024. This included four UK tertiary gynaecological oncology cancer centres: the South-East Wales Gynae-Oncology Cancer Centre, the North-Wales Gynae-Oncology Cancer Centre, the Royal United Hospitals Bath Foundation Trust and the University Hospitals Bristol. All patients with advanced ovarian cancer with intent for PDS or interval debulking surgery (IDS) who had been referred to a prehabilitation programme were eligible to participate. Patients with early stage disease (stages I–II), those with no surgical intent and those who did not agree to being contacted in the future were excluded from the study. The patient pathways are available in online supplemental material as an example of the multimodal prehabilitation interventions.

Study design

Recruitment

Purposive maximum variation sampling was used to capture a range of views and experiences,³¹ and reflective semi-structured interviews were conducted by the research fellow (JCM) using a thematic guide which was developed in collaboration with the research group. JCM was the primary researcher, with a background in gynaecological oncology, working as a clinical research fellow in Wales as part of the AWOCPP. None of the interviewees were known to JCM prior to interview. Eligible patients were contacted via telephone to introduce them to the study and written information was sent to those who accepted. Informed consent to participate was obtained from all patients. Interviews were conducted virtually, audio-recorded and then transcribed verbatim by an independent transcriber. Patient and public involvement was central to this qualitative study, ensuring the research was relevant and meaningful. This included patient involvement in the formation of study patient information leaflets and the interview structure.

Analysis

Thematic analysis was conducted on the data³² using an inductive approach. NVIVO qualitative analysis software was used to complete the thematic analysis.³³ Initial coding was carried out by the primary researcher (JCM). Recruitment continued until no new significant themes had been identified.³⁴ Findings were then discussed among the research group (DW, RP, SJ) and subsequently developed into relevant themes and subthemes. The Standards for Reporting Qualitative Research checklist was used to guide the reporting of this study.³⁵

Results

In total, 31 eligible patients were contacted, of which 25 agreed to participate and 21 completed semi-structured interviews. Of those who initially agreed, two patients felt too unwell to participate and two patients withdrew due to unavailability. Table 1 summarises the demographics of interviewees.

Table 1. Patient demographics.

Patient demographics		No. of patients (%) n=21
Median Age	56.5 years (range 37–89 years)	–
Cancer centre	AWOCPP HICO	10 (48) 11 (52)
Ethnicity	Caucasian	21 (100)
Highest educational achievement	No formal qualifications	2 (10)
	High school level qualification (General Certificate of Secondary Education [GCSE]/A-Level)	12 (57)
	University-level qualification	7 (33)

AWOCPP, All Wales Ovarian Cancer Prehabilitation Project; HICO, Holistic Integrated Care in Ovarian Cancer.

Themes identified during thematic analysis

Introduction to the programme

The first main theme identified related to how patients were introduced to the programme. Three subthemes were identified: timing of information, volume of information and content of information. Example quotations are provided in the text and in online supplemental material.

Timing of information

Most interviewees were introduced to the programme at their first clinical appointment and reported being given all the information regarding their diagnosis, treatment and prehabilitation at the same time. Many reported feeling overwhelmed or being too unwell to process the information presented to them at this time. Staggering the provision of information was suggested to help with this issue.

“I think it was pretty much the day that I got told everything all at once.” (HICO10)

“At the time, I was just a little bit too ill to deal with it.” (AWOCPP4)

Volume of information

There was a discrepancy in opinion regarding the appropriate volume of information that interviewees received. Most interviewees felt that there was too much information to process. Others suggested the need for an individualised approach, which would ensure that the level of detail is appropriate and manageable to enable them to make an informed choice about participation.

“All I remember is being deluged with information at the time.” (AWOCPP4)

“I think it was enough. You have all the packaging, and you can choose yourself.” (AWOCPP3)

Content of information

Interviewees reported an overall lack of understanding of the aims and potential benefits of prehabilitation in the peri-operative period. This indicated that more focused and understandable information would be useful in introducing the programme focusing on key messages about the aims and benefits of the programme for patients.

“I probably didn’t have enough understanding. I was given enough information, but I was lax in my understanding.” (AWOCPP9)

“Initially I didn’t really have a lot of idea what it was about, but the more time went on I had more understanding.” (AWOCPP9)

Perceived need

The second main theme relates to patients perceived need for the prehabilitation programme. Three subthemes were identified: support system, mindset—psychological and mindset—physical. Example quotations are provided in the text and in online supplemental material.

Support system

Patients who reported a strong support network from family or friends appeared less likely to engage with the programme due to a lack of perceived need, often saying that they could see the potential benefits for others who were less well supported. Interviewees who did not have a strong support network described feeling lonely or isolated as their motivation to engage.

“I, luckily, had a really good support network of husband, friends and family and so I think perhaps I maybe didn't need as much as somebody who was completely on their own.” (HICO10)

“I got all that from friends and family. I didn’t really approach any professionals for that.” (HICO11)

Mindset—psychological health

Patients with a self-reported positive or independent mindset were reluctant to engage with any psychological interventions. However, they appeared positive regarding the potential benefits of psychological support for others and felt it was a useful addition to the programme. Patients who had previous positive experiences with psychological therapies appeared more motivated to engage.

“I am very independent and resilient; I can do this on my own.” (AWOCPP4)

“I am quite independent and quite self-sufficient, so I haven’t felt the need. But it doesn’t mean for other people that it wouldn’t be very useful.” (AWOCPP10)

Mindset—physical health

Interviewees who had a self-reported good baseline physical health had a lack of perceived need for prehabilitation and this acted as a barrier to engagement. Those interviewees were more likely to compare themselves to other patients who they perceived as more likely to benefit from the programme due to being more unwell at the outset.

“I sat waiting to see the oncologist and kept seeing people who were obviously more unfit than me, more overweight, more unwell. I was thinking well there are probably people who need this more than I do.” (HICO11)

“It is good for people who are quite old. They need more help, but I sorted everything for myself.” (AWOCPP3)

Delivery of the programme

The third main theme relates to how the programme was delivered to patients. None of the interviewees reported engagement with a care of the elderly physician for medical optimisation; therefore, no data were collected relating to this aspect of prehabilitation. Five subthemes were identified: convenience of appointments, accessibility of staff, family involvement, individual interventions (exercise, psychological, nutritional) and group work. Example quotations are provided in the text and in online supplemental material, along with the AWOCPP and HICO pathways, as an example of the prehabilitation interventions.

Convenience of appointments

Overall, the location or timing of the prehabilitation appointments was not a barrier to engagement for the interviewees in this study. However, there was a desire to prioritise any appointments directly related to treatment. The flexibility of appointment scheduling was a positive factor for engagement, especially as not all appointments were face-to-face. There was an understanding that this could be an issue for patients in different circumstances. Specifically, those with little support at home, with long distances to travel, or those who rely on public transport. Some aspects of the prehabilitation interventions were delivered virtually or in the community, including the National Exercise Referral Scheme as part of the AWOCPP.

“I think there was quite a distance to travel for some.” (AWOCPP7)

“Any appointments that I couldn’t do in person they would be online instead.” (HICO7)

Accessibility of staff

The accessibility of staff was an overwhelmingly positive factor for engagement. Specifically, a timely response from staff to any patient contact was highlighted by the majority of interviewees. Additionally, interviewees felt that they knew who to contact for each prehabilitation intervention, which led to a more positive experience.

“I never met a nurse or anyone who wouldn’t down tools at that moment if you needed help.” (HICO1)

“Everything that I needed was at my fingertips if I needed it. I knew that if I needed to speak to anybody, they were just a phone call away.” (HICO2)

“It’s like having a friend there all the way through. They were just always there, you know, if I wanted to ask anything they were always there, just supportive in every way.” (AWOCPP5)

Family involvement

Having a strong support system has been highlighted across multiple domains of this study and interviewees expressed a desire to have more support for their family. This was also raised as a potential facilitator to engagement with prehabilitation in the future.

“Your family are standing on the side lines if you like.” (AWOCPP4)

“It would have been useful to have a partner/family thing as a component added in terms of family group sessions with other patients and families together.” (HICO3)

“Maybe there’s room for some sort of opportunity for family members to have a bit of a chat along the way somewhere.” (HICO3)

Individual interventions—exercise intervention

Having the opportunity to repeat physical intervention assessments throughout the programme led to a growth in confidence for the patients. This was also seen in those interviewees who initially declared a reluctance to engage due to the perception of a strong self-reported baseline physical health.

“I think the exercise programme was very useful.” (HICO6)

“I suppose I probably enjoyed the physical side of it the best really. They just gave me a sense of satisfaction with the challenge. I would go out for a daily walk even if I wasn't really feeling great and just little things like that made me think if I can carry on doing this, then it makes me feel better mentally as well as physically.” (HICO10)

Individual interventions—psychological intervention

There remained an overall reluctance to engage with the psychological intervention among the interviewees, particularly among those who felt they had sufficient support from their social networks, felt they were able to cope independently or felt that they had difficulty with opening up about their feelings. For those that did engage, the response was positive in relation to helping them come to terms with their diagnosis. Some felt that, although they had initially been reluctant to receive this support, it had been or could have been of benefit at a later point in time.

“I suppose to be told my devastating diagnosis; it was helpful in processing that. You are in a feeling of absolute turmoil and anxiety. I was fearful and worried for my children, and so it was helpful.” (HICO7)

“They decided that I probably would benefit from talking to the counsellor. I did speak to her, and she was very helpful actually. I didn’t think I needed her but actually I did.” (AWOCPP2)

“I think I did need it more, but I just kind of gritted my teeth and got on with it.” (HICO10)

Individual interventions—nutritional intervention

The interviewees perceived the input from a dietitian positively, especially for those who were experiencing the debilitating side effects of neoadjuvant chemotherapy. Many interviewees highlighted that the support they received with their diet, in the context of weight loss and nausea or vomiting, was very helpful. There was a reluctance to take the high-calorie protein drinks provided due to a dislike for the taste and texture. This led some patients to disengage from this intervention. Having the option of a variety of protein-rich drinks to choose from, based on personal taste, may have facilitated further engagement.

“I think I often felt sick during chemo, and I lost quite a lot of weight, so I had a lot of help there.” (HICO6)

“I was dealing with a lot of stomach pain and digestive issues and (the dietician) was invaluable. She really helped me.” (AWOCPP4)

Group work

Some interviewees reported a reluctance to engage due to social anxiety associated with group work during the programme for physical and psychological interventions. For those who did engage with groups during the programme, they reported disappointment that not all groups were specific to patients with ovarian cancer and felt they were not able to identify with others in the group. This acted as a barrier for any engagement with groups that were subsequently offered.

“I would have liked to go somewhere where everybody else had the same cancer.” (AWOCPP5)

“I didn’t find the group very beneficial because it was elderly men mainly. If it could have been one to one or with others who had ovarian or gynae cancer I think that would have been more beneficial.” (AWOCPP7)

“You are very lonely when you are not in the common denominator group.” (AWOCPP)

Suggestions for potential improvements to the prehabilitation programme

The fourth main theme related to how the programme could be delivered to patients in the future, to improve engagement. Two subthemes were identified: addressing postsurgical gynaecological health and closure. Example quotations are provided in the text and inonline supplemental material.

Addressing post-surgical gynaecological health

Multiple interviewees, of varying ages, raised concerns regarding the lack of support for postsurgical gynaecological health. This was in relation to fertility, psychosexual health and menopause support. It was highlighted that these issues affect all patients with ovarian cancer, to a certain extent, following cytoreduction surgery. The recommendation for future prehabilitation programmes was to prioritise these challenges as they affect both the physical and psychological health of postsurgical ovarian cancer patients.

“I was being put into surgical menopause in my mid 30’s and there was no, ‘this is what you can expect’ or ‘this is what we can offer’.” (AWOCPP6)

“I remember after my operation I asked the nurse a question about menopause, and she just said, ‘I don’t know.’ No one ever spoke to me about it.” (AWOCPP6)

Closure

Despite the positive impact of prehabilitation, there was a clear desire for an ending to the programme that gave them a sense of closure. Many interviewees raised the desire for a follow-up consultation to bring the programme to a close and signpost them to any ongoing support.

“But after recovery it was very much goodbye.” (AWOCPP6)

“The only thing that bothered me was that once you stop your treatment, they don’t do the follow up.” (AWOCPP10)

“A longer term follow up may be helpful if your treatment options change in the future.” (AWOCPP1)

Discussion

Summary of main results

The introduction and information presented to patients by healthcare professionals (HCP) about multimodal prehabilitation services was a barrier to engagement. Many patients felt that they received too much information at the beginning, yet there remained a lack of perceived need for and understanding of multimodal prehabilitation. The timing of the provision of information may contribute to this. Interviewees reported feeling unable to process information due to concurrent discussion about diagnosis and treatment options which were felt priority at the time, or because they felt too unwell. Interviewees with strong social support appeared less likely to engage due to a lack of perceived need yet highlighted a desire for their family and friends to be alongside them throughout this difficult journey. It may be beneficial to include the patient’s support network in discussions regarding multimodal prehabilitation to improve engagement. There is an appetite for more information regarding postsurgical gynaecological health, including psychosexual health, fertility desires and menopause, highlighting that this is an important aspect of the ovarian cancer treatment journey which could potentially be incorporated into prehabilitation or elsewhere in the care pathway.

The accessibility of HCPs was highlighted as a facilitator to patient engagement with multimodal prehabilitation, particularly in relation to a timely response to concerns, to reduce anxiety and create a safe environment. However, patients want closure from these relationships. They have built up trust in the HCPs involved in their care and many felt that the lack of follow-up was a barrier to future engagement.

Results in the context of published literature

The studies that have assessed multimodal prehabilitation are few, and most involve a mixture of cancer groups.²³,²⁶ Polen-De et al²⁷ qualitatively assessed patient views on exercise only in patients who underwent IDS for ovarian cancer. They found that patients’ physical symptoms related to their treatment were a potential barrier to engagement. Our results highlighted that physical symptoms were a potential barrier during the provision of information as some felt too unwell to process it, but it did not seem to influence engagement with the programme. Saggu et al, within a UK population, assessed patients undergoing PDS and found an overall positive approach to multimodal prehabilitation but highlighted a lack of perceived need. They found a deep concern for family and friends with mixed emotions regarding group sessions.³⁶ Morrison et al conducted a literature review assessing ovarian cancer patient perspectives on physical activity generally, not specifically in relation to multimodal prehabilitation, and found that lack of motivation or routine was a barrier to engagement.³⁷ These are consistent with our results in relation to perceived need, delivery of the programme and future engagement. They also highlight the self-determination theory,²⁹ indicating that intrinsic motivation could be important in increasing engagement. Digital home-based multimodal prehabilitation has been studied within other cancer sites.³⁸ This could improve engagement in relation to the convenience of appointments for in-person based prehabilitation interventions. Prehabilitation services remain central to the management of advanced ovarian cancer in both AWOCPP and HICO pathways, showing strong sustainability. This data provides vital information and direct patient insight to help structure any prehabilitation services going forward.

Strengths and weaknesses

Strengths of this study were the novel insights into engagement with multimodal prehabilitation in ovarian cancer that were obtained through in-depth analysis of the views and experiences of patients from four different gynaecological oncology centres, with a range of ages and educational backgrounds. Limitations of this study were that all patients were Caucasian and therefore, the cohort did not include an ethnically diverse population. All eligible patients were contacted and invited to participate, but the final cohort included Caucasian patients only, which is not reflective of the general UK population. No patients in this study participated in the medical optimisation intervention, so we were unable to provide insight into this aspect of multimodal prehabilitation. Although all eligible patients were contacted for recruitment, there is the possibility that those who agreed to participate were therefore more willing to engage in multimodal prehabilitation.

Implications for practice and future research

The focus of this study was to evaluate the qualitative acceptability of patients with ovarian cancer with regards to their engagement with multimodal prehabilitation. Although the aim was not to evaluate any educational outcomes or changes in patient knowledge, the results suggest that effective training of HCPs is paramount to ensure the successful delivery of multimodal prehabilitation in this cohort of patients, including details and potential benefits of each intervention in the perioperative period. The effective provision of information could improve engagement with multimodal prehabilitation by changing attitudes towards perceived need among patients and their support network. Further research is needed to explore how HCPs provide information to patients. PPI should be prioritised in any future delivery of multimodal prehabilitation. There is a lack of high-quality research assessing the physical and psychological benefits of multimodal prehabilitation in ovarian cancer more broadly. Patients with ovarian cancer in this study reported additional difficulties following cytoreductive surgery, including infertility, psychosexual difficulties and surgical menopause. These appear to be neglected within this cohort of patients, highlighting the need for more research addressing this aspect of the patient journey.

Conclusions

Multimodal prehabilitation is acceptable to patients with advanced ovarian cancer. HCPs should consider their accessibility to patients as well as the timing, quantity and methods of providing information in order to improve engagement. This, in turn, may provide an enhanced perceived need, especially if the patient’s social support network has an opportunity to be involved. In order to truly provide a personalised approach, it is paramount that HCPs listen to, and address, the opinions of patients who may avail of it.

Data availability statement

All data relevant to the study are included in the article or uploaded as supplementary information.