Northern Ireland ovarian cancer prehabilitation project
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Abstract
Patients with ovarian cancer are often diagnosed late, in advanced stages (stages III–IV) and are often deconditioned due to disease burden. Frailty is reported in up to 60% of gynaecological oncology patients and many report malnutrition, anxiety and depression. As surgery is the mainstay of treatment for ovarian cancer, with maximum surgical effort being a priority, patients are at increased risk of perioperative morbidity and mortality.
Multimodal prehabilitation aims to improve the functional capacity of surgical patients. Prehabilitation commonly includes physical, nutritional, medical optimisation, smoking cessation and emotional well-being interventions. Many surgical specialties have well established evidence for the use of prehabilitation showing a reduction in length of stay and perioperative complications. There is, however, limited evidence for the use of prehabilitation in the surgically vulnerable group of patients with advanced ovarian cancer.
This project aimed to introduce a multimodal prehabilitation pathway for patients with advanced ovarian cancer. All patients with advanced ovarian cancer were included, regardless of the treatment modality decided at the regional gynaecological oncology multidisciplinary team meeting. The pathway included exercise, nutritional and psychological interventions. The outcome measures included the Rockwood Frailty Score, 6 min Walk Test (6MWT), 30 s Chair to Stand test, grip strength and Eastern Cooperative Oncology Group performance status as a measure of functional capacity. Nutritional intervention outcomes included the Malnutrition Universal Screening Tool (MUST) score, Body mass index and mid-arm circumference. The psychological intervention outcomes included a holistic needs assessment, the distress thermometer and EQ-5D-5L quality of life status.
Of the 75 patients enrolled, 45 (60%) completed the project. In patients who completed the project improved 6MWT and 30-CST was observed in 67% and 44%, respectively, while 67% of patients with moderate to extreme anxiety/depression scores reported lowering from baseline level and 71% of patients with medium to high-risk MUST scores baseline weight was maintained or increased.
What is already known on this topic
Prehabilitation aims to improve the functional capacity of surgical patients. Multimodal prehabilitation has been shown to reduce the length of stay and perioperative complications in other surgical specialties.
What this study adds
This study investigates the impact of multimodal prehabilitation during the treatment (surgery and/or chemotherapy) on the functional capacity and psychological well-being of women with advanced ovarian cancer.
How this study might affect research, practice or policy
This study may prompt other centres to investigate the role of prehabilitation during treatment of advanced ovarian cancer and other gynaecological malignancies. If evidence of benefit is demonstrated, then prehabilitation may become embedded in the treatment pathway of advanced ovarian cancer. Further qualitative research on the acceptability of patients and any potential barriers to implementation may follow.
Problem
Prehabilitation guidelines have been developed as a result of collaborative work from the Royal College of Anaesthetists, the National Institute for Healthcare Research (NIHR) and Macmillan Cancer Support stating that, ‘the aims of prehabilitation are to empower patients to maximise resilience to treatment and improve long-term health’.1 This highlights the integral role prehabilitation can play in the management of patients with cancer to provide a more proactive and cost-effective approach to care. Research has shown that prehabilitation can lead to a reduced length of stay (LOS) in hospital, less intensive care unit (ICU) and high dependency unit(HDU) admissions1 and reduced postoperative complications2 3 while enhancing recovery and quality of life overall.
Prehabilitation has been adopted among other surgical specialities including colorectal, trauma and orthopaedics and cardiothoracic surgery.4 The European Society for Gynaecological Oncology states that prehabilitation should be integrated into the management pathway for patients with ovarian cancer.5 Prior to this project, patients with ovarian cancer in Northern Ireland (NI) had no access to prehabilitation services and, therefore, are likely suffering from avoidable treatment-related morbidity. The aim of this pilot project was to assess the implementation of a tailored, equitable, evidence-based prehabilitation pathway for patients diagnosed with advanced ovarian cancer in NI. The service aimed to enrol all patients diagnosed with advanced ovarian cancer (stages III–IV) irrespective of primary treatment (surgery or chemotherapy) in a 12- month period.
Background
Ovarian cancer remains the sixth most common female cancer in the UK with a higher incidence seen in those aged 75–79.6 In fact, over a quarter (28%) of ovarian cancers in the UK are diagnosed within this age group.6 7 The mainstay of treatment for ovarian cancer includes cytoreductive surgery (CRS), with the aim to achieve complete resection of all macroscopic disease (R0), in combination with platinum-based chemotherapy.8 The rationale for offering primary surgery is dependent on the disease burden, the likely ability to achieve complete resection and the fitness of the patient. If patients are not suitable for primary CRS, due to comorbidities and/or disease burden, they are offered neoadjuvant chemotherapy (NACT) with the aim to perform delayed CRS following 3–4 cycles of chemotherapy.8 9 Maximum surgical effort should be applied to both primary and delayed CRS to achieve R0 where possible, as this can incur a better survival outcome.10 11
The majority of patients are deconditioned at diagnosis as two-thirds present with advanced disease12 13 with perioperative frailty reported in up to 60%.14 Two-thirds of patients are malnourished at diagnosis,12 with anxiety and depression reported in up to 30%.15 Prehabilitation programmes aim to prepare patients for surgery by improving functional capacity.16 Multimodal prehabilitation programmes include exercise, nutritional, psychological well-being, medical optimisation and smoking cessation interventions.6 Prehabilitation has been shown to improve the perioperative pathway for patients with ovarian cancer resulting in a reduced LOS, lower postoperative complications and a reduced surgery to chemotherapy interval.16 17
The NI Cancer Registry reports an average annual incidence of 206 ovarian cancers (2017–2021), of which 62% have advanced (stages III-IV) disease.7 The NI cancer network is composed of a regional tertiary gynaecological oncology centre and four local cancer units of which all patients with ovarian cancer are discussed at a central gynaecological oncology multidisciplinary team (MDT) meeting. 80% of patients with advanced ovarian cancer in NI originate from outside the tertiary cancer centre and due to capacity issues, referrals to the specialist team can often be delayed. The combination of advanced-stage disease and pathway delays, particularly in older patients with pre-existing frailty, can lower their chances of being suitable for surgery and/or chemotherapy.
Measurement
Before the project commenced, a customised prehabilitation database was developed to record all measures and interventions. The individual measures were captured at baseline (prior to treatment), mid-chemotherapy (prior to cycle 4) and 1-month post-treatment. The mid-chemotherapy assessment for patients having primary CRS was after cycle 3 of adjuvant chemotherapy while for patients having NACT it coincided with the timing of interval surgery. The outcome of the interventions compares the baseline measures with the end-of-treatment measures. For all patients, the end of treatment was 1-month post-final chemotherapy.
Any deviations from the schedule were recorded in the database. Details on patients who discontinued prehabilitation (disease progression, death, benign or borderline disease confirmed at surgery) were also captured. Measures were required to be specific, reproducible and validated. The rationale for the measures chosen and any potential limitations are detailed in the attached supporting information (online supplemental appendix 1).
The measures we chose to assess the outcomes of the prehabilitation programme were as follows:
RFS is a validated, semiquantitative, tool used to estimate an individual’s degree of frailty on a scale of 1 (very fit) to 9 (terminally ill). Patients who score ≥5 are considered frail.
6 min Walk Test (6 MWT).
6MWT is a validated measure of functional exercise capacity relating to cardiopulmonary fitness. This is a reproducible test which has been validated in surgical populations.16 19 20 There is a linear correlation between the 6MWT and maximum oxygen consumption (VO2max) which is associated with perioperative complications and morbidity.16
30 s Chair to Stand test (30-CTS).
The 30-CTS is a validated measure assessing lower extremity strength, endurance and risk of falls, with good retest reliability and criterion validity in older adults.21 22
Grip strength.
Grip strength is a validated measure of forearm muscle strength that has been used to evaluate and track many health conditions, especially those associated with ageing. Reduced muscle strength has been associated with an increase in cardiovascular mortality.23
Eastern Cooperative Oncology Group (ECOG) performance status.
ECOG performance status relates to the ability to care for oneself including activities of daily living and physical mobility.24 25 This plays a key role in patients with advanced malignancy when planning treatment.26
Nutritional intervention
Body mass index (BMI).
Patients with an elevated BMI are at higher risk of cardiovascular complications, morbidity, mortality and a worse long-term prognosis.27 Weight management programmes have been associated with favourable metabolic and psychological benefits in obese patients.27
Malnutrition is an independent risk factor for perioperative morbidity and mortality.28 The MUST score is a five-step screening tool aimed at identifying malnourished patients, those at risk of malnutrition (undernutrition) or obese.29
Mid-arm circumference.
Psychological intervention
Holistic Need Assessment questionnaire developed by Macmillan Cancer Support.30
Distress thermometer developed by the National Comprehensive Cancer Network.31
Health-related quality of life was measured using the EQ-5D-5L.32 In addition, the EQ Visual Analogue Scale was used to measure the patient’s self-rated health.
Design
Patients were assessed by the gynae-oncology clinical nurse specialist (CNS) in the local cancer unit/centre, with recording of the RFS at the time of diagnosis. The patient’s RFS, their eligibility for prehabilitation and willingness to participate were included in the MDT referral form and relevant information was provided. All patients with ovarian cancer are discussed at the NI regional MDT to agree a treatment plan, irrespective of prehabilitation. Following MDT, suitable patients were referred to the prehabilitation clinic in Belfast for assessment. All advanced (stages 3–4) patients with ovarian cancer were eligible to participate, irrespective of treatment plan. Only those with borderline, benign or other tumours were excluded from the prehabilitation programme.
The baseline face-to-face prehabilitation visit included a triple screening assessment by the prehabilitation nurse, physiotherapist and dietitian. These assessments enabled an individualised exercise, nutritional and psychological intervention pathway to be assigned for each patient. Patients were then risk stratified to universal, targeted or specialist interventions, as per the collaborative guidance from the Royal College of Anaesthetists, NIHR and Macmillan.1 33 The prehabilitation clinic appointment was on the same day as the gynae-oncology surgical appointment to avoid delays and appointment burden. A weekly dedicated prehabilitation clinic was established with four clinic slots, each 2 hours long. Patients rotate through nursing, dietetics and physiotherapy to ensure the best use of time. In addition to the prehabilitation face-to-face clinic appointment, further support was provided by the prehabilitation team throughout the pathway, dependent on their individual assessment.
The project was led jointly by a gynaecological oncology consultant surgeon and the service manager for cancer services. The project team engaged with local councils, regarding access to local exercise programmes and sought guidance from other specialities who had engaged in prehabilitation previously. Once the pathways had been agreed a monthly prehabilitation team meeting was set up to discuss any positive results, patient feedback and potential barriers. The prehabilitation project team consisted of the following members:
Consultant gynaecological oncology surgeon.
Service managers.
Gynaecology CNS.
Physiotherapy lead.
Dietetic lead.
Medical advisor to cancer services.
Patient representative.
Macmillan service improvement manager.
Exercise intervention
The exercise intervention was conducted using the Macmillan Move More scheme or a targeted exercise coach (delivered virtually). This is a Macmillan-funded physical activity project delivered by community exercise professionals, in partnership with local NI councils and physical activity providers, offered to patients living with or beyond cancer.34 For those who declined referral to the Move More scheme an individualised home exercise programme (HEP) was developed by a prehabilitation physiotherapist at the prehabilitation clinic. The HEP aimed to provide three bespoke high-intensity interval training sessions per week. A pedometer and/or resistance band, along with activity recording sheets, were also provided to each patient. Patients were encouraged to record their pedometer readings in the activity recording booklets provided at the start of prehabilitation.
Nutritional intervention
General nutritional and healthy eating advice was provided to each patient along with a referral to a specialist dietician, if indicated. The specialist dietician was present at the prehabilitation clinic for an individual review, if required.
Psychological intervention
Baseline psychological support was provided by the gynae-oncology CNS at the prehabilitation clinic. Patients were referred to the local Macmillan Support and information centre with the provision of general emotional well-being support. These included a ‘worry leaflet’ and useful websites. A referral was then made to local psychological services if indicated.
More detailed information on the individual prehabilitation interventions, including referral criteria for specialist interventions, can be seen in online supplemental appendix 1.
Strategy
Patient engagement and involvement
In the early stages of the project, the clinical team identified a patient representative, with a history of advanced ovarian cancer, to join the project steering group. The patient representative was involved in the design and setup of the project, providing feedback on information materials. They provided invaluable insight into the individual interventions from a patient perspective. Additionally, the regional cancer centre holds a cancer services user forum to provide insight and feedback on improvement work or service developments. The project was presented to this user group to gain additional feedback on the service after a few months of operation. Real-time feedback from patients was collected and subsequently presented at the monthly steering group meetings. Using quality improvement methodology, interventions were agreed and implemented following these steering group meetings throughout the project.
Details of changes made to the programme are as follows:
A number of patients did not realise that their appointment would take several hours at the clinic. We then contacted the appointments team to amend the prehabilitation clinic letter and ensure the appointment staff were giving patients the correct information.
Some patients did not fully understand what prehabilitation was in the early stages of the project and were not sure what to expect from their appointments. We decided that the local cancer unit CNSs were best placed to promote the patient information leaflet and ensure all patients had information at that early stage.
A cohort of patients had concurrent appointments at the surgical clinic on the same day. They found the back-to-back appointments tiring due to a lack of break in between. We subsequently arranged for the catering team to provide soup and sandwiches for these patients.
Following poor uptake of the exercise pathway intervention, patient feedback highlighted potential barriers to engagement. These included severe disease-related symptoms such as fatigue, pain, ascites and shortness of breath. We subsequently modified the prehabilitation protocol to reoffer the exercise intervention at the mid-chemotherapy appointment.
One of the original data points on the agreed prehabilitation database was to have a presurgery assessment, in addition to the baseline assessment, for patients undergoing primary CRS. This proved challenging for the physiotherapist to perform due to patients being admitted on the day of surgery. The presurgery assessment point was subsequently removed in week eight of the project.
Results
The cliniciopathological data of the 75 patients enrolled in the prehabilitation project between February 2022 and 2023 are shown in table 1: median age 67 (range 32–87), high-grade serous histology (89%), stage III or IV disease (93%) and ECOG≥2 (39%).
Table 1
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Clinicopathological data of patients enrolled in prehabilitation project
Baseline assessment
Functional capacity
Baseline RFS indicated mild to moderate or vulnerable frailty scores in 35% of patients (n=26).
Baseline 6MWT’s indicated that 77% of patients (n=58) had reduced exercise capacity for age with 21% having severely reduced capacity (<250 m).
Nutritional status
Baseline MUST score indicated high risk of malnutrition in 31% of patients (N=23) and moderate risk in 21% (N=16).
Psychological well-being
Baseline distress thermometer scores were 6/10 or higher in 43% of patients and 36% of patients reported moderate, severe or extreme anxiety/depression scores ≥3.
Risk stratification
Following baseline assessment, patients were then risk stratified to universal, targeted or specialist interventions (table 1)
Treatment received during prehabilitation
The treatment modalities that the patients received throughout the prehabilitation period are shown in figure 1. 28% of patients had primary CRS plus adjuvant chemotherapy while 23% had NACT with interval CRS. 37% had chemotherapy alone, 3% had surgery only and 9% received the best supportive care.
Primary treatment modalities of patients included in the prehabilitation programme. CRS, cytoreductive surgery; NACT, neoadjuvant chemotherapy.
Adherence to prehabilitation
45 of the 75 patients enrolled (60%) completed the project. Reasons for discontinuation included early death (n=18), disease progression, symptom severity, appointment burden, travel time and patient choice.
Stage 4 patients were less likely to complete prehabilitation (50%) compared with stage 3 (63%).
One-third of patients declined referral to the Macmillan Move More scheme but were happy to accept advice on the HEP and pedometer use.
Outcome of interventions
Functional capacity
Of the 45 patients who completed prehabilitation improved 6MWT and 30-CST was observed in 67% and 44% respectively, while grip strength increased in only 31% (figure 2).
Functional status evaluation. 30-CTS, 30 s Chair to Stand test; 6MWT, 6 min Walk Test.
Psychological assessment
One-third of the 45 patients who completed prehabilitation reported moderate to extreme anxiety/depression scores (score≥3) at baseline assessment. 67% of these patients had lower scores (scores 1–2) at the completion of prehab.
Nutritional assessment
Just over half (53%) of patients who completed prehabilitation had medium to high-risk MUST scores at baseline assessment. In 71% of these patients, baseline weight was maintained or increased at the completion of prehabilitation. 24% of patients who completed prehabilitation had an increase in mid-arm circumference by the end of treatment; however. missing values in one-third of patients hinder the interpretation of this data.
Lessons and limitations
Discussion of outcome measures
Baseline assessments have confirmed the presence of frailty, reduced exercise capacity, risk of malnutrition and elevated stress levels in a considerable proportion of women prior to treatment for advanced ovarian cancer. This is in keeping with the current evidence available in relation to the baseline state and functional capacity of patients with advanced ovarian cancer.12 13 15
The lower-than-expected uptake of exercise referrals, particularly in the targeted pathway patients, provides insight into the acceptability of exercise intervention and motivation of patients with advanced ovarian cancer. This contradicts qualitative evidence from other studies which report a willingness to engage in exercise prehabilitation pathways.34 Barriers to engagement in the exercise pathway included significant fatigue, abdominal/pelvic pain, ascites and shortness of breath. In response to this, we modified our protocol to reoffer exercise referral at the mid-chemotherapy assessment to allow time for disease symptomatology to be reduced by chemotherapy. Further qualitative work should be undertaken in women with advanced ovarian cancer to assess the specific barriers to engagement in order to develop an acceptable exercise intervention.
40% of patients discontinued prehabilitation with reasons including disease progression, early death, disease symptomatology, appointment burden, travel time and patient choice. Preventable reasons for discontinuation such as appointment burden and travel time could possibly have been reduced by improved synchronisation of assessments with chemotherapy appointments.
Results from our post-treatment assessments of the patients completing prehabilitation (45/75) are encouraging as they demonstrate improved functional capacity, nutritional and psychological status in varying proportions of patients. These improvements, however, may be the result of disease control by chemotherapy/surgery so in the absence of a control group (no prehabilitation) the contribution of prehabilitation and treatment cannot be separately measured.
Successes
There were a lot of successes experienced throughout the project. Despite a very short time frame from project approval to commencement, we were able to successfully recruit staff, develop a standard operating procedure (SOP), identify a venue, develop the clinic, agree interventions and a pathway within 6 weeks of approval. This was due to support from senior management and the passion of the team members involved. Through good communication and regular meetings, we were able to get the support of the MDT and local units, without any resistance and embed prehabilitation into the MDT. The development of a bespoke prehabilitation database provided a central location for all patient data collected throughout the programme. Additionally, we secured support from the local councils throughout NI to access the Macmillan Move More Exercise Programme at no additional cost.
The clinic ran well throughout the year, and, despite staffing problems, we were able to identify cover and continue to provide the service for patients. Regular communication and the commitment of the staff involved were key. We worked collaboratively with our centres which were also introducing prehabilitation for ovarian cancer which provided the opportunity to share experiences and challenges of the different approaches. The pilot approach allowed us to test a model for prehabilitation, based on expert guidance, and subsequently bid to our commissioners for funding to extend this model following its success. A fully commissioned regional prehabilitation project is now active in NI for patients with advanced ovarian cancer. Therefore, this project provides excellent learning for collaborative working.
Challenges
We experienced challenges throughout the project and had to work closely together to make changes and overcome these. They are summarised below:
Tight deadline to establish project
There were difficulties early on with recruitment timelines, finding accommodation for the clinic and getting the relevant equipment. The project team had to work closely together, with support of senior management to overcome these.
Workforce planning
Three members of staff were recruited for the clinic, however, we did not plan for cover during periods of leave or sickness. There was a period of long-term sickness which put additional pressure on the existing team to provide cover and affected capacity at the clinic. For sustainability, we plan to recommend a move back to a prehabilitation model embedded within the service to address this issue.
Administrative support
There was no dedicated administrative support so we had to identify staff who could provide this in addition to their roles. Again, there were issues with sickness and no cross-cover when individuals were on leave. This meant the project lead nurse often had to pick up administrative tasks. We tried to identify additional cover during the project, but this was not always successful.
Data collection
A dataset was agreed early, but a number of changes needed to be made to the collection points and dataset due to difficulty getting access to the relevant information. For example, the removal of the presurgery assessment point from the prehabilitation database. This led to some missing data points in the final dataset
Patient experience
There were a number of patient experience factors which were raised throughout the project. As it was a regional clinic, some patients found the travel distance too long and preferred a virtual assessment. However, for the project evaluation, face-to-face appointments were required. We tried to ensure, where possible, that patients had their prehabilitation appointment on the same day as their surgical appointment. However, this meant that patients spent most of the day in hospital which was tiring for them. We were limited in what changes could be made during the pilot to address this, but in future, we plan to include virtual dietetic and physiotherapy appointments, where possible.
Project time
It would have been useful to have a dedicated project manager for the pilot, but this was not possible. To overcome this, the co-leads adopted this role in addition to their primary roles. Additional hours were also required for the project nurse which had not been accounted for in the original plan.
Completion of Electronic Holistic Needs Assessment concerns checklist
As part of the nursing assessment, the Electronic Holistic Needs Assessment checklist was emailed to patients for completion prior to the appointment. However, there were difficulties in completing this which often added significant time delays at the clinic appointment in order to complete this assessment. This meant that appointments were potentially longer than anticipated for some.
Conclusion
We feel that this project has achieved its principal aims and objectives. We have developed, set up and implemented a successful multimodal prehabilitation service for patients with advanced ovarian cancer within our MDT in NI. This was based on expert collaborative prehabilitation guidance,1 32 which provided an excellent framework to develop this service. This project has demonstrated the positive impact of embedding prehabilitation into the treatment pathway of women with advanced ovarian cancer with equity of access for all patients.
Further funding has been secured to continue prehabilitation programme for patients with advanced ovarian cancer. This was as a result of collaborative work with our commissioning colleagues early in the project which was flagged as a priority funding. This was achieved because prehabilitation is directly related to the objectives within the NI Cancer Strategy. We plan to alter the prehabilitation pathway to reduce the burden on patients to enable an earlier assessment and the development of a bespoke prehabilitation pathway which we feel will be more reproducible. In addition, the development of a patient portal will allow patients to communicate directly with prehabilitation team members via a mobile app. It is essential that investment is secured for specialist nursing, dietetics and physiotherapy for cancer services generally in order to enable wider spread of the prehabilitation model.
Contributors: JCM: data analysis and manuscript preparation, (guarantor). DL: research design, data acquisition, manuscript preparation. LR: research design, data acquisition, data analysis and interpretation, manuscript review, NG: research design, data acquisition, LM: research design, data acquisition, BM: research design, data acquisition, DO’H: research design, data acquisition, BN: research design, data acquisition, SD: research design, data acquisition, data interpretation, manuscript preparation and review, supervision.
Funding: Ovarian Cancer Action - IMPROVE-UK.
Competing interests: None declared.
Patient and public involvement: Patients and/or the public were involved in the design, or conduct, or reporting, or dissemination plans of this research. Refer to the Methods section for further details.
Provenance and peer review: Not commissioned; externally peer reviewed.
Supplemental material: This content has been supplied by the author(s). It has not been vetted by BMJ Publishing Group Limited (BMJ) and may not have been peer-reviewed. Any opinions or recommendations discussed are solely those of the author(s) and are not endorsed by BMJ. BMJ disclaims all liability and responsibility arising from any reliance placed on the content. Where the content includes any translated material, BMJ does not warrant the accuracy and reliability of the translations (including but not limited to local regulations, clinical guidelines, terminology, drug names and drug dosages), and is not responsible for any error and/or omissions arising from translation and adaptation or otherwise.
Data availability statement
All data relevant to the study are included in the article or uploaded as supplementary information.
Ethics statements
Patient consent for publication:
Not applicable.
Acknowledgements
Patients involved in the programme. Ovarian Cancer Action funding. IMPROVE-UK Prehabilitation Collaborative.
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