Patients’ and Oncologists’ Perspectives On A Novel Clinician Led Fear of Cancer Recurrence (CIFeR) Intervention

Purpose Despite strong demand from breast cancer survivors, there is a dearth of exibly delivered, accessible psychological interventions addressing fear of cancer recurrence (FCR). This study aimed to explore patients’ and clinicians’ perspectives concerning the experience, utility and barriers to a novel clinician-led FCR intervention (CIFeR). Methods Results


Introduction
Breast cancer prognosis has substantially improved in recent decades, yet survivors are often left with a range of unaddressed physical and psychological sequelae, including fear of cancer recurrence (FCR) [1]. FCR, the "fear, worry, or concern relating to the possibility that cancer will come back or progress," [2], is one of the most prevalent and severe unmet needs reported by cancer survivors globally [1,[3][4]. Fifty to 70% of breast cancer survivors report moderate to severe FCR, while 7-10% report severe and disabling FCR [1,3] manifesting as: 1) constant and intrusive thoughts about cancer, 2) avoidant or hypervigilant behaviours (e.g. excessive symptom monitoring, missing follow-up appointments) and 3) an inability to plan for the future [4]. This characteristic combination of preoccupation, worry and hypervigilance can maintain and intensify over time, detrimentally impacting survivors' quality of life and burdening medical and psycho-oncological resources in the health system [1,[5][6].
Recently, psychological therapies addressing FCR have shown small, yet sustained effects in abating modi able symptoms (e.g. perceived risk, self-e cacy, help-seeking) [7][8]. However, these existing interventions are often resource-intensive, psychologist or nurse-delivered and inaccessible to many breast cancer survivors [9]. Oncologists -as medical experts with sustained, long-term, caring relationships with patients -are uniquely positioned to detect and manage FCR. Yet a systematic review examining existing FCR interventions identi ed no doctor-led FCR interventions, with clinicians surveyed in the literature expressing discomfort in managing FCR and desire for further training [9].
To address this gap, we designed the Clinician Intervention to address FCR (CIFeR) as one component in a stepped care intervention model. By matching patients' needs to correspondingly resource-intensive interventions (i.e. low need patients can utilise self-help internet services, low to medium need patients can receive CIFeR, those with high need can receive specialist referrals), stepped care models simplify the delivery of effective interventions [10] with randomised controlled studies indicating their value in reducing health care system burdens [11,12]. The CIFeR intervention entailed: 1) Normalising FCR -as a valid and common phenomenon within survivorship 2) Providing concrete prognostic information tailored to patients' needs and preferences 3) Take-home education sheet: red-ag recurrence symptoms 4) Take-home Information sheet: simple psychological strategies to manage FCR-related worry and links to online resources.

5) Psychological referral (if appropriate)
Recently, the CIFeR single-arm Phase I-II study demonstrated that oncologists could deliver CIFeR in eightminutes at a follow up consultation; CIFeR was acceptable, feasible and reduced FCR severity 3-months post-intervention [13][14]. The current qualitative sub-study complements the quantitative CIFeR data, by exploring patients' and clinicians' experiences of receiving and delivering the CIFER intervention. It aims to examine the perceived utility of individual CIFeR components and clinical barriers to widespread adoption of CIFeR in routine cancer care. Given this is an exploratory study, no a priori hypotheses regarding patient and clinician perspectives on CIFeR were prepared.

Measures
Patients participated in a single semi-structured phone interview (see Table 4), exploring their experience of the overall intervention, speci c intervention components, and views on how CIFeR could best be delivered to survivors in routine care. Oncologists completed a 16-item online survey (with Likert scale and open-ended questions) which explored barriers and facilitators to integrating CIFeR into clinical practice (see Supplementary le).

Procedure
A convenience sample of CIFeR participants, who at the time of the main study consented to this qualitative sub-study, were approached via telephone 1-3 months post-intervention, to participate in a 30minute telephone interview, at any private, convenient location with a trained female qualitative research assistant (AS). Participants had no prior relationship or knowledge of research assistant and their motivations for involvement in this study. Recruitment continued, with eld notes recorded during the interviews until saturation of themes was achieved at twenty participants. All ve participating oncologists were emailed a brief Redcap survey at the conclusion of patient recruitment (6 months postinitial recruitment). Ethical approval was obtained and all participants provided written informed consent to participate.

Data analysis
Patient interviews were audio-recorded, transcribed verbatim (not returned to participants for comment), and analysed using six phases of thematic analysis, 1) data familiarisation, 2) initial coding and inferences, 3) code combination into overarching themes, 4) examination of coherence with theoretical perspective, 5) theme description and de nition, 6) checking for meaningful themes, validity and reliability across coders and participants (e.g. 'member checking') [17]. Two reviewers followed this iterative data-driven approach, double coding 30% of the interviews to ensure consistency and quality (discrepancies resolved through discussion) across two rounds of coding [18], stored in Microsoft word and Excel les. Data were then compared for those with clinically signi cant (de ned as total FCRI score ≥13) [15] versus subclinical FCR (total FCRI [15] score ≤13). Qualitative analyses were pre-planned and

Results
Twenty of 61 breast cancer survivors participating in CIFeR and all ve oncologists were recruited to the qualitative sub-study, with no attrition recorded. Independent t-tests and chi-squared testing indicated no differences between survivor interview participants and remaining CIFeR participants on age, years since diagnosis, education level or marital status (see Table 1).

Demographics
Survivors on average were 59.8 years old, with 12 women (60%) university educated and nine (45%) born outside of Australia (see Table 1). All participating oncologists were female, currently working at two large urban hospitals, on average 44.6 years old (SD = 9.4 years) 1 with 13.8 years (SD = 9.4 years) of oncology experience.
Almost all patients interviewed (n = 19/20) would recommend the CIFeR intervention to others, except one participant who felt that patients should not require any peer-recommendation to raise FCR with their oncologist. Two overarching themes (content and context) emerged in patient accounts (see Table 2 for additional quotes).
A. Intervention content Human, holistic intervention All patients found the 'human element' across the ve-component CIFeR intervention holistically addressed their needs and unique person-hoods, by reinforcing continuity of care and support across their cancer journey. CIFeR strengthened participants' relationship with their oncologist: "I left feeling quite positive, I felt she was very open with me...when you are looking for establishing a professional relationship, I look for the openness and candidness, the feeling there is some form of mutual respect to who I am as an individual" (ID 154, High FCR) while retaining the opportunity for specialist involvement (clinical psycho-oncologist or counsellor). In addition, CIFeR provided reassurance, permission and space for patients to explore their fears around FCR and other mental health concerns, with one patient stating "The list of things people want to talk about could be small but knowing it doesn't bother them [doctors] to discuss it is very helpful" (PID 49, High FCR).
The initial normalisation component also provided the acknowledgement, permission and safety required for women to begin discussing and clarifying misinformation contributing to FCR. Even women with low FCR severity scores pre-intervention perceived value in CIFeR, stating "Absolutely, I recommend that doctors talk about this to their patients. There are a huge number of patients who have quite signi cant fears around it. I actually think that everyone going through this should be screening, it should be a standard." (PID125, Low FCR).
Patients' self-e cacy and con dence in managing their FCR All patients felt CIFeR afforded them opportunities to address concrete aspects of survivorship (i.e. tailored, prognostic information), with most feeling con dent enough to self-monitor and manage their FCR as a result: "I cut down on the crazy google searching. I realised I could get my stats, speci cally, my risk, my grade, I walked away with my own stats and just to see that 1% on the paper, that was helpful. Personalised stats were really helpful. Google is way too generic. Tangible quantitative information. That was amazing, my Dr is amazing." (PID168, High FCR).
Most surveyed patients (n = 16) kept the take-home information sheets on red-ag recurrence symptoms and strategies to manage FCR, despite nine patients indicating prior use and familiarity with worry management and coping strategies detailed in CIFeR. These included reframing survivorship as a "second chance at life," help-seeking (i.e. talking to family, friends) (PID138, clinically signi cant FCR), and distraction through absorbing activities like puzzles (PID87, low FCR) or pilates (PID242, low FCR). Patients nonetheless valued the spectrum of cognitive, emotional and behavioural coping approaches in CIFeR nding it "helpful because she [oncologist] …told me not to dwell on it and let it take over.... If it comes into mind, I learnt to get active, get out in garden. I used to think about it a couple of times a month; now once a month or less, so it has helped me a lot." PID50, High FCR.
Finally, most interviewed patients appreciated yet declined psychological referrals, often noting su cient external support sources (i.e. friends, family, GPs) and beliefs that others with worse prognoses would more greatly bene t from specialist psycho-oncology services. The two patients who accepted referrals to psycho-oncology services indicated an inability to anticipate and buffer the impact of FCR on their daily lives, and poor pre-existing social supports. These patients felt exploring their FCR beyond the scope of CIFeR, normalised help-seeking, forti ed their trust in their oncologist, and bolstered their own con dence and competence in coping: "it prompted me to get help. I didn't choose the same person, but just the idea of being told to see someone was planted, it's ok to need someone. Going to therapy was one of the best things I've done." (PID168, High FCR).

B. Context of CIFeR intervention delivery
Many patients felt contextual factors (i.e. timing, integration with standard care) facilitated their engagement with the CIFeR intervention. Whilst timing preferences varied, most participants agreed that delivering CIFeR immediately to six months post-treatment was most bene cial because it coincided with emerging needs to cope with isolation and vulnerability due to transitioning to survivorship (i.e. reduced daily access to services and their treating oncology team) and life events (i.e. death in family or friends). Furthermore, patients felt that delivery at a routine follow-up consultation increased feasibility both for themselves and the health system, stating "Less worry, no negatives it's a good intervention point, everything is almost done and dusted, maybe the doctor could spend another 5 or 10 with me and it's a time she was seeing me anyway, it's not going to cost the system that much more and it will probably save other resources" (PID135, High FCR).
Oncologists' perspectives on CIFeR Practical bene ts and ease of integrating CIFeR intervention All ve participating clinicians perceived CIFeR as fast and moderately to very useful and helpful. Clinicians' perceived the delivery of CIFeR to take 0 -5 mins (n = 2) to 6 -10 minutes (n = 3), which matched objective measures indicating CIFeR delivery took 8 minutes on average. 14 All clinicians indicated they had used CIFeR with patients outside the study and would very likely continue using it in future: "Some women were reporting FCR many years later, and discussion was bene cial. Reminds us of the importance of discussing this topic with every patient during recovery from their treatment phase." (CID 242).

Usefulness of speci c CIFeR components
Participating oncologists named the most useful components of CiFeR as: normalisation (n = 5), provision of prognostic information (n = 3), the take home information sheet (n = 3), information distinguishing recurrence from other symptoms (n = 2) and referral to a psycho-oncology service (n = 1). Speci cally, all clinicians found utility in normalising FCR and discussing prognostic information, especially for highly anxious women, as: "something that is so obvious that we don't talk about it but it is so easy to say and I think has a huge impact for the patient knowing it is normal" (CID128).
After these frank discussions, oncologists noted most patients appeared signi cantly less anxious, with three oncologists stating the take-home sheets helped patients comfortably disclose their issues around FCR and seek help in their own time rather than seeking professional psycho-oncology referral. One clinician also stated that CIFeR introduced consistency by routinely reminding survivors about prognosis, as "some patients forget they've had chats about prognosis. Hence some believe that their risk of recurrence is much higher than it really is." (CID270) and that this reduced survivors' anxiety in later conversations about their risk of developing recurrence of their breast cancer.

Challenges and barriers to implementing CIFeR
Most clinicians perceived prognosis (n = 4) and psychological issues (n= 1) as the most challenging (albeit useful) components of CIFeR to discuss with patients. Some clinicians noted their own discomfort in discussing prognosis as "If a patient had a high-risk cancer it can be tricky/scary telling them when you are not sure if they have understood their prognosis since diagnosis" (CID128). Others noted di culties around estimating absolute risk, patients refusing survival statistics after treatment and in convincing patients to accept counselling referrals.
Suggested barriers to using CIFeR in routine care included time limitations, and language and cultural issues in delivering CIFeR to non-English speaking survivors, whilst two oncologists reported no barriers and high survivor interest and acceptance. Only two changes were suggested to improve the intervention -providing oncologists with a 'tick box' list of topics to address, and screening patients to assess their needs around FCR. Barriers aside, all ve clinicians were enthusiastic about routine use of CIFeR, stating it addressed an important survivor need, through a clear, simple and consistent structure. Oncologists also suggested offering CIFeR at the time of treatment completion or endocrine tolerability review and involving registrars in its delivery. 1 One clinician participant did not specify their exact age or years in oncology, replying they were in their "late 40s" and spent "15 to 20 years" in the profession. In order to proceed with analyses, the missing data were substituted with the mean values for age (47 years, between 45 -50 years) and years of experience (17 years, between 15-20 years) within the boundaries speci ed by the participant, per Salkind [16]. No other missing data was recorded.

Discussion
As FCR continues to impact an expanding survivorship population [4], patients and clinicians will likely bene t from incorporating stepped, FCR interventions into routine clinical oncology practice [9][10][11][12]. Whilst a few FCR-targeted supportive care interventions delivered by non-psychosocial staff have shown feasibility in clinic, they are typically nurse-led and resource intensive [9]. This CIFeR intervention aimed to provide a novel, e cacious and e cient clinical pathway to addressing FCR with inherently low resource costs (i.e. low clinical time dedicated to intervention delivery, training and implementation costs, psychooncologist referral load). This qualitative sub-study unpacked patients' and clinicians' experiences, respectively, of receiving and delivering the CIFeR intervention.
Both patients (across the FCR spectrum) and clinicians found CIFeR enhanced their clinical follow-up experience in a clear, structured and empathetic manner. Patients, especially those with clinically signi cant FCR, highly valued three CIFeR components: normalising FCR, re-iterating prognostic information and clarifying recurrence symptoms. These were reported to engender a warm, compassionate space in which to raise fears, correct misunderstandings about recurrence risks, and increase patients' self-e cacy in managing physical symptoms (i.e. distinguishing normal aging pains from recurrence symptoms). Furthermore, many patients interviewed reported greater engagement in their own FCR management and a reduced need for specialist psychological services to treat their FCR, as a result of CIFeR. Whilst interviews revealed reticence to accept referrals (due to patients feeling adequately supported), those who took up referrals felt supported by their oncologist and found therapy a worthwhile experience.
Importantly, patients perceived CIFeR as person-centric: strongly appreciating their clinician's 'whole person' approach, which valued their mental and physical health. This value patients placed in holistic care is consistent with ndings of a recent systematic review of 29 primarily qualitative studies examining patients' needs, values and preferences in oncology care [19]. Review ndings noted successful patient-centered care prioritised supporting patient values (autonomy, sincerity and hope) and exibility in coordinating care and accommodating preferences for information delivery and shared decision-making [19][20][21], much of which is featured in CIFeR.
Participating oncologists reported that CIFeR provided a structured, stepped approach to identifying and managing FCR. Four of the ve surveyed oncologists found FCR management to be challenging, which is comparable to other surveys of oncology clinicians, suggesting up to 96% of oncologists associate some level of challenge with FCR management [22][23]. Thewes et al [22], for example, indicated the majority of clinicians surveyed viewed managing FCR as somewhat (52.7%) to moderately (32.4%) challenging with all study participants (oncologists and other health professionals) interested in further FCR management training. Thus, CIFeR appears to be meeting a currently unaddressed need for oncologist education on this topic. Practical ways to potentially further increase the utility of CIFeR include, introducing routine FCR screening in clinic (as suggested by participating oncologists) and incorporating a checklist of CIFeR steps for oncologists.
Both patients and clinicians ideally felt delivering CIFeR at treatment end during follow-up could consolidate patients' understanding of prognosis, and help them self-manage detecting signs of recurrence and emotional responses. Importantly, patients also observed that delivering CIFeR during a routine consultation may improve uptake without utilising other resources unnecessarily (i.e. psychooncologists, breast care nurses, patient travel time), highlighting an important sustainability feature of the intervention. Schell et al. [24] demonstrates potential intervention bene ts are closely related to sustainability. Delivering CIFeR via current, trusted staff, within an existing consultation, could likely provide a cost-effective and sustainable approach for oncologists to address FCR.
Study ndings, however, must be considered in light of limitations. This sample was largely homogenous, with predominantly Caucasian married women over 50 years of age, limiting cross-cultural generalisability of ndings. A core study design strength involved using semi-structured interviews to facilitate in-depth comparison and contrast of stakeholder (clinician and patient) perspectives, yet wider interest in CIFeR uptake remains unclear.

Conclusion
This study suggests that an oncologist-delivered FCR intervention can provide an important stepped care model to reduce referral loads for psycho-oncology services. Oncologists, as experts in evidence-based medicine, can uniquely help reduce patients' FCR through tailoring prognostic and potential recurrence symptom information to suit patient preferences and clinical circumstances. Furthermore, delivering CIFeR can consolidate the doctor-patient relationship, and increase patients' likelihood of engaging in FCR management by reinforcing perceptions they are at the center of care provision. CIFeR appears to address a signi cant unmet educational need amongst oncologists, through its brief, evidence-based model for managing and ameliorating FCR symptoms. The strong qualitative support for integrating CIFeR into routine care shown by patients and clinicians alike will provide a foundation for a future implementation study.

Declarations Funding
The Avant Foundation and Sydney Breast Cancer Foundation funded this study.

Con icts of interest/Competing interests
The authors have no relevant nancial or non-nancial interests to disclose.
Availability of data and material (data transparency) Data is available in de-identi ed form as an excel spreadsheet on OSF under the link: https://osf.io/s9djt/ les/ Human Ethics committee prior to study commencement. All study phases (i.e. data collection, analysis and presentation) were conducted in adherence with these ethical standards around data protection, con dentiality and privacy.

Consent to participate and Consent for publication
All participants provided fully informed consent to participate in this study and for their data to be published in aggregate (de-identi ed) format. Note: SD = standard deviation, N = total number of patients, n = number of patients per sub-group, % = total percentage per group Table 2 Summary of emergent themes from patient perspectives on CIFeR Yes, just to know that somebody was interested in look beyond the base medical cancer, the whole person approach. I suppose the positive is you're recognised as a person, but somebody with a strictly medical diagnosis of cancer, the treatment is about making sure you're well in a whole manner, that to me ts my way of thinking. To know that the team you're working with, you yourself in their hands, understand there's more to than then slice and dice and treat. I had a problem with my surgeon in my local area, he had that approach. It didn't suit, the approach of the [Hospital] team was much more holistic which I think is very important and this study is just another part of that whole-PID163  • Concerns around interpretation of prognostic information

Tables
• Importance of informed consent, perceived patients to be fearful or uninterested in statistics -in contrast to patients interviewed • Requested checklist and further simpli cation before integrated into clinic Table 4 Guiding Semi-structured interview framework for patient interviews Per table below, the interviewer utilised exibly structured open questions discussing patients' impacts and experiences of CIFeR on their fear of cancer recurrence (FCR). This approach enabled patients to guide the depth and nature of their study experiences.