Patient experiences of the urgent cancer referral pathway—Can the NHS do better? Semi‐structured interviews with patients with upper gastrointestinal cancer

Abstract Background Timeliness is viewed as a key feature of health‐care quality. Internationally, this is challenging. In England, cancer waiting time targets are currently not being met. For example, between 2015 and 2018 only 71% of patients with upper gastrointestinal (UGI) cancer started treatment within the recommended 62 days of referral. Objective We explored patients’ experiences to identify areas for service improvement. Design Semi‐structured interviews were conducted. Setting and participants Twenty patients who were referred through the urgent (two‐week) GP referral route and were within six months of receiving first treatment were recruited. Data analysis Data from the interviews were analysed thematically. Results Four themes were developed: organization of care; diagnosis; support; and views and expectations of the NHS. Patients described cross‐cutting issues such as complex and varied pathways and uncertainty about what would happen next. They felt daunted by the intensity and speed of investigations. They were presented with a recommended course of action rather than options and had little involvement in decision making. They were grateful for care, reluctant to complain and resigned to the status quo. Discussion and conclusions In order to meet patient needs, the NHS needs to improve communication and streamline pathways. Future cancer pathways also need to be designed to support shared decision making, be truly person‐centred and informed by patient experience.


| BACKG ROU N D
Survival rates have improved for many cancers 1 but remain lower in England than in other developed countries. [2][3][4][5] Late diagnosis and sub-optimal access to treatment have been identified as significant drivers of poorer outcomes. [6][7][8][9][10][11] These findings have encouraged reforms, such as the NHS cancer plan in 2000 12 that patients in England with symptoms suggestive of suspected cancer should wait no longer than two weeks from urgent GP referral for a specialist appointment and no longer than 62 days from referral to starting treatment, an initiative introduced to reduce waiting times for diagnosis and treatment, minimize psychological distress and save lives. 13 There is evidence associating this pathway with shorter times to diagnosis and treatment 14 ; however, it remains uncertain whether this improves survival. 13,[15][16][17][18][19][20][21] A recent study identified a greater propensity to use referrals for suspected cancer was associated with lower mortality for all cancers combined and for the most common types of cancer. 22 This supports suggestions that increased primary care use of urgent suspected cancer referrals and associated diagnostic testing may reduce latestage diagnoses and mortality of patients with cancer. 23,24 There is considerable focus on this pathway (and associated cancer targets) from a policy perspective, and almost 40% of cancer patients in England are diagnosed through this route. 25 However, the study by Round et al (2020) 22 focused on primary care and GP referrals for suspected cancer but acknowledged the potential for variation once patients are referred, including in the clinical practice of individual specialists, treatments offered and in the wider health-care system 26 that are important to consider. 27 Therefore, there is a need to investigate patient experience of the urgent (two-week wait) pathway to examine progression through the pathway in greater detail.
Studies suggest there can be similarities in patient experience across cancers. 28 Whilst we can learn from other types of cancer pathways, the contrasting accounts of pathways described in previous studies also illustrate the diversity in patient experience 29 and the need to investigate the specific details within a pathway.
Existing qualitative research into patient experience of the upper GI cancer referral pathway is minimal. [30][31][32] Generally, research into patient experience often highlights patient-related factors. In contrast, factors related to potential improvements that could be made within the health-care system remain relatively under investigated. 33 Therefore, there is an imperative to investigate the specific patient experience for upper GI cancer patients in the UK.
Patients with upper gastrointestinal (UGI) cancer have some of the poorest outcomes and longest intervals between referral and commencement of treatment amongst all cancers in England. 34 In 2018, only 71% of patients with a UGI cancer diagnosis in England had started treatment within the recommended 62 days of referral. 34 A more efficient pathway could reduce delays, and the considerable variation that currently exists, hence improving equity and, given timeliness is a key feature of high-quality health care, could improve quality of care and, by implication, increase chances of meeting cancer targets. 35 One approach to system transformation is to engage patients throughout pathway redesign and implementation to ensure that changes benefit patients in terms of clinical outcomes and experiences of care. 34 Evidence shows that people have better experiences and improved health and well-being if their care is personalized and they can actively shape their care and support. 36,37 Despite evidence supporting the effectiveness of person-centred care, patient surveys over the past decade have consistently shown that person-centred care has not been implemented 'at scale' and is difficult to do. 38,39 Recently, the NHS Long Term Plan 37 has stated that the roll out of the NHS Comprehensive Model for Personalised Care 40 means patients will get more control over their own health and more personalized care when they need it.
Despite policy rhetoric on the importance of person-centred care in care pathway development, research on UGI cancer patient experience within the referral pathway remains limited [30][31][32] and factors related to potential improvements that could be made within the health-care system remain under-investigated. 33 The current study therefore aimed to explore patients' experiences of the NHS UGI urgent cancer care pathway to identify potential areas of service improvement.

| Methodological approach
Qualitative semi-structured telephone interviews were conducted.
The study was carried out in accordance with the consolidated criteria for reporting qualitative research (COREQ) 41 (COREQ checklist included within supporting information S1) and guidance on standards for reporting qualitative research findings. 42

| Participant Recruitment
Patients were eligible if they had initially been referred through the urgent (two-week wait) GP referral route in the North East and whether they still wished to take part in the study and, if so, to arrange an interview at a time convenient to them. Written informed consent was given by each participant before the interview was conducted. Patients were informed that they could withdraw at any time and that this would not affect their care. For confidentiality reasons, the care team (CNSs) were not informed as to whether the patient took part in the study. All participants were given a unique participant number, which allowed results to be anonymous. Patients were informed that anonymous, direct quotes could be used in published materials. The protocol stated that, if a patient became distressed the researcher would stop the interview, allow the patient some time, and then discuss with them whether/how they would wish to proceed; this did not occur. The patients were also advised to contact their cancer nurse specialists if participating in the study had raised by questions about their cancer care.

| Ethical approval
The study was classified as service evaluation by NHS HRA and re-

| Data collection
All interviews (except one, which was face-to-face at the interviewee's request) were conducted by one researcher (AH) via telephone, audio-recorded and transcribed verbatim. Interviews ranged between 20 and 60 minutes. Telephone interviews are an efficient way to collect data. In addition, they can improve participation of more marginalized groups, ease any participant discomfort, and the perception of greater anonymity can lead to greater disclosure. 47 They were supported by a topic guide (informed by a rapid literature review) (supporting information S2). The areas covered by the topic guide included seeking medical advice, the diagnostic process, information provision and treatment options. The topic guide was used flexibly, to let patients describe their experience in a way that was natural to them, and evolved as recruitment progressed, to enable emerging issues to be explored.
The researcher collecting data was a female health psychologist, PhD, with no role in the care of patients. She has training and previous experience in qualitative methods, particularly interviewing.

| Data analysis
Thematic analysis was used to analyse the data. A social constructionism/relativist, semantic and descriptive approach was used.
Inductive coding allowed themes to emerge from the data without prior categorization. 48 Thematic analysis was undertaken in parallel with data collection and used alongside field notes, so that the content of early interviews informed later ones, thus ensuring sufficient depth and that data saturation was reached. 49 Data saturation was defined using the principle outlined by Francis et al (2009) 50 'Stopping criterion -After 10 interviews, when three further interviews have been conducted with no new themes emerging, we will define this as the point of data saturation'. (P1234).
NVivo version 11 software was used to support coding and analysis. 51 One researcher (AH) coded all interview transcripts, with 20% (n = 4) independently coded by a second researcher (SS). The coding framework (supporting information S3) was then discussed, agreed within the full research team and applied to the remainder of the interview transcripts. Illustrative quotes have been provided to supplement narrative descriptions of the findings.
After development of the themes, the findings were interpreted by the researchers to provide recommendations for future service improvement (Appendix 1).

| RE SULTS
Twenty-seven patients were referred to the research team; four declined and three could not be contacted. Twenty patients (74% of referrals) were interviewed. All interviewees were white British, with 19 men and one woman. The mean age was 66 years (range 48-77).
Four themes were developed: organization of care; diagnosis; support; and views and expectations of the NHS. The themes included negative and positive aspects of care.

| Theme 1: Organization of care
Patients described complex and varied pathways. They were uncertain about what would happen next or how long things would take.
Particular issues related to immediate access to testing (endoscopy) versus specialist referral, referral across numerous hospital sites and expectations/communication of waiting times.
Most patients were offered immediate access to testing, but others required a specialist appointment first, which was unexpected.
'I thought I would then receive an appointment to go straight to the endoscopy department. I didn't, I received a letter saying that I had an appointment with a consultant gastroenterologist…the consultant said that she is the one that decides whether I need an endoscopy, not the GP'.

(Participant 14)
A few patients described short and simple pathways. Others had long and complex pathways, attending multiple appointments in multiple hospitals, often considerable distances apart. On average, patients had eight health-care appointments (range 4 -12) from referral to diagnosis. On average, they visited four different hospital sites (range 3 -6) from referral to initial treatment. It was unclear to patients why there were so many visits.
'Trying to keep track of where you're supposed to be and when… I mean, it's the time span in between your appointments. There was a two-week time span, for example, where each of those two weeks I was in three different hospitals. One visit involving overnight stay'. 'I did turn around to him and I did say, "Look, Mr [NAME], it's April now, this cancer has been growing inside me since January. It was diagnosed in February.
We are now into April, and still nobody has done anything to try and knock the cancer back?"' (Participant 14)

| Theme 2: Diagnosis
Patients described how processes and communication around diagnosis caused difficulties. Particular issues related to appropriate delivery of results, prior expectations of the purpose of visits, lack of clarity on timescales, communication and information personalized to patient needs.
Patients spoke about professionals using a range of terms, including cancer, biomass, lesion and tumour, when communicating the initial diagnosis. Several patients said they never heard the word cancer.
'Yes, after the endoscopy, the sister told me there was a lesion in the oesophagus'.
(Participant 9) Others described how their cancer diagnosis was explained through detailed understandable information.
'…everything was put in layman's terms so that I could understand. But the way it was put, and it was put to my wife as well, because she was there, it was exactly what I wanted it to be'. Patients contrasted the 'urgency' suggested by the requirements placed upon them (and therefore often upon family and friends) to attend numerous appointments, at short notice, in close succession, often across multiple hospital sites, with the seemingly long time taken to receive results, and the unsettling time spent waiting and 'not knowing' the results and prognosis.
'There seems to be an eight to ten day period for any test results to come back. I thought, hang on a second.

| Theme 4: Views and expectations of the NHS
Patients often thought that their personal experience was common practice and they were getting the same as everyone else. This was often a barrier to them suggesting potential improvements for the pathway as they were resigned to the status quo. Patients described feeling grateful for the NHS and felt that staff were time-pressured but working in their best interests. They spoke about not wanting to be seen as 'complaining' and were reluctant to express concerns about health-care professionals during the interviews. The interview findings allowed a range of cross-cutting issues to surface from our themes. All findings (including these cross-cutting issues) were used to inform the researchers' recommendations for future service improvement (Appendix 1).

| Statement of principal findings
Timeliness of care is an international challenge. Achieving cancerwaiting targets within the NHS is one example of this. A further challenge is delivering more patient-centred care and the inherent conflict between these two NHS policies. Furthermore, an uncompromising focus on pathway expediency may in some cases be detrimental to patient experience of care; for example patients may need time to make important treatment decisions. This study exposed wide variations in the lived experience of the UGI cancer pathway.
Whilst several patients reported short and simple pathways, most

| Strengths and limitations of the study
A patient representative was included in the steering group to ensure all patient-facing materials (eg information sheet) and the interview topic guide made sense, was sensitive and appropriate to context. Patients were interviewed within six months of their first treatment, thus ensuring that their recall of the events was likely to be reasonably fresh. They lived in different parts of the region, ranged from 48 to 77 years and had had a variety of treatments.
They also varied with respect to the number of hospitals they had visited (ranging from 3 to 6) and the number of appointments they had received during their care (ranging from 4 to 13).
The independence of the researcher to the patient's clinical care setting was also a strength as it provided assurance, alongside steps taken to preserve participant anonymity that any remarks made would not impact on the care the person subsequently received, thereby enabling participants to feel they could speak freely without judgement.
One limitation was the lack of female participants interviewed.
UGI cancer is more often diagnosed in males (two thirds), but the proportion is still lower than expected and may have impacted on

| Comparison to previous research
Organization of care within the present study suggested efficient communication between primary and secondary care was vital.
A potential contributor to patient delays identified in previous research is waiting to have appointments with specialist doctors or for specialist tests. 33,[53][54][55][56][57] In this study, a pathway variation was apparent, with some patients gaining direct access to testing, whilst others were surprised by initial specialist appointments before being sent for tests. This has also been identified in an endoscopy patient experience study 58 and highlights a potential area for improvement, as previous literature has identified that a straight-to-test protocol results in a reduction in times to cancer diagnosis and cancer treatment. 59,60 In addition, GP direct access testing performed as well as, and on some measures better than, consultant-triaged testing on measures of disease detection, appropriateness of referrals, interval from referral to testing, and patient and GP satisfaction. 61 At the referral stage, whilst health-care professionals may not want to create unnecessary anxiety for patients, previous research suggests fear can actually be increased if the patient feels unclear or unprepared for the cancer referral pathway. 62,63 Patients in a previous head and neck cancer study reported that health-care professionals rarely used the word 'cancer'. 64 Our study also identified several patients were never diagnosed using the word cancer, often leaving hospital unsure about their diagnosis and what to expect next in their care. This study revealed that even simple communication, such as each clinician introducing themselves or clinicians involving family and friends who were present, could affect the patient's experience when they are amidst a frantic appointment schedule. This links to previous research which suggested training for staff who have to break bad news to patients. 55 In a complex area such as UGI cancer, where symptoms are often unspecific and pathways variable, clarity, accuracy and honesty of information communication are critical.
Continuity of care was identified in previous literature as important to patients; however, this differed depending on where patients lived and what they were accustomed to. 53 Continuity of care was seen to be important for knowing who to contact if they were unsure about their care and also in terms of trusting decisions about their treatment. 31,32,53,[55][56][57] The current study confirmed this, with patients describing the importance of being assigned a clinical nurse specialist. However, continuity of care was difficult with other health-care professionals, as patients were often referred to numerous hospitals along the pathway.
Delays have been attributed to symptom investigation and the primary-secondary interface. 65 Previous studies revealed the key factors that patients perceived as impacting on their diagnosis were in the investigation stage. 33,[53][54][55][56][57]66 This study provides further insight into how diagnostic delay is complex and multifaceted, with patient pathways varying in relation to the number of hospitals they visited, appointments they attended and waiting times for test results. The current pathway is embedded in the concept of it being important to diagnose and treat cancer quickly, even though the clinical evidence shows uncertainty whether those who are treated more quickly have better survival. [15][16][17][18][19][20][21] The urgent referral pathway is giving a message to patients that rapid referral is important. Indeed, within this study, the fact they had been urgently referred established, for patients, the belief that it is important to act quickly to treat cancer. However, patients felt they were provided with a mixed message when the pathway would suddenly slow down and they were left waiting for tests, heightening anxiety rather than reducing it.
Guidance recommends that patients are involved in the decision-making process, 37,67,68 with services responding to what matters to the individual, empowering patients to be involved in choices about options for their care. 69,70 Patients from other cancer pathways have previously described having minimal involvement in decision making with regard to their care 53,62,71 and there is a particular challenge with multidisciplinary team decision making. 72 The present study supports this previous research, with patients stating that they were presented with treatment recommendations rather than options, with little evidence of involvement in decision making. In a recent National Cancer Patient Experience Survey, 21% of all cancer patients said they wanted more involvement in decisions about their care and treatment, with only 35% stating they were given a care plan. 73 Having an incongruent treatment decision-making experience has been associated with lower health-related-quality-of-life (HRQoL) among survivors.
These previous findings suggest that involving patients in treatment decisions to the degree to which they want to be involved may help improve cancer survivors' HRQoL. 74 This illustrates the further need for pathways to consider how patients are supported so they are involved in decision making. It has been acknowledged that the NHS also needs a more fundamental shift in how it works alongside patients and individuals to deliver more person-centred care. 70 Creating genuine partnerships requires professionals to work differently, as well as a systematic approach to engaging patients in decisions about their health and well-being. 37 The media portray the NHS as in crisis, with hospital specialities usually illustrated as under pressure. 75 Patients within this current study perceived health-care professionals to be time-pressured but working in their best interests. As a result, patients were often reluctant to comment on their care, criticize, complain or provide negative feedback, as they believed staff were doing the best they could in the circumstances. However, patients' gratitude for the NHS, stoic acceptance of the status quo and reluctance to suggest improvements should not be seen as justification for maintaining the status quo, which will fail to produce the transformations required within health care, 76 including achieving cancer waiting time targets and ensuring person-centred care throughout the pathways.
The value of this study is in shedding light on the urgent (twoweek wait) pathway, identifying the specific variation once patients are referred, including in the clinical practice of individual specialists, treatments offered, and in the wider health-care system, 26 information that was previously stated as lacking and acknowledged as important to consider. 27

| Recommendations for research
Within this paper there has not been the opportunity to report every detail of the interview findings. The primary purpose was to explore experiences and therefore issues like decision making are worthy of further detailed exploration and are identified as an area for further research. Further research into the experience of UGI patients throughout their cancer care pathway would be useful within other health-care systems which have undergone system transformation, such as the Danish model, 77 to attempt to reduce waiting times and/ or improve patient experience and outcomes. There is increasing emphasis on the use of co-production/co-design within the NHS and there is strong importance placed on including patient voice within service improvements. 68 This has been highlighted as an challenging area and demonstrates how further work is needed to shift the balance of power and to give patients agency to realize that raising quality improvement points will lead to action to improve services not only for themselves but for others. 68,70 Therefore, future research investigating how co-design, with both health-care professionals and patients, could be effectively incorporated within the cancer care pathways is vital.

| CON CLUS ION
In order to meet patient needs, the NHS needs to improve communication and streamline pathways. Future cancer pathways also need to be designed to support shared decision making, be truly personcentred and informed by patient experience.

ACK N OWLED G EM ENTS
We thank all the patients who gave their time to participate in the study, and the patient representative who worked with us to guide the design and delivery of the research. We would like to acknowl-

CO N FLI C T O F I NTE R E S T
The authors declare no conflict of interest.

AUTH O R S ' CO NTR I B UTI O N S
SS conceived the study with ML, RT and LS. AH conducted the interviews. Data analysis was conducted by AH and SS; other authors contributed to interpretation. AH drafted the manuscript, and all authors read and provided feedback on previous versions. All authors read and approved the final manuscript. SS is guarantor for the research.

CO N S E NT FO R PU B LI C ATI O N
All participants provided informed consent to publish the findings from the study. All data included in the manuscript are anonymized.

AVA I L A B I LIT Y O F DATA A N D M ATE R I A L S
The data collected and analysed during the current study are available from the corresponding author on reasonable request.

E TH I C S A PPROVA L A N D CO N S E NT TO PA RTI CI PATE
The study was approved by the Newcastle University

R E FE R E N C E S
A PPEN D I X 1

Theme 1 -NHS systems and pathways/organization of care
Recommendation -Pathways should be reviewed to reduce unwarranted variation and to simplify the patient's journey.
Clear communication is a necessary component but is insufficient in the absence of a review of the pathway.

Recommendation -Clearer communication with patients to
• Ensure they understand the pathway they are entering • Ensure they understand throughout what the next steps are (results, feedback).

Theme 2 -diagnosis
Recommendation -improve communication with patients to: • support clear expectations for each visit (patient information), • provide person-centred consultations and explain timescales for next steps (consultation skills), • provide results to patients through the appropriate channel (eg face to face with a clinician) and • review the process of engaging patients in shared decision making.

Theme 3 -support
Recommendation -improve communication with patients by: • clinicians introducing themselves (#mynameis), • sensitive but honest presentation of results (consultation skills) and • appreciating the importance of family and friends.

Theme 4 -Views and expectations of the NHS
Recommendation -patients' stoic acceptance of the status quo should not be seen as justification for maintaining the status quo.
Recommendation -there is a need to actively capture reliable and valid patient feedback on both positive and negative experiences of care to inform quality improvement. This could be enhanced by: • A review of the current methods and approaches to obtaining patient feedback, with consideration of independent (eg conducted by people outside of those delivering the service) and mixed methods (eg surveys, interviews and workshops) approaches.
• Clinicians and managers enabling and welcoming staff feedback and comment.