Is the early identification and referral of suspected head and neck cancers by community pharmacists feasible? A qualitative interview study exploring the views of patients in North East England

Abstract Introduction Head and neck cancer (HNC) is the eighth most common cancer in the United Kingdom. Survival rates improve when the cancer is diagnosed at an early stage, highlighting a key need to identify at‐risk patients. This study aimed to explore opportunistic HNC identification and referral by community pharmacists (CPs) using a symptom‐based risk assessment calculator, from the perspective of patients with a diagnosis of HNC. Methods Purposive sampling was used to recruit patients from the HNC pathway in three large teaching hospitals in Northern England. Qualitative methodology was used to collect data through an iterative series of semistructured telephone interviews. Framework analysis was utilised to identify key themes. Results Four main themes were constructed through the analytic process: (1) HNC presentation and seeking help; (2) the role of the CP; (3) public perception of HNC and (4) the role of a symptom‐based risk calculator. Participants agreed that CPs could play a role in the identification and referral of suspected HNCs, but there were concerns about access as patients frequently only encounter the medicine counter assistant when they visit the pharmacy. HNC symptoms are frequently attributed to common or minor conditions initially and therefore considered not urgent, leading to delays in seeking help. While there is public promotion for some cancers, there is little known about HNC. Early presentation of HNC can be quite variable, therefore raising awareness would help. The use of a symptom‐based risk calculator was considered beneficial if it enabled earlier referral and diagnosis. Participants suggested that it would also be useful if the public were made aware of it and could self‐assess their symptoms. Conclusion In principle, CPs could play a role in the identification and referral of HNC, but there was uncertainty as to how the intervention would work. Future research is needed to develop an intervention that would facilitate earlier identification and referral of HNC while not disrupting CP work and that would promote HNC and the risk calculator more widely. Patient or Public Contribution Patient and public involvement and engagement (PPIE) was integrated throughout the project. Initially, the proposal was discussed during a Cancer Head and Neck Group Experience (CHANGE) PPIE meeting. CHANGE was set up to support HNC research in 2018. The group is composed of seven members (four female, three male) with an age range of 50–71 years, who were diagnosed at Sunderland Royal Hospital. A patient representative from the University of Sunderland PPIE group and a trustee of the Northern HNC Charity were recruited as co‐applicants. They attended project management group meetings and reviewed patient‐facing documentation.


| INTRODUCTION
Head and neck cancer (HNC) is the eighth most common cancer in the United Kingdom and incidence rates are continuing to rise. HNC includes cancers of the oral cavity, larynx, pharynx, nose, throat, tonsils and salivary glands. HNC accounts for 3% of all new cancers diagnosed in the United Kingdom. 1 The North East of England has been identified as the region with the highest incidence of HNC, 2 with evidence supporting both increased incidence and mortality rates in areas of high deprivation. 3 Avoidable premature mortality amongst cancer patients is higher in the United Kingdom compared with the mean survival in Europe, and earlier detection could eradicate the gap. 4,5 A key ambition of the 2019 NHS Long Term Plan is to improve earlystage cancer diagnosis, with a target of 75% of patients diagnosed early by 2028. 6 However, it is recognised that at the point of diagnosis, many patients with HNC have progressed to advanced disease status 7,8 ; whereas survival rates improve when the cancer is diagnosed at an early stage, highlighting a key need to identify at-risk patients. 9 HNC is mostly diagnosed upon symptomatic presentation, which varies amongst patients. While oral cancers are frequently preceded by potentially malignant oral disorders (e.g., leukoplakia, erythroplakia, oral lichen planus etc.), other HNCs may initially present with ear pain, a sore throat or a neck obstruction. This means that patients may present their symptoms in a variety of healthcare settings. 10 Community pharmacies are easily accessible, with 90% of the UK population living within 20 minutes of their local pharmacy. 11 The 2022 Pharmacy Advice Audit report confirmed that UK pharmacies are saving 32 million general practitioner (GP) appointments per year. These data are being used to advocate for walk-in pharmacy advice services. 12 In June 2022, NHS England announced that pilot schemes would be created to allow community pharmacists (CPs) to refer potential cancer cases directly to hospitals. 13 In addition to the routine provision of overthe-counter treatments and advice for conditions that may be the result of an undetected HNC (e.g., persistent oral ulceration), CPs participate in healthy living promotion campaigns each year (e.g., smoking cessation counselling). 14 Research conducted alongside this study explored the views of CPs regarding their involvement in the early identification and referral of HNCs and found that while they would support such an intervention, further work was needed to develop a sustainable and cost-effective intervention that would include CP training for optimum patient care. 15 Clinical decision-making tools and risk calculators are available for a number of common cancers and are routinely used to aid prompt referral of high-risk individuals to specialist clinics for further assessment. [16][17][18] A validated HNC symptom-based risk assessment (www.ORLhealth.com) has been produced, which provides a straightforward web-based tool, that could potentially be used in a pharmacy setting. 19 Accordingly, our study aim was to explore opportunistic HNC identification and referral in a community pharmacy setting through the perspectives of patients with a diagnosis and lived experience of HNC.

| METHODS
To enhance the reporting of this study, the COnsolidated criteria for REporting Qualitative studies checklist 20 was used (see Supporting Information: File 1).

| Study design
Data were collected through an iterative series of semistructured interviews with patients who had a diagnosis of HNC. An initial topic guide was developed by the lead investigators (S. M. B. and A. S.) based around the following criteria: awareness of HNC symptoms; use of risk prediction tools and perceptions of potential future roles for CPs in HNC identification/referral. The semistructured style of interview provided flexibility to explore other topics that arose.

| Identification, invitation and recruitment of participants
Purposive sampling was used with the patients being invited to be contacted by the researchers via their HNC care team and hospital consultants working in three large teaching hospitals in Newcastle upon Tyne and Sunderland, United Kingdom. Patients were contacted by telephone, informed about the study and invited to participate by the lead investigator (S. M. B.), who also conducted the interviews. The overall objectives of the study, information about the funding source and key points relating to participation, confidentiality and anonymisation of data transcripts were explained to the participants and informed consent was obtained before commencing the interviews.

| Data collection and analysis
Individual semistructured interviews lasting up to 60 minutes were undertaken by telephone with the participant at home, sometimes alone and other times accompanied by a relative. Field notes were collated during the interview. Interviews were audio-recorded and transcribed verbatim to facilitate analysis. A conversational style of interviewing was used to encourage a comfortable and fluent dialogue. An iterative cycle of data collection and analysis facilitated the adaption of the topic guide to enable further exploration of new lines of enquiry in subsequent interviews. In the absence of a priori theory, framework analysis was utilised to identify key themes. 21 Initial analysis allowed familiarisation with the data, and this was followed by a process of revisiting data via the transcripts alongside audio-recording with manual coding of concepts to develop a thematic framework. There were no repeat interviews. Themes were reviewed by the lead investigators (S. M. B. and A.S.) and discussed with the wider research and patient, public, involvement and engagement team to establish definitive concepts.

| Reflexivity statement
The research team included experts in oral medicine, HNC, pharmacy, B. had not met the participants before, but they were informed that she worked at the Dental School.

| PARTICIPANTS' CHARACTERISTICS
Nineteen patients were approached: and 6 were lost to follow up or did not want to take part, whereas 13 participants signed consent and completed an interview (see Table 1). They were eight males and five females, aged between 42 and 79 years old. They were recruited from HNC pathways in three large hospitals in North East England: six from the Department of Oral and Maxillofacial Surgery, Sunderland Royal Hospital, four from Ear, Nose and Throat Department, Newcastle Freeman Hospital and three from Oral Medicine Department, Newcastle Dental Hospital. All participants received a referral for their symptoms from their primary care GP or general dental practitioner (GDP). Eight participants were ex-smokers and three had never smoked. Ten reported drinking alcohol within the current government guidelines and three admitted to drinking more than the recommended limits. One participant received a positive human papillomavirus diagnosis following his HNC diagnosis. Seven were 'problem-orientated dental attenders' or irregular attenders at a BISSETT ET AL. | 2091 dentist, only seeking care when having dental pain and problems, rather than attending for regular preventative care; and six were reluctant to go to the doctor, only going if they had to. Seven said they had previously attended their pharmacy for advice, while six said they went for prescription dispensing only.

| Findings
The thematic analysis methodology revealed four main themes that were identified through the analytic process.

| HNC presentation and seeking help
The participants had diagnoses of HNC that included cancers of the lip, tonsils, tongue, vocal cords and throat. The initial sign or symptom was often innocuous and included a persistent ulcer or sore, a lump or swelling, earache or hoarseness of the voice; and there was frequently no pain. Participants described initially attributing the signs and symptoms to a minor ailment like a cold sore; or an abrasion resulting from a broken tooth, or a side-effect of medication being taken for another chronic condition or a vitamin deficiency. Some participants used a variety of ways to self-treat their symptoms, but as time passed and symptoms persisted or worsened, participants would start to consider seeking help, although sometimes it took a family member or friend to persuade them to seek advice. Where there was inertia, this was attributed to living alone (easier to ignore),    34 The participants in this study appeared to be largely unaware of these resources.
A strength of this study is that it is the first that we are aware of that explores the views of patients regarding a CP's role in the early detection and referral of HNC. Furthermore, it includes a variety of subsites and patients at different stages of the HNC pathway. A limitation is the potential for selection bias. Potential participants were identified and initially approached by their consultant. All participants had received a diagnosis of HNC as we wished to explore the views of those who had lived experience, and we recruited from three hospitals in the region to find a range of perspectives.
Notwithstanding, our selection strategy may have influenced the findings, and this may limit their transferability to other areas of the country or to those presenting in emergency settings.
While the data support the concept of CPs delivering an intervention that could lead to earlier identification and referral of HNCs in principle, there was uncertainty as to how this would work BISSETT ET AL.
| 2095 in practice. Research conducted alongside this study explored the views of CPs regarding their involvement in such an intervention and although it was felt to be possible to support HNC awareness initiatives, early identification and referral, the findings suggested that further work was needed to develop a sustainable and costeffective intervention. 15 This study found that regarding accessibility, there were concerns about waiting times, privacy, CP training and support, which would suggest the need to raise public awareness about the clinical role of a CP. CP capacity to deliver the intervention would also need to be assessed and reviewed locally to consider staff time and strategies to mitigate disruption. Furthermore, if a CP could make a 2-week urgent referral via the Northern Cancer Alliance website, this could improve and add value to the intervention.

| CONCLUSION
The findings of this study suggest that the principle of utilising CPs in the early identification and referral of suspected HNC was accepted by all participants, with the agreement that it may encourage some people to make an appointment with their GP/GDP. However, there was uncertainty as to how the intervention would work. Future research will need to look at intervention development and implementation that includes CP and the wider community pharmacy team training and capacity building; and the design and delivery of an effective HNC public health campaign.

AUTHOR CONTRIBUTIONS
All authors contributed to the study conception, design, analysis and interpretation of data, and reviewed/revised the submission. Marco