Disease-related factors affecting timely lymphoma diagnosis: a qualitative study exploring patient experiences

Debra A Howell; Ruth I Hart; Alexandra G Smith; Una Macleod; Russell Patmore; Eve Roman

doi:10.3399/bjgp19X701009

Abstract

Background Expediting cancer diagnosis is widely perceived as one way to improve patient outcomes. Evidence indicates that lymphoma diagnosis is often delayed, yet understanding of issues influencing this is incomplete.

Aim To explore patients’ and their relatives’ perceptions of disease-related factors affecting time to diagnosis of Hodgkin and non-Hodgkin lymphoma.

Design and setting Qualitative UK study involving patients with indolent and aggressive lymphomas, and their relatives, from an established population-based cohort in the north of England.

Method Semi-structured interviews with 35 patients and 15 of their relatives. Interviews were audiorecorded and transcribed, and qualitative descriptive analysis was undertaken.

Results Participant accounts suggest that certain features of lymphoma can impact on patients’ and healthcare providers’ (HCPs) responses to disease onset. Three characteristics stand out: disease occurrence (rare), manifestation (varied), and investigative options (often inconclusive). Interviewees described how they, and some HCPs, lacked familiarity with lymphoma, seldom considering it a likely explanation for their symptoms. Symptoms reported were highly variable, frequently non-specific, and often initially thought to be associated with various benign, self-limiting causes. Blood tests and other investigations, while frequently able to detect abnormalities, did not reliably indicate malignancy. Interviewees reported the potential for improvements among HCPs in information gathering, communication of uncertainty, and re-presentation advice for non-resolving/progressive health changes.

Conclusion This study demonstrates the complex characteristics of lymphoma, perceived by patients as prolonging time to diagnosis, often despite significant effort by themselves, their relatives, and HCPs to expedite this process. The findings also illustrate why simple solutions to delayed diagnosis of lymphoma are lacking.

INTRODUCTION

Over a third of the 33 000 haematological malignancies diagnosed in the UK each year are lymphomas.¹ These cancers comprise a heterogeneous group, with many distinct subtypes, which differ markedly in incidence, clinical pathways, and outcomes.² For example, some subtypes are aggressive, progress rapidly, and are considered curable, such as diffuse large B-cell lymphoma and classical Hodgkin lymphoma; others are indolent, generally advance more gradually, and are incurable, including follicular lymphoma and marginal zone lymphoma; some may have both aggressive and indolent variants, for example, mantle cell lymphoma. Definitive diagnosis generally requires examination of lymph node, extranodal, and bone marrow tissue, along with a combination of specialist laboratory investigations, including morphological, cytogenetic, immunocytochemistry, and flow cytometry testing.

Early-stage diagnosis of cancer is important, as this is one means of improving patients’ survival³ and quality of life.⁴ Despite this, the time leading to identification of lymphoma may be protracted and associated with avoidable delay.⁵^,⁶ Unfortunately, although UK policy-based interventions, including referral guidance for GPs,⁷ have resulted in improvements for several malignancies, these have had less impact for people with lymphoma.⁸ Patients with lymphoma are still more likely to have multiple primary care appointments before hospital referral,⁹ and are less likely to have an urgent GP referral, whereby they are seen by a hospital specialist for suspected cancer within 2 weeks.¹⁰ Furthermore, recent data also indicate that as many as two in five lymphoma diagnoses occur after emergency presentation, a route associated with late-stage disease and poor survival.¹¹

Research into time to cancer diagnosis has grown significantly in recent years. For lymphoma, studies have calculated the duration of time between specific events before diagnosis, including onset of symptoms, first help seeking, and hospital referral, often drawing on survey data, either examining individual or combinations of subtypes, frequently alongside other cancers.⁵^,⁸^,¹²^,¹³ Theoretical models now exist to facilitate time to diagnosis research, and ensure consistency in definitions, methods, and reporting. The model of pathways to treatment is one example of this.¹⁴^,¹⁵ This builds on earlier classification systems,¹⁶^,¹⁷ and defines a linear series of intervals, events, and processes, with several cross-cutting factors (Figure 1). These include the ‘appraisal’ interval — detection of bodily changes to decision to consult a healthcare provider (HCP); the ‘help seeking’ interval — decision to consult a HCP to first consultation; and the ‘diagnostic’ interval — first HCP consultation to diagnosis, including HCP appraisal, investigations, referrals, and appointments.

How this fits in

Previous research identifies significant consequences of delayed cancer diagnosis, yet little is known about the factors affecting time to identification of lymphoma, despite these diseases being associated with late recognition. The current study explores the perceptions of patients with lymphoma, and their relatives, of disease-related issues impacting on time to diagnosis. It is one of few studies to use qualitative methods to explore patient experiences before and after first help seeking. It highlights three important factors: the rare occurrence of lymphoma, its varied manifestation, and the investigative options available, which may be inconclusive. This evidence furthers understanding of when and why lymphoma diagnosis may be delayed; how delay can occur despite significant efforts on the part of patients, their relatives, and healthcare providers; and how simple solutions to this issue are lacking.

Figure 1.

Model of pathways to treatment.

HCP = healthcare provider. Walter F, Webster A, Scott S, Emery J. J Health Serv Res Policy 2012; 17(2): 110–118, Copyright © 2012 by SAGE Publications. Reprinted by Permission of SAGE Publications, Ltd.

Factors affecting time to diagnosis remain relatively under-explored¹⁸^,¹⁹ however, and few studies have used qualitative methods to identify pertinent issues, including experiences after first help seeking, either for lymphomas or other cancers.²⁰^–²² The aim of the current study was to improve understanding of experiences in the time leading to lymphoma diagnosis by exploring the perspective of patients and family members and focusing on the impact of disease factors. To achieve this, a qualitative study was conducted, set within a large, ongoing patient cohort in the north of England,²³ based on the intervals and events described in the model of pathways to treatment.¹⁴^,¹⁵

METHOD

The study was carried out in accordance with the consolidated criteria for reporting qualitative research (COREQ)²⁴ and guidance on standards for reporting qualitative research findings.²⁵

Context

The study is nested within the Haematological Malignancy Research Network, an ongoing population-based patient cohort established to generate evidence on haematological malignancies for research purposes and to inform clinical practice.²^,²⁶ Approximately 2400 diagnoses annually, from a population of about 4 million in the Yorkshire and Humber region of the UK, are made by a single specialist laboratory and coded to the latest World Health Organization classification system.²⁷ Core data are abstracted from medical records and patients are invited to complete a routine postal questionnaire soon after diagnosis about their symptoms and help seeking, including dates.

Participants

Potential participants were identified from patients returning the routine Haematological Malignancy Research Network (HMRN) postal questionnaire. Purposive sampling was used to ensure maximum variation in disease subtype, sex, age, and time to diagnosis. Patients were invited to ask a relative to take part in the interview if they wished, both to promote recall and share their own perceptions.

Data collection

Potential participants were posted a study pack containing an introductory letter, information leaflet, response form, and prepaid return envelope. Those wishing to participate contacted the study team directly (via post or phone), and an interview was arranged. Two experienced qualitative researchers conducted the interviews, both of whom have significant experience in health services research, one of whom was a former registered nurse, with two decades of academic experience with haematology patients, their relatives, and clinicians. Neither researcher was known to participants.

All patients were assured of data confidentiality and gave written consent to take part in the study. Interviews were conducted face-to-face, largely within patients’ homes (although two took place at the hospital), and within a year of diagnosis. Several early pilot interviews were conducted, followed by an intensive period of fieldwork between November 2015 and May 2016. Data collection was semi-structured and guided by a schedule, which was informed by experience from within the research team and based on the appraisal, help-seeking, and diagnostic intervals, as defined in Walter et al ’s model of pathways to treatment.¹⁴^,¹⁵ Issues included in the interview schedule are summarised in Box 1. Precise questions were adapted during the interviews to accommodate the full range of experiences and the manner in which patients chose to describe them. Interviews were digitally audiorecorded and, on average, completed in around 45 minutes.

Interviewees were asked to describe:

The symptoms and health changes they experienced and how (in the appraisal, help-seeking, and diagnostic intervals) these:
- changed;
- were appraised and interpreted by themselves, relatives, and healthcare providers;
- were managed by themselves, relatives, and healthcare providers.
Factors promoting and preventing timely appraisal, help seeking, and diagnosis.
Their knowledge and experience of lymphoma before diagnosis.

Box 1.

Interview schedule

Data analysis

Recordings were transcribed verbatim, field notes were used to confirm accuracy, and transcripts were checked and anonymised before import into the data management software, ATLAS-ti (version 6.2.11). The methodological orientation was qualitative description, a pragmatic approach producing minimally theorised findings with practical applications.²⁸^,²⁹ Analysis was iterative, running alongside and informing data collection, which was discontinued once saturation was achieved.³⁰ After data familiarisation through reading/re-reading transcripts, several rounds of coding were undertaken, with constant comparison driving the refinement of codes. Memoing and mapping techniques were used to explore patterns, including similarities and differences between individuals, and relationships between codes.³¹ The wider research team had access to the data, analytical process, and pathway maps that, along with codes and emerging themes, were regularly discussed and refined until consensus was reached.

RESULTS

Of 58 individuals contacted, 35 responded and were interviewed (Table 1). Thirty patients had non-Hodgkin lymphoma (indolent and aggressive subtypes) and five had Hodgkin lymphoma; 18 were male; and median age at interview was 63 years (range 23–84 years). Fifteen spouses and/or partners agreed to take part in the interview, alongside the patient.

View this table:

Table 1.

Participant characteristics (n = 35)

Based on the routine HMRN postal questionnaire, in which patients document their symptoms and help-seeking activities, time from first symptom to diagnosis was found to vary markedly, the collective appraisal and help-seeking intervals having a median duration of 1 month (range 0.5–13 months), and the diagnostic interval 4 months (range 1–24 months). Accounts suggested that a combination of disease-related factors impacted on the behaviour of patients, their relatives, and HCPs (GPs and nurses) in primary care. Three significant themes emerged: the occurrence of lymphoma (rare), its manifestation (varied), and investigation (often inconclusive) (Figure 2). These issues impacted on the assessment, interpretation, and response to symptoms across the appraisal, help-seeking, and diagnostic intervals, with recurrent activities (for example, patient appraisal before and after first help seeking) preventing unilinear progression through each stage of the model of pathways to treatment before diagnosis. Each theme is described with verbatim quotes.

Figure 2.

Summary of interviewee perceptions about disease-related factors and their impact on time to lymphoma diagnosis. HCP = healthcare provider.

Occurrence

Interviewees perceived lymphoma as a relatively rare disease (in contrast with other cancers they were aware of, such as breast cancer), typically affecting older adults.

An unfamiliar disease

Few interviewees reported encountering anyone with lymphoma before diagnosis, and several had never heard of it. Those who had, often described their knowledge as limited: ‘I’d heard of non-Hodgkin’s lymphoma. I didn’t know quite what it meant.(Patient [P] 2)

Some said that at diagnosis, they had not initially known that lymphoma was a form of cancer. Awareness of Hodgkin lymphoma was somewhat greater, with several interviewees identifying this as life threatening. However, previous knowledge of symptoms was consistently low. Some, often younger, patients reported finding references to lymphoma when using the internet to facilitate symptom appraisal and the decision to seek help.

Several interviewees also perceived HCPs as having limited exposure to, and familiarity with, lymphoma: ‘Because it’s quite rare, a doctor … might only see one case in their existence.’(P7)

A few suggested HCPs were ill equipped to recognise symptoms: ‘The diagnosis was definitely late, no doubt about that … there’s not enough known about the early symptoms.’(P24)

This was said to prolong the diagnostic interval by holding up investigation and/or referral. Gaps in HCPs’ knowledge seemed most problematic where symptoms were subtle and gradual in onset. Accounts suggest that HCPs acted quickly and decisively when patients were acutely ill, for example, arranging emergency admission.

An improbable disease

Except for well-known common cancers associated with older age and sex, interviewees rarely perceived themselves as at risk of cancer as they appraised their symptoms: ‘I had this stupid notion that if I, if I ate properly and looked after myself, I’d never go down with anything like that.’(P4)

They drew attention to prior health, healthy lifestyles, and lack of a family history: ‘Cancer isn’t something that runs in our family.’(P31)

Where internet searches returned references to lymphoma, this could therefore seem an unlikely explanation for symptoms: ‘I went on the internet and read up. Well, when I started reading about cancer I just switched it off, because I thought, “No, no, that’s not right”.’(P5)

Some interviewees suggested that perceptions of lymphoma as rare also inclined HCPs to judge it unlikely, and discount it as an explanation for symptoms during the diagnostic interval. One interviewee surmised age was also significant, with lymphoma dismissed because of their (relative) youth: ‘I think the GPs knew the symptoms of, of lymphoma. I just don’t think they were willing to, er, consider them, because of my age.’(P6)

Manifestation

Accounts revealed marked differences in symptom type and combinations, speed of onset, progression, and intensity. Again, these characteristics affected the duration of the appraisal interval, the decision to seek help, and the length of the diagnostic interval.

Highly variable

Interviewees described a wide range of symptoms they had come to associate with onset of their lymphoma (Box 2). A few participants reported isolated changes, aside from which they felt well. In such instances, help seeking was often delayed, even where the symptom was widely associated with cancer, such as lumps or unexplained bleeding. The absence of pain seemed to provide reassurance: ‘For some strange reason I’d always assumed there would be pain.’(P2)

General feelings of ill health

‘can’t put finger on it’, ‘couldn’t do anything’, ‘generally looked ill’, ‘generally unwell’, ‘grotty’, ‘immunity whacked’, ‘just didn’t feel right’, ‘just felt rotten’, ‘lousy’, ‘something wrong’, ‘thinking “this isn’t right”’, ‘under par’, ‘not feeling well’, ‘not quite right’, ‘one thing after another’, ‘rough’, ‘something wasn’t right’, ‘terrible’, ‘under the weather’, ‘unwell’, ‘vaguely off’.

Specific symptoms

Bleeding: bruising, nosebleeds (‘pumping out’), vaginal bleeding.

Cognitive: confusion, loss of concentration, memory loss, mistakes at work.

Eating/drinking: appetite loss, heartburn, indigestion, nausea, reacting to alcohol/food, unable to eat, unable to keep food/water down, weight loss.

Faint/dizzy: blacking out, dizziness, lightheaded, near collapse, passing out, ‘weird turn’.

Gastrointestinal: bloated, bulges/change in shape of stomach, constipation, diarrhoea/loose stool, feeling like something lodged in stomach, flatulence, jaundice, pancreatitis, passing ‘white mass’, ‘pulsing’ of stomach, stomach upset.

Genitourinary: increased urination (‘at night’), loss of bladder control.

Lack of energy: fatigue, lethargy, tiredness, weakness. Characteristics: ‘abnormal’, ‘debilitating’, ‘desperate’, ‘extreme’, ‘immense’, ‘prolonged’, ‘really’, ‘very’.Impact (general): ‘depleted’, ‘flattened’,‘reserves disappearing’, ‘no reserve’, ‘running on empty’, ‘sleeping more’ (‘a lot’, ‘12 hours’ ), ‘shattered’, ‘exhaustion’, ‘worn out’, ‘honestly could drop’. Impact (on work/hobbies): ‘fluctuating capacity for work’, ‘unable to do as much at gym’, ‘losing fitness’, ‘deteriorating fitness’.

Mobility: difficulty walking, falls, tripping.

Mouth/taste: altered taste in mouth (‘metallic’, ‘nasty’, ‘taste buds changed’), mouth ulcers.

Infections: Characteristics: fungal, recurrent, viral. Types: colds, cold sores, flu, flu-like symptoms, perianal abscess, pneumonia, sore throats, thrush, upper respiratory, urinary.

Pain: Characteristics: ‘as bad as toothache’, ‘bent double’, ‘cramp’, ‘in agony’, ‘nagging’, ‘sciatic-like’, ‘stabbing’, ‘terrific’, ‘7–8 out of 10’. Areas: abdomen, arms, back, chest, feet, groin, head (‘pounding’, ’pulsating’), knee, legs, lower back, ovary, shins, shoulder, stomach, thigh, rectal.

Respiratory: breathing difficulties at night, breathlessness, cough (‘dry’, ‘bad’), hoarse voice, post-nasal drip, vocal changes.

Neurosensory: abnormal sensations (back: ‘something rubbing’, feet burning: ‘as if I’d been scalded’), loss of feeling in legs, numbness (legs), visual disturbances (‘black spots’ in front of eyes).

Skin: change in colour of skin and whites of eyes (yellow, green/yellow), itchiness, itchy rash, not healing properly, ‘swollen spongy scalp’.

Swellings/lumps: Areas (specific): groin, neck, armpit, abdomen/stomach, mouth, jawline, over collarbone, calf, ‘on waist’. Areas (general): leg/thigh/foot (‘ballooning’). Changes: ‘started to hurt’, ‘started to go a “bluey-purple” colour’, ‘growing … bigger than a grapefruit’.

Temperature/sweats: high temperature, hot flushes, ‘really cold’, running a temperature, sweats (‘day’, ‘night’, ‘horrendous’, ‘hot’).

Initial interpretation of symptoms by patients

Illnesses, comorbidities: allergy, back trouble, bad cold, cancer, Crohn’s disease, cyst, dengue fever, depression, diverticulitis, effects of surgery, existing musculoskeletal problems, grumbling appendix, haemorrhoids, hernia, hypochondria, irritable bowel, lupus, lymphoma, ME (myalgic encephalopathy), picked something up, prostate cancer, slipped a disc, some strange fungal thing, stomach cancer, testicular cancer, tumour, parathyroid problems, ulcer, varicose veins, vertigo, vitamin D deficiency, weakening muscles and bones.

Lifestyle, life stage: age/ageing, bored, busy life, driving, family problems, fasting, heavy work, hectic, hormonal changes, injury (gym), lifting weights, ‘one-off’, ‘overdone things’, ‘man change’, menopause, ‘middle-age spread’, responsibilities and worries, retirement, rushing around, stress, too much cycling, work.

Other: altitude, antibiotics, duvet too thick, season.

Box 2.

Pre-diagnostic symptoms considered due to lymphoma, and their initial interpretation, as described by interviewees

Sometimes medical attention arose from help seeking for other concerns. One interviewee described consulting their GP about a groin swelling: ‘She said it was a hernia, but she were more concerned about these [other] lumps, which I couldn’t understand … I wa’n’t [sic] having any problems with them.’(P19)

If multiple symptoms were experienced, patients and relatives said they were often slow to connect these or appraise them collectively. Some suggested HCPs were similarly late in doing this: ‘The … GPs … never pieced it together. Whilst we [patient and relative] were looking at the symptoms individually, they [HCPs] were too.’(P14)

Something or nothing?

Some patients, typically with a seemingly aggressive disease, described rapid symptom development, with marked changes in their health. Severe and disruptive symptoms encouraged early help seeking and — unless the sole symptom was pain — usually led to prompt investigation or referral to secondary care. However, many more described subtle symptoms, emerging insidiously or intermittently. These were often overlooked or, if appraised, judged unremarkable: ‘On reflection, I had, possibly some sweating … these things are sort of so slow and imperceptible that you don’t always … think much of it at the time.’(P13)

Non-specific feelings of being generally unwell were also often described (Box 2): ‘Vaguely off.’(P4) ‘Just didn’t feel right.’(P18)

Interviewees perceived HCPs as being under strain and felt a responsibility to determine if symptoms were important before seeking help: ‘You know, the NHS hasn’t got unlimited resources, infinite resources, and I don’t want to waste doctors’ time.’(P13)

As part of the appraisal process, they often consulted friends and family about their symptoms, and whether they should seek help from an HCP. Usually they were encouraged to see a doctor, but not always: ‘I showed the lump to my friends and they said, “You’re just freaking out, it’s nothing, we can’t even see the lump”.’(P23)

Intermittent symptoms were sometimes misconstrued as resolved, which could interrupt and extend the diagnostic interval, for example, because of the cancellation of investigations.

Plausible competing explanations

Interviewees described how, as part of the appraisal process, they often initially identified alternative explanations for symptoms (Box 2). This was also common among HCPs in the diagnostic interval. Expectations of age-related deterioration enabled patients to normalise many symptoms at this time, perceiving them as ‘change’, and not disease. Patients often attributed non-specific symptoms and localised pain to lifestyle, due to being busy and rushing around; to life stage, including being menopausal; or other conditions, such as depression or diverticulitis. They did not always report such changes to HCPs: ‘I wrongly assumed, at the time, that it [night sweats] was associated with this [other] problem … With hindsight, perhaps, I should have mentioned it.’(P30)

HCPs too were recalled as proposing a range of explanations for symptoms in the diagnostic interval, including non-physical causes: ‘ [The GP] said, “Well what’s probably happening is your body, you know, now that your mum’s gone in the [nursing] home, your body is saying, ‘Pffh, that’s it, you know, just relax’ … and this is why you’re sleeping so much”.’(P31)

A few HCPs were described as attributing symptoms to psychological conditions including stress, anxiety, and depression — these examples mostly came from patients aged <40 years. Many HCPs initially diagnosed other physical but non-malignant conditions: ‘The assumption [was] that it was, er, iron deficiency and the vitamin B12 … they were, perhaps a little bit more complacent about the symptoms than they ought to have been.’(P11)

These explanations often seemed plausible to patients, who had sometimes considered these explanations themselves, even in hindsight. Interviewees described their HCPs’ readiness to consider more serious explanations, including malignancy, as variable. Some HCPs were said to suspect cancer from the first help-seeking episode: ‘Honest to God this is how it happened, he turned and looked at me, and he went, “cancer clinic for you”. He knew, straightaway.’(P22)

Others, however, seem to have done so only after treatment failure excluded benign explanations: ‘He realised that it can’t be that [polymyalgia] because the steroids should have altered it, and it ha’n’t [sic] done.’(P16)

In many instances, patients re-appraised their symptoms after first help seeking and re-presented to their GP — sometimes on multiple occasions — before HCPs undertook re-appraisal, initiated investigations, and/or discussed referral.

Investigation

In the diagnostic interval, interviewees described undergoing blood tests, various imaging/scans, and one or more biopsies, and reflected on the timing, costs, and/or invasiveness of these, as well as the uncertainty of findings.

Variation in access

Participant accounts suggest considerable variation in when tests were undertaken, and at whose instigation. For example, some recalled having blood tests after first help seeking, and others only after several visits. One interviewee remarked: ‘There seems to be a reservation … about what bloods, you know, what bloods to take and what’s done with the [tests] — I suppose it’s money.’(P24)

A few described efforts to negotiate investigations, which were not always successful: ‘[the doctor] said, “Well, if we sent everybody for an X-ray who was complaining of a pain or something, there’d be queues outside miles long”.’(P21)

Access to MRI scans was portrayed as constrained, even where HCPs viewed this as appropriate. A related issue was that investigations were typically conducted in sequence, with the results of one determining the need for another. Some interviewees viewed staggering tests as sensible: ‘There is no point putting somebody through surgery [for a biopsy] that they don’t need.’(P19)

Others, however, were more critical: ‘You went for a biopsy later on … to find out what it was, what kind of cancer it was. But all these things, it drags on, and weeks go into months … it’s agonising.’(Relative of P20)

Results not always reliable or clear

Participants commented on the reliability of available tests and the certainty with which they could detect disease. Some interviewees described getting decisive evidence of abnormality, suggestive of lymphoma or another serious condition. Many, however, reported receiving ‘normal’ or inconclusive results, in particular from blood tests and, to a lesser extent, imaging: ‘Nothing showed up in my blood, no abnormalities.’(P18)

Accounts suggest patients often interpreted normal results as being given an ‘all clear’ and a disincentive to further appraisal and help seeking: ‘I think, looking back, that that scan was very reassuring … all blood tests were good, that radiologist said everything looked healthy … I felt quite reassured.’(P26)

Others recalled inconclusive or ambiguous results, which could prove challenging for HCPs to interpret: ‘[the GP] looked at the [blood results] … and he says, “I can’t make head nor tail of this”.’(P24)

A few interviewees inferred gaps in HCPs’ knowledge and understanding of how lymphoma might manifest in tests. They reported receiving a range of explanations for irregular bloods, such as infection, benign conditions, and contamination; and for enlarged lymph nodes, including infection and/or injury. Where the significance of results was unclear, tests were typically repeated, but not always promptly: ‘You waited 7 weeks for the [second] scan, which is too long. It had doubled, if not more, in size by that time.’(Relative of P32)

DISCUSSION

Summary

This study aimed to improve understanding of disease-related factors affecting the time to diagnosis of lymphoma within the appraisal, help-seeking, and diagnostic intervals described in Walter et al’s model of pathways to treatment.¹⁴^,¹⁵ The study is novel in that findings are derived from patients’ self-reported experiences, and it examines activities before and after first help seeking. Lymphoma occurrence was considered rare by interviewees, descriptions of its manifestation were varied, and patients often commented on the lack of specific investigations to clearly raise suspicion of cancer. These features resulted in a scenario whereby, with no, or very limited, knowledge, patients typically experienced the onset of subtle, non-specific symptoms or perceptions of ill health, which during appraisal were often attributed to benign, mundane conditions, and/or non-physical, lifestyle, and age-related factors. In the diagnostic interval, HCPs often faced an unfamiliar disease, with symptoms similar to those of other common, non-malignant conditions, for which investigations did not reliably show abnormality or suggest malignancy; until symptoms progressed, the case for further tests and/or hospital referral was often unclear.

Strengths and limitations

Using qualitative methods allowed engagement with the complexity of patients’ self-reported, pre-diagnostic experiences, something previously identified as an important challenge.³² This study included patients diagnosed with indolent and aggressive lymphoma subtypes, and covered a broad range of age groups, both sexes, and varying pre-diagnostic time intervals, including the period of time before and after first help seeking. The study sample and in-depth interview techniques yielded rich data that provide new insights into an important but under-researched area. To promote accurate recall, patients were mostly interviewed within a year of diagnosis, and reference to letters, calendars and diaries, and the involvement of family members, were encouraged.

Participant accounts were not corroborated by review of medical records or HCP perspectives, as this was not the objective of the study. Compliant with ethical approvals, transcripts and findings were not returned to interviewees for verification. Transcripts were checked alongside interview recordings for accuracy. Patients were included who had previously returned a routine postal questionnaire about their symptoms and help seeking, so did not capture the perspectives of those who either died soon after diagnosis, or who were not sent or did not return a questionnaire for other reasons, for example, if their health had deteriorated rapidly. Transferability, that is, consideration of findings in relation to their relevance for understanding similar issues and processes, is a key aspiration in qualitative research, rather than generalisability.³³ Extrapolation should therefore take into account any study-specific contextual factors, such as different healthcare systems, universal healthcare coverage, and so on, which may limit transferability.³⁴

Comparison with existing literature

Research into factors affecting time to lymphoma diagnosis specifically, and cancers more widely, has consistently identified patient tendencies to ascribe routine explanations to their symptoms such as stress or the normal ageing process/life phase, rather than recognising these as serious.²⁰^,²²^,³⁵^–³⁷ The results of the current study echo these findings; the broad range of symptoms described were often subtle, and did not always incorporate the common, or ‘red-flag’,³⁸ characteristics listed on public-targeted lymphoma-specific websites, such as swollen lymph nodes, fatigue, weight loss, or sweats.³⁹ Intermittent symptoms, interpreted by patients in the current study as potentially resolved, were also considered reassuring among patients with other malignancies, such as pancreatic cancer,⁴⁰ as were negative investigation results, by patients and GPs.⁴¹^–⁴³ A recent systematic review of factors impacting on cancer diagnosis reported patient difficulties in assessing the significance of vague, non-specific symptoms, and perceptions that HCPs had not taken their concerns seriously, had not taken a thorough history, and had not asked relevant questions; patients were also anxious that they themselves did not overburden or waste doctors’ time.⁴⁴

Studies exploring factors after first help seeking in primary care are perceived as limited, with respect to lymphoma and other less familiar cancers.²¹^,²² Available evidence suggests ‘practitioner delay’ is influenced by the nature of symptoms and how these are interpreted, as well as use of appropriate diagnostic testing and follow-up.⁴² The current study confirms that the relevance of these findings extends to lymphoma. Concurring with Walter et al’s model,¹⁴^,¹⁵ it also suggests patients’ interpretations and actions, such as re-appraisal and re-presentation for ongoing symptoms, remain significant after the first presentation, and that improved understanding of interactions between patients and HCPs is required.

Implications for research and practice

Although effective for some cancers,⁴⁵^,⁴⁶ the characteristics of lymphoma may mean interventions such as education campaigns, aiming to facilitate appraisal and encourage help seeking and specialist referral, are ineffective. This is due to the myriad symptoms that may be experienced, which can vary with site of disease origin and spread, and could potentially affect nodal and extra-nodal sites, and different organs and locations in the body. The vague symptoms noted as a consequence of ineffective lymphatic and bone marrow functioning, such as non-specific and/or multiple infections, and anaemia-related fatigue, further limit the value of education campaigns; as do differences in the severity, resulting dysfunction, and pace of symptom progression, which are contingent on the lymphoma variant. For relatively rare conditions such as lymphoma, campaigns encouraging people to take note of changes in their body that persist and/or worsen, or diverge from what is ‘normal’ for them, may be a more effective approach to encouraging help seeking.

Most people consult a GP before cancer diagnosis, even if the malignancy is identified following emergency presentation.⁴¹^,⁴⁷^,⁴⁸ Consequently, for insidious and acute manifestations, GPs are faced with the complex task of differentiating benign symptoms from those that may indicate cancer. These decisions are made more difficult because the only high-risk factors indicative of lymphoma are unexplained lymphadenopathy (if present) in people aged ≥60 years, and an increase in consultation frequency to a doubling from normal in the year before diagnosis.⁴⁹^,⁵⁰ Furthermore, the signs and symptoms of lymphoma cited in UK referral guidance, aiming to support GPs’ clinical evaluation and decision making,⁷ present only the most common symptoms, so are not ideal where clinical presentation deviates from this, a situation that the current study highlights as being common. The lack of investigations available to clearly identify or exclude lymphoma, as well as the propensity for normal inflammatory markers until late in the trajectory, contribute a further complication.⁴⁹^,⁵⁰ Unsurprisingly, a study with UK GPs reported the early detection of malignancy as particularly burdensome, because of the challenges in identifying potential cancer symptoms, managing cancer anxiety among patients and their families, and making appropriate referrals.⁵¹

Certain aspects of the diagnostic interval are modifiable by HCPs, however, and may address some of the challenges raised by patients in the current study. ‘Safety netting’ has been suggested as a means of managing diagnostic uncertainty, ensuring timely and appropriate follow-up, and avoiding emergency presentation, particularly where symptoms are non-specific or associated with ‘low’ cancer risk, but not ‘no’ cancer risk.⁷^,²¹^,⁴¹^,⁴⁴^,⁵² Strategies encouraged include: effective and precise GP communication to the patient and/or family about potential signs of deterioration/complications, what to expect over time, where to access test results, when, how, and where to seek further help for ongoing/worsening health issues, and documentation of issues such as uncertainty.³⁸^,⁵³ This approach would facilitate appropriate patient re-appraisal of symptoms and provide reassurance that repeated help seeking was justified, and indeed may be required. In the diagnostic interval, it would provide HCPs with a useful summary of events, and highlight that uncertainty had been recognised. Furthermore, research into vague and/or non-site-specific symptoms, such as weight loss, has led to recommendations for ways in which such manifestations should be managed, including the development of ‘vague symptoms’ pathways.⁷^,⁵⁴

Unfortunately, evidence from HCPs is absent for lymphoma, yet research with this group is crucial if the barriers and facilitators to timely diagnosis are to be wholly understood and relevant remedial strategies identified.

Acknowledgments

The authors are grateful to the patients and family members who contributed to this research.

Notes

Funding

This research was supported by funding from Cancer Research UK (National Awareness and Early Diagnosis Initiative: C38860/A13509); the Haematological Malignancy Research Network (HMRN) is funded by Bloodwise (Award: 15037).

Ethical approval

The study had National Research Ethics Service approval from Yorkshire & The Humber — South Yorkshire Research Ethics Committee (REC 12/YH/0149); the HMRN has ethical approval from Leeds West Research Ethics Committee (REC 04/01205/69).

Provenance

Freely submitted; externally peer reviewed.

Competing interests

The authors have declared no competing interests.

Discuss this article

Contribute and read comments about this article: bjgp.org/letters

Received July 20, 2018.
Revision requested August 22, 2018.
Accepted September 24, 2018.

This article is Open Access: CC BY-NC 4.0 licence (http://creativecommons.org/licences/by-nc/4.0/).

REFERENCES

1.↵
1. Haematology Malignancy Research Network
QuickStats, https://www.hmrn.org/statistics/quick (accessed 10 Dec 2018).
2.↵
1. Smith A,
2. Crouch S,
3. Lax S,
4. et al.
(2015) Lymphoma incidence, survival and prevalence 2004–2014: sub-type analyses from the UK’s Haematological Malignancy Research Network. Br J Cancer 112(9):1575–1584.
OpenUrl CrossRef PubMed
3.↵
1. Thomson CS,
2. Forman D
(2009) Cancer survival in England and the influence of early diagnosis: what can we learn from recent EUROCARE results? Br J Cancer 101(Suppl 2):S102–S109.
OpenUrl CrossRef PubMed
4.↵
1. Neal RD,
2. Tharmanathan P,
3. France B,
4. et al.
(2015) Is increased time to diagnosis and treatment in symptomatic cancer associated with poorer outcomes? Systematic review. Br J Cancer 112(Suppl 1):S92–S107.
OpenUrl CrossRef PubMed
5.↵
1. Howell DA,
2. Smith AG,
3. Jack A,
4. et al.
(2013) Time-to-diagnosis and symptoms of myeloma, lymphomas and leukaemias: a report from the Haematological Malignancy Research Network. BMC Hematol 13(1):9.
OpenUrl CrossRef PubMed
6.↵
1. Swann R,
2. McPhail S,
3. Witt J,
4. et al.
(2018) Br J Gen Pract, Diagnosing cancer in primary care: results from the National Cancer Diagnosis Audit. DOI: https://doi.org/10.3399/bjgp17X694169.
7.↵
1. National Institute for Health and Care Excellence
(2015) Suspected cancer: recognition and referral NG12 (NICE, London) https://www.nice.org.uk/guidance/ng12 (accessed 11 Jan 2018).
8.↵
1. Neal RD,
2. Din NU,
3. Hamilton W,
4. et al.
(2014) Comparison of cancer diagnostic intervals before and after implementation of NICE guidelines: analysis of data from the UK General Practice Research Database. Br J Cancer 110(3):584–592.
OpenUrl CrossRef PubMed
9.↵
1. Lyratzopoulos G,
2. Neal RD,
3. Barbiere JM,
4. et al.
(2012) Variation in number of general practitioner consultations before hospital referral for cancer: findings from the 2010 National Cancer Patient Experience Survey in England. Lancet Oncol 13(4):353–365.
OpenUrl CrossRef PubMed
10.↵
1. Zhou Y,
2. Mendonca SC,
3. Abel GA,
4. et al.
(2018) Variation in ‘fast-track’ referrals for suspected cancer by patient characteristic and cancer diagnosis: evidence from 670 000 patients with cancers of 35 different sites. Br J Cancer 118(1):24–31.
OpenUrl
11.↵
1. Kane E,
2. Howell D,
3. Smith A,
4. et al.
(2017) Emergency admission and survival from aggressive non-Hodgkin lymphoma: a report from the UK’s population-based Haematological Malignancy Research Network. Eur J Cancer 78:53–60.
OpenUrl
12.↵
1. Lyratzopoulos G,
2. Saunders CL,
3. Abel GA,
4. et al.
(2015) The relative length of the patient and the primary care interval in patients with 28 common and rarer cancers. Br J Cancer 112(Suppl 1):S35–S40.
OpenUrl CrossRef PubMed
13.↵
1. Keeble S,
2. Abel GA,
3. Saunders CL,
4. et al.
(2014) Variation in promptness of presentation among 10,297 patients subsequently diagnosed with one of 18 cancers: evidence from a National Audit of Cancer Diagnosis in Primary Care. Int J Cancer 135(5):1220–1228.
OpenUrl CrossRef PubMed
14.↵
1. Walter F,
2. Webster A,
3. Scott S,
4. Emery J
(2012) The Andersen Model of Total Patient Delay: a systematic review of its application in cancer diagnosis. J Health Serv Res Policy 17(2):110–118.
OpenUrl CrossRef PubMed
15.↵
1. Scott SE,
2. Walter FM,
3. Webster A,
4. et al.
(2013) The model of pathways to treatment: conceptualization and integration with existing theory. Br J Health Psychol 18(1):45–65.
OpenUrl CrossRef PubMed
16.↵
1. Andersen BL,
2. Cacioppo JT
(1995) Delay in seeking a cancer diagnosis: delay stages and psychophysiological comparison processes. Br J Soc Psychol 34(Pt 1):33–52.
OpenUrl CrossRef PubMed
17.↵
1. Safer MA,
2. Tharps QJ,
3. Jackson TC,
4. Leventhal H
(1979) Determinants of three stages of delay in seeking care at a medical clinic. Med Care 17(1):11–29.
OpenUrl PubMed
18.↵
1. Howell DA,
2. Warburton F,
3. Ramirez AJ,
4. et al.
(2015) Risk factors and time to symptomatic presentation in leukaemia, lymphoma and myeloma. Br J Cancer 113(7):1114–1120.
OpenUrl
19.↵
1. Din NU,
2. Ukoumunne OC,
3. Rubin G,
4. et al.
(2015) Age and gender variations in cancer diagnostic intervals in 15 cancers: analysis of data from the UK Clinical Practice Research Datalink. PLoS One 10(5):e0127717.
OpenUrl
20.↵
1. Howell DA,
2. Smith AG,
3. Roman E
(2008) Help-seeking behaviour in patients with lymphoma. Eur J Cancer Care (Engl) 17(4):394–403.
OpenUrl PubMed
21.↵
1. Black G,
2. Sheringham J,
3. Spencer-Hughes V,
4. et al.
(2015) Patients’ experiences of cancer diagnosis as a result of an emergency presentation: a qualitative study. PLoS One 10(8):e0135027.
OpenUrl
22.↵
1. Wall C,
2. Glenn S,
3. Poole H
(2011) Experiences prior to diagnosis of non-Hodgkin lymphoma: a phenomenological study. J Adv Nurs 67(11):2363–2372.
OpenUrl PubMed
23.↵
1. Smith A,
2. Howell D,
3. Crouch S,
4. et al.
(2018) Cohort profile: the Haematological Malignancy Research Network (HMRN): a UK population-based patient cohort. Int J Epidemiol 47(3):700–700g.
OpenUrl
24.↵
1. Tong A,
2. Sainsbury P,
3. Craig J
(2007) Consolidated criteria for reporting qualitative research (COREQ): a 32-item checklist for interviews and focus groups. Int J Qual Health Care 19(6):349–357.
OpenUrl CrossRef PubMed
25.↵
1. O’Brien BC,
2. Harris IB,
3. Beckman TJ,
4. et al.
(2014) Standards for reporting qualitative research: a synthesis of recommendations. Acad Med 89(9):1245–1251.
OpenUrl CrossRef PubMed
26.↵
1. Smith A,
2. Howell D,
3. Patmore R,
4. et al.
(2011) Incidence of haematological malignancy by sub-type: a report from the Haematological Malignancy Research Network. Br J Cancer 105(11):1684–1692.
OpenUrl CrossRef PubMed
27.↵
1. Swerdlow SH,
2. Campo E,
3. Pileri SA,
4. et al.
(2016) The 2016 revision of the World Health Organization classification of lymphoid neoplasms. Blood 127(20):2375–2390.
OpenUrl Abstract/FREE Full Text
28.↵
1. Sandelowski M
(2000) Whatever happened to qualitative description? Res Nurs Health 23(4):334–340.
OpenUrl CrossRef PubMed
29.↵
1. Sandelowski M
(2010) What’s in a name? Qualitative description revisited. Res Nurs Health 33(1):77–84.
OpenUrl CrossRef PubMed
30.↵
1. Glaser BG,
2. Strauss AL
(1967) The discovery of grounded theory: strategies for qualitative research (Aldine De Gruyter, New York, NY).
31.↵
1. Charmaz K
(2006) Constructing grounded theory: a practical guide through qualitative analysis (Sage Publications, London).
32.↵
1. Weller D,
2. Vedsted P,
3. Rubin G,
4. et al.
(2012) The Aarhus statement: improving design and reporting of studies on early cancer diagnosis. Br J Cancer 106(7):1262–1267.
OpenUrl CrossRef PubMed
33.↵
1. Lincoln YS,
2. Guba EG
(1985) Naturalistic inquiry (Sage Publications, Newbury Park, CA).
34.↵
1. Green J,
2. Thorogood N
(2018) Qualitative methods for health research (Sage Publications, London), 4th edn.
35.↵
1. Macleod U,
2. Mitchell ED,
3. Burgess C,
4. et al.
(2009) Risk factors for delayed presentation and referral of symptomatic cancer: evidence for common cancers. Br J Cancer 101(Suppl 2):S92–S101.
OpenUrl CrossRef PubMed
36.
1. Smith LK,
2. Pope C,
3. Botha JL
(2005) Patients’ help-seeking experiences and delay in cancer presentation: a qualitative synthesis. Lancet 366(9488):825–831.
OpenUrl CrossRef PubMed
37.↵
1. Corner J,
2. Hopkinson J,
3. Roffe L
(2006) Experience of health changes and reasons for delay in seeking care: a UK study of the months prior to the diagnosis of lung cancer. Soc Sci Med 62(6):1381–1391.
OpenUrl CrossRef PubMed
38.↵
1. Almond S,
2. Mant D,
3. Thompson M
(2009) Diagnostic safety-netting. Br J Gen Pract 59(568):872–874.
OpenUrl FREE Full Text
39.↵
1. Lymphoma Action.
Symptoms of lymphoma. https://lymphoma-action.org.uk/symptoms-of-lymphoma (accessed 10 Dec 2018).
40.↵
1. Evans J,
2. Chapple A,
3. Salisbury H,
4. et al.
(2014) ‘It can’t be very important because it comes and goes’: patients’ accounts of intermittent symptoms preceding a pancreatic cancer diagnosis: a qualitative study. BMJ Open 4(2):e004215.
OpenUrl Abstract/FREE Full Text
41.↵
1. Mitchell ED,
2. Rubin G,
3. Merriman L,
4. Macleod U
(2015) The role of primary care in cancer diagnosis via emergency presentation: qualitative synthesis of significant event reports. Br J Cancer 112(Suppl 1):S50–S56.
OpenUrl PubMed
42.↵
1. Renzi C,
2. Whitaker KL,
3. Winstanley K,
4. et al.
(2016) Br J Gen Pract, Unintended consequences of an ‘all-clear’ diagnosis for potential cancer symptoms: a nested qualitative interview study with primary care patients. DOI: https://doi.org/10.3399/bjgp16X683845.
43.↵
1. Lyratzopoulos G,
2. Vedsted P,
3. Singh H
(2015) Understanding missed opportunities for more timely diagnosis of cancer in symptomatic patients after presentation. Br J Cancer 112(Suppl 1):S84–S91.
OpenUrl CrossRef PubMed
44.↵
1. Heyhoe J,
2. Reynolds C,
3. Dunning A,
4. et al.
(2018) Br J Gen Pract, Patient involvement in diagnosing cancer in primary care: a systematic review of current interventions. DOI: https://doi.org/10.3399/bjgp18X695045.
45.↵
1. Ironmonger L,
2. Ohuma E,
3. Ormiston-Smith N,
4. et al.
(2015) An evaluation of the impact of large-scale interventions to raise public awareness of a lung cancer symptom. Br J Cancer 112(1):207–216.
OpenUrl CrossRef PubMed
46.↵
1. NHS
(2014) Be clear on cancer evaluation update. https://www.cancerresearchuk.org/sites/default/files/evaluation_results_2014.pdf (accessed 10 Dec 2018).
47.↵
1. Abel GA,
2. Mendonca SC,
3. McPhail S,
4. et al.
(2017) Br J Gen Pract, Emergency diagnosis of cancer and previous general practice consultations: insights from linked patient survey data. DOI: https://doi.org/10.3399/bjgp17X690869.
48.↵
1. Rubin G,
2. Elliott K,
3. McPhail S
(2011) National audit of cancer diagnosis in primary care (Royal College of General Practitioners).
49.↵
1. Shephard EA,
2. Neal RD,
3. Rose PW,
4. et al.
(2015) Br J Gen Pract, Quantifying the risk of non-Hodgkin lymphoma in symptomatic primary care patients aged ≥40 years: a large case-control study using electronic records. DOI: https://doi.org/10.3399/bjgp15X684793.
50.↵
1. Shephard EA,
2. Neal RD,
3. Rose PW,
4. et al.
(2015) Br J Gen Pract, Quantifying the risk of Hodgkin lymphoma in symptomatic primary care patients aged ≥40 years: a case–control study using electronic records. DOI: https://doi.org/10.3399/bjgp15X684793.
51.↵
1. Green T,
2. Atkin K,
3. Macleod U
(2015) Cancer detection in primary care: insights from general practitioners. Br J Cancer 112(Suppl 1):S41–S49.
OpenUrl
52.↵
1. UK Cancer Research
Safety netting. https://www.cancerresearchuk.org/health-professional/diagnosis/suspected-cancer-referral-best-practice/safety-netting (accessed 10 Dec 2018).
53.↵
1. Bankhead C,
2. Heneghan C,
3. Hewitson P,
4. Thompson M
(2011) Safety netting to improve early cancer diagnosis in primary care: development of consensus guidelines (Department of Primary Health Care, University of Oxford, Oxford).
54.↵
1. Lewis R
(2017) Improving diagnostic pathways for patients with vague symptoms. (Accelerate, Coordinate, Evaluate (ACE) Programme), https://www.macmillan.org.uk/_images/ace-vague-symptoms-report-final_tcm9-311011.pdf (accessed 10 Dec 2018).

In this issue

Download PDF

Download PowerPoint

Email Article

Citation Tools

Keywords

More in this TOC Section

Show more Research

Cited By...

Intended for Healthcare Professionals

[1] 1.↵
Haematology Malignancy Research Network
QuickStats, https://www.hmrn.org/statistics/quick (accessed 10 Dec 2018).

[2] Haematology Malignancy Research Network

[3] 2.↵
Smith A,
Crouch S,
Lax S,
et al.
(2015) Lymphoma incidence, survival and prevalence 2004–2014: sub-type analyses from the UK’s Haematological Malignancy Research Network. Br J Cancer 112(9):1575–1584.
OpenUrl CrossRef PubMed

[4] Smith A,

[5] Crouch S,

[6] Lax S,

[7] et al.

[8] 3.↵
Thomson CS,
Forman D
(2009) Cancer survival in England and the influence of early diagnosis: what can we learn from recent EUROCARE results? Br J Cancer 101(Suppl 2):S102–S109.
OpenUrl CrossRef PubMed

[9] Thomson CS,

[10] Forman D

[11] 4.↵
Neal RD,
Tharmanathan P,
France B,
et al.
(2015) Is increased time to diagnosis and treatment in symptomatic cancer associated with poorer outcomes? Systematic review. Br J Cancer 112(Suppl 1):S92–S107.
OpenUrl CrossRef PubMed

[12] Neal RD,

[13] Tharmanathan P,

[14] France B,

[15] et al.

[16] 5.↵
Howell DA,
Smith AG,
Jack A,
et al.
(2013) Time-to-diagnosis and symptoms of myeloma, lymphomas and leukaemias: a report from the Haematological Malignancy Research Network. BMC Hematol 13(1):9.
OpenUrl CrossRef PubMed

[17] Howell DA,

[18] Smith AG,

[19] Jack A,

[20] et al.

[21] 6.↵
Swann R,
McPhail S,
Witt J,
et al.
(2018) Br J Gen Pract, Diagnosing cancer in primary care: results from the National Cancer Diagnosis Audit. DOI: https://doi.org/10.3399/bjgp17X694169.

[22] Swann R,

[23] McPhail S,

[24] Witt J,

[25] et al.

[26] 7.↵
National Institute for Health and Care Excellence
(2015) Suspected cancer: recognition and referral NG12 (NICE, London) https://www.nice.org.uk/guidance/ng12 (accessed 11 Jan 2018).

[27] National Institute for Health and Care Excellence

[28] 8.↵
Neal RD,
Din NU,
Hamilton W,
et al.
(2014) Comparison of cancer diagnostic intervals before and after implementation of NICE guidelines: analysis of data from the UK General Practice Research Database. Br J Cancer 110(3):584–592.
OpenUrl CrossRef PubMed

[29] Neal RD,

[30] Din NU,

[31] Hamilton W,

[32] et al.

[33] 9.↵
Lyratzopoulos G,
Neal RD,
Barbiere JM,
et al.
(2012) Variation in number of general practitioner consultations before hospital referral for cancer: findings from the 2010 National Cancer Patient Experience Survey in England. Lancet Oncol 13(4):353–365.
OpenUrl CrossRef PubMed

[34] Lyratzopoulos G,

[35] Neal RD,

[36] Barbiere JM,

[37] et al.

[38] 10.↵
Zhou Y,
Mendonca SC,
Abel GA,
et al.
(2018) Variation in ‘fast-track’ referrals for suspected cancer by patient characteristic and cancer diagnosis: evidence from 670 000 patients with cancers of 35 different sites. Br J Cancer 118(1):24–31.
OpenUrl

[39] Zhou Y,

[40] Mendonca SC,

[41] Abel GA,

[42] et al.

[43] 11.↵
Kane E,
Howell D,
Smith A,
et al.
(2017) Emergency admission and survival from aggressive non-Hodgkin lymphoma: a report from the UK’s population-based Haematological Malignancy Research Network. Eur J Cancer 78:53–60.
OpenUrl

[44] Kane E,

[45] Howell D,

[46] Smith A,

[47] et al.

[48] 12.↵
Lyratzopoulos G,
Saunders CL,
Abel GA,
et al.
(2015) The relative length of the patient and the primary care interval in patients with 28 common and rarer cancers. Br J Cancer 112(Suppl 1):S35–S40.
OpenUrl CrossRef PubMed

[49] Lyratzopoulos G,

[50] Saunders CL,

[51] Abel GA,

[52] et al.

[53] 13.↵
Keeble S,
Abel GA,
Saunders CL,
et al.
(2014) Variation in promptness of presentation among 10,297 patients subsequently diagnosed with one of 18 cancers: evidence from a National Audit of Cancer Diagnosis in Primary Care. Int J Cancer 135(5):1220–1228.
OpenUrl CrossRef PubMed

[54] Keeble S,

[55] Abel GA,

[56] Saunders CL,

[57] et al.

[58] 14.↵
Walter F,
Webster A,
Scott S,
Emery J
(2012) The Andersen Model of Total Patient Delay: a systematic review of its application in cancer diagnosis. J Health Serv Res Policy 17(2):110–118.
OpenUrl CrossRef PubMed

[59] Walter F,

[60] Webster A,

[61] Scott S,

[62] Emery J

[63] 15.↵
Scott SE,
Walter FM,
Webster A,
et al.
(2013) The model of pathways to treatment: conceptualization and integration with existing theory. Br J Health Psychol 18(1):45–65.
OpenUrl CrossRef PubMed

[64] Scott SE,

[65] Walter FM,

[66] Webster A,

[67] et al.

[68] 16.↵
Andersen BL,
Cacioppo JT
(1995) Delay in seeking a cancer diagnosis: delay stages and psychophysiological comparison processes. Br J Soc Psychol 34(Pt 1):33–52.
OpenUrl CrossRef PubMed

[69] Andersen BL,

[70] Cacioppo JT

[71] 17.↵
Safer MA,
Tharps QJ,
Jackson TC,
Leventhal H
(1979) Determinants of three stages of delay in seeking care at a medical clinic. Med Care 17(1):11–29.
OpenUrl PubMed

[72] Safer MA,

[73] Tharps QJ,

[74] Jackson TC,

[75] Leventhal H

[76] 18.↵
Howell DA,
Warburton F,
Ramirez AJ,
et al.
(2015) Risk factors and time to symptomatic presentation in leukaemia, lymphoma and myeloma. Br J Cancer 113(7):1114–1120.
OpenUrl

[77] Howell DA,

[78] Warburton F,

[79] Ramirez AJ,

[80] et al.

[81] 19.↵
Din NU,
Ukoumunne OC,
Rubin G,
et al.
(2015) Age and gender variations in cancer diagnostic intervals in 15 cancers: analysis of data from the UK Clinical Practice Research Datalink. PLoS One 10(5):e0127717.
OpenUrl

[82] Din NU,

[83] Ukoumunne OC,

[84] Rubin G,

[85] et al.

[86] 20.↵
Howell DA,
Smith AG,
Roman E
(2008) Help-seeking behaviour in patients with lymphoma. Eur J Cancer Care (Engl) 17(4):394–403.
OpenUrl PubMed

[87] Howell DA,

[88] Smith AG,

[89] Roman E

[90] 21.↵
Black G,
Sheringham J,
Spencer-Hughes V,
et al.
(2015) Patients’ experiences of cancer diagnosis as a result of an emergency presentation: a qualitative study. PLoS One 10(8):e0135027.
OpenUrl

[91] Black G,

[92] Sheringham J,

[93] Spencer-Hughes V,

[94] et al.

[95] 22.↵
Wall C,
Glenn S,
Poole H
(2011) Experiences prior to diagnosis of non-Hodgkin lymphoma: a phenomenological study. J Adv Nurs 67(11):2363–2372.
OpenUrl PubMed

[96] Wall C,

[97] Glenn S,

[98] Poole H

[99] 23.↵
Smith A,
Howell D,
Crouch S,
et al.
(2018) Cohort profile: the Haematological Malignancy Research Network (HMRN): a UK population-based patient cohort. Int J Epidemiol 47(3):700–700g.
OpenUrl

[100] Smith A,

[101] Howell D,

[102] Crouch S,

[103] et al.

[104] 24.↵
Tong A,
Sainsbury P,
Craig J
(2007) Consolidated criteria for reporting qualitative research (COREQ): a 32-item checklist for interviews and focus groups. Int J Qual Health Care 19(6):349–357.
OpenUrl CrossRef PubMed

[105] Tong A,

[106] Sainsbury P,

[107] Craig J

[108] 25.↵
O’Brien BC,
Harris IB,
Beckman TJ,
et al.
(2014) Standards for reporting qualitative research: a synthesis of recommendations. Acad Med 89(9):1245–1251.
OpenUrl CrossRef PubMed

[109] O’Brien BC,

[110] Harris IB,

[111] Beckman TJ,

[112] et al.

[113] 26.↵
Smith A,
Howell D,
Patmore R,
et al.
(2011) Incidence of haematological malignancy by sub-type: a report from the Haematological Malignancy Research Network. Br J Cancer 105(11):1684–1692.
OpenUrl CrossRef PubMed

[114] Smith A,

[115] Howell D,

[116] Patmore R,

[117] et al.

[118] 27.↵
Swerdlow SH,
Campo E,
Pileri SA,
et al.
(2016) The 2016 revision of the World Health Organization classification of lymphoid neoplasms. Blood 127(20):2375–2390.
OpenUrl Abstract/FREE Full Text

[119] Swerdlow SH,

[120] Campo E,

[121] Pileri SA,

[122] et al.

[123] 28.↵
Sandelowski M
(2000) Whatever happened to qualitative description? Res Nurs Health 23(4):334–340.
OpenUrl CrossRef PubMed

[124] Sandelowski M

[125] 29.↵
Sandelowski M
(2010) What’s in a name? Qualitative description revisited. Res Nurs Health 33(1):77–84.
OpenUrl CrossRef PubMed

[126] Sandelowski M

[127] 30.↵
Glaser BG,
Strauss AL
(1967) The discovery of grounded theory: strategies for qualitative research (Aldine De Gruyter, New York, NY).

[128] Glaser BG,

[129] Strauss AL

[130] 31.↵
Charmaz K
(2006) Constructing grounded theory: a practical guide through qualitative analysis (Sage Publications, London).

[131] Charmaz K

[132] 32.↵
Weller D,
Vedsted P,
Rubin G,
et al.
(2012) The Aarhus statement: improving design and reporting of studies on early cancer diagnosis. Br J Cancer 106(7):1262–1267.
OpenUrl CrossRef PubMed

[133] Weller D,

[134] Vedsted P,

[135] Rubin G,

[136] et al.

[137] 33.↵
Lincoln YS,
Guba EG
(1985) Naturalistic inquiry (Sage Publications, Newbury Park, CA).

[138] Lincoln YS,

[139] Guba EG

[140] 34.↵
Green J,
Thorogood N
(2018) Qualitative methods for health research (Sage Publications, London), 4th edn.

[141] Green J,

[142] Thorogood N

[143] 35.↵
Macleod U,
Mitchell ED,
Burgess C,
et al.
(2009) Risk factors for delayed presentation and referral of symptomatic cancer: evidence for common cancers. Br J Cancer 101(Suppl 2):S92–S101.
OpenUrl CrossRef PubMed

[144] Macleod U,

[145] Mitchell ED,

[146] Burgess C,

[147] et al.

[148] 36.
Smith LK,
Pope C,
Botha JL
(2005) Patients’ help-seeking experiences and delay in cancer presentation: a qualitative synthesis. Lancet 366(9488):825–831.
OpenUrl CrossRef PubMed

[149] Smith LK,

[150] Pope C,

[151] Botha JL

[152] 37.↵
Corner J,
Hopkinson J,
Roffe L
(2006) Experience of health changes and reasons for delay in seeking care: a UK study of the months prior to the diagnosis of lung cancer. Soc Sci Med 62(6):1381–1391.
OpenUrl CrossRef PubMed

[153] Corner J,

[154] Hopkinson J,

[155] Roffe L

[156] 38.↵
Almond S,
Mant D,
Thompson M
(2009) Diagnostic safety-netting. Br J Gen Pract 59(568):872–874.
OpenUrl FREE Full Text

[157] Almond S,

[158] Mant D,

[159] Thompson M

[160] 39.↵
Lymphoma Action.
Symptoms of lymphoma. https://lymphoma-action.org.uk/symptoms-of-lymphoma (accessed 10 Dec 2018).

[161] Lymphoma Action.

[162] 40.↵
Evans J,
Chapple A,
Salisbury H,
et al.
(2014) ‘It can’t be very important because it comes and goes’: patients’ accounts of intermittent symptoms preceding a pancreatic cancer diagnosis: a qualitative study. BMJ Open 4(2):e004215.
OpenUrl Abstract/FREE Full Text

[163] Evans J,

[164] Chapple A,

[165] Salisbury H,

[166] et al.

[167] 41.↵
Mitchell ED,
Rubin G,
Merriman L,
Macleod U
(2015) The role of primary care in cancer diagnosis via emergency presentation: qualitative synthesis of significant event reports. Br J Cancer 112(Suppl 1):S50–S56.
OpenUrl PubMed

[168] Mitchell ED,

[169] Rubin G,

[170] Merriman L,

[171] Macleod U

[172] 42.↵
Renzi C,
Whitaker KL,
Winstanley K,
et al.
(2016) Br J Gen Pract, Unintended consequences of an ‘all-clear’ diagnosis for potential cancer symptoms: a nested qualitative interview study with primary care patients. DOI: https://doi.org/10.3399/bjgp16X683845.

[173] Renzi C,

[174] Whitaker KL,

[175] Winstanley K,

[176] et al.

[177] 43.↵
Lyratzopoulos G,
Vedsted P,
Singh H
(2015) Understanding missed opportunities for more timely diagnosis of cancer in symptomatic patients after presentation. Br J Cancer 112(Suppl 1):S84–S91.
OpenUrl CrossRef PubMed

[178] Lyratzopoulos G,

[179] Vedsted P,

[180] Singh H

[181] 44.↵
Heyhoe J,
Reynolds C,
Dunning A,
et al.
(2018) Br J Gen Pract, Patient involvement in diagnosing cancer in primary care: a systematic review of current interventions. DOI: https://doi.org/10.3399/bjgp18X695045.

[182] Heyhoe J,

[183] Reynolds C,

[184] Dunning A,

[185] et al.

[186] 45.↵
Ironmonger L,
Ohuma E,
Ormiston-Smith N,
et al.
(2015) An evaluation of the impact of large-scale interventions to raise public awareness of a lung cancer symptom. Br J Cancer 112(1):207–216.
OpenUrl CrossRef PubMed

[187] Ironmonger L,

[188] Ohuma E,

[189] Ormiston-Smith N,

[190] et al.

[191] 46.↵
NHS
(2014) Be clear on cancer evaluation update. https://www.cancerresearchuk.org/sites/default/files/evaluation_results_2014.pdf (accessed 10 Dec 2018).

[192] NHS

[193] 47.↵
Abel GA,
Mendonca SC,
McPhail S,
et al.
(2017) Br J Gen Pract, Emergency diagnosis of cancer and previous general practice consultations: insights from linked patient survey data. DOI: https://doi.org/10.3399/bjgp17X690869.

[194] Abel GA,

[195] Mendonca SC,

[196] McPhail S,

[197] et al.

[198] 48.↵
Rubin G,
Elliott K,
McPhail S
(2011) National audit of cancer diagnosis in primary care (Royal College of General Practitioners).

[199] Rubin G,

[200] Elliott K,

[201] McPhail S

[202] 49.↵
Shephard EA,
Neal RD,
Rose PW,
et al.
(2015) Br J Gen Pract, Quantifying the risk of non-Hodgkin lymphoma in symptomatic primary care patients aged ≥40 years: a large case-control study using electronic records. DOI: https://doi.org/10.3399/bjgp15X684793.

[203] Shephard EA,

[204] Neal RD,

[205] Rose PW,

[206] et al.

[207] 50.↵
Shephard EA,
Neal RD,
Rose PW,
et al.
(2015) Br J Gen Pract, Quantifying the risk of Hodgkin lymphoma in symptomatic primary care patients aged ≥40 years: a case–control study using electronic records. DOI: https://doi.org/10.3399/bjgp15X684793.

[208] Shephard EA,

[209] Neal RD,

[210] Rose PW,

[211] et al.

[212] 51.↵
Green T,
Atkin K,
Macleod U
(2015) Cancer detection in primary care: insights from general practitioners. Br J Cancer 112(Suppl 1):S41–S49.
OpenUrl

[213] Green T,

[214] Atkin K,

[215] Macleod U

[216] 52.↵
UK Cancer Research
Safety netting. https://www.cancerresearchuk.org/health-professional/diagnosis/suspected-cancer-referral-best-practice/safety-netting (accessed 10 Dec 2018).

[217] UK Cancer Research

[218] 53.↵
Bankhead C,
Heneghan C,
Hewitson P,
Thompson M
(2011) Safety netting to improve early cancer diagnosis in primary care: development of consensus guidelines (Department of Primary Health Care, University of Oxford, Oxford).

[219] Bankhead C,

[220] Heneghan C,

[221] Hewitson P,

[222] Thompson M

[223] 54.↵
Lewis R
(2017) Improving diagnostic pathways for patients with vague symptoms. (Accelerate, Coordinate, Evaluate (ACE) Programme), https://www.macmillan.org.uk/_images/ace-vague-symptoms-report-final_tcm9-311011.pdf (accessed 10 Dec 2018).

[224] Lewis R

Main menu

User menu

Search