Completed SEAs were received from 92 (45.5%) practices. Most provided a report of one lung cancer diagnosis, although some provided two, generating accounts for a total of 132 cases. The majority of lung diagnoses (84.8%) were made in 2008–2009, with the remainder diagnosed between 2003 and 2007. Average patient age at diagnosis was 67.9 years (standard deviation [SD] 11.1), and almost two-thirds were alive at SEA completion (Table 1).
Insights into the referral process for lung cancer
Patterns of presentation
Although, for many patients, initial presentation was about lung and lung-related symptoms, the nature of the presentations varied hugely (Box 1). In addition to the known tendency for smokers and for those with chronic obstructive pulmonary disease (COPD) to present with chest infection-type symptoms, presentation also occurred in the context of other illnesses. Three main presentation patterns emerged.
Box 1. Patterns of initial presentation in SEA accounts (n = 131)a
Chest symptom or symptom suggestive of malignancy (n = 97)
Symptom not generally indicative of lung cancer (n = 20)
Abdominal or epigastric pain
Arm pain
Atrial fibrillation
Blue lips (noticed by relatives)
Feeling of lump in throat
Lack of coordination of legs
Neck pain
Painful leg
Routine bloods abnormal
Vague symptoms
Weakness of left hand and arm
No presentation in primary care (n = 14)
Admitted to hospital by urgent care team
Accident and emergency attendance for other symptoms
Diagnosed overseas
Emergency admission for other condition
GP noticed rising inflammatory markers and falling haemoglobin on blood results for rheumatic disease
Incidental finding on dementia workup
Referred with lung symptom on follow-up for other cancer
aPresenting symptoms were not described in one SEA report. SEA = significant event audit.
Presentation with a chest symptom or symptom suggestive of malignancy. Haemoptysis, although reported, was described in only 10 of these cases. Much more common was a combination of symptoms that were initially suggestive of a chest infection, indeed almost half of the patients discussed in the SEAs presented in this way.
Presentation with a non-chest symptom that would not generally be considered to indicate lung cancer. For some of these patients, lung cancer was an incidental finding on investigation while, for others, the presentation was simply unusual or reflected metastatic disease.
Events in which diagnosis did not occur as a result of presentation to primary care. For these patients, diagnosis occurred in a variety of ways, including follow-up for other cancers, during work-ups (investigations) for other conditions, and on emergency admission for other causes.
GP responses to presentation
Responses described by GPs — both to initial presentation and subsequent consultations — were generally appropriate and in keeping with best practice.18 At first presentation with new chest symptoms, patients were frequently examined, with findings recorded, antibiotics prescribed, and chest X-ray ordered. Other responses included arranging follow-up review, advising of return if there was no improvement in symptoms, or onward referral to a specialist clinic or other primary care professional (such as a physiotherapist). Most patients were seen more than once and subsequent management was determined by the nature of symptoms; many were re-examined, some had further antibiotics. Those with non-resolving symptoms were commonly sent for a chest X-ray, while patients who became more unwell were often admitted to hospital as emergencies.
Factors related to longer referral for chest symptoms or symptoms suggestive of malignancy
The time interval from initial presentation to referral or acute admission was identifiable in most of the documented accounts, and many examples of good practice were evident (Table 2). In order to better understand the factors that related to longer referrals, accounts where this took more than 1 month (≥31 days) were analysed in detail (n = 45). A timed cut-off was used rather than considering patients with or without a 2-week wait referral (that is, when the patient should be seen by a specialist within 2 weeks of referral by a GP) as not all of the patients had symptoms that might indicate urgent referral. In addition, using type of referral would not provide the appropriate context from which to consider referral delay, as it does not take account of time from initial presentation.
Table 2. Accounts of events demonstrating exemplary practice
Three main themes emerged from analysis of these accounts; they related to issues with the initial chest X-ray report, patient-mediated factors, and complex presentations.
Initial chest X-ray reported as normal or consistent with benign disease.
For many patients, the chest X-ray was reported as normal or as showing no change from previous films. For others, it showed infection, inflammatory changes, or was inconclusive. In one unusual case, the radiologist advised referral to the breast clinic as the mass seen was thought to represent a breast tumour. In many of these cases, the chest X-ray was repeated, commonly as part of the ongoing primary care diagnostic process but, in some instances, at the suggestion of the radiologist.
Patient-mediated factors
There were several accounts in which patient factors had a substantial bearing on referral time. These included waiting several weeks after the first consultation before re-presenting with ongoing symptoms, declining referral when it was first offered or recommended by the GP, failing to attend an appointment at the chest clinic or for a chest X-ray, declining to see the GP when recommended by the nurse, and declining hospital admission.
Complexity of presentation
A number of the accounts described complex cases for which it would have been challenging to reach an earlier diagnosis. This complexity was often related to comorbidity, a plausible alternative diagnosis, or symptoms suggestive of a different malignancy (Box 2).
Box 2. Examples of complexity in the process of referral
Comorbidity
A patient (aged 78 years) presented with cough. Antibiotics were given and a follow-up arranged. The patient attended secondary care three times per week for renal dialysis; four unsuccessful attempts were made by the practice to contact the patient by telephone (patient was assumed to be unreachable because of the dialysis sessions). The patient was eventually admitted to hospital. The GP and community matron were both involved; in addition, the patient was seen at accident and emergency and discharged. On the first emergency admission with breathlessness, a chest X-ray showed fluid overload due to a valvular heart condition. The GP is still unclear as to how a diagnosis was eventually reached.
A healthcare assistant noted that the patient (aged 74 years) was coughing a lot. As the patient had been on an ACEi, initially it was thought that the cough was caused by this. The ACEi was changed to an ARB, to which the patient had a reaction. The patient also had numerous consultations with other symptoms (including numbness in arm, dizziness, shingles-type pain, leg cramps). In addition, a previous CT scan from general medicine showed incidental findings (40 weeks before abnormal chest X-ray). Diagnosis was eventually made on a chest X-ray carried out at a general medicine outpatient appointment; this showed dense left hilum, could be vascular or tumour, and referral to a chest physician was advised (35 weeks after initial consultation).
Plausible alternative diagnosis
A patient (aged 69 years) presented with a shoulder pain and a swollen arm that was red and sore. As the patient had been given the pneumococcal vaccine the day before, this was diagnosed as an adverse reaction. The patient next presented 13 weeks after the initial consultation complaining of back pain for which they had consulted seven times in the previous year. An MRI scan was carried out as there was concern about nerve root signs; this showed an aortic aneurysm and the patient was referred to the vascular surgeons. The patient next attended almost another month later with continuing shoulder pain and pain over the scapula on coughing. As the patient was a heavy smoker, they were sent for a chest X-ray, which showed a mass; an urgent referral was made. The patient’s back pain was not related to the cancer diagnosis.
A patient (aged 63 years) presented with shoulder pain, which had occurred after press-ups and was thought to be due to soft-tissue injury. The patient thought the pain was due to injury, but at the third consultation had also complained of tiredness and weight loss. On the fourth consultation with non-resolving shoulder pain, an urgent chest X-ray was arranged.
Symptoms suggestive of a different malignancy
A patient (aged 75 years) presented with persistent laryngeal discomfort and variable hoarseness, and was referred to ENT. At the ENT clinic, a laryngoscopy was carried out and was normal (approximately 8–12 weeks after initial consult). Symptoms persisted and the patient was re-referred to the ENT clinic approximately 1 year after initial consult; again, no abnormality was found. The patient was then referred to the chest clinic and was seen around 3 months later, when lung cancer was diagnosed.
ACEi = angiotensin converting enzyme inhibitor. ARB = angiotensin receptor blocker. CT = computer tomography. ENT = Ear, nose and throat. MRI = magnetic resonance imaging.
Opportunities for earlier diagnosis of lung cancer involving chest symptoms
Detailed analysis of the accounts highlighted some cases in which opportunities for earlier diagnosis may have been missed. As far as could be determined from the data, nine such cases were described; although these relate to only a small number of the patients who presented with chest symptoms or symptoms suggestive of malignancy, they afford particular opportunities for learning nonetheless (Box 3). The cases illustrated several key issues, most notably around the need for vigilant care.
Box 3. Potential missed opportunities for earlier diagnosis
Patient 1
62-year-old smoker with a 1-week history of cough, which was initially treated as a viral infection. Subsequent presentation 4 months later. Patient had seven consultations with various chest symptoms before being referred 63 weeks after first presentation.
Patient 2
Patient with two consultations, 3 weeks apart, for upper respiratory tract infection symptoms. Next presented 6 weeks later with shortness of breath, at which point a chest X-ray was carried out.
Patient 3
Increasing shortness of breath in a 63-year-old patient with known asbestos exposure. Chest X-ray ordered 2 months after initial consultation.
Patient 4
66-year-old patient with known COPD was seen five times over a 5-month period with exacerbations. Sent for chest X-ray after complaining of weight loss.
Patient 5
59-year-old non-smoker with 3-week history of cough was given antibiotics at initial presentation. Next presented 2 months later, still coughing, and was sent for urgent chest X-ray.
Patient 6
64-year-old patient with known COPD, well known to the respiratory team, presented with increasing shortness of breath, cough, wheeze, and leg weakness. A specialist respiratory nurse was also involved. Referral was made when symptoms worsened, by which time patient had superior vena cava obstruction.
Patient 7
59-year-old patient with a 2-month history of persistent cough with yellow phlegm was prescribed antibiotics. Chest X-ray was arranged at next presentation 2 months later.
Patient 8
82-year-old patient presented with a chesty cough with purulent sputum. Next presented 4 weeks later with similar symptoms, then again 3 weeks later. Chest X-ray was arranged at fourth consultation.
Patient 9
Patient presented with new onset of wheezing, and was seen several times with chest symptoms before chest X-ray was ordered. Patient factors also relevant as had a fear of investigations and hospitals.
COPD = chronic obstructive pulmonary disease.
Factors related to longer time to referral for non-chest symptoms
Of the accounts relating to patients who presented with symptoms that were not chest or malignancy related, five waited longer than 1 month before being referred. All had reasonable explanations for the longer referral interval (Box 4).
Box 4. Cases of longer time to referral for non-chest symptoms
Patient 1
Presented with epigastric pain; referral was made to gastroenterology after an ultrasound showed liver metastases.
Patient 2
Presented with neck pain and nausea. An ultrasound arranged by gastroenterology showed a pelvic mass and ovarian cancer was eventually diagnosed. A CT scan performed during work-up showed lung cancer, which appears to have been an incidental finding.
Patient 3
Presented with painful left arm. Pain was initially thought to be musculoskeletal so the patient was referred to physiotherapy 1 day after initial consultation. The physiotherapist suggested referral to orthopaedics some weeks later. Diagnosis was eventually non-small cell cancer invading the brachial plexus.
Patient 4
Presented with left arm and neck pain. Patient was referred to physiotherapy, although had normal investigations following an episode of haemoptysis within the previous year.
Patient 5
Presented with diarrhoea. Hyponatraemia was found during investigations for diarrhoea, but the initial chest X-ray was inconclusive.
CT = computer tomography.
Lessons learned in the diagnosis of lung cancer
The ways in which GPs described the circumstances surrounding these events indicated that they had learned from reflecting on, and discussing, the case — even if the process from initial patient presentation to referral had been ideal. Areas of learning highlighted by practices related to:
Presentation and diagnosis
Lessons learned around presentation and diagnosis of lung cancer centred on the: complexity associated with atypical symptoms; need for vigilance, even when symptoms seem straightforward; and usefulness and limitations of chest X-ray as a diagnostic tool:
‘… [the case] reminded all team members that cancer can have few general symptoms until disease is advanced, that patients may underplay symptoms, and that a simple, brief examination can reveal significant findings and is always worth doing even it if does not appear to be indicated.’ (LN-153A)
‘Always be aware of changes in patients with chronic chest disease and have a high suspicion for further investigation. Don’t assume it is simply the underlying problem.’ (LO-008B)
‘Chest X-rays are non invasive, cheap and easily arranged and we will continue to use them readily to pursue clinical suspicions.’ (LN-080A)
Practitioners considered the importance of chest X-ray in patients with prolonged symptoms, even if examination suggested infection, as well as the appropriate time for referral for chest X-ray in such patients. The question was also raised as to whether chest X-ray should be routinely used in the assessment for possible COPD, and whether patients with abnormal chest X-ray should be referred under the 2-week wait as a precaution.
System issues and the primary–secondary care interface
Many of the comments in this area focused on communication and record keeping, either between members of the primary care team, between primary and secondary care, or between primary care and other providers such as Macmillan nurses:
‘It was acknowledged that communication between clinicians is vitally important in the current climate of general practice as patients may not always be able to consult with the same GP on every occasion. Good documentation [is] paramount to ensure other clinicians have enough information to make further clinical decisions.’ (LN-168A)
In the main, the SEA accounts described examples of good team working and communication, but there were some instances of apparent lack of adequate communication at the primary–secondary care interface. This included the non-reporting of X-rays and a failure to provide practices with test results, or discharge or follow-up arrangements:
‘Poor communication from secondary to primary care. This [the details of the case] should have been noted and the information requested from the hospital rather than relying on patients accounts.’ (LN-034A)
Patient factors
There was recognition among practitioners that co-existing disease could mask symptoms of malignancy:
‘We reflected on other cases of lung cancer when delays in diagnosis had been present. Major causes of delay included delay in patient presentation and confusion of symptoms with co-existing illness such as COPD.’ (LN-036A)
As such, the possibility of a serious cause should be considered in patients with an existing respiratory condition (for example, asthma or COPD) or another disease. Similarly, the importance of having a high index of suspicion in patients who are smokers was also identified. Allied to this, was acknowledgement of a continuing need for patient education around smoking cessation and cancer symptoms in general:
‘We, as a team, felt that what is important is the patient education regarding these unspecific symptoms such as weight loss, “not entirely well”, tired all the time… [These] should be the points to advertise in surgeries, local/national papers.’ (LN-179A)
Practitioner issues
Practitioners described the importance of, and need for, safety-netting: the inclusion of a back-up process for dealing with an alternative outcome to the initial working diagnosis.19 Some practitioners used the term explicitly in their narratives, commenting on its importance as part of the consultation. The concept was also discussed more implicitly in relation to various aspects of diagnosis and management, including history taking and examination, follow-up (both of non-resolving symptoms and of negative test results), and ensuring continuity across consultations:
‘We are all agreed that safety-netting is an important part of the consultation. The natural history of the symptoms and information provided need to be clearly recorded. Routinely asking all patients to return for a check up following an infection, however, is not felt to be beneficial.’ (LN-081A)
‘Clinical awareness and examination are essential to get an early diagnosis.’ (LN-088A)
The role of guidelines
As part of the SEA process, GPs had often reviewed the role, content, and use within the practice of existing local and national guidelines, as well as the referral pathways involved in the documented cases:
‘[The] 2-week rule lung cancer referral guidelines were discussed and indications/criteria for referral were reinforced.’ (LN-187B)
‘We discussed the problems of using TWR [2-week rule] referrals for unclear CXR [chest X-ray] pathology as too many inappropriate urgent referrals just clogs the system.’ (LN-026A)
In many instances, the lessons learned related to the fact that guidelines had been followed. In others, however, they related to guidelines being inappropriate given the associated circumstances, including symptoms at initial presentation not meeting the criteria for referral, the patient presenting elsewhere (such as accident and emergency), the patient already being under specialist care, or the patient not wanting to be referred:
‘While the 2WW guidelines might have indicated a need for more rapid referral, in this case the patient and family were quite clear that active intervention was not wanted … As a result the referral pathway was negotiated with the patient, who retained control of that process and ongoing treatment. Although there is pressure to comply with guidelines it is important to remain patient centred.’ (LN-018A)
