Diagnosing cancer in primary care: results from the National Cancer Diagnosis Audit

Ruth Swann; Sean McPhail; Jana Witt; Brian Shand; Gary A Abel; Sara Hiom; Jem Rashbass; Georgios Lyratzopoulos; Greg Rubin; The National Cancer Diagnosis Audit Steering Group

doi:10.3399/bjgp17X694169

Abstract

Background Continual improvements in diagnostic processes are needed to minimise the proportion of patients with cancer who experience diagnostic delays. Clinical audit is a means of achieving this.

Aim To characterise key aspects of the diagnostic process for cancer and to generate baseline measures for future re-audit.

Design and setting Clinical audit of cancer diagnosis in general practices in England.

Method Information on patient and tumour characteristics held in the English National Cancer Registry was supplemented by information from GPs in participating practices. Data items included diagnostic timepoints, patient characteristics, and clinical management.

Results Data were collected on 17 042 patients with a new diagnosis of cancer during 2014 from 439 practices. Participating practices were similar to non-participating ones, particularly regarding population age, urban/rural location, and practice-based patient experience measures. The median diagnostic interval for all patients was 40 days (interquartile range [IQR] 15–86 days). Most patients were referred promptly (median primary care interval 5 days [IQR 0–27 days]). Where GPs deemed diagnostic delays to have occurred (22% of cases), patient, clinician, or system factors were responsible in 26%, 28%, and 34% of instances, respectively. Safety netting was recorded for 44% of patients. At least one primary care-led investigation was carried out for 45% of patients. Most patients (76%) had at least one existing comorbid condition; 21% had three or more.

Conclusion The findings identify avenues for quality improvement activity and provide a baseline for future audit of the impact of 2015 National Institute for Health and Care Excellence guidance on management and referral of suspected cancer.

INTRODUCTION

The timeliness of cancer diagnosis in patients who present with symptoms has long been a cause of public, professional, and political concern. The result has been an increasing focus on achieving earlier diagnosis,¹^,² supported by growing evidence for associations between time to diagnosis and clinical and patient experience outcomes,³^,⁴ and evidence of substantial variation in clinical primary care practice.⁵ Differences in cancer outcomes between the UK and other comparable health systems are thought to partly reflect differences in diagnostic timeliness, and insights into processes that might underpin these differences have been generated through the International Cancer Benchmarking Partnership.⁶

Forming part of the National Awareness and Early Diagnosis Initiative,⁷ the first English National Audit of Cancer Diagnosis in Primary Care (NACDPC) was undertaken in 2009–2010 in order to gain an understanding of the diagnostic process in primary care for patients subsequently diagnosed with cancer.⁸ It included information on 18 879 patients diagnosed with cancer, identified from the registers of nearly 1200 practices, and provided detailed information on the primary care pathways to cancer diagnosis.

The Achieving World Class Cancer Outcomes cancer strategy 2015–2020 contained a commitment to a second national audit of cancer diagnosis, alongside specific recommendations for clinical practice and the organisation of diagnostic services.⁹ It suggested that precautionary ‘safety netting’¹⁰^,¹¹ becomes more established and that direct access for GPs to diagnostic tests be increased, additionally including a target for achieving diagnostic resolution (cancer diagnosed or ruled out) in most patients within 28 days of referral.⁹ Building on the 2009–2010 NACDPC, a National Cancer Diagnosis Audit (NCDA) was formulated as a collaborative initiative between the key UK agencies in cancer diagnosis.

The aim of the NCDA was to generate a detailed understanding of the diagnostic process for cancer in primary care for patients who were diagnosed during 2014. At a national level, it would provide a baseline against which the impact of large-scale interventions, such as the revised 2015 National Institute for Health and Care Excellence (NICE) guidance for recognition and referral of patients with suspected cancer and the new national cancer strategy, could be re-audited in future.⁹^,¹¹ At a practice level, the indicators selected would map to cancer standards and guidelines in order to support quality improvement initiatives.

How this fits in

Unlike most previous studies, the National Cancer Diagnosis Audit has collected primary care referral data for a comparatively large and population-based cohort of patients with cancer. The audit aims to further understand the patient pathway from primary care to diagnosis, and to highlight where improvements can be made, shortening the time interval from presentation to diagnosis. It also provides a baseline for future audits to assess the impact of the 2015 National Institute for Health and Care Excellence guidelines on the recognition and referral of patients with suspected cancer. The authors summarise key methodological aspects of this project and its principal findings.

METHOD

Data

After excluding non-melanoma skin cancer, all incident malignant cancer cases among England residents in 2014 (n = 296 231) were assigned to the general practice in which they were registered at the time of their cancer diagnosis, using information from the Hospital Episodes Statistics and Cancer Waiting Times datasets (which hold patient administration and cancer target compliance data, respectively).

Participation in the NCDA was voluntary and promoted through the Royal College of General Practitioners’ (RCGP) website and e-newsletters to its members, and through Cancer Research UK and Macmillan Cancer Support primary care engagement processes. Once registered and verified, practices had access, via a secure web portal developed by Public Health England’s (PHE) National Cancer Registration and Analysis Service (NCRAS), to a list of all patients who were diagnosed with cancer in 2014 while registered at their practice. Verified GPs and other practice health professionals could then enter primary care data on the patient’s characteristics, place of presentation and symptoms presented, primary care-led investigations, the number of pre-referral consultations, the referral pathway, whether there was evidence of safety netting, and any diagnostic delays incurred. The audit portal remained open from September 2016 to February 2017.

Except for dates, all responses were selected from drop-down menus with predefined answers. Categories of avoidable delay were based on a taxonomy previously generated through analysis of free-text responses contained in the NACDPC.¹² Practices could verify screening-detection status but were not required to provide data on these cases. A payment of £10 per tumour record was given to participating practices that returned information on 95% or more of their NCDA patients (365 practices). Some clinical commissioning groups (CCGs) had encouraged participation through local incentive schemes before this funding became available and were later reimbursed.

Analysis

The authors describe key variables by sex, age group (0–24, 25–49, 50–64, 65–74, 75–84 and ≥85 years), and cancer site (for the 20 sites comprising >1% of the sample: bladder, brain, breast, cancer of unknown primary, colon, endometrial, leukaemia, liver, lung, lymphoma, melanoma, multiple myeloma, oesophageal, oral/oropharyngeal, ovarian, pancreatic, prostate, rectal, renal, stomach [all n ≥265]). The distribution of sex, age, stage at diagnosis, and cancer site of the NCDA cohort was compared with the 2014 national cancer registration statistics.¹³ Similarly, participating and non-participating practices were compared in respect of their key characteristics, key aspects of patients’ experience of primary care (access, continuity, satisfaction, and doctor communication) as reported by the 2013–2014 NHS General Practice Patient Survey (GPPS), https://gp-patient.co.uk, and rates of use of the 2-week wait (TWW) referrals for suspected cancer and related metrics (in England, clinical guidelines enable GPs to refer patients for specialist assessment within 2 weeks when certain symptoms are present and cancer is a suspected diagnosis).¹¹

Primary care-led investigations were grouped into blood, urinary, imaging, endoscopy, and other tests. The number of pre-referral consultations and also the number of comorbidities were categorised as 0, 1, 2, and ≥3. The data from patients with screen-detected cancers are reported separately (given in tables as ‘Screening’, n = 1006).

The authors focus on three diagnostic intervals: the primary care interval (PCI), the diagnostic interval (DI), and the time from referral to the date the patient was informed they had cancer, calculated for patients with available-date data. The PCI was defined as the number of days from first presentation with symptoms deemed to be relevant to the subsequent diagnosis of cancer to the date of first referral from primary care for suspected cancer, and the DI as the number of days from first relevant presentation to the date of diagnosis, as registered by NCRAS.

Interval times of <0 and >730 days were excluded, consistent with previous literature,¹⁴ or ‘interval’ hereafter. The median (50th), together with the 25th and 75th centiles are described, along with the percentage of patients who had a primary care interval or diagnostic interval >60 or 90 days (for PCI and DI), or >28 days (for time from referral to the date the patient was informed).

RESULTS

The authors report key results in this paper, with more detailed tables provided at www.ncin.org.uk/collecting_and_using_data/.

Sample characteristics

A total of 439 practices submitted data during the audit period, representing 5% of all (approximately 8000) English practices. During quality assurance, 22 patient records were excluded, chiefly because they represented duplicates or pre-2014 diagnoses. The final sample included 17 042 patients (6% of all cancers diagnosed in 2014 in England). Of those, 50% of patients were male, the median age was 69 years, and the most numerous cancer sites were female breast (16%), lung (13%), prostate (13%), and colon/rectal cancer (12%) (Table 1). Completeness of stage at diagnosis (0–IV) was 77%.

View this table:

Table 1.

Sample composition and referral type that led most directly to the cancer diagnosis (N = 17 042)

Most patients were white (95%) and native English speakers (95%). Among all patients, 23% were reported as living alone, 11% were housebound or lived in a care home, and 10% had communication difficulties. Only 24% of all patients had no recorded comorbidities before diagnosis, while 21% had ≥3. The most common comorbidities were hypertension, cardiovascular disease, and arthritis/musculoskeletal disease (38%, 21%, and 18%, respectively [Table 2]).

View this table:

Table 2.

Patient characteristics

Patient and practice comparisons

Patients included in the NCDA were representative of the 2014 national incident cohort in respect of sex, age, and cancer site.¹³ Participating and non-participating practices were similar regarding the age profile of registered patients, but participating practices were somewhat larger (median 8318 versus 6197 listed patients) and had slightly fewer patients per full-time equivalent GP (median 1466 versus 1673) (Table 3). There were relatively fewer participating practices in the least and most deprived quintiles. Participating and non-participating practices had similar patient experience scores, though differences were significant given the large sample size. The median rate of TWW referrals for suspected cancers (n per 100 000 population per year) was higher in participating practices compared with non-participating ones, though conversion and detection rates were similar.

View this table:

Table 3.

Comparison of key attributes of English general practices participating in the NCDA (N = 439) with non-participating practices

Presentation, consultations, and referrals

Most patients (72%) first presented at the GP surgery or had a home visit. Of these patients, 11 539 (94%) had at least one recorded symptom. A small proportion (n = 1176, 7%) of patients first presented to A&E.

Among patients with a consultation (n = 12 369, 73% of all patients), 74% had fewer than three consultations and 26% had three or more. The most common recorded reason for multiple (>3) consultations was symptoms suggestive of a different initial diagnosis (n = 1684, 11%) or comorbidity ‘blurring the picture’ (n = 851, 5%).

Approximately 52% of patients were referred through the TWW route: this percentage was lowest in the 0–24 age group (Table 1), and varied greatly by cancer site, ranging from 9% (brain cancer) to 78% (endometrial cancer).

In total, 2818 patients had an emergency referral (17% overall, but ranging from 0.5% for melanoma to 65% for brain cancer [Table 1]). Of those patients, 1326 (48%) had self-referred to A&E/hospital (26% of 2818 patients without any previous relevant GP consultations, 11% while waiting for referral/investigation arranged by the GP, and 11% having previously consulted the GP but not awaiting previously arranged tests or referrals) and 1286 patients (47%) were referred to A&E/hospital as an emergency by the GP or out-of-hours service (20% of 2818 patients without previous relevant GP consultations, 8% while awaiting to be assessed in hospital following referral, and 19% having previously consulted the GP but not awaiting previously arranged tests or referrals) (5% other reason). The results for the emergency referrals are not in a table within the main paper but will be supplied in the supplementary tables hosted on the following webpage: www.ncin.org.uk/collecting_and_using_data/.

Intervals and avoidable delays

The median PCI was 5 days (interquartile range [IQR] 0–27 days), with 8% of patients having a primary care interval longer than 90 days (Table 4). Females with breast cancer had the shortest PCI (median 0 days, IQR 0–0 days), whereas patients with multiple myeloma had the longest (median 23.5 days, IQR 4–57 days). The median DI for all patients was 40 days (IQR 15–86 days). Patients with breast cancer also had the shortest DI (median 14 days, IQR 10–19 days), whereas those with prostate cancer had a median DI of 55.5 days (IQR 29–126 days). The time from referral to being told the diagnosis of cancer exceeded 28 days in 54% of patients: 19% of patients with breast cancer having an interval longer than 28 days compared with 74% of melanoma patients.

View this table:

Table 4.

The distribution of the primary care interval (n = 10 493) and the diagnostic interval (n = 12 929) by patient characteristic and cancer diagnosis groups^a

For one in five patients the GP considered there to be an avoidable delay in the patient receiving their diagnosis, varying from 7% (breast) to 34% (stomach) (Table 5). Delays were most frequently attributed to the patient, primary/secondary care clinician, and system factors (26%, 28%, and 34%, respectively).

View this table:

Table 5.

Avoidable delays (n = 15 369)^a

Investigations and safety netting

Primary care-led investigation before referral was used in 45% of all patients, ranging from 3% (breast cancer) to 76% (prostate cancer) (Table 6). For 44% of patients, there was evidence in the clinical record that safety netting had been used, with limited variation by patient characteristics, but substantial variation by cancer site.

View this table:

Table 6.

Number of primary care-led investigations ordered by the GP as part of the diagnostic assessment prior to referral

DISCUSSION

Summary

About one in 20 English general practices participated in a major national audit initiative providing opportunities for targeted significant event analysis, reflective learning, and action planning, and additionally generating detailed information about how patients with cancer were diagnosed.

The findings provide the most detailed and accurate picture to date about the diagnostic process in a large, representative, nationwide population of patients with cancer. Overall, though, the median diagnosis interval was 40 days with a median primary care interval of 5 days.

Strengths and limitations

The key strength of the NCDA is the collection of detailed data on the diagnostic process by GPs, based on in-depth understanding of their patients, the detailed information included in the primary care patient record, and application of clinical judgement. The audit employed a population-based design, allowing for direct comparability of patients included with those not included in the audit. It linked rigorous case ascertainment and staging data with information unique to the primary care record and not available without direct extraction after expert clinical scrutiny.

Though both the included patients and participating practices were largely representative, participating practices may differ from non-participating practices in important aspects of the diagnostic process for which no comparative data exist (for example, in how often they use safety netting). Therefore, caution is needed when interpreting the findings as nationally representative, though comparisons of other characteristics of participating and non-participating practices are reassuring. Clinical judgement is inherently needed for certain data items (for example, to establish the date of the ‘first consultation with relevant symptoms’ for a patient subsequently diagnosed with cancer, particularly in patients with comorbidity). Therefore, the assignment of first relevant consultation (and related diagnostic intervals) can potentially contain errors. It should be acknowledged that clarity or vagueness of presenting symptoms may influence both the completeness and accuracy of how they are recorded in primary care records and the ability of auditing GPs to accurately extract and record this information. Validation studies (involving multiple raters) in sub-samples of patients would be merited. Another limitation is the degree of missing data, particularly regarding diagnostic interval measures and the assessment of whether delays have occurred (Tables 4 and 5).

Comparison with existing literature

This English (2014) NCDA builds on previous related initiatives in England (NACDPC 2009–2010),⁸ Scotland (2006–2008),¹⁵ and Denmark.¹⁶ It is complemented by nearly synchronous audits in both Scotland and North Wales.

The findings presented here reaffirm previous evidence on key determinants of variation in the measures and markers of diagnostic timeliness, particularly in respect of cancer site, with patients subsequently diagnosed with cancers characterised by non-specific symptom signatures (for example, lung, colon, stomach, and multiple myeloma) typically having longer primary care intervals and higher percentage of multiple pre-referral consultations.¹⁷^–¹⁹ Furthermore, we demonstrate that this variation by cancer site also applies to the soon-to-be-implemented 28-day faster diagnosis standard (from referral to receipt of diagnosis)⁹ and that performance in 2014 falls well short of the proposed 95% target for all sites.

The NCDA data provide information on referral type; this is analogous but not directly comparable with diagnostic route as described by the Routes to Diagnosis data.²⁰ Nonetheless, the proportion of patients with an emergency referral type in the NCDA was of similar order to that of patients being diagnosed through an emergency presentation according to the Routes to Diagnosis data for 2014 (17% and 20%, respectively).²¹ In about one in four emergency referrals the patient had not previously consulted with a GP, a finding consistent with other evidence,²²^,²³ and 19% were missed opportunities for earlier diagnosis (associated predictor: no prior GP contact (OR = 3.89; 95% CI 2.14 to 7.09). In the NCDA population, 52% of all patients were diagnosed following a TWW referral. The total number of TWW referrals increased by 71% in the relevant 5-year period 2009/2010 to 2014/2015, though the proportion of those receiving a cancer diagnosis decreased from 10.8% to 8.2%.²⁴

Implications for research and practice

For policymakers, this audit provides a baseline against which the impact of subsequent initiatives to improve cancer diagnosis, such as the 2015 NICE guidance on recognition and referral of suspected cancer¹¹ and the implementation of the Achieving World Class Cancer Outcomes Cancer Strategy 2015–2020,⁹^,²⁵ can be assessed. It provides pointers to where implementation efforts might best be directed, for example, in achieving the 28-day standard from referral to diagnosis. It appears that, despite efforts since 2012 to increase access to specialist investigations such as imaging or endoscopy, these are not widely ordered by GPs for patients subsequently diagnosed with cancer, who are however investigated after a specialist referral.²⁶

Individual practice feedback has already been provided along with quality improvement initiatives including the Quality Improvement toolkit from the RCGP and Cancer Research UK, specifically targeted at the NCDA,²⁷ and completion of cycles of audit. The novel methodology developed for this audit also permits continuous large-scale participation by practices in the future.

Acknowledgments

The authors would like to thank all GPs and health professionals who participated in the NCDA, and contributing Cancer Research UK staff, including Beccy Cummings, who managed the initial phase of the audit; the National Cancer Registration and Analysis Service, NHS England, the Royal College of General Practitioners, Macmillan Cancer Support, and Health Data Insight. Data for this audit are based on patient-level information collected by the NHS, as part of the care and support of cancer patients. The data are collated, maintained, and quality assured by the National Cancer Registration and Analysis Service, which is part of Public Health England. National Cancer Diagnosis Audit Steering Group: Sue Ballard (patient and public representative), Patricia Barnett, David H Brewster, Cathy Burton, Anthony Cunliffe, Jane Fenton-May, Anna Gavin, Sara Hiom (chair), Peter Hutchison, Dyfed Huws, Maggie Kemmner, Rosie Loftus, Georgios Lyratzopoulos, Emma McNair, John Marsh (patient and public representative), Jodie Moffat, Sean McPhail, Peter Murchie, Andy Murphy, Sophia Nicola, Imran Rafi, Jem Rashbass, Richard Roope, Greg Rubin, Brian Shand, Ruth Swann, Janet Warlow, David Weller, and Jana Witt (NHS England representative). Ruth Swann and Sean McPhail have contributed equally as first authors, and Georgios Lyratzopoulos and Greg Rubin as last in the present manuscript.

Notes

Funding

The National Cancer Diagnosis Audit (NCDA) received enabling support from Cancer Research UK, NHS England, and the National Cancer Registration and Analysis Service.

Ethical approval

This study uses data collected as part of a clinical audit and collated by the National Cancer Registration and Analysis Service under regulation 2 of the Health Service (Control of Patient Information) Regulations 2002.

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 August 30, 2017.
Revision requested September 30, 2017.
Accepted October 17, 2017.

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

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[1] 1.↵
Department of Health, NHS
(2007) Cancer reform strategy, http://www.nhs.uk/NHSEngland/NSF/Documents/CancerReformStrategy.pdf (accessed 20 Nov 2017).

[2] Department of Health, NHS

[3] 2.↵
Department of Health
(2011) Improving outcomes: a strategy for cancer, https://www.gov.uk/government/uploads/system/uploads/attachment_data/file/213785/dh_123394.pdf (accessed 20 Nov 2017).

[4] Department of Health

[5] 3.↵
Mendonca SC,
Abel GA,
Saunders CL,
et al.
(2016) Pre-referral general practitioner consultations and subsequent experience of cancer care: evidence from the English Cancer Patient Experience Survey. Eur J Cancer Care (Engl) 25(3):478–490.
OpenUrl

[6] Mendonca SC,

[7] Abel GA,

[8] Saunders CL,

[9] et al.

[10] 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

[11] Neal RD,

[12] Tharmanathan P,

[13] France B,

[14] et al.

[15] 5.↵
Abel GA,
Saunders CL,
Mendonca SC,
et al.
(2017) Variation and statistical reliability of publicly reported primary care diagnostic activity indicators for cancer: a cross-sectional ecological study of routine data. BMJ Qual Saf doi:10.1136/bmjqs-2017-006607.
OpenUrl Abstract/FREE Full Text

[16] Abel GA,

[17] Saunders CL,

[18] Mendonca SC,

[19] et al.

[20] 6.↵
Cancer Research UK
(2017) ICBP findings, International Cancer Benchmarking Partnership. http://www.cancerresearchuk.org/health-professional/early-diagnosis-activities/international-cancer-benchmarking-partnership-icbp/icbp-findings-and-impact (accessed 20 Nov 2017).

[21] Cancer Research UK

[22] 7.↵
Cancer Research UK
(2008) Early diagnosis initiative, http://www.cancerresearchuk.org/health-professional/early-diagnosis-activities/early-diagnosis-initiative (accessed 20 Nov 2017).

[23] Cancer Research UK

[24] 8.↵
Rubin G,
McPhail S,
Elliott K
(2011) National audit of cancer diagnosis in primary care. (Royal College of General Practitioners), http://www.rcgp.org.uk/policy/rcgp-policy-areas/national-audit-of-cancer-diagnosis-in-primary-care.aspx (accessed 20 Nov 2017).

[25] Rubin G,

[26] McPhail S,

[27] Elliott K

[28] 9.↵
Independent Cancer Taskforce.
(2015) Achieving world-class cancer outcomes. A strategy for England 2015–2020, http://www.cancerresearchuk.org/sites/default/files/achieving_world-class_cancer_outcomes_-_a_strategy_for_england_2015-2020.pdf (accessed 20 Nov 2017).

[29] Independent Cancer Taskforce.

[30] 10.↵
Nicholson BD,
Mant D,
Bankhead C
(2016) Can safety-netting improve cancer detection in patients with vague symptoms? BMJ 355:i5515.
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[31] Nicholson BD,

[32] Mant D,

[33] Bankhead C

[34] 11.↵
National Institute for Health and Care Excellence
(2015) Suspected cancer: recognition and referral. NG12. (NICE, London) http://www.nice.org.uk/guidance/NG12 (accessed 20 Nov 2017).

[35] National Institute for Health and Care Excellence

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Diagnosing cancer in primary care: results from the National Cancer Diagnosis Audit

Abstract

INTRODUCTION

How this fits in

METHOD

Data

Analysis

RESULTS

Sample characteristics

Patient and practice comparisons

Presentation, consultations, and referrals

Intervals and avoidable delays

Investigations and safety netting

DISCUSSION

Summary

Strengths and limitations

Comparison with existing literature

Implications for research and practice

Acknowledgments

Notes

Funding

Ethical approval

Provenance

Competing interests

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