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Open access Original research

BMJ Open: first published as 10.1136/bmjopen-2023-074399 on 14 February 2024. Downloaded from http://bmjopen.bmj.com/ on February 15, 2024 by guest. Protected by copyright.
Development of clinically meaningful
quality indicators for contemporary
lung cancer care, and piloting and
evaluation in a retrospective cohort;
experiences of the Embedding Research
(and Evidence) in Cancer Healthcare
(EnRICH) Program
Bea Brown ‍ ‍,1 Kirsty Galpin,1 John Simes,1 Michael Boyer,2 Chris Brown,1
Venessa Chin,3,4 Jane Young,5 on behalf of the Clinical Advisory Group

To cite: Brown B, Galpin K, ABSTRACT


Simes J, et al. Development Objectives Lung cancer continues to be the most
STRENGTHS AND LIMITATIONS OF THIS STUDY
of clinically meaningful quality common cause of cancer-­related death and the leading ⇒ A rigorous, multistep modified Delphi process was
indicators for contemporary lung undertaken to identify a set of clinically meaning-
cause of morbidity and burden of disease across
cancer care, and piloting and ful quality indicators to measure contemporary lung
evaluation in a retrospective
Australia. There is an ongoing need to identify and reduce
unwarranted clinical variation that may contribute to cancer care.
cohort; experiences of the
these poor outcomes for patients with lung cancer. An ⇒ The Clinical Advisory Group included multidisci-
Embedding Research (and
Evidence) in Cancer Healthcare Australian national strategy acknowledges clinical quality plinary lung cancer specialists from metropolitan
(EnRICH) Program. BMJ Open outcome data as a critical component of a continuously and regional areas, as well as patient representation.
2024;14:e074399. doi:10.1136/ improving healthcare system but there is a need to ensure ⇒ A pragmatic, iterative process was undertaken to
bmjopen-2023-074399 clinical quality indicators adequately measure evidence-­ ensure quality indicators met the key criteria of
based contemporary care, including novel and emerging being linked to evidence-­based care and readily
► Prepublication history
and additional supplemental treatments. This study aimed to develop a suite of lung measurable.
material for this paper are cancer-­specific, evidence-­based, clinically acceptable ⇒ While applicable to local contemporary lung cancer
available online. To view these quality indicators to measure quality of care and outcomes, care, indicators may not be directly transferable
files, please visit the journal and an associated comparative feedback dashboard across healthcare settings.
online (https://doi.org/10.1136/​ to provide performance data to clinicians and hospital
bmjopen-2023-074399). administrators.
Design A multistage modified Delphi process outcomes in use by national and international lung cancer
8 November 2023
was undertaken with a Clinical Advisory Group of clinical quality registries which, to our knowledge, have not
Received 06 April 2023 multidisciplinary lung cancer specialists, with patient been recently updated to reflect the changing lung cancer
Accepted 31 January 2024 representation, to update and prioritise potential treatment paradigm.
indicators of lung cancer care derived from a targeted
review of published literature and reports from national
and international lung cancer quality registries. BACKGROUND
Quality indicators were piloted and evaluated with Globally, lung cancer is the second most
multidisciplinary teams in a retrospective observational commonly diagnosed cancer, accounting for
cohort study using clinical audit data from the Embedding 11.4% of total cancer cases.1 It continues to
© Author(s) (or their Research (and Evidence) in Cancer Healthcare Program, a be the most common cause of cancer-­related
employer(s)) 2024. Re-­use prospective clinical cohort of over 2000 patients with lung death and is the leading cause of morbidity
permitted under CC BY-­NC. No cancer diagnosed from May 2016 to October 2021.
commercial re-­use. See rights and burden of disease in New South Wales
Setting and participants Six tertiary specialist cancer
and permissions. Published by (NSW), across Australia and elsewhere.2 The
centres in metropolitan and regional New South Wales,
BMJ. outlook for patients with lung cancer is poor,
Australia.
For numbered affiliations see
Results From an initial 37 potential quality indicators, a with a median survival time of only 5–20
end of article. months depending on clinical stage at diag-
final set of 10 indicators spanning diagnostic, treatment,
Correspondence to quality of life and survival domains was agreed. nosis. Overall 5-­year relative survival is 22%3
Dr Bea Brown; Conclusions These indicators build on and update increasing to 68% if diagnosed and treated
​bea.​brown@s​ ydney.​edu.a​ u previously available measures of lung cancer care and at an early stage.4 Concerningly, however,

Brown B, et al. BMJ Open 2024;14:e074399. doi:10.1136/bmjopen-2023-074399 1


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overall 5-­year survival is less than 5% for patients diag- METHODS
nosed with advanced stage disease. The quality indicator development, piloting and evalua-
Optimal care pathways and national clinical practice tion process is outlined in figure 1 and detailed further
guidelines5 6 have identified evidence-­based approaches below.
to diagnosis, treatment and supportive care that can
improve survival and quality of life for people with lung Review of Australian clinical practice guidelines
cancer, however, these recommendations are not always In November 2016, Grade A and B recommendations from
followed. Thus, there is an ongoing need to identify and the Cancer Council Australia Clinical practice guidelines for
reduce unwarranted clinical variation—defined as ‘care the management of lung cancer,6 most recently updated in
that differs in ways that are not a direct and proportionate 2012 based on evidence predominantly published prior
response to available evidence or to the healthcare needs to 2010, were reviewed by an expert panel of specialist
and informed choices of patients’—which may contribute clinicians (surgery, medical oncology, radiation oncology,
to poor outcomes for patients with lung cancer.7–9 palliative care, cancer nursing, respiratory medicine) to
Clinical quality indicators are evidence-­ based stan- assess their perceived continued relevance in the context
dards of care that describe the performance that should of emerging best practice and a rapidly changing lung
occur for specific health-­ related conditions, therefore, cancer treatment paradigm. Recommendations with less
allowing evaluation of whether or not care is consistent than 80% agreement were excluded from further review.
with these proposed standards.10–12 Quality indicators can
Targeted literature review
be measures of the structure, processes and/or outcomes
A targeted review of English language published litera-
of care. They can be disease specific, thus describing
ture6 8 9 13 19–28 and publicly available clinical quality registry
the quality of care related to a specific diagnosis, such
and other quality agency reports15 29–45 was undertaken by
that comparative performance enables identification of
two authors (BB, KG) to identify potential national and
unwarranted clinical variation. Further, quality indicators
international evidence-­based lung cancer clinical quality
act as a benchmark for quality improvement initiatives,
indicators.
enabling quantification of implemented changes,11 13
The targeted literature review was conducted in
and play a crucial role in setting appropriate and realistic
November 2016 and updated in July 2020 in PubMed
targets for better performance. Measurement and feed-
(Medline) using the search terms ‘quality indicators’ and
back of quality indicator performance data has demon-
‘lung cancer’ (title/abstract), limited to English language
strably resulted in clinical quality improvement in lung
and published from 1 January 2000 to 30 June 2020.
cancer care and outcomes in several international juris-
Grey literature was retrieved using purposive searching
dictions including Denmark, the Netherlands and the
of websites of national cancer agencies and national and
UK.14–17
international lung cancer quality registries and health-
Embedding Research (and Evidence) in Cancer
care quality agencies from equivalent healthcare systems.
Healthcare (EnRICH) is a programme of translational
Snowballing techniques were employed to review refer-
research in lung cancer, established in 2016 to describe
ence lists of known lung cancer quality indicator litera-
the natural history and patterns of care for lung cancer
ture and relevant search results.
and identify current gaps in evidence and practice for
clinical quality improvement.18 The EnRICH Program Draft quality indicators
includes six specialist cancer centres across three Based on the review of published literature and clinical
Local Health Districts in metropolitan and regional practice guidelines recommendations, an initial set of
NSW. To date, the EnRICH cohort includes over 2000 draft quality indicators was compiled for review and ratifi-
patients. Data collection is ongoing, and the dataset cation through a multistep modified Delphi process.
includes comprehensive patient, diagnostic, treatment
and outcome data, with up to 5-­year follow-­up for the Clinical Advisory Group
earliest enrolled patients. The EnRICH dataset provides In October 2020 an investigator meeting took place
a unique opportunity to leverage existing research infra- to review the scope of the draft quality indicators and
structure and comprehensive research quality clinical determine membership of the Clinical Advisory Group
audit data to measure routine clinical practice and iden- to include representation of each clinical specialty and
tify unwarranted clinical variation, with more granularity ensure results from the Delphi process would be gener-
than routinely collected data. alisable.46 Thereafter, a multidisciplinary Clinical Advi-
This paper describes the development of a set of sory Group was convened comprising 15 members from
evidence-­based lung cancer clinical quality indicators to a range of specialties (medical oncology n=4, surgery
measure contemporary lung cancer care, and an asso- n=1, pathology n=1, respiratory medicine n=1, pallia-
ciated interactive comparative feedback dashboard to tive care n=1, lung cancer nurse specialist n=1, health
provide performance data to clinicians and hospital service executive n=1, biostatistics n=1, epidemiology,
administrators, funded by a Cancer Institute NSW Inno- quality improvement and implementation research n=3,
vations in Cancer Control Grant (2019/INN1068) under consumer/patient representative n=1) with representa-
the auspices of the EnRICH Program. tion from metropolitan and regional clinical sites in NSW.

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Figure 1 Overview of quality indicator development process.

Modified Delphi process October 2021) regarding quality indicator definitions


Several iterative Delphi rounds took place to discuss the and inclusion/exclusion criteria.
initial set of draft clinical quality indicators as follows: ► Final prioritisation exercise (October 2021). A final
► Individual ranking (May 2021). The draft quality indi- online consensus meeting was held, which included
cator list was circulated to Clinical Advisory Group detailed discussion of definitions and patient inclu-
members who were asked to rank their top 10 most sion/exclusion criteria for each agreed quality
clinically meaningful quality indicators in order of indicator.
priority. Examples of performance data were provided
for the EnRICH cohort (calculated as proportions Dashboard development
with 95% CIs), alongside published Victorian Lung An interactive, html web-­hosted, comparative feedback
Cancer Registry data.29 dashboard was developed in RStudio. The dashboard
► Clinical Advisory Group consensus meeting (May content included a landing page with an overview of
2021). Following individual rankings, a moderated comparative performance data for each quality indicator
meeting was held online (due to COVID-­19 restric- stratified by cancer centre, and tabs detailing patient
tions), during which collated individual member characteristics and further stratification of indicators by
rankings were presented. The Group discussed the disease stage and treatment type, as applicable. Results
utility and feasibility of each ranked quality indicator were reported in the form of bar charts, box plots,
as a measure of local contemporary lung cancer care. Kaplan-­Meier curves and summary tables. See figure 2 for
At the end of the meeting the Clinical Advisory Group an example of the feedback dashboard overview page.
agreed a set of quality indicators to be piloted with
multidisciplinary teams (MDTs). Pilot with lung cancer MDTs
► Ongoing correspondence was undertaken with indi- The quality indicators and feedback dashboard were
vidual Clinical Advisory Group members (May 2021 to piloted in November and December 2021 with lung cancer

Brown B, et al. BMJ Open 2024;14:e074399. doi:10.1136/bmjopen-2023-074399 3


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Figure 2 Example of feedback dashboard overview page. EnRICH, Embedding Research (and Evidence) in Cancer Healthcare;
MDT, multidisciplinary team; NSCLC, non-­small cell lung cancer.

MDTs using clinical data from the EnRICH dataset for a Patient and public involvement statement
cohort of 750 patients diagnosed between 8 September Dr Diane McPhail, a qualified consumer/community
2016 and 23 May 2019 at specialist cancer centres, repre- representative, has been a member of the Clinical Advi-
senting both metropolitan and regional areas, namely: sory Group for this study since it’s conception in 2020,
Royal Prince Alfred Hospital; Chris O’Brien Lifehouse; and has been a member of the EnRICH Program Steering
Concord Repatriation General Hospital; St Vincent’s Committee, which informs the overall design and conduct
Hospital/The Kinghorn Cancer Centre; Orange Health of the Program and related sub-­studies, since 2018.
Service/Bathurst Base Hospital/Dubbo Base Hospital;
and Coffs Harbour Health Campus. Performance data
were circulated via the comparative feedback dashboard RESULTS
(figure 2) to MDT meeting lists. Clinician feedback was Review of Australian clinical practice guidelines
obtained through MDTs on the clarity and transparency Of 90 Grade A and B clinical practice recommendations
of the quality indicator definitions and inclusion/exclu- in the Cancer Council Australia clinical practice guide-
sion criteria, and the feedback dashboard format and lines for the management of lung cancer, there was less
usability. Changes were implemented as required. than 80% agreement with 31 (34%) (online supplemental
file 1). Of these recommendations, 1 related to surgery
(or lack thereof in unselected patients with stage IIIA
Evaluation of final quality indicators and feedback dashboard
non-­small cell lung cancer (NSCLC)), 19 to treatment-­
In July 2022, a second round of quality indicator perfor-
specific systemic therapy regimens and 11 to palliative
mance data was provided, via the updated dashboard,
and supportive care interventions.
from the EnRICH dataset for a cohort of 426 patients
diagnosed between 1 January and 28 October 2021 at Targeted literature review
the same six cancer centres. These data provided the The PubMed (Medline) search resulted in 54 abstracts
focus for an evaluation of the acceptability and utility and online searching and snowballing identified an addi-
of the clinical quality indicators, perceptions of the tional 29 articles. After excluding duplicates and arti-
accuracy of data provided in the comparative feedback cles that were not directly related to the development
dashboard, proposed performance benchmarks and or implementation of lung cancer quality indicators, 32
priorities for future quality improvement interventions to full-­text publications6 8 9 13 19–28 and reports15 29–45 from
address observed clinical variation (full evaluation results Australia, Belgium, Canada, Denmark, the Netherlands,
published elsewhere47). the UK (England and Scotland) and the USA were

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reviewed, resulting in 90 potential lung cancer quality included as a collectively agreed key outcome measure,
indicators (online supplemental file 2). Indicators were consistent with other jurisdictions.28 29 31 38
considered for inclusion for review if they were used by In order for the indicators to be used and impactful,
three or more jurisdictions. Some indicators meeting this the Clinical Advisory Group universally agreed that they
criterion were excluded based on local healthcare service should be able to be presented visually on a single over-
organisation/resourcing, for example, coordination of view page, with further information available by click
care/referral to a lung cancer nurse specialist as, despite through. Therefore, rather measuring every aspect of
advocacy, there are currently only 12 of these roles in care, a pragmatic decision was made to limit the indi-
the whole of Australia. Two-­year survival was retained as cators to a brief set of targeted and focused indicators,
a potential indicator, being used by both the Victorian29 which were evidence based and meaningful to a broad
and Danish Lung Cancer Registries38 to enable national audience—not limited to clinicians but also including
and international comparisons. A number of indicators nursing and allied health staff, healthcare administrators
related to timeliness of diagnosis and treatment, based and patients.
on timeframes specified in the Cancer Australia Optimal Following the final prioritisation exercise, consensus
Care Pathway for patients with lung cancer,5 were also was reached on definitions and inclusion/exclusion
included. criteria for a set of eight quality indicators spanning diag-
nostic, treatment, quality of life and survival domains that
Modified Delphi process were piloted with MDTs through the feedback dashboard.
These were by domain:
Based on the expert panel and targeted literature reviews,
Diagnosis
an initial set of 37 draft lung cancer quality indicators
► Proportion of patients diagnosed ≤28 days* of first
(table 1) was compiled for review by the Clinical Advisory
investigation of symptoms suspicious of lung cancer
Group through the modified Delphi process.
(earliest of clinical or pathological diagnosis).
Scores from individual rankings were reverse coded
► Proportion of patients with a pathological diagnosis
from 10 to 1 (indicators with a score of zero were
≤28 days* of first investigation of symptoms suspicious
excluded) and summed to give a final score and rank for
of lung cancer.
each quality indicator, such that the highest scoring indi-
► Proportion of patients with stage IV, non-­ squamous
cator was ranked first, the second highest scoring indi-
NSCLC with standard of care molecular testing.
cator ranked second and so on. Quality indicator sources
► Proportion of patients with stage III lung cancer
and collated rankings are detailed in table 1 and online
reviewed by an MDT prior to curative treatment.
supplemental file 3.
Treatment
Seven of the 37 quality indicators (19%) were not ► Proportion of patients with stage I–III lung cancer
ranked by any individual, resulting in a summed score initiating curative treatment ≤28 days* of diagnosis.
of zero. Individual rankings were variable and summed ► Proportion of patients with stage IV lung cancer initi-
scores for the remaining 30 indicators ranged from 29 to ating systemic treatment ≤28 days* of diagnosis.
1. Including those that scored evenly, 12 indicators were Quality of life
ranked as highest priority, eight of which related to time- ► Proportion of patients with stage IV NSCLC referred
liness of diagnosis. to palliative care ≤8 weeks* of diagnosis.
Rankings were discussed at the moderated Clinical Survival
Advisory Group meeting, initially focused on the top ► One-­year survival in patients with lung cancer.
12 quality indicators, which were included, excluded or *Refer to table 2 for rationale and justification of time
adapted based on discussion. Of the initial 12 indicators, thresholds.
six were excluded based on group discussion with reasons
detailed in table 1. Pilot with lung cancer MDTs
Following exclusion of these six indicators, further Quality indicators
discussion identified the need for indicators to be consis- While the included indicators were well accepted and
tently recorded in electronic medical records, so as to considered to be clinically meaningful measures of
be measurable, and to cover the full diagnostic and care quality of care and patient outcomes, MDT feedback
pathway, including all disease stage and treatment types, highlighted clinicians’ concerns about the potential for
rather than being heavily focused on diagnosis or being postdiagnostic delays in primary or secondary care, prior
highly treatment specific, as well as including a measure to tertiary referral, to impact the timeliness of treatment.
of quality of life. Based on randomised controlled trial The Clinical Advisory Group, therefore, proposed the
evidence demonstrating early integration of palliative addition of two extra treatment-­related quality indicators
care within 8 weeks of diagnosis in metastatic NSCLC related to time from first presentation at the treating clin-
improved quality of life and mood and reduced aggressive ical site to commencement of curative or systemic thera-
end-­of-­life care,48 referral to palliative care was included as pies as a measure of the quality of tertiary care:
a quality of life indicator. Although not ranked in the top ► Proportion of patients with stage I–III lung cancer initi-
10 based on individual ranking scores, 1-­year survival was ating curative treatment ≤28 days of site presentation.

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Table 1 Initial quality indicators identified through targeted literature review, review of clinical practice guidelines and clinical
quality registry reports
Domain Quality indicator Source(s) Collated ranking Included, excluded or adapted
1 Diagnosis Proportion of patients 26 28 29 43 4th Included
diagnosed within 28 days from
first presentation*
2 Diagnosis Proportion of patients with a 29 8th (equal) Excluded after consensus
clinical diagnosis within 28 meeting—pathological diagnosis
days of first presentation* prioritised
3 Diagnosis Proportion of patients with a 29 2nd Included
pathological diagnosis within
28 days of first presentation*
4 Diagnosis Proportion of patients CAG NR Excluded
diagnosed within 28 days of
site presentation
5 Diagnosis Proportion of patients with a CAG NR Excluded
clinical diagnosis within 28
days from site presentation
6 Diagnosis Proportion of patients with a CAG 5th Excluded after consensus
pathological diagnosis within meeting—majority have
28 days from site presentation pathological diagnosis prior to
site presentation
7 Diagnosis Proportion with performance 24 26 29 31 35 NR Excluded
status assessment at diagnosis
8 Diagnosis Proportion with documented 24 29 31 35 36 6th (equal) Excluded after consensus
clinical stage prior to definitive meeting—high compliance rate,
treatment other indicators prioritised as
evidence-­based metrics for
improved patient outcomes
9 Diagnosis Proportion with anatomical 29 31 35 37 NR Excluded
pathology studies after curative
resection (surgical only)
10 Diagnosis Proportion reviewed by 15 28 29 31 37 6th (equal) Included and adapted†
multidisciplinary team prior to
curative treatment
11 Diagnosis Proportion of patients with 28 29 31 32 36 37 NR Excluded
PET/CT available prior to
potentially curative treatment
12 Diagnosis Proportion of active smokers 24 35 36 42 1st Excluded after consensus
with lung cancer who have had meeting—compulsory for
smoking cessation counselling surgical patients, not reliably
discussion documented documented for others
13 Diagnosis Proportion of patients who 15 24 31 32 35 NR Excluded
underwent brain imaging
14 Diagnosis Proportion of patients who 31 32 36 NR Excluded
underwent a pulmonary
function test
15 Diagnosis Proportion of patients with 32 37 NR Excluded
NSCLC with a pathological
diagnosis of stage IIIB/C or IV
who have analysis of predictive
markers undertaken (excluding
squamous cell and PS 4)
16 Diagnosis Proportion of patients with 6 15 24 31 32 10th (equal) Included and adapted†
NSCLC with molecular testing
Continued

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Table 1 Continued
Domain Quality indicator Source(s) Collated ranking Included, excluded or adapted
17 Diagnosis Proportion of patients with 21 29 NR Excluded
NSCLC who have undergone a
surgical resection and clinical
stage agrees with pathological
stage
18 Treatment Proportion of patients initiating 29 33 NR Excluded—see ref 21
definitive treatment within 14
days from diagnosis date
19 Treatment Proportion of patients 29 NR Excluded
commencing curative treatment
within 14 days from clinical
diagnosis date
20 Treatment Proportion of patients 29 3rd Included and adapted†
commencing curative
treatment within 14 days from
pathological diagnosis date
21 Treatment Proportion of patients initiating 15 29–31 38 44 10th (equal) Excluded after consensus
definitive treatment within 42 meeting—time interval
days from first presentation from pathological diagnosis
prioritised
22 Treatment Proportion of patients 5 NR Excluded
commencing curative treatment
within 42 days from site
presentation
23 Treatment Proportion of patients with 29–31 36–38 44 NR Excluded
NSCLC who had a resection
(stages I–IIIA)
24 Treatment Proportion of patients with 6 15 24 35–37 45 NR Excluded (CAG increased to 6
NSCLC undergoing surgery nodes prior to ranking based on
who have adequate sampling newer evidence.)
of lymph nodes (5 or more
nodes) performed at time of
primary tumour resection
25 Treatment Proportion of patients with 29 31 35 NR Excluded
NSCLC with stage II or III
disease with surgical resection
who commenced adjuvant
chemotherapy within 6 weeks
26 Treatment 30-­day postoperative mortality 15 29 30 37 41 NR Excluded
27 Treatment Proportion of patients with 29 NR Excluded
NSCLC not undergoing surgery
who receive chemotherapy
28 Treatment Proportion of patients with 6 15 30 35 37 NR Excluded
NSCLC with inoperable
infiltrative stage III (N2,
3) and PS 0–1, receiving
curative intent platinum-­
based chemotherapy and
radiotherapy
29 Treatment Proportion of patients with 29 37 NR Excluded
NSCLC with stage IIIB/C or
IV and PS 0–1 not undergoing
surgery who receive platinum-­
based chemotherapy
Continued

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Table 1 Continued
Domain Quality indicator Source(s) Collated ranking Included, excluded or adapted
30 Treatment Proportion of patients with 6 31 37 NR Excluded
limited-­stage SCLC (I–IIIB,
T1–4, N0–3, M0, PS 0–1)
treated with curative intent
who receive both platinum-­
based chemotherapy and
radiotherapy at 40 Gy or
greater
31 Treatment Proportion of patients referred 27 37 40 8th (equal) Excluded after consensus
to/enrolled in clinical trials meeting—variability in
availability of trials between
metropolitan and regional areas
considered a confounder
32 QoL Proportion of patients with 6 15 27–29 10th (equal) Excluded after consensus
documented referral to meeting—inconsistently defined
supportive care services
33 QoL Proportion of advanced-­ 6 29 30 32 NR Included and adapted†
stage patients referred to
palliative care within 90 days of
diagnosis
34 QoL Proportion of patients who 29–31 37 NR Excluded
die within 30 days of active
treatment for lung cancer
35 QoL Proportion of patients receiving 29 NR Excluded
anticancer treatment
36 Survival 1-­year survival 28 29 31 38 NR Included after consensus
meeting as key outcome
measure
37 Survival 2-­year survival 29 38 NR Excluded
*Defined as first investigation of symptoms suspicious of lung cancer.
†See table 2 for definitions. Quality indicator definitions may vary between sources.
CAG, Clinical Advisory Group; NR, not ranked in top 10 after individual scores collated; NSCLC, non-­small cell lung cancer; PET, positron
emission tomography; PS, performance status; QoL, quality of life; SCLC, small cell lung cancer.

► Proportion of patients with stage IV lung cancer initi- and international lung cancer quality registries and
ating systemic treatment ≤28 days of site presentation. reviewed by an expert multidisciplinary Clinical Advi-
sory Group through a modified Delphi process to reach
Feedback dashboard consensus on a final set of 10 clinically meaningful indi-
The format of the feedback dashboard was acceptable to cators that reflect the lung cancer patient population
MDTs; it was considered clear, easy to navigate and gave and recent advancements in lung cancer diagnosis and
a satisfactory overview of all sites’ performance mapped
treatment. These 10 quality indicators span diagnostic,
against the quality indicators. Based on feedback, minor
treatment, quality of life and survival domains. Specific
changes were made to figure labelling and further infor-
indicators were selected based on the criteria of being:
mation was included on inclusion/exclusion criteria for
(1) linked to evidence-­based care, with the recognition
each indicator.
that some, such as survival rates, are indirect measures
Table 2 includes the final 10 lung cancer clinical quality
of clinical care; (2) reliably and accurately recorded in
indicators, their rationale, and their definitions and inclu-
sion and exclusion criteria. medical records and, therefore, readily measured. An
associated feedback dashboard was developed to provide
local and comparative performance data to clinicians and
DISCUSSION hospital administrators.
This paper describes the development of a set of clinical A 2021 review10 identified over 300 published lung
quality indicators to measure contemporary lung cancer cancer quality indicators but only 73 of these were deter-
care. Potential indicators were derived from a targeted mined to meet the minimum criteria of being evidence
review of published literature and reports from national based (or developed by RAND-­modified Delphi process),

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Table 2 Final set of prioritised quality indicators
ID Quality indicator Rationale Definition/inclusion/exclusion
1 Diagnosis Proportion of patients Inclusion: (1) All patients diagnosed
Date of ‘referral’ is frequently used but
diagnosed* ≤28 days of first with lung cancer with a first
inconsistently defined and recorded
investigation of symptoms presentation date. (2) All stages.
in electronic medical records. First
suspicious of lung cancer Exclusion: (1) Patients where
investigation of suspected lung cancer
diagnosis date was before first
(ie, date of imaging or biopsy) is more
presentation date. (2) No first
reliably recorded in electronic medical
records. 28-­day timeframe based presentation date available.
on Cancer Australia Optimal Care Denominator: All patients with a lung
cancer diagnosis (earliest clinical or
Pathway (OCP) for patients with lung
cancer5—first specialist appointment
pathological) and a first presentation
≤2 weeks of GP referral, diagnostic
date.
tests complete ≤2 weeks of first Numerator: Number of patients with a
specialist appointment. lung cancer diagnosis (earliest clinical
or pathological) within 28 days from
first presentation date.
2 Diagnosis Proportion of patients with a Pathological diagnosis is the gold Inclusion: (1) All patients with a
pathological diagnosis ≤28 standard to enable histological and pathological diagnosis of lung cancer.
days of first investigation of molecular typing and is consistent (2) All stages.
symptoms suspicious of lung with the Victorian Lung Cancer Exclusion: (1) Patients where the
cancer Registry quality indicator enabling pathological diagnosis date was
cross-­jurisdiction comparison. 28-­day before first presentation date. (2)
timeframe based on Cancer Australia Patients with missing pathological
OCP5—first specialist appointment ≤2 diagnosis date. (3) Patients with no
weeks of GP referral, diagnostic tests first presentation date available.
complete ≤2 weeks of first specialist Denominator: All patients with a
appointment. pathological diagnosis of lung cancer
and a first presentation date.
Numerator: Number of patients with a
pathological diagnosis within 28 days
of first presentation date.
3 Diagnosis Proportion of patients with Multiple guidelines recommend all Inclusion: All patients with stage III
patients be reviewed by an MDT. In
stage III lung cancer reviewed lung cancer.
by an MDT prior to curative the context of high patient volume at Exclusion: (1) All patients with stage
treatment (per documented specialist cancer centres, the Clinical I, II and IV lung cancer. (2) Patients
intent in electronic medicalAdvisory Group considered it was treated with palliative intent first-­line
record) not feasible or necessary to discuss therapy.
patients for whom there are clear Denominator: All patients with stage
evidence-­based treatment regimens. III lung cancer where treatment intent
The recommendation was rationalised is curative.
to include only stage III lung cancers Numerator: Number of stage III
due to their complexity and the patients who were reviewed by an
potential requirement for multimodal MDT prior to commencing curative
therapy. treatment.
4 Diagnosis Proportion of patients with Definition in line with Medicare Inclusion: All patients with stage IV
stage IV non-­squamous Benefits Schedule rebate for non-­squamous NSCLC.
NSCLC with standard of care molecular testing. Exclusion: (1) Stage I–III patients. (2)
molecular testing Proportion of all patients with Patients with SCLC. (3) Squamous cell
NSCLC with molecular testing is also carcinoma. (4) Patients with missing/
measured but not reported in the undefined lung cancer histological
feedback dashboard. type.
Denominator: All patients with a
stage IV lung cancer diagnosis.
Numerator: Number of patients with
a stage IV lung cancer diagnosis who
had molecular testing.
Continued

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Table 2 Continued
ID Quality indicator Rationale Definition/inclusion/exclusion
5 Treatment Proportion of patients with Multiple quality indicators focus only Inclusion: All stage I–III patients.
stage I–III lung cancer on surgery as curative treatment. The Exclusion: (1) Stage IV patients. (2)
initiating curative treatment Clinical Advisory Group considered Patients treated with palliative intent
≤28 days of diagnosis* all treatments with curative intent, first-­line therapy.
including chemotherapy and Denominator: All patients with a
radiotherapy, be included in this stage I–III lung cancer diagnosis.
indicator to reflect changes in Numerator: Number of patients with
evidence and best practice. 28-­day stage I–III lung cancer diagnosis who
timeframe proposed by CAG— commenced curative treatment within
reduced from 42 days in Cancer 28 days of diagnosis date.
Australia OCP.5
6 Treatment Proportion of patients with Indicator added by Clinical Advisory Inclusion: All stage I–III patients.
stage I–III lung cancer Group following piloting, based on Exclusion: (1) Stage IV patients. (2)
initiating curative treatment feedback from multidisciplinary Patients treated with palliative intent
≤28 days of site presentation teams, as a measure of the timeliness first-­line therapy.
of tertiary care, excluding potential Denominator: All patients with a
postdiagnostic delays in primary stage I–III lung cancer diagnosis.
or secondary care prior to site Numerator: Number of patients with
presentation. stage I–III lung cancer diagnosis who
commenced curative treatment within
28 days of site presentation date.
7 Treatment Proportion of patients with Indicator added by Clinical Advisory Inclusion: All patients with stage IV
stage IV lung cancer initiating Group as a measure of quality of lung cancer.
systemic treatment ≤28 days care for advanced-­stage patients Exclusion: (1) Stage I–III patients. (2)
of diagnosis* who comprise approximately 45% Stage IV patients treated with curative
of lung cancer diagnoses, including intent first-­line therapy.
chemotherapy, targeted therapy, Denominator: All patients with a
immunotherapy and palliative stage IV lung cancer diagnosis.
radiotherapy. 28-­day timeframe Numerator: Number of patients with
reduced from 42 days in Cancer stage IV lung cancer diagnosis who
Australia OCP5 by CAG based on commenced systemic treatment
patient input. within 28 days of diagnosis date.
8 Treatment Proportion of patients with Indicator added by Clinical Advisory Inclusion: All patients with stage IV
stage IV lung cancer initiating Group, following piloting, based lung cancer.
systemic treatment ≤28 days on feedback from multidisciplinary Exclusion: (1) Stage I–III patients. (2)
of site presentation teams, as a measure of the timeliness Stage IV patients treated with curative
of tertiary care, excluding potential intent first-­line therapy.
postdiagnostic delays in primary Denominator: All patients with a
or secondary care prior to site stage IV lung cancer diagnosis.
presentation. Numerator: Number of patients with
stage IV lung cancer diagnosis who
commenced systemic treatment within
28 days of site presentation date.
9 Quality of Proportion of patients with Timeframe based on published Inclusion: All patients with stage IV
life stage IV NSCLC referred to evidence.48 Clinical Advisory Group NSCLC.
palliative care ≤8 weeks of excluded patients with actionable Exclusion: (1) Stage I/II/IIIA/B/C
diagnosis* molecular mutations based on patients. (2) Patients with SCLC. (3)
availability of new targeted therapies Patients with missing/undefined lung
and related evidence demonstrating cancer type.
fewer symptoms and longer survival.52 Denominator: All patients with a
stage IV NSCLC diagnosis.
Numerator: Number of patients with
a stage IV NSCLC referred to palliative
care within 8 weeks of diagnosis.
Continued

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Table 2 Continued
ID Quality indicator Rationale Definition/inclusion/exclusion
10 Survival 1-­year survival in patients Globally agreed quality of care Inclusion: All patients with lung
with lung cancer outcome. cancer.
Calculated from date of pathological Exclusion: Patients deceased before
diagnosis (or clinical diagnosis if no/ 1 year.
inconclusive pathology). Denominator: All patients with lung
Date of death based on monthly cancer.
linkage with death notifications in Numerator: Number of patients
the NSW Registry of Births, Deaths where patient status=alive 1 year after
& Marriages. Patient assumed alive if diagnosis.*
not deceased on the first day of the
reporting month.
*Based on pathological diagnosis date—date of sample collection for earliest conclusive cytology/biopsy/or resection OR if no pathology,
clinical diagnosis date—date of first imaging with outcome ‘probable lung cancer’.
CAG, Clinical Advisory Group; GP, general practitioner; MDT, multidisciplinary team; NSCLC, non-­small cell lung cancer; SCLC, small cell lung
cancer.

feasible or measurable (assessed by documented measure- Advisory Group support the need for regular review to
ment with the quality indicator), and demonstrably able ensure they continue to be clinically relevant and fit for
to detect variation in care. The EnRICH quality indicators purpose.
developed through this study meet all of these criteria. Of note, throughout the modified Delphi process, clini-
The same review concluded that published indicators cians tended to prioritise indicators related to their own
disproportionately relate to preoperative and surgical specialty and clinical context. A strength of this study is
measures. Of note, the final set of EnRICH quality indi- the inclusion of a broad range of multidisciplinary lung
cators includes all evidence-­ based potentially curative cancer specialists from metropolitan and regional NSW,
therapies for early-­stage patients, and systemic and palli- as well as a patient representative, in the Clinical Advisory
ative therapies for advanced-­stage patients who comprise Group to ensure the final set of quality indicators is appli-
a significant proportion of lung cancer diagnoses. While cable to the diverse patient populations, case mixes and
there are additional quality indicators that could be clinical services available across the State. It is anticipated
considered, such as use of specific systemic therapies, that the indicators should, therefore, be generalisable at a
increased specificity has implications for data collection national, and potentially international, level. Definitions
and scrutiny, requiring much effort to identify appro- and explicit patient inclusion/exclusion criteria for each
priate patient groups. quality indicator have been provided for transparency,
The Australian National Clinical Quality Registry and and to enable others to measure and report on perfor-
Virtual Registry Strategy 2020–203049 acknowledges clin- mance in a comparable way. Inclusion/exclusion criteria
ical quality outcome data as a critical component of a additionally account for variation in risk level, whereby
continuously improving healthcare system and identifies recommended care is not applicable for some defined
a need to maximise the value of clinical quality outcome groups. A further strength of the study is the develop-
datasets with the potential to be expanded nationally in ment of an associated dashboard to provide a feedback
areas with the greatest burden of disease and cost to the loop for clinicians and hospital administrators to identify
Australian health system and/or with greatest variation clinical variation and to prompt examination of outliers
in care and outcomes, such as lung cancer. Others have on poor performing quality indicators to prioritise areas
echoed the need to develop a lung cancer clinical quality for service improvement. This dashboard is being used
registry to monitor the safety, quality and effectiveness of to feed back ongoing comparative performance data to
lung cancer care in Australia and New Zealand, building MDTs (2022 data were circulated in July 2023 and 2023
on the established Victorian Lung Cancer Registry,29 but data are anticipated to be circulated in July 2024) to iden-
note that quality indicators need to be further developed tify areas for quality improvement. Two initial clinician-­
to consider the inclusion of novel/emerging or under-­ prioritised quality improvement interventions are: (1) a
represented measures.50 The lung cancer quality indica- process to ensure all stage III patients are discussed by an
tors developed through the EnRICH Program build on MDT prior to commencing treatment; and (2) a referral
and update previously available measures of lung cancer pathway to palliative care within 8 weeks for patients diag-
care and outcomes in use by national29 and international nosed with stage IV disease.47
lung cancer clinical quality registries15 38 39 which, to our A limitation of the quality indicators developed
knowledge, have not been recently updated to reflect the through this study, and for clinical quality registries more
changing lung cancer treatment paradigm. The changes broadly, is the challenge arising from clinical audit data
to existing quality indicators proposed by the Clinical collection from electronic medical records and hospital

Brown B, et al. BMJ Open 2024;14:e074399. doi:10.1136/bmjopen-2023-074399 11


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5
administrative datasets. In the absence of a universal elec- School of Public Health, The University of Sydney, Camperdown, New South Wales,
tronic medical record system, with mandatory data points, Australia
data entry is necessarily manual and, therefore, highly
Acknowledgements We acknowledge the support and guidance of the Clinical
resource intensive. Future efforts to establish a national Advisory Group and the EnRICH Steering Committee, and data collection undertaken
lung cancer quality registry will need to ensure electronic by the EnRICH Project Team.
medical records adequately and accurately record the data Collaborators Clinical Advisory Group: Amy O’Donnell (Lung Cancer Nurse
required to calculate compliance with quality measures, Care Coordinator), Bea Brown (EnRICH Program Manager, Health Services/
and benchmarks for recording relevant data items could Implementation Research), Brian McCaughan (surgeon), David Barnes (respiratory
be included as discrete quality indicators. A further physician), Davinia Seah (palliative care physician), Diane McPhail (consumer
representative), Jane Young (EnRICH T2/T3 Lead, Epidemiology/Health Services
limitation of this study is that non-­English publications Research), John Simes (EnRICH Program Chair, medical oncologist), Karen
on international lung cancer quality improvement initia- Briscoe (medical oncologist), Kirsty Galpin (Health Services Research), Michael
tives were not included in the targeted literature review. Boyer (EnRICH Clinical Lead, medical oncologist), Ruth Jones (Director of Cancer
However, many such initiatives, for example, the Belgian Services), Venessa Chin (EnRICH T1/T2 Lead, medical oncologist), Wendy Cooper
(pathologist).
Health Care Knowledge Centre,31 the Danish Lung
Contributors BB contributed to study conceptualisation, methodology, literature
Cancer Registry38 and the Dutch Lung Cancer Audit,15 review and writing of the manuscript. KG contributed to literature review and
have published reports in English, and, therefore, were writing of the manuscript. JS, JY, MB and VC contributed to study conceptualisation
included. Necessarily, the literature review also excluded and methodology and reviewed the manuscript. CB provided biostatistics support,
publications after the most recent search in July 2020. developed the dashboard and reviewed the manuscript. BB is responsible for the
overall content as guarantor.
An updated search conducted in November 2023 identi-
fied an additional 26 publications potentially eligible for Funding This work was supported by the Cancer Institute New South Wales (grant
number: 2019/INN1068) and Sydney Local Health District.
inclusion, suggesting growing interest in this space.
The acceptability and utility of the clinical quality indi- Competing interests None declared.
cators, perceptions of the accuracy of data provided in the Patient and public involvement Patients and/or the public were involved in the
design, or conduct, or reporting, or dissemination plans of this research. Refer to
comparative feedback dashboard, proposed performance the Methods section for further details.
benchmarks and priorities for future quality improve-
Patient consent for publication Not applicable.
ment interventions to address observed clinical variation
have been formally evaluated and the results are reported Ethics approval Ethical approval for this project was authorised by Sydney Local
Health District Lead Human Research Ethics Committee (RPA Zone) under protocol
elsewhere.47 Performance on the quality indicators strati- number X16-­0447. Participants gave informed consent to participate in the study
fied by a number of patient, disease and hospital charac- before taking part.
teristics, as well as the impact of COVID-­19, has also been Provenance and peer review Not commissioned; externally peer reviewed.
reported elsewhere.51 Data availability statement Data are available upon reasonable request. Data are
Future research will explore the utility of these lung not reported in this paper. Analysis code for quality indicator calculations available
cancer quality indicators as a platform for the develop- on request, subject to necessary ethical approvals.
ment and evaluation of feasibility, acceptability, effec- Supplemental material This content has been supplied by the author(s). It has
tiveness and cost-­effectiveness of randomised discovery not been vetted by BMJ Publishing Group Limited (BMJ) and may not have been
and intervention-­based trials, including: (1) local prior- peer-­reviewed. Any opinions or recommendations discussed are solely those
of the author(s) and are not endorsed by BMJ. BMJ disclaims all liability and
ities for reducing variation in survival and quality of life; responsibility arising from any reliance placed on the content. Where the content
and (2) integration of novel diagnostic and therapeutic includes any translated material, BMJ does not warrant the accuracy and reliability
technologies. of the translations (including but not limited to local regulations, clinical guidelines,
terminology, drug names and drug dosages), and is not responsible for any error
and/or omissions arising from translation and adaptation or otherwise.
Open access This is an open access article distributed in accordance with the
CONCLUSIONS
Creative Commons Attribution Non Commercial (CC BY-­NC 4.0) license, which
The number and types of quality indicators integrated permits others to distribute, remix, adapt, build upon this work non-­commercially,
into clinical practice, and their measurability and ability and license their derivative works on different terms, provided the original work is
to detect variation, are an important consideration to properly cited, appropriate credit is given, any changes made indicated, and the use
is non-­commercial. See: http://creativecommons.org/licenses/by-nc/4.0/.
ensure they are clinically meaningful. Through a modi-
fied Delphi process, a set of 10 quality indicators, span- ORCID iD
ning diagnostic, treatment, quality of life and survival Bea Brown http://orcid.org/0000-0003-2851-1809
domains, was prioritised. These will be regularly reviewed
to ensure they continue to measure emerging and novel
therapies and resultant changes to the treatment and
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