Lung Screen Uptake Trial: Results from a single lung cancer screening round

Abstract

The Lung Screen Uptake Trial tested a novel invitation strategy to improve uptake and reduce socioeconomic and smoking-related inequalities in lung cancer screening (LCS) participation. It provides one of the first UK-based ‘real-world’ LCS cohorts. Of 2012 invited, 1058 (52.6%) attended a ‘lung health check’. 768/996 (77.1%) in the present analysis underwent a low-dose CT scan. 92 (11.9%) and 33 (4.3%) participants had indeterminate pulmonary nodules requiring 3-month and 12-month surveillance, respectively; 36 lung cancers (4.7%) were diagnosed (median follow-up: 1044 days). 72.2% of lung cancers were stage I/II and 79.4% of non-small cell lung cancer had curative-intent treatment.

Full text

Lung Screen Uptake Trial: results from a single lung
cancer screeninground
Mamta Ruparel ,1 Samantha L Quaife,2 Jennifer L Dickson,1 Carolyn Horst ,1
Sophie Tisi,1 Helen Hall,1 Magali Taylor,3 Asia Ahmed,3 Penny Shaw,3 Stephen Burke,4
May- Jan Soo,4 Arjun Nair,3 Anand Devaraj,5 Karen Sennett,6 Stephen W Duffy,7
Neal Navani ,1,8 Angshu Bhowmik,9 David R Baldwin,10 Sam M Janes 1
Brief communication
To cite: RuparelM,
QuaifeSL, DicksonJL, etal.
Thorax Epub ahead of print:
[please include Day Month
Year]. doi:10.1136/
thoraxjnl-2020-214703
►Additional material is
published online only. To view
please visit the journal online
(http:// dx. doi. org/ 10. 1136/
thoraxjnl- 2020- 214703).
For numbered affiliations see
end of article.
Correspondence to
Dr Sam M Janes, Lungs for
Living Research Centre, UCL
Respiratory, University College
London, London WC1E 6JJ, UK;
s. janes@ ucl. ac. uk
Received 24 February 2020
Revised 22 May 2020
Accepted 3 June 2020
© Author(s) (or their
employer(s)) 2020. Re- use
permitted under CC BY.
Published by BMJ.
ABSTRACT
The Lung Screen Uptake Trial tested a novel invitation
strategy to improve uptake and reduce socioeconomic
and smoking- related inequalities in lung cancer
screening (LCS) participation. It provides one of the first
UK- based ’real- world’ LCS cohorts. Of 2012 invited,
1058 (52.6%) attended a ’lung health check’. 768/996
(77.1%) in the present analysis underwent a low- dose
CT scan. 92 (11.9%) and 33 (4.3%) participants had
indeterminate pulmonary nodules requiring 3- month
and 12- month surveillance, respectively; 36 lung cancers
(4.7%) were diagnosed (median follow- up: 1044 days).
72.2% of lung cancers were stage I/II and 79.4% of
non- small cell lung cancer had curative- intent treatment.
INTRODUCTION
Lung cancer screening (LCS) by low- dose CT
(LDCT) has been repeatedly shown in clinical trials
to reduce lung cancer mortality.1–3 The benefits of
screening may be underestimated in these trials
due to participants being younger, of higher soci-
oeconomic position and disproportionately former
rather than current smokers compared with the
high- risk target population. The risk profile of the
population enrolled determines the prevalence and
stage of lung cancers, the false positive rate and
the mortality benefit. Screening the highest risk
quintiles can optimise the benefit- harm ratio while
making LCS more equitable, efficient and cost-
effective.4 5
Data from a prior UK- based ‘real world’
screening pilot in Manchester has shown compel-
ling results with high levels of attendance by those
from lower socioeconomic quintiles and radical
treatment rates.6 Here we report the nodule and
cancer outcomes from the Lung Screen Uptake Trial
(LSUT).
METHODS
The LSUT methods and primary attendance results
have been described previously7 8 and more detail
is included in the online supplementary appendix.
LSUT was a randomised controlled trial evaluating
the impact of ‘targeted, stepped and low burden’
invitation materials on attendance of a ‘lung health
check’ (LHC) appointment. Individuals aged 60
to 75 years, who had been recorded as ‘current
smokers’ within the seven preceding years were
sent an invitation letter from their usual general
practice doctor inviting them to an LHC. Those
attending were invited to participate in the study,
and those meeting any of the following criteria were
offered a single LDCT on the same day (or later if
preferred): ≥30 pack- years and if a former smoker
had quit ≤15 years ago, or a lung cancer risk of
≥1.51% or ≥2.5% as determined by the Prostate,
Lung, Colorectal and Ovarian study or the Liver-
pool Lung Project models, respectively.
Self- reported demographics, smoking, family and
medical history were recorded prospectively. Hand-
held pre- bronchodilator spirometry, height, weight
and blood pressure were recorded. LDCT findings
were evaluated and managed in accordance with
the British Thoracic Society (BTS) 2015 guidelines
for pulmonary nodules9 and the National Institute
for Health and Care Excellence (NICE) guidelines
for the diagnosis and management of lung cancer.10
Staging was carried out according to the 7th edition
TNM (tumour,node, metastases) classification
system.
In the present study, we report the outcomes
relating to LDCT scans with an indeterminate
pulmonary nodule or suspected lung cancer. Other
incidental finding outcomes have been reported
elsewhere.11 12 Study participants with complete
smoking and lung cancer risk data were included.
Descriptive statistics were used to present the data
pertaining to pulmonary nodules and lung cancer
outcomes.
RESULTS
Of the 1058 (52.6%) invitees (n=2012) attending
a LHC appointment between November 2015 and
July 2017, 996 were included in the present anal-
ysis. A total of 895 participants were eligible for
LDCT, though 36 were excluded due to prior CT
of the chest in the past year, or an inability to lie
flat and 91 participants declined or failed to attend
the CT. An LDCT examination was completed by
768 (77.1%) of the participants (figure 1). The
demographic characteristics of the 996 participants
included are presented in table 1.
At the baseline LDCT scan, a total of 125/768
participants had indeterminate pulmonary nodules
requiring 3- month (n=92 (11.9%)) or 12- month
(n=33 (4.3%)) surveillance and a further 33 (4.3%)
were considered to have lesions suspicious for lung
cancer that instigated referral to the local multi-
disciplinary meeting. The remaining 610 partic-
ipants had a ‘normal’ scan or had non- malignant
findings that have been discussed elsewhere.13 14
After a median follow- up of 1044 days, a total of
1RuparelM, etal. Thorax 2020;0:1–5. doi:10.1136/thoraxjnl-2020-214703

Brief communication
36 lung cancers (4.7%) were diagnosed. Of these, 17 (51.5% of
those referred to the lung cancer clinic) were diagnosed directly
following the baseline LDCT and the remainder were diag-
nosed following further surveillance CT scans of indeterminate
nodules in the 3- month (n=16, 17.4% of nodules in this group)
or 12- month surveillance groups (n=3, 9.1% of nodules in this
group).
For invasive investigations we report the data as a percentage
of the total number of lung cancers (table 2). Forty- nine (136%)
participants underwent positron emission tomography scan,
10 (27.8%) had endobronchial ultrasound and 5 (13.9%)
underwent percutaneous CT- guided lung biopsy. Numbers of
diagnostic investigations performed in those without a later
diagnosis of cancer are also detailed in table 2. Of note, there
were no adverse outcomes from diagnostic investigations in this
group. Twenty- one (58.3%) participants had a surgical resec-
tion without prior histological confirmation of malignancy (and
underwent frozen section at the time of the resection), though
some had undergone diagnostic staging examinations prior to
surgery. 2 out of 28 (7.1%) lung resections were subsequently
found to be benign and this represented 0.3% of participants
without lung cancer. There were no deaths within 90 days of
surgery.
Twenty- six (72.2%) of all lung cancers were stage I or II and 27
(79.4%) of those with non- small cell lung cancer (NSCLC) had
curative- intent treatment (including sublobar resection, lobectomy
Figure 1 Flow chart of invitees and participants demonstrating numbers identified, invited, enrolled, eligible for LDCT and that completed a LDCT
examination. DNA, did not attend; LDCT, low- dose CT; LLP, Liverpool Lung Project; MDT, multidisciplinary team; PLCOm2012, Prostate, Lung, Colorectal
and Ovarianstudy model 2012; USPSFT, United States Preventive Services Task Force.
2RuparelM, etal. Thorax 2020;0:1–5. doi:10.1136/thoraxjnl-2020-214703

Brief communication
Table 1 Participant characteristics by group (% totals may not sum up due to rounding or missing data)
Variables
No LDCT n=228
median (IQR) or n (%)
No lung cancer n=732
median (IQR) or n (%)
Lung cancers n=36
median (IQR) or n (%)
All groups n=996
median (IQR) or n (%)
Age (in years)
60–63 86 (37.7) 241 (32.9) 8 (22.2) 335 (33.6)
64–67 72 (31.6) 238 (32.5) 11 (30.6) 321 (32.2)
68–72 48 (21.1) 158 (21.6) 13 (36.1) 219 (22.0)
73–76 22 (9.7) 95 (13.0) 4 (11.1) 121 (12.2)
Gender
Female 109 (47.8) 317 (43.3) 23 (63.9) 449 (45.1)
Ethnicity
White 183 (80.3) 607 (82.9) 34 (94.4) 824 (82.7)
Black/African/Caribbean 23 (10.1) 77 (10.5) 1 (2.8) 101 (10.1)
Other 22 (9.7) 48 (6.6) 1 (2.8) 71 (7.1)
Highest level of education
Left school at or before age 15 105 (46.1) 395 (54.0) 20 (55.6) 520 (52.2)
GCSEs, O- levels or equivalent 26 (11.4) 75 (10.3) 3 (8.3) 104 10.4)
A- levels or equivalent 24 (10.5) 70 (9.6) 4 (11.1) 98 (9.8)
Further education 14 (6.1) 31 (4.2) 3 (8.3) 48 (4.8)
Bachelor degree 34 (14.9) 84 (11.5) 2 (5.6) 120 (12.1)
Further higher degree 20 (8.8) 64 (8.7) 4 (11.1) 88 (8.8)
Other 5 (2.2) 13 (1.8) 0 (0) 18 (1.8)
Index of Multiple Deprivation quintile
1 (most deprived) 117 (51.3) 402 (54.9) 19 (52.8) 538 (54.0)
2 87 (38.2) 245 (33.5) 12 (33.3) 344 (34.5)
3 3 (1.3) 17 (2.3) 1 (2.8) 21 (2.1)
4 0 (0) 2 (0.3) 0 (0) 2 (0.2)
5 (least deprived) 0 (0) 0 (0) 0 (0) 0 (0)
Smoking history
Current smoker 148 (64.9) 527 (72.0) 31 (86.1) 706 (70.9)
Years smoked (years) 42 (33 to 51) 47 (44 to 51) 51 (47 to 54) 47 (42 to 51)
Years quit (years) 0 (0 to 3) 0 (0 to 0) 0 (0 to 0) 0 (0 to 0)
Average smoking intensity (cigs/day) 14 (8 to 20) 20 (10 to 20) 20 (10 to 23) 17 (10 to 20)
Pack years 23 (10 to 41) 38 (26 to 51) 46 (26 to 63) 36 (21 to 50)
Lung cancer risk
PLCO (% 6- year risk) 1.40 (0.39 to 5.48) 3.74 (1.80 to 7.14) 5.68 (2.96 to 9.27) 3.43 (1.38 to 6.97)
LLP (% 5- year risk) 3.07 (1.55 to 7.16) 5.58 (3.79 to 8.75) 5.5 (4.58 to 9.77) 5.20 (3.16 to 8.56)
Physical measurements
FEV1 (l/min) 2.12 (1.68 to 2.57) 2.06 (1.64 to 2.56) 1.74 (1.12 to 2.2) 2.06 (1.64 to 2.55)
FEV1 (% predicted) 85 (69 to 98) 82 (66 to 96) 73 (53 to 89) 82 (67 to 97)
FEV/FVC (%) 70 (63 to 77) 69 (61 to 75) 62 (54 to 69) 69 (62 to 76)
BMI (kg/m2) 25.8 (22.9 to 29.1) 26.2 (23 to 29.4) 23.5 (22.5 to 26) 26.0 (22.9 to 29.2)
WHO Performance Status
0 - asymptomatic 203 (89.0) 660 (90.2) 28 (77.8) 891 (89.5)
1 - completely ambulatory 23 (10.1) 64 (8.7) 8 (22.2) 95 (9.5)
2 - <50% of day in chair/ bed 1 (0.4) 8 (1.1) 0 (0) 9 (0.9)
3 - >50% of day in chair/ bed 1 (0.4) 0 (0) 0 (0) 1 (0.1)
LDCT
Follow- up duration since LDCT (days) n/a 1007 (851 to 1143) 1044 (933 to 1153) 1008 (853 to 1144)
BMI, body mass index; cigs, cigarettes; CT, Computed Tomography scan; GCSE, General Certificate of Secondary Education; LDCT, low- dose CT; LLP, Liverpool Lung Project; PLCO,
Prostate, Lung, Colorectal and Ovarian study; USPSTF, United States Preventive Services Task Force; VATS, Video Assisted Thoracoscopic Surgery.
3RuparelM, etal. Thorax 2020;0:1–5. doi:10.1136/thoraxjnl-2020-214703

Brief communication
and stereotactic ablative radiotherapy). Of the two participants
with small cell lung cancer, both received concurrent chemora-
diation. Ten (27.8%) participants had advanced stage (III or IV)
disease, resulting in four (11.8%) of those with NSCLC under-
going palliative chemotherapy or radiotherapy (table 2). Online
supplementary table e1 presents details on all 36 lung cancers.
DISCUSSION
This observational cohort study demonstrated that despite the
very high risk of lung cancer in the cohort, 75.0% of lung cancers
detected were early stage and 79.4% of the patients with NSCLC
had treatment with curative intent. Indeterminate pulmonary
nodules for 3- month and 12- month surveillance were detected
in 11.9% and 4.3% of the participants screened, respectively, and
lung cancer was detected in 4.7%.
The rate of indeterminate pulmonary nodules (16.2%) was
lower than in NLST (National Lung Screening Trial; 24.2%)1
and NELSON trial (19.2%).15 This may have been in part due to
implementation of the 2015 BTS pulmonary nodule guidelines
which enables a more conservative approach to nodules smaller
than 5 mm.9 The lung cancer prevalence was significantly higher
than the majority of LCS trials, which have reported a 1% to
2% prevalence.1 16 17 However other higher- risk LCS cohorts have
demonstrated a similar lung cancer prevalence to that seen here.6 18
The proportion of participants with early- stage lung cancer who
received treatment with curative intent was slightly lower than
observed in UKLS,17 which again may reflect the population
screened. The number of invasive tests for those without a diag-
nosis of lung cancer was low, with only 4% of individuals without
cancer having a positron emissiontomography- CT (PET- CT) scan
or other invasive tests such as bronchoscopy or percutaneous
biopsy.
A strength of this study is that it demonstrates a method of
recruiting otherwise underserved populations as evidenced by the
low socioeconomic and education levels in the majority of the
cohort and as such this study illustrates a pragmatic, ‘real- world’
approach to LCS. It is limited by the small sample size and low
number of cancers. We acknowledge that this cohort had particu-
larly high lung cancer risk, however, in light of emerging evidence
advocating risk- based selection of LCS- eligible individuals,4 19 we
believe the findings reported here are generalisable to the LCS-
eligible population.
In conclusion, the rate of indeterminate pulmonary nodules
was lower and the rate of lung cancer was higher than previous
randomised LCS trials, and one in six individuals with an indeter-
minate nodule requiring 3- month surveillance LDCT were subse-
quently diagnosed with lung cancer. From these findings, as well
as the impressive early- stage disease and curative intent treatment
Table 2 Investigations rates, and stage, histology and treatments
from the baseline LDCT scan
Number in total
cohort
(% of total
lung cancers,
n=36 (*except
treatments)
Number among
those without a
diagnosis of lung
cancer
(% of total
participants
without lung
cancer, n=732)
Diagnostic or staging investigations
Positron emission tomography (PET) 49 (136) 16 (2.2)
Percutaneous non- lung biopsy 5 (13.9) 0 (0)
Other percutaneous biopsy 6 (16.7) 1 (0.1)
Cervical lymph node FNA 2 (5.6) 0 (0)
Fibreoptic bronchoscopy 12 (33.3) 9 (1.2)
Endobronchial ultrasound 10 (27.8) 1 (0.1)
Endoscopic ultrasound 1 (2.8) 0 (0)
VATS or open lung biopsy 21 (58.3) 2 (0.3)
Total: PET or invasive procedures 29 (4.0)
Histology
Invasive adenocarcinoma 16 (44.4)
Minimally invasive adenocarcinoma 3 (8.3)
Adenocarcinoma in situ 1 (2.8)
Squamous cell carcinoma 6 (16.7)
Mixed NSCLC (ie, adenosquamous) 2 (5.6)
Small cell lung cancer 2 (5.6)
Multiple or mixed histology (small
cell + NSCLC)
3 (8.3)
Radiological diagnosis 2 (5.6)
Carcinoid 1 (2.8)
Stage (TNM 7th edition)
Stage I & II 26 (72.2)
Ia 22 (61.1)
Ib 1 (2.8)
IIa 3 (8.3)
IIb 0 (0)
IIIa 6 (16.7)
IIIb 1 (2.8)
IV 3 (8.3)
Treatments (NSCLC) (*% are of total NSCLC)
Curative intent 27 (79.4)
Sub- lobar resection 11 (32.4)
Lobectomy 15 (44.1)
SABR 1 (2.9)
Concurrent chemoradiation 2 (5.9)
Palliative chemotherapy±radiation 4 (11.8)
Surveillance 1 (2.9)
Treatments (SCLC) (*% are of total
SCLC)
Radical chemoradiation 2 (100)
Continued
Number in total
cohort
(% of total
lung cancers,
n=36 (*except
treatments)
Number among
those without a
diagnosis of lung
cancer
(% of total
participants
without lung
cancer, n=732)
CT, CT scan; DNA, did not attend; FNA, fine needle aspiration; GCSE, General
Certificate of Secondary Education; LDCT, low- dose CT; LHC, lung health check;
MDT, multidisciplinary team; NSCLC, non- small cell lung cancer; SABR, stereotactic
ablative radiotherapy; SCLC, small cell lung cancer; TNM, tumour, node, metastases;
UKLS, United Kingdom Lung Cancer Screening Trial; USPSTF, United States
Preventive Services Task Force; VATS, video assisted thorascopic surgery.
Table 2 Continued
4RuparelM, etal. Thorax 2020;0:1–5. doi:10.1136/thoraxjnl-2020-214703

Brief communication
rates observed, we propose that LCS in a ‘real- world’ setting may
be less harmful, more efficient and more cost- effective than has
been seen in larger LCS studies.
Author affiliations
1Lungs for Living Research Centre, UCL Respiratory, University College London,
London, UK
2Research Department of Behavioural Science and Health, University College London,
London, UK
3Department of Radiology, University College London Hospitals NHS Foundation
Trust, London, UK
4Department of Radiology, Homerton University Hospital NHS Foundation Trust,
London, UK
5Department of Radiology, Royal Brompton Hospital, London, UK
6Killick Street Health Centre, London, UK
7Wolfson Institute of Preventive Medicine, Barts and London, London, UK
8Thoracic Medicine Department, University College London Hospitals NHS
Foundation Trust, London, UK
9Respiratory Medicine, Homerton University Hospital NHS Foundation Trust, London,
UK
10Respiratory Medicine Unit, David Evans Research Centre, Nottingham University
Hospitals NHS Trust, Nottingham, UK
Twitter Mamta Ruparel @mamta_ruparel and Arjun Nair @LUNGRADIOLOGIST
Contributors All authors were involved in the design and/or conduct of the study
or the interpretation of the results. All authors contributed to and approved the final
manuscript.
Funding This study was part of the Lung Screen Uptake Trial project, which was
funded by a National Awareness and Early Diagnosis Initiative (NAEDI) project grant
awarded by Cancer Research UK (CRUK) and a consortium of funders (Department
of Health (England); Economic and Social Research Council; Health and Social Care
R&D Division, Public Health Agency, Northern Ireland; National Institute for Social
Care and Health Research, Wales; Scottish Government) (SLQ and SMJ). SMJ is a
Wellcome Trust Senior Fellow in Clinical Science (WT107963AIA). SMJ is supported
by the Rosetrees Trust, the Roy Castle Lung Cancer Foundation, the Stoneygate Trust,
the Welton Trust, the Garfield Weston Trust and the UCLH Charitable Foundation. This
work was undertaken at UCLH/UCL who received a proportion of funding from the
Department of Health’s NIHR Biomedical Research Centre’s funding scheme (NN and
SMJ). SLQ is supported by a CRUK Postdoctoral Fellowship (C50664/A24460).
Competing interests SMJ, MR, JLD, CH, ST and HH are supported by funding
for a large trial of low dose CT screening, called the ’SUMMIT Study’ by GRAIL Inc.
SLQ and NN collaborate on the SUMMIT Study. SMJ has received honoraria from
AstraZeneca, BARD1 Bioscience and Janssen for being an Advisory Board Expert and
travel to a US conference. SMJ received grant funding from Owlstone for a separate
research study and has a family member who has a financial association with
AstraZeneca. MR has received travel funding for a conference from Takeda and an
honorarium for planning and speaking at educational meetings from AstraZeneca.
Patient consent for publication Not required.
Ethics approval This study is part of the Lung Screen Uptake Trial (LSUT), which
was granted ethical approval by the City Road and Hampstead NHS Research Ethics
Committee (REC; reference: 15/LO/1186) and was registered with ClinicalTrials. gov
(NCT02558101) and the International Standard Registered Clinical/soCial sTudy
Number (ISRCTN21774741).
Provenance and peer review Not commissioned; externally peer reviewed.
Open access This is an open access article distributed in accordance with the
Creative Commons Attribution 4.0 Unported (CC BY 4.0) license, which permits
others to copy, redistribute, remix, transform and build upon this work for any
purpose, provided the original work is properly cited, a link to the licence is given,
and indication of whether changes were made. See:https:// creativecommons. org/
licenses/ by/ 4. 0/.
ORCID iDs
MamtaRuparel http:// orcid. org/ 0000- 0001- 8880- 6567
CarolynHorst http:// orcid. org/ 0000- 0003- 2427- 6610
NealNavani http:// orcid. org/ 0000- 0002- 6412- 7516
Sam MJanes http:// orcid. org/ 0000- 0002- 6634- 5939
REFERENCES
1 National Lung Screening Trial Research Team, Aberle DR, Adams AM, etal. Reduced
lung- cancer mortality with low- dose computed tomographic screening. N Engl J Med
2011;365:395–409.
2 de Koning HJ, van der Aalst CM, de Jong PA, etal. Reduced lung- cancer mortality with
volume CT screening in a randomized trial. N Engl J Med 2020;382:503–13.
3 Pastorino U, Silva M, Sestini S, etal. Prolonged lung cancer screening reduced 10- year
mortality in the mild trial: new confirmation of lung cancer screening efficacy. Ann
Oncol 2019;30:1162–9.
4 Kovalchik SA, Tammemagi M, Berg CD, etal. Targeting of low- dose CT screening
according to the risk of lung- cancer death. N Engl J Med 2013;369:245–54.
5 Black WC, Gareen IF, Soneji SS, etal. Cost- effectiveness of CT screening in the
National lung screening trial. N Engl J Med Overseas Ed 2014;371:1793–802.
6 Crosbie PA, Balata H, Evison M, etal. Implementing lung cancer screening: baseline
results from a community- based ’Lung Health Check’ pilot in deprived areas of
Manchester. Thorax 2019;74:405–9.
7 Quaife SL, Ruparel M, Beeken RJ, etal. The Lung Screen Uptake Trial (LSUT): protocol
for a randomised controlled demonstration lung cancer screening pilot testing a
targeted invitation strategy for high risk and ’hard- to- reach’ patients. BMC Cancer
2016;16:281.
8 Quaife SL, Ruparel M, Dickson JL, etal. Lung screen uptake trial (LSUT): randomized
controlled clinical trial testing targeted invitation materials. Am J Respir Crit Care Med
2020;201:965–75.
9 Guideline Development Group. The British thoracic Society guidelines on the
investigation and management of pulmonary nodules. Thorax 2015;70:794–8.
10 Baldwin DR, White B, Schmidt- Hansen M, etal. Diagnosis and treatment of lung
cancer: summary of updated NICE guidance. BMJ 2011;342:d2110.
11 Ruparel M, Quaife SL, Dickson JL, etal. Evaluation of cardiovascular risk in a lung
cancer screening cohort. Thorax 2019;74:1140–6.
12 Ruparel M, Quaife SL, Dickson JL. Prevalence, symptom burden and under- diagnosis
of COPD in a lung cancer screening cohort, 2019. Available: www. atsjournals. org
[Accessed 7 Jun 2019].
13 Ruparel M, Quaife SL, Dickson JL, etal. Prevalence, symptom burden, and
underdiagnosis of chronic obstructive pulmonary disease in a lung cancer screening
cohort. Ann Am Thorac Soc 2020;17:869–78.
14 Ruparel M, Quaife SL, Dickson JL, etal. Is lung cancer screening an opportunity to
reduce cardiovascular mortality? 2019;259:A5896.
15 Horeweg N, van der Aalst CM, Vliegenthart R, etal. Volumetric computed
tomography screening for lung cancer: three rounds of the Nelson trial. Eur Respir J
2013;42:1659–67.
16 Horeweg N, van Rosmalen J, Heuvelmans MA, etal. Lung cancer probability in
patients with CT- detected pulmonary nodules: a prespecified analysis of data from the
Nelson trial of low- dose CT screening. Lancet Oncol 2014;15:1332–41.
17 Field JK, Duffy SW, Baldwin DR, etal. UK lung cancer RCT pilot screening trial:
baseline findings from the screening arm provide evidence for the potential
implementation of lung cancer screening. Thorax 2016;71:161–70.
18 Bechtel JJ, Kelley WA, Coons TA, etal. Lung cancer detection in patients with airflow
obstruction identified in a primary care outpatient practice. Chest 2005;127:1140–5.
19 Ten Haaf K, Tammemägi MC, Bondy SJ, etal. Performance and cost- effectiveness
of computed tomography lung cancer screening scenarios in a population- based
setting: a Microsimulation modeling analysis in Ontario, Canada. PLoS Med
2017;14:e1002225.
5RuparelM, etal. Thorax 2020;0:1–5. doi:10.1136/thoraxjnl-2020-214703