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Telephone risk-based eligibility assessment for low-dose CT lung cancer screening
  1. Jennifer L Dickson1,
  2. Helen Hall1,
  3. Carolyn Horst1,
  4. Sophie Tisi1,
  5. Priyam Verghese1,
  6. Anne-Marie Mullin2,
  7. Jonathan Teague2,
  8. Laura Farrelly2,
  9. Vicky Bowyer3,
  10. Kylie Gyertson3,
  11. Fanta Bojang3,
  12. Claire Levermore3,
  13. Tania Anastasiadis4,
  14. Karen Sennett5,
  15. John McCabe1,
  16. Anand Devaraj6,7,
  17. Arjun Nair3,
  18. Neal Navani1,3,
  19. Matthew EJ Callister8,
  20. Allan Hackshaw2,
  21. SUMMIT Consortium,
  22. Samantha L Quaife9,
  23. Sam M Janes1,3
    1. 1 Lungs for Living Research Centre, UCL Respiratory, University College London, London, UK
    2. 2 Cancer Research UK and UCL Cancer Trials Centre, University College London, London, UK
    3. 3 University College London Hospitals NHS Foundation Trust, London, UK
    4. 4 Tower Hamlets Clinical Commissioning Group, London, UK
    5. 5 Killick Street Health Centre, London, UK
    6. 6 Department of Radiology, Royal Brompton Hospital, London, UK
    7. 7 National Heart and Lung Institute, Imperial College London, London, UK
    8. 8 Department of Respiratory Medicine, Leeds Teaching Hospitals, Leeds, Yorkshire, UK
    9. 9 Centre for Prevention, Detection and Diagnosis, Wolfson Institute of Population Health, Barts and The London School of Medicine and Dentistry, Queen Mary University of London, London, UK
    1. Correspondence to Dr Sam M Janes, Lungs for Living Research Centre, UCL Respiratory, University College London, London, UK; s.janes{at}ucl.ac.uk

    Abstract

    Eligibility for lung cancer screening (LCS) requires assessment of lung cancer risk, based on smoking history alongside demographic and medical factors. Reliance on individual face-to-face eligibility assessment risks inefficiency and costliness. The SUMMIT Study introduced a telephone-based lung cancer risk assessment to guide invitation to face-to-face LCS eligibility assessment, which significantly increased the proportion of face-to-face attendees eligible for LCS. However, levels of agreement between phone screener and in-person responses were lower in younger individuals and minority ethnic groups. Telephone-based risk assessment is an efficient way to optimise selection for LCS appointments but requires further iteration to ensure an equitable approach.

    • Lung Cancer
    http://creativecommons.org/licenses/by-nc/4.0/

    This is an open access article distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is 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/.

    https://doi.org/10.1136/thoraxjnl-2021-218634

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      Introduction

      Lung cancer screening (LCS) using low-dose CT (LDCT) reduces lung cancer mortality in high-risk populations.1 2 Eligibility is determined by lung cancer risk calculations, comprising smoking history, demographic and medical factors. No comprehensive population-based system exists from which LCS eligibility can be determined, therefore necessitating individual risk assessment of all potentially eligible individuals. Up to 88% of adults approached based on age alone were ultimately ineligible for LCS.2 3 More targeted strategies including primary-care recorded smoking status or telephone screening of exclusion criteria (eg, current cancer treatment) still find 25%–50% of individuals ineligible at in-person assessment,4 5 resulting in unnecessary appointments and potential distress.6

      To reduce this inefficiency, the SUMMIT study introduced a telephone-based eligibility assessment (‘phone screener’) between the invitation and appointment to estimate individual lung cancer risk, in a similar approach to the Yorkshire Lung Screening Trial.7 This manuscript reports the feasibility and accuracy of the phone screener in the first 12 months of recruitment.

      Methods

      The SUMMIT study is a prospective observational cohort study aiming to assess the implementation of LDCT for LCS in a high-risk population and to validate a multicancer early detection blood test. Study eligibility was assessed via a three-step process: primary care invitation, phone screener and face-to-face ‘Lung Health Check’ (LHC) (table 1). Potentially eligible individuals were invited by post from across north central and east London, with those meeting either US Preventive Services Task Force (USPSTF) 2014 criteria8 or prostate, lung, colorectal, ovarian (PLCO)m2012 6-year lung cancer risk9 ≥1.3% invited to undergo LCS as part of the study.

      View this table:
      Table 1

      Three step eligibility assessment for the SUMMIT Study and comparison of data collected at phone screener versus Lung Health Check to calculate lung cancer risk

      The initial phone screener (V.1) verified age and smoking status only; however, due to a high proportion of LHC attendees being ineligible for LCS, questions were expanded (V.2, conducted by National Health Service (NHS) band four staff), enabling estimation of USPSTF and PLCOm2012 criteria (table 1). Eligible individuals were offered an LHC appointment at which NHS band five staff (blinded to phone screener responses) asked questions and measured height and weight to accurately assess USPSTF and PLCO m2012 criteria (taken as the ‘gold standard’).

      Analysis

      The accuracy of phone screener-based estimation of eligibility was quantified by the proportion of responders subsequently eligible for LCS at LHC appointment. Levels of agreement for individual participant responses during phone screener and LHC (for specific questions and overall eligibility status) were compared with Cohen’s Kappa (K) and interpreted as per Landis and Koch,10 for all LHC attendees and within age and ethnicity groups.

      Results

      Effectiveness of telephone-based eligibility estimation on efficient utilisation of LHC appointments

      Between March 2019 and April 2020, 30 759 individuals responded to the LHC invitation. The first 3.6% (n=1111) completed phone screener V.1, the remaining 96.4% (n=29 648) completed V.2 (figure 1). Significantly fewer individuals were eligible for an LHC using V.2 compared with V.1, (56.1% vs 86.9%, p<0.001). This resulted in an increased proportion of LHC attendees being LCS eligible (60.3% V.1 vs 82.6% V.2, p<0.001).

      Figure 1
      Figure 1

      Comparison between version 1 (A) and version 2 (B) of the phone screener in refining the population eligible for LHC. LCS, lung cancer screening; LHC, lung health check.

      Agreement between telephone screening and LHC assessments

      For the 14 714 individuals who completed phone screener V.2 and attended an LHC, the level of agreement between eligibility assessments conducted by phone screener versus LHC was fair (K=0.441) for USPSTF criteria and moderate (K=0.346) for PLCOm2012 criteria (table 2). Level of agreement between phone screener and LHC responses was substantial or ‘almost perfect’ for all categorical variables except educational status (K=0.347) (table 2). Statistically significant differences in mean pack-year history and body mass index were observed (table 2), but their magnitudes were unlikely to be clinically significant. The level of agreement for eligibility assessments was lowest in individuals from an Asian ethnic group and those aged 55–59 years and highest in the white ethnic group and those aged over 75 years (table 2).

      View this table:
      Table 2

      Agreement between the phone screener questions and LHC assessments of (A) individual questions/eligibility criteria for all responders and (B) eligibility criteria across age/ethnicity subgroups

      Discussion

      We present the first reported data demonstrating the impact of a telephone-based lung cancer risk assessment tool on optimising selection for LCS appointments. Introduction of the multifactor phone screener significantly increased the proportion of ineligible individuals identified, resulting in fewer face-to-face LHC appointments. Phone screener and LHC responses showed high levels of agreement for most eligibility questions. However, lower levels of agreement were seen for educational status in all individuals, and for overall eligibility criteria in younger and minority ethnic groups. Lower levels of agreement for USPSTF criteria (vs PLCOm2012) are likely explained by the greater influence of smoking consumption on this score. Ambiguous responses regarding smoking consumption during the phone screener were interpreted to maximise lung cancer risk estimates, allowing opportunity for face-to-face eligibility assessment for individuals with borderline eligibility criteria, which may account for some of this variation. With approximately 4–6 weeks between phone screener and LHC, responses may legitimately change between these timepoints. We are unable to assess the impact of potential data entry errors, but a minority of individuals were excluded due to implausible values, highlighting the need for real-time data validation. Finally, periods of smoking abstinence were included in pack-year calculations at the LHC (reported by 62.7%) but not during the phone screener.

      Blinding LHC staff to telephone screener responses allowed LHC responses to be evaluated independently. However, comparisons could only be drawn for those who both responded to the LHC invitation and were eligible during the phone screener, who may differ to non-responders and those who were found to be ineligible at phone screener. From this non-randomised study, it is not possible to ascertain if those considered ineligible by telephone screening were truly ineligible for LCS, and therefore the impact on the sensitivity of risk assessment, but this should be a small proportion.

      Further research should investigate validated multilingual translations, cultural variations with acceptability and inclusion of diverse educational categories to ensure equitability and accuracy. Additionally, efficiency gains resulting from the phone screener are likely to impact cost-effectiveness, which requires further evaluation alongside wider patient satisfaction and any potential added benefits of LHC attendance for ineligible individuals including cardiovascular risk assessment, spirometry and smoking cessation.

      Existing studies demonstrate targeted invitations followed by in-person LCS eligibility assessment lead to inefficient resource utilisation. The data presented here support telephone-based risk assessment as an efficient way to optimise selection for LCS appointments.

      Ethics statements

      Patient consent for publication

      Ethics approval

      Approval received from London City and East Research Ethics Committee (REC) and HRA approval for conduct in the UK (reference: 17/LO/2004). Specific approval was granted by the NHS Health Research Authority via recommendation from the NHS Confidentiality Advisory Group (reference: 18CAG0054) to extract and hold data on individuals prior to consent. Participants gave informed consent to participate in the study before taking part.

      Acknowledgments

      We would like to thank all of the participants who gave up their time to help with this research study. We are also incredibly grateful to all of those who are so dedicated to delivering the SUMMIT Study, which includes all staff at the participating academic, primary care and secondary care sites. Specifically, we thank the Lung Health Check contact centre team who oversaw delivery of the telephone screener (Julian McKee, Mark Clark). We are also hugely grateful to the Yorkshire Lung Screening Trial team (Irene Simmonds, Suzanne Rogerson) for their support and advice in introducing the telephone screener. We would also like to thank all those at GRAIL LLC. who have supported the SUMMIT Study, and particularly those who worked on programming the primary care data search and extraction, the Lung Health Check invitation mailings and the telephone screening questions (Thomas Rooney, Henry Armburg-Jennings, Eduardo Sosa, Jack Galilee, Marcus Foster).

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      Footnotes

      • SLQ and SMJ are joint senior authors.

      • Twitter @LUNGRADIOLOGIST, @QuaifeS, @lungsforliving

      • Collaborators SUMMIT Consortium: Sam M Janes (Lungs For Living Research Centre, UCL Respiratory, University College London, London), Jennifer L Dickson (Lungs For Living Research Centre, UCL Respiratory, University College London, London), Carolyn Horst (Lungs For Living Research Centre, UCL Respiratory, University College London, London), Sophie Tisi (Lungs For Living Research Centre, UCL Respiratory, University College London, London), Helen Hall (Lungs For Living Research Centre, UCL Respiratory, University College London, London), Priyam Verghese (Lungs For Living Research Centre, UCL Respiratory, University College London, London), Andrew Creamer (Lungs For Living Research Centre, UCL Respiratory, University College London, London), Thomas Callender (Lungs For Living Research Centre, UCL Respiratory, University College London, London), Ruth Prendecki (Lungs For Living Research Centre, UCL Respiratory, University College London, London), Amyn Bhamani (Lungs For Living Research Centre, UCL Respiratory, University College London, London), Mamta Ruparel (Lungs For Living Research Centre, UCL Respiratory, University College London, London), Allan Hackshaw (CRUK & UCL Cancer Trials Centre, University College London, London), Laura Farrelly (CRUK & UCL Cancer Trials Centre, University College London, London), Jon Teague (CRUK & UCL Cancer Trials Centre, University College London, London), Anne-Marie Mullin (CRUK & UCL Cancer Trials Centre, University College London, London), Kitty Chan (CRUK & UCL Cancer Trials Centre, University College London, London), Rachael Sarpong (CRUK & UCL Cancer Trials Centre, University College London, London), Malavika Suresh (CRUK & UCL Cancer Trials Centre, University College London, London), Samantha L Quaife (Centre for Prevention, Detection and Diagnosis, Wolfson Institute of Population Health, Barts and The London School of Medicine and Dentistry, Queen Mary University of London, London), Arjun Nair (University College London Hospitals NHS Foundation Trust, London), Anand Devaraj (Royal Brompton and Harefield NHS Foundation Trust, London; National Heart and Lung Institute, Imperial College, London), Kylie Gyertson (University College London Hospitals NHS Foundation Trust, London), Vicky Bowyer (University College London Hospitals NHS Foundation Trust, London), Ethaar El-Emir (University College London Hospitals NHS Foundation Trust, London), Judy Airebamen (University College London Hospitals NHS Foundation Trust, London), Alice Cotton (University College London Hospitals NHS Foundation Trust, London), Kaylene Phua (University College London Hospitals NHS Foundation Trust, London), Elodie Murali (University College London Hospitals NHS Foundation Trust, London), Simranjit Mehta (University College London Hospitals NHS Foundation Trust, London), Janine Zylstra (University College London Hospitals NHS Foundation Trust, London), Karen Parry-Billings (University College London Hospitals NHS Foundation Trust, London), Columbus Ife (University College London Hospitals NHS Foundation Trust, London), April Neville (University College London Hospitals NHS Foundation Trust, London), Paul Robinson (University College London Hospitals NHS Foundation Trust, London), Laura Green (University College London Hospitals NHS Foundation Trust, London), Zahra Hanif (University College London Hospitals NHS Foundation Trust, London), Helen Kiconco (University College London Hospitals NHS Foundation Trust, London), Ricardo McEwen (University College London Hospitals NHS Foundation Trust, London), Dominique Arancon (University College London Hospitals NHS Foundation Trust, London), Nicholas Beech (University College London Hospitals NHS Foundation Trust, London), Derya Ovayolu (University College London Hospitals NHS Foundation Trust, London), Christine Hosein (University College London Hospitals NHS Foundation Trust, London), Sylvia Patricia Enes (University College London Hospitals NHS Foundation Trust, London), Qin April Neville (University College London Hospitals NHS Foundation Trust, London), Jane Rowlands (University College London Hospitals NHS Foundation Trust, London), Aashna Samson (University College London Hospitals NHS Foundation Trust, London), Urja Patel (University College London Hospitals NHS Foundation Trust, London), Fahmida Hoque (University College London Hospitals NHS Foundation Trust, London), Hina Pervez (University College London Hospitals NHS Foundation Trust, London), Sofia Nnorom (University College London Hospitals NHS Foundation Trust, London), Moksud Miah (University College London Hospitals NHS Foundation Trust, London), Julian McKee (University College London Hospitals NHS Foundation Trust, London), Mark Clark (University College London Hospitals NHS Foundation Trust, London), Jeannie Eng (University College London Hospitals NHS Foundation Trust, London), Fanta Bojang (University College London Hospitals NHS Foundation Trust, London), Claire Levermore (University College London Hospitals NHS Foundation Trust, London), Anant Patel (Royal Free London NHS Foundation Trust, London), Sara Lock (Whittington Health NHS Trust, London), Rajesh Banka (Barking, Havering and Redbridge University Hospitals NHS Trust, Essex), Angshu Bhowmik (Homerton University Hospital Foundation Trust, London), Ugo Ekeowa (The Princess Alexandra Hospital NHS Trust, Essex), Zaheer Mangera (North Middlesex University Hospital NHS Trust, London), William M Ricketts (Barts Health NHS Trust, London), Neal Navani (North Bristol NHS Trust, Bristol), Terry O'Shaughnessy (Barts Health NHS Trust, London), Charlotte Cash (Royal Free London NHS Foundation Trust, London), Magali Taylor (University College London Hospitals NHS Foundation Trust, London), Samanjit Hare (Royal Free London NHS Foundation Trust, London), Tunku Aziz (Barts Health NHS Trust, London), Stephen Ellis (Barts Health NHS Trust, London), Anthony Edey (North Bristol NHS Trust, Bristol), Graham Robinson (Royal United Hospitals Bath NHS Foundation Trust, Bath), Alberto Villanueva (Surrey and Sussex Healthcare NHS Trust, Surrey), Hasti Robbie (King's College Hospital NHS Foundation Trust, London), Elena Stefan (The Princess Alexandra Hospital NHS Trust, London), Charlie Sayer (University Hospitals Sussex NHS Foundation Trust, Sussex), Nick Screaton (Royal Papworth Hospital NHS Foundation Trust, Cambridge), Navinah Nundlall (University College London Hospitals NHS Foundation Trust, London), Lyndsey Gallagher (University College London Hospitals NHS Foundation Trust, London), Andrew Crossingham (University College London Hospitals NHS Foundation Trust, London), Thea Buchan (University College London Hospitals NHS Foundation Trust, London), Tanita Limani (University College London Hospitals NHS Foundation Trust, London), Kate Gowers (Lungs For Living Research Centre, UCL Respiratory, University College London, London), Kate Davies (Lungs For Living Research Centre, UCL Respiratory, University College London, London), John McCabe (Lungs For Living Research Centre, UCL Respiratory, University College London, London), Joseph Jacob (Lungs For Living Research Centre, UCL Respiratory, University College London, London; Centre for Medical Image Computing (CMIC), London), Karen Sennett (Killick Street Health Centre, London), Tania Anastasiadis (Tower Hamlets Clinical Commissioning Group, London), Andrew Perugia (Noclor Research Support, London), James Rusius (Noclor Research Support, London).

      • Contributors SMJ and SLQ are joint senior authors. The concept of using telephone screening questions was developed by the study management team for the SUMMIT Study, led by SMJ and with advice provided by MEJC. JLD and HH prepared the manuscript for review and completed the data analysis. All authors contributed to the development and finalisation of the manuscript.

      • Funding The SUMMIT study is funded by GRAIL LLC. through a research grant awarded to SMJ as Principal Investigator. SMJ was a Wellcome Trust Senior Fellow in Clinical Science (WT107963AIA). SMJ is supported by CRUK programme grant (EDDCPGM/100002), the Rosetrees Trust, the Roy Castle Lung Cancer Foundation, the Garfield Weston Trust and UCLH Charitable Foundation. NN is supported by an MRC Clinical Academic Research Partnership (MR/T02481X/1). This work was partly undertaken at UCLH/UCL who received a proportion of funding from the Department of Health’s NIHR Biomedical Research Centre’s funding scheme (SMJ, AN, NN). SLQ is supported by a Cancer Research UK (CRUK) Population Research Fellowship (C50664/A24460) and Barts Charity (MRC&U0036).

      • Competing interests JLD, CH, ST, HH, PV, JM, AH and SMJ are investigators for the SUMMIT Study within which the present study cohort is embedded. SUMMIT is sponsored and conducted by University College London and funded by GRAIL LLC. through a research grant awarded to SMJ as principal investigator. SLQ collaborates on the SUMMIT study and has received honorarium from Elsevier for writing a book chapter. AN is a member of the advisory board for Aidence BV. AH has received an honorarium for an advisory board meeting for GRAIL, a consultation fee for Evidera Inc for a GRAIL initiated project, and previously owned shares in Illumina. SMJ has received honoraria from Astra Zeneca, BARD1 Bioscience and Jansen 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 is an employee of Astra Zeneca. SMJ has received travel funding for a conference from Takeda and an honorarium for planning and speaking at educational meetings from Astra Zeneca. All authors perceive that these disclosures pose no academic conflict for this study and declare no other relationships or activities that could appear to have influenced the submitted work.

      • Provenance and peer review Not commissioned; externally peer reviewed.