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CT screening for lung cancer: comparison of three baseline screening protocols

  • Computed Tomography
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European Radiology Aims and scope Submit manuscript

A Correction to this article was published on 04 February 2019

This article has been updated

Abstract

Purpose

Clinical management decisions arising from the baseline round for lung cancer screening are the most challenging, as findings have accumulated over a lifetime and may be of no clinical concern. To minimize unnecessary harms and costs of workup prior to the first, annual repeat screening, workup should be limited to participants with the highest suspicion of lung cancer while still aiming to identify small, early lung cancers.

Methods

We compared recommendations for immediate, delayed (by 3 or 6 months) workup to assess growth at a malignant rate, and the resulting overall and potential biopsies of three baseline screening protocols: I-ELCAP, the two scenarios of ACR-LungRADS, and the European Consortium. For each protocol, the efficiency ratio (ER) of each recommendation was calculated by dividing the number of participants recommended for that workup by the number of resulting lung cancer diagnoses. The ER for potential biopsies was calculated, assuming that biopsies were performed on all participants recommended for immediate workup as well as those diagnosed with lung cancer after delayed workup.

Results

For I-ELCAP, ACR-LungRADS Scenario 1, ACR-LungRADS Scenario 2, and the European consortium, the overall ER was 13.9, 18.3, 18.3, and 31.9, respectively, and for potential biopsies, it was 2.2, 8.1, 3.2, and 4.4, respectively. ER for immediate workup was 2.9, 8.6, 3.9, and 5.6, respectively, and for delayed workup was 36.1, 160.3, 57.8, and 111.9, respectively.

Conclusions

I-ELCAP recommendations had the lowest ER values for overall, immediate, and delayed workup, and for potential biopsies.

Key Points

• Small differences in protocol thresholds can lead to many unnecessary diagnostic workups.

• I-ELCAP recommendations were the most efficient for immediate and overall workup, and potential biopsies.

Definition of a “positive result” and recommendations for further workup in the baseline round needs to be continually reevaluated and updated.

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Change history

  • 04 February 2019

    The original version of this article, published on 03 December 2018, unfortunately contained a mistake.

Abbreviations

AAPM:

American Association of Physicists in Medicine

ACR:

American College of Radiology

CMS:

Centers for Medicare and Medicaid Services

ER:

Efficiency ratio

I-ELCAP:

International Early Lung Cancer Action Program

LDCT:

Low-dose computed tomography

LungRADS:

Lung Imaging Reporting and Data System

NCN:

Noncalcified nodules

NELSON:

The Dutch-Belgian Lung Cancer Screening Trial

PET:

Positron emission tomography

References

  1. Henschke CI, Salvatore M, Cham M et al (2018) Baseline and annual repeat rounds of screening: implications for optimal regimens of screening. Eur Radiol 28:1085–1094

    Article  PubMed  Google Scholar 

  2. Carter D, Vazquez M, Flieder DB et al (2007) Comparison of pathologic findings of baseline and annual repeat cancers diagnosed on CT screening. Lung Cancer 56:193–199

    Article  PubMed  Google Scholar 

  3. Vazquez M, Carter D, Brambilla E et al (2009) Solitary and multiple resected adenocarcinomas after CT screening for lung cancer: histopathologic features and their prognostic implications. Lung Cancer 64:148–154

    Article  PubMed  Google Scholar 

  4. National Lung Screening Trial Research Team, Aberle DR, Adams AM et al (2011) Reduced lungcancer mortality with low-dose computed tomographic screening. N Engl J Med 365:395–409

    Article  Google Scholar 

  5. van Klaveren RJ, Oudkerk M, Prokop M et al (2009) Management of lung nodules detected by volume CT scanning. N Engl J Med 361:2221–2229

    Article  PubMed  Google Scholar 

  6. Henschke CI, McCauley DI, Yankelevitz DF et al (1999) Early lung cancer action project: overall design and findings from baseline screening. Lancet 354:99–105

    Article  CAS  PubMed  Google Scholar 

  7. Henschke CI, Naidich DP, Yankelevitz DF et al (2001) Early lung cancer action project: initial findings on repeat screenings. Cancer 92:153–159

    Article  CAS  PubMed  Google Scholar 

  8. Pastorino U, Bellomi M, Landoni C et al (2003) Early lung-cancer detection with spiral CT and positron emission tomography in heavy smokers: 2-year results. Lancet 362:593–597

    Article  PubMed  Google Scholar 

  9. Veronesi G, Bellomi M, Mulshine JL et al (2008) Lung cancer screening with low-dose computed tomography: a non-invasive diagnostic protocol for baseline lung nodules. Lung Cancer 61:340–349

    Article  PubMed  Google Scholar 

  10. Henschke CI, Yip R, Yankelevitz DF, Smith JP, for the I-ELCAP Investigators (2013) Definition of a positive test result in computed tomography screening for lung cancer: a cohort study. Ann Intern Med 158:246–252

    Article  PubMed  Google Scholar 

  11. Yip R, Henschke CI, Yankelevitz DF, Smith JP (2014) CT screening for lung cancer: alternative definitions of positive test result based on the national lung screening trial and international early lung cancer action program databases. Radiology 273:591–596

    Article  PubMed  Google Scholar 

  12. Pinsky PF, Gierada DS, Black W et al (2015) Performance of Lung-RADS in the National Lung Screening Trial. A retrospective assessment. Ann Intern Med 162(7):485–491

    Article  PubMed  PubMed Central  Google Scholar 

  13. Henschke CI, Yankelevitz DF, Mirtcheva R, McGuinness G, McCauley DI, Miettinen OS (2002) CT screening for lung cancer: frequency and significance of part-solid and nonsolid nodules. AJR Am J Roentgenol 178:1053–1057

    Article  PubMed  Google Scholar 

  14. Yankelevitz DF, Yip R, Smith JP et al (2015) CT screening for lung cancer: nonsolid nodules in baseline and annual repeat rounds. Radiology 277:555–564

    Article  PubMed  Google Scholar 

  15. Henschke CI, Yip R, Wolf A et al (2016) CT screening for lung cancer: part-solid nodules in baseline and annual repeat rounds. AJR Am J Roentgenol 11:1–9

    Google Scholar 

  16. Yip R, Yankelevitz DF, Hu M et al (2016) Lung cancer deaths in the National Lung Screening Trial Attributed to nonsolid nodules. Radiology 281:589–596

    Article  PubMed  Google Scholar 

  17. Yip R, Wolf A, Tam K et al (2016) Outcomes of lung cancers manifesting as nonsolid nodules. Lung Cancer 97:35–42

    Article  PubMed  Google Scholar 

  18. Yip R, Henschke CI, Xu DM, Li K, Jirapatnakul A, Yankelevitz DF (2017) Lung cancers manifesting as partsolid nodules in the National Lung Screening Trial. AJR Am J Roentgenol 208:1011–1021.

  19. Yip R, Li K, Liu L et al (2018) Controversies on lung cancers manifesting as part-solid nodules. Eur Radiol 28:747–759

    Article  PubMed  Google Scholar 

  20. Travis WD, Brambilla E, Noguchi M et al (2011) International association for the study of lung cancer/American thoracic society/European respiratory society internationalmultidisciplinary classification of lung adenocarcinoma. J Thorac Oncol 6:244–285

    Article  PubMed  PubMed Central  Google Scholar 

  21. International Early Lung Cancer Action Program protocol (2016) www.IELCAP.org/sites/default/files/I-ELCAP-protocol.pdf. Accessed 1 May 2018

  22. National Comprehensive Cancer Network (2014) Clinical Practice Guidelines in Oncology (NCCN Guidelines). Version 1.2014 Lung Cancer Screening. Available from: http://www.nccn.org/professionals/physician_gls/pdf/lung_screening.pdf. Jan 3rd, 2018. Accessed 1 May 2018

  23. Gould MK, Donington J, Lynch WR et al (2013) Evaluation of individuals with pulmonary nodules: when is it lung cancer? Diagnosis and management of lung cancer, 3rd ed: American College of Chest Physicians evidence based clinical practice guidelines. Chest 143(5 Suppl):e93S–e120S

    Article  PubMed  PubMed Central  Google Scholar 

  24. MacMahon H, Naidich DP, Goo JM et al (2017) Guidelines for management of incidental pulmonary nodules detected on CT images: from the Fleischner Society 2017. Radiology 284:228–243

    Article  PubMed  Google Scholar 

  25. Kazerooni EA, Armstrong MR, Amorosa JK et al (2015) ACR CT accreditation program and the lung cancer screening program designation. J Am Coll Radiol 12:38–42

    Article  PubMed  Google Scholar 

  26. American College of Radiology (ACR) (2014) Lung CT screening reporting and data system (Lung-RADS Version 1.0). https://www.acr.org/Quality-Safety/Resources/LungRADS. Accessed 1 May 2018

  27. Oudkerk M, Devaraj A, Vliegenthart R et al (2017) European position statement on lung cancer screening. Lancet Oncol 18:e754–e766

    Article  PubMed  Google Scholar 

  28. Pinsky PF (2018) Does the evidence support the implementation of lung cancer screening with low-dose computed tomography? Expert Rev Respir Med 12:257–260

    Article  CAS  PubMed  Google Scholar 

  29. Centers for Medicare and Medicaid Services (CMS) (2015) Proposed decision memo for screening for Lung Cancer with low dose computed tomography (LDCT) (CAG-00439N). http://www.cms.gov/medicarecoverage-database/details/nca-proposed-decision-memo.aspx?NCAId=274, published January 2, 2015. Accessed 1 May 2018

  30. Jemel A, Fedewa SA (2017) Lung cancer screening with low-dose computed tomography in the United States-2010 to 2015. JAMA Oncol 3:1278–1281

    Article  Google Scholar 

  31. Piana R (2017) The ongoing challenges of lung cancer screening. http://www.ascopost.com/issues/may-25-2017/the-ongoingchallenges-of-lung-cancer-screening/. Published May 25, 2017. Accessed 14 May 2018

  32. Mulshine JL, Ambrose LF (2016) Implementing computed tomography-based lung cancer screening in the community. J Thorac Dis 8(10):E1304–E1306

    Article  PubMed  PubMed Central  Google Scholar 

  33. Wiener RS, Koppelman E, Bolton R et al (2018) Patient and clinician perspectives on shared decision making in early adopting lung cancer screening programs: a qualitative study. J Gen Intern Med 33:1035–1042

    Article  PubMed  PubMed Central  Google Scholar 

  34. Yankelevitz DF (2018) CT screening for lung cancer: successful trial, but failed understanding. J Thorac Oncol 13:12–15

    Article  PubMed  Google Scholar 

  35. Flores RM, Yankelevitz DF (2018) Lung cancer screening-the true benefit. Ann Thorac Surg. https://doi.org/10.1016/j.Athoracsur.2018.03.016

  36. Tanoue LT, Tanner NT, Gould MK, Silvestri GA (2016) Lung cancer screening. Am J Respir Crit Care Med 191:19–33

    Article  Google Scholar 

  37. Caverly TJ, Hayward RA, Reamer E et al (2016) Presentation of benefits and harms in US cancer screening and prevention guidelines: systematic review. J Natl Cancer Inst 108:djv436

    Article  PubMed  PubMed Central  Google Scholar 

  38. American Association of Physicists in Medicine (2017) AAPM position statement on radiation risks from medical imaging procedures. https://www.aapm.org/org/policies/details.asp?id=406&type=PP. Accessed 14 May 2018

  39. Li K, Yip R, Avila R, Henschke CI, Yankelevitz DF (2016) Size and growth assessment of pulmonary nodules: consequence of the rounding. J Thorac Oncol 12:657–662

    Article  PubMed  Google Scholar 

  40. Armato SG 3rd, McLennan G, McNitt-Gray MF et al (2004) Lung image database consortium: developing a resource for the medical imaging research community. Radiology 232:739–748

    Article  PubMed  Google Scholar 

  41. Radiologic Society of North America Quantitative Imaging Biomarkers Alliance (QIBA) Calculator (2017) http://accumetra.com/solutions/qiba-lung-nodule-calculator. Accessed 1 May 2018

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Acknowledgements

I-ELCAP Investigators

Mount Sinai School of Medicine, New York, NY: Claudia I. Henschke, Principal Investigator, David F. Yankelevitz, Rowena Yip, Dongming Xu, Mary Salvatore, Raja Flores, Andrea Wolf; Weill Cornell Medical College: Dorothy I. McCauley, Mildred Chen, Daniel M. Libby, Olli S. Miettinen, James P. Smith, Mark Pasmantier; Cornell University: A. P. Reeves; CBNS, City University of New York at Queens College, Queens, NY; Steven Markowitz, Albert Miller; Fundacion Instituto Valenciano de Oncologia, Valencia, Spain: Jose Cervera Deval; University of Toronto, Princess Margaret Hospital, Toronto, Canada: Heidi Schmidt, Demetris Patsios; Azumi General Hospital, Nagano, Japan: Shusuke Sone, Takaomi Hanaoka; Clinica Universitaria de Navarra, Pamplona, Spain: Javier Zulueta, Luis Montuenga, Maria D. Lozano; Swedish Medical Center, Seattle, WA: Ralph Aye; Christiana Care, Helen F. Graham Cancer Center, Newark, DE: Thomas Bauer; National Cancer Institute Regina Elena, Rome, Italy: Stefano Canitano, Salvatore Giunta; St.Agnes Cancer Center, Baltimore, MD: Enser Cole; LungenZentrum Hirslanden, Zurich, Switzerland: Karl Klingler; Columbia University Medical Center, New York, NY: John H.M. Austin, Gregory D. N. Pearson; Hadassah Medical Organization, Jerusalem, Israel: Dorith Shaham; Holy Cross Hospital Cancer Institute, Silver Spring, MD: Cheryl Aylesworth; Nebraska Methodist Hospital, Omaha NE: Patrick Meyers; South Nassau Communities Hospital, Long Island, NY: Shahriyour Andaz; Eisenhower Lucy Curci Cancer Center, Rancho Mirage, CA; Davood Vafai; New York University Medical Center, New York, NY: David Naidich, Georgeann McGuinness; Dorothy E. Schneider Cancer Center, Mills-Peninsula Health Services, San Mateo, CA: Barry Sheppard; State University of New York at Stony Brook, Stony Brook, NY: Matthew Rifkin; ProHealth Care Regional Cancer Center, Waukesha & Oconomowoc Memorial Hospitals, Oconomowoc, WI: M. Kristin Thorsen, Richard Hansen; Maimonides Medical Center, Brooklyn, NY: Samuel Kopel; Wellstar Health System, Marietta GA: William Mayfield; St. Joseph Health Center, St. Charles, MO: Dan Luedke; Roswell Park Cancer Institute, Buffalo, NY: Donald Klippenstein, Alan Litwin, Peter A. Loud; Upstate Medical Center, Syracuse, NY: Leslie J. Kohman, Ernest M. Scalzetti; Jackson Memorial Hospital, University of Miami, Miami, FL; Richard Thurer; State University of New York, North Shore-Long Island Jewish Health System, New Hyde Park, NY: Arfa Khan, Rakesh Shah; The 5th Affiliated Hospital of Sun Yat-Sen University, Zhuhai, China: Xueguo Liu; Mercy Medical Center, Rockville Center, NY: Gary Herzog; Shin Kong Wu Ho-Su memorial Hospital, Taipei, Taiwan: Diane Yeh; National Cancer Institute of China, Beijing, China: Ning Wu; Staten Island University Hospital, Staten Island NY: Joseph Lowry, Mary Salvatore; Central Main Medical Center: Carmine Frumiento; Mount Sinai School of Medicine, New York, NY: David S. Mendelson; Georgia Institute for Lung Cancer Research, Atlanta, GA: Michael V. Smith; The Valley Hospital Cancer Center, Paramus NJ: Robert Korst; Health Group Physimed/McGill University, Montreal, CA: Jana Taylor; Memorial Sloan-Kettering Cancer Center, New York, NY: Robert T. Heelan, Michelle S. Ginsberg; John Muir Cancer Institute, Concord CA: Michaela Straznicka; Atlantic Health Morristown Memorial Hospital, Morristown NJ: Mark Widmann; Alta Bates Summit Medical Center, Berkeley CA: Gary Cecchi; New York Medical College, Valhalla, NY: Terence A.S. Matalon; St. Joseph’s Hospital, Atlanta GA: Paul Scheinberg; Mount Sinai Comprehensive Cancer Center, Miami Beach, FL: Shari-Lynn Odzer; Aurora St. Luke’s Medical Center, Milwaukee WI: David Olsen; City of Hope National Medical Center, Duarte, CA: Fred Grannis, Arnold Rotter; Evanston Northwestern Healthcare Medical Group, Evanston, IL: Daniel Ray; Greenwich Hospital, Greenwich, CT: David Mullen; Our Lady of Mercy Medical Center, Bronx, NY: Peter H. Wiernik; Baylor University Medical Center, Dallas TX: Edson H. Cheung; Sequoia Hospital, Redwood City CA: Melissa Lim; Glens Falls Hospital, Glens Falls NY: Louis DeCunzo; Atlantic Medical Imaging, Atlantic City NJ: Robert Glassberg; Karmanos Cancer Institute, Detroit, MI: Harvey Pass, Carmen Endress; Rush University, Chicago IL: Mark Yoder, Palmi Shah; Building Trades, Oak Ridge TN: Laura Welch; Sharp Memorial Hospital, San Diego, CA: Michael Kalafer; Newark Beth Israel Medical Center, Newark NJ Jeremy Green; Guthrie Cancer Center, Sayre PA: Comprehensive Cancer Centers of the Desert, Palm Springs CA: Elmer Camacho; Dickstein Cancer Treatment Center, White Plains Hospital, White Plains NY: Cynthia Chin; Presbyterian Healthcare, Charlotte NC: James O’Brien; SUNY Downstate, Brooklyn NY: David Gorden; Bend Memorial Hospital, Bend OR: Albert Koch; University of Toledo, Toledo OH: James Wiley. The conclusions stated in this report are those of the authors and do not represent the views or policies of the Department of Veterans Affairs and the U.S. Government.

Funding

This study was partially funded by the Flight Attendants Medical Research Institute and the U. S. Department of Veterans Affairs.

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Authors and Affiliations

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Corresponding author

Correspondence to Claudia I. Henschke.

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Guarantor

The scientific guarantor of this publication is Dr. Claudia Henschke.

Conflict of interest

The authors of this manuscript declare relationships with the following companies:

Dr. Yankelevitz is a named inventor on a number of patents and patent applications relating to the evaluation of diseases of the chest including measurement of nodules. Some of these, which are owned by Cornell Research Foundation (CRF), are non-exclusively licensed to General Electric. As an inventor of these patents, Dr. Yankelevitz is entitled to a share of any compensation which CRF may receive from its commercialization of these patents. He is also an equity owner in Accumetra, a privately held technology company committed to improving the science and practice of image-based decision making. Dr. Yankelevitz also serves on the advisory board of GRAIL.

Dr. Henschke is the President and serves on the board of the Early Diagnosis and Treatment Research Foundation. She receives no compensation from the Foundation. The Foundation is established to provide grants for projects, conferences, and public databases for research on early diagnosis and treatment of diseases. Dr. Claudia Henschke is also a named inventor on a number of patents and patent applications relating to the evaluation of pulmonary nodules on CT scans of the chest which are owned by Cornell Research Foundation (CRF). Since 2009, Dr. Henschke does not accept any financial benefit from these patents including royalties and any other proceeds related to the patents or patent applications owned by CRF.

The other authors of this manuscript declare no relationships with any companies, whose products or services may be related to the subject matter of the article.

Statistics and biometry

Two of the authors have significant statistical expertise (Claudia Henschke and Rowena Yip).

Informed consent

Written informed consent was obtained from all subjects (patients) in this study.

Ethical approval

Institutional Review Board approval was obtained.

Study subjects or cohorts overlap

Some study subjects have been previously reported for lung findings but comparison of the three protocols and recommendations for invasive workup and resulting diagnoses have never been reported.

Methodology

• Retrospective

• Observational (cohort)

• Multicenter study

Additional information

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The original version of this article was revised: The presentation of Table 3 was incorrect.

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Henschke, C.I., Yip, R., Ma, T. et al. CT screening for lung cancer: comparison of three baseline screening protocols. Eur Radiol 29, 5217–5226 (2019). https://doi.org/10.1007/s00330-018-5857-5

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