Circulating Tumor Cells in Lung Cancer

  • Chapter
  • First Online:
Cancer Metastasis Through the Lymphovascular System
  • 1051 Accesses

Abstract

The detection and identification of circulating tumor cells (CTCs) and the analysis of the information they provide are often the subject of discussion in thoracic oncology, in particular for routine clinical use. However, CTCs are being used for an increasing range of applications in several domains of lung carcinoma. Thus, CTCs can participate in better defining not only the prognosis and diagnosis of lung cancer but also screening for the disease. CTCs can also contribute to the major therapeutic orientations through not only the study of the efficacy of targeted molecules but also of immunotherapy. In addition, the study of CTCs provides a better understanding of the natural history of lung cancer and of the mechanisms of metastasis. This review analyzes the different orientations and therapeutic approaches associated with the study of CTCs in the domain of thoracic oncology.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 99.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 129.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free ship** worldwide - see info
Hardcover Book
USD 179.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free ship** worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  1. Zhang Y, Luo G, Etxeberria J, Hao Y. Global patterns and trends in lung cancer incidence: a population-based study. J Thorac Oncol. 2021;16(6):933–44. https://doi.org/10.1016/j.jtho.2021.01.1626.

    Article  PubMed  Google Scholar 

  2. Heeke S, Benzaquen J, Hofman V, Ilié M, Allegra M, Long-Mira E, Lassalle S, Tanga V, Salacroup C, Bonnetaud C, Fayada J, Gazoppi L, Ribeyre L, Castelnau O, Garnier G, Cattet F, Nanni I, de Fraipont F, Cohen C, Berthet JP, Leroy S, Poudenx M, Marquette CH, Denis MG, Barlesi F, Hofman P. Critical assessment in routine clinical practice of liquid biopsy for EGFR status testing in non-small-cell lung cancer: a single-laboratory experience (LPCE, Nice, France). Clin Lung Cancer. 2020;21(1):56–65.e8. https://doi.org/10.1016/j.cllc.2019.07.010.

    Article  CAS  PubMed  Google Scholar 

  3. Heeke S, Hofman V, Benzaquen J, Otto J, Tanga V, Zahaf K, Allegra M, Long-Mira E, Lassalle S, Marquette CH, Ilie M, Hofman P. Detection of EGFR mutations from plasma of NSCLC patients using an automatic cartridge-based PCR system. Front Pharmacol. 2021;12:657743. https://doi.org/10.3389/fphar.2021.657743.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Hofman P. Next-generation sequencing with liquid biopsies from treatment-Naïve non-small cell lung carcinoma patients. Cancers (Basel). 2021;13(9):2049. https://doi.org/10.3390/cancers13092049.

    Article  CAS  Google Scholar 

  5. Alix-Panabières C. The future of liquid biopsy. Nature. 2020;579(7800):S9. https://doi.org/10.1038/d41586-020-00844-5.

    Article  CAS  PubMed  Google Scholar 

  6. Pantel K. Blood tests for early detection of lung cancer: challenges and promises. Lancet Respir Med. 2020;8(7):654–6.

    Article  Google Scholar 

  7. Hofman V, Ilie M, Long E, Guibert N, Selva E, Washetine K, Mograbi B, Mouroux J, Vénissac N, Reverso-Meinietti J, Milano G, Mazières J, Marquette CH, Paterlini-Bréchot P, Hofman P. Detection of circulating tumor cells from lung cancer patients in the era of targeted therapy: promises, drawbacks and pitfalls. Curr Mol Med. 2014;14(4):440–56.

    Article  CAS  Google Scholar 

  8. Hofman VJ, Ilie M, Hofman PM. Detection and characterization of circulating tumor cells in lung cancer: why and how? Cancer Cytopathol. 2016;124(6):380–7.

    Article  Google Scholar 

  9. Riethdorf S, O’Flaherty L, Hille C, Pantel K. Clinical applications of the CellSearch platform in cancer patients. Adv Drug Deliv Rev. 2018;125:102–21.

    Article  CAS  Google Scholar 

  10. Xu M, Liu W, Zou K, Wei S, Zhang X, Li E, Wang Q. Design and clinical application of an integrated microfluidic device for circulating tumor cells isolation and single-cell analysis. Micromachines (Basel). 2021;12(1):49.

    Article  Google Scholar 

  11. Rolfo C, Mack PC, Scagliotti GV, Baas P, Barlesi F, Bivona TG, Herbst RS, Mok TS, Peled N, Pirker R, Raez LE, Reck M, Riess JW, Sequist LV, Shepherd FA, Sholl LM, Tan DSW, Wakelee HA, Wistuba II, Wynes MW, Carbone DP, Hirsch FR, Gandara DR. Liquid biopsy for advanced non-small cell lung cancer (NSCLC): a statement paper from the IASLC. J Thorac Oncol. 2018;13(9):1248–68.

    Article  Google Scholar 

  12. Alix-Panabières C, Pantel K. Liquid biopsy: from discovery to clinical application. Cancer Discov. 2021;11(4):858–73. https://doi.org/10.1158/2159-8290.CD-20-1311.

    Article  PubMed  Google Scholar 

  13. Cortés-Hernández LE, Eslami-S Z, Alix-Panabières C. Liquid biopsy to detect circulating tumor cells: is it ready for a value proposition in laboratory medicine? J Appl Lab Med. 2020;5(5):1027–37.

    Article  Google Scholar 

  14. Cortés-Hernández LE, Eslami-S Z, Pantel K, Alix-Panabières C. Molecular and functional characterization of circulating tumor cells: from discovery to clinical application. Clin Chem. 2020;66(1):97–104.

    Article  Google Scholar 

  15. Ross K, Pailler E, Faugeroux V, Taylor M, Oulhen M, Auger N, Planchard D, Soria JC, Lindsay CR, Besse B, Vielh P, Farace F. The potential diagnostic power of circulating tumor cell analysis for non-small-cell lung cancer. Expert Rev Mol Diagn. 2015;15(12):1605–29. https://doi.org/10.1586/14737159.2015.1111139.

    Article  CAS  PubMed  Google Scholar 

  16. Chemi F, Mohan S, Guevara T, Clipson A, Rothwell DG, Dive C. Early dissemination of circulating tumor cells: biological and clinical insights. Front Oncol. 2021;11:672195. https://doi.org/10.3389/fonc.2021.672195.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Lindsay CR, Faugeroux V, Michiels S, Pailler E, Facchinetti F, Ou D, Bluthgen MV, Pannet C, Ngo-Camus M, Bescher G, Caramella C, Billiot F, Remon J, Planchard D, Soria JC, Besse B, Farace F. A prospective examination of circulating tumor cell profiles in non-small-cell lung cancer molecular subgroups. Ann Oncol. 2017;28(7):1523–31.

    Article  CAS  Google Scholar 

  18. Lindsay CR, Blackhall FH, Carmel A, Fernandez-Gutierrez F, Gazzaniga P, Groen HJM, Hiltermann TJN, Krebs MG, Loges S, López-López R, Muinelo-Romay L, Pantel K, Priest L, Riethdorf S, Rossi E, Terstappen L, Wikman H, Soria JC, Farace F, Renehan A, Dive C, Besse B, Michiels S. EPAC-lung: pooled analysis of circulating tumour cells in advanced non-small cell lung cancer. Eur J Cancer. 2019;117:60–8.

    Article  CAS  Google Scholar 

  19. Hofman V, Bonnetaud C, Ilie MI, Vielh P, Vignaud JM, Fléjou JF, Lantuejoul S, Piaton E, Mourad N, Butori C, Selva E, Poudenx M, Sibon S, Kelhef S, Vénissac N, Jais JP, Mouroux J, Molina TJ, Hofman P. Preoperative circulating tumor cell detection using the isolation by size of epithelial tumor cell method for patients with lung cancer is a new prognostic biomarker. Clin Cancer Res. 2011;17(4):827–35.

    Article  CAS  Google Scholar 

  20. Hou JM, Krebs MG, Lancashire L, Sloane R, Backen A, Swain RK, Priest LJ, Greystoke A, Zhou C, Morris K, Ward T, Blackhall FH, Dive C. Clinical significance and molecular characteristics of circulating tumor cells and circulating tumor microemboli in patients with small-cell lung cancer. J Clin Oncol. 2012;30(5):525–32. https://doi.org/10.1200/JCO.2010.33.3716.

    Article  PubMed  Google Scholar 

  21. Krebs MG, Sloane R, Priest L, Lancashire L, Hou JM, Greystoke A, Ward TH, Ferraldeschi R, Hughes A, Clack G, Ranson M, Dive C, Blackhall FH. Evaluation and prognostic significance of circulating tumor cells in patients with non-small-cell lung cancer. J Clin Oncol. 2011;29(12):1556–63. https://doi.org/10.1200/JCO.2010.28.7045.

    Article  PubMed  Google Scholar 

  22. Foy V, Lindsay CR, Carmel A, Fernandez-Gutierrez F, Krebs MG, Priest L, Carter M, Groen HJM, Hiltermann TJN, de Luca A, Farace F, Besse B, Terstappen L, Rossi E, Morabito A, Perrone F, Renehan A, Faivre-Finn C, Normanno N, Dive C, Blackhall F, Michiels S. EPAC-lung: European pooled analysis of the prognostic value of circulating tumour cells in small cell lung cancer. Transl Lung Cancer Res. 2021;10(4):1653–65. https://doi.org/10.21037/tlcr-20-1061.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Chemi F, Rothwell DG, McGranahan N, Gulati S, Abbosh C, Pearce SP, Zhou C, Wilson GA, Jamal-Hanjani M, Birkbak N, Pierce J, Kim CS, Ferdous S, Burt DJ, Slane-Tan D, Gomes F, Moore D, Shah R, Al Bakir M, Hiley C, Veeriah S, Summers Y, Crosbie P, Ward S, Mesquita B, Dynowski M, Biswas D, Tugwood J, Blackhall F, Miller C, Hackshaw A, Brady G, Swanton C, Dive C, TRACERx Consortium. Pulmonary venous circulating tumor cell dissemination before tumor resection and disease relapse. Nat Med. 2019;25(10):1534–9.

    Article  CAS  Google Scholar 

  24. Crosbie PA, Shah R, Krysiak P, Zhou C, Morris K, Tugwood J, Booton R, Blackhall F, Dive C. Circulating tumor cells detected in the tumor-draining pulmonary vein are associated with disease recurrence after surgical resection of NSCLC. J Thorac Oncol. 2016;11(10):1793–7. https://doi.org/10.1016/j.jtho.2016.06.017.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Farace F, Massard C, Vimond N, Drusch F, Jacques N, Billiot F, Laplanche A, Chauchereau A, Lacroix L, Planchard D, Le Moulec S, André F, Fizazi K, Soria JC, Vielh P. A direct comparison of CellSearch and ISET for circulating tumour-cell detection in patients with metastatic carcinomas. Br J Cancer. 2011;105(6):847–53.

    Article  CAS  Google Scholar 

  26. Hofman V, Ilie MI, Long E, Selva E, Bonnetaud C, Molina T, Vénissac N, Mouroux J, Vielh P, Hofman P. Detection of circulating tumor cells as a prognostic factor in patients undergoing radical surgery for non-small-cell lung carcinoma: comparison of the efficacy of the CellSearch Assay™ and the isolation by size of epithelial tumor cell method. Int J Cancer. 2011;129(7):1651–60.

    Article  CAS  Google Scholar 

  27. Alix-Panabières C, Mader S, Pantel K. Epithelial-mesenchymal plasticity in circulating tumor cells. J Mol Med (Berl). 2017;95:133–42. https://doi.org/10.1007/s00109-016-1500-6.

    Article  CAS  Google Scholar 

  28. Hofman V, Long E, Ilie M, Bonnetaud C, Vignaud JM, Fléjou JF, Lantuejoul S, Piaton E, Mourad N, Butori C, Selva E, Marquette CH, Poudenx M, Sibon S, Kelhef S, Vénissac N, Jais JP, Mouroux J, Molina TJ, Vielh P, Hofman P. Morphological analysis of circulating tumour cells in patients undergoing surgery for non-small cell lung carcinoma using the isolation by size of epithelial tumour cell (ISET) method. Cytopathology. 2012;23(1):30–8.

    Article  CAS  Google Scholar 

  29. Manjunath Y, Mitchem JB, Suvilesh KN, Avella DM, Kimchi ET, Staveley-O’Carroll KF, Deroche CB, Pantel K, Li G, Kaifi JT. Circulating Giant tumor-macrophage fusion cells are independent prognosticators in patients with NSCLC. J Thorac Oncol. 2020;15(9):1460–71.

    Article  CAS  Google Scholar 

  30. Chinniah C, Aguarin L, Cheng P, Decesaris C, Cutillo A, Berman AT, Frick M, Doucette A, Cengel KA, Levin W, Hahn S, Dorsey JF, Simone CB 2nd, Kao GD. Early detection of recurrence in patients with locally advanced non-small-cell lung cancer via circulating tumor cell analysis. Clin Lung Cancer. 2019;20(5):384–90.

    Article  Google Scholar 

  31. Blackhall F, Frese KK, Simpson K, Kilgour E, Brady G, Dive C. Will liquid biopsies improve outcomes for patients with small-cell lung cancer? Lancet Oncol. 2018;19(9):e470–e81.

    Article  Google Scholar 

  32. Shishido SN, Carlsson A, Nieva J, Bethel K, Hicks JB, Bazhenova L, Kuhn P. Circulating tumor cells as a response monitor in stage IV non-small cell lung cancer. J Transl Med. 2019;17(1):294.

    Article  Google Scholar 

  33. Pawlikowska P, Faugeroux V, Oulhen M, Aberlenc A, Tayoun T, Pailler E, Farace F. Circulating tumor cells (CTCs) for the noninvasive monitoring and personalization of non-small cell lung cancer (NSCLC) therapies. J Thorac Dis. 2019;11(Suppl 1):S45–56. https://doi.org/10.21037/jtd.2018.12.80.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Ge B, Wang Y, Lei S, Zhang J. Effect of phenotypic detection of circulating tumor cells marked by epithelial-mesenchymal transformation on the prognosis of lung cancer: a protocol for systematic review and meta-analysis. Medicine (Baltimore). 2020;99(44):e22960.

    Article  CAS  Google Scholar 

  35. Ilié M, Szafer-Glusman E, Hofman V, Chamorey E, Lalvée S, Selva E, Leroy S, Marquette CH, Kowanetz M, Hedge P, Punnoose E, Hofman P. Detection of PD-L1 in circulating tumor cells and white blood cells from patients with advanced non-small-cell lung cancer. Ann Oncol. 2018;29(1):193–9.

    Article  Google Scholar 

  36. Sinoquet L, Jacot W, Gauthier L, Pouderoux S, Viala M, Cayrefourcq L, Quantin X, Alix-Panabières C. Programmed cell death ligand 1-expressing circulating tumor cells: a new prognostic biomarker in non-small cell lung cancer. Clin Chem. 2021;6:hvab131. https://doi.org/10.1093/clinchem/hvab131.

    Article  Google Scholar 

  37. Murlidhar V, Reddy RM, Fouladdel S, Zhao L, Ishikawa MK, Grabauskiene S, Zhang Z, Lin J, Chang AC, Carrott P, Lynch WR, Orringer MB, Kumar-Sinha C, Palanisamy N, Beer DG, Wicha MS, Ramnath N, Azizi E, Nagrath S. Poor prognosis indicated by venous circulating tumor cell clusters in early-stage lung cancers. Cancer Res. 2017;77(18):5194–206. https://doi.org/10.1158/0008-5472.CAN-16-2072.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Hofman P. Liquid biopsy and therapeutic targets: present and future issues in thoracic oncology. Cancers (Basel). 2017;9(11):154.

    Article  Google Scholar 

  39. Hofman P, Heeke S, Alix-Panabières C, Pantel K. Liquid biopsy in the era of immuno-oncology: is it ready for prime-time use for cancer patients? Ann Oncol. 2019;30(9):1448–59.

    Article  CAS  Google Scholar 

  40. Maheswaran S, Sequist LV, Nagrath S, Ulkus L, Brannigan B, Collura CV, Inserra E, Diederichs S, Iafrate AJ, Bell DW, Digumarthy S, Muzikansky A, Irimia D, Settleman J, Tompkins RG, Lynch TJ, Toner M, Haber DA. Detection of mutations in EGFR in circulating lung-cancer cells. N Engl J Med. 2008;359(4):366–77. https://doi.org/10.1056/NEJMoa0800668.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Liu HE, Vuppalapaty M, Wilkerson C, Renier C, Chiu M, Lemaire C, Che J, Matsumoto M, Carroll J, Crouse S, Hanft VR, Jeffrey SS, Di Carlo D, Garon EB, Goldman J, Sollier E. Detection of EGFR mutations in cfDNA and CTCs, and comparison to tumor tissue in non-small-cell-lung-cancer (NSCLC) patients. Front Oncol. 2020;10:572895.

    Article  Google Scholar 

  42. Catelain C, Pailler E, Oulhen M, Faugeroux V, Pommier AL, Farace F. Detection of gene rearrangements in circulating tumor cells: examples of ALK-, ROS1-, RET-rearrangements in non-small-cell lung cancer and ERG-rearrangements in prostate cancer. Adv Exp Med Biol. 2017;994:169–79.

    Article  CAS  Google Scholar 

  43. Ilie M, Mazieres J, Chamorey E, Heeke S, Benzaquen J, Thamphya B, Boutros J, Tiotiu A, Fayada J, Cadranel J, Poudenx M, Moro-Sibilot D, Barlesi F, Thariat J, Clement-Duchene C, Tomasini P, Hofman V, Marquette CH, Hofman P, STALKLUNG01 Study Consortium Investigators. Prospective multi-center validation of the detection of ALK rearrangements of circulating tumor cells for non-invasive longitudinal management of patients with advanced non-small cell lung cancer. J Thorac Oncol. 2021;S1556-0864(21):01664–6. https://doi.org/10.1016/j.jtho.2021.01.1617.

    Article  CAS  Google Scholar 

  44. Ilie M, Szafer-Glusman E, Hofman V, Long-Mira E, Suttmann R, Darbonne W, Butori C, Lalvée S, Fayada J, Selva E, Yu W, Marquette CH, Shames DS, Punnoose E, Hofman P. Expression of MET in circulating tumor cells correlates with expression in tumor tissue from advanced-stage lung cancer patients. Oncotarget. 2017;8(16):26112–21.

    Article  Google Scholar 

  45. Hofman P. Detecting resistance to therapeutic ALK inhibitors in tumor tissue and liquid biopsy markers: an update to a clinical routine practice. Cell. 2021;10(1):168.

    Article  CAS  Google Scholar 

  46. Berger LA, Janning M, Velthaus JL, Ben-Batalla I, Schatz S, Falk M, Iglauer P, Simon R, Cao R, Forcato C, Manaresi N, Bramlett K, Buson G, Hanssen A, Tiemann M, Sauter G, Bokemeyer C, Riethdorf S, Reck M, Pantel K, Wikman H, Loges S. Identification of a high-level MET amplification in CTCs and cfTNA of an ALK-positive NSCLC patient develo** evasive resistance to Crizotinib. J Thorac Oncol. 2018;13(12):e243–e6.

    Article  CAS  Google Scholar 

  47. Ilie M, Hofman V, Dietel M, Soria JC, Hofman P. Assessment of the PD-L1 status by immunohistochemistry: challenges and perspectives for therapeutic strategies in lung cancer patients. Virchows Arch. 2016;468(5):511–25. https://doi.org/10.1007/s00428-016-1910-4.

    Article  CAS  PubMed  Google Scholar 

  48. Gosney JR, Boothman AM, Ratcliffe M, Kerr KM. Cytology for PD-L1 testing: a systematic review. Lung Cancer. 2020;141:101–6. https://doi.org/10.1016/j.lungcan.2020.01.010.

    Article  PubMed  Google Scholar 

  49. Janning M, Kobus F, Babayan A, Wikman H, Velthaus JL, Bergmann S, Schatz S, Falk M, Berger LA, Böttcher LM, Päsler S, Gorges TM, O’Flaherty L, Hille C, Joosse SA, Simon R, Tiemann M, Bokemeyer C, Reck M, Riethdorf S, Pantel K, Loges S. Determination of PD-L1 expression in circulating tumor cells of NSCLC patients and correlation with response to PD-1/PD-L1 inhibitors. Cancers (Basel). 2019;11(6):835.

    Article  CAS  Google Scholar 

  50. Calabrese F, Lunardi F, Pezzuto F, Fortarezza F, Vuljan SE, Marquette C, Hofman P. Are there new biomarkers in tissue and liquid biopsies for the early detection of non-small cell lung cancer? J Clin Med. 2019;8(3):414. https://doi.org/10.3390/jcm8030414.

    Article  CAS  PubMed Central  Google Scholar 

  51. Benzaquen J, Boutros J, Marquette C, Delingette H, Hofman P. Lung cancer screening, towards a multidimensional approach: why and how? Cancers (Basel). 2019;11(2):212. https://doi.org/10.3390/cancers11020212.

    Article  Google Scholar 

  52. Ilie M, Hofman V, Long-Mira E, Selva E, Vignaud JM, Padovani B, Mouroux J, Marquette CH, Hofman P. “sentinel” circulating tumor cells allow early diagnosis of lung cancer in patients with chronic obstructive pulmonary disease. PLoS One. 2014;9(10):e111597.

    Article  Google Scholar 

  53. Marquette CH, Boutros J, Benzaquen J, Ferreira M, Pastre J, Pison C, Padovani B, Bettayeb F, Fallet V, Guibert N, Basille D, Ilie M, Hofman V, Hofman P. AIR project study group. Lancet Respir Med. 2020;8(7):709–16.

    Article  Google Scholar 

  54. Carter L, Rothwell DG, Mesquita B, Smowton C, Leong HS, Fernandez-Gutierrez F, Li Y, Burt DJ, Antonello J, Morrow CJ, Hodgkinson CL, Morris K, Priest L, Carter M, Miller C, Hughes A, Blackhall F, Dive C, Brady G. Molecular analysis of circulating tumor cells identifies distinct copy-number profiles in patients with chemosensitive and chemorefractory small-cell lung cancer. Nat Med. 2017;23(1):114–9.

    Article  CAS  Google Scholar 

  55. Heeke S, Mograbi B, Alix-Panabières C, Hofman P. Never travel alone: the crosstalk of circulating tumor cells and the blood microenvironment. Cell. 2019;8(7):714.

    Article  CAS  Google Scholar 

  56. Alix-Panabières C. EPISPOT assay: detection of viable DTCs/CTCs in solid tumor patients. Recent Results Cancer Res. 2012;195:69–76. https://doi.org/10.1007/978-3-642-28160-0_6.

    Article  PubMed  Google Scholar 

  57. Ilie M, Hofman V, Long E, Bordone O, Selva E, Washetine K, Marquette CH, Hofman P. Current challenges for detection of circulating tumor cells and cell-free circulating nucleic acids, and their characterization in non-small cell lung carcinoma patients. What is the best blood substrate for personalized medicine? Ann Transl Med. 2014;2(11):107. https://doi.org/10.3978/j.issn.2305-5839.2014.08.11.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Connors D, Allen J, Alvarez JD, Boyle J, Cristofanilli M, Hiller C, Keating S, Kelloff G, Leiman L, McCormack R, Merino D, Morgan E, Pantel K, Rolfo C, Serrano MJ, Pia Sanzone A, Schlange T, Sigman C, Stewart M. International liquid biopsy standardization alliance white paper. Crit Rev Oncol Hematol. 2020;156:103112.

    Article  Google Scholar 

  59. Massard C, Borget I, Farace F, Aspeslagh S, Le Deley MC, Le Tourneau C, Bidard FC, Pierga JY, Dieras V, Hofman P, Spano JP, Ferte C, Lacroix L, Soria JC. RECIST response and variation of circulating tumour cells in phase 1 trials: a prospective multicentric study. Eur J Cancer. 2017;83:185–93.

    Article  Google Scholar 

  60. Nejlund S, Smith J, Kraan J, Stender H, Van MN, Langkjer ST, Nielsen MT, Sölétormos G, Hillig T. Cryopreservation of circulating tumor cells for enumeration and characterization. Biopreserv Biobank. 2016;14(4):330–7. https://doi.org/10.1089/bio.2015.007.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Paul Hofman .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2022 The Author(s), under exclusive license to Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Hofman, P. (2022). Circulating Tumor Cells in Lung Cancer. In: Leong, S.P., Nathanson, S.D., Zager, J.S. (eds) Cancer Metastasis Through the Lymphovascular System. Springer, Cham. https://doi.org/10.1007/978-3-030-93084-4_15

Download citation

Publish with us

Policies and ethics

Navigation