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The prognostic value of molecular residual disease (MRD) in non‐small cell lung cancer (NSCLC) cases using high‐depth circulating tumor DNA (ctDNA) sequencing has been well documented. The utility of MRD to direct individualized therapy has increasingly emerged in the clinical trial design of solid tumors, such as escalation or de‐escalation of adjuvant therapy based on MRD. And the efficiency of MRD assay is a key determinant to the success of clinical trials, especially the limitation of detection and predictive value. Here, we review the progress made in evaluating the clinical validity of ctDNA‐MRD test and provide insight into exploiting these developments to future clinical scenarios for improving the individualized therapy of NSCLC.
The prognostic value of molecular residual disease (MRD) in non‐small cell lung cancer (NSCLC) cases using high‐depth circulating tumor DNA (ctDNA) sequencing has been well documented. The utility of MRD to direct individualized therapy has increasingly emerged in the clinical trial design of solid tumors, such as escalation or de‐escalation of adjuvant therapy based on MRD. And the efficiency of MRD assay is a key determinant to the success of clinical trials, especially the limitation of detection and predictive value. Here, we review the progress made in evaluating the clinical validity of ctDNA‐MRD test and provide insight into exploiting these developments to future clinical scenarios for improving the individualized therapy of NSCLC.
Wu Y‐L, Lu S, Cheng Y, Zhou Q.‐H, Wang C.‐L, Wang L‐H, et al. Expert consensus of molecular residual disease for non‐small cell lung cancer. J Evidence‐Based Med. 2021;21: 6. https://doi.org/10.12019/j.issn.1671-5144.2021.03.001
Short NJ, Zhou S, Fu C, Berry DA, Walter RB, Freeman SD, et al. Association of measurable residual disease with survival outcomes in patients with acute myeloid leukemia: a systematic review and meta‐analysis. JAMA Oncol. 2020;6(12): 1890–9. https://doi.org/10.1001/jamaoncol.2020.4600
Berry DA, Zhou S, Higley H, Mukundan L, Fu S, Reaman GH, et al. Association of minimal residual disease with clinical outcome in pediatric and adult acute lymphoblastic leukemia: a meta‐analysis. JAMA Oncol. 2017;3(7): e170580. https://doi.org/10.1001/jamaoncol.2017.0580
Schuurhuis GJ, Heuser M, Freeman S, Bene MC, Buccisano F, Cloos J, et al. Minimal/measurable residual disease in AML: a consensus document from the European LeukemiaNet MRD Working Party. Blood. 2018;131(12): 1275–91. https://doi.org/10.1182/blood-2017-09-801498
Mailankody S, Korde N, Lesokhin AM, Lendvai N, Hassoun H, Stetler‐Stevenson M, et al. Minimal residual disease in multiple myeloma: bringing the bench to the bedside. Nat Rev Clin Oncol. 2015;12(5): 286–95. https://doi.org/10.1038/nrclinonc.2014.239
Kumar S, Paiva B, Anderson KC, Durie B, Landgren O, Moreau P, et al. International Myeloma Working Group consensus criteria for response and minimal residual disease assessment in multiple myeloma. Lancet Oncol. 2016;17(8): e328–46. https://doi.org/10.1016/S1470-2045(16)30206-6
Harousseau JL, Avet‐Loiseau H. Minimal residual disease negativity is a new end point of myeloma therapy. J Clin Oncol. 2017;35(25): 2863–5. https://doi.org/10.1200/JCO.2017.73.1331
Paiva B, van Dongen JJ, Orfao A. New criteria for response assessment: role of minimal residual disease in multiple myeloma. Blood. 2015;125(20): 3059–68. https://doi.org/10.1182/blood-2014-11-568907
Abbosh C, Birkbak NJ, Wilson GA, Jamal‐Hanjani M, Constantin T, Salari R, et al. Phylogenetic ctDNA analysis depicts early‐stage lung cancer evolution. Nature 2017;545(7691): 446‐51. https://doi.org/10.1038/nature25161
Chaudhuri AA, Chabon JJ, Lovejoy AF, Newman AM, Stehr H, Azad TD, et al. Early detection of molecular residual disease in localized lung cancer by circulating tumor DNA profiling. Cancer Discov. 2017;7(12): 1394–403. https://doi.org/10.1158/2159-8290.CD-17-0716
Moding EJ, Liu Y, Nabet BY, Chabon JJ, Chaudhuri AA, Hui AB, et al. Circulating tumor DNA dynamics predict benefit from consolidation immunotherapy in locally advanced non‐small‐cell lung cancer. Nat Cancer. 2020;1(2): 176–83. https://doi.org/10.1038/s43018-019-0011-0
Gale D, Heider K, Ruiz‐Valdepenas A, Hackinger S, Perry M, Marsico G, et al. Residual ctDNA after treatment predicts early relapse in patients with early‐stage non‐small cell lung cancer. Ann Oncol. 2022;33(5): 500–10. https://doi.org/10.1016/j.annonc.2022.02.007
Xia L, Mei J, Kang R, Deng S, Chen Y, Yang Y, et al. Perioperative ctDNA‐based molecular residual disease detection for non‐small cell lung cancer: a prospective multicenter cohort study (LUNGCA‐1). Clin Cancer Res. 2021;28(15): 3308–17. https://doi.org/10.1158/1078-0432.CCR-21-3044
Zhang JT, Liu SY, Gao W, Liu SM, Yan HH, Ji L, et al. Longitudinal undetectable molecular residual disease defines potentially cured population in localized non‐small cell lung cancer. Cancer Discov. 2022;12(7): 1690‐701. https://doi.org/10.1158/2159-8290.CD-21-1486
Qiu B, Guo W, Zhang F, Lv F, Ji Y, Peng Y, et al. Dynamic recurrence risk and adjuvant chemotherapy benefit prediction by ctDNA in resected NSCLC. Nat Commun. 2021;12(1): 6770. https://doi.org/10.1038/s41467-021-27022-z
Parikh AR, Van Seventer EE, Siravegna G, Hartwig AV, Jaimovich A, He Y, et al. Minimal residual disease detection using a plasma‐only circulating tumor DNA assay in colorectal cancer patients. Clin Cancer Res. 2021;27(20):5586–94. https://doi.org/10.1158/1078-0432.CCR-21-0410
Rolfo C, Mack P, Scagliotti GV, Aggarwal C, Arcila ME, Barlesi F, et al. Liquid biopsy for advanced non‐small cell lung cancer: a consensus statement from the International Association for the Study of Lung Cancer (IASLC). J Thorac Oncol, 2021;16(10):1647, 1662. https://doi.org/10.1016/j.jtho.2021.06.017
Pascual J, Attard G, Bidard FC, Curigliano G, De Mattos‐Arruda L, Diehn M, et al. ESMO recommendations on the use of circulating tumour DNA assays for patients with cancer: a report from the ESMO Precision Medicine Working Group. Ann Oncol. 2022;33(8):750–68. https://doi.org/10.1016/j.annonc.2022.05.520
Wen S, Dai L, Wang L, Wang W, Wu D, Wang K, et al. Genomic signature of driver genes identified by target next‐generation sequencing in Chinese non‐small cell lung cancer. Oncologist. 2019;24(11):e1070–81. https://doi.org/10.1634/theoncologist.2018-0572
Zhang XC, Wang J, Shao GG, Wang Q, Qu X, Wang B, et al. Comprehensive genomic and immunological characterization of Chinese non‐small cell lung cancer patients. Nat Commun. 2019;10(1):1772. https://doi.org/10.1038/s41467-019-09762-1
Chen J, Yang H, Teo ASM, Amer LB, Sherbaf FG, Tan CQ, et al. Genomic landscape of lung adenocarcinoma in East Asians. Nat Genet. 2020;52(2):177–86. https://doi.org/10.1038/s41588-019-0569-6
Zhang Y, Yao Y, Xu Y, Li L, Gong Y, Zhang K, et al. Pan‐cancer circulating tumor DNA detection in over 10,000 Chinese patients. Nat Commun. 2021;12(1):11. https://doi.org/10.1038/s41467-020-20162-8
Lam VK, Zhang J, Wu CC, Tran HT, Li L, Diao L, et al. Genotype‐specific differences in circulating tumor DNA levels in advanced NSCLC. J Thorac Oncol. 2020;16(4):601–609. https://doi.org/10.1016/j.jtho.2020.12.011
Abbosh C, Birkbak NJ, Swanton C. Early stage NSCLC – challenges to implementing ctDNA‐based screening and MRD detection. Nat Rev Clin Oncol. 2018;15(9):577–86. https://doi.org/10.1038/s41571-018-0058-3
Shen H, Jin Y, Zhao H, Wu M, Zhang K, Wei Z, et al. Potential clinical utility of liquid biopsy in early‐stage non‐small cell lung cancer. BMC Med. 2022;20(1):480. https://doi.org/10.1186/s12916-022-02681-x
Chen K, Shen H, Wu S, Zhu P, Wang C, Lizaso A, et al. Abstract 5916: tumor‐informed patient‐specific panel outperforms tumor‐naïve and tumor‐informed fixed panel for circulating tumor DNA (ctDNA)‐based postoperative monitoring of non‐small cell lung cancer (NSCLC). Cancer Res. 2022;82(Suppl 12):5916. https://doi.org/10.1158/1538-7445.Am2022-5916
Saussele S, Richter J, Guilhot J, Gruber FX, Hjorth‐Hansen H, Almeida A, et al. Discontinuation of tyrosine kinase inhibitor therapy in chronic myeloid leukaemia (EURO‐SKI): a prespecified interim analysis of a prospective, multicentre, non‐randomised, trial. Lancet Oncol. 2018;19(6):747–57. https://doi.org/10.1016/S1470-2045(18)30192-X
Mahon FX, Rea D, Guilhot J, Guilhot F, Huguet F, Nicolini F, et al. Discontinuation of imatinib in patients with chronic myeloid leukaemia who have maintained complete molecular remission for at least 2 years: the prospective, multicentre stop imatinib (STIM) trial. Lancet Oncol. 2010;11:1029–35. https://doi.org/10.1016/S1470-2045(10)70233-3
Rea D, Nicolini FE, Tulliez M, Guilhot F, Guilhot J, Guerci‐Bresler A, et al. Discontinuation of dasatinib or nilotinib in chronic myeloid leukemia: interim analysis of the STOP 2G‐TKI study. Blood 2017;129(7):846–54. https://doi.org/10.1182/blood-2016-09-742205
Ross DM, Pagani IS, Shanmuganathan N, Kok CH, Seymour JF, Mills AK, et al. Long‐term treatment‐free remission of chronic myeloid leukemia with falling levels of residual leukemic cells. Leukemia. 2018;32(12):2572–9. https://doi.org/10.1038/s41375-018-0264-0
Thielen N, van der Holt B, Cornelissen JJ, Verhoef GE, Gussinklo T, Biemond BJ, et al. Imatinib discontinuation in chronic phase myeloid leukaemia patients in sustained complete molecular response: a randomised trial of the Dutch‐Belgian cooperative trial for haemato‐oncology (HOVON). Eur J Cancer. 2013;49(15):3242–6. https://doi.org/10.1016/j.ejca.2013.06.018
Kimura S, Imagawa J, Murai K, Hino M, Kitawaki T, Okada M, et al. Treatment‐free remission after first‐line dasatinib discontinuation in patients with chronic myeloid leukaemia (first‐line DADI trial): a single‐arm, multicentre, phase 2 trial. Lancet Haematol. 2020;7(3):e218–25. https://doi.org/10.1016/S2352-3026(19)30235-2
Etienne G, Guilhot J, Rea D, Rigal‐Huguet F, Nicolini F, Charbonnier A, et al. Long‐term follow‐up of the French stop imatinib (STIM1) study in patients with chronic myeloid leukemia. J Clin Oncol 2017;35(3):298–305. https://doi.org/10.1200/JCO.2016.68.2914
Cross NC, White HE, Muller MC, Saglio G, Hochhaus A, et al. Standardized definitions of molecular response in chronic myeloid leukemia. Leukemia. 2012;26(10):2172–5. https://doi.org/10.1038/leu.2012.104
Hochhaus A, Saussele S, Rosti G, Mahon FX, Janssen JWM, Hjorth‐Hansen H, et al. Chronic myeloid leukaemia: ESMO clinical practice guidelines for diagnosis, treatment and follow‐up. Ann Oncol. 2018;29:iv261. https://doi.org/10.1093/annonc/mdy159
National Comprehensive Cancer Network. Chronic myeloid leukemia version 3. Pennsylvania, PA: National Comprehensive Cancer Network; 2021.
Gatenby RA, Brown JS. Integrating evolutionary dynamics into cancer therapy. Nat Rev Clin Oncol. 2020;17(11):675–86. https://doi.org/10.1038/s41571-020-0411-1
Zhang J, Cunningham JJ, Brown JS, Gatenby RA, et al. Integrating evolutionary dynamics into treatment of metastatic castrate‐resistant prostate cancer. Nat Commun. 2017;8(1):1816. https://doi.org/10.1038/s41467-017-01968-5
Song D, Zhen W, Qing Z, Lei Y, Jiatao Z, Yu C, et al. P49.01 drug holiday based on minimal residual disease status after local therapy following EGFR‐TKI treatment for patients with advanced NSCLC. J Thorac Oncol. 2021. Elsevier. https://doi.org/10.1016/j.jtho.2016.11.950
Guckenberger M, Lievens Y, Bouma AB, Collette L, Dekker A, de Souza NM, et al. Characterisation and classification of oligometastatic disease: a European society for radiotherapy and oncology and European organisation for research and treatment of cancer consensus recommendation. Lancet Oncol. 2020;21(1):e18–28. https://doi.org/10.1016/S1470-45(19)30718-1
Gomez DR, Blumenschein GR, Lee JJ, Hernandez M, Ye R, Camidge DR, et al. Local consolidative therapy versus maintenance therapy or observation for patients with oligometastatic non‐small‐cell lung cancer without progression after first‐line systemic therapy: a multicentre, randomised, controlled, phase 2 study. Lancet Oncol 2016;17(12):1672–82. https://doi.org/10.1016/S1470-2045(16)30532-0
Gomez DR, Tang C, Zhang J, Blumenschein GR, Jr, Hernandez M, Lee JJ, et al. Local consolidative therapy vs. maintenance therapy or observation for patients with oligometastatic non–small‐cell lung cancer: long‐term results of a multi‐institutional, phase Ⅱ, randomized study. J Clin Oncol. 2019;37(18):1558–65. https://doi.org/10.1200/JCO.19.00201
Bauml JM, Mick R, Ciunci C, Aggarwal C, Davis C, Evans T, et al. Pembrolizumab after completion of locally ablative therapy for oligometastatic non‐small cell lung cancer: a phase 2 trial. JAMA Oncol 2019;5(9):1283–90. https://doi.org/10.1001/jamaoncol.2019.1449
Thompson PA, Wierda WG. Eliminating minimal residual disease as a therapeutic end point: working toward cure for patients with CLL. Blood 2016;127(3):279–86. https://doi.org/10.1182/blood-2015-08-634816
Estey E, Othus M, Lee SJ, Appelbaum FR, Gale RP, et al. New drug approvals in acute myeloid leukemia: what's the best end point? Leukemia. 2016;30(3):521–5. https://doi.org/10.1038/leu.2015.262
Yoon JH, Yhim HY, Kwak JY, Ahn JS, Yang DH, Lee JJ, et al. Minimal residual disease‐based effect and long‐term outcome of first‐line dasatinib combined with chemotherapy for adult Philadelphia chromosome‐positive acute lymphoblastic leukemia. Ann Oncol. 2016;27(6):1081–8. https://doi.org/10.1093/annonc/mdw123
Chen YH, Hancock BA, Solzak JP, Brinza D, Scafe C, Miller KD, et al. Next‐generation sequencing of circulating tumor DNA to predict recurrence in triple‐negative breast cancer patients with residual disease after neoadjuvant chemotherapy. NPJ Breast Cancer. 2017;3(1):24. https://doi.org/10.1038/s41523-017-0028-4
McDonald BR, Contente‐Cuomo T, Sammut SJ, Odenheimer‐Bergman A, Ernst B, Perdigones N, et al. Personalized circulating tumor DNA analysis to detect residual disease after neoadjuvant therapy in breast cancer. Sci Transl Med. 2019;11(504):eaax7392. https://doi.org/10.1126/scitranslmed.aax7392
Li S, Lai H, Liu J, Liu Y, Jin L, Li Y, et al. Circulating tumor DNA predicts the response and prognosis in patients with early breast cancer receiving neoadjuvant chemotherapy. JCO Precis Oncol. 2020;4:244–57. PO.19.00292. https://doi.org/10.1200/PO.19.00292
Magbanua MJM, Swigart LB, Wu HT, Hirst GL, Yau C, Wolf DM, et al. Circulating tumor DNA in neoadjuvant‐treated breast cancer reflects response and survival. Ann Oncol. 2021;32(2):229–39. https://doi.org/10.1016/j.annonc.2020.11.007
Zhang Q, Luo J, Wu S, Si H, Gao C, Xu W, et al. Prognostic and predictive impact of circulating tumor DNA in patients with advanced cancers treated with immune checkpoint blockade. Cancer Discov 2020;10(12):1842–53. https://doi.org/10.1158/2159-8290.CD-20-0047
Forde PM, Spicer J, Lu S, Provencio M, Mitsudomi T, Awad MM, et al. Neoadjuvant nivolumab plus chemotherapy in resectable lung cancer. N Engl J Med. 2022;386(21):1973–85. https://doi.org/10.1056/NEJMoa2202170
Reck M, Rodriguez‐Abreu D, Robinson AG, Hui R, Csőszi T, Fülöp A, et al. Five‐year outcomes with pembrolizumab versus chemotherapy for metastatic non‐small‐cell lung cancer with PD‐L1 tumor proportion score >/= 50. J Clin Oncol. 2021;39(21):2339–49. https://doi.org/10.1200/JCO.21.00174
Mok T, Camidge DR, Gadgeel SM, Rosell R, Dziadziuszko R, Kim DW, et al. Updated overall survival and final progression‐free survival data for patients with treatment‐naive advanced ALK‐positive non‐small‐cell lung cancer in the ALEX study. Ann Oncol. 2020;31(8):1056–64. https://doi.org/10.1016/j.annonc.2020.04.478
Ramalingam SS, Vansteenkiste J, Planchard D, Cho BC, Gray JE, Ohe Y, et al. Overall survival with osimertinib in untreated, EGFR‐mutated advanced NSCLC. N Engl J Med 2020;382(1):41‐50. https://doi.org/10.1056/NEJMoa1913662
Dingemans AC, Hendriks LEL, Berghmans T, Levy A, Hasan B, Faivre‐Finn C, et al. Definition of synchronous oligometastatic non‐small cell lung cancer – a consensus report. J Thorac Oncol. 2019;14(12):2109–19. https://doi.org/10.1016/j.jtho.2019.07.025
Barton MK. Local consolidative therapy may be beneficial in patients with oligometastatic non‐small cell lung cancer. CA: Cancer J Clin. 2017;67(2):89–90. https://doi.org/10.3322/caac.21363
Weichselbaum RR, Hellman S. Oligometastases revisited. Nat Rev Clin Oncol. 2011;8(6):378–82. https://doi.org/10.1038/nrclinonc.2011.44
Arrieta O, Barron F, Maldonado F, Cabrera L, Corona‐Cruz JF, Blake M, et al. Radical consolidative treatment provides a clinical benefit and long‐term survival in patients with synchronous oligometastatic non‐small cell lung cancer: a phase Ⅱ study. Lung Cancer. 2019;130:67–75. https://doi.org/10.1016/j.lungcan.2019.02.006
Tang C, Lee WC, Reuben A, Chang L, Tran H, Little L, et al. Immune and circulating tumor DNA profiling after radiation treatment for oligometastatic non‐small cell lung cancer: translational correlatives from a mature randomized phase Ⅱ trial. Int J Radiat Oncol Biol Phys. 2020;106(2):349–57. https://doi.org/10.1016/j.ijrobp.2019.10.038
Hellmann MD, Nabet BY, Rizvi H, Chaudhuri AA, Wells DK, Dunphy MPS, et al. Circulating tumor DNA analysis to assess risk of progression after long‐term response to PD‐(L)1 blockade in NSCLC. Clin Cancer Res. 2020;26(12):2849–58. https://doi.org/10.1158/1078-0432.CCR-19-3418
This work was supported by the Guangdong Provincial People's Hospital Young Talent Project (Grant No. GDPPHYTP201902 to Wen‐Zhao Zhong). The funding sources had no role in the preparation of this manuscript.
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