First-site-metastasis pattern in patients with inoperable stage III NSCLC treated with concurrent chemoradiotherapy with or without immune check-point inhibition: a retrospective analysis.

Immune Checkpoint Inhibition Lung Cancer Metastasis Outcome Thoracic Radiotherapy

Journal

Strahlentherapie und Onkologie : Organ der Deutschen Rontgengesellschaft ... [et al]
ISSN: 1439-099X
Titre abrégé: Strahlenther Onkol
Pays: Germany
ID NLM: 8603469

Informations de publication

Date de publication:
17 Nov 2023
Historique:
received: 11 05 2023
accepted: 22 10 2023
medline: 17 11 2023
pubmed: 17 11 2023
entrez: 17 11 2023
Statut: aheadofprint

Résumé

The aim of this study was to investigate a first-site-metastasis pattern (FSMP) in unresectable stage III NSCLC after concurrent chemoradiotherapy (cCRT) with or without immune checkpoint inhibition (ICI). We defined three patient subgroups according to the year of initial multimodal treatment: A (2011-2014), B (2015-2017) and C (2018-2020). Different treatment-related parameters were analyzed. Observed outcome parameters were brain metastasis-free survival (BMFS), extracranial distant metastasis-free survival (ecDMFS) and distant metastasis-free survival (DMFS). 136 patients treated between 2011 and 2020 were included with ≥ 60.0 Gy total dose and concurrent chemotherapy (cCRT); thirty-six (26%) received ICI. Median follow-up was 49.7 (range:0.7-126.1), median OS 31.2 (95% CI:16.4-30.3) months (23.4 for non-ICI vs not reached for ICI patients, p = 0.001). Median BMFS/ecDMFS/DMFS in subgroups A, B and C was 14.9/16.3/14.7 months, 20.6/12.9/12.7 months and not reached (NR)/NR/36.4 months (p = 0.004/0.001/0.016). For cCRT+ICI median BMFS was 53.1 vs. 19.1 months for cCRT alone (p = 0.005). Median ecDMFS achieved 55.2 vs. 17.9 (p = 0.003) and median DMFS 29.5 (95% CI: 1.4-57.6) vs 14.93 (95% CI:10.8-19.0) months (p = 0.031), respectively. Multivariate analysis showed that age over 65 (HR:1.629; p = 0.036), GTV ≥ 78 cc (HR: 2.100; p = 0.002) and V20 ≥ 30 (HR: 2.400; p = 0.002) were negative prognosticators for BMFS and GTV ≥ 78 cc for ecDMFS (HR: 1.739; p = 0.027). After onset of brain metastasis (BM), patients survived 13.3 (95% CI: 6.4-20.2) months and 8.6 months (95% CI: 1.6-15.5) after extracranial-distant-metastasis (ecDM). Patients with ecDM as FSMP reached significantly worse overall survival of 22.1 (range:14.4-29.8) vs. 40.1 (range:18.7-61.3) months (p = 0.034) in the rest of cohort. In contrast, BM as FSMP had no impact on OS. This retrospective analysis of inoperable stage III NSCLC patients revealed that age over 65, V20 ≥ 30 and GTV ≥ 78 cc were prognosticators for BMFS and GTV ≥ 78 cc for ecDMFS. ICI treatment led to a significant improvement of BMFS, ecDMFS and DMFS. ecDM as FSMP was associated with significant deterioration of OS, whereas BM as FSMP was not.

Identifiants

pubmed: 37975883
doi: 10.1007/s00066-023-02175-6
pii: 10.1007/s00066-023-02175-6
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2023. The Author(s).

Références

Siegel RL, Miller KD, Fuchs HE et al (2021) Statistics, 2021. CA: a cancer journal for clinicians. Cancer 71(1):7–33. https://doi.org/10.3322/caac.21654
doi: 10.3322/caac.21654
Käsmann L, Taugner J, Eze C et al (2019) Performance Status and Its Changes Predict Outcome for Patients With Inoperable Stage III NSCLC Undergoing Multimodal Treatment. Anticancer Res 39(9):5077–5081. https://doi.org/10.21873/anticanres.13701
doi: 10.21873/anticanres.13701 pubmed: 31519618
Taugner J, Käsmann L, Eze C et al (2019) Survival score to characterize prognosis in inoperable stage III NSCLC after chemoradiotherapy. Transl Lung Cancer Res 8(5):593–604. https://doi.org/10.21037/tlcr.2019.09.19
doi: 10.21037/tlcr.2019.09.19 pubmed: 31737496 pmcid: 6835102
Taugner J, Eze C, Käsmann L et al (2020) Pattern-of-failure and salvage treatment analysis after chemoradiotherapy for inoperable stage III non-small cell lung cancer. Radiat Oncol 15(1):148. https://doi.org/10.1186/s13014-020-01590-8
doi: 10.1186/s13014-020-01590-8 pubmed: 32517716 pmcid: 7285541
(1995) Chemotherapy in non-small cell lung cancer: a meta-analysis using updated data on individual patients from 52 randomised clinical trials. Non-small Cell Lung Cancer Collaborative Group. BMJ : British Medical Journal 311(7010): 899–909
Remon J, Soria J‑C, Peters S (2021) Early and locally advanced non-small-cell lung cancer: an update of the ESMO Clinical Practice Guidelines focusing on diagnosis, staging, systemic and local therapy. Annals of oncology : official journal of the European Society for Medical Oncology 32(12): 1637–1642. https://doi.org/10.1016/j.annonc.2021.08.1994
Antonia SJ, Villegas A, Daniel D et al (2017) Durvalumab after Chemoradiotherapy in Stage III Non-Small-Cell Lung Cancer. N Engl J Med 377(20):1919–1929. https://doi.org/10.1056/NEJMoa1709937
doi: 10.1056/NEJMoa1709937 pubmed: 28885881
Spigel DR, Faivre-Finn C, Gray JE et al (2022) Five-Year Survival Outcomes From the PACIFIC Trial: Durvalumab After Chemoradiotherapy in Stage III Non-Small-Cell Lung Cancer. J Clin Oncol 40(12):1301–1311. https://doi.org/10.1200/JCO.21.01308
doi: 10.1200/JCO.21.01308 pubmed: 35108059 pmcid: 9015199
Rosset M, Reifegerste D, Baumann E et al. (2019) Langzeittrends beim Krebsinformationsdienst (KID) des Deutschen Krebsforschungszentrums (DKFZ) : Eine Analyse der Anfragen von Patientinnen und Patienten sowie Angehörigen von 1992 bis 2016 (Trends in cancer information services over 25 years : An analysis of inquiries from patients and relatives made to the Cancer Information Service of the German Cancer Research Center from 1992to 2016). Bundesgesundheitsblatt, Gesundheitsforschung, Gesundheitsschutz 62(9): 1120–1128. https://doi.org/10.1007/s00103-019-02996-w
Li W, Jiang J, Huang L et al (2022) Efficacy of PD-1/L1 inhibitors in brain metastases of non-small-cell lung cancer: pooled analysis from seven randomized controlled trials. Future Oncol 18(3):403–412. https://doi.org/10.2217/fon-2021-0795
doi: 10.2217/fon-2021-0795 pubmed: 34787500
Peters S, Felip E, Dafni U et al (2019) Safety evaluation of nivolumab added concurrently to radiotherapy in a standard first line chemo-radiotherapy regimen in stage III non-small cell lung cancer-The ETOP NICOLAS trial. Lung Cancer 133:83–87. https://doi.org/10.1016/j.lungcan.2019.05.001
doi: 10.1016/j.lungcan.2019.05.001 pubmed: 31200833
Peters S, Felip E, Dafni U et al (2021) Progression-Free and Overall Survival for Concurrent Nivolumab With Standard Concurrent Chemoradiotherapy in Locally Advanced Stage IIIA‑B NSCLC: Results From the European Thoracic Oncology Platform NICOLAS Phase II Trial (European Thoracic Oncology Platform 6–14). J Thorac Oncol 16(2):278–288. https://doi.org/10.1016/j.jtho.2020.10.129
doi: 10.1016/j.jtho.2020.10.129 pubmed: 33188912
Eze C, Schmidt-Hegemann N‑S, Sawicki LM et al (2021) PET/CT imaging for evaluation of multimodal treatment efficacy and toxicity in advanced NSCLC-current state and future directions. Eur J Nucl Med Mol Imaging 48(12):3975–3989. https://doi.org/10.1007/s00259-021-05211-8
doi: 10.1007/s00259-021-05211-8 pubmed: 33760957 pmcid: 8484219
Manapov F, Eze C, Holzgreve A et al (2022) PET/CT for Target Delineation of Lung Cancer Before Radiation Therapy. Semin Nucl Med 52(6):673–680. https://doi.org/10.1053/j.semnuclmed.2022.05.003
doi: 10.1053/j.semnuclmed.2022.05.003 pubmed: 35781392
Nestle U, de Ruysscher D, Ricardi U et al (2018) ESTRO ACROP guidelines for target volume definition in the treatment of locally advanced non-small cell lung cancer. Radiother Oncol 127(1):1–5. https://doi.org/10.1016/j.radonc.2018.02.023
doi: 10.1016/j.radonc.2018.02.023 pubmed: 29605476
Wiersma TG, Dahele M, Verbakel WFAR et al (2013) Concurrent chemoradiotherapy for large-volume locally-advanced non-small cell lung cancer. Lung Cancer 80(1):62–67. https://doi.org/10.1016/j.lungcan.2013.01.006
doi: 10.1016/j.lungcan.2013.01.006 pubmed: 23357464
van Reij EJF, Dahele M, van de Ven PM et al (2014) Changes in non-surgical management of stage III non-small cell lung cancer at a single institution between 2003 and 2010. Acta Oncol 53(3):316–323. https://doi.org/10.3109/0284186X.2013.819995
doi: 10.3109/0284186X.2013.819995 pubmed: 23957648
Taugner J, Käsmann L, Karin M et al (2022) Planning target volume as a predictor of disease progression in inoperable stage III non-small cell lung cancer patients treated with chemoradiotherapy and concurrent and/or sequential immune checkpoint inhibition. Invest New Drugs 40(1):163–171. https://doi.org/10.1007/s10637-021-01143-0
doi: 10.1007/s10637-021-01143-0 pubmed: 34351518
Karin M, Taugner J, Käsmann L et al (2020) Association of Planning Target Volume with Patient Outcome in Inoperable Stage III NSCLC Treated with Chemoradiotherapy: A Comprehensive Single-Center Analysis. Cancers. https://doi.org/10.3390/cancers12103035
doi: 10.3390/cancers12103035 pubmed: 33086481 pmcid: 7603086
Dubaere E, Goffaux M, Wanet M et al (2019) Long term outcome after 48 Gy stereotactic ablative body radiotherapy for peripheral stage I non-small cell lung cancer. Bmc Cancer 19(1):639. https://doi.org/10.1186/s12885-019-5863-2
doi: 10.1186/s12885-019-5863-2 pubmed: 31253136 pmcid: 6599378
Peng J, Pond G, Donovan E et al (2020) A Comparison of Radiation Techniques in Patients Treated With Concurrent Chemoradiation for Stage III Non-Small Cell Lung Cancer. Int J Radiat Oncol Biol Phys 106(5):985–992. https://doi.org/10.1016/j.ijrobp.2019.12.027
doi: 10.1016/j.ijrobp.2019.12.027 pubmed: 32007366
Merrow CE, Wang IZ, Podgorsak MB (2012) A dosimetric evaluation of VMAT for the treatment of non-small cell lung cancer. J Applied Clin Med Phys 14(1):4110. https://doi.org/10.1120/jacmp.v14i1.4110
doi: 10.1120/jacmp.v14i1.4110
Flentje M, Huber RM, Engel-Riedel W et al. (2016) GILT—A randomised phase III study of oral vinorelbine and cisplatin with concomitant radiotherapy followed by either consolidation therapy with oral vinorelbine and cisplatin or best supportive care alone in stage III non-small cell lung cancer. Strahlentherapie und Onkologie : Organ der Deutschen Rontgengesellschaft … [et al] 192(4): 216–222. https://doi.org/10.1007/s00066-016-0941-8
Gray JE, Villegas A, Daniel D et al (2020) Three-Year Overall Survival with Durvalumab after Chemoradiotherapy in Stage III NSCLC-Update from PACIFIC. J Thorac Oncol 15(2):288–293. https://doi.org/10.1016/j.jtho.2019.10.002
doi: 10.1016/j.jtho.2019.10.002 pubmed: 31622733
Antonia SJ, Villegas A, Daniel D et al (2018) Overall Survival with Durvalumab after Chemoradiotherapy in Stage III NSCLC. N Engl J Med 379(24):2342–2350. https://doi.org/10.1056/NEJMoa1809697
doi: 10.1056/NEJMoa1809697 pubmed: 30280658
Durm GA, Jabbour SK, Althouse SK et al (2020) A phase 2 trial of consolidation pembrolizumab following concurrent chemoradiation for patients with unresectable stage III non-small cell lung cancer: Hoosier Cancer Research Network LUN 14-179. Cancer 126(19): 4353–4361. https://doi.org/10.1002/cncr.33083
Kishi N, Matsuo Y, Shintani T et al (2023) Recurrence patterns and progression-free survival after chemoradiotherapy with or without consolidation durvalumab for stage III non-small cell lung cancer. JRR 64(1):142–153. https://doi.org/10.1093/jrr/rrac057
doi: 10.1093/jrr/rrac057
Offin M, Shaverdian N, Rimner A et al (2020) Clinical outcomes, local-regional control and the role for metastasis-directed therapies in stage III non-small cell lung cancers treated with chemoradiation and durvalumab. Radiother Oncol 149:205–211. https://doi.org/10.1016/j.radonc.2020.04.047
doi: 10.1016/j.radonc.2020.04.047 pubmed: 32361014 pmcid: 8239428
Jung HA, Noh JM, Sun J‑M et al (2020) Real world data of durvalumab consolidation after chemoradiotherapy in stage III non-small-cell lung cancer. Lung Cancer 146:23–29. https://doi.org/10.1016/j.lungcan.2020.05.035
doi: 10.1016/j.lungcan.2020.05.035 pubmed: 32505077
Käsmann L, Eze C, Taugner J et al (2020) Implementation of durvalumab maintenance treatment after concurrent chemoradiotherapy in inoperable stage III non-small cell lung cancer (NSCLC)—a German radiation oncology survey. Transl Lung Cancer Res 9(2):288–293. https://doi.org/10.21037/tlcr.2020.03.25
doi: 10.21037/tlcr.2020.03.25 pubmed: 32420068 pmcid: 7225149
Taugner J, Käsmann L, Eze C et al (2021) Real-world prospective analysis of treatment patterns in durvalumab maintenance after chemoradiotherapy in unresectable, locally advanced NSCLC patients. Invest New Drugs 39(4):1189–1196. https://doi.org/10.1007/s10637-021-01091-9
doi: 10.1007/s10637-021-01091-9 pubmed: 33704621 pmcid: 8280025
Taugner J, Käsmann L, Eze C et al (2021) Durvalumab after Chemoradiotherapy for PD-L1 Expressing Inoperable Stage III NSCLC Leads to Significant Improvement of Local-Regional Control and Overall Survival in the Real-World Setting. Cancers. https://doi.org/10.3390/cancers13071613
doi: 10.3390/cancers13071613 pubmed: 33807324 pmcid: 8037429
Flörsch B, Taugner J, Käsmann L et al (2022) Treatment patterns and prognosis of patients with inoperable stage III NSCLC after completion of concurrent chemoradiotherapy ± immune checkpoint inhibition: a decade-long single-center historical analysis. J Cancer Res Clin Oncol. https://doi.org/10.1007/s00432-022-04174-z
doi: 10.1007/s00432-022-04174-z pubmed: 35915184 pmcid: 10314870
Morgensztern D, Waqar S, Subramanian J et al (2012) Prognostic significance of tumor size in patients with stage III non-small-cell lung cancer: a surveillance, epidemiology, and end results (SEER) survey from 1998 to 2003. J Thorac Oncol 7(10):1479–1484. https://doi.org/10.1097/JTO.0b013e318267d032
doi: 10.1097/JTO.0b013e318267d032 pubmed: 22982648
Nagasaka M, Abdallah N, Crosby M et al. (2019) A retrospective study evaluating the pretreatment tumor volume (PTV) in non-small cell lung cancer (NSCLC) as a predictor of response to program death‑1 (PD-1) inhibitors. Lung Cancer: Targets and Therapy 10: 95–105. https://doi.org/10.2147/LCTT.S219886
Käsmann L, Niyazi M, Blanck O et al. (2018) Prädiktiver und prognostischer Wert des Tumorvolumens und seiner Veränderungen während radikaler Strahlentherapie beim nicht-kleinzelligen Bronchialkarzinom im Stadium III : Ein systematischer Review (Predictive and prognostic value of tumor volume and its changes during radical radiotherapy of stage III non-small cell lung cancer : A systematic review). Strahlentherapie und Onkologie : Organ der Deutschen Rontgengesellschaft … [et al] 194(2): 79–90. https://doi.org/10.1007/s00066-017-1221-y
Ostheimer C, Mäurer M, Ebert N et al. (2021) Prognostic impact of gross tumor volume during radical radiochemotherapy of locally advanced non-small cell lung cancer-results from the NCT03055715 multicenter cohort study of the Young DEGRO Trial Group. Strahlentherapie und Onkologie : Organ der Deutschen Rontgengesellschaft … [et al] 197(5): 385–395. https://doi.org/10.1007/s00066-020-01727-4
Garg S, Gielda BT, Kiel K et al (2014) Patterns of locoregional failure in stage III non-small cell lung cancer treated with definitive chemoradiation therapy. Pract Radiat Oncol 4(5):342–348. https://doi.org/10.1016/j.prro.2013.12.002
doi: 10.1016/j.prro.2013.12.002 pubmed: 25194104
Imai H, Kaira K, Minato K (2017) Clinical significance of post-progression survival in lung cancer. Thorac Cancer 8(5):379–386. https://doi.org/10.1111/1759-7714.12463
doi: 10.1111/1759-7714.12463 pubmed: 28627767 pmcid: 5582459
Ernani V, Stinchcombe TE (2019) Management of Brain Metastases in Non-Small-Cell Lung Cancer. JOP 15(11):563–570. https://doi.org/10.1200/JOP.19.00357
doi: 10.1200/JOP.19.00357 pubmed: 31715122 pmcid: 7098835
Delasos L, Wei W, Hassan KA et al (2023) Clinical outcomes with pembrolizumab-based therapies in recurrent/refractory NSCLC after chemoradiation and consolidative durvalumab. Clin Lung Cancer. https://doi.org/10.1016/j.cllc.2023.04.008
doi: 10.1016/j.cllc.2023.04.008 pubmed: 37188597

Auteurs

Kerstin Hofstetter (K)

Department of Radiation Oncology, University Hospital, LMU Munich, Munich, Germany.

Julian Taugner (J)

Department of Radiation Oncology, University Hospital, LMU Munich, Munich, Germany. Julian.Taugner@med.uni-muenchen.de.

Lukas Käsmann (L)

Department of Radiation Oncology, University Hospital, LMU Munich, Munich, Germany.
Comprehensive Pneumology Center Munich (CPC-M), Member of the German Center for Lung Research (DZL), Munich, Germany.
German Cancer Consortium (DKTK), Partner Site Munich, Munich, Germany.

Sina Mansoorian (S)

Department of Radiation Oncology, University Hospital, LMU Munich, Munich, Germany.

Benedikt Flörsch (B)

Department of Radiation Oncology, University Hospital, LMU Munich, Munich, Germany.

Chukwuka Eze (C)

Department of Radiation Oncology, University Hospital, LMU Munich, Munich, Germany.

Amanda Tufman (A)

Comprehensive Pneumology Center Munich (CPC-M), Member of the German Center for Lung Research (DZL), Munich, Germany.
Division of Respiratory Medicine and Thoracic Oncology, Department of Internal Medicine V, Thoracic Oncology Centre Munich, LMU Munich, Munich, Germany.

Niels Reinmuth (N)

Asklepios Kliniken GmbH, Asklepios Fachkliniken Muenchen, Gauting, Germany.

Thomas Duell (T)

Asklepios Kliniken GmbH, Asklepios Fachkliniken Muenchen, Gauting, Germany.

Claus Belka (C)

Department of Radiation Oncology, University Hospital, LMU Munich, Munich, Germany.
Comprehensive Pneumology Center Munich (CPC-M), Member of the German Center for Lung Research (DZL), Munich, Germany.
German Cancer Consortium (DKTK), Partner Site Munich, Munich, Germany.

Farkhad Manapov (F)

Department of Radiation Oncology, University Hospital, LMU Munich, Munich, Germany.
Comprehensive Pneumology Center Munich (CPC-M), Member of the German Center for Lung Research (DZL), Munich, Germany.
German Cancer Consortium (DKTK), Partner Site Munich, Munich, Germany.

Classifications MeSH