Oligometastatic non-small cell lung cancer: Impact of local and contemporary systemic treatment approaches on clinical outcome.
immunotherapy
locally ablative treatment
multimodal concepts
observational study
oligometastatic NSCLC
Journal
International journal of cancer
ISSN: 1097-0215
Titre abrégé: Int J Cancer
Pays: United States
ID NLM: 0042124
Informations de publication
Date de publication:
25 Sep 2024
25 Sep 2024
Historique:
revised:
01
07
2024
received:
15
04
2024
accepted:
07
08
2024
medline:
25
9
2024
pubmed:
25
9
2024
entrez:
25
9
2024
Statut:
aheadofprint
Résumé
Oligometastatic (OMD) non-small cell lung cancer (NSCLC) is a distinct but heterogeneous entity. Current guidelines recommend systemic therapy and consolidation with local ablative therapy (LAT). However, evidence regarding the optimal choice of multimodal treatment approaches is lacking, in particular with respect to the integration of immunotherapy. This real-world study identified 218 patients with OMD NSCLC (2004-2023, prespecified criteria: ≤5 metastases in ≤2 organ systems) from three major German comprehensive cancer centers. Most patients had one (72.5%) or two (17.4%) metastatic lesions in a single (89.9%) organ system. Overall survival (OS) was significantly longer with a single metastatic lesion (HR 0.54, p = .003), and female gender (HR 0.4, p < .001). Median OS of the full cohort was 27.8 months, with 29% survival at 5 years. Patients who had completed LAT to all NSCLC sites, typically excluding patients with early progression, had a median OS of 34.4 months (37.7% 5-year OS rate) with a median recurrence-free survival (RFS) of 10.9 months (13.3% at 5 years). In those patients, systemic treatment as part of first-line therapy was associated with doubling of RFS (12.3 vs. 6.4 months, p < .001). Despite limited follow-up of patients receiving chemo-immunotherapy (EU approval 2018/2019), RFS was greatly improved by adding checkpoint inhibitors to chemotherapy (HR 0.44, p = .008, 2-year RFS 51.4% vs. 15.1%). In conclusion, patients with OMD NSCLC benefitted from multimodality approaches integrating systemic therapy and local ablation of all cancer sites. A substantial proportion of patients achieved extended OS, suggesting a potential for cure that can be further augmented with the addition of immunotherapy.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2024 The Author(s). International Journal of Cancer published by John Wiley & Sons Ltd on behalf of UICC.
Références
Guckenberger M, Lievens Y, Bouma AB, 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:e18‐e28.
Giaj‐Levra N, Giaj‐Levra M, Durieux V, et al. Defining synchronous oligometastatic non‐small cell lung cancer: a systematic review. J Thorac Oncol. 2019;14:2053‐2061.
Chang JY, Verma V. Optimize local therapy for oligometastatic and oligoprogressive non‐small cell lung cancer to enhance survival. J Natl Compr Canc Netw. 2022;20:531‐539.
Dingemans A‐MC, Hendriks LEL, Berghmans T, et al. Definition of synchronous oligometastatic non‐small cell lung cancer—a consensus report. J Thorac Oncol. 2019;14:2109‐2119.
Iyengar P, All S, Berry MF, et al. Treatment of oligometastatic non‐small cell lung cancer: an ASTRO/ESTRO clinical practice guideline. Pract Radiat Oncol. 2023;13:393‐412.
Hendriks LE, Kerr KM, Menis J, et al. Non‐oncogene‐addicted metastatic non‐small‐cell lung cancer: ESMO clinical practice guideline for diagnosis, treatment and follow‐up. Ann Oncol. 2023;34:358‐376.
Sheu T, Heymach JV, Swisher SG, et al. Propensity score‐matched analysis of comprehensive local therapy for oligometastatic non‐small cell lung cancer that did not progress after front‐line chemotherapy. Int J Radiat Oncol Biol Phys. 2014;90:850‐857.
He J, Li Y, An J, Hu L, Zhang J. Surgical treatment in non‐small cell lung cancer with pulmonary oligometastasis. World J Surg Oncol. 2017;15:36.
Frost N, Tessmer A, Schmittel A, et al. Local ablative treatment for synchronous single organ oligometastatic lung cancer—a propensity score analysis of 180 patients. Lung Cancer. 2018;125:164‐173.
Chen X, Hou X, Li D, et al. Management of non‐small‐cell lung cancer patients initially diagnosed with 1 to 3 synchronous brain‐only metastases: a retrospective study. Clin Lung Cancer. 2021;22:e25‐e34.
Mitchell KG, Farooqi A, Ludmir EB, et al. Improved overall survival with comprehensive local consolidative therapy in synchronous oligometastatic non‐small‐cell lung cancer. Clin Lung Cancer. 2020;21:37‐46.e7.
Mitchell KG, Farooqi A, Ludmir EB, et al. Pulmonary resection is associated with long‐term survival and should remain a therapeutic option in oligometastatic lung cancer. J Thorac Cardiovasc Surg. 2021;161:1497‐1504.e2.
Gray PJ, Mak RH, Yeap BY, et al. Aggressive therapy for patients with non‐small cell lung carcinoma and synchronous brain‐only oligometastatic disease is associated with long‐term survival. Lung Cancer. 2014;85:239‐244.
Li H, Duan Z, Zhao C, et al. Combination of brachytherapy with Iodine‐125 seeds and systemic chemotherapy versus systemic chemotherapy alone for synchronous extracranial oligometastatic non‐small cell lung cancer. Cancer Manag Res. 2020;12:8209‐8220.
Song Y‐Q, Wang N, Qiao Y, et al. Treatment patterns and survival after 18F‐fluorodeoxyglucose positron emission tomography/computed tomography‐guided local consolidation therapy for oligometastatic non‐small cell lung cancer: a two‐center propensity score‐matched analysis. J Cancer Res Clin Oncol. 2020;146:1021‐1031.
Gomez DR, Tang C, Zhang J, 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;37:1558‐1565.
Iyengar P, Wardak Z, Gerber DE, et al. Consolidative radiotherapy for limited metastatic non‐small‐cell lung cancer: a phase 2 randomized clinical trial. JAMA Oncol. 2018;4:e173501.
Tsai CJ, Yang JT, Shaverdian N, et al. Standard‐of‐care systemic therapy with or without stereotactic body radiotherapy in patients with oligoprogressive breast cancer or non‐small‐cell lung cancer (consolidative use of radiotherapy to block [CURB] oligoprogression): an open‐label, randomised, controlled, phase 2 study. Lancet. 2024;403:171‐182.
Palma DA, Olson R, Harrow S, et al. Stereotactic ablative radiotherapy for the comprehensive treatment of oligometastatic cancers: long‐term results of the SABR‐COMET phase II randomized trial. JCO. 2020;38:2830‐2838.
Wang X‐S, Bai Y‐F, Verma V, et al. Randomized trial of first‐line tyrosine kinase inhibitor with or without radiotherapy for synchronous oligometastatic EGFR‐mutated non‐small cell lung cancer. J Natl Cancer Inst. 2023;115:742‐748.
Garassino MC, Gadgeel S, Speranza G, et al. Pembrolizumab plus pemetrexed and platinum in nonsquamous non‐small‐cell lung cancer: 5‐year outcomes from the phase 3 KEYNOTE‐189 study. JCO. 2023;41:1992‐1998.
Novello S, Kowalski DM, Luft A, et al. Pembrolizumab plus chemotherapy in squamous non‐small‐cell lung cancer: 5‐year update of the phase III KEYNOTE‐407 study. JCO. 2023;41:1999‐2006.
Bauml JM, Mick R, Ciunci C, et al. Pembrolizumab after completion of locally ablative therapy for oligometastatic non‐small cell lung cancer: a phase 2 trial. JAMA Oncol. 2019;5:1283‐1290.
Boch T, Frost N, Sommer L, et al. Pathologic responses in oligometastatic NSCLC patients treated with neoadjuvant immune checkpoint blockade with and without chemotherapy followed by surgery. Lung Cancer. 2022;164:46‐51.
Faehling M, Witte H, Sebastian M, et al. Real‐world multicentre analysis of neoadjuvant immunotherapy and chemotherapy in localized or oligometastatic non‐small cell lung cancer (KOMPASSneoOP). Ther Adv Med Oncol. 2022;14:17588359221085333.
Forde PM, Spicer J, Lu S, et al. Neoadjuvant nivolumab plus chemotherapy in resectable lung cancer. N Engl J Med [Internet]. 2022;386:1973‐1985. doi:10.1056/NEJMoa2202170
Wakelee H, Liberman M, Kato T, et al. Perioperative pembrolizumab for early‐stage non‐small‐cell lung cancer. N Engl J Med. 2023;389:491‐503.
Heymach JV, Harpole D, Mitsudomi T, et al. Perioperative durvalumab for resectable non‐small‐cell lung cancer. N Engl J Med. 2023;389:1672‐1684.
Chen Y, Wang Y, Yang Z, et al. Local consolidative therapy for synchronous oligometastatic non‐small cell lung cancer treated with first‐line pembrolizumab: a retrospective observational study. Thoracic Cancer. 2022;13:732‐741.
Jongbloed M, Bartolomeo V, Steens M, et al. Treatment outcome of patients with synchronous oligometastatic non‐small cell lung cancer in the immunotherapy era: analysis of a real‐life intention‐to‐treat population. Eur J Cancer [Internet]. 2023;190:112947. Accessed October 26, 2023. https://www.ejcancer.com/article/S0959-8049(23)00299-X/fulltext
Iyengar P, Hu C, Gomez DR, et al. NRG‐LU002: randomized phase II/III trial of maintenance systemic therapy versus local consolidative therapy (LCT) plus maintenance systemic therapy for limited metastatic non‐small cell lung cancer (NSCLC). JCO. 2024;42:8506.
Videtic GMM. Local treatments of oligometastatic and oligoprogressive NSCLC should become the standard of care. J Thorac Oncol. 2023;18:986‐989.
Macbeth F, Treasure T. Local treatments of oligometastatic and oligoprogressive NSCLC should not become the standard of care. J Thorac Oncol. 2023;18:981‐985.
R Core Team. R: A Language and Environment for Statistical Computing [Internet]. R Foundation for Statistical Computing; 2016. Accessed on September 05, 2024. https://www.R-project.org/
Wickham H, Averick M, Bryan J, et al. Welcome to the tidyverse. JOSS. 2019;4:1686.
Wickham H. ggplot2: Elegant Graphics for Data Analysis [Internet]. Springer‐Verlag; 2016. Accessed on September 05, 2024. http://ggplot2.org
Therneau TM. A Package for Survival Analysis in S [Internet]. Springer. 2015. Accessed on September 05, 2024. https://CRAN.R-project.org/package=survival
Kassambara A, Kosinski M. Survminer: Drawing Survival Curves Using “ggplot2” [Internet]. 2017. Accessed September 05, 2024. http://www.sthda.com/english/rpkgs/survminer/
Xu S, Ross C, Raebel MA, Shetterly S, Blanchette C, Smith D. Use of stabilized inverse propensity scores as weights to directly estimate relative risk and its confidence intervals. Value Health. 2010;13:273‐277.
Xie J, Liu C. Adjusted Kaplan–Meier estimator and log‐rank test with inverse probability of treatment weighting for survival data. Statist Med. 2005;24:3089‐3110.
Denz R, Klaaßen‐Mielke R, Timmesfeld N. A comparison of different methods to adjust survival curves for confounders. Stat Med. 2023;42:1461‐1479.
Pepe MS, Fleming TR. Weighted Kaplan–Meier statistics: a class of distance tests for censored survival data. Biometrics. 1989;45:497‐507.
Metzenmacher M, Griesinger F, Hummel H‐D, et al. Prognostic factors in non‐small‐cell lung cancer: insights from the German crisp registry. Eur Respir J [Internet]. 2022;61:2201336. Accessed April 17, 2023. https://erj.ersjournals.com/content/early/2022/09/14/13993003.01336-2022
Ashworth AB, Senan S, Palma DA, et al. An individual patient data metaanalysis of outcomes and prognostic factors after treatment of oligometastatic non‐small‐cell lung cancer. Clin Lung Cancer. 2014;15:346‐355.
Li S, Zhu R, Li D, Li N, Zhu X. Prognostic factors of oligometastatic non‐small cell lung cancer: a meta‐analysis. J Thorac Dis. 2018;10:3701‐3713.
Spaggiari L, Bertolaccini L, Facciolo F, et al. A risk stratification scheme for synchronous oligometastatic non‐small cell lung cancer developed by a multicentre analysis. Lung Cancer. 2021;154:29‐35.
Ye Y, Jing Y, Li L, et al. Sex‐associated molecular differences for cancer immunotherapy. Nat Commun. 2020;11:1779.
Pala L, Pas TD, Catania C, et al. Sex and cancer immunotherapy: current understanding and challenges. Cancer Cell. 2022;40:695‐700.
Conforti F, Pala L, Bagnardi V, et al. Sex‐based heterogeneity in response to lung cancer immunotherapy: a systematic review and meta‐analysis. J Natl Cancer Inst. 2019;111:772‐781.
Rheinheimer S, Heussel C‐P, Mayer P, et al. Oligoprogressive non‐small‐cell lung cancer under treatment with PD‐(L)1 inhibitors. Cancers (Basel). 2020;12:1046.