Is it advisable to perform radiosurgery for EGFR-TKI-controlled brain metastases? A retrospective study of the role of radiosurgery in lung cancer treatment.

Brain metastases Epidermal growth factor receptor Gamma-knife Non-small cell lung cancer Stereotactic radiosurgery Tyrosine-kinase inhibitor

Journal

Journal of neuro-oncology
ISSN: 1573-7373
Titre abrégé: J Neurooncol
Pays: United States
ID NLM: 8309335

Informations de publication

Date de publication:
Sep 2023
Historique:
received: 24 07 2023
accepted: 15 08 2023
medline: 23 10 2023
pubmed: 1 9 2023
entrez: 1 9 2023
Statut: ppublish

Résumé

Given the availability of TKIs with high central nervous system efficacy, the question arises as to whether upfront SRS provides additional clinical benefits. The goal of this study was to characterize the clinical outcomes of SRS as salvage therapy for TKI-uncontrolled BMs. This retrospective study included EGFR-mutant NSCLC patients presenting BMs at the time of primary tumor diagnosis. BMs were categorized into three subgroups, referred to as "Nature of TKI-treated BMs", "TKI-controlled brain metastases ± SRS", and "SRS salvage therapy". The first subgroup analysis characterized the effects of TKIs on tumor behavior. In the second subgroup, we compared outcomes of TKI-controlled BMs treated with TKI alone versus those treated with combined TKI-SRS therapy. The third subgroup characterized the outcomes of TKI-uncontrolled BMs treated with SRS as salvage therapy Clinical outcomes include local and distant tumor control. This study included 106 patients with a total of 683 BMs. TKI treatment achieved control in 63% of local tumors at 24 months. Among the TKI-controlled BMs, local tumor control was significantly higher in the combined TKI-SRS group (93%) than in the TKI-alone group (65%) at 24 months (p < 0.001). No differences were observed between the two groups in terms of distant tumor control (p = 0.832). In dealing with TKI-uncontrolled BMs, salvage SRS achieved local tumor control in 58% of BMs at 24 months. While upfront TKI alone proved highly effective in BM control, this study also demonstrated the outcomes of SRS when implemented concurrently with TKI or as salvage therapy for TKI-uncontrolled BMs. This study also presents a strategy of the precise timing and targeting of SRS to lesions in progression.

Identifiants

pubmed: 37656378
doi: 10.1007/s11060-023-04425-0
pii: 10.1007/s11060-023-04425-0
doi:

Substances chimiques

ErbB Receptors EC 2.7.10.1
EGFR protein, human EC 2.7.10.1

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

413-422

Informations de copyright

© 2023. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.

Références

Aoyama H, Shirato H, Tago M, Nakagawa K, Toyoda T, Hatano K, Kenjyo M, Oya N, Hirota S, Shioura H, Kunieda E, Inomata T, Hayakawa K, Katoh N, Kobashi G (2006) Stereotactic radiosurgery plus whole-brain radiation therapy vs stereotactic radiosurgery alone for treatment of brain metastases: a randomized controlled trial. JAMA 295:2483–2491. https://doi.org/10.1001/jama.295.21.2483
doi: 10.1001/jama.295.21.2483 pubmed: 16757720
Chang EL, Wefel JS, Hess KR, Allen PK, Lang FF, Kornguth DG, Arbuckle RB, Swint JM, Shiu AS, Maor MH, Meyers CA (2009) Neurocognition in patients with brain metastases treated with radiosurgery or radiosurgery plus whole-brain irradiation: a randomised controlled trial. Lancet Oncol 10:1037–1044. https://doi.org/10.1016/S1470-2045(09)70263-3
doi: 10.1016/S1470-2045(09)70263-3 pubmed: 19801201
Brown PD, Jaeckle K, Ballman KV, Farace E, Cerhan JH, Anderson SK, Carrero XW, Barker FG 2nd, Deming R, Burri SH, Menard C, Chung C, Stieber VW, Pollock BE, Galanis E, Buckner JC, Asher AL (2016) Effect of Radiosurgery alone vs Radiosurgery with Whole Brain Radiation Therapy on cognitive function in patients with 1 to 3 brain metastases: a Randomized Clinical Trial. JAMA 316:401–409. https://doi.org/10.1001/jama.2016.9839
Yamamoto M, Serizawa T, Shuto T, Akabane A, Higuchi Y, Kawagishi J, Yamanaka K, Sato Y, Jokura H, Yomo S, Nagano O, Kenai H, Moriki A, Suzuki S, Kida Y, Iwai Y, Hayashi M, Onishi H, Gondo M, Sato M, Akimitsu T, Kubo K, Kikuchi Y, Shibasaki T, Goto T, Takanashi M, Mori Y, Takakura K, Saeki N, Kunieda E, Aoyama H, Momoshima S, Tsuchiya K (2014) Stereotactic radiosurgery for patients with multiple brain metastases (JLGK0901): a multi-institutional prospective observational study. Lancet Oncol 15:387–395. https://doi.org/10.1016/S1470-2045(14)70061-0
doi: 10.1016/S1470-2045(14)70061-0 pubmed: 24621620
Chiou GY, Chiang CL, Yang HC, Shen CI, Wu HM, Chen YW, Chen CJ, Luo YH, Hu YS, Lin CJ, Chung WY, Shiau CY, Guo WY, Pan DH, Lee CC (2021) Combined stereotactic radiosurgery and tyrosine kinase inhibitor therapy versus tyrosine kinase inhibitor therapy alone for the treatment of non-small cell lung cancer patients with brain metastases. J Neurosurg 1–8. https://doi.org/10.3171/2021.9.JNS211373
Unger KR, Lominska CE, Chanyasulkit J, Randolph-Jackson P, White RL, Aulisi E, Jacobson J, Jean W, Gagnon GJ (2012) Risk factors for posttreatment edema in patients treated with stereotactic radiosurgery for meningiomas. Neurosurgery 70:639–645. https://doi.org/10.1227/NEU.0b013e3182351ae7
doi: 10.1227/NEU.0b013e3182351ae7 pubmed: 21904263
Loganadane G, Dhermain F, Louvel G, Kauv P, Deutsch E, Le Pechoux C, Levy A (2018) Brain Radiation Necrosis: current management with a focus on non-small cell Lung Cancer Patients. Front Oncol 8:336. https://doi.org/10.3389/fonc.2018.00336
doi: 10.3389/fonc.2018.00336 pubmed: 30234011 pmcid: 6134016
Miller JA, Bennett EE, Xiao R, Kotecha R, Chao ST, Vogelbaum MA, Barnett GH, Angelov L, Murphy ES, Yu JS, Ahluwalia MS, Suh JH, Mohammadi AM (2016) Association between Radiation Necrosis and Tumor Biology after Stereotactic Radiosurgery for Brain Metastasis. Int J Radiat Oncol Biol Phys 96:1060–1069. https://doi.org/10.1016/j.ijrobp.2016.08.039
doi: 10.1016/j.ijrobp.2016.08.039 pubmed: 27742540
Kang L, Mai J, Liang W, Zou Q, Huang C, Lin Y, Liang Y (2023) CNS efficacy of afatinib as first-line treatment in advanced non-small cell lung cancer patients with EGFR mutations. Front Oncol 13:1094195. https://doi.org/10.3389/fonc.2023.1094195
doi: 10.3389/fonc.2023.1094195 pubmed: 36910673 pmcid: 9996125
Zhao Y, Li S, Yang X, Chu L, Wang S, Tong T, Chu X, Yu F, Zeng Y, Guo T, Zhou Y, Zou L, Li Y, Ni J, Zhu Z (2022) Overall survival benefit of osimertinib and clinical value of upfront cranial local therapy in untreated EGFR-mutant nonsmall cell lung cancer with brain metastasis. Int J Cancer 150:1318–1328. https://doi.org/10.1002/ijc.33904
doi: 10.1002/ijc.33904 pubmed: 34914096
Yang JCH, Kim SW, Kim DW, Lee JS, Cho BC, Ahn JS, Lee DH, Kim TM, Goldman JW, Natale RB, Brown AP, Collins B, Chmielecki J, Vishwanathan K, Mendoza-Naranjo A, Ahn MJ (2020) Osimertinib in patients with epidermal growth factor receptor mutation-positive non-small-cell Lung Cancer and Leptomeningeal Metastases: the BLOOM Study. J Clin Oncol 38:538–547. https://doi.org/10.1200/JCO.19.00457
doi: 10.1200/JCO.19.00457 pubmed: 31809241
Park S, Lee MH, Seong M, Kim ST, Kang JH, Cho BC, Lee KH, Cho EK, Sun JM, Lee SH, Ahn JS, Park K, Ahn MJ (2020) A phase II, multicenter, two cohort study of 160 mg osimertinib in EGFR T790M-positive non-small-cell lung cancer patients with brain metastases or leptomeningeal disease who progressed on prior EGFR TKI therapy. Ann Oncol 31:1397–1404. https://doi.org/10.1016/j.annonc.2020.06.017
doi: 10.1016/j.annonc.2020.06.017 pubmed: 32634610
Reungwetwattana T, Nakagawa K, Cho BC, Cobo M, Cho EK, Bertolini A, Bohnet S, Zhou C, Lee KH, Nogami N, Okamoto I, Leighl N, Hodge R, McKeown A, Brown AP, Rukazenkov Y, Ramalingam SS, Vansteenkiste J (2018) CNS response to Osimertinib Versus standard epidermal growth factor receptor tyrosine kinase inhibitors in patients with untreated EGFR-Mutated Advanced Non-Small-Cell Lung Cancer. J Clin Oncol: JCO2018783118. https://doi.org/10.1200/JCO.2018.78.3118
doi: 10.1200/JCO.2018.78.3118
Patel PH, Palma D, McDonald F, Tree AC (2019) The Dandelion Dilemma Revisited for Oligoprogression: treat the whole lawn or weed selectively? Clin Oncol (R Coll Radiol) 31:824–833. https://doi.org/10.1016/j.clon.2019.05.015
doi: 10.1016/j.clon.2019.05.015 pubmed: 31182289
Langston J, Patil T, Ross Camidge D, Bunn PA, Schenk EL, Pacheco JM, Jurica J, Waxweiler TV, Kavanagh BD, Rusthoven CG (2023) CNS downstaging: an emerging treatment paradigm for extensive brain metastases in Oncogene-Addicted Lung Cancer. Lung Cancer 178:103–107. https://doi.org/10.1016/j.lungcan.2023.02.006
doi: 10.1016/j.lungcan.2023.02.006 pubmed: 36809719
Magnuson WJ, Lester-Coll NH, Wu AJ, Yang TJ, Lockney NA, Gerber NK, Beal K, Amini A, Patil T, Kavanagh BD, Camidge DR, Braunstein SE, Boreta LC, Balasubramanian SK, Ahluwalia MS, Rana NG, Attia A, Gettinger SN, Contessa JN, Yu JB, Chiang VL (2017) Management of brain metastases in tyrosine kinase inhibitor-naive epidermal growth factor receptor-mutant non-small-cell Lung Cancer: a retrospective multi-institutional analysis. J Clin Oncol 35:1070–1077. https://doi.org/10.1200/JCO.2016.69.7144
doi: 10.1200/JCO.2016.69.7144 pubmed: 28113019
Lee CC, Chou CL, Chen CJ, Yang HC, Wu HM, Shiau CY, Pan DH, Chung WY (2018) Stereotactic radiosurgery for hypervascular intracranial tumors. J Neurooncol 140:547–558. https://doi.org/10.1007/s11060-018-2980-8
doi: 10.1007/s11060-018-2980-8 pubmed: 30128688
Pai FY, Chen CJ, Wang WH, Yang HC, Lin CJ, Wu HM, Lin YC, Chen HS, Yen YS, Chung WY, Guo WY, Pan DH, Shiau CY, Lee CC (2019) Low-dose Gamma Knife Radiosurgery for Acromegaly. Neurosurgery 85:E20–E30. https://doi.org/10.1093/neuros/nyy410
doi: 10.1093/neuros/nyy410 pubmed: 30169716
Lee CC, Pan DH, Chung WY, Liu KD, Yang HC, Wu HM, Guo WY, Shih YH (2012) Brainstem cavernous malformations: the role of Gamma Knife surgery. J Neurosurg 117 Suppl:164–169. https://doi.org/10.3171/2012.8.GKS121066
doi: 10.3171/2012.8.GKS121066 pubmed: 23205805
Lee CC, Wintermark M, Xu Z, Yen CP, Schlesinger D, Sheehan JP (2014) Application of diffusion-weighted magnetic resonance imaging to predict the intracranial metastatic tumor response to gamma knife radiosurgery. J Neurooncol 118:351–361. https://doi.org/10.1007/s11060-014-1439-9
doi: 10.1007/s11060-014-1439-9 pubmed: 24760414
Lee CC, Yen CP, Xu Z, Schlesinger D, Sheehan J (2014) Large intracranial metastatic tumors treated by Gamma Knife surgery: outcomes and prognostic factors. J Neurosurg 120:52–59. https://doi.org/10.3171/2013.9.JNS131163
doi: 10.3171/2013.9.JNS131163 pubmed: 24160478
Shaw E, Scott C, Souhami L, Dinapoli R, Kline R, Loeffler J, Farnan N (2000) Single dose radiosurgical treatment of recurrent previously irradiated primary brain tumors and brain metastases: final report of RTOG protocol 90 – 05. Int J Radiat Oncol Biol Phys 47:291–298. https://doi.org/10.1016/s0360-3016(99)00507-6
doi: 10.1016/s0360-3016(99)00507-6 pubmed: 10802351
Lin YY, Guo WY, Lu CF, Peng SJ, Wu YT, Lee CC (2023) Application of artificial intelligence to stereotactic radiosurgery for intracranial lesions: detection, segmentation, and outcome prediction. J Neurooncol 161:441–450. https://doi.org/10.1007/s11060-022-04234-x
doi: 10.1007/s11060-022-04234-x pubmed: 36635582
Snell JW, Sheehan J, Stroila M, Steiner L (2006) Assessment of imaging studies used with radiosurgery: a volumetric algorithm and an estimation of its error. Technical note. J Neurosurg 104:157–162. https://doi.org/10.3171/jns.2006.104.1.157
doi: 10.3171/jns.2006.104.1.157 pubmed: 16509161
Peled N, Kian W, Inbar E, Goldstein IM, Zemel M, Rotem O, Rozenblum AB, Nechushtan H, Dudnik E, Levin D, Zer A, Keren-Rosenberg S, Yust-Katz S, Fuchs V, Remilah AA, Shelef I, Roisman LC (2022) Osimertinib in advanced EGFR-mutant lung adenocarcinoma with asymptomatic brain metastases: an open-label, 3-arm, phase II pilot study. Neurooncol Adv 4:vdab188. https://doi.org/10.1093/noajnl/vdab188
doi: 10.1093/noajnl/vdab188 pubmed: 35156036
Vogelbaum MA, Brown PD, Messersmith H, Brastianos PK, Burri S, Cahill D, Dunn IF, Gaspar LE, Gatson NTN, Gondi V, Jordan JT, Lassman AB, Maues J, Mohile N, Redjal N, Stevens G, Sulman E, van den Bent M, Wallace HJ, Weinberg JS, Zadeh G, Schiff D (2022) Treatment for Brain Metastases: ASCO-SNO-ASTRO Guideline. J Clin Oncol 40:492–516. https://doi.org/10.1200/JCO.21.02314
doi: 10.1200/JCO.21.02314 pubmed: 34932393
Yomo S, Oda K (2018) Impacts of EGFR-mutation status and EGFR-TKI on the efficacy of stereotactic radiosurgery for brain metastases from non-small cell lung adenocarcinoma: a retrospective analysis of 133 consecutive patients. Lung Cancer 119:120–126. https://doi.org/10.1016/j.lungcan.2018.03.013
doi: 10.1016/j.lungcan.2018.03.013 pubmed: 29656746
Dohm AE, Tang JD, Mills MN, Liveringhouse CL, Sandoval ML, Perez BA, Robinson TJ, Creelan BC, Gray JE, Etame AB, Vogelbaum MA, Forsyth P, Yu HM, Oliver DE, Ahmed KA (2022) Clinical outcomes of non-small cell lung cancer brain metastases treated with stereotactic radiosurgery and immune checkpoint inhibitors, EGFR tyrosine kinase inhibitors, chemotherapy and immune checkpoint inhibitors, or chemotherapy alone. J Neurosurg 1–8. https://doi.org/10.3171/2022.9.JNS221896
Shao J, Li J, Song L, He Q, Wu Y, Li L, Liu D, Wang C, Li W (2022) The number of brain metastases predicts the survival of non-small cell lung cancer patients with EGFR mutation status. Cancer Rep (Hoboken) 5:e1550. https://doi.org/10.1002/cnr2.1550
doi: 10.1002/cnr2.1550 pubmed: 34766737
Lin NU, Lee EQ, Aoyama H, Barani IJ, Barboriak DP, Baumert BG, Bendszus M, Brown PD, Camidge DR, Chang SM, Dancey J, de Vries EG, Gaspar LE, Harris GJ, Hodi FS, Kalkanis SN, Linskey ME, Macdonald DR, Margolin K, Mehta MP, Schiff D, Soffietti R, Suh JH, van den Bent MJ, Vogelbaum MA, Wen PY Response Assessment in Neuro-Oncology g (2015) response assessment criteria for brain metastases: proposal from the RANO group. Lancet Oncol 16: e270–278 https://doi.org/10.1016/S1470-2045(15)70057-4

Auteurs

Joseph Shang-En Hung (JS)

Department of Neurosurgery, Neurological Institute, Taipei Veterans General Hospital, Taipei, Taiwan.

Yan-Hua Su (YH)

Department of Neurosurgery, Neurological Institute, Taipei Veterans General Hospital, Taipei, Taiwan.

Ching-Jen Chen (CJ)

Department of Neurological Surgery, The University of Texas Health Science Center at Houston, Houston, TX, USA.

Chi-Lu Chiang (CL)

Department of Chest Medicine, Taipei Veterans General Hospital, Taipei, Taiwan.
School of Medicine, National Yang Ming Chiao Tung University, Taipei, Taiwan.
Institute of Clinical Medicine, School of Medicine, National Yang Ming Chiao Tung University, Taipei, Taiwan.

Chia-I Shen (CI)

Department of Chest Medicine, Taipei Veterans General Hospital, Taipei, Taiwan.
School of Medicine, National Yang Ming Chiao Tung University, Taipei, Taiwan.
Institute of Clinical Medicine, School of Medicine, National Yang Ming Chiao Tung University, Taipei, Taiwan.

Huai-Che Yang (HC)

Department of Neurosurgery, Neurological Institute, Taipei Veterans General Hospital, Taipei, Taiwan.
School of Medicine, National Yang Ming Chiao Tung University, Taipei, Taiwan.

Cheng-Ying Shiau (CY)

Institute of Clinical Medicine, School of Medicine, National Yang Ming Chiao Tung University, Taipei, Taiwan.
Cancer Center, Taipei Veterans General Hospital, Taipei, Taiwan.

Yung-Hung Luo (YH)

Department of Chest Medicine, Taipei Veterans General Hospital, Taipei, Taiwan.
School of Medicine, National Yang Ming Chiao Tung University, Taipei, Taiwan.
Institute of Clinical Medicine, School of Medicine, National Yang Ming Chiao Tung University, Taipei, Taiwan.

Hsiu-Mei Wu (HM)

School of Medicine, National Yang Ming Chiao Tung University, Taipei, Taiwan.
Department of Radiology, Taipei Veterans General Hospital, Taipei, Taiwan.

Yong-Sin Hu (YS)

School of Medicine, National Yang Ming Chiao Tung University, Taipei, Taiwan.
Department of Radiology, Taipei Veterans General Hospital, Taipei, Taiwan.

Chung-Jung Lin (CJ)

School of Medicine, National Yang Ming Chiao Tung University, Taipei, Taiwan.
Department of Radiology, Taipei Veterans General Hospital, Taipei, Taiwan.

Kang-Du Liu (KD)

Department of Neurosurgery, Neurological Institute, Taipei Veterans General Hospital, Taipei, Taiwan.
School of Medicine, National Yang Ming Chiao Tung University, Taipei, Taiwan.

Wen-Yuh Chung (WY)

Department of Neurosurgery, Neurological Institute, Taipei Veterans General Hospital, Taipei, Taiwan.
School of Medicine, National Yang Ming Chiao Tung University, Taipei, Taiwan.
Department of Neurosurgery, Shuang Ho Hospital, Taipei Medical University, Taipei, Taiwan.

Wan-Yuo Guo (WY)

School of Medicine, National Yang Ming Chiao Tung University, Taipei, Taiwan.
Department of Radiology, Taipei Veterans General Hospital, Taipei, Taiwan.

Cheng-Chia Lee (CC)

Department of Neurosurgery, Neurological Institute, Taipei Veterans General Hospital, Taipei, Taiwan. yfnaughty@gmail.com.
School of Medicine, National Yang Ming Chiao Tung University, Taipei, Taiwan. yfnaughty@gmail.com.
Brain Research Center, National Yang Ming Chiao Tung University, Taipei, Taiwan. yfnaughty@gmail.com.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH