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Timing of Development of Symptomatic Brain Metastases from Non-Small Cell Lung Cancer: Impact on Symptoms, Treatment, and Survival in the Era of Molecular Treatments

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Timing of Development of Symptomatic Brain Metastases from Non-Small Cell Lung Cancer: Impact on Symptoms, Treatment, and Survival in the Era of Molecular Treatments cancers Communication Timing of Development of Symptomatic Brain Metastases from Non-Small Cell Lung Cancer: Impact on Symptoms, Treatment, and Survival in the Era of Molecular Treatments 1,2, , 3,4, 2,5 2,5 Stephanie T. Jünger * y, Petra Schödel y, Daniel Ruess , Maximilian Ruge , Julia-Sarita Brand 5, Maike Wittersheim 6, Marie-Lisa Eich 6 , Nils-Ole Schmidt 3,4 , 1,2 1,2, 3,4, Roland Goldbrunner , Stefan Grau y and Martin Proescholdt y 1 Centre for Neurosurgery, Department of Neurosurgery, Faculty of Medicine and University Hospital, University of Cologne, 50931 Cologne, Germany; [email protected] (R.G.); [email protected] (S.G.) 2 Centre for Integrated Oncology, Faculty of Medicine and University Hospital, University of Cologne, 50931 Cologne, Germany; [email protected] (D.R.); [email protected] (M.R.) 3 Department of Neurosurgery, University Medical Centre Regensburg, 93053 Regensburg, Germany; [email protected] (P.S.); [email protected] (N.-O.S.); [email protected] (M.P.) 4 Wilhelm Sander Neuro-Oncology Unit, University Medical Centre Regensburg, 93053 Regensburg, Germany 5 Centre for Neurosurgery, Department of Stereotactic and Functional Neurosurgery, Faculty of Medicine and University Hospital, University of Cologne, 50931 Cologne, Germany; [email protected] 6 Department of Pathology, Faculty of Medicine and University Hospital, University of Cologne, 50931 Cologne, Germany; [email protected] (M.W.); [email protected] (M.-L.E.) * Correspondence: [email protected]; Tel.: +49-221-478-4550; Fax: +49-221-478-82825 Equal contribution. y Received: 4 November 2020; Accepted: 28 November 2020; Published: 3 December 2020 Simple Summary: In order to clarify whether an early development of brain metastases from non-small cell lung cancer represents a poor prognostic factor for further survival we analyzed 377 patients with brain metastases, treated by radiosurgery or surgery at two German institutions. Our results show that an early appearance of brain metastasis does not influence further survival in a comprehensive treatment setting. Abstract: Objective: We attempted to analyze whether early presentation with brain metastases (BM) represents a poor prognostic factor in patients with non-small cell lung cancer (NSCLC), which should guide the treatment team towards less intensified therapy. Patients and methods: In a retrospective bi-centric analysis, we identified patients receiving surgical treatment for NSCLC BM. We collected demographic-, tumor-, and treatment-related parameters and analyzed their influence on further survival. Results: We included 377 patients. Development of BM was precocious in 99 (26.3%), synchronous in 152 (40.3%), and metachronous in 126 (33.4%) patients. The groups were comparable in terms of age (p = 0.76) and number of metastases (p = 0.11), and histology (p = 0.1); however, mutational status significantly differed (p = 0.002). The precocious group showed the worst clinical status as assessed by Karnofsky performance score (KPS) upon presentation (p < 0.0001). Resection followed by postoperative radiotherapy was the predominant treatment modality for precocious BM, while in syn- and metachronous BM surgical and radio-surgical treatment was balanced. Overall survival (OS) did not differ between the groups (p = 0.76). A good postoperative clinical status (KPS 70) and the application of any kind of adjuvant systemic therapy were independent predictive ≥ factors for OS. Conclusion: Early BM presentation was not associated with worse OS in NSCLC BM patients. Cancers 2020, 12, 3618; doi:10.3390/cancers12123618 www.mdpi.com/journal/cancers Cancers 2020, 12, 3618 2 of 10 Keywords: brain metastasis; radiosurgery; neurosurgery; precocious; synchronous; metachronous; genetic mutations 1. Introduction Lung cancers represent the most frequent cancer type seeding to the brain [1,2]. While some patients may develop brain metastases (BM) during or after initial treatment for the primary tumors, others show early development of brain disease, sometimes even before the primary cancer is detected. In accordance, the pattern of appearance is termed synchronous (i.e., within three months of diagnosis) or metachronous (i.e., later than three months after diagnosis) and precocious (i.e., prior to diagnosis of the primary tumor) [3–5]. While precocious and most synchronous metastases are frequently treatment-naive compared to metachronous tumors, a different oncological course for these patients has been reported, with a rather dismal prognosis for patients with precocious tumors, possibly resulting in differing treatment decisions [6]. As (radio-)oncological treatment patterns have changed substantially over recent decades due to the substances available and frequency of treatment, and with postoperative treatment options advancing over the past two decades [7], the aim of this study was to evaluate the treatment course of patients with symptomatic brain metastases from non-small cell lung cancers (NSCLC) in relation to their time of appearance in the setting of comprehensive oncological treatment. 2. Results 2.1. Demographic and Baseline Clinical Data We identified 438 patients, who received treatment for brain metastases from lung cancer between 2010 and 2019. Sixty-one patients were excluded due to small cell histology, missing data, or postsurgical in-house mortality, leaving 377 patients in the analysis. Histology comprised adeno-carcinoma (n = 309; 82%), squamous cell carcinoma (n = 46; 12.2%), neuro-endocrine differentiation (n = 17; 4.5%), and not otherwise specified (n = 5; 1.3%) and was not statistically different with regard to BM timing (p = 0.10). The median age was 61 (range 25–87) years, of which 207 (54.9%) patients were male. Median timespan since initial tumor diagnosis was 1.8 (range 4–162) months, resulting in 99 (26.3%) precocious, − 152 (40.3%) synchronous, and 126 (33.4%) metachronous BM. Distribution of age (p = 0.76) and number of metastases (p = 0.11) were similar between these groups, while the pattern of driver mutations was different (p < 0.0001; Table1). Patients with precocious BM presented significantly more frequently with neurological symptoms (p < 0.0001) and had a worse clinical status than patients with synchronous and metachronous BM (p = 0.03). Detailed information regarding tumor location and symptoms is displayed in Table1. Cancers 2020, 12, 3618 3 of 10 Table 1. Demographics and baseline characteristics. Precocious Synchronous Metachronous All Parameter p-Value (n = 99) (n = 152) (n = 126) (n = 377) Age [median; range] 62 (38–87) 62 (32–85) 60 (25–83) 61 (25–87) 0.76 Male gender [n;%] 56 (56.6) 88 (57.9) 63 (50.0) 207 (54.9) 0.26 Controlled primary disease [n;(%)] 0 (0) 37 (24.3) 57 (45.2) 94 (24.9) <0.0001 Histology [n;%] Adeno 78 (78.8) 127 (83.5) 104 (82.5) 309 (82.0) Squamous cell 14 (14.1) 13 (8.6) 19 (15.1) 46 (12.2) 0.10 Neuro-endocrine 0 (0) 3 (2.0) 2 (1.6) 5 (1.3) NOS 7 (7.1) 9 (5.9) 1 (0.8) 17 (4.5) Previous treatment for primary disease none 99 (100) 16 (10.5) 4 (3.2) 119 Surgery 0 (0) 27 (17.8) 68 (54.0) 95 Neo-adjuvant Chemotherapy 0 (0) 14 (9.2) 20 (15.9) 34 Neo-adjuvant radiotherapy 0 (0) 0 (0) 12 (9.5) 12 <0.0001 Chemotherapy 0 (0) 63 (41.4) 89 (70.6) 152 Radiotherapy 0 (0) 21 (13.8) 47 (37.3) 68 Molecular treatment 0 (0) 6 (3.9) 26 (20.6) 32 Unknown 0 (0) 5 (3.3) 5 (4.0) 10 BM count [n;%] 1 BM 60 (60.6) 80 (52.6) 59 (46.8) 199 (52.8) 0.11 2–3 BM 29 (29.3) 51 (33.6) 38 (30.2) 118 (31.3) 4 BM 10 (10.1) 30 (19.8) 29 (23.0) 69 (18.3) ≥ Mutational status [n;%] N/A 29 (29.3) 79 (52.0) 34 (27.0) 142 (37.7) Wild type 36 (36.4) 18 (11.8) 40 (31.7) 94 (24.9) EGFR 4 (4.0) 28 (18.4) 19 (15.1) 51 (13.6) KRAS 7 (17.2) 20 (13.2) 21(16.7) 58 (15.4) MET 6 (6.1) 3 (2.0) 4 (3.2) 13 (3.4) 0.002 BRAF 1 (1.0) 0 (0) 1 (0.8) 2 (0.5) ALK 1 (1.0) 1 (0.7) 1 (0.8) 3 (0.8) ROS 0 (0) 0 (0) 3 (2.4) 3 (0.8) FGFR 2 (2.0) 1 (0.7) 1 (0.8) 4 (1.1) PIK3CA 0 (0) 2 (1.3) 0 (0) 2 (0.5) ErbB2 3 (3.0) 0 (0) 2 (1.6) 5 (1.3) Tumor location [n;(%)] Supratentorial 46 (46.5) 86 (56.6) 64 (50.8) 196 (52.0) 0.17 Infratentorial 22 (22.2) 25 (16.4) 11 (8.7) 58 (15.4) Supra- and infratentorial 31 (31.3) 41 (27.0) 51 (40.5) 123 (32.6) Symptomatic BM [n;(%)] Neurological deficits [n] 97 (98.0) 90 (59.2) 71 (56.3) 258 (68.4) Seizures 15 21 12 48 Aphasia 14 11 8 33 <0.0001 Hemiparesis 26 28 21 75 Visual field defects 1 13 5 19 Cerebellar signs 39 10 20 69 Signs of elevated intracranial pressure 30 26 18 74 KPS at presentation [median; range] 80 (40–100) 90 (40–100) 90 (50–100) 80 (40–100) 0.03 RPA class prior to BM treatment Class I 0 0 34 34 <0.0001 Class II 79 133 72 284 Class III 20 19 20 59 RPA class after BM treatment Class I 0 1 34 35 <0.0001 Class II 97 139 78 314 Class III 2 12 14 28 Treatment modality Surgery + postoperative radiotherapy 84 (84.8) 91 (59.9) 70 (55.6) 245 (65.0) <0.0001 Stereotactic radiosurgery 15 (15.2) 61 (40.1) 56 (44.4) 132 (35.0) Systemic medical treatment after BM Treatment modality (n = 238) 68 (68.7) 102 (67.1) 71 (56.3) 241 (63.9) 0.09 Chemotherapy 42 72 57 171 Molecular therapy 39 39 24 102 Dead by time of analysis 62 (62.6) 103 (67.8) 67 (53.2) 232 (61.5) Cause of death Unknown 8 (12.9) 67 (65.0) 23 (34.3) 101 (43.5) Neurological 4 (6.5) 7 (6.8) 10 (14.9) 21(9.1) <0.0001 Systemic disease progression 46 (74.1) 26 (25.2) 34 (50.7) 106 (45.7) others 4 (6.5) 3 (2.9) 6 (9.0) 13 (5.6) Abbreviations used in Table1: ALK (anaplastic lymphoma kinase), BM (Brain metastasis /es), BRAF (v-raf murine sarcoma viral oncogene homolog B1), EGFR (epidermal growth factor recetor), ErbB2 (Erb-B2 Receptor Tyrosine Kinase 2), FGFR (fibroblast growth factor receptor), KPS (Karnofsky Performance Status), KRAS (Kirsten rat sarcoma viral oncogene), MET (Mesenchymal–epithelial transition), N/A (not applicable), PIK3CA (Phosphatidylinositol-4,5-Bisphosphate 3-Kinase Catalytic Subunit Alpha), ROS (reactive oxygen species), RPA (recursive partitioning analysis).
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