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Bone Metastases and Immunotherapy in Patients with Advanced Non-Small-Cell Lung Cancer

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Bone Metastases and Immunotherapy in Patients with Advanced Non-Small-Cell Lung Cancer Landi et al. Journal for ImmunoTherapy of Cancer (2019) 7:316 https://doi.org/10.1186/s40425-019-0793-8 RESEARCH ARTICLE Open Access Bone metastases and immunotherapy in patients with advanced non-small-cell lung cancer Lorenza Landi1, Federica D’Incà2, Alain Gelibter3, Rita Chiari4, Francesco Grossi5, Angelo Delmonte6, Antonio Passaro7, Diego Signorelli8, Francesco Gelsomino9, Domenico Galetta10, Diana Giannarelli11, Hector Soto Parra12, Gabriele Minuti13, Marcello Tiseo14, Maria Rita Migliorino15, Francesco Cognetti11, Luca Toschi16, Paolo Bidoli17, Francovito Piantedosi18, Luana Calabro’19 and Federico Cappuzzo1* Abstract Background: Bone metastases (BoM) are a negative prognostic factor in non-small-cell lung cancer (NSCLC). Beyond its supportive role, bone is a hematopoietic organ actively regulating immune system. We hypothesized that BoM may influence sensitivity to immunotherapy. Methods: Pretreated non-squamous (cohort A) and squamous (cohort B) NSCLCs included in the Italian Expanded Access Program were evaluated for nivolumab efficacy according to BoM. Results: Cohort A accounted for 1588 patients with non-squamous NSCLC, including 626 (39%) with (BoM+) and 962 (61%) without BoM (BoM-). Cohort B accounted for 371 patients with squamous histology including 120 BoM+ (32%) and 251 (68%) BoM- cases. BoM+ had lower overall response rate (ORR; Cohort A: 12% versus 23%, p < 0.0001; Cohort B: 13% versus 22%, p = 0.04), shorter progression free survival (PFS; Cohort A: 3.0 versus 4.0 months, p < 0.0001; Cohort B: 2.7 versus 5.2 months, p < 0.0001) and overall survival (OS; Cohort A: 7.4 versus 15.3 months, p < 0.0001; Cohort B: 5.0 versus 10.9 months, p < 0.0001). Moreover, BoM negatively affected outcome irrespective of performance status (PS; OS in both cohorts: p < 0.0001) and liver metastases (OS cohort A: p < 0.0001; OS Cohort B: p = 0.48). At multivariate analysis, BoM independently associated with higher risk of death (cohort A: HR 1.50; cohort B: HR 1.78). Conclusions: BoM impairs immunotherapy efficacy. Accurate bone staging should be included in clinical trials with immunotherapy. Keywords: Bone metastases, Nivolumab, Immunotherapy, PD-L1, Non-small-cell lung cancer Introduction after platinum-doublet chemotherapy, whereas pembroli- In the last few years, improvements in cancer biology and zumab is the standard front line for untreated patients immune system knowledge significantly prolonged sur- with PD-L1 expression >50%[1–8]. As a consequence, vival of patients with metastatic non-small cell lung cancer the proportion of patients still candidate for exclusive (NSCLC) [1–3]. Agents targeting the programmed death- chemotherapy is gradually decreasing. At present, PD-L1 1 receptor (PD-1)/ PD-ligand 1 (PD-L1) pathway, also expression is the only validated biomarker adopted in named immune checkpoint inhibitors (ICIs), have clinical practice for selecting NSCLC candidate for emerged as powerful therapeutic strategy in different set- immunotherapy [8]. Several other biomarkers are under tings [1–7]. Nivolumab, pembrolizumab and atezolizumab investigation with Tumor Mutational Burden (TMB) as are three recommended options for patients who progress the one closest to a routine adoption [9]. Recently, some clinical factors such as performance status * Correspondence: [email protected] 1Department of Oncology and Hematology, AUSL Romagna, Ravenna, Italy Full list of author information is available at the end of the article © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Landi et al. Journal for ImmunoTherapy of Cancer (2019) 7:316 Page 2 of 9 and metastatic sites, emerged as potential predictors for patients aged ≥18 years, with histologically or cytologically immunotherapy efficacy [10–12]. In a retrospective study diagnosis of non-squamous or squamous NSCLC, pre- conducted in 201 Asian patients and treated with nivolu- treated with at least one systemic therapy for advanced dis- mab, poor performance status (ECOG PS > 2) and pres- ease and an Eastern Cooperative Oncology Group (ECOG) ence of lung or liver metastases independently associated PS < 2, were included onto the study if they had no evi- with shorter PFS [11]. Another study evaluated organ spe- dence of carcinomatous meningitis or serum positivity for cific response rate to second or subsequent line nivolumab HIV, HBV or HCV and no prior therapy checkpoint inhibi- in 52 patients with higher response observed in lymph tor. In both cohorts nivolumab 3 mg/kg was administered nodes (28%) followed by primary lung lesions (16%). Inter- intravenously every 2 weeks for ≤24 months. Patients in- estingly, among patients with bone metastases, 75% had cluded in the analysis had received at least 1 dose of nivolu- progressive bone lesions at the time of tumor progression mab. This study was conducted in accordance with the [12]. This data suggest that efficacy of immunotherapy Declaration of Helsinki (1964) and International Confer- can be modulated by tumor microenvironment, which dif- ence of Harmonization Guidelines for Clinical Practice and fers among organs. was approved by the appropriate Institutional Review Because of its large surface area and highly vascular Board/Independent Ethics Committee. All patients pro- supply, bone is a common site of metastatic spread in vided written informed consent before treatment. NSCLC [13, 14]. Implementation of diagnostic tools coupled with survival improvement have resulted in a Outcome measures raised incidence of bone metastases, with 20–30% of Tumor response was assessed using Response Evaluation NSCLC patients presenting with bone lesions at diagno- in Solid Tumors (RECIST) criteria version 1.0 [19]. sis and an additional 35–40% of cases developing bone Investigator-assessed objective response rate (ORR), pro- metastases during the course of their disease [15]. Pa- gression free survival (PFS) and overall survival (OS) tients with bone disease frequently experience skeletal- were evaluated. Patients were monitored for adverse related events entailing severe pain and deterioration in events (AEs) using the National Cancer Institute Com- their performance status (PS) and quality of life. Not mon Terminology Criteria for Adverse Events v4.0. surprisingly, bone metastases negatively affect overall survival [13]. In addition to its supportive role, bone is a Statistical analysis hematopoietic organ. Several evidences showed that Efficacy and safety analyses were conducted in all patients bone marrow plays active functions in regulating im- who received at least one nivolumab dose. ORR, PFS, OS mune system and trafficking of immune cells, including and safety were evaluated. Chi-square measured associ- regulatory T cells, conventional T cells, B cells, dendritic ation between patient characteristics and ORR. PFS was cells, natural killer T cells, neutrophils, myeloid-derived calculated as the time from the start of nivolumab treat- suppressor cells and mesenchymal stem cells [16]. ment until evidence of progressive disease or death which- Therefore, bone marrow is an immune regulatory organ ever occurred first. PFS and OS were estimated using potentially influencing response to immunotherapy. Kaplan-Meier method and 95% confidence intervals (CIs) However, none of the randomized studies specifically were derived using Hosmer and Lemeshow approach. Dif- investigated the consequences of bone involvement in ferences between survival curves were evaluated with log patients exposed to checkpoint inhibitors or stratified rank test. A Cox regression model was used to explore the patients according to presence of bone metastases. Aim association between patient characteristics and survival of the present study was to assess whether efficacy of times; Hazard Ratios (HRs) with 95% CIs were reported. nivolumab was influenced by presence of bone disease When performing a multivariate analysis, a stepwise pro- in a large pretreated, metastatic, NSCLC. cedure was used based on Wald statistics, enter and re- move values set to 0.05 and 0.10, respectively. Material and methods Study design, patients and treatment Results The trial was conducted in two cohorts (Cohort A = non- Patient populations squamous-cell histology, N = 1588; cohort B = squamous- Cohort A cell histology, N = 371) of advanced NSCLC patients treated Characteristics of non-squamous cohort are illustrated in 153 Italian centers and included in the nivolumab Ex- in Table 1. Among the 1588 patients, 626 (39%) had panded Access Program (EAP) from April 2015 to Septem- bone metastases (BoM+ group) and 962 (61%) had no ber 2016. The Italian EAP was a prospective, single-arm, evidence of bone involvement (BoM- group). BoM+ pa- open-label trial intended to provide early access to nivolu- tients were younger than BoM- (p = 0.001) with a signifi- mab. Details of main inclusion and exclusion criteria and cantly lower percentage of individuals older than 75 treatment have been previously published [17, 18]. Briefly years (p < 0.0001).
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