Editorial

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Open AccessEditorial

Update in Lung Cancer Molecular Pathology: Technological Advances and Clinical Practice

by Paolo Graziano and Giulio Rossi

Cancers 2023, 15(15), 3812; https://doi.org/10.3390/cancers15153812 - 27 Jul 2023

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This Special Issue of eleven articles, including six original works and five reviews, demonstrates the modern heterogenous approach to lung cancer by means of various methodologies from international experts from various countries [...] Full article

(This article belongs to the Special Issue Update in Lung Cancer Molecular Pathology: Technological Advances and Clinical Practice)

Research

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13 pages, 1313 KiB

Open AccessArticle

Robust Performance of the Novel Research-Use-Only Idylla GeneFusion Assay Using a Diverse Set of Pathological Samples with a Proposed 1-Day Workflow for Advanced NSCLC Evaluation

by Alvaro Leone, Lucia Anna Muscarella, Paolo Graziano, Andrea Tornese, Lucia Rosalba Grillo, Angela Di Lorenzo, Monica Bronzini, Stefania Scarpino, Angelo Sparaneo and Giulio Rossi

Cancers 2023, 15(1), 292; https://doi.org/10.3390/cancers15010292 - 31 Dec 2022

Cited by 5 | Viewed by 1889

Abstract

A range of different techniques are available for predictive biomarker testing for non-small-cell lung cancer (NSCLC) clinical management. International guidelines suggest next-generation sequencing (NGS) as the preferred procedure, but other reverse transcriptase-polymerase chain reaction (RT-PCR)-based methods are rapidly evolving. In this study, we [...] Read more.

A range of different techniques are available for predictive biomarker testing for non-small-cell lung cancer (NSCLC) clinical management. International guidelines suggest next-generation sequencing (NGS) as the preferred procedure, but other reverse transcriptase-polymerase chain reaction (RT-PCR)-based methods are rapidly evolving. In this study, we evaluated the reliability and accuracy of the Idylla^TM GeneFusion assay, a rapid and fully automated platform able to simultaneously detect ALK, ROS1, RET and NTRK1/2/3 and MET ex14 skipping mutations and compared its performance with routine reference methods. The cohort included thirty-seven NSCLCs plus two parotid gland carcinomas, previously characterized for the above alterations through either IHC, FISH, RT-PCR or NGS. In 36 of 39 cases, the Idylla GeneFusion assay and the reference methods were concordant (overall agreement: 92.3%). Tumor sections stored at room temperature for up to 60 days and 17 cases older than 2 years were successfully characterized. Our results suggest that the Idylla GeneFusion assay is a reliable tool to define gene fusion status and may be a valuable stand-alone diagnostic test when time efficiency is needed or NGS is not feasible. Full article

(This article belongs to the Special Issue Update in Lung Cancer Molecular Pathology: Technological Advances and Clinical Practice)

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16 pages, 1951 KiB

Open AccessArticle

Monitoring cfDNA in Plasma and in Other Liquid Biopsies of Advanced EGFR Mutated NSCLC Patients: A Pilot Study and a Review of the Literature

by Michela Verzè, Roberta Minari, Letizia Gnetti, Paola Bordi, Alessandro Leonetti, Agnese Cosenza, Leonarda Ferri, Maria Majori, Massimo De Filippo, Sebastiano Buti, Donatello Gasparro, Rita Nizzoli, Cinzia Azzoni, Lorena Bottarelli, Anna Squadrilli, Paola Mozzoni and Marcello Tiseo

Cancers 2021, 13(21), 5403; https://doi.org/10.3390/cancers13215403 - 28 Oct 2021

Cited by 7 | Viewed by 1929

Abstract

In order to study alternatives at the tissue biopsy to study EGFR status in NSCLC patients, we evaluated three different liquid biopsy platforms (plasma, urine and exhaled breath condensate, EBC). We also reviewed the literature of the cfDNA biological sources other than plasma [...] Read more.

In order to study alternatives at the tissue biopsy to study EGFR status in NSCLC patients, we evaluated three different liquid biopsy platforms (plasma, urine and exhaled breath condensate, EBC). We also reviewed the literature of the cfDNA biological sources other than plasma and compared our results with it about the sensitivity to EGFR mutation determination. Twenty-two EGFR T790M-mutated NSCLC patients in progression to first-line treatment were enrolled and candidate to osimertinib. Plasma, urine and EBC samples were collected at baseline and every two months until progression. Molecular analysis of cfDNA was performed by ddPCR and compared to tissue results. At progression NGS analysis was performed. The EGFR activating mutation detection reached a sensitivity of 58 and 11% and for the T790M mutation of 45 and 10%, in plasma and urine samples, respectively. Any DNA content was recovered from EBC samples. Considering the plasma monitoring study, the worst survival was associated with positive shedding status; both plasma and urine molecular progression anticipated the radiological worsening. Our results confirmed the role of plasma liquid biopsy in testing EGFR mutational status, but unfortunately, did not evidence any improvement from the combination with alternative sources, as urine and EBC. Full article

(This article belongs to the Special Issue Update in Lung Cancer Molecular Pathology: Technological Advances and Clinical Practice)

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30 pages, 2288 KiB

Open AccessArticle

Preliminary Report on Computed Tomography Radiomics Features as Biomarkers to Immunotherapy Selection in Lung Adenocarcinoma Patients

by Vincenza Granata, Roberta Fusco, Matilde Costa, Carmine Picone, Diletta Cozzi, Chiara Moroni, Giorgia Viola La Casella, Agnese Montanino, Riccardo Monti, Francesca Mazzoni, Roberta Grassi, Valeria Grazia Malagnino, Salvatore Cappabianca, Roberto Grassi, Vittorio Miele and Antonella Petrillo

Cancers 2021, 13(16), 3992; https://doi.org/10.3390/cancers13163992 - 07 Aug 2021

Cited by 47 | Viewed by 4068

Abstract

Purpose: To assess the efficacy of radiomics features obtained by computed tomography (CT) examination as biomarkers in order to select patients with lung adenocarcinoma who would benefit from immunotherapy. Methods: Seventy-four patients (median age 63 years, range 42–86 years) with histologically confirmed lung [...] Read more.

Purpose: To assess the efficacy of radiomics features obtained by computed tomography (CT) examination as biomarkers in order to select patients with lung adenocarcinoma who would benefit from immunotherapy. Methods: Seventy-four patients (median age 63 years, range 42–86 years) with histologically confirmed lung cancer who underwent immunotherapy as first- or second-line therapy and who had baseline CT studies were enrolled in this approved retrospective study. As a control group, we selected 50 patients (median age 66 years, range 36–86 years) from 2005 to 2013 with histologically confirmed lung adenocarcinoma who underwent chemotherapy alone or in combination with targeted therapy. A total of 573 radiomic metrics were extracted: 14 features based on Hounsfield unit values specific for lung CT images; 66 first-order profile features based on intensity values; 43 second-order profile features based on lesion shape; 393 third-order profile features; and 57 features with higher-order profiles. Univariate and multivariate statistical analysis with pattern recognition approaches and the least absolute shrinkage and selection operator (LASSO) method were used to assess the capability of extracted radiomics features to predict overall survival (OS) and progression free survival (PFS) time. Results: A total of 38 patients (median age 61; range 41–78 years) with confirmed lung adenocarcinoma and subjected to immunotherapy satisfied inclusion criteria, and 50 patients in a control group were included in the analysis The shift in the center of mass of the lesion due to image intensity was significant both to predict OS in patients subjected to immunotherapy and to predict PFS in patients subjected to immunotherapy and in patients in the control group. With univariate analysis, low diagnostic accuracy was reached to stratify patients based on OS and PFS time. Regarding multivariate analysis, considering the robust (two morphological features, three textural features and three higher-order statistical metrics) application of the LASSO approach and all patients, a support vector machine reached the best results for stratifying patients based on OS (area under curve (AUC) of 0.89 and accuracy of 81.6%). Alternatively, considering the robust predictors (six textural features and one higher-order statistical metric) and application of the LASSO approach including all patients, a decision tree reached the best results for stratifying patients based on PFS time (AUC of 0.96 and accuracy of 94.7%). Conclusions: Specific radiomic features could be used to select patients with lung adenocarcinoma who would benefit from immunotherapy because a subset of imaging radiomic features useful to predict OS or PFS time were different between the control group and the immunotherapy group. Full article

(This article belongs to the Special Issue Update in Lung Cancer Molecular Pathology: Technological Advances and Clinical Practice)

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13 pages, 1507 KiB

Open AccessArticle

Biomarkers and Gene Signatures to Predict Durable Response to Pembrolizumab in Non-Small Cell Lung Cancer

by Anello Marcello Poma, Rossella Bruno, Iacopo Pietrini, Greta Alì, Giulia Pasquini, Agnese Proietti, Enrico Vasile, Sabrina Cappelli, Antonio Chella and Gabriella Fontanini

Cancers 2021, 13(15), 3828; https://doi.org/10.3390/cancers13153828 - 29 Jul 2021

Cited by 6 | Viewed by 2568

Abstract

Pembrolizumab has been approved as first-line treatment for advanced Non-small cell lung cancer (NSCLC) patients with tumors expressing PD-L1 and in the absence of other targetable alterations. However, not all patients that meet these criteria have a durable benefit. In this monocentric study, [...] Read more.

Pembrolizumab has been approved as first-line treatment for advanced Non-small cell lung cancer (NSCLC) patients with tumors expressing PD-L1 and in the absence of other targetable alterations. However, not all patients that meet these criteria have a durable benefit. In this monocentric study, we aimed at refining the selection of patients based on the expression of immune genes. Forty-six consecutive advanced NSCLC patients treated with pembrolizumab in first-line setting were enrolled. The expression levels of 770 genes involved in the regulation of the immune system was analysed by the nanoString system. PD-L1 expression was evaluated by immunohistochemistry. Patients with durable clinical benefit had a greater infiltration of cytotoxic cells, exhausted CD8, B-cells, CD45, T-cells, CD8 T-cells and NK cells. Immune cell scores such as CD8 T-cell and NK cell were good predictors of durable response with an AUC of 0.82. Among the immune cell markers, XCL1/2 showed the better performance in predicting durable benefit to pembrolizumab, with an AUC of 0.85. Additionally, CD8A, CD8B and EOMES showed a high specificity (>0.86) in identifying patients with a good response to treatment. In the same series, PD-L1 expression levels had an AUC of 0.61. The characterization of tumor microenvironment, even with the use of single markers, can improve patients’ selection for pembrolizumab treatment. Full article

(This article belongs to the Special Issue Update in Lung Cancer Molecular Pathology: Technological Advances and Clinical Practice)

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13 pages, 1634 KiB

Open AccessArticle

Clinical and Molecular Features of Epidermal Growth Factor Receptor (EGFR) Mutation Positive Non-Small-Cell Lung Cancer (NSCLC) Patients Treated with Tyrosine Kinase Inhibitors (TKIs): Predictive and Prognostic Role of Co-Mutations

by Paolo Bironzo, Maria Lucia Reale, Tessa Sperone, Fabrizio Tabbò, Andrea Caglio, Angela Listì, Francesco Passiglia, Massimo Di Maio, Luisella Righi, Federico Bussolino, Giorgio V. Scagliotti and Silvia Novello

Cancers 2021, 13(10), 2425; https://doi.org/10.3390/cancers13102425 - 17 May 2021

Cited by 7 | Viewed by 1921

Abstract

Background: Tyrosine kinase inhibitors (TKIs) show variable efficacy in epidermal growth factor receptor mutation-positive (EGFR+) NSCLC patients, even in patients harbouring the same mutation. Co-alterations may predict different outcomes to TKIs. Methods: We retrospectively analysed all consecutive EGFR+ advanced NSCLC treated with first-line [...] Read more.

Background: Tyrosine kinase inhibitors (TKIs) show variable efficacy in epidermal growth factor receptor mutation-positive (EGFR+) NSCLC patients, even in patients harbouring the same mutation. Co-alterations may predict different outcomes to TKIs. Methods: We retrospectively analysed all consecutive EGFR+ advanced NSCLC treated with first-line TKIs at our Institutions. NGS with a 22 genes clinical panel was performed on diagnostic specimens. PD-L1 expression was also evaluated. Results: Of the 106 analysed specimens, 59 showed concomitant pathogenic mutations. No differences in OS (mOS 22.8 vs. 29.5 months; p = 0.088), PFS (mPFS 10.9 vs. 11.2 months; p = 0.415) and ORR (55.9% vs. 68.1%; p = 0.202) were observed comparing patients without and with co-alterations. Subgroup analysis by EGFR mutation type and TKIs generation (1st/2nd vs. 3rd) did not show any difference too. No correlations of PD-L1 expression levels by co-mutational status were found. Significant associations with presence of co-alterations and younger age (p = 0.018) and baseline lymph nodes metastases (p = 0.032) were observed. Patients without concomitant alterations had a significant higher risk of bone progression (26.5% vs. 3.3%, p = 0.011). Conclusions: Pathogenic co-alterations does not seem to predict survival nor efficacy of EGFR TKIs in previously untreated advanced NSCLC. Full article

(This article belongs to the Special Issue Update in Lung Cancer Molecular Pathology: Technological Advances and Clinical Practice)

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12 pages, 2467 KiB

Open AccessArticle

Quantitative Multiplexed Proteomics Could Assist Therapeutic Decision Making in Non-Small Cell Lung Cancer Patients with Ambiguous ALK Test Results

by Ho Jung An, Eunkyung An, Shahrooz Rabizadeh, Wei-Li Liao, Jon Burrows, Todd Hembrough, Jin Hyung Kang, Chan Kwon Park and Tae-Jung Kim

Cancers 2021, 13(10), 2337; https://doi.org/10.3390/cancers13102337 - 12 May 2021

Cited by 2 | Viewed by 1825

Abstract

Therapeutic guidance in non-small cell lung cancer (NSCLC) tumors that are positive for anaplastic lymphoma kinase (ALK) fluorescent in situ hybridization (FISH), but negative for ALK immunohistochemistry, is still challenging. Parallel routine screening of 4588 NSCLC cases identified 22 discordant cases. [...] Read more.

Therapeutic guidance in non-small cell lung cancer (NSCLC) tumors that are positive for anaplastic lymphoma kinase (ALK) fluorescent in situ hybridization (FISH), but negative for ALK immunohistochemistry, is still challenging. Parallel routine screening of 4588 NSCLC cases identified 22 discordant cases. We rechecked these samples using ALK antibodies and selected reaction monitoring (SRM) quantitative multiplexed proteomics screening multiple protein targets, including ALK and MET for the ALK tyrosine kinase inhibitor (TKI), and FR-alpha, hENT1, RRM1, TUBB3, ERCC1, and XRCC1 for chemotherapy. The presence of ALK (31.8%), MET (36.4%), FR-alpha (72.7%), hENT1 (18.2%), RRM1 (31.8%), TUBB3 (72.9%), ERCC1 (4.5%), and a low level of XRCC1 (54.4%) correlated with clinical outcomes. SRM was more sensitive than the ALK D5F3 assay. Among the eight cases receiving ALK TKI, four cases with ALK or MET detected by SRM had complete or partial responses, whereas four cases without ALK or MET showed progression. Twenty-seven treatment outcomes from 20 cases were assessed and cases expressing more than half of the specific predictive proteins were sensitive to matching therapeutic agents and showed longer progression-free survival than the other cases (p < 0.001). SRM showed a potential role in therapeutic decision making in NSCLC patients with ambiguous ALK test results. Full article

(This article belongs to the Special Issue Update in Lung Cancer Molecular Pathology: Technological Advances and Clinical Practice)

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Review

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18 pages, 3732 KiB

Open AccessEditor’s ChoiceReview

Treatment Strategies for KRAS-Mutated Non-Small-Cell Lung Cancer

by Éabha O’Sullivan, Anna Keogh, Brian Henderson, Stephen P. Finn, Steven G. Gray and Kathy Gately

Cancers 2023, 15(6), 1635; https://doi.org/10.3390/cancers15061635 - 07 Mar 2023

Cited by 11 | Viewed by 6268

Abstract

Activating mutations in KRAS are highly prevalent in solid tumours and are frequently found in 35% of lung, 45% of colorectal, and up to 90% of pancreatic cancers. Mutated KRAS is a prognostic factor for disease-free survival (DFS) and overall survival (OS) in [...] Read more.

Activating mutations in KRAS are highly prevalent in solid tumours and are frequently found in 35% of lung, 45% of colorectal, and up to 90% of pancreatic cancers. Mutated KRAS is a prognostic factor for disease-free survival (DFS) and overall survival (OS) in NSCLC and is associated with a more aggressive clinical phenotype, highlighting the need for KRAS-targeted therapy. Once considered undruggable due to its smooth shallow surface, a breakthrough showed that the activated G12C-mutated KRAS isozyme can be directly inhibited via a newly identified switch II pocket. This discovery led to the development of a new class of selective small-molecule inhibitors against the KRAS G12C isoform. Sotorasib and adagrasib are approved in locally advanced or metastatic NSCLC patients who have received at least one prior systemic therapy. Currently, there are at least twelve KRAS G12C inhibitors being tested in clinical trials, either as a single agent or in combination. In this study, KRAS mutation prevalence, subtypes, rates of occurrence in treatment-resistant invasive mucinous adenocarcinomas (IMAs), and novel drug delivery options are reviewed. Additionally, the current status of KRAS inhibitors, multiple resistance mechanisms that limit efficacy, and their use in combination treatment strategies and novel multitargeted approaches in NSCLC are discussed. Full article

(This article belongs to the Special Issue Update in Lung Cancer Molecular Pathology: Technological Advances and Clinical Practice)

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28 pages, 2471 KiB

Open AccessReview

Advances in the Molecular Landscape of Lung Cancer Brain Metastasis

by Vanessa G. P. Souza, Rachel Paes de Araújo, Mariana R. Santesso, Ana Laura Seneda, Iael W. Minutentag, Tainara Francini Felix, Pedro Tadao Hamamoto Filho, Michelle E. Pewarchuk, Liam J. Brockley, Fábio A. Marchi, Wan L. Lam, Sandra A. Drigo and Patricia P. Reis

Cancers 2023, 15(3), 722; https://doi.org/10.3390/cancers15030722 - 24 Jan 2023

Cited by 7 | Viewed by 3622

Abstract

Lung cancer is one of the most frequent tumors that metastasize to the brain. Brain metastasis (BM) is common in advanced cases, being the major cause of patient morbidity and mortality. BMs are thought to arise via the seeding of circulating tumor cells [...] Read more.

Lung cancer is one of the most frequent tumors that metastasize to the brain. Brain metastasis (BM) is common in advanced cases, being the major cause of patient morbidity and mortality. BMs are thought to arise via the seeding of circulating tumor cells into the brain microvasculature. In brain tissue, the interaction with immune cells promotes a microenvironment favorable to the growth of cancer cells. Despite multimodal treatments and advances in systemic therapies, lung cancer patients still have poor prognoses. Therefore, there is an urgent need to identify the molecular drivers of BM and clinically applicable biomarkers in order to improve disease outcomes and patient survival. The goal of this review is to summarize the current state of knowledge on the mechanisms of the metastatic spread of lung cancer to the brain and how the metastatic spread is influenced by the brain microenvironment, and to elucidate the molecular determinants of brain metastasis regarding the role of genomic and transcriptomic changes, including coding and non-coding RNAs. We also present an overview of the current therapeutics and novel treatment strategies for patients diagnosed with BM from NSCLC. Full article

(This article belongs to the Special Issue Update in Lung Cancer Molecular Pathology: Technological Advances and Clinical Practice)

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14 pages, 533 KiB

Open AccessReview

Extracellular Vesicles in Lung Cancer: Prospects for Diagnostic and Therapeutic Applications

by Taketo Kato, Jody V. Vykoukal, Johannes F. Fahrmann and Samir Hanash

Cancers 2021, 13(18), 4604; https://doi.org/10.3390/cancers13184604 - 14 Sep 2021

Cited by 10 | Viewed by 2864

Abstract

Extracellular vesicles (EVs) are nano-sized lipid-bound particles containing proteins, nucleic acids and metabolites released by cells. They have been identified in body fluids including blood, saliva, sputum and pleural effusions. In tumors, EVs derived from cancer and immune cells mediate intercellular communication and [...] Read more.

Extracellular vesicles (EVs) are nano-sized lipid-bound particles containing proteins, nucleic acids and metabolites released by cells. They have been identified in body fluids including blood, saliva, sputum and pleural effusions. In tumors, EVs derived from cancer and immune cells mediate intercellular communication and exchange, and can affect immunomodulatory functions. In the context of lung cancer, emerging evidence implicates EV involvement during various stages of tumor development and progression, including angiogenesis, epithelial to mesenchymal transformation, immune system suppression, metastasis and drug resistance. Additionally, tumor-derived EVs (TDEs) have potential as a liquid biopsy source and as a means of therapeutic targeting, and there is considerable interest in developing clinical applications for EVs in these contexts. In this review, we consider the biogenesis, components, biological functions and isolation methods of EVs, and the implications for their clinical utility for diagnostic and therapeutic applications in lung cancer. Full article

(This article belongs to the Special Issue Update in Lung Cancer Molecular Pathology: Technological Advances and Clinical Practice)

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28 pages, 1854 KiB

Open AccessReview

Exosomes in Lung Cancer: Actors and Heralds of Tumor Development

by Amaia Sandúa, Estibaliz Alegre and Álvaro González

Cancers 2021, 13(17), 4330; https://doi.org/10.3390/cancers13174330 - 27 Aug 2021

Cited by 13 | Viewed by 3550

Abstract

Lung cancer is a leading cause of cancer-related death worldwide and in most cases, diagnosis is reached when the tumor has already spread and prognosis is quite poor. For that reason, the research for new biomarkers that could improve early diagnosis and its [...] Read more.

Lung cancer is a leading cause of cancer-related death worldwide and in most cases, diagnosis is reached when the tumor has already spread and prognosis is quite poor. For that reason, the research for new biomarkers that could improve early diagnosis and its management is essential. Exosomes are microvesicles actively secreted by cells, especially by tumor cells, hauling molecules that mimic molecules of the producing cells. There are multiple methods for exosome isolation and analysis, although not standardized, and cancer exosomes from biological fluids are especially difficult to study. Exosomes’ cargo proteins, RNA, and DNA participate in the communication between cells, favoring lung cancer development by delivering signals for growth, metastasis, epithelial mesenchymal transition, angiogenesis, immunosuppression and even drug resistance. Exosome analysis can be useful as a type of liquid biopsy in the diagnosis, prognosis and follow-up of lung cancer. In this review, we will discuss recent advances in the role of exosomes in lung cancer and their utility as liquid biopsy, with special attention to isolating methods. Full article

(This article belongs to the Special Issue Update in Lung Cancer Molecular Pathology: Technological Advances and Clinical Practice)

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18 pages, 421 KiB

Open AccessReview

Prognostic and Predictive Biomarkers in Non-Small Cell Lung Cancer Patients on Immunotherapy—The Role of Liquid Biopsy in Unraveling the Puzzle

by Elien Augustus, Karen Zwaenepoel, Vasiliki Siozopoulou, Jo Raskin, Stephanie Jordaens, Geert Baggerman, Laure Sorber, Geert Roeyen, Marc Peeters and Patrick Pauwels

Cancers 2021, 13(7), 1675; https://doi.org/10.3390/cancers13071675 - 02 Apr 2021

Cited by 19 | Viewed by 4928

Abstract

In the last decade, immunotherapy has been one of the most important advances in the non-small cell lung cancer (NSCLC) treatment landscape. Nevertheless, only a subset of NSCLC patients benefits from it. Currently, the only Food and Drug Administration (FDA) approved diagnostic test [...] Read more.

In the last decade, immunotherapy has been one of the most important advances in the non-small cell lung cancer (NSCLC) treatment landscape. Nevertheless, only a subset of NSCLC patients benefits from it. Currently, the only Food and Drug Administration (FDA) approved diagnostic test for first-line immunotherapy in metastatic NSCLC patients uses tissue biopsies to determine the programmed death ligand 1 (PD-L1) status. However, obtaining tumor tissue is not always feasible and puts the patient at risk. Liquid biopsy, which refers to the tumor-derived material present in body fluids, offers an alternative approach. This less invasive technique gives real-time information on the tumor characteristics. This review addresses different promising liquid biopsy based biomarkers in NSCLC patients that enable the selection of patients who benefit from immunotherapy and the monitoring of patients during this therapy. The challenges and the opportunities of blood-based biomarkers such as cell-free DNA (cfDNA), circulating tumor cells (CTCs), exosomes, epigenetic signatures, microRNAs (miRNAs) and the T cell repertoire will be addressed. This review also focuses on the less-studied feces-based and breath-based biomarkers. Full article

(This article belongs to the Special Issue Update in Lung Cancer Molecular Pathology: Technological Advances and Clinical Practice)

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