Review
. 2021 Sep; 13(18):.
doi: 10.3390/cancers13184543.

NSCLC Biomarkers to Predict Response to Immunotherapy with Checkpoint Inhibitors (ICI): From the Cells to In Vivo Images

Virginia Liberini 1 Annapaola Mariniello 2 Luisella Righi 3 Martina Capozza 4 Marco Donatello Delcuratolo 2 Enzo Terreno 4 Mohsen Farsad 5 Marco Volante 3 Silvia Novello 2 Désirée Deandreis 1 
Affiliations
  • PMID: 34572771
  •     192 References
  •     2 citations

Abstract

Lung cancer remains the leading cause of cancer-related death, and it is usually diagnosed in advanced stages (stage III or IV). Recently, the availability of targeted strategies and of immunotherapy with checkpoint inhibitors (ICI) has favorably changed patient prognosis. Treatment outcome is closely related to tumor biology and interaction with the tumor immune microenvironment (TME). While the response in molecular targeted therapies relies on the presence of specific genetic alterations in tumor cells, accurate ICI biomarkers of response are lacking, and clinical outcome likely depends on multiple factors that are both host and tumor-related. This paper is an overview of the ongoing research on predictive factors both from in vitro/ex vivo analysis (ranging from conventional pathology to molecular biology) and in vivo analysis, where molecular imaging is showing an exponential growth and use due to technological advancements and to the new bioinformatics approaches applied to image analyses that allow the recovery of specific features in specific tumor subclones.

Keywords: PD-1; PD-L1; PET/CT; immune PET; immune checkpoint inhibitors; immunotherapy; non-small cell lung carcinoma; radiomics.

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Nat Med, 2018 Aug 08; 24(9). PMID: 30082870
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Absolute number of new lesions on 18F-FDG PET/CT is more predictive of clinical response than SUV changes in metastatic melanoma patients receiving ipilimumab.
Hoda Anwar, Christos Sachpekidis, +4 authors, Antonia Dimitrakopoulou-Strauss.
Eur J Nucl Med Mol Imaging, 2017 Nov 11; 45(3). PMID: 29124281
Assessing EGFR gene mutation status in non-small cell lung cancer with imaging features from PET/CT.
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Acad Radiol, 2019 May 31; 27(2). PMID: 31147234
Nivolumab plus Ipilimumab in Lung Cancer with a High Tumor Mutational Burden.
Matthew D Hellmann, Tudor-Eliade Ciuleanu, +21 authors, Luis Paz-Ares.
N Engl J Med, 2018 Apr 17; 378(22). PMID: 29658845    Free PMC article.
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The Role of VEGF Receptors as Molecular Target in Nuclear Medicine for Cancer Diagnosis and Combination Therapy.
Katarzyna Masłowska, Paweł Krzysztof Halik, +2 authors, Ewa Gniazdowska.
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Lucian Beer, Maximilian Hochmair, +10 authors, Helmut Prosch.
Clin Nucl Med, 2019 Apr 26; 44(7). PMID: 31021918
ARID1A alterations function as a biomarker for longer progression-free survival after anti-PD-1/PD-L1 immunotherapy.
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J Immunother Cancer, 2020 Mar 01; 8(1). PMID: 32111729    Free PMC article.
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Alexandra Snyder, Tavi Nathanson, +18 authors, Dean F Bajorin.
PLoS Med, 2017 May 30; 14(5). PMID: 28552987    Free PMC article.
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J Nucl Med, 2020 Feb 16; 61(4). PMID: 32060219
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The commensal microbiome is associated with anti-PD-1 efficacy in metastatic melanoma patients.
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Science, 2018 Jan 06; 359(6371). PMID: 29302014    Free PMC article.
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Metastatic non-small cell lung cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up.
D Planchard, S Popat, +9 authors, ESMO Guidelines Committee.
Ann Oncol, 2018 Oct 05; 29(Suppl 4). PMID: 30285222
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Guidelines for the evaluation of immune therapy activity in solid tumors: immune-related response criteria.
Jedd D Wolchok, Axel Hoos, +9 authors, F Stephen Hodi.
Clin Cancer Res, 2009 Nov 26; 15(23). PMID: 19934295
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Blood Immune Cell Biomarkers in Patient With Lung Cancer Undergoing Treatment With Checkpoint Blockade.
Miriam Möller, Steffi Turzer, +2 authors, Dagmar Riemann.
J Immunother, 2019 Oct 09; 43(2). PMID: 31592989    Free PMC article.
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J Clin Epidemiol, 2009 Jul 28; 62(10). PMID: 19631507
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Artificial Neural Networks in Cardiovascular Diseases and its Potential for Clinical Application in Molecular Imaging.
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Clin Cancer Res, 2016 Nov 09; 23(8). PMID: 27827313
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Commensal Bifidobacterium promotes antitumor immunity and facilitates anti-PD-L1 efficacy.
Ayelet Sivan, Leticia Corrales, +9 authors, Thomas F Gajewski.
Science, 2015 Nov 07; 350(6264). PMID: 26541606    Free PMC article.
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Gregory L Beatty, Edmund K Moon.
Oncoimmunology, 2015 May 06; 3(11). PMID: 25941599    Free PMC article.
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Matthew Kraman, Paul J Bambrough, +6 authors, Douglas T Fearon.
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Myeloid-Derived Suppressor Cells Hinder the Anti-Cancer Activity of Immune Checkpoint Inhibitors.
Rebekka Weber, Viktor Fleming, +5 authors, Viktor Umansky.
Front Immunol, 2018 Jun 27; 9. PMID: 29942309    Free PMC article.
Highly Cited. Review.
Vascular endothelial growth factor inhibits the development of dendritic cells and dramatically affects the differentiation of multiple hematopoietic lineages in vivo.
D Gabrilovich, T Ishida, +4 authors, D P Carbone.
Blood, 1998 Dec 03; 92(11). PMID: 9834220
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Genomic Features of Response to Combination Immunotherapy in Patients with Advanced Non-Small-Cell Lung Cancer.
Matthew D Hellmann, Tavi Nathanson, +29 authors, Jedd D Wolchok.
Cancer Cell, 2018 Apr 17; 33(5). PMID: 29657128    Free PMC article.
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Personalizing NSCLC therapy by characterizing tumors using TKI-PET and immuno-PET.
I Bahce, M Yaqub, +3 authors, N H Hendrikse.
Lung Cancer, 2016 Jun 21; 107. PMID: 27319335
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Cancer Cell, 2012 Jun 16; 21(6). PMID: 22698407    Free PMC article.
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Nat Med, 2018 Jun 13; 24(7). PMID: 29892065    Free PMC article.
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Comparison of iRECIST versus RECIST V.1.1 in patients treated with an anti-PD-1 or PD-L1 antibody: pooled FDA analysis.
Flora Mulkey, Marc R Theoret, +2 authors, Rajeshwari Sridhara.
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J Thorac Oncol, 2018 May 26; 13(9). PMID: 29800747    Free PMC article.
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A guide to cancer immunotherapy: from T cell basic science to clinical practice.
Alex D Waldman, Jill M Fritz, Michael J Lenardo.
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N Engl J Med, 2019 Sep 29; 381(21). PMID: 31562796
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Will FAPI PET/CT Replace FDG PET/CT in the Next Decade? Point-An Important Diagnostic, Phenotypic, and Biomarker Role.
Jeremie Calais, Christine E Mona.
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Ton N Schumacher, Robert D Schreiber.
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The Importance of Biopsy in the Era of Molecular Medicine.
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Trends Immunol, 2016 Feb 10; 37(3). PMID: 26858199    Free PMC article.
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Predictive Power of a Radiomic Signature Based on 18F-FDG PET/CT Images for EGFR Mutational Status in NSCLC.
Xiaofeng Li, Guotao Yin, +6 authors, Wengui Xu.
Front Oncol, 2019 Nov 05; 9. PMID: 31681597    Free PMC article.
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18F-fluorodeoxyglucose positron emission tomography/computed tomography-based radiomic features for prediction of epidermal growth factor receptor mutation status and prognosis in patients with lung adenocarcinoma.
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Nat Med, 2018 Nov 28; 24(12). PMID: 30478423
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Circulating T-cell Immunosenescence in Patients with Advanced Non-small Cell Lung Cancer Treated with Single-agent PD-1/PD-L1 Inhibitors or Platinum-based Chemotherapy.
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Cancer-associated fibroblasts and their influence on tumor immunity and immunotherapy.
Richard Lee Barrett, Ellen Puré.
Elife, 2020 Dec 29; 9. PMID: 33370234    Free PMC article.
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Fc-dependent depletion of tumor-infiltrating regulatory T cells co-defines the efficacy of anti-CTLA-4 therapy against melanoma.
Tyler R Simpson, Fubin Li, +11 authors, Sergio A Quezada.
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Sci Transl Med, 2017 Mar 03; 9(379). PMID: 28251903    Free PMC article.
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J Transl Med, 2021 Jan 08; 19(1). PMID: 33407613    Free PMC article.
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FDG PET/CT for Assessment of Immune Therapy: Opportunities and Understanding Pitfalls.
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68Ga-FAPI PET/CT: Tracer Uptake in 28 Different Kinds of Cancer.
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J Nucl Med, 2019 Apr 08; 60(6). PMID: 30954939    Free PMC article.
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Highly Cited. Review.
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Sho Koyasu, Mizuho Nishio, +2 authors, Kaori Togashi.
Ann Nucl Med, 2019 Oct 30; 34(1). PMID: 31659591
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Ludmil B Alexandrov, Serena Nik-Zainal, +72 authors, Michael R Stratton.
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First-in-Humans Imaging with 89Zr-Df-IAB22M2C Anti-CD8 Minibody in Patients with Solid Malignancies: Preliminary Pharmacokinetics, Biodistribution, and Lesion Targeting.
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Allele Frequency-Adjusted Blood-Based Tumor Mutational Burden as a Predictor of Overall Survival for Patients With NSCLC Treated With PD-(L)1 Inhibitors.
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J Thorac Oncol, 2019 Dec 18; 15(4). PMID: 31843683
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Incidence of Pseudoprogression during Immune Checkpoint Inhibitor Therapy for Solid Tumors: A Systematic Review and Meta-Analysis.
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Radiology, 2020 Aug 05; 297(1). PMID: 32749204    Free PMC article.
Systematic Review.
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Alexander Rühle, Anca-L Grosu, +8 authors, Nils H Nicolay.
Theranostics, 2020 Aug 18; 10(20). PMID: 32802199    Free PMC article.
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Hira Rizvi, Francisco Sanchez-Vega, +29 authors, Matthew D Hellmann.
J Clin Oncol, 2018 Jan 18; 36(7). PMID: 29337640    Free PMC article.
Highly Cited.
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Fabio Grizzi, Angelo Castello, Egesta Lopci.
Eur J Nucl Med Mol Imaging, 2018 Mar 14; 45(6). PMID: 29532102
18F-FDG PET/CT Can Predict Development of Thyroiditis Due to Immunotherapy for Lung Cancer.
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J Nucl Med Technol, 2018 Mar 31; 46(3). PMID: 29599403
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Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries.
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Imaging the Cancer Immune Environment and Its Response to Pharmacologic Intervention, Part 1: The Role of 18F-FDG PET/CT.
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Highly Cited. Review.
Immune Marker Profiling and Programmed Death Ligand 1 Expression Across NSCLC Mutations.
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J Thorac Oncol, 2018 Sep 30; 13(12). PMID: 30267840    Free PMC article.
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Eur J Nucl Med Mol Imaging, 2019 Nov 23; 47(5). PMID: 31754795
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Highly Cited. Review.
VEGF-A modulates expression of inhibitory checkpoints on CD8+ T cells in tumors.
Thibault Voron, Orianne Colussi, +15 authors, Magali Terme.
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Highly Cited.
Frequencies of circulating MDSC correlate with clinical outcome of melanoma patients treated with ipilimumab.
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Cancer Immunol Immunother, 2013 Dec 21; 63(3). PMID: 24357148
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Predicting Response to Immunotherapy by Evaluating Tumors, Lymphoid Cell-Rich Organs, and Immune-Related Adverse Events Using FDG-PET/CT.
Tomomi Nobashi, Lucia Baratto, +5 authors, Erik Mittra.
Clin Nucl Med, 2019 Jan 29; 44(4). PMID: 30688730
Patient HLA class I genotype influences cancer response to checkpoint blockade immunotherapy.
Diego Chowell, Luc G T Morris, +17 authors, Timothy A Chan.
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Early Detection of Checkpoint Inhibitor-Associated Myocarditis Using 68Ga-FAPI PET/CT.
Daniel Finke, Markus B Heckmann, +4 authors, Lorenz H Lehmann.
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PET Clin, 2019 Nov 19; 15(1). PMID: 31735296
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Elisabeth Brambilla, Gwénaël Le Teuff, +14 authors, Ming Sound Tsao.
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Highly Cited.
Commensal bacteria control cancer response to therapy by modulating the tumor microenvironment.
Noriho Iida, Amiran Dzutsev, +18 authors, Romina S Goldszmid.
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Highly Cited.
FDG PET/CT: EANM procedure guidelines for tumour imaging: version 2.0.
Ronald Boellaard, Roberto Delgado-Bolton, +26 authors, European Association of Nuclear Medicine (EANM).
Eur J Nucl Med Mol Imaging, 2014 Dec 03; 42(2). PMID: 25452219    Free PMC article.
Highly Cited.
Next Generation Imaging Techniques to Define Immune Topographies in Solid Tumors.
Violena Pietrobon, Alessandra Cesano, Francesco Marincola, Jakob Nikolas Kather.
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Radiother Oncol, 2018 May 22; 127(3). PMID: 29779918
Highly Cited. Systematic Review.
Proliferation of PD-1+ CD8 T cells in peripheral blood after PD-1-targeted therapy in lung cancer patients.
Alice O Kamphorst, Rathi N Pillai, +16 authors, Suresh S Ramalingam.
Proc Natl Acad Sci U S A, 2017 Apr 28; 114(19). PMID: 28446615    Free PMC article.
Highly Cited.
Atezolizumab in combination with bevacizumab enhances antigen-specific T-cell migration in metastatic renal cell carcinoma.
Jeffrey J Wallin, Johanna C Bendell, +19 authors, David F McDermott.
Nat Commun, 2016 Aug 31; 7. PMID: 27571927    Free PMC article.
Highly Cited.
PET/CT imaging for evaluation of multimodal treatment efficacy and toxicity in advanced NSCLC-current state and future directions.
Chukwuka Eze, Nina-Sophie Schmidt-Hegemann, +11 authors, Marcus Unterrainer.
Eur J Nucl Med Mol Imaging, 2021 Mar 25; 48(12). PMID: 33760957    Free PMC article.
Review.
Additional Value of PET Radiomic Features for the Initial Staging of Prostate Cancer: A Systematic Review from the Literature.
Priscilla Guglielmo, Francesca Marturano, +3 authors, Laura Evangelista.
Cancers (Basel), 2021 Dec 11; 13(23). PMID: 34885135    Free PMC article.
Review.
Non-conventional and Investigational PET Radiotracers for Breast Cancer: A Systematic Review.
Michele Balma, Virginia Liberini, +15 authors, Désirée Deandreis.
Front Med (Lausanne), 2022 May 03; 9. PMID: 35492341    Free PMC article.
Systematic Review.