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@ARTICLE{Scheiner:305098,
author = {B. Scheiner and P. Lombardi and A. D'Alessio and G. Kim and
M. Tafavvoghi and O. Petrenko and R. D. Goldin and C. A. M.
Fulgenzi and A. Torkpour and L. Balcar and F. A. Mauri and
K. Pomej and V. Himmelsbach and M. Barsch and C. Celsa and
G. Cabibbo and J. Cheon and A. Krall and F. Hucke and L. Di
Tommaso and M. Bernasconi and L. Rimassa and A. Samson and
B. Stefanini and B. Mozayani and M. Trauner and C. Lackner
and R. Stauber and F. Vasuri and F. Piscaglia and B. Bengsch
and F. Finkelmeier and M. Peck-Radosavljevic and L.-T.
Rasmussen Busund and T. Marafioti and M. Rahbari$^*$ and M.
Heikenwalder$^*$ and M. Pinter and H. J. Chon and M. Rakaee
and D. J. Pinato},
title = {{P}reliminary qualification of a machine learning-based
assessment of the tumor immune infiltrate as a predictor of
outcome in patients with hepatocellular carcinoma treated
with atezolizumab plus bevacizumab.},
journal = {Journal for ImmunoTherapy of Cancer},
volume = {13},
number = {10},
issn = {2051-1426},
address = {London},
publisher = {BioMed Central},
reportid = {DKFZ-2025-02050},
pages = {e010975},
year = {2025},
abstract = {Spontaneously immunogenic hepatocellular carcinoma (HCC),
identified by a dense immune cell infiltrate (ICI), responds
better to immunotherapy, although no validated biomarker
exists to identify these cases. We used machine learning
(ML) to quantify ICI from standard $H\&E-stained$ tissue and
evaluated its correlation with characteristics of the tumor
microenvironment (TME) and clinical outcome from
atezolizumab plus bevacizumab (A+B).We therefore employed a
supervised ML algorithm on 102 pretreatment $H\&E$ slides
collected from patients treated with A+B. We quantified
tumor, stroma and immune cell counts/mm2 and dichotomized
patients into ICI high and ICI low for clinicopathologic
analysis. We correlated ICI signature with characteristics
of the T-cell infiltrate (CD4+, FOXP3+, CD8+, PD1+) using
multiplex immunohistochemistry in 62 resected specimens and
evaluated gene expression profiles by bulk RNA sequencing in
44 samples.All patients treated with A+B were Child-Pugh A
and received first-line A+B treatment for Barcelona Clinic
Liver Cancer Stage C HCC (n=77, $75.5\%)$ on a background of
viral (n=53, $52\%)$ and non-viral (n=49, $48\%)$ liver
disease. Median ICI density was 429.9 (IQR: 194.6-666.7)
cells/mm2 Two-thirds of patients (n=67, $65.7\%)$ had ICI
counts≥236/mm2, derived as the optimal prognostic cut-off
(ICI-high). Baseline characteristics, including disease
etiology, liver function, performance status, stage, prior
therapy and alpha-fetoprotein (AFP) levels, were comparable
between ICI-high versus ICI-low patients. Patients with
ICI-high demonstrated a significantly longer overall
survival (OS) compared with ICI-low: 20.9 $(95\%$ CI: 13.8
to 27.9) versus 15.3 $(95\%$ CI: 6.0 to 24.6 months,
p=0.026). Multivariable analyses demonstrated ICI-low status
to remain as an independent prognostic parameter (adjusted
HR (aHR): 2.02, $95\%$ CI: 1.03 to 3.96) alongside AFP
concentration (per 100 ng/mL: aHR 1.00, $95\%$ CI: 1.00 to
1.00). ICI-high tumors were characterized by STC1
underexpression and enrichment in proinflammatory gene
expression sets previously associated with response to
immunotherapy. The proinflammatory environment identified by
ICI status was not exclusively mediated by T-cell phenotype
polarization as shown by a lack of correlation between
ICI-high status and CD4+, CD4+FOXP3+, CD8+ and CD8+PD1+
T-cell density.In conclusion, we propose a ML-based
algorithm to identify proinflamed HCC TMEs bearing a
positive correlation with the patient's OS. Digital
characterization of the TME should be validated as a tool to
improve precision delivery of anticancer immunotherapy.},
keywords = {Humans / Carcinoma, Hepatocellular: drug therapy /
Carcinoma, Hepatocellular: immunology / Carcinoma,
Hepatocellular: pathology / Carcinoma, Hepatocellular:
mortality / Liver Neoplasms: drug therapy / Liver Neoplasms:
immunology / Liver Neoplasms: pathology / Liver Neoplasms:
mortality / Bevacizumab: therapeutic use / Bevacizumab:
pharmacology / Male / Female / Antibodies, Monoclonal,
Humanized: therapeutic use / Antibodies, Monoclonal,
Humanized: pharmacology / Machine Learning / Middle Aged /
Antineoplastic Combined Chemotherapy Protocols: therapeutic
use / Antineoplastic Combined Chemotherapy Protocols:
pharmacology / Aged / Tumor Microenvironment: immunology /
Prognosis / Treatment Outcome / Biomarker (Other) /
Hepatocellular Carcinoma (Other) / Immunotherapy (Other) /
Tumor infiltrating lymphocyte - TIL (Other) / Bevacizumab
(NLM Chemicals) / Antibodies, Monoclonal, Humanized (NLM
Chemicals) / atezolizumab (NLM Chemicals)},
cin = {D440},
ddc = {610},
cid = {I:(DE-He78)D440-20160331},
pnm = {314 - Immunologie und Krebs (POF4-314)},
pid = {G:(DE-HGF)POF4-314},
typ = {PUB:(DE-HGF)16},
pubmed = {pmid:41052886},
doi = {10.1136/jitc-2024-010975},
url = {https://inrepo02.dkfz.de/record/305098},
}