An Imaging Biomarker of Tumor-Infiltrating Lymphocytes to Risk-Stratify Patients With HPV-Associated Oropharyngeal Cancer.


Journal

Journal of the National Cancer Institute
ISSN: 1460-2105
Titre abrégé: J Natl Cancer Inst
Pays: United States
ID NLM: 7503089

Informations de publication

Date de publication:
11 04 2022
Historique:
received: 18 05 2021
revised: 03 08 2021
accepted: 19 11 2021
pubmed: 2 12 2021
medline: 14 4 2022
entrez: 1 12 2021
Statut: ppublish

Résumé

Human papillomavirus (HPV)-associated oropharyngeal squamous cell carcinoma (OPSCC) has excellent control rates compared to nonvirally associated OPSCC. Multiple trials are actively testing whether de-escalation of treatment intensity for these patients can maintain oncologic equipoise while reducing treatment-related toxicity. We have developed OP-TIL, a biomarker that characterizes the spatial interplay between tumor-infiltrating lymphocytes (TILs) and surrounding cells in histology images. Herein, we sought to test whether OP-TIL can segregate stage I HPV-associated OPSCC patients into low-risk and high-risk groups and aid in patient selection for de-escalation clinical trials. Association between OP-TIL and patient outcome was explored on whole slide hematoxylin and eosin images from 439 stage I HPV-associated OPSCC patients across 6 institutional cohorts. One institutional cohort (n = 94) was used to identify the most prognostic features and train a Cox regression model to predict risk of recurrence and death. Survival analysis was used to validate the algorithm as a biomarker of recurrence or death in the remaining 5 cohorts (n = 345). All statistical tests were 2-sided. OP-TIL separated stage I HPV-associated OPSCC patients with 30 or less pack-year smoking history into low-risk (2-year disease-free survival [DFS] = 94.2%; 5-year DFS = 88.4%) and high-risk (2-year DFS = 82.5%; 5-year DFS = 74.2%) groups (hazard ratio = 2.56, 95% confidence interval = 1.52 to 4.32; P < .001), even after adjusting for age, smoking status, T and N classification, and treatment modality on multivariate analysis for DFS (hazard ratio = 2.27, 95% confidence interval = 1.32 to 3.94; P = .003). OP-TIL can identify stage I HPV-associated OPSCC patients likely to be poor candidates for treatment de-escalation. Following validation on previously completed multi-institutional clinical trials, OP-TIL has the potential to be a biomarker, beyond clinical stage and HPV status, that can be used clinically to optimize patient selection for de-escalation.

Sections du résumé

BACKGROUND
Human papillomavirus (HPV)-associated oropharyngeal squamous cell carcinoma (OPSCC) has excellent control rates compared to nonvirally associated OPSCC. Multiple trials are actively testing whether de-escalation of treatment intensity for these patients can maintain oncologic equipoise while reducing treatment-related toxicity. We have developed OP-TIL, a biomarker that characterizes the spatial interplay between tumor-infiltrating lymphocytes (TILs) and surrounding cells in histology images. Herein, we sought to test whether OP-TIL can segregate stage I HPV-associated OPSCC patients into low-risk and high-risk groups and aid in patient selection for de-escalation clinical trials.
METHODS
Association between OP-TIL and patient outcome was explored on whole slide hematoxylin and eosin images from 439 stage I HPV-associated OPSCC patients across 6 institutional cohorts. One institutional cohort (n = 94) was used to identify the most prognostic features and train a Cox regression model to predict risk of recurrence and death. Survival analysis was used to validate the algorithm as a biomarker of recurrence or death in the remaining 5 cohorts (n = 345). All statistical tests were 2-sided.
RESULTS
OP-TIL separated stage I HPV-associated OPSCC patients with 30 or less pack-year smoking history into low-risk (2-year disease-free survival [DFS] = 94.2%; 5-year DFS = 88.4%) and high-risk (2-year DFS = 82.5%; 5-year DFS = 74.2%) groups (hazard ratio = 2.56, 95% confidence interval = 1.52 to 4.32; P < .001), even after adjusting for age, smoking status, T and N classification, and treatment modality on multivariate analysis for DFS (hazard ratio = 2.27, 95% confidence interval = 1.32 to 3.94; P = .003).
CONCLUSIONS
OP-TIL can identify stage I HPV-associated OPSCC patients likely to be poor candidates for treatment de-escalation. Following validation on previously completed multi-institutional clinical trials, OP-TIL has the potential to be a biomarker, beyond clinical stage and HPV status, that can be used clinically to optimize patient selection for de-escalation.

Identifiants

pubmed: 34850048
pii: 6446037
doi: 10.1093/jnci/djab215
pmc: PMC9002277
doi:

Substances chimiques

Biomarkers 0

Types de publication

Journal Article Research Support, U.S. Gov't, Non-P.H.S. Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

609-617

Subventions

Organisme : NCI NIH HHS
ID : T32 CA094186
Pays : United States
Organisme : NCRR NIH HHS
ID : C06 RR012463
Pays : United States
Organisme : NCI NIH HHS
ID : P30 CA125123
Pays : United States
Organisme : BLRD VA
ID : I01 BX004121
Pays : United States
Organisme : NIBIB NIH HHS
ID : R43 EB028736
Pays : United States
Organisme : NCI NIH HHS
ID : U54 CA254566
Pays : United States
Organisme : CSRD VA
ID : IK2 CX001953
Pays : United States
Organisme : NIDCD NIH HHS
ID : T32 DC000027
Pays : United States

Informations de copyright

© The Author(s) 2021. Published by Oxford University Press.

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Auteurs

Germán Corredor (G)

Department of Biomedical Engineering, Center of Computational Imaging and Personalized Diagnostics, Case Western Reserve University, Cleveland, OH, USA.
Louis Stokes Cleveland VA Medical Center, Cleveland, OH, USA.

Paula Toro (P)

Department of Biomedical Engineering, Center of Computational Imaging and Personalized Diagnostics, Case Western Reserve University, Cleveland, OH, USA.

Can Koyuncu (C)

Department of Biomedical Engineering, Center of Computational Imaging and Personalized Diagnostics, Case Western Reserve University, Cleveland, OH, USA.

Cheng Lu (C)

Department of Biomedical Engineering, Center of Computational Imaging and Personalized Diagnostics, Case Western Reserve University, Cleveland, OH, USA.

Christina Buzzy (C)

Department of Biomedical Engineering, Center of Computational Imaging and Personalized Diagnostics, Case Western Reserve University, Cleveland, OH, USA.

Kaustav Bera (K)

Department of Biomedical Engineering, Center of Computational Imaging and Personalized Diagnostics, Case Western Reserve University, Cleveland, OH, USA.

Pingfu Fu (P)

Department of Population and Quantitative Health Sciences, Case Western Reserve University, Cleveland, OH, USA.

Mitra Mehrad (M)

Department of Pathology, Microbiology and Immunology, Vanderbilt University Medical Center, Nashville, TN, USA.

Kim A Ely (KA)

Department of Pathology, Microbiology and Immunology, Vanderbilt University Medical Center, Nashville, TN, USA.

Mojgan Mokhtari (M)

Department of Biomedical Engineering, Center of Computational Imaging and Personalized Diagnostics, Case Western Reserve University, Cleveland, OH, USA.

Kailin Yang (K)

Department of Radiation Oncology, Cleveland Clinic, Cleveland, OH, USA.

Deborah Chute (D)

Department of Anatomic Pathology, Cleveland Clinic, Cleveland, OH, USA.

David J Adelstein (DJ)

Department of Medicine, School of Medicine, Case Western Reserve University, Cleveland, OH, USA.

Lester D R Thompson (LDR)

Department of Pathology, Southern California Permanente Medical Group, Woodland Hills, CA, USA.

Justin A Bishop (JA)

Department of Pathology, University of Texas Southwestern Medical Center, Dallas, TX, USA.

Farhoud Faraji (F)

Division of Otolaryngology-Head and Neck Surgery, Department of Surgery, UC San Diego Health, La Jolla, CA, USA.

Wade Thorstad (W)

Department of Radiation Oncology, Washington University in St. Louis, St. Louis, MS, USA.

Patricia Castro (P)

Department of Pathology and Immunology, Baylor College of Medicine, Houston, TX, USA.

Vlad Sandulache (V)

Department of Otolaryngology-Head and Neck Surgery, Baylor College of Medicine, Houston, TX, USA.
ENT Section, Operative Care Line, Michael E. DeBakey Veterans Affairs Medical Center, Houston, TX, USA.
Center for Translational Research on Inflammatory Disease (CTRID), Michael E. DeBakey Veterans Affairs Medical Center, Houston, TX, USA.

Shlomo A Koyfman (SA)

Department of Radiation Oncology, Cleveland Clinic, Cleveland, OH, USA.

James S Lewis (JS)

Department of Pathology, Microbiology and Immunology, Vanderbilt University Medical Center, Nashville, TN, USA.

Anant Madabhushi (A)

Department of Biomedical Engineering, Center of Computational Imaging and Personalized Diagnostics, Case Western Reserve University, Cleveland, OH, USA.
Louis Stokes Cleveland VA Medical Center, Cleveland, OH, USA.

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