CT radiomic signature predicts survival and chemotherapy benefit in stage I and II HPV-associated oropharyngeal carcinoma

Abstract Chemoradiation is a common therapeutic regimen for human papillomavirus (HPV)-associated oropharyngeal squamous cell carcinoma (OPSCC). However, not all patients benefit from chemotherapy, especially patients with low-risk characteristics. We aim to develop and validate a prognostic and pre...

Full description

Bibliographic Details
Main Authors: Bolin Song, Kailin Yang, Vidya Sankar Viswanathan, Xiangxue Wang, Jonathan Lee, Sarah Stock, Pingfu Fu, Cheng Lu, Shlomo Koyfman, James S. Lewis, Anant Madabhushi
Format: Article
Language:English
Published: Nature Portfolio 2023-06-01
Series:npj Precision Oncology
Online Access:https://doi.org/10.1038/s41698-023-00404-w
_version_ 1827608119480418304
author Bolin Song
Kailin Yang
Vidya Sankar Viswanathan
Xiangxue Wang
Jonathan Lee
Sarah Stock
Pingfu Fu
Cheng Lu
Shlomo Koyfman
James S. Lewis
Anant Madabhushi
author_facet Bolin Song
Kailin Yang
Vidya Sankar Viswanathan
Xiangxue Wang
Jonathan Lee
Sarah Stock
Pingfu Fu
Cheng Lu
Shlomo Koyfman
James S. Lewis
Anant Madabhushi
author_sort Bolin Song
collection DOAJ
description Abstract Chemoradiation is a common therapeutic regimen for human papillomavirus (HPV)-associated oropharyngeal squamous cell carcinoma (OPSCC). However, not all patients benefit from chemotherapy, especially patients with low-risk characteristics. We aim to develop and validate a prognostic and predictive radiomic image signature (pRiS) to inform survival and chemotherapy benefit using computed tomography (CT) scans from 491 stage I and II HPV-associated OPSCC, which were divided into three cohorts D1–D3. The prognostic performance of pRiS was evaluated on two test sets (D2, n = 162; D3, n = 269) using concordance index. Patients from D2 and D3 who received either radiotherapy alone or chemoradiation were used to validate pRiS as predictive of added benefit of chemotherapy. Seven features were selected to construct pRiS, which was found to be prognostic of overall survival (OS) on univariate analysis in D2 (hazard ratio [HR] = 2.14, 95% confidence interval [CI], 1.1–4.16, p = 0.02) and D3 (HR = 2.74, 95% CI, 1.34–5.62, p = 0.006). Chemotherapy was associated with improved OS for high-pRiS patients in D2 (radiation vs chemoradiation, HR = 4.47, 95% CI, 1.73–11.6, p = 0.002) and D3 (radiation vs chemoradiation, HR = 2.99, 95% CI, 1.04–8.63, p = 0.04). In contrast, chemotherapy did not improve OS for low-pRiS patients, which indicates these patients did not derive additional benefit from chemotherapy and could be considered for treatment de-escalation. The proposed radiomic signature was prognostic of patient survival and informed benefit from chemotherapy for stage I and II HPV-associated OPSCC patients.
first_indexed 2024-03-09T07:05:19Z
format Article
id doaj.art-9af0373870a44d73b434824de5ed0858
institution Directory Open Access Journal
issn 2397-768X
language English
last_indexed 2024-03-09T07:05:19Z
publishDate 2023-06-01
publisher Nature Portfolio
record_format Article
series npj Precision Oncology
spelling doaj.art-9af0373870a44d73b434824de5ed08582023-12-03T09:39:57ZengNature Portfolionpj Precision Oncology2397-768X2023-06-017111310.1038/s41698-023-00404-wCT radiomic signature predicts survival and chemotherapy benefit in stage I and II HPV-associated oropharyngeal carcinomaBolin Song0Kailin Yang1Vidya Sankar Viswanathan2Xiangxue Wang3Jonathan Lee4Sarah Stock5Pingfu Fu6Cheng Lu7Shlomo Koyfman8James S. Lewis9Anant Madabhushi10Center for Computational Imaging and Personalized Diagnostics, Emory UniversityDepartment of Radiation Oncology, Taussig Cancer Center, Cleveland ClinicCenter for Computational Imaging and Personalized Diagnostics, Emory UniversitySchool of Automation, Nanjing University of Information Science and TechnologyImaging Institute, Cleveland ClinicImaging Institute, Cleveland ClinicDepartment of Population and Quantitative Health Sciences, Case Western Reserve UniversityCenter for Computational Imaging and Personalized Diagnostics, Emory UniversityDepartment of Radiation Oncology, Taussig Cancer Center, Cleveland ClinicDepartment of Pathology, Microbiology, and Immunology, Vanderbilt University Medical CenterCenter for Computational Imaging and Personalized Diagnostics, Emory UniversityAbstract Chemoradiation is a common therapeutic regimen for human papillomavirus (HPV)-associated oropharyngeal squamous cell carcinoma (OPSCC). However, not all patients benefit from chemotherapy, especially patients with low-risk characteristics. We aim to develop and validate a prognostic and predictive radiomic image signature (pRiS) to inform survival and chemotherapy benefit using computed tomography (CT) scans from 491 stage I and II HPV-associated OPSCC, which were divided into three cohorts D1–D3. The prognostic performance of pRiS was evaluated on two test sets (D2, n = 162; D3, n = 269) using concordance index. Patients from D2 and D3 who received either radiotherapy alone or chemoradiation were used to validate pRiS as predictive of added benefit of chemotherapy. Seven features were selected to construct pRiS, which was found to be prognostic of overall survival (OS) on univariate analysis in D2 (hazard ratio [HR] = 2.14, 95% confidence interval [CI], 1.1–4.16, p = 0.02) and D3 (HR = 2.74, 95% CI, 1.34–5.62, p = 0.006). Chemotherapy was associated with improved OS for high-pRiS patients in D2 (radiation vs chemoradiation, HR = 4.47, 95% CI, 1.73–11.6, p = 0.002) and D3 (radiation vs chemoradiation, HR = 2.99, 95% CI, 1.04–8.63, p = 0.04). In contrast, chemotherapy did not improve OS for low-pRiS patients, which indicates these patients did not derive additional benefit from chemotherapy and could be considered for treatment de-escalation. The proposed radiomic signature was prognostic of patient survival and informed benefit from chemotherapy for stage I and II HPV-associated OPSCC patients.https://doi.org/10.1038/s41698-023-00404-w
spellingShingle Bolin Song
Kailin Yang
Vidya Sankar Viswanathan
Xiangxue Wang
Jonathan Lee
Sarah Stock
Pingfu Fu
Cheng Lu
Shlomo Koyfman
James S. Lewis
Anant Madabhushi
CT radiomic signature predicts survival and chemotherapy benefit in stage I and II HPV-associated oropharyngeal carcinoma
npj Precision Oncology
title CT radiomic signature predicts survival and chemotherapy benefit in stage I and II HPV-associated oropharyngeal carcinoma
title_full CT radiomic signature predicts survival and chemotherapy benefit in stage I and II HPV-associated oropharyngeal carcinoma
title_fullStr CT radiomic signature predicts survival and chemotherapy benefit in stage I and II HPV-associated oropharyngeal carcinoma
title_full_unstemmed CT radiomic signature predicts survival and chemotherapy benefit in stage I and II HPV-associated oropharyngeal carcinoma
title_short CT radiomic signature predicts survival and chemotherapy benefit in stage I and II HPV-associated oropharyngeal carcinoma
title_sort ct radiomic signature predicts survival and chemotherapy benefit in stage i and ii hpv associated oropharyngeal carcinoma
url https://doi.org/10.1038/s41698-023-00404-w
work_keys_str_mv AT bolinsong ctradiomicsignaturepredictssurvivalandchemotherapybenefitinstageiandiihpvassociatedoropharyngealcarcinoma
AT kailinyang ctradiomicsignaturepredictssurvivalandchemotherapybenefitinstageiandiihpvassociatedoropharyngealcarcinoma
AT vidyasankarviswanathan ctradiomicsignaturepredictssurvivalandchemotherapybenefitinstageiandiihpvassociatedoropharyngealcarcinoma
AT xiangxuewang ctradiomicsignaturepredictssurvivalandchemotherapybenefitinstageiandiihpvassociatedoropharyngealcarcinoma
AT jonathanlee ctradiomicsignaturepredictssurvivalandchemotherapybenefitinstageiandiihpvassociatedoropharyngealcarcinoma
AT sarahstock ctradiomicsignaturepredictssurvivalandchemotherapybenefitinstageiandiihpvassociatedoropharyngealcarcinoma
AT pingfufu ctradiomicsignaturepredictssurvivalandchemotherapybenefitinstageiandiihpvassociatedoropharyngealcarcinoma
AT chenglu ctradiomicsignaturepredictssurvivalandchemotherapybenefitinstageiandiihpvassociatedoropharyngealcarcinoma
AT shlomokoyfman ctradiomicsignaturepredictssurvivalandchemotherapybenefitinstageiandiihpvassociatedoropharyngealcarcinoma
AT jamesslewis ctradiomicsignaturepredictssurvivalandchemotherapybenefitinstageiandiihpvassociatedoropharyngealcarcinoma
AT anantmadabhushi ctradiomicsignaturepredictssurvivalandchemotherapybenefitinstageiandiihpvassociatedoropharyngealcarcinoma