Integrative analysis of H&E and IHC identifies prognostic immune subtypes in HPV related oropharyngeal cancer

Abstract Background Deep learning techniques excel at identifying tumor-infiltrating lymphocytes (TILs) and immune phenotypes in hematoxylin and eosin (H&E)-stained slides. However, their ability to elucidate detailed functional characteristics of diverse cellular phenotypes within tumor immune...

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Main Authors: Sumanth Reddy Nakkireddy, Inyeop Jang, Minji Kim, Linda X. Yin, Michael Rivera, Joaquin J. Garcia, Kathleen R. Bartemes, David M. Routman, Eric. J. Moore, Chadi N. Abdel-Halim, Daniel J. Ma, Kathryn M. Van Abel, Tae Hyun Hwang
Format: Article
Language:English
Published: Nature Portfolio 2024-10-01
Series:Communications Medicine
Online Access:https://doi.org/10.1038/s43856-024-00604-w
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author Sumanth Reddy Nakkireddy
Inyeop Jang
Minji Kim
Linda X. Yin
Michael Rivera
Joaquin J. Garcia
Kathleen R. Bartemes
David M. Routman
Eric. J. Moore
Chadi N. Abdel-Halim
Daniel J. Ma
Kathryn M. Van Abel
Tae Hyun Hwang
author_facet Sumanth Reddy Nakkireddy
Inyeop Jang
Minji Kim
Linda X. Yin
Michael Rivera
Joaquin J. Garcia
Kathleen R. Bartemes
David M. Routman
Eric. J. Moore
Chadi N. Abdel-Halim
Daniel J. Ma
Kathryn M. Van Abel
Tae Hyun Hwang
author_sort Sumanth Reddy Nakkireddy
collection DOAJ
description Abstract Background Deep learning techniques excel at identifying tumor-infiltrating lymphocytes (TILs) and immune phenotypes in hematoxylin and eosin (H&E)-stained slides. However, their ability to elucidate detailed functional characteristics of diverse cellular phenotypes within tumor immune microenvironment (TME) is limited. We aimed to enhance our understanding of cellular composition and functional characteristics across TME regions and improve patient stratification by integrating H&E with adjacent immunohistochemistry (IHC) images. Methods A retrospective study was conducted on patients with Human Papillomavirus-positive oropharyngeal squamous cell carcinoma (OPSCC). Using paired H&E and IHC slides for 11 proteins, a deep learning pipeline was used to quantify tumor, stroma, and TILs in the TME. Patients were classified into immune inflamed (IN), immune excluded (IE), or immune desert (ID) phenotypes. By registering the IHC and H&E slides, we integrated IHC data to capture protein expression in the corresponding tumor regions. We further stratified patients into specific immune subtypes, such as IN, with increased or reduced CD8+ cells, based on the abundance of these proteins. This characterization provided functional insight into the H&E-based subtypes. Results Analysis of 88 primary tumors and 70 involved lymph node tissue images reveals an improved prognosis in patients classified as IN in primary tumors with high CD8 and low CD163 expression (p = 0.007). Multivariate Cox regression analysis confirms a significantly better prognosis for these subtypes. Conclusions Integrating H&E and IHC data enhances the functional characterization of immune phenotypes of the TME with biological interpretability, and improves patient stratification in HPV( + ) OPSCC.
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spelling doaj-art-3f1e8d33b96a4fab90e7deab9a6573352025-08-20T03:09:19ZengNature PortfolioCommunications Medicine2730-664X2024-10-014111010.1038/s43856-024-00604-wIntegrative analysis of H&E and IHC identifies prognostic immune subtypes in HPV related oropharyngeal cancerSumanth Reddy Nakkireddy0Inyeop Jang1Minji Kim2Linda X. Yin3Michael Rivera4Joaquin J. Garcia5Kathleen R. Bartemes6David M. Routman7Eric. J. Moore8Chadi N. Abdel-Halim9Daniel J. Ma10Kathryn M. Van Abel11Tae Hyun Hwang12Department of Artificial Intelligence and Informatics, Mayo ClinicDepartment of Artificial Intelligence and Informatics, Mayo ClinicDepartment of Artificial Intelligence and Informatics, Mayo ClinicDepartment of Otolaryngology-Head and Neck Surgery, Mayo ClinicDepartment of Laboratory Medicine and Pathology, Mayo ClinicDepartment of Laboratory Medicine and Pathology, Mayo ClinicDepartment of Otolaryngology-Head and Neck Surgery, Mayo ClinicDepartment of Radiation Oncology, Mayo ClinicDepartment of Artificial Intelligence and Informatics, Mayo ClinicDepartment of Otolaryngology-Head and Neck Surgery, Mayo ClinicDepartment of Radiation Oncology, Mayo ClinicDepartment of Laboratory Medicine and Pathology, Mayo ClinicDepartment of Artificial Intelligence and Informatics, Mayo ClinicAbstract Background Deep learning techniques excel at identifying tumor-infiltrating lymphocytes (TILs) and immune phenotypes in hematoxylin and eosin (H&E)-stained slides. However, their ability to elucidate detailed functional characteristics of diverse cellular phenotypes within tumor immune microenvironment (TME) is limited. We aimed to enhance our understanding of cellular composition and functional characteristics across TME regions and improve patient stratification by integrating H&E with adjacent immunohistochemistry (IHC) images. Methods A retrospective study was conducted on patients with Human Papillomavirus-positive oropharyngeal squamous cell carcinoma (OPSCC). Using paired H&E and IHC slides for 11 proteins, a deep learning pipeline was used to quantify tumor, stroma, and TILs in the TME. Patients were classified into immune inflamed (IN), immune excluded (IE), or immune desert (ID) phenotypes. By registering the IHC and H&E slides, we integrated IHC data to capture protein expression in the corresponding tumor regions. We further stratified patients into specific immune subtypes, such as IN, with increased or reduced CD8+ cells, based on the abundance of these proteins. This characterization provided functional insight into the H&E-based subtypes. Results Analysis of 88 primary tumors and 70 involved lymph node tissue images reveals an improved prognosis in patients classified as IN in primary tumors with high CD8 and low CD163 expression (p = 0.007). Multivariate Cox regression analysis confirms a significantly better prognosis for these subtypes. Conclusions Integrating H&E and IHC data enhances the functional characterization of immune phenotypes of the TME with biological interpretability, and improves patient stratification in HPV( + ) OPSCC.https://doi.org/10.1038/s43856-024-00604-w
spellingShingle Sumanth Reddy Nakkireddy
Inyeop Jang
Minji Kim
Linda X. Yin
Michael Rivera
Joaquin J. Garcia
Kathleen R. Bartemes
David M. Routman
Eric. J. Moore
Chadi N. Abdel-Halim
Daniel J. Ma
Kathryn M. Van Abel
Tae Hyun Hwang
Integrative analysis of H&E and IHC identifies prognostic immune subtypes in HPV related oropharyngeal cancer
Communications Medicine
title Integrative analysis of H&E and IHC identifies prognostic immune subtypes in HPV related oropharyngeal cancer
title_full Integrative analysis of H&E and IHC identifies prognostic immune subtypes in HPV related oropharyngeal cancer
title_fullStr Integrative analysis of H&E and IHC identifies prognostic immune subtypes in HPV related oropharyngeal cancer
title_full_unstemmed Integrative analysis of H&E and IHC identifies prognostic immune subtypes in HPV related oropharyngeal cancer
title_short Integrative analysis of H&E and IHC identifies prognostic immune subtypes in HPV related oropharyngeal cancer
title_sort integrative analysis of h e and ihc identifies prognostic immune subtypes in hpv related oropharyngeal cancer
url https://doi.org/10.1038/s43856-024-00604-w
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