A digital score of peri‐epithelial lymphocytic activity predicts malignant transformation in oral epithelial dysplasia

Author:

Bashir Raja Muhammad Saad1ORCID,Shephard Adam J1ORCID,Mahmood Hanya23,Azarmehr Neda3,Raza Shan E Ahmed1,Khurram Syed Ali23ORCID,Rajpoot Nasir M1ORCID

Affiliation:

1. Tissue Image Analytics Centre, Department of Computer Science University of Warwick Coventry UK

2. Academic Unit of Oral & Maxillofacial Surgery, School of Clinical Dentistry University of Sheffield Sheffield UK

3. Unit of Oral & Maxillofacial Pathology, School of Clinical Dentistry University of Sheffield Sheffield UK

Abstract

AbstractOral squamous cell carcinoma (OSCC) is amongst the most common cancers, with more than 377,000 new cases worldwide each year. OSCC prognosis remains poor, related to cancer presentation at a late stage, indicating the need for early detection to improve patient prognosis. OSCC is often preceded by a premalignant state known as oral epithelial dysplasia (OED), which is diagnosed and graded using subjective histological criteria leading to variability and prognostic unreliability. In this work, we propose a deep learning approach for the development of prognostic models for malignant transformation and their association with clinical outcomes in histology whole slide images (WSIs) of OED tissue sections. We train a weakly supervised method on OED cases (n = 137) with malignant transformation (n = 50) and mean malignant transformation time of 6.51 years (±5.35 SD). Stratified five‐fold cross‐validation achieved an average area under the receiver‐operator characteristic curve (AUROC) of 0.78 for predicting malignant transformation in OED. Hotspot analysis revealed various features of nuclei in the epithelium and peri‐epithelial tissue to be significant prognostic factors for malignant transformation, including the count of peri‐epithelial lymphocytes (PELs) (p < 0.05), epithelial layer nuclei count (NC) (p < 0.05), and basal layer NC (p < 0.05). Progression‐free survival (PFS) using the epithelial layer NC (p < 0.05, C‐index = 0.73), basal layer NC (p < 0.05, C‐index = 0.70), and PELs count (p < 0.05, C‐index = 0.73) all showed association of these features with a high risk of malignant transformation in our univariate analysis. Our work shows the application of deep learning for the prognostication and prediction of PFS of OED for the first time and offers potential to aid patient management. Further evaluation and testing on multi‐centre data is required for validation and translation to clinical practice. © 2023 The Authors. The Journal of Pathology published by John Wiley & Sons Ltd on behalf of The Pathological Society of Great Britain and Ireland.

Funder

University of Warwick

Cancer Research UK

Publisher

Wiley

Subject

Pathology and Forensic Medicine

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