Immune activation by DNA damage predicts response to chemotherapy and survival in oesophageal adenocarcinoma

Gut. 2019 Nov;68(11):1918-1927. doi: 10.1136/gutjnl-2018-317624. Epub 2019 Mar 9.

Abstract

Objective: Current strategies to guide selection of neoadjuvant therapy in oesophageal adenocarcinoma (OAC) are inadequate. We assessed the ability of a DNA damage immune response (DDIR) assay to predict response following neoadjuvant chemotherapy in OAC.

Design: Transcriptional profiling of 273 formalin-fixed paraffin-embedded prechemotherapy endoscopic OAC biopsies was performed. All patients were treated with platinum-based neoadjuvant chemotherapy and resection between 2003 and 2014 at four centres in the Oesophageal Cancer Clinical and Molecular Stratification consortium. CD8 and programmed death ligand 1 (PD-L1) immunohistochemical staining was assessed in matched resection specimens from 126 cases. Kaplan-Meier and Cox proportional hazards regression analysis were applied according to DDIR status for recurrence-free survival (RFS) and overall survival (OS).

Results: A total of 66 OAC samples (24%) were DDIR positive with the remaining 207 samples (76%) being DDIR negative. DDIR assay positivity was associated with improved RFS (HR: 0.61; 95% CI 0.38 to 0.98; p=0.042) and OS (HR: 0.52; 95% CI 0.31 to 0.88; p=0.015) following multivariate analysis. DDIR-positive patients had a higher pathological response rate (p=0.033), lower nodal burden (p=0.026) and reduced circumferential margin involvement (p=0.007). No difference in OS was observed according to DDIR status in an independent surgery-alone dataset.DDIR-positive OAC tumours were also associated with the presence of CD8+ lymphocytes (intratumoural: p<0.001; stromal: p=0.026) as well as PD-L1 expression (intratumoural: p=0.047; stromal: p=0.025).

Conclusion: The DDIR assay is strongly predictive of benefit from DNA-damaging neoadjuvant chemotherapy followed by surgical resection and is associated with a proinflammatory microenvironment in OAC.

Keywords: Dna damage; chemotherapy; immune response; oesophageal cancer.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenocarcinoma / immunology*
  • Adenocarcinoma / mortality
  • Adenocarcinoma / therapy*
  • Aged
  • Antineoplastic Agents / therapeutic use*
  • B7-H1 Antigen
  • CD8-Positive T-Lymphocytes
  • Chemotherapy, Adjuvant
  • DNA Damage / immunology*
  • Disease-Free Survival
  • Esophageal Neoplasms / immunology*
  • Esophageal Neoplasms / mortality
  • Esophageal Neoplasms / therapy*
  • Esophagectomy*
  • Female
  • Humans
  • Male
  • Middle Aged
  • Neoadjuvant Therapy*
  • Predictive Value of Tests
  • Survival Rate
  • Treatment Outcome

Substances

  • Antineoplastic Agents
  • B7-H1 Antigen
  • CD274 protein, human

Supplementary concepts

  • Adenocarcinoma Of Esophagus