Immune-related adverse events in the gastrointestinal tract: diagnostic utility of upper gastrointestinal biopsies

Histopathology. 2020 Jan;76(2):233-243. doi: 10.1111/his.13963. Epub 2019 Nov 13.

Abstract

Aims: Immune checkpoint inhibitors (ICIs) improve survival across a range of malignancies but are also associated with a spectrum of gastrointestinal (GI) immune-related adverse events (GI-irAEs). The aims of this study were to explore the diagnostic value of gastric and duodenal biopsies and to address considerations in the differential diagnosis.

Methods and results: We identified 39 patients who were treated with ICIs and had a subsequent upper GI biopsy. We recorded clinical data and endoscopic findings, and reviewed their gastric, duodenal and colonic biopsies. Twenty-one (54%) patients were treated with an anti-programmed cell death protein 1 (PD-1)/anti-programmed cell death ligand 1 antibody alone, and 17 (44%) patients were treated with a combination of anti-cytotoxic T-lymphocyte-associated protein-4 and anti-PD-1 antibodies. Thirty-two (82%) patients presented with diarrhoea. Gastric alterations included periglandular inflammation and granulomas, and duodenal changes included villous blunting, intraepithelial lymphocytosis, granulomas, and neutrophilic activity. We recognised four patterns of colonic injury: (i) acute self-limiting colitis; (ii) lymphocytic colitis; (iii) collagenous colitis; and (iv) apoptosis-only. Twenty-nine (74%) and 10 (26%) patients were diagnosed clinically as positive and negative for GI-irAEs, respectively. Gastric periglandular inflammation (P = 0.004) and an increased number of colonic lamina propria mononuclear cells (P = 0.04) correlated with the clinical diagnosis of a GI-irAE. Histological alterations associated with ICI injury were more often identified in upper GI biopsies (71%) than in colonic biopsies (65%).

Conclusions: The morphological spectrum of ICI-related GI disease is broad, and mimics a range of infectious and inflammatory diseases. Gastric periglandular inflammation represents one of the more characteristic histological features of GI-irAEs. The study underscores the importance of a comprehensive review of upper and lower GI biopsies for the diagnosis of GI-irAEs.

Keywords: CTLA-4; PD-1; checkpoint proteins; gastrointestinal; immune-mediated adverse events.

MeSH terms

  • Adult
  • Aged
  • Aged, 80 and over
  • Antibodies, Monoclonal / adverse effects*
  • Biopsy
  • CTLA-4 Antigen / antagonists & inhibitors*
  • Colitis / diagnosis
  • Colitis / immunology
  • Colitis / pathology
  • Colon / immunology
  • Colon / pathology
  • Diagnosis, Differential
  • Female
  • Gastritis / diagnosis
  • Gastritis / immunology
  • Gastritis / pathology
  • Gastrointestinal Diseases / diagnosis*
  • Gastrointestinal Diseases / immunology
  • Gastrointestinal Diseases / pathology
  • Humans
  • Inflammation / diagnosis*
  • Inflammation / immunology
  • Inflammation / pathology
  • Male
  • Middle Aged
  • Programmed Cell Death 1 Receptor / antagonists & inhibitors*
  • Retrospective Studies
  • Stomach / immunology
  • Stomach / pathology
  • Upper Gastrointestinal Tract / immunology
  • Upper Gastrointestinal Tract / pathology

Substances

  • Antibodies, Monoclonal
  • CTLA-4 Antigen
  • CTLA4 protein, human
  • PDCD1 protein, human
  • Programmed Cell Death 1 Receptor