A 5-Hydroxymethylcytosine-Based Noninvasive Model for Early Detection of Colorectal Carcinomas and Advanced Adenomas: The METHOD-2 Study

Clin Cancer Res. 2024 Aug 1;30(15):3337-3348. doi: 10.1158/1078-0432.CCR-24-0199.

Abstract

Purpose: Detection of colorectal carcinomas at a time when there are more treatment options is associated with better outcomes. This prospective case-control study assessed the 5-hydroxymethylcytosine (5hmC) biomarkers in circulating cell-free DNA (cfDNA) for early detection of colorectal carcinoma and advanced adenomas (AA).

Experimental design: Plasma cfDNA samples from 2,576 study participants from the multicenter METHOD-2 study (NCT03676075) were collected, comprising patients with newly diagnosed colorectal carcinoma (n = 1,074), AA (n = 356), other solid tumors (n = 80), and non-colorectal carcinoma/AA controls (n = 1,066), followed by genome-wide 5hmC profiling using the 5hmC-Seal technique and the next-generation sequencing. A weighted diagnostic model for colorectal carcinoma (stage I-III) and AA was developed using the elastic net regularization in a discovery set and validated in independent samples.

Results: Distribution of 5hmC in cfDNA reflected gene regulatory relevance and tissue of origin. Besides being confirmed in internal validation, a 96-gene model achieved an area under the curve (AUC) of 90.7% for distinguishing stage I-III colorectal carcinoma from controls in 321 samples from multiple centers for external validation, regardless of primary location or mutation status. This model also showed cancer-type specificity as well as high capacity for distinguishing AA from controls with an AUC of 78.6%. Functionally, differential 5hmC features associated with colorectal carcinoma and AA demonstrated relevance to colorectal carcinoma biology, including pathways such as calcium and MAPK signaling.

Conclusions: Genome-wide mapping of 5hmC in cfDNA shows promise as a highly sensitive and specific noninvasive blood test to be integrated into screening programs for improving early detection of colorectal carcinoma and high-risk AA.

Publication types

  • Multicenter Study

MeSH terms

  • 5-Methylcytosine* / analogs & derivatives
  • 5-Methylcytosine* / analysis
  • 5-Methylcytosine* / metabolism
  • Adenoma* / blood
  • Adenoma* / diagnosis
  • Adenoma* / genetics
  • Adenoma* / pathology
  • Adult
  • Aged
  • Biomarkers, Tumor* / blood
  • Biomarkers, Tumor* / genetics
  • Case-Control Studies
  • Cell-Free Nucleic Acids / blood
  • Cell-Free Nucleic Acids / genetics
  • Colorectal Neoplasms* / blood
  • Colorectal Neoplasms* / diagnosis
  • Colorectal Neoplasms* / genetics
  • Colorectal Neoplasms* / pathology
  • DNA Methylation
  • Early Detection of Cancer* / methods
  • Female
  • Humans
  • Male
  • Middle Aged
  • Neoplasm Staging
  • Prospective Studies

Substances

  • 5-hydroxymethylcytosine
  • 5-Methylcytosine
  • Biomarkers, Tumor
  • Cell-Free Nucleic Acids