Immune and gene-expression profiling in estrogen receptor low and negative early breast cancer

J Natl Cancer Inst. 2024 Dec 1;116(12):1914-1927. doi: 10.1093/jnci/djae178.

Abstract

Background: The cutoff of <1% positive cells to define estrogen receptor (ER) negativity by immunohistochemistry (IHC) in breast cancer (BC) is debated. We explored the tumor immune microenvironment and gene-expression profile of patients with early-stage HER2-negative ER-low (ER 1%-9%) BC, comparing them to ER-negative (ER <1%) and ER-intermediate (ER 10%-50%) tumors.

Methods: Among 921 patients with early-stage I-III, ER ≤50%, HER2-negative BCs, tumors were classified as ER-negative (n = 712), ER-low (n = 128), or ER-intermediate (n = 81). Tumor-infiltrating lymphocytes (TILs) were evaluated. CD8+, FOXP3+ cells, and PD-L1 status were assessed by IHC and quantified by digital pathology. We analyzed 776 BC-related genes in 116 samples. All tests were 2-sided at a <.05 significance level.

Results: ER-low and ER-negative tumors exhibited similar median TILs, statistically significantly higher than ER-intermediate tumors. CD8/FOXP3 ratio and PD-L1 positivity rates were comparable between ER-low and ER-negative groups. These groups showed similar enrichment in basal-like intrinsic subtypes and comparable expression of immune-related genes. ER-low and ER-intermediate tumors showed significant transcriptomic differences. High TILs (≥30%) were associated with improved relapse-free survival (RFS) in ER-low (5-year RFS 78.6% vs 66.2%, log-rank P = .033, hazard ratio [HR] 0.37 [95% CI = 0.15 to 0.96]) and ER-negative patients (5-year RFS 85.2% vs 69.8%, log-rank P < .001, HR 0.41 [95% CI = 0.27 to 0.60]).

Conclusions: ER-low and ER-negative tumors are similar biological and molecular entities, supporting their comparable clinical outcomes and treatment responses, including to immunotherapy. Our findings contribute to the growing evidence calling for a reevaluation of ER-positive BC classification and management, aligning ER-low and ER-negative tumors more closely.

MeSH terms

  • Adult
  • Aged
  • B7-H1 Antigen / analysis
  • B7-H1 Antigen / genetics
  • B7-H1 Antigen / metabolism
  • Biomarkers, Tumor* / genetics
  • Biomarkers, Tumor* / metabolism
  • Breast Neoplasms* / genetics
  • Breast Neoplasms* / immunology
  • Breast Neoplasms* / mortality
  • Breast Neoplasms* / pathology
  • Female
  • Forkhead Transcription Factors / genetics
  • Forkhead Transcription Factors / metabolism
  • Gene Expression Profiling*
  • Gene Expression Regulation, Neoplastic
  • Humans
  • Immunohistochemistry
  • Lymphocytes, Tumor-Infiltrating* / immunology
  • Middle Aged
  • Neoplasm Staging
  • Prognosis
  • Receptor, ErbB-2 / analysis
  • Receptor, ErbB-2 / metabolism
  • Receptors, Estrogen* / analysis
  • Receptors, Estrogen* / metabolism
  • Transcriptome
  • Tumor Microenvironment* / immunology

Substances

  • Receptors, Estrogen
  • Biomarkers, Tumor
  • B7-H1 Antigen
  • Receptor, ErbB-2
  • CD274 protein, human
  • FOXP3 protein, human
  • Forkhead Transcription Factors