Use of Molecular Tools to Identify Patients With Indolent Breast Cancers With Ultralow Risk Over 2 Decades

JAMA Oncol. 2017 Nov 1;3(11):1503-1510. doi: 10.1001/jamaoncol.2017.1261.

Abstract

Importance: The frequency of cancers with indolent behavior has increased with screening. Better tools to identify indolent tumors are needed to avoid overtreatment.

Objective: To determine if a multigene classifier is associated with indolent behavior of invasive breast cancers in women followed for 2 decades.

Design, setting, and participants: This is a secondary analysis of a randomized clinical trial of tamoxifen vs no systemic therapy, with more than 20-year follow-up. An indolent threshold (ultralow risk) of the US Food and Drug Administration-cleared MammaPrint 70-gene expression score was established above which no breast cancer deaths occurred after 15 years in the absence of systemic therapy. Immunohistochemical markers (n = 727 women) and Agilent microarrays, for MammaPrint risk scoring (n = 652 women), were performed from formalin-fixed paraffin-embedded primary tumor blocks. Participants were postmenopausal women with clinically detected node-negative breast cancers treated with mastectomy or lumpectomy and radiation enrolled in the Stockholm tamoxifen (STO-3) trial, 1976 to 1990.

Exposures: After 2 years of tamoxifen vs no systemic therapy, regardless of hormone receptor status, patients without relapse who reconsented were further randomized to 3 additional years or none.

Main outcomes and measures: Breast cancer-specific survival assessed by Kaplan-Meier analyses and multivariate Cox proportional hazard modeling, adjusted for treatment, patient age, year of diagnosis, tumor size, grade, hormone receptors, and ERBB2/HER2 and Ki67 status.

Results: In this secondary analysis of node-negative postmenopausal women, conducted in the era before mammography screening, among the 652 women with MammaPrint scoring available (median age, 62.8 years of age), 377 (58%) and 275 (42%) were MammaPrint low and high risk, respectively, while 98 (15%) were ultralow risk. At 20 years, women with 70-gene high and low tumors but not ultralow tumors had a significantly higher risk of disease-specific death compared with ultralow-risk patients by Cox analysis (hazard ratios, 4.73 [95% CI, 1.38-16.22] and 4.54 [95% CI, 1.40-14.80], respectively). There were no deaths in the ultralow-risk tamoxifen-treated arm at 15 years, and these patients had a 20-year disease-specific survival rate of 97%, whereas for untreated patients the survival rate was 94%. Recursive partitioning identified ultralow risk as the most significant predictor of good outcome. In tumors "not ultralow risk," tumor size greater than 2 cm was the most predictive of outcome.

Conclusions and relevance: The ultralow-risk threshold of the 70-gene MammaPrint assay can identify patients whose long-term systemic risk of death from breast cancer after surgery alone is exceedingly low.

Publication types

  • Randomized Controlled Trial

MeSH terms

  • Antineoplastic Agents, Hormonal / therapeutic use
  • Biomarkers, Tumor / analysis
  • Biomarkers, Tumor / genetics*
  • Breast Neoplasms / chemistry
  • Breast Neoplasms / genetics*
  • Breast Neoplasms / mortality
  • Breast Neoplasms / therapy
  • Chemotherapy, Adjuvant
  • Disease-Free Survival
  • Female
  • Gene Expression Profiling / methods*
  • Humans
  • Immunohistochemistry
  • Kaplan-Meier Estimate
  • Mastectomy
  • Mastectomy, Segmental
  • Middle Aged
  • Multivariate Analysis
  • Oligonucleotide Array Sequence Analysis*
  • Predictive Value of Tests
  • Proportional Hazards Models
  • Radiotherapy, Adjuvant
  • Risk Assessment
  • Risk Factors
  • Sweden
  • Tamoxifen / therapeutic use
  • Time Factors
  • Transcriptome*
  • Treatment Outcome
  • Tumor Burden

Substances

  • Antineoplastic Agents, Hormonal
  • Biomarkers, Tumor
  • Tamoxifen