Comprehensive Intrametastatic Immune Quantification and Major Impact of Immunoscore on Survival

J Natl Cancer Inst. 2018 Jan 1;110(1). doi: 10.1093/jnci/djx123.

Abstract

Background: This study assesses how the metastatic immune landscape is impacting the response to treatment and the outcome of colorectal cancer (CRC) patients.

Methods: Complete curative resection of metastases (n = 441) was performed for two patient cohorts (n = 153). Immune densities were quantified in the center and invasive margin of all metastases. Immunoscore and T and B cell (TB) score were analyzed in relation to radiological and pathological responses and patient's disease-free (DFS) and overall survival (OS) using multivariable Cox proportional hazards models. All statistical tests were two-sided.

Results: The spatial distribution of immune cells within metastases was nonuniform. Patients, as well as metastases of the same patient, had variable immune infiltrates and response to therapy. A beneficial response was statistically significantly associated with increased immune densities. Among all metastases, Immunoscore (I) and TB score evaluated in the least immune-infiltrated metastases were the strongest predictors for DFS and OS (five-year follow-up, Immunoscore: I 3-4: DFS rate = 27.9%, 95% CI = 15.2 to 51.3; vs I 0-1-2: DFS rate = 12.3%, 95% CI = 4.9 to 30.6; HR = 0.45, 95% CI = 0.28 to 0.70, P = .02; I 3-4: OS rate = 64.6%, 95% CI = 46.6 to 89.6; vs I 0-1-2: OS rate = 32.5%, 95% CI = 17.2 to 61.4; HR = 0.32, 95% CI = 0.15 to 0.66, P = .001, C-index = 65.9%; five-year follow-up, TB score: TB 3-4: DFS rate = 25.7%, 95% CI = 14.2 to 46.6; vs TB 0-1-2: DFS rate = 5.0%, 95% CI = 0.8 to 32.4; HR = 0.36, 95% CI = 0.22 to 0.57, P < .001; TB 3-4: OS rate = 63.7%, 95% CI = 46.4 to 87.5; vs TB 0-1-2: OS rate: 21.4%, 95% CI = 9.2 to 49.8; HR = 0.25, 95% CI = 0.12 to 0.51, P < .001, C-index = 67.8%). High TB score and Immunoscore patients had a median survival of 70.5 months, while low patients survived only 25.1 to 38.3 months. Nonresponding patients with high-immune infiltrates had prolonged DFS (HR = 0.28, 95% CI = 0.15 to 0.52, P = .001) and OS (HR = 0.25, 95% CI = 0.1 to 0.62, P = .001). The immune parameters remained the only statistically significant prognostic factor associated with DFS and OS in multivariable analysis (P < .001), while response to treatment was not.

Conclusions: Response to treatment and prolonged survival of metastatic CRC patients were statistically significantly associated with high-immune densities quantified into the least immune-infiltrated metastasis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aged
  • Antigens, CD20 / analysis
  • Antineoplastic Combined Chemotherapy Protocols / therapeutic use
  • B-Lymphocytes* / chemistry
  • CD3 Complex / analysis
  • CD8-Positive T-Lymphocytes
  • Chemotherapy, Adjuvant
  • Colorectal Neoplasms / immunology*
  • Colorectal Neoplasms / pathology
  • Colorectal Neoplasms / therapy
  • Disease-Free Survival
  • Follow-Up Studies
  • Forkhead Transcription Factors / analysis
  • Hepatectomy
  • Humans
  • Leukocyte Common Antigens / analysis
  • Liver Neoplasms / immunology*
  • Liver Neoplasms / secondary
  • Liver Neoplasms / therapy
  • Lung Neoplasms / immunology*
  • Lung Neoplasms / secondary
  • Lung Neoplasms / therapy
  • Lymphocyte Count
  • Lymphocytes, Tumor-Infiltrating*
  • Metastasectomy
  • Middle Aged
  • Neoplasm Metastasis
  • Pneumonectomy
  • Preoperative Period
  • Response Evaluation Criteria in Solid Tumors
  • Survival Rate
  • T-Lymphocytes* / chemistry
  • Tumor Microenvironment / immunology

Substances

  • Antigens, CD20
  • CD3 Complex
  • FOXP3 protein, human
  • Forkhead Transcription Factors
  • Leukocyte Common Antigens