Tumor-Infiltrating Lymphocytes and Macrophages in Intrahepatic Cholangiocellular Carcinoma. Impact on Prognosis after Complete Surgery

J Gastrointest Surg. 2019 Nov;23(11):2216-2224. doi: 10.1007/s11605-019-04111-5. Epub 2019 Jan 31.

Abstract

Background: Immune infiltrate impacts prognosis of several tumors. To assess the prognostic impact of tumor-infiltrating lymphocytes and macrophages in patients undergoing resection for intrahepatic cholangiocellular carcinoma (ICC).

Methods: All consecutive patients undergoing surgery for ICC between 2008 and 2016 were considered. Inclusion criteria were complete resection and follow-up > 12 months. Tissue sections were immunostained for CD3+, CD4+, CD8+, Foxp3+, and CD68+. The number of positive cells was quantified using a computer-aided image analysis system. Different cut-off values were tested as predictors of overall survival (OS).

Results: Fifty-three patients were analyzed. ICC were T1 in 28 patients, multifocal in 11, and N+ in 13. After a median follow-up of 42 months, 5-year OS was 52.1%. The following immune infiltrate values were associated with better OS: CD3+ > 0.10% (5-year OS 63.3% vs. 13.6% if ≤ 0.10%, p = 0.001); CD8+ > 0.10% (56.2% vs. 28.6% if ≤ 0.10%, p = 0.051); Foxp3+ absent (59.4% vs. 16.0% if present, p = 0.049). CD4+ and CD68+ infiltrates were not associated with OS. Three-year OS rates in patients with 0, 1, and ≥ 2 negative prognostic factors were 73.6%, 47.3%, and 14.3%, respectively (p < 0.001). CD3+ infiltrate stratified prognosis in T1 tumors (3-year OS 71.7% if CD3+ > 0.10% vs. 14.3% if ≤ 0.10%, p < 0.001).

Conclusions: Tumor-infiltrating lymphocytes are associated with prognosis of ICC patients after complete surgery. CD3+ and CD8+ infiltrate is associated with higher survival and lower recurrence risk, while Foxp3+ infiltrate is associated with worse prognosis. CD3+ infiltrate allows refining prediction of prognosis in early tumors.

Keywords: Immunology; Intrahepatic cholangiocellular carcinoma; Liver surgery; Prognosis and survival; Staging; Tumor-infiltrating lymphocytes and macrophages.

MeSH terms

  • Aged
  • Bile Duct Neoplasms / pathology
  • Bile Duct Neoplasms / surgery*
  • Bile Ducts, Intrahepatic / pathology
  • Bile Ducts, Intrahepatic / surgery*
  • Cholangiocarcinoma / mortality
  • Cholangiocarcinoma / pathology
  • Cholangiocarcinoma / surgery*
  • Female
  • Hepatectomy*
  • Humans
  • Immunity, Cellular*
  • Italy / epidemiology
  • Leukocyte Count
  • Lymphocytes, Tumor-Infiltrating / immunology
  • Lymphocytes, Tumor-Infiltrating / pathology*
  • Macrophages / pathology*
  • Male
  • Postoperative Period
  • Prognosis
  • Survival Rate / trends