Journal of Gastrointestinal Surgery

, Volume 23, Issue 11, pp 2216–2224 | Cite as

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

  • Luca Vigano
  • Cristiana Soldani
  • Barbara Franceschini
  • Matteo Cimino
  • Ana Lleo
  • Matteo Donadon
  • Massimo Roncalli
  • Alessio Aghemo
  • Luca Di Tommaso
  • Guido TorzilliEmail author
Original Article



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).


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).


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).


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.


Intrahepatic cholangiocellular carcinoma Tumor-infiltrating lymphocytes and macrophages Liver surgery Prognosis and survival Staging Immunology 


Authors’ Contribution

Substantial contributions to the conception or design of the work: Viganò, Roncalli, Aghemo, Torzilli

Acquisition, analysis, or interpretation of data for the work: Viganò, Soldani, Franceschini, Cimino, Lleo, Donadon, Di Tommaso

Drafting the work: Viganò, Soldani, Franceschini, Cimino, Lleo, Donadon, Di Tommaso

Revising it critically for important intellectual content: Viganò, Roncalli, Aghemo, Torzilli

Final approval of the version to be published: all the authors

Agreement to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved: all the authors

Compliance with Ethical Standards

The Institutional Review Board of our hospital approved this retrospective study and the requirement of informed consent was waived.

Conflicts of Interest

The authors declare that they have no conflict of interest.

Supplementary material

11605_2019_4111_MOESM1_ESM.docx (154 kb)
ESM 1 P values of different cut-offs values of CD3+ and CD8+ infiltrates (every 0.05% increase) when tested as predictors of overall survival. The lowest p value (white arrow) was used for the analyses. Dotted green line: p = 0.05 (DOCX 153 kb)


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Copyright information

© The Society for Surgery of the Alimentary Tract 2019

Authors and Affiliations

  • Luca Vigano
    • 1
    • 2
  • Cristiana Soldani
    • 1
  • Barbara Franceschini
    • 1
  • Matteo Cimino
    • 1
  • Ana Lleo
    • 2
    • 3
  • Matteo Donadon
    • 1
    • 2
  • Massimo Roncalli
    • 2
    • 4
  • Alessio Aghemo
    • 2
    • 3
  • Luca Di Tommaso
    • 2
    • 4
  • Guido Torzilli
    • 1
    • 2
    Email author
  1. 1.Department of Surgery, Division of Hepatobiliary & General SurgeryHumanitas Clinical and Research Center, IRCCSRozzano - MilanItaly
  2. 2.Department of Biomedical SciencesHumanitas UniversityPieve EmanueleItaly
  3. 3.Division of Internal Medicine and Hepatology, Department of Internal MedicineHumanitas Clinical and Research Center, IRCCSRozzanoItaly
  4. 4.Pathology UnitHumanitas Clinical and Research Center, IRCCSRozzanoItaly

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