Poor clinical outcomes and immunoevasive contexture in gastric cancer patients bearing p16 high phenotype.

Journal: Cancer

Study question
The investigators evaluated how different p16 (p16^INK4a) immunohistochemical staining patterns in gastric cancer relate to clinicopathologic features, survival, response to systemic therapy, and the tumor immune microenvironment.

Design and cohorts

  • Retrospective analysis of two cohorts:
    • Zhongshan Hospital (ZSHS): 443 patients
    • Samsung Medical Center (SMC): 43 patients
  • Tumor classification by p16 staining:
    • Loss
    • Wild-type (WT)
    • Overexpression (OE)

Key findings

1. Frequency and clinicopathologic features

  • Frequency of p16 overexpression:
    • In the ZSHS cohort, 20.3% (90/443) of cases showed p16 overexpression.
  • p16 OE tumors were associated with:
    • More advanced pT stage (p = .011)
    • Higher Ki-67 proliferation index (p < .001)
    • Higher rates of Rb loss (p < .001)
    • Higher CCNE1 overexpression (p < .001)

2. Survival

  • p16 OE and overall survival:
    • p16 OE was associated with worse overall survival compared with WT.
    • ZSHS cohort: OE vs WT, p = .004
    • The effect was particularly evident in MSI tumors (p = .019).
  • p16 loss vs WT:
    • p16 loss and WT tumors had similar overall survival (p = .424).

3. Response to adjuvant chemotherapy (ACT)

  • p16 OE tumors:
    • Patients with p16 OE tumors had inferior benefit from ACT compared with WT (p = .011).
    • This was especially evident in MSI tumors (p = .024).
  • p16 loss vs WT:
    • p16 loss and WT tumors showed comparable response to ACT (p = .834).

4. Response to immune checkpoint inhibitors (ICI)

  • p16 OE and ICI response:
    • p16 OE was associated with poorer response to ICI compared with WT (p = .045).
    • This negative association was particularly evident in:
      • PD-L1 CPS ≥1 tumors (p = .027)
      • Chromosomal instability (CIN) tumors (p = .032)
  • p16 loss vs WT:
    • p16 loss and WT tumors had similar outcomes with ICI (p = .223).

5. Immune microenvironment
p16 OE gastric cancers showed an “immune-evasive” profile, with:

  • Lower infiltration of antitumor immune cells:
    • M1 macrophages
    • Neutrophils
    • CD8 T cells
  • Higher expression of immunosuppressive / pro-tumor factors:
    • TGF-β
    • CD73
    • IDO

Conclusions and implications

  • Three-tier p16 staining pattern: Loss, WT, and OE define biologically and clinically distinct subgroups in gastric cancer.
  • p16 overexpression: Marks a subset with more aggressive disease, worse survival, reduced benefit from adjuvant chemotherapy and immune checkpoint blockade, and an immunosuppressive tumor microenvironment.
  • p16 loss: Behaves similarly to WT in this dataset, suggesting that overexpression rather than loss is the adverse phenotype in gastric cancer.

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