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Quantitative Effect of Natural Killer–Cell Licensing on Hepatocellular Carcinoma Recurrence after Curative Hepatectomy

Naoki Tanimine, Yuka Tanaka, Tsuyoshi Kobayashi, Hirotaka Tashiro, Daiki Miki, Michio Imamura, Hiroshi Aikata, Junko Tanaka, Kazuaki Chayama and Hideki Ohdan
Naoki Tanimine
1Gastroenterological and Transplant Surgery, Institute of Biomedical and Health Sciences, Hiroshima University, Hiroshima, Japan.
2Liver Research Project Center, Hiroshima University, Hiroshima, Japan.
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Yuka Tanaka
1Gastroenterological and Transplant Surgery, Institute of Biomedical and Health Sciences, Hiroshima University, Hiroshima, Japan.
2Liver Research Project Center, Hiroshima University, Hiroshima, Japan.
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Tsuyoshi Kobayashi
1Gastroenterological and Transplant Surgery, Institute of Biomedical and Health Sciences, Hiroshima University, Hiroshima, Japan.
2Liver Research Project Center, Hiroshima University, Hiroshima, Japan.
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Hirotaka Tashiro
1Gastroenterological and Transplant Surgery, Institute of Biomedical and Health Sciences, Hiroshima University, Hiroshima, Japan.
2Liver Research Project Center, Hiroshima University, Hiroshima, Japan.
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Daiki Miki
2Liver Research Project Center, Hiroshima University, Hiroshima, Japan.
3Laboratory for liver Disease, RIKEN Center for Genomic Medicine, Hiroshima, Japan.
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Michio Imamura
2Liver Research Project Center, Hiroshima University, Hiroshima, Japan.
4Medicine and Molecular Science, Institute of Biomedical and Health Sciences, Hiroshima University, Hiroshima, Japan.
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Hiroshi Aikata
2Liver Research Project Center, Hiroshima University, Hiroshima, Japan.
4Medicine and Molecular Science, Institute of Biomedical and Health Sciences, Hiroshima University, Hiroshima, Japan.
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Junko Tanaka
2Liver Research Project Center, Hiroshima University, Hiroshima, Japan.
5Epidemiology, Infectious Disease Control and Prevention, Institute of Biomedical & Health Sciences, Hiroshima University, Hiroshima, Japan.
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Kazuaki Chayama
2Liver Research Project Center, Hiroshima University, Hiroshima, Japan.
3Laboratory for liver Disease, RIKEN Center for Genomic Medicine, Hiroshima, Japan.
4Medicine and Molecular Science, Institute of Biomedical and Health Sciences, Hiroshima University, Hiroshima, Japan.
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Hideki Ohdan
1Gastroenterological and Transplant Surgery, Institute of Biomedical and Health Sciences, Hiroshima University, Hiroshima, Japan.
2Liver Research Project Center, Hiroshima University, Hiroshima, Japan.
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  • For correspondence: hohdan@hiroshima-u.ac.jp
DOI: 10.1158/2326-6066.CIR-14-0091 Published December 2014
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    Figure 1.

    The presence of a single functional compound of KIR-HLA genotype did not affect HCC recurrence. The effect of each compound genotype (KIR2DL1-C2, KIR2DL2-C1, KIR3DL1-BW4, KIR3DL2-A3/11) on HCC recurrence was analyzed by propensity score–matched studies using nine variables (age, sex, etiology, tumor number, maximum diameter, histologic differentiation, vascular invasion, satellite lesion, and surgical margin). The 5-year cumulative risk of recurrence was compared between one-to-two or two-to-one patient pairs with or without each compound KIR-HLA genotype. A, KIR2DL1-C2; B, KIR2DL2-C1; C, KIR3DL1-Bw4; and D, KIR3DL2-A3/11.

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    Figure 2.

    The multiplicity of compound KIR-HLA genotypes stratified the recurrence risk of HCC. Kaplan–Meier analyses of the 5-year cumulative risk of recurrence (A) and OS (B) for 170 patients were performed according to the number of functional compound KIR-HLA genotypes. Propensity score–matched analyses of the 5-year cumulative risk of recurrence (C) and OS (D) were also performed for patients with at least three compound genotypes (highly licensed NK group) and patients with one or two compound genotypes (poorly licensed NK group). The cumulative risk of recurrence in the highly licensed NK group was significantly lower than in the poorly licensed NK group. aHR, adjusted HR.

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    Figure 3.

    The lower cumulative risk of recurrence in the highly licensed NK group was significant among the non–HCV-related cohort. A, according to the presence or absence of HCV infection, Kaplan–Meier analyses of the 5-year cumulative risk of recurrence were performed for 138 matched patients belonging to the highly and poorly licensed NK groups. Further subgroup analyses were performed in non–HCV-related patients (B) and HCV-related patients (C).

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  • Table 1.

    Cumulative risk of recurrence and overall survival of patients with HCC according to clinicopathologic characteristics and compound KIR-HLA genotypes

    Total patients (N = 170)HCV-related patients (n = 97)
    Cumulative risk of recurrenceOSCumulative risk of recurrenceOS
    PHR (95% CI)PHR (95% CI)PHR (95% CI)PHR (95% CI)
    Age (≤65 vs. >65 years)0.745NA0.362NA0.626NA0.592NA
    Sex (male vs. female)0.0781.54 (0.99–2.53)0.966NA0.554NA0.216NA
    Etiology (HBV vs. HCV vs. others)0.448NA0.117NANANANANA
    Tumor number (≥2 vs. 1)0.0101.57 (1.06–2.31)0.0391.64 (1.11– 2.39)0.0881.56 (0.92–2.51)0.604NA
    Maximum diameter (≤50 mm vs. >50 mm)0.222NA0.511NA0.749NA0.313NA
    Histologic differentiation (G1+G2 vs. G3)0.253NA0.498NA0.866NA0.909NA
    Vascular invasion0.733NA0.851NA0.612NA0.454NA
    Satellite lesion0.657NA0.743NA0.451NA0.486NA
    Surgical margin (<5 mm vs. ≥5 mm)0.126NA0.162NA0.0391.88 (0.98–3.36)0.0031.88 (0.97 – 3.37)
    KIR2DL1-C20.113NA0.754NA0.189NA0.964NA
    KIR2DL2-C10.253NA0.945NA0.456NA0.745NA
    KIR2DL3-C10.793NA0.283NA0.694NA0.105NA
    KIR3DL1-Bw40.269NA0.359NA0.572NA0.935NA
    KIR3DL2-A3/110.585NA0.570NA0.845NA0.986NA
    Number of KIR-HLA genotypes (≥3 vs. ≤2)0.0160.61 (0.38–0.94)0.224NA0.130NA0.735NA

    NOTE: Cumulative risk of recurrence and OS were compared by log-rank statistics for univariate analysis. Cox proportional hazards model was conducted for multivariate survival analysis. Only variables presenting P < 0.1 in the univariate analysis were included in the multivariate model. P < 0.05 was considered statistically significant.

    Abbreviation: NA, not assessed.

    Additional Files

    • Figures
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    • Supplementary Table S1

      Files in this Data Supplement:

      • Data Supplement - One hundred seventy HCC patients who underwent curative hepatectomy were enrolled based on the following inclusion criteria: presence of histologically confirmed HCC; preserved preoperative liver function (Child-Pugh grade A); no residual tumor after surgery; and no evidence of comorbid malignant tumor. Background characteristics and prognoses of the patients and tumors are summarized.
      • Data Supplement - KIR and HLA genotyping was performed using the reverse SSP-PCR method. Presence of the HLA ligand for KIR was determined according to the HLA genotypes.
      • Data Supplement - Background characteristics of patients before and after propensity score matching for each functional compound KIR-HLA genotype are summarized.
      • Data Supplement - The effect of each compound genotype (KIR2DL1-C2, KIR2DL2-C1, KIR3DL1-BW4, and KIR3DL2-A3/11) on 5-year OS was analyzed by propensity score-matched studies using nine variables (age, sex, etiology, tumor number, maximum diameter, histological differentiation, vascular invasion, satellite lesion, and surgical margin). The 5-year OS was compared between one-to-two or two-to-one patient pairs with or without each compound KIR-HLA genotype. (A) KIR2DL1-C2; (B) KIR2DL2-C1; (C) KIR3DL1-Bw4; and (D) KIR3DL2-A3/11.
      • Data Supplement - Propensity score matching was performed using nine variables (age, sex, etiology, tumor number, maximum diameter, histological differentiation, vascular invasion, satellite lesion, and surgical margin) for patients with at least three compound genotypes (highly licensed NK group) and patients with one or two compound genotypes (poorly licensed NK group). Background characteristics before and after matching are summarized.
      • Data Supplement - (A) According to TNM stages, Kaplan-Meier analyses of the 5-year cumulative recurrence risk were performed for the 138 matched patients belonging to the highly and poorly licensed NK groups. Further subgroup analyses were performed for patients with (B) stage I, (C) stage II, and (D) stage IIIA HCC.
      • Data Supplement - Cumulative risk of recurrence and overall survival were compared by log-rank test for univariate analyses. The Cox proportional hazards regression model was performed for multivariate survival analysis. Only variables yielding P < 0.1 in the univariate analysis were included in the multivariate model.
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    Cancer Immunology Research: 2 (12)
    December 2014
    Volume 2, Issue 12
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    Quantitative Effect of Natural Killer–Cell Licensing on Hepatocellular Carcinoma Recurrence after Curative Hepatectomy
    Naoki Tanimine, Yuka Tanaka, Tsuyoshi Kobayashi, Hirotaka Tashiro, Daiki Miki, Michio Imamura, Hiroshi Aikata, Junko Tanaka, Kazuaki Chayama and Hideki Ohdan
    Cancer Immunol Res December 1 2014 (2) (12) 1142-1147; DOI: 10.1158/2326-6066.CIR-14-0091

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    Quantitative Effect of Natural Killer–Cell Licensing on Hepatocellular Carcinoma Recurrence after Curative Hepatectomy
    Naoki Tanimine, Yuka Tanaka, Tsuyoshi Kobayashi, Hirotaka Tashiro, Daiki Miki, Michio Imamura, Hiroshi Aikata, Junko Tanaka, Kazuaki Chayama and Hideki Ohdan
    Cancer Immunol Res December 1 2014 (2) (12) 1142-1147; DOI: 10.1158/2326-6066.CIR-14-0091
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