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Research ArticleOriginal Article

Role of adjuvant chemoradiotherapy and chemotherapy in patients with resected gallbladder carcinoma: a multi-institutional analysis (KROG 19-04)

Sung Uk Lee, Jinsil Seong, Tae Hyun Kim, Jung Ho Im, Woo Chul Kim, Kyubo Kim, Hae Jin Park, Tae Gyu Kim, Youngkyong Kim, Bae Kwon Jeong, Jin Hee Kim, Byoung Hyuck Kim and Taek-Keun Nam
Cancer Biology & Medicine June 2022, 19 (6) 931-944; DOI: https://doi.org/10.20892/j.issn.2095-3941.2020.0667
Sung Uk Lee
1Center for Proton Therapy and Center for Liver and Pancreatobiliary Cancer, National Cancer Center, Goyang 10408, Korea
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Jinsil Seong
2Department of Radiation Oncology, Yonsei Cancer Center, Yonsei University College of Medicine, Seoul 03722, Korea
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Tae Hyun Kim
1Center for Proton Therapy and Center for Liver and Pancreatobiliary Cancer, National Cancer Center, Goyang 10408, Korea
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  • For correspondence: [email protected] [email protected]
Jung Ho Im
2Department of Radiation Oncology, Yonsei Cancer Center, Yonsei University College of Medicine, Seoul 03722, Korea
3Department of Radiation Oncology, CHA Bundang Medical Center, CHA University School of Medicine, Seongnam 13497, Korea
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Woo Chul Kim
4Department of Radiation Oncology, Inha University Hospital, Inha University School of Medicine, Incheon 22332, Korea
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Kyubo Kim
5Department of Radiation Oncology, Ewha Womans University Mokdong Hospital, Ewha Womans University College of Medicine, Seoul 07985, Korea
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Hae Jin Park
6Department of Radiation Oncology, Hanyang University Medical Center, Hanyang University College of Medicine, Seoul 04763, Korea
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Tae Gyu Kim
7Department of Radiation Oncology, Samsung Changwon Hospital, Sungkyunkwan University School of Medicine, Changwon 51353, Korea
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Youngkyong Kim
8Department of Radiation Oncology, Kyung Hee University Hospital, Kyung Hee University College of Medicine, Seoul 02447, Korea
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Bae Kwon Jeong
9Department of Radiation Oncology, Gyeongsang National University Hospital, Gyeongsang National University College of Medicine, Jinju 52727, Korea
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Jin Hee Kim
10Department of Radiation Oncology, Dongsan Medical Center, Keimyung University School of Medicine, Daegu 41931, Korea
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Byoung Hyuck Kim
11Department of Radiation Oncology, Seoul Metropolitan Government Seoul National University Boramae Medical Center, Seoul 07061, Korea
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Taek-Keun Nam
12Department of Radiation Oncology, Chonnam National University Hwasun Hospital, Chonnam National University College of Medicine, Hwasun 58128, Korea
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  • Figure 1
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    Figure 1

    Patterns of failures among adjuvant treatment groups. (A) stage II, and (B) stage III–IV. LR, locoregional recurrence; DM, distant metastasis; NED, no evidence of disease; No-AT, no adjuvant treatment; CTx, chemotherapy; CRT, chemoradiotherapy.

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    Figure 2

    LRFS (A and D), RFS (B and E), and OS (C and F) curves among the adjuvant treatment groups in stage II and III–IV patients, respectively. LRFS, locoregional recurrence-free survival; RFS, recurrence-free survival; OS, overall survival; LR, locoregional recurrence; DM, distant metastasis; NED, no evidence of disease; No-AT, no adjuvant treatment; CTx, chemotherapy; CRT, chemoradiotherapy. *Log-rank test.

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    Figure 3

    LRFS (A), RFS (B), and OS (C) curves among the adjuvant treatment groups in stage II patients with of perineural invasion and/or Nx classification. LRFS, locoregional recurrence-free survival; RFS, recurrence-free survival; OS, overall survival; LR, locoregional recurrence; DM, distant metastasis; NED, no evidence of disease; No-AT, no adjuvant treatment; CTx, chemotherapy; CRT, chemoradiotherapy. *Log-rank test.

Tables

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    Table 1

    Comparison of the baseline patient characteristics among the adjuvant treatment groups

    CharacteristicsStage II (n = 381)Stage III–IV (n = 352)
    No-AT (n = 258)CTx (n = 82)CRT (n = 41)P valueNo-AT (n = 114)CTx (n = 133)CRT (n = 105)P value
    Gender, n (%)
     Male113 (44)33 (40)22 (54)0.364*44 (39)55 (41)43 (41)0.897*
     Female145 (56)49 (60)19 (46)70 (61)78 (59)62 (59)
    Age (years)
     Median [range]67 [29–87]61 [29–88]66 [44–81]0.000†71 [41–91]62 [38–87]63 [26–83]0.000†
     ≤60 years, n (%)53 (21)36 (44)10 (24)0.000*22 (19)52 (39)39 (37)0.002*
     >60 years, n (%)205 (79)46 (56)31 (76)92 (81)81 (61)66 (63)
    Tumor size (cm)
     Median [range]2.3 [0.1–8.8]2.7 [0.7–9.0]2.5 [0.5–10.5]0.420†3.4 [1.0–13]3.5 [0.9–13.0]3.5 [1.0–9.0]0.534†
     ≤3 cm, n (%)79 (67)38 (63)22 (65)0.846*35 (43)34 (44)37 (47)0.866*
     >3 cm, n (%)38 (33)22 (37)12 (35)47 (57)43 (56)42 (53)
    T classification, n (%)
     T2258 (100)82 (100)41 (100)–44 (39)58 (44)48 (46)0.554*
     T3–4–––70 (61)75 (56)57 (54)
    N classification, n (%)
     Nx52 (20)11 (13)3 (7)0.075‡8 (7)2 (2)1 (1)0.027‡
     N0206 (80)71 (87)38 (93)27 (24)25 (19)17 (16)
     N160 (53)90 (68)74 (71)
     N219 (17)16 (12)13 (12)
    Preop CA 19-9 level (U/mL)
     Median [range]10 [0.1–2,400]9 [0.8–383]10 [2–119]0.347†21 [0.1–2,960]21 [0.1–8,340]19 [0.1–9,410]0.370†
     ≤37 U/mL, n (%)168 (83)57 (84)29 (85)0.926*59 (64)81 (68)60 (67)
     >37 U/mL, n (%)35 (17)11 (16)5 (15)34 (37)39 (33)29 (33)
    Postop CA 19-9 level (U/mL)
     Median [range]8 [0.1–3,056]8 [0.7–62]9 [2.6–606]0.639†13 [0.1–3,487]15 [0.1–850]14 [0.1–1,445]0.064†
     ≤37 U/mL, n (%)204 (94)72 (97)34 (94)0.543‡70 (74)104 (83)78 (84)0.131*
     >37 U/mL, n (%)13 (6)2 (3)2 (6)25 (26)21 (17)15 (16)
    Histologic differentiation, n (%)
     WD/MD224 (90)69 (86)36 (90)0.639*74 (70)97 (76)73 (72)0.554*
     PD25 (10)11 (14)4 (10)31 (30)30 (24)29 (28)
    Resection margin, n (%)
     Negative249 (99)72 (95)38 (93)0.025‡97 (88)118 (90)96 (92)0.599*
     Positive3 (1)4 (5)3 (7)13 (12)13 (10)8 (8)
    LVSI, n (%)
     No187 (79)58 (82)27 (67)0.196*38 (36)51 (40)51 (50)0.122*
     Yes50 (21)13 (18)13 (33)68 (64)76 (60)52 (50)
    PNI, n (%)
     No193 (88)43 (80)31 (82)0.199*55 (54)50 (43)49 (49)0.280*
     Yes26 (12)11 (20)7 (18)47 (46)66 (57)52 (51)
    Extent of surgical resection, n (%)
     Non-radical60 (23)14 (17)5 (12)0.175*20 (18)7 (5)6 (6)0.001*
     Radical198 (77)68 (83)36 (88)94 (82)126 (95)99 (94)

    No-AT, no adjuvant therapy; CTx, chemotherapy; CRT, chemoradiotherapy; Preop, preoperative; Postop, postoperative; CA 19-9, carbohydrate antigen 19-9; WD, well differentiation; MD, moderate differentiation; PD, poor differentiation; LVSI, lymphovascular space invasion; PNI, perineural invasion; Non-radical, cholecystectomy ± lymph node dissection; Radical, radical cholecystectomy and lymph node dissection. *Pearson’s chi-square test. †One-way analysis of variance. ‡Fisher’s exact test.

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      Table 2

      Univariate analysis of LRFS, RFS, and OS according to tumor stage

      CharacteristicsnStage II (n = 381)nStage III–IV (n = 352)
      LRFSRFSOSLRFSRFSOS
      5-year (%)P value*5-year (%)P value*5-year (%)P value*5-year (%)P value*5-year (%)P value*5-year (%)P value*
      Gender
       Male16886.20.09678.30.62180.20.67214247.80.36032.20.44948.80.445
       Female21380.176.078.421052.036.144.2
      Age
       ≤60 years9991.00.02184.50.03990.60.00511348.60.50234.30.34254.70.007
       >60 years28279.374.074.823952.034.941.6
      T classification
       T2381––––––15063.1< 0.00148.40.00060.7<0.001
       T3–40–––20240.023.934.9
      N classification
       N031585.30.00380.8<0.00182.7<0.0016953.5<0.00137.80.00051.2<0.001
       N10–––22454.638.850.7
       N20–––4830.813.422.2
       Nx6668.756.762.6110.00.00.00
      Preop CA 19-9 level
       ≤37 U/mL25486.00.00181.10.00183.20.02620051.90.03735.80.04646.90.428
       >37 U/mL5169.761.364.310244.528.643.2
      Postop CA 19-9 level (U/mL)
       ≤3731084.90.00079.00.00083.70.00025255.2<0.00139.70.00082.40.000
       >371742.247.443.66125.66.314.4
      Histologic differentiation
       WD/MD32982.80.74077.20.60878.90.96424453.40.03638.50.00451.30.004
       PD4084.374.378.09044.825.234.1
      Resection margin
       Negative35984.10.00579.0<0.00181.8<0.00131150.60.11936.20.00148.50.001
       Positive1060.040.048.03439.111.118.1
      LVSI
       No27287.70.00083.2<0.00184.6<0.00114064.6<0.00148.50.00066.0<0.001
       Yes7663.955.865.119638.623.933.3
      PNI
       No26787.00.00083.1<0.00185.4<0.00115459.60.00144.20.00063.80.000
       Yes4457.245.549.616540.424.230.9
      Extent of surgical resection
       Non-radical7978.10.03671.30.03564.70.0093338.70.03634.50.33536.40.028
       Radical30283.978.483.131951.334.647.1
      Adjuvant treatment
       No-AT25883.90.51079.80.07678.30.94611437.9<0.00128.80.00635.4<0.001
       CTx8281.572.580.313345.030.045.7
       CRT4179.369.484.310567.845.256.9

      LRFS, locoregional recurrence-free survival; RFS, recurrence-free survival; OS, overall survival; n, number; No-AT, no adjuvant therapy; CTx, chemotherapy; CRT, chemoradiotherapy; Preop, preoperative; Postop, postoperative; CA 19-9, carbohydrate antigen 19-9; WD, well differentiation; MD, moderate differentiation; PD, poor differentiation; LVSI, lymphovascular space invasion; PNI, perineural invasion; Non-radical, cholecystectomy ± lymph node dissection; Radical, radical cholecystectomy and lymph node dissection. *Log-rank test.

        • View popup
        Table 3

        Multivariate analysis of LRFS, RFS, and OS according to tumor stage

        FactorsLRFSRFSOS
        HR (95% CI)P value*HR (95% CI)P value*HR (95% CI)P value*
        Stage II
         Age
          ≤ 60 years10.15710.14210.044
          > 60 years2.07 (0.75–5.70)1.97 (0.79–4.89)2.78 (1.02–7.53)
         N classification
          N010.0021<0.00110.024
          Nx3.53 (1.57–7.94)3.70 (1.81–7.58)2.55 (1.12–5.76)
         Preop CA 19-9 level
          ≤37 U/mL10.18110.12510.580
          >37 U/mL1.78 (0.76–4.19)1.81 (0.84–3.86)1.30 (0.51–3.29)
         Postop CA 19-9 level
          ≤ 37 U/mL10.04810.09410.038
          >37 U/mL3.60 (1.01–12.85)2.78 (0.84–9.21)4.27 (1.08–16.91)
         Resection margin
          Negative10.00110.00110.002
          Positive11.11 (2.70–45.65)10.82 (2.78–42.10)9.84 (2.25–42.98)
         LVSI
          No10.21710.40510.419
          Yes1.64 (0.74–3.61)1.35 (0.66–2.78)1.36 (0.64–2.92)
         PNI
          No10.0051<0.0011<0.001
          Yes3.25 (1.42–7.40)3.85 (1.86–7.98)4.16 (1.91–9.07)
         Extent of surgical resection
          Non-radical10.27810.53210.517
          Radical0.55 (0.18–1.61)0.74 (0.29–1.87)0.71 (0.26–1.97)
        Stage III–IV
         Age
          ≤ 60 years10.8950.70210.108
          > 60 years0.97 (0.63–1.48)1.07 (0.75–1.53)1.37 (0.93–2.03)
         T classification
          T210.04010.04810.054
          T3–41.64 (1.02–2.64)1.48 (1.00–2.19)1.51 (0.99–2.32)
         N classification
          N0111
          N12.02 (1.10–3.68)0.0221.77 (1.08–2.91)0.0231.68 (0.96–2.94)0.066
          N24.30 (2.22–8.29)<0.0013.91 (2.24–6.82)<0.0014.25 (2.31–7.79)<0.001
          Nx39.95 (9.33–170.98)<0.00121.56 (5.73–81.05)<0.0017.85 (1.62–37.84)0.010
         Preop CA 19-9 level
          ≤ 37 U/mL10.78910.89510.128
          > 37 U/mL1.06 (0.69–1.62)0.97 (0.67–1.40)0.73 (0.49–1.09)
         Postop CA 19-9 level
          ≤37 U/mL10.0021<0.0011<0.001
          >37 U/mL2.18 (1.33–3.56)2.76 (1.80–4.24)2.49 (1.59–3.89)
         Histologic differentiation
          WD/MD10.40210.12610.229
          PD1.20 (0.78–1.83)1.31 (0.92–2.19)1.26 (0.86–1.85)
         Resection margin
          Negative10.88910.15310.320
          Positive1.05 (0.48–2.31)1.54 (0.85–2.80)1.36 (0.74–2.50)
         LVSI
          No10.05510.06510.019
          Yes1.65 (0.98–2.75)1.46 (0.97–2.19)1.74 (1.09–2.77)
         PNI
          No10.12310.24110.051
          Yes1.42 (0.90–2.25)1.25 (0.86–1.81)1.52 (0.99–2.31)
         Extent of surgical resection
          Non-radical10.01010.16910.259
          Radical0.39 (0.19–0.79)0.62 (031–1.22)0.65 (0.30–1.37)
         Adjuvant treatment
          No-AT111
          CTx0.80 (0.50–1.29)0.3660.91 (0.60–1.39)0.6870.78 (0.51–1.21)0.280
          CRT0.28 (0.15–0.51)<0.0010.52 (0.33–0.82)0.0060.42 (0.25–0.70)0.001

        LRFS, locoregional recurrence-free survival; RFS, recurrence-free survival; OS, overall survival; HR, hazard ratio; CI, confidence interval; Preop, preoperative; Postop, postoperative; CA 19-9, carbohydrate antigen 19-9; LVSI, lymphovascular space invasion; PNI, perineural invasion; WD, well differentiation; MD, moderate differentiation; PD, poor differentiation; No-AT, no adjuvant therapy; CTx, chemotherapy; CRT, chemoradiotherapy. *Cox proportional hazards model.

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        Role of adjuvant chemoradiotherapy and chemotherapy in patients with resected gallbladder carcinoma: a multi-institutional analysis (KROG 19-04)
        Sung Uk Lee, Jinsil Seong, Tae Hyun Kim, Jung Ho Im, Woo Chul Kim, Kyubo Kim, Hae Jin Park, Tae Gyu Kim, Youngkyong Kim, Bae Kwon Jeong, Jin Hee Kim, Byoung Hyuck Kim, Taek-Keun Nam
        Cancer Biology & Medicine Jun 2022, 19 (6) 931-944; DOI: 10.20892/j.issn.2095-3941.2020.0667

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        Role of adjuvant chemoradiotherapy and chemotherapy in patients with resected gallbladder carcinoma: a multi-institutional analysis (KROG 19-04)
        Sung Uk Lee, Jinsil Seong, Tae Hyun Kim, Jung Ho Im, Woo Chul Kim, Kyubo Kim, Hae Jin Park, Tae Gyu Kim, Youngkyong Kim, Bae Kwon Jeong, Jin Hee Kim, Byoung Hyuck Kim, Taek-Keun Nam
        Cancer Biology & Medicine Jun 2022, 19 (6) 931-944; DOI: 10.20892/j.issn.2095-3941.2020.0667
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        Keywords

        • Gallbladder cancer
        • adjuvant treatment
        • chemoradiotherapy
        • locoregional recurrence-free survival
        • overall survival

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