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Research ArticleClinical Investigation

Long-Term Outcomes of Transarterial Radioembolization for Large Single Hepatocellular Carcinoma: A Comparison to Resection

Jihye Kim, Ju Yeon Kim, Jeong-Hoon Lee, Dong Hyun Sinn, Moon Haeng Hur, Ji Hoon Hong, Min Kyung Park, Hee Jin Cho, Na Ryung Choi, Yun Bin Lee, Eun Ju Cho, Su Jong Yu, Yoon Jun Kim, Jin Chul Paeng, Hyo Cheol Kim, Nam-Joon Yi, Kwang-Woong Lee, Kyung-Suk Suh, Dongho Hyun, Jong Man Kim and Jung-Hwan Yoon
Journal of Nuclear Medicine August 2022, 63 (8) 1215-1222; DOI: https://doi.org/10.2967/jnumed.121.263147
Jihye Kim
1Department of Internal Medicine and Liver Research Institute, Seoul National University College of Medicine, Seoul, Korea;
2Department of Internal Medicine, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea;
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Ju Yeon Kim
1Department of Internal Medicine and Liver Research Institute, Seoul National University College of Medicine, Seoul, Korea;
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Jeong-Hoon Lee
1Department of Internal Medicine and Liver Research Institute, Seoul National University College of Medicine, Seoul, Korea;
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Dong Hyun Sinn
2Department of Internal Medicine, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea;
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Moon Haeng Hur
1Department of Internal Medicine and Liver Research Institute, Seoul National University College of Medicine, Seoul, Korea;
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Ji Hoon Hong
1Department of Internal Medicine and Liver Research Institute, Seoul National University College of Medicine, Seoul, Korea;
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Min Kyung Park
1Department of Internal Medicine and Liver Research Institute, Seoul National University College of Medicine, Seoul, Korea;
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Hee Jin Cho
1Department of Internal Medicine and Liver Research Institute, Seoul National University College of Medicine, Seoul, Korea;
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Na Ryung Choi
1Department of Internal Medicine and Liver Research Institute, Seoul National University College of Medicine, Seoul, Korea;
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Yun Bin Lee
1Department of Internal Medicine and Liver Research Institute, Seoul National University College of Medicine, Seoul, Korea;
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Eun Ju Cho
1Department of Internal Medicine and Liver Research Institute, Seoul National University College of Medicine, Seoul, Korea;
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Su Jong Yu
1Department of Internal Medicine and Liver Research Institute, Seoul National University College of Medicine, Seoul, Korea;
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Yoon Jun Kim
1Department of Internal Medicine and Liver Research Institute, Seoul National University College of Medicine, Seoul, Korea;
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Jin Chul Paeng
3Department of Nuclear Medicine, Seoul National University College of Medicine, Seoul, Korea;
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Hyo Cheol Kim
4Department of Radiology, Seoul National University College of Medicine, Seoul, Korea;
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Nam-Joon Yi
5Department of Surgery, Seoul National University College of Medicine, Seoul, Korea;
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Kwang-Woong Lee
5Department of Surgery, Seoul National University College of Medicine, Seoul, Korea;
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Kyung-Suk Suh
5Department of Surgery, Seoul National University College of Medicine, Seoul, Korea;
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Dongho Hyun
6Department of Radiology and Center for Imaging Science, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea; and
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Jong Man Kim
7Department of Surgery, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea
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Jung-Hwan Yoon
1Department of Internal Medicine and Liver Research Institute, Seoul National University College of Medicine, Seoul, Korea;
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  • FIGURE 1.
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    FIGURE 1.

    Flowchart of study population. ECOG = Eastern Cooperative Oncology Group performance; Vp3 = tumor thrombus in first-order branches of the portal vein; Vp4 = tumor thrombus in the main trunk of the portal vein and/or contralateral portal vein branch to the primarily involved lobe.

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    FIGURE 2.

    Crude analysis: cumulative probability of OS (A), tumor progression (B), and intrahepatic tumor progression (C) according to treatment groups.

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    FIGURE 3.

    After using IPTW: cumulative probability of OS (A), tumor progression (B), and intrahepatic tumor progression (C) according to treatment groups.

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    TABLE 1.

    Baseline Characteristics of Study Population

    CharacteristicTARE (n = 57)Resection (n = 500)P
    Age (y)69.0 (60.0–77.0)60.0 (52.0–68.0)< 0.001
    Age< 0.001
     < 60 y13 (22.8%)246 (49.2%)
     ≥ 60 y44 (77.2%)254 (50.8%)
    Male sex50 (87.7%)417 (83.4%)0.52
    ASA classification0.047
     1 or 229 (50.9%)326 (65.2%)
     328 (49.1%)174 (34.8%)
    Etiology0.21
     Hepatitis B virus33 (57.9%)335 (67.0%)
     Hepatitis C virus3 (5.3%)31 (6.2%)
     Alcohol8 (14.0%)41 (8.2%)
     NASH0 (0.0%)15 (3.0%)
     Unknown13 (22.8%)78 (15.6%)
    Liver cirrhosis22 (38.6%)151 (30.2%)0.25
    ALBI grade0.30
     145 (78.9%)426 (85.2%)
     ≥ 2*12 (21.1%)74 (14.8%)
    α-fetoprotein (ng/mL)7.3 (4.3–132.4)15.4 (4.2–774.4)0.19
    α-fetoprotein0.09
     < 400 ng/mL47 (82.5%)355 (71.0%)
     ≥ 400 ng/mL10 (17.5%)145 (29.0%)
    Tiny satellite nodules4 (7.0%)22 (4.4%)0.33
    Tumor size (cm)10.0 (7.5–11.3)7.0 (5.5–9.2)< 0.001
    Tumor size< 0.001
     < 8 cm17 (29.8%)306 (61.2%)
     ≥ 8 cm40 (70.2%)194 (38.8%)
    Lobar involvement0.04
     Unilobar41 (71.9%)420 (84.0%)
     Bilobar16 (28.1%)80 (16.0%)
    Level of PVTT0.02
     Vp0 (absent)51 (89.5%)467 (93.4%)
     Vp11 (1.8%)23 (4.6%)
     Vp25 (8.8%)10 (2.0%)
    • ↵* One patient in resection group had ALBI grade 3.

    • NASH = nonalcoholic steatohepatitis; ALBI = albumin–bilirubin; ASA = American Society of Anesthesiologists; Vp0 = absence of tumor thrombus in the portal vein; Vp1 = tumor thrombus in distal to the second order branches of the portal vein, but not of the second order branches; Vp2 = tumor thrombus in second order branches of the portal vein.

    • Qualitative data are number and percentage; continuous data are median and IQR.

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    TABLE 2.

    Risk Factor Analysis for OS

    Univariable analysisMultivariable analysis
    VariableHRPHRP
    Age ≥ 60 (vs. < 60)0.74 (0.38–1.45)0.38
    Male (vs. female)1.22 (0.58–2.58)0.60
    ASA classification 3 (vs. 1 or 2)2.64 (1.34–5.21)0.0051.95 (0.88–4.32)0.10
    Hepatitis B virus–related (vs. the others)1.23 (0.62–2.43)0.56
    Liver cirrhosis2.51 (1.22–5.16)0.011.07 (0.43–2.65)0.89
    Albumin–bilirubin grade ≥ 2 (vs. 1)2.60 (1.23–5.49)0.011.98 (1.02–3.83)0.04
    AFP ≥ 400 ng/mL (vs. < 400 ng/mL)0.80 (0.40–1.60)0.53
    Satellite nodules1.47 (0.98–2.20)0.061.29 (0.87–1.90)0.20
    Tumor size ≥ 8 cm1.41 (0.63–3.14)0.40
    Bilobar involvement1.51 (0.73–3.12)0.26
    Vp2 (vs. Vp0 or Vp1)1.63 (0.94–2.81)0.081.57 (0.86–2.84)0.14
    TARE (vs. resection)0.98 (0.40–2.43)0.971.04 (0.42–2.59)0.93
    • Data are with weighted population, using variables with P value under 0.1 at univariable analysis. Data in parentheses are 95% CI.

    • AFP = α-fetoprotein; Vp0 = absence of tumor thrombus in the portal vein; Vp1 = tumor thrombus in distal to the second-order branches of the portal vein, but not of the second-order branches; Vp2 = tumor thrombus in second-order branches of the portal vein.

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    TABLE 3.

    Safety Assessment

    TARE (n = 57)Resection (n = 500)P
    Adverse eventAny gradeGrade 3 or 4Any gradeGrade 3 or 4Any gradeGrade 3 or 4
    Overall incidence25 (43.9%)5 (8.8%)500 (100%)500 (100%)< 0.001< 0.001
    Ascites0037 (7.4%)5 (1.0%)0.0241.00
    Fever3 (5.3%)0104 (20.8%)1 (0.2%)0.0081.00
    Nausea7 (12.3%)054 (10.8%)3 (0.6%)0.911.00
    Vomiting5 (8.8%)033 (6.6%)1 (0.2%)0.581.00
    Abdominal pain15 (26.3%)3 (5.3%)500 (100%)500 (100%)< 0.001< 0.001
    Biliary anastomotic leak0014 (2.8%)9 (1.8%)0.380.61
    Wound complication0028 (5.6%)3 (0.6%)0.101.00
    Dyspnea0014 (2.8%)5 (1.0%)0.381.00
    Gastrointestinal hemorrhage006 (1.2%)1 (0.2%)1.001.00
    AST elevation4 (7.0%)1 (1.8%)488 (97.6%)269 (53.8%)< 0.001< 0.001
    ALT elevation3 (5.3%)1 (1.8%)481 (96.2%)248 (49.6%)< 0.001< 0.001
    Bilirubin elevation2 (3.5%)1 (1.8%)350 (70.0%)37 (7.4%)< 0.0010.16
    Portal vein thrombosis0015 (3.0%)5 (1.0%)0.391.00
    Adverse events requiring intervention0NA16 (3.2%)NA0.39NA
    • Listed are adverse events, as defined by Common Terminology Criteria for Adverse Events (version 5.0). Data are number and percentage.

    • AST = aspartate aminotransferase; ALT = alanine transaminase; NA = not applicable.

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Journal of Nuclear Medicine: 63 (8)
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Long-Term Outcomes of Transarterial Radioembolization for Large Single Hepatocellular Carcinoma: A Comparison to Resection
Jihye Kim, Ju Yeon Kim, Jeong-Hoon Lee, Dong Hyun Sinn, Moon Haeng Hur, Ji Hoon Hong, Min Kyung Park, Hee Jin Cho, Na Ryung Choi, Yun Bin Lee, Eun Ju Cho, Su Jong Yu, Yoon Jun Kim, Jin Chul Paeng, Hyo Cheol Kim, Nam-Joon Yi, Kwang-Woong Lee, Kyung-Suk Suh, Dongho Hyun, Jong Man Kim, Jung-Hwan Yoon
Journal of Nuclear Medicine Aug 2022, 63 (8) 1215-1222; DOI: 10.2967/jnumed.121.263147

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Long-Term Outcomes of Transarterial Radioembolization for Large Single Hepatocellular Carcinoma: A Comparison to Resection
Jihye Kim, Ju Yeon Kim, Jeong-Hoon Lee, Dong Hyun Sinn, Moon Haeng Hur, Ji Hoon Hong, Min Kyung Park, Hee Jin Cho, Na Ryung Choi, Yun Bin Lee, Eun Ju Cho, Su Jong Yu, Yoon Jun Kim, Jin Chul Paeng, Hyo Cheol Kim, Nam-Joon Yi, Kwang-Woong Lee, Kyung-Suk Suh, Dongho Hyun, Jong Man Kim, Jung-Hwan Yoon
Journal of Nuclear Medicine Aug 2022, 63 (8) 1215-1222; DOI: 10.2967/jnumed.121.263147
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