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Research ArticleOriginal Article

Diagnostic value of 5 serum biomarkers for hepatocellular carcinoma with different epidemiological backgrounds: A large-scale, retrospective study

Dongming Liu, Yi Luo, Lu Chen, Liwei Chen, Duo Zuo, Yueguo Li, Xiaofang Zhang, Jing Wu, Qing Xi, Guangtao Li, Lisha Qi, Xiaofen Yue, Xiehua Zhang, Zhuoyu Sun, Ning Zhang, Tianqiang Song, Wei Lu and Hua Guo
Cancer Biology & Medicine February 2021, 18 (1) 256-270; DOI: https://doi.org/10.20892/j.issn.2095-3941.2020.0207
Dongming Liu
1Department of Hepatobiliary, Liver Cancer Research Center for Prevention and Therapy
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Yi Luo
2Department of Tumor Cell Biology
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Lu Chen
1Department of Hepatobiliary, Liver Cancer Research Center for Prevention and Therapy
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Liwei Chen
2Department of Tumor Cell Biology
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Duo Zuo
3Clinical Laboratory, Tianjin Medical University Cancer Institute and Hospital, National Clinical Research Center for Cancer, Key Laboratory of Cancer Prevention and Therapy, Tianjin, Tianjin’s Clinical Research Center for Cancer, Tianjin 300060, China
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Yueguo Li
3Clinical Laboratory, Tianjin Medical University Cancer Institute and Hospital, National Clinical Research Center for Cancer, Key Laboratory of Cancer Prevention and Therapy, Tianjin, Tianjin’s Clinical Research Center for Cancer, Tianjin 300060, China
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Xiaofang Zhang
4Medical Laboratory, Tianjin Medical University General Hospital, Tianjin 300052, China
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Jing Wu
5Clinical Laboratory, Tianjin Third Central Hospital, Tianjin 300170, China
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Qing Xi
2Department of Tumor Cell Biology
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Guangtao Li
2Department of Tumor Cell Biology
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Lisha Qi
6Department of Pathology, Tianjin Medical University Cancer Institute and Hospital, National Clinical Research Center for Cancer, Key Laboratory of Cancer Prevention and Therapy, Tianjin, Tianjin’s Clinical Research Center for Cancer, Tianjin 300060, China
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Xiaofen Yue
7Department of Tianjin Research Institute of Liver Diseases, Tianjin Second People’s Hospital, Tianjin 300192, China
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Xiehua Zhang
8Department of Infectious Diseases, The First Affiliated Hospital of Baotou Medical College, Inner Mongolia University of Science and Technology, Baotou 014010, China
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Zhuoyu Sun
9Department of Epidemiology and Biostatistics, School of Public Health, Tianjin Medical University, Tianjin 300070, China
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Ning Zhang
10The Center for Translational Cancer Research, Peking University First Hospital, Beijing 100034, China
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Tianqiang Song
1Department of Hepatobiliary, Liver Cancer Research Center for Prevention and Therapy
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  • For correspondence: [email protected] [email protected] [email protected]
Wei Lu
1Department of Hepatobiliary, Liver Cancer Research Center for Prevention and Therapy
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  • For correspondence: [email protected] [email protected] [email protected]
Hua Guo
2Department of Tumor Cell Biology
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  • For correspondence: [email protected] [email protected] [email protected]
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  • Figure 1
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    Figure 1

    The median plasma levels of AFP (A), AFU (B), GPC3 (C), GGT-II (D), and HGF (E) in the test cohort and AFP (F) and AFU (G) in the validation cohort. HC, healthy controls; CH, chronic hepatitis; LC, liver cirrhosis; HCC, hepatocellular carcinoma. *P < 0.05; **P < 0.01; ***P < 0.001; P > 0.05 means no significance (NS).

  • Figure 2
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    Figure 2

    The receiver operating characteristic curve of AFP (A), AFU (B), GPC3 (C), GGT-II (D), HGF (E), AFP + AFU + GGT-II + GPC3 + HGF (F), AFP + AFU + GPC3 + HGF (G), AFP + AFU + HGF (H), and AFP + AFU (I) in the detection of the NBNC-HCC test group. The sensitivity and specificity represented by the red dots are shown in detail (lower). (A). AFP sensitivity: 59.3% and specificity: 98.9%; (B). AFU sensitivity: 85.2% and specificity: 98.9%; (C). GPC3 sensitivity: 100.0% and specificity: 72.6%; (D). GGT-II sensitivity: 92.6% and specificity: 58.3%; (E). HGF sensitivity: 51.9% and specificity: 88.6%; (F). AFP + AFU + GPC3 + GGT-II + HGF sensitivity: 92.6% and specificity: 98.9%; (G). AFP + AFU + GPC3 + HGF sensitivity: 92.6% and specificity: 99.4%; (H). AFP + AFU + HGF sensitivity: 92.6% and specificity: 99.4%; (I). AFP + AFU sensitivity: 92.6% and specificity: 98.9%.

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    Figure 3

    Diagnostic outcomes and nomograms for the combination of serum AFP and AFU in the diagnosis of NBNC-HCC. (A). Receiver operating characteristic curves (ROCs) for AFU, AFP, or both for all patients with NBNC-HCC vs. HC in the test cohort. (B). ROC curves for AFU, AFP, or both for all patients with NBNC-HCC vs. HC in the validation cohort. (C). Nomogram of the combined AFP/AFU in diagnosing NBNC-HCC.

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    Figure 4

    The receiver operating characteristic curves of AFP (A), AFU (B), GPC3 (C), GGT-II (D), and HGF (E), AFP + AFU + HGF (F), AFP + AFU (G), AFP + HGF (H), AFU + HGF (I) in the detection of all-stage HBV-HCC and HCV-HCC of the test group. The sensitivity and specificity represented by the red dots are shown in detail (lower). (A). AFP sensitivity: 52.8% and specificity: 93.7%; (B). AFU sensitivity: 71.5% and specificity: 67.1%; (C). GPC3 sensitivity: 91.1% and specificity: 25.9%; (D). GGT-II sensitivity: 73.2% and specificity: 38.5%; (E). HGF sensitivity: 61.8% and specificity: 75.5%; (F). AFP + AFU + HGF sensitivity: 65.9% and specificity: 89.5%; (G). AFP + AFU sensitivity: 69.1% and specificity: 87.4%; (H). AFP + HGF sensitivity: 74.8% and specificity: 79.0%; (I). AFU + HGF sensitivity: 63.4% and specificity: 76.9%.

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    Figure 5

    The receiver operating characteristic curves of AFP (A), AFU (B), GPC3 (C), GGT-II (D), and HGF (E), AFP + AFU + HGF (F), AFP + AFU (G), AFP + HGF (H), and AFU + HGF (I) in the detection of early-stage HBV-HCC and HCV-HCC of the test group. The sensitivity and specificity represented by the red dots are shown in detail (lower). (A). AFP sensitivity: 44.3% and specificity: 93.7%; (B). AFU sensitivity: 63.9% and specificity: 67.1%; (C). GPC3 sensitivity: 86.9% and specificity: 28.0%; (D). GGT-II sensitivity: 96.7% and specificity: 11.9%; (E). HGF sensitivity: 50.8% and specificity: 75.5%; (F). AFP + AFU + HGF sensitivity: 52.5% and specificity: 90.2%; (G). AFP + AFU sensitivity: 52.5% and specificity: 91.6%; (H). AFP + HGF sensitivity: 50.8% and specificity: 90.9%; (I). AFU + HGF sensitivity: 34.4% and specificity: 93.0%.

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    Figure 6

    Diagnostic outcomes and nomogram for the combination of serum AFP and AFU of all-stage and early stage hepatitis-related hepatocellular carcinoma (HCC). (A). Receiver operating characteristic curves (ROCs) for AFU, AFP, or both for all patients with all-stage HBV-HCC and HCV-HCC vs. CH and LC in the test cohort. (B). ROC curves for AFU, AFP, or both for all patients with all-stage HBV-HCC and HCV-HCC vs. CH and LC in the validation cohort. (C). ROC curves for AFU, AFP, or both for all patients with early-stage HBV-HCC and HCV-HCC vs. CH and LC in the test cohort. (D). ROC curves for AFU, AFP, or both for all patients with early-stage HBV-HCC and HCV-HCC vs. CH and LC in the validation cohort. (E). Nomogram of the combined AFP/AFU in diagnosing HBV-HCC and HCV-HCC.

Tables

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    Table 1

    Results for the measurement of serum AFU, AFP, or both, in the diagnosis of NBNC-HCC

    TestValidation
    AUC
    (95% CI)
    Sensitivity
    (%)
    Specificity
    (%)
    PPV
    (%)
    NPV
    (%)
    Positive
    LR
    Negative
    LR
    P
    value
    AUC
    (95% CI)
    Sensitivity
    (%)
    Specificity
    (%)
    PPV
    (%)
    NPV
    (%)
    Positive
    LR
    Negative
    LR
    P
    value
    NBNC-HCC vs. HC (results for measurement of AFU, AFP, or both in the diagnosis of NBNC-HCC)
    AFP0.792 (0.729–0.845)59.3%98.9%88.9%94.0%51.850.41<0.0010.707 (0.639–0.769)51.9%97.7%77.8%92.8%22.250.490.002
    AFU0.967 (0.932–0.987)85.2%98.9%92.0%97.7%74.540.15<0.0010.948 (0.907–0.974)74.1%96.5%76.9%96.0%21.230.27<0.001
    AFP + AFU0.986 (0.958–0.997)92.6%98.9%92.6%98.9%81.020.075<0.0010.969 (0.934–0.988)88.9%94.8%72.7%98.2%16.990.12<0.001

    The diagnostic cutoff values of serum AFP and AFU were 43.23 ng/mL and 16.75 mU/mL, respectively.

      • View popup
      Table 2

      Results for measurement of serum AFU, AFP, or both, in the diagnosis of HBV-HCC and HCV-HCC

      TestValidation
      AUC
      (95% CI)
      Sensitivity
      (%)
      Specificity
      (%)
      PPV
      (%)
      NPV
      (%)
      Positive
      LR
      Negative
      LR
      P
      value
      AUC
      (95% CI)
      Sensitivity
      (%)
      Specificity
      (%)
      PPV
      (%)
      NPV
      (%)
      Positive
      LR
      Negative
      LR
      P
      value
      Hepatitis-HCC vs. CH and LC (results for the measurement of AFU, AFP, or both in diagnosis of hepatitis-HCC)
      AFP0.780 (0.725–0.828)52.8%93.7%87.8%69.8%8.400.50<0.0010.809 (0.755–0.855)62.8%90.2%85.4%72.7%6.410.41<0.001
      AFU0.752 (0.696–0.803)71.5%67.1%65.2%73.3%2.180.42<0.0010.727 (0.668–0.781)69.4%65.4%64.6%70.2%2.000.47<0.001
      AFP + AFU0.835 (0.784–0.877)69.1%87.4%82.5%76.7%5.490.35<0.0010.841 (0.790–0.884)71.9%86.5%82.9%77.2%5.310.32<0.001
      Early hepatitis-HCC vs. CH and LC (results for measurement of AFU, AFP, or both in diagnosis of early hepatitis-HCC)
      AFP0.741 (0.675–0.800)44.3%93.7%75.0%79.8%7.030.59<0.0010.758 (0.693–0.816)52.2%90.2%73.5%78.4%5.330.53<0.001
      AFU0.666 (0.597–0.730)63.9%67.1%45.3%81.4%1.940.54<0.0010.671 (0.602–0.736)56.5%65.4%45.9%74.4%1.630.67<0.001
      AFP + AFU0.776 (0.712–0.831)52.5%91.6%72.7%81.9%6.250.52<0.0010.791 (0.728–0.845)75.4%73.7%59.8%85.2%2.860.33<0.001

      The diagnostic cutoff values of serum AFP and AFU were 42.34 ng/mL and 13.94 mU/mL, respectively.

      Supplementary Materials

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      Diagnostic value of 5 serum biomarkers for hepatocellular carcinoma with different epidemiological backgrounds: A large-scale, retrospective study
      Dongming Liu, Yi Luo, Lu Chen, Liwei Chen, Duo Zuo, Yueguo Li, Xiaofang Zhang, Jing Wu, Qing Xi, Guangtao Li, Lisha Qi, Xiaofen Yue, Xiehua Zhang, Zhuoyu Sun, Ning Zhang, Tianqiang Song, Wei Lu, Hua Guo
      Cancer Biology & Medicine Feb 2021, 18 (1) 256-270; DOI: 10.20892/j.issn.2095-3941.2020.0207

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      Diagnostic value of 5 serum biomarkers for hepatocellular carcinoma with different epidemiological backgrounds: A large-scale, retrospective study
      Dongming Liu, Yi Luo, Lu Chen, Liwei Chen, Duo Zuo, Yueguo Li, Xiaofang Zhang, Jing Wu, Qing Xi, Guangtao Li, Lisha Qi, Xiaofen Yue, Xiehua Zhang, Zhuoyu Sun, Ning Zhang, Tianqiang Song, Wei Lu, Hua Guo
      Cancer Biology & Medicine Feb 2021, 18 (1) 256-270; DOI: 10.20892/j.issn.2095-3941.2020.0207
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      Keywords

      • hepatocellular carcinoma
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      • AFP
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