Cancer Research and Treatment

Original Articles

Gastrointestinal cancer

Evaluation of the American Joint Committee on Cancer (AJCC) 8th Edition Staging System for Hepatocellular Carcinoma in 1,008 Patients with Curative Resection: Sujin Park, Sangjoon Choi, Yoon Ah Cho, Dong Hyun Sinn, Jong Man Kim, Cheol-Keun Park, Sang Yun Ha; Cancer Res Treat. 2020;52(4):1145-1152. Published online April 28, 2020; DOI: https://doi.org/10.4143/crt.2020.208

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Purpose
Recently, the 8th edition staging system of the American Joint Committee on Cancer (AJCC) for hepatocellular carcinoma (HCC) was released, including a change in T category. We aimed to validate the new AJCC system.
Materials and Methods
The predictive value of the new AJCC was validated in comparison to the previous edition, in a total 1,008 patients who underwent curative resection for HCC as initial treatment.
Results
The 2-year area under the curve values for recurrence-free survival (RFS) and overall survival (OS) were comparable in the 7th and 8th editions. Stage migration was observed in 63 patients (6.3%); from T2 to T1a for 44 patients and from T3 to T4 for 19 patients. The RFS and OS were not different between T1a and T1b in the 8th edition. For solitary tumors ≤ 2 cm, those with microvascular invasion had lower RFS and OS values than those without although they were all classified as T1a in the 8th edition. Tumors involving a major branch of the portal or hepatic vein (T4 by the 8th edition and T3b by the 7th edition) had shorter RFS and OS than multifocal tumors, at least one of which was > 5 cm (T3 by the 8th edition and T3a by the 7th edition).
Conclusion
The AJCC 8th edition staging system for HCC showed comparable predictive performance to the 7th edition. It is desirable in a future revision to consider sub-stratification of solitary tumors ≤ 2 cm (T1a) depending on the presence of vascular invasion, which is not included in the 8th edition.

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Improving Adherence of Young Male Patients with HBV Infection to the Regular Follow-Up via Mobile Healthcare Platform Might Be Cost-Effective to Decrease the Morbidity of Advanced Liver Cancer
Hao Liang, Min Yang, Dan Luo, Ya-Kun Wu
Patient Preference and Adherence.2024; Volume 18: 2581. CrossRef
Prognostic impact of tumor size on isolated hepatocellular carcinoma without vascular invasion may have age variance
Yi Zhang, Jun-Gang Zhang, Wei Yu, Lei Liang, Chun Wu, Cheng-Wu Zhang, Ya-Ming Xie, Dong-Sheng Huang, Ying Shi
Frontiers in Surgery.2023;[Epub] CrossRef
Advances in post-operative prognostic models for hepatocellular carcinoma
Ziqin He, Xiaomin She, Ziyu Liu, Xing Gao, Lu Lu, Julu Huang, Cheng Lu, Yan Lin, Rong Liang, Jiazhou Ye
Journal of Zhejiang University-SCIENCE B.2023; 24(3): 191. CrossRef
2022 KLCA-NCC Korea practice guidelines for the management of hepatocellular carcinoma

Journal of Liver Cancer.2023; 23(1): 1. CrossRef
Overall survival among patients who undergo resection does not differ significantly between T1a and T1b hepatocellular carcinoma based on the 8th American Joint Commission on Cancer
Yueh-Wei Liu, Wei-Feng Li, Fang-Ying Kuo, Hock-Liew Eng, Chih-Chi Wang, Chih-Che Lin, Chee-Chien Yong, Yi-Hao Yen
Langenbeck's Archives of Surgery.2023;[Epub] CrossRef
Perfusion parameters of triphasic computed tomography hold preoperative prediction value for microvascular invasion in hepatocellular carcinoma
Li Zhang, Guodong Pang, Jing Zhang, Zhenguo Yuan
Scientific Reports.2023;[Epub] CrossRef
AATF inhibition exerts antiangiogenic effects against human hepatocellular carcinoma
Diwakar Suresh, Akshatha N. Srinivas, Akila Prashant, Suchitha Satish, Prashant Vishwanath, Suma M. Nataraj, Srinivas V. Koduru, Prasanna K. Santhekadur, Divya P. Kumar
Frontiers in Oncology.2023;[Epub] CrossRef
ESR1 Regulates the Obesity- and Metabolism-Differential Gene MMAA to Inhibit the Occurrence and Development of Hepatocellular Carcinoma
Yiyin Zhang, Jiaxi Cheng, Cheng Zhong, Qiming Xia, Yirun Li, Peng Chen, Xiaoxiao Fan, Qijiang Mao, Hui Lin, Defei Hong
Frontiers in Oncology.2022;[Epub] CrossRef
Efficacy of Postoperative Adjuvant Transcatheter Arterial Chemoembolization in Hepatocellular Carcinoma Patients With Microscopic Portal Vein Invasion
Yiwen Qiu, Yi Yang, Tao Wang, Shu Shen, Wentao Wang
Frontiers in Oncology.2022;[Epub] CrossRef
Nomogram Based on Inflammatory Biomarkers to Predict the Recurrence of Hepatocellular Carcinoma—A Multicentre Experience
Zehao Zheng, Renguo Guan, Yiping Zou, Zhixiang Jian, Ye Lin, Rongping Guo, Haosheng Jin
Journal of Inflammation Research.2022; Volume 15: 5089. CrossRef
CSTF2 Acts as a Prognostic Marker Correlated with Immune Infiltration in Hepatocellular Carcinoma
Wang Zhang, Yipeng Wan, Yue Zhang, Qi Liu, Xuan Zhu
Cancer Management and Research.2022; Volume 14: 2691. CrossRef
2022 KLCA-NCC Korea practice guidelines for the management of hepatocellular carcinoma

Clinical and Molecular Hepatology.2022; 28(4): 583. CrossRef
Revisiting Surgical Strategies for Hepatocellular Carcinoma With Microvascular Invasion
Er-lei Zhang, Qi Cheng, Zhi-yong Huang, Wei Dong
Frontiers in Oncology.2021;[Epub] CrossRef
Two-Trait Predictor of Venous Invasion on Contrast-Enhanced CT as a Preoperative Predictor of Outcomes for Early-Stage Hepatocellular Carcinoma After Hepatectomy
Xinming Li, Xuchang Zhang, Zhipeng Li, Chuanmiao Xie, Shuping Qin, Meng Yan, Qiying Ke, Xuan Jin, Ting Lin, Muyao Zhou, Wen Liang, Zhendong Qi, Zhijun Geng, Xianyue Quan
Frontiers in Oncology.2021;[Epub] CrossRef
Construction and Validation of an Immune Cell Signature Score to Evaluate Prognosis and Therapeutic Efficacy in Hepatocellular Carcinoma
Linfeng Xu, Xingxing Jian, Zhenhao Liu, Jingjing Zhao, Siwen Zhang, Yong Lin, Lu Xie
Frontiers in Genetics.2021;[Epub] CrossRef
Up-to-date Knowledge on the Pathological Diagnosis of Hepatocellular Carcinoma
Ji Hae Nahm, Young Nyun Park
The Korean Journal of Gastroenterology.2021; 78(5): 268. CrossRef

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The Overexpression of CCAR1 in Hepatocellular Carcinoma Associates with Poor Prognosis: Sang Yun Ha, Jeong Hoon Kim, Jung Wook Yang, Jimin Kim, Binnari Kim, Cheol-Keun Park; Cancer Res Treat. 2016;48(3):1065-1073. Published online October 16, 2015; DOI: https://doi.org/10.4143/crt.2015.302

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Purpose
Cell division cycle and apoptosis regulator 1 (CCAR1) plays a dynamic role in regulation of cell growth and apoptosis by serving as a cofactor of steroid/thyroid nuclear receptors, β- catenin, and p53 in a variety of cell types including different cancer cells. However, whether CCAR1 protein is overexpressed in hepatocellular carcinoma (HCC) and the prognostic significance of CCAR1 protein expression in HCC have not been reported. Materials and Methods In 167 HCC patients with long-term follow-up, CCAR1 protein expression was examined by immunohistochemistry.
Results
High CCAR1 protein expression was observed in 149 of the 167 HCC cases (89.2%) and showed significant correlation with microvascular invasion, intrahepatic metastasis, higher American Joint Committee on Cancer (AJCC) T stage, and early recurrence. High CCAR1 expression showed an unfavorable effect on recurrence-free survival (RFS) (p=0.002). In subgroup analysis, among patients with α-fetoprotein ≤ 20 ng/mL (n=54) and patients with AJCC T stage 1 (n=62), significant differences in RFS were observed between high CCAR1 expression groups and low CCAR1 expression groups (p=0.015 and p=0.004, respectively). High CCAR1 expression tended to be an independent predictor of shorter RFS (p=0.054) and showed an unfavorable effect on overall survival (OS) (p=0.015). In subgroup analysis, among patients with α-fetoprotein ≤ 20 ng/mL (n=54), significant difference in OS was observed between high CCAR1 expression group and low CCAR1 expression group (p=0.046). Conclusion CCAR1 protein could be a potential biomarker predicting RFS in HCC patients after curative hepatectomy. In addition, CCAR1 had prognostic values in HCC patients with normal serum α-fetoprotein levels or early stage HCC.

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Oncotarget.2016; 7(17): 24097. CrossRef

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The Prognostic Role of Mitotic Index in Hepatocellular Carcinoma Patients after Curative Hepatectomy: Sang Yun Ha, Misun Choi, Taebum Lee, Cheol-Keun Park; Cancer Res Treat. 2016;48(1):180-189. Published online March 18, 2015; DOI: https://doi.org/10.4143/crt.2014.321

Abstract PDF Supplementary Material PubReader ePub

Purpose
High proliferation rate is a hallmark of cancer. The mitotic index is a useful and simple method for analysis of cell proliferation. However, the practical utility of mitotic index as a predictor of prognosis in patients with hepatocellular carcinoma (HCC) has not been determined. Therefore, we examined mitotic index as a prognostic marker in HCC patients.
Materials and Methods
We counted the number of mitotic cells in 10 high-power fields of the tumor area on hematoxylin and eosin–stained slides representing 282 surgically resected HCCs. The highest number of mitotic cells was defined as the mitotic index.
Results
High mitotic index was observed in 127 of 282 HCCs. High mitotic index showed significant association with younger age, larger tumor size, higher Edmondson grade, microvascular invasion, major portal vein invasion, intrahepatic metastasis, higher American Joint Committee on Cancer (AJCC) T-stage, higher Barcelona Clinic Liver Cancer (BCLC) stage, higher alpha-fetoprotein level, hepatitis B virus etiology, and liver cirrhosis. Patients with high mitotic index had shorter disease-specific survival (DSS) (p < 0.001) and tended to have shorter recurrence-free survival (p=0.112). In subgroup analysis among patients with a larger tumor size, microvascular invasion, intrahepatic metastasis, higher AJCC T-stage, and higher BLCL stage, high mitotic index showed unfavorable influences on DSS (p=0.001, p=0.008, p=0.003, p=0.012, and p < 0.001, respectively). In addition, high mitotic index was an independent predictor of shorter DSS (p=0.004).
Conclusion
High mitotic index may be a novel predictor of DSS in patients with HCC and may have utility as an auxiliary prognostic factor in HCC.

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Gastroenteropancreatic Neuroendocrine Tumors with Liver Metastases in Korea: A Clinicopathological Analysis of 72 Cases in a Single Institute: Yooju Shin, Sang Yun Ha, Jiyeon Hyeon, Boram Lee, Jeeyun Lee, Kee-Taek Jang, Kyoung-Mee Kim, Young Suk Park, Cheol-Keun Park; Cancer Res Treat. 2015;47(4):738-746. Published online February 16, 2015; DOI: https://doi.org/10.4143/crt.2014.224

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Purpose
Management of gastroenteropancreatic (GEP) neuroendocrine tumors with liver metastases (NETLM) presents many clinical challenges. Assessment of the extent of disease and primary tumor site is crucial for management. In this study, we investigated the primary tumor sites and prognostic factors in GEP NETLM among Korean patients. Materials and Methods We reviewed the medical records of 72 Korean patients diagnosed with GEP NETLM between January 1999 and May 2013, focusing on their clinical and pathologic characteristics.
Results
The most frequently encountered primary tumor sites were the pancreas (n=25, 35%), stomach (n=8, 11%), gall bladder (n=4, 6%) and rectum (n=3, 4%). Twenty-five patients (35%) had occult primary tumor. Twelve patients (17%) had histological grade G1 tumors, 30 patients (42%) had G2 tumors, and 30 patients (42%) had G3 tumors. The mean follow-up period after histological confirmation of hepatic metastases was 11.30±2.44 months for G3 tumors, 19.67±4.09 months for G2 tumors, and 30.67±6.51 months for G1 tumors. Multivariate analyses revealed that an unknown primary tumor site (p=0.001) and higher histological grade (p < 0.001) were independent prognostic indicators for shorter overall survival (OS). Most long-term survivors (OS > 24 months) had received antitumor treatment. Conclusion The primary tumor site most frequently associated with GEP NETLM was the pancreas. Unknown primary tumor and higher histological grade were independent prognostic indicators for shorter OS. Patients identified as being at a risk of shorter OS should be followed up closely.

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ATAD2 as a Poor Prognostic Marker for Hepatocellular Carcinoma after Curative Resection: Hye Won Hwang, Sang Yun Ha, Heejin Bang, Cheol-Keun Park; Cancer Res Treat. 2015;47(4):853-861. Published online February 16, 2015; DOI: https://doi.org/10.4143/crt.2014.177

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Purpose
Cancer cells frequently express genes that are specifically or preferentially expressed in male germ cells under normal conditions. The ATPase family AAA domain-containing 2 (ATAD2) is one such and works as an important cofactor for MYC-dependent transcription. In hepatocellular carcinoma (HCC), ATAD2 has been identified as a candidate driver gene located within the amplified 8q24 locus. However, the prognostic significance of ATAD2 protein expression in HCC remains uncertain. Materials and Methods We investigated ATAD2 protein expression by immunohistochemistry in tumor tissue from 182 HCC patients who underwent curative resection. Associations of ATAD2 expression with clinicopathologic variables or prognosis of HCC patients were analyzed.
Results
ATAD2 expression was observed in 119 (65.4%) of the 182 HCCs and tended to be independent predictor of early recurrence (p=0.059). ATAD2 expression showed an unfavorable influence on recurrence-free survival (RFS) (p < 0.001). Subgroup analysis among patients with tumor size ≤ 5.0 cm (n=109), patients at Barcelona Clinic Liver Cancer stage 0 or A (n=92), and patients with α-fetoprotein ≤ 20 ng/mL (n=61), the ATAD2-positive groups unfavorably influenced RFS (p=0.008, p=0.009, and p=0.013, respectively). In addition, ATAD2 expression was an independent predictor of shorter RFS (p=0.002). ATAD2 expression showed an unfavorable influence on disease-specific survival (p=0.001), but was not an independent predictor of shorter disease-specific survival (p=0.109). Conclusion ATAD2 protein expression may be a potential predictor of RFS in HCC patients after curative resection and ATAD2 may have prognostic value in patients with early stage HCC or normal serum α-fetoprotein level.

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Expression of PEG10 Is Associated with Poor Survival and Tumor Recurrence in Hepatocellular Carcinoma: Heejin Bang, Sang Yun Ha, Soo Hyun Hwang, Cheol-Keun Park; Cancer Res Treat. 2015;47(4):844-852. Published online February 13, 2015; DOI: https://doi.org/10.4143/crt.2014.124

Abstract PDF PubReader ePub

Purpose
Paternally expressed gene 10 (PEG10), first identified as an imprinted gene, is paternally expressed and maternally silenced. In hepatocellular carcinoma (HCC), PEG10 has been identified as a potential target gene located within the amplified 7q21 locus. The purpose of this study was to investigate the expression of PEG10 protein in HCC and evaluate its prognostic significance. Materials and Methods PEG10 protein expression was examined by immunohistochemistry in tumor tissues from 218 HCC patients undergoing curative resection. Furthermore, the relationships between PEG10 expression and clinicopathologic features or postoperative survival of HCC patients were evaluated. The median follow-up period was 119.8 months for survivors.
Results
PEG10 expression was observed in 148 of the 218 HCCs (67.9%) and was significantly correlated with younger age, female, higher Edmondson grade, microvascular invasion, intrahepatic metastasis, higher American Joint Committee on Cancer T-stage, and higher α-fetoprotein level. PEG10 expression was an independent predictor of early recurrence (p=0.013), and it showed an unfavorable influence on recurrence-free survival (p < 0.001). A subgroup analysis showed that among patients with α-fetoprotein ≤ 20 ng/mL (80 patients), the PEG10-positive group also showed an unfavorable influence on recurrencefree survival (p=0.002). Moreover, a multivariate survival analysis identified PEG10 as an independent predictor of shorter recurrence-free survival (p=0.005). PEG10 expression showed an unfavorable influence on overall survival (p=0.007) but was not an independent predictor of shorter overall survival (p=0.128). Conclusion PEG10 protein could be a potential biomarker predicting early recurrence and recurrencefree survival in HCC patients after curative resection, even in those with normal serum α-fetoprotein levels.

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