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Volume 20(2); September 2020
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Review Articles
Imaging Modalities for Hepatocellular Carcinoma Surveillance: Expanding Horizons beyond Ultrasound
Hyo Jung Park, So Yeon Kim
J Liver Cancer. 2020;20(2):99-105.   Published online September 30, 2020
DOI: https://doi.org/10.17998/jlc.20.2.99
  • 2,989 Views
  • 166 Downloads
  • 1 Citation
AbstractAbstract PDF
In Asian countries favoring loco-regional treatment such as surgical resection or ablation, very early-stage hepatocellular carcinoma (HCC) should be the main target for surveillance. Even though ultrasound (US) has been accepted as a primary imaging modality for HCC surveillance, its performance in detecting very early-stage HCCs is insufficient. Moreover, in more than 20% of patients at high risk for HCC, visualization of the liver on US may be limited owing to the advanced distortion and heterogeneity of the liver parenchyma. Recently revised HCC clinical guidelines allow the use of alternative surveillance tools including computed tomography or magnetic resonance imaging in patients with inadequate US exams. This paper summarizes the findings of recent studies using imaging modalities other than US as surveillance tools for HCC as well as strengths and limitations of these modalities.

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Citations to this article as recorded by  
  • Imaging features of hepatobiliary MRI and the risk of hepatocellular carcinoma development
    Jong-In Chang, Dong Hyun Sinn, Woo Kyoung Jeong, Jeong Ah Hwang, Ho Young Won, Kyunga Kim, Wonseok Kang, Geum-Youn Gwak, Yong-Han Paik, Moon Seok Choi, Joon Hyeok Lee, Kwang Cheol Koh, Seung-Woon Paik
    Scandinavian Journal of Gastroenterology.2022; 57(12): 1470.     CrossRef
Prognostic Significance of Preoperative Controlling Nutritional Status Score in Patients Who Underwent Hepatic Resection for Hepatocellular Carcinoma
Bum-Soo Kim
J Liver Cancer. 2020;20(2):106-112.   Published online September 30, 2020
DOI: https://doi.org/10.17998/jlc.20.2.106
  • 2,004 Views
  • 70 Downloads
AbstractAbstract PDF
Malnutrition is common in patients with hepatocellualar carcinoma (HCC), and is associated with postoperative complications after hepatectomy, and also increased mortality. However, there is currently no recommendation for assessment of nutritional status in HCC patients. The controlling nutritional status (CONUT) score has been correlated with prognosis in gastrointestinal cancer patients, but there are few reports on the prognostic significance of the CONUT score in patients who underwent hepatectomy for HCC. Existing results show that patients with high CONUT scores who undergo hepatectomy for HCC have poorer survival outcomes, and experience more complications than other patients. In this paper, we review the literature, and reveal that patients who underwent hepatectomy for HCC with high preoperative CONUT scores had poorer outcomes than those with low CONUT scores. Therefore, we conclude that a preoperative CONUT score may be useful for prognostic prediction in patients with HCC undergoing curative hepatectomy.
Is Transarterial Chemoembolization Only Treatment Option in Patients with Intermediate Stage of Hepatocellular Carcinoma?: in Perspectives of Surgery
Ji Young Lim, Minjong Lee, Tae Hun Kim
J Liver Cancer. 2020;20(2):113-119.   Published online September 30, 2020
DOI: https://doi.org/10.17998/jlc.20.2.113
  • 2,457 Views
  • 116 Downloads
AbstractAbstract PDF
In the Barcelona Clinic Liver Cancer staging system, intermediate stage hepatocellular carcinoma (HCC) is defined as large multinodular tumors without vascular invasion or extrahepatic spread in an asymptomatic patient with good performance status. Intermediate stage HCC includes various subgroups and it is characterized by extensive heterogeneity. Current guidelines recommend transarterial chemoembolization (TACE) as the standard treatment modality for patients with intermediate stage HCC. Although TACE provides improved survival benefits compared with supportive care for patients with intermediate stage HCC, all of them are not good candidates for TACE. TACE refractoriness is another obstacle to effective treatment of patients with intermediate stage HCC. Given that many studies recently reported improved survival in patients treated with hepatic resection over TACE, we reviewed the survival outcomes of TACE and hepatic resection as a treatment strategy of intermediate stage HCC.
Original Articles
Validation of the Korean Liver Cancer Association-National Cancer Center 2018 Criteria for the Noninvasive Diagnosis of Hepatocellular Carcinoma Using Magnetic Resonance Imaging
Sunyoung Lee, Myeong-Jin Kim
J Liver Cancer. 2020;20(2):120-127.   Published online September 30, 2020
DOI: https://doi.org/10.17998/jlc.20.2.120
  • 2,060 Views
  • 78 Downloads
  • 1 Citation
AbstractAbstract PDF
Background
/Aims: This study aimed to assess the validity and diagnostic performance of the imaging criteria of Korean Liver Cancer Association-National Cancer Center (KLCA-NCC) 2018 using magnetic resonance imaging (MRI) in high-risk patients for HCC.
Methods
This retrospective study included 142 treatment-naïve patients (81 patients who underwent MRI with extracellular contrast agent and 61 who underwent MRI with hepatobiliary agent; 183 lesions including 149 HCCs) with a high risk of HCC who underwent multiphasic contrast-enhanced MRI from January to December 2015. All lesions were categorized according to the KLCA-NCC 2018 imaging diagnostic criteria by two readers, and per-lesion diagnostic performances were compared.
Results
According to the KLCA-NCC 2018, none (0%) of the 13 benign category lesions, 11 (44.0%) of 25 indeterminate category lesions, 15 (93.8%) of 16 probable HCC category lesions, and 97 (99.0%) of 98 definite HCC category lesions were ultimately diagnosed as HCCs. The sensitivity and specificity of definite HCC category were 65.1% and 97.1%, respectively, and those of the combination of definite and probable HCC categories were 75.2% and 94.1%, respectively. The sensitivity of the combination of definite and probable HCC categories was significantly higher than that of definite HCC (P<0.001), but the specificity was not significantly lower (P>0.999).
Conclusions
The noninvasive imaging diagnosis of KLCA-NCC 2018 on MRI is reliable and useful for diagnosing HCC in high-risk patients. Combining definite and probable HCC categories of KLCA-NCC 2018 improves the sensitivity while maintaining a high specificity.

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  • Diagnostic Performance of KLCA-NCC 2018 Criteria for Hepatocellular Carcinoma Using Magnetic Resonance Imaging: A Systematic Review and Meta-Analysis
    Dong Hwan Kim, Bohyun Kim, Seo Yeon Youn, Hokun Kim, Joon-Il Choi
    Diagnostics.2021; 11(10): 1763.     CrossRef
Infiltration of T Cells and Programmed Cell Death Ligand 1-expressing Macrophages as a Potential Predictor of Lenvatinib Response in Hepatocellular Carcinoma
Pil Soo Sung, Sung Woo Cho, Jaejun Lee, Hyun Yang, Jeong Won Jang, Si Hyun Bae, Jong Young Choi, Seung Kew Yoon
J Liver Cancer. 2020;20(2):128-134.   Published online September 30, 2020
DOI: https://doi.org/10.17998/jlc.20.2.128
  • 2,202 Views
  • 84 Downloads
  • 5 Citations
AbstractAbstract PDF
Background
/Aims: Lenvatinib was recently proven to be non-inferior to sorafenib in treating unresectable hepatocellular carcinoma (HCC) in a phase-3 randomized controlled trial. In this study, we investigated whether the response to lenvatinib was affected by tumor immunogenicity.
Methods
Between May 2019 and April 2020, nine patients with intermediate-to-advanced HCC, who were treated with lenvatinib after liver biopsy, were enrolled. Immunohistochemical staining and multi-color flow cytometry were performed on specimens obtained from liver biopsy.
Results
Among the nine patients enrolled, four showed objective responses (complete responses+partial responses). Immunohistochemical staining for CD3, CD68, and programmed cell death ligand 1 (PD-L1) demonstrated that patients with objective responses showed marked infiltration of T cells and PD-L1-expressing macrophages in intra-tumoral and peri-tumoral tissues compared to those without objective responses. A significant difference in the numbers of infiltrated T cells, both in the intra-tumoral (P<0.01) and peri-tumoral regions (P<0.05), were identified between responders and non-responders. Regarding the number of infiltrated macrophages, no significant difference was found between the responders and non-responders, although the number of PD-L1-expressing tumor-associated macrophages was significantly higher in responders than that in non-responders (P<0.05).
Conclusions
Tumor immunogenicity, as indicated by T cell and PD-L1-positive macrophage infiltration, affects lenvatinib response in unresectable HCC.

Citations

Citations to this article as recorded by  
  • Intrahepatic inflammatory IgA+PD-L1high monocytes in hepatocellular carcinoma development and immunotherapy
    Pil Soo Sung, Dong Jun Park, Pu Reun Roh, Kyoung Do Mun, Sung Woo Cho, Gil Won Lee, Eun Sun Jung, Sung Hak Lee, Jeong Won Jang, Si Hyun Bae, Jong Young Choi, Jonghwan Choi, Jaegyoon Ahn, Seung Kew Yoon
    Journal for ImmunoTherapy of Cancer.2022; 10(5): e003618.     CrossRef
  • Crosstalk between tumor-associated macrophages and neighboring cells in hepatocellular carcinoma
    Pil Soo Sung
    Clinical and Molecular Hepatology.2022; 28(3): 333.     CrossRef
  • Blood-based biomarkers for immune-based therapy in advanced HCC: Promising but a long way to go
    Pil Soo Sung, Isaac Kise Lee, Pu Reun Roh, Min Woo Kang, Jaegyoon Ahn, Seung Kew Yoon
    Frontiers in Oncology.2022;[Epub]     CrossRef
  • Immunological Mechanisms for Hepatocellular Carcinoma Risk after Direct-Acting Antiviral Treatment of Hepatitis C Virus Infection
    Pil Soo Sung, Eui-Cheol Shin
    Journal of Clinical Medicine.2021; 10(2): 221.     CrossRef
  • Preferential Expression of Programmed Death Ligand 1 Protein in Tumor-Associated Macrophages and Its Potential Role in Immunotherapy for Hepatocellular Carcinoma
    Dong-Jun Park, Pil-Soo Sung, Gil-Won Lee, Sung-Woo Cho, Sung-Min Kim, Byung-Yoon Kang, Won-Hee Hur, Hyun Yang, Soon-Kyu Lee, Sung-Hak Lee, Eun-Sun Jung, Chang-Ho Seo, Joseph Ahn, Ho-Joong Choi, Young-Kyoung You, Jeong-Won Jang, Si-Hyun Bae, Jong-Young Cho
    International Journal of Molecular Sciences.2021; 22(9): 4710.     CrossRef
Hepatocellular Carcinoma in Korea between 2012 and 2014: an Analysis of Data from the Korean Nationwide Cancer Registry
Young Eun Chon, Han Ah Lee, Jun Sik Yoon, Jun Yong Park, Bo Hyun Kim, In Joon Lee, Suk Kyun Hong, Dong Hyeon Lee, Hyun-Joo Kong, Eunyang Kim, Young-Joo Won, Jeong-Hoon Lee
J Liver Cancer. 2020;20(2):135-147.   Published online September 30, 2020
DOI: https://doi.org/10.17998/jlc.20.2.135
  • 2,487 Views
  • 121 Downloads
  • 10 Citations
AbstractAbstract PDFSupplementary Material
Background
/Aims: Considering the high prevalence and mortality of hepatocellular carcinoma (HCC) in Korea, accurate statistics for HCC are important. We evaluated the characteristics of Korean patients with newly diagnosed HCC.
Methods
We retrospectively evaluated data from the Korean Primary Liver Cancer Registry (KPLCR). The baseline characteristics, treatment modalities, and overall survival (OS) of 4,572 patients with HCC registered in the KPLCR between 2012 and 2014 were investigated.
Results
At the time of HCC diagnosis, the median age was 60.0 years, with male predominance (79.6%). Hepatitis B virus infection was the most common etiology (59.1%). The rates of Barcelona Clinic Liver Cancer (BCLC) stages 0, A, B, C, and D at diagnosis were 3.9%, 36.9%, 12.5%, 39.4%, and 7.3%, respectively. The proportion of very early or early stage HCC at diagnosis (BCLC stage 0 or A) in the 2012-2014 cohort was significantly lower than that in the 2008-2011 cohort (40.8% vs. 48.3%, P<0.001). Transarterial therapy (37.5%) was the most commonly performed initial treatment, followed by surgical resection (19.8%), best supportive care (19.1%), and local ablation (10.6%). The median OS was 2.9 years, and the 1-, 3-, and 5-year OS rates were 67.7%, 49.3% and 41.9%, respectively. The OS rate of the 2012-2014 cohort was significantly higher than that of the 2008-2011 cohort (log-rank, P<0.001).
Conclusions
The OS of HCC patients registered in the KPLCR between 2012 and 2014 significantly improved. Nevertheless, as about half of the HCC patients were diagnosed at an advanced stage, vigorous and optimized HCC screening strategies should be implemented.

Citations

Citations to this article as recorded by  
  • Hepatocellular carcinoma incidence is decreasing in Korea but increasing in the very elderly
    Young Eun Chon, Seong Yong Park, Han Pyo Hong, Donghee Son, Jonghyun Lee, Eileen Yoon, Soon Sun Kim, Sang Bong Ahn, Soung Won Jeong, Dae Won Jun
    Clinical and Molecular Hepatology.2023; 29(1): 120.     CrossRef
  • Surgical resection versus ablation for early hepatocellular carcinoma: The debate is still open
    Bo Hyun Kim
    Clinical and Molecular Hepatology.2022; 28(2): 174.     CrossRef
  • A case report of advanced hepatocellular carcinoma treated with hepatic arterial infusion chemotherapy and sorafenib combination therapy followed by metastasectomy of lung and muscle metastases
    Sang Yi Moon, Sang Young Han, Yang-Hyun Baek
    Journal of Liver Cancer.2022; 22(1): 57.     CrossRef
  • Cause of death and cause-specific mortality for primary liver cancer in South Korea: A nationwide population-based study in hepatitis B virus-endemic area
    Bo Hyun Kim, Dahhay Lee, Kyu-Won Jung, Young-Joo Won, Hyunsoon Cho
    Clinical and Molecular Hepatology.2022; 28(2): 242.     CrossRef
  • 2022 KLCA-NCC Korea practice guidelines for the management of hepatocellular carcinoma

    Clinical and Molecular Hepatology.2022; 28(4): 583.     CrossRef
  • Surveillance for hepatocellular carcinoma: It is time to move forward
    Bo Hyun Kim, Yuri Cho, Joong-Won Park
    Clinical and Molecular Hepatology.2022; 28(4): 810.     CrossRef
  • 2022 KLCA-NCC Korea Practice Guidelines for the Management of Hepatocellular Carcinoma

    Korean Journal of Radiology.2022; 23(12): 1126.     CrossRef
  • Hepatocellular Carcinoma in Korea: an Analysis of the 2015 Korean Nationwide Cancer Registry
    Jun Sik Yoon, Han Ah Lee, Hwi Young Kim, Dong Hyun Sinn, Dong Ho Lee, Suk Kyun Hong, Ju-Yeon Cho, Jonggi Choi, Young Chang, Hyun-Joo Kong, Eunyang Kim, Young-Joo Won, Jeong-Hoon Lee
    Journal of Liver Cancer.2021; 21(1): 58.     CrossRef
  • Cost-Effectiveness of Adjuvant Immunotherapy With Cytokine-Induced Killer Cell for Hepatocellular Carcinoma Based on a Randomized Controlled Trial and Real-World Data
    Jeong-Yeon Cho, Sun-Hong Kwon, Eui-Kyung Lee, Jeong-Hoon Lee, Hye-Lin Kim
    Frontiers in Oncology.2021;[Epub]     CrossRef
  • Efficacy of Hepatic Arterial Infusion Chemotherapy and Radiofrequency Ablation against Hepatocellular Carcinoma Refractory to Transarterial Chemoembolization and Vascular Variation: A Case Study
    Sang Yi Moon, Sang Young Han, Yang-Hyun Baek
    Kosin Medical Journal.2021; 36(2): 161.     CrossRef
Case Reports
Long-term Survival of a Patient with a Large Hepatocellular Carcinoma with Main Portal Vein Tumor Thrombosis and Spontaneous Tumor Rupture
Hyung-Woo Lee, Gi-Ae Kim, Chi Hyuk Oh, Jae-Jun Shim, Byung-Ho Kim
J Liver Cancer. 2020;20(2):148-153.   Published online September 30, 2020
DOI: https://doi.org/10.17998/jlc.20.2.148
  • 2,143 Views
  • 68 Downloads
AbstractAbstract PDF
Optimal treatments for patients with advanced hepatocellular carcinoma (HCC) are still limited and their prognosis remains dismal. Yet, there have been rare cases that have shed light on longer survival in these patients assisted by various treatments. This paper aims to present an extraordinary case of far advanced HCC that had been properly managed in spite of continuous recurrence. A patient visited the hospital with a ruptured large HCC with main portal vein tumor thrombosis but survived longer than 14 years owing to active and prompt interventions.
Ruptured Massive Hepatocellular Carcinoma Cured by Transarterial Chemoembolization
Ji Eun Lee, Joong-Won Park, In Joon Lee, Bo Hyun Kim, Seoung Hoon Kim, Hyun Beom Kim
J Liver Cancer. 2020;20(2):154-159.   Published online September 30, 2020
DOI: https://doi.org/10.17998/jlc.20.2.154
  • 1,761 Views
  • 48 Downloads
AbstractAbstract PDF
Spontaneous tumor rupture is a serious but rare complication of hepatocellular carcinoma (HCC) and has a low survival rate. Here, we report a case of massive HCC that ruptured and was treated successfully with transarterial chemoembolization (TACE). A 55-year-old man with abdominal pain was diagnosed with a 12-cm-wide ruptured HCC at segment 8. The overall liver function was scored as Child–Pugh A, but the single nodule tumor had ruptured; therefore, TACE treatment was initiated. After the first TACE treatment, residual tumors were found; thus, secondary TACE was performed 5 months later. No new lesions or extrahepatic metastases were found 16 months after the first TACE treatment, so hepatic resection was performed for curative treatment. The postoperative pathology results did not reveal any cancer cells; hence, TACE alone resulted in a cure. We report this case because the cure has been maintained for more than 3 years after resection.
Advanced Stage Hepatocellular Carcinoma Successfully Treated with Transarterial Radioembolization and Multi-tyrosine Kinase Inhibitor Therapy
Myung Ji Goh, Wonseok Kang, Dong Hyun Sinn, Geum-Youn Gwak, Yong-Han Paik, Moon Seok Choi, Joon Hyeok Lee, Kwang Cheol Koh, Seung Woon Paik
J Liver Cancer. 2020;20(2):160-166.   Published online September 30, 2020
DOI: https://doi.org/10.17998/jlc.20.2.160
  • 2,633 Views
  • 127 Downloads
AbstractAbstract PDF
Transarterial radioembolization (TARE) with yttrium-90 microspheres has become widely utilized in managing hepatocellular carcinoma (HCC). The utility of TARE is expanding with new insights through experiences from real-world practice and clinical trials, and recently published data suggest that TARE in combination with sorafenib may improve the overall survival in selected patients. Here, we report a case of advanced stage HCC that was successfully treated with TARE and sorafenib. The patient achieved complete response (CR) at 12 months after the initial treatment with TARE and sorafenib, followed by additional transarterial chemoembolization and proton beam therapy for local tumor recurrence at 19-month post-TARE. The patient was followed up every 3 months thereafter and still achieved CR both biochemically and radiologically for the following 12 months. A combination strategy of TARE and systemic therapy may be a useful alternative treatment option for selected patients with advanced stage HCC.
Huge Hepatocellular Carcinoma Exhibiting a Complete Response after Stereotactic Body Radiation Therapy
Kyung In Shin, Byoung Kuk Jang, Jin Hee Kim, Jae Seok Hwang
J Liver Cancer. 2020;20(2):167-172.   Published online September 30, 2020
DOI: https://doi.org/10.17998/jlc.20.2.167
  • 1,859 Views
  • 92 Downloads
AbstractAbstract PDF
To date, there are limited data and little consensus on treatment strategies for huge hepatocellular carcinoma (HCC). Surgical resection provides significantly better survival than other modalities for single large HCC regardless of tumor stage. Recently, with technological advances in radiation therapy, stereotactic body radiation therapy (SBRT) is considered an alternative treatment option for HCC. Herein, we present a case of huge HCC that was successfully managed by SBRT. Transarterial embolization, previously performed in Russia, was incomplete. It was also not suitable for resection and transarterial chemoembolization. Although the rationale for radiotherapy in huge HCC was insufficient, SBRT was performed because no other treatment options were available. Additional radiofrequency ablation was performed for small HCC in a different segment, and radiological complete response (CR) was achieved. The CR was maintained over 4 years. Therefore, SBRT may be an alternative treatment option for large HCC that is not suitable for curative treatment.
Rare Clinical and Radiologic Case of Cholangiocarcinoma Mimicking Pyogenic Abscess, Hepatic Echinococcal Cysts, and Metastases
Si Hyeong Lee, Soo Hyung Ryu, Dong Hoon Lee, Won Eui Yoon, Tae Young Park, Hye Kyung Lee, Jeong Seop Moon
J Liver Cancer. 2020;20(2):173-176.   Published online September 30, 2020
DOI: https://doi.org/10.17998/jlc.20.2.173
  • 1,865 Views
  • 62 Downloads
AbstractAbstract PDF
Cholangiocarcinoma is a biliary carcinoma with a wide spectrum of imaging, histological, and clinical features. In immunocompromised patients, pyogenic abscesses are relatively common and an echinococcal hepatic cysts are very rare. The authors experienced a very rare case of cholangiocarcinoma showing multiple hypodense masses with wall enhancement mimicking pyogenic liver abscess, echinococcal hepatic cyst, and cystic metastases. An 83-year-old man, complaining of fatigue and poor oral intake, presented to our outpatient clinic. Abdominal computed tomography (CT) revealed multiple, variable-sized hypodense masses with peripheral rim enhancement throughout the liver. Dynamic liver magnetic resonance images also showed findings similar to those of a CT scan. We performed ultrasound-guided biopsy of the mass which revealed cholangiocarcinoma.
Early Experience of Oncolytic Virus Injection Combined with Sorafenib in a Patient with Advanced Hepatocellular Carcinoma and Portal Vein Thrombosis
Hyun Ho Jo, Seong Joon Chun, Jeong-Ju Yoo, Min Hee Lee, Sang Gyune Kim, Young Seok Kim
J Liver Cancer. 2020;20(2):177-182.   Published online September 30, 2020
DOI: https://doi.org/10.17998/jlc.20.2.177
  • 2,500 Views
  • 62 Downloads
AbstractAbstract PDF
JX-594 is a modified oncolytic poxvirus designed to selectively replicate in and destroy cancer cells. In a pilot study, JX-594 injection followed by sorafenib was well-tolerated in three patients and associated with objective tumor responses. In this study, we report a case in which a patient with advanced hepatocellular carcinoma and portal vein thrombosis was treated with a combination of JX-594 and sorafenib.

JLC : Journal of Liver Cancer