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Review Article
Management of early-stage hepatocellular carcinoma: challenges and strategies for optimal outcomes
Jae Hyun Yoon, Sung Kyu Choi
J Liver Cancer. 2023;23(2):300-315.   Published online September 21, 2023
DOI: https://doi.org/10.17998/jlc.2023.08.27
  • 2,894 Views
  • 167 Downloads
  • 6 Citations
AbstractAbstract PDF
Although hepatocellular carcinoma (HCC) is associated with a poor prognosis, management of early-stage HCC is often successful with highly efficacious treatment modalities such as liver transplantation, surgical resection, and radiofrequency ablation. However, unfavorable clinical outcomes have been observed under certain circumstances, even after efficient treatment. Factors that predict unsuitable results after treatment include tumor markers, inflammatory markers, imaging findings reflecting tumor biology, specific outcome indicators for each treatment modality, liver functional reserve, and the technical feasibility of the treatment modalities. Various strategies may overcome these challenges, including the application of reinforced treatment indication criteria with predictive markers reflecting tumor biology, compensation for technical issues with up-to-date technologies, modification of treatment modalities, downstaging with locoregional therapies (such as transarterial chemotherapy or radiotherapy), and recently introduced combination immunotherapies. In this review, we discuss the challenges to achieving optimal outcomes in the management of early-stage HCC and suggest strategies to overcome these obstacles.

Citations

Citations to this article as recorded by  
  • Diosgenin potentiates the anticancer effect of doxorubicin and volasertib via regulating polo-like kinase 1 and triggering apoptosis in hepatocellular carcinoma cells
    Eman H. Yousef, Mohamed E. El-Mesery, Maha R. Habeeb, Laila A. Eissa
    Naunyn-Schmiedeberg's Archives of Pharmacology.2024; 397(7): 4883.     CrossRef
  • Comparison of Surgical Resection and Radiofrequency Ablation in Elderly Patients with Hepatocellular Carcinoma
    Jun Il Kim, Jayoun Lee, Gi Hong Choi, Min Woo Lee, Dong Ah Park, Jeong-Ju Yoo
    Digestive Diseases and Sciences.2024; 69(3): 1055.     CrossRef
  • Radiofrequency for hepatocellular carcinoma larger than 3 cm: potential for applications in daily practice
    Ji Hoon Kim, Pil Soo Sung
    Journal of Liver Cancer.2024; 24(1): 1.     CrossRef
  • Hepatocellular carcinoma outcomes and potential implications for surveillance in elderly patients
    Aryoung Kim, Goeun Park, Myung Ji Goh, Byeong Geun Song, Wonseok Kang, Geum-Youn Gwak, Yong-Han Paik, Moon Seok Choi, Joon Hyeok Lee, Dong Hyun Sinn
    Scientific Reports.2024;[Epub]     CrossRef
  • Trends in alcohol use and alcoholic liver disease in South Korea: a nationwide cohort study
    Jeong-Ju Yoo, Dong Hyeon Lee, Young Chang, Hoongil Jo, Young Youn Cho, Sangheun Lee, Log Young Kim, Jae Young Jang
    BMC Public Health.2024;[Epub]     CrossRef
  • Efficacy of Transarterial Chemoembolization (TACE) for Early-Stage Hepatocellular Carcinoma
    Moonhyung Lee, Hyun Phil Shin
    Medicina.2023; 59(12): 2174.     CrossRef
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Case Report
Curative liver transplantation after lung resection for advanced hepatocellular carcinoma with lung metastasis and inferior vena cava tumor thrombosis: a case report
Dong Jin Joo, Do Young Kim, Jinsil Seong, Hyun Jeong Kim, Jae Geun Lee, Dai Hoon Han, Gi Hong Choi, Myoung Soo Kim, Jin Sub Choi, Soon Il Kim
J Liver Cancer. 2021;21(2):181-186.   Published online September 30, 2021
DOI: https://doi.org/10.17998/jlc.2021.09.08
  • 4,133 Views
  • 98 Downloads
  • 1 Citation
AbstractAbstract PDF
Hepatocellular carcinoma (HCC) with distant metastasis is an absolute contraindication for liver transplantation (LT). However, it is still unclear whether LT is feasible or acceptable in such patients, albeit after being treated with a multidisciplinary approach and after any metastatic lesion is ruled out. We report one such successful treatment with living donor LT (LDLT) after completely controlling far-advanced HCC with inferior vena cava tumor thrombosis and multiple lung metastases. The patient has been doing well without HCC recurrence for eight years since LDLT. The current patient could be an anecdotal case, but provides a case for expanding LDLT indications in the context of advanced HCC and suchlike.

Citations

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  • Inferior Vena Cava Thrombectomy and Stenting as Bridge to Liver Transplantation After Radiotherapy-Induced Thrombosis
    Raphael PH Meier, Shani Kamberi, Josue Alvarez-Casas, Barton F. Lane, Chandra S. Bhati, Saad Malik, William Twaddell, Kirti Shetty, Adam Fang, Hyun S. Kim, Daniel G. Maluf
    Progress in Transplantation.2023;[Epub]     CrossRef
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Review Article
Liver transplantation for hepatocellular carcinoma with portal vein tumor thrombosis
Sang Jin Kim, Jong Man Kim
J Liver Cancer. 2021;21(2):105-112.   Published online September 2, 2021
DOI: https://doi.org/10.17998/jlc.2021.03.17
  • 5,424 Views
  • 234 Downloads
  • 3 Citations
AbstractAbstract PDF
Traditionally, liver transplantation for hepatocellular carcinoma with portal vein tumor thrombosis is not recommended. However, with recent developments in locoregional therapies for hepatocellular carcinoma, more aggressive treatments have been attempted for advanced hepatocellular carcinoma. Recently, various studies on locoregional therapies for downstaging followed by living donor liver transplantation reported inspiring overall survival and recurrence-free survival of patients. These downstaging procedures included three-dimensional conformal radiation therapy, trans-arterial chemoembolization, stereotactic body radiation therapy, trans-arterial radioembolization, hepatic arterial infusion chemotherapy and combinations of these therapies. Selection of the optimal downstaging protocol should depend on tumor location, biology and background liver status. The risk factors affecting outcome include pre-downstaging alpha-fetoprotein values, delta alpha-fetoprotein values, disappearance of portal vein tumor thrombosis on imaging and meeting the Milan criteria or not after downstaging. For hepatocellular carcinoma with portal vein tumor thrombosis, downstaging procedure with liver transplantation in mind would be helpful. If the reaction of the downstaged tumor is good, liver transplantation may be performed.

Citations

Citations to this article as recorded by  
  • Metastatic papillary renal cell carcinoma with portal vein tumor thrombosis confirmed on blind liver biopsy
    Hun Kim, Tae Hoon Roh, Jun Seop Lee, Min Seong Kim, Beom Kyung Kim
    Journal of Liver Cancer.2024; 24(1): 113.     CrossRef
  • Refining MRI-based criteria for portal vein invasion in hepatocellular carcinoma: improving sensitivity beyond portal vein tumor thrombosis
    Jeongju Kim, Woo Kyoung Jeong, Jong Man Kim, Sang Yun Ha, Kyunga Kim
    Abdominal Radiology.2023; 49(2): 437.     CrossRef
  • Prediction models of hepatocellular carcinoma recurrence after liver transplantation: A comprehensive review
    Sang Jin Kim, Jong Man Kim
    Clinical and Molecular Hepatology.2022; 28(4): 739.     CrossRef
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Case Report
Successful Sequential Therapy Involving Regorafenib after Failure of Sorafenib in a Patient with Recurrent Hepatocellular Carcinoma after Liver Transplantation
Soon Kyu Lee, Jeong Won Jang, Heechul Nam, Pil Soo Sung, Si Hyun Bae, Jong Young Choi, Seung Kew Yoon
J Liver Cancer. 2020;20(1):84-89.   Published online March 31, 2020
DOI: https://doi.org/10.17998/jlc.20.1.84
  • 3,635 Views
  • 92 Downloads
AbstractAbstract PDF
The efficacy and safety of sequential systemic therapy for the treatment of recurrent hepatocellular carcinoma (HCC) after liver transplantation (LT) are not well established. This study describes a successful experience where sequential therapy with sorafenib followed by regorafenib was used to treat recurrent HCC in a 54-year old male LT recipient. After HCC recurred in both lungs 10 months after LT, sorafenib was administered with radiation therapy to treat pulmonary metastases. However, after 4 months of sorafenib treatment showed progressive pulmonary metastases, sequential regorafenib treatment was started. After 3 months (cycles) of regorafenib treatment, tumor response was partial, and after 6 months (cycles), disease status remained stable without signs of progression or drug-related serious adverse events. This case suggests that sequential systemic therapy is feasible in patient with recurrent HCC after LT.
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Review Article
Liver Transplantation in Mixed Hepatocellular Carcinoma and Cholangiocarcinoma
Jong Man Kim
J Liver Cancer. 2019;19(2):85-90.   Published online September 30, 2019
DOI: https://doi.org/10.17998/jlc.19.2.85
  • 4,046 Views
  • 94 Downloads
  • 2 Citations
AbstractAbstract PDF
Mixed hepatocellular carcinoma and cholangiocarcinoma (HCC-CC) are rare tumors, and the risk factors associated with them are not well understood yet. Moreover, the diagnosis of mixed HCC-CC can be complicated due to the difficulty in distinguishing mixed HCC-CC from HCC and intrahepatic CCC on radiological images. Serum tumor markers are useful when the radiological images are inconclusive. It remains unclear whether the prognosis of mixed HCC-CC differs from that of HCC. However, several studies have reported that the tumor recurrence and patient survival rates of mixed HCC-CC were similar to those of HCC after liver transplantation (LT) and liver resection. In this paper, we report that LT in patients with mixed HCC-CC achieves outcomes which are similar to those seen in LT for HCC. Therefore, the diagnosis of mixed HCC-CC should not be considered as a contraindication for LT.

Citations

Citations to this article as recorded by  
  • Liver transplantation for combined hepatocellular carcinoma and cholangiocarcinoma: A multicenter study
    Jongman Kim, Dong-Jin Joo, Shin Hwang, Jeong-Moo Lee, Je-Ho Ryu, Yang-Won Nah, Dong-Sik Kim, Doo-Jin Kim, Young-Kyoung You, Hee-Chul Yu
    World Journal of Gastrointestinal Surgery.2023; 15(7): 1340.     CrossRef
  • The Role of Immunosuppression for Recurrent Cholangiocellular Carcinoma after Liver Transplantation
    Safak Gül-Klein, Paulina Schmitz, Wenzel Schöning, Robert Öllinger, Georg Lurje, Sven Jonas, Deniz Uluk, Uwe Pelzer, Frank Tacke, Moritz Schmelzle, Johann Pratschke, Ramin Raul Ossami Saidy, Dennis Eurich
    Cancers.2022; 14(12): 2890.     CrossRef
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Case Reports
Early Onset Polymorphic Post-transplant Lymphoproliferative Disease Mimicking a Solitary Necrotizing Abscess in a Graft Liver
Pil Soo Sung, Jaejun Lee, Joon Lee, Hee Chul Nam, Si Hyun Bae, Seung Kew Yoon
J Liver Cancer. 2019;19(2):165-170.   Published online September 30, 2019
DOI: https://doi.org/10.17998/jlc.19.2.165
  • 5,171 Views
  • 78 Downloads
AbstractAbstract PDF
Although post-transplantation lymphoproliferative disease (PTLD) after liver transplantation is very rare, its prognosis is worse than that of PTLD following other types of solid organ transplantation. Here, we report a rare case of early onset polymorphic PTLD in a graft liver occurring five months after deceased-donor liver transplantation due to hepatocellular carcinoma and hepatitis C virus infection. Initially, findings from contrast-enhanced magnetic resonance imaging mistakenly suspected the lesion was a necrotizing abscess with central necrosis. However, 18F-fluorodeoxyglucose positron emission tomography and biopsy findings confirmed an Epstein-Barr virus (EBV)-associated, B cell type polymorphic PTLD with central necrosis. Our case suggests regular monitoring of EBV serologic status for liver transplant recipients who were initially in an EBV seronegative state. Although early-onset PTLD is very rare after liver transplantation, PTLD should be suspected when recipients show the seroconversion for EBV proteins and the development of new tumors with various clinical presentations.
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A Case of Successful Living Donor Liver Transplantation after Downstaging of Hepatocellular Carcinoma with the Beyond Milan Criteria by Radioembolization, Hepatic Arterial Infusion Chemotherapy, and Stereotactic Body Radiation Therapy
Yeong Jin Kim, Yeon Seung Chung, Beom Kyung Kim, Jin Sil Sung, Do Young Kim
J Liver Cancer. 2017;17(2):182-185.   Published online September 30, 2017
DOI: https://doi.org/10.17998/jlc.17.2.182
  • 2,019 Views
  • 18 Downloads
AbstractAbstract PDF
Liver transplantation for patients with hepatocellular carcinoma (HCC) within the Milan criteria generally yields a 4-year overall survival rate of 75% and 4-year recurrence free survival rate of 83%. But, many HCC patients present with the disease beyond the Milan criteria. On the other hands, the overall survival of patients with advanced HCC with portal vein invasion is very poor. We report a
case
of successful living donor liver transplantation for advanced HCC with portal vein invasion by down-staging through radioembolization, hepatic arterial infusion chemotherapy, and stereotactic body radiation therapy.
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Review Article
Surgical Perspectives of Hepatocellular Carcinoma beyond the Barcelona Clinical Liver Cancer Guideline; Focusing on Liver Transplantation
Nam-Joon Yi, Gwang-Woong Lee, Kyoung-Suk Suh
J Liver Cancer. 2015;15(1):4-10.   Published online March 31, 2015
DOI: https://doi.org/10.17998/jlc.15.1.4
  • 960 Views
  • 16 Downloads
AbstractAbstract PDF
The management of hepatocellular carcinoma (HCC) is decided according to the evidence base recommendations generated by international societies especially by Barcelona clinical liver cancer (BCLC) guideline. However, the BCLC guideline based on studies of the Western countries, has not been well matched to real life cohort in Korea. In Western countries, a deceased donor liver transplantation has been well allocated to the HCC patients with preserved liver function. Patients with mild to moderate portal hypertension and certain BCLC B patients could be eligible for hepatic resection if a chance for 50% survival rate at 5 years is perceived. If liver transplantation (LT) is back up for liver resection in those patients as a salvage therapy, widening indication of liver resection could be much easily acceptable. On the other hands, new selection criteria of HCC beyond Milan criteria considering tumor biology, has been provided in the field of LT resulting in more than 50% survival rate at 5 years. Herein, surgical perspectives beyond the BCLC recommendation for LT for HCC would be reviewed in the respect of Korean surgeon’s view in this article.
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Case Report
Living Donor Liver Transplantation for Hepatocellular Carcinoma with Portal Vein Tumor Thrombus
YoungRok Choi, Kwang-Woong Lee, Hae Won Lee, Nam-Joon Yi, Kyung-Suk Suh
Journal of the Korean Liver Cancer Study Group. 2013;13(1):62-64.   Published online February 28, 2013
DOI: https://doi.org/10.17998/jlc.13.1.62
  • 1,289 Views
  • 8 Downloads
AbstractAbstract PDF
Malignant portal vein thrombosis is a contraindication to liver transplantation for hepatocellular carcinoma because of the high risk of its recurrence and the poor patient survival. With a newly developed immunosuppressant and a chemotherapeutic agent, however, living donor liver transplantation can be considered for a patient of hepatocellular carcinoma, showing a slow growth rate and good response for transarterial chemoembolization. We report a HBV related liver cirrhosis patient with HCC and portal vein tumor thrombus who underwent living donor liver transplantation and survived without recurrence of hepatocellular carcinoma for 18 months in our center.
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Review Articles
Strategies for the Curative Therapy of Early Stage HCC: Resection, Is It Real First Choice?
Wan-Bae Kim
Journal of the Korean Liver Cancer Study Group. 2012;12(2):97-101.   Published online September 30, 2012
  • 528 Views
  • 3 Downloads
AbstractAbstract PDF
Early stage HCC has generally been defined as the “Milan criteria”: a solitary tumor ≤ 5 cm in size, or ≤ 3 tumors each ≤ 3 cm in size and no evidence of gross vascular invasion. HCC is now increasingly detected at earlier stages. In addition, both liver transplantation and percutaneous ablative therapies have emerged as effective alternatives to hepatic resection. As a result, the ideal treatment strategy for patients with early stage HCC, particularly in the setting of well-preserved hepatic function, has become increasingly controversial. In the recent studies, the survival rates for transplantation in early stage HCC patients are excellent. However, when intention-to-treat analysis is used, dropouts from the waiting list due to death or disease progression clearly diminish long-term survival results and therefore patients are unlikely to benefit from liver transplantation. In addition, salvage transplantation after HCC resection may be performed without excessive morbidity and may result in equivalent survival rates compared with primary liver transplantation. In some studies, salvage transplantation may be feasible in up to 75-80% of patients with recurrence following hepatic resection. Similarly, locoregional therapies serve to sustain patients with HCC on the waiting list until a transplantation become available. While RFA and TACE are commonly used to prevent dropout, pretransplant therapy has not been associated with improved overall survival or disease-free survival due to persistenceof viable tumor. It is important to note that, while resection is a more invasive procedure, the benefit that it holds over nonresectional therapies is the complete removal of the tumor allowing for subsequent detailed pathologic examination of both the tumor and surrounding liver parenchyma. In conclusion, in patients with well-preserved hepatic function, liver resection remains the most appropriate and effective treatment.
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Strategies for the Curative Therapy of Early Stage HCC: First or SalvageTransplantation?
Nam-Joon Yi
Journal of the Korean Liver Cancer Study Group. 2012;12(2):102-108.   Published online September 30, 2012
  • 561 Views
  • 4 Downloads
AbstractAbstract PDF
Hepatocellular carcinoma (HCC) is a major cause of cancer mortality worldwide, especially in Asian countriesas well as Korea, and liver transplantation (LT) has potentials to improve survival for patients with HCC. However, major hamper to LT for HCC has been graft shortage. To solve this problem, liver resection (LR) has to be rejuvenated in the general algorithm of HCC treatment in the light of salvage transplantation (ST) strategies. The LR followed by ST in case of HCC recurrence is an attractive concept in early stage HCC and cirrhosis with acceptable liver function. These challenges in technique, indications, pre-LT observation and treatments for recurred HCC, and prioritization policies of patients on the waiting list have to be precise through prospective investigations that have to include individualization of prognosis, biological variables and pathology surrogates as stratification criteria. Accepting this challenges have been part of the history of LT and will endure for the future. This article will focus on the ST after LR in terms of intention-to-analysis
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Gobal Discrepancy of Practical Guidelines for Management of Hepatocellular Carcinoma-Resection and Transplanation
Kwang-Woong Lee
Journal of the Korean Liver Cancer Study Group. 2011;11(1):18-22.   Published online February 28, 2011
  • 518 Views
  • 3 Downloads
AbstractAbstract PDF
Hepatocellular carcinoma (HCC) usually appears in the setting of underlying liver disease. Therefore, HCC should be managed in multidisciplinary settings. Under these circumstances, several practice guidelines were introduced around the world. Clinically useful practice guidelines should be based on evidences, but socio-economic and medical status of the country should be considered as well. In this review, 6 well-known global practical guidelines (BCLC-AASLD, NCCN, 2 from Japan, APASL, Korean) were compared in terms of resection and liver transplantation (LT). BCLC-AASLD from Europe and the United States stressed more on LT for the patients within Milan criteria. However, the guidelines from the Asia had more extended indication of liver resection. The number of living donor LT in Korea is the highest in the world. Under this circumstance, indication of LT for HCC in Korea is inevitably being expanded. Compared to other guidelines, therefore, Korean guideline allowed a limited expansion of indication for HCC into patients with Child A and/or living donor LT with outside Milan HCC. However, to make more practical guidelines, high quality evidence from Korea and validation study of current Korean guideline are needed.
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Staging of Hepatocellular Carcinoma
Joon-Il Choi
Journal of the Korean Liver Cancer Study Group. 2011;11(1):26-32.   Published online February 28, 2011
  • 632 Views
  • 12 Downloads
AbstractAbstract PDF
Staging systems of HCC are very complex and disunited because multiple variables, including residual liver function, performance of patients and treatment modalities, can have influence on the survival of the patients and therefore, there is no united and generalized staging system of HCC. Staging systems of HCC can be classified as two categories; Anatomical staging systems and clinical staging systems. In anatomical staging systems, tumor factors are main elements that determine the stage of the patients and LCSGJ systems and AJCC/UICC systems are included in this category. Practice guideline and General rules of HCC by the Korean Liver Cancer Study Group adopted LCSGJ system. In clinical staging systems, not only tumor factors but also clinical factors such as liver function, performance of the patients and treatment modalities are considered to determine the stage of the patients. The BCLC system is the only system that provides treatment recommendations for each of the assigned stages based on the best treatment options currently available. Criteria for liver transplantation are on the way of expansion because of the widespread of living donor liver transplantation and several researchers presented various expanded criteria over Milan’s criteria with comparable survival data to those of Milan’s criteria. Upcoming researches of molecular biology and imaging can help the establishment of more precise and united staging systems for the patients with HCC.
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Case Report
A Case of Multiple Hepatocellular Carcinoma which was Performed Liver Transplantation after Down-staging by Transcatheter Arterial Chemoembolization
Hee-Jung Wang, Bong-Wan Kim, Sung-Won Cho, Je-Hwan Won
Journal of the Korean Liver Cancer Study Group. 2011;11(1):50-55.   Published online February 28, 2011
  • 543 Views
  • 3 Downloads
AbstractAbstract PDF
A case of multiple hepatocellular carcinoma (HCC) which was performed a living donor liver transplantation (LDLT) after down-staging by transcatheter arterial chemoembolization (TACE) is reviewed. Generally, the recommended therapeutic strategy for this kind of HCC is TACE. However, the response of multiple HCC of this 48 year-old male patient was relatively good after 4 times of TACE, and we performed LDLT on the concept of clinical trial under the informed consent of patient and his families. Although there were two times recurrences in the liver and lung, he has overcome them and is still alive 66 months after LDLT. We suggest that liver transplantation could be an alternative strategy in the multiple HCC cases who show good responses after TACE.
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Review Article
2009 Treatment Guideline for Hepatocellular Carcinoma: Surgical Resection and Liver Transplantation
Sung Hoon Kim, Kyung Sik Kim
Journal of the Korean Liver Cancer Study Group. 2010;10(1):6-10.   Published online June 30, 2010
  • 525 Views
  • 4 Downloads
AbstractAbstract PDF
The effort we are trying to set up the treatment guideline for hepatocellular carcinoma has produced various guidelines after drawing a conclusion from Barcelona EASL meeting in 2000. Especially in Korea, the Korean Liver Cancer Study Group and the National Cancer Center have collaborated on making treatment guideline for hepatocellular carcinoma in the early stage of setting up the guideline, 2003, and it was a great help to treatment, study and education. However, a need of revision had been raised due to many changes in the latest treatments and an accumulation of international and domestic experience. After the proposal of amending the treatment guideline for Hepatocellular carcinoma in the Cancer Control Forum of the National Cancer Control Planning Board on October 17th, 2008, “2009 Guideline” has been reported in the Conference of the Korean Liver Cancer Study Group held on June 27th, 2009. When revising the guideline, there are some suggestions of continuous modification to reflect evidence based medical knowledge, and recently there are some debates about the drawback of the surgical field which was not handled in EASL and AASLD Guidelines. Therefore, it will broaden your understanding of liver surgical resection and liver transplantation and it will also be a place for the discussion of disputable issues.
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JLC : Journal of Liver Cancer