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Liang, C.; He, Z.; Tao, Q.; Tang, X.; Jiang, L.; Tu, X.; Liu, Z.; Chen, H.; Xie, F.; Zheng, Y. Unresectable Hepatocellular Carcinoma. Encyclopedia. Available online: https://encyclopedia.pub/entry/55776 (accessed on 23 April 2024).
Liang C, He Z, Tao Q, Tang X, Jiang L, Tu X, et al. Unresectable Hepatocellular Carcinoma. Encyclopedia. Available at: https://encyclopedia.pub/entry/55776. Accessed April 23, 2024.
Liang, Chen, Zhaoqian He, Qiang Tao, Xiang Tang, Lingmin Jiang, Xinyue Tu, Zonghao Liu, Hua Chen, Feihu Xie, Yun Zheng. "Unresectable Hepatocellular Carcinoma" Encyclopedia, https://encyclopedia.pub/entry/55776 (accessed April 23, 2024).
Liang, C., He, Z., Tao, Q., Tang, X., Jiang, L., Tu, X., Liu, Z., Chen, H., Xie, F., & Zheng, Y. (2024, March 01). Unresectable Hepatocellular Carcinoma. In Encyclopedia. https://encyclopedia.pub/entry/55776
Liang, Chen, et al. "Unresectable Hepatocellular Carcinoma." Encyclopedia. Web. 01 March, 2024.
Unresectable Hepatocellular Carcinoma
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Hepatocellular carcinoma (HCC) is one of the most common malignant tumors in China, accounting for the majority of primary liver cancer cases. Liver resection is the preferred curative method for early-stage HCC.

hepatocellular carcinoma unresectable liver cancer conversion therapy

1. Introduction

Primary liver cancer is currently the fourth most common cancer and the second leading cause of cancer-related death in China, of which hepatocellular carcinoma (HCC) accounts for 75–85% of the incidence [1]. For patients with HCC, surgical treatment remains an important method to achieve long-term survival. However, most patients with hepatocellular carcinoma have an insidious onset and often lose the opportunity for surgery at the time of diagnosis. Inoperable liver cancer can be divided into technically unresectable, including patients with intolerable systemic conditions and insufficient residual liver volume, and oncologically resectable, which is technically resectable but cannot obtain better results than non-surgical treatment [2]. Owing to the large scale of HCC cases and clinical practice, the China Liver Cancer Staging (CNLC) system was established and has been widely adopted in China and abroad [3]. According to the CNLC system, radical treatments such as surgical resection, local ablation, and liver transplantation are recommended for patients with stage I a(single nodule ≤5 cm) and I b(single nodule >5 cm, or 2–3 nodules ≤3 cm) and selected patients with II a(2–3 nodules >3 cm) [1]. This is in line with the latest 2022 edition of the BCLC strategy, which recommends radical ablation, resection and transplantation for patients with stage 0 and stage A(Single, or 2–3 nodules each ≤3 cm), and transplantation for selected patients with stage B (multinodular) who meet the expanded criteria for liver transplantation [4]. However, concerning inadequate compensatory liver volume and insufficient residual liver function after radical treatment, usually predicted by preoperative evaluation, some patients may experience insufficient surgical margins. Additionally, patients with poor overall conditions may not tolerate surgery. These cases are classified as technically unresectable HCC.

2. Conversion Therapy for Technically uHCC: Making It Grow

Cirrhosis from various causes is the most important link in the process of hepatocellular carcinoma, and 85%~95% of patients with hepatocellular carcinoma have different degrees of cirrhotic background [5]. Post-hepatectomy liver failure (PHFL) is a potentially fatal complication following major liver resection. The indocyanine green (ICG) clearance test is one of the most widely used preoperative tests to assess the incidence of PHFL in all patients, including those with mild fibrosis and advanced fibrosis. Patients undergoing liver resection should meet certain criteria, including an indocyanine green retention rate at 15 min (ICG-R15) of less than 30% and a residual liver volume (RLV) above 30–40% of the standard liver volume (SLV) [1]. The ratio of RLV to SLV correlates with postoperative outcomes, especially with PHLF. The formula for calculating SLT is based on a linear correlation between total liver volume and body weight or body surface area (BSA), based on a large patient population or autopsy data.

Portal Vein Embolization and Associating Liver Partition and Portal Vein Ligation for Staged Hepatectomy (ALPPS)

Portal vein embolization (PVE) was first reported by Makuuchi et al., in 1982 [6]. In patients with insufficient FLR, embolization was performed by embolizing the portal vein branches near the tumor before surgery to promote enlargement of the remnant liver. However, due to the long waiting time for PVE to induce residual liver hypertrophy, there is a risk of further loss of surgical opportunity due to tumor progression.
German scholar Schlitt first proposed the two-stage liver resection technique known as associating liver partition and portal vein ligation for staged hepatectomy (ALPPS) in 2007. The first implementation of ALPPS was carried out by Schnitzbauer et al., in 2012 [7]. Since then, it has been widely used in the resection of colorectal liver metastases. The procedure follows two steps: in the first step, the liver is mobilized and the portal vein is ligated. It takes two to four weeks to let the liver compensate. And the tumor-containing liver lobe is resected after the remaining liver volume meets the requirements at step two. A randomized controlled study comparing portal vein embolization (PVE) and ALPPS in patients with liver cancer and hepatitis B-related cirrhosis showed that ALPPS patients achieved a higher surgical resection rate (97.8%) and were able to increase future liver remnant (FLR) volume more rapidly than PVE, both in the short term and long term, with comparable benefits [8]. However, in the presence of liver cirrhosis, the functional recovery of newly regenerated liver cells may be delayed. Even if the volume of the future liver remnant (FLR) increases, the liver’s function may not have fully recovered. Therefore, the timing of the second-stage surgery still needs to be determined based on the liver’s functional status. For patients with liver cirrhosis, ICG-R15 less than 40% after the first-stage surgery indicates sufficient FLR hypertrophy, and the second-stage surgery can be performed within one week. Another systematic review suggests that considering the surgical difficulty and complication rates, portal vein embolization (PVE) balances safety, effectiveness, and timeliness compared to ALPPS [9].
Charalel et al., conducted a systematic review comparing the outcomes of ALPPS and PVE. From the analysis of 21 PVE studies with mean percent FLR hypertrophy data and hepatectomy data, the random-effects pooled estimate of mean percent FLR hypertrophy was 30.9% with an average interval of 40.3 days (SD 26.3 days). In contrast, the analysis of four ALPPS studies revealed a random-effects pooled estimate of mean percent FLR hypertrophy of 54.9% over a mean interval of 11.1 days (SD 3.1 days) [9]. Another comparative study performed by Chan et al., indicated that ALPPS induced a much greater FLR hypertrophy than PVE (FLR volume gain by 48.8%, an additional 12.8% over 6 days). The increase in FLR volume was more significant in cases of chronic hepatitis compared to cirrhosis (52.7% vs. 32.5%) [8].
ALPPS could acquire the necessary liver volume more efficiently, but with a higher blood loss compared to PVE. Therefore, the choice between ALPPS or PVE as a transitional treatment should be based on the pros and cons of each. For patients with a future liver remnant (FLR) volume of 30–40% of the standard liver volume, PVE, which has smaller trauma and less blood loss, is sufficient to obtain the desired FLR volume. However, for patients with a higher risk of tumor progression and an FLR ratio of less than 40%, ALPPS should be considered. In general, ALPPS cannot completely replace the role of PVE. When selecting a transitional treatment strategy based on residual liver volume, clinical decisions should be made by considering the patient’s liver disease background, complication risks, and tumor progression. The goal is to maximize the patient’s survival benefits.
Furthermore, another multicenter retrospective study comparing liver venous deprivation (LVD) and ALPPS demonstrated that, with comparable complication and mortality rates, ALPPS exhibited faster hypertrophy of the residual liver and higher surgical resection rates. According to a global multicenter randomized controlled study, ALPPS surgery showed higher surgical resection rates (92% vs. 57%) compared to traditional two-stage hepatectomy (TSH) in patients with a future liver remnant (FLR) volume of less than 30% of the standard liver volume [10].
To reduce the complications and surgical risks associated with ALPPS and improve the second-stage resection rate, there have been continuous advancements in modified surgical techniques. Cillo et al. [11] reported a case of laparoscopic microwave ablation and portal vein ligation for staged hepatectomy (LAPS), where portal vein ligation was performed under laparoscopic assistance. Subsequently, ultrasound-guided microwave ablation was used to create an avascular trench along the pre-cut line of the liver, separating the residual liver from the embolized side. Microwave ablation ALPPS is a minimally invasive procedure that results in less trauma and faster recovery for patients compared to traditional ALPPS. Additionally, LAPS does not involve the transection of liver parenchyma, significantly reducing the risk of bile leakage and intraoperative bleeding. During the second surgery, the liver is opened along the ablation zone, improving the safety of the procedure.
Alvarez et al., performed partial ALPPS by dividing the portal vein of the diseased hemi-liver up to the middle hepatic vein, without extending the parenchymal transection further (up to the inferior vena cava) [12]. Compared to complete ALPPS, partial ALPPS results in comparable FLR hypertrophy and reduced morbidity [12][13]. A systematic review which included four studies and 124 patients showed the same result [14]. However, Chan et al., argues that complete ALPPS would induce more rapid FLR hypertrophy without increasing perioperative risk in chronic liver diseases [15]. Another meta-analysis performed subgroup analysis to evaluate patients with and without liver cirrhosis, and suggests that ALPPS had a better outcome in the cirrhotic group [16]. Petrowsky et al., contend that, though partial ALPPS perhaps induces slower hypertrophy when compared with complete ALPPS, it is sufficient to enable the rapid and beneficial second-stage operation leading to complete resection [13]. In summary, both partial and complete ALPPS procedures have similar effects in promoting remnant liver hypertrophy, but each of them has its advantages in different cohorts. Furthermore, additional research involving larger, homogeneous cohorts is required to further compare the outcomes of these two treatment approaches.

3. Conversion Therapy for Oncologically uHCC: Making It Shrink

Currently, the indications for surgery in advanced HCC vary widely between countries and institutions. According to the AASLD Practice Guidelines and EASL Clinical Practice Guidelines, both of which were based on the BCLC staging system, surgical resection is not indicated in patients with advanced HCC. However, Chinese clinical practice guidelines for HCC do not exclude the indication of surgical resection on the basis of the tumor size or macroscopic vascular invasion. Even limited extrahepatic metastases may be candidates for surgical resection according to the Japanese clinical practice guideline. A similar expansion of the surgical indication has been proposed by the Hong Kong Liver Cancer Staging System and the Korean Liver Cancer Study Group, respectively. The main reasons for differences in treatment recommendations for advanced HCC between East and West may be different etiologies, different patient populations and different health economic conditions.
Although surgical treatment for advanced-stage liver cancer has shown suboptimal outcomes, most patients who undergo surgery do not exhibit significant survival benefits compared to medical treatment alone. However, research has found that conversion therapy can promote tumor regression and even lower the staging of liver cancer, thereby providing patients with opportunities for surgery and liver transplantation, leading to improved long-term survival outcomes. With the rapid advancements in interventional therapy and systemic anti-tumor drugs in recent years, various combination treatment approaches have achieved significant success in the management of advanced-stage liver cancer, driving progress in transitional treatment. The objective response rate (ORR) is an important indicator of tumor treatment, and partial response (PR) or complete response (CR) not only reflects sensitivity to the treatment regimen but also represents the potential for resection and surgical feasibility [17]. A global consensus should be reached on the indications for surgery in advanced HCC.

3.1. Combination of Systemic Anti-Tumor Drugs

Anti-tumor medications are the first choice for advanced HCC. The combination of atezolizumab and bevacizumab has been approved as the first-line treatment regimen for unresectable liver cancer patients. In the global multicenter Phase III IMbrave150 study [18], the median overall survival for the Atezolizumab plus Bevacizumab group was 19.2 months, with a progression-free survival of 6.9 months, significantly longer than the sorafenib group with 13.4 months and 4.3 months, respectively. The overall response rate reached 33.2%, demonstrating clear clinical benefits in the combination therapy group. In the global randomized double-blind Phase III LEAP-002 study [19], Lenvatinib plus Pembrolizumab showed a median overall survival of 21.2 months, a median progression-free survival of 8.2 months, and an overall response rate of 36.0% in patients with unresectable hepatocellular carcinoma. Combining CTLA-4 inhibition during the immune priming phase with PD-1/PD-L1 inhibition during the immune effector phase has emerged as a promising strategy in the field of cancer medicine [20]. In the global open-label phase III HIMALAYA study, a single high dose of the CTLA-4 antibody Tremelimumab in combination with the PD-L1 antibody Durvalumab yielded an ORR of 20.1% [21][22]. Currently, the combination of targeted therapies and immune checkpoint inhibitors is an important treatment approach for unresectable or advanced-stage liver cancer. It is also one of the main strategies for potential conversion treatment in potentially resectable liver cancer [2].

3.2. Interventional Therapy

Hepatic arterial infusion chemotherapy (HAIC) is the main local treatment method for patients with advanced-stage liver cancer. In recent years, FOLFOX-HAIC has demonstrated excellent efficacy in Chinese patients with advanced hepatocellular carcinoma (HCC). Some patients who undergo HAIC treatment experience a significant reduction in tumor burden or noticeable shrinkage of major vascular tumor thrombus, thus providing opportunities for conversion resection or ablation therapy. In an open-label Phase III clinical trial [23], advanced HCC patients treated with FOLFOX-HAIC achieved a median overall survival of 13.9 months and a median progression-free survival of 7.8 months, showing significant benefits compared to the sorafenib treatment group (8.9 and 4.3 months, respectively). Additionally, 15 patients (12.3%) achieved tumor downsizing and underwent curative resection or ablation, resulting in a median survival of 20.8 months and a one-year overall survival rate of 93.8%.
In another Phase III clinical trial conducted by Shi et al. [24], FOLFOX-HAIC demonstrated better outcomes than transarterial chemoembolization (TACE) in patients with tumors ≥7 cm in longest diameter, without major vascular invasion or extrahepatic metastasis. FOLFOX-HAIC showed a higher overall response rate (ORR) compared to TACE (46% vs. 18%), and due to tumor shrinkage and liver regeneration, 24% of patients underwent conversion resection surgery. The combination of loco-regional treatment also provides a new perspective for conversion therapy. A study from Sun Yat-sen University Cancer Center indicated that the combination of TACE and HAIC achieved an ORR of 65.9% (based on mRECIST criteria) and a conversion resection rate of 48.8% in patients with unresectable liver cancer, which was significantly higher than traditional TACE alone [25].
In addition, there is an active exploration of multi-modality conversion therapies combining systemic drugs with local treatments. Peng et al. [26] reported a Phase III clinical trial of TACE combined with Lenvatinib for advanced hepatocellular carcinoma. Compared to monotherapy with Lenvatinib, the combination regimen achieved a higher overall response rate (ORR) (54.1% vs. 24%, based on mRECIST criteria), with 15.3% of patients achieving downsizing and subsequent resection. A Phase II single-arm clinical trial investigated the therapeutic effect of HAIC in combination with Toripalimab and Lenvatinib in patients with advanced-stage liver cancer [27]. Among the patients in this trial, 86.1% had portal vein tumor thrombus and 27.8% had extrahepatic metastasis. The triple combination treatment yielded an ORR of 66.7%, with 15 patients (41.7%) achieving a partial response (PR) in the initial radiological evaluation, and 5 patients successfully undergoing surgical resection. The researchers pointed out that Lenvatinib and chemotherapy drugs can modulate the tumor immune microenvironment by stimulating antigenicity, thereby enhancing the efficacy of PD-1 inhibitors.
Surgical resection is an important means for patients to achieve long-term survival after successful conversion, and the safety of surgery is an important assessment factor before conversion resection [28]. A retrospective study compared the complications and survival benefits between 320 patients who underwent conversion surgery after HAIC and patients who underwent direct surgery [29]. The HAIC surgery group consisted of 107 patients with initially unresectable advanced liver cancer. The HAIC surgery group showed a tendency toward postoperative liver dysfunction and intra-abdominal bleeding related to the number of HAIC treatments. Additionally, the recurrence-free survival (RFS) in the HAIC surgery group was comparable to that of the direct surgery group. Indeed, conversion therapy can bring hope for surgical resection to patients, but it can also cause damage to liver function and the overall physical condition of the patients. Therefore, it is essential to evaluate the general condition and liver function of patients during the process of conversion therapy and accurately determine the timing for surgical intervention.

References

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