|Year : 2021 | Volume
| Issue : 3 | Page : 764-770
Ultrasound-guided percutaneous microwave ablation for hepatocellular carcinoma originating in the caudate lobe: A pilot clinical study
Yuan Peng, Dan Cui, Weijian Li, Ming Ding, Yaoping Shi, Tao Wang, Donghua Shi, Jiachang Chi, Ping Li, Bo Zhai
Department of Interventional Oncology, Renji Hospital, School of Medicine, Shanghai Jiaotong University, Shanghai, China
|Date of Submission||09-Jan-2021|
|Date of Decision||08-Mar-2021|
|Date of Acceptance||10-Mar-2021|
|Date of Web Publication||9-Jul-2021|
Department of Interventional Oncology, Renji Hospital, School of Medicine, Shanghai Jiaotong University, Shanghai
Source of Support: None, Conflict of Interest: None
Objective: This study aimed to evaluate the efficacy, feasibility, and tolerability of ultrasound (US)-guided percutaneous microwave ablation (MWA) for treating hepatocellular carcinoma (HCC) originating in the caudate lobe.
Materials and Methods: The treatment and survival parameters of 32 patients with HCC in the caudate lobe, who met the inclusion criteria and had received US-guided percutaneous MWA in our department from November 2010 to October 2015, were retrospectively analyzed. Imaging examination (contrast-enhanced computed tomography or magnetic resonance) 1 month after MWA was used to evaluate the efficacy of US-guided MWA.
Results: Thirty-two patients underwent percutaneous MWA for caudate lobe HCC. The average tumor size was 3.42 ± 0.27 (range: 1–6.8) cm. The initial complete ablation (CA) rate was 87.5% (28/32), and the total CA rate was 96.88% (31/32). Furthermore, the median length of hospitalization was 4 days (range: 2–10 days), and no major complication was observed in this study. The overall survival rates were 87.5%, 50%, and 28.13% at 1, 2, and 3 years, respectively. The progression-free survival after MWA was 93.75%, 53.15%, and 28.13% at 6, 12, and 18 months, respectively.
Conclusions: US-guided percutaneous MWA was a safe and effective treatment. It is a promising alternative therapy for HCC originating in the caudate lobe.
Keywords: Caudate lobe, clinical study, hepatocellular carcinoma, percutaneous microwave ablation, ultrasound guided
|How to cite this article:|
Peng Y, Cui D, Li W, Ding M, Shi Y, Wang T, Shi D, Chi J, Li P, Zhai B. Ultrasound-guided percutaneous microwave ablation for hepatocellular carcinoma originating in the caudate lobe: A pilot clinical study. J Can Res Ther 2021;17:764-70
|How to cite this URL:|
Peng Y, Cui D, Li W, Ding M, Shi Y, Wang T, Shi D, Chi J, Li P, Zhai B. Ultrasound-guided percutaneous microwave ablation for hepatocellular carcinoma originating in the caudate lobe: A pilot clinical study. J Can Res Ther [serial online] 2021 [cited 2021 Aug 5];17:764-70. Available from: https://www.cancerjournal.net/text.asp?2021/17/3/764/321021
| > Introduction|| |
Hepatocellular carcinoma (HCC) is one of the most common and severe malignancies worldwide. In the past decades, incidences of HCC have risen steadily, accompanied by an increase in mortality rates. In China, HCC accounts for about 50% of the total number of new cases due to the high incidence of hepatitis B virus (HBV) infection., Liver resection and transplantation are traditional curative treatments for HCC patients of Barcelona Clinic Liver Cancer Stage 0-A. Unfortunately, only fewer than 20% of all patients are suitable candidates for these two treatments. This is because of severely compromised liver function, advanced stage of tumors, risky location of tumors, or poor clinical conditions. In clinical practice, interventional treatments including thermal ablation, transcatheter arterial chemoembolization (TACE), percutaneous ethanol injection, and radiotherapy have been introduced for unresectable HCC.,,,,
HCC originating from the caudate lobe is rare and the treatment is cumbersome, and challenging because of its location and complex anatomy. The caudate lobe is deeply located between the hepatic hilum (HH) and the inferior vena cava (IVC). Hepatectomy remains the best curative treatment for HCC. However, compared with tumors in other locations of the liver, studies have shown that using hepatectomy for HCC treatment in the caudate lobe has considerable technical difficulty because of the unique anatomy, more blood loss, longer hospitalization, and higher recurrence and mortality rates. At present, imaging-guided tumor ablation techniques play a key role in the treatment of early-stage HCC because they are less invasive than surgical resection but with equal efficacy. Among the various ablative therapies, radiofrequency ablation (RFA) is established as the primary ablative modality and is the most used therapy in medical institutions. Although RFA is a safe and effective treatment of liver tumors, there are difficulties and challenges with RTA in the treatment of HCC tumors in the caudate lobe because of the risk of collateral thermal damage to surrounding organs.
Recently, microwave ablation (MWA) is gaining momentum in the clinical application and has been successfully performed in selected patients with HCC in the caudate lobe. Several studies have shown that MWA offers several advantages over RFA, including faster heating over a large volume, simultaneous multiple applicator use, and no requirement for ground pads., However, there are few large-scale studies in which authors assess the safety and efficacy of MWA for HCC in the caudate lobe. Therefore, the present study was conducted to assess the feasibility, safety, and effectiveness of using MWA in the treatment of HCC in the caudate lobe under ultrasound (US) guidance.
| > Materials and Methods|| |
The protocol of this study was approved by the Ethics Committee of Renji Hospital, Shanghai Jiaotong University” and conformed to the ethical guidelines of the World Medical Association Declaration of Helsinki. All patients were provided with written informed consent for participation in the study.
Patient recruitment for the study
To study the safety and effectiveness of MWA treatment for HCC in the caudate lobe, 32 patients, 24 men and 8 women, aged 33–73 years (mean: 53.5 ± 1.89 years) were enrolled in this study. From November 2010 to October 2015, the recruited patients with HCC in the caudate lobe underwent US-guided percutaneous MWA in department of Interventional Oncology. The patient's characteristics and tumor features were analyzed. The baseline characteristics of the patients are shown [Table 1]. The mean maximum diameter of the tumors in the caudate lobe was 3.35 ± 0.31 cm (range: 1–6.8 cm). All enrolled patients met the following criteria: (1) at least one tumor in the caudate lobe; (2) unsuitability for resection because of surgical contraindications, or unwillingness to undergo surgery; (3) at least 2-mm safety interval between tumor margin and diaphragmatic dome or cavity viscera; (4) absence of extrahepatic metastases and refractory ascites; (5) Child–Pugh class A or B; and (6) adequate hematologic (platelet count >40 × 109/L and international normalized ratio <2.0) and renal (creatinine <2.0 mg/dL) functions. Patients with poor liver function (Child–Pugh class C) or serious coagulopathy (platelet count < 0 × 109/L cells and prothrombin activity <40%) were excluded.
|Table 1: Baseline characteristics of 32 patients with caudate hepatocellular carcinoma|
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The diagnosis of HCC was based on two specific imaging modalities (computed tomography [CT] or magnetic resonance imaging [MRI]) with elevated alpha-fetoprotein (AFP) or histological confirmation and was revised according to the European Association for the Study of the Liver guidelines, and the updated American Association for the Study of Liver Diseases practice guidelines for the management of HCC and the BCLC guidelines.,, Among these patients, 12 had a solitary tumor in the caudate lobe, and 20 patients had more than one tumor in the whole liver.
Microwave ablation procedures
All procedures were performed under real-time US guidance (MyLab Twice scanner or HM1498XS1 scanner) using a 3.5-MHz probe. MWA was performed using a 2450-MHz MTC-3C microwave generator and a 25-cm-long, 15-G cooled-shaft electrode probe (Vision Medical, Nanjing, China) with the 1.5-cm-long expandable needle. The generator can produce continuous power ranging from 5 to 100 W.
General anesthesia was administered following the protocol guidelines; subsequently, the ablative needle was inserted under US guidance to the site of the target tumor. In this study, the approach used in HCC treatment in the caudate lobe was the right intercostal and the pass-the-left approaches, which is similar to those reported by Kariyama et al. All tumors in the paracaval portion (PC) (n = 11) were treated by the right intercostal approach. All tumors in the caudate process (n = 7) were treated by the pass-the-left approach. Spiegel's tumors were treated by the right intercostal [n = 4, [Figure 1]] and pass-the-left (n = 10) approach. Special attention was paid to avoid vessels along the percutaneous route. Output power was set at 80–100 W according to tumor location. In some high-risk tumors such as gastrointestinal tract (GIT) and gallbladder, lower power was delivered. For other tumors in the caudate lobe, the maximum level of power was used throughout the procedure. For some small tumors (maximum diameter ≤2 cm) that were difficult to visualize on US, contrast-enhanced US (CEUS) was used to detect the tumor, guide the placement of the antenna, and to observe whether the lesion was completely ablated.
|Figure 1: Ultrasound-guided microwave ablation in a 65-year-old man with hepatocellular carcinoma in Spiegel's lobe. The tumor was 2.7 cm × 2.2 cm. (a) Preablation contrast-enhanced magnetic resonance scan reveals a hepatocellular carcinoma lesion in Spiegel's lobe (arrow). (b) A 15-G microwave antenna (arrow) was inserted into the center of the tumor after confirmation by contrast-enhanced ultrasound. A hyperechoic region covered the lesion during the ablation. (c) Contrast-enhanced ultrasound image was used to guarantee the lesion complete ablation (arrow). (d) Follow-up of the contrast-enhanced magnetic resonance image obtained 2 months after ablation revealed no enhancement in the ablation zone (arrow)|
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A vial of SonoVue was divided into two doses of 2.5 mL each. The first-half dose was injected intravenously to confirm tumor location, and the other half-dose was used for the CEUS guidance. The total ablation time reached a minimum of 60 s (mean: 343.13 s; range: 60–900 s). Ablation continued until the hyperechoic region on US covered the entire target lesion, including an ablative margin of at least 5 mm. If this minimum margin could not be achieved, conformal ablation with as wide an ablative margin as possible was performed. The peristaltic dump was then turned off to maintain sufficient energy to heat the needle track. When the antenna was withdrawn into the hepatic capsule, the MWA emission needed to last at least 5 s. The ablation region, IVC, and HH were carefully monitored under real-time US guidance. CEUS was used to guide the puncture where tumors were difficult to visualize on the conventional US. Vital signs were monitored continuously during the procedure.
Postoperative monitoring and assessment
The patients were examined and closely monitored for several hours in the recovery unit after MWA before being sent back to the ward. A complete panel of blood chemistry including liver and renal functions was examined pre- and postablation. In this study, major complications were defined as complications that resulted in admission to hospital for therapy, unplanned increase in the level of medical care, prolonged hospitalization, permanent adverse sequelae, or death.
To observe the efficacy of MWA, all patients underwent follow-up and were examined 1 month after ablation by enhanced CT or MRI. Complete ablation (CA) was defined as the absence of residual tumor enhancement on the enhanced CT or MRI. Overall survival (OS) was defined as the period from the date of ablation to the date of death or the date of the last follow-up visit. Progression-free survival (PFS) was defined as the interval between ablation and the date of any tumor recurrence. OS and PFS were used to evaluate the efficacy of the treatment.
Follow-up examinations of all the patients were performed 1 month after the treatment and every 3 months for the first year and 6 months thereafter. The examinations performed for all patients included hematological parameters and imaging modalities such as liver and kidney function, tumor markers (AFP and CA199), and contrast-enhanced CT or MRI. In patients where local tumor progression (LTP) or intrahepatic distant recurrence was observed, US angiography was performed. In patients with suspected extrahepatic metastases, positron emission tomography-CT was required. The follow-up was finalized on December 31, 2016.
A literature search was done to compare the results of this study with those of other studies on the treatment of caudate HCC. It was performed through PubMed (http://www.ncbi.nlm.nih.gov/pubmed) using the following keywords: “hepatocellular carcinoma,” “caudate lobe,” “treatment,” and “survival.” We excluded case reports, non-English/no abstracts, technical/radiology descriptions, articles without survival, or review articles. The OS and PFS rates were extracted.
In this study, all statistical analyses were performed with SPSS software (version 21.0, SPSS Inc., Chicago, IL, USA). Continuous parameters were expressed as means ± standard deviation, while categorical variables were expressed as number and percentage. The OS time and PFS time were estimated using the Kaplan–Meier method.
| > Results|| |
Patients and tumor characteristics
Of the 32 patients who were treated with MWA for HCC in the caudate lobe, 12 had a solitary HCC in the caudate lobe while 20 had additional tumors in other parts of the liver, and 27 had HBV infection. In Child–Pugh classification, 15 of the 32 belonged to class A, and 17 belonged to class B. None of the patients fell into class C. Cirrhosis had been confirmed in 26 patients. Before MWA, 30 of the patients recruited in this study were eligible for other various therapies such as liver resection, TACE, liver transplantation, RFA, and transjugular intrahepatic portosystemic stent shunt. The right intercostal approach was used in 15 patients, and the pass-the-left approach was used in 17 patients. Further details of the patients are displayed [Table 1] and [Table 2].
Safety of microwave ablation procedure as shown by the complications and hospitalization recorded following the procedure
MWA was successfully performed for all patients without any technical failures. Major complications, such as intractable hemorrhage, bile duct injury, liver abscess, tumor seeding, and hepatic failure, were not observed in this study. Nevertheless, some minor side effects occurred [Table 3], whereby one patient developed severe abdominal pain a day after MWA. This was revealed to be a right lower abdomen effusion after a CT scan was performed. We suspected that the patients had postoperative bleeding and thus performed an abdominocentesis. The patient was admitted, observed, and treated with hemostatic and silymarin. The patient eventually recovered and was discharged from the hospital.
Local pain was observed in 12 of the 32 patients (37.5%). Three patients required analgesics (50-mg intramuscular dolantin injection) and others had spontaneous remission in 1–3 days. Fever ranging from 37.3°C to 39.2°C was observed in 14 of the 32 patients (43.75%). Half a pellet of indomethacin was inserted through the anus for patients with a temperature >38°C. Blood transaminase and bilirubin levels increased in 16 of the 32 patients (50%) after ablation and dropped to normal levels spontaneously or after active liver-protective treatments (reduced glutathione sodium, polyene phosphatidylcholine, or magnesium isoglycyrrhizinate) within 1–2 weeks. The median length of hospitalization was 4 days (range: 2–10 days).
Efficacy of microwave ablation
Caudate lobe initial CA was achieved in 28 (87.5%, 28/32) patients [Figure 1] and residual lesions were observed in 4 (12.5% 4/32) patients a month later. The lesions included two tumors in the Spiegel's lobe (SP) and two in the PC. Among the patients within CA, three accepted secondary ablation and CA was finally achieved. The remaining one patient accepted TACE, and the tumor was eventually controlled. Of the 32 patients, 3 whose tumors were adjacent to the GIT received 125I brachytherapy as palliative therapy for residual tumors that could not be ablated technically. These patients finally experienced CA.
| > Follow-up results|| |
The median PFS was 13.5 months, with the 6-, 12-, and 18-month cumulative PFS rates of 93.75%, 53.15%, and 28.13%, respectively. A total of 23 of the 32 patients (71.88%) developed tumor recurrence until the last follow-up. Among these 23 patients, 4 of the 32 (12.5%) had caudate lobe tumor progression and 18 (56.25%) patients developed intrahepatic distance recurrence. One patient had the caudate lobe recurrence and the intrahepatic distance recurrence. The caudate lobe recurrence occurred at 4, 15, 24, and 30 months, respectively. Extrahepatic metastases were found in 7 of the 32 patients (21.88%), and their location included the lung (n = 2, 6.25%), portal vein tumor thrombus (n = 3, 9.36%), pelvic (n = 1, 3.13%), and adrenal (n = 1, 3.13%). The lung and adrenal metastases were treated by CT-guided microwave ablation while the portal vein tumor thrombus was treated by TACE combined with sorafenib.
During the follow-up periods, 5 of the 32 patients (15.63%) died: 2 from liver failure and 3 from cancer cachexia due to intrahepatic and extrahepatic metastases. The deaths were as a result of primary disease progression that was not directly attributable to the MWA procedure. The median OS time was 25 months, with 1-, 2-, and 3-year cumulative survival rates of 87.5%, 50%, and 28.13%, respectively.
Comparison of microwave ablation with other treatments
To compare the outcomes of MWA with other treatments, related studies were reviewed through a literature search and the detailed information is listed [Table 4]. Comparing with RFA and resection, the 12-month PFS rate (53.15%) of our study was at the middle level. The 1-year OS rate of our study was up to 87.5%. However, the 3-year OS rate was less than the published studies, with only 28.13%.
|Table 4: Systemic review of patients' survival in caudate lobe hepatocellular carcinoma with different treatments|
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| > Discussion|| |
It was very challenging to resect malignancies in the caudate lobe due to its deep location and proximity to complex regional structures. Moreover, resection causes more blood loss, longer hospitalization, high expenses, and higher rates of recurrence and mortality. Since the emergence of the MWA technique, more clinical practice guidelines have recommended this method as a radical treatment modality for hepatic carcinoma. In this study, percutaneous MWA showed satisfactory therapeutic efficacy for local cancer control. Nevertheless, the percutaneous MWA treatment was found to be inadequate in four patients. CEUS, CT, or MRI indicated that percutaneous MWA produced complete necrosis of tumors on the other 28 (87.5%) patients and thus successfully prevented LTP. No serious clinical complications arose from MWA. One of the patients who had postoperative bleeding was treated with hemostatic and silymarin and the bleeding stopped. Another patient's blood bilirubin increased sharply after ablation and was treated with a liver protectant, glucocorticoids. The glucocorticoids were administered intravenously for 3 days and the blood bilirubin levels normalized eventually. This may be due to the oppression of bile duct edema. The patients that had complications and recovered self-discharged from the hospital.
Studies have shown that tumor ablation in the caudate lobe would be more affected by the heat-sink effect because of the proximity of the lobe to the hepatic veins and the IVC. The caudate lobe is surrounded by the ligamentum venosum. The ligament is composed of fibrous tissue, which could insulate the heat and obstruct thermal propagation, thus helping to trap heat during ablation. Unfortunately, this might cause an asymmetric temperature distribution. The temperature in the tumor margin adjacent to large vessels might be lower than that adjacent to the ligamentum venosum, and this may increase the risk of LTP.
In this study, high-powered ablation and 125I particles were injected into the tumor margin adjacent to large vessels in some cases to balance this effect and thus enhance thermal efficacy. However, four cases still had residual tumors whose margins were too close to the IVC and HH and caused the technical failure. Among these four patients, two tumors were in the PC and the other two in the SP. The PC is located closer to the IVC and HH than the other two portions of the caudate lobe, which greatly increased the heat-sink effect and decreased thermal efficacy. This may be the reason the MWA of tumors in the PC was more likely to cause technical failure. For tumors in the caudate lobe, it is quite difficult to increase the ablative margin because of the complex surrounding tissues. Portal vein tumor thrombus was treated by TACE combined with sorafenib, and during follow-up, the tumor thrombus reduced significantly. Some scholars have already reported that TACE and sorafenib could improve OS for HCC patients with tumor thrombus.
As a primary treatment, surgical resection remains the choice for caudate HCC. It would be of remarkable clinical significance to compare the efficacy and safety between surgical resection and MWA through a well-designed clinical study. The negative effects of liver resection which are more blood loss, longer hospitalization, and higher rates of recurrence are well known. It is currently impossible to compare survival and disease-free outcomes between resection and MWA as there are no data from randomized clinical trials. Data generated from observational studies and/or case reports are heterogeneous [Table 4]. Ideally, indications of both treatments are different from patient to patient, and from institution to institution.
In our study, the median OS time was 25 months, with 1-, 2-, and 3-year cumulative survival rates of 87.5%, 50%, and 28.13%, respectively. The cumulative 6-, 12-, and 18-month PFS rates were 93.75%, 53.15%, and 28.13%, respectively. The median PFS was 13.5 months. Comparing with resection and RFA, the 12-month PFS rate (53.15%) of our study was at the middle level. The 1-year OS rate of our study was up to 87.5%, however, the 3-year OS rate was less than the published studies, with only 28.13%. In related studies, all the patients had primary tumors in the caudate lobe. In this study, however, most patients' tumors (93.75%, 30/32) reappeared after resection with various therapies such as hepatectomy, MWA, RFA, TACE, and so on. The patients recruited in our study were not eligible for resection because of poor liver function, and multiple tumors. Therefore, patients with these conditions would be more likely to benefit from MWA with possible cure or prolongation of life as MWA is safe and efficient.
The limitations of the study included inevitable selection biases in the study population due to the study being retrospective. Second, since the vast majority (27/32) of patients had HBV infection, the antiviral treatments they received may also have impacted both RFS and OS and thus should be taken into consideration. However, these data are missing in our study. The other limitation was the inability to assess the therapeutic efficacy, through an urgent need for controlled clinical trials that will compare this therapeutic modality with surgical resection or other percutaneous local treatments. Finally, the number of patients was small and the follow-up time was inadequate.
| > Conclusions|| |
Percutaneous MWA for caudate lobe HCC is a safe and feasible procedure without perioperative mortality. Through a systematic review of other therapeutic options on caudate HCC, its overall outcome is comparable to that of surgical resection. Therefore, MWA can potentially become an alternative treatment for caudate lobe HCC.
Dan Cui and Wei-Jian Li collected the data of the patients, designed the pipeline of the analysis, and drafted the manuscript. Min Ding performed the statistical analysis, and drafted the manuscript. Bo Zhai conceived and coordinated the overall study and revised the manuscript. All authors read and approved the final manuscript.
Informed consent was obtained from all individual participants included in the study.
Financial support and sponsorship
This research was supported by a grant from the National Natural Science Fund (No. 81472845).
Conflicts of interest
There are no conflicts of interest.
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[Table 1], [Table 2], [Table 3], [Table 4]