• OPEN ACCESS

Ablation for Benign Liver Tumors: Current Concepts and Limitations

  • Hitoshi Maruyama1,* ,
  • Maki Tobari1,
  • Hiroaki Nagamatsu1,
  • Tadashi Yamaguchi2 and
  • Shuichiro Shiina1
 Author information
Journal of Clinical and Translational Hepatology 2023;11(1):244-252

DOI: 10.14218/JCTH.2022.00205

Abstract

Percutaneous ablation under imaging guidance is a curative treatment that can induce complete tumor necrosis with advantages of minimal invasiveness and a low risk of complications. Thermal ablation, which includes radiofrequency ablation and microwave ablation, is a representative technique that has sufficient antitumor effects in cases of hepatocellular carcinoma with ≤3 lesions measuring ≤3 cm and preserved liver function. The short- and long-term outcomes of patients are comparable with those achieved with surgical resection. Despite their nonmalignant nature, some benign liver tumors require treatment for symptoms caused by the presence of the tumor and/or continuous enlargement. Ablation may be the treatment of choice because it has lower burden on patients than surgical treatment. This review describes the recent concepts, progress, and limitations of ablation-based treatment for benign liver tumors.

Keywords

Liver tumor, Radiofrequency ablation, Microwave ablation, Benign

Introduction

Percutaneous ablation under imaging guidance is a curative treatment with the advantages of minimal invasiveness and a low risk of complications.1 It includes energy-based ablation techniques, such as radiofrequency ablation (RFA), microwave ablation (MWA), cryoablation, irreversible electroporation, laser ablation, and chemical-based ablation techniques, such as percutaneous ethanol injection.2 Patients with hepatocellular carcinoma (HCC), ≤3 lesions measuring ≤3 cm and Child-Pugh class A or B are good candidates for thermal ablation by RFA or MWA, which save more of the surrounding nontumor liver tissues than surgical treatment.3–5 In fact, recent studies have shown comparable results between ablation and surgical treatment for HCC (Table 1).6–8 The data strongly suggest that surgical treatment has no therapeutic or survival advantages over ablation in the study cohort.

Table 1

Comparison of outcomes between ablation and surgical treatment for HCC

RFS/PFS/DFSp-valueOSp-valueReference
RFASurgeryRFASurgery6
  54.7%/5y*50.5%/5y*0.49870.4%/5y*74.6%/5y*0.828
MWASurgeryMWASurgery7
  38.7%/5y#35.7%/5y#0.80171.9%/5y#67.6%/5y#0.879
MWALaparoscopicMWALaparoscopic8
  49.7%/5y§55.6%/5y§0.07166.8%/5y§66.2%/5y§0.46

Development of various imaging tools have made it possible to identify benign liver tumors that are incidentally found as focal hepatic lesions.9 In 1994, the World Congress of Gastroenterology reported a heterogeneous group of lesions with different cellular origins, including hemangioma, focal nodular hyperplasia (FNH), and hepatocellular adenoma (HCA).10 Despite their nonmalignant nature, some benign liver tumors require treatment for symptoms caused by the presence of the tumor and/or continuous enlargement. Ablation may be the treatment of choice because it is less invasive than surgery. Moreover, there is a quite difference in the cost burden, which is approximately $10,000 for hepatic resection and approximately $5,000 for ablation in Japan, being much more economical for the patients in the latter.

Against that background, this review describes recent trends, progress, and limitations of ablation-based treatment for benign liver tumors. The aim was to recognize and understand the current concepts, to extract problems, and to discuss future directions in relevant fields.

Methods

Literature search and study selection

We searched PubMed and the Web of Science core collection databases using the terms “ablation” AND “liver” OR “hepatic” OR “hepatic lesion” OR “hepatic nodule” AND “benign”.

Eligibility criteria and data extraction

Full-text articles published in English were included, except for reviews. To widen the scope of our research, we did not exclude case reports or studies that included pediatric populations (Fig. 1). Two independent hepatologists extracted bibliographic information, including the first author’s name, country, journal name, and demographic information, including the sample size, age, and characteristics and size of hepatic lesions; symptoms, reasons for ablation, and ablation details, methods, guidance, results, and complications.

Flow diagram for literature research.
Fig. 1  Flow diagram for literature research.

Results

Hepatic hemangioma

Hepatic hemangioma is the most common primary benign liver tumor, with a prevalence of 2.5–3.3%.11–13 Hemangiomas are usually small (<4 cm) and solitary, but clinicians occasionally encounter patients with hemangiomas measuring 10–20 cm in diameter, with most patients being asymptomatic.14 The following indications are usually applied to choose the treatment of hemangioma: (1) presence of persistent symptoms such as abdominal pain/discomfort and dyspepsia because of disturbance of bowel movements by mass effects related to hemangioma that are difficult to manage with medical treatments or (2) progressive enlargement of 1–2 cm per year even in asymptomatic patients.

Before treatment, the location of hemangiomas needs to be carefully examined to determine whether they are eligible for approach with an ablation needle (RFA electrode or MWA antenna) with an adequate sonographic window. A laparoscopic approach may be preferred in cases in which the percutaneous approach is difficult. Ultrasound (US) is the most frequently used tool for guiding ablation needles. Computed tomography (CT) guidance is used when US guidance is insufficient to support needle visualization and advancement. According to recent studies, either the laparoscopic/surgical or percutaneous approach is predominantly used with US guidance (Tables 2 and 3).15–29 Complete ablation was reported in >86% of patients with RFA and >84.6% with MWA. The resolution of clinical symptoms was achieved by most patients, complete resolution of clinical symptoms in 50–90.9% by RFA, and 50–100% by MWA.15–24 There are some possible complications of ablation for hemangioma, most of which are classified as Clavien-Dindo grade 1, with hemoglobinuria, fever, and pain being common events (Tables 4 and 5). 15–23,25–29 According to Wu et al.,25 the rates of achieving complete ablation and procedure-related complications were similar in 253 patients with hemangiomas of 5–9.9 cm and 38 patients with hemangiomas of ≥10 cm.25 However, the rates of hemolysis-related and systemic inflammatory response syndrome-related complications were higher in patients with hemangiomas of ≥10 cm than in those with hemangiomas of 5–9.9 cm. In addition, the postoperative stay was longer in the former than in the latter (9.04 vs. 5.73 days, p<0.001). The data suggest that care should be taken when performing ablation for hemangiomas of ≥10 cm in terms of safety risk and patient burden.

Table 2

Effectiveness of RFA for hemangioma

NSize in mmUS/CTApproachEffectiveness
Reference
Symptom-relatedTumor reduction-related
44 (50)50–100USLaparoscopy/Percutaneous86% with complete effect*16
4106–145USSurgical50% with complete relief58–92% volume reduction17
12 (15)25–95USPercutaneous58.3% with significant/complete relief38–79% (mean, 67%) volume reduction15
291 (304)50–200US/CTLaparoscopy/Percutaneous99% with complete effect*25
2728–100USLaparoscopy52% with complete relief100% with complete effect*20
24 (25)40–150USPercutaneous71.4% with complete relief92% with complete effect*19
215.7–25USLaparoscopy50% with complete relief56% and 32% reduction18
106**5–12.8USPercutaneous90.9%/65% with complete relief86.5%/40.7%†† with complete effect26
66#40–100USLaparoscopy76.5% with complete relief94.4% with complete effect*28
72≤50, <100US/CTLaparoscopy/Percutaneous94.4% with complete effect29
Table 3

Effectiveness of MWA for hemangioma

NSize in mmUS/CTApproachEffectiveness
Reference
Symptom-relatedTumor reduction-related
46 (47)50–96USPercutaneous91.5% with complete effect*21
44106–145USPercutaneous50% with complete relief93.2% with complete effect*22
8250–100USPercutaneous88.6% with complete relief89.0% with complete effect*27
12 (13)100–145USPercutaneous100% with complete relief84.6% with complete effect*23
40 (42)41–108USPercutaneous95% with clinical effectiveness100% with technical effectiveness#24
72≤50, <100US/CTLaparoscopy/Percutaneous95.8% with complete effect*29
Table 4

Complications related to RFA for hemangioma

NSize in mmComplicationsReference
4450–100Clavien-Dindo Grade 1*16
  Hemoglobinuria18.2%
  Hemolytic jaundice anemia11.3%
  Elevated serum transaminase11.3%
  Fever9.1%
  Skin burns9.1%
  Transient renal damage6.9%
  Hydrothorax6.9%
Clavien-Dindo Grade 3a*
  Pneumothorax2.3%
  Liver abscess2.3%
4106–145  Self-limiting postprocedural pain lasting for 6 days25%17
  Macroscopic hematuria lasting for 24 h25%
1225–95NONE15
29150–200Clavien-Dindo Grade 125
  Hemoglobinuria81.9%
  Anemia13.2%
  Lung injury1.6%
  SIRS39.1%
  Postprocedural pain7.2%
  Transient hepatic injury16.1%
  Asymptomatic pleural effusion5.9%
  Skin burn1%
Clavien-Dindo Grade 2
  Esophageal injury0.3%
  Myocardial dysfunction0.3%
Clavien-Dindo Grade 2–3
  Diaphragmatic injury1.3%
  AKI1%
Clavien-Dindo Grade 3
Symptomatic pleural effusion0.3%
  Bleeding at the electrode entry site1.3%
  Rupture of hepatic hemangioma1%
Clavien-Dindo Grade 4
  ARDS0.3%
2728–100Postoperative low-grade fever48.1%**20
  Elevated serum transaminase48.1%**
2440–150Abdominal pain16.7%***19
  Fever8.3%***
  Anemia8.3%***
  Jaundice12.5%***
  Ascites4.2%***
215.7–25AKI, anemia100%18
1065–12.8Clavien-Dindo Grade 126
  Pleural effusion7.5%
Clavien-Dindo Grade 2
  Fever8.5%
  Hemoglobinuria2.8%
  Moderate anemia1.9%
  Acute renal insufficiency2.8%
  Jaundice16%
Clavien-Dindo Grade 3
  Abdominal Hemorrhage0.9%
66#40–100Fever18.8%28
  Hemoglobinuria3.1%
  Transient renal damage3.1%
  Jaundice3.1%
144##Clavien-Dindo Grade 129
  Hemoglobinuria76.4%
  SIRS30.6%
  Hemolytic jaundice8.3%
  Anemia6.9%
  Postprocedural pain8.3%
  Transient hepatic injury12.5%
  Asymptomatic pleural effusion2.8%
Table 5

Complications related to MWA for hemangioma

NSize in mmComplicationsReference
46 (47)50–96Minor complications (fever, mild pain and transient hepatic dysfunction)*78.3%21
Major complications (2 with acute renal dysfunction** , 2 with symptomatic pleural effusion**, and 1 with Hyperbilirubinemia)10.9%
44106–145Clavien-Dindo Grade 122
  Pain22.7%
  Excessive wound exudate6.8%
  Low-grade fever4.5%
  Coprostasis13.6%
  Stomach discomfort4.5%
  AKI6.8%
Clavien-Dindo Grade 3
  Diaphragmatic hernia2.3%
8250–100Major complications9.8%SIR#27
  Diaphragmatic hernia1.2%D
  Symptomatic pleural effusion2.4%C
  Jaundice2.4%C
  Acute renal dysfunction3.7%C
Minor complications43.9%
  Fever6.1%B
  Abdominal pain22%B
  Both fever and pain6.1%B
  Other discomfort9.8%A
12 (13)100–145Fever (≧38)15.4%23
  Constipation30.8%
  Slight wound pain30.8%
  Stomach discomfort7.7%
  High bilirubin (total bilirubin >34.2 mmol/L)53.8%
  Anemia (hemoglobin <100 g/L)30.8%
  Elevated serum transaminase (>80 U/L)100%
  Elevated serum creatinine15.4%
40 (42)41–108Fever (37.2–8.5 Celsius degrees lasting 1–2 days)15%
  Pleura effusion without drainage5%
  Hemoglobinuria at the first urination after ablation37.5%
  AKI caused by massive heat-induced intravascular hemolysis##2.5%
144§Clavien-Dindo Grade 129
  Hemoglobinuria48.6%
  SIRS15.3%
  Hemolytic jaundice2.8%
  Anemia4.2%
  Postprocedural pain4.2%
  Transient hepatic injury4.2%
  Asymptomatic pleural effusion1.4%

Regarding technical aspects, Qu et al.26 recommended the use of three-step RFA for hepatic hemangiomas of 5–12.8 cm, briefly defined by the ablation of the target lesion following ablation of the feeding artery and aspiration of blood from the tumor. The technique appears to increase the efficiency of RFA, with a shorter ablation time, fewer punctures, improved effectiveness and safety, better complete ablation rate, better maximum postoperative pain score, better symptomatic relief, and lower rate of severe complication. In addition, as they reported a shorter hospital stay, three-step RFA may benefit patients by reducing the burden, but there was no description of the financial aspect.

According to the study comparing MWA (n=82, 6.9±1.8 cm) and transcatheter arterial embolization (TAE; n=53, 7.1±1.5 cm) for the treatment of large hepatic hemangiomas,27 the MWA group had a significantly higher rate of complete radiological response defined as no obvious enhancement of lesions on contrast-enhanced CT/magnetic resonance imaging (MRI; 89.0% vs. 37.7%, p<0.001) and complete clinical response defined as disappearance of hemangioma-related symptoms (88.6% vs. 69.2%, p=0.046). MWA was associated with fewer minor complications, defined as events without substantial morbidity or disability that increased the level of care (43.9% vs. 66.0%, p=0.019), shorter time of analgesic use (p<0.001), and shorter hospital stay (p=0.003) than the TAE group. The study suggests that TAE has limited effectiveness for volume reduction of hemangioma. Meanwhile, Wang et al.30 reported the outcome of TAE followed by percutaneous US-guided MWA for hemangioma (95 × 97 × 117 mm), with an 80% reduction with no complications, which might have potential as an option for the treatment of large hemangioma. A recent prospective study compared the clinical results of laparoscopic RFA (6.4 cm, 4.0–9.3) and open resection (6.5 cm, 4.0–9.8) for the treatment of symptomatic-enlarging hepatic hemangiomas.28 Although radiological and clinical responses were comparable between the groups, the laparoscopic RFA group had a significantly shorter operative time and less blood loss than the open resection group. In addition, patients who underwent laparoscopic RFA experienced significantly less pain, required less analgesia, had a significantly shorter length of hospital stay, and had lower hospital costs compared with those who underwent open resection. Another study retrospectively compared the effectiveness of percutaneous MWA and surgical resection (open 62 and laparoscopic 6) for hemangiomas (6.3±1.4 cm, 5.0–9.6); the MWA group had a significantly shorter operative time, less blood loss, and a lower rate of prophylactic abdominal drainage than the surgical resection group.22 In addition, postoperative recovery was significantly better and duration of hospital stay was significantly shorter in the MWA group than in the surgical resection group. However, there was no significant difference in effectiveness between the groups. Taken together, despite the limited number of studies comparing ablation and surgical treatment, ablation appears to provide an sufficient therapeutic effect compared with open surgery, with the advantages of safety and less burden for patients. However, difference of clinical effectiveness between RFA and MWA for hemangioma has not been fully described, as limited studies have compared the two methods. In a recent study, MWA had a shorter ablation time, fewer hemolysis-related complications, and a shorter hospital stay.29 Additional studies may be required to compare RFA and MWA, and long-term outcomes of ablation for hemangioma with cost effectiveness.

Hepatocellular adenoma (HCA)

HCA is a benign liver tumor that most often develops in young women taking oral contraceptives, with an incidence of approximately 3 per 100,000 women.31 Complications such as hemorrhage (15–20%) or malignant transformation (5%) appear to increase with increase in tumor size. Therefore, surgical treatment is recommended for HCAs of >5 cm.32

There are limited reports regarding the ablative effects of HCA (Table 6).33–37 Rocourt et al.33 reported a 13-year-old patient in whom a liver tumor measuring 35 mm was incidentally detected and was histologically diagnosed as adenoma by percutaneous biopsy.33 Because of the relatively small lesion, RFA was selected as the treatment of choice. US-guided percutaneous RFA was performed under general anesthesia with three sequential overlapping ablations of 12 min each. No evidence of recurrence was seen on MRI 2 years after treatment. A study of three cases of multiple HCAs (2–5 cm) treated with hepatic resection combined with RFA (intraoperative approach with no complications) was reported in the USA in the same year.34 An RFA study by McDaniel et al.35 used four cool-tip 15 cm long electrodes (Radionics, Burlington, MA, USA) and a 3 cm ablative zone, under laparoscopic US guidance with a four-way laparoscopic 8666-RF intraoperative transducer (BK Medical, Peabody, MA, USA) to treat HCA (segment 7; 5.5 cm) adjacent to the right hemidiaphragm in an 11-year-old patient with chronic liver disease secondary to alpha-1-antitrypsin deficiency. The patient did well after treatment and was discharged on the third post-operative day. The follow-up MRI performed 19 months after the first RFA procedure showed a further decrease in the ablation zone size, with no residual tumor. Costa et al.36 treated 16 patients with 26 HCAs between 11 and 48 mm with US/CT-guided RFA using coaxial 14–18 gauge RFA needles and 3–4 cm cool-tip needle systems.36 The treatment was uneventful and technically successful in all cases. Only one patient (4%) had residual lesions that increased in size over time, but showed no further enlargement in or around the ablated area after re-ablation. The mean follow-up was 27 (range: 2–84) months. The authors also found that fat in the ablation zone of HCAs was a common finding on MRI, which, in isolation, does not indicate residual tumors. Thus, RFA seems to have beneficial effects in the treatment of HCAs, meanwhile, there is a case report that demonstrated the effect of percutaneous CT-guided irreversible electroporation, a nonthermal ablation of a 5 cm HCA in a 28-year-old woman who wanted to get pregnant.37 It was effective, with rapid and impressive tumor shrinkage without any complications. However, it should be noted that HCAs are benign tumors, and treatment is limited to preventing bleeding or malignant transformation. Radical treatment needs to be selected according to the subtype, as described in recently published guidelines endorsing the use of personalized clinical care.38 Following the guidelines, the indications for treatment are any HCA in men regardless of size and subtype and HCAs of >5 cm or much rarer smaller HCAs with worrisome features such as β-catenin activation or rapid growth in women.38 Appropriate selection of surgical or nonsurgical treatment including various ablation techniques, should be further investigated in studies with large patient populations.

Table 6

Ablation for hepatocellular adenoma

NSize in mmMethodGuidanceApproachEffectReference
155RFAUSLaparoscopyNo residual tumor, 19 months35
135RFAUSPercutaneousNo recurrence, 2 years33
3 (*)20–50RFAUSSurgical1 residual tumor**34
16 (26)11–48RFAUS/CTPercutaneous1/26 (4%) with residual tumor**36
150IRECTPercutaneousRapid tumor shrinkage37

Hepatic epithelioid hemangioendothelioma

Hepatic epithelioid hemangioendothelioma (HEHE) is a rare vascular tumor that consists of epithelioid and histiocytoid vascular endothelial cells in a myxoid or fibrotic stroma. HEHE has a variable clinical course. It is generally considered less aggressive than angiosarcoma, but is not completely benign.39 There is no standard/consensus therapeutic strategy, and there are several treatment options, including liver transplantation, liver resection, chemotherapy, and locoregional/radiation therapy. Cao et al.40 evaluated the medical records of 12 patients with histologically proven HEHE who were followed up for a mean of 39.6±20.1 (range: 15–82) months.40 Three patients, including one with three lesions of a maximum 3.5 cm, one with >5 lesions, and one with 4 lesions, who underwent RFA were without recurrence for a median 36 (range: 28–63) months of follow-up. Although the sample size was small, RFA showed favorable results for HEHE.

FNH

There were two reports of cases with FNH treated by ablation and having favorable outcomes. One was treated by CT-guided percutaneous cool-tip RFA that unfortunately resulted in incomplete ablation of a 22 mm FNH, but provided disappearance of right upper quadrant pain with no complications and required only a 2 day hospital stay.41 The second was a US-guided percutaneous MWA that resulted in complete ablation of a 29 mm FNH with no complications and a 6 day hospital stay.42 However, it should be noted that Cheng et al.43 reported regrowth of residual FNH after treatment with US-guided percutaneous MWA, which was finally treated by TAE. Although it is difficult to draw a conclusion because of the small number of studies, indication of treatment and methodology of ablation need to be further evaluated for FNH. In addition, selection of post-treatment monitoring should be discussed because of the possibility of enlargement of residual lesion.

Cysts

Kim et al.44 described the treatment of 14 hepatic cysts with a mean diameter of 7.8 (range: 3.7–12.7) cm and mean initial cyst volume of 243.7 (range: 25.1–1,057.2) mL in 14 patients by US-guided percutaneous cool-tip RFA performed after aspiration of the cyst contents until the diameter was ≤3 cm in diameter. Eight of nine cysts ≤8.5 cm in diameter significantly decreased in volume. The mean reduction was 93.6% (range: 76.8–100), and one cyst was surgically removed because of regrowth. Four cysts 8.5–12.0 cm in diameter were reduced by 61.7% (range: 26.0–98.8). There were no major complications. The data suggest that RFA has a role as an option alternative to conventional sclerotherapy or surgery, and volume reduction rate showed relation with pre-treatment size and presence of septum.

Summary, recent progress, limitations, and future planning

A recent advance in ablation-based treatment is the introduction and spread of MWA which has become a representative therapy for the treatment of benign and malignant tumors. Another advance is the development of imaging techniques having improved time and spatial resolution in support of the ablation procedure. As already shown, thermal ablation appears to be an effective treatment method for hepatic hemangiomas and HCAs. The burden on patients undergoing MWA may be smaller than in patients undergoing surgical treatment in terms of operative time, complications, and duration of hospital stay. However, for patients undergoing RFA, because limited studies have been conducted, it may be difficult to draw a definite conclusion. Moreover, there are a few reports of ablation of angiomyolipoma with malignant potential,45 or FNH,46,47 the effectiveness of ablation for such tumors should be investigated in future studies.

At this time, there are some limitations in this field. First, histological diagnosis of hepatic lesions is usually made by needle biopsy in cases treated by ablation. There is a risk that malignant potential or combined malignancy cannot completely be excluded by the limited sample, and distinguishing HCA and FNH or HCA and well-differentiated HCC can still be challenging, even for an expert pathologist.31 In such a situation, we need to be mindful of the risk of incomplete ablation and residual lesions, the possible need of subsequent surgery, increased medical expense, and patient discomfort. Second, a definitive indication for ablation for benign liver tumors has not been determined, and the selection of treatment is generally performed based on clinicians’ judgment. In that regard, establishment of international guidelines may be needed. Third, there is a risk of complications, particularly in cases with large hemangiomas, and hemolysis-related complications such as acute kidney injury that may cause serious condition. Therefore, future studies should be conducted to determine how to prevent or reduce the risk of complications. In addition, ablation techniques to treat benign liver tumors other than thermal-based methods should be studied. Against these background, it is strongly recommended to plan future studies of (1) risk stratification of benign hepatic lesions based on resected specimens, (2) ablative techniques other than thermal-based methods for various benign hepatic lesions including the occurrence of complications, and (3) large, prospective studies to provide international guidelines.

Conclusion

Although there are many positive results of the effectiveness of the ablative treatment for benign hepatic tumors, more studies with larger patient populations are required to confirm their benefits, including cost effectiveness and to provide specific measures against possible complications. Further, organization of medical care, including those for pre-ablation, ablation, and post-ablation may help the improvement of the quality in the practical management of benign hepatic tumors.

Abbreviations

CT: 

computed tomography

FNH: 

focal nodular hyperplasia

HCA: 

hepatocellular adenoma

HCC: 

hepatocellular carcinoma

HEHE: 

hepatic epithelioid hemangioendothelioma

MRI: 

magnetic resonance imaging

MWA: 

microwave ablation

RFA: 

radiofrequency ablation

TAE: 

transcatheter arterial embolization

Declarations

Funding

None to declare.

Conflict of interest

The authors have no conflict of interests related to this publication.

Authors’ contributions

Conception and design (HM), administrative support (SS), provision of study materials or patients (TY), collection and assembly of data (MT, HN), data analysis and interpretation (HM, SS), manuscript writing and final approval of manuscript (all authors).

References

  1. Salati U, Barry A, Chou FY, Ma R, Liu DM. State of the ablation nation: a review of ablative therapies for cure in the treatment of hepatocellular carcinoma. Future Oncol 2017;13(16):1437-1448 View Article PubMed/NCBI
  2. Hinshaw JL, Lubner MG, Ziemlewicz TJ, Lee FT, Brace CL. Percutaneous tumor ablation tools: microwave, radiofrequency, or cryoablation—what should you use and why?. Radiographics 2014;34(5):1344-1362 View Article PubMed/NCBI
  3. Tan W, Deng Q, Lin S, Wang Y, Xu G. Comparison of microwave ablation and radiofrequency ablation for hepatocellular carcinoma: a systematic review and meta-analysis. Int J Hyperth 2019;36(1):264-272 View Article PubMed/NCBI
  4. Han J, Fan YC, Wang K. Radiofrequency ablation versus microwave ablation for early stage hepatocellular carcinoma: A PRISMA-compliant systematic review and meta-analysis. Medicine (Baltimore) 2020;99(43):e22703 View Article PubMed/NCBI
  5. Luo W, Zhang Y, He G, Yu M, Zheng M, Liu L, et al. Effects of radiofrequency ablation versus other ablating techniques on hepatocellular carcinomas: a systematic review and meta-analysis. World J Surg Oncol 2017;15(1):126 View Article PubMed/NCBI
  6. Kudo M, Hasegawa K, Kawaguchi Y, Takayama T, Izumi N, Yamanaka M, et al. A multicenter randomized controlled trial to evaluate the efficacy of surgery versus radiofrequency ablation for small hepatocellular carcinoma (SURF trial): Analysis of overall survival. J Clin Oncol 2021;39_suppl:4093-4093 View Article PubMed/NCBI
  7. Zheng H, Xu C, Wang X, Li J, Zhao X, Qi J, et al. Microwave ablation shows similar survival outcomes compared with surgical resection for hepatocellular carcinoma between 3 and 5 cm. Int J Hyperthermia 2020;37:1345-1353 View Article PubMed/NCBI
  8. Wang Z, Liu M, Zhang DZ, Wu SS, Hong ZX, He GB, et al. Microwave ablation versus laparoscopic resection as first-line therapy for solitary 3-5-cm HCC. Hepatology 2022;76(1):66-77 View Article PubMed/NCBI
  9. European Association for the Study of the Liver. EASL Clinical Practice Guidelines on the management of benign liver tumours. J Hepatol 2016;65(2):386-398 View Article PubMed/NCBI
  10. International working party. Terminology of nodular hepatocellular lesions. Hepatology 1995;22(3):983-993 View Article PubMed/NCBI
  11. Kaltenbach TE, Engler P, Kratzer W, Oeztuerk S, Seufferlein T, Haenle MM, et al. Prevalence of benign focal liver lesions: ultrasound investigation of 45,319 hospital patients. Abdom Radiol (NY) 2016;41(1):25-32 View Article PubMed/NCBI
  12. Mocchegiani F, Vincenzi P, Coletta M, Agostini A, Marzioni M, Baroni GS, et al. Prevalence and clinical outcome of hepatic haemangioma with specific reference to the risk of rupture: A large retrospective cross-sectional study. Dig Liver Dis 2016;48(3):309-314 View Article PubMed/NCBI
  13. Liu X, Yang Z, Tan H, Xu L, Liu L, Huang J, et al. Patient age affects the growth of liver haemangioma. HPB (Oxford) 2018;20(1):64-68 View Article PubMed/NCBI
  14. Gandolfi L, Leo P, Solmi L, Vitelli E, Verros G, Colecchia A. Natural history of hepatic haemangiomas: clinical and ultrasound study. Gut 1991;32(6):677-680 View Article PubMed/NCBI
  15. Cui Y, Zhou LY, Dong MK, Wang P, Ji M, Li XO, et al. Ultrasonography guided percutaneous radiofrequency ablation for hepatic cavernous hemangioma. World J Gastroenterol 2003;9(9):2132-2134 View Article PubMed/NCBI
  16. Wen SQ, Wan M, Len KM, Hu QH, Xie XY, Wu Q, et al. Safety and Efficacy of Laparoscopic Radiofrequency Ablation for Hepatic Hemangiomas: A Multicenter Retrospective Study. Ann Hepatol 2018;17(2):268-273 View Article PubMed/NCBI
  17. van Tilborg AA, Nielsen K, Scheffer HJ, van den Tol P, van Waesberghe JH, Sietses C, et al. Bipolar radiofrequency ablation for symptomatic giant (>10 cm) hepatic cavernous haemangiomas: initial clinical experience. Clin Radiol 2013;68(1):e9-e14 View Article PubMed/NCBI
  18. van Tilborg AAJM, Dresselaars HF, Scheffer HJ, Nielsen K, Sietses C, van den Tol PM, et al. RF Ablation of Giant Hemangiomas Inducing Acute Renal Failure: A Report of Two Cases. Cardiovasc Intervent Radiol 2016;39(11):1644-1648 View Article PubMed/NCBI
  19. Park SY, Tak WY, Jung MK, Jeon SW, Cho CM, Kweon YO, et al. Symptomatic-enlarging hepatic hemangiomas are effectively treated by percutaneous ultrasonography-guided radiofrequency ablation. J Hepatol 2011;54(3):559-565 View Article PubMed/NCBI
  20. Fan RF, Chai FL, He GX, Wei LX, Li RZ, Wan WX, et al. Laparoscopic radiofrequency ablation of hepatic cavernous hemangioma. A preliminary experience with 27 patients. Surg Endosc 2006;20(2):281-285 View Article PubMed/NCBI
  21. Tang XY, Wang Z, Wang T, Cui D, Zhai B. Efficacy, safety and feasibility of ultrasound-guided percutaneous microwave ablation for large hepatic hemangioma. J Dig Dis 2015;16(9):525-530 View Article PubMed/NCBI
  22. Tang X, Ding M, Lu B, Chi J, Wang T, Shi Y, et al. Outcomes of ultrasound-guided percutaneous microwave ablation versus surgical resection for symptomatic large hepatic hemangiomas. Int J Hyperthermia 2019;36(1):632-638 View Article PubMed/NCBI
  23. Wang Z, Tang X, Qi X, Shi Y, Chi J, Li P, et al. Feasibility, safety, and efficacy of ultrasound-guided percutaneous microwave ablation for giant hepatic hemangioma. Int J Hyperthermia 2018;35(1):246-252 View Article PubMed/NCBI
  24. Liu F, Yu X, Liang P, Cheng Z, Han Z, Yu J. Ultrasonography-guided percutaneous microwave ablation for large hepatic cavernous haemangiomas. Int J Hyperthermia 2018;34(7):1061-1066 View Article PubMed/NCBI
  25. Wu S, Gao R, Yin T, Zhu R, Guo S, Xin Z, et al. Complications of Radiofrequency Ablation for Hepatic Hemangioma: A Multicenter Retrospective Analysis on 291 Cases. Front Oncol 2021;11:706619 View Article PubMed/NCBI
  26. Qu C, Liu H, Li XQ, Feng K, Ma K. Percutaneous ultrasound-guided ‘three-step’ radiofrequency ablation for giant hepatic hemangioma (5–15 cm): a safe and effective new technique. Int J Hyperthermia 2020;37(1):212-219 View Article PubMed/NCBI
  27. Shi Y, Song J, Ding M, Tang X, Wang Z, Chi J, et al. Microwave ablation versus transcatheter arterial embolization for large hepatic hemangiomas: clinical outcomes. Int J Hyperthermia 2020;37(1):938-943 View Article PubMed/NCBI
  28. Zhang X, Yan L, Li B, Wen T, Wang W, Xu M, et al. Comparison of laparoscopic radiofrequency ablation versus open resection in the treatment of symptomatic-enlarging hepatic hemangiomas: a prospective study. Surg Endosc 2016;30(2):756-763 View Article PubMed/NCBI
  29. Kong J, Gao R, Wu S, Shi Y, Yin T, Guo S, et al. Safety and efficacy of microwave versus radiofrequency ablation for large hepatic hemangioma: a multicenter retrospective study with propensity score matching. Eur Radiol 2022;32(5):3309-3318 View Article PubMed/NCBI
  30. Wang LZ, Wang KP, Mo JG, Wang GY, Jin C, Jiang H, et al. Minimally invasive treatment of hepatic hemangioma by transcatheter arterial embolization combined with microwave ablation: A case report. World J Clin Cases 2021;9(24):7154-7162 View Article PubMed/NCBI
  31. Nault JC, Bioulac-Sage P, Zucman-Rossi J. Hepatocellular benign tumors-from molecular classification to personalized clinical care. Gastroenterology 2013;144(5):888-902 View Article PubMed/NCBI
  32. Nault JC, Couchy G, Balabaud C, Morcrette G, Caruso S, Blanc JF, et al. Molecular Classification of Hepatocellular Adenoma Associates With Risk Factors, Bleeding, and Malignant Transformation. Gastroenterology 2017;152(4):880-894 View Article PubMed/NCBI
  33. Rocourt DV, Shiels WE, Hammond S, Besner GE. Contemporary management of benign hepatic adenoma using percutaneous radiofrequency ablation. J Pediatr Surg 2006;41(6):1149-1152 View Article PubMed/NCBI
  34. Fujita S, Kushihata F, Herrmann GE, Mergo PJ, Liu C, Nelson D, et al. Combined hepatic resection and radiofrequency ablation for multiple hepatic adenomas. J Gastroenterol Hepatol 2006;21(8):1351-1354 View Article PubMed/NCBI
  35. McDaniel JD, Kukreja K, Ristagno RL, Yazigi N, Nathan JD, Tiao G. Radiofrequency ablation of a large hepatic adenoma in a child. J Pediatr Surg 2013;48(6):E19-E22 View Article PubMed/NCBI
  36. Costa AF, Kajal D, Pereira A, Atri M. Should fat in the radiofrequency ablation zone of hepatocellular adenomas raise suspicion for residual tumour?. Eur Radiol 2017;27(4):1704-1712 View Article PubMed/NCBI
  37. Scheffer HJ, Melenhorst MC, van Tilborg AA, Nielsen K, van Nieuwkerk KM, de Vries RA, et al. Percutaneous irreversible electroporation of a large centrally located hepatocellular adenoma in a woman with a pregnancy wish. Cardiovasc Intervent Radiol 2015;38(4):1031-1035 View Article PubMed/NCBI
  38. European Association for the Study of the Liver. EASL Clinical Practice Guidelines on the management of benign liver tumours. J Hepatol 2016;65(2):386-398 View Article PubMed/NCBI
  39. Studer LL, Selby DM. Hepatic Epithelioid Hemangioendothelioma. Arch Pathol Lab Med 2018;142(2):263-267 View Article PubMed/NCBI
  40. Cao L, Hong J, Zhou L, Ye Y, Liu Y, Yu J, et al. Selection of treatment for hepatic epithelioid hemangioendothelioma: a single-center experience. World J Surg Oncol 2019;17(1):183 View Article PubMed/NCBI
  41. Hedayati P, vanSonnenberg E, Shamos R, Gillespie T, McMullen W. Treatment of symptomatic focal nodular hyperplasia with percutaneous radiofrequency ablation. J Vasc Interv Radiol 2010;21(4):582-585 View Article PubMed/NCBI
  42. Yao Z, Zeng Q, Yu X, Lin S, Jiang S, Ma D, et al. Case Report: Ultrasound-Guided Percutaneous Microwave Ablation of Focal Nodular Hyperplasia in a 9-Year-Old Girl. Front Pediatr 2021;9:710779 View Article PubMed/NCBI
  43. Cheng Z, Liang P, Yu X, Han Z, Liu F, Yu J, et al. Percutaneous microwave ablation for benign focal liver lesions: Initial clinical results. Oncol Lett 2017;13(1):429-434 View Article PubMed/NCBI
  44. Kim PN, Lee Y, Won HJ, Shin YM. Radiofrequency ablation of hepatic cysts: Evaluation of therapeutic efficacy. J Vasc Interv Radiol 2014;25(1):92-96 View Article PubMed/NCBI
  45. Calame P, Tyrode G, Weil Verhoeven D, Félix S, Klompenhouwer AJ, Di Martino V, et al. Clinical characteristics and outcomes of patients with hepatic angiomyolipoma: A literature review. World J Gastroenterol 2021;27(19):2299-2311 View Article PubMed/NCBI
  46. Mounajjed T. Hepatocellular Adenoma and Focal Nodular Hyperplasia. Clin Liver Dis (Hoboken) 2021;17(4):244-248 View Article PubMed/NCBI
  47. Virgilio E, Cavallini M. Managing Focal Nodular Hyperplasia of the Liver: Surgery or Minimally-invasive Approaches? A Review of the Preferable Treatment Options. Anticancer Res 2018;38(1):33-36 View Article PubMed/NCBI
  • Journal of Clinical and Translational Hepatology
  • pISSN 2225-0719
  • eISSN 2310-8819
  • Copyright © 2022 JCTH. All Rights Reserved.
  • Published by Xia & He Publishing Inc.
  • Address: 14090 Southwest Freeway, Suite 300, Sugar Land, Texas 77478, USA
  • Email: service@xiahepublishing.com