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Open Access

Peer-reviewed

Research Article

Efficacy and safety of ultrasound-guided radiofrequency ablation combined with transhepatic artery embolization chemotherapy for hepatocellular carcinoma: A meta-analysis

  • Kerui Pan,

    Roles Conceptualization, Data curation, Formal analysis, Investigation, Resources, Software, Supervision, Validation, Visualization, Writing – original draft, Writing – review & editing

    Affiliation Lianyungang First People’s Hospital, China

    ⨯
  • Sisi Wang,

    Roles Data curation, Formal analysis, Funding acquisition, Investigation, Resources, Validation, Visualization, Writing – original draft, Writing – review & editing

    Affiliation Lianyungang First People’s Hospital, China

    ⨯
  • Xueping Li,

    Roles Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Resources, Software, Supervision, Visualization, Writing – review & editing

    Affiliation Lianyungang First People’s Hospital, China

    ⨯
  • Shuoming Wu

    Roles Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Software, Supervision, Validation, Visualization, Writing – review & editing

    withyou31@163.com

    Affiliation Lianyungang First People’s Hospital, China

    ⨯

Abstract

Objective

Meta-analysis was used to assess the efficacy and safety of ultrasound-guided radiofrequency ablation combined with transhepatic artery embolization chemotherapy for hepatocellular carcinoma.

Methods

Randomized controlled studies on ultrasound-guided radiofrequency ablation combined with transhepatic artery embolization chemotherapy for hepatocellular carcinoma were searched in the databases of PubMed, Embase, Cochrane library, web of science with a search deadline of March 14, 2024. Data were analyzed using Stata 15.0.

Result

Six randomized controlled studies involving 520 individuals were finally included, the results of meta-analysis showed that ultrasound-guided radiofrequency ablation combined with TACE can improve objective response rate [RR = 1.52, 95%CI (1.28, 1.81)], improve disease control rate [RR = 1.15, 95%CI (1.06, 1.24)], The survival rate [RR = 1.34, 95%CI (1.19,1.51)] did not increase adverse reactions [RR = 1.34, 95%CI (1.00,1.79)].

Conclusion

Based on the findings of the current study, ultrasound-guided radiofrequency ablation combined with TACE was found to improve the objective remission rate, disease control rate, and did not increase adverse events in patients with hepatocellular carcinoma.

Citation: Pan K, Wang S, Li X, Wu S (2024) Efficacy and safety of ultrasound-guided radiofrequency ablation combined with transhepatic artery embolization chemotherapy for hepatocellular carcinoma: A meta-analysis. PLoS ONE 19(9): e0305965. https://doi.org/10.1371/journal.pone.0305965

Editor: Ashraf Elbahrawy, Al-Azhar University, EGYPT

Received: March 25, 2024; Accepted: June 8, 2024; Published: September 6, 2024

Copyright: © 2024 Pan et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Data Availability: All relevant data are within the paper and Supporting Information files.

Funding: The author(s) received no specific funding for this work.

Competing interests: The authors have declared that no competing interests exist.

Introduction

Liver cancer is a major health problem, with more than 850,000 cases per year worldwide [1]. This tumor is currently the second leading cause of cancer-related deaths globally, and this number is rising [2, 3]. Globally, liver cancer is the sixth most common cancer and the second leading cause of cancer-related deaths (approximately 800,000 cases per year) [4]. 85–90% of all primary liver cancers are Hepatocellular carcinoma (HCC). Various risk factors for the development of HCC are well defined such as cirrhosis (regenerating nodules to differentiate cirrhosis from fibrosis), hepatitis B virus (HBV) infection, hepatitis C virus (HCV) infection, alcoholism, and metabolic syndrome [5–7]. Due to the high incidence of HCC, the economic burden on society and families is high. Therefore, a better treatment needs to be found [8]. Currently, radical surgery is the first choice for primary liver cancer treatment, but due to the lack of obvious symptoms in the early stage of the disease and the insidious progression of the disease [9], most patients are in the advanced stage of liver cancer when diagnosed and miss the best time for surgery, while transcatheter arterial chemoembolization, molecular targeted therapy, radiotherapy, radiofrequency ablation and other means are the mainstays of the treatment of this kind of patients [10–12].

Transcatheter arterial chemoembolization (TACE) blocks the arteries supplying blood to the liver cancer tissues by blocking the arterial blood supply, and then instills chemotherapeutic drugs to achieve the purpose of inhibiting and killing liver cancer cells [13], but due to the incomplete filling of the embolus agent in the tumor, the overall therapeutic effect is not satisfactory, and most of the patients with primary cancers have been treated with chemotherapy [14]. However, due to the possibility of incomplete filling of embolic agents in the tumor, the overall therapeutic effect is not satisfactory, and most patients with primary liver cancer will undergo secondary surgery, and the prognosis of patients is poor due to the inability of some patients to tolerate the secondary surgery or the high risk of the secondary surgery [14, 15]. Ultrasound plays an important role in the early diagnosis of hepatocellular carcinoma, and the application of ultrasound-guided radiofrequency ablation in hepatocellular carcinoma has gradually matured with the promotion of minimally invasive surgery, which has the characteristics of small trauma and high reproducibility [16, 17]. Ultrasound-guided radiofrequency ablation is a minimally invasive surgical method, which can directly remove the tumor lesions, and can effectively make up for the therapeutic defects of TACE by performing more accurate and safe surgical operations under ultrasound guidance [18, 19]. The efficacy of ultrasound-guided radiofrequency ablation combined with TACE in hepatocellular carcinoma is still controversial [20], so the present study hopes to resolve the controversy by meta-analysis and provide a new choice for clinical patients in the treatment.

Method

The systematic review described herein was accepted by the online PROSPERO international prospective register of systematic reviews [21] of the National Institute for Health Research (CRD42024519464). This meta-analysis does not involve human subjects. IRB review is not required.

Inclusion and exclusion criteria

The included population met the diagnostic criteria for hepatocellular carcinoma [22]. ultrasound-guided radiofrequency ablation combined with TACE was used in the experimental group and TACE was used in the control group, and the primary outcome were objective response rate, disease control rate, and the secondary outcome were survival and adverse event, the randomized controlled trial was included in this study.

Conference abstracts, meta-analyses, systematic reviews, animal experiments, Full text is not available and case reports, people who have previously received other treatments will be considered for exclusion.

Literature retrieval

Randomized controlled trials on ultrasound-guided radiofrequency ablation combined with TACE versus TACE for hepatocellular carcinoma were searched in PubMed, Embase, Cochrane Library, Web of science, with a search deadline of March 14, 2024, using the mesh word combined with a free word: ultrasound, radiofrequency ablation, hepatocellular carcinoma, and TACE. Detailed search strategies are provided in S1 Table.

Data extract

Two authors (Shuoming Wu and Sisi Wang) rigorously screened the literature based on predetermined inclusion and exclusion criteria. In case of any disagreement, they resolved it through discussion or sought the opinion of a third person (Kerui Pan) to negotiate and reach consensus. Information extracted from the included studies included the following key details: study, year, sample size, age, gender, tumor staging, child-Pugh liver function, and outcome.

Included studies’ risk of bias

Two investigators (Shuoming Wu and Sisi Wang) independently assessed the risk of bias as low, unclear, or high using the Cochrane Collaboration’s tools [23]. If there was any disagreement, a third person (Kerui Pan) was consulted to reach consensus. The assessment included seven areas: generation of randomized sequences (selective bias), allocation concealment (selective bias), blinding of implementers and participants (implementation bias), blinding of outcome assessors (observational bias), completeness of outcome data (follow-up bias), selective reporting of study results (reporting bias), and other potential sources of bias. Each included study was assessed individually against these criteria. If a study fully met all criteria, it was at "low risk" of bias, indicating a high-quality study and low overall risk of bias. If a study partially met the criteria, its quality was categorized as ’unclear risk’, indicating a moderate likelihood of bias. If a study did not meet the criteria at all, it was categorized as "high risk", indicating a high risk of bias and low quality of the study.

Data analysis

The collected data were statistically analyzed using Stata 15.0 software (Stata Corp, College Station, TX, USA). Heterogeneity between included studies was assessed using I2 values or Q-statistics. I2 values of 0%, 25%, 50%, and 75% indicated no heterogeneity, low heterogeneity, moderate heterogeneity, and high heterogeneity, respectively. If the I2 value was equal to or greater than 50%, a sensitivity analysis was performed to explore potential sources of heterogeneity. If heterogeneity was less than 50 per cent, analyses were conducted using a fixed-effects model. Standardized mean difference (SMD) and 95% confidence interval (CI) were used for continuous variables and odds ratio (OR) and 95% confidence interval (CI) for dichotomous variables. In addition, random effects model and Egger’s test were used to assess publication bias.

Result

Fig 1 shows our literature search process, which initially retrieved 4422 documents, removed 1639 duplicates, removed 2767 articles by reading titles and abstracts, removed 10 papers by reading the full text, and finally included 6 randomized controlled trials [24–29] for analysis.

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Fig 1. Literature search flow chart.

https://doi.org/10.1371/journal.pone.0305965.g001

Basic characteristics and risk of bias of the included studies

Six randomized controlled studies involving 520 individuals were finally included, aged 48–62 years, Baseline characteristics are shown in Table 1 The six included studies clearly accounted for the method of randomization used, and the risk of bias results are shown in Figs 2 and 3.

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Fig 2. Risk of bias graph.

https://doi.org/10.1371/journal.pone.0305965.g002

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Fig 3. Risk of bias summary.

https://doi.org/10.1371/journal.pone.0305965.g003

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Table 1. Basic features of literature.

https://doi.org/10.1371/journal.pone.0305965.t001

Result of meta-analysis

Objective response rate.

5 articles mentioned the objective response rate, which was tested for heterogeneity (I2 = 0%, P = 0.911), therefore fixed effects model was used. The results of the analysis (Fig 4) suggested that ultrasound-guided radiofrequency ablation combined with TACE can improve objective response rate [RR = 1.52, 95% CI (1.28, 1.81)].

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Fig 4. Forest plot of objective response rate meta-analysis.

https://doi.org/10.1371/journal.pone.0305965.g004

Disease control rate.

5 articles mentioned the disease control rate, which was tested for heterogeneity (I2 = 48%, P = 0.103), therefore fixed effects model was used. The results of the analysis (Fig 5) suggested that ultrasound-guided radiofrequency ablation combined with TACE can improve disease control rate [RR = 1.15, 95% CI (1.06, 1.24)].

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Fig 5. Forest plot of disease control rate meta-analysis.

https://doi.org/10.1371/journal.pone.0305965.g005

Survival rate.

4 article mentioned the survival rate, the heterogeneity test (I2 = 33.8%,P = 0.137), so the fixed effect model was used for the analysis, and the results (Fig 6) of the analysis suggested that ultrasound-guided radiofrequency ablation combined with TACE can improve the survival rate [RR = 1.34,95%CI(1.19,1.51)], and we performed subgroup analyses based on survival time, in which one-year survival [RR = 1.31, 95%CI (1.13,1.50)], two-year survival [RR = 1.28, 95%CI (1.01,1.62)], three-year survival [RR = 2.12, 95%CI (1.36, 3.31)].

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Fig 6. Forest plot of survival rate meta-analysis.

https://doi.org/10.1371/journal.pone.0305965.g006

Adverse events.

4 articles mentioned adverse reactions (including fever, vomiting, and jaundice), and the test of heterogeneity (I2 = 49%,P = 0.056), therefore, the analysis was performed using a fixed-effects model, and the results (Fig 7) of the analysis suggested that ultrasound-guided radiofrequency ablation combined with TACE does not increase adverse reactions [RR = 1.34, 95%CI (1.00,1.79)], we which fever [RR = 1.62, 95%CI (0.97,2.70)], vomiting [RR = 1.26, 95%CI (0.87,1.83)], jaundice [RR = 1.01, 95%CI (0.37,2.72)].

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Fig 7. Forest plot of adverse reactions meta-analysis.

https://doi.org/10.1371/journal.pone.0305965.g007

Published bias.

Publication bias was assessed by an Egger’s test for objective response rate, disease control rate, survival rate, adverse reactions. Which showed no publication bias for objective response rate (p = 0.08), disease control rate (P = 0.24), survival rate (P = 0.21), adverse events (P = 0.133).

Discussion

Previous study have investigated radiofrequency ablation combined with TACE in the treatment of hepatocellular carcinoma, but without ultrasound induction [30]; therefore, to the best of our knowledge, this is the first time to evaluate the efficacy and safety of ultrasound-guided radiofrequency ablation combined with TACE in the treatment of hepatocellular carcinoma. Ultrasound-guided radiofrequency ablation is a new therapeutic modality, the main mechanism of which is to insert radiofrequency electrodes into the tumor under the guidance of ultrasound, turn on the electrodes, emit electromagnetic waves, oscillate the tumor tissues, emit huge heat energy, distribute the tumor tissues at a temperature of 90~100°C, cleave the DNA chain of the tumor at a high temperature, denature the proteins, coagulate the blood vessels around the tumor, and thus treat the liver cancer cells and the liver cancer cells [31, 32]. This can effectively prevent the metastasis of liver cancer cells to the liver or the whole body.

In our current study, we found that the ultrasound-guided radiofrequency ablation modality combined with TACE increased the objective remission rate, disease control rate, and survival rate of hepatocellular patients, and did not increase adverse events, The high survival rate and disease remission rate after combined treatment may be due to the following reasons: first, iodide precipitates around the lesion during combined treatment. Therefore, it can not only be used as a marker for radiofrequency ablation to facilitate the operator to recognize the ablation area, but also as a heat-conducting medium to improve the ablation efficiency and keep the surrounding hepatocellular carcinoma microenvironment in a static state [33, 34]. By improving the ablation effect, tumor recurrence can be reduced; second, TACE can reduce the heat loss during RF ablation by blocking blood flow into the tumor [35]; third, chemotherapeutic agents targeting malignant tumors increase the effect of high body temperature on cancer cells. Finally, TACE can further treat microscopic lesions that cannot be detected by the naked eye or imaging, thus improving patient survival and disease remission rates. According to the Barcelona Clinical Hepatocellular Carcinoma Group guidelines [36, 37], unresectable hepatocellular carcinoma outside the criteria for ablation is considered unsuitable for ablation, and palliative treatments, such as TACE, are recommended. TACE can reveal preoperatively undetected microscopic lesions, embolize blood vessels supplying the tumor, and at the same time reduce the "heat-loss effect", kill tumor cells, and reduce the size and number of tumors to achieve stage reduction [38]. The size and number of tumor cells can be reduced, and the tumor can be downstage. TACE and combined ultrasound-guided radiofrequency ablation as a treatment for hepatocellular carcinoma beyond the ablation standard has a good long-term effect. Shi et al. [39] studied the efficacy of combined ultrasound-guided radiofrequency ablation (72 cases) and ultrasound-guided radiofrequency ablation (357 cases) after downstage of TACE, and the results showed that the 1-, 3-, and 5-year OS in the combined group and the ultrasound-guided radiofrequency ablation group were 99%, 80%, 66%, and 94%, 84%, and 66%, respectively, 66% and 94%, 84%, 69%, respectively. The efficacy of TACE combined with ultrasound-guided radiofrequency ablation compared with ultrasound-guided radiofrequency ablation alone for the treatment of a single hepatocellular carcinoma of 3.1–5.0 cm in diameter has also been reported in the literature [40], which concluded that TACE combined with ultrasound-guided radiofrequency ablation for the treatment of hepatocellular carcinoma of 3.1–5.0 cm in diameter of a single node showed a better local tumor control rate and patient survival than that of ultrasound-guided radiofrequency ablation therapy alone [41].

However, our current study still has several limitations. First, the studies were all from Asian populations, using differences in Child-Pugh classification, tumor size, tumor number, and tumor stage. These factors may affect the reliability of the conclusions; second, due to the limited number of included studies, the results should be interpreted with caution; third, the inclusion of malefactors lacked detailed implementation details about the blinding and random allocation methods, which increased the risk of correlation bias.

Conclusion

Based on the results of the current study, ultrasound-guided radiofrequency ablation combined with TACE may improve the objective remission rate and disease control rate in patients with hepatocellular carcinoma without increasing adverse events. However, due to the existence of study limitations, we hope that more high-quality randomized controlled studies will be available in the future to support our opinion.

References

  1. 1. García-Criado Á. and Bruix J., Screening for liver cancer: The good, the bad, and the ugly. Hepatology, 2024. 79(1): p. 12–14. pmid:37505215
  2. 2. Terrault N.A., et al., Liver Transplantation 2023: Status Report, Current and Future Challenges. Clin Gastroenterol Hepatol, 2023. 21(8): p. 2150–2166. pmid:37084928
  3. 3. Wu S., et al., Smart nanoparticles and microbeads for interventional embolization therapy of liver cancer: state of the art. J Nanobiotechnology, 2023. 21(1): p. 42. pmid:36747202
  4. 4. Gourd E., Growing liver cancer death rates in the UK call for healthier lifestyle choices. Lancet Oncol, 2023. 24(8): p. e329. pmid:37482069
  5. 5. Forner A., Reig M., and Bruix J., Hepatocellular carcinoma. Lancet, 2018. 391(10127): p. 1301–1314. pmid:29307467
  6. 6. Jelic S., Hepatocellular carcinoma: ESMO clinical recommendations for diagnosis, treatment and follow-up. Ann Oncol, 2009. 20 Suppl 4: p. 41–5. pmid:19454459
  7. 7. Simon S.M., Fighting rare cancers: lessons from fibrolamellar hepatocellular carcinoma. Nat Rev Cancer, 2023. 23(5): p. 335–346. pmid:36932129
  8. 8. Taieb J., Barbare J.C., and Rougier P., Medical treatments for hepatocellular carcinoma (HCC): what’s next? Ann Oncol, 2006. 17 Suppl 10: p. x308–14. pmid:17018744
  9. 9. Befeler A.S. and Di Bisceglie A.M., Hepatocellular carcinoma: diagnosis and treatment. Gastroenterology, 2002. 122(6): p. 1609–19. pmid:12016426
  10. 10. Cabibbo G. and Bruix J., Radiological endpoints as surrogates for survival benefit in hepatocellular carcinoma trials: All that glitters is not gold. J Hepatol, 2023. 78(1): p. 8–11. pmid:36323356
  11. 11. Llovet J.M. and Beaugrand M., Hepatocellular carcinoma: present status and future prospects. J Hepatol, 2003. 38 Suppl 1: p. S136–49. pmid:12591191
  12. 12. Parikh N.D. and Pillai A., Recent Advances in Hepatocellular Carcinoma Treatment. Clin Gastroenterol Hepatol, 2021. 19(10): p. 2020–2024. pmid:34116048
  13. 13. Lu J., et al., Management of patients with hepatocellular carcinoma and portal vein tumour thrombosis: comparing east and west. Lancet Gastroenterol Hepatol, 2019. 4(9): p. 721–730. pmid:31387735
  14. 14. Liu B., et al., The combination of transcatheter arterial chemoembolisation (TACE) and thermal ablation versus TACE alone for hepatocellular carcinoma. Cochrane Database Syst Rev, 2022. 1(1): p. Cd013345. pmid:34981511
  15. 15. Lee K.H., et al., Transcatheter arterial chemoembolization for hepatocellular carcinoma: anatomic and hemodynamic considerations in the hepatic artery and portal vein. Radiographics, 2002. 22(5): p. 1077–91. pmid:12235337
  16. 16. Lindblad K.E. and Lujambio A., Imaging for better responses to immunotherapy in hepatocellular carcinoma. Hepatology, 2023. 77(1): p. 6–9. pmid:35727179
  17. 17. Parikh N.D., Tayob N., and Singal A.G., Blood-based biomarkers for hepatocellular carcinoma screening: Approaching the end of the ultrasound era? J Hepatol, 2023. 78(1): p. 207–216. pmid:36089157
  18. 18. Kim J.W., et al., Ultrasound-Guided Percutaneous Radiofrequency Ablation of Liver Tumors: How We Do It Safely and Completely. Korean J Radiol, 2015. 16(6): p. 1226–39. pmid:26576111
  19. 19. Wu C.H., et al., Iodized oil computed tomography versus ultrasound-guided radiofrequency ablation for early hepatocellular carcinoma. Hepatol Int, 2021. 15(5): p. 1247–1257. pmid:34338971
  20. 20. Cha D.I., et al., Combined Transarterial Chemoembolization and Radiofrequency Ablation for Hepatocellular Carcinoma Infeasible for Ultrasound-Guided Percutaneous Radiofrequency Ablation: A Comparative Study with General Ultrasound-Guided Radiofrequency Ablation Outcomes. Cancers (Basel), 2023. 15(21). pmid:37958370
  21. 21. Page M.J., et al., The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. Bmj, 2021. 372: p. n71. pmid:33782057
  22. 22. El-Serag H.B., et al., Diagnosis and treatment of hepatocellular carcinoma. Gastroenterology, 2008. 134(6): p. 1752–63. pmid:18471552
  23. 23. Higgins J.P., et al., The Cochrane Collaboration’s tool for assessing risk of bias in randomised trials. Bmj, 2011. 343: p. d5928. pmid:22008217
  24. 24. Puli Zhu, Wang DESheng, and Tian Defu, Clinical observation of 124 cases of primary liver cancer treated by hepatic arterial chemoembolization combined with radiofrequency ablation. Journal of Hepatobiliary and Pancreatic Surgery, 2018. 30(01): p. 1–4.
  25. 25. Wang JX, Liu TB, and Li XH, Effect of transcranial arterial embolization chemotherapy combined with ultrasound-guided radiofrequency ablation for primary liver cancer. Chinese Journal of Practical Medicine, 2018. 13(30): p. 22–23.
  26. 26. Wang LING-Ting and Ji Ting-Ting, Effects of simultaneous ultrasound guided radiofrequency ablation of hepatic artery chemoembolization on apoptotic molecules and immune function of primary liver cancer. Journal of Clinical Medicine Research and Practice, 2022. 7(30): p. 60–63+78.
  27. 27. Wang Minglei, Yin Dawei, and Zhu Xiana, Effect of ultrasound-guided unipolar cold cycle radiofrequency ablation combined with TACE in the treatment of liver cancer. Primary Medicine Forum, 2017. 21(10): p. 1268–1269.
  28. 28. Lili Xu, Chunhui Li, and Bing Zhang, Efficacy and complications of ultrasound-guided radiofrequency ablation combined with TACE in the treatment of advanced primary liver cancer. Guizhou Medicine, 2016. 40(03): p. 265–267.
  29. 29. He JG and Chen Yru, Effects of ultrasound-guided radiofrequency ablation combined with targeted therapy on serum IgG, IgM and IgA concentrations in patients with advanced hepatocellular carcinoma. Chinese Modern Drug Application, 2021. 15(10): p. 100–103.
  30. 30. Zhao S., et al., Transcatheter arterial chemoembolization combined with radiofrequency ablation for the treatment of hepatocellular carcinoma: A systematic review and meta analysis. Journal of Interventional Radiology (China), 2013. 22(11): p. 908–913.
  31. 31. Noel J.E. and Sinclair C.F., Radiofrequency Ablation for Benign Thyroid Nodules. J Clin Endocrinol Metab, 2023. 109(1): p. e12–e17. pmid:37401778
  32. 32. Di Gialleonardo L., et al., Endoscopic Ultrasound-Guided Locoregional Treatments for Solid Pancreatic Neoplasms. Cancers (Basel), 2023. 15(19). pmid:37835413
  33. 33. Yang D., et al., Ultrasound-Guided Human Islet Transplantation: Safety, Feasibility, and Efficacy Analysis. Acad Radiol, 2023. 30 Suppl 1: p. S268–s277. pmid:37280129
  34. 34. Jasinski M., et al., Ultrasound-Guided Percutaneous Thermal Ablation of Renal Cancers-In Search for the Ideal Tumour. Cancers (Basel), 2023. 15(2). pmid:36672467
  35. 35. Khoury T., Sbeit W., and Napoléon B., Endoscopic ultrasound guided radiofrequency ablation for pancreatic tumors: A critical review focusing on safety, efficacy and controversies. World J Gastroenterol, 2023. 29(1): p. 157–170. pmid:36683710
  36. 36. Prete A.M. and Gonda T.A., Endoscopic Ultrasound-Guided Local Ablative Therapies for the Treatment of Pancreatic Neuroendocrine Tumors and Cystic Lesions: A Review of the Current Literature. J Clin Med, 2023. 12(9). pmid:37176764
  37. 37. Dhar J., et al., Endoscopic ultrasound-guided radiofrequency ablation of pancreatic insulinoma: a state of the art review. Expert Rev Gastroenterol Hepatol, 2024: p. 1–17. pmid:38383965
  38. 38. Conticchio M., et al., Hepatocellular Carcinoma with Bile Duct Tumor Thrombus: A Case Report and Literature Review of 890 Patients Affected by Uncommon Primary Liver Tumor Presentation. J Clin Med, 2023. 12(2). pmid:36675352
  39. 39. Shi F., et al., Radiofrequency Ablation Following Downstaging of Hepatocellular Carcinoma by Using Transarterial Chemoembolization: Long-term Outcomes. Radiology, 2019. 293(3): p. 707–715. pmid:31638492
  40. 40. Borrelli de Andreis F., et al., Safety and efficacy of endoscopic ultrasound-guided radiofrequency ablation for pancreatic insulinoma: A single-center experience. Pancreatology, 2023. 23(5): p. 543–549. pmid:37236853
  41. 41. Lesmana C.R.A., Impact of endoscopic ultrasound-guided radiofrequency ablation in managing pancreatic malignancy. World J Gastrointest Surg, 2023. 15(2): p. 163–168. pmid:36896311