Skip to main content
SpringerLink
Log in

Outcomes of laparoscopic radiofrequency ablation versus percutaneous radiofrequency ablation for hepatocellular carcinoma

  • Published:
Surgical Endoscopy Aims and scope Submit manuscript

Abstract

Background

Few studies have compared the therapeutic outcomes in patients with HCC who underwent laparoscopic radiofrequency ablation (LRFA) versus percutaneous radiofrequency ablation (PRFA) for hepatocellular carcinoma (HCC). Therefore, this study compared the recurrence and survival outcomes of the two RFA methods in patients with HCC.

Methods

Recurrence and overall survival outcomes were evaluated in 307 patients who underwent LRFA (n = 151) or PRFA (n = 156) as a treatment method for de novo HCC. Inverse probability of treatment weighting (IPTW) analysis was performed to reduce the impact of treatment selection bias.

Results

There were no significant differences in major baseline characteristics between the LRFA and PRFA groups. However, the proportion of cirrhotic patients was higher in the LRFA group, whereas the LRFA group had more tumors and a more advanced tumor-node-metastasis stage. Moreover, the mean tumor size was significantly larger in the LRFA group than in the PRFA group. In a multivariate analysis, serum albumin level, more than three tumors, and the RFA method were identified as significant predictors of recurrence-free survival. Moreover, for the overall survival of HCC patients, serum albumin levels, days of hospital stay during RFA, and the RFA method were independent predictors. In the IPTW-adjusted analysis, the LRFA group showed significantly higher recurrence-free survival and overall survival.

Conclusions

Our study revealed that compared with PRFA, LRFA was associated with longer recurrence-free survival and favorable overall survival in patients with HCC. Therefore, LRFA should be considered the primary therapy in patients with HCC eligible for RFA.

Graphical abstract

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Data availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

Abbreviations

HCC:

Hepatocellular carcinoma

RFA:

Radiofrequency ablation

PRFA:

Percutaneous radiofrequency ablation

LRFA:

Laparoscopic radiofrequency ablation

CT:

Computed tomography

MRI:

Magnetic resonance imaging

AFP:

Alpha-fetoprotein

PIVKA-II:

Prothrombin induced by vitamin K absence II

TACE:

Transarterial chemoembolization

IPTW:

Inverse probability treatment weighting

IOUS:

Intraoperative ultrasound

References

  1. McGlynn KA, Petrick JL, El-Serag HB (2021) Epidemiology of hepatocellular carcinoma. Hepatology 73(Suppl 1):4–13

    Article  CAS  PubMed  Google Scholar 

  2. Lee HW, Lee JM, Yoon JH, Kim YJ, Park JW, Park SJ, Kim SH, Yi NJ, Suh KS (2018) A prospective randomized study comparing radiofrequency ablation and hepatic resection for hepatocellular carcinoma. Ann Surg Treat Res 94:74–82

    Article  PubMed  PubMed Central  Google Scholar 

  3. Jia JB, Zhang D, Ludwig JM, Kim HS (2017) Radiofrequency ablation versus resection for hepatocellular carcinoma in patients with Child-Pugh A liver cirrhosis: a meta-analysis. Clin Radiol 72:1066–1075

    Article  CAS  PubMed  Google Scholar 

  4. Qi X, Tang Y, An D, Bai M, Shi X, Wang J, Han G, Fan D (2014) Radiofrequency ablation versus hepatic resection for small hepatocellular carcinoma: a meta-analysis of randomized controlled trials. J Clin Gastroenterol 48:450–457

    Article  PubMed  Google Scholar 

  5. Eun HS, Lee BS, Kwon IS, Yun GY, Lee ES, Joo JS, Sung JK, Moon HS, Kang SH, Kim JS, Shin HJ, Kim TK, Chun K, Kim SH (2017) Advantages of laparoscopic radiofrequency ablation over percutaneous radiofrequency ablation in hepatocellular carcinoma. Dig Dis Sci 62:2586–2600

    Article  PubMed  Google Scholar 

  6. Imamura H, Matsuyama Y, Tanaka E, Ohkubo T, Hasegawa K, Miyagawa S, Sugawara Y, Minagawa M, Takayama T, Kawasaki S, Makuuchi M (2003) Risk factors contributing to early and late phase intrahepatic recurrence of hepatocellular carcinoma after hepatectomy. J Hepatol 38:200–207

    Article  PubMed  Google Scholar 

  7. Nault JC, Sutter O, Nahon P, Ganne-Carrie N, Seror O (2018) Percutaneous treatment of hepatocellular carcinoma: State of the art and innovations. J Hepatol 68:783–797

    Article  PubMed  Google Scholar 

  8. Yang Y, Chen Y, Ye F, Cao X, Xin Y, Wang Y, Lei Y, Li X, Feng D, Zhou X, Fan Q (2021) Late recurrence of hepatocellular carcinoma after radiofrequency ablation: a multicenter study of risk factors, patterns, and survival. Eur Radiol 31:3053–3064

    Article  PubMed  Google Scholar 

  9. Zheng J, Chou JF, Gonen M, Vachharajani N, Chapman WC, Majella Doyle MB, Turcotte S, Vandenbroucke-Menu F, Lapointe R, Buettner S, Groot Koerkamp B, Ijzermans JNM, Chan CY, Goh BKP, Teo JY, Kam JH, Jeyaraj PR, Cheow PC, Chung AYF, Chow PKH, Ooi L, Balachandran VP, Kingham TP, Allen PJ, D’Angelica MI, DeMatteo RP, Jarnagin WR, Lee SY (2017) Prediction of hepatocellular carcinoma recurrence beyond milan criteria after resection: validation of a clinical risk score in an international cohort. Ann Surg 266:693–701

    Article  PubMed  Google Scholar 

  10. Xu XF, Xing H, Han J, Li ZL, Lau WY, Zhou YH, Gu WM, Wang H, Chen TH, Zeng YY, Li C, Wu MC, Shen F, Yang T (2019) Risk factors, patterns, and outcomes of late recurrence after liver resection for hepatocellular carcinoma: a multicenter study from China. JAMA Surg 154:209–217

    Article  PubMed  Google Scholar 

  11. Kim PN, Choi D, Rhim H, Rha SE, Hong HP, Lee J, Choi JI, Kim JW, Seo JW, Lee EJ, Lim HK (2012) Planning ultrasound for percutaneous radiofrequency ablation to treat small (</= 3 cm) hepatocellular carcinomas detected on computed tomography or magnetic resonance imaging: a multicenter prospective study to assess factors affecting ultrasound visibility. J Vasc Interv Radiol 23:627–634

    Article  PubMed  Google Scholar 

  12. Si MB, Yan PJ, Hao XY, Du ZY, Tian HW, Yang J, Han CW, Yang KH, Guo TK (2019) Efficacy and safety of radiofrequency ablation versus minimally invasive liver surgery for small hepatocellular carcinoma: a systematic review and meta-analysis. Surg Endosc 33:2419–2429

    Article  PubMed  Google Scholar 

  13. Santambrogio R, Barabino M, D’Alessandro V, Galfrascoli E, Zappa MA, Piccolo G, Zuin M, Opocher E (2020) Laparoscopic thermoablation for hepatocellular carcinoma in patients with liver cirrhosis: an effective procedure for tricky tumors. Med Oncol 37:32

    Article  PubMed  Google Scholar 

  14. Mulier S, Ni Y, Jamart J, Ruers T, Marchal G, Michel L (2005) Local recurrence after hepatic radiofrequency coagulation: multivariate meta-analysis and review of contributing factors. Ann Surg 242:158–171

    Article  PubMed  PubMed Central  Google Scholar 

  15. Liao M, Zhong X, Zhang J, Liu Y, Zhu Z, Wu H, Zeng Y, Huang J (2017) Radiofrequency ablation using a 10-mm target margin for small hepatocellular carcinoma in patients with liver cirrhosis: a prospective randomized trial. J Surg Oncol 115:971–979

    Article  PubMed  Google Scholar 

  16. Nakazawa T, Kokubu S, Shibuya A, Ono K, Watanabe M, Hidaka H, Tsuchihashi T, Saigenji K (2007) Radiofrequency ablation of hepatocellular carcinoma: correlation between local tumor progression after ablation and ablative margin. AJR Am J Roentgenol 188:480–488

    Article  PubMed  Google Scholar 

  17. Berber E, Siperstein A (2008) Local recurrence after laparoscopic radiofrequency ablation of liver tumors: an analysis of 1032 tumors. Ann Surg Oncol 15:2757–2764

    Article  PubMed  Google Scholar 

  18. Kim YS, Rhim H, Cho OK, Koh BH, Kim Y (2006) Intrahepatic recurrence after percutaneous radiofrequency ablation of hepatocellular carcinoma: analysis of the pattern and risk factors. Eur J Radiol 59:432–441

    Article  CAS  PubMed  Google Scholar 

  19. Ke S, Ding XM, Qian XJ, Zhou YM, Cao BX, Gao K, Sun WB (2013) Radiofrequency ablation of hepatocellular carcinoma sized > 3 and </= 5 cm: is ablative margin of more than 1 cm justified? World J Gastroenterol 19:7389–7398

    Article  PubMed  PubMed Central  Google Scholar 

  20. Hirooka M, Kisaka Y, Uehara T, Ishida K, Kumagi T, Watanabe Y, Abe M, Matsuura B, Hiasa Y, Onji M (2009) Efficacy of laparoscopic radiofrequency ablation for hepatocellular carcinoma compared to percutaneous radiofrequency ablation with artificial ascites. Dig Endosc 21:82–86

    Article  PubMed  Google Scholar 

  21. Vahldiek JL, Erxleben C, Bressem KK, Gemeinhardt O, Poch F, Hiebl B, Lehmann KS, Hamm B, Niehues SM (2018) Multipolar RFA of the liver: Influence of intrahepatic vessels on ablation zones and appropriateness of CECT in detecting ablation dimensions—results of an in-vivo porcine liver model. Clin Hemorheol Microcirc 70:467–476

    Article  PubMed  Google Scholar 

  22. Smith MK, Mutter D, Forbes LE, Mulier S, Marescaux J (2004) The physiologic effect of the pneumoperitoneum on radiofrequency ablation. Surg Endosc 18:35–38

    Article  CAS  PubMed  Google Scholar 

  23. Okusaka T, Okada S, Ueno H, Ikeda M, Shimada K, Yamamoto J, Kosuge T, Yamasaki S, Fukushima N, Sakamoto M (2002) Satellite lesions in patients with small hepatocellular carcinoma with reference to clinicopathologic features. Cancer 95:1931–1937

    Article  PubMed  Google Scholar 

  24. Han J, Li ZL, Xing H, Wu H, Zhu P, Lau WY, Zhou YH, Gu WM, Wang H, Chen TH, Zeng YY, Wu MC, Shen F, Yang T (2019) The impact of resection margin and microvascular invasion on long-term prognosis after curative resection of hepatocellular carcinoma: a multi-institutional study. HPB (Oxford) 21:962–971

    Article  PubMed  Google Scholar 

  25. Giuliante F, Ardito F, Pinna AD, Sarno G, Giulini SM, Ercolani G, Portolani N, Torzilli G, Donadon M, Aldrighetti L, Pulitano C, Guglielmi A, Ruzzenente A, Capussotti L, Ferrero A, Calise F, Scuderi V, Federico B, Nuzzo G (2012) Liver resection for hepatocellular carcinoma </=3 cm: results of an Italian multicenter study on 588 patients. J Am Coll Surg 215:244–254

    Article  PubMed  Google Scholar 

  26. Nguyen-Khac V, Brustia R, Rhaiem R, Regnault H, Sessa A, Mule S, Duvoux C, Laurent A, Leroy V, Calderaro J, Luciani A, Roudot-Thoraval F, Amaddeo G, Sommacale D (2022) Liver resection for single large hepatocellular carcinoma: a prognostic factors study. Ann Hepatol 27:100739

    Article  CAS  PubMed  Google Scholar 

  27. Zhuang BW, Li W, Wang W, Li B, Lu MD, Kuang M, Xie XH, Xie XY (2021) Treatment effect of radiofrequency ablation versus liver transplantation and surgical resection for hepatocellular carcinoma within Milan criteria: a population-based study. Eur Radiol 31:5379–5389

    Article  PubMed  Google Scholar 

  28. Seror O, N’Kontchou G, Van Nhieu JT, Rabahi Y, Nahon P, Laurent A, Trinchet JC, Cherqui D, Vicaut E, Beaugrand M, Sellier N (2014) Histopathologic comparison of monopolar versus no-touch multipolar radiofrequency ablation to treat hepatocellular carcinoma within Milan criteria. J Vasc Interv Radiol 25:599–607

    Article  PubMed  Google Scholar 

  29. de la Serna S, Vilana R, Sanchez-Cabus S, Calatayud D, Ferrer J, Molina V, Fondevila C, Bruix J, Fuster J, Garcia-Valdecasas JC (2015) Results of laparoscopic radiofrequency ablation for HCC. Could the location of the tumour influence a complete response to treatment? A single European centre experience. HPB (Oxford) 17:387–393

    Article  PubMed  Google Scholar 

  30. Chinnaratha MA, Chuang MY, Fraser RJ, Woodman RJ, Wigg AJ (2016) Percutaneous thermal ablation for primary hepatocellular carcinoma: a systematic review and meta-analysis. J Gastroenterol Hepatol 31:294–301

    Article  PubMed  Google Scholar 

  31. Santambrogio R, Barabino M, De Nicola E, Galfrascoli E, Giovenzana M, Zappa MA (2020) Laparoscopic ablation therapies for hepatocellular carcinoma: could specific indications for the laparoscopic approach influence the effectiveness? Updates Surg 72:435–443

    Article  PubMed  Google Scholar 

  32. Kokudo N, Bandai Y, Imanishi H, Minagawa M, Uedera Y, Harihara Y, Makuuchi M (1996) Management of new hepatic nodules detected by intraoperative ultrasonography during hepatic resection for hepatocellular carcinoma. Surgery 119:634–640

    Article  CAS  PubMed  Google Scholar 

  33. Torzilli G, Olivari N, Moroni E, Del Fabbro D, Gambetti A, Leoni P, Montorsi M, Makuuchi M (2004) Contrast-enhanced intraoperative ultrasonography in surgery for hepatocellular carcinoma in cirrhosis. Liver Transpl 10:S34-38

    Article  PubMed  Google Scholar 

  34. Lee MW, Kang D, Lim HK, Cho J, Sinn DH, Kang TW, Song KD, Rhim H, Cha DI, Lu DSK (2020) Updated 10-year outcomes of percutaneous radiofrequency ablation as first-line therapy for single hepatocellular carcinoma < 3 cm: emphasis on association of local tumor progression and overall survival. Eur Radiol 30:2391–2400

    Article  PubMed  Google Scholar 

  35. Lo C-M, Lai E, Liu C-L, Fan S-T, Wong J (1998) Laparoscopy and laparoscopic ultrasonography avoid exploratory laparotomy in patients with hepatocellular carcinoma. Ann Surg 227:527

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Bartos A, Iancu I, Ciobanu L, Badea R, Sparchez Z, Bartos DM (2020) Intraoperative ultrasound in liver and pancreatic surgery. Med Ultrason. https://doi.org/10.11152/mu-2853

    Article  PubMed  Google Scholar 

  37. Takigawa Y, Sugawara Y, Yamamoto J, Shimada K, Yamasaki S, Kosuge T, Makuuchi M (2001) New lesions detected by intraoperative ultrasound during liver resection for hepatocellular carcinoma. Ultrasound Med Biol 27:151–156

    Article  CAS  PubMed  Google Scholar 

  38. Pace C, Nardone V, Roma S, Chegai F, Toti L, Manzia TM, Tisone G, Orlacchio A (2019) Evaluation of contrast-enhanced intraoperative ultrasound in the detection and management of liver lesions in patients with hepatocellular carcinoma. J Oncol 2019:6089340

    Article  PubMed  PubMed Central  Google Scholar 

  39. Battaglia V, Cervelli R (2017) Liver investigations: updating on US technique and contrast-enhanced ultrasound (CEUS). Eur J Radiol 96:65–73

    Article  PubMed  Google Scholar 

Download references

Funding

There is no funding to be declared.

Author information

Author notes

  1. Hong Jae Jeon and Hyuk Soo Eun have contributed equally to this work.

Authors and Affiliations

  1. Department of Gastroenterology, Chungnam National University Sejong Hospital, 20, Bodeum 7-ro, Sejong-si, 30099, Republic of Korea

    Hong Jae Jeon & Woo Sun Rou

  2. Department of Internal Medicine, School of Medicine, Chungnam National University, 266, Munhwa-ro, Jung-gu, Daejeon, 35015, Republic of Korea

    Hong Jae Jeon, Hyuk Soo Eun, Byung Seok Lee, Eaum Seok Lee, Woo Sun Rou, Jae Kyu Sung, Hee Seok Moon, Sun Hyung Kang, Hyun Seok Lee & Seok Hyun Kim

  3. Department of Gastroenterology, Chungnam National University Hospital, 282, Munhwa-ro, Jung-gu, Daejeon, 35015, Republic of Korea

    Hyuk Soo Eun, Byung Seok Lee, Eaum Seok Lee, Jae Kyu Sung, Hee Seok Moon, Sun Hyung Kang, Hyun Seok Lee & Seok Hyun Kim

  4. Clinical Trials Center, Chungnam National University Hospital, 282, Munhwa-ro, Jung-gu, Daejeon, 35015, Republic of Korea

    In Sun Kwon

  5. Department of Surgery, Chungnam National University Hospital, 282, Munhwa-ro, Jung-gu, Daejeon, 35015, Republic of Korea

    Seok-Hwan Kim & Kwangsik Chun

  6. Department of Surgery, School of Medicine, Chungnam National University, 266, Munhwa-ro, Jung-gu, Daejeon, 35015, Republic of Korea

    Seok-Hwan Kim & Kwangsik Chun

Authors
  1. Hong Jae Jeon
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hyuk Soo Eun
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. In Sun Kwon
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Byung Seok Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Eaum Seok Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Woo Sun Rou
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jae Kyu Sung
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Hee Seok Moon
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Sun Hyung Kang
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Hyun Seok Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Seok-Hwan Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Kwangsik Chun
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Seok Hyun Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

SHK and HSE designed the study. BSL, ESL, WSR, JKS, HSM, SHK, HSL, SHK, and KC performed the study selection, literature search, and data extraction. HJJ and HSE performed statistical analyses. ISK provided statistical advice on the study design and data analysis. HJJ, HSE, KC, and SHK wrote the first draft of the manuscript. All authors contributed to the interpretation of the data and critically reviewed the manuscript.

Corresponding authors

Correspondence to Kwangsik Chun or Seok Hyun Kim.

Ethics declarations

Disclosures

Hong Jae Jeon, Hyuk Soo Eun, In Sun Kwon, Byung Seok Lee, Eaum Seok Lee, Woo Sun Rou, Jae Kyu Sung, Hee Seok Moon, Sun Hyung Kang, Hyun Seok Lee, Seok-Hwan Kim, Kwangsik Chun, and Seok Hyun Kim have no conflicts of interest or financial ties to disclosure.

Ethical approval

This study was approved by the Institutional Review Board of Chungnam National University Hospital (IRB Number: CNUH 2016-06-009-011). All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

Patient consent

The requirement for obtaining written consent was waived because of the retrospective design of the study.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 42 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jeon, H., Eun, H., Kwon, I. et al. Outcomes of laparoscopic radiofrequency ablation versus percutaneous radiofrequency ablation for hepatocellular carcinoma. Surg Endosc 37, 5176–5189 (2023). https://doi.org/10.1007/s00464-023-09956-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00464-023-09956-1

Keywords

Search

Navigation