Skip to main content
Log in

Efficacy and safety of radiofrequency ablation versus minimally invasive liver surgery for small hepatocellular carcinoma: a systematic review and meta-analysis

  • Review Article
  • Published:
Surgical Endoscopy Aims and scope Submit manuscript

Abstract

Background

The aim of this study was to compare radiofrequency ablation (RFA) with minimally invasive liver surgery (MIS) in the treatment of small hepatocellular carcinoma (SHCC) and to assess short-term and long-term clinical outcomes.

Methods

PubMed, Embase, Cochrane Library, Web of science, and CBM were systematically searched for articles from inception to July 2018, comparing RFA and MIS in SHCC treatment. We evaluated overall survival (OS), disease-free survival (DFS), local recurrence, and complication rates, as well as hospitalization duration and operation times.

Results

Six retrospective studies were analyzed, including a total of 597 patients, 313 treated with RFA and 284 treated with MIS. OS rates were significantly higher in patients treated with MIS at 3 years, when compared to RFA (OR 0.55; 95% CI 0.36 to 0.84). The 3-year DFS MIS rates were also superior to RFA (OR 0.63; 95% CI 0.41 to 0.98). In contrast, when compared to MIS, RFA demonstrated a significantly higher rate of local intrahepatic recurrences, (OR 2.24; 95% CI 1.47 to 3.42), and a lower incidence of postoperative complications (OR 0.34; 95% CI 0.22 to 0.53), as well as shorter operation times (OR − 145.31, 95% CI − 200.24 to − 90.38) and hospitalization duration (OR − 4.02,95% CI − 4.94 to − 3.10).

Conclusions

We found that MIS led to higher OS, DFS, and lower local recurrences in SHCC patients. Meanwhile, RFA treatments led to significantly lower complication rates, shorter operation times, and hospitalization duration. Considering long-term outcomes, MIS was found to be superior to RFA. However, RFA may be an alternative treatment for patients presenting a single SHCC nodule (≤ 3 cm), given its minimally invasive nature and its comparable long-term efficacy with MIS. Nevertheless, our findings should be explained with caution due to the low level of evidence obtained.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  1. Organization WH (2018) International Agency for Research on Cancer. https://gco.iarc.fr/today/data/factsheets/cancers/11-Liver-fact-sheet.pdf

  2. Deng GL, Zeng S, Shen H (2015) Chemotherapy and target therapy for hepatocellular carcinoma: new advances and challenges. World J Hepatol 7:787–798

    Article  PubMed  PubMed Central  Google Scholar 

  3. Zhou Y, Zhao Y, Li B, Xu D, Yin Z, Xie F, Yang J (2010) Meta-analysis of radiofrequency ablation versus hepatic resection for small hepatocellular carcinoma. BMC Gastroenterol 10:78

    Article  PubMed  PubMed Central  Google Scholar 

  4. Xu G, Ma J, Jia W, Ge Y, Yu J (2011) The clinical value of contrast-enhanced ultrasonography in diagnosing primary hepatocellular carcinoma. J Hepatobiliary Surg 4:261–264

    Google Scholar 

  5. Mazzaferro V, Regalia E, Doci R, Andreola S, Pulvirenti A, Bozzetti F, Montalto F, Ammatuna M, Morabito A, Gennari L (1996) Liver transplantation for the treatment of small hepatocellular carcinomas in patients with cirrhosis. N Engl J Med 334:693–699

    Article  CAS  PubMed  Google Scholar 

  6. Bruix J, Sherman M (2011) Management of hepatocellular carcinoma: an update. Hepatology (Baltimore, MD) 53:1020–1022

    Article  Google Scholar 

  7. Song J, Chen J, Li J, Fan Y, Wang X, Zheng S (2017) Clinical analysis of laparoscopic hepatectomy and radiofrequency ablation in the treatment of early hepatocellular carcinoma. J Hepatobiliary Surg 25:349–353

    Google Scholar 

  8. Xu Z, Xu G, Ma J, Jia W, Ge Y, Pan T (2017) Ultrasound guided percutaneous radiofrequency ablation versus laparoscopic hepatectomy for small primary liver cancer. Chin J Gen Surg 26:18–24

    Google Scholar 

  9. Qiu J, Chen S, Chengyou D (2016) A systematic review of robotic-assisted liver resection and meta-analysis of robotic versus laparoscopic hepatectomy for hepatic neoplasms. Surg Endosc 30:862–875

    Article  PubMed  Google Scholar 

  10. Buchs NC, Oldani G, Orci LA, Majno PE, Mentha G, Morel P, Toso C (2014) Current status of robotic liver resection: a systematic review. Expert Rev Anticancer Ther 14:237–246

    Article  CAS  PubMed  Google Scholar 

  11. Yin Z, Fan X, Ye H, Yin D, Wang J (2013) Short- and long-term outcomes after laparoscopic and open hepatectomy for hepatocellular carcinoma: a global systematic review and meta-analysis. Ann Surg Oncol 20:1203–1215

    Article  PubMed  Google Scholar 

  12. Hirokawa F, Hayashi M, Miyamoto Y, Asakuma M, Shimizu T, Komeda K, Inoue Y, Uchiyama K (2015) Short- and long-term outcomes of laparoscopic versus open hepatectomy for small malignant liver tumors: a single-center experience. Surg Endosc 29:458–465

    Article  PubMed  Google Scholar 

  13. Minami Y, Kudo M (2010) Radiofrequency ablation of hepatocellular carcinoma: current status. World J Radiol 2:417–424

    Article  PubMed  PubMed Central  Google Scholar 

  14. Casaccia M, Santori G, Bottino G, Diviacco P, Andorno E (2017) Laparoscopic resection vs laparoscopic radiofrequency ablation for the treatment of small hepatocellular carcinomas: a single-center analysis. World J Gastroenterol 23:653–660

    Article  PubMed  PubMed Central  Google Scholar 

  15. Kim GA, Shim JH, Kim MJ, Kim SY, Won HJ, Shin YM, Kim PN, Kim KH, Lee SG, Lee HC (2016) Radiofrequency ablation as an alternative to hepatic resection for single small hepatocellular carcinomas. Br J Surg 103:126–135

    Article  CAS  PubMed  Google Scholar 

  16. Lei JY, Wang WT, Yan LN, Wen TF, Li B (2014) Radiofrequency ablation versus surgical resection for small unifocal hepatocellular carcinomas. Medicine 93:e271

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Yao FY, Ferrell L, Bass NM, Watson JJ, Bacchetti P, Venook A, Ascher NL, Roberts JP (2001) Liver transplantation for hepatocellular carcinoma: expansion of the tumor size limits does not adversely impact survival. Hepatology (Baltimore, MD) 33:1394–1403

    Article  CAS  Google Scholar 

  18. Stang A (2010) Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol 25:603–605

    Article  PubMed  Google Scholar 

  19. Xiu-xia L, Ya Z, Yao-long C, Ke-hu Y, Zong-jiu Z (2015) The reporting characteristics and methodological quality of Cochrane reviews about health policy research. Health Policy (Amsterdam, Netherlands) 119:503–510

    Article  Google Scholar 

  20. Melsen WG, Bootsma MC, Rovers MM, Bonten MJ (2014) The effects of clinical and statistical heterogeneity on the predictive values of results from meta-analyses. Clin Microbiol Infect 20:123–129

    Article  CAS  PubMed  Google Scholar 

  21. Yao L, Sun R, Chen YL, Wang Q, Wei D, Wang X, Yang K (2016) The quality of evidence in Chinese meta-analyses needs to be improved. J Clin Epidemiol 74:73–79

    Article  PubMed  Google Scholar 

  22. Casaccia M, Santori G, Bottino G, Diviacco P, Negri AD, Moraglia E, Adorno E (2015) The procedure outcome of laparoscopic resection for ‘small’ hepatocellular carcinoma is comparable to vlaparoscopic radiofrequency ablation. J Minim Access Surg 11:231–235

    Article  PubMed  PubMed Central  Google Scholar 

  23. Song J, Wang Y, Ma K, Zheng S, Bie P, Xia F, Li X, Li J, Wang X, Chen J (2015) Laparoscopic hepatectomy versus radiofrequency ablation for minimally invasive treatment of single, small hepatocellular carcinomas. Surg Endosc 30:4249–4257

    Article  PubMed  Google Scholar 

  24. Vitali GC, Laurent A, Terraz S, Majno P, Buchs NC, Rubbia-Brandt L, Luciani A, Calderaro J, Morel P, Azoulay D, Toso C (2015) Minimally invasive surgery versus percutaneous radio frequency ablation for the treatment of single small (</=3 cm) hepatocellular carcinoma: a case-control study. Surg Endosc 30:2301–2307

    Article  PubMed  Google Scholar 

  25. Tian J, Zhang J, Ge L, Yang K, Song F (2017) The methodological and reporting quality of systematic reviews from China and the USA are similar. J Clin Epidemiol 85:50–58

    Article  PubMed  Google Scholar 

  26. Egger M, Davey Smith G, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ (Clinical research ed) 315:629–634

    Article  CAS  Google Scholar 

  27. Wang Y, Luo Q, Li Y, Deng S, Wei S, Li X (2014) Radiofrequency ablation versus hepatic resection for small hepatocellular carcinomas: a meta-analysis of randomized and nonrandomized controlled trials. PLoS ONE 9:e84484

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Xu XL, Liu XD, Liang M, Luo BM (2018) Radiofrequency ablation versus hepatic resection for small hepatocellular carcinoma: systematic review of randomized controlled trials with meta-analysis and trial sequential analysis. Radiology 287:461–472

    Article  PubMed  Google Scholar 

  29. Rhim H, Lim HK (2010) Radiofrequency ablation of hepatocellular carcinoma: pros and cons. Gut Liver 4(Suppl 1):S113–118

    Article  PubMed  PubMed Central  Google Scholar 

  30. Xu Q, Kobayashi S, Ye X, Meng X (2014) Comparison of hepatic resection and radiofrequency ablation for small hepatocellular carcinoma: a meta-analysis of 16,103 patients. Sci Rep 4:7252

    Article  PubMed  PubMed Central  Google Scholar 

  31. Lau WY, Lai EC (2009) The current role of radiofrequency ablation in the management of hepatocellular carcinoma: a systematic review. Ann Surg 249:20–25

    Article  PubMed  Google Scholar 

  32. Podnos YD, Henry G, Ortiz JA, Ji P, Cooke J, Cao S, Imagawa DK (2001) Laparoscopic ultrasound with radiofrequency ablation in cirrhotic patients with hepatocellular carcinoma: technique and technical considerations. Am Surg 67:1181–1184

    CAS  PubMed  Google Scholar 

  33. Benson AB 3rd, D’Angelica MI, Abbott DE, Abrams TA, Alberts SR, Saenz DA, Are C, Brown DB, Chang DT, Covey AM, Hawkins W, Iyer R, Jacob R, Karachristos A, Kelley RK, Kim R, Palta M, Park JO, Sahai V, Schefter T, Schmidt C, Sicklick JK, Singh G, Sohal D, Stein S, Tian GG, Vauthey JN, Venook AP, Zhu AX, Hoffmann KG, Darlow S (2017) NCCN guidelines insights: hepatobiliary cancers, version 1.2017. J Natl Compr Cancer Netw 15:563–573

    Article  Google Scholar 

  34. Adachi E, Maeda T, Kajiyama K, Kinukawa N, Matsumata T, Sugimachi K, Tsuneyoshi M (1996) Factors correlated with portal venous invasion by hepatocellular carcinoma: univariate and multivariate analyses of 232 resected cases without preoperative treatments. Cancer 77:2022–2031

    Article  CAS  PubMed  Google Scholar 

  35. Buell JF, Cherqui D, Geller DA, O’Rourke N, Iannitti D, Dagher I, Koffron AJ, Thomas M, Gayet B, Han HS, Wakabayashi G, Belli G, Kaneko H, Ker CG, Scatton O, Laurent A, Abdalla EK, Chaudhury P, Dutson E, Gamblin C, D’Angelica M, Nagorney D, Testa G, Labow D, Manas D, Poon RT, Nelson H, Martin R, Clary B, Pinson WC, Martinie J, Vauthey JN, Goldstein R, Roayaie S, Barlet D, Espat J, Abecassis M, Rees M, Fong Y, McMasters KM, Broelsch C, Busuttil R, Belghiti J, Strasberg S, Chari RS (2009) The international position on laparoscopic liver surgery: the Louisville Statement, 2008. Ann Surg 250:825–830

    Article  PubMed  Google Scholar 

  36. Ma Y, Zhang P, Wang F, Yang J, Liu Z, Qin H (2011) Association between vitamin D and risk of colorectal cancer: a systematic review of prospective studies. J Clin Oncol 29:3775–3782

    Article  CAS  PubMed  Google Scholar 

  37. 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 

  38. Li L, Zhang J, Liu X, Li X, Jiao B, Kang T (2012) Clinical outcomes of radiofrequency ablation and surgical resection for small hepatocellular carcinoma: a meta-analysis. J Gastroenterol Hepatol 27:51–58

    Article  PubMed  Google Scholar 

  39. Hu L, Yao L, Li X, Jin P, Yang K, Guo T (2018) Effectiveness and safety of robotic-assisted versus laparoscopic hepatectomy for liver neoplasms: a meta-analysis of retrospective studies. Asian J Surg 41:401–416

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

The authors thank the institution (Evidence Based Medicine Center of Lanzhou University) for their help and support to the methodology and meta process.

Disclosure

Mou-Bo Si, Pei-Jing Yan, Xiang-Yong Hao, Zhen-Ying Du, Hong-Wei Tian, Jia Yang, Cai-Wen Han, Ke-Hu Yang, and Tian-Kang Guo have declared that they have no conflicts of interest or financial ties to disclose.

Funding

Supported by Natural Science Foundation for Young Scientists of Gansu Province and the Science & Technology Planning Project of Gansu Province (Grant No.: 18JR3RA058). Supported by Key Laboratory of Evidence Based Medicine and Knowledge Translation Foundation of Gansu Province (Grant No. GSXZYZH2018006). Supported by Foundation of Lanzhou Science and Technology Bureau (Grant No. 2017-ZD-38). Supported by Research Projects of Gansu Provincial Hospital (Grant No.18GSSY3-1). Supported by Research Projects of Gansu Provincial Hospital (Grant No. 18GSSY3-8).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Ke-Hu Yang or Tian-Kang Guo.

Additional information

Publisher's Note

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

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 36 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Si, MB., Yan, PJ., Hao, XY. et al. 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 (2019). https://doi.org/10.1007/s00464-019-06784-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00464-019-06784-0

Keywords

Navigation