Skip to main content
SpringerLink
Log in

A Comparative Study of Ablation Boundary Sharpness After Percutaneous Radiofrequency, Cryo-, Microwave, and Irreversible Electroporation Ablation in Normal Swine Liver and Kidneys

  • Laboratory Investigation
  • Published:
CardioVascular and Interventional Radiology Aims and scope Submit manuscript

Abstract

Purpose

To compare ablation boundary sharpness after percutaneous radiofrequency ablation (RFA), cryoablation (CA), microwave ablation (MWA) and irreversible electroporation (IRE) ablation in normal swine liver and kidney.

Materials and Methods

Percutaneous CT-guided RFA (n = 5), CA (n = 5), MWA (n = 5) and IRE (n = 5) were performed in the liver and kidney of four Yorkshire pigs. Parameters were chosen to produce ablations 2–3 cm in diameter with a single ablation probe. Contrast-enhanced CT imaging was performed 24 h after ablation, and animals were killed. Treated organs were removed and processed for histologic analysis with hematoxylin and eosin, and terminal deoxynucleotidyl transferase dUTP nick end labeling (TUNEL). Three readers independently analyzed CT, H&E and TUNEL stained images of the ablation boundary to delineate regions of (1) viable cells, (2) complete necrosis or (3) mixture of viable and necrotic cells which was defined as the transition zone (TZ). The width of TZ was compared across the techniques and organs.

Results

Ablations appeared as non-contrast-enhancing regions on CT with sharp transition to enhancing normal tissue. On TUNEL stained slides, the mean width (μm) of the TZ after MWA was 319 ± 157 in liver and 267 ± 95 in kidney, which was significantly lower than RFA (811 ± 477 and 938 ± 429); CA (452 ± 222 and 700 ± 563); and IRE (1319 ± 682 and 1570 ± 962) (all p < 0.01). No significant differences were observed between the organs.

Conclusion

Under similar conditions, the width of the TZ at the ablation boundary varies significantly between different ablation techniques.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Kim YS, Lee WJ, Rhim H, Lim HK, Choi D, Lee JY. The minimal ablative margin of radiofrequency ablation of hepatocellular carcinoma (>2 and <5 cm) needed to prevent local tumor progression: 3D quantitative assessment using CT image fusion. AJR Am J Roentgenol. 2010;195:758–65.

    Article  PubMed  Google Scholar 

  2. Beland M, Mueller PR, Gervais DA. Thermal ablation in interventional oncology. Semin Roentgenol. 2007;42:175–90.

    Article  PubMed  Google Scholar 

  3. Savic LJ, Chapiro J, Hamm B, Gebauer B, Collettini F. Irreversible electroporation in interventional oncology: where we stand and where we go. Rofo. 2016;188:735–45.

    Article  CAS  PubMed  Google Scholar 

  4. Trojan J, Zangos S, Schnitzbauer AA. Diagnostics and treatment of hepatocellular carcinoma in 2016: standards and developments. Visc Med. 2016;32:116–20.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Balageas P, Cornelis F, Le Bras Y, Hubrecht R, Bernhard JC, Ferriere JM, et al. Ten-year experience of percutaneous image-guided radiofrequency ablation of malignant renal tumours in high-risk patients. Eur Radiol. 2013;23:1925–32.

    Article  CAS  PubMed  Google Scholar 

  6. Ge BH, Guzzo TJ, Nadolski GJ, Soulen MC, Clark TWI, Malkowicz SB, et al. Percutaneous renal cryoablation: short-axis ice-ball margin as a predictor of outcome. J Vasc Interv Radiol. 2016;27:403–9.

    Article  PubMed  Google Scholar 

  7. Goldberg SN. Radiofrequency tumor ablation: principles and techniques. Eur J Ultrasound. 2001;13:129–47.

    Article  CAS  PubMed  Google Scholar 

  8. Sotirchos VS, Petrovic LM, Gönen M, Klimstra DS, Do RKG, Petre EN, et al. Colorectal cancer liver metastases: biopsy of the ablation zone and margins can be used to predict oncologic outcome. Radiology. 2016;280:949–59.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Wang X, Sofocleous CT, Erinjeri JP, Petre EN, Gonen M, Do KG, et al. Margin size is an independent predictor of local tumor progression after ablation of colon cancer liver metastases. Cardiovasc Interv Radiol. 2013;36:166–75.

    Article  CAS  Google Scholar 

  10. Vandenbroucke F, Vandemeulebroucke J, Ilsen B, Verdries D, Belsack D, Everaert H, et al. Predictive value of pattern classification 24 hours after radiofrequency ablation of liver metastases on CT and positron emission tomography/CT. J Vasc Interv Radiol. 2014;25:1240–9.

    Article  PubMed  Google Scholar 

  11. Kim YS, Rhim H, Lim HK, Choi D, Lee MW, Park MJ. Coagulation necrosis induced by radiofrequency ablation in the liver: histopathologic and radiologic review of usual to extremely rare changes. Radiographics. 2011;31:377–90.

    Article  PubMed  Google Scholar 

  12. Li D, Kang J, Madoff DC. Locally ablative therapies for primary and metastatic liver cancer. Expert Rev Anticancer Ther. 2014;14:931–45.

    Article  CAS  PubMed  Google Scholar 

  13. Solomon SB, Silverman SG. Imaging in interventional oncology. Radiology. 2010;257:624–40.

    Article  PubMed  Google Scholar 

  14. Brace CL. Radiofrequency and microwave ablation of the liver, lung, kidney, and bone: what are the differences? Curr Probl Diagn Radiol. 2009;38:135–43.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Rai R, Richardson C, Flecknell P, Robertson H, Burt A, Manas DM. Study of apoptosis and heat shock protein (HSP) expression in hepatocytes following radiofrequency ablation (RFA). J Surg Res. 2005;129:147–51.

    Article  CAS  PubMed  Google Scholar 

  16. Dong BW, Zhang J, Liang P, Yu XL, Su L, Yu DJ, et al. Sequential pathological and immunologic analysis of percutaneous microwave coagulation therapy of hepatocellular carcinoma. Int J Hyperth. 2003;19:119–33.

    Article  CAS  Google Scholar 

  17. Srimathveeravalli G, Silk M, Wimmer T, Monette S, Kimm S, Maybody M, et al. Feasibility of catheter-directed intraluminal irreversible electroporation of porcine ureter and acute outcomes in response to increasing energy delivery. J Vasc Interv Radiol. 2015;26:1059–66.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Spritzer CE, Afonso PD, Vinson EN, Turnbull JD, Morris KK, Foye A, et al. Bone marrow biopsy: RNA isolation with expression profiling in men with metastatic castration-resistant prostate cancer--factors affecting diagnostic success. Radiology. 2013;269:816–23.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Clasen S, Krober SM, Kosan B, Aebert H, Fend F, Bomches A, et al. Pathomorphologic evaluation of pulmonary radiofrequency ablation: proof of cell death is characterized by DNA fragmentation and apoptotic bodies. Cancer. 2008;113:3121–9.

    Article  PubMed  Google Scholar 

  20. Kasper H-U, Bangard C, Gossmann A, Dienes HP, Stippel DL. Pathomorphological changes after radiofrequency ablation in the liver. Pathol Int. 2010;60:149–55.

    Article  PubMed  Google Scholar 

  21. Choi H, Loyer EM, DuBrow RA, Kaur H, David CL, Huang S, et al. Radio-frequency ablation of liver tumors: assessment of therapeutic response and complications. Radiographics. 2001;21:S41–54.

    Article  PubMed  Google Scholar 

  22. Morgan MSC, Ozayar A, Lucas E, Friedlander JI, Shakir NA, Cadeddu JA. Comparative effects of irreversible electroporation, radiofrequency ablation, and partial nephrectomy on renal function preservation in a porcine solitary kidney model. Urology. 2016;94:281–7.

    Article  PubMed  Google Scholar 

  23. Wang L-G, Jiang W-J, Fan W-J, Zheng Y-B, Song X-P, Liu S, et al. Microwave ablation: the differences between biliary cirrhosis and normal porcine liver using a cooled-tip electrode. Anticancer Res. 2016;36:1221–6.

    CAS  PubMed  Google Scholar 

  24. Ierardi AM, Floridi C, Fontana F, Chini C, Giorlando F, Piacentino F, et al. Microwave ablation of liver metastases to overcome the limitations of radiofrequency ablation. Radiol Med. 2013;118:949–61.

    Article  PubMed  Google Scholar 

  25. Shady W, Petre EN, Gonen M, Erinjeri JP, Brown KT, Covey AM, et al. Percutaneous radiofrequency ablation of colorectal cancer liver metastases: factors affecting outcomes—a 10-year experience at a single center. Radiology. 2016;278:601–11.

    Article  PubMed  Google Scholar 

  26. Tsoumakidou G, Buy X, Garnon J, Enescu J, Gangi A. Percutaneous thermal ablation: how to protect the surrounding organs. Tech Vasc Interv Radiol. 2011;14:170–6.

    Article  PubMed  Google Scholar 

  27. Cornelis F, Buy X, Andre M, Oyen R, Bouffard-Vercelli J, Blandino A, et al. De novo renal tumors arising in kidney transplants: midterm outcome after percutaneous thermal ablation. Radiology. 2011;260:900–7.

    Article  PubMed  Google Scholar 

  28. Wright AS, Sampson LA, Warner TF, Mahvi DM, Lee FT. Radiofrequency versus microwave ablation in a hepatic porcine model. Radiology. 2005;236:132–9.

    Article  PubMed  Google Scholar 

  29. Hong B, Chen G, Zhao Y, Du X, Yang Y, Zhang X, et al. [Experimental study on ablation zone and characteristics of microwave ablation in porcine kidney in vitro]. Zhonghua Yi Xue Za Zhi. 2015;95:2644–6.

    PubMed  Google Scholar 

  30. Lee YJ, Lu DS, Osuagwu F, Lassman C. Irreversible electroporation in porcine liver: acute computed tomography appearance of ablation zone with histopathologic correlation. J Comput Assist Tomogr. 2013;37:154–8.

    Article  PubMed  Google Scholar 

  31. Deodhar A, Monette S, Single GW Jr, Hamilton WC Jr, Thornton R, Maybody M, et al. Renal tissue ablation with irreversible electroporation: preliminary results in a porcine model. Urology. 2011;77:754–60.

    Article  PubMed  Google Scholar 

  32. Sugimoto K, Moriyasu F, Kobayashi Y, Kasuya K, Nagakawa Y, Tsuchida A, et al. Assessment of various types of US findings after irreversible electroporation in porcine liver: comparison with radiofrequency ablation. J Vasc Interv Radiol. 2015;26:279–87e3.

    Article  PubMed  Google Scholar 

  33. Chung DJ, Sung K, Osuagwu FC, Wu HH, Lassman C, Lu DSK. Contrast enhancement patterns after irreversible electroporation: experimental study of CT perfusion correlated to histopathology in normal porcine liver. J Vasc Interv Radiol. 2016;27:104–11.

    Article  PubMed  Google Scholar 

  34. Niu L, Li J, Zeng J, Zhou L, Wang S, Zhou X, et al. Comparison of percutaneous cryoablation with microwave ablation in a porcine liver model. Cryobiology. 2014;68:194–9.

    Article  PubMed  Google Scholar 

  35. Lim HK, Choi D, Lee WJ, Kim SH, Lee SJ, Jang HJ, et al. Hepatocellular carcinoma treated with percutaneous radio-frequency ablation: evaluation with follow-up multiphase helical CT. Radiology. 2001;221:447–54.

    Article  CAS  PubMed  Google Scholar 

  36. Liu D, Brace CL. Numerical simulation of microwave ablation incorporating tissue contraction based on thermal dose. Phys Med Biol. 2017;62:2070–86.

    Article  PubMed  Google Scholar 

  37. Tracy CR, Kabbani W, Cadeddu JA. Irreversible electroporation (IRE): a novel method for renal tissue ablation. BJU Int. 2011;107:1982–7.

    Article  PubMed  Google Scholar 

  38. Charpentier KP, Wolf F, Noble L, Winn B, Resnick M, Dupuy DE. Irreversible electroporation of the liver and liver hilum in swine. HPB. 2011;13:168–73.

    Article  PubMed  PubMed Central  Google Scholar 

  39. Wendler JJ, Porsch M, Huhne S, Baumunk D, Buhtz P, Fischbach F, et al. Short- and mid-term effects of irreversible electroporation on normal renal tissue: an animal model. Cardiovasc Interv Radiol. 2013;36:512–20.

    Article  CAS  Google Scholar 

  40. Srimathveeravalli G, Cornelis F, Wimmer T, Monette S, Kimm SY, Maybody M, et al. Normal porcine ureter retains lumen wall integrity but not patency following catheter-directed irreversible electroporation: imaging and histologic assessment over 28 days. J Vasc Interv Radiol. 2017. doi:10.1016/j.jvir.2017.02.032.

    PubMed  Google Scholar 

  41. Sano MB, Fan RE, Hwang GL, Sonn GA, Xing L. Production of spherical ablations using nonthermal irreversible electroporation: a laboratory investigation using a single electrode and grounding pad. J Vasc Interv Radiol. 2016;27:1432–40e3.

    Article  PubMed  Google Scholar 

Download references

Funding

The project was supported by a philanthropic grant from the Thompson Foundation. The authors acknowledge the support of NIH Cancer Center Support Grant (P30 CA008748) for core laboratory services that were used for the presented work.

Author information

Authors and Affiliations

  1. Department of Radiology, Memorial Sloan-Kettering Cancer Center, 1275 York Avenue, New York, NY, 10065, USA

    Francois H. Cornelis, Jeremy C. Durack, Stephen B. Solomon & Govindarajan Srimathveeravalli

  2. Department of Urology, Palo Alto Medical Foundation, Palo Alto, CA, USA

    Simon Y. Kimm

  3. Medical University of Graz, Graz, Austria

    Thomas Wimmer

  4. Division of Urology, Department of Surgery, Memorial Sloan-Kettering Cancer Center, 1275 York Avenue, New York, NY, 10065, USA

    Jonathan A. Coleman

  5. Weill Cornell Medical College, New York, NY, USA

    Govindarajan Srimathveeravalli

Authors
  1. Francois H. Cornelis
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jeremy C. Durack
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Simon Y. Kimm
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Thomas Wimmer
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jonathan A. Coleman
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Stephen B. Solomon
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Govindarajan Srimathveeravalli
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Govindarajan Srimathveeravalli.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical Approval

All applicable international, national and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cornelis, F.H., Durack, J.C., Kimm, S.Y. et al. A Comparative Study of Ablation Boundary Sharpness After Percutaneous Radiofrequency, Cryo-, Microwave, and Irreversible Electroporation Ablation in Normal Swine Liver and Kidneys. Cardiovasc Intervent Radiol 40, 1600–1608 (2017). https://doi.org/10.1007/s00270-017-1692-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00270-017-1692-3

Keywords

Search

Navigation