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Digestive Diseases and Sciences

, Volume 56, Issue 5, pp 1548–1556 | Cite as

Pringle Maneuver Deteriorates Gut Barrier Dysfunction Induced by Extended-Liver Radiofrequency Ablation

  • Petros Ypsilantis
  • Maria Lambropoulou
  • Anastasia Grapsa
  • Ioannis Tentes
  • Christina Tsigalou
  • Maria Panopoulou
  • Constantinos Simopoulos
Original Article

Abstract

Background

Large volume radiofrequency ablation (RFA) of the liver disrupts intestinal mucosa barrier with subsequent bacterial translocation.

Aims

To investigate the effect of the Pringle maneuver applied concurrently with extended liver RFA on gut barrier integrity and bacterial translocation.

Materials and Methods

Rats were subjected to 30% liver RFA following laparotomy (group RFA), RFA plus 30 min Pringle (group RFA + P), Pringle (group P) or sham operation (group S). Intestinal tissue specimens were excised for histopathological examination and assessment of mucosal morphometry, apoptotic activity, mitotic activity and oxidative state. Tissue specimens were collected from the mesenteric lymph nodes, non-ablated liver parenchyma, kidneys and lungs for bacterial culture. Blood samples were collected from the portal and systemic circulation for endotoxin level measurement.

Results

In group RFA + P, intestinal histopathologic lesions, mucosal atrophy and crypt cell apoptosis were more prominent compared to group RFA. Mitotic activity was suppressed. Oxidative stress was equally induced in all experimental groups. The incidence of positive bacterial cultures, bacterial counts and endotoxin levels were higher in group RFA + P compared to the other groups.

Conclusion

The application of the Pringle maneuver concurrently with extended liver RFA aggravates gut barrier dysfunction with more aggressive translocation of endotoxins and intestinal bacteria.

Keywords

Radiofrequency ablation Pringle Gut barrier Bacterial translocation 

References

  1. 1.
    Mulier S, Mulier P, Ni Y, et al. Complications of radiofrequency coagulation of liver tumours. Br J Surg. 2002;89:1206–1222.PubMedCrossRefGoogle Scholar
  2. 2.
    Bleicher RJ, Allegra DP, Nora DT, Wood TF, Foshag LJ, Bilchik AJ. Radiofrequency ablation in 447 complex unresectable liver tumors: lessons learned. Ann Surg Oncol. 2003;10:52–58.PubMedCrossRefGoogle Scholar
  3. 3.
    Livraghi T, Solbiati L, Meloni MF, Gazelle GS, Halpern EF, Goldberg SN. Treatment of focal liver tumors with percutaneous radio-frequency ablation: complications encountered in a multicenter study. Radiology. 2003;226:441–451.PubMedCrossRefGoogle Scholar
  4. 4.
    Rhim H. Complications of radiofrequency ablation in hepatocellular carcinoma. Abdom Imaging. 2005;30:409–418.PubMedCrossRefGoogle Scholar
  5. 5.
    Curley SA, Marra P, Beaty K, et al. Early and late complications after radiofrequency ablation of malignant liver tumors in 608 patients. Ann Surg. 2004;239:450–458.PubMedCrossRefGoogle Scholar
  6. 6.
    Jansen MC, van Duijnhoven FH, van Hillegersberg R, et al. Adverse effects of radiofrequency ablation of liver tumours in the Netherlands. Br J Surg. 2005;92:1248–1254.PubMedCrossRefGoogle Scholar
  7. 7.
    Dodd GD III, Napier D, Schoolfield JD, Hubbard L. Percutaneous radiofrequency ablation of hepatic tumors: postablation syndrome. Am J Roentgenol. 2005;185:51–57.Google Scholar
  8. 8.
    Ypsilantis P, Panopoulou M, Lambropoulou M, et al. Bacterial translocation in a rat model of large volume hepatic radiofrequency ablation. J Surg Res. 2010;161:250–258.PubMedCrossRefGoogle Scholar
  9. 9.
    Rossi S, Garbagnati F, De Drancesco I. Relationship between the shape and size of radiofrequency induced thermal lesions and hepatic vascularization. Tumori. 1999;85:128–132.PubMedGoogle Scholar
  10. 10.
    Aschoff AJ, Merkle EM, Wong V, et al. How does alteration of hepatic blood flow affect liver perfusion and radiofrequency-induced thermal lesion size in rabbit liver? J Magn Reson Imaging. 2001;13:57–63.PubMedCrossRefGoogle Scholar
  11. 11.
    Chinn SB, Lee FT Jr, Kennedy GD, et al. Effect of vascular occlusion on radiofrequency ablation of the liver: results in a porcine model. Am J Roentgenol. 2001;176:789–795.Google Scholar
  12. 12.
    Wiersinga WJ, Jansen MC, Straatsburg IH, et al. Lesion progression with time and the effect of vascular occlusion following radiofrequency ablation of the liver. Br J Surg. 2003;90:306–312.PubMedCrossRefGoogle Scholar
  13. 13.
    Lu DS, Raman SS, Vodopich DJ, Wang M, Sayre J, Lassman C. Effect of vessel size on creation of hepatic radiofrequency lesions in pigs: assessment of the “heat sink” effect. Am J Roentgenol. 2002;178:47–51.Google Scholar
  14. 14.
    Lu DS, Raman SS, Limanond P, et al. Influence of large peritumoral vessels on outcome of radiofrequency ablation of liver tumors. J Vasc Interv Radiol. 2003;14:1267–1274.PubMedGoogle Scholar
  15. 15.
    Filos KS, Kirkilesis I, Spiliopoulou I, et al. Bacterial translocation, endotoxaemia and apoptosis following Pringle manoeuvre in rats. Injury. 2004;35:35–43.PubMedCrossRefGoogle Scholar
  16. 16.
    Lorente L, Aller MA, Rodriguez J, et al. Surgical anatomy of the liver in Wistar rats. Surg Res Commun. 1995;17:113–121.Google Scholar
  17. 17.
    Friberger P, Knos M, Mellstam L. A quantitative endotoxin assay utilizing LAL and a chromogenic substrate. In: Watson SW, Levin J, Novitsky TJ, eds. Endotoxins and their detection with the Limulus amebocyte lysate test. New York: Alan R. Liss; 1982:195–206.Google Scholar
  18. 18.
    Balzan S, de Almeida Quadros C, de Cleva R, de Cleva R, Zilberstein B, Cecconello I. Bacterial translocation: overview of mechanisms and clinical impact. J Gastroenterol Hepatol. 2007;22:464–471.PubMedCrossRefGoogle Scholar
  19. 19.
    Wiest R, Garcia-Tsao G. Bacterial translocation (BT) in cirrhosis. Hepatology. 2005;41:422–433.PubMedCrossRefGoogle Scholar
  20. 20.
    Assimakopoulos SF, Scopa CD, Vagianos CE. Pathophysiology of increased intestinal permeability in obstructive jaundice. World J Gastroenterol. 2007;13:6458–6464.PubMedCrossRefGoogle Scholar
  21. 21.
    Wang XD, Parsson H, Andersson R, Soltesz V, Johansson K, Bengmark S. Bacterial translocation, intestinal ultrastructure and cell membrane permeability early after major liver resection in the rat. Br J Surg. 1994;81:579–584.PubMedCrossRefGoogle Scholar
  22. 22.
    Ypsilantis P, Lambropoulou M, Tentes I, Kortsaris A, Papadopoulos N, Simopoulos C. Mesna protects intestinal mucosa from ischemia-reperfusion injury. J Surg Res. 2006;134:278–284.PubMedCrossRefGoogle Scholar
  23. 23.
    Ypsilantis P, Lambropoulou M, Anagnostopoulos C, Tentes I, Tsigalou C, Pitiakoudis M, Kortsaris A, Papadopoulos N, Simopoulos C. Mesna preserves hepatocyte regenerating capacity following liver radiofrequency ablation under Pringle maneuver. J Surg Res. 2009 Oct 25 [Epub ahead of print].Google Scholar
  24. 24.
    Ypsilantis P, Papakostas C, Lambropoulou M, et al. Liver radiofrequency ablation leads to systemic inflammatory response in the rat. In: 23rd Northern Greek medical congress, Thessaloniki, 27–29th March 2008.Google Scholar
  25. 25.
    Liu DL, Jeppsson B, Hakansson CH, Odselius R. Multiple-system organ damage resulting from prolonged hepatic inflow interruption. Arch Surg. 1996;131:442–447.PubMedGoogle Scholar
  26. 26.
    Yoshidome H, Kato A, Edwards MJ, Lentsch AB. Interleukin-10 inhibits pulmonary NF-kappa B activation and lung injury induced by hepatic ischemia-reperfusion. Am J Physiol. 1999;277:L919–L923.PubMedGoogle Scholar
  27. 27.
    Jiang H, Meng F, Li W, Tong L, Qiao H, Sun X. Splenectomy ameliorates acute multiple organ damage induced by liver warm ischemia reperfusion in rats. Surgery. 2007;141:32–40.PubMedCrossRefGoogle Scholar
  28. 28.
    Ypsilantis P, Lambropoulou M, Tentes I, et al. Impaired liver regeneration following partial hepatectomy using the Pringle maneuver. Protective effect of mesna. J Gastroent Hepatol. 2008;24:623–632.CrossRefGoogle Scholar
  29. 29.
    Takeuchi D, Yoshidome H, Kurosawa H, et al. Interleukin-18 exacerbates pulmonary injury after hepatic ischemia/reperfusion in mice. J Surg Res. 2010;158:87–93.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • Petros Ypsilantis
    • 1
  • Maria Lambropoulou
    • 2
  • Anastasia Grapsa
    • 3
  • Ioannis Tentes
    • 4
  • Christina Tsigalou
    • 5
  • Maria Panopoulou
    • 3
  • Constantinos Simopoulos
    • 1
  1. 1.Laboratory of Experimental Surgery and Surgical Research, School of MedicineDemocritus University of ThraceAlexandroupolisGreece
  2. 2.Laboratory of Histology and Embryology, School of MedicineDemocritus University of ThraceAlexandroupolisGreece
  3. 3.Laboratory of Microbiology, School of MedicineDemocritus University of ThraceAlexandroupolisGreece
  4. 4.Laboratory of Biochemistry, School of MedicineDemocritus University of ThraceAlexandroupolisGreece
  5. 5.Laboratory of BiochemistryUniversity General Hospital of AlexandroupolisAlexandroupolisGreece

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