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

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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.

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References

  1. Mulier S, Mulier P, Ni Y, et al. Complications of radiofrequency coagulation of liver tumours. Br J Surg. 2002;89:1206–1222.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  4. Rhim H. Complications of radiofrequency ablation in hepatocellular carcinoma. Abdom Imaging. 2005;30:409–418.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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. 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.

    Article  PubMed  Google Scholar 

  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.

    PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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. 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.

    PubMed  Google Scholar 

  15. Filos KS, Kirkilesis I, Spiliopoulou I, et al. Bacterial translocation, endotoxaemia and apoptosis following Pringle manoeuvre in rats. Injury. 2004;35:35–43.

    Article  PubMed  Google Scholar 

  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. 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. 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.

    Article  PubMed  CAS  Google Scholar 

  19. Wiest R, Garcia-Tsao G. Bacterial translocation (BT) in cirrhosis. Hepatology. 2005;41:422–433.

    Article  PubMed  CAS  Google Scholar 

  20. Assimakopoulos SF, Scopa CD, Vagianos CE. Pathophysiology of increased intestinal permeability in obstructive jaundice. World J Gastroenterol. 2007;13:6458–6464.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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].

  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.

  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.

    PubMed  CAS  Google Scholar 

  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.

    PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Laboratory of Experimental Surgery and Surgical Research, School of Medicine, Democritus University of Thrace, University General Hospital of Alexandroupolis, 68100, Alexandroupolis, Greece

    Petros Ypsilantis & Constantinos Simopoulos

  2. Laboratory of Histology and Embryology, School of Medicine, Democritus University of Thrace, Alexandroupolis, Greece

    Maria Lambropoulou

  3. Laboratory of Microbiology, School of Medicine, Democritus University of Thrace, Alexandroupolis, Greece

    Anastasia Grapsa & Maria Panopoulou

  4. Laboratory of Biochemistry, School of Medicine, Democritus University of Thrace, Alexandroupolis, Greece

    Ioannis Tentes

  5. Laboratory of Biochemistry, University General Hospital of Alexandroupolis, Alexandroupolis, Greece

    Christina Tsigalou

Authors
  1. Petros Ypsilantis
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  2. Maria Lambropoulou
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  3. Anastasia Grapsa
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  4. Ioannis Tentes
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  5. Christina Tsigalou
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  6. Maria Panopoulou
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  7. Constantinos Simopoulos
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Correspondence to Petros Ypsilantis.

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Ypsilantis, P., Lambropoulou, M., Grapsa, A. et al. Pringle Maneuver Deteriorates Gut Barrier Dysfunction Induced by Extended-Liver Radiofrequency Ablation. Dig Dis Sci 56, 1548–1556 (2011). https://doi.org/10.1007/s10620-010-1462-4

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  • DOI: https://doi.org/10.1007/s10620-010-1462-4

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