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Effects of different pressure levels of CO2 pneumoperitoneum on liver regeneration after liver resection in a rat model

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Abstract

Background

A recent study demonstrated that high pressure of carbon dioxide (CO2) pneumoperitoneum before liver resection impairs postoperative liver regeneration. This study was aimed to investigate effects of varying insufflation pressures of CO2 pneumoperitoneum on liver regeneration using a rat model.

Methods

180 male Wistar rats were randomly divided into three groups: control group (without preoperative pneumoperitoneum), low-pressure group (with preoperative pneumoperitoneum at 5 mmHg), and high-pressure group (with preoperative pneumoperitoneum at 10 mmHg). After pneumoperitoneum, all rats were subjected to 70 % partial hepatic resection and then euthanized at 0 min, 12 h, and on postoperative days (PODs) 1, 2, 4, and 7. Following outcome parameters were used: liver regeneration (liver regeneration rate, mitotic count, Ki-67 labeling index), hepatocellular damage (serum aminotransferases), oxidative stress [serum malondialdehyde (MDA)], interleukin-6 (IL-6), and hepatocyte growth factor (HGF) expression in the liver tissue.

Results

No significant differences were observed for all parameters between control and low-pressure groups. The liver regeneration rate and mitotic count were significantly decreased in the high-pressure group than in control and low-pressure groups on PODs 2 and 4. Postoperative hepatocellular damage was significantly greater in the high-pressure group on PODs 1, 2, 4, and 7 compared with control and/or low-pressure groups. Serum MDA levels were significantly higher in the high-pressure group on PODs 1 and 2, and serum IL-6 levels were significantly higher in the high-pressure group at 12 h and on POD 1, compared with control and/or low-pressure groups. The HGF tissue expression was significantly lower in the high-pressure group at 12 h and on PODs 1 and 4, compared with that in control and/or low-pressure groups.

Conclusions

High-pressure pneumoperitoneum before 70 % liver resection impairs postoperative liver regeneration, but low-pressure pneumoperitoneum has no adverse effects. This study suggests that following laparoscopic liver resection using appropriate pneumoperitoneum pressure, no impairment of liver regeneration occurs.

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References

  1. Polychronidis A, Laftsidis P, Bounovas A, Simopoulos C (2008) Twenty years of laparoscopic cholecystectomy: Philippe Mouret—March 17, 1987. JSLS 12(1):109–111

    PubMed Central  PubMed  Google Scholar 

  2. Gagner M, Rheault M, Dubuc J (1992) Laparoscopic partial hepatectomy for liver tumor. Surg Endosc 6:97–98

    Google Scholar 

  3. Lee KF, Chong CN, Wong J, Cheung YS, Wong J, Lai P (2011) Long-term results of laparoscopic hepatectomy versus open hepatectomy for hepatocellular carcinoma: a case-matched analysis. World J Surg 35(10):2268–2274

    Article  PubMed  Google Scholar 

  4. Abu HM, Di FF, Syed S, Wiltshire R, Dimovska E, Turner D, Primrose JN, Pearce NW (2013) Assessment of the financial implications for laparoscopic liver surgery: a single-centre UK cost analysis for minor and major hepatectomy. Surg Endosc 27(7):2542–2550

    Article  Google Scholar 

  5. Nguyen KT, Gamblin TC, Geller DA (2009) World review of laparoscopic liver resection: 2,804 patients. Ann Surg 250(5):831–841

    Article  PubMed  Google Scholar 

  6. Viganò L, Tayar C, Laurent A, Cherqui D (2009) Laparoscopic liver resection: a systematic review. J Hepatobiliary Pancreat Surg 16(4):410–421

    Article  PubMed  Google Scholar 

  7. Nguyen KT, Marsh JW, Tsung A, Steel JJ, Gamblin TC, Geller DA (2011) Comparative benefits of laparoscopic vs open hepatic resection: a critical appraisal. Arch Surg 146(3):348–356

    Article  PubMed  Google Scholar 

  8. Nitta H, Sasaki A, Fujita T, Itabashi H, Hoshikawa K, Takahara T, Takahashi M, Nishizuka S, Wakabayashi G (2010) Laparoscopy-assisted major liver resections employing a hanging technique: the original procedure. Ann Surg 251(3):450–453

    Article  PubMed  Google Scholar 

  9. Lin NC, Nitta H, Wakabayashi G (2013) Laparoscopic major hepatectomy: a systematic literature review and comparison of 3 techniques. Ann Surg 257:205–213

    Article  PubMed  Google Scholar 

  10. Dagher I, O’Rourke N, Geller DA, Cherqui D, Belli G, Gamblin TC, Lainas P, Laurent A, Nguyen KT, Marvin MR, Thomas M, Ravindra K, Fielding G, Franco D, Buell JF (2009) Laparoscopic major hepatectomy: an evolution in standard of care. Ann Surg 250(5):856–860

    Article  PubMed  Google Scholar 

  11. Pross M, Schulz HU, Flechsig A, Manger T, Halangk W, Augustin W, Lippert H, Reinheckel T (2000) Oxidative stress in lung tissue induced by CO2 pneumoperitoneum in the rat. Surg Endosc 14(12):1180–1184

    Article  CAS  PubMed  Google Scholar 

  12. Schäfer M, Sägesser H, Reichen J, Krähenbühl L (2001) Alterations in hemodynamics and hepatic and splanchnic circulation during laparoscopy in rats. Surg Endosc 15:1197–1201

    Article  PubMed  Google Scholar 

  13. Eleftheriadis E, Kotzampassi K, Papanotas K, Heliadis N, Sarris K (1996) Gut ischemia, oxidative stress, and bacterial translocation in elevated abdominal pressure in rats. World J Surg 20:11–16

    Article  CAS  PubMed  Google Scholar 

  14. Polat C, Aktepe OC, Akbulut G, Yilmaz S, Arikan Y, Dilek ON, Gokce O (2003) The effects of increased intra-abdominal pressure on bacterial translocation. Yonsei Med J 44(2):259–264

    PubMed  Google Scholar 

  15. Smith HS (2011) Carbon dioxide embolism during pneumoperitoneum for laparoscopic surgery: a case report. AANA J 79:371–373

    PubMed  Google Scholar 

  16. Eiriksson K, Fors D, Rubertsson S, Arvidsson D (2011) High intra-abdominal pressure during experimental laparoscopic liver resection reduces bleeding but increases the risk of gas embolism. Br J Surg 98(6):845–852

    Article  CAS  PubMed  Google Scholar 

  17. Gutt CN, Schmandra TC (1999) Portal venous flow during CO2 pneumoperitoneum in the rat. Surg Endosc 13:902–905

    Article  CAS  PubMed  Google Scholar 

  18. Schmandra TC, Kim ZG, Gutt CN (2001) Effect of insufflation gas and intraabdominal pressure on portal venous flow during pneumoperitoneum in the rat. Surg Endosc 15:405–408

    Article  CAS  PubMed  Google Scholar 

  19. Jakimowicz J, Stultiëns G, Smulders F (1998) Laparoscopic insufflation of the abdomen reduces portal venous flow. Surg Endosc 12(2):129–132

    Article  CAS  PubMed  Google Scholar 

  20. Richter S, Olinger A, Hildebrandt U, Menger MD, Vollmar B (2001) Loss of physiologic hepatic blood flow control (“hepatic arterial buffer response”) during CO2 pneumoperitoneum in the rat. Anesth Analg 93:872–877

    Article  CAS  PubMed  Google Scholar 

  21. Schmidt SC, Schumacher G, Klage N, Chopra S, Neuhaus P, Neumann U (2010) The impact of carbon dioxide pneumoperitoneum on liver regeneration after liver resection in a rat model. Surg Endosc 24:1–8

    Article  CAS  PubMed  Google Scholar 

  22. Avital S, Itash R, Szomstein S, Rosenthal R, Inbar R, Sckornik Y, Weinbroum A (2009) Correlation of CO2 pneumoperitoneal pressures between rodents and humans. Surg Endosc 23(1):50–54

    Article  PubMed  Google Scholar 

  23. Perrin M, Fletcher A (2004) Laparoscopic abdominal surgery. Contin Educ Anaesth Crit Care Pain 4(4):107–110

    Article  Google Scholar 

  24. Matsumoto T, Tsuboi S, Dolgor B, Bandoh T, Yoshida T, Kitano S (2001) The effect of gases in the intraperitoneal space on cytokine response and bacterial translocation in a rat model. Surg Endosc 15:80–84

    Article  CAS  PubMed  Google Scholar 

  25. Martins PNA, Theruvath TP, Neuhaus P (2007) Rodent models of partial hepatectomies. Liver Int 28:3–11

    Article  PubMed  Google Scholar 

  26. Okano T, Ohwada S, Nakasone Y, Sato Y, Ogawa T, Tago K, Morishita Y (2001) Blood transfusion causes deterioration in liver regeneration after partial hepatectomy in rats. J Surg Res 101(2):157–165

    Article  CAS  PubMed  Google Scholar 

  27. Endo Y, Ohta M, Sasaki A et al (2007) A comparative study of the long-term outcomes after laparoscopy-assisted and open left lateral hepatectomy for hepatocellular carcinoma. Surg Laparosc Endosc Percutan Tech 19:171–174

    Article  Google Scholar 

  28. Güven HE, Oral S (2007) Liver enzyme alterations after laparoscopic cholecystectomy. J Gastrointest Liver Dis 16:391–394

    Google Scholar 

  29. Glantzounis GK, Tselepis AD, Tambaki AP, Trikalinos TA, Manataki AD, Galaris DA, Tsimoyiannis EC, Kappas AM (2001) Laparoscopic surgery-induced changes in oxidative stress markers in human plasma. Surg Endosc 15:1315–1319

    Article  CAS  PubMed  Google Scholar 

  30. Eryılmaz HB, Memis D, Sezer A, Inal MT (2012) The effects of different insufflation pressures on liver functions assessed with LiMON on patients undergoing laparoscopic cholecystectomy. Sci World J. doi:10.1100/2012/172575 (Epub 24 April 2012)

  31. Morino M, Giraudo G, Festa V (1998) Alterations in hepatic function during laparoscopic surgery: an experimental clinical study. Surg Endosc 12:968–972

    Article  CAS  PubMed  Google Scholar 

  32. Ferrari R (1994) Oxygen-Free radicals at myocardial level: effects of ischemia and reperfusion. Adv Exp Med Biol 366:99–111

    Article  CAS  PubMed  Google Scholar 

  33. Kloner RA, Przyklenk K, Whittaker P (1989) Deleterious effects of oxygen radicals in ischemia/reperfusion. Resolved and unresolved issues. Circulation 80:1115–1127

    Article  CAS  PubMed  Google Scholar 

  34. Foschi D, Castoldi L, Lesma A, Musazzi M, Benevento A, Trabucchi E (1993) Effects of ischaemia and reperfusion on liver regeneration in rats. Eur J Surg 59:393–398

    Google Scholar 

  35. Camargo CA Jr, Madden JF, Gao W, Selvan RS, Clavien PA (1997) Interleukin-6 protects liver against warm ischemia/reperfusion injury and promotes hepatocyte proliferation in the rodent. Hepatology 26(6):1513–1520

    Article  CAS  PubMed  Google Scholar 

  36. Usami M, Furuchi K, Shiroiwa H, Saitoh Y (1994) Effect of repeated portal-triad cross-clamping during partial hepatectomy on hepatic regeneration in normal and cirrhotic rats. J Surg Res 57(5):541–548

    Article  CAS  PubMed  Google Scholar 

  37. Hazebroek EJ, Haitsma JJ, Lachmann B, Steyerberg EW, de Bruin RW, Bouvy ND, Bonjer HJ (2002) Impact of carbon dioxide and helium insufflation on cardiorespiratory function during prolonged pneumoperitoneum in an experimental rat model. Surg Endosc 16:1073–1078

    Article  CAS  PubMed  Google Scholar 

  38. Nickkholgh A, Barro-Bejarano M, Liang R, Zorn M, Mehrabi A, Gebhard MM, Büchler MW, Gutt CN, Schemmer P (2008) Signs of reperfusion injury following CO2 pneumoperitoneum: an in vivo microscopy study. Surg Endosc 22:122–128

    Article  PubMed  Google Scholar 

  39. Kaya Y, Aral W, Coskun T, Erkasap N, Var A (2002) Increased intraabdominal pressure impairs liver regeneration after partial hepatectomy in rats. J Surg Res 108:250–257

    Article  PubMed  Google Scholar 

  40. Yagmurdur MC, Basaran O, Ozdemir H, Gur G, Turan M, Karakayali H, Haberal M (2004) The impact of transient elevation of intraabdominal pressure on liver regeneration in the rat. J Investig Surg 17:315–322

    Article  Google Scholar 

  41. Gagner M (2010) High-pressure carbon dioxide pneumoperitoneum before major liver resection in a rat model is not realistic and cannot be transposed to humans when studying liver regeneration. Surg Endosc 25:988–989

    Article  Google Scholar 

  42. Sammour T, Mittal A, Loveday BP, Kahokehr A, Phillips AR, Windsor JA, Hill AG (2009) Systematic review of oxidative stress associated with pneumoperitoneum. Br J Surg 96:836–850

    Article  CAS  PubMed  Google Scholar 

  43. Xu GS, Liu HN, Li J, Wu XL, Dai XM, Liu YH (2009) Hepatic injury induced by carbon dioxide pneumoperitoneum in experimental rats. World J Gastroenterol 15(24):3060–3064

    Article  PubMed Central  PubMed  Google Scholar 

  44. Biffl WL, Moore EE, Moore FA, Peterson VM (1996) Interleukin-6 in the injured patient marker of injury or mediator of inflammation? Ann Surg 224:647–664

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  45. Xing Z, Gauldie J, Cox G, Baumann H, Jordana M, Lei XF, Achong MK (1998) IL-6 is an antiinflammatory cytokine required for controlling local or systemic acute inflammatory responses. J Clin Investig 101:311–320

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  46. Otsuka Y, Katagiri T, Ishii J, Maeda T, Kubota Y, Tamura A, Tsuchiya M, Kaneko H (2013) Gas embolism in laparoscopic hepatectomy: what is the optimal pneumoperitoneal pressure for laparoscopic major hepatectomy? J Hepatobiliary Pancreat Sci 20:137–140

    Article  PubMed  Google Scholar 

  47. Are C, Fong Y, Geller DA (2005) Laparoscopic liver resection. Adv Surg 39:57–75

    Article  PubMed  Google Scholar 

  48. Buell JF, Koffron AJ, Thomas MJ, Rudich S, Abecassis M, Woodle ES (2005) Laparoscopic liver resection. J Am Coll Surg 200:472–480

    Article  PubMed  Google Scholar 

  49. Cannon RM, Brock GN, Marvin MR, Buell JF (2011) Laparoscopic liver resection: an examination of our first 300 patients. J Am Coll Surg 213:501–507

    Article  PubMed  Google Scholar 

  50. Leister I, Schüler P, Vollmar B, Füzesi L, Kahler E, Becker H, Markus PM (2004) Microcirculation and excretory function of the liver under conditions of carbon dioxide pneumoperitoneum. Surg Endosc 18:1358–1363

    Article  CAS  PubMed  Google Scholar 

  51. Junghans T, Böhm B, Meyer E (2000) Influence of nitrous oxide anesthesia on venous gas embolism with carbon dioxide and helium during pneumoperitoneum. Surg Endosc 14:1167–1170

    Article  CAS  PubMed  Google Scholar 

  52. Nesek-Adam V, Rasić Z, Vnuk D, Schwarz D, Rasić D, Crvenković D (2010) Ischemic preconditioning decreases laparoscopy induced oxidative stress in the liver. Coll Antropol 34:571–576

    CAS  PubMed  Google Scholar 

  53. Cevrioglu AS, Yilmaz S, Koken T, Tokyol C, Yilmazer M, Fenkci IV (2004) Comparison of the effects of low intra-abdominal pressure and ischaemic preconditioning on the generation of oxidative stress markers and inflammatory cytokines during laparoscopy in rats. Hum Reprod 19:2144–2151

    Article  PubMed  Google Scholar 

  54. Avraamidou A, Marinis A, Asonitis S, Perrea D, Polymeneas G, Voros D, Argyra E (2012) The impact of ischemic preconditioning on hemodynamic, biochemical and inflammatory alterations induced by intra-abdominal hypertension: an experimental study in a porcine model. Langenbecks Arch Surg 397:1333–1341

    Article  PubMed  Google Scholar 

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Acknowledgments

We are grateful to Ms. Mayumi Takeda for her technical assistance.

Disclosures

The authors declare no conflicts of interest. No financial support was received for this study.

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Correspondence to Yoko Komori.

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Komori, Y., Iwashita, Y., Ohta, M. et al. Effects of different pressure levels of CO2 pneumoperitoneum on liver regeneration after liver resection in a rat model. Surg Endosc 28, 2466–2473 (2014). https://doi.org/10.1007/s00464-014-3498-6

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  • DOI: https://doi.org/10.1007/s00464-014-3498-6

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