Top

Surgical Endoscopy

Published in:

01-01-2010

The impact of carbon dioxide pneumoperitoneum on liver regeneration after liver resection in a rat model

Authors: S. C. Schmidt, G. Schumacher, N. Klage, S. Chopra, P. Neuhaus, U. Neumann

Published in: Surgical Endoscopy | Issue 1/2010

Abstract

Background

In recent years, laparoscopic hepatic resection is performed by an increasing number of surgeons. Despite many advantages of the laparoscopic procedure, it is unclear whether the pneumoperitoneum affects the postoperative liver regeneration after liver resection. The current study aimed to investigate the influence of a carbon dioxide (CO₂) pneumoperitoneum on liver regeneration in a rat model.

Methods

In this study, 60 male Wistar rats were subjected to 70% partial hepatic resection. Of these 60 animals, 30 underwent preoperative pneumoperitoneum at 9 mmHg for 60 min. After hepatic resection, the rats were killed at 12, 24, and 48 h, and on days 4 and 7. The outcome parameters were hepatocellular injury (plasma aminotransferases), oxidative stress (plasma malondialdehyde), interleukin-6 (IL-6), and liver regeneration (mitotic index, KI-67; regenerating liver mass).

Results

The mitotic index was significantly lower in the pneumoperitoneum group than in the group without pneumoperitoneum at all time points (p < 0.05). In the pneumoperitoneum group, KI-67 was significantly lower on day 4 (p < 0.05). The liver regeneration rate was significantly lower for the animals with pneumoperitoneum on days 2 and 4 (p < 0.05). The postoperative hepatocellular injury was significantly greater after pneumoperitoneum at 12, 24, and 48 h (p < 0.05). Plasma malondialdehyde and IL-6 were significantly higher in the pneumoperitoneum group at 24 h and on day 4 (p < 0.05).

Conclusion

This study showed that pneumoperitoneum before extended liver resection impaired postoperative liver regeneration. Oxidative stress reaction and hepatocellular damage was markedly higher after pneumoperitoneum. Further investigations, especially with patients that have impaired liver function, are necessary for clinical consequences to be drawn from these results.

Buell JF, Thomas MJ, Doty TC, Gersin KS, Merchen TD, Gupta M, Rudich SM, Woodle ES (2004) An initial experience and evolution of laparoscopic hepatic resectional surgery. Surgery 136:804–811CrossRefPubMed

Gutt CN, Riemer V, Kim ZG, Erceg J, Lorenz M (2001) Impact of laparoscopic surgery on experimental hepatic metastases. Br J Surg 8:371–375CrossRef

Belli G, Fantini C, D’Agostino A, Cioffi L, Langella S, Russolillo N, Belli A (2007) Laparoscopic versus open liver resection for hepatocellular carcinoma in patients with histologically proven cirrhosis: short- and middle-term results. Surg Endosc 21:2004–2011CrossRefPubMed

Dagher I, Lainas P, Carloni A, Caillard C, Champault A, Smadja C, Franco D (2008) Laparoscopic liver resection for hepatocellular carcinoma. Surg Endosc 22:372–378CrossRefPubMed

Koffron AJ, Auffenberg G, Kung R, Abecassis M (2007) Evaluation of 300 minimally invasive liver resections at a single institution: less is more. Ann Surg 246:385–392CrossRefPubMed

Vibert E, Perniceni T, Levard H, Denet C, Shahri NK, Gayet B (2006) Laparoscopic liver resection. Br J Surg 93:67–72CrossRefPubMed

Chen HY, Juan CC, Ker CG (2008) Laparoscopic liver surgery for patients with hepatocellular carcinoma. Ann Surg Oncol 15:800–806CrossRefPubMed

Simillis C, Constantinides VA, Tekkis PP, Darzi A, Lovegrove R, Jiao L, Antoniou A (2007) Laparoscopic versus open hepatic resections for benign and malignant neoplasms: a meta-analysis. Surgery 141:203–211CrossRefPubMed

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

10.

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 14:1180–1184CrossRefPubMed

11.

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 20:11–16CrossRefPubMed

12.

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 93:872–877CrossRefPubMed

13.

Diebel LN, Wilson RF, Dulchavsky SA, Saxe J (1992) Effect of increased intraabdominal pressure on hepatic arterial, portal venous, and hepatic microcirculatory blood flow. J Trauma 33:279–282PubMedCrossRef

14.

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

15.

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

16.

Andrei VE, Schein M, Margolis M, Rucinski JC, Wise L (1998) Liver enzymes are commonly elevated following laparoscopic cholecystectomy: is elevated intraabdominal pressure the cause? Dig Surg 15:256–259CrossRefPubMed

17.

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

18.

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 22:122–128CrossRefPubMed

19.

Yilmaz S, Polat C, Kahraman A, Koken T, Arikan Y, Dilek ON, Gökçe O (2004) The comparison of the oxidative stress effects of different gases and intraabdominal pressures in an experimental rat model. J Laparoendosc Adv Surg Tech A 14:165–168CrossRefPubMed

20.

Sare M, Hamamci D, Yilmaz I, Birincioglu M, Mentes BB, Ozmen M, Yesilada O (2002) Effects of carbon dioxide pneumoperitoneum on free radical formation in lung and liver tissues. Surg Endosc 2002(16):188–192CrossRef

21.

Vittimberga FJ Jr, Foley DP, Meyers WC, Callery MP (1998) Laparoscopic surgery and the systemic immune response. Ann Surg 227:326–334CrossRefPubMed

22.

Zulfikaroglu B, Koc M, Soran A, Isman FK, Cinel I (2002) Evaluation of oxidative stress in laparoscopic cholecystectomy. Surg Today 32:869–874CrossRefPubMed

23.

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

24.

Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95:351–358CrossRefPubMed

25.

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 101:157–165CrossRefPubMed

26.

Gayet B, Cavaliere D, Vibert E, Perniceni T, Levard H, Denet C, Christidis C, Blain A, Mal F (2007) Totally laparoscopic right hepatectomy. Am J Surg 194:685–689CrossRefPubMed

27.

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 Invest Surg 17:315–322CrossRefPubMed

28.

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 15:1315–1319CrossRefPubMed

29.

Li C, Jackson RM (2002) Reactive species mechanisms of cellular hypoxia-reoxygenation injury. Am J Physiol Cell Physiol 282:C227–C241PubMed

30.

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

31.

Saber AA, Laraja RD, Nalbandian HI, Pablos-Mendez A, Hanna K (2000) Changes in liver function tests after laparoscopic cholecystectomy: not so rare, not always ominous. Am Surg 66:699–702PubMed

32.

Tan M, Xu FF, Peng JS, Li DM, Chen LH, Lv BJ, Zhao ZX, Huang C, Zheng CX (2003) Changes in the level of serum liver enzymes after laparoscopic surgery. World J Gastroenterol 9:364–367PubMed

33.

Sakorafas G, Anagnostopoulos G, Stafyla V, Koletis T, Kotsifopoulos N, Tsiakos S, Kassaras G (2005) Elevation of serum liver enzymes after laparoscopic cholecystectomy. N Z Med J 118:U1317PubMed

34.

Schemmer P, Barro-Bejarano M, Mehrabi A, Gebhard MM, Kraus T, Büchler MW, Gutt CN. Laparoscopic organ retrieval for living donor liver transplantation does not prevent graft injury. Transplant Proc 37:1625–1627

35.

Tsuboi S, Kitano S, Yoshida T, Bandoh T, Ninomiya K, Baatar D (2002) Effects of carbon dioxide pneumoperitoneum on hemodynamics in cirrhotic rats. Surg Endosc 16:1220–1225CrossRefPubMed

36.

Okaya T, Lentsch AB (2003) Cytokine cascades and the hepatic inflammatory response to ischemia and reperfusion. J Invest Surg 16:141–147PubMed

37.

Altindis M, Yilmaz S, Polat C, Serteser M (2004) Sequential periods of preconditioning decrease laparoscopy-related elevations in hepatic TNF-alpha and IL-6 levels in rats. J Laparoendosc Adv Surg Tech A 14:380–383PubMed

38.

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

39.

Court FG, Wemyss-Holden SA, Dennison AR, Maddern GJ (2002) The mystery of liver regeneration. Br J Surg 89:1089–1095CrossRefPubMed

40.

Kimura F, Shimizu H, Yoshidome H, Ohtsuka M, Kato A, Yoshitomi H, Nozawa S, Furukawa K, Mitsuhashi N, Sawada S, Takeuchi D, Ambiru S, Miyazaki M (2006) Circulating cytokines, chemokines, and stress hormones are increased in patients with organ dysfunction following liver resection. J Surg Res 133:102–112CrossRefPubMed

41.

Peralta C, Prats N, Xaus C, Gelpí E, Roselló-Catafau J (1999) Protective effect of liver ischemic preconditioning on liver and lung injury induced by hepatic ischemia-reperfusion in the rat. Hepatology 30:1481–1489CrossRefPubMed

42.

Bilzer M, Gerbes AL (2000) Preservation injury of the liver: mechanisms and novel therapeutic strategies. J Hepatol 32:508–515CrossRefPubMed

43.

Glanemann M, Münchow S, Schirmeier A, Al-Abadi H, Lippek F, Langrehr JM, Dietel M, Neuhaus P, Nussler AK (2004) Steroid administration before partial hepatectomy with temporary inflow occlusion does not influence cyclin D1 and KI-67-related liver regeneration. Langenbecks Arch Surg 389:380–386CrossRefPubMed

44.

Schmidt SC, Hamann S, Langrehr JM, Höflich C, Mittler J, Jacob D, Neuhaus P (2007) Preoperative high-dose steroid administration attenuates the surgical stress response following liver resection: results of a prospective randomized study. J Hepatobiliary Pancreat Surg 14:484–492CrossRefPubMed

45.

Bickel A, Drobot A, Aviram M, Eitan A (2007) Validation and reduction of the oxidative stress following laparoscopic operations: a prospective randomized controlled study. Ann Surg 246:31–35CrossRefPubMed

46.

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

47.

Dinckan A, Sahin E, Ogus M, Emek K, Gumuslu S (2008) The effect of pentoxifylline on oxidative stress in CO₂ pneumoperitoneum. Surg Endosc 18 March 2008 Epub ahead of print

48.

Ypsilantis P, Tentes I, Anagnostopoulos K, Kortsaris A, Simopoulos C (2008) Mesna protects splanchnic organs from oxidative stress induced by pneumoperitoneum. Surg Endosc 27 March Epub ahead of print

49.

Sato K, Kawamura T, Wakusawa R (2000) Hepatic blood flow and function in elderly patients undergoing laparoscopic cholecystectomy. Anesth Analg 90:1198–1202CrossRefPubMed

Title: The impact of carbon dioxide pneumoperitoneum on liver regeneration after liver resection in a rat model
Authors: S. C. Schmidt
G. Schumacher
N. Klage
S. Chopra
P. Neuhaus
U. Neumann
Publication date: 01-01-2010
Publisher: Springer-Verlag
Published in: Surgical Endoscopy / Issue 1/2010
Print ISSN: 0930-2794
Electronic ISSN: 1432-2218
DOI: https://doi.org/10.1007/s00464-009-0536-x

Keynote webinar | Spotlight on medication adherence

Springer Medicine

The impact of carbon dioxide pneumoperitoneum on liver regeneration after liver resection in a rat model

Abstract

Background

Methods

Results

Conclusion

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Background

Methods

Results

Conclusion

Please log in to get access to this content

Other articles of this Issue 1/2010

Umbilicus, navel, belly button—Vitruvian guide for esthetic cosmetics: a Da Vinci code for beautiful informed consent

Does a laparoscopic approach affect the number of lymph nodes harvested during curative surgery for colorectal cancer?

Support vector machines improve the accuracy of evaluation for the performance of laparoscopic training tasks

Letter in response to: Mazeh H, Greenstein AJ, Swedish K, Nguyen SQ, Lipskar A, Weber KJ, Chin EH, Divino CM (2009) Laparoscopic and open reversal of Hartmann’s procedure—a comparative retrospective analysis (Surg Endosc 23:496–502)

Laparoscopic oesophageal cardiomyotomy without fundoplication in children with achalasia: a 10-year experience

Is BMI greater than 60 kg/m2 a predictor of higher morbidity after laparoscopic Roux-en-Y gastric bypass?