Skip to main content
SpringerLink
Log in

Renal oxidative stress following CO2 pneumoperitoneum-like conditions

  • Published:
Surgical Endoscopy Aims and scope Submit manuscript

Abstract

Background

Physiologic renal changes associated with pneumoperitoneum (PNP) have been described and various underlying mechanisms have been suggested. We investigated the possibility that PNP-associated renal damage is pressure dependent, and that oxidative stress is thereby involved.

Materials and methods

Seventy Wistar rat kidneys (n = 10 per group) were isolated. They were perfused with oxygenated, warm, Krebs–Henseleit solution containing 5% albumin within an isolated environment and subjected to various CO2 pressures (0 [control], 3, 5, 8, 12, 15, and 18 mmHg) for 60 min. Half of each group was additionally perfused for 30 min at 0 mmHg pressure.

Results

Renal flow decreased proportionately to the applied pressure as did urine output: both decreased (P < 0.05) after 60 and 90 min when pressure ≥8 mmHg was applied. Oxygen extraction decreased (P < 0.05) during PNP in all pressurized groups. Xanthine oxidase (XO) activity and reduced glutathione in the tissues increased (P < 0.05) proportionately to pressures ≥8 mmHg. All parameters slightly reversed toward baseline values, upon the release of the intra-chamber pressure, except for the 18 mmHg group’s values.

Conclusions

CO2-PNP pressure induces kidney injury, possibly reversible immediately after pressure is annulled. Pressure is associated with oxidative stress, which interferes with cellular metabolism and function, possibly via an ischemic-reperfusion-like mechanism.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Schachtrupp A, Toens Ch, Hoer J, Klosterhalfen B, Lawong AG, Schumpelick V (2002) A 24-h pneumoperitoneum leads to multiple organ impairment in a porcine model. J Surg Res 106:37–45

    Article  PubMed  CAS  Google Scholar 

  2. Hazebroek EJ, de Bruin RW, Bouvy ND, Marquet RL, Bonthuis F, Bajema IM, Hayes DP, Ijzermans JN, Bonjer HJ (2003) Long-term impact of pneumoperitoneum used for laparoscopic donor nephrectomy on renal function and histomorphology in donor and recipient rats. Ann Surg 237:351–357

    Article  PubMed  Google Scholar 

  3. Horvath KD, Whelan RL, Lier B, Viscomi S, Barry L, Buck K, Bessler M (1998) The effects of elevated intraabdominal pressure, hypercarbia, and positioning on the hemodynamic responses to laparoscopic colectomy in pigs. Surg Endosc 12:107–114

    Article  PubMed  CAS  Google Scholar 

  4. Koivusalo AM, Kellokumpu I, Scheinin M, Tikkanen I, Halme L, Lindgren L (1996) Randomized comparison of the neuroendocrine response to laparoscopic cholecystectomy using either conventional or abdominal wall lift techniques. Br J Surg 83:1532–1536

    Article  PubMed  CAS  Google Scholar 

  5. Pérez J, Taurá P, Rueda J, Balust J, Anglada T, Beltran J, Lacy AM, Garcia-Valdecasas JC (2002) Role of dopamine in renal dysfunction during laparoscopic surgery. Surg Endosc 16:1297–1301

    Article  PubMed  Google Scholar 

  6. McDougall EM, Monk TG, Wolf JS Jr, Hicks M, Clayman RV, Gardner S, Humphrey PA, Sharp T, Martin K (1996) The effect of prolonged pneumoperitoneum on renal function in an animal model. J Am Coll Surg 182:317–328

    PubMed  CAS  Google Scholar 

  7. Kirsch AJ, Hensle TW, Chang DT, Kayton ML, Olsson CA, Sawczuk IS (1994) Renal effects of CO2 insufflation: oliguria and acute renal dysfunction in a rat pneumoperitoneum model. Urology 43:453–459

    Article  PubMed  CAS  Google Scholar 

  8. Ortega AE, Peters JH, Incarbone R, Estrada L, Ehsan A, Kwan Y, Spencer CJ, Moore-Jeffries E, Kuchta K, Nicoloff JT (1996) A prospective randomized comparison of the metabolic and stress hormonal responses of laparoscopic and open cholecystectomy. J Am Coll Surg 183:249–256

    PubMed  CAS  Google Scholar 

  9. Hazebroek EJ, de Vos tot Nederveen Cappel R, Gommers D, van Gelder T, Weimar W, Steyerberg EW, Bonjer HJ, IJzermans JN (2002) Antidiuretic hormone release during laparoscopic donor nephrectomy. Arch Surg 137:600–604; discussion 605

    Article  PubMed  CAS  Google Scholar 

  10. Price HL (1960) Effects of carbon dioxide on the cardiovascular system. Anesthesiology 21:652–663

    Article  PubMed  CAS  Google Scholar 

  11. Koivusalo AM, Scheinin M, Tikkanen I, Yli-Suomu T, Ristkari S, Laakso J, Lindgren L (1998) Effects of esmolol on haemodynamic response to CO2 pneumoperitoneum for laparoscopic surgery. Acta Anaesthesiol Scand 42:510–517

    Article  PubMed  CAS  Google Scholar 

  12. Micali S, Silver RI, Kaufman HS, Douglas VD, Marley GM, Partin AW, Moore RG, Kavoussi LR, Docimo SG (1999) Measurement of urinary N-acetyl-beta-D-glucosaminidase to assess renal ischemia during laparoscopic operations. Surg Endosc 13:503–506

    Article  PubMed  CAS  Google Scholar 

  13. London ET, Ho HS, Neuhaus AM, Wolfe BM, Rudich SM, Perez RV (2000) Effect of intravascular volume expansion on renal function during prolonged CO2 pneumoperitoneum. Ann Surg 231:195–201

    Article  PubMed  CAS  Google Scholar 

  14. Nogueira JM, Cangro CB, Fink JC, Schweitzer E, Wiland A, Klassen DK, Gardner J, Flowers J, Jacobs S, Cho E, Philosophe B, Bartlett ST, Weir MR (1999) A comparison of recipient renal outcomes with laparoscopic versus open live donor nephrectomy. Transplantation 67:722–728

    Article  PubMed  CAS  Google Scholar 

  15. Flowers JL, Jacobs S, Cho E, Morton A, Rosenberger WF, Evans D, Imbembo AL, Bartlett ST (1997) Comparison of open and laparoscopic live donor nephrectomy. Ann Surg 226:483–9 discussion 489–490

    Article  PubMed  CAS  Google Scholar 

  16. 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  PubMed  CAS  Google Scholar 

  17. Hashimoto S (1974) A new spectrophotometric assay method of xanthine oxidase in crude tissue homogenate. Anal Biochem 62:426–435

    Article  PubMed  CAS  Google Scholar 

  18. Parks DA, Williams TK, Beckman JS (1998) Conversion of xanthine dehydrogenase to oxidase in ischemic rat intestine: a reevaluation. Am J Physiol 254:768–774

    Google Scholar 

  19. Tan S, Yokoyama Y, Dickens E, Cash TG, Freeman BA, Parks DA (1993) Xanthine oxidase activity in the circulation of rats following hemorrhagic shock. Free Radic Biol Med 15:407–414

    Article  PubMed  CAS  Google Scholar 

  20. Aranda R, Doménech E, Rus AD, Real JT, Sastre J, Viña J, Pallardó FV (2007) Age-related increase in xanthine oxidase activity in human plasma and rat tissues. Free Radic Res Sep 28:1–6 [Epub ahead of print]

    Google Scholar 

  21. Cotgreave IA, Grafström RC, Moldeus P (1986) Modulation of pneumotoxicity by cellular glutathione and precursors. Bill Rur Physiopathol Respir 22:263s–266s

    CAS  Google Scholar 

  22. Jain A, Martensson J, Stole E, Auld PA, Meister A (1991) Glutathione deficiency leads to mitochondrial damage in brain. Proc Natl Acad Sci USA 88:1913–1917

    Article  PubMed  CAS  Google Scholar 

  23. Weinbroum A, Nielsen VG, Gelman S, Tan S, Matalon S, Skinner KA, Bradley E Jr, Parks DA (1995) Liver ischemia-reperfusion increases pulmonary permeability in rat: role of circulating xanthine oxidase. Am J Physiol 268(6 Pt 1):G988–G996

    PubMed  CAS  Google Scholar 

  24. Gelman S (1995) The pathophysiology of aortic cross-clamping and unclamping. Anesthesiology 82:1026–1060

    Article  PubMed  CAS  Google Scholar 

  25. Szold A, Weinbroum AA (2008) Carbon dioxide pneumoperitoneum-related liver injury is pressure dependent: a study in an isolated-perfused organ model. Surg Endosc 22:365–371

    Article  PubMed  Google Scholar 

  26. Nakache R, Rudick V, Fiodorov D, Klausner JM, Almogy N, Karckevski E, Weinbroum AA (1999) Cumulative damaging effect of liver hypoperfusion and cyclosporine A on the peribiliary capillary plexus: a study in an isolated dually perfused rat model. Transplantation 68:1651–1660

    Article  PubMed  CAS  Google Scholar 

  27. Nakache R, Isretil I, Ekstein P, Almogy N, Fedorov D, Lifschitz-Mercer B, Weinbroum AA (2007) Nontoxic effect of tacrolimus on normally perfused isolated liver and protective effect on hypoperfused liver. Med Sci Monit 13:BR32–BR39

    PubMed  CAS  Google Scholar 

  28. Weinbroum AA, Hochhauser E, Rudick V, Kluger Y, Karchevsky E, Vidne BA (1999) Multiple organ dysfunction following remote circulatory arrest: common pathway of radical oxygen species? J Trauma 47:691–698

    Article  PubMed  CAS  Google Scholar 

  29. Friedl HP, Smith DJ, Till GO, Thomson PD, Louis DS, Ward PA (1990) Ischemia-reperfusion in humans. Appearance of xanthine oxidase activity. Am J Pathol 136:491–495

    PubMed  CAS  Google Scholar 

  30. Nielsen VG, Weinbroum A, Tan S, Samuelson PN, Gelman S, Parks DA (1994) Xanthine oxidoreductase release after descending thoracic aorta occlusion and reperfusion in rabbits. J Thorac Cardiovasc Surg 107:1222–1227

    PubMed  CAS  Google Scholar 

  31. Nielsen VG, Tan S, Baird MS, McCammon AT, Parks DA (1996) Gastric intramucosal pH and multiple organ injury: impact of ischemia-reperfusion and xanthine oxidase. Crit Care Med 24:1339–1344

    Article  PubMed  CAS  Google Scholar 

  32. Nielsen VG, Tan S, Baird MS, Samuelson PN, McCammon AT, Parks DA (1997) Xanthine oxidase mediates myocardial injury after hepatoenteric ischemia-reperfusion. Crit Care Med 25:1044–1050

    Article  PubMed  CAS  Google Scholar 

  33. O’Leary AM, Veall G, Butler P, Anderson GH (1990) Acute pulmonary oedema after tourniquet release. Can J Anaesth 37:826–827

    PubMed  CAS  Google Scholar 

  34. Tan S, Gelman S, Wheat JK, Parks DA (1995) Circulating xanthine oxidase in human ischemia reperfusion. South Med J 88:479–482

    PubMed  CAS  Google Scholar 

  35. Weinbroum A, Goldman G, Hag M, Hazam A, Marmour S, Sorkine P, Rudick V, Klausner JM (1997) Bowel ischemia/reperfusion-induced liver and lung injury: role of eicosanoids and oxygen free radicals. Med Sci Monit 5:624–630

    Google Scholar 

  36. Weinbroum AA, Hochhauser E, Rudick V, Kluger Y, Sorkine P, Karchevsky E, Graf E, Boher P, Flaishon R, Fjodorov D, Niv D, Vidne BA (1997) Direct induction of acute lung and myocardial dysfunction by liver ischemia-reperfusion. J Trauma 43:627–635

    Article  PubMed  CAS  Google Scholar 

  37. Neglen P, Jabs CM, Eklof B (1989) Plasma metabolic disturbances and reperfusion injury following partial limb ischaemia in man. Eur J Vasc Surg 3:165–172

    Article  PubMed  CAS  Google Scholar 

  38. Huval WV, Lelcuk S, Allen PD, Mannick JA, Shepro D, Hechtman HB (1984) Determinants of cardiovascular stability during abdominal aortic aneurysmectomy (AAA). Ann Surg 199:216–222

    Article  PubMed  CAS  Google Scholar 

  39. Cross CE, Halliwell B, Borish ET, Pryor WA, Ames BN, Saul RL, McCord JM, Harman D (1987) Oxygen radicals and human disease [clinical conference]. Ann Intern Med 107:526–545

    PubMed  CAS  Google Scholar 

  40. McCord JM (1985) Oxygen-derived free radicals in postischemic tissue injury. N Engl J Med 312:159–163

    PubMed  CAS  Google Scholar 

  41. Koelzow H, Gedney JA, Baumann J, Snook NJ, Bellamy MC (2002) The effect of methylene blue on the hemodynamic changes during ischemia reperfusion injury in orthotopic liver transplantation. Anesth Analg 94:824–829

    Article  PubMed  CAS  Google Scholar 

  42. Giler S, Sperling O, Brosh S, Urca I, De Vries A (1975) Serum xanthine oxidase in jaundice. Clin Chim Acta 63:37–40

    Article  PubMed  CAS  Google Scholar 

  43. Weinbroum AA, Kluger Y, Rudick V (2000) Impairment of aortal tone by no flow-reflow conditions and its partial amelioration by mannitol. Ann Thorac Surg 69:1439–1444

    Article  PubMed  CAS  Google Scholar 

  44. Hazebroek EJ, de Bruin RW, Bouvy ND, van Duikeren S, Bonthuis F, Marquet RL, Bajema IM, Hayes DP, IJzermans JN, Bonjer HJ (2002) Short-term impact of carbon dioxide, helium, and gasless laparoscopic donor nephrectomy on renal function and histomorphology in donor and recipient. Surg Endosc 16:245–251

    Article  PubMed  CAS  Google Scholar 

  45. Lee BR, Cadeddu JA, Molnar-Nadasdy G, Enriquez D, Nadasdy T, Kavoussi LR, Ratner LE (1999) Chronic effect of pneumoperitoneum on renal histology. J Endourol 13:279–282

    Article  PubMed  CAS  Google Scholar 

  46. Avital S, Inbar R, Ben-Abraham R, Szomstein S, Rosenthal R, Sckornik Y, Weinbroum AA (2007) Effect of small bowel perforation during laparoscopy on end-tidal carbon dioxide: observation in a small animal model. J Surg Res 143:368–371

    Article  PubMed  Google Scholar 

  47. Blobner M, Bogdanski R, Kochs E, Henke J, Findeis A, Jelen-Esselborn S (1998) Effects of intraabdominally insufflated carbon dioxide and elevated intraabdominal pressure on splanchnic circulation: an experimental study in pigs. Anesthesiology 89:475–482

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Division of General Surgery B, Tel Aviv Sourasky Medical Center and the Sackler Faculty of Medicine, Tel-Aviv University, Tel Aviv, Israel

    Wisam Khoury, Amir Szold & Joseph M. Klausner

  2. Department of Pathology and Animal Research Laboratory, Tel Aviv Sourasky Medical Center and the Sackler Faculty of Medicine, Tel-Aviv University, Tel Aviv, Israel

    Letizia Schreiber

  3. Post-Anesthesia Care Unit and Animal Research Laboratory, Tel Aviv Sourasky Medical Center, 6 Weizman Street, Tel Aviv, 64239, Israel

    Avi A. Wienbroum

Authors
  1. Wisam Khoury
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Letizia Schreiber
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Amir Szold
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Joseph M. Klausner
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Avi A. Wienbroum
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Avi A. Wienbroum.

Additional information

This paper was presented in part in the 15th EAES, July 2007, Athens, Greece.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Khoury, W., Schreiber, L., Szold, A. et al. Renal oxidative stress following CO2 pneumoperitoneum-like conditions. Surg Endosc 23, 776–782 (2009). https://doi.org/10.1007/s00464-008-0054-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00464-008-0054-2

Keywords

Search

Navigation