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Published in: Surgical Endoscopy 5/2012

01-05-2012

Oxidants as important determinants of renal apoptosis during pneumoperitoneum: a study in an isolated perfused rat kidney model

Authors: Wisam Khoury, Avi A. Weinbroum

Published in: Surgical Endoscopy | Issue 5/2012

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Abstract

Introduction

Pneumoperitoneum-associated ischemia–reperfusion (IR) may initiate renal dysfunction. Whether oxidants are responsible for renal structural damage, such as cell apoptosis, has not yet been evaluated. We investigated such eventuality in an isolated rat kidney model.

Methods

Thirty-five rat kidneys with their vessels and ureter were harvested and perfused within a closed environment at flow of 15 ml min−1. After stabilization, kidneys were assigned to one of five groups (n = 7 per group): CO2-induced intrachamber pressure of 8, 12, or 0 mmHg (control), and 8 or 12 mmHg pressure applied to kidneys from rats treated pre-experimentally with tungsten for 14 days. Pressurization lasted 60 min.

Results

Organ perfusion pressure raised as intrachamber pressure increased. Urinary output decreased in the two pressurized nonpretreated groups. Intrachamber pressure was directly associated with an increase in postexperimental xanthine oxidase tissue levels. Twofold apoptosis was documented (p < 0.05) in cortex of nonpretreated kidney in the 12 mmHg group compared with the 8 or 0 mmHg groups. Tungsten pretreatment significantly (p < 0.05) attenuated the abnormalities documented in the 12 mmHg group, but less so in the 8 mmHg pressurized nontreated counterparts.

Conclusions

Pneumoperitoneal pressure applied to isolated perfused kidney is associated with renal apoptosis. This rapidly induced structural renal damage is oxidant dependent and can be attenuated by antioxidants. Further studies may shed more light on the role of antioxidants in preventing pneumoperitoneum-induced kidney dysfunction.
Literature
1.
go back to reference 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 43:453–459PubMedCrossRef 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 43:453–459PubMedCrossRef
2.
go back to reference Price HL (1960) Effects of carbon dioxide on the cardiovascular system. Anesthesiology 21:652–663PubMedCrossRef Price HL (1960) Effects of carbon dioxide on the cardiovascular system. Anesthesiology 21:652–663PubMedCrossRef
3.
go back to reference Shimizu T, Tanabe K, Ishida H, Toma H, Yamaguchi Y (2004) Histopathological evaluation of 0-h biopsy specimens of donor kidney procured by laparoscopic donor nephrectomy. Clin Transplant 18(suppl 1):24–28PubMedCrossRef Shimizu T, Tanabe K, Ishida H, Toma H, Yamaguchi Y (2004) Histopathological evaluation of 0-h biopsy specimens of donor kidney procured by laparoscopic donor nephrectomy. Clin Transplant 18(suppl 1):24–28PubMedCrossRef
4.
go back to reference Khoury W, Schreiber L, Szold A, Klausner JM, Wienbroum AA (2009) Renal oxidative stress following CO2 pneumoperitoneum-like conditions. Surg Endosc 23(4):776–782PubMedCrossRef Khoury W, Schreiber L, Szold A, Klausner JM, Wienbroum AA (2009) Renal oxidative stress following CO2 pneumoperitoneum-like conditions. Surg Endosc 23(4):776–782PubMedCrossRef
5.
go back to reference Weinbroum A, Nielsen VG, Tan S, Gelman S, Matalon S, Skinner KA, Bradley E Jr, Parks DA (1995) Liver ischemia-reperfusion increases pulmonary permeability in rats: Role of circulating xanthine oxidase. Am J Physiol 268:G988–G996PubMed Weinbroum A, Nielsen VG, Tan S, Gelman S, Matalon S, Skinner KA, Bradley E Jr, Parks DA (1995) Liver ischemia-reperfusion increases pulmonary permeability in rats: Role of circulating xanthine oxidase. Am J Physiol 268:G988–G996PubMed
6.
go back to reference Marzi I, Buhren V, Schuttler A, Trentz O (1993) Value of superoxide dismutase for prevention of multiple organ failure after multiple traumas. J Trauma 35:110–119PubMedCrossRef Marzi I, Buhren V, Schuttler A, Trentz O (1993) Value of superoxide dismutase for prevention of multiple organ failure after multiple traumas. J Trauma 35:110–119PubMedCrossRef
7.
go back to reference Greene EL, Paller MS (1992) Xanthine oxidase produces O 2 −· in posthypoxic injury of renal epithelial cells. Am J Physiol 263(2 Pt 2):F251–F255PubMed Greene EL, Paller MS (1992) Xanthine oxidase produces O 2 −· in posthypoxic injury of renal epithelial cells. Am J Physiol 263(2 Pt 2):F251–F255PubMed
8.
go back to reference Parks DA, Granger DN (1986) Xanthine oxidase: biochemistry, distribution and physiology. Acta Physiol Scand Suppl 548:87–99 ReviewPubMed Parks DA, Granger DN (1986) Xanthine oxidase: biochemistry, distribution and physiology. Acta Physiol Scand Suppl 548:87–99 ReviewPubMed
9.
go back to reference Parks DA, Granger DN (1986) Contributions of ischemia and reperfusion to mucosal lesion formation. Am J Physiol 250:G749–G753PubMed Parks DA, Granger DN (1986) Contributions of ischemia and reperfusion to mucosal lesion formation. Am J Physiol 250:G749–G753PubMed
10.
go back to reference Terada LS, Guidot DM, Leff JA, Willingham IR, Hanley ME, Piermattei D, Repine JE (1992) Hypoxia injures endothelial cells by increasing endogenous xanthine oxidase activity. Proc Natl Acad Sci USA 89(8):3362–3366PubMedCrossRef Terada LS, Guidot DM, Leff JA, Willingham IR, Hanley ME, Piermattei D, Repine JE (1992) Hypoxia injures endothelial cells by increasing endogenous xanthine oxidase activity. Proc Natl Acad Sci USA 89(8):3362–3366PubMedCrossRef
11.
go back to reference 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 and reperfusion. J Trauma 43:627–633PubMedCrossRef 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 and reperfusion. J Trauma 43:627–633PubMedCrossRef
12.
go back to reference Khoury W, Jakowlev K, Fein A, Orenstein H, Nakache R, Weinbroum AA (2008) Renal apoptosis following carbon dioxide pneumoperitoneum in a rat model. J Urol 180(4):1554–1558PubMedCrossRef Khoury W, Jakowlev K, Fein A, Orenstein H, Nakache R, Weinbroum AA (2008) Renal apoptosis following carbon dioxide pneumoperitoneum in a rat model. J Urol 180(4):1554–1558PubMedCrossRef
13.
go back to reference Cunningham PN, Dyanov HM, Park P, Wang J, Newell KA, Quigg RJ (2002) Acute renal failure in endotoxemia is caused by TNF acting directly on TNF receptor-1 in kidney. J Immunol 168:5817–5823PubMed Cunningham PN, Dyanov HM, Park P, Wang J, Newell KA, Quigg RJ (2002) Acute renal failure in endotoxemia is caused by TNF acting directly on TNF receptor-1 in kidney. J Immunol 168:5817–5823PubMed
14.
go back to reference Wan L, Bellomo R, Di Giantomasso D, Ronco C (2002) The pathogenesis of septic acute renal failure. Curr Opin Crit Care 9:496–502CrossRef Wan L, Bellomo R, Di Giantomasso D, Ronco C (2002) The pathogenesis of septic acute renal failure. Curr Opin Crit Care 9:496–502CrossRef
15.
go back to reference Glynne PA, Evans TJ (1999) Inflammatory cytokines induce apoptotic and necrotic cell shedding from human proximal tubular epithelial cell monolayers. Kidney Int 55:2573–2597PubMedCrossRef Glynne PA, Evans TJ (1999) Inflammatory cytokines induce apoptotic and necrotic cell shedding from human proximal tubular epithelial cell monolayers. Kidney Int 55:2573–2597PubMedCrossRef
16.
go back to reference Jo SK, Cha DR, Cho WY, Kim HK, Chang KH, Yun SY, Won NH (2002) Inflammatory cytokines and lipopolysaccharide induce Fas-mediated apoptosis in renal tubular cells. Nephron 91:406–415PubMedCrossRef Jo SK, Cha DR, Cho WY, Kim HK, Chang KH, Yun SY, Won NH (2002) Inflammatory cytokines and lipopolysaccharide induce Fas-mediated apoptosis in renal tubular cells. Nephron 91:406–415PubMedCrossRef
17.
go back to reference Zhang M, Zhou M, Van Etten RL, Stauffacher CV (1997) Crystal structure of bovine low molecular weight phosphotyrosyl phosphatase complexed with the transition state analog vanadate. Biochemistry 36(1):15–23PubMedCrossRef Zhang M, Zhou M, Van Etten RL, Stauffacher CV (1997) Crystal structure of bovine low molecular weight phosphotyrosyl phosphatase complexed with the transition state analog vanadate. Biochemistry 36(1):15–23PubMedCrossRef
18.
go back to reference Nam HJ, Poy F, Saito H, Frederick CA (2005) Structural basis for the function and regulation of the receptor protein tyrosine phosphatase CD45. J Exp Med 201(3):441–452PubMedCrossRef Nam HJ, Poy F, Saito H, Frederick CA (2005) Structural basis for the function and regulation of the receptor protein tyrosine phosphatase CD45. J Exp Med 201(3):441–452PubMedCrossRef
19.
go back to reference Uskoković-Marković S, Milenković M, Topić A, Topić A, Kotur-Stevuljević J, Stefanović A, Antić-Stanković J (2007) Protective effects of tungstophosphoric acid and sodium tungstate on chemically induced liver necrosis in wistar rats. J Pharm Pharm Sci 10(3):340–349PubMed Uskoković-Marković S, Milenković M, Topić A, Topić A, Kotur-Stevuljević J, Stefanović A, Antić-Stanković J (2007) Protective effects of tungstophosphoric acid and sodium tungstate on chemically induced liver necrosis in wistar rats. J Pharm Pharm Sci 10(3):340–349PubMed
20.
go back to reference Avital S, Itah 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):50–54PubMedCrossRef Avital S, Itah 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):50–54PubMedCrossRef
21.
go back to reference Flaishon R, Szold O, Weinbroum AA (2006) Acute lung injury following pancreas ischaemia-reperfusion: role of xanthine oxidase. Eur J Clin Invest 36(11):831–837PubMedCrossRef Flaishon R, Szold O, Weinbroum AA (2006) Acute lung injury following pancreas ischaemia-reperfusion: role of xanthine oxidase. Eur J Clin Invest 36(11):831–837PubMedCrossRef
22.
go back to reference Tamion F, Richard V, Lacoume Y, Thuillez C (2002) Intestinal preconditioning prevents systemic inflammatory response in hemorrhagic shock. Role of HO-1. Am J Physiol Gastrointest Liver Physiol 283:G408–G414PubMed Tamion F, Richard V, Lacoume Y, Thuillez C (2002) Intestinal preconditioning prevents systemic inflammatory response in hemorrhagic shock. Role of HO-1. Am J Physiol Gastrointest Liver Physiol 283:G408–G414PubMed
23.
go back to reference Hashimoto S (1974) A new spectrophotometric assay method of xanthine oxidase in crude tissue homogenate. Anal Biochem 62:426–435PubMedCrossRef Hashimoto S (1974) A new spectrophotometric assay method of xanthine oxidase in crude tissue homogenate. Anal Biochem 62:426–435PubMedCrossRef
24.
go back to reference Cotgreave IA, Grafstro¨m RC, Moldeus P (1986) Modulation of pneumotoxicity by cellular glutathione and precursors. Bill Rur Physiopathol Respir 22:263s–266s Cotgreave IA, Grafstro¨m RC, Moldeus P (1986) Modulation of pneumotoxicity by cellular glutathione and precursors. Bill Rur Physiopathol Respir 22:263s–266s
25.
go back to reference Jain A, Martensson J, Stole E, Auld PA, Meister A (1991) Glutathione deficiency leads to mitochondrial damage in brain. Proc Natl Acad Sci USA 88:1913–1917PubMedCrossRef Jain A, Martensson J, Stole E, Auld PA, Meister A (1991) Glutathione deficiency leads to mitochondrial damage in brain. Proc Natl Acad Sci USA 88:1913–1917PubMedCrossRef
26.
go back to reference Akbulut G, Polat C, Aktepe F, Yilmaz S, Kahraman A, Serteser M, Gökçe C, Gökçe O (2004) The oxidative effect of prolonged CO2 pneumoperitoneum on renal tissue of rats. Surg Endosc 18:1384–1388PubMedCrossRef Akbulut G, Polat C, Aktepe F, Yilmaz S, Kahraman A, Serteser M, Gökçe C, Gökçe O (2004) The oxidative effect of prolonged CO2 pneumoperitoneum on renal tissue of rats. Surg Endosc 18:1384–1388PubMedCrossRef
27.
go back to reference Victorino GP, Ramirez RM, Chong TJ, Curran B, Sadjadi J (2008) Ischemia-reperfusion injury in rats affects hydraulic conductivity in two phases that are temporally and mechanistically separate. Am J Physiol Heart Circ Physiol 295(5):H2164–H2171PubMedCrossRef Victorino GP, Ramirez RM, Chong TJ, Curran B, Sadjadi J (2008) Ischemia-reperfusion injury in rats affects hydraulic conductivity in two phases that are temporally and mechanistically separate. Am J Physiol Heart Circ Physiol 295(5):H2164–H2171PubMedCrossRef
28.
go back to reference Khoury W, Szold A, Klausner JM, Weinbroum AA (2008) The hemodynamic effects of CO2-induced pressure on the kidney in an isolated perfused rat kidney model. Surg Laparosc Endosc Percutan Tech 18(6):573–578PubMedCrossRef Khoury W, Szold A, Klausner JM, Weinbroum AA (2008) The hemodynamic effects of CO2-induced pressure on the kidney in an isolated perfused rat kidney model. Surg Laparosc Endosc Percutan Tech 18(6):573–578PubMedCrossRef
29.
go back to reference Weinbroum AA, Rudick V, Ben-Abraham R, Karchevski E (2000) N-acetyl-l-cysteine for preventing lung reperfusion injury after liver ischemia-reperfusion: a possible dual protective mechanism in a dose-response study. Transplantation 69(5):853–859PubMedCrossRef Weinbroum AA, Rudick V, Ben-Abraham R, Karchevski E (2000) N-acetyl-l-cysteine for preventing lung reperfusion injury after liver ischemia-reperfusion: a possible dual protective mechanism in a dose-response study. Transplantation 69(5):853–859PubMedCrossRef
30.
go back to reference 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(5):1439–1444PubMedCrossRef 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(5):1439–1444PubMedCrossRef
31.
go back to reference Beeri R, Symon Z, Brezis M, Ben-Sasson SA, Baehr PH, Rosen S, Zager RA (1995) Rapid DNA fragmentation from hypoxia along the thick ascending limb of rat kidneys. Kidney Int 47:1806–1810PubMedCrossRef Beeri R, Symon Z, Brezis M, Ben-Sasson SA, Baehr PH, Rosen S, Zager RA (1995) Rapid DNA fragmentation from hypoxia along the thick ascending limb of rat kidneys. Kidney Int 47:1806–1810PubMedCrossRef
32.
go back to reference Chien CT, Lee PH, Chen CF, Ma MC, Lai MK, Hsu SM (2001) De novo demonstration and co-localization of free-radical production and apoptosis formation in rat kidney subjected to ischemia/reperfusion. J Am Soc Nephrol 12:973–982PubMed Chien CT, Lee PH, Chen CF, Ma MC, Lai MK, Hsu SM (2001) De novo demonstration and co-localization of free-radical production and apoptosis formation in rat kidney subjected to ischemia/reperfusion. J Am Soc Nephrol 12:973–982PubMed
33.
go back to reference Khoury W, Namnesnikov M, Fedorov D, Abu-Ghazala S, Weinbroum AA (2010) Mannitol attenuates kidney damage induced by xanthine oxidase-associated pancreas ischemia-reperfusion. J Surg Res 160(1):163–167PubMedCrossRef Khoury W, Namnesnikov M, Fedorov D, Abu-Ghazala S, Weinbroum AA (2010) Mannitol attenuates kidney damage induced by xanthine oxidase-associated pancreas ischemia-reperfusion. J Surg Res 160(1):163–167PubMedCrossRef
34.
go back to reference Weinbroum AA, Dembo G, Hochhauser E, Rudick V, Vidne BA (2001) External pacing does not potentiate allopurinol protection of the heart from liver ischemia-reperfusion–a study in an isolated perfused liver-heart rat model. Med Sci Monit 7(6):1145–1152PubMed Weinbroum AA, Dembo G, Hochhauser E, Rudick V, Vidne BA (2001) External pacing does not potentiate allopurinol protection of the heart from liver ischemia-reperfusion–a study in an isolated perfused liver-heart rat model. Med Sci Monit 7(6):1145–1152PubMed
35.
go back to reference Wolfs TG, de Vries B, Walter SJ, Peutz-Kootstra CJ, van Heurn LW, Oosterhof GO, Buurman WA (2005) Apoptotic cell death is initiated during normothermic ischemia in human kidneys. Am J Transplant 5(1):68–75PubMedCrossRef Wolfs TG, de Vries B, Walter SJ, Peutz-Kootstra CJ, van Heurn LW, Oosterhof GO, Buurman WA (2005) Apoptotic cell death is initiated during normothermic ischemia in human kidneys. Am J Transplant 5(1):68–75PubMedCrossRef
36.
go back to reference Genescà M, Sola A, Hotter G (2006) Actin cytoskeleton derangement induces apoptosis in renal ischemia/reperfusion. Apoptosis 11(4):563–571PubMedCrossRef Genescà M, Sola A, Hotter G (2006) Actin cytoskeleton derangement induces apoptosis in renal ischemia/reperfusion. Apoptosis 11(4):563–571PubMedCrossRef
37.
go back to reference Brasile L, Stubenitsky B, Haisch CE, Kon M, Kootstra G (2005) Potential of repairing ischemically damaged kidneys ex vivo. Transplant Proc 37(1):375–376PubMedCrossRef Brasile L, Stubenitsky B, Haisch CE, Kon M, Kootstra G (2005) Potential of repairing ischemically damaged kidneys ex vivo. Transplant Proc 37(1):375–376PubMedCrossRef
38.
go back to reference 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(3):351–357PubMed 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(3):351–357PubMed
39.
go back to reference 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(4):824–829PubMedCrossRef 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(4):824–829PubMedCrossRef
40.
go back to reference Levin RL, Degrange MA, Bruno GF, Del Mazo CD, Taborda DJ, Griotti JJ, Boullon FJ (2004) Methylene blue reduces mortality and morbidity in vasoplegic patients after cardiac surgery. Ann Thorac Surg 77(2):496–499PubMedCrossRef Levin RL, Degrange MA, Bruno GF, Del Mazo CD, Taborda DJ, Griotti JJ, Boullon FJ (2004) Methylene blue reduces mortality and morbidity in vasoplegic patients after cardiac surgery. Ann Thorac Surg 77(2):496–499PubMedCrossRef
41.
go back to reference Hazebroek EJ, Gommers D, Schreve MA, van Gelder T, Roodnat JI, Weimar W, Bonjer HJ, IJzermans JN (2002) Impact of intraoperative donor management on short-term renal function after laparoscopic donor nephrectomy. Ann Surg 236(1):127–132PubMedCrossRef Hazebroek EJ, Gommers D, Schreve MA, van Gelder T, Roodnat JI, Weimar W, Bonjer HJ, IJzermans JN (2002) Impact of intraoperative donor management on short-term renal function after laparoscopic donor nephrectomy. Ann Surg 236(1):127–132PubMedCrossRef
Metadata
Title
Oxidants as important determinants of renal apoptosis during pneumoperitoneum: a study in an isolated perfused rat kidney model
Authors
Wisam Khoury
Avi A. Weinbroum
Publication date
01-05-2012
Publisher
Springer-Verlag
Published in
Surgical Endoscopy / Issue 5/2012
Print ISSN: 0930-2794
Electronic ISSN: 1432-2218
DOI
https://doi.org/10.1007/s00464-011-2049-7

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