Abstract
Background
Previously, the authors demonstrated that an intraabdominal pressure (IAP) of 14 mmHg in normal rats reduced kidney function/hemodynamics. These adverse effects are related to interference with the nitric oxide (NO) system. This study was designed to compare the effects of NO synthase (NOS) inhibition on kidney function/hemodynamics during increases in IAP from 0 mmHg to 7, 10, and 14 mmHg.
Methods
The rats were divided into six groups. After an IAP of 0 (baseline), the first three groups were subjected to increasing IAPs as follows: 7 mmHg (group 1), 10 mmHg (group 2), and 14 mmHg (group 3). Each pressure was applied for 1 h, followed by a deflation period of 60 min (recovery). An additional three groups were pretreated with nitro-l-arginine methyl ester (l-NAME), an NOS inhibitor, before pressures of 7 mmHg (group 4), 10 mmHg (group 5) and 14 mmHg (group 6) were applied for 1 h. Urine flow rate (V), Na+ excretion (UNaV), glomerular filtration rate (GFR), and renal plasma flow (RPF), were determined throughout the experiments.
Results
There were no significant changes in V, UNaV, GFR, or RPF during 7-mmHg insufflation. However, significant reductions in these parameters were observed during 10 and 14 mmHg, with V decreasing from 9.95 ± 1.34 μl/min to 6.8 ± 1.1 and 6.1 ± 0.5 μl/min (p < 0.05) and UNaV decreasing from 1.29 ± 0.28 to 0.43 ± 0.32 μEq/min (p < 0.05), and 0.39 ± 0.09 μEq/min (p < 0.05). These alterations in excretory functions were associated with considerable declines in GFR, from 1.98 ± 0.2 to 1.05 ± 0.18 ml/min (p < 0.05) and 0.95 ± 0.06 ml/min (p < 0.05) and RPF from 8.66 ± 0.62 to 3.94 ± 0.88 ml/min (p < 0.05) and 3.08 ± 0.71 ml/min (p < 0.05), respectively. When the animals were pretreated with l-NAME, the adverse renal effects of an IAP of 14 mmHg, but not 10 mmHg, were substantially aggravated.
Conclusion
Decreased renal function/perfusion is induced by IAP pressures of 10 and 14 mmHg but not 7 mmHg. Inhibition of NOS aggravates the adverse renal effects of high (14 mmHg) but not low (7 or 10 mmHg) IAP, indicating that NO deficiency may contribute to the renal dysfunction during high IAP.
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References
Demyttenaere S, Feldman LS, Fried GM (2007) Effect of pneumoperitoneum on renal perfusion and function: a systematic review. Surg Endosc 21:152–160
Ratner LE, Hiller J, Sroka M, Weber R, Sikorsky I, Montgomery RA, Kavoussi LR (1997) Laparoscopic live donor nephrectomy removes disincentives to live donation. Transplant Proc 29:3402–3403
Chang DT, Kirsch AJ, Sawczuk IS (1994) Oliguria during laparoscopic surgery. J Endourol 8:349–352
Nishio S, Takeda H, Yokoyama M (1999) Changes in urinary output during laparoscopic adrenalectomy. BJU Int 83:944–947
Richards WO, Scovill W, Shin B, Reed W (1983) Acute renal failure associated with increased intraabdominal pressure. Ann Surg 197:183–187
Harman PK, Kron IL, McLachlan HD, Freedlender AE, Nolan SP (1982) Elevated intraabdominal pressure and renal function. Ann Surg 196:594–597
Chiu AW, Azadzoi KM, Hatzichristou DG, Siroky MB, Krane RJ, Babayan RK (1994) Effects of intraabdominal pressure on renal tissue perfusion during laparoscopy. J Endourol 8:99–103
Chiu AW, Chang LS, Birkett DH, Babayan RK (1996) A porcine model for renal hemodynamic study during laparoscopy. J Surg Res 60:61–68
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
Junghans T, Bohm B, Grundel K, Schwenk W, Muller JM (1997) Does pneumoperitoneum with different gases, body positions, and intraperitoneal pressures influence renal and hepatic blood flow? Surgery 121:206–211
Lindberg F, Bergqvist D, Bjorck M, Rasmussen I (2003) Renal hemodynamics during carbon dioxide pneumoperitoneum: an experimental study in pigs. Surg Endosc 17:480–484
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
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
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
Ho HS, Saunders CJ, Gunther RA, Wolfe BM (1995) Effector of hemodynamics during laparoscopy: CO2 absorption or intraabdominal pressure? J Surg Res 59:497–503
Zacherl J, Thein E, Stangl M, Feussner H, Bock S, Mittlbock M, Erhardt W, Siewert JR (2003) The influence of periarterial papaverine application on intraoperative renal function and blood flow during laparoscopic donor nephrectomy in a pig model. Surg Endosc 17:1231–1236
Hamilton BD, Chow GK, Inman SR, Stowe NT, Winfield HN (1998) Increased intraabdominal pressure during pneumoperitoneum stimulates endothelin release in a canine model. J Endourol 12:193–197
Ambrose JA, Onders RP, Stowe NT, Simonson MS, Robinson AV, Wilhelm S, Schulak JA (2001) Pneumoperitoneum upregulates preproendothelin-1 messenger RNA. Surg Endosc 15:183–188
Gudmundsson FF, Viste A, Myking OL, Bostad L, Grong K, Svanes K (2003) Role of angiotensin II under prolonged increased intraabdominal pressure (IAP) in pigs. Surg Endosc 17:1092–1097
Joris JL, Chiche JD, Canivet JL, Jacquet NJ, Legros JJ, Lamy ML (1998) Hemodynamic changes induced by laparoscopy and their endocrine correlates: effects of clonidine. J Am Coll Cardiol 32:1389–1396
Nguyen NT, Perez RV, Fleming N, Rivers R, Wolfe BM (2002) Effect of prolonged pneumoperitoneum on intraoperative urine output during laparoscopic gastric bypass. J Am Coll Surg 195:476–483
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
Borba MR, Lopes RI, Carmona M, Neto BM, Nahas SC, Pereira PR (2005) Effects of enalaprilat on the renin–angiotensin–aldosterone system and on renal function during CO2 pneumoperitoneum. J Endourol 8:1026–1031
Lindström P, Wadström J, Ollerstam A, Johnsson C, Persson AE (2003) Effects of increased intraabdominal pressure and volume expansion on renal function in the rat. Nephrol Dial Transplant 18:2269–2277
Yilmaz S, Koken T, Tokyol C, Kahraman A, Akbulut G, Serteser M, Polat C, Gokce C, Gokce O (2003) Can preconditioning reduce laparoscopy-induced tissue injury? Surg Endosc 17:819–824
Kone BC (2004) Nitric oxide synthesis in the kidney: isoforms, biosynthesis, and functions in health. Semin Nephrol 4:299–315
Lahera V, Salom MG, Miranda-Guardiola F, Moncada S, Romero JC (1991) Effects of NG-nitro-l-arginine methyl ester on renal function and blood pressure. Am J Physiol 261:F1033–F1037
Mattson DL, Roman RJ, Cowley AW Jr (1992) Role of nitric oxide in renal papillary blood flow and sodium excretion. Hypertension 19:766–769
Moncada S, Palmer RM, Higgs EA (1991) Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol Rev 43:109–142
Abassi Z, Bishara B, Karram T, Khatib S, Winaver J, Hoffman A (2008) Adverse effects of pneumoperitoneum on renal function: involvement of the endothelin and nitric oxide systems. Am J Physiol Regul Integr Comp Physiol 294:842–850
Bishara B, Karram T, Khatib S, Ramadan R, Schwartz H, Hoffman A, Abassi Z (2009) Impact of pneumoperitoneum on renal perfusion and excretory function: beneficial effects of nitroglycerin. Surg Endosc 23:568–576
Brodsky S, Gurbanov K, Abassi Z, Hoffman A, Ruffolo RR Jr, Feuerstein GZ, Winaver J (1998) Effects of eprosartan on renal function and cardiac hypertrophy in rats with experimental heart failure. Hypertension 32:746–752
Smith HW, Finkelstein N, Aliminosa L (1945) The renal clearances of substituted hippuric acid derivatives and other aromatic acids in dogs and men. J Clin Invest 24:388–404
Cisek LJ, Gobet RM, Peters CA (1998) Pneumoperitoneum produces reversible renal dysfunction in animals with normal and chronically reduced renal function. J Endourol 2:95–100
Mertens zur Borg IR, Lim A, Verbrugge SJ, IJzermans JN, Klein J (2004) Effect of intraabdominal pressure elevation and positioning on hemodynamic responses during carbon dioxide pneumoperitoneum for laparoscopic donor nephrectomy: a prospective controlled clinical study. Surg Endosc 18:919–923
Hawasli A, Oh H, Schervish E, Frontera R, Gonsherova I, Khoury H (2003) The effect of pneumoperitoneum on kidney function in laparoscopic donor nephrectomy. Am Surg 69:300–303
Kohan DE, Hughes AK, Perkins SP (1992) Characterization of endothelin receptors in the inner medullary collecting duct of the rat. J Biol Chem 267:12336–12340
Kohzuki M, Johnston CI, Chai SY, Casley DJ, Mendelsohn FAO (1989) Localization of endothelin receptors in rat kidney. Eur J Pharmacol 160:193–194
Arai H, Hori S, Aramori I, Ohkubo H, Nakanishi S (1990) Cloning and expression of a cDNA encoding an endothelin receptor. Nature 348:730–732
Khoury W, Schreiber L, Szold A, Klausner JM, Wienbroum AA (2009) Renal oxidative stress following CO2 pneumoperitoneum-like conditions. Surg Endosc 23:776–782
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 180:1554–1558
Hayashi T, Yano K, Matsui-Hirai H, Yokoo H, Hattori Y, Iguchi A (2008) Nitric oxide and endothelial cellular senescence. Pharmacol Ther 120:333–339
Rask-Madsen C, King GL (2007) Mechanisms of disease: endothelial dysfunction in insulin resistance and diabetes. Nat Clin Pract Endocrinol Metab 3:46–56
Thomas SR, Chen K, Keaney JF Jr (2003) Oxidative stress and endothelial nitric oxide bioactivity. Antioxid Redox Signal 5:181–194
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The authors are grateful to Aviva Kaballa for her expert technical assistance.
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Bishara, B., Ramadan, R., Karram, T. et al. Nitric oxide synthase inhibition aggravates the adverse renal effects of high but not low intraabdominal pressure. Surg Endosc 24, 826–833 (2010). https://doi.org/10.1007/s00464-009-0672-3
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DOI: https://doi.org/10.1007/s00464-009-0672-3