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Postconditioning in Major Vascular Surgery: Prevention of Renal Failure

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Postconditioning in Major Vascular Surgery: Prevention of Renal Failure Aranyi et al. Journal of Translational Medicine (2015) 13:21 DOI 10.1186/s12967-014-0379-7 RESEARCH Open Access Postconditioning in major vascular surgery: prevention of renal failure Peter Aranyi1, Zsolt Turoczi1, David Garbaisz1, Gabor Lotz2, Janos Geleji3, Viktor Hegedus1, Zoltan Rakonczay4, Zsolt Balla4, Laszlo Harsanyi1 and Attila Szijarto1* Abstract Background: Postconditioning is a novel reperfusion technique to reduce ischemia-reperfusion injuries. The aim of the study was to investigate this method in an animal model of lower limb revascularization for purpose of preventing postoperative renal failure. Methods: Bilateral lower limb ischemia was induced in male Wistar rats for 3 hours by infrarenal aorta clamping under narcosis. Revascularization was allowed by declamping the aorta. Postconditioning (additional 10 sec reocclusion, 10 sec reperfusion in 6 cycles) was induced at the onset of revascularization. Myocyte injury and renal function changes were assessed 4, 24 and 72 hours postoperatively. Hemodynamic monitoring was performed by invasive arterial blood pressure registering and a kidney surface laser Doppler flowmeter. Results: Muscle viability studies showed no significant improvement with the use of postconditioning in terms of ischemic rhabdomyolysis (4 h: ischemia-reperfusion (IR) group: 42.93 ± 19.20% vs. postconditioned (PostC) group: 43.27 ± 27.13%). At the same time, renal functional laboratory tests and kidney myoglobin immunohistochemistry demonstrated significantly less expressed kidney injury in postconditioned animals (renal failure index: 4 h: IR: 2.37 ± 1.43 mM vs. PostC: 0.92 ± 0.32 mM; 24 h: IR: 1.53 ± 0.45 mM vs. PostC: 0.77 ± 0.34 mM; 72 h: IR: 1.51 ± 0.36 mM vs. PostC: 0.43 ± 0.28 mM), while systemic hemodynamics and kidney microcirculation significantly improved (calculated reperfusion area: IR: 82.31 ± 12.23% vs. PostC: 99.01 ± 2.76%), and arterial blood gas analysis showed a lesser extent systemic acidic load after revascularization (a defined relative base excess parameter: 1st s: IR: 2.25 ± 1.14 vs. PostC: 1.80 ± 0.66; 2nd s: IR: 2.14 ± 1.44 vs. PostC: 2.44 ± 1.14, 3rd s: IR: 3.99 ± 3.09 vs. PostC: 2.07 ± 0.82; 4th s: IR: 3.28 ± 0.32 vs. PostC: 2.05 ± 0.56). Conclusions: The results suggest a protective role for postconditioning in major vascular surgeries against renal complications through a possible alternative release of nephrotoxic agents and exerting a positive effect on hemodynamic stability. Keywords: Myoglobinuria, Postconditioning, Renal microcirculation, HSP72 Background to an emerging suprarenal aortic clamping [2,3]. Another An acute deterioration of renal function is a common explanation for the pathogenesis is the muscular injury of observation after major vascular surgery [1]. The etiology the lower limb [4,5]. Crossclamping of the aorta or major and mechanisms of the perioperative renal dysfunction arteries leads to an ischemia-reperfusion (IR) injury to a can be related to preexistent functional compromise, large skeletal muscle mass. Myocyte damage causes a re- perioperative systemic or local hemodynamic distur- lease of intracellular nephrotoxic contents (like excess bances, injury to the urinary tract, pre- and perioperative myoglobin) into the circulation, triggers local inflamma- drug-induced nephropathy, neuroendocrine stress re- tory processes, and can lead to a profound metabolic dis- sponse and inflammatory changes, and renal ischemia due order with hyperkalemia, hypocalcemia, and systemic acidosis [6]. * Correspondence: [email protected] Several brief episodes of ischemia and reperfusion in- 11st Department of Surgery, Semmelweis University, Budapest, Hungary duced immediately after the relief of a longer occlusion - Full list of author information is available at the end of the article © 2015 Aranyi et al.; licensee BioMed Central. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Aranyi et al. Journal of Translational Medicine (2015) 13:21 Page 2 of 12 a method called postconditioning - has been widely 10 seconds’ reocclusion at the onset of reperfusion. studied in recent years and claimed to exert protective (Reperfusion intervals: 4, 24, and 72 h, 8 animals in effect against the IR injury [7]. McAllister et al. were the each subgroup). first who studied postconditioning in a skeletal muscle 3) In the sham-operated group (n = 15), rats were not model and demonstrated a reduction in muscle infarction subjected to aortic clamping, other interventions size, also in muscle myeloperoxidase activity and mito- and measurements were performed in the same chondrial calcium concentration in a porcine muscle flap manner as in the animals subjected to limb ischemia. model [8]. In a former study of our scientific group, the Samples were taken 4 (n = 5), 24 (n = 5) and 72 h postoperative systemic complications, the so-called reper- (n = 5) postoperatively. fusion syndrome was also investigated in a rat abdominal 4) For base excess measurements, additional 10 animals aorta occlusion model, and we demonstrated a significant underwent 180 min of bilateral lower limb ischemia. improvement of postoperative systemic inflammatory re- In 5 of the 10 animals postconditioning was sponse and redox homeostasis [9]. performed. 0.3 ml blood samples were taken from This present study further investigates the effect of post- the right common carotid artery 5 times in each conditioning on muscle injury and the evolving renal dys- animal: just before the onset of reperfusion and at function as a serious postoperative complication in a rat the end of the 1st,2nd,3rd,4th min of the model of open abdominal aortic surgery. reperfusion. Materials and methods Laboratory measurements Surgical preparation Blood samples were harvested from the right ventricle of Inbred male Wistar rats (250-280 g, Charles River the heart by direct puncture. Hungary Ltd, Budapest, Hungary) were anesthetized Urine samples were collected in the 4 h subgroups (intraperitoneal injection of 75 mg/kg ketamine, and from the second hour on after declamping (i.e. for 3 h). 7.5 mg/kg xylazine). In the 4 h reperfusion subgroups, a In the surviving animals urine samples were taken 22-gauge catheter was inserted into the right carotid ar- through a laparatomy by a needle puncture of the urin- tery to monitor arterial blood pressure. ary bladder. The right jugular vein was cannulated for administra- Samples were snap-frozen in liquid nitrogen and tion of intraoperative saline infusion (3 ml/kg/h), main- stored at −70°C. Analysis was performed by an auto- taining anesthesia (25 mg/kg/h ketamine, 2.5 mg/kg/h mated clinical chemistry analyzer (Beckman Coulter xylazine), and injection of heparin (60 IU/kg before the AU480/2011, Beckman Coulter Inc, Brea, CA, USA). aortic clamping). Through a median laparotomy the retroperitoneal space was opened. Except for the sham-operated ani- Muscle viability mals, all rats underwent 180 min of bilateral lower limb Rectus femoris muscle samples were rapidly frozen in li- ischemia by infrarenal crossclamping of the abdominal quid nitrogen and stored at −70°C until processed. Slices aorta using an atraumatic microvascular clip (Aesculap (3 μm) were incubated in dark for 30 min in 0.025% nitro- FT260T; B.Braun AG, Melsungen, Germany). blue tetrazolium chloride (NBT, Sigma-Aldrich Inc, St. The experiment was approved by the Animal Care Louis, MO, USA), dissolved in pH7.6 tri-hydroxymethyl- Committee of Semmelweis University (License No: 22.1/ aminomethane (TRIS) buffer containing 0.05 mmol/l 2409/3/2011) in consistence with the US National Institute nicotinamide-adenine-dinucleotide (NADH). Unbound of Health guidelines (Publication No. 85–23, revised 1996; NBT was eliminated from the sections with 30, 60 and MD, USA). 90% acetone solutions in increasing and decreasing concentrations. Experimental groups Under standardized conditions, photographs were taken, under light microscope (5 randomly selected areas per 1) IR (ischemia-reperfusion) group (n = 24): After each animal). Staining density was measured using a mor- 180 min lower limb ischemia, a reperfusion period phometric software (Leica Qwin Pro, Leica Microsystems of 240 min followed (n = 8). The rest of the animals GmbH, Weltzer, Germany). The relative area of a preset were allowed a survival time after revascularization. wavelength-range (blue: 175/66, green: 105/0, red: 150/0 Sample-taking was performed 24 h (n = 8) and 72 h on the RGB scale) was determined as a quotient of the oc- (n = 8) later. cupied area and the total area of the picture. 2) The Postconditioned (PostC) group (n = 24) was Untreated controls (n = 5) were also involved in the ex- subjected to IR and postconditioning, consisting of periment. In all operated animals, viability was expressed 6 cycles of 10-seconds’ aortic declamping and as a percentage of the untreated animals’ staining density. Aranyi et al. Journal of Translational Medicine (2015) 13:21 Page 3 of 12 Anti-myoglobin immunohistochemistry transformations (Gaussian smoothing) for the purpose Kidney samples were fixed in 4% neutral-buffered forma- of calculations and better comparability of the individual
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