Departments of 1 Obstetrics and Gynaecology, 2 General Surgery, 3 Biochemistry, , 4 Pathology, Faculty of Medicine, Afyon Kocatepe University, 03200, Afyon, Turkey
5 To whom correspondence should be addressed at: Department of Obstetrics and Gynaecology, Faculty of Medicine, Afyon Kocatepe University, 03200, Afyon, Turkey. Tel: +90 272 2136707 (ext.) 209; Fax: +90 272 2144996
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Abstract |
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Key words: cytokine/intra-abdominal pressure/ischaemia/laparoscopy/oxidative stress
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Introduction |
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It is reported that the intra-abdominal pressure (IAP) exerted for pneumoperitoneum (Pp) during laparoscopic operations, which is generally set at about 1215 mmHg, can be increased to 20 mmHg in obese patients (Hulka and Reich, 1998). Several studies have demonstrated that IAP above the normal physiologic portal circulation pressure (710 mmHg) caused a marked reduction in blood flow to hepatic, renal and intestinal circulation (Chiu et al., 1995
; Eleftheriadis and Kotzampasi, 1998
; O'Malley and Cunningham, 2001
; Richter et al., 2001
; Neudecker et al., 2002
). Although deflation restores visceral perfusion, it does not necessarily relieve oxidative stress in the tissue. Moreover, oxidative stress caused by reactive oxygen species (ROS) induced after the restoration of blood flow is one of the most important mechanisms contributing to organ dysfunction following ischaemia and reperfusion (I/R) injury (Li and Jackson, 2002
). Therefore, organ dysfunction following Pp is caused not only by splanchnic or visceral ischaemia, but also by oxidative stress seen after I/R insult (Eleftheriadis et al., 1996
; Seven et al., 1999
; Glantzounis et al., 2001
).
During laparoscopic operations the parietal peritoneum, as well as splanchnic organs, is exposed to ischaemic trauma. In humans an IAP of 15 mmHg decreased blood flow in the parietal peritoneum significantly, whereas no changes were observed with pressures of 10 mmHg (Schilling et al., 1997). It was shown that carbon dioxide (CO2), the gas most frequently used for Pp, led to local (intraperitoneal) and systemic acidosis and aggravated ischaemic organ injury further (O'Malley and Cunningham, 2001
). The peritoneum, which includes a network of widespread capillaries and lymphs in the sub-mesothelial connective tissue, secretes many inflammatory mediators, vasoactive kinins, fibrins, and cytokines, and ROS such as superoxide anion, H2O2 and hydroxyl radical in response to I/R insults (Vittimberga et al., 1998
; Holmdahl and Ivarsson, 1999
; Gupta and Watson, 2001
; Li and Jackson, 2002
).
In order to minimize the harmful effects that Pp with high IAP causes during laparoscopy it is recommended to select the minimal IAP value that will ensure sufficient visualization of the area to be operated on, rather than using the same Pp pressure value in all patients (Neudecker et al., 2002). Another method recommended for decreasing ischaemic injury associated with laparoscopy is ischaemic-preconditioning (IP), which is performed at the start of laparoscopy. IP is an endogenous protective mechanism by which short periods of I/R cycles may be followed by enhanced resistance to exacerbated cellular re-oxygenation injury (Peralta et al., 1999
; Li and Jackson, 2002
). Studies carried out on the assumption that an IAP increase and the following deflation during laparoscopy provided a model conducive to I/R showed that short periods of insufflation and deflation performed at the beginning of laparoscopy (mimicking the laparoscopic preconditioning) were effective in reducing ischaemic injury in intra-abdominal organs (Yilmaz et al., 2003a,b
).
The present study aimed to compare the effects of low-pressure Pp and IP methods on the reduction of I/R injury associated with pressure values normally used during laparoscopy.
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Materials and methods |
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Animals
Thirty-two female, non-pregnant SpragueDawley rats, weighing 264±28 g, bred in isolation from male rats were included in this study. The animals were housed in the Animal Services Centre Laboratory at Afyon Kocatepe University. They were kept at temperatures between 20 and 25°C, with relative humidity between 40 and 70%, and 12 h lightdark cycles, and were given standard rat food and water ad libitum. The experiments were performed in accordance with the 1996 revised form of the guide for care and use of laboratory animals published by the United States National Institutes of Health. The study was approved by the University Ethics Committee. Unnecessary animal suffering was avoided throughout the study. At the beginning of the experiment, each rat was given a number, from 1 to 32. Then the rats were chosen randomly and put into separate cages for each group. The numbers of the rats in each cage were recorded by the principle author.
Anaesthesia
The rats were anaesthetized at the beginning of the experimental procedures by an intramuscular (i.m.) injection of ketamine (5 mg/kg, Ketalar®; Eczacibasi-Werner Lambert, Istanbul-Turkey). Rats that moved during the experiment were given an additional dose (1 mg/kg, i.m.) of ketamine.
Surgical technique
After stabilization of anaesthesia, the animals were placed in a supine position with the limbs secured to the table. The rats were randomly assigned to one of the four groups: Group Pp15 (n=8) was subjected to 60 min of Pp with 15 mmHg of IAP followed by 30 min of deflation (D). Group Pp10, (n=8) was subjected to 60 min of Pp with 10 mmHg IAP followed by 30 min of D. Group IPPp15 (n=8) was subjected to the same Pp and D procedures as Group Pp15 after IP. For the purpose of this study, IP was defined as 10 min of Pp with 15 mmHg IAP followed immediately by 10 min of D. The control group (n=8) was subjected to a sham operation at the end of the 90 min anaesthesia period, without Pp.
Group IPPp15 remained under anaesthesia for a total of 110 min (10 min Pp + 10 min D + 60 min Pp + 30 min D), whereas the total anaesthesia period in the other groups was 90 min.
Two rats in the Pp15 and IPPp15 groups moved during the experiment and were administered an additional dose of anaesthesia. During the Pp procedures one of the rats in the Pp15 mmHg group died. Another rat in the control group was excluded from evaluation upon the observation of a cancer-compatible mass of intestinal origin during laparotomy. As a result, the experiment was concluded with seven rats each in the Pp15 and control groups and eight rats each in the other two groups.
Creation of pneumoperitoneum
The abdomen was shaved with a safety razor and disinfected with polyvidone iodine solution (Batticon; Trommsdorff-Adeka Ilac Sanayi, Samsun, Turkey). A 1 cm midline incision was made beneath the umbilicus to allow access to the peritoneum. The system used to obtain Pp enabled simultaneous CO2 insufflation into eight rats under the same pressure. This simultaneous insufflation procedure involved insufflating a cannula extending from the insufflator divided into right and left branches with the help of a stopcock. From each of these two branches, four auxiliary branches (a total of eight branches) were created, again by the use of stopcocks. The diameters of the main and auxiliary cannulae were equal. Thus it was ensured that carbon dioxide was given to all rats at the same time and pressure during insufflation (Akbulut et al., 2002;Yilmaz et al., 2003a, b
). In order to make sure that there was no gas leakage from the cannulae, the ends of all cannulae were clamped before insufflation, the insufflator set at 15 mmHg was turned on and the pressure values were checked on the monitor. One end of a 25 cm long piece of plastic tubing was inserted into the peritoneal cavity as the vehicle for creating Pp, after which the incision was closed with a tight purse-string suture to prevent leakage of CO2 from the abdomen. The other end of the tubing was connected to the CO2 insufflator (Nortech, Model No: 3-315-00, Fribourg, Switzerland). The pressure of the CO2 insufflator was fixed at 15 or 10 mmHg except for in the controls. An automatic insufflator provided CO2 insufflation for the required intra-abdominal pressure. In the event of the intra-abdominal pressure decreasing due to transperitoneal CO2 absorption or a possible gas leakage from the trocar entry site, the insufflator was automatically activated and pumped CO2 into the abdominal cavities of the animals to keep the intra-abdominal pressure at the determined level.
Tissue and blood sampling and preparation for further studies
At the end of Pp and D in each group, the surgeons (the first and second authors) and their assistants divided the rats between the two teams and performed surgical dissection. After the Pp catheters were removed, laparotomy incisions were opened and extended, and 1 x 1 cm squares of parietal peritoneum examples from the right and left lower abdominal walls were grasped with atraumatic forceps and excised with scissors. Blood samples were taken from the intra-thoracic aorta with a 22 G needle attached to a 5 cc syringe. Blood samples were drawn into heparinized tubes. The rats were then killed with an intra-cardiac potassium injection while still under anaesthesia. It took 2 min on average to dissect the abdomen, collect blood and peritoneum samples and inject intra-cardiac potassium in each rat.
Half of the peritoneal tissue samples were washed with ice-cold lactated Ringer's solution and stored at 20°C until analysis. The other half of the samples were immersed in 10%formaldehyde for later examination under the light microscope. Each tissue and blood sample was assigned a code number by the principal investigator and referred to the biochemists and pathologist participating in the study, who were blinded to the procedures applied to specific groups. All results were reported in relation to the sample code numbers.
Biochemical analysis
During the biochemical analysis, peritoneal tissue samples were initially homogenized (Ultra Turrax Homogenizer, T18 Basic, IKA, Wilmington, NC) in 0.1 M ice-cold phosphate buffer of pH 7.4. After homogenization, tissue samples were centrifuged at 3000 g and 4°C for 10 min. The supernatants were removed and used to determine oxidative stress markers and inflammatory cytokines. The tissue protein concentration was measured by the Biuret method. Results were expressed as µmol/g protein for malondialdehyde (MDA) and reduced glutathione (GSH), U/g protein for glutathione reductase (GR), and ng/g protein for tumor necrosis factor alpha (TNF-) and interleukin-6 (IL-6).
Blood samples were drawn into heparinized tubes during the experimental procedure. Plasma was separated by centrifugation at 800 g and 4°C over 10 min. Erythrocytes were washed three times with ice-cold physiological saline. The buffy coat together with part of the upper erythrocyte layer was removed and discarded after each washing step. After the washing procedure, the packed cells and plasma were stored at 20°C until analysis. The packed erythrocyte haemoglobin concentration was determined spectrophotometrically in lysed cells by the cyanomethaemoglobin method. Results were expressed as µmol/g haemoglobin for GSH and U/g haemoglobin for GR, µmol/l for plasma MDA, and pg/ml for plasma TNF- and IL-6.
Plasma and tissue MDA levels were determined by the thiobarbituric acid method of Okhawa et al. (1979). MDA is an indicator of oxidative stress, since it results from the breakdown of lipid peroxyl radicals. MDA is also important as it can cause further oxidative injury by oxidizing protein molecules (Stadtman and Berlett, 1997
). Despite these advantages, MDA reflects changes in numerous other biochemical systems as well as ROS, in particular the prostaglandins. Therefore, in the evaluation of oxidative stress we examined not only MDA, but also markers showing antioxidant status (GR and GSH). GR enzyme plays a part in the further reduction of the GSH, which is bound to the free oxygen radical (ROS), inactivates it and becomes oxidized in the process (Meister, 1994
; Li and Jackson, 2002
). Erythrocyte and tissue reduced GSH levels and GR enzyme activities were determined as an indicator of erythrocyte or tissue antioxidant capacity, using the methods described by Beutler et al. (1957)
and Goldberg and Spooner (1983)
. Erythrocyte and tissue GR activities were measured with a Hitachi 917 autoanalyser using commercial kits obtained from Randox Laboratories (Randox Laboratories Ltd, County Antrim, UK). Plasma and tissue cytokine (TNF-
and IL-6) levels were determined as an indicator of the activation of the systemic immune system, using a commercially available rat ELISA kit (Biosource Europe SA, Nivelles, Belgium). Other chemicals used in the evaluation of tissue and blood GSH and MDA were purchased from the Sigma Chemical Co. (St Louis, MO).
Histopathological examination
Tissue samples were fixed in 10%neutral buffered formalin. Samples were embedded in paraffin, cut into sections 3 µm thick and stained with haematoxylineosin. One section of each peritoneal tissue sample was systematically analysed by a pathologist blinded to the study groups. Each section was evaluated for intracellular oedema, congestion, haemorrhage and interstitial inflammatory cell infiltration, using the semiquantitative scale described by Hauet et al. (1997). Sample results were reported under their respective code numbers. The total sum of histopathological scores was obtained for all groups by combining the individual parameters (Table I).
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Results |
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The highest peritoneal tissue MDA values were in the Pp15 group, followed by the Pp10, IPPp15 and control groups, in descending order (P<0.001; Pp15 vs Pp10, and IPPp15, and C). There was no apparent difference among the Pp10, IPPp15 and control groups in terms of peritoneal MDA values (Figure 1).
Erythrocyte and tissue GR levels
When the groups were examined in terms of erythrocyte GR activities, values in the Pp15 group were lower than those in the IPPp15 and control groups (P<0.001), but there was no statistically significant difference between the values in the Pp10 and Pp15 groups. Erythrocyte GR values in the Pp10 group were lower than those in the IPPp15 (P<0.05) and control (P<0.001) groups. No difference was found between erythrocyte GR values in the IPPp15 and control groups.
Peritoneal GR values in the Pp15 group were lower than those in the Pp10 (P<0.05), IPPp15 and control groups (P<0.001). There was no statistically significant difference between peritoneal GR values in the Pp10 and IPPp15 groups, but the values of the former were significantly lower than those in the control group (P<0.01). No difference was found between peritoneal GR values in the IPPp15 and control groups (Figure 2).
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Peritoneal TNF- values were higher in the Pp15 group than those in all other groups (P<0.05), but no difference was determined between peritoneal TNF-
values in the Pp10 group and those in the IPPp15 and control groups. No difference was found between peritoneal TNF-
values in the IPPp15 and control groups (Figure 4).
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Peritoneal IL-6 values were significantly higher in the Pp15 group than those in the Pp10 (P<0.05), IPPp15 and control groups (P<0.001). Peritoneal IL-6 levels in the Pp10 group were higher than those in the control (P<0.01) group only. Peritoneal IL-6 values in the IPPp15 group were higher than those in the control group (P<0.05) (Figure 5).
Histopathological findings
Light microscopy revealed no evidence of overt injury in any peritoneal tissue sample. Despite a small numerical difference, there was no statistical difference among the groups in terms of the histopathological scoring system (Table II).
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Discussion |
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Values of the markers that were studied in both blood (plasma and erythrocyte) and parietal peritoneum samples that indicated oxidative stress (MDA) and cytokine response (TNF- and IL-6) were higher in the group receiving 15 mmHg IAP. In addition, levels of the markers showing anti-oxidant activity (erythrocyte GSH and GR) were lower in this group. It was seen that IP, a manoeuvre used to reduce surgical trauma, provided an evident decrease in oxidative stress and inflammatory cytokine response alike, while low-pressure (10 mmHg) Pp was not as effective as IP (Figures 1 to 5).
Lower-pressure Pp procedures were tried in animal and human models to reduce tissue ischaemia associated with high-pressure Pp. In a laparoscopic cholecystectomy using a gasless technique and 14 and 10 mmHg pressure, Giraudo et al. (2001) compared hepatic function test results and showed that transaminase values increased more in the group operated on with 14 mmHg IAP, while transaminase values in the 10 mmHg and gasless groups were similar. Samel et al. (2002)
demonstrated in a rat model that intra-abdominal pressures of 10 and 15 mmHg caused a significant stepwise decrease in the jejunal mucosa perfusion index (29 and 78%, respectively), resulting in a severe impairment of mucosal microcirculation. However, there are also studies in rat (Yilmaz et al., 2004
) and human (Polat et al., 2003
) models showing that no statistically significant difference could be found in oxidative stress response between 10 and 15 mmHg pressure applications.
In the present study, a comparison of the Pp15 and Pp10 groups in terms of oxidative stress and inflammatory cytokine response demonstrated that there was a significant difference (P<0.001) between the groups only in terms of MDA, which was studied in both plasma and peritoneum, and that there was either no difference in terms of GSH levels or the difference was only in peritoneum samples in terms of GR, TNF- and IL-6 parameters (P<0.05). Our findings suggest that low-pressure Pp can be effective to a degree in reducing oxidative stress and inflammatory cytokine response, particularly at the peritoneal level.
The second manoeuvre we employed to reduce ischaemic injury associated with laparoscopy was IP. This is an injury-limiting mechanism initially described as the attenuation of cardiac damage due to a severe I/R insult by previous short I/R cycles (Murry et al., 1986). The liver and kidney have also been shown to benefit from IP (Peralta et al., 1999
; Ogawa et al., 2000
). However, in these experiments a mechanical obstruction was performed on the vascular pedicle of the studied organ to induce ischaemic insult, whereas we evaluated laparoscopic Pp applied at 15 mmHg pressure as the ischaemic insult model (Yilmaz et al., 2003a,b
). The most important piece of information that guided authors of the study in this procedure was that when IAP values used for Pp were above normal portal venous pressure (710 mmHg), this would lead to ischaemia in intra-abdominal organs by reducing portal blood flow and organ circulation would return to normal after deflation (Richter et al., 2001
; Samel et al., 2002
). Thus, it was speculated that the use of short-term Pp and deflation before long-term Pp could create an IP effect on splanchnic organs, and especially the parietal peritoneum.
Experiments conducted to demonstrate the efficacy of IP in reducing long-term ischaemia and the following reperfusion (I/R) injury have various IP application times, but IP was generally performed in the form of 510 min of ischaemia, followed by 510 min of reperfusion (Sola et al., 2000; Clavien et al., 2000; Gonj et al., 2004
). Reinheckel et al. (2000)
showed in a rat model that protein carbonyls, a marker of oxidative stress, are detected in mitochondrial proteins after 10 min hypoxia and 5 min re-oxygenation. Based on the exemplary IP times used in the literature, the ischaemia (insufflation) and reperfusion (deflation) times of the IP procedure in this experiment were determined to be 10 min each. It was seen that the levels of the markers that were studied in both blood and peritoneal tissue and that showed oxidative stress and inflammatory response were similar in laparoscopic IP and control groups, but the levels in the former were significantly different in comparison to those in the Pp15 and Pp10 groups (Figures 1, 2, 4 and 5). Our findings support the thesis that the IP procedure carried out in the experiment made the rats more resistant to the next and longer ischaemic stimulation.
Raising intra-abdominal pressure leads to ischaemia and the formation of ROS in the peritoneum in a time- and pressure-level-dependent manner (Diebel et al., 1992; Li and Jackson, 2002
). When aerobic conditions are restored after reperfusion, ROS increase and scavenger antioxidant substances decrease initially, but tissue antioxidant defences build up over time and eliminate high levels of ROS from the medium (Li and Jackson, 2002
). Some cellular proteins released during ischaemic preconditioning are also known to make the cell resistant to the harmful effects of ROS. For instance, preconditioning causes over-expression of the anti-apoptotic gene product called heat shock 70 (HSP70) in coronary endothelial cells and this reduces hypoxic injury (Suzuki et al., 1998
). Our finding suggests that substances released from the peritoneum in response to short-term ischaemia in the group to which preconditioning was applied made tissues more resistant to the next and longer ischaemia, and thus made oxidative stress and inflammatory cytokine response milder.
Although the pressure we applied (10 mmHg) to determine the effect of low-pressure Pp is below 15 mmHg, it still has the potential to cause ischaemia since it is above the 710 mmHg normal intra-abdominal pressure value (Richter et al., 2001). It was shown that even if an IAP value (5 mmHg) lower than the normal IAP value interval were used, it could cause oxidative stress (Bentes de Souza et al., 2003b
). This finding implies that oxidative stress response might stem from the gas used (CO2) rather than IAP during Pp. It was reported that hypercapnia and acidosis that developed as a result of trans-peritoneal absorption of the CO2 used in Pp could bring about vasoconstriction and increase vascular resistance and hypo-perfusion (O'Malley and Cunningham, 2001
). Yesildaglar and Koninckx (2000)
showed in a rabbit endoscopic surgery model that increasing IAP values used during CO2 Pp (5 vs 20 mmHg), as well as increasing insufflation flow rates (1 l/min vs 10 l/min), enhanced mesothelial hypoxaemia and therefore peritoneal adhesion formation. However, the haemodynamic effects caused by CO2 Pp on human tissues may be different from those on rat tissues. Bentes de Souza et al. (2003a)
compared peritoneal MDA levels in gynaecological operations performed with laparoscopy and open surgery and showed that while there was no marked MDA increase in the laparoscopy group, there was an increase in MDA in the laparotomy group. This finding suggests that peritoneal tissue response levels of humans to laparoscopic ischaemia even at similar IAP values may be different from those of rats.
It may be beneficial to use intubation and mechanical ventilation as well as blood gas follow-up and close haemodynamic monitoring, especially in experiments in which a high intra-abdominal pressure model is used, in order to reduce evaluation errors that could result from differences in the gas used in Pp, the insufflation system, and the intra-abdominal volume of the subject. Mynbaev et al. (2002) showed in a rabbit endoscopic surgery model that CO2 Pp with 10 mmHg IAP profoundly affected blood gases and acid base homeostasis, resulting in metabolic hypoxaemia. Since we did not perform intubation and mechanical ventilation and did not follow up blood gases during the experiment, we cannot tell whether hypercapnia or elevated intra-abdominal pressure influenced the rise in MDA and inflammatory cytokines. Nonetheless, despite the fact that the IPPp15 group and Pp15 group were subjected to the same IAP values during the Pp, oxidative stress and inflammatory cytokine response in the IPPp15 group were similar to those in the control group, showing that IP can be beneficial even in such circumstances.
The fact that we collected blood and tissue samples only at the end of the experiment in order to show oxidative stress and inflammatory cytokine response prevented us from following the synthesis and elimination cycles of these markers at different stages of the experiment. More objective data could have been obtained if blood and peritoneum levels of these markers had been examined at the beginning of the experiment, during Pp and after deflation. Since we conducted our study on rats, we did not have the opportunity to place trocars in the abdomen during the experiment or to collect peritoneal tissue samples at various times. In order to reduce the risk of misinterpretation that could result from our failure to identify at one single time the reactions associated with an ischaemic insult, we used multiple oxidative stress and inflammatory response markers. Similarly, we evaluated both blood and peritoneum samples at the same time and thus we were able to study the correlation between local and systemic responses. Furthermore, the fact that the parameters we studied were at similar levels in the blood and peritoneum showed that the parietal peritoneum could provide valuable information reflecting the general response of the organism.
Another aspect of our findings that could be criticized is that although there were differences among the groups in terms of oxidative stress and inflammation markers studied in tissue homogenates, there were no signs of ischaemic injury in the peritoneal tissue examinations carried out with the light microscope (Table II). Our literature search did not reveal another study presenting light microscopy findings of ischaemic injury caused by Pp in the peritoneum compared with oxidative stress and inflammatory responses in the peritoneal tissue homogenates. It is possible that the changes we found in oxidative stress and inflammation markers in peritoneal tissue homogenates were accompanied by tissue damage that could only be revealed with electron microscopy in its early stages.
In conclusion, the findings of our experiment suggest that ischaemia preconditioning applied in the form of 10 min pneumoperitoneum and deflation periods can be more effective than low-pressure pneumoperitoneum in reducing the oxidative stress and inflammatory cytokine response associated with laparoscopy. Our experimental protocol of preconditioning may be too lengthy to be recommended for direct use in humans. Nonetheless, studies can be conducted to identify the minimum period that will suffice to reveal the effect of preconditioning.
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Acknowledgements |
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References |
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---|
Bentes de Souza AM, Rogers MS, Wang CC, Yuen PM and Ng PS (2003a) Comparison of peritoneal oxidative stress during laparoscopy and laparotomy. J Am Assoc Gynecol Laparosc 10, 6574.[Medline]
Bentes de Souza AM, Wang CC, Chu CY, Lam MP and Rogers MS (2003b) The effect of intra-abdominal pressure on the generation of 8-iso prostaglandin F2 during laparoscopy in rabbits. Human Reprod 18, 21812188.
Beutler E, Robson MJ and Buttenwieser E (1957) The glutathione instability of drug sensitivity to red cells. J Lab Clin Med 49, 8489.
Chiu AW, Chang LS, Birkett DH and Babayan RK (1995) The impact of pneumoperitoneum and gassles laparoscopy on systemic and renal hemodynamics. J Am Coll Surg 181, 397406.[Medline]
Clavien P-A, Yadav S, Sindram D and Bentley RC (2000) Protective effects of ischemic preconditioning for liver resection performed under inflow occlusion in humans. Ann Surg 232, 155162.[CrossRef][Medline]
Diebel LN, Saxe J and Dulchavsky SA (1992) Effect of increased intra-abdominal pressure on abdominal wall blood flow. Am Surg 583, 573576.
Eleftheriadis E, Kotzampassi K, Papanotas K, Heliadis N and Sarris K (1996) Gut ischaemia, oxidative stress and bacterial translocation in elevated abdominal pressure in rats. World J Surg 20, 1116.[CrossRef][Medline]
Eleftheriadis E and Kotzampasi K (1998) Influence of pneumoperitoneum on the mesenteric circulation. In Rosenthal RJ, Friedman RL, and Philips EH (eds) The pathophysiology of pneumoperitoneum. Springer, New York, USA, pp 4961.
Giraudo G, Brachet CR, Cacceta M and Morino M (2001) Gasless laparoscopy could avoid alterations in hepatic function. Surg Endosc 15, 741746.[CrossRef][Medline]
Glantzounis GK, Tselepis AD, Tambuki AP, Trikalinos TA, Manataki AD, Galaris DA, Tsimoyiannis EC and Kappas AM (2001) Laparoscopic surgery-induced changes in oxidative stress markers in human plasma. Surg Endosc 15, 13151319.[Medline]
Goldberg DM and Spooner RJ (1983) Glutathione reductase. In Bergmeyen HV (ed.) Methods of Enzymatic Analysis. Verlog, Deerfield Beach, USA, pp 258265.
Gonj JP, Tu B, Wang W, Peng Y, Li SB and Yan LN (2004) Protective effect of nitric oxide induced by ischemic preconditioning on reperfusion injury of rat liver graft. World J Gastroenterol 10, 7376.[Medline]
Gupta A and Watson DI (2001) Effect of laparoscopy on immune function. Br J Surg 88, 12961306.[CrossRef][Medline]
Hauet T, Mothes D, Goujon JM, Caritez JL, Carretier M, le-Moyec L, Eugene M and Tillement JP (1997) Trimetazidine prevents renal injury in the isolated perfused pig kidney exposed to prolonged ischaemia. Transplantation 64, 10821086.[CrossRef][Medline]
Holmdahl L and Ivarsson ML (1999) The role of cytokines, coagulation, and fibrinolysis on peritoneal tissue repair. Eur J Surg 165, 10121019.[CrossRef][Medline]
Hulka JF and Reich H (1998) Textbook of laparoscopy, 3rd edn. W B Saunders Company, Philadelphia, USA.
Li C and Jackson RM (2002) Reactive species mechanisms of cellular hypoxia-reoxygenation injury. Am J Physiol Cell 282, 227241.
Meister A (1994) Glutathione-ascorbic acid antioxidant system in animals. J Biol Chem 269, 93979400.
Murry CE, Jenning RB and Reimer KA (1986) Preconditioning with ischaemia: a delay of lethal cell injury in ischemic myocardium. Circulation 74, 11241136.[Abstract]
Mynbaev OA, Molinas CR, Adamyan LV, Vanacker B and Koninckx PR (2002) Reduction of CO(2)-pneumoperitoneum-induced metabolic hypoxaemia by the addition of small amounts of O(2) to the CO(2) in a rabbit ventilated model. A preliminary study. Hum Reprod 17, 16231629.
Neudecker J, Sauerland S, Neugebauer E, Bargamaschi R, Bonjer HJ, Cuschieri A, Fuchs KH, Jacobi CH, Jansen FW, Koivusola A et al. (2002) European Association for Endoscopic Surgery clinical practice guideline on the pneumoperitoneum for laparoscopic surgery. Surg Endosc 16, 11211143.[CrossRef][Medline]
Ogawa T, Mimura Y, Hiki N, Kanauchi H and Kaminishi M (2000) Ischaemic preconditioning ameliorates functional disturbance and impaired renal perfusion in rat ischaemia-reperfused kidneys. Clin Exp Pharmacol Physiol 27, 9971001.[CrossRef][Medline]
Okhawa H, Ohishi N and Yagi K (1979) Assay for lipid peroxidase in animal tissues by thiobarbituric acid reaction. Annal Biochem 95, 351358.[Medline]
O'Malley C and Cunningham AJ (2001) Physiologic changes during laparoscopy. Anesthesiol Clin North Am 19, 119.[Medline]
Peralta C, Prats N, Xaus C, Gelpi E and Rosello-Catafau J (1999) Protective effect of liver ischaemic preconditioning on liver and lung injury induced by hepatic ischaemia-reperfusion in the rat. Hepatology 30, 14811489.[Medline]
Polat C, Yilmaz S, Serteser M, Koken T, Kahraman A and Dilek ON (2003) The effect of different intra-abdominal pressures on lipid peroxidation and protein oxidation status during laparoscopic cholecystectomy. Surg Endosc 17, 17191722.[CrossRef][Medline]
Reinheckel T, Korn S, Mohring S, Augustin W, Halangk W and Schild L (2000) Adaptation of protein carbonyl detection to the requirements of proteome analysis demonstrated for hypoxia/reoxygenation in isolated rat liver mitochondria. Arch Biochem Biophys 376, 5965.[CrossRef][Medline]
Richter S, Olinger A, Hildebrandt U, Menger MD and Vollmar B (2001) Loss of physiologic hepatic blood flow control (hepatic arterial buffer response) during CO2-pneumoperitoneum in the rat. Anesth Analg 93, 872877.
Samel ST, Neufang T, Mueller A, Leister I, Becker H and Post SA (2002) New abdominal cavity chamber to study the impact of increased intra-abdominal pressure on microcirculation of gut mucosa by using video microscopy in rats. Crit Care Med 30, 18541858.[Medline]
Schilling MK, Redaelli C, Krahenbuhl L, Signer C and Buchler MW (1997) Sphlanchnic microcirculatory changes during CO2 laparoscopy. J Am Coll Surg 184, 378382.[Medline]
Seven R, Seven A, Erbil Y, Mercan S and Burcak G (1999) Lipid peroxidation and antioxidant state after laparoscopic and open cholecystectomy. Eur J Surg 165, 871874.[CrossRef][Medline]
Sies H (1997) Oxidative stress: Oxidants and antioxidants. Exp Physiol 182, 291295.
Sola A, Hotter G, Prats N, Xaus C, Gelpi E and Rosello-Catafau J (2000) Modification of oxidative stress in response to intestinal preconditioning. Transplantation 69, 767772.[Medline]
Stadtman ER and Berlett BS (1997) Reactive oxygen-mediated protein oxidation in aging and disease. Chem Res Toxicol 10, 485494.[CrossRef][Medline]
Suzuki K, Sawa Y, Kaneda Y, Ichikawa H, Shirakura R and Matsuda H (1998) Over expressed heat shock protein 70 attenuates hypoxic injury in coronary endothelial cells. J Mol Cell Cardiol 30, 11291136.[CrossRef][Medline]
Vittimberga FJ, Foley DP, Meyers WC and Callery MP (1998) Laparoscopic surgery and the sysytemic immune response. Ann Surg 227, 326334.[CrossRef][Medline]
Yesildaglar N and Koninckx PR (2000) Adhesion formation in intubated rabbits increases with high insufflation pressure during endoscopic surgery. Hum Reprod 15, 687691.
Yilmaz S, Koken T, Tokyol C, Kahraman A, Akbulut G, Serteser M, Polat C, Gokce C and Gokce O (2003a) Can preconditioning reduce laparoscopy-induced tissue injury? Surg Endosc 17, 819824.[Medline]
Yilmaz S, Ates E, Polat C, Koken T, Tokyol C, Akbulut G and Gokce O (2003b) Ischaemic preconditioning decreases laparoscopy-induced oxidative stress in small intestine. Hepatogastroenterology 50, 979982.[Medline]
Yilmaz S, Polat C, Kahraman A, Koken T, Arikan Y, Dilek ON and Gokce O (2004) The comparison of the oxidative stress effects of different gases and intra-abdominal pressures in an experimental rat model. J Laparoendos Adv Surg Techn. In press.
Submitted on January 21, 2004; accepted on May 24, 2004.
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