Hum. Reprod. Advance Access published online on January 5, 2007
Human Reproduction, doi:10.1093/humrep/del482
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© The Author 2007. Published by Oxford University Press on behalf of the European Society of Human Reproduction and Embryology. All rights reserved. For Permissions, please email: journals.permissions@oxfordjournals.org
Peritoneal tissue-oxygen tension during a carbon dioxide pneumoperitoneum in a mouse laparoscopic model with controlled respiratory support
1 Université d'Auvergne – Clermont I, Centre d'Endoscopie et des Nouvelles Techniques Interventionnelles (CENIT), Faculté de Médecine, Clermont-Ferrand, France 2 CHU Clermont-Ferrand, Polyclinique-Hôtel-Dieu, Gynécologie Obstétrique et Médecine de la Reproduction, France 3 CHU Clermont-Ferrand, Hotêl Dieu, Service d'Anesthésie Réanimation, France
4 To whom correspondence should be addressed at: CHU Clermont-Ferrand, Polyclinique-Hôtel-Dieu, Gynécologie Obstétrique et Médecine de la Reproduction, Boulevard Léon Malfreyt, 63058 Clermont-Ferrand, France. Tel.: +33 4 7375 0138; Fax: +33 4 7393 1706; E-mail: sachikoma{at}aol.com
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Abstract |
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BACKGROUND: Previous animal studies suggested that the peritoneal environment during a carbon dioxide (CO2) pneumoperitoneum is hypoxic and that this may contribute to the formation of intra-abdominal adhesions or the growth of malignant cells. There is no study, however, that investigates the relationship between anaesthesia, ventilation and the laparoscopic peritoneal environment to the development of hypoxia. The objective of this study is to monitor the peritoneal tissue-oxygen tension (PitO2) under various conditions including anaesthesia alone, during a CO2 pneumoperitoneum at both low and high intraperitoneal pressure (IPP), and laparotomy, in animal models with controlled respiratory support (CRS). METHODS: C57BL6 mice were divided into eight groups (n=5) consisting of anaesthesia alone or with CO2 pneumoperitoneum at low (2 mmHg) or high (8 mmHg) IPP or undergoing laparotomy. Groups were further subdivided into those with or without CRS with endotracheal intubation and mechanical ventilation. Over the course of the 1 h procedure, PitO2 was continuously monitored. RESULTS: Protocol 1. The PitO2 levels (104.2±7.8 mmHg, mean±SEM) in non-injured peritoneum during a CO2 pneumoperitoneum at a low IPP were elevated
2-fold over the levels during laparotomy (49.8±15.0 mmHg) in ventilated mice. Protocol 2. After insufflation with CO2, the PitO2 was immediately elevated and maintained at a higher level. Following laparotomy, it decreased immediately. This elevation was not seen with air insufflation. CONCLUSION: In mice, a significant elevation in PitO2 occurs during a CO2 pneumoperitoneum at low IPP with CRS.
Key words: anaesthesia/laparoscopy/peritoneal environment/pneumoperitoneum/tissue-oxygen tension
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Introduction |
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Laparoscopic, or minimally invasive, surgery has revolutionized the surgical field. The technology has evolved dramatically over the past two decades and continues to advance. Laparoscopic surgery offers numerous patient benefits including less post-operative pain and impairment of lung function, better cosmetic results, shorter hospitalization and earlier recovery (Korolija et al., 2004
; Schwenk et al., 2005). It is not, however, without limitations. Post-operative adhesion formation and peritoneal dissemination remain major clinical problems (Ray et al., 1998; Ellis et al., 1999; Canis et al., 2001; Koppe et al., 2006). Recent animal experiments suggest that the laparoscopic peritoneal environment is hypoxic (Molinas and Koninckx, 2000; Yesildaglar and Kininckx, 2000; Molinas et al., 2001; Mynbaev et al., 2002; Binda et al., 2003; Wildbrett et al., 2003; Elkelani et al., 2004; Molinas et al., 2004). Given that hypoxia has many adverse effects on biological systems (Crowther et al., 2001; Murdoch et al., 2004; Lewis and Murdoch, 2005), it is plausible that it may contribute to the formation of adhesions or to the growth of malignant cells (Molinas and Koninckx, 2000; Yesildaglar and Koninckx, 2000; Molinas et al., 2001, 2004; Mynbaev et al., 2002; Binda et al., 2003; Wildbrett et al., 2003; Elkelani et al., 2004).
In interpreting the results of animal studies, one must consider whether the findings obtained in the animal model are generalizable to the human clinical setting. A serious limitation of many of the laparoscopic experiments performed in rodent models is the lack of attention paid to confounding factors including the type of anaesthesia used, whether or not respiratory support was used and what insufflation pressures were used in the peritoneum (Gitzelmann et al., 2000; Shiromizu et al., 2000; Carter et al., 2003). A recent study has clearly demonstrated that hypoxaemia and acidosis occur in anaesthetized, non-ventilated rats (Heijnen et al., 2002). Both hypoxaemia and acidosis can induce hypoxia. In another study in which laparoscopic surgeries were performed in mice anesthetized with respiratory support, the animals developed a severe acidosis (Molinas et al., 2004). As is commonly practised in many laboratories (Gitzelmann et al., 2000; Shiromizu et al., 2000; Carter et al., 2003), these investigators applied the same absolute pneumoperitoneum pressure levels used in humans rather than a pressure level proportionate to the animals' size (Molinas et al., 2001, 2004). It is likely that an excessively high intraperitoneal pressure (IPP) contributes to the development of acidosis. There is no study, however, that investigates the relationship between anaesthesia, ventilation and the laparoscopic peritoneal environment to the development of hypoxia, hypoxaemia and acidosis.
In this study, we developed mouse laparoscopic and laparotomy models that utilized controlled respiratory support (CRS). CRS was enabled by videoendoscopic endotracheal intubation and mechanical ventilation. We used this model to measure the peritoneal tissue-oxygen tension (PitO2) in non-injured peritoneum under various conditions including anaesthesia alone, during a carbon dioxide (CO2) pneumoperitoneum at both low and high IPP and laparotomy. We compared our findings in this model with those obtained when CRS was not used.
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Animals
Animals were maintained in accordance with the National Institutes of Health Guide for the Care and Use of Laboratory Animals (US Departament of Health and Human Services, Public Health Service, 1985), and institutional review board approval was obtained for the current study. Studies were conducted in adult (8-week-old, 18–20 g) female C57BL6 mice (Iffa-Credo, Lyon, France). The mice were maintained in a light-and-temperature-controlled environment (14-h light, 10-h dark cycle, 22–25°C) and allowed a 2-week period of acclimation to the vivarium before any procedure was performed. After completion of the experiment, all mice were euthanized with an anaesthetic overdose.
Anaesthesia and videoendoscopy-assisted endotracheal intubation
All mice were anaesthetized in a container with 3–5% vaporized isoflurane with air. Each spontaneously breathing, anaesthetized animal was placed in a supine position on a surgical table. A 2 cm loop made from 4-0 suture was placed behind the front upper incisors and fixed to the surgical table and the mouse secured to the table with adhesive tape by the tail. A rigid 2 mm endoscope (Karl Storz Endoscopy & GmbH, Tuttlingen, Germany) was used to visualize the epiglottis, larynx and vocal cords with the image displayed on a monitor (Figure 1A and B). An endotracheal tube (24 gauge i.v. catheter, Insyte, Becton Dickinson, Le pont de claix, France), with a blunted and bent metal insertion needle as a stylet, was inserted parallel to the scope and threaded carefully and gently between the vocal cords under direct visualization. Anaesthesia was maintained by delivering 3–5% of vaporized isoflurane with air through a nose cone during the intubation. After intubation, the stylet was removed and the catheter connected to a mechanical ventilator (Mini vent type 845, Harvard apparatus GmbH, March-Hugestetten, Germany). We performed preliminary studies to ensure that the ventilation patterns chosen for each experimental condition would maintain the partial pressure of CO2 (PaCO2) in a normal range (25–35 mmHg) (Schwarte et al., 2000). In a previous study (Molinas et al., 2005), mechanically ventilated C57BL6 mice (mean body weight 20.4 g) received a very high tidal volume of 500 µl. However, our preliminary studies showed that ventilated mice C57BL6 with high tidal volumes (225, 250, 275 or 300 µl) were not hypercarbic, but acidaemic (data not shown), suggesting that high tidal volumes could cause metabolic acidosis. In addition, the use of a muscle relaxant was necessary to allow a mechanical ventilation. Our preliminary studies showed that mice without a muscle relaxant developed a hypercarbic acidosis (data not shown). Molinas et al. (2004) reported that anaesthetized mice with respiratory support developed a severe acidosis during a CO2 pneumoperitoneum. Our preliminary studies suggested that their use of a very high tidal volume without a muscle relaxant might cause a severe acidosis in ventilated mice in their study.
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Finally, based on our preliminary experiments, the mice were ventilated with a tidal volume of 200 µl at 250 strokes (laparoscopy: CO2 gas or air) or 220 strokes (laparotomy, anaesthesia alone (control)) per minute. Blood gas parameters for mice with air pneumoperitoneum at 2 mmHg of IPP with CRS were within the normal range (PaO2, 105.3±2.0; PaCO2, 28.9±1.0; pH, 7.367±0.012, mean±SEM, n=3, our preliminary studies). Then, sufentanil (narcotic analgesic, 25 µg/kg, 0.05 ml) and vecuronium bromide (muscle relaxant, 0.4 mg/kg, 0.08 ml) were injected s.c. (right lateral upper quadrant). Vecuronium bromide was injected every 30 min. Anaesthesia was maintained by delivering 2% vaporized isoflurane with air. In the groups without CRS, following the injection of sufentanil (25 µg/kg) s.c. (right lateral upper quadrant), the spontaneously breathing mice received 2% vaporized isoflurane with air through a nose cone.
Surgical procedures
In the pneumoperitoneum group, a 24 gauge i.v. catheter was inserted into the middle of the abdomen and the peritoneal space insufflated with CO2 or air to a pressure of 2 or 8 mmHg (flow rate: 2 l min–1 for both pressure) for 1 h using a Storz electronic endoflator (Karl Storz Endoscopy & GmbH). This electronic endoflator is suitable for both gas. An 18 gauge catheter was inserted i.p. (right lower quadrant) and connected to a water valve to permit the continuous escape of gas. The insufflation of gas was balanced with its exit to maintain a constant pressure.
In the laparotomy group, a 3 cm abdominal incision was made extending from the xiphoid to the pubis and two 5-0 sutures were applied to expose peritoneum to the air for 60 min.
Homeothermia
After the induction of anaesthesia, all procedures were performed on a thermostatically regulated, feedback-controlled heating pad (Homeothermic Blanket Control Unit, Harvard apparatus GmbH). After intubation, a temperature probe was inserted into the rectum. A rectal temperature of 37°C was maintained during the surgical procedure.
Peritoneal tissue-oxygen tenxion
A 16 gauge i.v. catheter was inserted into the retroperitoneal space (beneath the peritoneal membrane) from the left lateral upper quadrant to left lateral lower quadrant, just before surgical procedures. A polarographic oxygen electrode (Integra Neuroscience, Sophia Antipolis, France) was inserted through the catheter and placed in the retroperitoneal space just near the left lateral abdominal mammarygland to measure the PitO2. The PitO2 was continuously monitored on a LICOX CMP monitor (CC1.P1, oxygen sensitive part diameter, 0.65 mm; oxygen sensitive area, 18 mm2; Integra Neuroscience) during procedures. To obtain reliable PitO2 readings, the tissue was allowed to stabilize following the microtrauma of implantation, and the intraoperative values were averaged across the last 30 min of the procedure in each mouse. The resulting values were then averaged among the mice in each group for Protocol 1 (see below). This is a well-established method for evaluating tissue-oxygen Pa (Akca et al., 1999; Greif et al., 2000).
Experimental design
Protocol 1
A total of 40 mice were randomized into the following eight groups of five animals each: (i) anaesthesia alone; (ii) anaesthesia with CRS provided by endotracheal intubation and mechanical ventilation; (iii) anaesthesia plus CO2 pneumoperitoneum at 2 mmHg of IPP (the minimum required to perform the surgery according to our preliminary study); (iv) anaesthesia plus CO2 pneumoperitoneum at 2 mmHg of IPP with CRS; (v) anaesthesia plus CO2 pneumoperitoneum at 8 mmHg of IPP (the maximum reported in many studies (Gitzelmann et al., 2000; Shiromizu et al., 2000; Carter et al., 2003)); (vi) anaesthesia plus CO2 pneumoperitoneum at 8 mmHg of IPP with CRS; (vii) anaesthesia plus laparotomy and (viii) anaesthesia plus laparotomy with CRS.
Over the course of the 60-min procedure, the PitO2 was continuously monitored. At the end of the procedure before the cessation of anaesthesia, respiratory support and CO2 pneumoperitoneum (Groups 3–6), a blood sample was obtained from the carotid artery using the previously published method with some minor modifications (Molinas et al., 2004). Blood gas analysis (O2, CO2 and pH) was performed using a Synthesis blood gas analyzer (Instrumentation Laboratory, Paris, France).
Protocol 2
Protocol 2 included two groups of three mice. In Group 1, following 1 h of anaesthesia with CRS, the abdomen was insufflated with CO2 gas at 2 mmHg and the pressure maintained for 1 h. Laparotomy was then performed and the peritoneum exposed for 1 h. In Group 2, following 1 h of anaesthesia with CRS, the abdomen was insufflated with air at 2 mmHg and the pressure maintained for 1 h. Laparotomy was then performed and the peritoneum exposed for 1 h. PitO2 was monitored throughout the procedures.
Statistical analysis
The Statview 4.5 program (Abacus Concepts, Inc., Berkeley, CA, USA) was used for statistical analysis. Comparisons were made using the one-way analysis of variance with Fisher's post hoc analysis for multiple comparisons or the Mann–Whitney U-test. Statistical significance was defined as P<0.05.
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Arterial blood gas analysis
Results are shown in Table I. Animals in the CO2 pneumoperitoneum groups without CRS (Groups 3 and 5) developed a hypercarbic acidosis. The PaCO2 in these animals was considerably higher than the normal value of 25–35 mmHg (Schwarte et al., 2000
) in mice. In addition, mice in Group 5 (CO2 pneumoperitoneum, high IPP, no CRS) developed mild hypoxaemia. In contrast, mice in Group 6 (CO2 pneumoperitoneum, high IPP, CRS) were mildly acidaemic, but not hypercarbic. Blood gas parameters for all of the other groups (1, 2, 4 and 6–8) were within the normal range.
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Peritoneal tissue-oxygen tension
Protocol 1
Results are shown in Table I. The PitO2 was significantly higher in Group 4 (CO2 pneumoperitoneum, low IPP, CRS) than in the other groups, except Group 3 (CO2 pneumoperitoneum group, low IPP, no CRS). There was no significant difference in PitO2 with and without CRS within the same surgical group (laparotomy, CO2 at a low IPP, CO2 at a high IPP, control).
Protocol 2
Results are shown in Figure 2A and B. When PitO2 was measured during anaesthesia alone, CO2 (Figure 2A) or air (Figure 2B) pneumoperitoneum and laparotomy, the PitO2 was immediately elevated and maintained at a higher level during CO2 pneumoperitoneum, whereas no change in PitO2 was detected during air pneumoperitoneum.
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The PitO2 was significantly higher during CO2 pneumoperitoneum than that during air pneumoperitoneum (Mann–Whitney U test, P<0.05).
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This study demonstrates that a CO2 pneumoperitoneum is in itself enough to cause acidosis in non-ventilated mice. In non-ventilated mice subjected to a high IPP, the acidosis was accompanied by hypercarbia and mild hypoxaemia. In ventilated mice, a mild metabolic acidosis was the only blood gas abnormality. As demonstrated in a recent haemodynamic study, an IPP of 6–8 mmHg in a rat (420–490 g) is comparable to an IPP of 15 mmHg in a human (Gutt and Schmandra, 2000). Thus, insufflation to 8 mmHg in a 20 g mouse is not equivalent to what is experienced by a human from a haemodynamic standpoint. Laparoscopic rodent experiments utilizing a disproportionately high IPP, particularly without CRS, are probably quantitatively and qualitatively different from the conditions in the human. Continued advancement in the field of laparoscopic surgery depends on the use of adequate animal models with sufficient similarity to human physiology as to enable valid comparisons. Their small size and relatively low maintenance cost make rodent models ideal for surgical studies, particularly those incorporating a time course. This study clearly demonstrates that both the use of an IPP in proportion to the animal's size and mechanical ventilation are necessary in order to obtain near physiological conditions in the rodent, which are comparable to the conditions in the human.
Technical difficulties associated with endotracheal intubation are the main reason why only a limited number of laboratories use mechanical ventilation in rodent models. Several methods require a great deal of skill to perform (Molinas et al., 2001; Tarnavski et al., 2004). Additionally, the complication rates of these methods are high because even relatively mild iatrogenic laryngeal trauma could cause respiratory difficulties post-operatively. Consistent with studies in rats (Fuentes et al., 2004), the method of videoendoscopic endotracheal intubation used in this study is easy to learn and simple to perform accurately.
In this study, the highest PitO2 levels were seen in ventilated mice subjected to a CO2 pneumoperitoneum at a low IPP. Thus, in Protocol 2, we sought to investigate whether the PitO2 levels could also be elevated during an air pneumoperitoneum at a low IPP. Air insufflation at the same IPP, however, did not result in an increased PitO2. These findings suggest that it is the biological activity of CO2 gas that is contributing to the increase in peritoneal tissue-oxygen pressure levels during a CO2 pneumoperitoneum at a low IPP. PitO2 is based on the following factors: (i) delivery of oxygen from the lungs to the tissue (i.e. oxygenation of arterial blood, circulation); (ii) transport of oxygen from the blood to the tissue (i.e. PaO2 in blood, the diffusion distance); (iii) oxygen consumption in the tissue (Gottrup, 2004). There are several possible explanations for the elevated PitO2 seen in the low IPP–CO2 pneumoperitoneum group. First, in rat laparoscopic models, the peritoneum becomes locally acidotic during a CO2 pneumoperitoneum with CRS, even when the systemic pH is corrected (Hanly et al., 2005). The decreased pH and increased CO2 in peritoneal tissues during a CO2 pneumoperitoneum could increase the transport of oxygen from the blood to the tissue through the Bohr Effect. In the present study, we did not use humidified insufflation gas.
The hypothermic effect of laparoscopic insufflation is absolved by the use of humidified gas (Bessell and Maddern, 1996) and thus, increased temperature might increase the transport of oxygen from the blood to the tissue through the Bohr effect. Further studies are necessary to investigate whether the use of humidified insufflation gas could increase the PitO2 levels. Second, in ventilated pigs, a CO2 pneumoperitoneum at 5–12 mmHg of IPP increases peritoneal blood flow (Brundell et al., 2002; Yavuz et al., 2003). It is likely that the increased peritoneal blood flow increases the delivery of oxygen to the tissue. In this study, the PitO2 during the CO2 pneumoperitoneum at the high IPP was significantly lower than that at the low IPP in ventilated mice. It is plausible that the high IPP would decrease peritoneal blood flow by a mechanical effect, resulting in a lower PitO2. Further studies are necessary to confirm whether the PitO2 during a CO2 pneumoperitoneum depends on IPP levels.
A recent study by Wildbrett et al. (2003) demonstrated a significant decrease in the tissue-oxygen tension during a CO2 pneumoperitoneum in a rat model without CRS. There are several possible explanations for the difference in findings. Primarily, their applied methodology was different from ours (i.p. injection of pentobarbital, absence of CRS and so on). Second, hypoxaemia might occur in their non-ventilated animals (Heijnen et al., 2002).
Normal level of tissue-oxygen tension is considered to be around 40 mmHg (Guyton and Hall, 2000) and thus, the present results suggested that non-injured peritoneal tissues in ventilated mice are not hypoxic during surgery. However, tissue hypoxia in wounds is common (Crowther et al., 2001) and thus, it is plausible that during surgical procedures in which the peritoneum is injured, the PitO2 level might be lower than the level in the non-injured peritoneum. Tissue oxygenation is one of the most important determinants in wound healing, adhesion formation and tumour growth (Crowther et al., 2001). Although it is necessary to investigate the PitO2 level in injured peritoneum under various surgical conditions, it is likely that the use of a low IPP during laparoscopic surgery may, through minimization of hypoxia, reduce the incidence of complications such as adhesions. Further studies are necessary to investigate the biological significance of an elevated PitO2 in normal peritoneum, the relationship between the IPP and PitO2 and complications such as adhesion formation or the peritoneal dissemination of tumours.
However, there are several methodological limitations to this study. First, we did not perform haemodynamics studies. Further studies are necessary to determine the most physiological IPP in mice, so that it mimics the situation in a clinical setting. Second, a polarographic oxygen electrode was placed in the retroperitoneal space to avoid any direct effects of CO2 gas. The present method measures overall average tissue oxygen tension, and thus, we might measure overall average tissue-oxygen tension for peritoneum and the surrounding tissues. Further studies are necessary to evaluate whether the peritoneal environment during a CO2 pneumoperitoneum is not hypoxic in each cellular level of the peritoneal membrane, using a hypoxia marker (Haroon et al., 2000).
In conclusion, we used a mouse laparoscopic model to gain new insight into peri-operative peritoneal physiology. We demonstrated that an elevation in PitO2 occurs during a CO2 pneumoperitoneum at a low IPP with CRS. The present findings did not support the previous studies that the peritoneal environment during a CO2 pneumoperitoneum is hypoxic. The present method is well established for evaluating human tissue-oxygen partial pressure (Akca et al., 1999; Greif et al., 2000). Further studies should be performed to confirm our present findings in a clinical setting.
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We are grateful to the anaesthesiology staff at CHU Clermont-Ferrand for their invaluable discussions. We are indebted to all staff in le Centre International de la Chirurgie Endoscopique (Clermont-Ferrand, France) and technicians in the department of explorations fonctionelles respiratoires et sportives, CHU Clermont-Ferrand for technical support. We are indebted to Karl Storz Endoscopy & GmbH (Tuttlingen, Germany), Integra Neuroscience (Sophia Antipolis, France) and Organon (Paris, France) for providing laparoscopic equipments, LICOX CMP monitor and vecuronium bromide, respectively. N.B. is a recipient of a fellowship from la Fondation pour la Recherche Médicale (Paris, France).
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Submitted on July 28, 2006; resubmitted on October 9, 2006; resubmitted on November 20, 2006; accepted on November 29, 2006.
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