Pleura and Peritoneum 2017; 2(1): 17–31
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Pleura and Peritoneum 2017; 2(1): 17–31 Opinion Paper Robert B. Wilson* Changes in the coelomic microclimate during carbon dioxide laparoscopy: morphological and functional implications DOI 10.1515/pap-2017-0001 Keywords: arachidonic acid, carbon dioxide, HIF-1α,humi- Received January 30, 2017; accepted February 17, 2017; dification, hyaluronan, hypothermia, hypoxia, IL-1β, intra- previously published online March 17, 2017 abdominal pressure (IAP), laparoscopy, perfusion, perito- Abstract: In this article the adverse effects of laparoscopic neal metastasis, tumour cell implantation, VEGF CO2-pneumoperitoneum and coelomic climate change, and their potential prevention by warmed, humidified carbon dioxide insufflation are reviewed. The use of pres- Introduction surized cold, dry carbon dioxide (C0 ) pneumoperitoneum 2 Over 200 years ago, the German naturalist Alexander von causes a number of local effects on the peritoneal Humboldt [1] explored various planetary ecosystems and mesothelium, as well as systemic effects. These can be defined the intricate relationships between humidity, observed at a macroscopic, microscopic, cellular and temperature, barometric pressure, rainfall and climate. metabolic level. Local effects include evaporative cooling, In analogy, the peritoneal cavity is a micro-ecosystem oxidative stress, desiccation of mesothelium, disruption of where factors such as humidity, pressure and tempera- mesothelial cell junctions and glycocalyx, diminished ture play a major physiological role. In this article, the scavenging of reactive oxygen species, decreased perito- detrimental effects of laparoscopic carbon-dioxide (CO )- neal blood flow, peritoneal acidosis, peritoneal hypoxia or 2 pneumoperitoneum and coelomic climate change, and necrosis, exposure of the basal lamina and extracellular their potential prevention are reviewed. matrix, lymphocyte infiltration, and generation of perito- neal cytokines such as IL-1, IL-6, IL-8 and TNFα.Such damage is increased by high CO2 insufflation pressures and gas velocities and prolonged laparoscopic proce- Coelomic microclimate dures. The resulting disruption of the glycocalyx, mesothelial cell barrier and exposure of the extracellular The coelom forms the crucial interface between the parietal matrix creates a cascade of immunological and pro- and visceral peritoneal surfaces. The physical, chemical inflammatory events and favours tumour cell implanta- and biological properties of the peritoneal cavity contribute tion. Systemic effects include cardiopulmonary and to its controlled microclimate. It is isothermic and fully respiratory changes, hypothermia and acidosis. Such coe- humidified, with an intra-abdominal pressure (IAP) of 0–3 lomic climate change can be prevented by the use of mmHg [2, 3]. This provides stability for the function of the lower insufflation pressures and preconditioned warm intra-abdominal viscera and maintains splanchnic blood humidified CO2. By achieving a more physiological flow, immunocompetence, temperature regulation and temperature, pressure and humidity, the coelomic micro- fluid balance. The total peritoneal surface area in an adult environment can be better preserved during pneumoper- human (1.5–2m2) is similar to the skin surface area. The itoneum. This has the potential clinical benefits of visceral component comprises approximately 70 % and par- maintaining isothermia and perfusion, reducing post- ietal 30 % of the total peritoneal surface area [4]. The operative pain, preventing adhesions and inhibiting can- mesothelial surface of the peritoneum normally acts as a cer cell implantation in laparoscopic surgery. semipermeable membrane for solute and nutrient transfer and a barrier to larger molecules or foreign objects such as cancer cells. Changing the microclimate of the coelom can *Corresponding author: Robert B. Wilson, Department of Upper Gastrointestinal Surgery, Liverpool Hospital, Elizabeth St, Liverpool, disrupt the normal homeostatic state of the peritoneum and Sydney, NSW, 2170, Australia, E-mail: [email protected] abdominal viscera [2–15]. 18 Wilson: Effects of carbon dioxide pneumoperitoneum shows some similarities to the polar jetstream of the Carbon dioxide (CO2) Northern hemisphere. Both have a rapid, relatively pneumoperitoneum narrow, turbulent flow and contain dense, cold, dry gas. Both create vertical and horizontal wind shear forces Carbon dioxide is an ideal gas for pneumoperitoneum as causing turbulence, vortex formation and influencing it is inert, soluble, easily diffusible, quickly buffered and (micro-)climate patterns [16]. Suction devices, tissue com- excretable, commercially cheap and readily available. In bustion plumes, gas evacuation systems, large CO2 fluxes comparison to CO2, the relative solubility of oxygen and high insufflation velocities during laparoscopic sur- respectively is 1/24 and nitrogen 1/46; relative diffusion gery further increase gas use, turbulence and vortices. of oxygen 1/20 and nitrogen 1/37. This means that CO2 Such vortices create convection currents, which can gas is readily absorbed and rapidly excreted. Thus the affect areas of the peritoneum distant from the direct perioperative risks of gas embolism, retained gas, pneu- path of the CO2 gas jetstream [2]. Thus the entire visceral mothorax and potentially pain are less with CO2 insuffla- and parietal peritoneum can be affected, including phre- tion compared to air [5–7]. nic nerve nociceptors on the subdiaphragmatic surface [5, Standard pneumoperitoneum for laparoscopic surgery 11]. The extent of peritoneal evaporation is related to the involves insufflation of cold, dry carbon dioxide gas. temperature and humidity of the insufflated CO2 gas, but Carbon dioxide is contained in gas cylinders at a pressure also the stability of its interaction with the peritoneal of 57 atm as a liquid. As it passes the throttle valve on the surface, and the total volume of insufflated gas [17]. cylinder head the CO vaporizes, expands and cools as a 2 When cold-dry CO2 is used for insufflation, peritoneal result of the Joule-Thomson effect. When it enters the coe- climate change occurs, which can be detrimental to the lom via the gas insufflator, the relative humidity of intro- patient [5]. duced dry CO2 gas is 0.0002 % [5], with a temperature of 20 °C and a high velocity [2, 5, 9]. The use of cold-dry CO2 gas causes a number of local effects on the peritoneal – mesothelium, as well as systemic effects in the subject [5]. Peritoneum structural These can be observed at a macroscopic, microscopic, cel- and functional physiology lular and metabolic level [2–15]. Local effects include evaporative cooling, oxidative Mesothelial cells originate from the mesoderm and are stress [10–12], desiccation of mesothelium, disruption of usually flattened squamous like cells with epithelial-like mesothelial cell junctions and glycocalyx, diminished microvilli which project into the coelom. The microvilli scavenging of reactive oxygen species (ROS), decreased are covered by a thin serous layer (60 μm) of peritoneal peritoneal blood flow, peritoneal acidosis, peritoneal fluid and glycosaminoglycans, phospholipids, proteo- hypoxia or necrosis, increased ROS production, exposure glycans, surfactants and coagulant precursors secreted of the basal lamina and extracellular matrix (ECM), lympho- by mesothelial cells. This provides a protective, slippery cyte infiltration, and generation of prostaglandins and peri- glycocalyx barrier to abrasions, infections and tumour toneal cytokines such as IL-1, IL-6, IL-8 and TNFα [2,5,13, cell implantation and allows apposing serosal surfaces 14]. Factors that increase evaporation include an increase in to slide without friction. Microvilli greatly increase the gas flow (“wind”) or surface area, or a decrease in humidity. peritoneal surface area and potentially enhance this The human-induced climate change, deforestation, water tribologic protective barrier. High molecular weight hya- evaporation and barren land that von Humboldt first luronan (HMWHA), a linear glycosaminoglycan, is a observed in Venezuela in 1800 has parallels to the damage major component of the glycocalyx and is produced to the coelomic microenvironment observed with cold, dry locally by the peritoneal mesothelial cells (PMC). It is a CO2-pneumoperitoneum [1]. large hydrophilic anionic polymer with unique hygro- scopic, rheologic and viscoelastic properties. Another component of the glycocalyx produced by the PMC is Jetstream-like effects of CO surfactant (phosphatidylcholine) which also contributes 2 to lubrication and stable fluid balance. Movement of insufflation fluids and molecules across the peritoneal surface is facilitated by the microvilli and occurs via passive trans- The cold, dry CO2 stream from the pressurized gas insuf- port, transcellular transport, pinocytosis, plasmalemmal flator has a velocity of up to 20–30 m/s [2, 3, 5, 15] and vesicles and stomata [8]. Wilson: Effects of carbon dioxide pneumoperitoneum 19 Mesothelial cells are connected by tight gap junc- established and maintained. Desiccation of the peritoneal tions, integrins and cadherins and anchored to the actin mesothelium begins within 30 s with direct gas flow and cytoskeleton. The visceral peritoneal mesothelium con- in 8–10 min with indirect gas flow [2, 5, 19]. Along the tains flat, squamous like cells with lower resting meta- direct path of the CD CO2 jetstream the exposed tissues bolic rate and tight gap junctions, as compared to the can be rapidly cooled with a tissue