Intra-Operative Tissue Oxygen Tension Is Increased by Local Insufflation of Humidified-Warm CO2 during Open Abdominal Surgery in a Rat Model

Marshall, Jean K.; Lindner, Pernilla; Tait, Noel; Maddocks, Tracy A.; Riepsamen, Angelique H; Linden, Jan van der

doi:10.1371/journal.pone.0122838

Cited by 17 publications

(24 citation statements)

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“…The mechanism(s) that drive this propensity for tumorigenesis include exposure of the ECM, and the induction of inflammatory processes demonstrable by the expression of COX‐2 and VEGF‐A. The loss of mesothelial cell integrity additionally affects oxygen tension during laparotomy, and the robust marker of hypoxia, HIF‐1α, was induced during laparotomy in the present study. HIF‐1α was evident 1 day after open surgery, indicating a persistence of the signals that induce the expression of, and/or lead to, HIF‐1α protein stabilization.…”

Section: Discussionmentioning

confidence: 56%

“…Here, the delivery of HWCO 2 under laparotomy conditions was investigated, in the presence and absence of simulated surgical damage, to evaluate the primary objective of induced hypoxia, tissue damage and tissue repair. Others have reported maintenance of oxygenation of the peritoneum with HWCO 2 and, in view of these data, the expression of a sentinel marker of hypoxia, hypoxia inducible factor (HIF) 1α, was examined. The secondary objective was to assess changes in the potential of cancer cells to attach to sites of surgical damage.…”

Section: Introductionmentioning

confidence: 99%

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Experimental study of delivery of humidified-warm carbon dioxide during open abdominal surgery

Carpinteri

Sampurno

Malaterre

et al. 2018

Journal of British Surgery

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BackgroundThe aim of this study was to monitor the effect of humidified‐warm carbon dioxide (HWCO2) delivered into the open abdomen of mice, simulating laparotomy.MethodsMice were anaesthetized, ventilated and subjected to an abdominal incision followed by wound retraction. In the experimental group, a diffuser device was used to deliver HWCO2; the control group was exposed to passive air flow. In each group of mice, surgical damage was produced on one side of the peritoneal wall. Vital signs and core temperature were monitored throughout the 1‐h procedure. The peritoneum was closed and mice were allowed to recover for 24 h or 10 days. Tumour cells were delivered into half of the mice in each cohort. Tissue was then examined using scanning electron microscopy and immunohistochemistry.ResultsPassive air flow generated ultrastructural damage including mesothelial cell bulging/retraction and loss of microvilli, as assessed at 24 h. Evidence of surgical damage was still measurable on day 10. HWCO2 maintained normothermia, whereas open surgery alone led to hypothermia. The degree of tissue damage was significantly reduced by HWCO2 compared with that in controls. Peritoneal expression of hypoxia inducible factor 1α and vascular endothelial growth factor A was lowered by HWCO2. These effects were also evident at the surgical damage sites, where protection from tissue trauma extended to 10 days. HWCO2 did not reduce tumorigenesis in surgically damaged sites compared with passive air flow.ConclusionHWCO2 diffusion into the abdomen in the context of open surgery afforded tissue protection and accelerated tissue repair in mice, while preserving normothermia. Surgical relevanceDamage to the peritoneum always occurs during open abdominal surgery, by exposure to desiccating air and by mechanical trauma/damage owing to the surgical intervention. Previous experimental studies showed that humidified‐warm carbon dioxide (HWCO2) reduced peritoneal damage during laparoscopic insufflation. Additionally, this intervention decreased experimental peritoneal carcinomatosis compared with the use of conventional dry‐cold carbon dioxide.In the present experimental study, the simple delivery of HWCO2 into the open abdomen reduced the amount of cellular damage and inflammation, and accelerated tissue repair. Sites of surgical intervention serve as ideal locations for cancer cell adhesion and subsequent tumour formation, but this was not changed measurably by the delivery of HWCO2.

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Section: Discussionmentioning

confidence: 56%

Section: Introductionmentioning

confidence: 99%

Experimental study of delivery of humidified-warm carbon dioxide during open abdominal surgery

Carpinteri

Sampurno

Malaterre

et al. 2018

Journal of British Surgery

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“…During open abdominal surgery, however, intra-abdominal tissue O 2 tension was increased by local insufflation of warm humid CO 2 in a rat model. The degree of improvement in peritoneal oxygenation (PtO 2 ) was 28.8 mmHg or 96.6 % [45].…”

Section: Systemic Effects Of Co 2 -Pneumoperitoneum In Animal Modelsmentioning

confidence: 99%

“…After laparoscopic or open colonic surgery, both the human peritoneal cytokine response and the incidence of postoperative adhesions are similar. This suggests both operative approaches can be equally traumatic to the mesothelial surface [45,49,68,69]. Peritoneal cytokine levels rise rapidly after peritoneal injury, starting with TNFα and quickly followed by IL-1β.…”

Section: Postoperative Adhesionsmentioning

confidence: 99%

Changes in the coelomic microclimate during carbon dioxide laparoscopy: morphological and functional implications

Wilson

2017

Pleura and Peritoneum

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In this article the adverse effects of laparoscopic CO 2 -pneumoperitoneum and coelomic climate change, and their potential prevention by warmed, humidified carbon dioxide insufflation are reviewed. The use of pressurized cold, dry carbon dioxide (C0 2 ) pneumoperitoneum causes a number of local effects on the peritoneal mesothelium, as well as systemic effects. These can be observed at a macroscopic, microscopic, cellular and metabolic level. Local effects include evaporative cooling, oxidative stress, desiccation of mesothelium, disruption of mesothelial cell junctions and glycocalyx, diminished scavenging of reactive oxygen species, decreased peritoneal blood flow, peritoneal acidosis, peritoneal hypoxia or necrosis, exposure of the basal lamina and extracellular matrix, lymphocyte infiltration, and generation of peritoneal cytokines such as IL-1, IL-6, IL-8 and TNFα. Such damage is increased by high CO 2 insufflation pressures and gas velocities and prolonged laparoscopic procedures. The resulting disruption of the glycocalyx, mesothelial cell barrier and exposure of the extracellular matrix creates a cascade of immunological and proinflammatory events and favours tumour cell implantation. Systemic effects include cardiopulmonary and respiratory changes, hypothermia and acidosis. Such coelomic climate change can be prevented by the use of lower insufflation pressures and preconditioned warm humidified CO 2 . By achieving a more physiological temperature, pressure and humidity, the coelomic microenvironment can be better preserved during pneumoperitoneum. This has the potential clinical benefits of maintaining isothermia and perfusion, reducing postoperative pain, preventing adhesions and inhibiting cancer cell implantation in laparoscopic surgery.

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“…The air may be "changed" more than 300 times per hour at a flow velocity of 0.2-0.5 m/s. This continual flow is a relevant variable when recapitulating the operating environment in animal models of open abdominal surgery as it may impact the local temperature of the wound and the evaporative capacity of the operating environment has a desiccating effect on abdominal surfaces [5,18].…”

Section: Statistical Analysesmentioning

confidence: 99%

Modeling open surgery in mice to explore peritoneal damage, carbon dioxide humidification and desmoidogenesis

Chittleborough¹,

Sampurno²,

Carpinteri³

et al. 2019

Pleura and Peritoneum

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BackgroundThe exposure of the peritoneum to desiccation during surgery generates lasting damage to the mesothelial lining which impacts inflammation and tissue repair. We have previously explored open abdominal surgery in mice subjected to passive airflow however, operating theatres employ active airflow. Therefore, we sought an engineering solution to recapitulate the active airflow in mice. Similarly, to the passive airflow studies we investigated the influence of humidified-warm carbon dioxide (CO2) on this damage in the context of active airflow. Additionally, we addressed the controversial role of surgery in exacerbating desmoidogenesis in a mouse model of familial adenomatous polyposis.MethodsAn active airflow mouse-operating module manufactured to produce the equivalent downdraft airflow to that of a modern operating theatre was employed. We quantified mesothelial cell integrity by scanning electron microscopy (SEM) sampled from the peritoneal wall that was subjected to mechanical damage or not, with and without the delivery of humidified-warm CO2. To explore the role of open and laparoscopic surgery in the process of desmoidogenesis we crossed Apcmin/+ C57Bl/6 mice with p53+/− mice to generate animals that developed desmoid tumors with 100% penetrance.ResultsOne hour of active airflow generates substantial damage to peritoneal mesothelial cells and their microvilli as measured at 24 h post intervention, which is significantly greater than that generated by passive airflow. Use of humidified-warm CO2 mostly protects the mesothelium that had not experienced additional mechanical (surgical) damage at 24 h. Maximal damage was evident in all treatment groups regardless of flow or use of gas. At day 10 mechanically-damaged peritoneum remains in mice but is essentially repaired in the gas-treated groups. Regarding desmoidogenesis, operating procedures did not increase the frequency of desmoid tumors but their frequency correlated with time following surgery but not age of mice.ConclusionsActive airflow generates more peritoneal damage than passive airflow and is reduced significantly by the use of humidified-warm CO2. Introduced peritoneal damage is largely repaired in mice by day 10 with gas. Desmoid tumor incidence is not increased substantially by surgery itself but rises over time following surgery compared to non-surgery mice.

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Intra-Operative Tissue Oxygen Tension Is Increased by Local Insufflation of Humidified-Warm CO2 during Open Abdominal Surgery in a Rat Model

Cited by 17 publications

References 59 publications

Experimental study of delivery of humidified-warm carbon dioxide during open abdominal surgery

Experimental study of delivery of humidified-warm carbon dioxide during open abdominal surgery

Changes in the coelomic microclimate during carbon dioxide laparoscopy: morphological and functional implications

Modeling open surgery in mice to explore peritoneal damage, carbon dioxide humidification and desmoidogenesis

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