Extracorporeal circulation increases proliferation in the intestinal mucosa in a large animal model

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Abstract

Objective:

Extracorporeal circulation induces ischemia/reperfusion injury in the small intestinal wall. One reason for this damage is a perfusion shift from the muscular toward the mucosal layer. This study investigated the effect of this perfusion shift on the small-intestinal apoptosis and proliferation.

Methods:

Twenty-eight pigs were randomly assigned to the following cohorts and underwent a thoracolaparotomy and a 1 hour main procedure: cohort I: control; cohort II: thoracic aortic cross-clamping (TAC) without perfusion; cohort III: TAC and distal aortic perfusion (DAP); cohort IV: TAC, DAP, and selective visceral perfusion. The main procedure was followed by 2 hours of reperfusion in all cohorts. Tissue samples were taken during the experiment, stained, and analyzed for apoptosis and proliferation (caspase-3, annexin-V, terminal deoxynucleotide transferase-mediated deoxy uridine triphosphate nick-end labeling, and proliferating cell nuclear antigen). Six animals died unexpectedly during the experiment and were excluded from the analysis.

Results:

Extensive tissue damage and necrosis was only found in cohort II after the main procedure. In the mucosa, the proliferation was increased in cohort III at the end of the experiment (P= .0157 cohort I vs II). In contrast, the annexin-V/proliferating cell nuclear antigen ratio was significantly higher in cohorts II and IV than in cohorts I and II at the end of the experiment (P= .0034). Furthermore, the caspase-3/annexin-V ratio was increased in all cohorts at the end of the experiment (P= .0015).

Conclusions:

Mucosal proliferation is the early repair mechanism of the limited small intestinal ischemia/reperfusion injury after DAP. Furthermore, the extensive surgical trauma shifted the mucosal apoptosis into an advanced state.

Clinical Relevance:

This study investigated the effect of extracorporeal circulation (ECC) with distal aortic perfusion or selective visceral perfusion on intestinal mucosal proliferation and apoptosis in a porcine model. Our results demonstrate that the mucosal apoptosis is moved into an advanced state due to the surgical trauma. The mucosal proliferation increases after distal aortic perfusion as an early repair mechanism of the ECC-induced ischemia/reperfusion injury of the intestine. Our study is important for the better understanding of the pathophysiology of ECC-related intestinal ischemia/reperfusion injury. In addition, it is of interest for the improvement of extracorporeal perfusion techniques during complex vascular surgical procedures.

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