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Sera From Children After Cardiopulmonary Bypass Reduces Permeability of Capillary Endothelial Cell Barriers
Richard W Pierce1, Riad Abou Zahr2, Sarah Kandil1
1Department of Pediatrics, Yale University, New Haven, CT.
Insights
Cardiopulmonary bypass in children unexpectedly reduces capillary leak. Post-bypass serum, unlike pre-bypass serum, showed less disruption of endothelial cell junctions and no significant inflammatory gene changes.
Area of Science:
- Pediatric cardiology
- Vascular biology
- Surgical research
Background:
- Children undergoing cardiopulmonary bypass (CPB) can experience capillary leak, a condition with unclear causes.
- A prevailing hypothesis suggests CPB circuit exposure triggers inflammatory mediators that disrupt endothelial cell junctions, leading to capillary leak.
Purpose of the Study:
- To investigate the effects of serum from children before and after CPB on capillary endothelial cell function and structure.
- To determine if CPB-associated serum induces inflammatory gene expression in endothelial cells.
Main Methods:
- Analyzed the impact of 10% patient sera (pre- and post-CPB) on cultured human dermal and pulmonary microvascular endothelial cells.
- Assessed barrier function using transendothelial electrical resistance (TEER).
- Examined junctional protein organization (claudin-5, VE-cadherin) via immunofluorescence and inflammatory gene expression via qRT-PCR.
Main Results:
- All sera initially increased TEER transiently, followed by a persistent loss of barrier function.
- Unexpectedly, post-CPB sera caused significantly less barrier dysfunction compared to pre-CPB sera.
- Junctional protein disruption was reduced with post-CPB sera, and inflammatory gene expression remained largely unaffected.
Conclusions:
- Contrary to the hypothesis, serum from children after CPB induced less capillary barrier disruption than pre-CPB serum.
- Patient sera did not significantly alter the expression of common inflammatory genes.
- The etiology of capillary leak during CPB requires further investigation beyond the tested inflammatory pathways.
Objectives:
Children undergoing cardiopulmonary bypass develop clinically impactful capillary leak of unclear etiology. A widely held hypothesis that exposure of circulating cells to the cardiopulmonary bypass circuit induces the release of inflammatory mediators that act to disrupt intercellular junctions of capillary endothelial cells inducing paracellular capillary leak either directly or through new gene expression.
Design:
Cohort study.
Setting:
Tertiary pediatric hospital.
Patients:
Twenty children undergoing surgery with cardiopulmonary bypass for congenital heart disease. Serum was collected before cardiopulmonary bypass, 2 hours after cardiopulmonary bypass, and 18 hours after cardiopulmonary bypass.
Interventions:
None.
Measurements And Main Results:
We analyzed the effects of 10% patient sera on the "function, structure, and gene expression" of cultured human dermal and pulmonary microvascular endothelial cells. Changes in barrier "function" were measured using transendothelial electrical resistance. Associations between changes in transendothelial electrical resistance and subject characteristics were analyzed using linear mixed effects model with area under the resistance curve as outcome. Changes in junctional "structure" were assessed by analyzing the organization of the endothelial cell junctional proteins claudin-5 and VE-cadherin using immunofluorescence microscopy. Changes in inflammatory "gene expression" were measured using real-time quantitative reverse transcription-polymerase chain reaction. All serum samples induced a transient, 120-minute increase in transendothelial electrical resistance followed by persistent loss of barrier function. Unexpectedly, sera collected postcardiopulmonary bypass-induced significantly less loss of barrier function in both dermal and pulmonary capillary endothelial cell compared with precardiopulmonary bypass sera. Consistent with the transendothelial electrical resistance results, claudin-5 and vascular endothelial-cadherin junctional staining showed less disruption in cultures treated with postcardiopulmonary bypass sera. Expression of genes commonly associated with inflammation was largely unaffected by patient sera.
Conclusions:
Contrary to the hypothesis, sera taken from children after cardiopulmonary bypass induces less capillary barrier disruption relative to sera taken from children before cardiopulmonary bypass, and none of the sera induced significant changes in expression of inflammatory genes.
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