Postoperative microcirculatory perfusion and endothelial glycocalyx shedding following cardiac surgery with cardiopulmonary bypass

Dekker, Nicole; Veerhoek, Dennis; Koning, Nick J.; Leeuwen, Anoek L I van; Elbers, Paul; Brom, Charissa E. van den; Vonk, Alexander B.A.; Boer, Christa

doi:10.1111/anae.14577

Cited by 88 publications

(117 citation statements)

References 40 publications

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“…In both studies, median PBR values remained unchanged while an improvement in microvascular parameters was seen in the treatment groups. In contrast, two longitudinal studies conducted in patients undergoing cardiac surgery suggested the existence of an association between the alterations in microcirculation parameters and eGC dimensions [18,41]: Koning et al assessed the sublingual microcirculation and eGC dimensions perioperatively in 36 patients undergoing cardiac surgery with or without cardiopulmonary bypass (CPB) [18]. The CPB procedure increased the PBR and decreased the PVD, whereas offpump surgery decreased the PBR without affecting the PVD.…”

Section: Discussionmentioning

confidence: 99%

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Association of sublingual microcirculation parameters and endothelial glycocalyx dimensions in resuscitated sepsis

et al. 2019

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Background The endothelial glycocalyx (eGC) covers the luminal surface of the vascular endothelium and plays an important protective role in systemic inflammatory states and particularly in sepsis. Its breakdown leads to capillary leak and organ dysfunction. Moreover, sepsis-induced alterations of sublingual microcirculation are associated with a worse clinical outcome. The present study was performed to investigate the associations between eGC dimensions and established parameters of microcirculation dysfunction in sepsis. Methods This observational, prospective, cross-sectional study included 40 participants, of which 30 critically ill septic patients were recruited from intensive care units of a university hospital and 10 healthy volunteers served as controls. The established microcirculation parameters were obtained sublingually and analyzed according to the current recommendations. In addition, the perfused boundary region (PBR), an inverse parameter of the eGC dimensions, was measured sublingually, using novel data acquisition and analysis software (GlycoCheck™). Moreover, we exposed living endothelial cells to 5% serum from a subgroup of study participants, and the delta eGC breakdown, measured with atomic force microscopy (AFM), was correlated with the paired PBR values. Results In septic patients, sublingual microcirculation was impaired, as indicated by a reduced microvascular flow index (MFI) and a reduced proportion of perfused vessels (PPV) compared to those in healthy controls (MFI, 2.93 vs 2.74, p = 0.002; PPV, 98.53 vs 92.58, p = 0.0004). PBR values were significantly higher in septic patients compared to those in healthy controls, indicating damage of the eGC (2.04 vs 2.34, p < 0.0001). The in vitro AFM data correlated exceptionally well with paired PBR values obtained at the bedside (rs = − 0.94, p = 0.02). Both PBR values and microcirculation parameters correlated well with the markers of critical illness. Interestingly, no association was observed between the PBR values and established microcirculation parameters. Conclusion Our findings suggest that eGC damage can occur independently of microcirculatory impairment as measured by classical consensus parameters. Further studies in critically ill patients are needed to unravel the relationship of glycocalyx damage and microvascular impairment, as well as their prognostic and therapeutic importance in sepsis. Trial registration Retrospectively registered: Clinicaltrials.gov, NCT03960307 Electronic supplementary material The online version of this article (10.1186/s13054-019-2542-2) contains supplementary material, which is available to authorized users.

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Section: Discussionmentioning

confidence: 99%

“…The CPB procedure increased the PBR and decreased the PVD, whereas offpump surgery decreased the PBR without affecting the PVD. Dekker et al analyzed the sublingual microvasculature in 17 patients undergoing non-pulsatile CPB [41]. They found a small increase in PBR and a sustained decrease in PVD and PPV during the 72-h follow-up.…”

Section: Discussionmentioning

confidence: 99%

Association of sublingual microcirculation parameters and endothelial glycocalyx dimensions in resuscitated sepsis

et al. 2019

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“…Loss of glycocalyx dimensions in the phosphorylcholine coating group after cardiac surgery is most likely the result of step-by-step shedding of its constituents, which is in accordance with previous studies. 5,7,20 The endothelial glycocalyx consists of core proteoglycans, such as syndecans, that are firmly bound to the endothelial cell membrane. These proteoglycans are the backbone for binding glycosaminoglycan side chains, such as the negatively charged glycosaminoglycan heparan sulphate, that influences the interaction of chemokines with endothelial receptors and is distributed predominately on the luminal side of the glycocalyx.…”

Section: Discussionmentioning

confidence: 99%

Microvascular Alterations During Cardiac Surgery Using a Heparin or Phosphorylcholine-Coated Circuit

Dekker

Veerhoek

Leeuwen

et al. 2020

Journal of Cardiothoracic and Vascular Anesthesia

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Objective: Heparin biocompatible coating frequently is used to reduce inflammation and blood coagulation during cardiopulmonary bypass (CPB) in cardiac surgery. Whether heparin coating is protective or damaging to the vascular endothelium is unclear. The authors investigated whether heparin-coated (HC) circuits are associated with better preservation of microcirculatory perfusion and glycocalyx dimensions compared with nonheparin phosphorylcholine-coated (PC) circuits. Design: Prospective, randomized blinded study. Setting: Tertiary university hospital. Participants: A total of 26 adults undergoing elective coronary artery bypass graft surgery with CPB. Interventions: PC (n = 13) versus HC circuits (n = 13). Measurements and Main Results: Sublingual microcirculatory perfusion was measured before, during, and after CPB using sidestream dark field imaging and analyzed for perfused vessel density and perfused boundary region, an inverse parameter for glycocalyx dimensions. Onset of CPB was associated with an increase in perfused boundary region in the PC group that continued until the third postoperative day (2.0 § 0.2 to 2.5 § 0.2 mm; p = 0.018). This was paralleled by increased plasma syndecan-1 levels in the PC group. Contrastingly, both parameters remained unaltered in the HC group compared with baseline levels. CPB decreased perfused vessel density in both groups (CPB v pre-CPB: PC: 17 § 2 to 13 § 2 mm/mm 2 , p = 0.006; HC: 16 § 2 to 11 § 2 mm/mm 2 , p = 0.003) and remained equally altered in the first 3 postoperative days. Conclusion: The use of an HC circuit is associated with better preservation of the endothelial glycocalyx compared with PC circuits, whereas microcirculatory perfusion was disturbed equally in both groups. Hence, CPB-induced microcirculatory perfusion disturbances seem to be coating independent.

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“…Endogenous NO was prone to be depleted by extracorporeal circulation in cardiac surgery, which may impair microcirculation and cause tissue ischemia, metabolic abnormalities, and organ dysfunction . In our study, intravenous administration of high‐dose NTG provided exogenous NO, which may normalize the physiologic regulation of microvascular networks during CPB.…”

Section: Discussionmentioning

confidence: 71%

“…CPB in cardiac surgery carries the risk of end‐organ damage, exerting a significant impact on outcomes in cardiac surgical patients . CPB‐related microcirculatory derangement contributes to the pathogenesis of organ damage, including tissue hypoperfusion, ischemia‐reperfusion, oxidative stress response, and hemolysis . Hemolysis elevates concentration of plasma free hemoglobin, which may scavenge and deplete intravascular NO …”

Section: Introductionmentioning

confidence: 99%

High‐dose nitroglycerin administered during rewarming preserves erythrocyte deformability in cardiac surgery with cardiopulmonary bypass

Tai

Chu

et al. 2020

Microcirculation

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Objective:We aimed to determine whether high-dose nitroglycerin, a nitric oxide donor, preserves erythrocyte deformability during cardiopulmonary bypass and examines the signaling pathway of nitric oxide in erythrocytes. Methods:In a randomized and controlled fashion, forty-two patients undergoing cardiac surgery with hypothermic cardiopulmonary bypass were allocated to high-dose (N = 21) and low-dose groups (N = 21). During rewarming period, patients were given intravenous nitroglycerin with an infusion rate 5 and 1 µg·kg −1 ·min −1 in high-dose and low-dose groups, respectively. Tyrosine phosphorylation level of non-muscle myosin IIA in erythrocyte membrane was used as an index of erythrocyte deformability and analyzed using immunoblotting.Results: Tyrosine phosphorylation of non-muscle myosin IIA was significantly enhanced after bypass in high-dose group (3.729 ± 1.700 folds, P = .011) but not low-dose group (1.545 ± 0.595 folds, P = .076). Phosphorylation of aquaporin 1, vasodilator-stimulated phosphoprotein, and focal adhesion kinase in erythrocyte membrane was also upregulated in high-dose group after bypass. Besides, plasma nitric oxide level was highly correlated with fold change of non-muscle myosin IIA phosphorylation (Pearson's correlation coefficient .871). Conclusions: High-dose nitroglycerin administered during cardiopulmonary bypass improves erythrocyte deformability through activating phosphorylation of aquaporin 1, vasodilator-stimulated phosphoprotein, and focal adhesion kinase in erythrocytes. K E Y W O R D S aquaporin 1, focal adhesion kinase, nitric oxide, non-muscle myosin IIA, vasodilatorstimulated phosphoprotein S U PP O RTI N G I N FO R M ATI O N Additional supporting information may be found online in the Supporting Information section.

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Postoperative microcirculatory perfusion and endothelial glycocalyx shedding following cardiac surgery with cardiopulmonary bypass

Cited by 88 publications

References 40 publications

Association of sublingual microcirculation parameters and endothelial glycocalyx dimensions in resuscitated sepsis

Association of sublingual microcirculation parameters and endothelial glycocalyx dimensions in resuscitated sepsis

Microvascular Alterations During Cardiac Surgery Using a Heparin or Phosphorylcholine-Coated Circuit

High‐dose nitroglycerin administered during rewarming preserves erythrocyte deformability in cardiac surgery with cardiopulmonary bypass

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