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Eur J Cardiothorac Surg 1999;14:290-295
© 1999 Elsevier Science NL

Soluble adhesion molecules in reperfusion during coronary bypass grafting¹

^a J. Strus Hospital Poznan, Poland
^b Imperial College School of Medicine, Division of NHLI, St. Mary's Hospital, London, UK
^c University of Medical Sciences, Poznan, Poland

Received 10 March 1998; received in revised form 19 May 1998; accepted 3 June 1998.

Corresponding author. Department of Cardiology, Przybyszewskiego 49, 60–355 Poznan, Poland. Tel.: +48 61 691391; fax: +48 61 671232.

	Abstract

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Objective: Adhesion of activated leukocytes to the endothelial cells as a result of myocardial ischaemia/reperfusion during open chest coronary artery surgery has been shown to be involved in the development of tissue damage. Activated leukocytes adhere to endothelium via adhesion molecules expressed by both cell types, resulting in the impairment of coronary capillary flow. Upon cell activation, adhesion proteins may be released in the soluble form to circulating blood. The purpose of our study was to verify whether myocardial ischaemia/reperfusion occurring during coronary artery bypass grafting results in release of the soluble adhesion molecules VCAM-1, ICAM-1, E-selectin and L-selectin into the circulation. Methods: Plasma levels of the soluble adhesion molecules were measured in vein, arterial and coronary sinus blood samples taken from 15 patients undergoing coronary artery bypass grafting (CABG). Blood samples for estimations were collected during the procedure: before aorta cross-clamping, at the beginning of reperfusion and 30 min after reperfusion. Soluble adhesion molecules levels were measured by standard ELISA assays. Results: Mean plasma levels of soluble VCAM-1 in arterial samples increased significantly at the beginning of reperfusion and 30 min after reperfusion. In contrast, soluble L-selectin plasma levels in arterial samples remained unchanged. In coronary sinus samples, levels of soluble ICAM-1 significantly increased 30 min after reperfusion. Moreover, in coronary sinus samples collected 30 min after reperfusion, soluble ICAM-1 levels were significantly higher than in arterial samples obtained at the same time. The mean concentration of soluble E-selectin in samples obtained from coronary sinus decreased significantly 30 min after reperfusion. Moreover, plasma levels of soluble E-selectin in coronary sinus samples obtained 30 min after reperfusion were significantly decreased compared with these observed in arterial samples collected at the same time. Conclusions: The reperfusion of ischaemic myocardium during CABG results in a significant increase in plasma levels of the soluble endothelial adhesion molecules VCAM-1 and ICAM-1 and significant decrease in soluble E-selectin plasma levels. L-selectin plasma levels during CABG procedure remain unchanged. We propose that the increased plasma concentrations of soluble VCAM-1 and ICAM-1 are a result of endothelial cell activation during ischaemia/reperfusion following bypass surgery.

Key Words: Soluble ICAM-1 • VCAM-1 • E-selectin and L-selectin • Coronary artery bypass grafting

	Introduction

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There is considerable evidence suggesting that leukocyte/endothelial cells adhesive interactions may play an essential role in the genesis of tissue damage in ischaemia/reperfusion disorders. The adhesion of monocytes and neutrophils to vascular endothelial cells requires the expression of adhesion molecules on the surface of these cells. These proteins belong to one of three major families of adhesion molecules: the integrins, the immunoglobulin superfamily and the selectins family.

Vascular cell adhesion molecule-1 (VCAM-1, CD106) is a member of the immunoglobulin supergene family and is predominantly expressed by synovial lining cells, germinal centre dendritic cells, bone marrow derived fibroblasts, and macrophages [1]. Unstimulated endothelial cells (EC) expressed very little cell surface VCAM-1. During exposure to the pro-inflammatory agents, however, this adhesion molecule becomes prominently expressed by EC [2]. Agonists which induce VCAM-1 expression on endothelium surface are IL-1ß, IL-4, TNF and TNF [3].

Intracellular adhesion molecule-1 (ICAM-1, CD54) also belongs to the immunoglobulin family of adhesion receptors that mediate many cell-cell adhesive interactions with endothelium. ICAM-1 is weakly expressed on leukocytes and resting endothelial cells, as well as some other cell types, but its expression is increased following the exposure of EC to IL-1ß, TNF and lipopolysaccharides (LPS) [4]. Interactions between ICAM-1 and integrins, such as leukocyte function-associated antigen-1 (LFA-1, CD11a/CD18) or macrophage-1 antigen (Mac-1, CD11b/CD18) play an important role in the margination and extravasation of leukocytes into inflammatory sites. [4]

E-selectin (ELAM-1, CD62E) is also known to mediate endothelial cell interactions with leukocytes. E-selectin is expressed on activated microvascular endothelium, predominantly in a variety of acute and chronic inflammatory conditions. Its expression is induced by IL-1, TNF and LPS [5]. This selectin is very slowly and moderately activated over the initial 4–5 h of activation during reperfusion [6]. E-selectin is probably involved in the same adherence pathway of neutrophils to the endothelium as neutrophilic L-selectin and thus mediates PMN margination and transvasation [7].

L-selectin (LAM-1, CD62L) is constitutively expressed by resting leukocytes (mainly lymphocytes and neutrophils), and is rapidly shed from the surface of these cells following their activation [6] [8]. L-selectin is an important factor in the regulation of PMN trafficking and the earliest contact between the leukocytes and the endothelial cells – leukocyte rolling along endothelium [9]. Administration of monoclonal antibody (mAb) against L-selectin reduces cardiac necrosis and preserves coronary vascular endothelial functions in an experimental model of myocardial ischaemia-reperfusion [10]. Several studies have confirmed the involvement of leukocyte and endothelial adhesion molecules in the enhanced leukocyte adherence to endothelial cells during myocardial ischaemia. In patients with unstable angina, PMN taken from the coronary sinus showed increased expression of the CD11b/CD18 complex, in comparison with neutrophils taken from the aorta, indicating a transcardiac increase in expression of PMN adhesion molecules as a result of myocardial ischaemia [8]. Recent studies have shown that L-selectin is involved in neutrophil extravasation and their subsequent accumulation in ischaemic myocardium [6]. Administration of mAbs against L-selectin diminishes myocardial necrosis and decreases accumulation of PMN in ischaemic myocardium in experimental model of ischaemia/reperfusion [11] [12]. Similarly, administration of mAbs against epitopes of ICAM-1 reduces myocardial infarct size in rabbit model of coronary artery occlusion and reperfusion [15].

During acute myocardial infarction plasma contains a variety of stimuli capable of PMN and endothelial cells activation [13]. In this condition, adhesion molecules may be released by both these cells into circulating blood and be detected in their soluble form [14].

In the present study, we investigated the plasma concentrations of endothelial adhesion molecules VCAM-1, ICAM-1 and E-selectin, and leukocyte L-selectin during coronary artery bypass grafting.

	Material and methods

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Plasma concentration of soluble adhesion molecules were studied in 15 patients (four females and 11 males; aged 45–72 years, mean 61.2 years) who underwent first-time coronary-artery bypass grafting. Patients who had repeated surgery and those with diabetes mellitus were excluded. Exclusion criteria also included inotropic support or use of an intra-aortic balloon pump at the time of surgery. In six cases the indication for surgery was left main stem stenosis. In five cases the reason for the operation was combined disease of the proximal LAD and circumflex coronary artery and, in four cases, three-vessel coronary artery disease. The operative procedure was performed using cardiopulmonary bypass at moderate hypothermia (30–32°C) with hemodilution. Cardioplegic arrest was induced with cold high-potassium solution and maintained with additional doses administered at approximately 15–20 min intervals. After grafting, the patients were rewarmed to 36°C and separated from cardiopulmonary bypass by the gradual reduction of venous return to the bypass circuit. Samples of arterial, vein and coronary sinus blood for determination of plasma soluble VCAM-1, ICAM-1, E-selectin and L-selectin concentrations, were drawn before aorta cross-clamping (at the start of cardiopulmonary bypass), at the beginning of reperfusion and at 30 min after reperfusion. The samples were centrifuged immediately and the plasma was deeply frozen (-70°C) until analysis.

Soluble (s) adhesion molecules VCAM-1, ICAM-1, E-selectin and L-selectin were assayed using a double primary antibody sandwich ELISA (R and D Systems, Abingdon) in which one antibody (clone) was coated to the well surface (96-well format) and the second probe antibody was horseradish peroxidase (HRP)-conjugated, in solution. Upon thawing, samples were diluted 1:20 in a 96 well plate in dilution buffer. Standards and reagent controls were added to the plate. EDTA (4 mM) was added to the L-selectin dilution buffer to maintain an anticoagulant medium. HRP-conjugate was added to the plate (100 µl/well) and the reaction was started by transferring the samples and standards (100 µl) to the test plate. After 90 min, wells were washed 200 mlx7 and drained. HRP substrate solution (benzidine, 100 µl/well) was added, followed, after 30 min, by incubation by H₂SO₄ 2 M 100µl/well to stop the reaction. The plates were read in a Titretec Multiscan II (Labsystems, Basingstoke) 96-well plate spectrometer at 450 nm, with care being taken to remove bubbles prior to measurement. Reagent blank readings were subtracted from all data. Standard data were reduced by least squares linear regression, and sample concentrations were calculated.

Since our data were not normally distributed, as assessed by the Kolomogorov–Smirnov test, comparison of the groups was performed by the non-parametric Mann–Whitney test and comparisons within groups by non-parametric ANOVA. Data are given as mean±SEM.

	Results

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In patients subjected to coronary-artery bypass surgery, soluble VCAM-1 plasma mean concentration determined in arterial blood samples obtained before cardiopulmonary bypass was 610±27.9 ng/ml and increased significantly at the beginning of reperfusion and at 30 min after reperfusion (896.6±20.8 and 1105.1±19.9 ng/ml, respectively; P<0.05) ( Fig. 1 ). In contrast to soluble VCAM-1, soluble L-selectin plasma levels in arterial blood samples obtained at the start of bypass surgery were 733.4±38.5 ng/ml and did not decrease significantly at the beginning of reperfusion and at 30 min after reperfusion (699.0±37.7 and 677.9±92.2 ng/ml, respectively) ( Fig. 2 ).

View larger version (34K): [in this window] [in a new window]   Fig. 1. Soluble VCAM-1 plasma concentrations (mean±SEM) in blood samples obtained from coronary sinus (cor. sin.), peripheral artery (per. art.) and peripheral vein (per. vein), before aortal cross-clamping (before ischaemia), at the beginning of reperfusion (start of reperf.) and at 30 min of reperfusion. *P<0.05 versus before schema **P<0.05 versus peripheral artery.

View larger version (46K): [in this window] [in a new window]   Fig. 2. Soluble L-selectin plasma concentrations (mean±SEM) in blood samples obtained from coronary sinus (cor. sin.), peripheral artery (per. art.) and peripheral vein (per. vein), before aortal cross-clamping (before ischaemia), at the beginning of reperfusion (start of reperf.) and at 30 min of reperfusion.

View larger version (32K): [in this window] [in a new window]   Fig. 3. Soluble ICAM-1 plasma concentrations (mean±SEM) in blood samples obtained from coronary sinus (cor. sin.), peripheral artery (per. art.) and peripheral vein (per. vein), before aortal cross-clamping (before ischaemia), at the beginning of reperfusion (start of reperf.) and at 30 min of reperfusion. *P<0.05 versus beginning of reperfusion, **P<0.05 versus peripheral artery.

View larger version (51K): [in this window] [in a new window]   Fig. 4. Soluble E-selectin plasma concentrations (mean±SEM) in blood samples obtained from coronary sinus (cor. sin.), peripheral artery (per. art.) and peripheral vein (per. vein), before aortal cross-clamping (before ischaemia), at the beginning of reperfusion (start of reperf.) and at 30 min of reperfusion. *P<0.05 versus beginning of reperfusion, **P<0.05 versus peripheral artery.

	Discussion

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ICAM-1 belongs to the most abundant family of cell surface molecules, immunoglobulin superfamily. Elevated plasma levels of biologically active form of ICAM-1 are found in patients with various inflammatory syndromes such as septic shock, leukocyte adhesion deficiency, cancer and transplantation [16]. Soluble ICAM-1 plasma levels rise not only following the acute exposure of endothelial cell to pro-inflammatory cytokines but also in many chronic disorders of the cardiovascular system. Tsutamoto et al. [17] showed that in patients with chronic congestive heart failure, plasma concentrations of soluble ICAM-1 increase with the severity of disease and decrease in some cases after treatment with improvements in symptoms. Another adhesion molecule that is found in a soluble form in plasma following endothelial cells activation is VCAM-1. This adhesion molecule appears to play a major role in the initial binding of T lymphocytes to cytokine-activated endothelium [18]. The VCAM-1 are also well-known participants in extravasation of lymphocytes already bound to the EC (during interaction with VLA-4 on a surface of these cells) [19].

The results of our study indicate that myocardial ischaemia/reperfusion occurring during CABG is associated with a significantly increased release of soluble VCAM-1 and ICAM-1 into the circulation. These data may suggest a pivotal role for VCAM-1 and ICAM-1 in the mediation of the interaction between endothelium and circulating blood cells after CABG. Increased levels of ICAM-1 and VCAM-1 found in the coronary sinus during reperfusion, as compared to the peripheral artery samples, confirm their transcardiac release.

Neutrophilic L-selectin appears to mediate the initial adhesive interactions between non-activated leukocytes and the stimulated endothelium (leukocyte rolling and reversible sticking). Lymphocytes and neutrophils exhibit a reversible loss of L-selectin expression within minutes after cellular activation due to endoproteolytic release of the molecules from the cell surface [6].

Von Adrian et al. [10] report that systemic administration of anti-L-selectin monoclonal antibody (mAb) reduced the number of rolling cells in an in vitro rabbit model. The soluble form of L-selectin presumably blocked a ligand on activated endothelial cells. Studies in vivo demonstrated that reduction in number of polymorphonuclear neutrophils marginating on endothelial monolayers (e.g. with anti-L-selectin mAb) reduced transendothelial migration of these cells [20]. This observation may indicate the anti-inflammatory effects of the sL-selectin.

Gearing and Newman [21] have found elevated levels of L-selectin in the plasma of patients with AIDS and leukaemia, whereas decreased levels of this selectin were observed in the blood of patients with ARDS.

In the current study, we did not observe significant changes in soluble L-selectin plasma levels during myocardial reperfusion after coronary artery bypass grafting. It seems probable that the lack of detectable shedding of this selectin from leukocytes during CABG may be at least partially related by their de novo synthesis upon cell activation. Our previous observations showed that during myocardial ischaemia following angina pectoris episodes, the levels of sL-selectin may actually decrease [22]. We have also observed a decrease in sL-selectin plasma concentrations in patients with ischaemic heart disease after administration of dipyridamole, possibly as a result of `trapping' of circulating L-selectin by increased tissue expression of its counter receptors. We suggested that the lack of changes in plasma levels of soluble L-selectin during bypass surgery may be due to the balance between its increased shedding from activated leukocytes and increased banding to its tissue ligands (i.e. sialyl Lewis X). L-selectin plasma concentrations in patients subjected to coronary bypass grafting, on the other hand, may remain unchanged because of their de novo synthesis upon cell activation. Time needed for the release of soluble L-selectin may be longer than the duration of the procedure [6].

In contrast to L-selectin, E-selectin is expressed by activated endothelial cells, maximally 2–4h after activation via different inflammatory mediators and bacterial endotoxins [6]. It is found in arthritic joints, in heart and renal allografts undergoing rejection, and delayed-type of hypersensitivity reactions [6]. Mulligan et al. [23] reported that anti-E-selectin mAb administered systematically inhibited immune complex-induced inflammation in the skin and lungs.

In the present work we have found significantly decreased concentrations of soluble E-selectin in coronary sinus blood samples obtained at 30 min after reperfusion in comparison with those observed at the start of reperfusion. At the same time, plasma levels of sE-selectin measured in arterial blood samples remained unchanged. The exclusively transcardiac decrease of sE-selectin plasma concentrations during reperfusion indicates that tissue expression of counter-receptors for this selectin increase following CABG. Ligands for E-selectin were found on neutrophils (E-selectin Ligand-1; ESL-1), monocytes and lymphocytes (P-selectin Glycoprotein Ligand-1; PSGL-1) [6]. Moreover, E-selectin recognises and binds to phosphorylated oligosaccharides as ligands, for example, the sialyl-Lewis X and A [24].

The present investigation demonstrates that a statistically significant increase in plasma VCAM-1 and ICAM-1 adhesion molecules occurs in patients subjected to coronary artery bypass grafting. Furthermore, we noted a significant decrease in soluble E-selectin concentrations whereas L-selectin plasma levels remained unchanged. These observations indicate that stimuli inducing VCAM-1 and ICAM-1 expression appear in circulating blood during CABG. In addition, the increased shedding of adhesion molecules observed during coronary bypass grafting may be associated with their enhanced de novo synthesis and/or increased tissue expression of counter-receptors for these molecules. The intensity of this phenomenon may indicate the extent of cell activation during bypass surgery. Moreover, soluble adhesion molecules released during myocardial reperfusion into the circulation may modify endothelial-leukocyte-platelet interactions [25]. It may be speculated that therapeutic interventions, including the cardioplegic solutions, may modify cell activation and subsequent adhesion molecules release, however their clinical importance remains to be established.

	Acknowledgments

 
The study was supported by grant from Komitet Badan Naukowych (4P05A 02413).

	Footnotes

 
Presented in part at the XIX Congress of the European Society of Cardiology, Stockholm 1997 and published in abstract form in Eur. Heart J. 1997; 18 suppl.: 659.

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Kalawski, R. Articles by Siminiak, T. Search for Related Content PubMed PubMed Citation Articles by Kalawski, R. Articles by Siminiak, T.