Ann Thorac Surg 2004;78:543-548
© 2004 The Society of Thoracic Surgeons
Original article: cardiovascular
Chronic ultrastructural effects of temporary intraluminal shunts in a porcine off-pump model
Jens Wippermann, MDa*,
Johannes M. Albes, MDb,
Raimund Bruhin, MDa,
Martin Hartrumpf, MDb,
Rüdiger Vollandt, MDd,
Hartwig Kosmehl, MDc,
Thorsten Wahlers, MDa
a Department of Cardiothoracic and Vascular Surgery, University Hospital Jena, Jena, Germany
d Department of Medical Statistics, Informatics and Documentation, University Hospital Jena, Jena, Germany
b Heart-Center Brandenburg, Bernau, Germany
c Institute of Pathology, Helios Hospital, Erfurt, Germany
Accepted for publication February 18, 2004.
* Address reprint requests to Dr Wippermann, Department of Cardiothoracic and Vascular Surgery, University Hospital Jena, Erlanger Allee 101, 07747 Jena-Lobeda, Germany
e-mail: jens.wippermann{at}med.uni-jena.de
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Abstract
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BACKGROUND: Temporary intraluminal shunts (TILS) are routinely used in off-pump revascularization to facilitate the anastomosis while maintaining myocardial blood supply. Whereas tourniquet-occlusion can cause vessel wall trauma, potentially adverse chronic effects of TILS on the coronary intima have not been evaluated yet. This chronic large animal study investigated ultrastructural effects of TILS on the vessel wall.
METHODS: Four groups of acute and chronic pigs with either tourniquet-occlusion (TOUR) or TILS (40 kg; acute, n = 12; chronic, n = 20) were analyzed. Animals underwent median sternotomy, heparin (150 U/kg) administration, and left anterior descending coronary artery exposure. In groups with TOUR the left anterior descending coronary artery was temporarily occluded (10 minutes) with a tourniquet. In groups with TILS a silicone shunt (1.5 mm diameter, 12 mm length) was placed in the left anterior descending coronary artery more than 10 minutes and then removed, and the insertion was repaired. Thirty minutes after reperfusion all acute animals were sacrificed whereas chronic animals were extubated, maintained for 3 months, and then sacrificed. The left anterior descending coronary artery regions of occlusion or placement of the TILS silicone bulbs were examined histopathologically by scanning and transmission electron microscopy by a blinded pathologist.
RESULTS: In both acute and chronic investigations animals in the TILS group exhibited significantly less morphologic damage than animals in the TOUR group. In the acute phase significantly more loss of cell junction (p = 0.037), loss of endothelium (p = 0.032), and intimal edema (p = 0.037) in the TOUR group than in the TILS group was observed. Three months later, characteristic features with a changed pattern were detected: vacuolization of the cell (p = 0.03), loss of cell junction (p = 0.042), and removal of basal membrane (p = 0.046) as well as extensive loss of endothelium (p = 0.003) in the TOUR group compared with the TILS group.
CONCLUSIONS: Intimal lesions occur with both maneuvers early and late. However, animals in the TOUR group exhibited injuries significantly more often and more severely. Therefore, acute and chronic intimal integrity of the coronary vessel may be better preserved using TILS and may thus have a positive impact on the extent of de novo stenosis and long-term prognosis of the revascularized region.
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Introduction
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During a brief period, a large body of evidence has been accumulated regarding the potential benefits of off-pump coronary artery bypass grafting surgery as an alternative to conventional coronary artery bypass grafting surgery. Reports showing reduced neurocognitive deficits, less blood loss, shorter hospital stay, and reduced costs resulted in an increasing acceptance of this method [1–4]. Short-term and intermediate-term patency rate of the bypass grafts appear to match the results seen with conventional coronary artery bypass grafting [5, 6]. However, in contrast to conventional surgery, manipulation of the target coronary artery vessel is inevitable to achieve a bloodless surgical field and to perform a high-quality anastomosis. In the early experience with this new approach, flow of the incised vessel was controlled by means of tourniquet occlusion or intraluminal flow arrest. However, it was shown that both measures can result in critical myocardial ischemia with the potential result of cardiac fibrillation [7, 8]. Interestingly, temporary intraluminal shunts (TILS), which maintain adequate blood flow, had been introduced into clinical practice as early as 1975 [9]. We could recently demonstrate the feasibility of TILS in off-pump surgery in terms of avoidance of myocardial ischemia [10, 11]. It also allows us to accomplish the distal coronary anastomosis in a bloodless field and prevents inadvertent stitching of the back wall of the coronary artery. Tourniquet occlusion can be completely avoided when using TILS. This is important because it has been reported that tourniquets can be responsible for coronary artery damage [12, 13]. In a recent study we confirmed these findings of acute severe endothelial injury using tourniquets [13]. No studies exist so far demonstrating potentially adverse effects of TILS in the chronic situation. This study therefore was designed to investigate chronic ultrastructural effects of TILS in contrast to tourniquet occlusion on coronary artery vessels.
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Material and methods
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Study
All experiments were performed using juvenile white domestic pigs (40 ± 2 kg). The study was approved by the Animal Care and Use Committee of the Friedrich-Schiller University Jena. All animals received humane care in compliance with the "Guide for the Care and Use of Laboratory Animals" as revised by the National Institutes of Health in 1985. In the acute arm of the study 12 animals were randomly assigned to a tourniquet-occlusion group (TOUR; n = 6) or a temporary shunt group (TILS; n = 6). In the chronic arm, 20 pigs were randomly assigned to a TOUR group (n = 10) or a TILS group (n = 10).
Operative technique
Animals were anesthetized with intravenous injection of 150 µg · kg–1 · min–1 propofol (Disoprivan 2%, emulsion, Astra Zeneca, Wedel, Germany) and bolus injection of 2 to 5 µg/kg fentanyl (Janssen Cilag, Neuss, Germany). Ventilation support was established by intubation and connection to a respirator (Evita II dura; Dräger, Lübeck, Germany). Oxygen supplementation was given to maintain an arterial oxygen saturation of 97%. The animals were placed in a supine position. After preparation, a 19-gauge detaining needle was inserted into the right internal carotid artery for blood pressure monitoring and blood gas analysis. A 4F catheter was placed into the right external jugular vein for measurement of central venous pressure and volume replacement. After median sternotomy was performed, we exposed the heart by incising the pericardium, and heparin (300 U/kg) was given. We administered 100 mg of lidocaine (Xylocaine, 2%; Astra Zeneca, Wedel, Germany) to prevent fibrillating of the heart during preparation and metoprolol (7.5 mg Beloc, Astra Zeneca, Wedel, Germany) to reduce the heart rate from 120 beats/min to 70 beats/min. The mean arterial pressure was 72 ± 3 mm Hg. The midportion of the left anterior descending coronary artery (LAD) far distal to the first diagonal branch was dissected and prepared as for anastomosis in all animals. In the TOUR group the LAD was temporarily snared with monofilament (4-0 Prolene; Ethicon Inc, Somerville, NJ) suture approximately 1 cm proximal to the anastomosis. To reduce the risk of vascular injury very soft silicone tubes served as tourniquets. We used a wide stitch to avoid direct compression of the coronary vessel wall, providing a liberal amount of epimyocardial tissue. The same encircling suture was placed distal to the anastomotic site. The distance between both tourniquets varied from 2 to 3 cm. A small incision was made in the LAD to control for sufficient tension on the tourniquets to create a bloodless operative field. Tourniquet tension was applied with utmost care until blood flow ceased. After 10 minutes of occlusion tourniquets were released and the sutures were tied loosely to identify the regions for later investigation. Reperfusion was performed for 30 minutes. In the TILS group a commercially available silicone shunt (1.5 mm diameter, 12 mm length, AnastaFlo; Research Medical Inc, Midvale, UT) was placed in the LAD through a 2-mm longitudinal incision. The vessel was exposed under mechanical stabilization (CTS, Cupertino, CA). In every case the shunt diameter was slightly oversized compared with the respective size of the coronary artery. For the TILS insertion maneuver the proximal LAD was briefly occluded to obtain a bloodless surgical field. Insertion usually required not more than 35 seconds. After 10 minutes of perfusion the shunt was carefully removed, and the insertion was repaired by 8-0 Prolene suture, which simultaneously marked the region for further investigation. Thirty minutes of reperfusion followed. Whereas for the acute experiments animals of both groups were sacrificed at the end of the operative procedure by injection of pentobarbital (16% solution. Narcoren; Merial, Germany), for the chronic experiments they were allowed to grow for 3 months in a stable with free access to food and water and were then sacrificed in an identical fashion. During this period complete reendothelialization of the intimal layer was expected, as observed chronically after minimally invasive coronary artery stenting [14].
Procurement of tissue
After sacrificing the animals, resternotomy was performed using an oscillating saw. The heart was excised. The LAD was carefully dissected free from the myocardium and divided into 3-mm rings, including the regions of interest. Coronary cylinders of the TOUR group contained the areas of occlusions and of the TILS group, the placement of the shunts-silicone bulbs 7 mm apart from the insertion on each side. One cylinder of each group was investigated by scanning electron microscopy (SEM), the other one by transmission electron microscopy (TEM). Scanning electron microscope images provided an excellent three-dimensional overview of the intimal layer and its integrity, whereas more detailed information about alterations of the subendothelial matrix was given by TEM.
Histologic analysis
The tissue specimens were preserved by using 2.5% buffered glutaraldehyde and transferred to the Institute of Pathology. Samples were divided for TEM and SEM assessment. The latter samples were dehydrated through an ethanol series and freeze-dried. The tissue specimens including the coronary endothelial surface were coated with gold and analyzed by SEM (LEO 1450 VP/REM; Oberkochen-Zeiss, Germany). The analysis of preserved acute and chronic samples was performed by an independent pathologist in a blinded fashion, who graded the alterations: grade 0, characteristic injuries not found; grade 1, isolated existing; grade 2, usually existing; grade 3, always existing. The following characteristic injuries were applied for TEM: vacuolization (edema of mitochondria, Golgi apparatus, and endoplasmic reticulum blebs), loss of cell–cell junction (diminution of cell to cell contacts), removal of basal membrane (significant fenestration of the basal membrane), loss of endothelium (denudation of larger areas of endothelial cells), and intimal edema (marked fluid deposits in the subendothelial matrix). Injuries detected by SEM were described as uneven surface (resembling the paving-stone relief of the endothelium), endothelial delamination (exposure of subendothelial tissue), and extensive loss of endothelium (severe aggravation of local endothelial denudation).
Statistical analysis
Data were collected in a computerized database (Excel for Windows; Microsoft Corp, Redmond, WA). All morphologic features of both groups were compared by analysis of variance using SPSS for Windows statistical software package (SPSS, Inc, Chicago, IL). The frequency of the respective gradual values was compared with Pearson's 
2 test. A two-sided exact significance was assumed if p was less than 0.05.
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Results
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Clear evidence for local thrombus formation in the instrumented segments was not found in both groups, either acutely or in the chronic course. Injuries were distributed over the entire circumference, with no preference to a specific region of the vessel wall.
Acute experiments
In both TEM and SEM analysis, TOUR animals more often revealed grade 2 and 3 injuries than TILS animals (Table 1). With TEM the statistical comparison exhibited significantly less loss of cell junction (p = 0.037), less loss of endothelium (p = 0.032), and less intimal edema (p = 0.037) in TILS than in TOUR, whereas vacuolization and removal of basal membrane did not exhibit significant differences. Scanning electron microscope did not show statistical differences between TOUR and TILS in terms of uneven surface, endothelial delamination, and extensive loss of endothelium (Table 2).
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Table 1. Individual Injury Scores of Acute and Chronic Animals in Transmission and Scanning Electron Microscope Analysisa
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Chronic experiments
The extent of morphologic alterations decreased slightly in both groups after 3 months. Again, the occurrence of grade 2 and 3 injuries was higher in the TOUR group (Table 1). Transmission electron microscope exhibited significantly less vacuolization (p = 0.03), less loss of cell junction (p = 0.042), and less removal of basal membrane (p = 0.046) between TILS and TOUR whereas intimal edema (p = 0.077) and loss of endothelium did not differ statistically. In SEM statistical differences regarding uneven surface and endothelial delamination were not observed, whereas extensive loss of endothelium was significantly more pronounced in TOUR than in TILS (p = 0.03; Table 2).
An exemplary TEM view of an animal of the TILS group exhibiting a rather mild chronic injury is provided in Figure 1. In contrast, a severe chronic intimal damage is shown in an exemplary view of an animal of the TOUR group in Figure 2. Exemplary SEM views of mild endothelial damage in the TILS cohort and still-existing denudation in the TOUR group 3 months after surgery are presented in Figures 3 and 4.
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Fig 1. Transmission electron microscopy (x3,300) shows an example of mild injury in the temporary intraluminal shunt group after 3 months. (V1 = vacuolization, grade 1; V2 = loss of cell–cell junction with intimal edema, grade 1; V3 = intact endothelium.)
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Fig 2. Transmission electron microscopy (x3,550) reveals an existence of a severe intimal injury in the tourniquet occlusion group after 3 months. (V1 = loss of endothelial layer, grade 3; V2 = intimal edema, grade 3.)
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Fig 3. Three months after surgery. Scanning electron microscopy (x835) represents an example of an intact endothelial surface after temporary intraluminal shunt insertion. The surface is uneven, grade 2, but without delamination or extensive loss of endothelium. (WD = work distance.)
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Fig 4. Scanning electron microscopy (x1,480) showing a denuded area in the chronic tourniquet occlusion group. Uneven surface, grade 3, and endothelial delamination, grade 3. (WD = work distance.)
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Comment
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Endothelial injury represents a critical initiating event in the pathogenesis of various vascular diseases including spontaneous arteriosclerosis. With the growing popularity of minimally invasive and off-pump coronary artery bypass grafting procedures, which require local control of the target artery to achieve a stabilized and dry operative field, the integrity of the endothelium is an important issue. Good visualization is mandatory to perform high-quality anastomoses, which are crucial for graft patency [15]. Local occlusion maneuvers involving tourniquet occlusion of the proximal and distal part of the coronary artery are considered to induce lesions resulting in stenosis in the respective location [12, 16]. In unfortunate situations, tourniquet placement and manipulation can even impede a septal branch with the consequence of septal myocardial infarction [17]. The use of TILS appears to be superior to the occlusion technique in terms of myocardial stunning and infarction [7, 11]. However, the ultrastructural effects of these devices on the coronary vessel wall have not yet been thoroughly assessed. In 1992, Gundry and coworkers [18] expressed concerns regarding the occurrence of coronary arterial lesions at the site of encircling tourniquets during off-pump surgery. Some case reports support this theory. Pagni and associates [12] described tourniquet injury in 15 patients after occlusion with 4-0 polypropylene suture. Izzat and colleagues [19] reported an atheromatous breakoff with distal embolization occurring from proximal tourniquet occlusion of the target coronary artery. However, Cremer and coworkers [20] performed tourniquet occlusion in 306 patients receiving a minimally invasive coronary artery bypass grafting procedure with excellent results. In a porcine model, Perrault and colleagues [21] demonstrated that occlusion of the proximal and distal LAD with a polytetrafluoroethylene suture over a silicone tubing prevented acute endothelial dysfunction. In an organ chamber, endothelium-dependent relaxation to serotonin was studied with rings taken from the LAD at the proximal snare site. Responses to potassium chloride and bradykinin were also compared. The authors arrived at the conclusion that snaring of the coronary artery does not cause endothelial dysfunction. Interestingly, the same group demonstrated in a consecutive study that removal of blood in the operative field by means of an air-jet (blower) alone resulted in endothelial damage [22]. In previous studies, we were able to show that TILS do maintain adequate flow conditions during anastomosis [7]. Additionally, we and others [13, 23] found clear evidence for a more severe acute damage of the coronary intima when using tourniquets compared with TILS. Temporary intraluminal shunts therefore appeared to be a reasonable alternative to tourniquet occlusion and have gained widespread acceptance during conventional and beating heart surgery during recent years [9]. Rivetti and Gandra [24] reported excellent short-term and long-term results in 500 consecutive off-pump cases. Nevertheless, particular concerns were raised regarding an assumed brushing effect on the endothelium [25]. In our study we could indeed demonstrate such an effect on the endothelium, perhaps owing to the inserting maneuver and use of a slightly oversized shunt. These findings diminished but still existed after 3 months. In contrast, our data demonstrated a marked and prolonged damage after tourniquet occlusion, in which loss of endothelial cell coverage was still detectable after a 3-month period. Fortunately, however, also after tourniquet occlusion chronic damage was lower compared with the initial extent. Considering the response to injury hypothesis [26], these chronic injuries may very well accelerate intimal hyperplasia. It is basic knowledge that chronic damage of the arterial endothelium leads to accumulation of lipid, adhesion of monocytes and platelets, and release of various growth factors, resulting in later migration and proliferation of smooth muscle cells [27]. Eventually, an injury applied acutely will result in development of significant stenosis or even occlusion independent of the quality of the anastomosis.
Limitations of the study
In this porcine model the coronary arteries are free of arteriosclerosis, so the experiment does not fully correspond with the real clinical setting. Thus, similar results may only be expected in humans with mild to moderate coronary artery disease. However, we believe that the loss of intimal cell coverage is even enhanced in patients with coronary sclerosis. The endothelium in these arteries is already dysfunctional so that repair mechanisms, which can be assumed in our healthy coronary model, are impeded [28]. Therefore, in humans the damage on the coronary vessel wall may be more pronounced after application of TILS or tourniquets. The particular mode of tourniquet occlusion of this study can be criticized. We used a simple but clinically established method used in quite a large and successful series by Cremer and colleagues [20] as well as in one of our clinical studies comparing the functional aspects of shunts versus tourniquets [7, 8]. The widespread use of occlusion techniques, however, has already resulted in a considerable evolution. As a consequence, a multitude of techniques currently exist [29, 30]. Some surgeons prefer elastic ligatures whereas others use silicone tubes as additional cushions anterior to the vessel. Furthermore, a variety of commercially available stabilizing plates with integrated ligature loops are also used. The benefit of a particular tourniquet occlusion technique can therefore only be elucidated in a different study comparing several of these strategies. Clearly, the most important aspect when using tourniquet occlusion is the force used to tighten the loop. If tension is applied too liberally, all protective measures such as cushions or soft ligatures will fail. The particular force that can be applied without creating harm to an individual vessel, however, can hardly be measured properly and remains elusive.
Conclusion
The results of our present study suggest that TILS cause only moderate trauma to the vessel and may therefore be superior regarding acute and chronic intimal integrity in contrast to tourniquet occlusion. A positive impact on the absence of de novo stenosis and long-term prognosis of the revascularized region can therefore be assumed. However, our findings also shed light on the paradigm that the best anastomotic measure appears to be an intimal no-touch technique. Such a technique still exists in conventional coronary artery bypass grafting procedures with extracorporeal circulation, cardioplegic arrest, and venting of the aortic root. In light of the excellent long-term results of conventionally operated left internal mammary artery grafts, a definitive answer regarding the true value of off-pump coronary artery bypass grafting anastomoses may still be many years away.
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Acknowledgments
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The authors are most grateful for the financial support provided by a grant from the "Deutsche Forschungsgemeinschaft" AL-562/1–1.
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Abstract
Introduction
