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Ann Thorac Surg 1996;62:1158-1163
© 1996 The Society of Thoracic Surgeons

Original Articles: Cardiovascular

Endothelial Effects of Hemostatic Devices for Continuous Cardioplegia or Minimally Invasive Operations

Louis P. Perrault, MD, Philippe Menasché, MD, PhD, Michel Wassef, MD, Jean-Pierre Bidouard, PhD, Philip Janiak, DPharm, PhD, Nicole Villeneuve, PhD, Christine Jacquemin, Gérard Bloch, MD, Jean-Paul Vilaine, MD, Paul M. Vanhoutte, MD, PhD

Cardiovascular Division, Institut de Recherches Servier, Suresnes; and Departments of Cardiovascular Surgery and Pathology, Hôpital Lariboisière, Paris, France

Accepted for publication May 18, 1996.


   Abstract
Top
 Footnotes
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
Background. Improvements in myocardial protection may include the continuous delivery of normothermic blood cardioplegia. Technical aids are required for optimal visualization of the operative field during the performance of coronary anastomoses if cardioplegia is to be given continuously or during minimally invasive operations. However, the effects of the different hemostatic devices on coronary endothelial function are unknown.

Methods. We compared the effects on endothelial function of two commonly used hemostatic techniques, coronary clamping and gas jet insufflation, with those of a technique using extravascular balloon occlusion to mimic systolic luminal closure by the surrounding myocardium. The three techniques were applied for 15 minutes on porcine epicardial coronary arteries from explanted hearts. For coronary clamping, standard bulldog clamps were used. Gas jet insufflation was applied by blowing oxygen (12 L/min) tangentially at a 45-degree angle 1 cm away from a 3-mm arteriotomy. Extravascular balloon occlusion was achieved with a needle-tipped silicone loop, the midportion of which, once positioned beneath the coronary artery, was inflated to push a myocardial "cushion" against the back of the vessel until its occlusion. Control rings were taken from the same coronary artery. The endothelial function of control and instrumented arterial rings was then studied in organ chambers filled with modified Krebs-Ringer bicarbonate solution.

Results. Contractions to potassium chloride and prostaglandin F2{alpha} and endothelium-independent relaxation to sin-1, a nitric oxide donor, were unaffected in all groups. Endothelium-dependent relaxation to serotonin was impaired after clamping and preserved after gas jet insufflation and extravascular balloon occlusion. Maximal endothelium-dependent relaxation to serotonin was as follows: for coronary clamping, 63% ± 6% versus 87% ± 3% in controls; for gas jet insufflation, 67% ± 12% versus 88% ± 7%; and for extraluminal balloon occlusion, 79% ± 6% versus 85% ± 5%.

Conclusions. Whereas commonly used hemostatic devices may impair endothelial function, extravascular balloon occlusion appears to achieve effective hemostasis while preserving endothelial integrity.


   Introduction
Top
 Footnotes
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
Improvements in myocardial protection during cardiac operations include the continuous delivery of normothermic blood cardioplegia through the antegrade route or the coronary sinus [1]. Technical aids are required for optimal visualization of the operative field during the performance of coronary anastomoses in the course of coronary artery bypass grafting without interrupting cardioplegia delivery. Such aids are also required during the recently introduced minimally invasive operative revascularization techniques done without aortic cross-clamping when the operation is performed on the beating heart with local isolation of the target blood vessel [2, 3]. The techniques in use include saline solution irrigation through a syringe, intraluminal occluders, gas jet insufflation [4], clamping of coronary arteries, and extravascular occlusion with silicone loops or polypropylene sutures. However, the effects of these hemostatic devices on coronary arterial endothelial function are unknown.

The purpose of this study was to compare the effects on endothelial integrity of two commonly used hemostatic techniques, coronary clamping and oxygen gas jet insufflation, with those of a system specifically designed for minimizing arterial injury using extravascular balloon occlusion.


   Material and Methods
Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 Acknowledgments
 References
 
Operative Technique
All experiments were performed using Large White swine of either sex, aged 8 ± 1 weeks and weighing 23 ± 2 kg. Animals were treated in compliance with the "Guide for the Care and Use of Laboratory Animals" published by the National Institutes of Health (NIH publication 85-23, revised 1985). After anesthesia with a mixture of tiletamine and zolazepam (15 mg/kg) injected intramuscularly, the hearts were removed rapidly through a left thoracotomy and placed in modified Krebs-bicarbonate solution (composition in mmol/L: NaCl, 118.3; KCl, 4.7; MgSO4, 1.2; KH2PO4, 1.2; glucose, 11.1; CaCl2, 2.5; NaHCO3, 25; and calcium ethylenediamine tetraacetic acid, 0.026 [control solution]). Oxygenation was ensured using a carbogen mixture (95% O2 and 5% CO2). For coronary clamping and gas jet insufflation, the coronary arteries were dissected from the myocardium and placed in a silicone dish before application of the devices. Extraluminal balloon occlusion was applied on the heart immersed in physiologic solution before dissection of the coronary artery. The three hemostatic devices were applied for 15 minutes to mimic a longer than average duration of coronary anastomosis. Proximal epicardial segments of the left anterior descending, circumflex, and right coronary arteries were used randomly.

Experimental Groups
In the coronary clamping group (n = 9), a vascular bulldog clamp (no. 19-8090; Codman, Chatenay-Malabray, France) was applied before the removal of epicardial fat to simulate the perivascular cushion seen in clinical practice. The force needed to displace the jaws of the clamp more than 1 mm was 80 g. In the gas jet insufflation group (n = 7), oxygen insufflation at a mean flow of 12 L/min was applied tangentially at a 45-degree angle 1 cm away from a 3-mm coronary arteriotomy using a Visuflo surgical site visualization wand (Research Medical Inc, Midvale, UT). Endothelial function studies were performed on segments 3 mm proximal and distal, but not contiguous, to the arteriotomy. In some rings (n = 6), gas insufflation was applied directly in the lumen to study the effect of endoluminal gas delivery.

In the extravascular balloon occlusion group (n = 8), the extraluminal balloon occluder (Quest Medical, Allen, TX) consisted of a silicone loop mounted with a blunt half-circle 1-cm long needle with a 3-cm long balloon, 3 ml in volume, in its midsection (Fig 1Go). The occluder was applied by passage of the needle with a needle holder through the myocardium under the coronary artery at an approximate depth of 5 mm, and the silicone balloon was positioned symmetrically on both sides of the vessel. The balloon was initially inflated with 2.5 mL of air or saline, and coronary occlusion was confirmed using gentle irrigation with physiologic solution through the coronary vessel under study. After the occlusion period, the coronary artery was dissected free from the myocardium and divided into 4-mm rings, including the instrumented rings (with devices). Control rings were taken from the same coronary artery.



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  		Fig 1. . Extraluminal balloon occluder (69% of actual size).

 
Endothelial Function
The endothelial function of control and instrumented arterial rings was studied in organ chambers filled with control solution (20 mL). Responses to potassium chloride, serotonin, and sin-1 (3-morpholino sydnonimine, a nitric oxide donor) were compared. All studies were performed in the presence of indomethacin (10-5 mol/L, to exclude the production of endogenous prostanoids), propranolol (10-7 mol/L, to prevent the activation of ß-adrenergic receptors), and ketanserin (10-6 mol/L, to block serotonin 5HT-2 receptors). Each preparation was stretched to the point of its active length curve (usually 4 g), as determined by measuring the contraction to potassium chloride (30 mmol/L) at different levels of stretch, and then stabilized for 90 minutes. The maximal contraction was determined with potassium chloride. After washing and a 30-minute stabilization period, prostaglandin F2{alpha} (range, 2 x 10-6 to 10-5 mol/L) was added to achieve a contraction averaging 50% to 70% of the maximal contraction to KCl (60 mmol/L). Ketanserin was incubated 40 minutes before the addition of serotonin (10-10 to 10-5 mol/L). Endothelium-independent function was studied using increasing concentrations of sin-1 (10-9 to 10-5 mol/L). Before sin-1 was applied, the endothelium was gently removed by rubbing the luminal surface of the ring with a small wooden stick.

Morphologic Studies
Silver nitrate staining was used to evaluate the endothelial cell coverage. Staining was performed immediately after application of the hemostatic devices for 15 minutes. Coronary artery rings were opened longitudinally and pinned down on a silicone dish under a small amount of tension to ensure a uniform surface. Silver nitrate staining was performed for each set of rings (n = 6). Evaluation of endothelial coverage was performed by an independent evaluator. The protocol was as follows. The rings were first fixed for 10 minutes with buffered paraformaldehyde 4%. The rings were then washed for 1 minute with a HEPES sucrose buffer solution. Silver nitrate 0.25% was applied for 1 minute. Washing was performed for 1 minute before a second fixation for 2 minutes. The rings were exposed to light for 24 hours in a cacodylate buffer solution. En face endothelial preparations of coronary artery segments were made and examined under the light microscope. Microphotographs of representative areas were taken.

Light microscopic examination with Masson trichrome staining was performed on the myocardium surrounding the coronary artery (left anterior descending artery), under which the extravascular balloon occlusion device was applied. The device was applied in three distinct situations: (1) after passage of the needle and loop without inflation on an explanted, nonreperfused heart; (2) after 15 minutes of inflation on an explanted, nonreperfused heart; and (3) after 15 minutes of inflation on a beating heart and 30 minutes of reperfusion after deflation of the occluder.

Drugs
All solutions were prepared daily. Five-hydroxytryptamine creatinine sulfate (serotonin), prostaglandin F2{alpha}, ketanserin, indomethacin, and propranolol were purchased from Sigma Chemical Co (St. Quentin Falavier, France). Sin-1 was synthesized at the Servier Research Institute.

Statistical Analysis
Rings were excluded if they failed to contract to potassium chloride (exclusion rate less than 10%). Relaxation was calculated as a percentage of maximal contraction for each group and was expressed as mean ± standard error of the mean; n refers to the number of animals studied. Student's t test for paired or unpaired observations was used for statistical analysis. A p value of less than 0.05 was considered significant. Analysis of variance was performed to compare dose-response curves. The Newman-Keuls test was used as the post hoc test.


   Results
Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 Acknowledgments
 References
 
Endothelial Function
There were no differences in the amplitude of contractions to potassium chloride and prostaglandin F2{alpha} between the instrumented rings or the control group (Table 1Go). Maximal relaxation to serotonin was significantly lower in the coronary clamping group than in controls. Maximal relaxation was significantly lower in the gas jet insufflation group compared with controls. There was no difference in maximal relaxation between the extravascular balloon occlusion group and controls (see Table 1Go).


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  		Table 1. . Contraction and Relaxation Results in Coronary Arteries After Clamping, Gas Jet Insufflation, and Extravascular Balloon Occlusiona
 
Coronary rings submitted to clamping showed a significant reduction in relaxation to serotonin compared with controls (Fig 2AGo). Coronary rings submitted to gas jet insufflation showed no significant reduction of the relaxation to serotonin overall compared with control rings. Endoluminal application of the gas jet insufflator caused a significant reduction in the relaxation to serotonin compared with instrumented rings and control rings (Fig 2BGo). There were no differences in the relaxation to serotonin between rings submitted to the extravascular balloon occlusion and controls (Fig 2CGo).



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  		Fig 2. . (A, B, C) Cumulative concentration-response curves to serotonin in rings of porcine coronary arteries submitted to coronary clamping (n = 9), gas jet insufflation (n = 7), and extraluminal balloon occlusion (n = 8) (squares) or controls (circles). Responses are given as percentage of relaxation to the contraction induced by prostaglandin (PG) F2{alpha}. Results are presented as mean ± standard error of the mean. Triangles = endoluminal gas jet insufflation. (D) Cumulative dose-response curves of porcine coronary artery rings without endothelium submitted to coronary clamping (n = 6) (squares) or control (circles). (Statistically significant differences between the two preparations from the indicated concentration: *p < 0.05, **p < 0.01, ***p < 0.001, §p < 0.05, and §§p < 0.01.)

 
Coronary artery rings without endothelium submitted to clamping showed a significant reduction of relaxation to sin-1 at two concentrations. There was no difference in maximal endothelium-independent relaxation to sin-1 between the coronary clamping group and controls (Fig 2DGo).

Histologic Findings
Coronary rings submitted to coronary clamping showed marked endothelial cell loss, with nonconfluent islands of endothelial cells separated by denuded areas (Fig 3AGo). Coronary artery rings exposed to gas jet insufflation and to extravascular balloon occlusion showed minimal damage, with preservation of endothelial continuity and architecture (Figs 3B, 3CGoGo).



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  		Fig 3. . Silver staining (x250 before 45% reduction) of coronary artery rings after coronary clamping (A), after gas jet insufflation (B), and after extraluminal balloon occlusion (C).

 
In the first experiment, the channel created by the noninflated device measured 0.5 to 1.5 mm in height and 50 to 100 µm in width; the overlying artery and vein were intact and there was minimal disruption of the myocardium. In the second experiment, after inflation of the balloon, the channel measured 2.7 to 4 mm in height and up to 0.5 mm in width and was surrounded by an area of condensed myocardium up to 0.8 mm thick. The artery was intact, and there was disruption of a small epicardial vein. In the third experiment, after deflation and reperfusion, the channel made by the device measured up to 2 mm in diameter and was filled with a small amount of blood clot (Fig 4AGo). The myocardium showed a moderate interstitial hemorrhagic infiltration, with a ring of condensed myocardial cells averaging 500 µm in width (Fig 4BGo). An intramyocardial vein showed a recent thrombosis, but epicardial vessels were free of lesions (see Fig 4BGo).



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  		Fig 4. . Light microscopic examination of myocardium after deflation and reperfusion. (A) The channel made by the device measured up to 2 mm in diameter and contained a small amount of blood clot (x30 before 38% reduction). (B) The myocardium showed a moderate interstitial hemorrhagic infiltration, with a ring of condensed myocardial cells averaging 500 µm in width (x160 before 38% reduction).

 

   Comment
Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
Acknowledgments
 References
 
Obstruction of the operative field during performance of coronary anastomoses for coronary artery bypass grafting may occur with the use of any cardioprotective technique because of mediastinal collateral flow. It is more often encountered with the use of normothermic continuous cardioplegia delivery through either the antegrade or retrograde route. Although its superiority is not clearly established in all clinical situations, normothermic cardioplegia is both safe and reliable and may be especially beneficial in subsets of high-risk patients with multilevel coronary occlusions, poor ventricular function, acute ischemia, and long cross-clamp times [5]. Different technical maneuvers involving manipulation of the coronary arteries have been used to optimize visualization of the operative field during coronary artery bypass grafting, with apparent clinical safety, but none have been studied specifically for their effects on endothelial integrity. The key role of the endothelium in vascular homeostasis has been established [6, 7].

In the present study, extraluminal balloon occlusion and gas jet insufflation had no significant effects on endothelium-dependent relaxation when applied for 15 minutes, whereas coronary clamping altered these responses. The contractile function and endothelium-independent relaxation were unaffected by the use of all three techniques, demonstrating the integrity of the underlying smooth muscle cells. Coronary clamping over a thick epicardial fat cushion may partly protect the vessel wall from injury, but caution should be used. Design improvements such as the addition of rubber covers or nylon fibril, as was done for internal thoracic artery clamps, may help minimize injury from this device [8–10]. In this model, coronary clamping with standard bulldog clamps clearly led to endothelial cell injury and loss, as shown by the silver staining studies. The loss of endothelial cell coverage may be important clinically, as regenerated endothelium presents a selective dysfunction that may accelerate the occurrence of vasospasm and atherosclerosis [11–13].

The gas jet insufflation technique is safe in clinical use, with no histologic evidence of injury on venous grafts to which it was applied [4]. Numerous potential problems have been recognized with the use of this technique, such as saturation of the operative field with oxygen, creating a fire hazard; gaseous embolism; carbon dioxide deloading if CO2 is used; potential contamination from nonsterile medical gases; and nebulization of viral particles [14–16]. Another risk is potential endothelial injury from accidental high-flow gas delivery inside the coronary artery lumen, a technique in fact used in microvascular reactivity studies to remove the endothelium selectively [17]. This type of injury was confirmed in the present study. The lack of endothelial impairment seen with extraluminal balloon occlusion may be related to the occlusion of the coronary vessel by surrounding tissue, much like the physiologic compression exerted by the myocardium upon the coronary artery during systole. Proper use of the device necessitates placement of two loops, one on each side of the arteriotomy, with positioning in the depth of the epicardial fat and in the myocardium under the coronary artery. There is a potential danger of coronary artery or vein injury and hemorrhage, and this concern warranted the histologic studies that we performed. Although a small channel is created by the passage of the loop and inflation of the balloon, a major disruption of myocardial fibers and subsequent intramyocardial dissection and hemorrhage seem unlikely from the histologic studies performed. No adverse events have been encountered in preliminary studies in human clinical practice (unpublished observations). Use of this device for minimally invasive operations may be suboptimal because the beating heart creates progressive dislodgment of the balloon and, subsequently, incomplete hemostasis.

Other techniques are used to ensure hemostasis during the performance of anastomosis. Among them, the traditional endoluminal balloon occluder placed inside the lumen has the potential for causing endothelial denudation because of the unavoidable contact with the vessel lumen. Other disadvantages include encroachment in the operative field and the potential for incomplete occlusion and easy dislodgment. Techniques such as looping and snaring of the coronary artery with a polypropylene suture and interposition of a pledget or a small piece of silicone tubing are currently in use in minimally invasive operations. Saline irrigation can be effective for improving visualization, although it requires constant application and carries the risk of hemodilution if large volumes are used.

Obvious limitations exist in this model. First, the use of an explanted, nonperfused heart may not provide the same tissue turgor as the heart under continuous cardioplegic arrest and perfusion. However, the use of the explanted heart model has the advantage of ensuring gentle application of the device and precise identification of the coronary segment to which it was applied. Although placement of the devices upon dissected, explanted coronary arteries may cause injury because of the additional manipulation required, this was controlled for by using control rings from the same coronary artery near the site where the device was applied. In addition, the young swine heart has minimal epicardial fat compared with the human adult heart, which may offer more protection from application of the coronary clamp. In the case of gas jet insufflation, because the study technique necessitated complete coronary artery rings, the ring bearing the arteriotomy could not be studied. However, nearby rings did show signs of endothelial dysfunction, as evidenced by lower maximal endothelium-dependent relaxation. This finding was surprising considering that the gas stream was applied at a distance from the endothelial surface. Small amounts of gas may reach the lumen of the artery through the arteriotomy and alter endothelial function. Blood flowing through the arteriotomy may prevent this, although a sufficiently forceful gas flow may still permit gas to reach the arterial lumen. Different gases and different flow rates applied for shorter periods may produce less injury. Finally, the inflation volumes used to fill the balloon of the extravascular occluding device and thus, the compressive forces exerted upon the coronary artery to produce complete occlusion in a nonperfused heart, may be smaller than those needed during continuous cardioplegia delivery or normal coronary perfusion. We did, however, confirm complete occlusion of the artery by testing saline injection during inflation of the balloon.

In conclusion, different hemostatic techniques are used for optimal visualization of the coronary artery in the course of coronary artery bypass grafting during continuous delivery of cardioplegia or when the operation is performed on the beating heart with local isolation of the target vessel. Potential complications may be avoided through knowledge of the effects of the devices on coronary endothelial function. The results of the present study suggest that coronary clamping and gas jet insufflation techniques may impair endothelial function, whereas extravascular balloon occlusion, which mimics the physiologic systolic compression, may achieve effective hemostasis while preserving endothelial integrity.


   Acknowledgments
Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
References
 
We are thankful to Catherine Gitton-Canovi and Isabelle Delescluse for technical assistance, to Corinne Thomas-Haimez and Lisa Maiofiss for the statistical work, and to Roselyne Prioux for aid in preparation of the manuscript.

Doctor Perrault is supported by the Clinician-Scientist program from the Medical Research Council of Canada.


   Footnotes
Top
 Footnotes
Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
Address reprint requests to Dr Vanhoutte, Institut de Recherches Internationales Servier, 6 place des Pléiades 92415, Courbevoie, France.


   References
Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 

  1. Lichtenstein SV, Ashe KA, El Dalati H, Cusimano RJ, Panos A, Slutski AS. Warm heart surgery. J Thorac Cardiovasc Surg 1991;101:269–74.[Abstract]
  2. Subramanian VA, Sani G, Benetti FJ, Calafiore AM. Minimally invasive coronary bypass surgery: a multi-center report of preliminary clinical experience [Abstract]. Circulation 1995;92(Suppl 1):645.
  3. Pirk J, Kellovsky P. An alternative to cardioplegia. Ann Thorac Surg 1995;60:464–5.[Abstract/Free Full Text]
  4. Teoh KHT, Panos AL, Harmantas AA, Lichtenstein SV, Salerno TA. Optimal visualization of coronary artery anastomoses by gas jet. Ann Thorac Surg 1991;52:564.[Abstract/Free Full Text]
  5. Lichtenstein SV, Abel JG, Panos A, Slutsky AS, Salerno TA. Warm heart surgery: experience with long cross-clamp times. Ann Thorac Surg 1991;52:1009–13.[Abstract/Free Full Text]
  6. Furchgott RF, Vanhoutte PM. Endothelium-derived relaxing and contracting factors. FASEB J 1989;3:2007–18.[Abstract]
  7. Vanhoutte PM. The endothelium—modulator of vascular smooth-muscle tone. N Engl J Med 1988;319:412–3.
  8. Fonger JD, Yang XM, Cohen RA, Haudenschild CC, Shemin RJ. Human mammary artery endothelial sparing with fibrous jaw clamping. Ann Thorac Surg 1995;60:551–5.[Abstract/Free Full Text]
  9. Fonger JD, Yang XM, Cohen RA, Haudenschild CC, Shemin RJ. Impaired relaxation of the human mammary artery after temporary clamping. J Thorac Cardiovasc Surg 1992;104:966–71.[Abstract]
  10. Kuo J, Ramstead K, Coumbe A, Graham TR, Lewis CT. Effect of vascular clamp on endothelial integrity of the internal mammary artery. Ann Thorac Surg 1993;55:923–6.[Abstract/Free Full Text]
  11. Shimokawa H, Aarhus L, Vanhoutte PM. Porcine coronary arteries with regenerated endothelium have a reduced endothelium-dependent responsiveness to aggregating platelets and serotonin. Circ Res 1987;61:256–70.[Abstract/Free Full Text]
  12. Lin PJ, Pearson PJ, Cartier R, Schaff HV. Superoxide anion mediates the endothelium-dependent contractions to serotonin by regenerated endothelium. J Thorac Cardiovasc Surg 1991;102:378–85.[Abstract]
  13. Cartier R, Pearson PJ, Lin PJ, Schaff HV. Time course and extent of recovery of endothelium-dependent contractions and relaxations after direct arterial injury. J Thorac Cardiovasc Surg 1991;102:371–7.[Abstract]
  14. Pulton TJ. Optimal visualization of coronary artery anastomoses by gas jet [Letter]. Ann Thorac Surg 1992;54:598–9.[Free Full Text]
  15. Bognolo G, Bognolo DA, Chiariello L. Use of CO2 blower for internal mammary artery harvesting. Ann Thorac Surg 1995;59:1025.[Abstract/Free Full Text]
  16. Sasaguri S, Hosoda Y, Yamamoto S. Carbon dioxide gas blow for the safe visualization of coronary artery anastomosis [Letter]. Ann Thorac Surg 1995;60:1861.[Free Full Text]
  17. Bjorling DE, Saban R, Tengowski MW, Gruel SM, Rao VK. Removal of venous endothelium with air. J Pharmacol Toxicol Methods 1992;28:149–57.[Medline]



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H. B. Hangler, K. Pfaller, H. Antretter, O. E. Dapunt, and J. O. Bonatti
Coronary endothelial injury after local occlusion on the human beating heart
Ann. Thorac. Surg., January 1, 2001; 71(1): 122 - 127.
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L. P. Perrault, C. Nickner, N. Desjardins, and M. Carrier
Effects on coronary endothelial function of the Cohn stabilizer for beating heart bypass operations
Ann. Thorac. Surg., September 1, 2000; 70(3): 1111 - 1114.
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O. Chavanon, L. P. Perrault, P. Menasche, M. Carrier, and P. M. Vanhoutte
Endothelial Effects of Hemostatic Devices for Continuous Cardioplegia or Minimally Invasive Operations
Ann. Thorac. Surg., September 1, 1999; 68(3): 1118 - 1120.
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L. P. Perrault, P. Menasche, and P. M. Vanhoutte
High-flow gas insufflation to facilitate MIDCAB
Ann. Thorac. Surg., March 1, 1999; 67(3): 893 - 893.
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L. P. Perrault, P. Menasche, J.-P. Bidouard, C. Jacquemin, N. Villeneuve, J.-P. Vilaine, and P. M. Vanhoutte
Snaring of the Target Vessel in Less Invasive Bypass Operations Does Not Cause Endothelial Dysfunction
Ann. Thorac. Surg., March 1, 1997; 63(3): 751 - 755.
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