Ann Thorac Surg 1998;66:493-499
© 1998 The Society of Thoracic Surgeons
Original articles: cardiovascular
Experience with antegrade bihemispheric cerebral perfusion in aortic arch operations
Ramesh S. Veeragandham, MDa,b,c,
Ian N. Hamilton, Jr, MDa,b,c,
Christopher OConnor, MDa,b,c,
Vincenzo Rizzo, CCPa,b,c,
Hassan Najafi, MDa
a Department of Cardiovascular-Thoracic Surgery, Rush Medical College and Rush-Presbyterian-St. Lukes Medical Center, Chicago, Illinois, USA
b Department of Anesthesiology, Rush Medical College and Rush-Presbyterian-St. Lukes Medical Center, Chicago, Illinois, USA
c Rush Heart Institute, Rush Medical College and Rush-Presbyterian-St. Lukes Medical Center, Chicago, Illinois, USA
Accepted for publication March 29, 1998.
Address reprint requests to Dr Najafi, Department of Cardiovascular-Thoracic Surgery, 1725 W Harrison St, Suite 1156, Chicago, IL 60612
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Abstract
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Background. Various techniques have been used for cerebral protection in aortic arch operations. Antegrade cerebral perfusion has lost its popularity to hypothermic circulatory arrest to overcome the so-called cluttered operative field. Hypothermic circulatory arrest has its own problems of coagulopathy, time constraints, and prolongation of cardiopulmonary bypass time.
Methods. Since June 1986 we have used antegrade bihemispheric cerebral perfusion with moderate hypothermia in 20 patients with aortic arch disease. Twelve patients had aneurysm, 7 had dissection, and 1 had traumatic tear. Five patients had had previous sternotomy for ascending aortic replacement. In addition to arch reconstruction, 7 patients had aortic valve replacement or repair, 2 patients had Bentall procedure, and 3 had selective innominate reconstruction. The mean cerebral perfusion time was 51 ± 29 minutes. In 7 patients the cerebral perfusion time was between 60 and 120 minutes.
Results. There was no in-hospital or 30-day mortality. The blood product requirements were significantly less with moderate hypothermia. One patient suffered cerebrovascular accident (5%). None of the 7 patients with cerebral perfusion times of 60 to 120 minutes had any neurologic deficits. These results are superior to those reported for hypothermic circulatory arrest with or without retrograde cerebral perfusion.
Conclusions. Antegrade bihemispheric cerebral perfusion is an optimal adjunct for cerebral protection during aortic arch operations.
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Introduction
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After the report by DeBakey and associates [1] of the first successful aortic arch aneurysmectomy in 1957, multiple techniques were used to provide cerebral protection during aortic arch reconstruction. These included antegrade cerebral perfusion with cannulation of one, two, or three brachiocephalic vessels, single or separate pump heads for systemic and cerebral circulations, and variable levels of temperature and flow rates [2]. Technical mishaps with these diverse techniques resulted in suboptimal outcomes and prompted the application of hypothermic circulatory arrest in aortic arch operations [3]. The proposed advantages included simplified extracorporeal circuit, a bloodless operative field devoid of cannulas, and a decreased incidence of cerebral embolization. However, hypothermic circulatory arrest was found to be associated with prolongation of cardiopulmonary bypass time, increased perioperative bleeding, greater transfusion requirements, postoperative multiorgan dysfunction, and a limited period of safe cerebral ischemia [4]. In recent years retrograde cerebral perfusion through the superior vena cava was added to hypothermic circulatory arrest to improve cerebral protection and extend the period of safe cerebral ischemia [5]. These goals have not been fully attained and the complications of hypothermic circulatory arrest have remained largely unchanged.
In 1986 we abandoned hypothermic circulatory arrest and began using antegrade bihemispheric cerebral perfusion during aortic arch reconstruction. Herein we present the clinical course, operative techniques, and results in 20 consecutive aortic arch reconstructions using this modality of cerebral protection.
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Patients and methods
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Patient characteristics
Twenty-one consecutive patients underwent operations for aortic arch disease by a single surgeon (H.N.) between June 1986 and October 1996. One patient who had previously undergone aortic valve and ascending aortic replacement for aortic dissection exsanguinated at the time of resternotomy because of entry into the aortic false lumen. The remaining 20 patients required simultaneous temporary perfusion of both the innominate and left common carotid arteries, thus classified as an aortic arch reconstruction as defined by Cooley and colleagues [6]. The review of records of these patients forms the basis for this report. There were 12 men and 8 women with ages ranging from 18 to 82 years (mean, 56 years). Eight patients (40%) were older than 70 years.
Twelve patients presented with aneurysmal disease, 7 with dissection, and 1 with a traumatic tear. Two patients had Marfans syndrome. Thirteen patients were operated on electively, 6 urgently, and 1 emergently. The emergent operation was performed for an 18-year-old man who had been involved in a car accident and had suffered a linear tear in the posterior aspect of the aortic arch. Four patients had had one previous sternotomy for ascending aortic or aortic valve replacement. One patient had had two previous sternotomies. Two patients had had previous descending thoracic aortic operations.
The significant past medical history included hypertension in 12 patients, chronic obstructive pulmonary disease in 5, coronary artery disease in 3, and smoking in 8. The aneurysm involved the innominate artery in 3 patients and the descending thoracic aorta in 2 patients. The 3 patients with innominate artery aneurysm had experienced transient ischemic attacks.
Ten patients had associated valvular lesions needing correction in conjunction with aortic arch repair. These included aortic regurgitation in 6, aortic stenosis in 2, perivalvular aortic leak in 1, and combined aortic and mitral regurgitation in 1. Six patients had aortic valve replacements, 1 had resuspension of the aortic valve, and 1 had repair of a perivalvular aortic dehiscence. Two patients underwent Bentall procedure. One of these patients had mitral regurgitation and underwent transaortic mitral valve replacement before the conduit was inserted. Three patients had associated coronary lesions. One underwent concomitant coronary revascularization. The lesions were diffuse in the remaining 2 patients.
In 13 patients the superior aspect of the aortic arch containing the orifices of the brachiocephalic vessels, in continuity with the descending aorta, was incorporated in the distal anastomosis. In these patients all cerebral vessels with the exception of the left subclavian artery were perfused to maintain cerebral blood flow during the radical incision of the arch and its reconstruction. None have required a further operation on the aortic arch during the follow-up period of 1 to 11 years. The innominate artery was involved in 3 patients and was replaced with a separate graft. In 1 patient the innominate and left common carotid arteries were anastomosed to the side of the graft using a button of the aorta. One patient had a 3-cm traumatic vertical tear in the posterior wall of the aortic arch. Primary repair was done from within the arch while perfusing the innominate and left common carotid arteries. Two patients had complex reconstructions and deserve special mention. In one, the aneurysm was diffuse and involved the ascending aorta, the arch, and the innominate, right subclavian, and left common carotid arteries (Fig 1). This was further compounded by aortic regurgitation and supravalvular aortic stenosis. His complex repair is shown in Figure 2. The other patient had had two previous sternotomies, the first for aortic valve replacement and the second for ascending aortic replacement for acute aortic dissection. She presented with paravalvular aortic leak and a large dissecting aneurysm involving the aortic arch and particularly the entire descending thoracic aorta (Fig 3). Her unremitting left intrascapular pain was suggestive of impending rupture. Initially she was considered inoperable because of nearly insurmountable lesions. Her unquestionably fatal course, however, led to the extensive and unconventional procedure depicted in Figure 4. The symptomatic descending aortic aneurysm was excluded from the circulation.

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Fig 1. Supravalvular aortic stenosis and diffuse aneurysm involving the ascending aorta, the arch, and the brachiocephalic vessels. (© 1997 by Rachid F. Idriss. Reprinted with permission.)
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Fig 2. Completed procedure consisting of the replacement of the aortic valve and of the ascending aorta, the arch, and the innominate and proximal segments of the right subclavian and left common carotid arteries. (© 1997 by Rachid F. Idriss. Reprinted with permission.)
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Fig 3. Chronic dissecting aneurysm involving the aortic arch and the entire descending aorta further complicated by paravalvular aortic dehiscence.
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Fig 4. Completed procedure consisting of repair of the paravalvular aortic leak, tube graft replacement of the aortic arch, exclusion of the descending aortic aneurysm, and bypass graft from the ascending to the abdominal aorta.
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Operative technique
Before the induction of anesthesia an oximetric pulmonary artery catheter and right radial and femoral arterial catheters were placed. Anesthesia was introduced with moderate doses of fentanyl, midazolam, and a long-acting muscle relaxant. Anesthesia was maintained with isoflurane in 100% oxygen and supplemental intravenous opioids. A bladder catheter provided core temperature monitoring and transesophageal echocardiography was used to evaluate ventricular performance and valvular function and to aid in purging intracardiac air. A Neurometrics Life scan 2-channel processed electroencephalographic monitor was used to assess symmetrical cortical electrical activity during the procedure. After median sternotomy, cardiopulmonary bypass was established with femoral arterial and a two-stage right atrial cannulation. Femoral venous and superior vena caval cannulation was used in some redo cases earlier in the series. The arch vessels were mobilized and encircled with tapes. The innominate vein was left intact in every instance. Great care was exercised to avoid blunt dissection of the aneurysm. Cardiopulmonary bypass was established and cooling was begun early during the course of dissection to conserve time. Femoral arterial inflow was initiated slowly to minimize iatrogenic retrograde aortic dissection. With the patient on total cardiopulmonary bypass and the heart fibrillating, the ascending aorta was clamped and antegrade cold blood cardioplegia was given to thoroughly cool the heart. Ice slush was used for topical myocardial hypothermia and protection of the right ventricle. If necessary the aortic valve was dealt with at this stage with either replacement or repair. In one patient the mitral valve was replaced through the aortic root before the arch was reconstructed and an aortic conduit was inserted. Dissection and control of the proximal descending aorta was deferred until the ascending aorta was transected and the arch could be rotated for better exposure. Care was taken to protect the recurrent laryngeal nerve. Once the target temperature was reached, the descending thoracic aorta and arch vessels were clamped and the transverse arch opened. Within a minute or two cerebral perfusion was initiated and maintained until the distal portion of reconstruction was completed.
The cerebral perfusion system consisted of an independent pump head and a bifurcated or trifurcated arterial perfusion line. Two Javid carotid shunts (Bard Inc, Murray Hill, NJ) (for cannulation of innominate and left common carotid arteries) or three Javid carotid shunts (for right subclavian, right common carotid, and left common carotid arteries) were attached to the bifurcated or trifurcated arterial line, respectively. The Javid shunts were carefully inserted into the brachiocephalic arteries and were then secured with Rommel tourniquets. Great care was taken to prevent air embolization. Cerebral flow was initiated at 10 mL/min per kilogram of body weight and adjusted to maintain a mean right radial pressure of 50 mm Hg. With the descending aorta clamped at its origin, the femoral arterial flow was proportionately reduced at this time. Hence, the systemic flow through the femoral artery and cerebral perfusion were maintained throughout the procedure except for a minute or two to insert or remove the indwelling catheters before opening the arch, and after its repair the operative field was organized to avoid the so-called cluttered field (Fig 5). An appropriately sized, woven, collagen-impregnated graft (Hemashield, Meadox Medicals Inc, Oakland, NJ) was chosen and reconstruction of the arch was carried out as described before. After completing all distal arch and brachiocephalic anastomoses the patient was placed in moderate Trendelenburg position. The Javid shunts were removed and blood was allowed to fill the graft thus expelling all air. The graft was clamped proximal to the reconstructed arch thereby restoring cerebral flow through the femoral arterial catheter. The flow rates were adjusted to provide for the added brachiocephalic circulation. The remainder of the operation varied from simple proximal anastomosis between the graft and the supracoronary aorta or insertion of a composite graft.
-Aminocaproic acid (amicar) was commonly administered at the start of cardiopulmonary bypass (150 mg/kg) followed by an infusion of 15 mg/kg per hour. After adequate air removal maneuvers the cross-clamp was removed to reestablish coronary blood flow. After separation from the cardiopulmonary bypass, blood products were administered on the basis of clinical assessment of the adequacy of hemostasis in conjunction with coagulation testing including thromboelastography. Hemostasis was achieved using thrombin-soaked absorbable gelatin sponges (Gelfoam, Upjohn Co, Kalamazoo, MI). Patients were extubated in the surgical intensive care unit when they met the standard criteria of normothermia, adequate mentation, and cardiopulmonary stability.

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Fig 5. Operative field with two arterial perfusion catheters in the innominate and left common carotid arteries. The arch aneurysm had been excised. The operation field is conducive to any reconstructive surgical procedure.
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Seventeen patients underwent antegrade bihemispheric cerebral perfusion with innominate and left common carotid cannulation. The remaining 3 patients had innominate artery aneurysm requiring perfusion of the right subclavian, right common carotid, and left common carotid arteries. The mean bypass time (231 ± 50 minutes) and myocardial ischemic time (153 ± 59 minutes) varied depending on the complexity of the procedure. The first 2 patients were cooled to 14°C, the next 15 patients were cooled to 24°C, and the last 3 patients were cooled to 28°C. The blood component requirements varied with the core temperature with an average requirement of 5.4 ± 5 units in the 15 patients cooled to 24°C and 0.3 ± 0.6 units in the last 3 patients cooled to 28°C. The mean cerebral perfusion time was 51 ± 29 minutes. The cerebral perfusion time varied whether brachiocephalic implantation was required or not (81 ± 30 versus 41 ± 22 minutes). To compare this data with the safe hypothermic circulatory arrest times quoted in the literature, the cerebral perfusion times were subcategorized. The duration of cerebral perfusion was less than 30 minutes in 6 patients, 30 to 44 minutes in 3 patients, 45 to 59 minutes in 4 patients, and 60 to 120 minutes in 7 patients. Overall time to extubation, intensive care unit length of stay, and postoperative hospital length of stay were 23 hours, 1.4 days, and 9.3 days, respectively.
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Results
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There was no operative, in-hospital, or 30-day mortality. There have been four late deaths from pneumonia in 2 septuagenarians, and colon carcinoma and upper gastrointestinal bleeding in 1 patient each. The remaining 16 patients are alive and well at a median follow-up period of 4 years (range, 1 to 11 years). Postoperative complications included stroke in 1 patient (5%), subendocardial myocardial infarction in 1 (5%), and vocal cord paralysis in 2 (10%). The patient with neurologic complication had cerebral perfusion time of 52 minutes. None of the 7 patients with cerebral perfusion times between 60 and 120 minutes demonstrated any neurologic complications. Three patients (15%) with long-standing chronic obstructive pulmonary disease exhibited pulmonary insufficiency requiring prolonged ventilatory support. The patient undergoing descending thoracic aortic exclusion suffered sustained postoperative lower extremity paraparesis. She is one of the 2 patients with late death consequent to pneumonia. No patient required reoperation for bleeding. There were no instances of sepsis, renal insufficiency, multiorgan failure, or wound infection.
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Comment
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In 1957 DeBakey and associates [1] used cardiopulmonary bypass with perfusion of the innominate and left common carotid arteries to successfully resect and reconstruct an aortic arch aneurysm. Pearce and colleagues [2] used bilateral brachial and left carotid perfusion catheters with a single pump head for both systemic and cerebral perfusion to further simplify the extracorporeal circuit. Two more catheters were added to perfuse the coronary arteries. The presence of multiple catheters in the field contributed to technical mishaps necessitating alternative techniques. The successful use of profound hypothermia and circulatory arrest in infants and, less frequently, in adults lead Ergin and Griepp [3] to popularize hypothermic circulatory arrest for aortic arch surgical procedures. They used core cooling to 14°C, and the average cerebral ischemic time was 42 minutes. Most patients had pulmonary dysfunction and bleeding was a significant problem. Similar problems and 50% in-hospital mortality led to the use of moderate hypothermia (22° to 26°C) with relatively better outcome [4]. Experience with excessive bleeding and pulmonary complications rekindled interest in antegrade cerebral perfusion with moderate hypothermia [7]. However, unilateral cerebral perfusion was used, which required some form of preoperative assessment to establish the completeness of the circle of Willis.
Disenchanted with hypothermic circulatory arrest, we began using antegrade bihemispheric cerebral perfusion for arch reconstruction in June of 1986. This modality of brain preservation has been used in 20 consecutive patients. After the first 2 patients the core cooling was raised to 24°C (15 patients), and the last 3 patients were cooled to 28°C. To compare the results using the two principal methods of cerebral protection during arch operations, we reviewed the recent literature.
Hypothermic circulatory arrest
The experience with hypothermic circulatory arrest in several series is summarized in Table 1 [811]. The noncardiac mortality ranged from 4.5% to 19.5% and the incidence of neurologic complications ranged from 6.9% to 26%. Major complications associated with hypothermic circulatory arrest included perioperative bleeding secondary to coagulopathy, cerebral infarction, and multiorgan failure. In a retrospective analysis of 656 patients undergoing hypothermic circulatory arrest, the frequency of neurologic complications correlated with the duration of circulatory arrest [10]. The incidence of stroke was 4% with 7 to 29 minutes, 7.5% with 30 to 44 minutes, 10.7% with 45 to 59 minutes, and 14.6% with greater than 60 minutes of hypothermic circulatory arrest. Mortality increased markedly after 65 minutes of circulatory arrest. The safe period of circulatory arrest for prevention of stroke was found to be 40 minutes. Often this proves to be an insufficient time for complex arch reconstruction.
In the present series of 20 patients the cerebral perfusion times were less than 30 minutes in 6 patients, 30 to 44 minutes in 3 patients, 45 to 59 minutes in 4 patients, and between 60 and 120 minutes in 7 patients. There was no in-hospital or 30-day mortality. One patient (5%) with 52 minutes of cerebral perfusion suffered stroke. The unique advantage of bihemispheric antegrade cerebral perfusion is its ability to protect the brain when prolonged periods of interruption of native brachiocephalic circulation are needed. The 7 patients needing 60 to 120 minutes of antegrade cerebral perfusion had no neurologic complications. This contrasts sharply with cerebral complication rates quoted for similar duration of cerebral ischemia in patients subjected to hypothermic circulatory arrest (14.6%) [10].
Antegrade cerebral perfusion
The published experience with antegrade cerebral perfusion is summarized in Table 2 [7, 1214]. The noncardiac mortality ranged from 0% to 13.7% with the incidence of neurologic complications ranging from 0% to 6.7%. Various authors have used selective cerebral perfusion with four distinct modifications. These include unihemispheric versus bihemispheric cerebral perfusion, variable rates of cerebral blood flow, single versus multiple pump heads for cerebral and systemic perfusion, and different levels of core temperature. Antegrade bihemispheric cerebral perfusion appears preferable. Assuming an average adult brain weight of approximately 1,250 g and normal cerebral blood flow averaging 54 mL/min per 100 grams of brain tissue, a total cerebral flow if 675 mL/min (10 mL/min per kilogram of body weight) appears adequate [15]. Separate pump heads for cerebral and systemic perfusion provide a degree of flexibility and safety during the procedure. With adequate cerebral perfusion, profound hypothermia is not necessary and may in fact be detrimental. Bleeding was the main complication in the series reported by Shinpo and colleagues [12] in which antegrade cerebral perfusion was used with profound hypothermia.
Two studies have compared hypothermic circulatory arrest with antegrade cerebral perfusion for aortic arch surgical procedures (Table 3). In the first study there were fewer complications with antegrade cerebral perfusion as compared with hypothermic circulatory arrest [16]. The major complications associated with hypothermic circulatory arrest were uncontrolled bleeding and multiorgan failure. In the second study hypothermic circulatory arrest was compared with hypothermic circulatory arrest with antegrade cerebral perfusion to evaluate whether the addition of cerebral perfusion provided an added protective effect [17]. No significant difference was found in overall mortality nor in the incidence of neurologic complications. A close analysis of this study shows that the cerebral perfusion was delivered inconsistently with one or two cannulas and perfusion was provided by a single pump head. Additionally in 13 of the 16 patients in the antegrade cerebral perfusion group the cerebral blood flow was only 200 to 300 mL/min. Even though one can argue that lower flows are sufficient during deep hypothermia, when transcranial Doppler was used in the last 3 patients in this series, the cerebral blood flow had to be increased to 500 to 700 mL/min to achieve satisfactory flows in the middle cerebral artery. This may explain the high incidence of neurologic complications in the antegrade cerebral perfusion group in this particular study.
Retrograde cerebral perfusion
To improve the cerebral protection during hypothermic circulatory arrest, retrograde cerebral perfusion was introduced by Ueda and coworkers in 1990 [5]. The theoretical advantage of retrograde cerebral perfusion was strengthened by the findings of significant desaturation of blood returning to the aortic arch, indicating continued cerebral oxygen consumption during hypothermic circulatory arrest. However, there is no conclusive evidence that retrograde cerebral perfusion actually perfuses the brain in humans. In baboons 90% of the blood was shunted to the inferior vena cava without significant flow detection in the brains of these primates [18]. Using magnetic resonance spectroscopy to monitor brain metabolism, adequacy of cerebral protection was tested during cardiopulmonary bypass, hypothermic circulatory arrest, antegrade cerebral perfusion, and retrograde cerebral perfusion [19]. The intracellular pH and high-energy phosphate levels were essentially normal during cardiopulmonary bypass and antegrade cerebral perfusion. Hypothermic circulatory arrest was associated with the lowest pH and the slowest recovery of high-energy phosphates. Hypothermic circulatory arrest with retrograde cerebral perfusion was also associated with low intracellular pH but with slightly better high-energy phosphate recovery during reperfusion. In summary, the benefit of retrograde cerebral perfusion in addition to that provided by hypothermic circulatory arrest may only be from its ability to flush air and debris from the cerebral circulation. The best modality for cerebral protection during interruption of cerebral blood flow may be antegrade cerebral perfusion [19].
Although some human studies have demonstrated good results using hypothermic circulatory arrest with retrograde cerebral perfusion [20], a large multiinstitutional study (228 patients from 49 centers in Japan) reported a 20.2% overall neurologic complication rate, 11.8% stroke rate, and 19.7% in-hospital mortality rate [21]. In this study the most significant predictor for permanent neurologic dysfunction was the duration of circulatory arrest with retrograde cerebral perfusion time of more than 60 minutes. Comparison of these data with a previous study of hypothermic circulatory arrest without retrograde cerebral perfusion demonstrates an identical incidence if overall neurologic dysfunction with cerebral ischemic times of more than 60 minutes [10]. This calls into question the benefit imparted by the addition of retrograde cerebral perfusion to hypothermic circulatory arrest and argues in favor of the routine use of antegrade bihemispheric cerebral perfusion during aortic arch reconstruction. There are, however, some situations when hypothermic circulatory arrest will be advantageous. These include patients with extremely friable or calcified aortic tissues in which aortic cross-clamping can be hazardous and the aorta is intimately adherent to or has eroded into the sternum.
Conclusion
Antegrade bihemispheric cerebral perfusion with moderate hypothermia (24° to 28°C) is a safe modality for cerebral protection during aortic arch reconstruction. It significantly limits the need for blood products, extends the safe period of interruption of native brachiocephalic blood flow, and obviates ischemic multiorgan injuries. The advantages of hypothermic circulatory arrest including simplified extracorporeal circuit with fewer cannulas in the operative field are superseded by the complications of bleeding, organ dysfunction, time-limited cerebral protection, and prolongation of cardiopulmonary bypass time.
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Footnotes
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This article has been selected for the open discussion forum on the STS Web site: http://www.sts.org/annals
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References
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