Protection of the brain by retrograde cerebral perfusion during circulatory arrest

Protection of the brain by retrograde cerebral perfusion during circulatory arrest Hypothermic circulatory arrest is commonly used to facilitate repair of complex congenital heart defects and aortic lesions and for complex neurosurgical procedures. However, extended periods of circulatory arrest may impair cerebral metabolism and cause ischemic injury. Retrograde cerebral perfusion has been applied recently in aortic surgery to protect the brain. From January 1991 to December 1993, 29 patients underwent emergency operations to repair acute type A aortic dissection with the aid of hypothermic circulatory arrest. Six patients received hypothermic circulatory arrest without retrograde cerebral perfusion with a rectal temperature .of 16.4 0 ± 0.9 0 C (mean ± standard error of the mean, group 1). Retrograde cerebral perfusion during hypothermic circulatory arrest was performed in 15 patients with a rectal temperature of 15.9 0 ± 0.5 0 C (group 2) and in eight patients with a rectal temperature of 21.7 0 ± 0.8 0 C (group 3). The hypothermic circulatory arrest times were 25 ± 4, 42 ± 4, and 63 ± 6 minutes, respectively (p < 0.05). The cardiopulmonary bypass times were 173 ± 5; 184 ± 7, and 143 ± 6 minutes, respectively (p < 0.05). AU patients survived the operation and regained consciousness with no neurologic defects. Follow-up (mean 23.2, 14.5, and 5.1 months, respectively) was complete in all patients except one. This patient, from group 2, was killed in a road traffic accident 12 months after the operation. Our experience suggests that retrograde cerebral perfusion can effectively protect the brain from ischemic injury and extend the safe period of hypothermic circulatory arrest. With the aid of retrograde cerebral perfusion, prolonged circulatory arrest can probably be performed safely with moderate hypothermia. (J THoRAc CARDIOVASC SURG 1994;108:969-74)

Pyng Jing Lin, MD,a Chau-Hsiung Chang, MD,a Peter P. C. Tan, MD,b Chun-Chieh Wang, MD,c Jen-Ping Chang, MD,a Dah-Wel Liu, MD,a Jaw-Ji Chu, MD,a Kuei-Ton Tsai, MD,a Chiung-Lun Kao, MD,a and Ming-Jang Hsieh, MD,a Taipei, Taiwan, Republic of China

Hypothermic circulatory arrest has been used with increasing frequency since its clinical introduction. 1 Its major advantage is that it can provide a bloodless operative field. The technique of hypothermic circulatory arrest has been applied for surgical intervention in aortic

From the Division of Thoracic and Cardiovascular Surgery," Department of Anesthesiology," Division of Cardiology," Chang Gung Memorial Hospital, Chang Gung Medical College, Taipei, Taiwan, Republic of China. Received for publication Jan. 27, 1994. Accepted for publication May 31,1994. Address for reprints: Pyng Jing Lin, MD, Division of Thoracic and Cardiovascular Surgery, Chang Gung Memorial Hospital, 199, Tun-Hwa North Rd., Taipei, Taiwan, Republic of China. Copyright © 1994 by Mosby-Year Book, Inc. 0022-5223/94 $3.00 + 0

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lesions.v?complex congenital heart disease.? and complex neurosurgical procedures." Ischemic injury to the brain is the most serious complication of hypothermic circulatory arrest. Forty minutes has been considered to be the safe limit at 18° to 20° e.8, 9 So that the safe period of circulatory arrest could be extended, retrograde cerebral perfusion through the superior vena cava was clinically introduced.v 10-12 Retrograde cerebral perfusion has been applied recently in aortic operations for short periods (less than 60 minutes) of deep hypothermic circulatory arrest to protect the brain.o 12, 13 However, prolonged periods of cardiopulmonary bypass during operations with deep hypothermia are associated with complications such as increased bleeding and a higher mortality rate.' Indeed, deep hypothermia might not be necessary if retrograde cerebral perfusion could protect the brain from ischemic

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Lin et ai.

Table I. Clinical data Age (yr) Mean Range Gender (M/F) Cardiac tamponade with shock Severe aortic insufficiency Intimal tear in aortic arch Preop. multipleorgan failure Total bypass time (min) HCA time (min) Rectal temp. during HCA (0C) RCP Drainage 6 hr pOSIOp. (mil

Group 1

Group 2

55.2 ± 5.8 42-74 3/3

50.4 ± 3.2 34-60 10/5 5

I 3 2

o

173 ± 5 25 ± 4 16.4 ± 0.9

5 3 3

184 ± 7 42 ± 4* 15.9 ± 0.5

No

Yes

342 ± 30

256 ± 25

Group 3

53.4 ± 7.0 38-88 5/3 4 3 2

2 143±6t+ 63 ± 6tt 21.7 ± 0.8t+

Yes 220 ± 21

HCA, Hypothermic circulatory arrest; RCP, retrograde cerebral perfusion.

*p < 0.05 when comparing group 2 with group I. tp < 0.05 when comparing group 3 with group I. :j:p < 0.05 when comparing group 3 with group 2.

injury. However, no clinical information has been published concerning retrograde cerebral perfusion for protection of the brain during a prolonged period (more than 60 minutes) of moderate (> 20 0 C) hypothermic circulatory arrest. In this report, we present our clinical experience in brain protection using retrograde cerebral perfusion during hypothermic circulatory arrest for surgical repair of acute type A aortic dissection.

Methods and patients Twenty-nine patients with acute type A ascending aortic dissection underwent repair of the defect between January 1991 and December 1993. The group comprised 17 male and 12 female patients from 34 to 88 years of age (Table 0. Diagnosis was confirmed by echocardiography (transthoracic or transesophageal) and computed tomography of the chest. Aortography was not performed before the operation in any of the patients. The operation for repair of the aortic dissection was performed immediately after establishment of the diagnosis. Preoperative comprehensive neurologic and psychologic studies were not performed because the operations were performed on an emergency basis. Written consent was obtained from the family members of the patients before the operation. . Patients were divided into three groups according to the methods used for brain protection. In the earliest portion of this series, traditional deep hypothermic circulatory arrest with a rectal temperature of 16.4° ± 0.9° C (mean ± standard error of the mean) was applied during repair of aortic dissection in six patients without retrograde cerebral perfusion (group I). Retrograde cerebral perfusion during hypothermic circulatory arrest was performed in the second portion of the series (15 patients) with a rectal temperature of 15.9° ± 0.5° C (group 2) and in the most recent part of the series (eight patients) with a rectal temperature of 21.7° ± 0.8° C (group 3) (see Table 0. Surgical technique. The surgical technique for repairing the dissection of the ascending aorta has been previously reported.f In brief, cardiopulmonary bypass was established by femoral

arterial and right atrial cannulation with a bubble oxygenator (c. R. Bard, Inc., Tewksbury, Mass.). In nine patients with preoperative cardiac tamponade, femoro-femoral bypass was set up before sternotomy. Another cannula was inserted into the superior vena cava via the right auricle and was connected to the arterial line of the extracorporeal system for retrograde perfusion of the brain during hypothermic circulatory arrest in all except the first six patients (group I) in this series. Intermittent infusion of crystalloid cardioplegic solution (Plegisol, Abbott Laboratories, North Chicago, IIl.) was used for myocardial protection. Circulatory arrest was started when the desired rectal temperature was reached in patients of group 2 and group 3 before the aorta was opened. The patient was kept in a headdown position. The femoral arterial cannula was clamped. After the cannula in the superior vena cava was snared, oxygenated blood (ISo to 18 ° C) from the oxygenator was pumped to the bilateral internal jugular veins for retrograde cerebral perfusion- at a flow rate of 150 ml/ min in group 2 patients and 300 ml/ min in group 3 patients. The pressure of the distal superior vena cava was found to be 7 to 12 mm Hg. A suction device was placed in the aortic arch to remove the "venous" return from the carotid arteries. In group I patients, the middle part of the ascending aorta was crossclamped until the aortic valve had been resuspended and the proximal spool of the intraluminal graft had been seated; then circulatory arrest was started with the crossclamp removed while the tear in the aortic arch was repaired and the distal spool of the intraluminal graft was seated. The aortic valve was resuspended in II patients who had severe preoperative aortic regurgitation. The intimal tears located at the aortic arch in seven patients were repaired primarily with interrupted 4-0 pledget-supported sutures. The pledgets were placed on the inner and outer sides of the aorta so as to "sandwich" the tears. An intraluminal sutureless vascular graft (Meadox Medicals, Inc., Oakland, N.J.) was used for replacement of the ascending aorta in all 29 patients. After the intraluminal prosthesis was seated, extracorporeal circulation was restarted with femoro-atrial or femoro-femoral bypass, and retrograde cerebral perfusion was terminated. After air was

The Journal of Thoracic and Cardiovascular Surgery Volume 108, Number 5

removed the aorta was closed over the graft with continuous running~utures. A woven Dacrongraft (M.eadox Medicals).was used to wrap the ascendingaorta (extending beyond proximal and distal spools) in 26 patients. A modified Cabrol shunt was created with a 5 mm polytetrafluoroethylene vascular graft* connecting the perigraft space and the right atrium in seven patientsincludedin the early part of this series. Routine decannulation and closure were then performed. Oxygen extraction study. Before the end of retrograde cerebral perfusion and start of cardiopulmonarybypass, bl.ood samples weretaken from the distal superiorvenacavaand fight carotid artery in patients of group 2 and group 3. ~ontrol s~m­ pies were taken from the right internal jugular vein and fight femoral artery of 21 patients (10 male and II female) aged 12 to 68 years (mean 39 years) while electrop~ysiologic studiesfor Wolff-Parkinson-White syndromewere being done. The blood samples weresent for bloodgas analysis. The oxygen extraction ratio was calculated from the following formula: (Oxygensaturation of blood from the superior vena cava or right femoral artery - Oxygensaturation of bloodfrom the carotid artery or right internal jugular vein)jOxygen saturation of blood from the superiorvena cava or right femoral artery. Data analysis. The data were expressed as means ± standard error of the mean. Statistical evaluation of data between groups was performed by Student's t test for unpaireddata or by a one-wayanalysisof variance. Statistical significance was set at a probabilityvalue (p) of lessthan 0.05. Results- . No difference was detected between groups in terms of age, gender, other associated medical illnesses, or severity of aortic dissection and hemodynamic status of the patients. However, more patients in groups 2 and 3 than in group I had preoperative multiorgan system failure (see Table I). Systemic hypothermia was maintained with the rectal temperature at 16.4° ± 0.9° C (range 13° to 18° C) in group I patients, 15.9° ± 0.5° C (range 13.5° to 17° C) in group 2 patients, and 21.7° ± 0.8° C (range 20° to 24.8 ° C;p < 0.05 compared with groups I and 2) in group 3 patients during hypothermic circulatory arrest. The duration of hypothermic circulatory arrest was 25 ± 4 minutes in group I (range 14 to 37 minutes), 42 ± 4 minutes in group 2 (range 27 to 67 minutes), and 63 ± 6 minutes in group 3 (range 49 to 93 minutes; p < 0.05 when comparing group 3 with groups 1 and 2). The total bypass times were 173 ± 5, 184 ± 7, and 143 ± 6 minutes, respectively (p < 0.05 when comparing group 3 with groups I and 2). The oxygen extraction ratios were 39% ± 3%,29% ± 4%, and 26% ± 3% from blood samples of group 2, group 3, and control samples, respectively (p < 0.05 when comparing blood samples of group 2 with control samples) (Table 11). Drainage during the first 6 postoperative hours was 342 ± 30, 256 ± 25, and 220 ± 21 ml in groups 1, 2, and 3, "Gore-Tcx vascular graft; registered trademarkofW. L. Gore & Associates, Inc., Elkton, Md.

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Table II. Laboratory data S02 (%)

EXR (%)

Group 2

Group 3

Cotitrol

61 ± 3* 39 ± 3*

71 ± 4 29 ± 4

68 ± 4 26 ± 3

The data are expressed as means ± standard error of the mean. SOl, Oxygen saturation of blood samples from right carotid artery in group 2 and group 3and from right internal jugular vein from control samples; EXR, oxygen extraction ratio. 'Significant difference between blood samples from group 2 and control samples.

respectively (p > 0.05, see Table I). All patients survived the operations and regained consciousness without neurologic defects, and no hospital deaths occurred. Complications included pneumonia in two patients who were successfully treated with antibiotics and a minor stroke 5 days after the operation in one patient who subsequently made a full recovery. Brain computed tomographic studies of this patient showed a small lacunar infarction. Electroencephalographic studies performed before discharge of group 3 patients showed no abnormalities. All patients were discharged in good condition. Follow-up (mean 23.2,14.5, and 5.1 months, respectively in groups 1,2, and 3) was complete in all patients except in one patient of group 2 who died as a result of a road traffic accident 12 months after his operation. All the survivors were in New York Heart Association functional class I or II. Transthoracic echocardiographic studies showed trivial to mild aortic insufficiency in 11 patients who had severe aortic insufficiency before the operation. All of the modified Cabrol shunts were non functioning. Follow-up chest computed tomographic studies showed decreased size of the false lumen in the aortic arch and descending aorta, even in those patients who had an intimal tear in the aortic arch. Thrombus in the false lumen was noted in 15 of the 29 patients. No evidence of graft-related complications, including thrombosis, thromboembolism, pseudoaneurysm formation, graft erosion, or graft migration, was detected.

Discussion In this report, all patients survived and regained consciousness with no neurologic defects in the early postoperative period after surgical repair of acute type A aortic dissection. However, the duration of circulatory arrest of group 2 (42 ± 4 minutes, range 27 to 59 minutes) and group 3 patients (63 ± 6 minutes, range 49 to 93 minutes), with retrograde cerebral perfusion used for brain protection, was significantly longer than that of group 1 patients (25 ± 4 minutes, range 14 to 37 minutes); in group 1 patients traditional deep hypothermia without the aid of retrograde cerebral perfusion was applied during circulatory arrest. This observation indi-

9 7 2 Lin et al.

cated that retrograde cerebral perfusion could effectively protect the brain from ischemic injury in prolonged circulatory arrest. Furthermore, the rectal temperature during circulatory arrest and the duration of circulatory arrest of group 3 patients (21.7° C ± 0.8° C, range 20° to 24.8 ° C, and 63 ± 6 minutes) were significantly higher and longer than those of group 2 patients (15.9° ± 0.5° C,range13.5°to 17°C,and42 ± 4minutes). These differences indicate that prolonged circulatory arrest in moderate hypothermia could be safe with the aid of retrograde cerebral perfusion. Comparing the oxygen extraction ratio among the three groups, a flow rate of 300 ml/rnin was adequate for cerebral metabolism. In addition, repair of acute ascending aortic dissection with an intraluminal sutureless vascular graft during hypothermic circulatory arrest is a safe, easy, and effective procedure. The brain is the organ most sensitive to oxygen deprivation. Cessation of blood flow produces unconsciousness in 10 to 15 seconds because the cerebral oxygen stores are completely depleted. In 5 minutes, all aerobic and anaerobic metabolism stops, which results in cell swelling and brain death.!" Human beings can tolerate a body temperature of less than 20° C without permanent ill effects, thereby affording brain protection during hypothermic circulatory arrest. Forty minutes has been considered the safe limit at 18° to 20° C.8, 9 During hypothermic circulatory arrest, 45 minutes of cerebral ischemia is associated with a higher risk of stroke and 65 minutes of ischemia is associated with a high mortality rate.? Even with "safe" periods of circulatory arrest, apparent brain injury occurs in up to 4% of children" and 15% of adults.f IS This observation indicates that deep ( < 18° C) hypothermia during circulatory arrest does not provide adequate cerebral protection for all patients. The optimal temperature for brain protection during circulatory arrest has not yet been defined.l" Continuous brain perfusion during circulatory arrest might be the only way to protect the brain from ischemic injury during prolonged periods of circulatory arrest. \7 Cannulation of the vessels of the aortic arch might be difficult or troublesome in small children or in patients with aortic arch aneurysm or dissection. Retrograde cerebral perfusion through the superior vena cava was introduced clinically to extend the safe period of circulatory arrest and to obviate its side effects.S 10-12 The mechanisms of action of retrograde cerebral perfusion include (I) maintaining metabolic function, (2) providing oxygen, (3) removing lactic acid and waste products from the brain, and (4) flushing out any emboli that might have reached the brain. 9 Experimental studies with rats showed the

The Journal of Thoracic and Cardiovascular Surgery November 1994

efficacy of retrograde cerebral perfusion in protecting the brain from focal cerebral ischemia.lf 19 Retrograde cerebral perfusion has been applied recently in aortic surgery during short periods (less than 60 minutes) of hypothermic circulatory arrest to protect the brain.o 12, 13 We5 have previously demonstrated that retrograde cerebral perfusion is effective in protecting the brain during deep «18° C) hypothermic circulatory arrest from 27 to 67 minutes (mean 45 minutes) in four of ten patients receiving surgical correction of acute type A aortic dissection. Prolonged cardiopulmonary bypass required for deep hypothermia is associated with increased bleeding and a higher mortality rate.' Indeed, deep hypothermia might be not necessary if retrograde cerebral perfusion could protect the brain from ischemic injury. All of the patients in groups 2 and 3 of our series regained consciousness promptly after the operation without any neurologic defects, albeit preoperative comprehensive neurologic and psychologic studies were not performed. This good result demonstrated that the safe period of hypothermic circulatory arrest could be extended up to 93 minutes with the aid of retrograde cerebral perfusion. In group 3 patients, hypothermic circulatory arrest was performed with a rectal temperature of 21.7° ± 0.8° C. However, because oxygenated blood (15 ° to 18° C) from the oxygenator was pumped to the bilateral internal jugular veins for retrograde cerebral perfusion, the brain was actually in a deep hypothermic condition, although we did not measure its temperature. Results of the electroencephalographic studies were within normal limits in all eight patients of this group. This indicates that deep hypothermia of the body is probably not necessary when the brain is retrogradely perfused. With the aid of retrograde cerebral perfusion, operations in which hypothermic circulatory arrest is used could be performed more meticulously and slowly. The technique might allow younger surgeons to operate, as in our group 3 patients. However, comprehensive neurologic and psychologic studies, especially intellectual and cognitive function, are mandatory before routine application of retrograde cerebral perfusion with moderate hypothermic circulatory arrest. Weare currently performing these studies postoperatively for all of the patients who survived. The oxygen saturation (see Table II) of the blood samples taken from the carotid artery (venous blood) indicated that brain tissue could effectively extract oxygen from the oxygenated blood perfused retrogradely. A significant difference was noted in oxygen extraction ratio between blood samples of group 2 and control samples but no significant difference between that of group 3 and control samples. This discrepancy indicates that retro-

The Journal of Thoracic and Cardiovascular Surgery Volume 108, Number 5

grade cerebral perfusion with a flow rate of 150 ml/min was inadequate for cerebral metabolism even during deep hypothermic circulatory arrest. However, a higher flow rate, 300 ml/rnin, was sufficient even at a higher rectal temperature (more than 20° C) with an increased cerebral metabolic rate. Surgical treatment of patients with acute type A aortic dissection is accompanied by a high operative mortality rate. The hospital mortality rate has been 5% to 30%.20-24 These grave results are related to difficult hemostasis, which results from technical problems associated with the construction of conventional sutured anastomoses between a tubular prosthesis and a dissected aortic walJ.25 The use of a tie-in sutureless intraluminal prosthesis with rigid spools was introduced to reduce the complications and mortality rate by obviating the need for sutured anastomoses in aortic dissection. 26-28 With the use of an intraluminal graft and the technique described (wrapping of the ascending aorta, modified Cabrol shunt) in both this report and our previous report.' hemostasis was not a problem. In our experience, wrapping of the ascending aorta is most useful for hemostasis. We seldom used the modified Cabrol shunt in our most recent patients. The amount of postoperative drainage for the first 6 hours was usually less than 500 ml (see Table I). This demonstrated that surgical treatment of acute type A aortic dissection with an intraluminal graft and the techniques described herein could be an easy, safe, and practical procedure and could be performed by a group of surgeons, including younger surgeons. Hypothermic circulatory arrest had been applied in the repair of acute ascending aortic dissection to avoid crossclamping of the fragile dissecting aorta. 29 However, prolonged cardiopulmonary bypass was needed for cooling and rewarming, as in the operations for group 1 and 2 patients. This requirement could be overcome by performing circulatory arrest with moderate hypothermia with the aid of retrograde cerebral perfusion to protect the brain, as in the operations for group 3 patients. Their total bypass time was significantly shorter than that of group I and 2 patients, although the circulatory arrest time was significantly longer (see Table I). The mortality rate is even higher when the arch is included in the repair, 16% to 55% when traditional sutured anastomoses are used. 23, 24, 28, 30, 31 Our previous report' and this report suggest that primary repair of an intimal tear located in the aortic arch and replacement of the dissected ascending aorta with intraluminal sutureless grafts can be performed successfully and safely, with good short-term results, in these high-risk patients. Follow-up

Lin et al.

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computed tomographic studies of the chest demonstrated a decrease in size of the false lumen in the aortic.arch and descending aorta. None of our seven patients whose intimal tears in the aortic arch were primarily repaired needed further surgical intervention during the follow-up period. However, a longer follow-up time is necessary with these patients. In conclusion, retrograde cerebral perfusion can effectively protect the brain from ischemic injury and extend the safe period of hypothermic circulatory arrest. With the aid of retrograde cerebral perfusion, prolonged circulatory arrest can probably be performed safely with moderate hypothermia. Deep hypothermia is probably not necessary. Sutureless intraluminal grafts make surgical repair of acute type A aortic dissection an easy, safe, and practical procedure. REFERENCES 1. Niazi SA, Lewis FJ. Profound hypothermia: report of a case. Ann Surg 1957;147:264-6. 2. Ergin MA, O'Connor J, Guinto R, et al. Experiencewith profound hypothermia and circulatory arrest in the treatment of aneurysms of the aortic arch. J THORAC CARDIOVASCSURG 1982;84:649-55. 3. Livesay JJ, CooleyDA, Reul GJ, et al. Resectionof aortic arch aneurysms: a comparisonof hypothermic techniques in 60 patients. Ann Thorac Surg 1983;36: 19-28. 4. DavisEA, Gillinov AM, Cameron DE, et al. Hypothermic circulatoryarrest as a surgicaladjunct: a 5-year experience with 60 adult patients. Ann Thorac Surg 1992;53:402-7. 5. Liu DW, Lin PJ, Chang CH. Treatment of acute type A aortic dissection with intraluminal sutureless prosthesis. Ann Thorac Surg 1994;57:987-91. 6. Tharion J, Johnson DC, Celermajer JM, et al. Profound hypothermia with circulatory arrest. Nine years' clinical experience. J THORAC CARDIOVASC SURG 1992;84:66-72. 7. Baumgartner WA, Silverberg GD, Roam AH, et al. Reappraisal of cardiopulmonarybypasswith deep hypothermia and circulatory arrest for complex neurosurgical operations. Surgery 1983;94:242-7. 8. Fessatidis IT, Thomas VL, Shore DF, et al. Brain damage after profoundly hypothermic circulatory arrest: correlations between neurophysiologic and neuropathologic findings. J THORAC CARDIOVASC SURG 1993;106:32-41. 9. Svensson LG, Crawford ES, Hess KR, et al. Deep hypothermia with circulatory arrest: determinants of stroke and early mortality in 656 patients. J THORAC CARDIOVASC SURG 1993;106:19-31. 10. Veda Y, Miki S, Kusuhara K, Okita Y, Tahata T, Yamanaka K. Surgicaltreatment ofaneurysmor dissection involving the ascendingaorta and aortic arch, utilizingcirculatory arrest and retrograde cerebral perfusion. J Cardiovasc Surg 1990;31 :553-8. 11. Veda Y, Miki S, Kusuhara K, Okita Y, Tahata T,

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22. Glower DD, Speier RH, White WD, Smith LR, Rankin JS, Wolfe WG. Management and long-term outcome of aortic dissection. Ann Surg 1991;214:31-41. 23. Yun KL, Glower DD, Miller DC, et al. Aortic dissection resulting from tear of transverse arch: Is concomitant arch repair warranted? J THORAC CARDIOVASC SURG 1991; 102:355-70. 24. Crawford ES, Kirklin JW, Naftel DC, Svensson LG, Coselli JS, Safi HJ. Surgery for acute dissection of ascending aortic: Should the arch be included? J THORAC CARDIOVASC SURG 1992;104:46-59. 25. Berger RL, Karlson KJ, Dunton RF, Leonardi HK. Replacement of the thoracic aorta with intraluminal sutureless prosthesis. Ann Thorac Surg 1992;53:920-7. 26. Dureau G, Villard J, George M, Deliry P, Froment JC, Clermont A. New surgical technique for the operative management of acute dissections of the ascending aorta. J THORAC CARDIOVASC SURG 1978;76:385-9. 27. Ablaza SG, Ghosh SC, Grana VP. Use of a ringed intraluminal graft in the surgical treatment of dissecting aneurysms of the thoracic aorta. J THORAC CARDIOVASC SURG 1978;76:390-6. 28. Lemole GM, Strong MD, Spagna PM, Karmilowicz MP. Improved results for dissecting aneurysms: intraluminal sutureless prosthesis. J THORAC CARDIOVASC SURG 1982; 83:249-55. 29. Cooley DA. Experience with hypothermic circulatory arrest and the treatment of aneurysms of the ascending aorta. Semin Thorac Cardiovasc Surg 1991;3:166-70. 30. Graham JM, Stinnett DM. Operative management of acute aortic arch dissection using profound hypothermia and circulatory arrest. Ann Thorac Surg 1987;44:192-8. 31. Bachet J, Teodori G, Goudot B, et al. Replacement of the transverse aortic arch during emergency operations for type A acute aortic dissection: report of 26 cases. J THORAC CARDIOVASC SURG 1988;96:878-86.