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Replacement of the thoracic aorta with collagen-impregnated woven Dacron grafts
Replacement of the thoracic aorta with collagen-impregnated woven Dacron grafts Early results We used the collagen-impregnated woven double-velour Dacron graft in 120 patients undergoing 122 aortic reconstructions. Seventy-nine aortic root, ascending, or arch replacements were performed during cardiopulmonary bypass with or without circulatory arrest; 53 of the 79 were for acute aortic dissection. In addition, three infants and one child underwent repair of truncus arteriosus. There were no deaths caused by hemorrhage or bleeding-related complications. For-aortic root replacement, the impervious nature of the collagen-impregnated woven double velour Dacron graft allowed elimination of wraparound techniques. Eight deaths occurred as a result of multisystem organ failure, which followed late diagnosis of type A dissection. Two patients underwent reoperation for late complications of type A dissection. Thirty-nine patients underwent treatment for disease of the descending aorta; eight of these patients underwent a central cannulation technique with profound hypothermic cardiopulmonary bypass. The other 31 underwent repair with aortic crossclamping without bypass. Four of these patients died: two as a result of multisystem organ failure, one as a result of uncontrolled bleeding from the native dissected aorta, and one as a result of intestinal necrosis. Follow-up studies for 2 months to 5 years revealed three late deaths caused by the rupture of a persistent aneurysmal false lumen after type A dissection. The intraoperative advantages of the collagen-impregnated woven double velour Dacron graft represent an important advance in vascular graft technology. Its handling and suturing characteristics are excellent, and the graft is completely impervious in its originally manufactured state. Needle holes self-seal rapidly. Medium-term follow-up by clinical, angiographic, computed tomographic, and magnetic resonance imaging techniques showed no late graft complicationsspecifically, no dilatation or thrombus formation. (J THORAe CARDIOVASC SURG 1993;106:427-33)
S. Westaby, MS, FRCS, A. Parry, FRCS, N. Giannopoulos, MD, and R. Pillai, FRCS, Oxford, England
Bleeding problems remain an important cause of morbidity and mortality in operations on the thoracic aorta, particularly for aortic dissection. I, 2 Operative methods have long been influenced by the relatively porous nature of vascular prostheses. Indeed, the classic wraparound techniques for aortic root replacement, as described by Bentall and De Bono.' with modifications by Cabrol and associates,"were designed specifically to cope with oozing From the Oxford Heart Centre, Oxford, England. Received for publication Mar. 9, 1992. Accepted for publication Aug. 4, 1992. Address for reprints: S. Westaby, Oxford Heart Centre, John Radcliffe Hospital, Headington, Oxford, OX3 9DU, England. Copyright © 1993 by Mosby-Year Book, Inc. 0022-5223/93 $1.00 +.10
12/1/41631
through porous grafts. Hemorrhage contributes to morbidity by prolonging the duration of operation and predisposing the patient to renal and pulmonary dysfunction after multiple transfusions. Prolonged hypothermic cardiopulmonary bypass itself leads to coagulation prob-
lems.' As a rule, the lower the porosity of a vascular graft, the stiffer the wall and the higher the resistance to suture penetration. Low-porosity (50 ml/cm 2 per minute) woven grafts are designed specifically for use in patients who require systemic heparinization for replacement of the thoracic aorta. However, handling characteristics are particularly poor and preclotting is still advisable. We have used either coating with autologous or heterologous plasma followed by microwave coagulation or samegroup fresh donor blood preclotting.P- 7 Both processes are 427
428
The Journal of Thoracic and Cardiovascular Surgery September 1993
Westaby et al.
Table I. Primary diseases of the thoracic aorta
M/F
Age range (yr)
53 10 8'
38/15 7/3 5/3
31-79 36-64 39-73
2
1/1
71-81
4
3/1
I/O
63-75 57
13
11/2
19-61
12 5
9/3 5/0
12-47 63-72
4
4/0
56-74
4
4/0
32-71
4 120
..JJ.J:.
No. of patients Type A dissection Aortoannularectasia Ascending aortic aneurysm Ascending and arch aneurysm Aortic arch aneurysm Infectedaortic root (previous AVR) Traumatic aortic transection Coarctation Descending aortic aneurysm Acute type B aortic dissection Thoracoabdominal aneurysm Truncus arteriosus
Table II. Thoracic and thoracoabdominal aortic
I
76/25
reconstruction with Hemashield grafts No. of Elective/ Hospital patients emergency deaths Aortic root replacement Aortic root and arch replacement Ascending aortic replacement Aortic arch replacement Descending aortic replacement Descending aortic bypass Thoracoabdominal replacement Coarctationpatch angioplasty Truncus arteriosus repair
~2-9 ~12-81
AVR, Aortic valvereplacement.
'One chronictype A dissection with abdominal aortic aneurysm.
tedious and increase graft stiffness and resistance to the passage of sutures. The use of a nonporous vascular graft would therefore simplify operative technique considerably. Hemashield material (Meadox Medicals, Inc., Oakland, N.J.) is low-porosity woven double-velour Dacron graft material (H-WDV) that is impregnated with type I collagen, derived from fresh, young calf skin. The collagen is absorbable and is rendered nonantigenic by cross-linking on the graft surface. g, 9 The resulting vascular prosthesis is completely impervious (zero porosity) and blood compatible and does not induce platelet aggregation or intravascular clotting.!" We report our early experience with this graft in 120 patients.
Patients and methods Between June 1987 and June 1992, l20'patients underwent 122 operations on the thoracic aorta with the H-WDV graft. The primary pathologic process and the surgical procedures are summarized in Tables I and II, respectively. During this time frame, 34 other patients underwent operations on the thoracic aorta: 19 for aortic root replacement, 5 for direct repair of traumatic aortic laceration, 7 for resection and end-to-end anastomosis in adult coarctation, and 3 for truncus arteriosus repair with homograft tissue only. Of the patients undergoing aortic root replacement with grafts other than H-WDV, 14 had a Medtronic composite valved conduit (Medtronic, Inc., Minneapolis, Minn.), one had a St. Jude Medical valved conduit (St. Jude Medical, Inc., St. Paul, Minn.), and four had aortic
Mortality (%) «u 6 (6.25)
16'
11/5
2
0/2
0
56t
7/49
9
16(±10)
5:1:
3/2
2
40
26
8/18
3
II ± 9 (I 1.5)
4
4/0
0
4§
3/1
5
5/0
0
0
4
~
I
25
122
45/77
17
14%
0
0 25
CL, Confidence limit.
'Including one reoperation after repair of type A dissection. [One in combination with abdominalaortic replacement. :j:Including one reoperation after repair of type A dissection. §Twofor coarctationand one thromboexclusion technique.
homograft repair. These patients were not considered further in the study. Ascending aorta and arch. Ofthe 53 patients with acute type A dissection, 50 underwent ascending aortic replacement with valve resuspension. In three patients the aortic root was severely damaged, requiring replacement with a composite graft of H- WDV into which a Starr-Edwards ball valve (Baxter Healthcare Corp., Edwards Division, Santa Ana, Calif.) was sewn. Two of these patients had Marfan syndrome. Six patients with aortic dissection required coronary grafts in addition to ascending aortic replacement. One patient had previously undergone coronary grafting procedures and underwent replacement of the ascending aorta with excision of the proximal ends of the bypass grafts on buttons of aortic wall, which were then reimplanted into the ascending aortic graft. This method was also used in a patient with chronic type A dissection. Two patients with chronic type A dissection underwent combined aortic root and arch replacement. Ten patients underwent elective aortic root replacement for annuloaortic ectasia; two of these patients had Marfan syndrome. Seven others underwent elective replacement of the ascending aorta for aneurysms. One of these seven patients also underwent elective repair of an abdominal aortic aneurysm during the same operation. Four other patients underwent aortic arch replacement, one for rupture of a syphilitic arch aneurysm with exsanguination into the left side of the chest. A Jehovah's Witness underwent successful emergency ascending aorta and arch replacement for a leaking chronic type A dissection. In patients undergoing replacement of the aortic root and ascending aorta, the diseased aorta was excised and was not used
The Journal of Thoracic and Cardiovascular Surgery Volume 106, Number 3
Westaby et al. 4 2 9
Fig. 1. Follow-up nuclear magnetic resonance scan of a 40 em Hemashield graft after the thromboexclusion operation for a massive descending thoracic aneurysm. The patient was a Jehovah's Witness. for wraparound. The coronary ostia were mobilized and implanted directly into the graft. In patients with aortic dissection, the aortic wall was reconstituted with gelatin-resorcinol glue. Twenty-five hospital survivors of acute type A dissection repair underwent follow-up studies with nuclear magnetic resonance imaging, which detected need for reoperation in two patients. The first reoperation was done to replace progressively aneurysmal aortic sinuses by root replacement with a composite Starr-Edwards (Baxter Healthcare, Corp.)-H-WDV graft; the second was done to replace a massive aortic arch aneurysm with another H-WDV graft. Descending thoracic and thoracoabdominal aorta. Thirteen patients underwent replacement of a segment of the descendingthoracic aorta (3 to 10 em) for traumatic aortic laceration. Twelve adult patients underwent repair of coarctation of the aorta, fiveby diamond patch angioplasty, four by resection and tube graft reconstruction, and three by tube bypass of the coarctation. The fourth patient to undergo descending aortic bypasswas a Jehovah's Witness with a massive,chronic type B dissection extending from midaortic arch to the renal arteries. For this patient, the thromboexclusion technique was used with a 40 em graft from the ascending aorta that was taken through the diaphragm and anastomosed to the infrarenal aorta. Coronary grafting procedures were performed for a left main-stem lesion, and then the aortic arch was stapled off between the left carotid and left subclavian arteries (Fig. 1). Four patients with acute type B aortic dissection required
operation for leak into the left pleural cavity. Other patients with type B dissection underwent conservative treatment. Nine patients underwent repair of descending thoracic or thoracoabdominal aneurysm. Three had a rupture necessitating emergency operation. In one patient a ruptured thoracoabdominal aneurysm required replacement from the left subclavian artery to below the renal vessels, with reimplantation of the celiac axis, the superior mesenteric artery, and the right and left renal arteries. The procedure was performed through a retroperitoneal approach, and subsequently laparotomy was required for ischemic gut, which was present before the first surgical procedure. Despite this complication, the patient survived. In patients with descending thoracic or thoracoabdominal aneurysms, attempts were made to identify and conserve the principal spinal artery. Pediatric patients. Three infants and one 9-year-old child underwent repair of truncus arteriosus with a composite graft of H-WDV and homograft material. In the three infants, a small aortic homograft was anastomosed to the H-WDV graft. In the 9-year-old child, the pulmonary arteries were discontinuous with the left pulmonary artery, originating from the ductus arteriosus outside the pericardium. A fresh pulmonary homograft, comprising valve and main and branch pulmonary arteries, was harvested, transplanted directly into the patient, and attached to a H-WDV graft. Perfusion techniques. All patients who underwent operation of the aortic root, ascending aorta, or aortic arch underwent
4 30
Westaby et al.
cardiopulmonary bypass with moderate or profound hypothermia, with or without totalcirculatory arrest. One patient with an aneurysm of the ascending aortaalso underwent abdominal aneurysm repair with continuous hypothermic perfusion. For patients with acuteaortic dissection, aortic arch pathology, or ascending aortic aneurysms extending intothe aortic arch, the arterial cannula was positioned in the right or left femoral artery. Patients with aortic rootdisease, in cases in which the aneurysm stopped 2 to 3 em before the innominate artery, underwent arterial cannulation oftheaortajustproximal tothe innominate artery. In two thirds of the patients with type A aortic dissection, thedistal anastomosis was performed with the open-ended technique described by Cooley and Livesay. I I For patients undergoing total circulatory arrest, a combination of thiopental sodium, nimodipine, andmannitol was used forcerebral protection. In eight patients with typeBdissection or thoracoabdominal aneurysm, cardiopulmonary bypass with profound hypothermia and periods of circulatory arrestwere used. The right atrium was first cannulated with a two-stage venous cannula inserted through the right internal jugular vein. The patient was then positioned for left thoracotomy, and the arterial cannula was placed in the proximal aortic arch.l? Repairs of traumatic aorticlaceration, coarctation of theaorta, andremaining descendingthoracic aneurysms were performed bysimple crossclamping without the use of shunts, heparinization, or perfusion. Systemic heparinization was used for 87 of 122 procedures. Aprotinin was used in patients with acutedissection but notin patients undergoing elective operations or in those who didnot undergo bypass. The cell saver device (Haemonetics Corp., Braintree, Mass.) andautotransfusion were used routinely. We did notspecifically study postoperative blood loss because this is a multifactorial problem and the graft itself is completely impervious. Results The graft. H-WDV is soft and pliable and no fragmentation of collagen occurred during preparation. Although needles pass effortlessly through the material, needle holes self-seal rapidly. Suture materials as fine as 5-0 and 6-0 Prolene sutures (Ethicon, Inc., Somerville, N.J.) can be used for continuousanastomoses(for example, with coronary reimplantation during aortic root replacement) without the needfor newneedlesduring the procedure. The graft is completely impervious to heparinized blood, thus eliminating preclotting procedures. There was no significantbleedingthrough either the graft itself or the needle or air holes. In one patient with Marfan syndrome who had disseminated intravascular coagulation with defibrination after aortic root replacement, all cut surfaces bled profusely, yet there was no bleeding through or around the H-WDV graft. There was no evidence that collagenhad been eluted from the graft during defibrination. In two patients in whom reoperation was done for late complicationsof type A dissection, a sample of the original graft was taken for histologic examination.Analysis
The Journal of Thoracic and Cardiovascular Surgery September 1993
showed no evidence of residual collagen 2 years after implantation.There was nodifficulty in anastomosing the new H-WDV graft to the preexistingone. Postmortem findings in patients whodied in the hospital after repair of type A dissection (n = 6) or descending aortic replacement (n = 3) showed no thrombus on the graft despiteprolongedperiodsof lowcardiac output and, in some patients, sepsis. Angiographic studies 10 days after full-length thoracoabdominal replacement in one patient showed the 40 em graft to be clean and smooth with patent endarterectomized reimplanted vessels. Patients. Hospital mortality and cause of death are shownin Tables II and III. There wasoneoperativedeath caused by hemorrhage during operation for a ruptured type B dissection. Reentry for bleedingwas done in four patients after type A dissection repair. In each case the graft was dry. For patients with acute type A aortic dissection, only two hospitaldeaths occurred when operation wascarried out within 48 hours of the acute event, even when streptokinase had been administered inadvertently.P Seven deaths occurred in patients who had late diagnosis after acute aortic dissection with associatedproblems, such as renal impairment, ischemicgut, adult respiratorydistress syndrome, and coagulopathy. One patient with Marfan syndrome had paraplegia after resection of the entire thoracoabdominal aorta with profound hypothermia. A second patient also had paraplegia after repair of traumatic aortic rupture but had waited 36 hourswithcompromised distal perfusion before interhospital transfer and operation. There were no deaths in patients with coarctation of the aorta and no other instance of paraplegia in survivors of descending aortic operations. We had no graft-related infection or reoperations for graft-related problems. Medium-term follow-up. One hundred three of the 120 patients were discharged from the hospital. Followup ranged from 2 months to 5 years (median 21 months). Three suddenlate deaths occurredin patientsoperatedon for type A dissection. These deaths probably followed rupture of the false lumen, although this was not proved by postmortem examination. Twenty-five survivors of type A dissection were studied with nuclear magnetic resonance scan between 6 weeks and 4.5 years after the operation. Thirteen patients had persistent flow in the falsechannel of the descendingaorta and two had further aneurysm formation requiring reoperation (aortic root and aortic arch replacements). The H-WDV graft remained unchanged, with no dilation or thrombus formation. A follow-up magnetic resonanceimagingscan 3 months after thoracoabdominal bypass grafting proce-
The Journal of Thoracic and Cardiovascular Surgery Volume 106, Number 3
Westaby et al.
431
Table III. Causes of hospital mortality (n = 17) Operation
Deaths
Aortic root replacement
Ascending aortic replacement
Cause of death Myocardial ischemia
9
Late rupture (n
= 2)
Multisystem failure (n = 7)
Aortic arch replacement
2
Descending aortic replacement
3
Cerebral emboli and ischemic legs (n = I) Multisystem failure (n= I) Multiple trauma (n = I) Bleeding (n = I)
Thoracoabdominal replacement Truncus arteriosus
Ischemic gut (n = I) Multisystem failure (n = I) Pulmonary hypertension
Comment Reoperation on a patient with renal transplant with aortic dissection, previous CABGs, and severe diffuse coronary disease Distal aortic rupture in two patients with type A dissection and Marfan syndrome, respectively, at 12 days Occurred in patients with established ischemic gut, renal failure, coagulopathy, or ARDS left untreated for more than 48 hours Diffuse embolism from an atherosclerotic clot-filled aneurysm Exsanguination from a ruptured syphilitic arch aneurysm Transected aorta repaired successfully Type B dissection that had ruptured into the pleural cavity; operation not completed Present before operation; unresolved Surgical bleeding led to multiple transfusion and prolonged operation Nine-year-old patient with discontinuous pulmonary arteries and fixed elevated pulmonary vascular resistance
CABGs, Coronary artery bypass grafts; ARDS, adult respiratory distress syndrome.
dures is shown in Fig. 1. We did not use magnetic resonance imaging for restudy of patients who did not have dissection. One patient had transient cerebral ischemic attacks after replacement of the ascending aorta for type A dissection, which included the underside of the aortic arch. The symptoms occurred 3 weeks after the operation and were attributed to a persistently dissected innominate artery. Platelet microemboli from the graft or an anastomotic site could also be responsible. This patient underwent anticoagulation with warfarin and was given aspirin as an antiplatelet agent. The symptoms ended without residual defect. No other neurologic symptoms or peripheral emboli that could be attributed to graft thrombus formation were found.
Discussion We consider the completely impervious nature of the H-WDV graft together with its excellent handling characteristics, ease of suture passage, and availability for implantation directly from the shelf to represent an important advance in vascular graft technology. It has allowed us to simplify thoracic aortic operations by eliminating wraparound techniques. Our method for aortic root replacement decreases the potential for coronary
artery false aneurysms by preventing accumulation of blood between the graft and the native, reconstituted diseased aortic wall. The particularly soft and flexible nature of H-WDV is beneficial when the native aorta is heavily calcified and has resulted in irregular vascular margins. Graft compliance facilitates a snug fit at the anastomosis and minimizes bleeding at the anastomotic site. Use of H-WDV has shortened the duration of some thoracic operations and reduced bleeding complications when compared subjectively with previous grafts. Collagen tubes have been used as vascular grafts in the past with limited success.14, 15 Many forms of collagen are thrombogenic, and this tendency has limited the usefulness of previous prostheses. With H-WDV, it has been established that thrombogenicity and other characteristics can be altered by cross-linking collagen with naturally occurring mucopolysaccharide or by reaction with selected chemical agents." These processes form a fully blood-compatible substance that can be used as a bioimplant. The collagen for H-WDV is prepared from calf skin by a sequence of steps including mechanical cleansing, washing, and chemical treatment.!" The processed skin is then homogenized to produce a paste composed primarily of collagen microfibers. This material consisting of 90% pure collagen is used to coat a woven double-
432
The Journal of Thoracic and Cardiovascular Surgery September 1993
Westaby et al.
velour Dacron polyester graft. Electron microscopy demonstrates that the collagen layer completely covers the fibers and interstices of the fabric. The prosthesis is biocompatible in terms of pyrogenicity, cytotoxicity, and antigenicity. Scott and associates'" implanted collagen-impregnated and control grafts into the thoracic aorta of dogs. The animals were killed at intervals of I to 180 days, and the grafts were examined for deposition of thrombus, inflammatory reaction, endothelialization, and rate of disappearance of the collagen. There was no significant difference in inflammatory reaction or thrombogenicity. Less than 10% of the bovine collagen remained on the graft after 30 days, and no collagen was identifiable 180 days after implantation. There was no evidence that collagen impaired healing in any way, induced platelet aggregation, or caused intravascular clotting. It was originally thought that high-porosity (knitted) grafts were necessary to allow endothelial cells and their subendothelial matrixes to invade and adhere to the inner surface of a vascular graft. However, although prosthetic grafts may develop neoendothelium in canine and primate models, experience in human beings has shown that reendothelialization occurs only sporadically if at all. 16- 18 Experimental work has demonstrated no difference in patency of woven versus knitted Dacron grafts. Robicsek and associates'? designed an aortic bifurcation graft in which one limb was knitted and the other was woven. These were implanted in 143 consecutive patients with atherosclerotic aortoiliac occlusion or abdominal aortic aneurysm and failed to reveal any difference in patency at periods of 1 month to 2 years. Although our overall hospital mortality for replacement of the ascending aorta was 16%, this is for a group in which emergency procedures were done for 87% of the patients; Other recent reports show an operative mortality of 10% for elective replacement of the ascending aorta and 24% for emergency operations.P We have previously reported the influence of delayed operation on mortality after acute type A dissection, and none of the deaths was directly related to operative hemorrhage" One patient who underwent elective replacement of the ascending aorta together with repair of abdominal aortic aneurysm died. He underwent the dual procedure because it was considered that his extremely poor respiratory function (forced expiratory volume 0.8 L) precluded survival of two separate major procedures.F Since our early experimental work with aprotinin, we have used this agent for operation of acute aortic dissection. 23 Because of the multifactorial nature of postoperative bleeding in this situation, particularly after profound
hypothermia.! we could not demonstrate significant benefit from aprotinin, and, in one patient, severe coagulopathy required massive blood transfusion and treatment with platelets, fresh frozen plasma, and cryoprecipitate. It is likely that profound hypothermia and total circulatory arrest have negative effects on platelet function that are not attenuated but are perhaps worsened by this drug. 24 REFERENCES 1. Carpentier A, Deloche A, Fabiani IN, et al. New surgical approach to aortic dissection: flow reversal and thromboexelusion. J THORAC CARDIOVASC SURG 1981;81:659-68. 2. Seguin JR, Frapier JM, Colson P, Chaptal PA. Fibrin sealant improves surgical results of type A acute aortic dissections. Ann Thorac Surg 1991;52:745-9. 3. Bentall HH, De Bono A. A technique for complete replacement of the ascending aorta. Thorax 1968;23: 338-9. 4. Cabrol C, Pavie A, Mesnildrey P, et al. Long-term results with total replacement of the ascending aorta and reimplantation of the coronary arteries. J THoRAc CARDIOVASC SURG 1986;91:17-25. 5. Harker LA. Bleeding after cardiopulmonary bypass. N Engl J Med 1986;314:1446-8. 6. Bethea MC, Reemtsma K. Graft hemostasis; an alternative to pre-clotting. Ann Thorac Surg 1979;27:374. 7. Cooley DA, Romagnoli A, Milam JD, Bossant ML. A method for preparing woven Dacron grafts to prevent interstitial hemorrhage. Bull Texas Heart Inst 1991;8:48. 8. Ruhland D, Wigges J, Bottcher K, von Bassewitz DB. Fate of collagen following implantation on microvel Hemashield grafts in the dog. Angio Archiv BD 1985;9:22-32. 9. Quinores-Baldrich WJ, Moore WAS, Ziomek S, Chvapil M. Development of a leak-proof knitted Dacron vascular prosthesis. J Vase Surg 1986;6:895-903. 10. Scott SM, Gaddy LR, Sahmel R, Hoffman H. A collagen coated vascular prosthesis. J Cardiovasc Surg 1987;28:498504. 11. Cooley DA, Livesay JJ. Technique of open distal anastomosis for ascending and transverse aortic resection. Cardiovasc Dis 1981;8:421-6. 12. Westaby S. Hypothermic thoracic and thoraco-abdominal aneurysm surgery: a central cannulation technique. Ann Thorac Surg 1992;54:253-8. 13. Butler J, Davies AH, Westaby S. Streptokinase in acute aortic dissection. Br Med J 1990;300:517-9. 14. Humphries AW, Hawk WA, Cuthbertson AM. Arterial prosthesis of collagen-impregnated Dacron tulle. Surgery 1961;50:947-54. 15. Kott I, Pierce EC, Mitty HA, Geller SA, Jacobson JH. The tissue tube as a vascular prosthesis. Arch Surg 1973; 106:206-7. 16. Dillin ML, Scott SM, Vasquez MD, Postlethwait RW,
The Journal of Thoracic and Cardiovascular Surgery Volume 106, Number 3
Dart CH. Tissue response to an arterial substitute of bovine origin. Arch Surg 1972;105:577-81. 17. Zacharias RK, Kirkman TR, Clowes AW. Mechanisms of healing in synthetic grafts. J Vase Surg 1987;6:429-36. 18. Keshishian JM, Smyth NPD, Adkins PC, Camp F, Yahn WZ. Clinical experience with the modified bovine arterial heterograft. Ann Surg 1970;172:690-700. 19. Robicsek F, Duncan GD, Anderson CE, et a!. Indium Ill-labelled platelet deposition in woven and knitted Dacron bifurcated aortic grafts with the same patient as a clinical model. J Vase Surg 1987;5:833-7. 20. Lytle BW, Mahfood SS, Cosgrove DM, Loop FD. Replacement of the ascending aorta: early and late results. J THORAC CARDIOVASC SURG 1990;99:651-8.
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21. Butler J, Ormerod OJM, Giannopoulos N, Pillai R, Westaby S. Diagnostic delay and outcome in surgery for type A aortic dissections. Q J Med 1991;289:391-6. 22. Westaby S, Parry A, Grebenik C, Pillai R, Lamont P. Combined cardiac and abdominal aortic aneurysm operations: the dual operation on cardiopulmonary bypass. J THORAC CARDIOVASC SURG 1992;104:990-5. 23. van Oeveran W, Jansen NJG, Bidstrup BP, eta!. Effects of aprotinin on hemostatic mechanisms during cardiopulmonary bypass. Ann Thorac Surg 1987;44:640-5. 24. Westaby S. Aprotinin in perspective. Ann Thorac Surg [In press].
Boundvolumes available to subscribers Boundvolumes of THE JOURNAL OF THORACIC AND CARDIOVASCULAR SURGERY are availableto subscribers(only) for the 1993issues from the Publisher,at a cost of $75.00for domestic, $98.25for Canadian, and $93.00for internationalsubscribersfor Vol. 105 (JanuaryJune) and Vol. 106 (July-December).Shipping charges are included. Each bound volumecontains a subject and author index and all advertising is removed. Copiesare shippedwithin60 days after publicationof the last issueof the volume.The bindingis durable buckram with the JOURNAL name, volumenumber, and year stamped in gold on the spine. Payment must accompany all orders. Contact Mosby, Subscription Services, 11830WestlineIndustrialDrive,St. Louis,Missouri63146-3318, USA; phone I (800) 453-4351 or (314) 453-4351. Subscriptions must be in force to qualify.Boundvolumes are not available in place of a regular JOURNAL subscription.
S. Westaby, MS, FRCS, A. Parry, FRCS, N. Giannopoulos, MD, and R. Pillai, FRCS, Oxford, England
Bleeding problems remain an important cause of morbidity and mortality in operations on the thoracic aorta, particularly for aortic dissection. I, 2 Operative methods have long been influenced by the relatively porous nature of vascular prostheses. Indeed, the classic wraparound techniques for aortic root replacement, as described by Bentall and De Bono.' with modifications by Cabrol and associates,"were designed specifically to cope with oozing From the Oxford Heart Centre, Oxford, England. Received for publication Mar. 9, 1992. Accepted for publication Aug. 4, 1992. Address for reprints: S. Westaby, Oxford Heart Centre, John Radcliffe Hospital, Headington, Oxford, OX3 9DU, England. Copyright © 1993 by Mosby-Year Book, Inc. 0022-5223/93 $1.00 +.10
12/1/41631
through porous grafts. Hemorrhage contributes to morbidity by prolonging the duration of operation and predisposing the patient to renal and pulmonary dysfunction after multiple transfusions. Prolonged hypothermic cardiopulmonary bypass itself leads to coagulation prob-
lems.' As a rule, the lower the porosity of a vascular graft, the stiffer the wall and the higher the resistance to suture penetration. Low-porosity (50 ml/cm 2 per minute) woven grafts are designed specifically for use in patients who require systemic heparinization for replacement of the thoracic aorta. However, handling characteristics are particularly poor and preclotting is still advisable. We have used either coating with autologous or heterologous plasma followed by microwave coagulation or samegroup fresh donor blood preclotting.P- 7 Both processes are 427
428
The Journal of Thoracic and Cardiovascular Surgery September 1993
Westaby et al.
Table I. Primary diseases of the thoracic aorta
M/F
Age range (yr)
53 10 8'
38/15 7/3 5/3
31-79 36-64 39-73
2
1/1
71-81
4
3/1
I/O
63-75 57
13
11/2
19-61
12 5
9/3 5/0
12-47 63-72
4
4/0
56-74
4
4/0
32-71
4 120
..JJ.J:.
No. of patients Type A dissection Aortoannularectasia Ascending aortic aneurysm Ascending and arch aneurysm Aortic arch aneurysm Infectedaortic root (previous AVR) Traumatic aortic transection Coarctation Descending aortic aneurysm Acute type B aortic dissection Thoracoabdominal aneurysm Truncus arteriosus
Table II. Thoracic and thoracoabdominal aortic
I
76/25
reconstruction with Hemashield grafts No. of Elective/ Hospital patients emergency deaths Aortic root replacement Aortic root and arch replacement Ascending aortic replacement Aortic arch replacement Descending aortic replacement Descending aortic bypass Thoracoabdominal replacement Coarctationpatch angioplasty Truncus arteriosus repair
~2-9 ~12-81
AVR, Aortic valvereplacement.
'One chronictype A dissection with abdominal aortic aneurysm.
tedious and increase graft stiffness and resistance to the passage of sutures. The use of a nonporous vascular graft would therefore simplify operative technique considerably. Hemashield material (Meadox Medicals, Inc., Oakland, N.J.) is low-porosity woven double-velour Dacron graft material (H-WDV) that is impregnated with type I collagen, derived from fresh, young calf skin. The collagen is absorbable and is rendered nonantigenic by cross-linking on the graft surface. g, 9 The resulting vascular prosthesis is completely impervious (zero porosity) and blood compatible and does not induce platelet aggregation or intravascular clotting.!" We report our early experience with this graft in 120 patients.
Patients and methods Between June 1987 and June 1992, l20'patients underwent 122 operations on the thoracic aorta with the H-WDV graft. The primary pathologic process and the surgical procedures are summarized in Tables I and II, respectively. During this time frame, 34 other patients underwent operations on the thoracic aorta: 19 for aortic root replacement, 5 for direct repair of traumatic aortic laceration, 7 for resection and end-to-end anastomosis in adult coarctation, and 3 for truncus arteriosus repair with homograft tissue only. Of the patients undergoing aortic root replacement with grafts other than H-WDV, 14 had a Medtronic composite valved conduit (Medtronic, Inc., Minneapolis, Minn.), one had a St. Jude Medical valved conduit (St. Jude Medical, Inc., St. Paul, Minn.), and four had aortic
Mortality (%) «u 6 (6.25)
16'
11/5
2
0/2
0
56t
7/49
9
16(±10)
5:1:
3/2
2
40
26
8/18
3
II ± 9 (I 1.5)
4
4/0
0
4§
3/1
5
5/0
0
0
4
~
I
25
122
45/77
17
14%
0
0 25
CL, Confidence limit.
'Including one reoperation after repair of type A dissection. [One in combination with abdominalaortic replacement. :j:Including one reoperation after repair of type A dissection. §Twofor coarctationand one thromboexclusion technique.
homograft repair. These patients were not considered further in the study. Ascending aorta and arch. Ofthe 53 patients with acute type A dissection, 50 underwent ascending aortic replacement with valve resuspension. In three patients the aortic root was severely damaged, requiring replacement with a composite graft of H- WDV into which a Starr-Edwards ball valve (Baxter Healthcare Corp., Edwards Division, Santa Ana, Calif.) was sewn. Two of these patients had Marfan syndrome. Six patients with aortic dissection required coronary grafts in addition to ascending aortic replacement. One patient had previously undergone coronary grafting procedures and underwent replacement of the ascending aorta with excision of the proximal ends of the bypass grafts on buttons of aortic wall, which were then reimplanted into the ascending aortic graft. This method was also used in a patient with chronic type A dissection. Two patients with chronic type A dissection underwent combined aortic root and arch replacement. Ten patients underwent elective aortic root replacement for annuloaortic ectasia; two of these patients had Marfan syndrome. Seven others underwent elective replacement of the ascending aorta for aneurysms. One of these seven patients also underwent elective repair of an abdominal aortic aneurysm during the same operation. Four other patients underwent aortic arch replacement, one for rupture of a syphilitic arch aneurysm with exsanguination into the left side of the chest. A Jehovah's Witness underwent successful emergency ascending aorta and arch replacement for a leaking chronic type A dissection. In patients undergoing replacement of the aortic root and ascending aorta, the diseased aorta was excised and was not used
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Fig. 1. Follow-up nuclear magnetic resonance scan of a 40 em Hemashield graft after the thromboexclusion operation for a massive descending thoracic aneurysm. The patient was a Jehovah's Witness. for wraparound. The coronary ostia were mobilized and implanted directly into the graft. In patients with aortic dissection, the aortic wall was reconstituted with gelatin-resorcinol glue. Twenty-five hospital survivors of acute type A dissection repair underwent follow-up studies with nuclear magnetic resonance imaging, which detected need for reoperation in two patients. The first reoperation was done to replace progressively aneurysmal aortic sinuses by root replacement with a composite Starr-Edwards (Baxter Healthcare, Corp.)-H-WDV graft; the second was done to replace a massive aortic arch aneurysm with another H-WDV graft. Descending thoracic and thoracoabdominal aorta. Thirteen patients underwent replacement of a segment of the descendingthoracic aorta (3 to 10 em) for traumatic aortic laceration. Twelve adult patients underwent repair of coarctation of the aorta, fiveby diamond patch angioplasty, four by resection and tube graft reconstruction, and three by tube bypass of the coarctation. The fourth patient to undergo descending aortic bypasswas a Jehovah's Witness with a massive,chronic type B dissection extending from midaortic arch to the renal arteries. For this patient, the thromboexclusion technique was used with a 40 em graft from the ascending aorta that was taken through the diaphragm and anastomosed to the infrarenal aorta. Coronary grafting procedures were performed for a left main-stem lesion, and then the aortic arch was stapled off between the left carotid and left subclavian arteries (Fig. 1). Four patients with acute type B aortic dissection required
operation for leak into the left pleural cavity. Other patients with type B dissection underwent conservative treatment. Nine patients underwent repair of descending thoracic or thoracoabdominal aneurysm. Three had a rupture necessitating emergency operation. In one patient a ruptured thoracoabdominal aneurysm required replacement from the left subclavian artery to below the renal vessels, with reimplantation of the celiac axis, the superior mesenteric artery, and the right and left renal arteries. The procedure was performed through a retroperitoneal approach, and subsequently laparotomy was required for ischemic gut, which was present before the first surgical procedure. Despite this complication, the patient survived. In patients with descending thoracic or thoracoabdominal aneurysms, attempts were made to identify and conserve the principal spinal artery. Pediatric patients. Three infants and one 9-year-old child underwent repair of truncus arteriosus with a composite graft of H-WDV and homograft material. In the three infants, a small aortic homograft was anastomosed to the H-WDV graft. In the 9-year-old child, the pulmonary arteries were discontinuous with the left pulmonary artery, originating from the ductus arteriosus outside the pericardium. A fresh pulmonary homograft, comprising valve and main and branch pulmonary arteries, was harvested, transplanted directly into the patient, and attached to a H-WDV graft. Perfusion techniques. All patients who underwent operation of the aortic root, ascending aorta, or aortic arch underwent
4 30
Westaby et al.
cardiopulmonary bypass with moderate or profound hypothermia, with or without totalcirculatory arrest. One patient with an aneurysm of the ascending aortaalso underwent abdominal aneurysm repair with continuous hypothermic perfusion. For patients with acuteaortic dissection, aortic arch pathology, or ascending aortic aneurysms extending intothe aortic arch, the arterial cannula was positioned in the right or left femoral artery. Patients with aortic rootdisease, in cases in which the aneurysm stopped 2 to 3 em before the innominate artery, underwent arterial cannulation oftheaortajustproximal tothe innominate artery. In two thirds of the patients with type A aortic dissection, thedistal anastomosis was performed with the open-ended technique described by Cooley and Livesay. I I For patients undergoing total circulatory arrest, a combination of thiopental sodium, nimodipine, andmannitol was used forcerebral protection. In eight patients with typeBdissection or thoracoabdominal aneurysm, cardiopulmonary bypass with profound hypothermia and periods of circulatory arrestwere used. The right atrium was first cannulated with a two-stage venous cannula inserted through the right internal jugular vein. The patient was then positioned for left thoracotomy, and the arterial cannula was placed in the proximal aortic arch.l? Repairs of traumatic aorticlaceration, coarctation of theaorta, andremaining descendingthoracic aneurysms were performed bysimple crossclamping without the use of shunts, heparinization, or perfusion. Systemic heparinization was used for 87 of 122 procedures. Aprotinin was used in patients with acutedissection but notin patients undergoing elective operations or in those who didnot undergo bypass. The cell saver device (Haemonetics Corp., Braintree, Mass.) andautotransfusion were used routinely. We did notspecifically study postoperative blood loss because this is a multifactorial problem and the graft itself is completely impervious. Results The graft. H-WDV is soft and pliable and no fragmentation of collagen occurred during preparation. Although needles pass effortlessly through the material, needle holes self-seal rapidly. Suture materials as fine as 5-0 and 6-0 Prolene sutures (Ethicon, Inc., Somerville, N.J.) can be used for continuousanastomoses(for example, with coronary reimplantation during aortic root replacement) without the needfor newneedlesduring the procedure. The graft is completely impervious to heparinized blood, thus eliminating preclotting procedures. There was no significantbleedingthrough either the graft itself or the needle or air holes. In one patient with Marfan syndrome who had disseminated intravascular coagulation with defibrination after aortic root replacement, all cut surfaces bled profusely, yet there was no bleeding through or around the H-WDV graft. There was no evidence that collagenhad been eluted from the graft during defibrination. In two patients in whom reoperation was done for late complicationsof type A dissection, a sample of the original graft was taken for histologic examination.Analysis
The Journal of Thoracic and Cardiovascular Surgery September 1993
showed no evidence of residual collagen 2 years after implantation.There was nodifficulty in anastomosing the new H-WDV graft to the preexistingone. Postmortem findings in patients whodied in the hospital after repair of type A dissection (n = 6) or descending aortic replacement (n = 3) showed no thrombus on the graft despiteprolongedperiodsof lowcardiac output and, in some patients, sepsis. Angiographic studies 10 days after full-length thoracoabdominal replacement in one patient showed the 40 em graft to be clean and smooth with patent endarterectomized reimplanted vessels. Patients. Hospital mortality and cause of death are shownin Tables II and III. There wasoneoperativedeath caused by hemorrhage during operation for a ruptured type B dissection. Reentry for bleedingwas done in four patients after type A dissection repair. In each case the graft was dry. For patients with acute type A aortic dissection, only two hospitaldeaths occurred when operation wascarried out within 48 hours of the acute event, even when streptokinase had been administered inadvertently.P Seven deaths occurred in patients who had late diagnosis after acute aortic dissection with associatedproblems, such as renal impairment, ischemicgut, adult respiratorydistress syndrome, and coagulopathy. One patient with Marfan syndrome had paraplegia after resection of the entire thoracoabdominal aorta with profound hypothermia. A second patient also had paraplegia after repair of traumatic aortic rupture but had waited 36 hourswithcompromised distal perfusion before interhospital transfer and operation. There were no deaths in patients with coarctation of the aorta and no other instance of paraplegia in survivors of descending aortic operations. We had no graft-related infection or reoperations for graft-related problems. Medium-term follow-up. One hundred three of the 120 patients were discharged from the hospital. Followup ranged from 2 months to 5 years (median 21 months). Three suddenlate deaths occurredin patientsoperatedon for type A dissection. These deaths probably followed rupture of the false lumen, although this was not proved by postmortem examination. Twenty-five survivors of type A dissection were studied with nuclear magnetic resonance scan between 6 weeks and 4.5 years after the operation. Thirteen patients had persistent flow in the falsechannel of the descendingaorta and two had further aneurysm formation requiring reoperation (aortic root and aortic arch replacements). The H-WDV graft remained unchanged, with no dilation or thrombus formation. A follow-up magnetic resonanceimagingscan 3 months after thoracoabdominal bypass grafting proce-
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Table III. Causes of hospital mortality (n = 17) Operation
Deaths
Aortic root replacement
Ascending aortic replacement
Cause of death Myocardial ischemia
9
Late rupture (n
= 2)
Multisystem failure (n = 7)
Aortic arch replacement
2
Descending aortic replacement
3
Cerebral emboli and ischemic legs (n = I) Multisystem failure (n= I) Multiple trauma (n = I) Bleeding (n = I)
Thoracoabdominal replacement Truncus arteriosus
Ischemic gut (n = I) Multisystem failure (n = I) Pulmonary hypertension
Comment Reoperation on a patient with renal transplant with aortic dissection, previous CABGs, and severe diffuse coronary disease Distal aortic rupture in two patients with type A dissection and Marfan syndrome, respectively, at 12 days Occurred in patients with established ischemic gut, renal failure, coagulopathy, or ARDS left untreated for more than 48 hours Diffuse embolism from an atherosclerotic clot-filled aneurysm Exsanguination from a ruptured syphilitic arch aneurysm Transected aorta repaired successfully Type B dissection that had ruptured into the pleural cavity; operation not completed Present before operation; unresolved Surgical bleeding led to multiple transfusion and prolonged operation Nine-year-old patient with discontinuous pulmonary arteries and fixed elevated pulmonary vascular resistance
CABGs, Coronary artery bypass grafts; ARDS, adult respiratory distress syndrome.
dures is shown in Fig. 1. We did not use magnetic resonance imaging for restudy of patients who did not have dissection. One patient had transient cerebral ischemic attacks after replacement of the ascending aorta for type A dissection, which included the underside of the aortic arch. The symptoms occurred 3 weeks after the operation and were attributed to a persistently dissected innominate artery. Platelet microemboli from the graft or an anastomotic site could also be responsible. This patient underwent anticoagulation with warfarin and was given aspirin as an antiplatelet agent. The symptoms ended without residual defect. No other neurologic symptoms or peripheral emboli that could be attributed to graft thrombus formation were found.
Discussion We consider the completely impervious nature of the H-WDV graft together with its excellent handling characteristics, ease of suture passage, and availability for implantation directly from the shelf to represent an important advance in vascular graft technology. It has allowed us to simplify thoracic aortic operations by eliminating wraparound techniques. Our method for aortic root replacement decreases the potential for coronary
artery false aneurysms by preventing accumulation of blood between the graft and the native, reconstituted diseased aortic wall. The particularly soft and flexible nature of H-WDV is beneficial when the native aorta is heavily calcified and has resulted in irregular vascular margins. Graft compliance facilitates a snug fit at the anastomosis and minimizes bleeding at the anastomotic site. Use of H-WDV has shortened the duration of some thoracic operations and reduced bleeding complications when compared subjectively with previous grafts. Collagen tubes have been used as vascular grafts in the past with limited success.14, 15 Many forms of collagen are thrombogenic, and this tendency has limited the usefulness of previous prostheses. With H-WDV, it has been established that thrombogenicity and other characteristics can be altered by cross-linking collagen with naturally occurring mucopolysaccharide or by reaction with selected chemical agents." These processes form a fully blood-compatible substance that can be used as a bioimplant. The collagen for H-WDV is prepared from calf skin by a sequence of steps including mechanical cleansing, washing, and chemical treatment.!" The processed skin is then homogenized to produce a paste composed primarily of collagen microfibers. This material consisting of 90% pure collagen is used to coat a woven double-
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Westaby et al.
velour Dacron polyester graft. Electron microscopy demonstrates that the collagen layer completely covers the fibers and interstices of the fabric. The prosthesis is biocompatible in terms of pyrogenicity, cytotoxicity, and antigenicity. Scott and associates'" implanted collagen-impregnated and control grafts into the thoracic aorta of dogs. The animals were killed at intervals of I to 180 days, and the grafts were examined for deposition of thrombus, inflammatory reaction, endothelialization, and rate of disappearance of the collagen. There was no significant difference in inflammatory reaction or thrombogenicity. Less than 10% of the bovine collagen remained on the graft after 30 days, and no collagen was identifiable 180 days after implantation. There was no evidence that collagen impaired healing in any way, induced platelet aggregation, or caused intravascular clotting. It was originally thought that high-porosity (knitted) grafts were necessary to allow endothelial cells and their subendothelial matrixes to invade and adhere to the inner surface of a vascular graft. However, although prosthetic grafts may develop neoendothelium in canine and primate models, experience in human beings has shown that reendothelialization occurs only sporadically if at all. 16- 18 Experimental work has demonstrated no difference in patency of woven versus knitted Dacron grafts. Robicsek and associates'? designed an aortic bifurcation graft in which one limb was knitted and the other was woven. These were implanted in 143 consecutive patients with atherosclerotic aortoiliac occlusion or abdominal aortic aneurysm and failed to reveal any difference in patency at periods of 1 month to 2 years. Although our overall hospital mortality for replacement of the ascending aorta was 16%, this is for a group in which emergency procedures were done for 87% of the patients; Other recent reports show an operative mortality of 10% for elective replacement of the ascending aorta and 24% for emergency operations.P We have previously reported the influence of delayed operation on mortality after acute type A dissection, and none of the deaths was directly related to operative hemorrhage" One patient who underwent elective replacement of the ascending aorta together with repair of abdominal aortic aneurysm died. He underwent the dual procedure because it was considered that his extremely poor respiratory function (forced expiratory volume 0.8 L) precluded survival of two separate major procedures.F Since our early experimental work with aprotinin, we have used this agent for operation of acute aortic dissection. 23 Because of the multifactorial nature of postoperative bleeding in this situation, particularly after profound
hypothermia.! we could not demonstrate significant benefit from aprotinin, and, in one patient, severe coagulopathy required massive blood transfusion and treatment with platelets, fresh frozen plasma, and cryoprecipitate. It is likely that profound hypothermia and total circulatory arrest have negative effects on platelet function that are not attenuated but are perhaps worsened by this drug. 24 REFERENCES 1. Carpentier A, Deloche A, Fabiani IN, et al. New surgical approach to aortic dissection: flow reversal and thromboexelusion. J THORAC CARDIOVASC SURG 1981;81:659-68. 2. Seguin JR, Frapier JM, Colson P, Chaptal PA. Fibrin sealant improves surgical results of type A acute aortic dissections. Ann Thorac Surg 1991;52:745-9. 3. Bentall HH, De Bono A. A technique for complete replacement of the ascending aorta. Thorax 1968;23: 338-9. 4. Cabrol C, Pavie A, Mesnildrey P, et al. Long-term results with total replacement of the ascending aorta and reimplantation of the coronary arteries. J THoRAc CARDIOVASC SURG 1986;91:17-25. 5. Harker LA. Bleeding after cardiopulmonary bypass. N Engl J Med 1986;314:1446-8. 6. Bethea MC, Reemtsma K. Graft hemostasis; an alternative to pre-clotting. Ann Thorac Surg 1979;27:374. 7. Cooley DA, Romagnoli A, Milam JD, Bossant ML. A method for preparing woven Dacron grafts to prevent interstitial hemorrhage. Bull Texas Heart Inst 1991;8:48. 8. Ruhland D, Wigges J, Bottcher K, von Bassewitz DB. Fate of collagen following implantation on microvel Hemashield grafts in the dog. Angio Archiv BD 1985;9:22-32. 9. Quinores-Baldrich WJ, Moore WAS, Ziomek S, Chvapil M. Development of a leak-proof knitted Dacron vascular prosthesis. J Vase Surg 1986;6:895-903. 10. Scott SM, Gaddy LR, Sahmel R, Hoffman H. A collagen coated vascular prosthesis. J Cardiovasc Surg 1987;28:498504. 11. Cooley DA, Livesay JJ. Technique of open distal anastomosis for ascending and transverse aortic resection. Cardiovasc Dis 1981;8:421-6. 12. Westaby S. Hypothermic thoracic and thoraco-abdominal aneurysm surgery: a central cannulation technique. Ann Thorac Surg 1992;54:253-8. 13. Butler J, Davies AH, Westaby S. Streptokinase in acute aortic dissection. Br Med J 1990;300:517-9. 14. Humphries AW, Hawk WA, Cuthbertson AM. Arterial prosthesis of collagen-impregnated Dacron tulle. Surgery 1961;50:947-54. 15. Kott I, Pierce EC, Mitty HA, Geller SA, Jacobson JH. The tissue tube as a vascular prosthesis. Arch Surg 1973; 106:206-7. 16. Dillin ML, Scott SM, Vasquez MD, Postlethwait RW,
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Dart CH. Tissue response to an arterial substitute of bovine origin. Arch Surg 1972;105:577-81. 17. Zacharias RK, Kirkman TR, Clowes AW. Mechanisms of healing in synthetic grafts. J Vase Surg 1987;6:429-36. 18. Keshishian JM, Smyth NPD, Adkins PC, Camp F, Yahn WZ. Clinical experience with the modified bovine arterial heterograft. Ann Surg 1970;172:690-700. 19. Robicsek F, Duncan GD, Anderson CE, et a!. Indium Ill-labelled platelet deposition in woven and knitted Dacron bifurcated aortic grafts with the same patient as a clinical model. J Vase Surg 1987;5:833-7. 20. Lytle BW, Mahfood SS, Cosgrove DM, Loop FD. Replacement of the ascending aorta: early and late results. J THORAC CARDIOVASC SURG 1990;99:651-8.
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21. Butler J, Ormerod OJM, Giannopoulos N, Pillai R, Westaby S. Diagnostic delay and outcome in surgery for type A aortic dissections. Q J Med 1991;289:391-6. 22. Westaby S, Parry A, Grebenik C, Pillai R, Lamont P. Combined cardiac and abdominal aortic aneurysm operations: the dual operation on cardiopulmonary bypass. J THORAC CARDIOVASC SURG 1992;104:990-5. 23. van Oeveran W, Jansen NJG, Bidstrup BP, eta!. Effects of aprotinin on hemostatic mechanisms during cardiopulmonary bypass. Ann Thorac Surg 1987;44:640-5. 24. Westaby S. Aprotinin in perspective. Ann Thorac Surg [In press].
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