The Healing Characteristics of Autogenous Saphenous Vein Used in the Reconstruction of Previouslv Implanted Arterial Saphenous Vein Grafts

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1 The Healing Characteristics of Autogenous Saphenous Vein Used in the Reconstruction of Previouslv Implanted Arterial Saphenous Vein Grafts Karl J. Karlson, M.D., M.M.S., Robert Brescia, M.D., and Hassan Najafi, M.D. ABSTRACT Aortocoronary saphenous vein grafts with early isolated stenoses pose the technical problem of how to deal with these grafts at reoperation. The advisability of using a portion of old graft when reconstructing these grafts was examined. An experimental model was devised in which the anatomical and pathological interfaces between fresh vein and previously inserted vein were studied. Superficial femoral artery from the thigh of 15 dogs was replaced by reversed autogenous saphenous vein. Four months later, the animals were divided into two groups. Group 1 consisted of 8 animals that underwent transection and reimplantation of the middle 4 cm of the vein graft in exactly the same position in which it had been. In Group 2, the 7 animals had the middle 4 cm of the graft replaced with newly harvested reversed saphenous vein. Six months after initial vein graft implantation, the animals were studied. No critical stenoses were seen in the grafts. Pathological study of Group 1 grafts revealed fibrous graft disease of uniform seventy throughout the graft, thereby demonstrating that new anastomoses in an old graft do not affect graft disease. Group 2 grafts revealed that the seventy of disease in the new interposed segment of the vein graft was less than in the old retained portions of the graft. No untoward reaction causing acceleration of graft disease occurred between old and new vein. Operations using undiseased portions of old vein grafts should be considered a viable option in repeat coronary revascularization for early stenoses. Saphenous vein graft stenosis is not uncommon in patients seen with recurrent symptoms after coronary artery revascularization. Isolated narrowing in otherwise adequate coronary artery bypass grafts (with or without other disease) poses the technical problem of how to deal with this obstruction at the time of reoperation. The choices of how to handle these grafts are (1) to abandon completely the old graft that is anatomically satisfactory From the Department of Cardiovascular-Thoracic Surgery, Rush- Presbyterian-St. Luke s Medical Center, 1753 W Congress Pkwy, Chicago, IL. Accepted for publication Oct 27, Address reprint requests to Dr. Najafi, Department of Cardiovascular- Thoracic Surgery, Rush-Presbyterian-St. Luke s Medical Center, 1753 W Congress Pkwy, Chicago, IL except for a segmental stricture, and replace it or (2) to reconstruct the old graft by resection of the narrowed portion with interposition of a new segment of saphenous vein, or bypass of the stenotic area. The fundamental concern behind this decision centers on whether or not interposing a new segment of vein in an old graft causes accelerated graft stenosis either by a localized reaction at the anastomotic sites between the new and old veins, or simply by the presence of a new anastomosis in an old graft with the ensuing turbulence that must accompany it. If either of these hypotheses proved true, it obviously would be prudent to insert a parallel graft in place of the old one. Alternatively, if no acceleration of graft stenosis occurred in the old graft with an interposed segment of fresh vein, then more expeditious and technically simpler reoperations could be performed in these patients because only the narrowed portion of the stenotic graft would need to be replaced or bypassed. To assess the merit of performing a procedure that would include the old vein in the technical revision of stenotic saphenous vein grafts, an experimental model was devised in which the anatomical and pathological interfaces between fresh vein and previously inserted vein were studied. Material and Methods Fifteen mongrel dogs weighing 25 to 30 kg were used in the experimental protocol. Under general endotracheal anesthesia with sodium pentobarbital, a 9-cm length of superficial femoral artery was removed from the thigh of each animal. A 9-cm length of reversed autogenous saphenous vein harvested from the same leg was then interposed in place of the excised arterial segment using end-to-end anastomoses with running 6-0 polypropylene suture. The procedures were performed under regional heparinization by injecting 1,000 units of heparin sodium into the proximal and distal ends of each femoral artery while it was clamped during the procedure. The saphenous veins were handled gently and treated in the same careful manner as is customary during coronary artery bypass operations. The veins were flushed with a heparinized saline solution containing Xylocaine (lidocaine hydrochloride) using a low-pressure system. Care was taken to avoid excessive manipulation and distention of the veins during the harvesting procedure. All 15 animals were allowed to recover fully. Excellent distal pulses were palpable in all animals. After 30 days, angiography was performed to visualize the anastomoses and verify the patency of the vein grafts (Fig 1). All 648 Ann Thorac Surg , June 1987

2 649 Karlson, Brescia, Najafi: Autogenous Saphenous Vein in Vein Graft Reconstruction A 0 C D Fig 3. Sections of vein grafts (A-D) where histological study was performed. Fig I. Angiogram of interposed vein graft (arrows) GROUP 1 Fig 2. Operation performed on Group 1 and on Group 2 fifteen grafts were patent and showed no evidence of graft stenosis. The animals were then observed so that a subsequent study on the fate of the grafts could be conducted. The dogs were divided randomly into two groups. Group 1 consisted of 8 animals that underwent operative isolation of the saphenous vein graft about 4 months after the initial implantation. After regional heparinization, the middle 4 cm of each vein graft was transected, removed, flushed, and then reimplanted in exactly the same position in which it had been (Fig 2). Anastomoses were performed using running 6-0 polypropylene suture. The wounds were closed, and the dogs were allowed to recuperate. Group 2 consisted of 7 animals that likewise underwent operative isolation of the saphenous vein graft an average of 4 months after the initial implantation. After regional heparinization, the middle 4 cm of each of these grafts also was excised. In this group, however, the removed segment of vein graft was discarded and replaced with a newly harvested reversed autogenous sa- phenous vein taken from the contralateral leg of the animal (see Fig 2). These new segments of vein were handled in the same careful manner as the original vein grafts. There were no deaths in either group. Both groups of animals underwent angiography once again and then were killed an average of 2 months (Group 1, 69 days and Group 2, 48 days) after the reoperation. The angiograms were analyzed for evidence of new graft stenosis. Tissue sections of the vein grafts in both groups were taken from four discrete areas. The selection of sites for pathological study took into consideration the proximity of the suture lines between artery and vein as well as old and new vein. The middle portion of the old vein distant from all anastomotic sites was examined as a control. Sections were obtained from the following four discrete areas: position A, adjacent to the proximal arteriovenous anastomosis; B, from the old vein graft distant from all suture lines; C, from the old vein graft adjacent to the venovenous anastomosis; and D, from the new vein graft adjacent to the venovenous anastomosis (Fig 3). By selecting these sites, all possible representative areas of tissue were sampled. The tissue sections were fixed in 10% buffered formalin, and histological evaluation was performed. Results Angiograms made just before the animals were killed and histological sections of the vein grafts were reviewed in all animals. The results are summarized in Tables 1 and 2. Angiograms were reviewed for patency of the final grafts as well as for evidence of critical stenoses. Graft thrombosis developed in 1 animal in each group. Autopsies revealed that the thrombosis was due to technical errors. Angiograms from all other animals revealed patent grafts without any major areas of discrete stenosis. The results of histological sections taken from the four specific sections of the grafts (see Fig 3) revealed changes that seemed to vary in severity directly with the age of the graft. The following changes occurred in the grafts: (1) disruption of the endothelium; (2) intimal proliferation and thickening with deposition of fibrin and collagen; (3) medial thickening with some loss of smooth muscle cells and an increase in collagen; and (4) mild adventitial fibrosis with some loss of elastic fibers and thickening of the vasa vasorum (Fig 4). These changes were seen to some extent in all grafts and were graded mild, moderate, and severe.

3 650 The Annals of Thoracic Surgery Vol 43 No 6 June 1987 Table I. Findings on Histological Sections and Results of Angiography in Group 1 Severity of Histological Reaction in Graft Sections Dog No. A B C D Angiogram 1 Mild Severe Severe Severe Patent, no stenosis 2 Mild Moderate Moderate Moderate Patent, no stenosis 3 Mild Severe Severe Moderate Patent, no stenosis 4 Mild Moderate Moderate Moderate Patent, no stenosis 5 Mild Mild Mild Mild Patent, no stenosis 6 Moderate Moderate Moderate Moderate Patent, no stenosis 7 Moderate Severe Severe Moderate Patent, no stenosis 8 Moderate Moderate Moderate Moderate Graft thrombosed Table 2. Findings on Histological Sections and Results of Angiography in Group 2 Severity of Histological Reaction in Graft Sections Dog No. A B C D Angiogram 1 Mild Moderate Moderate Mild Graft thrombosed 2 Moderate Moderate Moderate Moderate Patent, no stenosis 3 Mild Moderate Moderate Mild Patent, no stenosis 4 Mild Moderate Moderate Mild Patent, no stenosis 5 Moderate Severe Severe Mild Patent, no stenosis 6 Moderate Mild Moderate Mild Patent, no stenosis 7 Mild Moderate Moderate Mild Patent, no stenosis Fig 4. Microscopic section of vein graft demonstrating disruption of endothelium, intimal proliferation with fibrin and collagen deposition, and medial thickening. The animals in Group 1 demonstrated that the severity of disease in the reimplanted segments of old vein graft roughly paralleled the disease in other portions of the graft. Sections taken adjacent to the venovenous anastomoses showed no more or no less tissue reaction than those taken from other sections of the vein graft. This indicated that the presence of suture lines did not affect the severity of graft disease. The animals in Group 2 showed that the severity of disease in the new interposed segments of vein graft was much less than in the older retained portions of the graft (position D). The severity of the degenerative process in both groups varied directly only with the age of the segment of graft examined. There was no evidence of worsening of graft disease simply as a result of the presence of a new anastomosis (Group 1 animals) or of acceleration of graft degeneration by the interposition of a newly harvested segment of saphenous vein (Group 2 animals). There was some individual variation in the aggressiveness of graft disease among animals, but the data support the observation that the older the graft in a given animal, the greater the degree of reaction. Altering existing grafts by the addition of either suture lines or new segments of vein did not affect graft disease. Comment With the advent of reoperation for coronary artery disease, there has unfolded a divergence of opinions on how to handle patients with stenotic bypass grafts. It has been reported that 10 to 12% of coronary artery bypass grafts either occlude or develop areas of substantial narrowing during the first year after operation, and that those rates go even higher later [l-31. These early lesions are those that can be addressed using our data.

4 651 Karlson, Brescia, Najafi: Autogenous Saphenous Vein in Vein Graft Reconstruction There may be a difference in the pathology of graft disease between the early- and late-appearing lesions, with intimal hyperplasia and fibrosis being seen early and graft atherosclerosis appearing later [l, 2, 4, 51. Reoperations are performed frequently today for graft failure, progression of underlying disease, and previously incomplete revascularization and mortality is 2 to 4% ( The techniques used during these opsrations, however, vary widely from institution to institution when patent grafts with segmental areas of sterissis are encountered. Suggestions as to how to deal with the patent but stenotic grafts have ranged from insertion of entirely new conduits from the aorta to the native coronary arteries, to reconstruction using the patent sections of the old grafts for either the proximal or distal portions of a new conduit [12, 131. The surgeon s goal should be to use the simplest and safest procedure that will provide the best possible results. Because working on vein grafts is simpler than reconstructing entirely new grafts, we wanted to be sure that venovenous anastomoses would be an effective alternative to consider. This represents an easier operation, and occasionally it can be accomplished without cardiopulmonary bypass in a small percentage of patients. Also, in certain circumstances, operation could be performed through a left thoracotomy, thereby avoiding a redo sternotomy (141. This experiment has shown that a segment of newly harvested vein can be interposed in an old graft without untoward sequelae. We saw no evidence of a reactive process between the new and old segments of vein graft during the time frame that we examined, and the presence of some degenerative changes in the old portions of a graft did not cause acceleration of disease in the new portion of the graft (Group 2 animals). The disease seen in the grafts of our animals consisted for the most part of subintimal fibrosis and medial thickening with fibrin and collagen deposition. These changes have been reported by others [l, 5, 15, 161. Frank intimal necrosis, aneurysm formation, and the appearance of atheromas have also been reported in saphenous vein grafts [17, 18, 191. We did not find these manifestations of graft disease in our animals. It is likely that we would have seen atheromatous disease in our grafts had the animals been hypertensive or on high-lipid diets and followed for a longer period [20]. Also, the fibrosis that was seen in our grafts may merely represent the first stage in atheroma formation [21]. Because neither the presence of new anastomoses nor old vein-new vein interfaces cause accelerated graft disease, it becomes possible not only to repair grafts with interposed segments of new vein, but also to use existing grafts as takeoff points for new grafts. We emphasize that to consider these alternatives, the disease in the old vein grafts should consist of either intimal hyperplasia or fibrosis as is seen in patients with lesions early after coronary artery bypass. We do not believe that the length of this study provides adequate data to support the use of this technique in late graft stenoses that most likely represent atherosclerotic disease, although this may ultimately prove to be a useful addition to the surgeon s armamentarium in atherosclerotic disease as well. In using this technique, additional proximal anastomoses on diseased aortas or even additional distal anastomoses to native coronary arteries could be avoided in some instances. Manipulation of the old grafts must be avoided to prevent embolization of debris from the diseased segment. If any evidence of diffuse disease is seen in the old grafts, then an entirely new conduit should be inserted. The results of this study have allayed our previously held concerns about using portions of previously implanted saphenous vein grafts in early reoperations for coronary artery disease. The experimental study sbows that no untoward reaction occurs between segments of new and old vein when they are joined together to form a new conduit. The portion of old graft will continue to function satisfactorily. Based on these observations, in our clinical practice we have used old vein in the reconstruction of the coronary vasculature in select patients who were seen with early segmental stenoses of coronary grafts. We believe that operations using old vein should be considered as good alternatives in instances where they represent technically simpler and safer operations than the construction of new grafts from a diseased aorta to unenticing native coronary arteries. References 1. Grondin CM, Lesperance J, Bourassa MG, et al: Serial angiographic evaluation in 60 consecutive patients with aortocoronary artery vein grafts 2 weeks, 1 year and 3 years after operation. J Thorac Cardiovasc Surg 671, Campeau L, Enjalbert M, Lesperance J, et al: Atherosclerosis and later closure of aortocoronary saphenous vein grafts. Circulation 68:Suppl 2:1, Grondin CM, Campeau L, Lesperance J, et al: Atherosclerotic changes in coronary vein grafts six years after operation. J Thorac Cardiovasc Surg 77:24, Brody WR, Kosek JC, Angel1 WW: Changes in vein grafts following aortocoronary bypass induced by pressure and ischemia. J Thorac Cardiovasc Surg , Vlodaner Z, Edwards JE: Pathologic changes in aortocoronary arterial saphenous vein grafts. Circulation 44:719, Allen RH, Stinson EB, Oyer PE, Shumway NE: Predictive variables in reoperation for coronary artery disease. J Thorac Cardiovasc Surg 75:186, Pucci JJ, Walesby RK, Smith EEJ, et al: Reoperation for failed aortocoronary bypass grafts. J Cardiovasc Surg (Torino) 23:453, Loop FD, Lytle RW, Gill CC, et al: Trends in selection and results of coronary artery reoperations. Ann Thorac Surg 36:380, Loop FD, Cosgrove DM, Kramer JR, et al: Late clinical arteriographic results in 500 coronary artery reoperations. J Thorac Cardiovasc Surg 81:675, Schaff HV, Orszular TA, Gersh BJ, et al: The morbidity and mortality of reoperation for coronary artery disease and analysis of late results with use of actuarial estimate of event-free interval. J Thorac Cardiovasc Surg 85:508, Laird-Meeter K, VanDenBrand MJEM, Seruys PW, et al: Reoperation after aortocoronary bypass procedure. Br Heart J 50:157, 1983

5 652 The Annals of Thoracic Surgery Vol 43 No 6 June Grondin C, Pomar JL, Herbert Y, et al: Reoperation in patients with patent atherosclerotic coronary vein grafts. J Thorac Cardiovasc Surg 87379, Akins CW: Reoperation for stenotic saphenous vein bypass,. grafts without cardiopulmonary bypass. Ann Thorac Surg 35:201, Far0 RS, Javid H, Najafi H, Serry C: Left thoracotomy for reoperation for coronary revascularization. J Thorac Cardiovasc Surg 84:453, Lawrie GM, Lie JT, Morns GC, Beagley HL: Vein graft patency and intimal proliferation after aortocoronary bypass: early and long-term angiopathologic correlations. Am J Cardiol 38:856, Jones M, Conble DM, Ferrans VJ, et al: Lesions observed in arterial autogenous vein grafts. Circulation 67:Suppl 3:198, Lie JT, Lawrie GM, Morns GC: Aortocoronary bypass saphenous vein graft atherosclerosis. Am J Cardiol 40:906, Stein AA, Rosenblum I, Leather R: Intimal sclerosis in human veins. Arch Pathol81:548, Szilagyi DE, Elliott JP, Hageman JH, et al: Biologic fate of autogenous vein implants as arterial substitutes. Ann Surg 178:232, Scott HW, Morgan CV, Bolasny B, et al: Experimental atherosclerosis in autogenous venous grafts. Arch Surg 101:677, Geiringer E: Venous atheroma. Arch Pathol48:410, 1949 Notice from the Southern Thoracic Surgical Association The thirty-fourth Annual Meeting of the Southern Thoracic Surgical Association will be held at the Boca Raton Hotel and Club, Boca Raton, FL, November 5-7, There will be a $125 registration fee for nonmember physicians except for guest speakers, authors and coauthors on the program, and residents. There will be a $50 registration fee for attendees of the Postgraduate Course on Saturday, November 7, The Postgraduate Course of the Southern Thoracic Surgical Association has been expanded to a full day and will provide in-depth coverage of thoracic surgical topics selected primarily as a means to enhance and broaden the knowledge of practicing thoracic and cardiac surgeons. Applications for membership should be completed by July 1, 1987, and forwarded to the Southern Thoracic Surgical Association, 111 East Wacker Dr, Chicago, IL The Southern Thoracic Surgical Association is accredited by the Accreditation Council for Continuing Medical Education to sponsor continuing medical education for physicians. Gordon F. Murray, M.D. Secretary-Treasurer Southern Thoracic Surgical Association Basic Science Center West Virginia University Morgantown, WV 26506