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Ann Thorac Surg 2001;71:797-800
© 2001 The Society of Thoracic Surgeons


Original article: cardiovascular

High early patency of saphenous vein graft for coronary artery bypass harvested with surrounding tissue

Domingos S.R. Souza, MDa, Vollmer Bomfim, PhDa, Helge Skoglund, MDb, Michael R. Dashwood, PhDc, Jan W. Borowiec, PhDd, Lennart Bodin, PhDe, Derek Filbey, PhDf

a Department of Cardiothoracic Surgery, Örebro Medical Centre Hospital, Örebro, Sweden
b Department of Radiology, Örebro Medical Centre Hospital, Örebro, Sweden
c Department of Molecular Pathology and Clinical Biochemistry and Surgery, The Royal Free and University College Medical School, Royal Free Campus, London, England, United Kingdom
d Department of Thoracic and Cardiothoracic Surgery, University Hospital, Uppsala, Sweden
e Department of Biostatistics, Örebro Medical Centre Hospital, Örebro, Sweden
f Department of Transfusion Medicine, Örebro Medical Centre Hospital, Örebro, Sweden

Accepted for publication October 18, 2000.

Address reprint requests to Dr Souza, Department of Cardiothoracic Surgery, Örebro Medical Centre Hospital, SE 701 85 Örebro, Sweden
e-mail: domingos.souza{at}orebroll.se


    Abstract
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 
Background. Surgical trauma to the saphenous vein, used as a conduit for coronary artery bypass grafting, affects their occlusion rate. This study evaluates the early patency of saphenous vein grafts harvested with a pedicle of surrounding tissue that protects the vein from spasm and trauma.

Methods. Fifty-two patients underwent coronary artery bypass grafting with saphenous veins harvested with surrounding tissue. Forty-five patients, who received a total of 124 vein grafts and 42 left internal mammary arteries, underwent angiographic follow-up at a mean of 18 months (9 to 24 months).

Results. Patency for saphenous vein grafts was 95.4% and for left internal mammary arteries, it was 93.3%. Twenty-nine of 30 (96.7%) vein grafts anastomosed to arteries 2.0 mm or more, 65 of 67 (97%) grafts to 1.5 mm, and 10 of 13 (77%) anastomosed to 1-mm arteries were patent. Nineteen of 22 (86.4%) vein grafts with flow rates 20 mL/min or less, 32 of 34 (94.1%) with flow between 20 and 40 mL/min, and 50 of 51 (98%) with flow more than 40 mL/min were patent. Other registered surgical and clinical factors did not contribute to vessel occlusion.

Conclusions. Early patency rate of saphenous veins harvested with surrounding tissue is very high, even in saphenous vein grafts demonstrating low blood flow. Preservation of graft endothelium using our harvesting technique may be the explanation of this success.


    Introduction
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 
Despite the poor patency rate as compared to the left internal mammary artery (LIMA), the saphenous vein (SV) is still the most commonly used conduit in coronary artery bypass grafting (CABG) [1], and the high occlusion rate of SV grafts limits its success in myocardial revascularization. The occlusion rate of SV graft within 1 year after operation varies between 10% and 20% [2]. The high rate of early thrombotic occlusion of vein graft can be a consequence of technical surgical factors and may also be attributable to damage to the endothelium that occurs during SV harvesting [3]. Therefore, the use of any refined harvesting technique should include protecting the vein wall from trauma before vein graft implantation [4]. When the vein is stripped of its adventitial layer, vascular spasm often occurs, demanding high pressure distention. This procedure causes extensive damage to the vein wall, particularly to the endothelial lining [5]. Because spasm can be prevented by not touching the vein, we have devised a new method of SV preparation where the SV is harvested together with a pedicle of surrounding tissue. This obviates the need for distention, thus preserving the vein endothelium as demonstrated by a morphologic study using scanning electron microscopy [6]. The aim of the present study was to determine the early patency rate of vein grafts harvested with surrounding tissue using previously described technique [7].


    Material and methods
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 
Fifty-two patients underwent elective CABG with SV graft harvested with its surrounding tissue. All patients were operated on by the same surgeon (DSRS) at the Department of Cardiothoracic Surgery, Örebro Medical Center Hospital, Örebro, Sweden. The patients gave their informed consent and the local ethics committee approved the study. As we intend to follow-up these patients for more than 10 years we used the following exclusion criteria: age, more than 70 years; unstable angina; insulin-dependent diabetes mellitus; S-creatinine, more than 120 mmol/L; anticoagulant therapy; ejection fraction, less than 40%; combined procedure; and redo CABG. Forty-five patients underwent the angiographic follow-up 18 months (range, 9 to 24 months) after operation. Seven patients declined to undergo the angiographic examination.

Patient characteristics
There were 7 female and 38 male patients and the mean age was 58 years (range, 43 to 67 years). Nineteen patients were smokers. Twenty-five patients were on lipid-lowering drug therapy. Mean left ventricular function was 67% (range, 40% to 86%). Aspirin was started on the day after the operation with a dose of 160 mg/day. At the time of the angiographic examination 35 patients were receiving a dose of 160 mg, 7 patients had 75 mg, and 3 were not taking antiplatelet drug therapy.

Operative technique
The vein is dissected with a pedicle of surrounding tissue (Fig 1). It is left in situ unligated until extracorporeal circulation is started to allow continuous heparinized blood perfusion. After removal, the vein is stored in blood obtained from the aortic cannula before cooling. To check for leakage from distal anastomosis, the proximal end of the graft is briefly connected to the arterial cannula. Accordingly, the graft is neither flushed nor dilated manually.



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Fig 1. The saphenous vein harvested with a pedicle of surrounding tissue.

 
Cardiopulmonary bypass, moderate hypothermia (28°C to 30°C) and cold blood intermittent retrograde cardioplegia (4°C) was routinely used. Malleable calibrated probes with 0.5-mm increments were used to measure the diameter of target coronary arteries. The anastomoses of the vein grafts to the coronary arteries were performed with double-armed 7-0 Prolene continuous sutures. All LIMAs were anastomosed to the left anterior descending coronary artery in a continuous fashion using 8-0 Prolene. The proximal anastomoses were performed with a continuous 6-0 polypropylene suture. A total of 124 vein grafts and 42 LIMA were inserted giving an average of 3.7 grafts per patient. In all, 109 were single grafts and 15 were sequential grafts. The LIMA grafts were considered not suitable for implantation in 3 patients. There was no thromboendarterectomy.

The size and quality of recipient coronary arteries, the quality, length, and origin (distal, medial, proximal part) of SV grafts were recorded. The graft blood flow rate was also routinely measured by ultrasonic transit time method (Research flowmeters, Transonic Systems Inc, Ithaca, NY). The measurements were made after weaning from the extracorporeal circulation and when stable hemodynamic conditions were achieved.

Angiography
All angiograms were made according to the transfemoral technique described by Judkins [8]. The angiographic assessment was performed by one radiologist and the angiographic findings were assessed with regard to graft patency and degree of localized or diffuse changes. Occlusion was identified by visualization of a remaining stump by selective injection or by lack of opacification after a 50-mL bolus injection of dye in the ascending aorta.

Statistical analysis
The difference in frequency of occluded and nonoccluded grafts was analyzed with {chi}2 tests in case of univariate analysis and logistic regression models when two or more explanatory variables were considered. The actual calculations were performed with the statistical programs StatXact and LogXact (Cytel Software Corporation, Cambridge, MA).


    Results
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 
There were no perioperative myocardial infarctions or deaths. In the patient population undergoing the study, 41 patients were in New York Health Association functional class I and 4 in class II. The total patency rate was 118 of 124 (95.4%) for vein grafts and 39 of 42 (93.3%) for LIMA. The following surgical factors possibly responsible for graft occlusion were analyzed.

Site of insertion
Occlusion occurred in 0 of 37 (0%) grafts anastomosed to the right coronary artery, in 3 of 39 (7.7%) to the circumflex coronary artery, and in 3 of 33 (9.1%) to the diagonal branches. The only single saphenous vein graft that was inserted to the left anterior descending coronary artery was open. Most of the proximal parts of the veins, 24 of 32 (75%), were anastomosed to the right coronary artery, 27 of 42 (64.3%) medial parts were inserted to the diagonal branches, and 31 of 35 (88.6%) of the distal parts to the circumflex branches.

Three of 15 sequential grafts were anastomosed to diagonal branches, two between the circumflex and diagonal branches, one between the left anterior descending coronary artery and the diagonal branch, 8 between the circumflex branches, and 1 between the posterior descending artery and the posterial lateral artery (PLA). All sequential grafts had one single aortic anastomosis for 2 recipients coronary arteries and all were patent.

Size of artery bypass grafted
Occlusion occurred in 1 of 29 (3.4%) grafts sutured to arteries of 2 mm or larger, in 2 of 67 (3.0%) grafts anastomosed to 1.5 mm arteries, and in 3 of 13 (23.1%) grafts anastomosed to arteries with diameter of 1 mm. The occlusion rate with the size of the target artery was statistically significant (p = 0.03).

Quality of the recipient arteries
No direct influence of local quality of the recipient coronary arteries on graft occlusion could be identified (p = 0.62). A prerequisite was that the grafted vessel at the anastomotic site was permeable and technically feasible.

Intraoperative graft flow
We found occlusion in 3 of 22 (13.6%) single grafts that had flow rates of less than 20 mL/min, in 2 of 34 (5.9%) with a flow rate between 20 and 40 mL/min, and in 1 of 53 (1.9%) with a flow rate more than 40 mL/min. The flow rate of the sequential grafts ranged from 15 to 180 mL/min with a mean value of 85 mL/min. No statistical significance was reached regarding flow rate (p = 0.12).

When we compared the flow rate to the size of the coronary arteries we found a trend toward graft occlusion (24%) for those grafts anastomosed to small coronary arteries (1 mm) with a flow rate of 20 mL/min or less. However, all grafts that were anastomosed to 1-mm arteries and had a flow rate of more than 20 mL/min or those that had a flow rate of 20 mL/min or less but were anastomosed to arteries of 1.5 mm or more were patent (Table 1).


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Table 1. Number of Patent Single Grafts Stratified According to Flow Rate and Size of Target Coronary Arteries

 
Length of graft
No influence of the length of the grafts on occlusion was found even when associated with other important factors such as vein quality, graft flow rate, recipient coronary artery diameter or quality.

The angiographic examinations revealed that the grafts were either completely occluded or completely open. There was neither localized nor diffuse significant narrowing. However, six grafts showed mild diffuse irregularities. No stenosis was seen at the site of anastomosis. There were six occluded grafts, of which three were anastomosed to small coronary arteries and had low flow rates and one of these three vein grafts was of poor quality. Two other occluded grafts had high flow rates; however, the veins were of poor quality. One occluded graft was of good quality and had a high flow rate. Accordingly, the quality of SV before harvesting is an important factor for the outcome of the venous graft (p = 0.02). No kinking of the grafts occurred, not even when the graft was excessively long.

No association between vein occlusion and clinical factors such as age, New York Heart Association functional class, number of preoperative infarctions, cholesterol level, smoking habits, hypertension, or the use of antiplatelet drug therapy was observed.


    Comment
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 
It has been reported that when using the SV graft harvested by the conventional technique approximately 10% of venous grafts occlude during the first month and about another 10% within the first year [9]. Handling the vein with surgical instruments, stripping of the adventitial layer, and distention to overcome spasm are common with the conventional technique and are traumatic to the vein wall [10]. Many strategies, such as pharmacologic interventions [11], gene transfer before grafting [12], and external stenting of the vein graft [13] have been used to prevent early graft occlusion and the changes in vein grafts. In addition, the high early patency rate that was found with this new no-touch technique showed that a refined SV harvesting technique is another strategy to improve the early patency rate.

Because endothelial injury is inevitable when the SV is handled by the conventional technique, the use of antithrombotic therapy should also be started peroperatively with a dose of 325 mg/day of aspirin [14]. In the present study we started using aspirin the day after the operation at a low dose of 160 mg/day. Some patients were on a dose of only 75 mg/day and a few patients were not using aspirin at the time of the angiographic assessment. On the basis of our results, pharmacologic inhibition of platelet function has not been found to be of major importance in preventing vein graft occlusion if the SV endothelium remains intact.

It is recognized that vein grafts that have a very low flow rate occlude quickly as a result of thrombus formation triggered by endothelial damage [15]. In agreement with one other study [16], a strong influence in the graft attrition was observed for grafts with low flow rates anastomosed to small-sized coronary arteries. However, our findings showed that most vein grafts with low flow rates were patent.

The quality of the vein before its harvesting was another important factor in determining the fate of the graft. However, surgical factors such as the quality of the recipient coronary arteries, the length and the distribution of the grafts to the coronary arteries, as well as the classic clinical factors such as hyperlipidemia, hypertension, or smoking habits did not play an important role in affecting the patency rate.

It is a well-known fact that kinking will occur if the graft is too long. Many techniques have been applied to deal with this issue [17]. Nevertheless, when the vein is supported by the surrounding tissue no kinking will occur. This may be an additional contributory factor explaining the high patency rate in this study.

Damage to the saphenous nerve is inevitable, but there was no patient who experienced any severe neurological disturbances. In a retrospective blind study we found that the sensory reduction around the wound was the most common neurological finding. Similarly in another study, most patients who had their veins harvested by the conventional technique presented neurological symptoms at the site of the leg corresponding to the saphenous nerve innervation [18].

It should be mentioned that this new no-touch technique is not suitable for patients with SVs lying too superficially.

In conclusion, we found that a careful SV harvesting technique, preserving a pedicle of surrounding tissue, was associated with the high early patency rate of SV graft in CABG. The maintenance of a structural and feasibly functional integrity of vein endothelium is crucial for the patency of the grafts, particularly for those with low flow rates.


    Acknowledgments
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 
We thank Eva Holst-Norgren, Ulla-Britt Lindqvist, Margaretha Sandin, and Jane Strand for valuable technical assistance, the theater and ward nurses for their expert help, and Örebro Medical Center Hospital for financial support in carrying out this study.


    References
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 

  1. Izzat M., West R., Bryan A. Coronary artery bypass surgery: current practice in the United Kingdom. Br Heart J 1994;71:382-385.[Abstract/Free Full Text]
  2. Manninen H.I., Jaakola P., Sukonen M., Rehnberg S., Vuounniemi R., Matsi P.J. Angiographic predictors of graft patency, and disease progression after coronary artery bypass grafting with arterial, and venous grafts. Ann Thorac Surg 1998;66:1289-1294.[Abstract/Free Full Text]
  3. Malone J.M., Kischer C.W., Moore W.S. Changes in venous endothelium fibrinolytic activity and histology with in vitro venous distention and arterial implantation. Am J Surg 1981;142:178-186.[Medline]
  4. Adcock O.T., Adcock G.L.D., Wheeler J.R., Gregory R.T., Snyder S.O., Gayle R.G. Optimal techniques for harvesting and preparation of reversed autogenous vein grafts for use as arterial substitutes: a review. Surgery 1984;96:886-894.[Medline]
  5. Angelini G.D., Passani S.L., Breckenridge I.M., Newby A.C. Nature and pressure dependence of damage induced by distention of saphenous vein coronary artery bypass grafts. Cardiovasc Res 1987;21:902-907.[Medline]
  6. Souza D.S.R., Christofersson R.H.B., Bomfim V., Filbey D. "No-touch" technique by using saphenous vein harvested with its surrounding tissue for coronary artery bypass grafting maintains an intact endothelium. Scand J Thorac Cardiovasc Surg 1999;33:323-329.
  7. Souza D. A new no-touch preparation technique. Scand J Thorac Cardiovasc Surg 1996;30:41-44.[Medline]
  8. Judkins M.P. Selective coronary arteriography. : Part I: A percutaneous transfemoral technique. Radiology 1967;89:815-824.[Medline]
  9. FitzGibbon G.M., Leach A.J., Keon W.J., Burton J.R., Kafka H.P. Coronary bypass graft fate: angiographic study of 1,179 vein grafts early, one year, and five years after operation. J Thorac Cardiovasc Surg 1986;91:773-778.[Abstract]
  10. Qvist W.C., Handenschield C.C., Logerfo F.W. Qualitative microscopy of implanted vein grafts. J Thorac Cardiovasc Surg 1992;103:671-677.[Abstract]
  11. Rosenfeldt F.L., He G.-W., Buxton B.F., Angus J.A. Pharmocology of coronary artery bypass grafts. Ann Thorac Surg 1999;67:878-888.[Abstract/Free Full Text]
  12. Imagawa H., Taniguchi K., Takahashi T. Gene transfer with hemagglutinating virus of Japan liposome into human saphenous vein graft; preventive way against vein graft disease. Circulation 1996;94:477.[Abstract/Free Full Text]
  13. Mehta D., George S.J., Jeremy J.Y., et al. External stenting reduces long-term medial and neointimal thickening and platelet derived growth factor expression in a pig model of arteriovenous bypass grafting. Nature Med 1998;4:235-239.[Medline]
  14. Goldman S., Copeland J., Moritz T., et al. Saphenous vein graft patency 1 year after coronary artery bypass surgery and effects of antiplatelet therapy: results of a veterans administration cooperative study. Circulation 1989;80:1190-1197.[Abstract/Free Full Text]
  15. Lusher T.F. Vascular biology of coronary bypass grafts. Curr Sci 1991;6:868-876.
  16. Cataldo G., Braga M., Pirotta N., Lavezzari M., Rovelli F., Marubini E. Factors influencing 1-year patency of coronary artery saphenous vein grafts. Circulation 1993;88:93-98.
  17. Durrani A., Sim E.K.W., Grignani R.T. Accurate length adjustment of aortocoronary saphenous vein bypass grafts. Ann Thorac Surg 1998;66:966-967.[Abstract/Free Full Text]
  18. Mountney J., Wilkinson G.A.L. Saphenous neuralgia after coronary artery bypass grafting. Eur J Cardiothorac Surg 1999;16:440-443.[Abstract/Free Full Text]



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