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Ann Thorac Surg 2005;80:118-123
© 2005 The Society of Thoracic Surgeons

Original article: Cardiovascular

Skeletonized Gastroepiploic Artery as a Composite Graft for Total Arterial Revascularization

Sang-Wan Ryu, MDa, Byoung-Hee Ahn, MD, PhDa,*, Suk-Jung Choo, MD, PhDc, Kook-Ju Na, MD, PhDa, Young-Keun Ahn, MD, PhDb, Myung-Ho Jeong, MD, PhDb, Sang-Hyung Kim, MD, PhDa

a Department of Thoracic and Cardiovascular Surgery, Chonnam National University Hospital, Gwang-ju, Seoul, South Korea
b Department of Cardiology, Chonnam National University Hospital, Gwang-ju, Seoul, South Korea
c Department of Thoracic and Cardiovascular Surgery, Asan Medical Center, Seoul, South Korea

Accepted for publication February 1, 2005.

* Address reprint requests to Dr Ahn, Chonnam National University Hospital, 8 Hak-dong, Dong-gu, Gwang-ju, 501-757 Korea (Email: bhahn{at}chonnam.ac.kr).

Presented at the Poster Session of the Fortieth Annual Meeting of The Society of Thoracic Surgeons, San Antonio, TX, Jan 26–28, 2004.


   Abstract
Top
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 Online Discussion Forum
 Acknowledgments
 References
 
BACKGROUND: Despite the purported advantages of using a gastroepiploic artery graft during coronary artery bypass, insufficient potential flow capacity and vasospasm remain major concerns. We assessed the efficacy and results of using a skeletonized composite gastroepiploic artery graft in situations in which bilateral internal thoracic and radial arteries could not be used.

METHODS: Between January 2000 and August 2002, 37 patients (25 men, 12 women; mean age, 59.9 years) underwent grafting with composite grafts using a skeletonized left internal thoracic artery plus the gastroepiploic artery. Coronary angiograms were performed in the immediate (median, 14 days, 36 patients) and early (median, 348 days, 32 patients) postoperative periods. Off-pump coronary artery bypass grafting was performed in all but 2 patients.

RESULTS: There were no deaths. The respective postoperative patencies of the left internal thoracic artery and gastroepiploic artery were 36 of 37 (97.2%) and 73 of 75 (97.3%) at the immediate period, and 34 of 34 and 62 of 67 (92.5%) at the early period. During follow-up, only 1 patient required percutaneous intracoronary intervention for gastroepiploic artery occlusion.

CONCLUSIONS: Skeletonized composite gastroepiploic artery grafts showed satisfactory clinical and angiographic results in situations in which bilateral internal thoracic and radial arteries could not be used. Although it needs longer follow-up, these early results demonstrated that the gastroepiploic artery may be a useful option in some situations of total arterial revascularization, used either as an in situ or as a composite graft.


   Introduction
Top
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 Online Discussion Forum
 Acknowledgments
 References
 
Total coronary arterial revascularization has been frequently achieved with either bilateral internal thoracic arteries (BITAs) or radial artery (RA) composite grafts with left internal thoracic artery (LITA) inflow [1–5]. However the availability of BITAs or the RA may be limited by graft or patient factors. In such cases, other sources of arterial conduits may be required for total arterial revascularization.

The gastroepiploic artery (GEA) is an arterial conduit that is mostly used as an in situ graft for the right coronary system. Some authors have reported satisfactory results [6–9], whereas others have found their experience more disappointing [10, 11]. As the GEA has greater histologic similarity to the ITA than the RA, it is expected to show greater resistance to atherosclerosis and better long-term patency [12]. However, many surgeons remain hesitant about using the GEA because of concerns over potential insufficient flow capacity and vasospasm. We believe that the less frequent use and thus lack of familiarity with this conduit, in either its in situ or its pedicled form, is largely responsible for the general sense of discomfort associated with its use. It is our contention that this artery has a favorable histological composition; thus, by utilizing the skeletonized GEA as a composite graft with LITA inflow, it should be possible to optimize its use in coronary artery repair.

We have used the skeletonized composite LITA-GEA grafts for total arterial revascularization when BITA harvesting was expected to increase perioperative morbidity or when the RA was considered unsuitable for use. We herein report our early clinical and angiographic results to evaluate the usefulness of this approach.


   Material and Methods
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 Abstract
 Introduction
 Material and Methods
Results
 Comment
 Online Discussion Forum
 Acknowledgments
 References
 
Between January 2000 and August 2002, 229 patients received coronary artery bypass grafting (CABG) at Chonnam National University Hospital. Of these, 37 patients (16%) received CABG with LITA-GEA composite grafts, of which 25 were men (68%) ranging in age from 43 to 73 years (mean, 59.9 years). Preoperative clinical, echocardiographic, and angiographic characteristics are listed in Table 1.


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  		Table 1. Preoperative Characteristicsa
 
Although BITAs or RAs were most frequently used for total arterial revascularization, the availability of these sources was either limited or contraindicated in some patients. The use of BITAs was commonly avoided in the elderly (≥ 70 years old), obese (body mass index, ≥ 25), or uncontrolled insulin-dependent diabetic patients, because of concerns relating to possible postoperative wound complications [13]. The use of the RA was also avoided in patients presenting with a positive Allen test, arteriosclerosis in the RA, renal dysfunction, trauma to the upper limbs, presence of Raynaud’s disease, or recent transradial coronary angiography [14, 15]. Therefore a skeletonized GEA graft with LITA inflow was used to overcome the limited availability of arterial conduits. This study received approval from the Ethics Research Committee and informed consent was obtained from all patients.

Only one surgeon (BHA) operated on all the patients in these series. The GEA was harvested through a 2- to 4-cm caudal extension of the standard median sternotomy incision. After the GEA had been evaluated by finger palpation, the anterior layer of the great omentum was separated by electrocautery, and later in this series by using the Harmonic scalpel (Ethicon Endo-Surgery, Cincinnati, OH). The spaces between the GEA and its satellite veins were then dissected, and the arterial branches were divided with either hemoclips or the Harmonic scapel (Ethicon Endo-Surgery). During and after harvesting, warm diluted papaverine saline solution (1 mg/mL) was sprayed externally. Intraluminal injection was not performed. The harvested graft was wrapped with gauze soaked in warm diluted papaverine saline solution until use (Fig 1).



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  		Fig 1. A skeletonized gastroepiploic artery. After the artery is evaluated by finger palpation, the anterior layer of the great omentum, its satellite veins, and its gastric and omental branches are divided with electrocautery and hemoclips (later using the ultrasonic scapel). The harvested graft is wrapped with gauze soaked in warm diluted papaverine saline solution until use.

 
The LITA was also harvested in skeletonized fashion with electrocautery and hemoclips (cold dissection). The distal end of the LITA and the proximal and distal ends of the GEA were cut after systemic heparinization (100 U/kg). The activated clotting time was maintained at greater than 300 seconds during heparinization.

All CABGs were initially performed off pump, but conversion to on-pump beating CABG was necessary in 2 patients because of hemodynamic instability. Off-pump CABG was performed using a suction-type mechanical stabilizer with intracoronary shunt and CO2 blower mister. The composite graft was constructed where the LITA entered the pericardial space.

Generally, the left anterior descending artery (LAD) was first revascularized with the LITA regardless of the development of collateral circulation. The GEA graft was revascularized to a diagonal or obtuse marginal branch, or both diagonal and obtuse marginal branch, with > 70% target vessel stenosis and > 1.5 mm diameter of the target coronary vessel. After experiencing the "string sign" in two GEA grafts anastomosed to the right coronary system with moderate proximal stenosis early in our experience, the GEA graft was anastomosed only to the right coronary system with a high degree of stenosis (> 90%). Consequently, vessels with moderate stenosis and need of revascularization have since been resolved using percutaneous coronary intervention. Distal anastomoses were achieved using continuous running 8-0 polypropylene suture. Distal side-to-side anastomoses were made with diamond-shaped sutures and the end-to-side anastomoses were made using parallel sutures.

Protamine was administered only when the activated clotting time at the end of the procedure exceeded 200 seconds. Intravenous calcium-channel blockers were commonly used for 24 hours perioperatively, depending on the patient’s hemodynamic status. Oral calcium-channel blockers were prescribed at discharge, and continued for a variable period (usually 6 months).

The mean follow-up duration was 22.3 ± 10.2 months (range, 12 to 42). Immediate postoperative angiography (median, 14 days) was performed in all patients except in 1 patient with severe atherosclerotic changes to both iliac arteries. All patients were followed up, and early postoperative angiography (median, 348 days) was performed on 32 patients regardless of the presence of angina. Graft failure was defined as occlusion or stenosis > 70%. The presence of diffuse conduit narrowing or string sign was considered a functional occlusion, but was documented as graft failure. Two surgeons and a cardiologist determined graft patency for each patient.


   Results
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 Abstract
 Introduction
 Material and Methods
 Results
Comment
 Online Discussion Forum
 Acknowledgments
 References
 
Although 5 patients received prior abdominal surgery, this did not affect GEA harvesting. The conduit types used and the grafted coronary arteries are shown in Table 2. The in situ LITA was anastomosed to the LAD in all but 1 patient, who had severe mid-LITA atherosclerosis. The LITA was extended with an RA graft in this patient. The GEA was usually grafted evenly to the non-LAD arteries. In a patient with severe tandem lesion of the LAD, the remaining segment of the GEA graft was anastomosed to the proximal LAD through a "Y-Y" connection with the LITA. In 2 patients in whom the GEA was too short to reach the right coronary system, the additional length was acquired using an RA graft extension. The mean number (±standard error of the mean) of distal anastomoses per patient was 3.4 ± 0.93, and the mean number of anastomoses with a GEA graft was 2.13 ± 0.6 per patient.


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  		Table 2. Distribution of Distal Anastomosis
 
There was no early or late mortality. Perioperative myocardial infarction occurred in 1 patient who showed total occlusion of the LITA to LAD anastomosis on immediate postoperative angiography. Percutaneous coronary intervention was attempted but failed. Low cardiac output occurred in 2 patients and mediastinitis in 1. We did not experience any patients with strokes or abdominal complications (Table 3).


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  		Table 3. Operative and Postoperative Dataa
 
Immediate postoperative angiography demonstrated 36 of the 37 (97%) LITA grafts were patent. Two GEA grafts to the right coronary system with moderate proximal stenoses (< 70%) were positive for a string sign caused by competitive flow. In these patients, a GEA "T" graft was used to sequentially graft the obtuse marginal branch and the distal right coronary artery or one of its branches, and the string sign was evident only in the segment beyond this graft point to the right coronary artery. The other GEA grafts were fully patent (73 of 75, 97%). All three RA grafts used as a conduit extension (one to the LITA and two to the GEA) were patent.

On early postoperative angiography, all LITA grafts (32 of 32), 62 of 67 (92%) of the GEA grafts, and all three of the RA grafts were patent. Five GEA graft failures were noted, of which four were asymptomatic. In these patients, no further surgical treatment was performed. In 1 patient angina recurred and percutaneous coronary intervention was performed successfully. The two GEA grafts that showed a string sign on immediate postoperative angiography had progressed to the obtuse marginal branch. Two other GEA grafts showed greater than 70% stenosis at the GEA and distal right coronary artery anastomosis sites.


   Comment
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 Abstract
 Introduction
 Material and Methods
 Results
 Comment
Online Discussion Forum
 Acknowledgments
 References
 
The use of arterial grafts in coronary bypass surgery has steadily increased since initial reports such as those published by the Cleveland Clinic showed superior survival with BITA grafts [16–19]. Of the several strategies for total arterial revascularization, composite graft construction with one arterial conduit attached to the side of the LITA has gained popularity. Although this strategy has the potential for hypoperfusion [20], Muneretto and colleagues [21] recently reported a prospective randomized trial showing that this strategy leads to improved patient outcome in terms of freedom from cardiac events, recurrence of angina, and the need for percutaneous coronary intervention when compared with conventional arterial and venous grafting. Furthermore, the importance of this strategy has been expanding with the increased ages of patients undergoing CABG, the greater prevalence of preoperative risk factors, and longer life expectancy of treated patients, and consequently a greater probability of needing reoperation.

Among those arterial grafts, including the right internal thoracic artery, the RA, GEA, and the inferior epigastric artery, the RA or free right internal thoracic artery have been commonly used as secondary grafts for composite graft construction [1–5]. Therefore, when the availability of the other arterial grafts is limited because pathology or patient factors preclude their use, the right internal thoracic artery and RA can be readily utilized.

Because the right internal thoracic artery is histologically similar to the LITA, it was considered an ideal arterial graft with matching expectations for good long-term patency. However, concerns of sternal infection, dehiscence, and mediastinitis led to a more conservative approach to BITAs usage, with a tendency for avoidance in elderly, obese, or diabetic patients [13]. In addition, several studies have shown free right internal thoracic artery grafts to be associated with increased early and late postoperative graft failure rates [22, 23]. Although our primary strategy for total arterial revascularization involved BITAs, alternative arterial grafts were selected in those patients in whom this approach could not be used.

Because of the apparent histological differences between the RA and ITA, the RA was thought to be associated with a greater risk of developing atherosclerosis, intimal hyperplasia, and medial calcification [12, 24]. In a recent interim report, Buxton and colleagues [25] found RA grafts not to be necessarily superior to saphenous vein grafts in terms of patency. However, despite these and other negative reports, the RA has recently gained increasing popularity as an excellent second composite graft with the LITA because it offers technical advantages; it is easier to harvest and the grafting process can be completed while the LITA is being harvested [4, 5]. The RA was commonly avoided in patients with a positive Allen test, the presence of arteriosclerosis, renal dysfunction, trauma to upper limbs, and the presence of Raynaud’s disease. In addition, the use of the RA should be particularly avoided if patients have had a recent trans-radial coronary angiography [14, 15].

Essentially, the GEA is histologically more similar to the ITA than to the RA with a potential for greater resistance to atherosclerosis. Therefore one would expect better long-term patency with the GEA than with the RA [12, 26]. However, the GEA is the fourth branch of the aorta and has wide variations in size [27]. There is a significantly lower diastolic pressure in the GEA than in the LITA [28]. Therefore, the in situ GEA may be more prone to insufficient flow in the presence of coronary flow competition. A smaller GEA with a low flow relative to the native coronary artery may be associated with poor angiographic patency [29, 30]. Unlike the RA, the GEA is mainly bypassed as an in situ graft to the right coronary system, a region that is subject to controversy regarding graft selection [10, 11]. Consequently, despite the purported histologic advantages of the GEA, its use has not been shown to be as effective.

A randomized comparative study by Santos and colleagues showed a superior early patency rate (89.6%) with the RA than with the GEA (68.9%) when used as a composite graft. They could not find an exact explanation for the superior results seen with the RA, but the greater tendency for the GEA to undergo spasm was suggested as a possible mechanism [31]. We agree that this may be one cause for the differences in outcome between the two grafts. Therefore, to overcome this problem, we employed skeletonization to harvest the GEA in addition to a protocol of preventing spasm pharmacologically.

Such skeletonization of the GEA has been reported to reduce vasospasm and to provide an arterial conduit of longer length and larger caliber [32]. The use of an ultrasonic scapel for skeletonization may further decrease or avoid graft injury, and prevent graft spasm [32, 33]. Straightening of the tortuous vessel by skeletonization may allow the use of a conduit with a larger distal diameter. This may be advantageous in enhancing graft patency, as reported by Ochi and colleagues [34]. Therefore, if the BITAs and the RA were not available, we used the skeletonized free GEA composite graft for total arterial revascularization.

Our results with LITA-GEA composite grafts were similar to the reported patency rates of the RA composite graft by other authors, which ranged from 82% to 100% [35–37]. Although it is too early to ascertain any definite conclusions, the patency rate of the GEA composite graft in this study was similar to the reported results of the in situ graft with patencies between 88% and 92%, and better than that of the free graft attached directly to the ascending aorta [9, 38]. Accordingly, anastomosis of meticulously skeletonized GEA composite graft to well-selected coronary targets may result in patency rates approaching those of in situ GEA or RA composite graft.

Restriction of the follow-up period to the immediate and early phases of recovery in this study is a limitation. The serial angiographic GEA composite graft patency rate at 1-year and 5-year follow-ups reported by Suma and colleagues [39] and Hirose and colleagues [7] were 91.7% and 98.7%, and 80.5% and 84.4%, respectively. These authors argued that the anastomosis of nonfunctioning GEA grafts to high-flow vessels might have led to these relatively poor long-term results.

Another limitation was a lack of comparison with other methods of GEA graft use. Although the LITA to LAD anastomosis is an established gold standard, the ideal conduits or methods for revascularizing other coronary vessels are yet to be determined. There is no one single best approach and thus, the more options there are, the greater the chances of success. Therefore, further investigation may be required to develop and advance surgical techniques.

In conclusion, using LITA-GEA composite grafts may be a viable strategy for total arterial revascularization in the presence of limited availability of BITAs or the RA. However, it is important to skeletonize the graft to secure a large distal diameter. Although it needs longer follow-up, these early results demonstrated that the GEA graft may be a useful option in some situations of total arterial revascularization, used either as an in situ or as a composite graft.


   Online Discussion Forum
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 Material and Methods
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 Online Discussion Forum
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 References
 
Each month, we select an article from the The Annals of Thoracic Surgery for discussion within the Surgeon’s Forum of the CTSNet Discussion Forum Section. The articles chosen rotate among the six dilemma topics covered under the Surgeon’s Forum, which include: General Thoracic Surgery, Adult Cardiac Surgery, Pediatric Cardiac Surgery, Cardiac Transplantation, Lung Transplantation, and Aortic and Vascular Surgery.

Once the article selected for discussion is published in the online version of The Annals, we will post a notice on the CTSNet home page (http://www.ctsnet.org) with a FREE LINK to the full-text article. Readers wishing to comment can post their own commentary in the discussion forum for that article, which will be informally moderated by The Annals Internet Editor. We encourage all surgeons to participate in this interesting exchange and to avail themselves of the other valuable features of the CTSNet Discussion Forum and Web site.

For July, the article chosen for discussion under the Adult Cardiac Dilemma Section of the Discussion forum is:

Alternate Waiting List Strategies for Heart Transplantation Maximize Donor Organ Utilization

Jonathan M. Chen, MD, Mark J. Russo, MD, MS, Kim M. Hammond, RN, Donna M. Mancini, MD, Aftab R. Kherani, MD, Jen M. Fal, BA, Pamela A. Mazzeo, BA, Sean P. Pinney, MD, Niloo M. Edwards, MD, and Yoshifumi Naka, MD, PhD

Tom R. Karl, MD

The Annals Internet Editor, UCSF Children’s Hospital, Pediatric Cardiac Surgical Unit, 505 Parnassus Ave, Room S-549, San Francisco, CA 94143-0118, Phone: (415) 476-3501, Fax: (212) 202-3622, e-mail: mailto:karlt{at}surgery.ucsf.edu


   Acknowledgments
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 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Online Discussion Forum
 Acknowledgments
References
 
We are grateful to Dr Dong-Hun Kim for his assistance and counsel in preparing this article.


   References
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 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Online Discussion Forum
 Acknowledgments
 References
 

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