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Ann Thorac Surg 1999;67:624-628
© 1999 The Society of Thoracic Surgeons

Original Articles

Noninvasive assessment of right gastroepiploic artery graft patency using transcutaneous color Doppler echocardiography

Giuseppe Tavilla, MDa, Nico H.J. Pijls, MD, PhDb, Eric Berreklouw, MD, PhDa, Kathinka H. Peels, MDb

a Department ofCardiothoracic Surgery, Catharina Hospital, Eindhoven, The Netherlands
b Department ofCardiology, Catharina Hospital, Eindhoven, the Netherlands

Accepted for publication July 24, 1998.

Address reprint requests to Dr Tavilla, Department of Cardiothoracic Surgery, University Hospital Leiden, K6-S, Postbus 9600, 2300 RC Leiden, the Netherlands


   Abstract
Top
 Abstract
Introduction
 Material and methods
 Results
 Comment
 References
 
Background. Because the right gastroepiploic artery graft (GEA), when routed antegastrically, is situated just behind the abdominal wall, we investigated the possibility of evaluating graft patency and flow characteristics using transabdominal color Doppler echocardiography.

Methods. The right GEA graft was evaluated in 71 patients who underwent complete arterial revascularization, 4 months (range, 2 to 17 months) postoperatively. Selective angiography of the right GEA was performed in the patients in whom the graft could not be visualized using color Doppler echocardiography.

Results. Flow in the right GEA graft was detected in 65 (91.5%) of 71 patients using color Doppler echocardiography. In all visualized right GEAs, a biphasic flow pattern was observed, with higher peak velocity during systole. Mean (± standard deviation) peak systolic velocity was 76 ± 16 cm/s. Mean (± standard deviation) velocity was 41 ± 14 cm/s. Selective angiography of the right GEA in 5 patients in whom the graft could not be visualized using echocardiography showed four patent and functional grafts and one graft that was open but not functional ("slender sign"). One patient died before angiography could be performed. The sensitivity of noninvasive ultrasound assessment of the patency of the right GEA graft was 94% (65 of 69 patients). In this group of patients, an overall right GEA graft patency rate of 97% (69 of 71 patients) was found at mean follow-up of 4 months (range, 2 to 17 months).

Conclusions. The right GEA graft is an adequate coronary artery graft with a good short-term patency rate, and transcutaneous color Doppler echocardiography is a useful tool for evaluating its patency and flow characteristics. Selective angiography of the right GEA can be avoided in most cases and is indicated only when the graft cannot be detected using Doppler echocardiography.


   Introduction
Top
 Abstract
 Introduction
Material and methods
 Results
 Comment
 References
 
The use of arterial grafts has increased substantially since it was shown that the long-term patency of the internal thoracic artery (ITA) graft is superior to that of the saphenous vein graft [1]. In addition to both ITAs, the right gastroepiploic artery (GEA) can be used as an arterial conduit in myocardial revascularization [2] because of its functional similarity to the ITAs [3]. When it is routed antegastrically, the GEA graft can be detected relatively easily by transcutaneous color Doppler echocardiography because of its position just behind the abdominal wall [4]. The aim of this study was to evaluate noninvasively the patency and flow characteristics of the GEA graft with the use of transcutaneous color Doppler echocardiography.


   Material and methods
Top
 Abstract
 Introduction
 Material and methods
Results
 Comment
 References
 
Patient population
The study population consisted of 71 of 77 consecutively seen patients who underwent total arterial myocardial revascularization between April 1994 and October 1995. The other 6 patients did not undergo postoperative Doppler echocardiography. Two patients died in the hospital 1 day after operation of myocardial infarction despite emergency reoperation and additional venous bypass grafting. Two patients had postoperative ischemia several hours after the initial procedure; they underwent reoperation at which the GEA graft was ligated and venous grafts were added. One patient died 7 months after hospital discharge before Doppler echocardiographic examination, and another patient refused to undergo Doppler echocardiographic examination.

Of the 71 studied patients, there were 63 men and 8 women, with a mean age of 53.7 years (range, 37 to 66 years). Thirty-four patients (48%) had had a previous myocardial infarction, and 9 patients (13%) had unstable angina. There were 6 patients (8%) who had undergone previous coronary artery bypass grafting and 1 patient who had undergone reoperation. At operation in all patients, the GEA was mobilized and routed to the pericardial cavity through a hole in the diaphragm, passing the stomach and the liver anteriorly [5]. The GEA was used in combination with both ITAs in 62 patients, with only the left ITA in 7 patients, and as the only conduit in 2 patients (one reoperation [6] and one re-reoperation). All the arterial grafts were used as pedicled grafts, without any venous grafts (complete arterial revascularization).

A total of 250 anastomoses were constructed, with a mean of 3.5 per patient. The GEA always was used as a single graft (71 anastomoses), whereas 179 anastomoses were constructed with the ITAs (2.5 per patient) (Table 1). The GEA was anastomosed to the right posterior descending artery in 57 patients, to the distal main right coronary artery in 12 patients, and to the circumflex artery in 2 patients (Table 2). The study protocol was approved by the institutional review board, and informed consent for all investigations was obtained from all the participants.


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  		Table 1. Characteristics of the Arterial Grafts

 

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  		Table 2. Target Coronary Arteries of the Arterial Grafts

 
Echocardiographic detection of the gastroepiploic artery graft and registration of flow
Evaluation of the GEA graft was performed a mean of 4 months (range, 2 to 17 months) after coronary artery bypass grafting. Echocardiography was performed using a Hewlett-Packard Sonos 1000 ultrasound system (Andover, MA) with a 2.5- and 3.5-MHz transducer by a transcutaneous transabdominal approach. The patients were examined in the supine position while breathing normally. With the transducer positioned below the right chondral margin lateral to the midline, the GEA graft flow was detected by color Doppler echocardiography. Although many smaller veins and arteries could be seen below the ventral abdominal wall, the GEA graft was identified based on the following three criteria:
  1. A vessel with a diameter of 1.5 to 3 mm containing high-speed blood flow velocities indicating an arterial signal, with a general flow pattern in a caudocranial direction.
  2. A collar of abnormal echo-intensive perivascular tissue, as is not observed around normal native arteries in that area.
  3. A typical tortuous and unpredictable course, in some sections perpendicular to the transducer and in other sections almost tangentially imaged.

Because the systolic-to-diastolic flow pattern in a GEA graft is not expected to be typical and is strongly dependent on both the relative distance to its origin and the size of the distribution area of the recipient coronary artery, the systolic-to-diastolic flow pattern was not used as a criterion for identifying a GEA graft. The criteria outlined earlier were never observed in nonoperated patients and, when present, were considered to be specific for the GEA graft.

Guided by color Doppler imaging, a pulsed Doppler flow signal was acquired with the sample positioned in the GEA graft as parallel as possible to the visualized color Doppler flow signals (Fig 1). From the pulsed Doppler flow velocity spectrum, maximal and mean velocity were measured on-line. The echocardiographic images and Doppler signals were registered on super-VHS videotape for off-line analysis and archiving. Flows are represented as mean flow plus or minus the standard deviation of the mean.



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  		Fig 1. Postoperative transcutaneous Doppler echocardiographic imaging of the right gastroepiploic artery (GEA) graft showing a biphasic velocity pattern, with the highest velocity in systole and a second, lower peak in diastole. Notice the typical collar of abnormal echo-intensive perivascular tissue around the artery (small arrows).

 
Angiography of the gastroepiploic artery graft
In those patients in whom the GEA graft could not be identified using Doppler echocardiography, a 6-French sidewinder catheter was introduced into the right femoral artery and advanced into the celiac truncus and then into the common hepatic artery using a Terumo (Terumo Corp, Leuven, Belgium) guidewire up to the gastroduodenal artery, which was the best position possible in which to visualize the GEA. Angiograms were made from two preferably orthogonal projections at a film rate of 25 frames per second, using a power injection of 10 mL of Telebrix (Querbet, Roissy, France) at an injection rate of 3 mL/s. Patency of the GEA graft was defined as complete visualization of the graft and filling of the recipient artery during the imaging procedure. According to the method of Nakao and Kawaue [7], we defined the thinning-down phenomenon ("slender sign") of the GEA graft as a diameter of no greater than that of a 5-French catheter with ineffective graft flow.


   Results
Top
 Abstract
 Introduction
 Material and methods
 Results
Comment
 References
 
Transcutaneous doppler echocardiography
A blood vessel identified as a GEA graft was detected in 65 (91.5%) of 71 patients using color Doppler echocardiography. In all visualized GEAs, a biphasic flow pattern was observed, with higher peak velocity during systole. The waveform observed in the GEA graft consisted of a biphasic velocity pattern, with the highest velocity in almost all cases in systole and a second, lower peak in diastole (Fig 1). Mean (plus or minus standard deviation) peak systolic velocity was 76 ± 15 cm/s. Mean (plus or minus standard deviation) velocity was 41 ± 14 cm/s.

Angiography
In 6 patients, the GEA graft was not visualized using color Doppler echocardiography. In 5 patients, selective angiography of the GEA graft was performed after echocardiographic examination was unsuccessful. In 4 patients, the GEA graft was patent and could be seen along with the anastomosed native coronary artery (Fig 2). In 1 patient, the GEA graft presented a slender sign and was considered to be functionally occluded (Fig 3). One patient died before undergoing angiography. Therefore, the sensitivity of Doppler echocardiography in detecting a patent GEA was 94% (65 of 69 patients). When it is assumed that the patient who died before undergoing angiography, after having had a negative control Doppler examination, had an occluded GEA graft, and when the patient who had a functionally occluded GEA graft (slender sign) is considered, the overall patency of the GEA grafts (by Doppler echocardiography and angiography) in our study population was 97% (69 of 71 patients) at a mean of 4 months of follow-up (range, 2 to 17 months).



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  		Fig 2. Selective angiography of the right gastroepiploic (GEA) artery showing a patent graft that could not be detected using transcutaneous Doppler echocardiography. (RDP = right posterior descending artery.)

 


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  		Fig 3. A "slender sign" of a right gastroepiploic artery (GEA) graft, as demonstrated by selective angiography. This graft could not be detected using transcutaneous Doppler echocardiography.

 

   Comment
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
References
 
The better long-term patency rate of the ITA graft compared with the saphenous vein graft [8] has led to the increased use of arterial grafts in coronary artery bypass grafting. The use of one or both ITA grafts has resulted in improved long-term survival free of cardiac-related events and the need for reoperation [9]. However, to achieve complete arterial myocardial revascularization in a patient with three-vessel disease, a third arterial conduit is needed in addition to both pedicled ITAs. The GEA, a branch of the gastroduodenal artery, first was used as a direct bypass graft to the right coronary artery in January 1974 by Dr W. Sterling Edwards [10]. The GEA has become the preferred third arterial conduit among numerous investigators with large series of patients [11–14]. Although the GEA is similar to the ITA in its size and flow characteristics [15], its histologic traits [5] and pharmacologic responses [16] are somewhat different.

Until recently, there were no reliable methods other than invasive coronary angiography for determining the postoperative patency of coronary artery bypass grafts. In November 1987, Fusejima [17] reported the first successful clinical measurement of coronary artery blood flow velocity with the use of combined transthoracic two-dimensional and pulsed Doppler echocardiography. In 1990, Fusejima and coworkers [18] reported their experience with the measurement of blood flow velocity in saphenous vein grafts and ITA grafts, and the consequent flow patterns in the recipient left anterior descending artery. In the latter study, the rate of flow detection was 79% for ITA grafts and 87% for saphenous vein grafts.

This relatively low detection rate for the left ITA graft can be explained by the fact that the ITA is no longer positioned in its original anatomic location close to the chest wall, and by the fact that the acoustic window between the clavicle and the first rib or between the first and second ribs is too small to allow identification of the left ITA. This finding was confirmed by de Bono and associates [19], who detected flow in the nongrafted ITA in all 19 patients who had a unilateral ITA graft, but identified flow in the proximal part of an ITA grafted to a left anterior descending coronary artery in only 16 (61%) of 26 patients who had undergone this procedure. However, with increasing experience, Crowley and Shapiro [20] and Canver and colleagues [21] reported reproducibility rates for successful imaging of postoperative left ITA grafts of 81% and greater than 90%, respectively.

In the GEAs visualized in this study, the higher peak velocity almost always occurred during systole with a lower diastolic flow. This flow pattern is different from the one detected in saphenous vein grafts or ITA grafts, in which the higher velocity occurs during diastole [18]. This might be explained by the muscular nature of the GEA [5] associated with the higher resistance to flow in the longer vessel.

We [22] first reported the intraoperative use of pulsed Doppler echocardiography to evaluate the effectiveness of the GEA as a coronary artery bypass graft. In that study, we analyzed the flow pattern of the GEA before takedown and after completion of the anastomosis just before sternal closure. Before takedown, the flow pattern of the GEA was typical of peripheral arterial flow, with the highest velocity during systole. After anastomosis of the GEA to the coronary artery, the graft flow pattern showed two phases of antegrade systolic and diastolic flow. In most cases, the lowest bypass flow velocity occurred during systole and the highest flow velocity occurred during diastole. Therefore, the intraoperative postanastomosis flow pattern of the GEA graft was different from the one we detected in this study with the use of transcutaneous Doppler echocardiography.

When it is routed antegastrically, the GEA lies just behind the abdominal wall, in the epigastric region. This location, and the typical caudocranial flow direction of the GEA graft, makes it possible to detect the graft on color Doppler echocardiography. Using this technique, Nishida and coworkers [4] detected flow in the GEA graft in 39 (89%) of 44 patients, whereas Gryspeerdt and associates [23] detected flow in 65 (84%) of 77 patients. In this study, we were able to visualize the GEA graft in 65 (94%) of 69 patients. Various factors can interfere with echocardiographic visualization of the GEA graft and lead to a false-negative diagnosis of graft patency. Some of these factors are patient-related, such as the amplified movement of the abdominal wall that results from the need to continue breathing. Other factors could be related to graft characteristics, such as a less superficial position of the graft.

In 1993, Nakao and Kawaue [7] reported the angiographic finding of a "thinning-down" phenomenon of the right GEA, defined as a graft diameter of no greater than that of a 5-French catheter, with ineffective graft flow; this finding was termed the slender sign. In their report, the slender sign was detected in 4 (7.8%) of 51 GEA grafts. The authors stated that the development of the slender sign is caused by competitive native coronary flow, narrowing of the perfused coronary artery, and poor runoff, similar to the situation sometimes encountered in internal thoracic operations (the so-called string sign) [24]. In the three patients with a slender sign whom they described [7], there was good native coronary flow and no sign of ischemia in the perfused region, indicative of sufficient blood supply to the myocardium. Thus, the slender sign indicates a patent but poorly functioning or nonfunctioning graft.

A thin artery with low graft flow may be difficult to detect using color Doppler echocardiography. In this study, we could not detect the GEA graft in 6 patients using color Doppler echocardiography and had to perform postoperative angiography to study the GEA. One patient died before angiography could be performed. Only one of the five angiographic studies performed revealed a slender sign of the GEA graft. In the remaining 4 patients, a patent, well-functioning graft was found; therefore, the results of the Doppler echocardiographic examination had been falsely negative in these patients. In contrast to its high sensitivity, the specificity of Doppler echocardiography in identifying a patent GEA is low. Although the results of the Doppler echocardiographic examinations were not validated by the performance of angiography in every case (angiography was performed only when the noninvasive technique was unsuccessful), we believe that adherence to the three criteria described earlier for identifying the GEA graft is sufficient to avoid the pitfalls of the Doppler technique.

In conclusion, evaluation of a GEA graft by transcutaneous Doppler echocardiography is easier than evaluation of an ITA graft or a saphenous vein graft because its location is almost motionless and it is not affected by the beating heart, which allows its reliable detection, as shown in this study. The GEA graft is an adequate coronary artery graft with a good short-term patency rate, and color Doppler echocardiography is a useful tool for evaluating its patency and flow characteristics. Most patent GEA grafts can be detected in this way (sensitivity = 94%). However, the specificity of the technique is low (20%). Selective angiography remains the gold standard for evaluating GEA graft patency when Doppler echocardiographic imaging is unsuccessful.


   References
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 

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