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Ann Thorac Surg 1997;64:426-431
© 1997 The Society of Thoracic Surgeons

Original Articles: Cardiovascular

Intraoperative Blood Flow Measurement of the Right Gastroepiploic Artery Using Pulsed Doppler Echocardiography

Giuseppe Tavilla, MD, Jack Jackimovicz, MD, PhD, Eric Berreklouw, MD, PhD

Department of Cardiothoracic Surgery, St. Antonius Hospital, Nieuwegein, and Departments of General Surgery and Cardiothoracic Surgery, Catharina Hospital, Eindhoven, the Netherlands

Accepted for publication February 4, 1997.


   Abstract
Top
 Footnotes
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
Background. In coronary artery revascularization, the right gastroepiploic artery (GEA) has become the third arterial conduit of choice after both internal thoracic arteries. To evaluate the function of the right GEA, we used intraoperative ultrasonographic Doppler measurement of the blood flow of this artery.

Methods. From November 1992 to December 1993, in 41 consecutive patients, graft flow velocity, diameter, and blood flow were measured in the proximal part of the GEA before takedown and after completion of the anastomosis just before sternal closure. We also analyzed the predictors of postoperative ischemia.

Results. Flow volume of the GEA after anastomosis with the coronary artery has a significant correlation with the diameter of the target coronary artery (p = 0.0011). Two patients had development of ischemia postoperatively. In both, volume flow of the GEA was less than 25 mL/min before takedown compared with an average flow of 55.78 mL/min in the patients without ischemia postoperatively. This was found to be a prognostic indicator of poor graft performance with consequent ischemia.

Conclusions. When the GEA blood flow volume before takedown is less than 25 mL/min, we suggest that this artery not be used as a bypass graft for myocardial revascularization.


   Introduction
Top
 Footnotes
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
See also page 431.

To achieve complete revascularization with only arterial conduits in extensive coronary artery disease, the gastroepiploic artery (GEA) is being used more and more often in addition to both internal thoracic arteries (ITAs) [1]. To evaluate the function of the GEA in coronary artery bypass grafting and to identify potential GEA flow predictors of postoperative ischemia, we used an ultrasonographic pulsed Doppler device to measure blood flow before takedown and after anastomosis with the target coronary artery.


   Material and Methods
Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 Acknowledgments
 References
 
From November 1992 to December 1993, 41 consecutive patients underwent complete myocardial revascularization with both pedicled ITA, and the pedicled right GEA. No saphenous vein grafts were used. All patients were men with a mean age of 50 years (range, 40 to 61 years). Six patients (15%) had had a previous myocardial infarction, and 4 patients (10%) had unstable angina. All patients were having primary coronary artery bypass grafting.

Preoperative coronary angiography revealed triple-vessel disease in every patient. Preoperative variables that were recorded included the patient's weight and height and the angiographic degree of stenosis of the coronary artery that received the GEA [2]. For all patients, we used intraoperative pulsed ultrasonographic Doppler measurements to assess the GEA velocity, diameter, and calculated flow so that we could estimate the appropriateness of use of the artery and after the anastomosis, the function of the graft. For the GEA, we prefer to use pulsed Doppler rather than electromagnetic flow measurement (which we apply routinely for ITA and saphenous vein grafts) because of the risk of damaging the artery during dissection to position the almost circular head of the electromagnetic flowmeter.

Surgical Procedures and Doppler Measurements
To prepare the GEA, the midline sternal incision was extended about 5 cm below the xiphoid process. Measurement of diameter and blood velocity was performed with the GEA in its anatomic position before takedown was begun. To avoid spasm in the artery, care was taken to handle the vessel very gently while measurements were performed.

We used an echo camera (Aloka SSD-650 duplex scanner; Tokyo, Japan) equipped with a transducer combined with a 7.5-MHz, pulsed-wave, direction-sensitive Doppler flow detector with a 7.5 B-mode option. The transducer was placed directly on the GEA about 5 cm distal from its origin from the gastroduodenal artery and held at a constant angle of 60 degrees to the axis of blood flow. A real-time, fast Fourier-transform spectrum analyzer was used to assess the GEA waveform in regard to turbulence and flow velocities [3]. The diameter of the vessel was measured with the B-mode. After a steady-state flow velocity was observed for at least 2 minutes, the following variables were recorded: peak systolic flow velocity (cm/s), end-diastolic flow velocity (cm/s), and diameter (cm). Mean velocity (cm/s) was obtained directly from the computer. Mean blood flow of the artery was calculated using the following formula [4]


where r is one half of the GEA diameter (cm) and 60 is the angle between the transducer and the axis of the GEA as determined by the echo camera.

The GEA was dissected using staplers (LDS 15 W; United States Surgical Corporation, Norwalk, CT) to divide its branches to the stomach and the omentum. When the branches to the stomach were too short, they were ligated. The GEA was dissected distally for two thirds of the greater curvature of the stomach and proximally to the pylorus.

After systemic heparinization, both ITAs and the GEA were transected distally. Free flow in the conduits was not measured. The ITAs were wrapped in gauze soaked in papaverine hydrochloride solution without intraluminal injections. For the GEA, we used 0.25 mL of diluted papaverine (12.5 mg in 20 mL of normal saline solution) injected intraluminally with an epidural catheter. Gauze soaked in a solution containing papaverine was wrapped around the GEA pedicle.

The GEA pedicle was routed behind the stomach and the left lobe of the liver and passed through a hole in the diaphragm to reach the target coronary artery [5]. The GEA–coronary artery anastomoses were made using a running 8-0 polypropylene suture. The GEA was anastomosed in antegrade fashion with the heel of the graft placed on the proximal end of the arteriotomy when the target coronary artery was the right posterior descending coronary artery or branches of the circumflex artery. The GEA–coronary artery anastomosis was constructed in a retrograde fashion with the heel of the graft on the distal aspect of the arteriotomy when the target artery was the right coronary artery and in one case, the left anterior descending coronary artery. In all instances, complete cardiopulmonary bypass was accomplished with cardioplegic arrest and moderate hypothermia (32°C).

At operation, the diameters of the target coronary artery and the GEA at the site of anastomosis were measured with calibrated probes with differences of a quarter of a millimeter. The size of the GEA at the site of the distal anastomosis ranged from 1.5 to 2.25 mm.

Forty-one GEA grafts were used to construct 43 anastomoses. The GEA was used to graft the distal right coronary artery in 11 patients, the right posterior descending artery in 26 patients, branches of the circumflex artery in 2 patients, and the left anterior descending coronary artery in 1 patient (Table 1Go). An additional 95 anastomoses were constructed with both ITAs, for a total of 138 anastomoses (mean number, 3.4 per patient) (Table 2Go). No saphenous vein grafts were used.


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  		Table 1. . Graft Placement
 

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  		Table 2. . Graft Construction
 
After revascularization and cessation of cardiopulmonary bypass, Doppler measurement of the GEA graft was repeated at the same site as before takedown. Again, the variables were measured after a steady-state flow velocity was observed for at least 2 minutes. During the Doppler flow studies, the mean arterial pressure was stabilized at 60 to 80 mm Hg.

Data Collection and Statistical Methods
All data were compiled in a computerized databank and analyzed with the Number Cruncher Statistical System (Hintze, Kaysville, UT). Statistical analysis of categoric variables was performed on cross-tables using the Pearson {chi}2 test. Continuous variables were analyzed with the two-sample t test if the variance of the groups was equal; otherwise, the Mann-Whitney U test was used. The predictors of GEA flow were calculated from the beta estimates with 95% confidence limits using the standard errors of the beta estimates. The same method was used to calculate the relative risks for the appearance of postoperative ischemia. In all statistical tests, a two-sided p value of less than 0.05 was considered significant.


   Results
Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 Acknowledgments
 References
 
An example of resting blood flow pattern in the right GEA before takedown is shown in Figure 1Go. The flow pattern was typical of peripheral arterial flow, with the highest velocity during systole. The systolic component of the waveform had a peak, and the end-diastolic velocity was close to zero (see Fig 1Go). After anastomosis of the GEA to the coronary artery, the graft flow pattern showed two phases of antegrade systolic and diastolic flow. The lowest bypass flow velocity occurred during systole; the highest flow velocity was during diastole and in most instances was without a peak (Fig 2Go). We did not notice differences in flow pattern between GEAs grafted to the right coronary system (38 patients) versus those grafted to the left coronary system (3 patients).



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  		Fig 1. . Example of right gastroepiploic artery ( GEA) velocity before takedown: highest velocity during systole.

 


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  		Fig 2. . Example of right gastroepiploic artery ( GEA) velocity after anastomosis with coronary artery: graft flow velocity highest during diastole.

 
Before takedown of the GEA, the graft flow volume ranged from 18 to 109 mL/min (mean volume, 55 ± 20 mL/min ± standard deviation), and the diameter by ultrasonography ranged from 2.5 to 3.5 mm (mean diameter, 2.8 mm). After anastomosis of the GEA, the graft flow volume ranged from 19 to 113 mL/min (mean volume, 61 ± 24 mL/min) (p = not significant) and the diameter at the same site as before, from 2.5 to 3.5 mm (mean diameter, 2.9 mm) (p = not significant). The differences in GEA flow volume before takedown and after anastomosis with the target coronary artery are shown in Figure 3Go.



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  		Fig 3. . Differences in flow volume (mL/min) of right gastroepiploic artery before takedown and after anastomosis with target coronary artery.

 
GEA Graft Flow Volume and Postoperative Ischemia
Two patients (4.9%) had development of ischemia postoperatively (Table 3Go). In 1 patient it occurred just after arrival in the intensive care unit and in the other, in the operating room during skin closure. In the first patient, blood flow volume of the GEA before takedown was 18 mL/min. The GEA was anastomosed to a right posterior descending artery of good quality with a diameter of 1.5 mm. The left ITA was anastomosed to the circumflex artery and the right ITA, to the left anterior descending coronary artery. The blood flow volume after GEA–coronary artery anastomosis was 19 mL/min.


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  		Table 3. . Predictors of Postoperative Ischemiaa
 
In the second patient, the GEA was anastomosed to a large (2 mm) marginal branch of the circumflex artery. The blood flow volume of the GEA before takedown was 22 mL/min. The left ITA was anastomosed to the left anterior descending coronary artery and the right ITA, to the right coronary artery. The blood flow volume of the GEA after anastomosis was 71 mL/min (Fig 4Go). In both patients, cardiopulmonary bypass was reestablished on an emergency basis, and an additional triple saphenous vein bypass was performed, as is routinely done in our hospitals under these conditions. At reoperation, all previous arterial grafts were checked and found to be fully patent. Both patients recovered well without new Q waves on the electrocardiogram. Thereafter, during the study period, we discarded two GEAs because before takedown, both had poor flow volume (less than 25 mL/min) (Fig 5Go).



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  		Fig 4. . Flow pattern of right gastroepiploic artery ( GEA) in a patient with postoperative ischemia: (A) before takedown and (B) after anastomosis with circumflex artery. (Small arrow = peak systole; large arrow = middiastole.)

 


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  		Fig 5. . Example of flow pattern of right gastroepiploic artery ( GEA) not taken because of poor blood flow volume (less than 25 mL/mn). (Small arrow = peak systole; big arrow = middiastole.)

 
Predictors of GEA Graft Flow Volume
The flow volume of the GEA before takedown showed no significant correlation with weight or height of the patient. After anastomosis with the target coronary artery, the flow volume of the GEA had a significant correlation with the diameter of the target coronary artery (p = 0.0005). We could not demonstrate a correlation between the GEA flow after anastomosis to the target coronary artery and the GEA flow volume before takedown, the GEA diameter before takedown, or the degree of stenosis in the target coronary artery (Table 4Go).


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  		Table 4. . Predictors of Right Gastroepiploic Artery Flow After Anastomosis
 

   Comment
Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
Acknowledgments
 References
 
The potential advantages of arterial conduits compared with venous conduits have prompted the use of alternative arterial conduits such as the right GEA [6, 7]. Angiographic [8] and anatomic [5] studies have demonstrated that the pedicled right GEA can reach any coronary artery. Bandik and colleagues [9] reported their experience with the measurement of blood flow velocity of ITA and saphenous vein grafts at operation. In this report, pulsed Doppler spectral analysis of graft perfusion demonstrated preponderantly diastolic flow with a variable multiphasic flow pattern in systole. Analysis of the phasic flow patterns permitted an assessment of functional graft patency.

Using an ultrasonographic Doppler miniprobe, Takayama and associates [10] measured the blood flow of ITA and GEA grafts at the time of operation in 16 patients. Graft flow velocity was obtained four times: before and after takedown of the ITA and the GEA, after weaning from extracorporeal circulation, and before sternal closure. They noticed that graft flow after takedown and just after weaning from extracorporeal circulation showed a tendency to decrease, but it recovered just before sternal closure to be almost equal to that before takedown.

As stated by Baird and co-workers [11], the physical factors determining flow in coronary artery bypass grafts are the driving pressure (the difference between aortic and intraventricular or coronary sinus pressure, whichever is greater) and the coronary vascular resistance. In the heart, the vascular resistance of the coronary graft is related to the caliber of the conduit and outflow vessels, the degree of dilatation of the distal coronary arterial bed, and the magnitude of extrinsic compression of the coronary vessels by the surrounding myocardium. As the coronary arteries penetrate the ventricular muscle, they are subjected to the intramural compressive forces developed during systole.

Therefore, the interaction between the driving aortic pressure and the ventricular compressive forces results in a blood flow pattern in coronary bypass grafts with maximum forward flow in diastole and high-frequency phasic flow components during systole. Pulsed Doppler spectral analysis of coronary bypass grafts demonstrated that phasic blood flow patterns in ITAs and reversed saphenous veins are similar to the flow in normal coronary arteries [10].

This supports our findings that the phasic blood flow pattern in the right GEA graft is similar to the flow in normal coronary arteries. In our study, at the first measurement, the flow pattern of the GEA was typical of peripheral arterial flow, with the highest velocity during systole and the end-diastolic velocity close to zero. The second measurement was performed just before sternal closure. The GEA graft flow pattern showed the velocity was highest and without a peak during diastole and zero in early systole.

From our data analysis, we found a significant correlation between the flow volume of the GEA graft and the diameter of the target coronary artery. The graft flow volume after GEA–coronary artery anastomosis in our patients was the same or greater than the graft flow volume before takedown of the artery in most instances. When the target coronary artery had a small diameter (less than 1.5 mm) or was of poor quality, the graft flow volume after anastomosis was sometimes slightly less than it was before takedown. When the GEA was anastomosed to a large coronary artery, we noticed an increased blood flow through the graft.

There seems to be a significant correlation between the pretakedown mean velocity and mean arterial flow of the GEA and the incidence of postoperative ischemia. There apparently is no significant correlation with the mean velocity and mean arterial flow after the anastomosis because 1 of the 2 patients with ischemia had a relatively high GEA blood flow after the anastomosis. In both patients with ischemia, the pattern of blood flow after the anastomosis was normal, thus indicating that no technical errors had been made. Although we cannot exclude the role of other causes for the appearance of postoperative ischemia in these 2 patients, we think that probably the blood flow volume of the GEA grafts was not enough to supply the myocardial area of the target coronary arteries.

The advantage of using pulsed Doppler echocardiography for measuring blood flow of the GEA before takedown compared with free measurement after takedown is that we have immediate information about the diameter at the origin and the blood flow volume of the GEA with minimal manipulation of the artery. The advantage of pulsed Doppler echocardiography in measuring flow pattern and blood flow volume of the GEA after anastomosis with the target coronary artery is that we have direct data about the function of the anastomosis.

In conclusion, intraoperative pulsed Doppler blood flow measurement of the GEA is technically feasible, has no negative effects, and allowed us to check directly the patency of the GEA–coronary artery anastomosis. Although the number of patients with ischemia was low, there might be a correlation between the preoperative mean blood flow of the GEA (less than 25 mL/min) and the incidence of postoperative ischemia. Therefore if the in situ GEA blood flow is less than 25 mL/min preoperatively, we suggest that this artery not be used as a bypass graft for myocardial revascularization.


   Acknowledgments
Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
References
 
We are very grateful to Jaap Buth, MD, for the analysis of the Doppler measurements and to Freddy Vermeulen, MD, Nico Pijls, MD, PhD, and Kathinka Peels, MD, for reviewing the manuscript.


   Footnotes
Top
 Footnotes
Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
Address reprint requests to Dr Tavilla, Department of Cardiothoracic Surgery, St. Antonius Hospital, Postbus 2500, 3430 EM Nieuwegein, the Netherlands.


   References
Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 

  1. Suma H, Wanibuchi Y, Terada Y, Fukuda S, Takayama T, Furuta S. The right gastroepiploic artery graft. Clinical and angiographic midterm results in 200 patients. J Thorac Cardiovasc Surg 1993;105:615–23.[Abstract]
  2. Austen WG, Edwards JE, Frye RL, et al. A reporting system on patients evaluated for coronary artery disease. Circulation 1975;51:5–40.[Medline]
  3. Kajiya F, Ogasawara Y, Tsuioka K, et al. Evaluation of human coronary blood flow with an 80 channel 20 MHz pulsed Doppler velocimeter and zero-cross and Fourier transform methods during cardiac surgery. Circulation 1986;74 (Suppl 3):53–60.
  4. Canver CC, Ricotta JJ, Bhayana JN, Fiedler RC, Mentzer RM Jr. Use of duplex imaging to assess suitability of the internal mammary artery for coronary artery surgery. J Vasc Surg 1991;13:294–301.[Medline]
  5. Tavilla G, van Son JAM, Verhagen AF, Smedts F. Retrogastric versus antegastric routing and histology of the right gastroepiploic artery. Ann Thorac Surg 1992;53:1057–61.[Abstract]
  6. Pym J, Brown PM, Charrette EJP, et al. Gastroepiploic– coronary artery anastomosis. A viable alternative bypass graft. J Thorac Cardiovasc Surg 1987;94:256–9.[Abstract]
  7. Suma H, Fukumoto H, Takeuchi A. Coronary artery bypass grafting by utilizing in situ right gastroepiploic artery: basic study and clinical application. Ann Thorac Surg 1987;44:394–7.[Abstract]
  8. Saito T, Suma H, Terada Y, Wanibuchi Y, Fukuda S, Furuta S. Availability of the in situ right gastroepiploic artery for coronary artery bypass. Ann Thorac Surg 1992;53:266–8.[Abstract]
  9. Bandik DF, Galbraith TA, Haasler GB, Almassi GH. Blood flow velocity of internal mammary artery and saphenous vein grafts to the coronary arteries. J Surg Res 1988;44:324–51.
  10. Takayama T, Suma H, Wanibuchi Y, et al. Doppler miniprobe to measure arterial graft flow in coronary artery bypass grafting. Ann Thorac Surg 1991;52:322–4.[Abstract]
  11. Baird RJ, Manktelow RT, Shah PA, Ameli FM. Intramyocardial pressure. A study of its regional variations and its relationship to intraventricular pressure. J Thorac Cardiovasc Surg 1970;59:810–23.[Medline]

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