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Ann Thorac Surg 2005;80:594-598
© 2005 The Society of Thoracic Surgeons


Original article: Cardiovascular

Prediction of Graft Flow Impairment by Intraoperative Transit Time Flow Measurement in Off-Pump Coronary Artery Bypass Using Arterial Grafts

Ki-Bong Kim, MD, PhD * , Chang Hyun Kang, MD, Cheong Lim, MD, PhD

Department of Thoracic and Cardiovascular Surgery, Seoul National University Hospital, Seoul, Korea

Received for publication February 15, 2005. * Address reprint requests to Dr Kim K-B, Department of Thoracic and Cardiovascular Surgery, Seoul National University Hospital, 28 Yeun-Kun Dong, Chong-Ro Ku, Seoul 110-744, Korea. (Email: kimkb{at}snu.ac.kr).


    Abstract
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 
BACKGROUND: We assessed the validity of intraoperative transit time flow measurement (TTFM) in predicting graft flow abnormalities.

METHODS: Intraoperative graft flow measurement using TTFM and early postoperative coronary angiography was performed in 58 patients who underwent total arterial off-pump coronary artery bypass. Five variables (flow pattern, mean flow, pulsatility index, insufficiency ratio, and fast Fourier transformation ratio) were measured and compared between 103 normal and 14 abnormal (occluded or competitive) grafts.

RESULTS: The grafts anastomosed to the right coronary territories showed significantly less diastolic dominant pattern, lower mean flow and fast Fourier transformation ratio, and higher pulsatility index than grafts to the left coronary artery territories (p < 0.05). None of the abnormal grafts showed a diastolic dominant flow pattern. The abnormal grafts demonstrated significantly lower mean flow and fast Fourier transformation ratio and higher pulsatility index and insufficiency ratio than normal grafts (p < 0.05). When our criteria for detection of abnormal graft flow, [(1) systolic dominant or balanced pattern of the flow curve in the left coronary territories, systolic dominant pattern of the flow curve in the right coronary territories; (2) mean flow < 15 mL/min; (3) pulsatility index > 3 in the left coronary territories and > 5 in the right coronary territories; and (4) insufficiency ratio > 2%] were applied, the sensitivity and specificity of TTFM to detect the graft flow abnormality were 96.2% and 76.9%, respectively.

CONCLUSIONS: Our data suggest that TTFM is a reliable intraoperative tool to predict graft flow impairment.


    Introduction
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 
With resurgent interest in off-pump coronary artery bypass grafting (OPCAB), there have been concerns about the accuracy of anastomosis and patency of graft [1–3]. Several methods, including manual palpation of the graft, direct probing of the anastomosis, graft patency testing with syringe, electromagnetic flow meters, and ultrasound-based flow meters such as Doppler and transit time flow measurement (TTFM; BF1001, Medi-Stim AS, Oslo, Norway), and intraoperative angiography, have been used to assess graft patency intraoperatively. Among these methods, TTFM has been used with increasing frequency because it is considered to be a convenient and reliable way to document graft patency [4–7]. Although several studies have demonstrated the usefulness of intraoperative assessment of graft flow by TTFM, the cutoff values of TTFM variables to distinguish the grafts with flow impairment from those with normal flow have not been well-established.

The aims of this study were the following: (1) to present the normal flow pattern of grafts anastomosed to the right and left coronary territories; (2) to assess the validity of TTFM by comparing it with graft patency assessment from early postoperative angiography; and (3) to establish cutoff values for the TTFM variables for detecting graft flow impairment in OPCAB patients who received arterial grafts.


    Patients and Methods
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 
Since we began performing OPCAB at our institution in 1998, we have performed early postoperative coronary angiography in almost all of our patients to assess the accuracy of the anastomosis and graft patency. We recognized the importance of assessing graft patency intraoperatively during OPCAB and began using TTFM in July 2000. However, we did not know appropriate TTFM cutoff values for abnormal anastomotic arterial grafts in OPCAB patients, and intraoperative graft revision was performed only when TTFM demonstrated unexpectedly low flow (< 3 mL/min) or a high pulsatility index value (> 20).

In this study, 58 patients who underwent total arterial OPCAB, intraoperative graft flow measurement using TTFM, and early postoperative coronary angiography (postoperative days 1.1 ± 0.4) between November 2000 and August 2001, were studied retrospectively (Table 1). One hundred and seventeen anastomoses from a total of 185 distal arterial graft anastomoses were included in this study. Thirty-four sequential anastomoses and another 34 anastomoses distal to the sequential anastomoses were excluded from this study because the graft flow through the proximal sequential and distal anastomoses could affect each other and the interpretation of graft flow pattern was difficult and complicated. The grafts used for distal anastomoses were left internal thoracic artery (ITA) (n = 39), right ITA (n = 39), right gastroepiploic artery (n = 38), and radial artery (n = 1). The arterial grafts were used as in situ grafts (n = 93), Y-composite grafts (n = 22), or free grafts anastomosed onto the ascending aorta (n = 2). All the left ITAs were grafted to left coronary territory. The right ITAs were grafted to the left coronary territory in 32 patients and to the right coronary territory in 7 patients. The right gastroepiploic arteries were anastomosed to the right coronary territory in 37 patients and to the left coronary territory as a Y-composite graft in one patient. One radial artery was grafted to the left coronary territory as a Y-composite graft (Table 2). Flow measurement for all grafts was performed just before sternal closure and all data were recorded and stored in the flow meter for future analysis. Mean blood pressure was maintained between 80 and 90 mm Hg during the flow measurement and a properly fitted probe (2 or 3 mm) was used for flow measurement. In patients with a Y-composite graft, flow was measured separately in each arm of the Y-composite graft. After the flow measurement, the following five variables were obtained and analyzed: (1) flow curve pattern; (2) mean graft flow; (3) pulsatility index ([maximal flow-minimal flow]/mean flow); (4) insufficiency ratio (percentage of backward flow); and (5) fast Fourier transformation ratio (= F0/H1, where F0 is a power of the fundamental frequency and H1 is a power of the first harmonic). The flow curve pattern was classified into three patterns based on the maximal flow value: (1) balanced (where the difference between peak systolic and peak diastolic flows was less than 10% of peak diastolic flow); (2) systolic dominant (where peak systolic flow exceeded peak diastolic flow by 10%); (3) diastolic dominant (where peak diastolic flow exceeded peak systolic flow by 10%).


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Table 1. Preoperative Characteristics and Risk Factors of the Study Patients
 

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Table 2. Grafts and Their Target Coronary Arteries
 
Four-plane selective coronary angiography was performed 1.1 ± 0.4 days postoperatively to determine abnormal graft. One physician initially reviewed all the coronary angiograms and consensus was reached after review. All of the anastomoses were reviewed and defined as patent graft with unimpaired run-off, stenotic graft with anastomotic narrowing of greater than 50%, occluded graft, and competitive graft in which the distal coronary artery was not clearly visualized by graft angiography, but was visualized through retrograde filling without anastomotic narrowing by native coronary angiography. Written, informed consent was obtained from each participating patient.

Surgical Technique
OPCAB was performed as previously described [8]. All operations were performed through a median sternotomy incision. A standard skeletonizing technique for harvesting the ITA was used. If use of bilateral ITAs as in situ or Y-composite grafts did not achieve complete revascularization, a short lower extension of the median incision was made to harvest the right gastroepiploic artery in a skeletonized fashion. The radial artery was harvested in a patient undergoing redo coronary artery bypass grafting. Patients received an initial dose of 1.5 mg/kg of heparin and periodically received supplemental doses to maintain an activated clotting time of greater than 300 seconds. After systemic heparinization, the skeletonized arterial grafts were clipped distally, immersed in a 10 mL syringe filled with warm diluted papaverine saline solution (1 mg/mL), and allowed to dilate pharmacologically. Intraluminal injection of papaverine solution was not used. The distal anastomosis was constructed using a continuous technique with 8-0 polypropylene sutures. If needed, proximal anastomoses on the ascending aorta were constructed after the distal anastomoses, using partial clamping of the aorta and a 7-0 polypropylene continuous suture. Protamine was not administered at the end of the procedure. The operations were all performed by a single surgeon (K-BK).

Statistical Analysis
Statistical analysis was performed with the Statistical Analysis System software package (version 6.12; SAS Institute, Cary, NC). The significance of differences between the two groups was assessed by the unpaired Student’s t test, the {chi}2 test, and Fisher’s exact test. All results were expressed as mean ± standard deviation, and a p value of less than 0.05 was considered to be statistically significant.


    Results
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 
Angiographic Results
Three in situ right gastroepiploic artery grafts anastomosed to the right coronary territories were occluded as shown by postoperative coronary angiography. Flow competitions were observed in 11 distal anastomoses (6/73 in the left coronary territories vs 5/44 in the right coronary territories, p = not significant). None of the grafts showed anastomotic stenosis of greater than 50% of the grafted coronary artery. Three grafts showed mild stenosis of less than 50% of the grafted coronary artery, and they were regarded as patent grafts.

Normal Versus Abnormal Flow Pattern
The TTFM variables measured in patent grafts were compared with those of 14 angiographically demonstrated abnormal grafts (3 occluded and 11 competitive grafts) (Table 3). None of the abnormal grafts showed the diastolic dominant flow pattern. The abnormal grafts showed significantly lower mean flow and fast Fourier transformation ratio and higher pulsatility index and insufficiency ratio than the patent grafts. There were significant differences in all five variables between the patent and abnormal grafts (p < 0.05).


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Table 3. Comparison of Transit Time Flow Measurement Variables Between Normal and Abnormal Grafts
 
Right Versus Left Coronary Territories
To identify any difference in the normal flow patterns between the right and left coronary artery territories, the TTFM variables of 103 patent grafts were analyzed according to the location of the graft (Table 4). The right coronary territories included the right coronary artery, posterior descending artery, and posterolateral branches; the left coronary territories included the left anterior descending artery, diagonal branches, left circumflex artery, and obtuse marginal branches. The grafts anastomosed to the right coronary territories showed significantly less diastolic dominant pattern, lower mean flow and fast Fourier transformation ratio, and higher pulsatility index than grafts anastomosed to the left coronary artery territories (p < 0.05). The insufficiency ratio in the right coronary territories was lower than that of the left coronary system but without significant difference between the two.


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Table 4. Comparison of the Normal Graft Flow Variables Between the Right and Left Coronary Artery Territories
 
To identify any difference in the normal flow patterns between the right gastroepiploic artery and ITA, we also analyzed the TTFM variables of 36 patent grafts anastomosed to the right coronary territories. When we compared the TTFM findings based on the feeding arteries, there were no significant differences between the groups of right gastroepiploic artery (n = 28) and ITA (n = 8) in the TTFM findings; diastolic dominant or balanced flow curve patterns (14/28 vs 7/8, p = 0.079), mean graft flow (24.1 ±11.8 mL/min vs 31.4 ± 14.5 mL/min, p = 0.153), pulsatility index (3.3 ± 1.5 vs 2.4 ± 1.5, p = 0.170), insufficiency ratio (5.3 ± 6.5% vs 2.3 ± 5.6%, p = 0.241), and fast Fourier transformation ratio (1.5 ± 0.9 vs 0.8 ± 0.7, p = 0.065).

Occluded Versus Competitive Grafts
There were no significant differences in any of the TTFM variables between the occluded and competitive grafts (Table 5). Although the fast Fourier transformation ratios of the occluded grafts were less than 1.0, those of the competitive grafts were widely distributed from 0.1 to 2.0 and there was no significant difference between the two groups.


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Table 5. Comparison of the Variables Between Occluded and Competitive Grafts
 
Predictability of the Graft Flow Abnormality
We derived the criteria to predict abnormal grafts (including occluded and competitive grafts) from four variables that could be displayed simultaneously on a real-time screen as follows: (1) systolic dominant or balanced pattern of the flow curve in the left coronary territories, systolic dominant pattern of the flow curve in the right coronary territories; (2) mean flow less than 15 mL/min; (3) pulsatility index greater than 3 in the left coronary territories, and greater than 5 in the right coronary territories; and (4) insufficiency ratio greater than 2%.

By using these criteria under a mean blood pressure of between 80 and 90 mm Hg, the sensitivity and specificity of TTFM to detect graft flow abnormality were 96.2% and 76.9%, respectively. The fast Fourier transformation ratio was not included in the criteria but was calculated and displayed on a different screen and used to differentiate between occluded and patent grafts.


    Comment
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 
This study revealed three main findings. First, the flow patterns of patent grafts as measured by TTFM were different between the right and left coronary territories. Second, the criteria to predict abnormal (occluded or competitive) grafts had to be applied differently between the right and left coronary systems. Third, when our criteria for abnormal grafts were applied, we were able to predict graft flow abnormality with a sensitivity of 96.2% and a specificity of 76.9%, respectively. The TTFM has become increasingly popular to detect intraoperative graft patency, particularly the OPCAB procedure, because TTFM is noninvasive, simple, quick, reproducible, and representative of the real flow within the graft [4–7]. However, graft assessment by TTFM has the potential shortcoming of being affected by dynamic variables such as blood pressure, heart rate, distal coronary resistance, graft diameter, and flow competition. Among the TTFM variables, mean graft flow is determined by the function of blood pressure and vascular resistance, and a low graft flow is considered to be associated with anastomotic error. However, it is difficult to interpret anastomotic quality as a single function of mean graft flow. It was demonstrated that mean graft flow did not decrease significantly until graft stenosis was greater than 75% [9]. The pulsatility index value is regarded as a good predictor of graft quality. The cutoff value of the pulsatility index to detect a patent graft has been suggested to be less than 3 [10] to 5 [3]. In these regards, more sophisticated analyses of the flow pattern are crucial in predicting intraoperative graft patency. Several studies have demonstrated the usefulness of intraoperative graft flow measurement using TTFM [2, 4, 11]. Abnormal grafts showed absent diastolic filling, extremely low mean flow, high pulsatility index value, and high insufficiency ratio. However, normal TTFM patterns of grafts have not been established. The intraoperative mean graft flow is reported to be lower in OPCAB compared with on-pump CABG, and higher in a saphenous vein graft compared with an arterial graft [7]. In this study, we analyzed the TTFM variables in patients undergoing OPCAB who received arterial grafts.

The hemodynamic characteristics in a patent graft are similar to those in the coronary circulation, and the flow curve pattern is mainly diastolic dominant with minimal systolic peaks during the isovolumetric ventricular contraction. Because the right coronary arteries are less compressed by ventricular contraction than the left coronary arteries, more blood flow takes place during systole and more of the systolic flow can be observed in a patent graft to the right coronary territories. Therefore, different flow patterns are to be expected between the right and left coronary territories. When we analyzed the TTFM variables of patent grafts in the OPCAB patients, the grafts anastomosed to the right coronary territories demonstrated the diastolic dominant pattern in less than one third of the patients, and lower mean flow and fast Fourier transformation ratio, and higher pulsatility index and insufficiency ratio than the left coronary artery grafts. This result suggested that the cutoff values to detect abnormal grafts should be different between the right and left coronary territories.

Although flow competition does not suggest anastomotic failure, we regard it as abnormal because flow competition does not allow effective distal coronary revascularization and it can cause graft failure [12]. In this study, none of the grafts showed anastomotic stenosis of more than 50% of the grafted coronary artery. Three grafts showed mild stenosis of less than 50% of the grafted coronary artery, and they were regarded as patent grafts. When we defined the abnormal graft as occluded or competitive graft by postoperative angiography, the TTFM parameters of those abnormal grafts were significantly different from those of normal grafts. None of the abnormal grafts demonstrated a diastolic dominant flow pattern, and the abnormal grafts showed significantly lower mean flow and fast Fourier transformation ratio and higher pulsatility index and insufficiency ratio than the patent grafts.

We selected a cutoff value for each variable with a wide range to obtain higher sensitivity, and applied a collective and stepwise interpretation of the variables to detect abnormal grafts (Fig 1). Sensitivity was considered more important than specificity in this study because a false-negative value should be as small as possible, even if some grafts with false-positive values underwent unnecessary revision.



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Fig 1. Flowmeter diagram to detect abnormal graft intraoperatively.

 
We derived the criteria to predict the abnormal grafts (including occluded and competitive grafts) from four variables (flow curve pattern, mean graft flow, pulsatility index, and insufficiency ratio) that could be displayed simultaneously on a real-time screen. By using these criteria under a mean blood pressure of between 80 and 90 mm Hg, the sensitivity and specificity of TTFM to detect graft flow abnormality were 96.2% and 76.9%, respectively. We found three false positive and two false negative grafts at retrospective data review. Two of the three false positive grafts showed a good visualization of graft-coronary artery anastomosis with early wash out of native coronary artery in the postoperative angiography. We believed that these grafts showed a mild form of flow competition and TTFM might be more sensitive than coronary angiography for detecting flow competition. Two false negative grafts showed high mean flow (19 mL/min) and low pulsatility index (2.9), respectively. However, the postoperative angiography showed flow competition in those two false negative cases.

Although the fast Fourier transformation ratio was reported to be useful to distinguish occluded from patent grafts in intraoperative flow measurement [6], it was not included in the criteria. The fast Fourier transformation ratio was not able to differentiate between competitive and normal grafts and had to be calculated by power spectral analysis of the flow waveform using fast Fourier transformation and displayed on a different screen, not on the real-time screen. In case of grafts with unclear results, we included the fast Fourier transformation ratio of less than 1 to differentiate the occluded grafts.

The differentiation between the competitive and occluded grafts could be performed by proximal snaring of native coronary artery in conjunction with the analysis of the TTFM variables [3]. However, the snaring of the proximal coronary artery was performed in selected cases because it can cause myocardial bleeding in areas lacking epicardial fat and aggravate the proximal coronary stenosis by the trauma created by the snare.

There are limitations to the present study that must be recognized. First, the present study did not include abnormal grafts with significant anastomotic stenosis of more than 75% in the analysis because none of the grafts showed anastomotic stenosis of more than 50% of the grafted coronary artery. Second, the present study excluded the sequential anastomoses and anastomoses distal to the sequential anastomoses, which made exclusion of 68 anastomoses of 185 anastomoses. Third, coronary angiography to evaluate the graft was performed postoperatively, not perioperatively. Some grafts may have occluded early postoperatively and other grafts may have shown abnormal flow patterns due to vasospasm occurring toward the end of surgery, which would affect the difference between the intraoperative TTFM findings and early postoperative angiography. In conclusion, we may predict graft abnormality with a high sensitivity and improve graft patency by revising the anastomosis intraoperatively under a collective interpretation of TTFM variables.


    References
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 

  1. Louagie YAG, Jamart J, Buche M, et al. Intraoperative hemodynamic assessment of gastroepiploic artery and saphenous vein bypass graftsa comparative study. J Thorac Cardiovasc Surg 1999;118:330-338.[Abstract/Free Full Text]
  2. Lin JC, Fisher DL, Szwerc MF, Magovern JA. Evaluation of graft patency during minimally invasive coronary artery bypass grafting with Doppler flow analysis Ann Thorac Surg 2000;70:1350-1354.[Abstract/Free Full Text]
  3. D’Ancona G, Karamanoukian HL, Ricci M, Schmid S, Bergsland J, Salerno TA. Graft revision after transit time flow measurement in off-pump coronary artery bypass grafting Eur J Cardiothorac Surg 2000;17:287-293.[Abstract/Free Full Text]
  4. Walpoth BH, Bosshard A, Genyk I, et al. Transit-time flow measurement for detection of early graft failure during myocardial revascularization Ann Thorac Surg 1998;66:1097-1100.[Abstract/Free Full Text]
  5. Beldi G, Bosshard A, Hess OM, Althaus U, Walpoth BH. Transit time flow measurementexperimental validation and comparison of three different systems. Ann Thorac Surg 2000;70:212-217.[Abstract/Free Full Text]
  6. Takami Y, Ina H. Relation of intraoperative flow measurement with postoperative quantitative angiographic assessment of coronary artery bypass grafting Ann Thorac Surg 2001;72:1270-1274.[Abstract/Free Full Text]
  7. Schmitz C, Ashraf O, Schiller W, et al. Transit time flow measurement in on-pump and off-pump coronary artery surgery J Thorac Cardiovasc Surg 2003;126:645-650.[Abstract/Free Full Text]
  8. Kim K-B, Kang CH, Chang W-I, et al. Off-pump coronary artery bypass with complete avoidance of aortic manipulation Ann Thorac Surg 2002;74:S1377-S1382.[Abstract/Free Full Text]
  9. Jaber SF, Koenig SC, BhaskerRao B, et al. Role of graft flow measurement technique in anastomotic quality assessment in minimally invasive CABG Ann Thorac Surg 1998;66:1087-1092.[Abstract/Free Full Text]
  10. Louagie YAG, Haxhe J-P, Jamart J, Buche M, Schoevaerdts J-C. Intraoperative assessment of coronary bypass grafts using a pulsed Doppler flowmeter Ann Thorac Surg 1994;58:742-749.[Abstract]
  11. Jakobsen HL, Kjaergard HK. Severe impairment of graft flow without electrocardiographic changes during coronary artery bypass grafting Scand Cardiovasc J 1998;32:1-3.
  12. Shimizu T, Hirayama T, Suesada H, Ikeda K, Ito S, Ishimaru S. Effect of flow competition on internal thoracic artery graftpostoperative velocimetric and angiographic study. J Thorac Cardiovasc Surg 2000;120:459-465.[Abstract/Free Full Text]



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