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Ann Thorac Surg 2005;80:2155-2161
© 2005 The Society of Thoracic Surgeons

Original article: Cardiovascular

Intraoperative Transit Time Flow Measurement: Off-Pump Versus On-Pump Coronary Artery Bypass

Wael Hassanein, MD a , Alexander A. Albert, MD a , * , Bert Arnrich, MS b , Joerg Walter, PhD b , Ina Carolin Ennker, MD a , Ulrich Rosendahl, MD a , Stefan Bauer, MD a , Juergen Ennker, MD a

a Clinic for Cardiothoracic Surgery, Heart Institute Lahr/Baden, Lahr, Germany
b Institute of Neuroinformatics, University of Bielefeld, Bielefeld, Germany

Accepted for publication March 30, 2005.

* Address correspondence to Dr Albert, Herzzentrum Lahr/Baden, 77933 Lahr, Germany (Email: alexander.albert{at}heart-lahr.com).


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 References
 
BACKGROUND: Off-pump coronary artery bypass grafting (OPCAB) has attracted increasing attention. Performing the anastomosis off-pump is technically more demanding. The objective of the study is to assess the quality of anastomosis in OPCAB in comparison with conventional on-pump coronary artery bypass grafting using the transit time flow measurement.

METHODS: Four hundred forty-five patients operated on using OPCAB technique were included in the study. For each patient in this group a similar patient from the on-pump coronary artery bypass grafting population was selected according to the number of grafts, bypass material, and target coronary arteries. The mean flow and the pulsatile index were measured in every bypass graft in both groups.

RESULTS: The average pulsatile index in OPCAB was 2.09 ± 1.03 (mean flow, 39 ± 22.63 mL/min), whereas with on-pump coronary artery bypass grafting it was 1.9 ± 0.98 (mean flow, 44.19 ± 23.58 mL/min); p = 0.005. Subgroup analysis showed significantly lower mean flows and higher pulsatile index with OPCAB in grafts to the obtuse marginal, diagonal, and right coronary artery, but not to the left anterior descending territory.

CONCLUSIONS: The quality of the anastomosis performed using the OPCAB technique might be jeopardized by less accessibility as in the case of lateral and posterior wall coronary arteries. Techniques to optimize the accessibility of the coronary artery like combining sling support with cup stabilizers, together with systematic training, should be strongly considered in OPCAB. Whenever there is good accessibility of the coronary artery as in the case of the left anterior descending, the anastomosis performed under OPCAB has a quality as good as that performed using the conventional technique.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 References
 
Coronary artery bypass grafting (CABG) is the current surgical benchmark for coronary revascularization. Cardiopulmonary bypass (CPB) and cardioplegic cardiac arrest have been used routinely in CABG in the last three decades. Continued pharmacologic and mechanical innovations in CPB and improved preservation of cardiac function during CABG, together with bloodless and accessible coronary artery sites for anastomosis, have made this procedure safe and common [1, 2].

Nevertheless, CPB has long been claimed to be responsible for systemic inflammation and multiple organ dysfunction after CABG [3]. Because of these potential hazards, off-pump coronary artery bypass grafting (OPCAB) has attracted considerable attention in the past few years. The fact that performing the anastomosis during OPCAB is technically more demanding has raised interests and concerns about the quality of anastomosis.

Transit time flow measurement has recently been introduced as an effective and reliable method for intraoperative evaluation of coronary artery grafts. This technology allows for flow determination independently of vessel size, shape, and Doppler angle used [4, 5]. The objective of this study was to assess the quality of anastomosis in OPCAB in comparison with conventional on-pump CABG using the transit time flow measurement.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 References
 
Off-pump CABG has been performed regularly in our institute since 1996, whereas transit time flow measurement has been used routinely in all cases of CABG since the end of 1998. From January 1999 to August 2003, 525 patients underwent isolated CABG procedures using the OPCAB technique in our institute. Patients who got sequential grafts, emergency cases, and patients who had had previous open heart operations were excluded from the study. That left us with 468 patients. Nine patients had grafts needing revision of the anastomosis (3 patients with left anterior descending coronary artery [LAD] grafts, 2 with right coronary artery [RCA], 1 with diagonal, 3 with obtuse marginal [OM]), and they were excluded from the study. Distal anastomosis was repeated only after exclusion of any problem in the proximal anastomosis or in the bypass material. Fourteen patients were converted intraoperatively to the conventional technique using the heart-lung machine, and they were also excluded from the study.

The remaining 445 patients constitute the first group of the study. Using our institutional database [6], a second group of patients was selected from the patients operated on electively for isolated CABG during the same period using the heart-lung machine, so that each patient of the off-pump group has a corresponding patient from the on-pump group with the same number of grafts, bypass material, and target coronary arteries, without having sequential anastomoses or previous cardiac operations. Five surgeons, all of them have long experience with both techniques, performed all the operations in both groups. For analysis of the influence of the target coronary vessels, each group was further subdivided into four subgroups intercrossing with each other: patients receiving LAD graft (LAD subgroup), diagonal (D subgroup), OM graft (OM subgroup), and RCA graft (RCA subgroup).

All patients signed an informed consent for the operation and for quality-control measures including flow measurements, and received a copy of flow measurements after discharge. A copy of the flow measurement was also sent to the referring doctor.

Surgical Technique—Off-Pump Coronary Artery Bypass Grafting
A median sternotomy was used in all cases. Internal mammary artery, saphenous vein, or radial artery grafts were harvested using standard techniques. Intravenous heparin (300 IU/kg) was given to maintain activated clotting time greater than 400 seconds.

Exposure of the different coronary branches was based on a single sling anchored with a tourniquet in the oblique sinus of the pericardium [7, 8]. Stabilization of the anastomotic region during revascularization was accomplished with the assistance of either Octopus (Medtronic Inc, Minneapolis, MN) or the CTS II (Cardiovascular Systems, Cupertino, CA) or Genzyme Immobilizer (Genzyme, Cambridge, MA). Visibility was aided by carbon dioxide–water spray, and hemostasis was obtained by using a soft plastic flow-shunt passed into the coronary arteriotomy. Occlusion of the coronary vessels was avoided in nearly all patients. Left internal mammary artery to LAD anastomosis was always performed first, followed by other distal anastomoses, and lastly the proximal ones. Proximal anastomoses were sewn to the aorta under a single partial occlusion clamping time. In cases in which a segment of the internal mammary artery (right or left) was used as a free graft to the diagonal or OM artery, the proximal end was sewn to left internal mammary artery. After all anastomoses were completed, heparin was neutralized with protamine sulfate (0.5 mg per 100 units of heparin).

Surgical Technique—Cardiopulmonary Bypass
Cardiopulmonary bypass was performed with standard equipment and techniques under systemic normothermia, and cardiac arrest was achieved with cold hyperkalemic blood. Apart from performing the proximal anastomoses with the aorta totally clamped, the anastomotic technique was the same as in OPCAB.

Transit Time Flow Measurement
Transit time flow was measured in both groups in all bypass grafts before reversal of heparin. The same device was used for measurement in all cases in both groups; Transonic Flow Measurement HT311 (Transonic Systems Inc, Ithaca, NY), with probes measuring between 2 and 4 mm in size to fit perfectly around the graft.

Before making any measurement, adequate systemic blood pressure was maintained, traction on the pericardium was released, and the stabilizer was removed from the pericardial surface to allow the heart to return to its anatomic position. Great care was taken to avoid spasm of arterial grafts caused by manipulations. In patients with borderline values, flow measurement was repeated once or twice including at least one time just before sternal closure, and the best value was recorded. The mean flow in milliliters per minute was measured, together with the maximum and minimum flows. By dividing the difference between the maximum and minimum flow by the value of the mean flow, the pulsatile index (PI) is obtained. Figure 1 shows the flow tracing in different PI values. Notice the abrupt descent of the tracing in diastole and low diastolic flow (absence of diastolic pattern) in Figure 1C with high PI.



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  		Fig 1. (A) Flow measurement tracing in a graft with pulsatile index (PI) of 1.4. (B) Flow measurement tracing in a graft with PI of 2.6. (C) Flow measurement tracing in a graft with PI of 8.1. (CX = graft to a branch from the circumflex [obtuse marginal]; LIMA = left internal mammary artery; RIVA = ramus interventricularis anterior; RIVP = ramus interventricularis posterior.)

 
Unlike the mean flow, which is very dependent on the size and quality of the revascularized coronary artery, the PI, expressed as an absolute number, is a good indicator of the flow pattern and, consequently, of the quality of the anastomosis. The possibility of a technical error in the anastomosis increases for PI values higher than 5 [4]. However, some anastomoses with PI higher than 5 in the patients included in the study were not repeated according to the surgeon's judgment at the time of the operation, eg, no technical error is evident, no electrocardiographic changes or hemodynamic instability. Patients who had any anastomosis repeated were excluded from the study.

Statistical Analysis
The PIs and mean flows were expressed as mean ± standard deviation. To compare the on-pump group and its subgroups (LAD, diagonal, OM, and RCA) with the off-pump group and its corresponding subgroups, unpaired Student's t test and Kolmogorov-Smirnov tests were used. Because both groups were well matched and no important differences were found between them regarding the demographic data and preoperative risk factors, no logistic regression analysis was needed. All statistics were obtained by version 5 of the JMP Software (SAS Institute Inc, Cary, NC).


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 References
 
The two groups were similar in terms of demographic characteristics. The mean age in the OPCAB group was 65.48 ± 10.24 years versus 64.34 ± 9.5 years in the on-pump group (p = 0.087). There were 106 women in the OPCAB group (23.85%) versus 109 (24.5%) in the on-pump group (p = 0.184). The preoperative risk factors were also similar in both groups (EUROscore 3.38 ± 2.45 in the OPCAB group versus 3.15 ± 2.33 in the on-pump group; p = 0.184).

The total number of bypasses in each group was 845 bypasses (1.9 ± 0.79 bypass/patient). The bypass material used was identical in both groups, left internal thoracic artery (472 bypasses), great saphenous vein (256 bypasses), radial artery (97 bypasses), and right internal thoracic artery (20 bypasses). Also the target coronary arteries are equal in both groups: LAD, 429 bypasses; diagonal, 143 bypasses; OM, 129 bypasses; and RCA, 143 bypasses. In each group 152 patients received only one bypass (34%), 197 patients received two bypasses (44%), 85 patients received three bypasses (19%), and 11 patients received four bypasses (2%).

The postoperative 30-day mortality and postoperative myocardial infarction were similar in both groups (5 mortalities [1.1%] and 7 infarctions [1.6%] in each group).

There were lower average flows and higher PIs in OPCAB patients. The average mean flow in all grafts in the OPCAB group was 39.39 ± 22.63 mL/min, whereas in the on-pump group it was 44.19 ± 23.58 mL/min (p = 0.002); the average PI in the OPCAB group was 2.09 ± 1.03, whereas in the on-pump group it was 1.9 ± 0.98 (p = 0.005).

As shown in Table 1, apart from the LAD territory, there were significantly higher mean flows and lower PIs in grafts performed in the conventional way in comparison with those performed under OPCAB.


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  		Table 1. Mean Flow (mL/min) and Pulsatile Index in Different Coronary Territories
 
The cumulative distribution plot of PI values shows exactly the same curves for both groups in LAD territory, whereas cumulative distribution of PI values for OM, RCA, diagonal grafts identified more patients with higher PIs in the OPCAB groups (Fig 2). In addition to the comparison using Student's t test (Table 1), the differences in PIs between the two groups was analyzed using the Kolmogorov-Smirnov test. This analysis revealed no significant difference in LAD territory (p = 0.773), whereas the PI was significantly higher in cases of OPCAB in diagonal (p = 0.0177), OM (p = 0.0098), and RCA (p = 0.005).



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  		Fig 2. Cumulative distribution of pulsatile index (PI) in different coronary territories. (CPB = cardiopulmonary bypass; D = diagonal; LAD = left anterior descending; OM = obtuse marginal; OPCAB = off-pump coronary artery bypass grafting; RCA = right coronary artery.)

 
Bypasses with PI more than 5 were more numerous in the OPCAB group. The difference was most evident in case of OM (11 bypasses in the OPCAB group and 2 bypasses in the CPB group; p = 0.022). The difference was clear in the diagonal artery and RCA groups, although it did not reach a statistically significant value. In bypasses to the diagonal artery, there were 5 bypasses with PI more than 5 in the OPCAB group and 1 bypass in the CPB group (p = 0.217). In RCA bypasses, there were 7 in the OPCAB group and 3 in the CPB group (p = 0.341). On the other hand, in the LAD bypasses, there were 7 bypasses in the OPCAB group and 9 bypasses in the CPB group with PI more than 5 (p = 0.626).

The follow-up period for OPCAB patients ranged from 1 to 74 months, with a mean of 10.73 ± 15.2 months. For CPB, the follow-up period ranged from 1 to 67 months, with a mean of 9.74 ± 12.5 months. The difference in follow-up periods was not statistically significant (p = 0.86).

During the follow-up period, there were 15 mortalities in the OPCAB group and 13 mortalities in the CPB group (p = 0.79). Because the number of events is relatively small, no correlation with intraoperative flow measurements could be proved.

During the follow-up period, 58 patients from the OPCAB group and 49 patients from the CPB group experienced anginal pain at least once (p = 0.818). An interesting finding was the significantly lower intraoperative flow in LAD grafts in patients who later on experienced anginal pain (42.81 ± 26 mL/min in patients without angina versus 37.17 ± 21.1 mL/min in patients with angina; p = 0.015).

Coronary angiography was indicated in 21 patients (12 patients from the OPCAB group and 9 patients from the CPB group). The catheterization was performed 18.7 ± 17.1 months after the operation in the OPCAB group (range, 1 to 48 months) and 23 ± 18.5 months in the CPB group (range, 6 to 49 months; p = 0.477). The occluded to patent grafts in the OPCAB and CPB groups in different coronary territories were as follows: LAD, 4 to 8, 1 to 8 (p = 0.237); diagonal, 1 to 1, 3 to 1 (p = 0.54); OM, 6 to 1, 0 to 2 (p = 0.023); RCA, 2 to 1, 2 to 1 (p = 1). The number of events in each coronary territory was too small to prove a correlation with intraoperative flow measurements.


   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
References
 
Since it was launched by Kolesov [9] in the 1960s, the off-pump approach has always been present. In spite of the widespread clinical success and reliability of CPB, extracorporeal circuits expose blood to shear stresses and contact with large areas of synthetic surfaces, which may contribute to the development of generalized inflammatory response and organ dysfunction [10–12].

Because of these hazards OPCAB procedures have gained increasing popularity during the last few years. Despite the growing use of cardiac stabilizers, construction of the anastomosis on the beating heart is technically demanding. This has raised concerns about technical limitations of this technique and the quality of the anastomosis performed using it.

Presently, transit time flow probes are the most commonly used devices for assessment of anastomotic quality, as they are easy to use intraoperatively and they have proven high reliability and accuracy [13–18]. In addition, a correlation has been found between the intraoperative flow in saphenous vein grafts and early occlusion [19]. Also a correlation has been found between intraoperative transit time flow measurement and postoperative magnetic resonance imaging findings of the internal mammary artery grafts [15]. Even if the flow value is influenced by other variables, including the size of the graft and quality of the coronary artery distal territory, PI value is, per se, very suggestive of the actual status of the anastomosis [4]. This corresponds with our findings, which show a complete shift of the cumulative distribution function in the OM grafts with OPCAB toward higher PIs, suggesting an impact of anastomosis quality even in low PI values.

Nevertheless, an interesting study concluded that flow tracing and mean flow can reliably detect only nearly occluded grafts [20]. The authors reached this conclusion by creating variable degrees of stenosis in left internal mammary artery to LAD anastomoses in 10 dog models and sending a questionnaire to 19 surgeons with the mean flow and flow tracings, asking them whether they would repeat the anastomosis. All surgeons agreed to redo only anastomoses with more than 90% stenosis with variable acceptance rates for other degrees of stenosis. In view of the basic physical law that the flow is inversely proportional to the resistance in a linear way, the results of this questionnaire are not to be considered a contradiction with the findings of the above-mentioned studies and the logical assumption that the less resistant the anastomosis, the better will be the flow and PI.

Although most studies published about OPCAB are mainly demonstrating the clinical outcome, only one study has yet compared the quality of anastomoses performed in OPCAB with those performed in conventional CABG using the intraoperative flow measurements [21]. In this study significantly lower flows have been found in all coronary territories in grafts performed using OPCAB in comparison with those performed conventionally. However, PI was not measured in this study. The explanation of this difference in flow in this study was postulated that in cases of on-pump and cardioplegic arrest there is myocardial ischemia causing coronary vasodilatation, whereas in cases of OPCAB vasoconstrictors are commonly given, causing coronary vasoconstriction and consequently less flow. In view of our results, we disagree with this explanation. First, we did not use vasoconstrictor drugs in OPCAB operations in higher doses than in CPB cases. Also, in our study there was no difference in flow in the LAD territory although the differences were significant in other territories. In addition, apart from the LAD, there were significant differences in PI between our two groups, a factor, to some extent, not dependent on coronary vessel size. We have also found significant differences between the two groups in flows in both radial artery (highly sensitive to vasoactive drugs) and vein (less sensitive) in OM anastomoses.

One study has found significantly less patency of saphenous vein grafts 1 year after OPCAB in comparison with conventional CABG, an evidence of the lower quality of anastomoses performed in OPCAB [22]. The same study did not find a significant difference between OPCAB and conventional CABG in patency of the left internal mammary artery 1 year after the operation. Considering that the left internal mammary artery is mainly used in LAD territory, whereas the saphenous vein is mainly used in other territories, the results of this study are in line with our results. The lower patency of anastomoses performed using the OPCAB technique was reproduced in a recent prospective randomized study [23].

Studies demonstrating good graft patency after OPCAB have performed the angiography a few days after the operation, and they did not compare the patency rate after OPCAB with that after conventional CABG [24, 25]. Long-term patency has been less studied. However, one study has found significantly less graft patency and a twofold increase in cardiac reintervention rate during a 7-year period with off-pump in comparison with on-pump CABG [26]. However, the patients included in this study have been operated on before the era of modern cardiac stabilizers.

In our study, despite the excellent clinical outcome in OPCAB patients, significantly lower flows and higher pulsatile indices were found in anastomoses performed in OPCAB in comparison with conventional CABG. Although these differences are not found in LAD territory, they are most significant in circumflex territory. This was reflected in the data obtained from the coronary angiography performed during the follow-up period. More grafts performed under OPCAB were occluded than those performed under CPB. This difference reached a statistically significant level in OM territory.

Accessibility to the circumflex territory in OPCAB was less than optimal in many situations. With less accessibility, uncertainty is increased and anastomotic quality is reduced. We believe that the less accessibility and the subsequent difficulty play an important role in limiting the acceptance and spread of OPCAB among cardiac surgeons. The use of the deep pericardial stitch and sling support alone did not provide optimal access to the posterolateral coronaries [7, 8]. A remarkable development in OPCAB surgery is the introduction of cup stabilizers, which markedly improved the exposure of posterior coronary arteries. Unfortunately, we used them rarely at the time of the study.

In addition to accessibility, an important factor in achieving an anastomotic quality as good as that performed using the CPB is the way of acquiring the skills needed to perform the anastomoses on the beating heart. Reengineering of the training program and the performance of an adequate number of anastomoses in a stress-free environment using nonliving material can play a fundamental role in performing a high-quality anastomosis using the OPCAB technique [27, 28]. Consequently, this can promote the acceptance of OPCAB.

The clear scientific importance of our study is that we could prove that whenever there is good accessibility of the coronary artery as in the case of the LAD, the anastomosis performed under OPCAB has a quality as good as that performed using the conventional technique. Whenever the equipment and skills needed to expose the target vessels and perform the anastomosis are acquired, complete myocardial revascularization with high quality can be achieved using the OPCAB technique.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 

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Wael Hassanein
Alexander A. Albert
Ina Carolin Ennker
Ulrich Rosendahl
Stefan Bauer
Juergen Ennker
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