Ann Thorac Surg 2001;72:S2253-S2258
© 2001 The Society of Thoracic Surgeons
a Peachtree Cardiovascular & Thoracic Surgeons, Atlanta, Georgia, USA
* Address reprint requests to Dr Wolfe, Peachtree Cardiovascular & Thoracic Surgeons, 5669 Peachtree Dunwoody Road, Suite 3890, Atlanta, GA 30342, USA
Presented at Monitoring and Improving Patient Safety During and Following Cardiac Surgery, San Diego, CA, May 5, 2001.
The outcome of coronary artery bypass grafting procedures is highly dependent on the technical adequacy of the distal anastomosis. Various methodologies, including flow measurement and imaging techniques, have been used by the cardiothoracic surgeon to assess the adequacy of the distal anastomosis. The limitations of these techniques outweigh their advantages and limit their widespread clinical applicability. Recent improvements in the technique for online measurement of regional myocardial pH provide a promising new metabolic approach to assessing the adequacy of the distal anastomosis in cardiac surgery.
Coronary artery bypass grafting (CABG) continues to be one of the most frequently performed surgical procedures in the United States. The outcome of this operation is highly dependent on the technical adequacy of the vascular anastomoses performed during the operation. The evolution of this procedure continues toward a less invasive approach, mainly to avoid mechanical circulatory support and to achieve better cosmetic results. Less invasive procedures include a left minithoracotomy approach, without cardiopulmonary bypass, either for isolated anterior wall vessel disease (minimally invasive direct coronary artery bypass [MIDCAB]) or as a part of a hybrid procedure. The desire to achieve a more complete surgical revascularization has led to the development of off-pump coronary bypass grafting (OPCAB) techniques through a full midsternotomy. Despite recent advances in instrumentation that allow adequate stabilization of the beating heart, technical failure at the anastomotic site is known to occur and may be both underrecognized and underreported. In one recent series of patients undergoing immediate angiography after MIDCAB, investigators reported a 9% incidence of "less than perfect" graft patency . The purpose of this communication is to provide a critical review of the various methodologies that have been used to date to assess the intraoperative adequacy of the distal coronary anastomosis in both "on-pump" and "off-pump" operations.
Electromagnetic versus Doppler techniques
The earliest reports of intraoperative flow measurements of coronary bypass conduits used an electromagnetic flow (EMF) probe. These initial studies, while indirectly assessing the adequacy of the coronary anastomosis, were designed to assess the predictive value of bypass graft flow measurements. Nevertheless, they showed conflicting results. Several investigators reported that intraoperative EMF measurements in saphenous vein grafts (SVG) were an important determinant of postoperative angiographic patency . Others reported that intraoperative mean EMF values were of no predictive value [6, 7]. Later studies were designed not to specifically assess anastomotic integrity but, rather, to ascertain whether the internal mammary artery (IMA) was a suitable bypass conduit under most clinical conditions. Louagie and coworkers performed more than 600 EMF measurements in 262 patients undergoing CABG . They reported flow rates ranging from 34 to 50 mL/min in IMA grafts and from 61 to 117 mL/min in SVG supplying the same vascular bed. They concluded that resistance of both the outflow bed as well as the diameter of the conduit itself influenced flow in the grafted IMA. The technical integrity of the anastomosis did not appear to correlate with flow. Canver and coworkers  measured EMF and Doppler ultrasonic flow rates in both IMA and SVG conduits in 66 patients undergoing elective CABG. The EMF measurements were consistently higher than the ultrasonic flows in all conduits. No intraoperative graft revisions were necessary, and there was no correlation between measured flow rates and clinical outcomes.
More recent studies have used pulsed Doppler ultrasound to measure graft flow velocity, as well as internal vessel diameter, thereby allowing for derived quantitative flow measurements. Louagie and colleagues  performed pulsed Doppler flow measurements on more than 900 bypass grafts in 352 consecutive patients undergoing CABG and found good correlation between Doppler and EMF measurements. They also measured both flow velocity and resistance of the graft and coronary bed expressed as a pulsatility index. The pulsatility index is a dimensionless variable of resistance derived from a comparison of the maximum, minimum, and mean Doppler transmission frequencies . Technical errors were identified in seven grafts (2%) by abnormal velocity waveform configuration, low diastolic flow and velocity, and high pulsatility index. After graft revision, the flow rates and waveform configuration normalized consistent with improved blood flow hemodynamics. In a later follow-up study, Louagie and coworkers  reported on 85 patients undergoing late angiographic evaluation for recurrent anginal symptoms. This study provided for a visual assessment of 214 grafts (89 arterial and 125 venous) that had been measured by pulsed Doppler flowmeter at initial surgery. In the 168 grafts found to be intact, mean flow rate measured intraoperatively was 60 mL/min and the resistance was 1.8 peripheral resistance units. In contrast, mean intraoperative flow was only 36 mL/min and resistance averaged 5.9 peripheral resistance units in the 25 grafts found to be occluded. Univariate analysis suggested that reduced flow, reduced velocity, increased resistance, and increased pulsatility index were all significantly associated with a higher occlusion rate. Multivariate analysis, however, selected increased resistance as the only independent variable associated with postoperative occlusion. The etiology of this resistance, in terms of anastomotic adequacy versus distal runoff bed, was unclear. The addition of color imaging to pulsed Doppler ultrasonography allowed a more visual assessment of graft patency. Oda and colleagues  reported on 15 patients undergoing left internal mammary artery to left anterior descending coronary artery (LIMA-to-LAD) grafting who were assessed with a microprobe Doppler device allowing both imaging and flow measurements. Their results confirmed similar flow rates in the range of 50 mL/min and further suggested that patency could be easily confirmed by color Doppler imaging of the anastomosis.
Transit time flow
Another modification of ultrasonography, known as transit time flow measurement, has been used more recently during CABG procedures. The transit time methodology measures volume flow by using two piezoelectric crystals transmitting ultrasound to a reflector on the opposite side of the vessel and calculating the differences between transit times upstream and downstream . Using three different commercially available systems in an experimental blood flow model, Beldi and associates  reported high correlation between transit time flow and true flow measurements using both arterial and venous conduits. Walpoth and colleagues  used this methodology to measure LIMA-to-LAD bypass graft flow in 46 patients undergoing conventional CABG surgery. The LIMA graft flow was normal (>20 mL/min) in 43 patients; however, in 3 patients, a low flow (<0.5 mL/min) was identified in the LIMA graft along with significantly elevated vascular resistance and pulsatility index. Evaluation of these three grafts revealed a distal LIMA dissection in 1 patient, an obstructing anastomotic flap in another, and an intramural hematoma in the third patient. Interestingly, in only 1 of these 3 patients were transient electrocardiographic changes and poor contractility of the anterior wall of the left ventricle observed. After graft revision, flow rates and resistance measurements returned to control values. More recently, DAncoma and colleagues  performed transit time flow measurements on 409 patients undergoing OPCAB. Of the 1,145 grafts, 37 (3.2%) were revised in 33 patients (7.6%). Among the 34 grafts revised secondary to low flow, abnormal flow curve patterns, and high pulsatility index, all flow values and patterns improved after revision consistent with the various technical anastomotic problems identified. In the 3 grafts revised for low flow rates (<7 mL/min) despite normal flow patterns, there were no technical problems identified, and both flow values and curve patterns remained unchanged after revision. These investigators concluded that all grafts demonstrating both low flow values and high pulsatility index (ie, high resistance) should be revised.
In a canine model of off-pump IMA to LAD anastomosis, Jaber and colleagues  measured transit time flow rates and flow tracing morphology under various degrees of stenosis and concluded that although useful, surgeons should be cautious in making intraoperative decisions based solely on these variables. Specifically, they reported that mean graft flow differences and graft flow morphologies were indistinguishable in anastomoses with mild (<25%) to moderately severe (<75%) stenoses. Differences became detectable only in anastomoses with angiographically severe (>75%) stenoses. They concluded that transit timederived flow measurements correlated poorly with anastomotic quality and, thus, limited clinical usefulness.
Calibrated pump flow
Sharma and coworkers  described a simple technique in which the cardioplegic solution was pumped through the proximal end of the graft at a mean pressure of 100 mm Hg after the completion of the distal anastomosis (Fig 1). The flow through the graft was calculated from the revolutions per minute of the precalibrated roller pump head. These investigators obtained more consistent and reproducible results with this technique than with EMF meters and showed that the measurements obtained intraoperatively correlated very well with the patency of the saphenous vein grafts at 1 year postoperatively.
Thermal coronary angiography
Another technique developed to noninvasively assess intraoperative anastomotic patency during CABG operations is thermal coronary angiography (TCA). This technique uses an infrared camera to detect temperature differences between graft injectant and the adjacent epimyocardium, resulting in a "heat picture" that outlines the anastomosis. In 1989, Mohr and colleagues  first reported the use of TCA in 50 patients undergoing routine CABG operations. The 173 angiograms obtained provided an image of the graft, anastomosis, and native coronary stenoses. Unsuspected stenoses were detected at the distal anastomotic site in four grafts. In 10 grafts, the angiograms were obscured by excess epicardial fat. In a more recent study, Falk and colleagues  used TCA to evaluate 693 SVG and 370 IMA grafts in 370 patients undergoing routine CABG. The TCA technique revealed 99% intraoperative patency in SVG grafts. In all, 19 (5.3%) IMA graft occlusions were identified and revised. Similar observations have been reported during both MIBCAB and OPCAB procedures as well using an endoscopic TCA camera .
Coronary angiographythe "gold standard"
Angiography to assess coronary anastomotic patency after MIDCAB historically has been performed in a fixed standard cardiac catheterization laboratory either immediately after  or during the first several days postoperatively . Goldstein and colleagues  demonstrated the feasibility of using a portable digital fluoroscopic system to obtain intraoperative coronary angiograms on a series of 26 patients undergoing MIDCAB. Angiography demonstrated technically unsuspected and clinically silent fixed stenoses in 11 patients (42%), 6 of which were anastomotic problems with the remainder due either to kinking or to native vessel snare injury. In 9 of these 11 patients, the fixed stenoses were sufficiently severe to require intraoperative intervention by either surgical revision (5 patients) or graft angioplasty (4 patients). Nine patients had angiographically significant vasospasm that responded promptly to vasodilators.
Elbeery and coworkers  reported a series a 50 patients undergoing MIDCAB who were evaluated by both intraoperative angiography and concomitant Doppler ultrasound. Clinically unsuspected yet significant anastomotic problems were identified and corrected in 4 (8%) patients. The salutary effect of concomitant Doppler assessment was questionable: namely, three grafts found to be widely patent by angiography had either poor or questionable Doppler signals, and 4 patients with occluded grafts by angiography had persistent Doppler flow signals suggesting a patent graft. Despite 100% graft occlusion, in no case was the Doppler flow signal consistently zero.
Recent improvements in the technique for the online measurement of regional myocardial tissue pH provide a promising new metabolic approach to the assessment of the adequacy of distal coronary artery graft anastomoses in cardiac surgery. The technique, originally described by Khuri and associates , uses a tissue pH electrode (combined with thermister) that is inserted into segments of the left ventricular wall subtended by the coronary arteries being revascularized. Interruption of blood flow during the construction of the distal anastomosis leads to progressive regional myocardial tissue acidosis as a result of both increased anaerobic metabolism and decreased tissue washout of the hydrogen ion . Reversal of acidosis with the establishment of flow through the graft indicates adequate revascularization (Fig 2). Failure of the newly constructed graft to reverse regional myocardial acidosis after reperfusion indicates either a technically inadequate anastomosis (Fig 3), or a limited distal runoff caused by severe coronary artery disease (Fig 4).
This review documents the evolution of various methodologies used by the cardiothoracic surgeon to assess the adequacy of the distal coronary anastomosis. Each new methodology has evolved, in part, to address the limitations of earlier techniques. For example, electromagnetic flow probes, although highly accurate when used in the experimental laboratory, have several limitations that limit their widespread applicability in clinical practice. Accurate measurements require precalibration, constant zeroing, segmental exposure of the vessel wall, and a range of sterilized probes of varying diameters to ensure a snug fit around the vessel wall. Electromagnetic flowmeters developed for clinical use have, in part, sacrificed accuracy for the sake of user-friendliness. The Doppler flowmeter addresses several of the shortcomings of the electromagnetic flowmeters, in that only one probe is required and skeletonization of the vessel is not necessary for application of the probe; however, it remains essentially a velocimeter and does not provide a measurement of vessel diameter or quantitative volume flow. Pulsed Doppler technology provides a determination of internal vessel diameter and thus allows for simultaneous measurement of flow, velocity, resistance, and pulsatility index in association with analysis of phasic flow patterns. The accuracy of this methodology, however, decreases significantly in vessels with an internal diameter of less than 2.0 mm [32, 33]. Transit time flow measurement represents a further improvement in that measured flow is independent of vessel size. Correct interpretation of flow findings may prove difficult, however, unless flow curves, flow values, and pulsatility index are evaluated simultaneously . In addition, transit time flow measurements should be obtained both with and without a proximal coronary snare, thereby introducing the possibility of iatrogenic native vessel injury. Computer simulation modeling of an IMA to LAD bypass graft suggests that IMA flow patterns are highly dependant on the degree of LAD stenosis, the integrity of the anastomosis, and the resistance of the distal runoff bed as related to coronary blood flow demands . These observations suggest that occlusion of the distal LAD (beyond the anastomosis) to induce a reactive hyperemia might also be necessary to ensure an adequate anastomosis, again increasing the number of required measurements and the possibility of iatrogenic vessel trauma. Clearly the predictive value of quantitative flow rates and flow curves obtained by transit time measurement ultimately may be limited by the inability to control for parallel flow pathways and intrinsic myocardial flow demands.
A simple technique, which also employs flow measurement in the assessment of the adequacy of the distal anastomoses, is that described by Sharma and associates  and illustrated here in Figure 1. By counting the revolutions per minute of a precalibrated pump, this technique avoids the need for and the limitations of other techniques that require various types of flowmeters. It is also one of the few techniques in which the intraoperative flow measurements have been shown to predict 1-year graft patency. The advantage of this technique is that it allows the revision of the anastomosis (if deemed necessary based on poor flow) to be performed while the aorta is still clamped. Its disadvantage is a lack of applicability to in situ arterial grafts such as the left internal mammary artery graft.
Other techniques that are not based on direct measurement of aortocoronary graft flow, namely thermal imaging and intraoperative angiography, have both found limited clinical applicability as evidenced by the scarcity of reports in the literature. Intraoperative evaluation of thermal angiograms appears highly subjective and the frequent presence of significant epicardial fat in fact markedly limits the reliability of the technique. Intraoperative angiography, although highly accurate as the obvious gold standard, necessitates cannulation of a peripheral artery and requires an operating room equipped with high quality fluoroscopic imaging capabilities. Again, few such reports in the literature suggest that most cardiothoracic surgeons are not inclined to achieve this level of accuracy. The predicted evolution of the cardiac surgical suite towards a more comprehensive multidisciplinary diagnostic imaging suite might obviate current limitations with this methodology.
A review of the current literature clearly suggests that a routine objective analysis of the adequacy of the distal coronary anastomosis is often not part of the intraoperative assessment after surgical revascularization. There are multiple reports detailing the safety and efficacy of OPCAB procedures in which there is no mention of any technique used to assess the technical precision of the distal coronary anastomosis . Indeed, in a recent survey of 162 practicing cardiothoracic surgeons detailing individual experiences with minimally invasive coronary bypass grafting, 64% of respondents indicated that no routine evaluation of anastomotic patency was performed. Of those surgeons who did use an objective technique, 9% performed postoperative angiography, 20% used Doppler flow evaluation, and 7% used both techniques . Anecdotal reports from senior cardiothoracic surgeons in both academic and community hospitals suggest that, in the absence of concomitant electrocardiographic or hemodynamic abnormalities, insertion of a Parsonnet probe through the partially completed distal anastomosis is the most common "objective" assessment of technical adequacy in most on-pump, MIDCAB, and OPCAB patients.
The diversity and limitations of the techniques for assessment of the adequacy of the distal anastomoses, coupled with the scarcity of proper studies that correlate these techniques to long-term graft patency and other outcomes, account for the lack of consensus among cardiac surgeons in regard to the utility of assessing the adequacy of the distal anastomoses in their current practice. They also provide an impetus for continued research and development in this field. A promising new technology is the metabolic assessment of the adequacy of regional myocardial revascularization using a tissue pH electrode, as described earlier here and illustrated in Figures 2 through 4. The ability of the myocardial pH electrode to detect, in a quantitative manner, tissue ischemia evidenced by accumulation of the hydrogen ion has been validated in numerous experimental and clinical studies . The electrode has also been shown to reliably detect, during cardiopulmonary bypass procedures, the physiologic significance of coronary artery stenoses . Therefore, the extent of washout of the hydrogen ion and reversal of acidosis in myocardial segments subtended by newly constructed grafts is a good quantitative indicator of the adequacy of revascularization. Although this metabolic technique has not been used to date during OPCAB procedures, it provides the basis for a potentially promising intraoperative assessment tool in both "on-pump" and "off-pump" operations, when it becomes commercially available in the near future.
To ensure our patients safety as well as improve the long-term outcome of surgical revascularization procedures, there needs to be a continued critical evaluation of all current and future techniques designed to assess the technical adequacy of the distal coronary anastomosis.
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