Intraoperative Fluorescence Imaging After Transit-Time Flow Measurement During Coronary Artery Bypass Grafting

Kuroyanagi, Satoshi MD; Asai, Tohru MD, PhD; Suzuki, Tomoaki MD, PhD

Innovations: Technology & Techniques in Cardiothoracic & Vascular Surgery:
doi: 10.1097/IMI.0b013e318281260c
Original Articles

Objective: This report describes the complementary use of transit-time flow measurement (TTFM) and intraoperative fluorescence imaging (IFI) during off-pump coronary artery bypass grafting (OPCAB) and compares their results with those of subsequent coronary angiography.

Methods: The subjects were 159 OPCAB patients, with a total of 435 grafts at a single center between April 2009 and November 2011. During surgery, all grafts were assessed initially by both TTFM and IFI. Transit-time flow measurement was used for screening grafts for possible revision, then IFI was applied to check patency. For IFI, indocyanine green was injected into the superior vena cava, then the presence and timing of fluorescent enhancement were monitored in coronary and graft vessels.

Results: Twelve grafts were revised after poor TTFM scores. Despite some poor TTFM scores even after revision, subsequent IFI showed that all grafts were enhanced. However, two grafts showed delayed enhancement. In one internal thoracic artery (ITA), delay was caused by competitive flow from a mildly stenotic native coronary artery. The other delayed-enhancement ITA was revised. Reanastomosis was constructed with shorter ITA at the larger lumen size. After about 1 week, all patients underwent coronary angiography (plain angiography for 31, computed tomography angiography for 128). These demonstrated that all 385 arterial grafts, and 48 out of 50 venous grafts, were patent.

Conclusions: Our OPCAB series using TTFM and IFI achieve extremely high graft patency in the early graft assessments. “Delayed enhancement” of one ITA in comparison with the other suggested either native competitive flow or a bypass graft problem.

Author Information

From the Department of Cardiovascular Surgery, Shiga University of Medical Science, Shiga, Japan.

Accepted for publication November 23, 2012.

Disclosure: The authors declare no conflict of interest.

Address correspondence and reprint requests to Satoshi Kuroyanagi, MD, Department of Cardiovascular Surgery, Shiga University of Medical Science, Setatsukinowa, Ootsu, Shiga, 520-2192, Japan. E-mail:

Article Outline

Coronary artery bypass grafting (CABG) is a standard approach for severe coronary artery disease, and major studies (such as SYNTAX trial1) provide evidence of its effectiveness. Although there have been concerns about mortality and morbidity during and soon after surgery, the risks have been reduced recently, especially since the introduction of off-pump CABG (OPCAB).2 Postoperative graft patency in CABG is critical for patient quality of life and lifespan because it determines coronary artery revascularization.3 Assessment of intraoperative graft quality, avoidance of graft failure, and revision of any failed anastomosis are therefore most important to patient well-being. In many centers, two systems have been recently used for intraoperative graft assessment: intraoperative fluorescence imaging (IFI) and transit-time flow measurement (TTFM). We used both IFI and TTFM during 159 OPCAB procedures between April 2009 and November 2011 and compared the results of those tests with the results of x-ray or computed tomography (CT) angiography done “early” (about 1 week) after OPCAB surgery, to assess the value of IFI and TTFM in predicting graft patency. Our results, as described below, confirm the usefulness of the combined methodologies of TTFM and IFI and also demonstrate the potential value of comparing the timing of IFI when graft vessels of similar path lengths are used—in this case bilateral internal thoracic arteries (ITAs)—as a relative delay of enhancement in one side may indicate a problem in some cases.

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The present study is a retrospective analysis of data from consecutive patients at a single center. From April 2009, when IFI was introduced, to November 2011, 159 underwent TTFM followed by IFI during their OPCAB surgery, with angiography by x-ray or CT about 1 week after surgery.

All arterial graft vessels were harvested in a skeletonized manner using a harmonic scalpel. Most saphenous vein grafts (SVGs) were harvested using an open technique, but one was taken endoscopically. In these 159 patients, the assessment covered 142 right ITAs (RITAs) with 144 anastomoses, 155 left ITAs (LITAs) with 216 anastomoses, 88 gastroepiploic arteries (GEAs) with 130 anastomoses, and 50 SVGs with 88 anastomoses.

After each anastomosis was created, we used one of two TTFM devices for initial assessment: either a BUTTERFLY FLOWMETER or the later model VeriQC (both by Medistim, Oslo, Norway). In 62 early cases and 11 later cases using the BUTTERFLY FLOWMETER, two parameters were assessed: mean graft flow (MGF) and pulsatility index [PI = (QmaximumQminimum)/Qmean]. In other cases, using the VeriQC system, an additional third parameter was available: diastolic filling index [DFI = Qdiastole/(Qsystole + Qdiastole)]. We applied TTFM at the proximal portion of the first anastomosis in each diverted artery and vein.

Then, IFI was applied using an SPY system (Novadaq Technologies, Inc, Mississauga, ON Canada), for further assessment. We injected indocyanine green (ICG) into the superior vena cava and checked blood flow with the IFI system for about 20 to 25 seconds after injection. We monitored fluorescence during this period without clamping any vessels and noted first the incoming fluorescent “enhancement” of the native coronary arteries (from about 5–10 seconds after injection), then the enhancement of the graft vessels a few seconds later where patent anastomoses allowed good flow.

For early graft assessment about 1 week after surgery, 31 patients underwent plain x-ray coronary angiography and 128 others had CT angiography. It has been a common practice to perform early postoperative confirmation angiography before discharge in Japan, and this is reimbursed by insurance.

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Initial TTFM scores were substandard for several grafts, and after inspection, approximately 2% (12/578 anastomoses) were promptly revised. Flow was then checked by IFI. Two grafts were revised at this stage because one graft was not enhanced and another graft was slowly enhanced by the contralateral ITA. This “delayed-enhancement” ITA was anastomosed to the left anterior descending coronary artery, and we thought it might be problematic; thus, we revised the graft. Reanastomosis was constructed more proximally in the ITA to take advantage of the wider lumen. Then enhancement was no longer delayed. In postoperative angiography, all arterial grafts were found patent, and 48 of 50 venous grafts were patent (Table 1). The two patients with occluded SVGs were further investigated with stress myocardial scintigraphy and were not found to have myocardial ischemia.

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Intraoperative fluorescence imaging and TTFM are fundamentally different approaches to intraoperative graft assessment, with each having characteristic strengths and weaknesses; thus, they can be used to complement each other.

A number of reports show that TTFM is valuable for intraoperative graft assessment.4–7 In addition, according to those reports, grafts found positive for blood flow by IFI also proved patent in early angiographic assessments despite substandard scores in some cases by TTFM. Therefore, IFI is considered more effective for intraoperative graft assessment. At our center, where skeletonized arterial CABG is the basic technique, all anastomoses in this series of 159 patients were seen to be patent by IFI.

With IFI being a substantially direct method, it lacks certain technical vulnerabilities of TTFM, and thus, IFI is, in some ways, more reliable. Intraoperative fluorescence imaging showed positive flow in all anastomoses in our series. If IFI shows positive flow, early graft patency can be expected even where the TTFM score is poor, and concern about such discrepancies has been reported.9–11 Transit-time flow measurement analyzes the blood flow pattern through an echo probe, and thus, false-negative errors may arise from factors such as probe-contact failure with mismatched graft diameter and technique errors. The superior reliability of IFI, in contrast, lies in its direct evidence of graft blood flow. Skeletonized arterial grafts and SVGs, in particular, are easy to test using IFI.

Transit-time flow measurement as performed with VeriQC can show three parameters: PI, MGF, and DFI. Some reports suggest that to be satisfactory, grafts need to meet the following values: PI less than 5.0, DFI greater than 50, and MGF greater than 10 or 15 mL/min.5,6 By those criteria, among our 159 patients, 12 RITAs (8%), 13 LITAs (8%), 20 GEAs (23%), and 10 SVGs (20%) failed to achieve satisfactory PI scores (with PI being immeasurably high in some cases). Among these poor-scoring grafts, additional substandard DFI scores were found in two LITAs and six GEAs, and among the grafts with substandard PI and DFI scores, one LITA and one GEA also had substandard MGF scores (<10 mL/min).

Of course, even the best intraoperative results cannot guarantee lasting patency. Among our 159 patients, there were 385 artery grafts (490 anastomoses), all found to be still patent at the time of angiography, but despite good scores in intraoperative IFI and TTFM, 2 vein grafts (4% of the 50 SVGs) were occluded within about a week after surgery, as seen by angiography. There is some suspicion that vein grafts are more susceptible to blockage by kinks and coagulation than are artery grafts, and there is further suspicion8 that veins harvested endoscopically are more susceptible than are those taken openly; one of those two veins had been harvested endoscopically.

A false-negative IFI result might conceivably arise if the outer wall of a graft vessel, perhaps an artery gathered using the pedicle technique, were so thick as to obscure the fluorescent medium.

The great advantage of IFI assessment is that it makes blood flow through a grafted vessel visible, and where there is no enhancement in the graft, revision of the graft is obviously required. In this series, one graft was unenhanced by IFI, in addition to having a substandard score in TTFM (Figs. 1A, B), and we had no difficulty in deciding to revise it. That revised graft remained patent in the angiographic graft assessment about 1 week later.

However, IFI has the disadvantage of not allowing blood flow to be scored; there are no clear intermediate criteria between “enhanced” and “not enhanced” by which to assess graft quality, and it may be difficult to decide whether to revise in cases where IFI indicates positive but slow enhancement of the graft vessel. One such case was a LITA graft with anastomosis to the left circumflex coronary artery. By IFI, this graft showed slower blood flow through the LITA than through the RITA (Figs. 2A–C).

In IFI, the enhancement effect develops from ICG injected through the venous line, through the superior vena cava and right side of the heart, and the pulmonary vasculature, emerging from the left side of the heart. The time until enhancement of graft or other vessels is thus influenced by various factors such as arterial anatomic path length and blood flow velocity (involving cardiac output, systemic vascular resistance, and any limitation of blood flow velocity in a graft vessel as dictated by flow rate through anastomoses). Thus, for example, the enhancement effect normally arrives later in the GEA than in the ITA because of greater distance from the heart, but when enhancement (due to ICG fluorescence) begins, it should move along each graft vessel at a speed dictated by the blood flow velocity through the anastomoses.

Intraoperative fluorescence imaging arrival times can be important. In view of path length differences, it might seem inappropriate to use the delay until manifestation of fluorescent enhancement to assess graft quality. However, we found the delay to start of enhancement to be very important where both RITA and LITA are used together. They represent similar path lengths from the heart, and if blood flows through both at similar rates, then the time to start of enhancement should also be similar. In practice, delayed enhancement is very useful for finding problematic grafts. In the case of the problematic LITA graft described above, the time to start of enhancement was longer for the LITA than for the RITA. About a week after surgery, the LITA anastomosis was seen to be patent on plain coronary angiography, although with slow blood flow, but the anastomosis could not be located in coronary CT angiography 1 year later. This was because of the native coronary artery being sufficiently open for flow competition to occur. There was only one patient with slow flow in a LITA graft identified in early postoperative angiography in this study group. Because the fate of this LITA graft seemed unclear, this patient exceptionally received 1-year CT angiography. We have not routinely been conducting 1-year systematic angiography of the others in this study group. In another patient, there was delayed enhancement in the RITA (compared with the LITA) (Figs. 3A–C). The TTFM scores for this anastomosis were substandard, thought not poor enough clearly to warrant revision of the anastomosis. The problematic RITA graft was a little over-long, and kinking of that graft vessel, rather than anastomotic stenosis or occlusion, was suspected. On the basis of IFI delay, however, the anastomosis was revised, and reanastomosis was constructed with shorter ITA at the larger lumen size. (Figs. 4A, B), and good TTFM scores resulted. This demonstrates the use of IFI timing to identify failed grafts, especially in the ITA.

In recent years, there have been reports on the benefits of using bilateral ITAs,12,13 and this is increasingly important in current CABG, especially off-pump surgery. In this study, we had only two cases of delayed enhancement. Delayed enhancement of one ITA in comparison with the other suggested either native competitive flow or a bypass graft problem.

One methodological limitation of this work was that we obtained only qualitative data by IFI, whereas quantitative data would be preferable. In addition, we hope to accumulate long-term follow-up data on clinical outcomes and long-term graft function. Furthermore, we would like to develop some more sophisticated application of IFI to distinguish a well-functioning bypass from a failing bypass.

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We use both TTFM and IFI, and although each methodology includes a risk of false results for graft patency, the combination of modalities should give the maximum chance of successful grafts. Our results are broadly consistent with previous reports, but we find that when two approximately symmetrical graft vessels are used, it may also be worth comparing the timing of IFI enhancement because delayed enhancement may indicate either native competitive flow or, perhaps, the need for graft revision.

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We thank Piers Vigers for reviewing our manuscript.

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This is an interesting clinical report from the group at University of Medical Science in Shiga, Japan, describing the complimentary use of transit-time flow measurement and intraoperative fluorescent imaging (IFI) during off-pump coronary artery bypass grafting in a series of 159 patients. They used transit-time flow measurement for screening grafts for revision and then used IFI subsequently to check for patency. All patients underwent follow-up angiography at 1 week, the great majority with computed tomography. This study demonstrated that all 385 arterial grafts and 48 of the 50 venous grafts were patent.

The graft patency that was able to be achieved with this strategy was impressive. Their findings suggest that compulsive evaluation of bypass grafts during off-pump surgery can improve clinical results. Most of the problems were picked up by transit-time flow measurement, and approximately 2% of the grafts were promptly revised. The flow was then checked by IFI, and two further grafts were revised because of either delayed or no enhancement. These two grafts represented only 0.3% of the total 578 anastomoses. This is relatively little gain for the application of this technology. One drawback of IFI is that the data are qualitative rather than quantitative. However, in rare instances, it does seem to supply useful information. The authors are to be congratulated for their attention to detail and superb clinical follow-up.


CABG; Intraoperative fluorescence imaging; Intraoperative graft assessment; Transit-time flow measurement; Bilateral ITA

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