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J Thorac Cardiovasc Surg 2004;128:238-244
© 2004 The American Association for Thoracic Surgery

Cardiopulmonary support and physiology

Does off-pump total arterial grafting increase the incidence of intraoperative graft failure?

Lognathen Balacumaraswami, FRCSa, Yasir Abu-Omar, MRCSa, Kyriakos Anastasiadis, MDa, Bikram Choudhary, MBBSa, David Pigott, FRCAb, Siu-Kae Yeongc, David P. Taggart, MD, PhD, FRCSa,*

a Departments of Department of Cardiothoracic Surgery, John Radcliffe Hospital, Oxford, United Kingdom,
b Department of Anaesthesia, John Radcliffe Hospital, Oxford, United Kingdom
c National Research Council of Canada, Ottawa, Ontario, Canada

Received for publication September 19, 2003; revisions received November 18, 2003; accepted for publication November 20, 2003.

* Address for reprints: David P. Taggart, MD, Department of Cardiothoracic Surgery, John Radcliffe Hospital, Headley Way, Headington, Oxford OX3 9DU, United Kingdom
david.taggart{at}orh.nhs.uk


   Abstract
Top
 Abstract
Material and methods
 Results
 Discussion
 References
 
BACKGROUND: Early graft failure is a common cause of cardiac mortality and morbidity after coronary artery bypass grafting, but there is little information on its natural incidence. Furthermore, there is particular concern about graft patency in off-pump coronary artery bypass grafting and total arterial grafting.

METHODS: We performed a prospective observational study to assess intraoperative graft patency in patients undergoing off-pump and on-pump coronary artery bypass grafting, who also underwent total arterial grafting. We used an intraoperative imaging system, SPY (Novadaq Technologies Inc), based on the fluorescent properties of indocyanine green dye.

RESULTS: We assessed the intraoperative graft patency of 533 conduits in 200 patients. The mean number of grafts was 2.7 per patient. Of these patients, 155 (78%) had off-pump coronary artery bypass grafting, and 45 (22%) had on-pump coronary artery bypass grafting. Overall, 161 (80%) had total arterial grafting, with composite arterial grafting performed in 120 (60%) patients. Fluorescence, confirming graft patency, was observed in all but 8 (1.5%) conduits in 8 (4%) patients, necessitating graft revision. Six (3.9%) and 2 (4.4%) of these patients, respectively, had off-pump coronary artery bypass grafting and on-pump coronary artery bypass grafting.

CONCLUSION: Intraoperative fluorescence imaging demonstrated a low (1.5%) but well-defined incidence of intraoperative graft failure, which affects around 4% of patients. This emphasizes the need for routine assessment of graft patency. Intraoperative fluorescence imaging permits detection and revision of failed grafts in the operating room. We found no difference in the incidence of failed grafts when comparing on-pump and off-pump total arterial grafting.


Taggart, Balacumaraswami, Pigott, Abu-Omar, and Choudhary (left to right)


There is growing evidence that arterial grafts1-3 and off-pump coronary artery bypass grafting (OPCABG)4 improve the outcome of coronary revascularization. However, total arterial grafting (TAG) and OPCABG are considered to be technically more demanding, and there are continuing concerns that OPCABG results in both a reduced number of grafts5 and inferior patency rates.6-8 Cheng and colleagues5 reported that technical difficulties in constructing anastomoses resulted in incomplete revascularization in patients undergoing OPCABG (mean distal anastomoses, 1.9 vs 3.3; P < .001) when compared with those undergoing on-pump coronary artery bypass grafting (ONCABG).5 Sabik and colleagues9 likewise reported a significantly lower number of grafts in patients undergoing OPCABG (2.8 vs 3.5, P < .001), particularly to the circumflex and right coronary territories. Gundry and associates7 reported that 20% of patients undergoing OPCABG required either a coronary angioplasty or redo coronary artery bypass grafting (CABG) for recurrent symptoms. Most recently, in a prospective randomized trial of 104 patients allocated to ONCABG or OPCABG, Khan and colleagues8 reported an inferior 3-month angiographic patency rate of 88% in the OPCABG group compared with 98% in the ONCABG group (P < .01).

Recently, we described the value of an intraoperative fluorescence imaging (IFI) system (SPY, Novadaq Technologies Inc) to confirm graft patency.10 We have now used this system to prospectively compare graft patency in patients undergoing, predominantly, total arterial grafts in the setting of ONCABG and OPCABG.


   Material and methods
Top
 Abstract
 Material and methods
Results
 Discussion
 References
 
All patients undergoing CABG performed by a single surgeon (DPT) between November 2001 and June 2003 were included in the study, with the exception of a few cases when the imaging system was not available. Our general principle is to perform off-pump TAG whenever practical and feasible. In general, ONCABG is performed in patients with poor left ventricular function (ejection fraction, <25%). Likewise, there is a higher use of vein grafts rather than radial artery grafts in patients with poor left ventricular function because of the higher likelihood of need for inotropic support.

Intraoperative graft patency data were collected prospectively in patients undergoing CABG with the IFI system (SPY, Novadaq Technologies Inc) on the basis of fluorescence of indocyanine green (ICG). We have described this technique previously.10 Briefly, ICG rapidly binds to plasma proteins when injected intravenously and fluoresces (emits light at 830 nm) when illuminated with a monochromatic laser light source at 806 nm. The fluorescence is captured on a charged couple device video camera. The low-intensity laser, with a total output of 2.7 W over an area of 7.5 x 7.5 cm at a distance of 30 cm above the heart, has an excellent safety profile for both the patient and theater staff. In particular, it does not require any eye protection. The system has CE marking in Europe, which allows patient use in the European community.

ICG has been widely used in clinical practice, particularly in ophthalmic angiography, for over 4 decades and has an excellent safety profile. The incidence of allergic reaction to ICG is approximately 1:40,000 and has been reported especially in patients allergic to iodine.11 The risk is strongly dose dependent, being greatest with doses greater than 0.5 mg/kg body weight.

The sterile draped camera head, guided by a range detector diode, was positioned at 30 cm above the heart. After completion of the distal coronary anastomosis, 1 mL (0.03 mg/kg weight) of ICG dye was injected into the oxygenator in the ONCABG group or through the central venous line and flushed through with 10 mL of normal saline in the OPCABG group. Screening was started at the time of injection, and the grafts were imaged as the fluorescent dye passed through them. Images were then recorded on the computer hard drive. The procedure took approximately 3 minutes per anastomosis. Skeletonized conduits provided better visualization than pedicled ones. The appearance of fluorescent images as the dye passed through the bypass grafts confirmed graft patency.

Surgical technique
All patients underwent CABG through a median sternotomy. Both internal thoracic arteries (ITAs) were harvested as skeletonized conduits. The radial artery (RA) was harvested and stored in heparinized blood containing phenoxybenzamine in the earlier patients12 and additional verapamil in the later patients13 before performing the anastomosis. The long saphenous vein was harvested by using a minimally invasive technique.

Although there are several variations depending on precise coronary anatomy and disease patterns, our basic primary strategy for construction of anastomoses was to place the right ITA (RITA) to the left anterior descending artery, the left ITA (LITA) to the obtuse marginal branch of the circumflex artery, and a composite RA graft from the LITA to the posterior descending branch of the right coronary artery.

The ITA conduits were used as in situ grafts to perform single or sequential distal coronary anastomoses. Some of the ITA and RA conduits were recycled and used for constructing composite Y grafts to maximize their use. In a few cases, the recycled free ITA conduits were anastomosed as Y grafts from the parent in situ ITA to achieve composite grafting. Where possible, composite multivessel grafting was performed to achieve TAG, with complete avoidance of aortic manipulation.

ONCABG
Cardiopulmonary bypass (CPB) was instituted by using ascending aortic cannulation and a 2-stage venous cannulation in the right atrium. A standard CPB circuit incorporated a roller pump (Jostra HL 20) and a hollow-fiber membrane oxygenator (Affinity NT, Medtronic). The extracorporeal circuit was primed with 1000 mL of Hartmann solution and 2500 IU of heparin. Nonpulsatile flow with a flow rate of 2.4 L · m–2 · min–1 was maintained. Arterial filtration was not used. Cardiotomy suction was used. Acid-base balance was managed with alpha-stat control. The temperature was allowed to drift to 34°C during construction of anastomoses before rewarming. Myocardial protection was achieved with intermittent antegrade cold crystalloid cardioplegia. On completion of all distal anastomoses, the aortic crossclamp was removed, and the proximal anastomosis was performed with partial clamping.

OPCABG
Complete anticoagulation with heparin was achieved as in the CPB group. The lateral and inferior walls were exposed by means of a combination of a deep pericardial stay suture, Trendelenberg and right decubitus positions, and opening of the right side of the pericardium to the inferior vena cava. Regional myocardial immobilization was achieved with a suction stabilizer (Octopus, Medtronic Inc; Guidant, Cardiothoracic Systems Inc). The target coronary vessels were snared proximally with a silastic sling. In our earlier experience, an intracoronary shunt (Guidant Axius) was used when there were signs of electrocardiographic instability or excessive bleeding during construction of the anastomosis. Latterly shunts have been used routinely. A surgical blower-mister device enhanced visualization (Medtronic Clearview, Medtronic Inc).

Off-pump TAG with avoidance of aortic manipulation was achieved in 84.5% of cases. In the occasional cases in which saphenous vein grafts were performed, proximal anastomoses were made to the ascending aorta at a controlled systolic pressure of between 70 and 80 mm Hg and a side-biting vascular clamp.

Statistical analysis
Results for categoric variables are expressed as numbers (percentages of total). Continuous variables are presented as means ± SD. The {chi}2 test was used for comparison of categoric variables. The continuous variables were compared by using the Student t test.


   Results
Top
 Abstract
 Material and methods
 Results
Discussion
 References
 
Intraoperative graft patency was assessed in 200 patients. Our previously reported preliminary experience of 84 patients is included in this study.10 A total of 533 distal coronary anastomoses were constructed. The ONCABG group includes 3 patients with concomitant aortic valve replacement and 1 patient undergoing reoperative CABG. In the OPCABG group 5 patients underwent reoperative CABG.

The mean number of distal anastomoses was 2.7 per patient. Of these patients, 155 (78%) underwent OPCABG, and 45 (22%) underwent ONCABG (Figure 1) . The mean number of distal anastomoses for the ONCABG group was 2.9 per patient compared with 2.6 per patient for the OPCABG group (P < .05, Table 1). However, the OPCABG group had a higher proportion of patients with single-vessel or double-vessel disease. In patients with triple-vessel disease, the mean number of grafts for the OPCABG and ONCABG groups was similar (OPCABG, 3.2 ± 0.4; ONCABG, 3.3 ± 0.5), with no difference between the 2 groups.



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  		Figure 1. Flow diagram. OPCABG, Off-pump coronary artery bypass grafting; ONCABG, on-pump coronary artery bypass grafting; TAG, total arterial graft; SVG, saphenous vein graft.

 

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  		TABLE 1. Mean age and anastomoses, diseased vessels, conduits used, and composite grafts in patients

 
Overall, 161 (80%) patients had TAG, of which composite arterial grafting was performed in 120 (60%) patients. TAG was performed in 136 (88%) patients in the OPCABG group and 25 (56%) patients in the ONCABG group. A total of 100 (65%) composite grafts were performed in patients undergoing OPCABG, which was significantly more (P = .05) than the 20 (44%) grafts in the ONCABG group (Table 1). Excluding those with single-vessel disease, bilateral ITA conduits were used in 109 (59%) patients: 87 (62%) in the OPCABG group and 22 (51%) in the ONCABG group.

There was no significant difference in the number and location of coronary arteries bypassed or the number of ITA grafts between the 2 groups. There were significantly more saphenous vein grafts (OPCABG, 6% of grafts; ONCABG, 24% of grafts; P < .01) and significantly fewer RA grafts (OPCABG, 29% of grafts; ONCABG, 18% of grafts; P < .05) used in constructing the distal anastomoses in the ONCABG group because of a higher proportion of patients with poor left ventricular function in the ONCABG group. The overall pattern of conduit use include the LITA in 216 (40.5%) distal anastomoses, the RITA in 119 (23%) distal anastomoses, the RA in 141 (25.5%) distal anastomoses, the gastroepiploic artery in 2 (0.4%) distal anastomoses, and the long saphenous vein in 57 (10.6%) distal anastomoses. The configuration of conduits anastomosed to various distal coronary targets is shown in Table 2. Overall, the LITA was used as a recycled conduit or in sequential grafts in 20 (10%) patients. The RITA and RA conduits were each recycled in 3 patients.


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  		TABLE 2. Overall configuration of conduit use in distal anastomoses (patients, n = 200; conduits, n = 533)

 
Eight (1.5%) grafts in 8 (4%) patients demonstrated no fluorescence within the conduits during image acquisition (Table 3). None of these grafts were imaged again to demonstrate flow. Hence we cannot label any of these as spasm. None of these patients demonstrated intraoperative electrocardiographic or hemodynamic changes. In 2 patients graft failure was caused by dissection in the conduit wall, in 2 patients it was caused by intimal flaps in the native coronary vessel, in 1 patient it was caused by an inadvertent stitch in the posterior wall of the coronary vessel, and in 1 patient it was caused by kinking at the heel of the anastomoses. In 2 patients there was no readily discernable cause. Two (4.4%) of these patients underwent ONCABG, and 6 (3.9%) underwent OPCABG. There was no statistical difference in the number of grafts revised between the 2 groups. The occluded grafts were revised, after which the grafts were reimaged and patency was confirmed with the IFI system.


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  		TABLE 3. Revised grafts

 
On initial imaging, 5 (0.9%) grafts performed to the posterior descending coronary artery and 4 (0.75%) to the obtuse marginal branch of the circumflex artery did not demonstrate fluorescence, whereas the heart was "distorted" by being "upended" with a suction cap. However, on subsequent imaging, with the heart in its natural position, flow could be seen in the proximal portion of the graft, confirming graft patency. We assume that lack of flow in initial imaging was due to a transient decrease in cardiac output and systemic arterial pressure combined with compression of the graft between the lateral border of the heart and the sternal edge. In one patient the RITA-to-intermediate-artery anastomosis did not demonstrate fluorescence on initial imaging in its natural position but did demonstrate satisfactory flow, with a higher systemic arterial pressure on subsequent imaging. In this case intrinsic graft spasm might be the cause.


   Discussion
Top
 Abstract
 Material and methods
 Results
 Discussion
References
 
Although the need for coronary angiography for quality control is universally accepted for percutaneous interventions, most CABG operations are still performed without any immediate confirmation of a satisfactory technical result. Indeed, until recently and in the absence of suitable devices for assessment of graft patency, the current natural incidence of intraoperative graft failure has been poorly documented. Although intraoperative graft failure might be asymptomatic, it can contribute to early morbidity and mortality and adversely affect long-term outcomes.14 Consequently, there is a growing appreciation of the desirability to confirm graft patency in the operating room, particularly in the setting of new operative techniques and interventions, such as OPCABG and TAG.

Our current prospective study of 200 patients undergoing both on-pump and off-pump CABG confirms our own preliminary experience10 and the findings of others6 that there is a small but definite incidence of intraoperative graft failure that can be detected and corrected in the operating room. We found that 8 (1.5%) grafts in 8 (4%) patients were occluded, necessitating revision (Figures 2 and 3) . It is of particular importance in these cases of graft occlusion that the surgeon was unsuspecting and that there was no hemodynamic instability or electrocardiographic evidence of myocardial ischemia in the area subtended by the grafted artery. Without formal assessment of graft patency, graft occlusion would have remained undetected.



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  		Figure 2. A, Image showing in situ left internal thoracic artery (LITA) graft to the left anterior descending (LAD) artery. A composite radial artery (RA) graft from the LITA is anastomosed to the obtuse marginal (OM) artery. Note fluorescence is not seen within the RA. B, This image was taken after revision of the LITA-to-RA anastomosis seen in panel A. Note that fluorescence is now seen in the RA and OM coronary artery.

 


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  		Figure 3. A, Image showing in situ anastomosis of the left internal thoracic artery (LITA) to the obtuse marginal (OM) artery. Note that no fluorescence is seen in the LITA graft but is seen in the OM artery as a result of native flow. B, Image obtained after revision of the anastomosis in panel A. Note that fluorescence is seen in both the LITA and the OM coronary artery.

 
However, in contrast to the findings of others,5,7-9 we did not find that OPCABG either reduced the number of grafts or increased the failure rate in comparison with ONCABG. Although the overall mean number of distal coronary anastomoses was significantly higher in the ONCABG group because of a higher proportion of patients with single-vessel or double-vessel disease in the OPCABG group, there was no significant difference in the mean number of distal anastomoses in patients with triple-vessel disease in the 2 groups (OPCABG, 3.2 ± 0.4; ONCABG, 3.3 ± 0.5).

The plethora of techniques that have been proposed to confirm graft patency (Table 4)15-21 emphasizes the lack of a single and universally accepted method. Conventional coronary angiography is the gold standard technique for graft assessment but is highly invasive (requiring arterial puncture), increases operating time, and is infrequently available in the operating room. Although numerous other methods on the basis of electromagnetic,22 ultrasound,6,15,23 Doppler flow analysis,16 echocardiographic,24 and thermal angiography techniques25 have been described, all have limitations precluding their widespread use. Currently, transit-time flowmetry (TTFM) and IFI appear most promising.


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  		TABLE 4. Graft revision reports in the literature

 
TTFM uses the principle of ultrasound to measure flow in bypass grafts. A flow probe housing 2 ultrasonic transducers and an acoustic reflector is used to obtain the transit time taken for the wave of ultrasound to travel from one transducer to another. The difference between the integrated transit times is a measure of the flow volume. By using TTFM, D'Ancona and colleagues6 reported the need to revise 37 (3.2%) of 1145 grafts in 33 (7.6%) of 409 patients undergoing OPCABG. They emphasized the reliance on correct analysis of TTFM flow patterns to correct abnormalities. Absolute mean flow values are of little value, particularly in low-flow situations, and appropriate interpretation of certain derived values, such as the pulsatility index and the diastolic flow index, are variable.

The IFI system, on the contrary, is a simple, safe, and reproducible intraoperative imaging technique that enables routine assessment of graft patency in the operating room. IFI visibly demonstrates graft patency by means of fluorescence of ICG dye as it passes through the graft. The ICG dye transit time is dependent on various factors, including the diameter of the conduit, systemic arterial pressure, competitive native coronary flow (depends on severity of the native stenoses), and size and state of the distal coronary vascular bed. Proximal snaring of the target coronary vessel with a Silastic sling after completion of the anastomosis6 eliminates competitive flow and results in a shorter dye transit time with superior fluorescent images.

Although several groups have reported intraoperative patency rates in CABG, to our knowledge, this is the first reported study of intraoperative imaging for graft patency assessment in both ONCABG and OPCABG, which provides evidence to support its routine use in CABG.

Limitations
This is an observational study with all grafts performed by a single surgeon and might overestimate or underestimate the true natural incidence of graft failure. The results are, however, consistent with the incidence of graft failure observed in other reports in the literature. Although the IFI system confirms intraoperative graft patency, it does not permit precise angiographic assessment of the quality of the anastomosis and hence cannot ensure long-term patency, which would require angiographic follow-up studies. The IFI system would be considerably enhanced by means of quantification of graft flow.

Conclusion
IFI demonstrated a low but well-defined incidence of intraoperative graft failure in both on-pump and off-pump operations, which underlines the need for routine assessment of graft patency. An IFI system allows verification of graft patency and immediate correction of failed grafts and should be considered for routine use in patients undergoing CABG.


   Acknowledgments
 
The camera and the dye were provided by Novadaq Technologies Inc (Toronto, Canada) for investigational purposes.


   Footnotes
 
Lognathen Balacumaraswami (the first author) was partly funded by the Oxford University Medical Research Fund.


   References
Top
 Abstract
 Material and methods
 Results
 Discussion
 References
 

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R. Flaumenhaft, E. Tanaka, G. J. Graham, A. M. De Grand, R. G. Laurence, K. Hoshino, R. J. Hajjar, and J. V. Frangioni
Localization and Quantification of Platelet-Rich Thrombi in Large Blood Vessels With Near-Infrared Fluorescence Imaging
Circulation, January 2, 2007; 115(1): 84 - 93.
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A. Parolari, F. Alamanni, G. Polvani, M. Agrifoglio, Y. B. Chen, S. Kassem, F. Veglia, E. Tremoli, and P. Biglioli
Meta-Analysis of Randomized Trials Comparing Off-Pump With On-Pump Coronary Artery Bypass Graft Patency
Ann. Thorac. Surg., December 1, 2005; 80(6): 2121 - 2125.
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L. Balacumaraswami, Y. Abu-Omar, B. Choudhary, D. Pigott, and D. P. Taggart
A comparison of transit-time flowmetry and intraoperative fluorescence imaging for assessing coronary artery bypass graft patency
J. Thorac. Cardiovasc. Surg., August 1, 2005; 130(2): 315 - 320.
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T. D.L. Keenan, Y. Abu-Omar, and D. P. Taggart
Bypassing the Pump: Changing Practices in Coronary Artery Surgery
Chest, July 1, 2005; 128(1): 363 - 369.
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