Abstract

Background: This study aims to compare the effects of measurements taken with indocyanine green fluorescence imaging (IFI) and transittime flowmeter measurement (TTFM) methods on the surgical outcomes of coronary artery bypass grafting.

Methods: Between December 2023 and May 2024, a total of 70 patients (53 males, 17 females; mean age: 64.2±9.1 years; range, 43 to 82 years) who underwent on-pump coronary artery bypass grafting via median sternotomy by the same surgical team were included in this prospective study. The control group (TTFM group, n=35) consisted of patients who had intraoperative TTFM, while the remaining patients received both TTFM and IFI measurements during surgery (TTFM+IFI group, n=35). The groups were compared in terms of first-month survival, ejection fraction preservation, intra-aortic balloon pump use, need for extracorporeal membrane oxygenation, postoperative myocardial infarction, and length of intensive care unit and hospital stay.

Results: In our clinic, distal anastomoses were performed in a mean of 3.3±0.7 vessels in the TTFM group and in a mean of 3.7±0.8 vessels in the TTFM+IFI group. The total number of distal anastomoses in the TTFM group and TTFM+IFI group was 115 and 130, respectively. According to the TTFM and IFI measurements taken during the surgery, no revision was required in any of the grafts. There was no statistically significant difference between the two compared groups in terms of early survival, postoperative myocardial infarction, need for intra-aortic balloon pump, need for extracorporeal membrane oxygenation, preservation of ejection fraction, length of stay in the intensive care unit, and time to discharge (p>0.05).

Conclusion: The use of IFI yields no significant effect on early-term outcomes and TTFM is solely adequate for assessing graft functionalities in coronary artery bypass grafting.

Coronary artery bypass grafting (CABG) is the most commonly performed cardiac surgical procedure, with over 600,000 operations carried out annually worldwide.[1] It has been shown to improve survival for individuals with multiple coronary artery disease (CAD), diabetic patients, and patients with left main coronary artery stenosis.[2-5] Therefore, it is essential that surgeons use trustworthy techniques to assess anastomosis and graft quality intraoperatively in CABG.

Transit-time flowmeter measurement (TTFM) has been reported to be a suitable method for easy and rapid intraoperative evaluation of bypass grafts.[6,7] Indocyanine green (ICG) angiography can provide quantitative assessment of myocardial perfusion in response to coronary stenosis severity.[8]

In the present study, we, therefore, aimed to compare the intraoperative detection of graft dysfunction by TTFM and ICG indocyanine fluorescence imaging (IFI) in on-pump CABG and to examine their effects on surgical outcomes.

Methods

This single-center, prospective study was conducted at Atatürk University Faculty of Medicine, Department of Cardiovascular Surgery between December 2023 and May 2024. A total of 70 patients (53 males, 17 females; mean age: 64.2±9.1 years; range, 43 to 82 years) who underwent on-pump CABG via median sternotomy by the same surgical team were included. The patients were randomized into two equal groups. Graft measurements were performed with TTFM in 35 patients after the heart-lung machine support was terminated, and these patients constituted the control group (TTFM group). In the other 35 patients, both TTFM measurements were performed and IFI was performed by administering ICG via a central venous catheter after the heart-lung machine was turned off. These patients constituted the experimental group (TTFM+IFI group). Written informed consent was obtained from each patient. The study protocol was approved by the Atatürk University Faculty of Medicine Clinical Research Ethics Committee (Date: 25.03.2021, No: B.30.2.ATA.0.01.00/118). The study was conducted in accordance with the principles of the Declaration of Helsinki.

Surgical procedure
All patients were premedicated with midazolam. The patients were operated under general anesthesia. For the cardiopulmonary bypass (CPB) procedure, after systemic heparinization with 400 IU/kg heparin sodium, clotting time was provided with an activated coagulation time (ACT) value of over 400 sec. If necessary, additional heparin doses were administered during follow-up. The CPB was applied with mild systemic hypothermia (32 to 34°C), moderate hemodilution (hematocrit 20 to 25%), flow rate 2 to 2.4 L/min/m² and mean arterial pressure 50 to 70 mmHg. Cardiac arrest was achieved with cold (8 to 15 °C) cardioplegic fluid (Del Nido solution) administered through the aortic root cannula during CPB. Arterial cannulation was performed from the ascending aorta in all patients. Venous cannulation was performed from the right atrial appendage with a two-stage cannula. Cardioplegia solution was administered antegradely in all patients. Pulsatile flow was applied during cross-clamping and continuous flow was applied after the heart started to pump.

In all patients, median sternotomy was performed. Left internal mammary artery (LIMA), saphenous and radial grafts were prepared to be used simultaneously in all our patients. Radial artery grafts were used in two patients in the TTFM group and in one patient in the TTFM+IFI group. Patients in whom radial grafts would be harvested also had a systemic infusion of diltiazem hydrochloride initiated during the procedure. In patients whose radial arteries were harvested, radial grafts were kept in solutions consisting of heparin sodium, glycerol trinitrate, autologous blood and warm water. Following the cross-clamp application, first the distal anastomoses of the free grafts (radial artery, saphenous vein) were performed, and then the anastomoses (end-to-side) of the internal mammary artery (IMA) to the left anterior descending (LAD) artery were performed. For distal anastomoses, 7/0 and 8/0 prolene sutures were used. After the cross-clamp was removed, hot-shot cardioplegia was performed from the heart-lung machine. By placing a side clamp on the ascending aorta, the proximal anastomoses of the radial artery and saphenous vein grafts were anastomosed end-to-side to the ascending aorta. For the proximal anastomoses, 6/0 prolene sutures were used. Protamine hydrochloride infusions were given centrally to the patients following decannulation to restore normal ACT levels.

Intraoperative TTFM measurements
After the patients were separated from the heart-lung machine support and heparin was neutralized with protamine infusion, TTFM (MEDI-STIM VeriQ-4122, Norway) measurements of all grafts were performed and recorded. During TTFM measurements, the mean blood pressure was adjusted to 80 to 100 mmHg with the support of vasoactive drugs if necessary. The TTFM probe was selected in sizes compatible with the grafts, completely encircled the graft and was placed perpendicular to the graft during the measurement. The mean graft flow (MGF-mL/min), pulsatility index (PI), diastolic flow (DF-%), reflux percentage obtained with TTFM, and graphics formed on the device screen were evaluated. A MGF of >20 mL/min, a PI of <5, a DF of >55% were targeted.

Intraoperative IFI measurements
After the patients were separated from the heart-lung machine support, 1 cc of ICG was administered via the central line. Images appeared 2 to 20 sec after the injection. Images were recorded with SPY IFI (SP 3055 Novadaq™; Novadaq Technologies, Inc., Ontario, Canada). Measurement was activated by pressing the CONTOUR icon on the device. There is a PERCENTAGE (%) icon under the CONTOUR icon. The round "100%" sign was placed on a point with good perfusion as a reference point and other relevant points were selected on the screen for the points to be measured. The points to be measured received %values according to the "100%" reference marker.

Statistical analysis
Statistical analysis was performed using the IBM SPSS version 20.0 software (IBM Corp., Armonk, NY, USA). Data were presented in mean ± standard deviation (SD), median (min-max) or number and frequency, where applicable. The normal distribution of continuous variables was examined using the Shapiro-Wilk test, Kolmogorov-Simirnov test, Q-Q plot, skewness and kurtosis. In comparisons between two independent groups, the independent samples t-test was used when the normal distribution condition was met, while the Mann-Whitney U test was used when it was not met. The chi-square test was used in comparisons between two ratios. The Bonferroni correction was used to adjust the significance level for multiple comparisons. The effects of the groups on survival were determined using survival analysis. The survival of the patients was determined using the Kaplan-Meier method in survival analysis. The log-rank test was used to compare survival curves. Survival curves were drawn using the survival function. A p value of < 0.05 was considered statistically significant.

Results

Demographic characteristics and intraoperative data of both groups are shown in Table 1 and Table 2, respectively. The mean number of bypassed vessels was 3.3±0.7 in the TTFM group and 3.7±0.8 in the TTFM+IFI group (p=0.024). The incidences of all variables which could affect clinical results were similar in both groups (p>0.05). The mean EuroSCORE II values of the patients were 3.36±3.39 in the TTFM group and 2.67±3.64 in the TTFM+IFI group (p>0.05). The most frequently bypassed vessel in both groups was the LAD, and the most frequently used graft was the saphenous vein graft. Except for one patient in the TTFM group, all grafts bypassed to the LAD were LIMA grafts. In one patient, the LIMA was not removed, as it was thin and non-palpable.

Table 1. Demographic features and preoperative risk factors of patients

Table 2. Intraoperative data of patients

The TTFM measurements were performed in all 70 patients in both groups and in all grafts (Figure 1). Following the termination of extracorporeal circulatory support and the stages of decannulation and heparin neutralization, MGF (mL/min), PI, DF (%) values were measured and recorded with TTFM. According to TTFM results, no graft required revision. No statistically significant difference was found between the two groups in terms of TTFM findings (p>0.05). Comparison of MGF (mL/min), PI, DF (%) values is shown in Table 3.

Figure 1. Transit-time flowmeter measurement monitoring. Satisfactory TTFM values for (a) LIMA with LAD and (b) RCA with SVG.
TTFM: Transit-time flowmeter measurement; LIMA: Left internal mammarian artery; LAD: Left anterior descending; RCA: Right coronary artery; SVG: Saphenous vein graft; PI: Pulsatility index; DF: Diastolic flow; HR: Heart rate; ECG: Electrocardiogram.

Table 3. Intraoperative TTFM findings

In 35 patients in the TTFM+IFI group, IFI measurements were performed in addition to the TTFM procedure (Figure 2). Quantitative measurements were made on images taken after the termination of extracorporeal circulatory support. As a result of IFI measurements, the flow increased in all grafts compared to the values before revascularization. Pre- and postoperative IFI measurements are shown in Table 4.

Figure 2. Indocyanine fluorescence imaging. (a) LIMA-LAD anastomosis and distal coronary bed, (b) Aorta-saphenous-RCA, (c) LIMA-LAD distal bed, (d) Aorta-saphenous-CX distay.
LIMA: Left internal mammary artery; LAD: Left anterior descending artery; RCA: Right coronary artery; CX: Circumflex artery.

Table 4. Intraoperative IFI findings

Table 5 shows mortality, morbidity and major postoperative complications. Early survival, postoperative myocardial infarction (MI), need for intra-aortic balloon pump (IABP), need for extracorporeal membrane oxygenation (ECMO), ejection fraction (EF) preservation, intensive care unit (ICU) length of stay and discharge time were not statistically different (p>0.05). The median ICU length of stay was 4.3 and 4.4 days in the TTFM group and TTFM+IFI group, respectively, and the median time to discharge was 10.0 and 10.2 days, respectively (p>0.05). Figure 3 also shows the survival graph.

Table 5. Complication and mortality rate

Figure 3. Survival graph.
TTFM: Transit-time flowmeter measurement; IFI: Indocyanine fluorescence imaging.

Discussion

Despite advances in treatment and prevention strategies, CAD continues to be a leading cause of death worldwide, making it a topical issue worthy of study. Despite advances in medical treatment methods, invasive treatment options, percutaneous coronary intervention (PCI) and CABG, continue to be applied with significant frequency currently, and cardiologists and cardiac surgeons continue to develop their methods accordingly to achieve more satisfactory results. In this context, in the present study, we compared two intraoperative methods for detecting graft failure which is an important concern in CABG surgery. Our study findings demonstrated that IFI did not offer any additional benefit over TTFM in terms of early postoperative outcomes.

Graft-related causes of perioperative MI after cardiac surgery include thrombosis, kinking, stretching, angulation, competing coronary flow, spasm, and technical errors.[9] Studies using intra- and early postoperative coronary angiography (CAG) to assess graft patency have shown an incidence of early graft failure of approximately 5% for IMA grafts and 11% for vein grafts.[10-13] More favorable postoperative outcomes would follow from the intraoperative diagnosis of technical issues related to the graft's length or shortness such as bending, rotation, or stenotic grafts, and their treatment during the procedure.

Coronary angiography, TTFM, high-resolution epicardial ultrasonography (HR-ECUS), and IFI are methods developed to evaluate graft patency during surgery. Although CAG provides the most accurate information to evaluate graft patency, the number of hybrid operating rooms that meet these conditions is quite low. Therefore, TTFM, which is easy to apply, is the most commonly used method. In studies on TTFM, sensitivity has been reported to vary between 0.250 and 0.457 and specificity between 0.939 and 0.984.[14] The reported negative predictive values ranged between 0.719 and 0.980 and positive predictive values ranged between 0.100 and 0.840.[14]

Furthermore, TTFM is a method that has been used for many years and has become quite widespread in the evaluation of graft and anastomosis quality. There are studies that TTFM is an important tool in deciding whether a graft is functioning well or not and that it improves the results with revisions made to grafts that are deemed inadequate during the operation. Becit et al.[15] reported the short-term results of 100 patients who had TTFM measurements performed prospectively during CABG compared with 100 patients who previously underwent surgery without TTFM evaluation. In the aforementioned study, 3% of the total grafts in 9% of the patients were revised due to failure to achieve the desired targets in TTFM measurements. The incidences of mortality (p<0.05), postoperative MI (p<0.05), and IABP requirement (p<0.05) were found to be significantly lower in patients who had TTFM measurements.

Di Giammarco et al.[6] reported the results of 304 grafts in 157 patients who underwent intraoperative TTFM and postoperative angiography at a mean follow-up of 6.7±4.8 months after surgery. The peak flow, MGF, PI, and percent reflux were found to be independent predictors of graft failure in 38 grafts. The receiver operating characteristic (ROC) curve analysis concluded that MGF <15 mL/min, PI >3, and percent reflux >3% were more accurate predictors of adverse short-term outcomes. In another study evaluating the TTFM results of 1000 arterial grafts in 336 patients, mortality following non-emergency surgery was significantly higher in patients with PI >5 than in patients with PI ≤5.[16] Q uin et a l.[17] also found better patency rates in the group with TTFM at one year follow-up compared to those without (p<0.01). In the same study, the graft rates in at least one occlusion were lower in patients with TTFM measurement (p=0.01). In our study, we targeted these limit values specified in the literature for flowmetric measurements in grafts.

In the 2018 European Society of Cardiology/ European Association for Cardio-Thoracic Surgery (ESC/EACTS) Myocardial Revascularization Guidelines, routine intraoperative TTFM measurement is recommended with a Class IIA (Level of Evidence B) recommendation.[18] Intraoperative flow imaging is a method that has been increasingly used in cardiac surgery in recent years and is used to evaluate coronary anatomy intraoperatively using fluorescent images created with ICG. In a study conducted by Desai et al.,[19] 8.6% of 139 grafts were abnormal/occluded in CAG. The IFI detected 83% of these abnormal/occluded grafts. However, there is a concern in creating adequate images in pedicled LIMA, radial artery and saphenous vein grafts. Again, during the intramyocardial course of the coronary arteries, it becomes difficult to create a fluorescent image due to the thickening of epicardial fat tissues. In addition, due to the positions given to the heart for the purpose of imaging the grafts, the grafts, anastomosis areas and distal coronary bed are examined when they are not in their natural position. During these positions given to the heart, blood flow to the coronary arteries is disrupted. In our clinic, we prefer using all arterial and venous grafts as pedicled. Although this approach makes it more challenging to fully evaluate all grafts, unlike other intraoperative flow imaging studies, we were able to obtain sufficient information regarding flow after revascularization. We maintained the advantages of pedicled grafts by performing quantitative measurements at segments where the distal coronary artery became superficial following anastomosis. Another downside to IFI is cost. Takahashi et al.[20] reported that the cost of the procedure in Europe was 200 to 350 Euros per patient.

The Graft Imaging to Improve Patency (GRIIP) clinical trial reported that intraoperative TTFM and ICG fluorescence measurements did not show a significant difference in mortality, MI, and repeat revascularization after one year compared to patients who did not undergo intraoperative graft evaluation.[21] However, the study was probably underpowered in terms of the reported results and included a small number of patients. Furthermore, only four (1.7%) grafts in this study had isolated TTFM measurements, providing limited information on the true efficacy of TTFM. However, the same study also found no significant difference between patients who underwent only TTFM and only IFI. Similarly, in our study, we found no additional benefit of IFI on early outcomes of CABG when used alongside TTFM.

In a meta-analysis on the effect of TTFM measurement, revision was performed in 4.3% of patients and 2.0% of total grafts.[14] Series based on IFI reported a graft revision rate between 1.4% and 4.2%.[20,22] The proximal LIMA stenosis/dissection, inadequate distal coronary bed, anastomotic stenosis, kinked, twisted, and short grafts are among the reasons for graft revision.[15,23] In our patients, no graft revision was required in the TTFM and TTFM+IFI groups. In our routine practice, we have been using TTFM for many years in all CABG procedures. Likely due to our routine practice of proactively identifying and addressing potential technical issues with grafts failure before they arise, none of the grafts in our series required revision. In our study comparing patients who underwent isolated on-pump CABG by the same surgical team and the same procedures, we attempted to measure the contribution of IFI to postoperative results without giving up TTFM measurements in any patient. Comparing demographic characteristics and preoperative risk factors, we found no significant difference between the two groups except for the number of vessels bypassed. In our study comparing the results in the first month after surgery, no statistically significant difference was observed in terms of early survival, postoperative MI, need for IABP, need for ECMO, EF preservation, length of ICU stay, and discharge time.

Our inability to reach larger patient groups due to cost issues is a limiting factor for our study. Further multi-center, large-scale, prospective, randomized-controlled studies are needed to investigate intraoperative problems related to grafts, which is one of the major technical aspects of coronary artery bypass grafting.

In conclusion, one of the crucial ways to achieve more satisfactory results in coronary artery bypass grafting is to improve the quality of grafts and anastomosis, to detect possible problems during the operation and to make the necessary corrections. Our study showed that indocyanine fluorescence imaging did not contribute to the operation in any additional way compared to Transit-time flowmeter measurement. In addition, indocyanine fluorescence imaging increased the costs and prolonged the operation times, although it was not statistically significant. Based on these findings, we conclude that Transit-time flowmeter measurement measurements alone, which have been used for many years for intraoperative graft evaluation, are sufficient. We believe that, as the number of such studies increases, coronary artery bypass grafting results would be associated with more favorable early and long-term results.

Data Sharing Statement: The data that support the findings of this study are available from the corresponding author upon reasonable request.

Author Contributions: Idea/concept: H.U., A.Ç., U.K., I.J.; Design: H.U., A.Ç., I.J., A.Y.; Control/supervision: H.U., A.Ç., U.K., M.C., I.J., A.Y.; Data collection and/or processing: H.U., A.Y.; Analysis and/or interpretation: H.U., M.C., I.J., A.Y.; Literature review: H.U., A.Ç., I.J.; Writing the article: H.U., A.Ç., M.C., A.Y.; Critical review: H.U., U.K., I.J., A.Y.; References and fundings: H.U.; Materials: H.U.; A.Ç., I.J.; Other: A.Y.

Conflict of Interest: The authors declared no conflicts of interest with respect to the authorship and/or publication of this article.

Funding: The authors received no financial support for the research and/or authorship of this article.

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