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Adult: Coronary| Volume 15, P95-106, October 2022

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Graft flow evaluation with intraoperative transit-time flow measurement in off-pump versus on-pump coronary artery bypass grafting

Open AccessPublished:May 17, 2022DOI:https://doi.org/10.1016/j.xjtc.2022.05.002

      Abstract

      Objective

      We aimed to compare transit-time flow measurement (TTFM) parameters for on-pump (ONCAB) and off-pump (OPCAB) coronary artery bypass procedures.

      Methods

      The database of the Registry for Quality AssESsmenT with Ultrasound Imaging and TTFM in Cardiac Bypass Surgery (REQUEST) study was retrospectively reviewed. Only single grafts were included (ie, no sequential or Y/T grafts). Primary end points were mean graft flow (MGF), pulsatility index (PI), diastolic fraction (DF), and backflow (BF). Unadjusted and propensity score-matching comparisons were performed.

      Results

      Of 1016 patients in the REQUEST registry, 846 had at least 1 graft for which TTFM was performed. Of these, 512 patients (60.6%) underwent ONCAB and 334 (39.4%) OPCAB procedures. Mean arterial pressure (MAP) during measurements was higher in the OPCAB group. After propensity score-matching, 312 well balanced pairs were left. In these matched patients, MGF was higher for the ONCAB versus the OPCAB group (32 vs 28 mL/min, respectively, for all grafts [P < .001]; 30 vs 27 mL/min for arterial grafts [P = .002]; and 35 vs 31 mL/min for venous grafts [P = .006], respectively). PI was lower in the ONCAB group (2.1 vs 2.3, for all grafts; P < .001). Diastolic fraction was slightly lower in the ONCAB group (65% vs 67.5%; P < .001). The backflow was also lower in the ONCAB group (0.6 vs 1.3; P < .001) with trends similar to MGF and PI for venous and arterial grafts. There were 21 (3.3%) revisions in the OPCAB group and 14 (2.1%) in the ONCAB group (P = .198).

      Conclusions

      ONCAB surgery was associated with higher MGF and lower PI values, especially in venous grafts. Different TTFM cutoff values for ONCAB versus OPCAB surgery might be considered.

      Graphical abstract

      Figure thumbnail fx1

      Key Words

      Abbreviations and Acronyms:

      ACI (acoustic coupling index), BF (backflow), CABG (coronary artery bypass grafting), DF (diastolic fraction), LAD (left anterior descending), LIMA (left internal mammary artery), MAP (mean arterial pressure), MGF (mean graft flow), OM (obtuse marginal), ONCAB (on-pump coronary artery bypass), OPCAB (off-pump coronary artery bypass), PI (pulsatility index), PSM (propensity score matching), RA (radial artery), REQUEST (Registry for Quality AssESsmenT with Ultrasound Imaging and TTFM in Cardiac Bypass Surgery), RIMA (right internal mammary artery), SVG (saphenous vein graft), TTFM (transit-time flow measurement)
      Figure thumbnail fx2
      Typical result of a graft evaluation using TTFM.
      On-pump bypass surgery was associated with higher flows and lower pulsatility indices than off-pump coronary bypass.
      We sought to investigate if there is a difference in TTFM parameters between on-pump and off-pump CABG. We found that on-pump surgery was associated with higher mean graft flows and lower pulsatility indices, especially in venous grafts. Different TTFM cutoff values for on-versus off-pump bypass surgery might be considered.
      Technological advances paved the way for the development of devices that can be used to assess grafts for intraoperative failure. Graft patency can be measured in various ways, but the most widespread technique is transit-time flow measurement (TTFM) because of its ease of use.
      • Thuijs D.J.F.M.
      • Bekker M.W.A.
      • Taggart D.P.
      • Kappetein A.P.
      • Kieser T.M.
      • Wendt D.
      • et al.
      Improving coronary artery bypass grafting: a systematic review and meta-analysis on the impact of adopting transit-time flow measurement.
      A meta-analysis by Thuijs and colleagues
      • Thuijs D.J.F.M.
      • Bekker M.W.A.
      • Taggart D.P.
      • Kappetein A.P.
      • Kieser T.M.
      • Wendt D.
      • et al.
      Improving coronary artery bypass grafting: a systematic review and meta-analysis on the impact of adopting transit-time flow measurement.
      revealed a pooled rate of graft revisions of 4.3% per patient, and 2.0% per graft. In the grafts with an abnormal measurement, the pooled rate of graft revision was 25.1%. This frequency implies that there will be improvement in clinical outcomes with higher adoption rates and improved quality of intraoperative graft assessment,
      • Niclauss L.
      Techniques and standards in intraoperative graft verification by transit time flow measurement after coronary artery bypass graft surgery: a critical review.
      as shown in the recent Registry for Quality AssESsmenT with Ultrasound Imaging and TTFM in Cardiac Bypass Surgery (REQUEST) trial.
      • Taggart D.P.
      • Thuijs D.J.F.M.
      • Di Giammarco G.
      • Puskas J.D.
      • Wendt D.
      • Trachiotis G.D.
      • et al.
      Intraoperative transit-time flow measurement and high-frequency ultrasound assessment in coronary artery bypass grafting.
      There is still debate regarding the possible advantages and disadvantages of on-pump (ONCAB) versus off-pump (OPCAB) coronary artery bypass graft procedures.
      • Lamy A.
      • Devereaux P.J.
      • Prabhakaran D.
      • Taggart D.P.
      • Hu S.
      • Straka Z.
      • et al.
      Five-year outcomes after off-pump or on-pump coronary-artery bypass grafting.
      • Shroyer A.L.
      • Hattler B.
      • Wagner T.H.
      • Collins J.F.
      • Baltz J.H.
      • Quin J.A.
      • et al.
      Five-year outcomes after on-pump and off-pump coronary-artery bypass.
      • Chikwe J.
      • Lee T.
      • Itagaki S.
      • Adams D.H.
      • Egorova N.N.
      Long term outcomes after off-pump versus on-pump coronary artery bypass grafting by experienced surgeons.
      Regardless of these perceived advantages and disadvantages, few previous reports have compared the flow rates in these 2 types of procedures, and conflicting results have been reported.
      • Schmitz C.
      • Ashraf O.
      • Schiller W.
      • Preusse C.J.
      • Esmailzadeh B.
      • Likungu J.A.
      • et al.
      Transit time flow measurement in on-pump and off-pump coronary artery surgery.
      • Kjaergard H.K.
      • Irmukhamedov A.
      • Christensen J.B.
      • Schmidt T.A.
      Flow in coronary bypass conduits on-pump and off-pump.
      • Hassanein W.
      • Albert A.A.
      • Arnrich B.
      • Walter J.
      • Ennker I.C.
      • Rosendahl U.
      • et al.
      Intraoperative transit time flow measurement: off-pump versus on-pump coronary artery bypass.
      • Balacumaraswami L.
      • Abu-Omar Y.
      • Selvanayagam J.
      • Pigott D.
      • Taggart D.P.
      The effects of on-pump and off-pump coronary artery bypass grafting on intraoperative graft flow in arterial and venous conduits defined by a flow/pressure ratio.
      • Amin S.
      • Madsen P.L.
      • Werner R.S.
      • Krasopoulos G.
      • Taggart D.P.
      Intraoperative flow profiles of arterial and venous bypass grafts to the left coronary territory.
      However, these studies were limited by being either single-center series, by a relatively small sample size, or by type of grafts used and the parameters measured. If differences in flow rates do indeed exist, this discrepancy might suggest that there should be different thresholds for the TTFM parameters when evaluating graft quality in ONCAB versus OPCAB.
      In this study, we sought to quantify differences in TTFM parameters for ONCAB and OPCAB using a retrospective review of the REQUEST trial—a large, multicenter cohort. Any existing differences could be used to help correlate successful procedures with specific cutoff values for each type of procedure, and eventually improve the quality of intraoperative decision-making in coronary artery bypass grafting (CABG).

      Methods

      Study Design

      REQUEST is an international, multicenter, prospective registry that enrolled 1016 patients in 7 cardiac surgery centers (4 in Europe and 3 in North America) between April 2015 and December 2017. Patients underwent isolated CABG with intraoperative assessment of multiple surgical sites, such as the ascending aorta (for cannulation, crossclamping, and proximal anastomoses, if any), coronary targets, conduits, and finally proximal and distal anastomoses, using high-frequency ultrasound and graft assessment using transit time flowmetry (TTFM) with the MiraQ or VeriQ C devices (Medistim ASA).
      The registry was designed to capture information on any changes in the proposed surgical procedure on the basis of high-frequency ultrasound and/or TTFM findings. The results, along with the study protocol, were reported in a previous publication.
      • Taggart D.P.
      • Thuijs D.J.F.M.
      • Di Giammarco G.
      • Puskas J.D.
      • Wendt D.
      • Trachiotis G.D.
      • et al.
      Intraoperative transit-time flow measurement and high-frequency ultrasound assessment in coronary artery bypass grafting.
      Institutional review board approval from each participating center was obtained before screening and enrollment. Informed consent was obtained from all enrolled patients (approval number for the various institutions: site 1: June 30, 2015 [15-63060-BO]; site 2: April 23, 2015 [REB15-0090]; site 3: August 6, 2015 [HS 053-15]; site 4: June 18, 2015; site 5: April 22, 2015 [15/SC/0194]; site 6: April 24, 2015 [01,731]; and site 7: July 20, 2015 [MEC-2015-448]).
      The original REQUEST study
      • Taggart D.P.
      • Thuijs D.J.F.M.
      • Di Giammarco G.
      • Puskas J.D.
      • Wendt D.
      • Trachiotis G.D.
      • et al.
      Intraoperative transit-time flow measurement and high-frequency ultrasound assessment in coronary artery bypass grafting.
      was funded by Medistim. The principal investigators and authors had complete scientific freedom. This subanalysis received no funding. The study is registered at ClinicalTrials.gov (NCT02385344).

      Overall Patient Population

      Patients diagnosed with multivessel coronary artery disease and scheduled for isolated CABG were eligible to be included. Patients were excluded from enrollment if undergoing emergency surgery, when concomitant surgical procedures were planned (eg, valve repair or replacement, surgery for arrhythmias, etc), if the medical history included the presence of a muscle disorder (eg, myopathy, myalgia, myasthenia), or if the patient was known to be suffering from any psychological, developmental, or emotional disorder. The decision of performing the CABG operation with versus without the aid of cardiopulmonary bypass (ONCAB vs OPCAB) was left to the discretion of the operating surgeon.
      It was highly recommended, but not mandatory, to assess each conduit used for CABG intraoperatively using TTFM. Only TTFM studies with an acoustic coupling index (ACI; as a correlate of the quality or reliability of the TTFM measurements) >30% were included in the analysis.
      The following 4 TTFM parameters were defined as the primary outcome and were measured and recorded: mean graft flow (MGF; usually represented in mL/min and coupled with electrocardiogram), pulsatility index (PI; this is an absolute number that provides information on resistance and flow patterns with lower values representing lower resistance), diastolic fraction (DF; this is the percent of diastolic flow in the graft. Ideally, this should be more than 50%) and backflow (BF; this represents the percent of backward flow over the anastomosis during 1 cardiac cycle). Such parameters were measured after protamine administration for heparin reversal. When a graft was revised, the measurements included in the analysis were those measured after graft revision.

      Inclusion and Exclusion Criteria

      We considered only single grafts (ie, with only 1 distal anastomosis and no or 1 proximal anastomosis) with postprotamine TTFM performed with an ACI >30 (Figure 1). Sequential and Y/T grafts were therefore excluded from our analysis. We compared the median values of such parameters in ONCAB versus OPCAB procedures, considering all conduits (venous, arterial, and combined venous-arterial), completely arterial conduits, completely venous conduits, and specific conduit to target subsets: left internal mammary artery (LIMA) to left anterior descending (LAD), right internal mammary artery (RIMA) to LAD, RIMA to obtuse marginal (OM), radial artery (RA) to OM, RA to posterior descending artery, saphenous vein graft (SVG) to diagonal branch, SVG to OM, SVG to posterior descending artery, and SVG to right coronary artery.
      Figure thumbnail gr1
      Figure 1Inclusion and exclusion criteria. REQUEST, Registry for Quality Assessment with Ultrasound Imaging and TTFM in Cardiac Bypass Surgery; ACI, acoustic coupling index; TTFM, transit-time flow measurements; MGF, mean graft flow; PI, pulsatility index; DF, diastolic fraction; BF, backflow; ONCAB, on-pump coronary artery bypass; OPCAB, off-pump coronary artery bypass.

      Statistical Analysis

      Continuous data are reported as median (25th-75th percentile; ie, interquartile range), and categorical data as number (percentage). Comparisons were performed using the χ2, Fisher exact, and Wilcoxon rank sum tests as deemed appropriate (because normality was not established on the basis of Q-Q plots and the Shapiro–Wilk test), with the co-primary (ie, TTFM parameters) end points analyzed with P < .0125, taking into account multiple testing (Bonferroni correction). As a secondary analysis, propensity score matching (PSM; 1:1 ratio) was performed to balance the OPCAB and the ONCAB groups. The PSM was done using Greedy matching, and it was performed for all unbalanced variables (ie, age, body mass index, and New York Heart Association classification). The co-primary end points were analyzed with P < .0125, considering multiple testing (Bonferroni correction). We also analyzed the number of grafts not reaching specific parameter thresholds (MGF <20 mL/min, PI < 5, BF >3%, DF < 50%) and reviewed whether these grafts were revised. Analyses were performed using SAS 9.4 software (SAS Institute Inc).

      Results

      Patient Groups

      Of 1016 patients enrolled in the REQUEST registry, 846 had at least 1 single graft for which TTFM was performed (after protamine administration) with an ACI >30% and were included in our study (809 grafts were excluded for sequential grafting or Y/T grafting, 158 had an ACI <30%, and 519 grafts had both exclusion criteria). Of these, 512 patients (60.6%) underwent ONCAB and 334 (39.4%) OPCAB, corresponding to 1050 ONCAB grafts (61.1%) and 669 OPCAB grafts (38.9%).
      Baseline characteristics and postoperative in-hospital outcomes are reported in Table 1. Before PSM, patients in the ONCAB group were slightly older compared with the OPCAB patients (68 years vs 66 years, respectively; P = .006). Patients in the ONCAB group had a slightly lower rate of type 2 diabetes mellitus (28.3% vs 32.0%, respectively; P = .27). Other than age, the only other difference between groups was the body mass index, which was slightly lower for the ONCAB group than the OPCAB group (27.6 vs 28.3; P = .03). In-hospital morbidity and mortality rates were very low, with a numerically lower rate of stroke in the OPCAB group (1.8% for ONCAB vs 0.3% for OPCAB; P = .1) Use of PSM resulted in 2 well balanced groups of 312 patients each (Table 2).
      Table 1Baseline characteristics and in-hospital outcomes of patient who underwent on- versus off-pump coronary artery bypass grafting
      ONCAB (n = 512 patients)OPCAB (n = 334 patients)P value
      Baseline characteristics
       Age, y66.6 (9.9)65.1 (8.7).024
       Female sex14.3 (73/512)13.5 (45/334).75
       Body mass index28.4 (5.1)29 (5.3).07
       Diabetes mellitus28.3 (145/512)32.0 (107/334).25
       History of stroke5.7 (29/512)6.3 (21/334).71
       History of myocardial infarction35.2 (180/512)31.1 (104/334).23
       History of revascularization
      CABG0.4 (2/512)0.52
      PCI24.0 (123/512)26.4 (88/334).45
       NYHA classification
      I42.4 (197/465)31.1 (97/312).001
      II37.0 (172/465)50.6 (158/312)
      III16.8 (78/465)15.7 (49/312)
      IV3.9 (18/465)2.6 (8/312)
      In-hospital postoperative MACCE
       Death0.6 (3/512)0.9 (3/334).69
       Myocardial infarction0.4 (2/512)0.52
       Stroke1.2 (6/512)0.3 (1/334).25
       Repeat revascularization00NA
      Data are reported as mean (standard deviation) or %(n/N).
      ONCAB, On-pump coronary artery bypass; OPCAB, off-pump coronary artery bypass; CABG, coronary artery bypass grafting; PCI, percutaneous coronary intervention; NYHA, New York Heart Association; MACCE, major adverse cardiac and cerebrovascular events; NA, not applicable.
      Table 2Baseline characteristics and in-hospital outcomes of patient who underwent on-versus off-pump coronary artery bypass grafting after propensity score matching
      ONCAB (n = 312 patients)OPCAB (n = 312 patients)P Value
      Baseline characteristics
       Age, y65.3 (10.1)65.2 (8.7).87
       Female sex12.5 (39/312)13.5 (42/312).72
       Body mass index28.9 (4.9)28.9 (5.2).81
       Diabetes mellitus30.5 (95/312)32.7 (102/312).55
       History of stroke5.8 (18/312)6.1 (19/312).87
       History of myocardial infarction32.1 (100/312)31.4 (98/312).86
       History of revascularization
      CABG0.64 (2/312)0.50
      PCI26.9 (84/312)25.3 (79/312).65
       NYHA classification
      I31.1 (97/312)31.1 (97/312).88
      II49.4 (154/312)50.6 (158/312)
      III17.6 (55/312)15.7 (49/312)
      IV1.92 (6/312)2.6 (8/312)
      In-hospital postoperative MACCE
       Death0.64 (2/312)0.96 (3/312)>.99
       Myocardial infarction0.64 (2/312)0.50
       Stroke0.96 (3/312)0.32 (1/312).62
       Repeat revascularization00NA
      Data are reported as mean (standard deviation) or % (n/N).
      ONCAB, On-pump coronary artery bypass; OPCAB, off-pump coronary artery bypass; CABG, coronary artery bypass grafting; PCI, percutaneous coronary intervention; NYHA, New York Heart Association; MACCE, major adverse cardiac and cerebrovascular events; NA, not applicable.

      Grafts

      Results of the comparison of ONCAB and OPCAB grafts (per graft analysis after PSM) are reported in Table 3 and Figure 2. Of note, 64% of LAD grafts in the ONCAB group were available for analysis and 75% of the LAD grafts were available in the OPCAB group. Most of the exclusions in this group of grafts were because of sequential grafting with a low ACI being the second most common reason (no major between group differences). Of the 406 single LIMA grafts in this analysis, 4 (0.98%) were free grafts anastomosed to the aorta. Of the 62 single RIMA grafts available for analysis, 11 (17%) were free grafts. MAP during measurements was higher in the OPCAB group. MGF was higher for ONCAB versus OPCAB (32 mL/min vs 28 mL/min, respectively, for all grafts; P < .001). This difference was more pronounced in venous than in arterial grafts (35 mL/min vs 31 mL/min [P = .005] and 30 mL/min vs 27 mL/min [P = .002], respectively). MGF was higher in ONCAB procedures for most conduit to target subsets taken together (apart from RIMA to LAD and SVG to RCA).
      Table 3Comparison of transit time flowmetry parameters of on-versus off-pump coronary artery bypass procedures after propensity score matching
      ONCABOPCABP value
      Grafts, nValueGrafts, nValue
      All
       MGF63332 (20-54)62028 (18-40)<.001
       PI6332.1 (1.6-2.9)6202.3 (1.8-3.1)<.001
       DF55665 (57-72)56267.5 (59-75).0007
       BF6210.6 (0-2.7)5961.3 (0.1-3.8)<.001
      Arterial
       MGF30730 (18-49)35927 (16-36).002
       PI3072.2 (1.8-2.9)3592.3 (1.8-3).036
       DF27970 (63-75)32671 (63-76).081
       BF3011.3 (0.1-3.8)3451.6 (0.3-4.1).174
      Venous
       MGF32635 (21-58)26131 (19-44).005
       PI3261.9 (1.5-2.8)2612.4 (1.7-3.5)<.001
       DF27761 (54-67)23662 (54-69).055
       BF3200.2 (0-1.9)2511 (0-3.7)<.001
      LIMA to LAD
       MGF19434 (18-54)21226 (17-36).002
       PI1942.2 (1.8-2.9)2122.4 (2-3.1).006
       DF17071 (66-76)19374 (69-78).015
       BF1911.7 (0.2-4)2052.2 (0.5-5.1).062
      RIMA to LAD
       MGF531 (25-35)2131 (18-43).922
       PI52.1 (1.4-2.1)212.1 (1.7-3).378
       DF572 (72-74)2173 (70-77).744
       BF51.3 (0-1.9)201.6 (0.3-3.8).357
      RIMA to OM
       MGF2925 (19-32)718 (12-23).180
       PI292.2 (1.6-3.1)72.1 (1.7-2.3).688
       DF2769 (63-73)668 (62-72).606
       BF290.5 (0-2.8)70.1 (0-1.5).744
      RA to OM
       MGF1936 (23-58)3326 (13-44).061
       PI191.9 (1.4-3)332.3 (1.7-3.1).241
       DF1866 (61-77)2763 (59-72).577
       BF180.2 (0-3)291.2 (0.1-3.9).143
      RA to PDA
       MGF1334 (30-53)1726 (22-32).065
       PI131.7 (1.2-2)172 (1.7-2.7).160
       DF1365 (55-70)1760 (51-66).208
       BF120.2 (0-2.5)160.1 (0-1.2).902
      SVG to Diag
       MGF3137 (25-45)3430.5 (20-39).226
       PI311.9 (1.5-2.6)342 (1.8-2.4).406
       DF2669 (63-76)3071.5 (67-75).542
       BF310.3 (0-1.6)310.8 (0.1-2.6).121
      SVG to OM
       MGF10436.5 (19.5-61)7630 (20-44.5).084
       PI1041.8 (1.4-2.5)762.3 (1.7-3.3).002
       DF8663 (58-69)7164 (56-71).381
       BF1020.1 (0-2.1)741 (0-3.8).011
      SVG to PDA
       MGF9336 (20-52)8132 (19-48).344
       PI932.2 (1.6-3)812.5 (1.7-3.9).095
       DF8658.5 (52-63)7461 (54-66).305
       BF900.4 (0-2.1)780.8 (0-3.1).196
      SVG to RCA
       MGF5636 (24-75)3436.5 (25-49).303
       PI561.9 (1.3-2.9)342.6 (1.7-3.3).038
       DF4755 (47-61)3157 (48-62).339
       BF560.1 (0-1.1)320.9 (0-2.8).074
      Data are reported as median (interquartile range). Units: MGF, mL/min; DF, %; and BF, %. Postprotamine TTFM measurements.
      ONCAB, On-pump coronary artery bypass; OPCAB, off-pump coronary artery bypass; MGF, mean graft flow; PI, pulsatility index; DF, diastolic fraction; BF, backflow; LIMA, left internal mammary artery; LAD, left anterior descending artery; RIMA, right internal mammary artery; OM, obtuse marginal; RA, radial artery; SVG, saphenous vein graft; Diag, diagonal; PDA, posterior descending artery; RCA, right coronary artery.
      Figure thumbnail gr2
      Figure 2A, Mean graft flows and (B) pulsatility indices for on-pump coronary artery bypass (ONCAB) versus off-pump coronary artery bypass (OPCAB) in all grafts, arterial grafts, venous grafts, and according to territory: single grafts with ACI > 30. The box upper and lower limits represent the 75th and 25th quartiles, respectively. The lower and upper whiskers represent the minimum and maximum values of nonoutliers. The middle horizontal line represents the median and the circle represents the mean. Data are reported as medians. MGF, Mean graft flow; PI, pulsatility index; ACI, acoustic coupling index; LIMA, left internal mammary artery; LAD, left anterior descending; SVG, saphenous vein graft; OM, obtuse marginal; PDA, posterior descending artery.
      PI was lower in the ONCAB group (2.1 vs 2.3, for all grafts; P < .001). This difference was more pronounced in venous grafts than in arterial grafts (1.9 vs 2.4 [P < .001] and 2.2 vs 2.3 [P = .369], respectively). DF was slightly lower in the ONCAB group than in the OPCAB group (65% vs 67.5%, respectively; P < .001). The DF measured separately for venous and arterial grafts showed the same trend. The BF was also lower in ONCAB than in OPCAB (0.6 vs 1.3, respectively, for all grafts; P < .001) with similar trends for venous and arterial grafts as MGF and PI (Figure 3). Regarding anastomotic revisions, there were 21 (3.3%) revisions in the OPCAB group and 14 (2.1%) in the ONCAB group (P = .198; Table 4). In the OPCAB group, most of these revisions were for a LIMA to LAD and in the ONCAB there was a more equal distribution (Table 4). Between group comparisons of grafts that did not meet parameter thresholds showed that almost 50% of grafts had at least 1 parameter that did not reach the accepted parameter threshold (Table 5). The only parameter that was different between ONCAB and OPCAB was BF for which it was much more common for OPCAB patients to not reach the threshold (32.9% OPCAB vs 23.9% ONCAB; P = .006). For the 2 most common threshold parameters (ie, MGF and PI), we also checked whether grafts not reaching the thresholds were more likely to undergo revision and found no difference for the 2 groups (Table 5).
      Figure thumbnail gr3
      Figure 3Visual summary of main findings. CABG, Coronary artery bypass grafting; TTFM, transit-time flow measurement; OPCAB, off-pump coronary artery bypass; ONCAB, on-pump coronary artery bypass; PI, pulsatility index; MGF, mean graft flow; BF, backflow.
      Table 4Anastomotic revision rates and details according to group
      OPCAB (n = 627)ONCAB (n = 645)P value
      Revision rate21 (3.3%)14 (2.1%).20
      Grafts.29
       LIMA114
       RIMA25
       RA42
       SVG43
      Target.38
       LAD103
       DiagonalN/A1
       OM45
       RCA21
       PDA54
      Change.05
       Distal155
       Proximal21
       Other48
      OPCAB, Off-pump coronary artery bypass; ONCAB, on-pump coronary artery bypass; LIMA, left internal mammary artery; RIMA, right internal mammary artery; RA, radial artery; SVG, saphenous vein graft; LAD, left anterior descending artery; OM, obtuse marginal; RCA, right coronary artery; PDA, posterior descending artery.
      Table 5Grafts not reaching threshold parameters and revision rates
      Parameter (threshold)OPCAB, %ONCAB, %P value
      Any abnormal parameter298 (47.5%)291 (45.1%).38
      MGF (<20 mL/min)

      Revisions
      206 (33.2%)

      11 (5.3%)
      172 (27.1%)

      6 (3.5%)
      .02

      .38
      PI (>5)

      Revisions
      41 (6.6%)

      7 (17%)
      31 (4.9%)

      2 (6.45%)
      .19

      .28
      DF (<50%)56 (9.96%)75 (13.5%).06
      BF (>3%)196 (32.8%)149 (23.9%).0006
      OPCAB, Off-pump coronary artery bypass; ONCAB, on-pump coronary artery bypass; MGF, mean graft flow; PI, pulsatility index; DF, diastolic fraction; BF, backflow.

      Discussion

      In one of the largest multicenter cohorts existing thus far, ONCAB MGF was higher than OPCAB MGF and ONCAB PI was lower than OPCAB PI, despite consistently higher MAP values during measurement in the OPCAB patients. This finding was true for all grafts and for most coronary territories, but the difference was more pronounced in venous than in arterial grafts. The difference in MGF values ranged from no difference (RIMA to LAD and SVG to RCA) to 10 mL/min (RA to OM; P = .061) whereas the difference in PI ranged from no difference (RIMA to OM and RIMA to LAD) to 0.5 (SVG to OM; P = .002). These differences in MGF and PI for ONCAB and OPCAB could be an inherent characteristic of the procedures (ie, due to vasodilatation resulting from the use of cardiopulmonary bypass and the reactive hyperemia resulting from ischemic arrest) or a sign of the higher technical demands of OPCAB grafting. Regardless of the reason—this difference might have clinical implications, especially regarding MGF in venous grafts for which differences were substantial compared with the accepted cutoff value of 20 mL/min.
      Previous reports have shown conflicting results regarding whether the differences in MGF and PI are inherent to the procedures themselves or a marker of the technical difficulty of OPCAB.
      • Schmitz C.
      • Ashraf O.
      • Schiller W.
      • Preusse C.J.
      • Esmailzadeh B.
      • Likungu J.A.
      • et al.
      Transit time flow measurement in on-pump and off-pump coronary artery surgery.
      • Kjaergard H.K.
      • Irmukhamedov A.
      • Christensen J.B.
      • Schmidt T.A.
      Flow in coronary bypass conduits on-pump and off-pump.
      • Hassanein W.
      • Albert A.A.
      • Arnrich B.
      • Walter J.
      • Ennker I.C.
      • Rosendahl U.
      • et al.
      Intraoperative transit time flow measurement: off-pump versus on-pump coronary artery bypass.
      • Balacumaraswami L.
      • Abu-Omar Y.
      • Selvanayagam J.
      • Pigott D.
      • Taggart D.P.
      The effects of on-pump and off-pump coronary artery bypass grafting on intraoperative graft flow in arterial and venous conduits defined by a flow/pressure ratio.
      • Amin S.
      • Madsen P.L.
      • Werner R.S.
      • Krasopoulos G.
      • Taggart D.P.
      Intraoperative flow profiles of arterial and venous bypass grafts to the left coronary territory.
      Schmitz and colleagues
      • Schmitz C.
      • Ashraf O.
      • Schiller W.
      • Preusse C.J.
      • Esmailzadeh B.
      • Likungu J.A.
      • et al.
      Transit time flow measurement in on-pump and off-pump coronary artery surgery.
      reported significantly lower graft flow values in the OPCAB group but with less myocardial damage, as reflected by lower postoperative cardiac enzyme levels in the OPCAB group (896 patients, 695 ONCAB and 201 OPCAB), with a total of 2247 grafts (1952/295, respectively). They attributed the higher flow rates and the higher levels of cardiac enzymes in the ONCAB group to myocardial hyperemia in response to metabolic acidosis caused by myocardial ischemia during crossclamp application. In contrast, Kjaergard and colleagues
      • Kjaergard H.K.
      • Irmukhamedov A.
      • Christensen J.B.
      • Schmidt T.A.
      Flow in coronary bypass conduits on-pump and off-pump.
      reported no significant difference in graft flow values for the ONCAB and OPCAB groups after correction for flow per anastomosis; they attributed the lower total flow rates in the OPCAB group to fewer total grafts (120 ONCAB, 97 OPCAB). Hassanein and colleagues
      • Hassanein W.
      • Albert A.A.
      • Arnrich B.
      • Walter J.
      • Ennker I.C.
      • Rosendahl U.
      • et al.
      Intraoperative transit time flow measurement: off-pump versus on-pump coronary artery bypass.
      reported lower OPCAB graft flow rates and higher PI values in all myocardial territories except for the LAD territory, which had flow rates and PI values similar to the ONCAB group (445 OPCAB patients paired with 445 ONCAB with 845 bypasses in each group). They concluded that this discrepancy between the OPCAB flow rates and PI of the LAD territory and the other territories might be the result of technical reasons related to accessibility of target vessels in the lateral and posterior territories. Balacumaraswami and colleagues
      • Balacumaraswami L.
      • Abu-Omar Y.
      • Selvanayagam J.
      • Pigott D.
      • Taggart D.P.
      The effects of on-pump and off-pump coronary artery bypass grafting on intraoperative graft flow in arterial and venous conduits defined by a flow/pressure ratio.
      reported higher MGF and a higher flow-to-pressure ratio (because MGF is dependent on MAP) for all conduits in the ONCAB group despite a significantly lower MAP (80 OPCAB patients and 20 ONCAB; 203/63 grafts, respectively). They offered 2 explanations for this finding—the aforementioned increase in coronary blood flow as a result of ischemia in ONCAB and systemic vasodilatation as a result of a more pronounced inflammatory response in the ONCAB. Last, in a more recent report, Amin and colleagues
      • Amin S.
      • Madsen P.L.
      • Werner R.S.
      • Krasopoulos G.
      • Taggart D.P.
      Intraoperative flow profiles of arterial and venous bypass grafts to the left coronary territory.
      focused on grafts to the left system, reported higher flows in arterial grafts in ONCAB versus OPCAB (with higher MGF rates measured in the arterial and the venous grafts compared with the REQUEST database). They reported no difference in PI for ONCAB and OPCAB, both in arterial and venous grafts.
      In a recent meta-analysis of intraoperative graft flow profiles ONCAB versus OPCAB MGF was compared as a secondary outcome.
      • Silva M.
      • Rong L.Q.
      • Naik A.
      • Rahouma M.
      • Hameed I.
      • Robinson B.
      • et al.
      Intraoperative graft flow profiles in coronary artery bypass surgery: a meta-analysis.
      The authors combined data from 8 studies with a total of 5041 grafts and reported MGF was higher in ONCAB versus OPCAB surgery with no difference in PI for the 2 procedures.
      The original REQUEST study
      • Taggart D.P.
      • Thuijs D.J.F.M.
      • Di Giammarco G.
      • Puskas J.D.
      • Wendt D.
      • Trachiotis G.D.
      • et al.
      Intraoperative transit-time flow measurement and high-frequency ultrasound assessment in coronary artery bypass grafting.
      was designed to prospectively evaluate the implementation of intraoperative graft quality assessment with TTFM and high-frequency ultrasound. It enrolled 1046 patients who underwent CABG, 30 of whom were excluded on the basis of predetermined criteria. Of the procedures, 39.6% (402/1016) were performed off-pump with a total of 1606 ONCAB grafts and 1069 OPCAB grafts. There was no difference in in-hospital mortality for the 2 groups. There was also no difference in in-hospital major cardiac and cerebrovascular events, strokes or transient ischemic attacks, myocardial infarctions, or repeat revascularizations. We retrospectively reviewed the REQUEST database to compare TTFM parameters for ONCAB versus OPCAB procedures. MGF was higher for ONCAB versus OPCAB (32 mL/min vs 28 mL/min, respectively, for all grafts; P < .001). This difference was more pronounced in venous than in arterial grafts (35 mL/min vs 31 mL/min [P = .005] and 30 mL/min vs 27 mL/min [P = .002], respectively). The PI was lower in the ONCAB versus the OPCAB group (2.1 vs 2.3, respectively; P < .001) with a more pronounced difference in the venous grafts.
      Anastomotic revision rates were lower in this specific cohort (3.3% OPCAB, 2.1% ONCAB; Table 4) than in the REQUEST trial. This might stem from the fact that we used only single grafts in this analysis (in an attempt to reduce confounding) and thus less complex grafting required fewer revisions. There were more LIMA to LAD revisions in the OPCAB group, but the numbers were small, preventing comparison.
      When interpreting TTFM values as threshold values (Table 5) we found that almost 50% of grafts had at least 1 parameter that did not meet parameter thresholds. Regarding revision rates for the most frequently used parameters (MGF and PI), we could not ascertain that surgeons have a different approach to cutoff values for OPCAB and ONCAB.

      Conclusions

      In our cohort, the increased MGF in ONCAB procedures did not correlate with better in-hospital clinical outcomes in the REQUEST trial. This finding is in accordance with previous studies that showed comparable postoperative angiographic patency for ONCAB and OPCAB, despite these reduced TTFM parameters.
      • Puskas J.D.
      • Williams W.H.
      • Mahoney E.M.
      • Huber P.R.
      • Block P.C.
      • Duke P.G.
      • et al.
      Off-pump vs conventional coronary artery bypass grafting: early and 1-year graft patency, cost, and quality-of-life outcomes: a randomized trial.
      ,
      • Lingaas P.S.
      • Hol P.K.
      • Lundblad R.
      • Rein K.A.
      • Mathisen L.
      • Smith H.J.
      • et al.
      Clinical and radiologic outcome of off-pump coronary surgery at 12 months follow-up: a prospective randomized trial.
      It follows that the lower flow rates and higher PI values measured in OPCAB surgery could be intrinsic to the procedure. These differences probably result from the lack of ischemia (and subsequent hyperemia) in OPCAB.
      • Jin X.Y.
      • Gibson D.G.
      • Pepper J.R.
      The effects of cardioplegia on coronary pressure-flow velocity relationships during aortic valve replacement.
      If this hypothesis is true, then we must examine the clinical implications that these data might have. We need to consider for example, the higher immediate graft flow in ONCAB (especially when using venous grafts) when choosing the most appropriate surgical revascularization technique in an urgent scenario (ie, a patient in an acute myocardial infarction or in cardiogenic shock) versus an elective CABG. Furthermore, investigation is needed to correlate off- and on-pump parameters with graft patency and determine specific, clinically significant cutoff values for each type of procedure because lower MGF might still be satisfactory in the OPCAB patient. This is especially relevant when considering that a cutoff value of MGF >20 mL/min is considered adequate and the difference in flow for OPCAB and ONCAB reached 10 mL/min in some of the grafts in our study. By tracking this change in flow for ONCAB versus OPCAB we hope to improve intraoperative decision-making in the evaluation of graft quality using TTFM (Video Abstract).

      Limitation

      The major limitation of this study stems from the lack of randomization of the patients in the REQUEST trial to ONCAB versus OPCAB. Furthermore, there was no equal distribution of OPCAB procedures performed in the various participating centers. As such, the differences in flow parameters in this study might have been the result of unidentified and unmeasured confounding variables for ONCAB and OPCAB patients not controlled for by PSM or the result of divergent surgical techniques of the different centers. Follow-up was limited to 30 days with no angiographic results, limiting our ability to draw clinical conclusions from our findings.

      Webcast

      You can watch a Webcast of this AATS meeting presentation by going to: https://www.aats.org/resources/1944.
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      Conflict of Interest Statement

      D. J. Thuijs, G. Di Giammarco, D. Wendt, T. M. Kieser, A. P. Kappetein, S. J. Head, J. D. Puskas, and D. P. Taggart reported traveling support/speaking fees from Medistim. A. P. Kappetein and S. J. Head reported Medtronic employment. D. P. Taggart reported Medistim research funding, speaking, traveling honoraria, and consultant. All other authors reported no conflicts of interest.
      The Journal policy requires editors and reviewers to disclose conflicts of interest and to decline handling or reviewing manuscripts for which they may have a conflict of interest. The editors and reviewers of this article have no conflicts of interest.

      Supplementary Data

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