Intraoperative graft patency validation: Friend or foe?
Rami Akhrass, Faisal G. Bakaeen
Abstract
Central MessageGraft flow assessment is a useful quality assurance adjunct but not a substitute for good technique and sound judgment. Judicious interpretation of flow readings ensures unnecessary graft revisions.See Commentaries on pages 138, 140, 142, and 144. Graft flow assessment is a useful quality assurance adjunct but not a substitute for good technique and sound judgment. Judicious interpretation of flow readings ensures unnecessary graft revisions. See Commentaries on pages 138, 140, 142, and 144. It is estimated that 3% to 5% of internal thoracic artery (ITA) and 20% of saphenous vein grafts (SVGs) fail at 1 year, frequently attributed to technical issues.1Balacumaraswami L. Taggart D.P. Intraoperative imaging techniques to assess coronary artery bypass graft patency.Ann Thorac Surg. 2007; 83: 2251-2257Abstract Full Text Full Text PDF PubMed Scopus (85) Google Scholar The PREVENT IV (Project of Ex-vivo Vein Graft Engineering via Transfection) trial reported a 30% vein graft failure rate at 1 year, most without a major adverse cardiac event.2Alexander J.H. Hafley G. Harrington R.A. Peterson E.D. Ferguson T.B. Lorenz T.J. et al.Efficacy and safety of edifoligide, an E2F transcription factor decoy, for prevention of vein graft failure following coronary artery bypass graft surgery: PREVENT IV: a randomized controlled trial.J Am Med Assoc. 2005; 294: 2446-2454Crossref PubMed Scopus (537) Google Scholar Coronary artery bypass grafting (CABG) in the United States is typically performed on cardiopulmonary bypass (CPB), which provides surgeons with good visualization in a bloodless and motionless field, allowing them to “perfect” their work! In addition, greater than 85% of all grafts in the United States use SVGs as conduits that are forgiving and easy-to-use.3Aldea G.S. Bakaeen F.G. Pal J. Fremes S. Head S.J. Sabik J. et al.The Society of Thoracic Surgeons clinical practice guidelines on arterial conduits for coronary artery bypass grafting.Ann Thorac Surg. 2016; 101: 801-809Abstract Full Text Full Text PDF PubMed Scopus (197) Google Scholar Once the distal anastomosis is completed, selective perfusion of the vein graft provides flow measurements and solid information of a successful anastomosis. The improved graft patency and clinical outcomes with arterial conduits compared with veins have increased calls for multiarterial grafting (MAG) and to maximize myocardial supply by ITA grafts.3Aldea G.S. Bakaeen F.G. Pal J. Fremes S. Head S.J. Sabik J. et al.The Society of Thoracic Surgeons clinical practice guidelines on arterial conduits for coronary artery bypass grafting.Ann Thorac Surg. 2016; 101: 801-809Abstract Full Text Full Text PDF PubMed Scopus (197) Google Scholar, 4Loop F.D. Lytle B.W. Cosgrove D.M. Stewart R.W. Goormastic M. Williams G.W. Influence of the internal-mammary-artery graft on 10-year survival and other cardiac events.N Engl J Med. 1986; 314: 1-6Crossref PubMed Scopus (2163) Google Scholar, 5Lytle B.W. Blackstone E.H. Loop F.D. Houghtaling P.L. Arnold J.H. Akhrass R. et al.Two internal thoracic artery grafts are better than one.J Thorac Cardiovasc Surg. 1999; 117: 855-872Abstract Full Text Full Text PDF PubMed Scopus (718) Google Scholar, 6Rocha R.V. Tam D.Y. Karkhanis R. Nedadur R. Fang J. Tu J.V. et al.Multiple arterial grafting is associated with better outcomes for coronary artery bypass grafting patients.Circulation. 2018; 138: 2081-2090Crossref PubMed Scopus (30) Google Scholar, 7Bakaeen F.G. Ravichandren K. Blackstone E.H. Houghtaling P.L. Soltesz E.G. Johnston D.R. et al.Coronary artery target selection and survival after bilateral internal thoracic artery grafting.J Am Coll Cardiol. 2020; 75: 258-268Crossref PubMed Scopus (22) Google Scholar However, arteries are more delicate and susceptible to injuries, such as dissections and hematomas, that may compromise flow. In addition, arteries are “dynamic” structures with flow substantially influenced by a myriad of factors, such as spasm, hemodynamic parameters, and target-vessel specifications (especially the severity of stenosis), making routine intraoperative flow verification prudent. From a quality assurance perspective, validation of intraoperative graft patency provides the opportunity, if needed, to correct any technical issues before leaving the operating room. Since intraoperative completion angiography is impractical and rarely performed, other flow and imaging modalities have made the stage, but their role and value in modern-day practice continues to evolve. Here, we review some of the available tools to assess intraoperative graft patency and evaluate their impact on the conduct and outcomes of CABG. Several modalities that can aid in verifying conduit patency. TTFM (Figure 1) is based on the difference between the transit time of ultrasonic energy from 2 transducers in a probe passing through a liquid.8Kieser T.M. Graft quality verification in coronary artery bypass graft surgery: how, when and why?.Curr Opin Cardiol. 2017; 32: 722-736Crossref PubMed Scopus (11) Google Scholar Basic knowledge of TTFM is easy to grasp, with a quick learning curve. Flow characteristics may vary depending on hemodynamics, postbypass myocardial recovery, spasm, or air in the graft. Several measurements should be taken before rushing into graft revisions, unless a cause is identified. TTFM cut-off values that were shown to influence patency are as follows8Kieser T.M. Graft quality verification in coronary artery bypass graft surgery: how, when and why?.Curr Opin Cardiol. 2017; 32: 722-736Crossref PubMed Scopus (11) Google Scholar, 9Thuijs D.J.F.M. Bekker M.W.A. Taggart D.P. Pieter Kappetein A. 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.Eur J Cardiothorac Surg. 2019; 56: 654-663Crossref PubMed Scopus (17) Google Scholar, 10Di Giammarco G. Pano M. Cirmeni S. Pelini P. Vitolla G. Di Mauro M. Predictive value of intraoperative transit-time flow measurement for short-term graft patency in coronary surgery.J Thorac Cardiovasc Surg. 2006; 132: 468-474Abstract Full Text Full Text PDF PubMed Scopus (105) Google Scholar, 11Di Giammarco G. Canosa C. Foschi M. Rabozzi R. Marinelli D. Masuyama S. et al.Intraoperative graft verification in coronary surgery: increased diagnostic accuracy adding high-resolution epicardial ultrasonography to transit-time flow measurement.Eur J Cardiothorac Surg. 2014; 45: 41-45Crossref PubMed Scopus (44) Google Scholar:1.Flow: acceptable >20 mL/min.2.Pulsatility index (PI): measures resistance. It is the difference between the maximum and minimum flow divided by the mean flow. PI = Qmax – Qmin/Qmean (Q = flow). Ideally, PI is <3; acceptable <5.3.Diastolic filling (DF) is defined as the percentage of coronary filling during diastole (60%-70% for the left and 50%-60% for the right coronary).4.Back flow or insufficiency ratio: flow back into the conduit. Typically, this should be less than 3% and is closely related to PI. TTFM is measured at 4 intervals:1.Once the distal anastomosis is completed and crossclamp still on. PI should be very low, with flatness of the curve due to nonpulsatile pump flow.2.This is optional: same as stated previously, but with manual or snare proximal target occlusion (PTO), reducing retrograde flow into the coronary that may contribute to increased false negativity (TTFM good but bypass bad with distal obstruction).3.Off-pump before administration of protamine. PTO may be performed if concerned about competitive flow.4.Before chest closure. ECUS is typically performed in conjunction with TTFM and best performed on a resting heart, providing an anatomical picture of the anastomosis and bypass graft. In one study, the false positivity of TTFM was dramatically lowered with the addition of ECUS, where only 2 of 39 grafts initially labeled as “failed” were reclassified as such.11Di Giammarco G. Canosa C. Foschi M. Rabozzi R. Marinelli D. Masuyama S. et al.Intraoperative graft verification in coronary surgery: increased diagnostic accuracy adding high-resolution epicardial ultrasonography to transit-time flow measurement.Eur J Cardiothorac Surg. 2014; 45: 41-45Crossref PubMed Scopus (44) Google Scholar However, the majority of the false positivity was due to either retrograde or competitive flow, both can perhaps be excluded with PTO or “snare test.” ICG dye is excited with dispersed laser light creating an angiographic depiction of the graft, anastomosis, and native vessel. A randomized trial comparing TTFM with ICG found greater sensitivity and specificity with ICG12Desai N.D. Miwa S. Kodama D. Koyama T. Cohen G. Pelletier M.P. et al.A randomized comparison of intraoperative indocyanine green angiography and transit-time flow measurement to detect technical errors in coronary bypass grafts.J Thorac Cardiovasc Surg. 2006; 132: 585-594Abstract Full Text Full Text PDF PubMed Scopus (105) Google Scholar; however, it did not gain traction, perhaps due to its cumbersome use and need to obtain several views for complete graft visualization. Although it might be considered the gold standard, coronary angiography did not gain widespread adoption, due to the added time and needed personnel and hybrid operating rooms not commonly available. In a report by Hol and colleagues,13Desai N.D. Miwa S. Kodama D. Koyama T. Cohen G. Pelletier M.P. et al.Intraoperative angiography leads to graft revision in coronary artery bypass surgery.Ann Thorac Surg. 2004; 78: 502-505Abstract Full Text Full Text PDF PubMed Scopus (42) Google Scholar where post-CABG intraoperative angiography was carried out, a 4.2% immediate graft revision was undertaken (1.1% for on-pump vs 6.4% off-pump). An important finding was that two-thirds of the identified “lesions” were in the conduit itself rather than the anastomosis. Compromised flow may result from suboptimal techniques in conduit harvesting, anastomosis suturing, or misjudging the length or lay of a graft. A dissection or hematoma of an arterial graft, or a displaced clip of a branch, may compromise luminal flow and go unnoticed. “Purse-stringing” or “backwalling” during suture placement can narrow the inflow or outflow. A raised intimal flap or plaque disruption can be a threat to graft patency. While some problems such as a proximally located kink or twist in a graft are readily visible, other technical issues are perhaps less apparent and adjunct graft flow measurements or imaging modalities may add value. The flow through a graft can be borderline or even poor due to competitive native flow (Figure 2), seen when the stenosis of the target vessel is not severe. Reduced graft patency has been documented when the radial artery is used for moderate stenosis, leading to a “string sign.”14Cao C. Manganas C. Horton M. Bannon P. Munkholm-Larsen S. Ang S.C. et al.Angiographic outcomes of radial artery versus saphenous vein in coronary artery bypass graft surgery: a meta-analysis of randomized controlled trials.J Thorac Cardiovasc Surg. 2013; 146: 255-261Abstract Full Text Full Text PDF PubMed Scopus (71) Google Scholar Slightly reduced graft patency has been reported when the ITA is used to bypass a moderately diseased target.15Raza S. Blackstone E.H. Houghtaling P.L. Olivares G. Ravichandren K. Koprivanac M. et al.Natural history of moderate coronary artery stenosis after surgical revascularization.Ann Thorac Surg. 2018; 105: 815-821Abstract Full Text Full Text PDF PubMed Scopus (9) Google Scholar A correlation was documented between the degree of target vessel stenosis and the TTFMs of ITA grafts, where a “string sign” was noted in 50% of nonstenotic lesions (fractional flow reserve ≥0.75).16Honda K. Okamura Y. Nishimura Y. Uchita S. Yuzaki M. Kaneko M. et al.Graft flow assessment using a transit time flow meter in fractional flow reserve-guided coronary artery bypass surgery.J Thorac Cardiovasc Surg. 2015; 149: 1622-1628Abstract Full Text Full Text PDF PubMed Scopus (31) Google Scholar In another report, 75% of ITA grafts with competitive flow at initial angiography were found occluded at 5 years.17Nakajima H. Kobayashi J. Tagusari O. Niwaya K. Funatsu T. Kawamura A. et al.Angiographic flow grading and graft arrangement of arterial conduits.J Thorac Cardiovasc Surg. 2006; 132: 1023-1029Abstract Full Text Full Text PDF PubMed Scopus (26) Google Scholar Intraoperatively, marginal flow of an arterial graft bypassing a moderately diseased vessel can create a dilemma for an unsuspecting surgeon where the anastomosis “was just perfect,” especially with no other electrocardiogram or transesophageal echocardiogram findings suggestive of ischemia. Anticipation is key. We find it very helpful to measure flow after the completion of each bypass while on CPB with crossclamp on and perfusing the graft only. This is easily accomplished by removing the clamp off the ITA or perfusing the SVG with cardioplegia under a pressure of 80 to 120 mm Hg and flow measured by the perfusionist. Establishing good flow characteristics without competitive native flow provides reassurance in case of marginal flow later once off CPB that might lure the surgeon into revising the graft unnecessarily. After separation from CPB, or in off-pump coronary artery bypass (OPCAB) cases, competitive native flow can be negated with PTO by manual or snare compression. Placing a vein graft in close proximity to an arterial graft with no significant disease between them may result in arterial “string sign” (Figure 3). An example would be left ITA–left anterior descending, with an SVG diagonal and no hemodynamically significant disease in-between. Left ITA flow may be poor but improves with occluding the vein graft. In such a situation, it been not to graft the diagonal or to use the ITA or as Flow can be measured at of the conduit to their patency. A flow not an occluded or anastomosis if 1 or more other in the are (Figure when one of an arterial graft is used to bypass a target that is not flow may be noted in the that It is best not to a graft if one of the at is not the ITA that anterior target is and taken off as a graft. (Figure when the ITA is used with proximal stenosis, in of flow into the the ITA at its and using it as a graft or the stenosis with a or imaging can lesions and this is important in with disease especially when a technique is the inflow is based on 1 or 2 can arterial conduits and coronary It typically with hemodynamic or use of or While significant at the distal anastomosis can or kink a coronary can cause air can cause but can The have found the administration of or or into vein grafts with a to be in flow in where coronary is The of graft patency in the of intraoperative graft Williams et vs coronary artery bypass grafting: and graft and a randomized trial.J Am Med Assoc. 2004; PubMed Scopus Google Scholar The is we have to the use of adjunct modalities for graft and et with off-pump coronary artery bypass grafting: from Thorac Cardiovasc Surg. Full Text Full Text PDF PubMed Scopus Google Scholar reported better patency in arterial grafts in after use of TTFM but not with vein values for grafts flow PI for and PI for 50% of the grafts that with TTFM after revision were on et with off-pump coronary artery bypass grafting: from Thorac Cardiovasc Surg. Full Text Full Text PDF PubMed Scopus Google Scholar Di Giammarco and Giammarco G. Pano M. Cirmeni S. Pelini P. Vitolla G. Di Mauro M. Predictive value of intraoperative transit-time flow measurement for short-term graft patency in coronary surgery.J Thorac Cardiovasc Surg. 2006; 132: 468-474Abstract Full Text Full Text PDF PubMed Scopus (105) Google Scholar noted that intraoperative TTFM arterial and vein grafts A significant of their were and a vein graft patency rate of at 1 was A review by and D.J.F.M. Bekker M.W.A. Taggart D.P. Pieter Kappetein A. 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.Eur J Cardiothorac Surg. 2019; 56: 654-663Crossref PubMed Scopus (17) Google Scholar noted that of of graft however, of all grafts as only were The that while TTFM due to the was In in 50% of a in their the was made without the need for D.J.F.M. Bekker M.W.A. Taggart D.P. Pieter Kappetein A. 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.Eur J Cardiothorac Surg. 2019; 56: 654-663Crossref PubMed Scopus (17) Google Scholar In a study, and intraoperative TTFM with found that cut-off values of flow and PI were of grafts but were not leading to unnecessary graft T.M. Graft quality verification in coronary artery bypass graft surgery: how, when and why?.Curr Opin Cardiol. 2017; 32: 722-736Crossref PubMed Scopus (11) Google K. T. T. J. L. value of transit-time flow measurement for coronary artery bypass grafting: a J Cardiothorac Surg. PubMed Scopus Google Scholar Several have shown no correlation between TTFM and clinical M. R. G. flow and index the outcomes after coronary artery bypass Cardiovasc Surg. 2020; PubMed Scopus Google N.D. G. H. J. et al.The graft imaging to patency clinical trial Thorac Cardiovasc Surg. Full Text Full Text PDF PubMed Scopus Google Scholar However, Kieser and T.M. S. R. flow outcomes in coronary artery bypass graft a of arterial J Cardiothorac Surg. PubMed Scopus Google Scholar reported a correlation between PI values and major adverse cardiac but a greater of than typically T.M. S. R. flow outcomes in coronary artery bypass graft a of arterial J Cardiothorac Surg. PubMed Scopus Google Scholar The randomized Graft to N.D. G. H. J. et al.The graft imaging to patency clinical trial Thorac Cardiovasc Surg. Full Text Full Text PDF PubMed Scopus Google Scholar found no in graft failure at 1 by coronary angiography between the and intraoperative In addition, TTFM did not with graft in the to the TTFM based on the and of them TTFM for more than one were in the TTFM for revision and only one were 75% of the TTFM grafts were The for with and Flow in was a Graft revision in but with the of the study, it was of were to of surgical rather than The that with the of post-CABG angiographic no be routine graft assessment improves graft patency or clinical D.P. D.J.F.M. Di Giammarco G. Wendt D. et al.Intraoperative transit-time flow measurement and assessment in coronary artery bypass grafting.J Thorac Cardiovasc Surg. 2020; Full Text Full Text PDF PubMed Scopus Google Scholar It has been that the of TTFM is its false a bad graft but good TTFM due to retrograde flow into the coronary in of a distal or an TTFM with or with should the into a such as by T.M. Graft quality verification in coronary artery bypass graft surgery: how, when and why?.Curr Opin Cardiol. 2017; 32: 722-736Crossref PubMed Scopus (11) Google Scholar In the dilemma and is the false positivity graft, bad surgeons into revising grafts unnecessarily. especially the are conduits that are rarely by and intimal that contribute to graft However, are delicate and structures compared with making them more to if were a graft to fail due to technical it should be the ITA and not the graft for even failure the of factors, coronary target quality and in conduit N.D. G. H. J. et al.The graft imaging to patency clinical trial Thorac Cardiovasc Surg. Full Text Full Text PDF PubMed Scopus Google Scholar Several may have the widespread of intraoperative quality verification of bypass surgeons may that can with and other tools such as and transesophageal that would them to issues to myocardial ischemia. of intraoperative TTFM measurements can be about of the which may to unnecessary revisions, and only of grafts with TTFM were T.M. Graft quality verification in coronary artery bypass graft surgery: how, when and why?.Curr Opin Cardiol. 2017; 32: 722-736Crossref PubMed Scopus (11) Google D.J.F.M. Bekker M.W.A. Taggart D.P. Pieter Kappetein A. 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.Eur J Cardiothorac Surg. 2019; 56: 654-663Crossref PubMed Scopus (17) Google Scholar the of are just with tools noted that to of “lesions” identified at intraoperative or angiography and all can a R. S. P. K. et al.The of intraoperative angiographic findings for patency in coronary artery bypass Thorac Surg. Full Text Full Text PDF PubMed Scopus (17) Google Scholar the surgeon into revising an anastomosis is a especially when a diseased vessel ECUS was added to the of to in a the need to T.M. Graft quality verification in coronary artery bypass graft surgery: how, when and why?.Curr Opin Cardiol. 2017; 32: 722-736Crossref PubMed Scopus (11) Google Giammarco G. Canosa C. Foschi M. Rabozzi R. Marinelli D. Masuyama S. et al.Intraoperative graft verification in coronary surgery: increased diagnostic accuracy adding high-resolution epicardial ultrasonography to transit-time flow measurement.Eur J Cardiothorac Surg. 2014; 45: 41-45Crossref PubMed Scopus (44) Google Scholar Flow measurement and graft imaging modalities are not to substitute technique and surgical judgment. in that use intraoperative assessment the to a graft or not is influenced by the rather than Graft patency in is more related to rather than technical T.M. Graft quality verification in coronary artery bypass graft surgery: how, when and why?.Curr Opin Cardiol. 2017; 32: 722-736Crossref PubMed Scopus (11) Google Giammarco G. Canosa C. Foschi M. Rabozzi R. Marinelli D. Masuyama S. et al.Intraoperative graft verification in coronary surgery: increased diagnostic accuracy adding high-resolution epicardial ultrasonography to transit-time flow measurement.Eur J Cardiothorac Surg. 2014; 45: 41-45Crossref PubMed Scopus (44) Google N.D. G. H. J. et al.The graft imaging to patency clinical trial Thorac Cardiovasc Surg. Full Text Full Text PDF PubMed Scopus Google Scholar While that the of technical errors still it perhaps for a percentage of graft than Flow especially of the arterial grafts, is with the increased and of and the to the ITA conduits to In we can and to the flow meter use is and its routine use is in and off-pump use of the flow meter is if are any about the of the graft as a to the clinical judgment. a assessment and the surgeon should be with flow measurements are best performed when the are with no or on to flow measurements a of a graft compromise but should not an graft flow, flow, and arterial are more of poor flow measurements than technical or flow is associated with a graft and surgeon are the 2 of the that to to a poor graft flow In intraoperative graft flow assessment with increased use of go in and are significant in the of surgical the of improved and Surgeons should their with quality assurance and The reported no of The and to of and to or for which may have a of The and of this have no of The would to for in the with Bakaeen the about intraoperative graft patency available with Bakaeen the about intraoperative graft patency available