Role of Graft Flow Measurement Technique in Anastomotic Quality Assessment in Minimally Invasive CABG Saad F. Jaber, MD, Steven C. Koenig, PhD, Bobby BhaskerRao, MD, Daniel J. VanHimbergen, BA, Patricia B. Cerrito, PhD, Daniel J. Ewert, PhD, Laman A. Gray, Jr, MD, and Paul A. Spence, MD Division of Thoracic and Cardiovascular Surgery, Department of Surgery, University of Louisville, School of Medicine, Louisville, Kentucky
Background. Anastomotic quality is currently the critical issue in minimally invasive coronary surgery. Although little is known about its effectiveness, surgeons routinely assess grafts intraoperatively using flow probes. This study was designed to determine whether mean flow and the pattern of flow tracing in internal mammary artery grafts obtained with a transit-time flow probe are reliable indicators of anastomotic quality. Methods. Mongrel dogs (n 5 14, 30 to 35 kg) underwent off-pump left, right, or left and right internal mammary artery to left anterior descending artery anastomosis (23 grafts). Moderate to severe degrees of stenosis were created at the anastomosis by an additional suture. Internal mammary artery graft flow was measured before and after the stenosis was created with the left anterior descending artery occluded. Angiography was performed at random postoperatively to validate the degree
of stenosis. Mean flow and flow tracing morphology were compared under various degrees of stenosis. Results. There were no significant differences in mean graft flow or the morphology of the flow tracing between patent (<15%), mild (<25%), moderate (<50%), and moderately severe (<75%) stenosis. However, mean graft flow decreased (p < 0.05) with severe stenosis (>75%). Conclusions. Although differences in mean graft flow and graft flow morphology were detectable in anastomoses with severe stenosis (>75%), they were indistinguishable in anastomoses with mild (<25%) to moderately severe (<75%) stenosis. Flow measurement techniques are valuable tools intraoperatively, but surgeons should exercise caution in their interpretation.
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pared. However, it is invasive, costly, time consuming, and not always readily accessible in the operating room. A variety of flow measurement techniques have gained increasing popularity in assessing anastomotic quality. These techniques provide accurate flow tracings and mean flows through the graft, which surgeons have used to assess anastomotic quality. Transit time flow probes are easier to use and more readily available than angiography. Since 1995, we have performed mini-CABG procedures at the University of Louisville. We have assessed the quality of the anastomosis by evaluating the flow tracing and mean flow obtained with transit-time flow probes placed around the graft. However, we recently reported on two early mammary artery graft failures caused by anastomotic errors [11], which prompted us to reevaluate the role of flow probes in detecting technical errors at the anastomosis.
oronary artery bypass grafting (CABG) without cardiopulmonary bypass has been practiced for more than a decade [1–3], although it currently lacks universal acceptance because of concern for the quality of the anastomoses [4]. The introduction of minimally invasive CABG (mini-CABG) [5, 6] raised enthusiasm among cardiac surgeons, cardiologists, and patients. The combined advantages of mammary artery graft to the left anterior descending coronary artery (LAD) [7–10], smaller incision, and shorter hospital stay with reduced costs have allowed mini-CABG to quickly become a widely accepted procedure. However, even greater concern about the quality of the anastomoses in mini-CABG persists because of the increased technical difficulty in performing this challenging procedure. A myriad of methods has been employed in assessing the quality of the anastomosis intraoperatively. Angiography is universally considered the “gold standard” technique, to which all other methods should be comPresented at “Facts and Myths of Minimally Invasive Cardiac Surgery: Current Trends in Thoracic Surgery IV,” New Orleans, LA, Jan 24, 1998. Address reprint requests to Dr Spence, Cardiovascular Research Institute, 500 S Floyd St, Louisville, KY 40292.
© 1998 by The Society of Thoracic Surgeons Published by Elsevier Science Inc
(Ann Thorac Surg 1998;66:1087–92) © 1998 by The Society of Thoracic Surgeons
Material and Methods Surgical Technique Fourteen mongrel dogs (25 to 35 kg) were anesthetized with pentobarbial sodium (30 mg/kg), and anesthesia was maintained with 2% isoflurane. Respiration was 0003-4975/98/$19.00 PII S0003-4975(98)00752-8
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maintained with a volume-controlled respirator on 100% oxygen. A continuous electrocardiogram was monitored throughout the procedure. Arterial blood gases were sampled every 30 minutes, and bicarbonate was added as needed to maintain a physiologic pH between 7.35 and 7.45. Aortic blood pressure was monitored with a 5Fmicromanometer-tipped catheter (Millar Instruments, Houston, TX) introduced through the left femoral artery. Through a left fifth interspace anterolateral thoracotomy, the mammary arteries were dissected from their origin to their bifurcation and wrapped with gauze soaked in papaverine solution (1 mL of papaverine diluted in 10 mL of normal saline solution). The pericardium was opened and the margins were sutured to the edges of the wound. The LAD distal to the first diagonal artery was selected for receiving the left mammary artery graft, followed by grafting of the right mammary artery to the proximal LAD. The anastomotic region was controlled proximally and distally with 3.0 Prolene (Ethicon, Somerville, NJ) snares. Heparin (1 mg/kg) was given intravenously, followed by two periods of ischemic preconditioning (3 minutes each) before the selected site of the LAD was opened. A flexible cardiac stabilizer (Origin, Menlo Park, CA) was used to mechanically stabilize the grafting site. The mammary artery to LAD anastomosis was then constructed “offpump” with 7.0 continuous Prolene suture technique. Stenosis was created by placing a blind suture through the heel of the anastomosis (8.0 Prolene), thereby reducing the cross-sectional area. Postoperative angiography was randomly used to determine the extent of the stenosis created. The degree of stenosis was categorized as patent (,15%), mild (,25%), moderate (,50%), moderately severe (,75%), or severe (.75%). Adenosine (0.1 mg/kg intravenously) was injected and flow measurements were repeated for each degree of stenosis. All animals received humane care in compliance with the “Guide for the Care and Use of Laboratory Animals” published by the National Institutes of Health (NIH publication 85-23, revised 1985).
Experimental Design Twenty-three patent (,15% stenosis) left or right IMA grafts to the LAD were constructed. Transit-time flow probes (model 3SB; Transonic Systems Inc, Ithaca, NY) placed on the graft(s) were used to measure graft flow (Fig 1). Continuous beat-to-beat graft flow was recorded with the LAD occluded and the graft to LAD anastomosis under patent (,15%), mild (,25%), moderate (,50%), moderately severe (,75%), and severe (.75%) stenosis conditions. One-minute data sets containing graft flow, arterial pressure, and electrocardiogram were converted from analog to digital, sampled at 100 Hz, and recorded on a MacLAB data acquisition system (MacLAB, Milford, MA) during each experimental condition. The degree of anastomotic stenosis was determined by random postoperative angiography. Beat-to-beat analysis of graft flow, arterial, pressure, and electrocardiogram for each 1-minute data set (approximately 60 beats) were calculated using custom soft-
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Fig 1. Surgical procedure used for internal mammary artery to left anterior descending artery graft flow measurements.
ware developed in MatLAB (MathWorks, Cambridge, MA). Mean arterial pressure, heart rate, mean flow (Qmean), mean systolic flow, mean diastolic flow, maximum systolic flow (Qsmax), maximum diastolic flow, minimum systolic flow, and minimum diastolic flow (Qdmin) were calculated on a beat-to-beat basis. In addition, a systolic/diastolic mean flow ratio (Qratio) was computed [12]: Qratio 5 (Qsmax 2 Qdmin)/Qmean. Because mongrel dogs were used and each dog had several different degrees of stenosis, the general linear model with two variables was used to analyze the data by dog (a) and degree of internal mammary artery stenosis (b): yijk 5 m 1 ai 1 bj 1 «ijk. To determine where differences in flow were statistically significant, we used the method of least squares to estimate the flow parameters. Pairwise tests of significance at the 0.05 level were conducted on the least square means. The Wilcoxon signed rank test was used to statistically analyze flow changes before and after the addition of adenosine. In addition, the KolmogorovSmirnov goodness-of-fit test was used to determine differences in flow tracing morphology at each level of stenosis by examining the tracings as density functions.
Results Sample flow tracings for patent (,15%) anastomoses and those with mild (,25%), moderate (,50%), moderately severe (,75%), and severe (.75%) stenosis are shown in Figure 2. Degrees of anastomotic stenoses were verified by postoperative angiography (Fig 3). Mean, systolic, and diastolic graft flow parameter values were significantly higher in patent to mildly stenotic anastomoses than in severely stenotic anastomoses (p ,
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0.05) (see Figs 4 – 6). Further, no significant differences in those parameters were detected between moderately to moderately severely stenotic and severely stenotic anastomoses (p . 0.05) (see Figs 4 – 6). The Kolmogorov-Smirnov goodness-of-fit test showed that the differences in flow tracing morphology between the patent to mild stenosis groups and moderately severe to severe stenosis groups were statistically significant (p , 0.05). The addition of intravenous adenosine significantly (by Wilcoxon signed rank test) increased flow in patent and moderately stenosed (,50%) grafts, whereas in grafts with an anastomotic stenosis greater than 50%, the addition of adenosine significantly decreased graft flow.
Comment Minimally invasive CABG has many advantages including reduced cost, fewer wound complications, decreased transfusion requirements, less neurologic derangement, and shorter hospital stay [13]. Many technical advances such as the use of thoracoscopic internal mammary artery harvesting and mechanical stabilizers have reduced the technical difficulty of this procedure and significantly improved clinical outcome [14]. To be universally accepted, the quality of the anastomoses in minimally invasive direct CABG should be better than or equal to those performed using standard CPB. Clearly,
Fig 2. Sample graft flow: (a) patent (,15%), (b) mild stenosis (,25%), (c) moderate stenosis (,50%), (d) moderately severe stenosis (,75%), and (e) severe stenosis (.75%).
0.05) (Table 1; Figs 4, 5). The flow ratio was significantly higher in the severely stenotic anastomoses than in the patent to mildly stenotic anastomoses (p , 0.05) (Fig 6). No statistical difference in mean, systolic, and diastolic graft flow parameter values and graft flow ratio were detected between patent to mildly stenotic and moderately to moderately severely stenotic anastomoses (p .
Fig 3. Sample angiogram of (A) patent and (B) stenotic (;50%) anastomoses.
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Table 1. Graft Flow Parameters Mean Q Stenosis (%) ,15 ,25 ,50 ,75 .75
Mean Qs
LSMEAN
Standard Error
23.80 23.20 17.50 13.81 12.28
1.75 4.49 3.14 2.83 3.14
LSMEAN
Standard Error
20.38 21.27 16.65 14.28 11.90
1.44 3.68 2.57 2.33 2.57
Max Qs
Min Qs
LSMEAN
Standard Error
43.11 51.67 37.42 33.95 34.00
2.40 6.13 4.29 3.88 4.29
Mean Qd
LSMEAN
Standard Error
LSMEAN
Standard Error
20.88 20.48 24.49 1.22 25.55
1.34 3.43 2.40 2.17 2.40
25.46 24.17 17.43 12.91 11.55
2.05 5.25 3.67 3.32 3.67
AoP 5 arterial pressure; HR 5 heart rate; LSMEAN 5 least squares mean; Max 5 maximum; flow; Qd 5 diastolic flow; Q Ratio 5 systolic/diastolic flow ratio; Qs 5 systolic flow.
Min 5 minimum;
Q 5 graft
the best time to revise a faulty anastomosis is during the primary operation. Unfortunately, a proven reliable technique for intraoperative assessment of the quality of anastomoses does not exist. Surgeons traditionally relied on probing the anastomosis, absence of hemodynamic compromise, or the absence of abnormalities in the electrocardiogram as methods for determining the adequacy of their anastomosis. These crude methods are unreliable and may only detect very poor anastomoses. A variety of flow measurement techniques have been employed with increasing frequency. Flow probes provide a continuous flow tracing and mean flows through the graft with a high degree of accuracy [15, 16]. Because of the peculiar physiology of the coronary circulation, flow through the coronary grafts occurs during diastole with a short systolic peak. Absence of diastolic flow in a graft is indicative of an occluded graft, which should serve as a warning to the surgeon to consider revising the graft. In a graft that is not occluded but still has some degree of stenosis, the flow is also predominantly diastolic, but with taller systolic peaks. The decision whether or not to revise these anastomoses intraoperatively can be difficult, particularly for the intermediate-quality anastomoses. In this study, we were able to create reproducible stenoses in the mammary artery to LAD anastomosis and
analyze the changes in graft flow tracings and graft flow parameters. Because of the dynamic character of the variables that affect graft flow (blood pressure, heart rate, coronary resistance, and graft diameter), the initial optimal mean flow could not be defined. Furthermore, in our experiments graft flow did not change significantly until graft stenosis was greater than 75% (see Figs 4, 5). It is more likely that low graft flow is associated with anastomotic error; however, it may also be possible to have a patent anastomosis with a low graft flow. Conversely, high graft flow is more likely to be associated with a patent anastomosis, but again, it may also be possible to have high graft flow with a stenotic anastomosis. Therefore, guidelines for interpretation of anastomotic quality as a function of graft flow are difficult to establish. Perhaps this may explain why investigators have been unable to correlate graft flow with clinical outcome [17, 18]. In this study, differences in flow tracing morphology were virtually indistinguishable from patent to moderately stenotic anastomoses. Further, grafts with up to 75% stenosis still had predominantly diastolic flow, and only grafts with greater than 75% stenosis showed significantly reduced diastolic flow (see Fig 2). One possible explanation is that the autoregulation of the coronary circulation may mask potentially poor grafts by acutely
Fig 4. Mean graft flow (Mean Q) and mean (Mean Qs), maximum (Max Qs), and minimum (Min Qs) systolic graft flow values for patent anastomoses (,15%) and those with mild (,25%), moderate (,50%), moderately severe (,75%), and severe (.75%) stenosis.
Fig 5. Mean graft flow (Mean Q) and mean (Mean Qd), maximum (Max Qd), and minimum (Min Qd) diastolic graft flow values for patent anastomoses (,15%) and those with mild (,25%), moderate (,50%), moderately severe (,75%), and severe (.75%) stenosis.
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Table 1. Continued Max Qd LSMEAN 37.41 36.97 28.16 20.66 20.92
Min Qd
Standard Error 2.78 7.11 4.97 4.49 4.97
Mean AoP
LSMEAN
Standard Error
20.055 0.11 23.8 1.29 25.07
1.33 3.4 2.38 2.15 2.38
LSMEAN
Standard Error
84.2 72.7 75.8 77 81.9
2.75 4.73 2.66 2.92 2.24
increasing flow through the stenotic anastomosis. This may also explain the increase of flow in nonrestrictive grafts (,50%) with adenosine infusion, whereas in restrictive grafts (.50%) graft flow is decreased as the coronary bed is maximally dilated and the net effect of adenosine infusion is a decrease in flow. Diagnosing lesser degrees of stenosis is less critical, as those grafts have shown the potential of remodeling on repeat angiography [19]. This study focused on application of time domain analyses of flow parameters and flow tracing morphology characteristics in evaluating anastomotic quality. Other pattern recognition techniques, such as spectral analysis and neural networks, may yield better results. Other methods of intraoperative assessment of anastomotic quality are being used. Thermography [20] provides anatomic imaging of the anastomosis, but the quality of the available technology allows only for the detection of a grossly stenosed anastomosis. Furthermore, thermal coronary imaging is only suitable when temperature gradients exist, rendering it an unsuitable tool for anastomotic assessment during mini-CABG procedures. High-frequency epicardial echocardiography is a promising technique, but the available technology is not always accurate in tracing coronary arteries because of shadowing of calcified arterial segments [21], and cannot detect with accuracy the quality of anastomosis. Angioscopy, intravascular ultrasound, contrast echocardiography, and intraoperative digital subtraction angiography
Fig 6. Graft flow ratio (Qratio) for patent anastomoses (,15%) and those with mild (,25%), moderate (,50%), moderately severe (,75%), and severe (.75%) stenosis.
HR
Q Ratio Index
LSMEAN
Standard Error
LSMEAN
Standard Error
106 109 104 105 101
3.7 5.7 4.2 5.8 5.1
2.18 3.31 2.37 2.06 5.32
0.52 0.83 0.92 1.32 0.92
have been described for anastomotic assessment; however, they are invasive procedures, and their role and accuracy have not been clearly defined. The inability of current technology to delineate with accuracy the anatomic details of the anastomotic site has led some surgeons to consider reintroducing routine coronary angiography intraoperatively. In conclusion, minimally invasive CABG has been growing in popularity, and patency rates are improving. The need for an accurate intraoperative method to assess anastomotic quality is well recognized. Transit-time flow probes can accurately measure flow; however, graft flow does not reliably correlate well with anastomotic quality. Flow parameters and flow tracing morphology can be used to detect a severely stenosed anastomosis; however, lesser degrees of stenosis at risk for failure may go undetected, and patent grafts may inadvertently be redone. This study was supported by a grant from the Jewish Hospital Heart and Lung Research Foundation and University of Louisville.
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