Ann Thorac Surg 2005;79:2004-2012
© 2005 The Society of Thoracic Surgeons
Original article: Cardiovascular
Do Coronary Bypass Graft Flows Differ Between On-Pump and Off-Pump Operations?
Yves A.G. Louagie, MD, PhDa,*,
Jacques Jamart, MDb,
André Gruslin, ECCPc
a Department of Cardiovascular and Thoracic Surgery University Clinics of Mont Godinne, Université Catholique de Louvain, Yvoir, Belgium
b Department of Biostatistics University Clinics of Mont Godinne, Université Catholique de Louvain, Yvoir, Belgium
c Department of the Perfusion Unit, University Clinics of Mont Godinne, Université Catholique de Louvain, Yvoir, Belgium
Accepted for publication November 17, 2004.
* Address reprint requests to Prof Louagie, Cardiovascular and Thoracic Surgery, University Clinics of Mont Godinne, 1 av Therasse, B-5530 Mont Yvoir, Belgium (E-mail: louagie{at}chir.ucl.ac.be).
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Abstract
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BACKGROUND: The aim of this study is to compare hemodynamic factors in coronary bypass grafts on-pump and off-pump.
METHODS: Two propensity score-matched groups of 89 patients each including 408 dual beam Doppler flow measurements were compared. The study included only patent and single terminolateral bypass grafts.
RESULTS: Flow was 64.9 ± 37.3 mL/min in the on-pump group versus 58.6 ± 35.0 mL/min in the off-pump group (p = 0.063); velocity was 23.8 ± 10.5 versus 20.5 ± 10.4 cm/s (p = 0.004); resistance measured as mm Hg/(mL/min–1) was 1.50 ± 1.09 versus 1.76 ± 1.14 (p = 0.020); pulsatility index was 1.98 ± 1.52 versus 2.44 ± 1.62 (p = 0.004). The hematocrit was 23.5 ± 3.8% in the on-pump and 32.9 ± 4.1% in the off-pump groups (p < 0 0.001). Multivariate analysis showed that hematocrit was the most significant factor influencing flow (p < 0.001) and velocity (p < 0.001), along with resistance (p = 0.004) and pulsatility index (p < 0.001). In a subset of 50 hemodynamic measurements made on left internal thoracic arteries implanted onto left anterior descending arteries and matched for hematocrit, there were no differences between on-pump and off-pump groups regarding flow, velocity, resistance, or pulsatility index.
CONCLUSIONS: Off-pump compared with on-pump bypass surgery is associated with lower velocity and higher resistance in the grafts, mainly caused by changes in hematocrit and viscosity related to hemodilution.
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Introduction
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With the advent of beating heart coronary surgery, increased attention has been paid to the assessment of anastomosis patency using flowmeters [1–6]. Reduced flow in grafts achieved off-pump in comparison with on-pump techniques has been demonstrated [1, 2, 6]. This decreased mean flow could lead to a high graft revision rate, although flow patterns are acceptable.
Three questions need to be answered. Is there a difference? If the answer is yes, is it significant enough to lead to an excessive graft revision rate? What is the reason for that difference?
We therefore reviewed our experience with thorough hemodynamic assessment of on-pump and off-pump bypass grafting using the dual beam Doppler method. To overcome the shortcomings of a nonrandomized analysis, we made a propensity case-matched analysis as recommended by Blackstone [7] and used in similar comparative studies [8, 9].
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Patients and Methods
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The study includes patients undergoing isolated coronary artery bypass grafting (CABG) by the same surgeon. The on-pump procedures were carried out from March 14, 1997 to March 31, 2003 and the off-pump procedures from February 18, 1998 to February 14, 2003. Our institutional review board approved this study including intraoperative flow measurements.
Patients who needed preoperative or intraoperative implantation of intraaortic balloon counterpulsation were excluded. Patients undergoing beating heart surgery with assist extracorporeal circulation or who were converted to on-pump surgery were excluded as well.
Monitoring was performed using an arterial pressure line, a Swan-Ganz catheter, and transesophageal echocardiography. The anesthesia protocol included propofol, sufentanil, and cisatracurium, administered intravenously. All surgery was by a median sternotomy.
In the group operated upon under cardioplegic arrest, myocardial protection was obtained using blood cardioplegic solution (8:1 dilution ratio) administered continuously antegrade and retrograde at 8°C. The procedure was carried out at 28°C hypothermia.
In the beating heart patient group, systemic anticoagulation with heparin was established using half of the cardiopulmonary bypass (CPB) loading dose and was periodically supplemented, to maintain an activated clotting time of between 200 and 300 seconds. The patient was placed in the Trendelenburg position and tilted to the right. Temperature homeostasis (>35.5°C) was achieved throughout the procedure using room temperature (>20°C), mattresses with circulating warm water, and warm infusion solutions. Traction sutures were applied to the margins of the pericardium, displacing the heart superiorly. Deep pericardial stitches were used to anastomose the marginal arteries. In all cases, suction-based tissue stabilizers Octopus 1 to 3 (Medtronic Octopus system, Medtronic, Inc, Minneapolis, MN), designed by Jansen and colleagues in Utrecht, were applied [10]. A 4 to 0 Prolene suture (Ethicon, Somerville, NJ) was applied around the coronary artery, proximal and distal to the site selected for the arteriotomy. The proximal suture was snared with a thin silicone tube and the distal part of the suture was simply lifted. A microblower was used (Visuflo, Research Medical Inc, Midvale, UT). All anastomoses were done by the same surgeon (YL) using 8 to 0 monofilament sutures and 6x magnification under headlight illumination.
Graft flow assessment was carried out systematically for all patients intraoperatively, using an 8 MHz pulsed-wave Doppler ultrasound flowmeter (Scimed OPDOP 130, Bristol, UK). The flowmeter uses a single-crystal pulsed Doppler probe with two receiver gates. Flow measurements are obtained by constraining the vessel in an acrylic cuff whose two halves are clipped around it. The mean diameter of the cuffs used in the study was 4 mm. The ultrasound pencil probe is slotted into the cuff and acoustically coupled to the vessel by a small amount of sterile gel. In that way, the probe to vessel angle is fixed at 60 degrees. A detailed description of the method, including a validation study, has been published previously [11]. Briefly, the technique was validated in three ways. First, the Doppler probe was assessed in vitro on saphenous vein grafts by connecting the vessel to a roller pump and determining the flow by timed-volume collection, using as fluid whole citrated human blood. There was an excellent correlation between both flow measurements: r = 0.97, p less than 0.001, n = 14. Second, in vivo assessments were realized on pediculated left internal thoracic artery (LITA) grafts after harvesting. Results obtained with Doppler ultrasound were correlated with measures realized simultaneously on the same LITA graft by timed-volume collection of blood when the distal LITA graft was open. The correlation between both measurements was satisfactory: r = 0.86, p less than 0.0001, n = 32. Finally, Doppler ultrasound determinations were compared with measures realized concurrently on the same implanted LITA graft with an electromagnetic flowmeter. Again, the correlation was excellent: r = 0.97, p less than 0.0001, n = 12.
The flows were measured at the end of cardiopulmonary bypass before reversal of heparin, when core temperature was more than 36°C, in the on-pump cases and immediately after completing the graft implantation in the off-pump cases. Having obtained a satisfactory probe to vessel acoustic coupling, and a constant Doppler waveform, flow, velocity, resistance, and pulsatility index measurements in association with analysis of phasic flow pattern were realized simultaneously. One set of these flow-derived measurements was obtained for each graft. All resistances were expressed in peripheral resistance units (PRU), where 1 PRU = 1 mm Hg/(mL/min–1). These measurements were gathered prospectively in a database. Only flow measures made on single terminolateral bypass grafts were considered. Thus, sequential and T grafts were excluded from the analysis.
The system provides the criteria required to detect technical errors or flow limitations. Criteria of graft occlusion were the following: resistance greater than 2 PRU; pulsatility index greater than 3; flow less than 30 mL/min; velocity less than 10 cm/s and a characteristic phasic flow pattern [11]. The same criteria were used in both groups. During the study period, three grafts needed distal anastomosis revision because of abnormal Doppler flow. All these grafts had been completed off-pump. One distal anastomosis of a LITA graft realized on-pump was redone because of dissection. These hemodynamic data indicating graft occlusion and leading to revision were excluded from the study.
Because hemodilution at the moment of Doppler measurement could influence viscosity and flow velocities, hematocrit values measured immediately after Doppler flow measurements were collected. In the on-pump group, flow measurements were completed altogether at the end of CPB and the blood sample taken at the end of CPB was considered. Conversely, in the off-pump group, flows were measured at various instances during surgery. As hematocrit determinations were not synchronized with flow measurements, the mean hematocrit value of the samples taken during the period of beating heart surgery was used.
The selection criteria for off-pump surgery in our current practice are increased age, lung disease, a history of hematologic disease, and immunosupression regimen. Relative contraindications are extreme obesity and the need to realize multiple (> 3) distal anastomoses. In the study population subset, 112 patients underwent off-pump operation and 344 patients underwent on-pump operation. To reduce the influence of selection on the comparison, we used propensity-score pairwise matching. The propensity score is the probability of being treated by one of two methods based only on the individual’s covariate measures [7, 12]. It can be used to balance the covariates in the two groups, and thus reduce bias. Here, the propensity score was estimated using logistic regression analysis. This was carried out using a forward stepwise selection of variables using the Wald test at a probability level of 0.05; the dependent variable being procedure performed on-pump or off-pump. The independent variables associated with group membership are listed in Appendix 1.
Using the model determined by regression analysis, namely the probability of having the procedure performed off-pump, an estimate of the propensity toward belonging to one group versus another was calculated for every individual. This constituted the estimated propensity score. Matching was completed by using the nearest available matching for each patient on the estimated propensity score. This method randomly ordered the treated and control subjects according to the propensity score, then selected the first treated subject and found the control subject with the closest propensity score. Both subjects were then removed from consideration for matching and the next treated subject was selected. Eighty-nine pairs of patients could be matched and are the subjects of this study.
Perioperative data were collected and entered prospectively into a clinical database by the surgeon. Values are presented as means ± standard deviations. Numerical and categorical variables were compared between both matched groups by Wilcoxon signed-rank and binomial tests, respectively. Graft-host vessel features were compared between both groups by Pearson 
2 test for the independence of the rows and columns. Univariate and multivariate analysis of hemodynamics in bypass grafts was performed by regression analysis using generalized estimating equations (GEE) as described by Liang and Zeger [13]. Statistical analyses were performed using SPSS for Windows (SPSS Inc, Chicago, IL) software, except for the GEE analysis for which the repeated measures (RM)GEE program was used [14].
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Results
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The groups were well-balanced in terms of risk factor distribution (Table 1) and preoperative clinical data (Table 2). The only difference between the groups consisted of a higher incidence of preoperative corticotherapy and immunosupression regime in the off-pump group. This bias resulted from a strict avoidance of CPB in patients with malignant hematologic disease or those receiving corticotherapy for severe chronic obstructive pulmonary disease. Regarding graft-host vessel features (Table 3), the groups were well-matched except for a lower incidence of 51% to 70% of proximal stenoses in the off-pump group. This can be explained by the surgeon’s concern to induce ischemia while clamping moderately stenosed arteries to complete off-pump coronary grafting. The mean pump time was 120.6 ± 30.0 minutes and the mean cross-clamp time was 83.4 ± 24.9 minutes in the on-pump group. The hematocrit measured at the end of CPB was 23.5 ± 3.8% in the on-pump group whereas the average hematocrit was 32.9 ± 4.1% in the off-pump group (p < 0.001). Inotropic support by dopamine was necessary to wean patients from CPB in eight (9.0%) patients in the on-pump group and two (2.2%) patients in the off-pump group (p = 0.11). Dobutamine treatment was needed in 18 patients (20.2%) in the on-pump group and in 10 (11.0%) in the off-pump group (p = 0.18). There was no need to administer epinephrine in these patients.
A total of 408 flow measurements made on single terminolateral grafts were analyzed (Table 4). Lower velocity, increased resistance, and pulsatility index characterized the off-pump group. Furthermore, there was a trend toward lower flow in the latter group. The mean arterial pressure at the time of the measurement was similar.
Resistance was significantly influenced by the graft-host vessel combination of right gastroepiploic grafts implanted onto the posterior descending arteries (p = 0.013) and by off-pump operation (p = 0.017). The influence of the nature of the bypass conduit on graft resistance is shown in Figure 1 and the resistance distributed according to the recipient coronary artery is shown in Figure 2.
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Fig 1. Box plot of resistance distributed according to the nature of the bypass graft conduit. Off-pump procedure is represented by gray boxes and on-pump procedure by empty boxes. The central line depicts median values; the upper and the lower hinges represent the 75th and 25th percentiles, respectively. (GSV = greater saphenous vein; LITA = left internal thoracic artery; PRU = peripheral resistance units; RGEA = right gastroepiploic artery; RITA = right internal thoracic artery.)
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Fig 2. Box plot of resistance distributed according to the target vessels. Off-pump procedure is represented by gray boxes and on-pump procedure by empty boxes. The central line depicts median values; the upper and the lower hinges represent the 75th and 25th percentiles, respectively. (DIAG = diagonal artery; LAD = left anterior descending artery; OM = obtuse marginal artery; PDA = posterior descending artery; PRU = peripheral resistance units; RCA = right coronary artery.)
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Four sets of GEE multivariate analyses were performed using, as dependent variables, flow, velocity, resistance, and pulsatility index, successively. The 18 variables used in the analysis are described in Appendix 2, and the results of these analyses are presented in Table 5. Hematocrit influenced all hemodynamic variables strongly and consistently. It reduced flow and velocity, and increased resistance and pulsatility index. By contrast, the use of CPB did not independently influence the target variables. Furthermore, the nature of the recipient artery (left anterior descending artery [LAD] vs other) and, to a lesser extent coronary morphology, had a significant impact on graft hemodynamic variables. Regarding the nature of the bypass conduit, use of venous grafts was associated with a reduced flow and the use of the right gastroepiploic artery (RGEA) increased resistance. A previous percutaneous transluminal coronary angioplasty (PTCA) of the recipient coronary artery was associated with reduced resistance and pulsatility index in the graft.
To confirm the key role of hematocrit and to offset possible interference with the nature of bypass conduits and of the recipient vessel, the hemodynamics of LITA grafts implanted onto the LAD were compared after matching for hematocrit. Thus, fifty pairs of hemodynamic sets having identical hematocrit values were matched. Their comparison showed the following nonsignificant results: flow in the LITA-LAD grafts was 64.4 ± 37.1 mL/min on-pump versus 67.3 ± 41.7 mL/min off-pump (p = 0.732); the velocity was 21.5 ± 10.1 cm/s versus 22.2 ± 10.7 cm/s (p = 0.717); the resistance was 1.48 ± 0.72 PRU versus 1.57 ± 1.17 PRU (p = 0.739); and the pulsatility index was 2.10 ± 1.10 versus 2.28 ± 1.61 (p = 0.898). In the subset group of LITA grafts implanted onto the LAD, hematocrit and graft resistance showed a weak but significant correlation (r = 0.224, p = 0.009) (Fig 3).
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Fig 3. Scatter plot of the correlation between hematocrit and resistance in left internal mammary artery grafts implanted onto left anterior descending arteries. The heavy line represents linear regression and the dashed lines are the 90% confidence limits. (PRU = peripheral resistance units.)
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Comment
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Recent studies reported significantly lower transit time flow measurements after CABG without CPB. In a comparative study analyzing 896 patients and a total of 2,247 grafts, Schmitz and colleagues [1] observed a flow in grafts after off-pump surgery that was about half the flow in grafts after CPB. For example, the average flow in the LITA in LAD grafts was 40.3 mL/min in the on-pump group and 27.2 mL/min in the off-pump group. In the study of Güden and colleagues [6], 300 patients undergoing only CABG procedures were enrolled in a prospective randomized manner into three groups. Group 1 consisted of 100 patients undergoing operations with standard cardiopulmonary bypass techniques, group 2 consisted of 100 patients scheduled for revascularizations using off-pump techniques, and group 3 consisted of 100 patients who underwent operations with off-pump techniques under controlled hemodilution (hematocrit levels kept between 25% and 28%). The flow values for the off-pump group were lower than those of on-pump and off-pump with hemodilution for left anterior descending and right coronary artery territories (p < 0.05). The flow values for the circumflex artery area showed the same trend but the differences did not reach statistical significance. Hu and colleagues [2] showed that the flow of grafts in obtuse marginal vessels was higher in the on-pump group than in the off-pump group. However, they concurred that the difference could be explained by a higher frequency of sequential grafts in that territory in the on-pump group.
Our data partially corroborate these previous studies; velocity was significantly lower, whereas resistance and pulsatility were significantly higher in the off-pump group. Nevertheless, flow did not differ significantly among the groups despite a trend toward lower flow in the off-pump group. In addition, the difference did not reach a 50% reduction because the average flow value for all grafts was 64.9 mL/min in the on-pump group versus 58.6 mL/min in the off-pump group.
To explain these discrepancies, several characteristics of the previous studies need to be discussed. The study by Schmitz and colleagues [1] analyzed 2,247 grafts, including 268 LITA grafts on the LAD, the other grafts being predominantly saphenous vein grafts (except for eight LITA and seven right internal thoracic artery [RITA] grafts). In the present study, arterial grafts predominated. Schmitz and colleagues [1] made no attempt to compensate for the absence of randomization and major differences were found between the two groups: the off-pump coronary bypass patients had a higher incidence of previous cardiac surgery and lower incidence of unstable angina and of emergent operations. Flow measurements were made in all patients, including off-pump, after partially antagonizing heparin. By contrast, we assessed flows immediately after the construction of each bypass graft in the off-pump group. It is thus possible that a hyperemic effect induced by the restoration of regional coronary flow could have influenced our results. Indeed, measurements of coronary velocity and reactive hyperemia in the coronary circulation of humans show that the duration of the hyperemic response progressively increased with increases in the duration of occlusion [15]. In addition, two methods of cardioplegia (Bretschneider’s or Buckberg’s cold blood cardioplegia) were used by Schmitz and colleagues [1]. As hypothesized by that group, acidosis develops in the coronary artery system during myocardial anaerobiosis, and this might result in vasodilation of the coronary arteries [16]. However, with blood cardioplegia, acidosis is reduced as demonstrated by continuous pH monitoring in the human hypertrophied heart [17]. This may explain why the differences were less marked in our series where blood cardioplegia was used in all on-pump patients. The results of Güden and colleagues [6] need to be interpreted cautiously because abnormal flow studies leading to graft revision were included in their comparative analysis. The pulsatility indices did not differ between groups in that study.
Lower blood flows measured in off-pump groups [1, 6] were not associated with a worse clinical outcome. We also did not find a difference in postoperative cardiovascular hemodynamic performance [18]. This is not surprising because it was demonstrated in a previous study that flow measurements do not correlate with clinical outcome [19].
There are several reasons why flow is higher and resistance is lower in grafts after on-pump surgery. The most likely explanation is the hemodilution induced by CPB. Indeed, there is a relationship among hematocrit, blood velocity, and vascular resistance. An increase in hematocrit after transfusion of anemic human fetuses was associated with an increase of pulsatility index, a marker of vascular impedance, as measured in the umbilical and cerebral arteries [20]. Conversely, with increasing anemia, there is an increase in blood flow and peak velocity as measured by Doppler in the descending aorta [21]. The patients operated on-pump are hemodiluted whereas the off-pump patients are not. Eckmann and colleagues [22] determined the effects of temperature, shear rate, hematocrit, and different volume expanders on blood viscosity in conditions mimicking deep hypothermia for cardiac operations: blood viscosity decreased by a factor 1.3 to 2.6 as the hematocrit was decreased from 35% to 22.5%. Güden and colleagues [6] showed that off-pump CABG patients with hemodilution (hematocrit levels kept between 25% and 28%) had significantly higher graft flows than off-pump CABG patients without hemodilution and had flows comparable with on-pump CABG patients. Our data corroborate this: there was a marked difference in hematocrit between the on-pump and the off-pump group, confirming the extent of hemodilution related to CPB. In our multivariate analysis hematocrit was the most significant variable, influencing every hemodynamic target variable, and CPB lost its influence when hematocrit was taken into account. Finally, by establishing a comparison between pairs matched on hematocrit values, the flow-derived variables in a subgroup of LITA on LAD bypass grafts were similar.
Further hypotheses need to be discussed. In the present study, use of dopamine and dobutamine was more frequent, though not statistically significant, in the on-pump group at the end of CPB; it has been demonstrated that dopamine decreases coronary vascular resistance [23]. In the on-pump group the measurements were made while weaning from CPB, before the reversal of heparin use. During that period the heart is not fully working because the patient is on partial bypass. Coronary resistance of the arrested heart averaged 1.57 mm Hg·mL·min and increased significantly to 1.75 mm Hg·mL·min after reversal of heparin [24]. This was attributed to the dynamic resistance of the working heart. As measurements were made at the end of CPB when the heart is partially assisted, it is possible that coronary resistance at this point is less than in the fully working heart as in off-pump operation. However, this hypothesis is not corroborated by sequential flow analyses. Indeed, in a study including 601 electromagnetic flow measurements made in LITA and greater saphenous vein grafts, the average flow was 51 mL/min on CPB, 70 mL/min after weaning from CPB and 51 mL/min at chest closure (time effect, p = 0.022) [25]. Thus, flow did not decrease when the heart was fully working.
We observed that the RGEA graft implanted onto the posterior descending artery (PDA) showed a specifically high resistance in the off-pump group, in contrast with the rest of the grafts. These results could be influenced by the timing of flow measurements. Indeed, in the on-pump procedure measurements were made in all grafts after having completed the proximal aortic anastomoses and during the weaning of patients from CPB. By contrast, in the off-pump group these measurements were made in arterial grafts immediately after the completion of the distal anastomosis. There was thus less time left for the graft to adapt and to vasodilate. It has been shown that the flow in the RGEA is comparable with values obtained in other grafts implanted onto the PDA [26]. Furthermore, there were no flow differences between RGEA and saphenous vein grafts implanted into the same coronary bed in similar groups of patients [27]. The high resistance specific to RGEA grafts onto the PDA did not have clinical effects in our series. Furthermore, total arterial grafting including the RGEA done off-pump is safe even in high-risk patients [28].
Our study had several limitations. The first was the absence of randomization. We tried to overcome that bias by a propensity score case match and by multivariate analysis. The matching was effective, limiting the differences between the groups to corticoids-immunosupressive drugs intake and the distribution of host vessel proximal stenoses.
The difference in the distribution of the degree of proximal stenosis could have an impact on the flow results. Indeed, a low degree stenosis (< 70%) could induce competitive flow, increase graft resistance, and finally lead to graft occlusion. This is particularly true for RGEA grafts. However, in our study, the incidence of low degree proximal stenosis (51% to 70%) in the off-pump group is half the incidence of the on-pump group (6.3% vs 13.7% [Table 3]). In addition, the degree of proximal stenosis was included as a variable in the GEE multivariate analysis. Therefore, it is unlikely that the degree of stenosis of the recipient artery could bias the results and conclusions regarding the impact of hematocrit on flow-derived data.
Analysis of the results poses an important methodologic problem attributable to the characteristics of patients; ie, age, diabetes, and dyslipidemia. These features are correlated with various features of several bypass grafts and recipient arteries; ie, flow and coronary artery morphologic characteristics. Indeed, each bypass graft was considered individually for the purpose of the analysis. Thus, patient-related factors, such as diabetes, will influence the hemodynamics of all the grafts of a given patient and thus will be taken into account several times (equivalent to the amount of distal anastomoses) in regression analysis. Therefore, the generalized estimating equation approach, which takes into account and corrects the latter bias, was preferred to the more usual multiple regression analysis.
Hematocrit measurements, given the retrospective nature of the study, were not done precisely at the moment of Doppler flow measurement. This bias affected principally the off-pump group, where flow measurements were carried out at various moments. However, the differences between the two groups were still very significant and the independent influence of hematocrit in the multivariate analyses is consistent and strong. We believe that a perfect synchronicity between flow and hematocrit measurements could only reinforce the conclusions of the study and probably improve the correlation between hematocrit and hemodynamic variables.
In conclusion, off-pump surgery was characterized by a reduced velocity and increased resistance and pulsatility index. However, the flow differences were limited, contrasting with previous comparative studies. Therefore, in our opinion, there is no need to reconsider the criteria for graft anastomosis revision. The variation in hemodynamic variables is not related to off-pump operation by itself but can be explained by reduced hemodilution leading to higher viscosity. We thus confirm that hematocrit is an important variable in the assessment of graft flow hemodynamics, particularly when methods associated with marked changes in hemodilution are compared.
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Appendix 1
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Variables Included in the Propensity Score Model
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Appendix 2
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List of Variables Included in the GEE Multivariate Analysis
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Abstract
Introduction
