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Ann Thorac Surg 2001;72:408-415
© 2001 The Society of Thoracic Surgeons
a Division of Cardiothoracic Surgery, Charleston, South Carolina, USA
b Extracorporeal Circulation Technology Program, Medical University of South Carolina, Charleston, South Carolina, USA
c Division of Pediatric Cardiology, Charleston, South Carolina, USA
Address reprint requests to Dr Bradley, Division of Cardiothoracic Surgery, Medical University of South Carolina, 96 Jonathan Lucas St, Charleston, SC 29425
e-mail: bradlesm{at}musc.edu
Presented at the Forty-seventh Annual Meeting of the Southern Thoracic Surgical Association, Marco Island, FL, Nov 9–11, 2000.
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Abstract |
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Methods. The APC flow was directly measured in 32 patients undergoing Fontan procedures from July 1997 to September 2000. The APC flow was measured in the operating room during total cardiopulmonary bypass, and was expressed as a percentage of total bypass pump flow.
Results. The APC flow ranged from 9% to 49% of total pump flow (median, 18%). Higher preoperative systemic oxygen saturation, pulmonary artery oxygen saturation, pulmonary to systemic flow ratio, and angiographic APC grade correlated with higher APC flow. There were no operative deaths; there was one Fontan takedown (APC flow = 14%). The APC flow had no significant effects on postoperative Fontan pressure, common atrial pressure, transpulmonary gradient, duration of effusions, or resource utilization after the Fontan procedures.
Conclusions. In patients undergoing a Fontan procedure, APC flow is omnipresent, although its extent varies widely. Increased APC flow has no significant effect on the outcome of a Fontan procedure. This conclusion applies to patients who are well prepared for a Fontan procedure, but may not extend to patients at higher risk.
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Introduction |
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Aortopulmonary collaterals carry blood from the aorta or its branches into the pulmonary vascular bed. As such, there are obvious potential disadvantages of APCs in a patient undergoing a Fontan operation. Aortopulmonary collaterals should volume load the single ventricle, should increase pulmonary blood flow, pulmonary artery pressure, and transpulmonary gradient, and should compete with systemic venous flow through the pulmonary vascular bed after a Fontan procedure. Ventricular volume load and elevated pulmonary artery pressure have been identified as risk factors for a Fontan procedure [2–5]. However, previous studies examining the effects of APCs in Fontan patients have produced conflicting results. Spicer and colleagues [7] found that patients with significant APCs identified at preoperative catheterization had prolonged drainage of effusions after Fontan procedures. In contrast, McElhinney and colleagues [9] found that patients with significant APCs were less likely to have prolonged effusions after a Fontan procedure. These conflicting results may be partially explained by the limitations of cardiac catheterization in identifying APCs. Catheterization provides a qualitative, rather than a quantitative measure of APC flow. Identification of collaterals during catheterization is also dependent on the particular angiographic techniques used, and therefore can vary greatly from one catheterization to the next.
In an attempt to add quantitative information to the debate on the importance of APCs, we undertook a study to directly measure APC flow in patients undergoing Fontan procedures. The APC flow was measured in the operating room as the volume of blood returning from the pulmonary venous vent during total cardiopulmonary bypass. The aims of this study were to define the incidence and extent of APC flow in patients undergoing Fontan procedures, to identify risk factors for APC flow, and to determine if APC flow had a measurable effect on the outcome of the Fontan procedure.
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Material and methods |
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TopAbstractIntroductionMaterial and methodsResultsCommentAcknowledgmentsDiscussionReferences |
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All patients underwent cardiac catheterization before the Fontan procedure. Median pulmonary artery pressure was 9.0 mm Hg (range, 5.0 to 14.0 mm Hg), atrial pressure was 4.5 mm Hg (range, 2.0 to 10.0 mm Hg), ventricular end-diastolic pressure was 8.0 mm Hg (range, 4.0 to 12.0 mm Hg), transpulmonary gradient was 4.0 mm Hg (range, 2.0 to 9.0 mm Hg), and pulmonary to systemic flow ratio (Qp:Qs) was 0.6 (range, 0.4 to 1.2). Median Nakata index was 172 mm2/m2 (range, 94 to 341 mm2/m2). All angiograms were retrospectively reviewed by a single observer (WAKR), who was unaware of the amount of directly measured APC flow. APCs were graded on a scale from 0 (no significant APCs) to 4 (severe APCs); median APC grade was 2.0 (range, 0.5 to 3.5). No patient had pulmonary arteriovenous malformations seen by angiography. Atrioventricular valve regurgitation was graded by echo on a scale from 0 (none) to 4 (severe); median regurgitation was 0.5 (range, 0 to 2.5).
The technique of Fontan procedure was a total cavopulmonary connection in all patients: intraatrial lateral tunnel in 24 patients and extracardiac conduit in 8 patients. All Fontan procedures included a fenestration, 4 mm in 28 patients, 5 mm in 2 patients, and 6 mm in 2 patients. Nine patients underwent concomitant procedures: atrioventricular (tricuspid) valve repair in 4 patients, pulmonary artery patch augmentation in 2 patients, pulmonary vein repair in 1 patient, main pulmonary artery division in 1 patient, and pacemaker generator change in 1 patient. Median cardiopulmonary bypass time for the Fontan procedure was 133 minutes (range, 95 to 217 minutes); aortic cross-clamp time was 54 minutes (range, 0 to 84 minutes). Bilateral pleural chest tubes were placed in all patients and managed by a protocol in which they were removed once drainage was less than 2 mL/kg/d/tube. It has been our experience that this protocol minimizes the need for chest tube reinsertion after removal. For at least 24 hours after operation, direct pressure monitoring included the Fontan, or central venous pressure (through an internal jugular line ending in the superior vena cava), and common atrial pressure (through a transthoracic line placed in the operating room). Transpulmonary gradient was derived as Fontan minus common atrial pressure.
Three acyanotic, control patients also underwent direct intraoperative measurement of APC flow. These 3 patients were undergoing closure of ventricular septal defects and were approximately the same age as the study patients.
Study protocol
The APC flow was measured intraoperatively during total cardiopulmonary bypass as follows. Both the superior vena cava and inferior vena cava were individually cannulated and snared so that all systemic venous return was drained to the bypass circuit. The pulmonary arteries were unopened so that all APC flow returned to the heart through the pulmonary veins. Mean systemic arterial pressure was adjusted to 40 to 45 mm Hg by adjusting bypass pump flow. Vasoactive agents (nitroprusside, phenylephrine) were not used during the study. A pulmonary venous vent was placed into the common atrium and suction was adjusted to completely drain the heart. The volume from the vent was measured for one minute (time 1). This measurement was then repeated after the aorta was cross-clamped and the heart was arrested with cardioplegia (time 2). The volume measured at time 2 included neither systemic venous or coronary sinus return, and was taken as APC flow. The APC flow was expressed as a percentage of total cardiopulmonary bypass flow at the time of the measurement. All patients had vent volume measured at time 1, and 31 of 32 patients at time 2. There was good correlation between the volumes measured at time 1 and time 2 (r = 0.86, p < 0.0001 by linear regression). At time 2, median patient core temperature was 27.0oC (21.6°C to 32.5°C.); cardiopulmonary bypass pump flow was 116 mL/kg/min (range, 73 to 154 mL/kg/min).
Exclusions
During the period of this study, 10 patients underwent a Fontan procedure but were not included in the study. Five patients had bilateral superior vena cavae, the left of which was not cannulated during the procedure. Because systemic venous return was not completely diverted from the pulmonary vascular bed, APC flow could not be determined in these patients. Three patients undergoing conversion of an atriopulmonary Fontan to total cavopulmonary connection were excluded. Two patients were excluded because of technical difficulties with intraoperative flow measurement.
Analysis and statistics
The preoperative variables analyzed for association with APC flow were as follows. Anatomic diagnosis (hypoplastic left heart syndrome vs other), echocardiographic ventricular function (normal vs depressed) and atrioventricular valve regurgitation, cardiac catheterization pressures (pulmonary artery, common atrium, ventricular end-diastolic, transpulmonary gradient), saturations (superior vena cava, pulmonary artery, aorta), flows (pulmonary, systemic, Qp:Qs), Nakata index, pulmonary artery distortion (yes vs no), angiographic APC grade (scale, 0 to 4), coil occlusion of APCs before Fontan procedure (yes vs no), patient age and weight at Fontan procedure, and time between superior cavopulmonary connection and Fontan procedure. The effect of APC flow was analyzed on the following outcome variables: Fontan pressure, common atrial pressure, transpulmonary gradient, and systemic oxygen saturation at 0, 6, 12, 18, and 24 hours after Fontan procedure; duration of effusions; prolonged effusions; length of mechanical ventilation; intensive care unit stay; and hospital stay. Continuous variables were analyzed by simple linear regression, and categorical variables by unpaired t test. Data are shown as mean ± standard deviation unless noted. Statistical significance was defined as p less than 0.05.
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Results |
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Effect of APC flow on the outcome of the Fontan procedure
Among the 32 study patients, there were no deaths. One patient underwent Fontan takedown caused by thrombotic complications of heparin-induced thrombocytopenia; this patient’s APC flow was 14%, which was below the median of 18% for the study group.
Early postoperative hemodynamics were examined as potentially more sensitive measures of outcome than death or Fontan takedown. However, the extent of APC flow had no significant effect on Fontan pressure, common atrial pressure, or transpulmonary gradient at 0, 6, 12, 18, or 24 hours after operation. Figure 2 shows the relationship between APC flow and these three hemodynamic factors 12 hours postoperatively. There was no tendency for patients with higher APC flow to have higher Fontan pressure, common atrial pressure, or transpulmonary gradient in the early postoperative period.
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Comment |
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Early postoperative hemodynamic status is an outcome measure potentially more sensitive than Fontan failure. For example, the Fontan (central venous) pressure early after a Fontan operation has been shown to be a predictor of failure [2, 3, 5]. Furthermore, it would seem logical that a left-to-right shunt from APC flow should increase pulmonary blood flow and volume load the single ventricle, thereby increasing pulmonary artery pressure, transpulmonary gradient, and ventricular filling pressure. In the current study, these 3 variables were directly monitored for the first 24 hours after operation. Patients with higher APC flow had no tendency to have higher Fontan pressure, common atrial pressure, or transpulmonary gradient during this time period (Fig 2). Thus, APC flow had no demonstrable effect on early postoperative hemodynamic status after a Fontan procedure.
The duration of effusions is another important measure of the outcome of a Fontan procedure. The duration of effusions in the current study was similar to that in other recent series of Fontan operations [9, 12]. The current study demonstrated no effect of APC flow on the duration of effusions, and a tendency for patients with prolonged effusions to have less APC flow than patients without prolonged effusions (Table 3 and Fig 3). Finally, we identified no effect of APC flow on postoperative resource utilization (ie, length of mechanical ventilation, intensive care unit stay, or hospital stay). In summary, we found no effect of APC flow on the outcome of a Fontan procedure, as assessed by Fontan failure, early postoperative hemodynamic status, duration of effusions, or resource utilization.
This study provides information on the incidence and extent of APC flow in patients undergoing a Fontan procedure. Previous studies have shown that APCs are common, being identified in 59% to 65% of patients after a bidirectional Glenn shunt [9, 10], and in 84% of patients undergoing pre-Fontan catheterization [7]. In the current study, the lowest APC flow among the study patients was 9%. This was six times higher than the APC flow in the control patients (0.5% to 1.4%). This finding shows that not just most, but probably all patients undergoing a Fontan procedure have APC flow many times higher than control patients. The extent of this APC flow also varied widely, from a low of 9% to almost half of total pump flow.
In this study, we sought to identify risk factors for increased APC flow. Previous studies have found a correlation between APCs and previous systemic-to-pulmonary artery shunts [9, 10], use of and length of cardiopulmonary bypass for a previous superior cavopulmonary connection [9], longer time between superior cavopulmonary connection and Fontan procedure [9], older age at Fontan procedure [6], higher ventricular end-diastolic pressure [9], higher pulmonary vascular resistance [9], higher systemic oxygen saturation [6], and lower pulmonary artery index [6]. In the current study, the only preoperative variables that correlated with higher APC flow were higher angiographic APC grade, higher systemic and pulmonary artery oxygen saturation, and higher Qp:Qs at catheterization (Tables 1 and 2). These correlations are presumably caused by APC flow carrying oxygenated blood into the pulmonary arteries, increasing pulmonary flow and secondly, systemic oxygen saturation. The lack of correlation between APC flow and the other variables found to be significant in previous studies is probably caused by differences in patient population or methods of detecting APC flow, or both.
Noteworthy, the current study found no correlation between APC flow and either the length of time between superior cavopulmonary connection and Fontan procedure, or the age at Fontan operation. In our patients, APC flow did not seem to increase in a linear fashion over time. This finding (along with the lack of effect of APC flow on outcome) suggests that concern over APCs should not be used as a criterion for choosing the timing of a Fontan procedure after a previous superior cavopulmonary connection. Within the age range of our patients (1 to 9 years), earlier Fontan completion may not avoid APC development, and later Fontan completion may not be preceded by increased APC formation.
Several previous studies have examined the effects of APCs on the outcome of a Fontan procedure [6–9, 12]. Studies that have used cardiac catheterization to identify APCs have produced directly conflicting results. Spicer and colleagues [7] found that patients with significant APCs identified at preoperative catheterization had prolonged drainage of effusions after Fontan procedures; preoperative coil occlusion of APCs decreased the duration of effusions. In contrast, McElhinney and colleagues [9] found that patients with significant APCs were less likely to have prolonged effusions after Fontan procedures; preoperative coil occlusion of APCs had no effect on the duration of effusions. These conflicting results may be partially explained by the limitations of cardiac catheterization in identifying APCs. Catheterization provides a qualitative, rather than a quantitative measure of APC flow. Identification of collaterals by catheterization is also highly dependent on the particular angiographic techniques used. In a comprehensive study of APCs in 268 catheterizations, Triedman and colleagues [10] found that 68% of the APCs originated from branches of the subclavian artery. However, only 9% of these were visualized on aortography, while 91% were seen by selective angiography in the subclavian or more distal vessels. Angiography limited to injections in the ventricle or aorta may be insufficient to identify the majority of APCs. The importance of angiographic technique makes it difficult to interpret the results of catheterization-based studies for which the details of technique are not given [7, 8].
One previous study used direct intraoperative measurement to evaluate APC flow [6]. Ichikawa and colleagues [6] measured APC flow in 33 patients undergoing a Fontan procedure using methods similar to those of the current study. Ichikawa and colleagues’ [6] patients and their study findings both had important differences from ours. Their patients tended to be older (mean age, 6.7 vs 3.0 years), had fewer previous Glenn anastomoses (3% vs 100%), underwent more atriopulmonary Fontan procedures (60% vs 0%), and had no Fontan fenestrations (0% vs 100%). Fontan failure occurred in 9 of 33 patients (27%). Measured APC flow was similar in both extent and distribution to that in the current study. However, all 4 patients with APC flow more than 33% had Fontan pressures more than 17 mm Hg and were Fontan failures [6]. This negative impact of high APC flow contrasts with our findings. It is possible that APC flow can become a risk factor in patients who are at higher risk by virtue of older age, technical approach to the Fontan procedure (nonstaged, nonfenestrated, atriopulmonary connection), or other risk factors.
Some groups believe that coil occlusion of APCs is effective in reducing APC flow, and can improve the outcome of a Fontan operation [7, 8]. The current study was not designed to address these issues. We found that the 10 study patients who underwent preoperative coil occlusion of APCs had higher mean APC flow intraoperatively than the 22 patients who did not (Table 2). This likely reflects an initial selection of patients with higher APC flow for coil occlusion. The amount of APC flow in these 10 patients would be fascinating if they not had coils placed, but this amount is unknown. In our experience, APCs are typically multifocal in origin and diffuse in nature, so effective elimination by coils can be difficult. Ultimately, the question of whether coil occlusion of APCs is effective can only be answered by a study of patients with APCs undergoing coil occlusion in a randomized fashion; important to this type of study would be the timing of preoperative APC occlusion. In the current study, a shorter time (< 2 months) between coil placement and Fontan procedure correlated with lower APC flow measured intraoperatively (Table 2). This finding suggests that if APCs are coil occluded, they should be occluded within a short time of the Fontan procedure. This finding is obviously limited by the small number of patients in our study who underwent coil occlusion of APCs.
The method of direct intraoperative measurement of APC flow used in this study has both strengths and limitations. The primary strength of the method is that it gives a quantitative measurement of APC flow. This is an advantage over cardiac catheterization, which gives a qualitative estimate of APC flow. Other strengths of the methods used in this study were the standardization of blood pressure from patient to patient, the normalization of APC flow by expression as a percentage of total pump flow, and the avoidance of vasoactive agents that might have affected APC flow. The correlation between the two APC flow measurements in each patient is an indication of the consistency of the method.
The primary limitation of direct intraoperative measurement is that APC flow is measured under nonphysiologic conditions during general anesthesia and total cardiopulmonary bypass. Differences between these conditions and a normal physiologic state include nonpulsatile arterial waveform, central venous and pulmonary venous pressures equal to or less than zero, lack of lung ventilation, lack of pulmonary blood flow through the pulmonary arteries, and subnormal temperature. Any of these differences might affect APC flow so that direct intraoperative measurement does not accurately reflect APC flow under physiologic conditions. The correlations between APC flow and preoperative systemic oxygen saturation, pulmonary artery oxygen saturation, Qp:Qs, and angiographic APC grade (Table 1) suggest that directly measured flow does reflect flow under physiologic conditions. Nonetheless, the nonphysiologic conditions at the time of measurement are a methodological limitation of our study.
The conclusions of this study may also be limited by the characteristics of the patients in the study. These patients underwent a fairly consistent approach to the Fontan procedure. All patients had a previous bilateral superior cavopulmonary connection and a Fontan procedure consisting of a total cavopulmonary connection with fenestration. The age at Fontan procedure was fairly uniform, with 90% from 1 to 4 years of age, and 93% undergoing a Fontan procedure between 10 and 35 months after superior cavopulmonary connection. Most of the patients had few risk factors for a Fontan procedure. Out of 32 patients, only 2 patients had atrioventricular valve regurgitation more than grade 2/4, 3 patients had mean pulmonary artery pressure more than 13 mm Hg, 1 patient had transpulmonary gradient more than 6 mm Hg, 4 patients had ventricular end-diastolic pressure more than 12 mm Hg, and 5 patients had depressed ventricular function. These patient characteristics are similar to those in recent series of Fontan procedures [5, 11, 12]. Thus, our findings are probably applicable to most patients undergoing a Fontan procedure in the current era. However, it is possible that APC flow may be more important in patients undergoing a different approach to a Fontan procedure (see Ref 6).
This study does leave open the possibility that APC flow is important in an occasional patient. This seems particularly true in a patient with prolonged drainage of effusions after a Fontan procedure. In such a patient, we advocate aggressive diagnostic evaluation, including cardiac catheterization. If no correctable anatomic defects other than APCs are found, then coil occlusion of the APCs is a reasonable approach. While there is no hard (randomized) data to support this approach, coil occlusion is generally a low risk procedure, and several groups have experience with a small number of such patients who stop draining after coil occlusion [7, 8]. One patient in the current study (with intraoperative APC flow of 12%) underwent coil occlusion of APCs on postoperative day 27, and stopped draining 4 days later. In cases like this, even a small amount of APC flow may combine with other factors to put a patient over a threshold for prolonged drainage of effusions.
In summary, this study used direct intraoperative measurements to quantify APC flow in patients undergoing a Fontan procedure. The APC flow was present in all of the study patients in amounts many times higher than control patients. The extent of APC flow varied widely, from 9% to almost half of total pump flow. Patients with higher preoperative aortic and pulmonary arterial oxygen saturations, higher Qp:Qs, and higher angiographic APC grade had higher APC flow. Increased APC flow had no significant effect on the outcome of the Fontan procedure, as assessed by Fontan failure, early postoperative hemodynamic status, duration of effusions, or resource utilization. These conclusions likely apply to most patients who are well prepared for a Fontan procedure, but may not extend to patients at higher risk. The effect of preoperative coil occlusion of APCs awaits a randomized study, although coil occlusion may be useful in the patient with prolonged postoperative effusions.
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Acknowledgments |
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TopAbstractIntroductionMaterial and methodsResultsCommentAcknowledgmentsDiscussionReferences |
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Discussion |
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TopAbstractIntroductionMaterial and methodsResultsCommentAcknowledgmentsDiscussionReferences |
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As you stated, my colleagues in San Diego looked at this issue, and we found that there was a correlation between the grade of the collaterals (ie, the size and number of collateral vessels) and the incidence of effusions. In parallel thinking, we looked at patients undergoing a bidirectional Glenn, and when you look at patients with or without accessory pulmonary blood flow, those with accessory pulmonary blood flow had an incidence of effusions about eight times higher than those without. So it is my personal belief that increased left to right shunt in these patients does play a role in the pathophysiology of effusions.
My question is as follows: In your study, you performed coil occlusion in 10 of 31 patients, and so this is not the natural history, but an intervened history. I wondered if you were not selecting the patients who would have had extremely high Qp/Qs values if you had not coiled them, and these patients may have been the ones who would have had effusion troubles had you not coiled them preoperatively.
DR BRADLEY: Thank you for your comments. I think I basically addressed most of the comments in my talk. There, I think, is a substantial difference between evaluating collateral flow by directly measuring it, as we did, and evaluating it by catheterization, as in previous studies for the reasons which I mentioned. My bias going into the study was the same as yours, that patients with increased pulmonary collateral flow should have a worse outcome, and I was a little surprised by the data, but the data is as I presented it.
The question you asked is a very good one. It is impossible to know, of course, what collateral flow in patients who were coiled would have been had they not been coiled. So it is an unknown. The only way to figure that out is probably going to be to randomize patients preoperatively with high collaterals identified at catheterization to coil or not coil and then see what their outcome is, maybe even see what their intraoperatively measured collateral flow is. That would be a great study. I hope it can be undertaken.
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