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Ann Thorac Surg 2007;84:888-893
© 2007 The Society of Thoracic Surgeons

Original Articles: Cardiovascular

Persistent Antegrade Pulmonary Blood Flow Post-Glenn Does Not Alter Early Post-Fontan Outcomes in Single-Ventricle Patients

Robert G. Gray, MDa, Karen Altmann, MDa, Ralph S. Mosca, MDa, Ashwin Prakash, MDa, Ismee A. Williams, MD, MSa, Jan M. Quaegebeur, MD, PhDa, Jonathan M. Chen, MDb,*

a Columbia University College of Physicians and Surgeons, New York, New York
b Joan and Sanford Weill Medical College of Cornell University, New York, New York

Accepted for publication April 24, 2007.

* Address correspondence to Dr Chen, Pediatric Cardiac Surgery, 525 E 68th St, Suite F695B, New York, NY 10023 (Email: jmc23{at}columbia.edu).

Presented at the Forty-third Annual Meeting of The Society of Thoracic Surgeons, San Diego, CA, Jan 29–31, 2007.


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 Discussion
 References
 
Background: The bidirectional Glenn cavopulmonary anastomosis (BDG) represents the standard interim procedure in treatment of patients with single-ventricle physiology. Anterograde pulmonary blood flow (APBF) maintained after BDG has been shown both to improve and to complicate postoperative clinical course. We studied its effects on outcome after BDG and eventual Fontan completion.

Methods: From November 1995 to November 2005, 60 patients underwent BDG and Fontan. All patients had APBF from the ventricle to the pulmonary artery at time of BDG. In group 1 (n = 39) APBF was maintained after BDG, whereas APBF was interrupted at BDG in group 2 (n = 21). Cardiac catheterization data, interstage morbidity, and postoperative outcome variables were recorded.

Results: Pre-BDG hemodynamics differed only in that the mean pulmonary artery pressure was higher in group 2 (17.0 ± 4.4 mm Hg) than in group 1 (13.8 ± 4.5 mm Hg; p = 0.03). There were no differences between groups 1 and 2 in BDG outcome variables. At pre-Fontan catheterization, group 1 had higher mean pulmonary artery pressure (13.3 versus 10.9 mm Hg, p = 0.01), arterial oxygen saturation (85.8 versus 80.9%, p = 0.0001), and fewer collateral vessels were coil embolized than in group 2 (0.9 versus 1.6, p = 0.02). Mean ventricular end-diastolic pressure was similar between groups. The Nakata index in group 1 remained stable from pre-BDG to pre-Fontan (348 versus 391, p = 0.24), but it decreased in group 2 (375 versus 227, p = 0.046).

Conclusions: Patients with anterograde pulmonary blood flow after BDG had a modest increase in pulmonary artery growth and arterial oxygen saturations, and decreased collateral vessel formation. This did not, however, confer additional benefit on outcome after BDG or on eventual Fontan completion.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 Discussion
 References
 
The bidirectional Glenn cavopulmonary anastomosis (BDG) represents the standard interim procedure in the surgical palliation of patients with single-ventricle physiology toward eventual Fontan circulation [1–3]. Physiologic advantages include a reduction in ventricular volume load with improved mechanical efficiency, improved arterial oxygen saturation, and prevention of pulmonary hypertension. However, the BDG provides less pulmonary blood flow than the normal or eventual Fontan circulation, which may lead to limited pulmonary artery (PA) growth before Fontan completion [4, 5].

The utility of anterograde pulmonary blood flow (APBF) or forward flow from the ventricle into the pulmonary arteries, maintained after BDG, remains controversial [6, 7]. In this setting, such APBF has been demonstrated both to improve and to complicate immediate postoperative and interstage clinical courses after the BDG procedure [8–15]. Proponents of preserving APBF after BDG suggest that it may increase arterial oxygen saturations, increase PA growth, reduce perioperative morbidity, and reduce collateral vessel formation. APBF may elevate central venous pressure, increase ventricular volume load, and negatively impact Fontan candidacy, however, and can also lead to increased interstage morbidity, including prolonged chest tube drainage, increased pulmonary vascular resistance, and longer hospital length of stay if this flow is excessive.

This study evaluated our single-center experience during a 10-year period with regard to the effects of APBF on clinical outcome after BDG and its consequence upon eventual Fontan completion in single-ventricle patients undergoing both BDG and Fontan procedures.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 Discussion
 References
 
Patient Population
The clinical and surgical records of 60 patients with single-ventricle physiology who underwent both BDG and Fontan procedures at the Morgan Stanley Children’s Hospital of New York-Presbyterian were retrospectively evaluated from November 1995 to November 2005. Patients undergoing the hemi-Fontan procedure were excluded.

All patients had APBF through a stenosed or banded main PA at the time of BDG and were subsequently divided into two cohorts according to the presence (group 1) or absence (group 2) of persistent APBF after the BDG procedure. All patients were followed up through Fontan completion.

The Columbia University Institutional Review Board approved this study and waived the requirement for patient consent.

Clinical Data
Pre-BDG and pre-Fontan cardiac catheterization data consisting of arterial oxygen saturation, hemoglobin concentration, mean PA and systemic ventricular end-diastolic pressure, number of collateral vessels that required coil embolization, PA pulse pressure, and PA size were recorded. PA pulse pressure was defined as the difference between the maximum systolic and minimal diastolic PA pressure. PA size was analyzed using the methods of Nakata and colleagues [16]. PA diameters were measured immediately proximal to their hilar bifurcation; cross-sectional areas were calculated, summed, and divided by the body surface area, resulting in a value termed the Nakata index.

Intraoperative and postoperative data obtained at the time of BDG and Fontan palliation included age and BSA, cardiopulmonary bypass and aortic cross-clamp times, length of intubation, length of chest tube drainage, and length of stay in the intensive care unit and hospital. Morbidity included chest tube drainage of 10 days or more, hospital length of stay of 14 days or more, need for hospital readmission, emergency cardiac catheterization, or reoperation.

Echocardiographic Data
Transthoracic echocardiographic data was obtained before the BDG and Fontan procedures, as well as after Fontan completion. Systemic ventricular contractility was qualitatively graded as 1, normal; 2, mildly decreased; 3, moderately decreased; 4, severely decreased. Single-ventricular ejection fraction or shortening fraction calculations were not routinely performed secondary to differing ventricular morphologies (morphologic right versus left) as well as frequent conduction abnormalities that limit the accuracy and reproducibility of such measurements. Atrioventricular valve regurgitation (AVVR) was qualitatively graded as 1, none; 2, mild; 3, moderate; and 4, severe.

Surgical Technique
BDG was performed at our institution secondary to severe cyanosis or before 1 year of age. Cardiopulmonary bypass was routinely used, with occasional aortic cross-clamping. The cavopulmonary anastomosis consisted of an end-to-side connection of the superior vena cava to the PA. All central or modified Blalock-Taussig shunts were ligated and divided during BDG.

The decision to leave APBF at the time of BDG was made by the operating surgeon at the time of operation. Our practice is to base this decision in part upon the pre-BDG PA pressure, the size of the native PAs, and any technical difficulty anticipated for its removal at the time of eventual Fontan. In situations in which the resistance is believed to be low and the PA pressure is 20 mm Hg or more, we routinely eliminate antegrade flow. However, if the patient is a marginal BDG candidate (eg, small branch PAs, history of chronic lung disease), we often leave ABPF to afford adequate oxygenation. The pulmonary bands are not adjusted or tightened at the time of BDG; rather, the APBF is allowed to remain or is removed.

The Fontan procedure was generally performed before 4 years of age. The total cavopulmonary circuit was completed using a lateral tunnel intraatrial baffle or an external conduit, with or without fenestration, at the discretion of the operating surgeon. Any residual APBF was excluded at the time of Fontan completion.

Statistical Analysis
Preoperative and postoperative data were analyzed and compared between groups. Continuous variables are expressed as mean ± standard deviation. A two-sample, unpaired Student t test was used to compare variables between groups, a paired t test was used to compare the Nakata index pre-BDG and pre-Fontan, and {chi}2 analysis was used to compare frequencies of categoric variables. Calculations were done with InStat 2.01 software (GraphPad Software Inc, San Diego, CA). A value of p ≤ 0.05 indicated statistical significance.


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 Discussion
 References
 
Patient Demographics
Patient anatomic characteristics are summarized in Table 1, and surgical data are summarized in Table 2. During the study period, an additional 85 patients underwent BDG and are currently awaiting Fontan completion.


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  		Table 1 Patient Anatomic Characteristics
 

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  		Table 2 Patient Procedure Summary
 
Pre-Bidirectional Glenn Catheterization
There were no significant differences between groups 1 and 2 in arterial oxygen saturation (78% ± 5% versus 78% ± 6%, p = 0.86), hemoglobin concentration (16.0 ± 1.9 versus 14.6 ± 2.2 g/dL, p = 0.07), systemic ventricular end-diastolic pressure (8.0 ± 2.9 versus 8.5 ± 4.1 mm Hg, p = 0.58), PA pulse pressure (8.3 ± 7.3 versus 11.5 ± 8.1 mm Hg, p = 0.20), or PA size (350 ± 185 versus 375 ± 164, p = 0.70). Mean PA pressure was higher in group 2 (17.0 ± 4.4 mm Hg) than in group 1 (13.8 ± 4.5 mm Hg; p = 0.03) before BDG.

Bidirectional Glenn Perioperative Variables
There were no differences between groups 1 and 2 in age at surgery (1.0 ± 0.8 versus 1.1 ± 1.3 years, p = 0.61), BSA (0.37 ± 0.09 versus 0.37 ± 0.09 m2, p = 0.89), cardiopulmonary bypass time (92 ± 61 versus 110 ± 41 minutes, p = 0.23), cross-clamp time (33 ± 43 versus 38 ± 31 minutes, p = 0.69), length of intubation (2.3 ± 3.3 versus 2.2 ± 2.8 days, p = 0.95), length of chest tube drainage (5.3 ± 8.9 versus 3.7 ± 3.0 days, p = 0.42), or length of stay in the intensive care unit (4.9 ± 3.6 versus 5.4 ± 4.2 days, p = 0.67) or in the hospital (9.7 ± 9.6 versus 8.4 ± 4.5 days, p = 0.55). Chest tube drainage of 10 days or more was seen in three patients (8%) in group 1 and two patients (10%) in group 2 (p = 1.00). Four patients (10%) in group 1 and two patients (10%) in group 2 had hospital stays of 14 days or more (p = 1.00).

Interstage complications were similar between groups. Three patients (8%) in group 1 required hospital readmission owing to pleural effusions requiring chest tube placement. Two patients in group 2 (10%) were readmitted, one with a chylous pericardial effusion requiring a surgical pericardial window and one with a sternal wound infection (p = 1.00). In addition, three patients (8%) in group 1 and two patients (10%) in group 2 underwent cardiac catheterization postoperatively (p = 1.00).

One patient in each cohort required reoperation (p = 1.00). The patient in group 1 required aortic valve repair after subaortic obstruction resection at the time of BDG, and the patient in group 2 underwent recurrent coarctation repair.

Morbidity between groups did not differ significantly. There was no immediate or interstage mortality. The incidence of clinical superior vena caval syndrome, defined as marked swelling of the head and upper chest, did not differ between groups.

Pre-Fontan Catheterization
Mean PA pressure (central venous pressure), PA pulse pressure, and arterial oxygen saturation were significantly higher in group 1 compared with group 2 (Table 3). Fewer collateral vessels were coil embolized in group 1 than group 2. There was no difference in ventricular end-diastolic pressure between cohorts (8.9 ± 2.3 versus 8.3 ± 1.7 mm Hg).


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  		Table 3 Comparisons of Pre-Fontan Cardiac Catheterization Variables
 
Fontan Perioperative Variables
No significant differences were found between groups 1 and 2 in patient age (3.4 ± 1.1 versus 3.6 ± 1.7 years, p = 0.57), BSA (0.57 ± 0.08 versus 0.60 ± 1.3 m2, p = 0.37), cardiopulmonary bypass time (129 ± 39 versus 125 ± 41 minutes, p = 0.70), cross-clamp time (59 ± 21 versus 53 ± 29 minutes, p = 0.40), length of intubation (2.6 ± 4.2 versus 4.0 ± 6.3 days, p = 0.33), length of chest tube drainage (11.3 ± 9.8 versus 13.2 ± 8.1 days, p = 0.44), and length of stay in the intensive care unit (7.1 ± 6.2 versus 6.4 ± 5.8 days, p = 0.67), or hospital (16.6 ± 17.4 versus 17.5±10.2 days, p = 0.83).

Cardiac catheterization for low cardiac output or persistent chest tube drainage was required within the immediate postoperative period in four patients (10%) in group 1 and in four patients (19%) in group 2 (p = 0.43). Chest tube drainage of 10 days or more occurred in twelve patients (31%) in group 1 and in fourteen patients (67%) in group 2 (p = 0.01). Fourteen patients (36%) in group 1 and twelve patients (57%) in group 2 (p = 0.17) had a prolonged hospital stay of 14 days or more. Death due to severe AVVR occurred in one patient in each group.

Echocardiographic Data
No significant differences were found between groups in systemic ventricular contractility from pre-BDG (1.1 ± 0.2 versus 1.1 ± 0.4, p = 0.31) through Fontan completion (1.2 ± 0.4 versus 1.3 ± 0.5, p = 0.33). AVVR was also similar between groups from pre-BDG (1.4 ± 0.6 versus 1.7 ± 0.9, p = 0.16) through Fontan completion (1.7 ± 0.6 versus 1.9 ± 0.8, p = 0.17). Analysis within groups (Table 4), however, revealed a modest but significant decrease in systemic ventricular contractility (p = 0.03) as well as an increase in AVVR (p = 0.002) in group 1 from pre-BDG to post-Fontan. Similarly, systemic ventricular contractility decreased and AVVR increased in group 2 from pre-BDG to post-Fontan; however, only the increase in AVVR reached statistical significance (p = 0.04).


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  		Table 4 Intragroup Analysis of Transthoracic Echocardiographic Data
 
Pulmonary Artery Growth
The Nakata index was not different between groups 1 and 2 at the time of pre-BDG catheterization (348 ± 182 versus 375 ± 164, p = 0.67) or at time of pre-Fontan catheterization (386 ± 266 versus 227 ± 158, p = 0.06; Table 5). However, analysis within group 1 demonstrated PA growth commensurate with increases in BSA, while a significant decrease in Nakata index (375 ± 164 versus 227 ± 158, p = 0.046; Fig 1) occurred in group 2 patients from the pre-BDG to pre-Fontan catheterization.


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  		Table 5 Nakata Index Comparison Between Patient Cohorts
 

Figure 1
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  		Fig 1. Interstage pulmonary artery growth comparison from time of pre-bidirectional Glenn (BDG; clear bars) to pre-Fontan catheterization (black bars) according to the Nakata index. Group 1 had pulmonary artery growth commensurate with increases in body surface area, but group 2 did not.

 

   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
Discussion
 References
 
Outcomes after the modified Fontan palliation for single-ventricle patients have improved substantially with the introduction of a staged approach using the interim BDG procedure [1, 2, 3]. The advantages of this strategy are thought to be the concurrent provision of effective pulmonary blood flow with decrement in ventricular volume load. Disadvantages include decreased pulmonary blood flow possibly influencing PA growth [4. 5].

Maintaining APBF at time of BDG has been demonstrated to increase arterial oxygen saturations and improve PA growth; however, the possible provision of excessive flow may contribute to interstage morbidity [13]. This study demonstrates that patients with APBF post-BDG enjoyed a modest increase in PA growth and interstage arterial oxygen saturations as well as decreased collateral vessel formation compared with those without APBF. Persistent APBF did not, however, confer additional benefit on outcome after BDG or on eventual Fontan completion. Our results are notable for several key observations.

First, previous investigators have demonstrated a high incidence of prolonged pleural drainage immediately after BDG and interstage rehospitalization with pleural effusions requiring drainage, thought to be due to increased central venous pressure leading to decreased lymphatic drainage [6, 11, 13]. More recent reports have suggested that "controlled" APBF with a pulmonary artery band to limit PA pressure while providing additional pulmonary flow may attenuate this finding and decrease postoperative morbidity [8, 9]. Our results did not demonstrate prolonged chest tube drainage or increased incidence of hospital readmission with pleural effusions in patients with unregulated APBF after BDG. In fact, more patients without APBF demonstrated prolonged chest tube drainage after Fontan than those with APBF after BDG, although the cohorts are small.

Second, others have suggested that provision of APBF after BDG may lead to increased postoperative arterial oxygen saturation and shortened lengths of intubation and hospital stay [7, 9]. In our study, although group 1 had persistently higher oxygen saturations (86% versus 81%) and decreased hemoglobin levels (15.4 versus 16.6 mg/dL) at the time of Fontan compared with group 2, this did not lead to decreased postoperative morbidity.

Third, most of the controversy over the maintenance of pulsatile APBF after BDG surrounds the potential enhancement of PA growth after BDG [4, 5, 17–20]. We demonstrated that those without APBF did not enjoy the same degree of PA growth as those with APBF. These differences, however, were modest and did not correlate with appreciable differences in clinical outcome after BDG or Fontan.

Of note, 5 patients with APBF after BDG who required reintervention for recurrent or persistent pleural effusions have not yet undergone their Fontan completion and therefore were not included in the study cohort. In 3 patients, the antegrade flow was interrupted by transcatheter device closure during cardiac catheterization, and they are currently awaiting programmed Fontan completion. Of these, only 1 had a PA pressure of 15 mm Hg or less pre-BDG.

Two patients, however, became profoundly cyanotic upon balloon occlusion of APBF during catheterization and therefore did not tolerate device closure. One patient with severe AVVR required BDG reversal with concurrent central shunt placement and died shortly thereafter; his pre-BDG PA pressure was 20 mm Hg. The other patient, whose pre-BDG PA pressure was 13 mm Hg, underwent no additional therapy and had normal mean PA pressures (13 mm Hg) 26 months after BDG; however, the patient died 16 months later from complications related to an underlying genetic disorder.

Although these 5 patients were not included in the study cohort, they underscore a potential significant morbidity that could affect Fontan candidacy in patients with maintained APBF.

Several limitations deserve comment. This evaluation is subject to the restrictions of a retrospective, nonrandomized study of a relatively small number of patients. The intraoperative decision to preserve or eliminate APBF after BDG and the type (lateral tunnel or extracardiac conduit) of completion Fontan was at the discretion of the surgeon. By its nature and follow-up, this study does not include patients who are currently awaiting Fontan. The preoperative characteristics of both groups were slightly different, with group 1 having lower pre-BDG PA pressures, possibly affecting group comparisons and likely reflecting our own practice patterns. The effects of APBF within group 1 were likely heterogeneous, as its magnitude was not regulated. Finally, Fontan outcome assessment was limited to the immediate postoperative period and the long-term affects of APBF after BDG are unknown at this time.

In summary, although BDG with APBF improves arterial oxygen saturations and PA growth and decreases collateral artery formation, it conferred no additional benefit to the outcome at the time of modified Fontan completion. At our institution, the decision to maintain APBF at the time of BDG is made by the operating surgeon at time of surgery and is partly based on the pre-BDG PA pressure, the size of the native PAs, any technical difficulty anticipated for its removal at the time of eventual Fontan, and the likelihood that its elimination will result in insufficient pulmonary blood flow. We cautiously endorse this strategy, with the understanding that in selected patients, the maintenance of antegrade flow could negatively affect Fontan candidacy.


   Discussion
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Discussion
References
 
DR JEFFREY P. JACOBS (St. Petersburg, FL): Thank you for that very nice presentation addressing what is obviously a decision we all have to make almost every time we go to do a Glenn to decide what we are going to do with the pulmonary artery.

I wanted to ask, by excluding patients from the study who haven’t yet had the Fontan that means potentially you are going to completely exclude patients who never make it to Fontan for whatever reason. So doesn’t that kind of bias what you are doing by just making it that those patients never be part of the study?

DR GRAY: Thank you Dr Jacobs, that is a great question. This study was not undertaken to evaluate risk factors affecting eventual Fontan candidacy, but rather to look at the effects of antegrade pulmonary blood flow on outcome after both BDG and upon Fontan completion.

At our institution, we have three surgeons with differing opinions regarding antegrade flow; therefore, we undertook the study to try and elucidate whether leaving antegrade flow at the time of BDG is the best method. Even though we did not find marked differences between groups, the observed increase in PA growth found in patients with antegrade flow would likely be beneficial in situations such as small pulmonary arteries or bilateral SVCs.

That being said, also included in the discussion are data on patients with antegrade flow that have required interstage cardiac catheterization secondary to recurrent or persistent pleural effusions. Although these patients were not included in the study cohort, they underscore a potential significant morbidity that could affect subsequent Fontan candidacy, which is the subject of ongoing investigation.

DR HILLEL LAKS (Los Angeles, CA): I very much enjoyed your paper, and I was pleased that some of the conclusions you had were similar to ours. We have advocated having antegrade flow as part of a bidirectional Glenn procedure for many years with the hope that we would have better pulmonary artery development, less collateral development, and also a greater response to exercise because you can increase flow with exertion. As the blood pressure is raised, the antegrade flow increases as well.

The concern has always been and those who are against it was that you might have increased pulmonary vascular resistance, and we have always felt that the way to control that has been to know how much antegrade flow that you have and to control the antegrade flow and to aim for a Qp/Qs including your Glenn flow and your antegrade flow of no more than about 1 or 1.3 maximum. So that if your Glenn is providing 35% or 30% of venous return, depending on the age of the child, you would still have a shunt from the antegrade flow which would be no more than 0.6 or so, maybe 0.7.

And, therefore, it becomes very important as to what you do with the antegrade flow at the time of the Glenn, how you are timing your Glenns. So that institutions that wait until children become profoundly cyanotic before doing the Glenn, the Qp/Qs is already down at that level, and you don’t need to modify the antegrade flow. Whereas an institution that is doing the Glenns electively at 3 or 4 months, the Qp/Qs from the antegrade flow could be 1.5 to 1. And if you simply add a Glenn to that situation, then you are stuck with a prolonged time of increased flow.

So it is always our practice to do Glenns early but to tighten the band on the pulmonary artery or narrow the shunt at the time if the estimated Qp/Qs from the antegrade flow is greater than what was desired. Do you have any idea in your series what was done with antegrade flow, the timing of the Glenns, and to what extent antegrade flow was or was not controlled as part of the original Glenn?

DR GRAY: Thank you for that very interesting question. Others have recently written about the benefits of controlled antegrade pulmonary blood flow, and although I do not have quantitative shunt data readily available, our patients who had antegrade flow interrupted as part of their Glenn procedure had significantly higher preoperative oxygen saturations, implying that antegrade flow was more often taken down when excessive, and maintained when physiologically limited.

It is our practice to leave antegrade flow through the native pulmonary artery and not through interposition grafts. We do not, however, manipulate the flow by tightening pulmonary artery bands, for example.

Currently we perform the BDG by 4 to 6 months of age or sooner if they become profoundly cyanotic; however in this series, the mean age of patients undergoing BDG was 1 year.

DR LAKS: Thank you. I just think it is important that at the time of the Glenn, the surgeon consciously tries to calculate what the Qp/Qs from antegrade flow is and makes it appropriate to avoid overcirculation. Thank you.

DR GRAY: Thank you.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Discussion
 References
 

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