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Ann Thorac Surg 1995;59:433-437
© 1995 The Society of Thoracic Surgeons

Extent of Aortopulmonary Collateral Blood Flow as a Risk Factor for Fontan Operations

Hajime Ichikawa, MD, Toshikatsu Yagihara, MD, Hidefumi Kishimoto, MD, Fumitaka Isobe, MD, Fumio Yamamoto, MD, Kyouichi Nishigaki, MD, Osamu Matsuki, MD, Tsuyoshi Fujita, MD

Department of Cardiovascular Surgery, National Cardiovascular Center, Osaka, Japan

Accepted for publication October 6, 1994.


   Abstract
Top
 Footnotes
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
Between November 1987 and January 1990, 33 patients (tricuspid atresia, 9 patients; mitral atresia, 3; single ventricle, 15; others, 6) underwent Fontan operations. The rate of blood flow returning to the heart during aortic cross-clamping was measured as an indication of the extent of development of aortopulmonary collateral arteries. Percent cardiac return (calculated by dividing the blood flow rate returning to the heart by the cardiopulmonary bypass blood flow rate and expressing the value as a percentage), were 1% to 9%, 7 patients; 10% to 19%, 11; 20% to 29%, 9; 30% to 39%, 4; 40% to 49%, 1; and 50% to 59%, 1 patient. Percent cardiac return showed a significant correlation with postoperative mean systemic venous pressure (r = 0.6, p < 0.01). In those patients in whom percent cardiac return was more than 33%, the mean systemic venous pressure after operation was high (more than 17 mm Hg), and none of these patients survived. To predict percent cardiac return preoperatively, the conventional indices of systemic ventricular volume, pulmonary artery area index, arterial blood oxygen saturation, pulmonary blood flow index, and pulmonary vascular resistance were analyzed. None of these showed significant correlation with percent cardiac return. However, all the patients who had a high percent cardiac return (more than 30%) also had both high arterial blood oxygen saturation (more than 75% in room air) and small pulmonary artery area index (less than 55%). In addition, the age at operation showed good correlation (r = 0.6, p < 0.01) to percent cardiac return. We conclude that high percent cardiac return is one of the risk factors for Fontan operations and can be predicted preoperatively, even if the collateral arteries are not always visible on angiography. If aortopulmonary collaterals are visible on angiography, it is suggested that their preoperative embolization may decrease percent cardiac return and hence operative risk.


   Introduction
Top
 Footnotes
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
A lthough the outcome of Fontan operations for tricuspid atresia has improved due to greater preoperative morphologic and hemodynamic assessment, and by the better selection criteria for operations [1, 2], extension of these criteria to more severe cases and complex cardiac anomalies [3] is still controversial [4].

The hypotheses for this study were (1) The outcome of Fontan operations is related to the extent of development of aortopulmonary collateral arteries and (2) the extent of aortopulmonary collaterals can be assessed preoperatively and may be regarded as an independent risk factor for predicting the outcome of Fontan operations.

We measured the rate of blood flow returning to the heart during cardiac arrest as an indication of the extent of aortopulmonary collateral arteries. The correlation of the extent of these collaterals to preoperative and postoperative hemodynamic and morphologic indices and to the outcome of the patients is discussed. The usefulness of preoperative embolization of aortopulmonary collateral arteries also is discussed.


   Material and Methods
Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 Acknowledgments
 References
 
Patients
Thirty-three patients who underwent Fontan operations between November 1987 and January 1990, and in whom the rates of nonpulmonary collateral flow during aortic cross-clamping were measured, were included in this series of analysis. The study consisted of 15 patients with situs solitus (tricuspid atresia, 9; mitral atresia, 3; single ventricle, 1; pulmonary atresia, 1; pulmonary stenosis, 1); 2 patients with situs inversus (double-outlet right ventricle) and 16 patients with right isomerism (single ventricle, 15Au: OK? [left ventricular type, 4; right ventricular type, 11]; double-outlet right ventricle, 1). The age of the patients ranged from 1 to 16 years (mean ± standard deviation, 6.7 ± 3.8 years).

Eighteen patients had undergone a palliative cardiovascular operation previously (modified Blalock-Taussig shunt, 16 patients; Glenn anastomosis, 1; modified Waterston shunt, 1; pulmonary arterial banding, 1; atrial septal defect creation, 1 patient).

Embolization of nonpulmonary collateral vessels were performed in 4 patients who showed significant major aortopulmonary collateral arteries (MAPCA) by aortography.

The preoperative hemodynamic and morphologic indices were as follows: pulmonary blood flow index (QpI), 1.6 to 8.3 L/m2 (4.1 ± 2.0 L/m2); pulmonary vascular resistance index, 0.4 to 3.7 Um2 (2.1 ± 1.7 Um2); systemic ventricular end-diastolic volume index, 82 to 294 mL/m2 (149 ± 46 mL/m2); systemic ventricular end-systolic volume index, 29 to 148 mL/m2 (68 ± 27 mL/m2); ejection fraction of the systemic ventricle, 0.42 to 0.75 (0.55 ± 0.09); pulmonary arterial area index (PAAI; mean pulmonary artery (PA) sectional area divided by normal right PA area), 0.35 to 1.36 (0.67 ± 0.29). Normal right PA area was obtained using the equation of Hernandez and Castellanos [5].

Surgical Techniques
Direct anastomosis of the right atrium to the pulmonary artery and closure of atrial septal defect was performed in 20 patients. In the remaining 13 patients, the intraatrial grafting method was used, as described by Humes and colleagues [6]. Briefly, the superior vena cava was anastomosed directly to the pulmonary artery in an end-to-side manner and the inferior vena cava was anastomosed to the pulmonary artery with an intraatrial tube graft (Gore-Tex; W. L. Gore, Flagstaff, AZAu: location of manufacturer OK?) of appropriate size (Fig 1Go)fig 1Go.



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  		Fig 1. . Schematic illustration of the modified Fontan procedure for complex anomalies. The superior vena cava (SVC) is anastomosed directly to the pulmonary artery. The inferior vena cava (IVC) also is anastomosed to the pulmonary artery but with an intraatrial Gore-Tex conduit.

 
Measurement of Aortopulmonary Blood Flow
Palliative shunts were occluded immediately after cardiopulmonary bypass was started. During cardioplegic arrest, the aortopulmonary collateral blood flow returning to the heart by the pulmonary vein was measured immediately after the atrium was opened. This was achieved by placing two suction tubes in the heart that continuously sucked the blood returning to the heart. The volume of blood was measured in a isolated cardiotomy reservoir during a 1-minute period, on more than three separate occasions, and an average rate of blood flow was calculated. Contamination with ice slush was carefully avoided by the use of wall suction. The flow rate of the cardiopulmonary bypass was adjusted to maintain the perfusion pressure about 40 mm Hg and ranged from 40 to 230 mL/kg (mean, 127 ± 29 mL/kg). The duration of cardiopulmonary bypass and cardiac arrest ranged from 70 to 448 minutes (mean, 168 ± 72 minutes) and from 18 to 130 minutes (mean, 55 ± 30 minutes), respectively. Chlorpromazine was used routinely as a vasodilator up to 2 mg/kg.

Calculation of Percent Cardiac Return
The extent of collateral flow was expressed by the percentage (percent cardiac return, %CR) of this flow rate to the blood flow from cardiopulmonary bypass.

Statistics
The significance of relations between variables was evaluated by linear regression analysis. A p value less than 0.05 was considered significant.


   Results
Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 Acknowledgments
 References
 
Distribution of Percent Cardiac Return
The %CR ranged from 6% to 55%; 1% to 9%, 7 patients; 10% to 19%, 11; 20% to 29%, 9; 30% to 39%, 4; 40% to 49%, 1; and 50% to 59%, 1 patient (Fig 2Go)fig 2Go. The %CR of patients with or without preoperative systemic to pulmonary shunt operation were 22.6% ± 11.9% and 15.4% ± 9.4%, respectively. There was no significant difference.



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  		Fig 2. . Number of patients is grouped by percent cardiac return (%CR). The hatched section represents the patients who underwent preoperative embolization of the aortopulmonary collaterals.

 
Percent Cardiac Return and Patient Outcomes
The necessity to take down the Fontan operation and hospital death occurred in 4 patients and 8 patients (including 3 patients in which the Fontan procedure was taken down), respectively. Patients who only underwent the planned Fontan procedure and survived were defined as successful, whereas patients in whom the operation had to be revised or patients who died in hospital were defined as unsuccessful.

Systemic venous pressure 6 hours after operation and %CR showed a significant correlation (r = 0.6, p < 0.01) (Fig 3Go)fig 3Go. There was no significant difference in postoperative systemic venous pressure between the two operative procedures. All patients with a %CR of more than 33% were unsuccessful and had high systemic venous pressure (more than 17 mm Hg, n = 4, filled circle in Fig 3AGou: no filled circles in Fig 4Go; Fig 3Go OK?) after operation. The %CR did not show any significant correlation with postoperative left atrial pressure or the difference between left atrial and systemic venous pressure (data not shown).



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  		Fig 3. . Relationship between percent cardiac return (%CR) and postoperative mean systemic venous pressure; unsuccessful cases are represented by filled circles. (RAP = right atrial pressure.)

 


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  		Fig 4. . Preoperative end-diastolic volume (EDVI) of the systemic ventricle plotted against percent cardiac return (%CR). Patients who underwent preoperative embolization of the major aortopulmonary collateral arteries were excluded in this analysis.

 
Relationship Between Percent Cardiac Return and Conventional Indices Before Operation
There was no significant correlation between preoperative end-diastolic systemic ventricular volume and %CR (Fig 4Go) nor any significant correlation between PAAI and %CRfig 4. However, many of the patients who had high %CR were distributed in the PAAI below 0.55 area (Fig 5Go). Figure 6Go shows the plot between PAAI and preoperative arterial blood oxygen saturation in room airfig 6. Patients with high %CR (more than 30%) had a low PAAI (less than 55%) and a high arterial blood oxygen saturation (more than 75%). Moreover, CR had no significant correlation with pulmonary vascular resistance or pulmonary vascular flow index (data not shown).



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  		Fig 5. . Preoperative pulmonary arterial area index (PAAI) plotted against percent cardiac return (%CR). The dotted line represents a pulmonary arterial area index of 0.55. Patients who had a high percent cardiac return were distributed below this line. Patients who underwent preoperative embolization of the major aortopulmonary collateral arteries were excluded in this analysis.

 


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  		Fig 6. . Relationship between percent cardiac return (%CR), preoperative oxygen saturation of arterial blood (SaO2), and pulmonary arterial area index (PAAI). Vertical and horizontal lines Au: no dotted lines in artrepresent a pulmonary arterial area index of 0.55 and an oxygen saturation of arterial blood of 75%, respectively. All the patients with a high percent cardiac return showed a high oxygen saturation of arterial blood (more than 75%) and a low pulmonary arterial area index (less than 0.55%). The incidence of the high percent cardiac return (more than 30%) in the left upper area of the plot was significantly higher than that of other groups (55% versus 0%).

 
The age at operation was significantly related to the %CR in those patients who had not undergone embolization (r = 0.6, p < 0.01) (Fig 7Go), suggesting that longer hypoxic periods may lead to highly developed aortopulmonary collateral anastomoses.



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  		Fig 7. . Relationship between percent cardiac return (%CR) and age at operation.

 
In addition, in a 16-year-old patient with a single ventricle (which is usually associated with the development of aortopulmonary collaterals), we found MAPCAs arising both from the thoracic and the abdominal aorta and embolized them 10 days before operation. The %CR was exceptionally low (9%) for this age and the postoperative course was uneventful.


   Comment
Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
Acknowledgments
 References
 
The selection criteria for Fontan operations is based mainly on the morphology of the pulmonary artery and the hemodynamics of the pulmonary circulation [7, 8]. By applying these criteria, the outcome of Fontan operations for tricuspid atresia has improved [9], but not for complex cardiac anomalies even when the pulmonary arteries are in a satisfactory condition. In this study we quantified the degree of aortopulmonary collaterals by measuring blood flow returning to the heart during cardioplegic arrest and demonstrated that highly developed aortopulmonary collaterals, which remains postoperatively, can be an independent major risk factor for Fontan operations and suggest that it is possible to predict this risk factor preoperatively.

As the size of the central pulmonary artery represents the degree of the development of the pulmonary vascular bed, central pulmonary arterial size is considered as one of the most important factors among the classic 10 criteria for Fontan operations. The pulmonary vascular resistance calculated by the Fick's method is also an important factor by the same reason.

There are, however, several reasons to be skeptical regarding the use of pulmonary vascular resistance, as measured by Fick's method, as a criterion for deciding on the suitability of Fontan operation. First, as the pulmonary blood flow is a low pressure circulation, the error may be bigger when vascular resistance is calculated. Palliative procedures performed before Fontan operation also make accurate measurement difficult, particularly in patients with complex cardiac anomalies. Second, the pulmonary vascular resistance measured before operation represents the resistance when the blood flow is pulsatile, whereas after Fontan operation pulmonary blood flow becomes nonpulsatile. Therefore, the static resistance must be predicted from the dynamic resistance [10]. Finally, as the QpI calculated by Fick's method includes the blood flow through the aortopulmonary arteries, the resistance to the blood flow through the main pulmonary artery after Fontan operation is higher than the calculated value, particularly in patients whose aortopulmonary collaterals are highly developed (which is frequent in the cyanotic patients who are candidates for Fontan operations).

In the present study, a high %CR was associated with a high systemic venous pressure after Fontan operation (see Fig 3Go), possibly attributable to an increase in the resistance of the pulmonary artery (not including collaterals). This high systemic venous pressure usually causes postoperative complications such as supraventricular arrhythmias and liver dysfunction [11]. Furthermore, with a high %CR, the heart must produce a high cardiac output to maintain sufficient blood flow to perfuse systemic organs (excluding the lung). The heart usually cannot achieve such a high cardiac output without volume expansion. Thus, a vicious circle ensues because the most effective way to obtain an adequate cardiac output is to increase the systemic venous pressure that is already high. The correlation between %CR and postoperative left atrial pressure is not good, which suggests that left (or systemic) atrial pressure is affected by other factors such as systemic ventricular performance or atrioventricular valve regurgitation.

In the patients with high %CR, pulmonary vessels are exposed to the increased blood flow by highly developed collaterals during cardiopulmonary bypass. This "flooding of the lung'' may also be the cause of high pulmonary vascular resistance after Fontan operation.

Even without MAPCAs, patients with cyanotic congenital heart disease frequently have high amounts of collateral flow by numerous small collaterals. These secondary developed systemic pulmonary collaterals originated from bronchial, intercostal, and subclavian arteries. It is difficult to diagnose the existence of these highly developed collaterals by preoperative angiography.

To determine if it was possible to predict preoperatively patients with a high %CR, data from conventional hemodynamic indices were analyzed retrospectively.

First, the hypothesis that a high %CR would be a cause of volume overload to the heart could not be proved because of the poor correlation of %CR with end-systolic volume index or end-diastolic volume indexAu: spelling out of ESVI and EDVI OK? data. This discrepancy may be explained by the fact that ventricular volume is affected by many factors, particularly by common atrioventricular valve regurgitation that was often seen in our patients. Alternatively it may be explained simply because the QpI was not high enough to cause volume overload to the heart.

Second, as the development of aortopulmonary collaterals is in compensation for the poor development of pulmonary arteries, it was also hypothesized that there may be an inverse correlation between PAAI and %CR. This hypothesis was also revealed to be negative (see Fig 5Go).

A pulmonary arterial pressure (PAP) of more than 25 mm Hg is thought to be an expression of excessive pulmonary blood flow [12] and can be a good candidate for the index of high %CR. In the present study, as more than half of the patients underwent palliative operation before Fontan operation and more than half of our patients had complex cardiac anomalies, it was often impossible to obtain accurate PAP data before Fontan operation. Therefore, we did not show the analysis of the preoperative PAP data.

We could not find an independent index that showed good correlation with %CR. However, we found that patients with a small PAAI and a high arterial blood oxygen saturation had a high %CR. This phenomenon may be explained partly by the fact that the development of aortopulmonary collaterals is one of the compensation processes for low arterial oxygen content due to low pulmonary flow.

The age of the patients at the time of Fontan operation and %CR showed good correlation, suggesting that the physiologic compensation for hypoxia progresses with age.

We have shown that it is possible to predict a high %CR before Fontan operation. However, it is necessary to recognize that in those patients who have undergone palliative shunts previously, the accuracy of the hemodynamic and morphologic indices is questionable.

We have demonstrated that preoperative embolization of visible MAPCAs may reduce %CR, and hence the risk of Fontan operations. It must, however, be borne in mind that preoperative embolization is an invasive procedure with potential risks and complications. Therefore, further studies are required to establish if a high %CR is an independent risk factor for Fontan operation and more important, if any intervention (including preoperative embolization of MAPCAs) can reduce %CR to improve the results of Fontan operations.


   Acknowledgments
Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
References
 
We express our gratitude to Dr Clyde B. R. Saldanha at St Thomas' Hospital, London, for useful discussion and correction of English.


   Footnotes
Top
 Footnotes
Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
Address reprint requests to Dr Ichikawa, First Department of Surgery, Osaka University Hospital, 2–2 Yamadaoka Suita, Osaka 565, Japan.


   References
Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 

  1. Fontan F, Baudet E. Surgical repair of tricuspid atresia. Thorax 1971;26:240–8.[Abstract/Free Full Text]
  2. Fontan F, Kirklin JW, Fernandez G, et al. Outcome after a ``perfect'' Fontan operation. Circulation 1990;81:1520–36.[Abstract/Free Full Text]
  3. Gale AW, Danielson GK, McGoon DC, Mair DD. Modified Fontan operation for univentricular heart and complicated congenital lesions. J Thorac Cardiovasc Surg 1979;78:831–8.[Medline]
  4. Matsuda H, Kawashima Y, Kishimoto H, et al. Problems in the modified Fontan operation for univentricular heart of the right ventricular type. Circulation 1987;76(Suppl 3):45–52.
  5. Hernandez F, Castellanos AW. The pulmonary artery segment in normal and in valvular pulmonary stenosis. Angiology 1981;32:311–20.
  6. Humes RA, Feldt RH, Porter CJ, Julsrud PR, Puga FJ, Danielson GK. The modified Fontan operation for asplenia and polysplenia syndromes. J Thorac Cardiovasc Surg 1988;96:212–8.[Abstract]
  7. Capsi J, Coles JG, Tabinovich M, et al. Morphological findings contributing to a failed Fontan procedure: twelve-year experience. Circulation 1990;82(Suppl 4):177–82.
  8. Mair DD, Hagler DJ, Puga FJ, Schaff HV, Danielson GK. Fontan operation in 176 patients with tricuspid atresia: results and a proposed new index for patient selection. Circulation 1990;82(Suppl 4):164–9.[Abstract/Free Full Text]
  9. Kirklin JK, Blackstone EH, Kirklin JW, Pacifico AD, Bargeron LM. The Fontan operation: ventricular hypertrophy, age, and date of operation as risk factors. J Thorac Cardiovasc Surg 1986;92:1049–64.[Abstract]
  10. Sawatari K, Imai Y, Kurosawa H, et al. New selection criterion for Fontan procedure: pulmonary artery clamping test pulmonary vascular resistance in increased pulmonary blood flow. Nippon Kyoubu Geka Gakkai Zasshi 1989;37:208–17.
  11. Matsuda H, Covino E, Hirose H, et al. Acute liver dysfunction after modified Fontan operation for complex cardiac lesions: analysis of the contributing factors and its relation to the early prognosis. J Thorac Cardiovasc Surg 1988;96: 219–26.[Abstract]
  12. Laks H, Breda MA. Tricuspid atresia. In: Baue AE, Geha AS, Hammond GL, Laks H, Naunheim KS, eds. Glenn's thoracic and cardiovascular surgery. Englewood Cliffs, NJ: Prentice-Hall, 1991:1259–72.



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