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Ann Thorac Surg 2009;87:826-831. doi:10.1016/j.athoracsur.2008.10.075
© 2009 The Society of Thoracic Surgeons
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Original Articles: Pediatric Cardiac

Absence of Pulmonary Artery Growth After Fontan Operation and Its Possible Impact on Late Outcome

Stanislav Ovroutski, MDa,*, Peter Ewert, MD, PhDa, Vladimir Alexi-Meskishvili, MD, PhDb, Katinka Hölschera, Oliver Miera, MDa, Björn Peters, MDa, Roland Hetzer, MD, PhDb, Felix Berger, MD, PhDa

a Department of Congenital Heart Diseases, German Heart Institute Berlin, Berlin, Germany
b Department of Cardiothoracic and Vascular Surgery, German Heart Institute Berlin, Berlin, Germany

Accepted for publication October 27, 2008.

* Address correspondence to Dr Ovroutski, Deutsches Herzzentrum Berlin, Augustenburger Platz 1, Berlin, 13533, Germany (Email: ovroutski{at}dhzb.de).


Pediatric cardiac surgery: The Annals of Thoracic Surgery CME Program is located online at http://cme.ctsnetjournals.org. To take the CME activity related to this article, you must have either an STS member or an individual non-member subscription to the journal.

 

   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 
Background: The purpose of this study was to evaluate the development of the pulmonary arteries (PAs) after Fontan operation in children at long term.

Methods: Thirty-five patients in whom Fontan operation was performed at median age of 4.2 years (range, 1.5 to 16.1 years) underwent angiographic measurements of the central and lower lobe PA diameter before Fontan operation and during the median follow-up of 4.6 years (range, 1.4 to 15.1 years). The median patient age at follow-up was 8.6 years (range, 3.4 to 27.2 years). Body surface area–dependent PA index and lower lobe index were calculated, and preoperative and follow-up values were compared. A correlation between the PA indices and the duration of the follow-up as well as between PA indices and the outcome was investigated.

Results: Although percentile parallel somatic development of the children could be documented by body surface area measurements (0.62 to 0.93 m2 during the follow-up; p < 0.001), the PA showed no gain in diameter at all. The PA index and lower lobe index (preoperative median, 261 and 138 mm2/m2, respectively) decreased significantly during the follow-up period (median, 177 and 109 mm2/m2;p < 0.001). The lowest PA index was noted in patients who had the longest follow-up (R = 0.5; p = 0.009). We found a correlation between a low PA index and an unfavorable Fontan outcome (n = 10, p = 0.002).

Conclusions: Growth of PAs after Fontan operation is clearly reduced despite somatic growth. This phenomenon may lead to an increase in pulmonary vascular resistance and could be a limit for optimal Fontan circulation in grown children in the long term.

Low pulmonary vascular resistance is one of the most important variables for optimal long-term Fontan outcome. Absence of pulmonary artery (PA) distortions and low pulmonary vascular resistance were originally noted to be important selection criteria for the operation [1, 2]. The criteria have been modified during the past three decades, and other factors, such as the Nakata index for the central pulmonary artery (PAI) and the lower lobe index (LLI) for the peripheral vessels, were introduced to optimize preoperative patient selection [3–7].

In the past different authors discussed small PAI as a risk factor for the postoperative outcome [5,6]. With attempts to make selection criteria more precise, the LLI was proposed to be more predictive of the development of the PA tree, given that the central stenotic part could be enlarged before or during Fontan completion [3, 7, 8].

Young age (2 to 4 years) is no longer considered a risk factor, but is regarded as the optimal age for circuit separation. Furthermore, to optimize the long-term prognosis of the single-ventricle function, volume offload and cyanosis removal should be performed in early childhood [1, 3, 9–11]. It is postulated, however, that the absence of pulsatile flow in the PAs after circuit separation restricts their development [12–14]. To test this hypothesis, we measured the PA diameters in children during the follow-up after Fontan operation and compared these values with the preoperative measurements. To identify a possible impact of inadequate PA growth on the Fontan outcome, we looked for a correlation between low PAI and signs of unfavorable postoperative Fontan circulation such as recurrent ascites, pleural effusions, or protein-losing enteropathy syndrome.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 Acknowledgments
 References
 
The study was approved by the institutional review board.

In all postoperatively catheterized consecutive patients operated on in our institution between 1992 and 2005 (n = 73 of the total of 124), the diameter of the central and lower lobe PA was measured preoperatively and postoperatively using contrast angiography in the systolic phase according to the original method published by Nakata and colleagues [6] and Reddy and associates [7] and our previously published data [15, 16], as shown in Figure 1. The general indications for postoperative catheterization have been described elsewhere [17]. Patients who underwent the final catheterization earlier than 1 year postoperatively (n = 26) were excluded to avoid misleading PA growth data based on the short follow-up period only. Further, those who were adult (>18 years of age, n = 12) at Fontan operation were also excluded from the study. Therefore, 35 patients who fulfilled the selection criteria were analyzed and are presented in the current study. Patients included in the study received either a lateral tunnel (n = 11) or an extracardiac conduit (n = 24) for completion of the Fontan circulation. The diameter of the extracardiac conduits was selected according to the diameter of the inferior caval vein and ranged between 16 and 24 mm (median, 20 mm), as reported elsewhere [15]. The median age at Fontan operation was 4.2 years (range, 1.5 to 15.9 years). The median follow-up was 4.6 years (range, 1.4 to 15.1 years). Median patient age at the end of the follow-up was 8.6 years (range, 3.4 to 27.2 years).


Figure 1
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  		Fig 1. (A) Angiogram of the cavopulmonary anastomosis and pulmonary arteries before Fontan operation. The vessel diameter and the body surface area (BSA) are shown. Stenosis of the central part of left pulmonary artery (LPA) is visible. The peripheral pulmonary vessels are well developed. The pulmonary artery index (Nakata index; [{pi} x (RPA2 + LPA2)/4]/BSA mm2/m2) is 158 mm2m2; the total lower lobe index ([{pi} x (RLLA2 + LLLA2)/4]/BSA mm2/m2) is 145 mm2/m2. (B) The same patient 9 years after Fontan operation with additional enlargement of the central left pulmonary artery. Heart catheterization was performed because of the first episode of protein-losing enteropathy. No local stenosis of the pulmonary arteries with very low pulmonary indices (pulmonary artery [Nakata] index = 81 mm2/m2; total lower lobe index = 89 mm2/m2) were found. (LLLA = left lower lobe artery; RLLA = right lower lobe artery; RPA = right pulmonary artery.)

 
The preoperative measurements were performed immediately during pre-Fontan catheterization, between 2 days and 12 months (median, 3 months) before surgery.

In 6 patients with preoperative localized stenoses of the central PAs, these were enlarged during Fontan operation. In 7 patients, the PA stenoses were treated by balloon dilation or stent implantation after Fontan completion. We compared preoperative and postoperative native vessel diameters as well as the body surface area (BSA)-dependent variables PAI and LLI.

Ten patients (8% of the total of 124) experienced chronic or recurrent ascites or pleural effusions and were assigned to a subgroup with unfavorable Fontan outcome. Eight of them had clinical signs of protein-losing enteropathy, and 4 of them (3%) died 1.3, 3.2, 3.5, and 4.7 years postoperatively.

SPSS for Windows, version 12.0 (SPPS Inc, Chicago, IL), was used to perform statistical calculations. Data are expressed as median and ranges. Paired two-tailed Student's t test analysis was used to assess the significance of within-patient changes in vessel diameter, somatic development, and PA indices between pre-Fontan and post-Fontan catheterization. Linear regression analysis was used to detect significant correlations between follow-up duration and PAI. The Mann-Whitney U test was performed to detect a correlation between low PA indices and unfavorable Fontan outcome. All probability values of less than or equal to 0.05 were considered significant.


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 Acknowledgments
 References
 
Somatic Development
Percentile parallel somatic development was noted after Fontan operation (Fig 2): The median gain in body weight and length was 9.9 kg (maximum, 46.3 kg) and 23.5 cm (maximum, 93 cm), respectively, leading to an increase in BSA from 0.62 m2 (range, 0.42 to 1.52 m2) preoperatively to 1.0 m2 (range, 0.6 to 1.8 m2) at the end of the follow-up period (Table 1).


Figure 2
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  		Fig 2. Changes in Nakata index (pulmonary artery index [PAI]) and lower lobe index (LLI) of the pulmonary arteries during follow-up. Box-plot diagram demonstrates a significant decrease in the pulmonary artery index as well as the lower lobe index according to the stable somatic development of the children and nondevelopment of the pulmonary arteries.

 

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  		Table 1 Pre-Fontan and Post-Fontan Pulmonary Artery Sizes and Indices and Body Surface Area a
 
Pulmonary Artery Development
The PA diameters did not show any increase during follow-up, either for the central PAs or for the lower lobes (Table 1; Fig 1). Consequently, the BSA-dependent PAI and LLI (preoperative median, 261 and 138 mm2/m2, respectively) decreased significantly from the preoperative examination to the end of the follow-up (median, 177 and 109 mm2/m2, respectively; p < 0.001; Fig 2). In 7 patients even a diameter reduction was observed. The lowest PAI was noted in patients with the longest follow-up (Fig 3; r = 0.5; p = 0.009), whereas the age of the patients at the postoperative catheterization showed no correlation with PAI. A statistically significant correlation was found between a low PAI (<150 mm2/m2) at the end of the follow-up and the incidence of an unfavorable Fontan outcome (Fig 4; n = 10; p = 0.002). Also, in patients who died (n = 4) there was a correlation with low PAI (p = 0.011), especially accompanied by elevated PA pressure (PAP; p = 0.001). There were no differences in the PAI (median, 195 versus 181 mm2/m2; p = 0.87) and LLI (median, 118 versus 105 mm2/m2; p = 0.67) between patients after extracardiac conduit or lateral tunnel Fontan operation, respectively.


Figure 3
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  		Fig 3. Scatter-diagram shows significant decrease in the pulmonary artery index (PAI; Nakata index) of the central pulmonary arteries according to the duration of the follow-up. The lowest pulmonary artery index is to be noted in the patients with longest follow-up.

 

Figure 4
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  		Fig 4. Correlation between low pulmonary artery index (PAI) and Fontan outcome. Block diagram shows significant differences in the long-term postoperative outcome between patients with low pulmonary artery index (<150 mm2/m2) and those with pulmonary artery index greater than 150 mm2/m2. In patients with pulmonary artery index less than 150 mm2/m2 at the end of the follow-up, unfavorable outcome was observed more frequently than in those with pulmonary artery index greater than 150 mm2/m2.

 
Pulmonary Artery Pressure Development
We observed no changes in the PAP preoperatively and postoperatively. Before the Fontan operation the median PAP was 10 mm Hg (range, 6 to 19 mm Hg), and it remained stable during the follow-up (median 11 mm Hg [range, 4 to 24 mm Hg]). However, the rate of patients with elevated PAP (>15 mm Hg) and decreased PAI (<150 mm2/m2) in the total group late after surgery was clearly increased in comparison to preoperatively (Fig 5).


Figure 5
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  		Fig 5. Changes in the pulmonary artery pressure (PAP) during the follow up. Black triangles indicate patients with low pulmonary artery index (PAI < 150 mm2/m2). (OP = operation.)

 

   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
Acknowledgments
 References
 
In our present study, the growth and development of the PAs after Fontan operation were clearly reduced, and even totally stopped in some cases. Neither the central PA nor the lower lobe PA showed an increase in diameter. It has to be emphasized that all patients were strictly selected according to our preoperative selection criteria or optimally "prepared" for the Fontan circulation by preoperative interventions or surgical removal of central vessel stenoses. Therefore, all patients started with normal PA size and indices [3, 7, 8, 18]. Postoperatively, if assessed on echocardiography or clinically, stenoses were treated by catheter interventions and checked during the follow-up, as reported elsewhere [17].

Therefore, despite the absence of PA stenoses postoperatively, we observed no long-term changes in vessel diameters. This was emphasized by those cases with unilateral PA stenosis: the contralateral, nonstenotic segment also showed no gain in vessel diameter despite a theoretically enhanced unilateral flow. Further, no differences in PA growth between extracardiac conduit and lateral tunnel Fontan were noted. Although the flow within the extracardiac conduit was described previously as showing more energy dissipation and absence of pulsatility, the differences between the overall venous flow in different Fontan modifications seem to be not sufficient to influence the PA growth [19]. These phenomena lead us to assume that the pulsatility, but not the flow volume, is responsible for the PA growth.

Choussat and colleagues [1], writing in 1977, described "well developed pulmonary arteries without distortions" as one of the most important prerequisites for well functioning Fontan circulation. In an attempt to apply this statement more precisely, Nakata and associates [6] introduced the PAI in 1984 and set the limit for high risk Fontan candidates at 250 mm2/m2. Knott-Craig and coworkers [5] reduced it to 170 mm2/m2 in 1993. After further investigation of the pre-Fontan selection criteria Reddy and colleagues [7] recommended in 1996 that the lower lobe branches be measured for better prediction of the PA tree development. Consequently, more patients with small central parts of the PAs were accepted for Fontan operation, and the risk level of the PAI was lowered, assuming that stenotic central parts could be enlarged before or during Fontan completion with good early postoperative outcome [3, 5, 7, 8]. Thus, the LLI may be a better variable for preoperative patient selection than the central PAI. Nevertheless, we would argue that the central PAI should be used as a variable with good sensitivity for the postoperative follow-up of the vessels' development, if preoperative stenoses are removed, which was rigorously done in each affected patient in this study.

Adachi and colleagues [8] found no influence on the postoperative outcome of small PAs, but noted a reduction of the related indices during the follow-up of 2.8 ± 2.7 years. We followed our patients for a longer time (mean 5.1 ± 3.7 years), and even then we could not document any increase in the PA diameter despite favorable somatic development of the children. Although the development of the PA is not linear regarding somatic body growth, different authors have demonstrated the usefulness of the indexed PA diameter in all age groups [6, 20]. If we compare our vessel diameter measurements with normal values, presented in different studies and summarized by Kirklin and Barratt-Boyes [21], then we observed significantly lower diameters in all patient groups, especially late postoperatively. The PA diameter late after Fontan operation is significantly lower than in normal individuals, both isolated in the right and left PA as the sum value, and equally if compared in cross-sectional area per BSA or in diameter per BSA [6, 20, 21].

Sievers and coworkers [20] showed a nonlinear, but statistically highly significant, positive correlation between PA diameter and BSA in infants, children, and adolescents. They described an increase in stroke volume according to the somatic growth in children with normal cardiac anatomy and found a highly significant correlation of the increase of stroke volume with an increase in cross section of the right PA [20]. Thus, our findings may be supportive of the theory that stroke volume generates pulsatility and therefore in our Fontan patients the absence of pulsatility is responsible for the stagnation in vessel growth. Obviously, if early circuit separation with removal of cyanosis and unloading of the single ventricle supports normal somatic growth of the children, the development of the PA is significantly reduced [16, 22, 23].

Interestingly, Reddy and associates [7] wrote that PA indices, including the LLI, do not change significantly after bidirectional cavopulmonary shunt during medium-term follow-up and thus do not influence the Fontan outcome. Nevertheless, the authors noted in their publication a slight decrease in the overall mean total PAI and total LLI during relatively short follow-up of median 18 months before Fontan operation. Because Fontan operation is usually performed approximately 9 to 12 months after bidirectional cavopulmonary shunt, little gain in vessel size could be expected during this period, whereas absence of PA diameter increase late after Fontan operation, when somatic development increases in adolescence, may lead to significant mismatch.

According to our observations, the post-Fontan PA growth seems to be discouraging. Together with other factors that are under debate, such as endothelin receptor activation in the slow venous flow system or recurrent microthromboembolism of the PAs [12, 24], the absence of PA growth may contribute to an increase in vascular resistance. This is in accordance with the correlation between low value of the central PA indices and unfavorable Fontan outcome in our patients.

The PAP remains stable in the total group without increase during the follow-up. These findings support our strategy for patient selection and the good long-term results in our total series. Indirectly, stable and low PAP also speaks for good ventricular function late after Fontan. Nevertheless, we observed that more patients with small PAs and low PAI are inclined to experience elevated PAP late after surgery. Furthermore, both these factors together correlated significantly with unfavorable Fontan outcome and late mortality. Also, although the early mortality risk is decreased in the modern era, the long-term results are highly dependent on the pulmonary resistance, which is in turn dependent on the PA development. From our point of view, only strict preoperative selection of patients with low PAP and well-developed PA provides optimal Fontan circulation in the long term.

There are at present no approved strategies to maintain the "biventricular circuit energetics" in the univentricular flow system. It has been claimed that an additional aortopulmonary shunt could be beneficial for PA growth in patients with bidirectional cavopulmonary shunt [7, 25]. Whether similar strategies such as an aortopulmonary shunt or an arteriovenous fistula could be beneficial for Fontan patients needs further clinical investigation.

The problem of the failing Fontan circulation remains multifactorial, and deterioration of the ventricular function or elevated PAP contributes significantly to its limitations. Thus, although the Fontan operation remains a temporally limited palliation, it should be performed in early childhood to remove cyanosis and volume overload and to improve quality of life. From our point of view, however, if the total circuit separation is performed in early childhood, especially in children with small PA, nongrowth of the pulmonary vessels should definitely be added to the factors that limit optimal long-term Fontan circulation.


   Acknowledgments
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
References
 
We are grateful to Anne M. Gale for editorial assistance.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 

  1. Choussat A, Fontan F, Besse P, Vallot F, Chauve A, Bricaud H. Selection criteria for Fontan's procedureIn: Anderson RH, Shinebourne EA, editors. Paediatric cardiology. Edinburgh: Churchill Livingstone; 1977. pp. 559-566.
  2. Fontan F, Baudet E. Surgical repair of tricuspid atresia Thorax 1971;26:240-248.[Abstract/Free Full Text]
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  4. Bridges ND, Farrell Jr PE, Pigott JDd, Norwood WI, Chin AJ. Pulmonary artery index: a nonpredictor of operative survival in patients undergoing modified Fontan repair Circulation 1989;80(Suppl I):216-221.
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  6. Nakata S, Imai Y, Takanashi Y, et al. A new method for the quantitative standardization of cross-sectional areas of the pulmonary arteries in congenital heart diseases with decreased pulmonary blood flow J Thorac Cardiovasc Surg 1984;88:610-619.[Abstract]
  7. Reddy VM, McElhinney DB, Moore P, Petrossian E, Hanley FL. Pulmonary artery growth after bidirectional cavopulmonary shunt: is there a cause for concern? J Thorac Cardiovasc Surg 1996;112:1180-1190.[Abstract/Free Full Text]
  8. Adachi I, Yagihara T, Kagisaki K, et al. Preoperative small pulmonary artery did not affect the midterm results of Fontan operation Eur J Cardiothorac Surg 2007;32:156-162.[Abstract/Free Full Text]
  9. Mahle WT, Wernovsky G, Bridges ND, Linton AB, Paridon SM. Impact of early ventricular unloading on exercise performance in preadolescents with single ventricle Fontan physiology J Am Coll Cardiol 1999;34:1637-1643.[Abstract/Free Full Text]
  10. Petrossian E, Reddy VM, McElhinney DB, et al. Early results of the extracardiac conduit Fontan operation J Thorac Cardiovasc Surg 1999;117:688-696.[Abstract/Free Full Text]
  11. Weber HS, Gleason MM, Myers JL, Waldhausen JA, Cyran SE, Baylen BG. The Fontan operation in infants less than 2 years of age J Am Coll Cardiol 1992;19:828-833.[Abstract]
  12. Khambadkone S, Li J, de Leval MR, Cullen S, Deanfield JE, Redington AN. Basal pulmonary vascular resistance and nitric oxide responsiveness late after Fontan-type operation Circulation 2003;107:3204-3208.[Abstract/Free Full Text]
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