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J Thorac Cardiovasc Surg 1994;107:1284-1290
© 1994 Mosby, Inc.

SURGERY FOR CONGENITAL HEART DISEASE

Central pulmonary artery growth patterns after the bidirectional Glenn procedure

Ann Arbor, Mich.

Dr. Mendelsohn is supported in part by NRSA HL08709-01, National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, Md.

Presented in part at the Forty-second Scientific Sessions, American College of Cardiology, Anaheim, Calif., March 15-18, 1993.

Received for publication May 13, 1993. Accepted for publication Sept. 14, 1993. Address for reprints: Robert H. Beekman III, MD, FACC, Division of Pediatric Cardiology, University of Michigan Medical Center, MCHC F1310, Box 0204, 1500 E. Medical Center Dr., Ann Arbor, MI 48109-0204.

Abstract

The changes in pulmonary artery size and hemodynamics in 30 patients with univentricular cardiac anatomy were examined before and after bidirectional Glenn procedures done between October 1989 and February 1992. Serial angiographic and hemodynamic examinations before and 17.6 ± 1.6 months after bidirectional Glenn procedures were compared. At the follow-up study there was no significant change in diameter of the pulmonary artery ipsilateral to the bidirectional Glenn shunt; however, a significant decrease was noted in the diameter of the pulmonary artery contralateral to the bidirectional Glenn shunt (p = 0.04). There was also a 32% decrease in the Nakata index of total cross-sectional pulmonary artery area after the bidirectional Glenn procedure (p = 0.004). Total pulmonary blood flow and mean pulmonary artery pressure had decreased, and arterial oxygen saturation had increased at follow-up. These changes, however, did not correlate with the observed changes in pulmonary artery size. By linear regression analysis, a significant relationship was identified between the Nakata index before the bidirectional Glenn procedure and the absolute change in Nakata index (r = 0.83). A significant decrease in Nakata index occurred only in patients with a bidirectional Glenn shunt in place more than 15 months. Sixteen of the 30 patients subsequently underwent total cavopulmonary anastomosis with 7 requiring concurrent surgical pulmonary artery reconstruction. Changes in pulmonary artery size observed more than 15 months after the bidirectional Glenn procedure may have implications for subsequent Fontan repair in children with univentricular anatomy. (J THORACCARDIOVASCSURG1994;107:1284-90)

Anastomosis of the superior vena cava to the right pulmonary artery as therapy for cyanotic heart disease was first performed clinically by Glenn ¹ and by Bakulev and Kolesnikov, ² and the utility of this procedure has been extensively examined. ^3-6 Modifications by Haller and associates ⁷ were made to include a bidirectional superior vena cava–to–pulmonary artery anastomosis without pulmonary artery division. The bidirectional procedure has anatomic and physiologic advantages over the standard unidirectional Glenn shunt. ^8,9 Previous studies, however, have described preferential flow to the right pulmonary artery in patients with a right-sided bidirectional Glenn procedure. ⁸ These data raise the possibility that growth of the pulmonary artery ipsilateral and contralateral to a bidirectional Glenn shunt may be unequal. To test this hypothesis, we evaluated pulmonary artery growth by serial cineangiography in children undergoing a bidirectional Glenn procedure. We sought to determine long-term changes in central pulmonary artery size and to identify potential predictive factors for changes in pulmonary artery anatomy after the bidirectional Glenn procedure.

PATIENTS AND METHODS

Patients with univentricular cardiac anatomy who underwent a bidirectional Glenn procedure between October 1989 and February 1992 at C. S. Mott Children's Hospital, the University of Michigan, were eligible for inclusion in this study. All patients underwent complete hemodynamic and angiographic studies before the bidirectional Glenn procedure and had previous aortopulmonary shunts as the major source of pulmonary artery flow. The bidirectional Glenn anastomosis, with ligation of an aortopulmonary shunt and/or the main pulmonary artery if patent, was done by one of two surgeons (E.L.B., F.M.L.). Bilateral bidirectional Glenn connections were done in patients with dual superior vena caval drainage. Pulmonary artery reconstruction was also done at the time of the bidirectional Glenn procedure for patients with significant branch pulmonary artery stenosis. All patients subsequently underwent follow-up hemodynamic and angiographic studies before planned total cavopulmonary (Fontan) anastomosis.

Both sets of catheterization and angiographic data (before and after bidirectional Glenn procedure) were compared, with particular attention paid to pulmonary artery anatomy and hemodynamics. Measurements of the right and left pulmonary artery diameters were made immediately proximal to the first branch point of each pulmonary artery. The largest diameters in either the anteroposterior or lateral projections of the study before the bidirectional Glenn procedure were recorded and the same projection used for pulmonary artery measurements at the follow-up study after the bidirectional Glenn procedure. Images were corrected for magnification by use of filmed 1 cm grids in both projections. The pulmonary arteries were characterized by their relationship to the side of the bidirectional Glenn anastomosis; that is, ipsilateral or contralateral to the bidirectional Glenn anastomosis. In patients who underwent bilateral bidirectional Glenn procedures, the right and left pulmonary arteries were both considered ipsilateral to the bidirectional Glenn shunt. Pulmonary artery cross-sectional areas were calculated by the method of Nakata and associates. ¹⁰ The absolute and percentage changes inNakata indices were calculated, and the Z scores for each Nakata index value were determined by the method described by Kirklin and Barratt-Boyes ¹¹: Z = 1n (Nakata index/290)/0.1856. Hemodynamic data obtained at cardiac catheterization before and after the bidirectional Glenn procedure were also compared and included ventricular end-diastolic pressure, total and effective pulmonary flow calculated from measured oxygen consumption, mean pulmonary artery pressure measured either within the pulmonary artery or by pulmonary venous wedge pressures, and systemic arterial oxygen saturation.

Statistical analysis
Data were evaluated by a computer statistical package (Statview II, Abacus Concepts, Inc., Berkeley, Calif.) and are presented as mean plus or minus one standard error of the mean. Group data were compared by group Student's t tests, and comparisons within groups used repeated-measures analysis of variance. Linear regression analysis techniques were used to evaluate correlation between multiple factors. Statistical significance was defined as a p value less than or equal to 0.05.

RESULTS

Between October 1989 and February 1992, 50 patients with univentricular cardiac anatomy underwent a bidirectional Glenn procedure. Five patients (10%) died before follow-up cardiac catheterization (three in-hospital and two within 6 months after the bidirectional Glenn procedure). Ten patients are followed up at other institutions and five patients have not yet undergone a repeat cardiac catheterization. The remaining 30 patients (15 male, 15 female) constitute our study population. The diagnoses included hypoplastic left heart syndrome (n = 13), pulmonary atresia/intact ventricular septum (n = 5), univentricular heart of the right ventricular type (n = 4), tricuspid atresia (n = 4), double-inlet left ventricle (n = 3), and Ebstein's anomaly (n = 1). These patients underwent a bidirectional Glenn procedure at 19.0 ± 3.4 months of age (range 2 to 94 months). The bidirectional Glenn procedure was done with the right superior vena cava in 23 patients, the left superior vena cava in 2 patients, and bilateral superior venae cavae in 5 patients. At the time of the bidirectional Glenn procedure, two patients underwent patch angioplasty of the pulmonary artery contralateral to the bidirectional Glenn anastomosis for discrete stenosis. Follow-up cardiac catheterization and angiography was performed 17.6 ± 1.6 months (range 1 to 39 months; mode = 15 months) after the bidirectional Glenn procedure. The patients had grown from 0.38 ± 0.02 m² to 0.52 ± 0.02 m² (p = 0.0001) at the time of the follow-up study.

Angiographic data
Comparison of the central pulmonary artery diameters before and after the bidirectional Glenn procedure in all 30 patients (including those with bilateral bidirectional Glenn shunts) revealed no significant change in the ipsilateral pulmonary artery diameter (7.8 ± 0.4 mm versus 8.2 ± 0.5 mm, p = not significant [NS]). However, the diameter of the pulmonary artery contralateral to the bidirectional Glenn shunt decreased significantly (7.4 ± 0.5 mm versus 6.4 ± 0.4 mm; p = 0.04; Figs. 1 and 2). This represented a 13.5% decrease in the contralateral pulmonary artery diameter. There was also a significant decrease in the Nakata index after the bidirectional Glenn procedure from 272.4 ± 28 mm²/m² to183.9 ± 15.9 mm ²/m ², a 32% decrease in the indexed cross-sectional pulmonary arterial area (p = 0.004; Fig. 3). Mean Z scores for the Nakata index decreased from –1.07 ± 0.52 (range –6.61 to 5.65) to –2.96 ± 0.47 (range –7.36 to 1.4) after the bidirectional Glenn procedure.

View larger version (19K): [in this window] [in a new window]   Fig. 1. Pulmonary artery diameters ipsilateral (left panel) and contralateral (right panel) to bidirectional Glenn shunt.There is significant decrease (p = 0.04) incontralateral pulmonary artery diameter after bidirectional Glenn procedure (POST).PRE Before bidirectional Glenn procedure.

View larger version (95K): [in this window] [in a new window]   Fig. 2. Pulmonary artery cineangiograms of patient with hypoplastic left heart syndrome before (left panel) and after (right panel) bidirectional Glenn procedure. Corrected for magnification, right pulmonary artery (ipsilateral to bidirectional Glenn shunt) increased from 6.9 to 7.8 mm. Left pulmonary artery (contralateral to bidirectional Glenn shunt) decreased from 3.8 mm to 3.3 mm. Total Nakata index decreased from 184 mm2/m2 to 122 mm 2/m 2.

View larger version (19K): [in this window] [in a new window]   Fig. 3. Nakata index measurements before (PRE) and after (POST) bidirectional Glenn procedure. This index of pulmonary artery cross-sectional area decreased by 32% after bidirectional Glenn shunt.

Hemodynamic data
Hemodynamic data obtained before and 17.6 months after the bidirectional Glenn procedure are summarized in Table 1. Total pulmonary blood flow decreased from 4.6 ± 0.4 to 2.0 ± 0.1 L/min per square meter (p = 0.001) after the bidirectional Glenn procedure. There was no significant change, however, in the effective pulmonary blood flow. Mean pulmonary artery pressure and ventricular end-diastolic pressure decreased significantly, whereas systemic arterial oxygen saturations increased slightly from 78% to 82% (all p < 0.05). There was no change in pulmonary vascular resistance after the bidirectional Glenn procedure. None of these hemodynamic changes correlated significantly (by linear regression analysis) with the changes identified in pulmonary artery diameter or Nakata index. There was also no significant relationship between the changes in pulmonary artery size and age at bidirectional Glenn procedure, change in body surface area, diagnosis, or dominant ventricular morphologic condition (right versus left ventricle). However, a significant relationship was identified between the Nakata index before the bidirectional Glenn procedure and the absolute change in Nakata index after the bidirectional Glenn procedure (Fig. 4). The greatest decrease in total Nakata index over the time interval between the bidirectional Glenn procedure and follow-up evaluation occurred in patients with the largest Nakata index before the bidirectional Glenn procedure (r = 0.83).

View larger version (28K): [in this window] [in a new window]   Fig. 4. Linear regression analysis of Nakata index before bidirectional Glenn procedure (PRE) and absolute decrease in Nakata index. Patients with larger Nakata index before bidirectional Glenn procedure appear to have largest decreases in Nakata index after bidirectional Glenn procedure.

View larger version (28K): [in this window] [in a new window]   Fig. 5. Nakata indices in groups A and B before (PRE) and after (POST) bidirectional Glenn procedure. Although there is no significant difference between Nakata indices before bidirectional Glenn procedure between groups, there is significant difference between Nakata index in groups A and B after bidirectional Glenn shunt (p = 0.05).

View larger version (104K): [in this window] [in a new window]   Fig. 6. Pulmonary artery angiograms of patient with hypoplastic left heart syndrome before (left panel) and after (right panel) modified Fontan procedure in whom a balloon-expandable stent was implanted at time of Fontan procedure. Corrected for magnification, left pulmonary artery diameter before stenting was 3.7 mm at first branch point and 11.0 mm after stent implantation.

DISCUSSION

The Glenn shunt and its bidirectional modification have proved efficacious as a staging procedure before completion of the total cavopulmonary anastomosis in patients with a univentricular heart. ^4-6,8 Our study, which documents beneficial hemodynamic changes after the bidirectional Glenn procedure (Table I), is consistent with previous studies. We found a significant decrease in mean pulmonary artery pressure and ventricular end-diastolic pressure and a significant increase in systemic arterial saturation after the bidirectional Glenn procedure. This study, however, is the first to describe changes in central pulmonary artery size after the bidirectional Glenn procedure. We identified a 32% decrease in indexed cross-sectional pulmonary artery area (from 272.4 mm²/m² to 183.9 mm²/m²) at a mean interval of 17.6 months after the bidirectional Glenn procedure. There was a 13.5% decrease in pulmonary artery diameter contralateral to the bidirectional Glenn shunt, without a significant change in the ipsilateral pulmonary artery diameter.

The decrease in size of the central pulmonary artery contralateral to the bidirectional Glenn shunt is most likely caused by diminished blood flow to that lung. We did not do lung perfusion scans systematically in these patients, but previous studies have documented preferential flow to the right pulmonary artery in cases of right-sided bidirectional Glenn shunts. ⁸ Whether the smaller appearance of the contralateral pulmonary artery is due to true changes in vessel morphologic status or is simply a manifestation of diminished vessel distention is difficult to know with certainty. The data suggest, however, that the findings of this study reflect real changes in the growth of the contralateral pulmonary artery after the bidirectional Glenn shunt. First, significant changes were observed only after the bidirectional Glenn shunt had been in place for more than 15 months. If the angiographic findings were due solely to poor vessel distention, then similar changes in measured pulmonary artery size would be expected in all patients regardless of the follow-up duration. Second, the angiographic assessment of pulmonary artery size appears to have had important clinical implications. Seven patients required surgical intervention for pulmonary artery hypoplasia or stenosis (findings confirmed by intraoperative observations), and the only two deaths in this series occurred in patients with an angiographically derived Nakata index less than 125 mm²/m². Finally, we were unable to find a significant correlation between the changes in pulmonary artery size and changes in pulmonary artery pressure or total pulmonary blood flow after the bidirectional Glenn procedure. Thus our data are best explained by real morphologic changes in the contralateral pulmonary artery, which are probably the consequence of preferential blood flow to the ipsilateral vessel after the bidirectional Glenn procedure. This concept is consistent with our finding of decreased left pulmonary artery diameter after a right-sided but not a left-sided bidirectional Glenn procedure and no decrease in the diameter of either pulmonary artery in five patients with a bilateral bidirectional Glenn shunt.

Because pulmonary artery size is widely regarded as a risk factor for poor outcome after the Fontan operation, ^13,14 our findings raise concerns related to the use of the bidirectional Glenn procedure as a pre-Fontan staging operation. The only early postoperative deaths after the Fontan operation in our series occurred in two of six patients with a Nakata index less than 125 mm²/m². In their original work, Nakata and associates ¹⁰ noted 100% mortality in patients undergoing the Fontan procedure with preoperative Nakata indices 250 mm²/m² or less. Fontan and associates ¹³ reported a multicenter study of 334 patients who underwent classic Fontan procedures, in whom multifactorial risk analysis for success or failure (death, need for takedown of Fontan) of the operation was described. The authors found only a 25% (2 of 8) success rate in patients with a McGoon ratio less than 1.5. In a randomly selected group of 34 of these patients (some of whom had the smallest right and left pulmonary arteries in the series), Nakata indices were calculated as well. In this subgroup, the mean Nakata index was 283 ± 25.9 mm²/m² (range 85 to 723mm²/m²) and the mean McGoon ratio 2.1 ± 0.13 (range 0.82 to 4.0). The postoperative outcome of this subgroup was not reported, however. In comparison, the mean Nakata index at the time of pre-Fontan cardiac catheterization in our study population was less (183.9 ± 15.9 mm²/m², range 85 to 376 mm²/m²) than that of the subgroup reported in the multicenter trial. Some reports, however, have regarded the Nakata index as a poor predictor of postoperative survival after the Fontan procedure. ^15,16 In the study by Girod and associates, ¹⁵ 90 patients undergoing the Fontan procedure had the pulmonary arteries measured intraoperatively. No difference inmortality was identified on the basis of pre-Fontan (intraoperative) pulmonary artery diameter. However, the smallest pulmonary artery index reported in that series was 188 mm²/m², a value at which all of the patients in our series survived as well. Further, the intraoperative measurement of pulmonary artery size used in that study differed from our angiographic technique. Bridges and colleagues ¹⁶ also reported no correlation between preoperative pulmonary artery diameter and survival after the modified Fontan procedure. The study, however, did note a trend between smaller pulmonary arteries and decreased survival.

In summary, we identified a 32% decrease in Nakata index in 30 children 17.6 months after the bidirectional Glenn procedure, primarily because of a decrease in the diameter of the contralateral pulmonary artery. Reductions in central pulmonary artery diameter appeared to be more prominent in children who had the bidirectional Glenn shunt in place for more than 15 months. Because pulmonary artery stenosis or hypoplasia is regarded as a risk factor for poor outcome after the Fontan operation, these findings raise concern about the potential impact of the bidirectional Glenn staging procedure on post-Fontan morbidity and mortality. Further investigation appears necessary to determine the long-term sequelae of these pulmonary artery changes and the role they play in the surgical approach to the univentricular heart. The findings of this study may support earlier timing of the Fontan repair after a bidirectional Glenn procedure.

Footnotes

From the Department of Pediatrics,^a Division of Pediatric Cardiology, and Department of Surgery,^b Section of Thoracic Surgery, University of Michigan Medical Center, Ann Arbor, Mich.

References

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