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Ann Thorac Surg 2005;80:976-981
© 2005 The Society of Thoracic Surgeons


Original article: Cardiovascular

Appropriate Additional Pulmonary Blood Flow at the Bidirectional Glenn Procedure is Useful for Completion of Total Cavopulmonary Connection

Masahiro Yoshida, MD a , * , Masahiro Yamaguchi, MD, PhD a , Naoki Yoshimura, MD, PhD a , Hirohisa Murakami, MD, PhD a , Hironori Matsuhisa, MD a , Yutaka Okita, MD, PhD b

a Department of Cardiothoracic Surgery, Kobe Children’s Hospital, Kobe, Hyogo, Japan
b Division of Cardiovascular, Thoracic, and Pediatric Surgery, Department of Cardiopulmonary and Vascular Medicine, Kobe University Graduate School of Medicine, Kobe, Hyogo, Japan

Accepted for publication March 21, 2005.

* Address reprint requests to Dr Yoshida, Department of Cardiothoracic Surgery, Kobe Children’s Hospital, 1-1-1 Takakuradai Suma-ku, Kobe, 654-0081, Japan (Email: yoshidamasa_kch{at}hp.pref.hyogo.jp).

Presented at the Poster Session of the Forty-first Annual Meeting of The Society of Thoracic Surgeons, Tampa, FL, Jan 24–26, 2005.


    Abstract
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 
BACKGROUND: The role and effect of additional pulmonary blood flow at the time of bidirectional Glenn procedure (BDG) is controversial. We assessed our experiences to clarify the effects of controlled additional pulmonary blood flow on outcomes after BDG.

METHODS: Thirty-eight patients who underwent BDG (2.1 ± 2.1 years of age) were enrolled in this study. In group A (n = 29) additional pulmonary blood flow was controlled by the banding of the pulmonary trunk, or the previously created Blalock-Taussig shunt, to keep the central venous pressure equal to or less than 16 mm Hg at BDG. In group B (n = 9), BDG was the only source of pulmonary blood flow.

RESULTS: One operative death occurred in group B. In group A, 24 patients underwent total cavopulmonary connection (TCPC) 14 ± 6 months after BDG, and the remaining 5 patients are waiting for TCPC in good condition. In group B, 6 patients underwent TCPC 8 ± 7 months after BDG. One patient is awaiting TCPC and the remaining patient is considered unsuitable for TCPC. Cardiac catheterization performed in 32 patients showed significant decrease of pulmonary artery (Nakata) index from 307 ± 73 to 215 ± 45 mm2/m2 after BDG in group B (p < 0.05). On the other hand, the Nakata index stayed in higher range from 316 ± 115 to 287 ± 74 mm2/m2 in group A, and there was a significant correlation between the Nakata index and the percentage of its difference (Y = 40.823 – 0.144 X; n = 26, R = 0.740, p < 0.0001).

CONCLUSIONS: Appropriate additional pulmonary blood flow is useful for the completion of TCPC by means of suppressing the decrease in the size of the pulmonary artery, especially in patients with underdeveloped pulmonary arteries.


    Introduction
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 
Since the first report in 1971 by Fontan and Baudet [1], the results of the Fontan-type operations have significantly improved recently by the better understanding of Fontan circulation during the perioperative period, adequate patient selection, and appropriate palliations. Specifically, the staged approach that is most often performed by means of the bidirectional Glenn procedure (BDG) is considered one of the reasons for good results in the Fontan-type operations [2–6]. Advantages of the staged approach for the Fontan-type operations are giving effective pulmonary blood flow and stepwise adaptation of ventricular geometry to the reduction in volume load [7]. The role and effect of additional pulmonary blood flow (APF) at the time of BDG is still controversial. The bidirectional Glenn procedure with APF may provide patients with higher oxygen saturation and more growth of pulmonary arteries than BDG without APF [8–10]. However, there are disadvantages to BDG with APF, such as the elevation of venous pressure and volume overload on the ventricle [11, 12]. We started to regulate APF to avoid excessive blood flow at the time of BDG from November 2000. We assessed our experiences to clarify the effects of controlled APF on outcomes after BDG.


    Material and Methods
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 
Patients and Surgical Technique
Thirty-eight patients were enrolled in this study. This includes 9 patients who underwent BDG with APF before we started to regulate APF, and 29 consecutive patients who underwent BDG from November 2000 to February 2004. Average age at the time of BDG was 2.1 ± 2.1 years old. All of the patients had functional single ventricle morphology. Ten patients had univentricular hearts, 7 had double outlet right ventricles, 12 had single atrioventricular valves including tricuspid atresia and mitral valve atresia, and the remaining 9 patients had other cardiac malformations. Six of them had isomerism hearts, in which isomerism of the right appendage was seen in 5 and the left in one. The bidirectional Glenn procedure was the first surgical procedure in 6 patients. A total of 43 previous palliative procedures were performed in 32 patients (Table 1).


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Table 1. Patients’ Profile
 
The bidirectional Glenn procedure was performed through a median sternotomy in all patients but one who had a left thoracotomy because his situs was the inverted version and a central shunt was previously performed through a median sternotomy. In 26 patients BDG was completed without cardiopulmonary bypass, using temporary bypass between the superior vena cava and the atrium. Cardiopulmonary bypass was used in 12 patients who required an intracardiac procedure or whose circulation could not be maintained without cardiopulmonary bypass during the procedure. Pulmonary arterioplasty using autologous pericardium was performed in 15 patients, interatrial septectomy in 5, Damus-Kaye-Stansel anastomosis [13–15] in 2, and atrioventricular valvuloplasty in 2 at the time of BDG. Central venous pressure was monitored in all cases by a catheter placed in the superior vena cava. Additional pulmonary blood flow was left and controlled by banding the pulmonary trunk (pulmonary artery banding [PAB]) or previously created Blalock-Taussig (BT) shunt with the following methods to keep the central venous pressure to or less than 16 mm Hg immediately after the bidirectional Glenn anastomosis. For banding the pulmonary trunk, an expanded polytetrafluoroethylene tube (ePTFE, Gore-Tex, WL Gore & Associates, Inc, Elkton, MD), 3 mm in width, was used. If the patient had preceding PAB before BDG, the PAB was tightened by fixing the previous tube tighter. For banding the BT shunt, an ePTFE graft of 8 mm length and same with the shunt or smaller in size was used to wrap the previously created BT shunt. Controlled APF could be left in 29 patients by these methods. In 6 patients PAB had been performed before BDG; then the PAB was tightened in 4 patients, and the previous PAB was left alone in 2. Of 6 patients with the stenotic pulmonary trunk, 5 had PAB at the time of BDG and one had ligation of the patent ductus arteriosus. In 4 patients, a previously created BT shunt was ligated and the stenotic pulmonary trunk was left alone in 3 and PAB was performed in 1. In 13 patients who did not have the pulmonary trunk, previously created BT shunt was left in 9, and in 3 the BT shunt was banded. In one patient, a central shunt was established using ePTFE graft of 3 mm in diameter to give APF at BDG (Table 2). In 7 patients central venous pressure exceeded 16 mm Hg without APF; then APF could not be left. In 2 patients APF was not left because there was no proper APF source like the pulmonary trunk or BT shunt after performing bidirectional Glenn anastomosis. During the procedure, patients were ventilated with 80% oxygen without inhalation of nitrogen-oxide. After the regulation of APF, nitrogen-oxide was used when necessary.


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Table 2. Source of Pulmonary Blood Flow Before and After BDG
 
Patients were divided into two groups. In group A (n = 29) pulmonary blood flow was maintained by BDG with APF. In group B (n = 9), BDG was the only source of pulmonary blood flow. Statistically, there was no difference between the two groups in age, body weight, pulmonary resistance, Nakata index (pulmonary artery index [PAI]) [16], pulmonary arterial pressure, systemic ventricular end-diastolic volume, and ventricular ejection fraction at the time of BDG. The percentage of patients who required cardiopulmonary bypass was significantly higher in group B than in group A (Table 3).


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Table 3. Comparisons of Preoperative Data Between Groups
 
Cardiac catheterization was performed 9 ± 5 months after BDG to estimate suitability for the Fontan operation. If the patient was judged suitable for the Fontan operation, total cavopulmonary connection (TCPC) using an ePTFE graft of 18 to 22 mm in diameter was performed [17, 18]. Extracardiac conduit TCPC was chosen for almost all cases except for patients who had apicocaval juxtaposition [19], in whom intraatrial conduit TCPC was chosen.

Statistical Analysis
Preoperative and postoperative data were analyzed and compared between the groups. Data are expressed as mean ± standard deviation. The volumes of the left-dominant-type ventricle were calculated using the area-length method [20], and the volumes of the right-dominant-type ventricle were calculated according to Simpson’s rule [21]. The systemic ventricular end-diastolic volume was described as a percentage compared with the anticipated normal value calculated from body surface area. The paired t test was used to compare PAI before and after BDG, the unpaired t test was used to compare variables between groups, and the {chi}2 test was used to compare the frequency of things using StatView-4.11 for Macintosh (Abacus Concepts, Inc, Berkeley, CA). 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
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 
One operative death occurred in group B. This patient had severe cyanosis with pulmonary atresia, moderate common atrioventricular valve regurgitation, and isomerism of the right appendage. He underwent BDG at 3 months of age and died 2 weeks after the operation due to increased valve regurgitation.

In group A, central venous pressure measured at the operating theater, at the intensive care unit, and after extubation was 15.0 ± 1.5, 15.6 ± 2.1, and 12.0 ± 2.3 mm Hg, respectively. Twenty-four patients underwent TCPC 14 ± 6 months after BDG and 4 patients are awaiting TCPC in good condition. The ligation of APF was required 13 months after BDG in one patient who had right isomerism to decrease common atrioventricular valve regurgitation. Except for the abovementioned patient, the aggravation of atrioventricular valve regurgitation was not seen in any patients by echocardiography.

In group B, 6 patients underwent TCPC 8 ± 7 months after BDG. Four of them showed severe hypoxia and required oxygen inhalation until TCPC was completed. One patient is awaiting TCPC in good condition. Balloon angioplasty was required in one patient before TCPC for restenosis at the site of pulmonary arterioplasty. A thrombus formation occurred at the site of pulmonary arterioplasty in 2 patients. One of them underwent TCPC and the other was judged not amenable to surgery.

The comparisons of 30 patients in the two groups who underwent TCPC are shown in Table 4. There was a significant difference between the two groups in the period between BDG and TCPC. There was one hospital death after TCPC in each group. Both patients had right isomerism hearts; one died the day after TCPC due to arrhythmia and the other died of liver dysfunction one month after TCPC.


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Table 4. Comparisons of TCPC Completion Cases Between Groups
 
Cardiac catheterizations were performed in 32 patients before and after BDG. Major pulmonary arteriovenous malformations were not seen in any patients. In group B, PAI significantly decreased from 307 ± 73 to 215 ± 45 mm2/m2 (p < 0.05). On the other hand, PAI stayed in a higher range, from 316 ± 115 to 287 ± 74 mm2/m2, in group A. We employed a new index, PAI%-change, to evaluate the growth ratio of the pulmonary artery, which is calculated by PAI before BDG (pre-PAI) and PAI after BDG (post-PAI) for every patient as follows: PAI%-change = (post-PAI – pre-PAI) / pre-PAI x 100. There was a significant correlation between pre-PAI and PAI%-change (Fig 1) in group A. This correlation shows that the size of the pulmonary artery was maintained or increased by APF for the patients who had smaller pulmonary arteries at the time of BDG.



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Fig 1. Correlations Between pre-PAI and PAI%-change PAI%-change = (post-PAI – pre-PAI) / pre-PAI x 100 pre-PAI : PAI calculated from pulmonary angiography before bidirectional Glenn procedure (BDG). post-PAI : PAI calculated from pulmonary angiography after BDG. Open circles indicate the patients in group A and solid circles indicate the patients in group B. In group A, Y = 40.823 – 0.144 X; n = 26, R = 0.740, p < 0.0001 (solid line). In group B, Y = –6.128 – 0.074 X; n = 6, R = 0.431, p = 0.394 (dotted line). (PAI = pulmonary artery [Nakata] index.)

 
Postoperative cardiac catheterization studies were performed in 24 patients after TCPC. There was no difference between the two groups in cardiac output and central venous pressure (CVP) (Table 4). Cardiac output, CVP, and post-PAI were plotted and shown in Figure 2. Although there was no correlation between cardiac output and post-PAI, there was a significant correlation between CVP and post-PAI.



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Fig 2. Correlations between (top) cardiac output, (bottom) central venous pressure (CVP), after total cavopulmonary connection (TCPC) and post-pulmonary artery index (post-PAI) in 24 patients ({circ}). (post-PAI: PAI calculated from pulmonary angiography after bidirectional Glenn procedure, that is, before TCPC). There is no correlation between cardiac output and post-PAI (solid line in upper figure); however, there is significant correlation between CVP and post-PAI (solid line in lower figure); (Y = 17.174-0.01X; R = 0.420, p = 0.041).

 

    Comment
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 
Recently, the results of the Fontan-type operations have been significantly improved by the understanding of Fontan circulation during the perioperative period, adequate patient selection, and appropriate palliations. The bidirectional Glenn procedure, by means of the staged approach, played one of the most important roles in improving the results of the Fontan-type operations [2–6]. Advantages of the staged approach for the Fontan-type operations are giving effective pulmonary blood flow and stepwise adaptation of ventricular geometry to the reduction in volume load [7].

The role and effect of APF at the time of BDG has not been made clear enough. Reported advantages of APF were maintenance of higher oxygen saturation and better growth of pulmonary arteries than BDG without APF [8–10]. On the other hand, disadvantages of APF were also reported [11, 12]. Mainwaring and colleagues [12] described that both operative and late mortality were higher in the patients with APF than without APF. Additional pulmonary blood flow resulted in elevation of venous pressure and volume overload on the ventricle. We started this study expecting that these disadvantages could be reduced by avoiding excessive APF and that appropriate APF would provide better results than uncontrolled APF.

What is appropriate APF? There is a report that recommends antegrade pulmonary blood flow to be controlled [22] and we also believe that APF should be reduced at BDG. There is no report that describes the amount of regulation of APF. We started to use CVP as a criterion of regulation to get appropriate APF during operation. We assumed that the CVP of 16 mm Hg or less might be ideal at the operating theater as it is well known from our experience that CVP decreases 2 to 3 mm Hg by extubation after BDG. As a result, CVP decreased to 12 ± 2.3 mm Hg after extubation in our series with controlled APF. Although to regulate shunt flow appropriately was more difficult than pulmonary trunk flow, our criterion of CVP was also useful in avoiding excessive shunt flow.

Decrease of PAI after BDG without APF has been described in several reports [5, 23]. It is speculated that the pulmonary blood flow of BDG may not be enough to maintain the PAI and to grow suitably with body size. The greatest advantage of APF is the growth of the pulmonary artery after BDG. Our series also indicated that the APF could maintain the size of the pulmonary artery by increasing pulmonary blood flow. Furthermore, there was a significant correlation between pre-PAI and PAI%-change in group A in this study. This correlation shows APF is more effective in patients who have underdeveloped pulmonary arteries. Increase of PAI could be expected after BDG in patients who had less than 250 of PAI before BDG. There was no significant correlation between them in group B because of the small number of patients, but the regression line was at a much lower level than that of group A. We consider the difference between these lines as just the effectiveness of suppressing the decrease of PAI.

Disadvantages of APF are also expected to be reduced by our method of controlled APF. There was only one patient who developed common atrioventricular valve regurgitation after BDG with APF. She had right isomerism heart and presented with mild regurgitation of the atrioventricular valve. It may be a contraindication to leave APF for the patients who have isomerism hearts because they have incomplete atrioventricular valve morphology that may easily develop regurgitation [24].

When the patient has no proper source of APF, it may be difficult to get APF. We had only one patient who underwent a new central shunt using a small graft to get APF at the time of BDG. There were two patients who did not have a new shunt, despite their pulmonary pressures being less than 16 mm Hg at the time of operation. We think we should have placed a new small shunt because one of them developed a complication of thrombus formation and the other required balloon angioplasty for restenosis at the site of pulmonary arterioplasty. By the controlled APF with our method, it is expected to avoid these complications as there was no patient who had such complications after BDG with APF. At present, we consider that the efforts to establish APF at the time of BDG be made even in patients who have no proper source.

Masuda and colleagues [5] claim that small PAI is not so important as a risk factor of Fontan completion, since the staged approach became the main strategy. However, we are reluctant to perform TCPC for a patient whose PAI is 150 or less, as it is shown that the smaller the PAI before TCPC, the higher the CVP after TCPC in our series [18].

By our method of controlling APF reported in this study, it was possible to get an appropriate APF. However, this is not a randomized study. Accurate comparison is difficult, as there were differences in preoperative conditions and ratios of patients who required cardiopulmonary bypass, between the two groups. Patients in group B had more compromised pulmonary circulation as evidenced by the higher CVP observed in the presence of APF and the higher proportion of cardiopulmonary bypass required at the time of BDG. Further study seems to be necessary to clarify our opinion.

In conclusion, appropriate APF is useful for completion of TCPC by means of suppressing the decrease in size of the pulmonary artery, especially in patients with underdeveloped pulmonary arteries.


    References
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 

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  8. Uemura H, Yagihara T, Kawashima Y, et al. Use of the bidirectional Glenn procedure in the presence of forward flow from the ventricles to the pulmonary arteries Circulation 1995;92(suppl 2):228-232.[Abstract/Free Full Text]
  9. Miyaji K, Shimada M, Sekiguchi A, Ishizawa A, Isoda T. Usefulness of pulsatile bidirectional cavopulmonary shunt in high-risk Fontan patients Ann Thorac Surg 1996;61:845-850.[Abstract/Free Full Text]
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  11. Frommelt MA, Frommelt PC, Berger S, et al. Does an additional source of pulmonary blood flow alter outcome after a bidirectional cavopulmonary shunt? Circulation 1995;92(suppl 2):240-244.[Abstract/Free Full Text]
  12. Mainwaring RD, Lamberti JJ, Uzark K, Spicer RL, Cocalis MW, Moore JW. Effect of accessory pulmonary bidirectional Glenn procedure Circulation 1999;100(suppl 2):151-156.
  13. Damus PS. Letter to the editor Ann Thorac Surg 1975;20:724-725.
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  18. Yoshimura N, Yamaguchi M, Oshima Y, et al. Risk factors influencing early and late mortality after total cavopulmonary connection Eur J Cardiothorac Surg 2001;20:598-602.[Abstract/Free Full Text]
  19. Kitayama H, Oku H, Matsumoto T, Onoe M. Total cavopulmonary connection using a pedicled pericardial conduit for a patient with apicocaval juxtaposition Ann Thorac Surg 2001;72:1393-1394.[Abstract/Free Full Text]
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