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Management of failing bidirectional cavopulmonary shunt: Influence of additional systemic-to-pulmonary-artery shunt with classic Glenn physiology

  • Caecilia Euringer
    Affiliations
    Department of Congenital and Pediatric Heart Surgery, German Heart Center Munich, Technische Universität München, Munich, Germany

    Division of Congenital and Pediatric Heart Surgery, University Hospital of Munich, Ludwig-Maximilian-University of Munich, Munich, Germany
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  • Takashi Kido
    Affiliations
    Department of Congenital and Pediatric Heart Surgery, German Heart Center Munich, Technische Universität München, Munich, Germany

    Division of Congenital and Pediatric Heart Surgery, University Hospital of Munich, Ludwig-Maximilian-University of Munich, Munich, Germany
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  • Bettina Ruf
    Affiliations
    Department of Pediatric Cardiology and Congenital Heart Disease, German Heart Center Munich, Technische Universität München, Munich, Germany
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  • Melchior Burri
    Affiliations
    Department of Cardiovascular Surgery, German Heart Center Munich, Technische Universität München, Munich, Germany
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  • Paul Philipp Heinisch
    Affiliations
    Department of Congenital and Pediatric Heart Surgery, German Heart Center Munich, Technische Universität München, Munich, Germany

    Division of Congenital and Pediatric Heart Surgery, University Hospital of Munich, Ludwig-Maximilian-University of Munich, Munich, Germany
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  • Janez Vodiskar
    Affiliations
    Department of Congenital and Pediatric Heart Surgery, German Heart Center Munich, Technische Universität München, Munich, Germany

    Division of Congenital and Pediatric Heart Surgery, University Hospital of Munich, Ludwig-Maximilian-University of Munich, Munich, Germany
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  • Martina Strbad
    Affiliations
    Department of Congenital and Pediatric Heart Surgery, German Heart Center Munich, Technische Universität München, Munich, Germany

    Division of Congenital and Pediatric Heart Surgery, University Hospital of Munich, Ludwig-Maximilian-University of Munich, Munich, Germany
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  • Julie Cleuziou
    Affiliations
    Department of Congenital and Pediatric Heart Surgery, German Heart Center Munich, Technische Universität München, Munich, Germany

    Division of Congenital and Pediatric Heart Surgery, University Hospital of Munich, Ludwig-Maximilian-University of Munich, Munich, Germany
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  • Daniel Dilber
    Affiliations
    Department of Pediatrics, University Hospital Centre Zagreb, School of Medicine Zagreb, Zagreb, Croatia
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  • Alfred Hager
    Affiliations
    Department of Pediatric Cardiology and Congenital Heart Disease, German Heart Center Munich, Technische Universität München, Munich, Germany
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  • Peter Ewert
    Affiliations
    Department of Pediatric Cardiology and Congenital Heart Disease, German Heart Center Munich, Technische Universität München, Munich, Germany
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  • Jürgen Hörer
    Affiliations
    Department of Congenital and Pediatric Heart Surgery, German Heart Center Munich, Technische Universität München, Munich, Germany

    Division of Congenital and Pediatric Heart Surgery, University Hospital of Munich, Ludwig-Maximilian-University of Munich, Munich, Germany
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  • Masamichi Ono
    Correspondence
    Address for reprints: Masamichi Ono, MD, PhD, Department of Congenital and Pediatric Heart Surgery, German Heart Center Munich, Lazarettstraße 36, 80636 Munich, Germany.
    Affiliations
    Department of Congenital and Pediatric Heart Surgery, German Heart Center Munich, Technische Universität München, Munich, Germany

    Division of Congenital and Pediatric Heart Surgery, University Hospital of Munich, Ludwig-Maximilian-University of Munich, Munich, Germany
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Open AccessPublished:June 10, 2022DOI:https://doi.org/10.1016/j.xjon.2022.06.007

      Abstract

      Objectives

      Severe hypoxemia in the early postoperative period after bidirectional cavopulmonary shunt (BCPS) is a critical complication. We aimed to evaluate patients who underwent additional systemic to pulmonary shunt and septation of central pulmonary artery (partial takedown) after BCPS.

      Methods

      The medical records of all patients who underwent BCPS between 2007 and 2020 were reviewed. Patients who underwent partial takedown were extracted and their outcomes were analyzed.

      Results

      Of 441 BCPS patients, 27 patients (6%) required partial takedown. Most frequent diagnosis was hypoplastic left heart syndrome (n = 14; 52%). Additional complicating factors included pulmonary artery hypoplasia (n = 12) and pulmonary venous obstruction (n = 3). Thirteen patients (48%) underwent partial takedown on the same day of BCPS, and all of them survived the procedure. The remaining 14 patients (52%) underwent partial takedown between postoperative 1 to 64 days. The reasons for partial takedown were: postoperative high pulmonary vascular resistance (n = 4), early BCPS (<90 days) with PA hypoplasia (n = 3), mediastinitis/pneumonia (n = 3), pulmonary venous obstruction (n = 2), ventricular dysfunction (n = 1), and recurrent pneumothorax (n = 1). Four patients experienced hospital deaths. Six patients died after discharge, 10 achieved Fontan completion, and 6 were alive and waiting for Fontan. Overall survival after partial takedown was 54% at 3 years. The pulmonary venous obstruction (P = .041) and genetic/extracardiac anomalies (P = .085) were identified as risks for mortality after partial takedown.

      Conclusions

      The partial takedown resulted in a 3-year survival rate of more than 50%. Of these patients, a significant number underwent successful Fontan completion who would exhibit potential early death with conservative treatment.

      Graphical abstract

      Key Words

      Abbreviations and Acronyms:

      AVV (atrioventricular valve), BCPS (bidirectional cavopulmonary shunt), CPB (cardiopulmonary bypass), ECMO (extracorporeal membrane oxygenation), HLHS (hypoplastic left heart syndrome), PA (pulmonary artery), PAP (pulmonary artery pressure), PVO (pulmonary venous obstruction), SVC (superior vena cava), TCPC (total cavopulmonary connection), VF (ventricular function)
      Figure thumbnail fx2
      Schematic drawing of additional systemic-to-pulmonary shunt with classic Glenn physiology.
      In 27 patients who underwent additional systemic-to-pulmonary shunt for failing bidirectional cavopulmonary shunt, survival at 3 years was 54% and Fontan completion was done or planed in 16 patients.
      Additional systemic-to-pulmonary-artery shunt with classic Glenn physiology was performed for heterogeneous reasons in 27 patients with failing bidirectional cavopulmonary shunt. Although these patients frequently develop thrombus and need ECMO, survival and successful Fontan completion rate are encouraging. Refinement of this strategy might improve the survival of this high-risk population.
      Because we actually experience no early mortality after stage III Fontan palliation, concerns have been focused on the indication, timing, and postoperative management of stage II palliation by means of bidirectional cavopulmonary shunt (BCPS) procedure in patients with functional single ventricle physiology.
      • Ono M.
      • Burri M.
      • Mayr B.
      • Anderl L.
      • Strbad M.
      • Cleuziou J.
      • et al.
      Risk factors for failed Fontan procedure following stage 2 palliation.
      • Ono M.
      • Kido T.
      • Burri M.
      • Anderl L.
      • Ruf B.
      • Cleuziou J.
      • et al.
      Risk factors for thrombus formation at stage 2 palliation and its effect on long-term outcome in patients with univentricular heart.
      • Kido T.
      • Ono M.
      • Anderl L.
      • Burri M.
      • Strbad M.
      • Balling G.
      • et al.
      Factors influencing length of intensive care unit stay following a bidirectional cavopulmonary shunt.
      Although low pulmonary artery pressure (PAP) is the most important criteria for successful BCPS, there are many other issues to be considered, such as pulmonary artery (PA) hypoplasia, pulmonary venous obstruction (PVO), reduced systemic ventricular function (VF), atrioventricular valve (AVV) regurgitation, and other underlying patient diseases.
      • Lee T.M.
      • Aiyagari R.
      • Hirsch J.C.
      • Ohye R.G.
      • Bove E.L.
      • Devaney E.J.
      Risk factor analysis for second-stage palliation of single ventricle anatomy.
      ,
      • Tan A.M.
      Fontan completion rate and outcomes after bidirectional cavo-pulmonary shunt.
      Despite sophisticated preoperative patient selection, we encounter certain patients who demonstrated severe hypoxemia after BCPS, so called failing BCPS. A fundamental concern of BCPS is that pulmonary blood flow is entirely dependent on passive superior vena cava (SVC) flow, and the success of BCPS is considered to be exquisitely dependent on an unobstructed, low-resistance pulmonary vascular bed.
      • Freedom R.M.
      • Nykanen D.
      • Benson L.N.
      The physiology of the bidirectional cavopulmonary connection.
      When a BCPS fails without any SVC-PA pathway obstruction, SVC flow is insufficient to supply pulmonary blood flow in both lungs to maintain BCPS circulation. Differential diagnoses include postoperative high pulmonary vascular resistance (occasionally due to pulmonary infection), PVO, AVV regurgitation, or systemic ventricular dysfunction. These conditions are difficult to manage.
      • Kido T.
      • Euringer C.
      • Burri M.
      • Vodiskar J.
      • Strbad M.
      • Cleuziou J.
      • et al.
      Impact of hypoxemia and re-interventions on clinical outcomes after bidirectional cavopulmonary shunt.
      In this setting, complete takedown of BCPS to the shunt dependent pulmonary circulation is a standard option. However, previous studies have shown that this approach has a high mortality rate.
      • Zampi J.D.
      • Hirsch-Romano J.C.
      • Armstrong A.K.
      Early cyanosis after stage II palliation for single ventricle physiology: etiologies and outcomes.
      ,
      • Luo S.
      • Haranal M.
      • Deng M.X.
      • Varenbut J.
      • Runeckles K.
      • Steve Fan C.P.
      • et al.
      Low preoperative superior vena cava blood flow predicts bidirectional cavopulmonary shunt failure.
      Since 2007, we have consistently performed another option, so-called partial takedown (ie, placement of additional systemic-to-pulmonary shunt and interruption of central pulmonary artery between BCPS and systemic-to-pulmonary shunt) to overcome this severe situation (Figure 1). Therefore, we undertook the present study to determine the short- to midterm outcomes of patients who underwent partial takedown for failing BCPS to evaluate the usefulness of this option and to analyze the risks for survival after partial takedown.
      Figure thumbnail gr1
      Figure 1Outcomes of partial takedown in 27 patients who presented with prohibitive cyanosis after bidirectional cavopulmonary shunt (BCPS) during the study period between 2007 and 2020. More than half of the patients were diagnosed with hypoplastic left heart syndrome. The causes of partial takedown were left pulmonary artery hypoplasia in 10 patients, elevated pulmonary vascular resistance in 5 patients, mediastinitis/pneumonia in 4 patients, early BCPS <90 days in 3 patients, pulmonary venous obstruction in 3 patients, ventricular dysfunction in 1 patient, and recurrent pneumothorax in 1 patients. There were 4 hospital deaths and 7 late deaths. Kaplan-Meier estimate transplant-free survival was 54% at 3 years. During the follow-up, 10 patients completed the Fontan procedure. IQR, Interquartile range.

      Materials and Methods

      We reviewed data on all patients who underwent staged II BCPS palliation at the German Heart Center Munich between January 2007 and December 2020 and extracted the patients who underwent partial takedown (additional systemic-to-pulmonary shunt with interruption of the PA continuity between BCPS and additional systemic-to-pulmonary shunt). The Institutional Review Board of the Technische Universität München approved the study and waived the requirement for patient consent (approved ID: 65/20 S-KH; February 18, 2020). Review of medical records, including in-hospital and outpatient notes, echocardiography, and cardiac catheterization was performed.

      Pre-BCPS Assessment

      In our institution, all patients routinely underwent cardiac catheterization and echocardiography as the preoperative evaluation before BCPS. Cardiac catheterization was performed to obtain hemodynamic data and angiographic assessment of PA, and echocardiography to assess systemic VF and AVV regurgitation. Systemic VF was assessed qualitatively, and reduced VF was defined as ejection fraction <50%. The AVV regurgitation was graded as previously described.
      • Ono M.
      • Cleuziou J.
      • Pabst von Ohain J.
      • Beran E.
      • Burri M.
      • Strabad M.
      • et al.
      Atrioventricular valve regurgitation in patients undergoing total cavopulmonary connection: impact of valve morphology and underlying mechanisms on survival and reintervention.
      Moderate or more AVV regurgitation was defined as a significant AVV regurgitation.

      Surgical Techniques

      BCPS was performed with mild hypothermic cardiopulmonary bypass (CPB) and standard bicaval cannulation, as described in our previous reports.
      • Ono M.
      • Burri M.
      • Mayr B.
      • Anderl L.
      • Strbad M.
      • Cleuziou J.
      • et al.
      Risk factors for failed Fontan procedure following stage 2 palliation.
      ,
      • Schreiber C.
      • Cleuziou J.
      • Cornelsen J.K.
      • Hörer J.
      • Eicken A.
      • Lange R.
      Bidirectional cavopulmonary connection without additional pulmonary blood flow as an ideal staging for functional univentricular hearts.
      A catheter to monitor central venous pressure was routinely inserted into the right internal jugular vein. Cardioplegic arrest was used only for patients who required intracardiac procedures. The azygos vein was routinely divided before initiation of CPB. The BCPS anastomosis and PA reconstruction were performed in an on-pump beating state. Any antegrade pulmonary blood flow was routinely eliminated at the time of BCPS by dividing the main PA and oversewing the pulmonary valve, or by dividing previous systemic-to-pulmonary shunt.
      • Schreiber C.
      • Cleuziou J.
      • Cornelsen J.K.
      • Hörer J.
      • Eicken A.
      • Lange R.
      Bidirectional cavopulmonary connection without additional pulmonary blood flow as an ideal staging for functional univentricular hearts.
      The SVC was anastomosed to the right PA in an end-to-side fashion using 7–0 or 8–0 polydioxanone continuous sutures (Ethicon Inc).
      Partial takedown was performed in patients who demonstrated severe hypoxemia after BCPS (Figure 2). On CPB, an additional systemic-to-pulmonary shunt was placed to the left of BCPS anastomosis with 3.0 mm, 3.5 mm, or 4.0 mm polytetrafluoroethylene graft. Shunt size was determined by the surgeons according to patient's size, pulmonary artery size, and estimation of the pulmonary vascular resistance of the affected lung. Proximal anastomosis was performed in the innominate artery, or in the ascending aorta (central aortopulmonary shunt). In some patients, the preexisting shunt was applied for partial takedown. The interruption of PA continuity was accomplished by ligation, clipping, or patch insertion of the middle portion between the BCPS and the additional systemic-to-pulmonary shunt. Methods of PA interruption were chosen at the surgeon's preference.
      Figure thumbnail gr2
      Figure 2Schematic drawing of partial takedown (additional systemic to pulmonary shunt with classic Glenn physiology). BT, Blalock-Taussig shunt; SVC, superior vena cava; LPA, left pulmonary artery; PA, pulmonary artery.

      Postoperative Management

      As for the anticoagulation strategies, postoperative standard thrombosis prophylaxis after BCPS consisted of intravenous administration of unfractionated heparin (5000 IU/m2/d) with a target partial thromboplastin time of 60 seconds, until all central lines (usually a 4.5Fr catheter was used) were removed (usually 4-5 postoperative days). Later, no routine antithrombotic prophylaxis was given after BCPS. Nevertheless, patients who underwent partial takedown received acetylsalicylic acid or warfarin due to a persistent aortopulmonary shunt. In patients who needed extracorporeal membrane oxygenation (ECMO) support, anticoagulation was performed using intravenous administration of unfractionated heparin with the target range of anti-Xa 0.35 to 0.50 U/mL, activated clotting time within 180 to 200 seconds and partial thromboplastin time of 60 to 80 seconds.

      Follow-up Data

      Patients were followed-up by pediatric cardiologists as outpatients, and follow-up times were defined per patient as the time from the day of partial takedown to the last visit. For the patients who died, the data were collected at the time of death. Because no heart transplantation was performed in the entire cohort during the study period, the primary outcome of interest was the composite end point of Fontan completion or death. The follow-up data from time of surgery until the last known record of the patients were regularly tracked using our institutional single ventricle patient database system.

      Statistical Analysis

      Categorical variables are presented as absolute numbers and percentages. A χ2 test was used for categorical data. Continuous variables are expressed as mean ± SD or median with interquartile range (IQR), if appropriate. An independent sample t test was used to compare normally distributed variables. Mann-Whitney test was used for variables that were not normally distributed. Survival after BCPS partial takedown was analyzed using the Kaplan-Meier method. A univariable Cox proportional hazard regression model was used to assess the association between preoperative risk factors and mortality after partial takedown. The proportional hazard assumption was tested using Schoenfeld residuals. We did not correct for multiple testing in all tests and models we performed. Data analysis and graphing were performed with the Statistical Package for the Social Sciences version 28.0 for Windows (IBM-SPSS Inc) and state package and CMPRSK package in R version 4.0.3 (R Foundation for Statistical Computing).

      Results

      Patient's Characteristics and Pre-BCPS Hemodynamic Assessment

      Among 441 patients who underwent BCPS at our institution between January 2007 and December 2020, 27 patients (6%) needed partial takedown. Patient characteristics are shown in Table 1. Primary diagnoses included 14 (52%) hypoplastic left heart syndromes (HLHS), 4 (15%) tricuspid atresia, and 3 (11%) unbalanced atrioventricular septal defects. Genetic/extracardiac anomalies were associated in 9 patients (33%).
      Table 1Patient characteristics and bidirectional cavopulmonary shunt (BCPS) data
      Patient No.DiagnosisGenetic/extracardiac anomaliesStage I palliationShunt sizePA hypoplasiaLPA indexBCPS age (mon)PCPC height (cm)Interval (d)Causes of hypoxemiaAdditional shuntShunt size
      1HLHSNorwood5.0LPA (2.6 mm)385.061ConHypo LPASano LPA5.0
      2DILV, TGA, IAANorwood4.0LPA (3.2 mm)433.760ConHypo LPABT LPA3.5
      3HLHSDandy-WalkerNorwood5.0LPA (2.5 mm)275.160ConHypo LPASano LPA5.0
      4DORV, MSTetrasomie 18pNorwood3.5LPA (1.2 mm)313.856ConHypo LPABT LPA3.5
      5TA IbVACTERLno2792.259ConLow SVC flowBT LPA3.5
      6HLHSCleft palateNorwood3.0LPA (1.5 mm)124.653ConHypo LPABT LPA3.0
      7HLHSNorwood3.5LPA (1.9 mm)354.760ConHypo LPABT LPA3.5
      8HLHSNorwood3.0763.150ConLow SVC flowBT LPA3.0
      9DORV, MANorwood3.5LPA (3.0 mm)294.254ConHypo LPABT LPA3.5
      10HLHS, TAPVCNorwood3.5865.157ConLow SVC flowCS LPA3.5
      11HLHSNorwood3.5863.652ConLow SVC flowBT LPA3.5
      12HLHSNorwood3.5LPA (2.0 mm)351.8550Hypo LPABT LPA3.5
      13DIRV, TGA, PAPDA stent4.0LPA (3.5 mm)443.4570Hypo LPACS RPA3.5
      14HLHS, PAPVCNorwood3.5533.4581PVOBT LPA3.5
      15UAVSD, TGA, PACHARGEPDA stent3.51487.5643high PVRCS LPA4.0
      16HLHSNorwood3.5664.5544high PVRBT LPA3.0
      17HLHSNorwood3.5LPA (3.0 mm)522.7545Early BCPSBT LPA3.5
      18HLHS, TAPVCNorwood3.5852.8619Early BCPSBT LPA3.5
      19UAVSDTrisomy 21PAB33612.87813high PVRCS LPA4.0
      20HLHSNorwood5.0824.35817TR, reduced VFBT LPA3.5
      21PAIVS, EbsteinMBTS3.5984.16121MediastinitisCS LPA3.5
      22UAVSD, DORV, PSTracheal stenosisMBTS3.51843.25823PVOBT LPA3.5
      23TA IaPDA stent4.0LPA (2.7 mm)885.26429high PVRCS LPA3.0
      24TA IbPDA stent3.5662.95633Early BCPSCS LPA3.5
      25ccTGA, TA, IAANotch-GenNorwood3.5LPA (2.6 mm)724.16235MediastinitisBT LPA3.5
      26TA IcRenal anomaliesMBTS3.51074.16262PneumothoraxBT LPA4.0
      27HLHSNorwood5.0863.56063MediastinitisBT LPA3.5
      PA, Pulmonary artery; LPA, left pulmonary artery; PCPC, partial cavopulmonary connection; HLHS, hypoplastic left heart syndrome, Con, concomitant; Sano, Sano shunt (right ventricle to pulmonary artery conduit); DILV, double inlet left ventricle; TGA, transposition of the great arteries; IAA, interrupted aortic arch; BT, Blalock-Taussig; DORV, double outlet right ventricle; MS, multiple sclerosis; TA, tricuspid atresia; VACTERL, VACTERL syndrome; SVC, superior vena cava; TAPVC, total anomalous pulmonary venous return; CS, central shunt; RPA, right pulmonary artery; DIRV, double inlet right ventricle; PA, pulmonary artery; PAPVC, partial anomalous pulmonary venous connection; PVO, pulmonary venous obstruction; UAVSD, unbalanced atrioventricular septal defect; PVR, pulmonary vascular resistance, LPA, left pulmonary artery; PAB, pulmonary artery banding; TR, tricuspid valve regurgitation; VF, ventricular function; MBTS, modified Blalock-Taussig shunt; CHARGE, CHARGE association; PAIVS, pulmonary atresia with intact ventricular septum; Ebstein, Ebstein anomaly; PS, pulmonary stenosis; PDA, patent ductus arteriosus; ccTGA, congenitally corrected transposition of the great arteries.
      Pre-BCPS cardiac catheterization data are shown in Table 2. Hemodynamic assessment revealed mean PAP of 14.5 ± 3.9 mm Hg, mean transpulmonary gradient of 7.4 ± 2.7 mm Hg, systemic ventricular end-diastolic pressure of 9.5 ± 2.9 mm Hg, and arterial oxygen saturation of 75.5% ± 6.1%. Pulmonary vascular pathology included left PA hypoplasia in 12 patients (Figure E1) and PVO in 3 patients. In these 3 patients with PVO, total/partial anomalous pulmonary venous connection had been repaired at the time of stage I or II palliation, and PVO had at least 1 lobar pulmonary vein branch. No patient demonstrated abundant aortopulmonary collaterals, sizable systemic venous-venous collaterals, or re-coarctation of the aorta. A preoperative echocardiography performed immediately before BCPS showed reduced VF in 3 patients and significant AVV regurgitation in 5 patients.
      Table 2Pre-bidirectional cavopulmonary shunt catheterization and echocardiographic data
      VariableResult
      Catheterization data
       Hemoglobin (g/dL)13.8 ± 1.9
       Mean pulmonary artery pressure (mm Hg)14.5 ± 3.9
       Mean left atrial pressure (mm Hg)6.9 ± 2.5
       Transpulmonary gradient (mm Hg)7.4 ± 2.7
       Systolic ventricular pressure (mm Hg)78.0 ± 12.4
       Ventricular endodiastolic pressure (mm Hg)9.5 ± 2.9
       Aortic oxygen saturation (%)75.5 ± 6.1
      Echocardiographic data
       Ventricular function
      Normal23 (85.2)
      Mildly impaired2 (7.4)
      Moderately impaired2 (7.4)
       Atrioventricular valve regurgitation
      None3 (11.1)
      Trivial10 (37.0)
      Mild9 (33.3)
      Moderate4 (14.8)
      Severe1 (3.7)
       (Neo) aortic insufficiency
      None20 (74.1)
      Trivial6 (22.2)
      Mild1 (3.7)
      Values are presented as n (%) or mean ± SD.

      Operative and Early Postoperative Outcomes

      Patient-specific details and additional procedures at the time of BCPS are listed in Table 3. Median age and weight at BCPS were 4.1 months (IQR, 3.2-4.8 months) and 4.7 kg (IQR, 4.1-5.6 kg), respectively. Right BCPS was performed in 26 patients and left BCPS was performed in 1 patient with situs inversus and a single left SVC. No patient after bilateral BCPS demonstrated failing BCPS, so there was no patient who underwent bilateral BCPS. The median CPB time was 69 minutes (IQR, 52-107 minutes), and aortic crossclamp was needed in 5 patients (19.2%) with a median duration of 18 minutes (IQR, 15-33 minutes). Intracardiac procedures included 11 PA reconstructions (including 6 out of 12 patients with left PA hypoplasia), 2 AVV repairs, 2 atrioseptectomies, (Blalock-Hanlon procedure), and 1 pulmonary valve closure. An autologous or xeno pericardium was used for PA reconstruction.
      Table 3Perioperative variables
      VariableResult
      No. of patients27
      Operative data
       Age at BCPS (mo)4.1 (3.2-4.8)
       Weight at BCPS (kg)4.7 (4.1-5.6)
       Type of BCPS
      Unilateral27 (100)
      Right BCPS26 (96.3)
      Left BCPS1 (3.7)
      Bilateral0 (0.0)
       CPB time (min)69 (52-107)
       Aortic crossclamp5 (18.5)
       Aortic crossclamp time (min)18 (15-33)
       Concomitant procedure
      PA reconstruction11 (40.7)
      AVV procedure2 (7.4)
      Atrioseptectomy2 (7.4)
      Pulmonary valve closure1 (3.7)
      Partial takedown
       On same day of BCPS3 (48.1)
      Concomitant with BCPS11 (40.7)
      Separately after BCPS2 (7.4)
       On separate day after BCPS14 (51.9)
       Interval after BCPS (d)19 (5-34)
       Shunt size (mm)
      3.04 (14.8)
      3.518 (66.7)
      4.03 (11.1)
      5.02 (7.4)
       Septation of central PA
      Clip16 (59.3)
      Ligation8 (29.6)
      Patch3 (11.1)
      Values are presented as n (%) or median (interquartile range). BCPS, Bidirectional cavopulmonary shunt; CPB, cardiopulmonary bypass; PA, pulmonary artery; AVV, atrioventricular valve.
      Partial takedown was performed either on the same day of BCPS in 13 patients or between postoperative days 1 and 64 in 14 patients (Table 1 and Figure 3). Among the 13 patients who underwent partial takedown on the same day as BCPS, there were 11 cases that were performed simultaneously with BCPS procedure, and 2 cases that were performed separately several hours after BCPS procedure. Notably, 11 of the 13 patients had previous Norwood procedure, and 9 patients demonstrated left PA hypoplasia (Tables 1 and 4). In 11 concomitant cases, systemic oxygen saturation after weaning from CPB and modified ultrafiltration varied between 40% and 60% even with nitric oxide inhalation therapy. An additional systemic-to-pulmonary shunt was constructed immediately. A new modified Blalock-Taussig shunt was placed in 4 patients, and the preexisting shunt was used in remaining 7 patients. Also, pulmonary septation was performed using a vascular clip (n = 6) or simple ligation (n = 3) or patch (n = 2) placed between the BCPS and the systemic-to-pulmonary shunt. Systemic oxygen saturation increased to 75% to 90%, and SVC pressure was acceptable (<20 mm Hg) after partial takedown in all patients. Another 2 patients underwent partial takedown as a separate operation. They demonstrated severe hypoxemia shortly after admission to intensive care unit, and were operated on again several hours later. A new, 3.5-mm modified Blalock-Taussig shunt was placed and septation was performed using a vascular clip in both cases. In the 13 patients who underwent partial takedown on the same day of BCPS, median stay in the intensive care unit was 7 days (IQR, 6-15 days), and all were successfully discharged from hospital a median of 18 days (IQR, 13-32 days) after partial takedown.
      Figure thumbnail gr3
      Figure 3Flow chart of the 27 patients who underwent partial takedown. BCPS, Bidirectional cavopulmonary shunt; IQR, interquartile range.
      Table 4Causes of hypoxemia and outcomes of partial takedown
      GroupnOutcomes
      ECMOThrombusHDLDFontanWaiting Fontan
      Partial takedown on the same day13000372
       LPA hypoplasia9000351
       High PVR/low SVC flow4000022
      Partial takedown on the different day149114433
       Early BCPS <90 d3120012
       Pulmonary venous obstruction2221100
       High PVR4342110
       TR and reduced VF1110100
       Mediastinitis and pneumonia3221110
       Pneumothorax1000001
      ECMO, Extracorporeal membrane oxygenation; HD, hospital death; LD, late death; LPA, left pulmonary artery; PVR, pulmonary vascular resistance; SVC, superior vena cava; BCPS, bidirectional cavopulmonary shunt; TR, tricuspid regurgitation; VF, ventricular function.
      The remaining 14 patients underwent partial takedown on a different day, and they had complicated postoperative courses. Postoperative data of these patients are shown in Tables 4 and 5. The interval between BCPS and partial takedown was a median of 19 days (IQR, 5-34 days). Median stay in intensive care unit was 45 days (IQR, 30-81 days) and median hospital stay was 59 days (IQR, 42-101 days). These patients had initial arterial oxygen saturation more than 70% but demonstrated progressive hypoxemia. All underwent postoperative cardiac catheterization at a median of 12 days (IQR, 2-19 days) after BCPS to confirm etiology of severe hypoxemia. The following causes of cyanosis were identified: early BCPS before 90 days with mild-to-moderate PA hypoplasia in 3 patients, PVO in 2 patients, post-BCPS high pulmonary vascular resistance in 4 patients, severe tricuspid valve regurgitation and systemic ventricular dysfunction in 1 patient, post-BCPS mediastinitis and pneumonia in 3 patients, and postoperative recurrent pneumothorax in 1 patient (Table 4). The postoperative causes in these patients are shown in Table E1.
      Table 5Postoperative data in 14 patients with separate partial takedown (PTD)
      VariableResult
      Timing of PTD
       Interval between BCPS and PTD (d)19 (5-34)
      Postoperative data
       ICU stay (d)45 (30-81)
       Hospital stay (d)59 (42-101)
       Hospital stay after PTD (d)38 (18-60)
      Possible causes of PTD
       High pulmonary vascular resistance4 (28.6)
       Early BCPS <90 d3 (21.4)
       Mediastinitis/pneumonia3 (21.4)
       Pulmonary venous obstruction2 (14.3)
       Systemic ventricular dysfunction1 (7.1)
       Repeat pneumothorax1 (7.1)
      Complications
       Reoperation with CPB
      Thrombectomy4 (28.6)
      BCPS pathway revision2 (14.3)
      AVV replacement1 (7.1)
      PV patch enlargement1 (7.1)
      Complete takedown1 (7.1)
       Reoperation without CPB
      Thoracic exploration2 (14.3)
      Pacemaker implantation1 (7.1)
      Diaphragm plication1 (7.1)
       Intervention
      Stent implantation in PA4 (28.6)
      v-v collateral coil closure3 (21.4)
      APCs coil closure1 (7.1)
       Complications
      Thrombus formation12 (85.7)
      Pleural effusion7 (50.0)
      Pneumothorax5 (35.7)
      Mediastinitis4 (28.6)
      Chylothorax3 (21.4)
       ECMO implantation9 (64.3)
      Values are presented as n (%) or median (interquartile range). BCPS, Bidirectional cavopulmonary shunt; ICU, intensive care unit; CPB, cardiopulmonary bypass; AVV, atrioventricular valve; PV, pulmonary vein; PA, pulmonary artery; v-v, veno-venous; APC, aorto pulmonary collaterals; ECMO, extracorporeal membrane oxygenation.
      There were 4 hospital deaths before discharge, and the cause of deaths was considered as 2 high pulmonary vascular resistance, 1 PVO, and 1 mediastinitis/pneumonia. As morbidity, a thrombus formation was detected in 11 of 14 patients (78.6%). Six out of 11 patients developed thrombus between initial BCPS and partial takedown, and the remaining 5 patients developed thrombus after partial takedown. Thrombolysis was done in all patients and operative removal of thrombus was performed in 5 patients. Of the 5 patients who required surgical removal of thrombosis, thrombus was located in SVC to PA in 4 patients and in right atrium in 1 patient. ECMO therapy was needed in 9 of 14 (64.3%) patients. ECMO was needed before partial takedown in 6 patients. One patient successfully weaned from ECMO before partial takedown and 3 weaned from ECMO at the time of partial takedown. ECMO support was needed after partial takedown in the remaining 3 patients. Median duration of ECMO support was 10 days (IQR, 5-19 days; minimum, 4 days; and maximum, 43 days).
      Development of the left PA was evaluated in 24 patients who underwent postpartial takedown cardiac catheterization at the median of 5.9 months (IQR, 1.4-15.1 months) after partial takedown (Table E2). Left PA index was significantly increased (from 79 ± 58 to 104 ± 77 mm2/m2; P < .001). Of the 12 patients with left PA hypoplasia, we had an angiogram after partial takedown in 11 patients. Their left PA index also increased (from 43 ± 21 to 54 ± 20 mm2/m2; P = .159), but was not statistically significant.

      Follow-up Outcomes

      For the 23 hospital survivors, the median follow-up time after partial takedown was 2.0 years (IQR, 0.7-5.9 years). There were 7 late deaths (interstage mortality between discharge after partial takedown and before Fontan completion) on 61, 73, 96, 181, 599, 720, and 967 days after partial takedown. HLHS and its variant were the cause of death in 6 patients. The causes of deaths were ventricular dysfunction in 5 patients, progressive PVO in 1 patient, and hypoxia due to high pulmonary vascular resistance in 1 patient. The remaining 16 patients were alive at a median of 5.0 years (IQR, 1.2-8.3 years) after partial takedown, 10 patients underwent Fontan procedure at the median age of 1.9 years (IQR, 1.4-5.1 years) and median interval of 1.7 years (IQR, 1.1-4.8 years) after partial takedown. Total cavopulmonary connection before cardiac catheterization (pre-TCPC) data are shown in Table E3. There were no deaths after Fontan completion at a median follow-up period of 5.8 years (IQR, 2.0-10.6 years). The remaining 6 patients were waiting for Fontan completion. Overall survival after partial takedown was 69% at 1 year and 54% at 3 years (Figure 4).
      Figure thumbnail gr4
      Figure 4Transplant-free survival in patients after partial takedown. Kaplan-Meier estimate for freedom from death or transplantation after the partial takedown showed 53.5% survival at 3 years follow-up: The mean follow-up after the partial takedown was 1.8 days (interquartile range, 0.3-5.6 days). CI is 95%.
      As for the surgical intervention for AVV regurgitation, 5 patients underwent AVV repair (3 tricuspid valve repair concomitant with BCPS, 1 mitral valve repair 524 days after partial takedown, and 1 tricuspid valve repair concomitant with TCPC). One patient, who needed tricuspid valve replacement after tricuspid valve repair concomitant with BCPS, died as a result of ventricular dysfunction. The remaining 4 patients survived without significant AVV regurgitation.

      Risk Factor Analysis for Mortality after Partial Takedown

      Unbalanced atrioventricular septal defect (hazard ratio [HR], 4.913; P = .026), genetic/extracardiac anomalies (HR, 3.083; P = .066), and PVO (HR, 10.982; P = .019) showed P values < .1 for deaths after partial takedown (Table E4). Methods of PA interruption had no influence on outcomes.

      Discussion

      Summary of the Results

      The current study was undertaken to determine whether or not partial takedown was a reasonable procedure in 27 failing BCPS patients. The causes for partial takedown were: 10 left PA hypoplasia, 7 low SVC flow/high pulmonary vascular resistance, 3 early BCPS, 3 mediastinitis/pneumonia, 2 PVO, 1 pneumothorax, and 1 severe ventricular dysfunction. There were 4 hospital deaths and 7 interstage deaths. Survival at 3 years was 54%. Fontan completion was possible in 10 patients (Figure 1, Video 1, and Online Data Supplement).

      Potential Therapeutic Options for Prohibitive Cyanosis after BCPS without Pathway Obstruction

      In general, BCPS has a relatively low early mortality rate with survival to Fontan operation.
      • Ono M.
      • Burri M.
      • Mayr B.
      • Anderl L.
      • Strbad M.
      • Cleuziou J.
      • et al.
      Risk factors for failed Fontan procedure following stage 2 palliation.
      ,
      • Scheurer M.A.
      • Hill E.G.
      • Vasuki N.
      • Maurer S.
      • Graham E.M.
      • Bandisode V.
      • et al.
      Survival after bidirectional cavopulmonary anastomosis: analysis of preoperative risk factors.
      • Alsoufi B.
      • Manlhiot C.
      • Awan A.
      • Alfadley F.
      • Al-Ahmadi M.
      • Al-Wadei A.
      • et al.
      Current outcomes of the Glenn bidirectional cavopulmonary connection for single ventricle palliation.
      • Tanoue Y.
      • Kado H.
      • Boku N.
      • Tatewaki H.
      • Nakano T.
      • Fukae K.
      • et al.
      Three hundred and thirty-three experiences with the bidirectional Glenn procedure in a single institute. Interact.
      Nevertheless, certain patients develop significant hypoxemia and inadequate physiology after the procedure, even when the BCPS pathway is unobstructed. To rescue such patients, potential treatment options other than heart transplantation are complete takedown and partial takedown. Patients requiring complete takedown may be among the candidates at greatest risk for stage II palliation for single-ventricle anatomy. The mortality associated with complete takedown is high.
      • Luo S.
      • Haranal M.
      • Deng M.X.
      • Varenbut J.
      • Runeckles K.
      • Steve Fan C.P.
      • et al.
      Low preoperative superior vena cava blood flow predicts bidirectional cavopulmonary shunt failure.
      ,
      • Alejos J.C.
      • Williams R.G.
      • Jarmakani J.M.
      • Galindo A.J.
      • Isabel-Jones J.B.
      • Drinkwater D.
      • et al.
      Factors influencing survival in patients undergoing the bidirectional Glenn anastomosis.
      ,
      • Cleveland J.D.
      • Tran S.
      • Takao C.
      • Wells W.J.
      • Starnes V.A.
      • Kumar S.R.
      Need for pulmonary arterioplasty during Glenn independently predicts inferior surgical outcome.
      The concept of an additional aortopulmonary shunt to the targeted lung was reported by Sakamoto and colleagues in 2007.
      • Sakamoto K.
      • Ikai A.
      • Fujimoto Y.
      • Ota N.
      Novel surgical approach ‘intrapulmonary-artery septation' for Fontan candidates with unilateral pulmonary arterial hypoplasia or pulmonary venous obstruction.
      They named this procedure intrapulmonary-artery septation and performed it in 20 patients with severe unbalanced PAs. Subsequently, they reported the efficacy of this technique in both unilateral PA hypoplasia
      • Tachi M.
      • Murata M.
      • Ide Y.
      • Ito H.
      • Kanno K.
      • Imai K.
      • et al.
      Efficacy of the ‘intrapulmonary-artery septation' surgical approach for Fontan candidates with unilateral pulmonary arterial hypoplasia.
      and pulmonary vein obstruction.
      • Ishidou M.
      • Ota K.
      • Watanebe K.
      • Koshiyama H.
      • Kanno K.
      • Ito H.
      • et al.
      Impact of intrapulmonary-artery septation to pulmonary vein obstruction for two-lung Fontan.
      In 2018, Casella and colleagues
      • Casella S.L.
      • Kaza A.
      • Del Nido P.
      • Lock J.E.
      • Marshall A.C.
      Targeted increase in pulmonary blood flow in a bidirectional Glenn circulation.
      demonstrated the targeted increase of pulmonary blood flow at BCPS, and performed unilateral Glenn shunt, a systemic-to-pulmonary shunt in the contralateral lung, and a narrow banding between Glenn and systemic-to-pulmonary shunt in 20 patients with unilateral pulmonary vascular abnormalities. Recently, Turkoz and Dogan
      • Türköz R.
      • Doğan A.
      Management for bidirectional cavopulmonary shunt failure: adding aortopulmonary shunt without takedown.
      reported 2 patients who underwent additional aortopulmonary shunt immediately after the BCPS procedure. In both cases, an aortopulmonary shunt was placed to the left lung and tight central pulmonary artery banding was performed between the BCPS and the aortopulmonary shunt. Our concept is nearly the same as this report. Although the reasons for performing partial takedown are different in this study, the rationale for partial takedown are the same: A unilateral Glenn shunt should be established; an additional customized aortopulmonary shunt may increase contralateral pulmonary blood flow to increase oxygen saturation. A complete septation of the central PA prevents SVC syndrome and provides adequate driving pressure to the affected PA. In this study, growth of affected PA was observed after partial takedown.

      Surgical Options: Complete Takedown or Partial Takedown

      We realized that the lack of a comparison group is a weakness of this study. In the study period, only 1 patient underwent complete takedown, and died 2 months postoperatively (mortality of 100%). In the literature, there are relatively scant descriptions of survival after complete takedown. Luo and colleagues
      • Luo S.
      • Haranal M.
      • Deng M.X.
      • Varenbut J.
      • Runeckles K.
      • Steve Fan C.P.
      • et al.
      Low preoperative superior vena cava blood flow predicts bidirectional cavopulmonary shunt failure.
      showed that 5 out of 7 (71.4%) patients died after complete takedown. Greenberg and colleagues demonstrated that 4 out of 6 (66.6%) patients died (n = 3) or needed heart transplantation (n = 1) after complete takedown.
      • Greenberg J.W.
      • Pribble C.M.
      • Singareddy A.
      • Ta N.A.
      • Sescleifer A.M.
      • Fiore A.C.
      • et al.
      The failed bidirectional Glenn shunt: risk factors for poor outcomes and the role of early reoperation.
      We know that complete takedown is associated with substantial mortality, usually more than 50%. Additionally, we performed a total of 572 staged Fontan procedure between 1994 and 2021. There was no patient who experienced previous BCPS complete takedown. In the literature, we could not find a report where a successful Fontan procedure after BCPS complete takedown was described. Therefore, it can be said that partial takedown may be better tolerable than complete takedown and could keep good Fontan candidacy.
      Our current determining criteria for a partial or complete takedown are as following: partial takedown is the first choice if unilateral Glenn shunt could be maintained. In these cases, additional systemic-to-pulmonary shunt improves hypoxemia, and partial takedown would be tolerable. Whereas complete takedown is indicated if the unilateral Glenn circulation could not be maintained, due to too high pulmonary vascular resistance, too-low SVC flow, or existence of PVO at Glenn side. Another option is the placement of larger systemic-to-pulmonary shunt and aggressive PA reconstruction. In patients with dominant left ventricle (such as tricuspid atresia or double inlet left ventricle) and good systemic ventricular function, this strategy might be the method of choice. However, in patients with dominant right ventricle, partial takedown might be indicated rather than upsizing the shunt. In contrast to complete takedown, partial takedown remains a step toward TCPC. All of our patients directly underwent TCPC following partial takedown without any additional procedure. In this study, 10 patients underwent Fontan palliation at a median of 1.7 years after partial takedown, and central PA could be reconstructed concomitantly in all patients.

      Technical Aspect of Partial Takedown

      After placement of an additional aortopulmonary shunt, whether or not to band or to septate the central PA is a great concern. When central PA is banded, a relatively small aortopulmonary shunt should be used as a protective measure against increased pressures in the Glenn pathway.
      • Casella S.L.
      • Kaza A.
      • Del Nido P.
      • Lock J.E.
      • Marshall A.C.
      Targeted increase in pulmonary blood flow in a bidirectional Glenn circulation.
      When central PA is interrupted, the unilateral Glenn works without any additional driving force.
      • Sakamoto K.
      • Ikai A.
      • Fujimoto Y.
      • Ota N.
      Novel surgical approach ‘intrapulmonary-artery septation' for Fontan candidates with unilateral pulmonary arterial hypoplasia or pulmonary venous obstruction.
      A relatively large shunt can be placed to the affected lung. Either banding or septation is performed, this strategy might help patients with inadequate SVC flow to achieve reasonable saturation by providing an additional source of pulmonary blood flow.
      • Alghamdi A.A.
      Bidirectional Glenn with additional pulmonary blood flow: systematic review and evidence-based recommendations.
      The trade-off is an increased volume load on the systemic ventricle. However, apparent negative effects on systemic ventricular function were not observed in this study. Second concern is the shunt size. In this study, a 3.5-mm shunt was most commonly used. When central PA is interrupted, the shunt size can be chosen for the requirements of the affected PA. The amount of aortopulmonary collaterals flow to the affected lung, pulmonary vascular resistance, and size of the PA might be the decision-making components. As for interruption method, it was surgeon's preference and it did not affect the outcomes. Actually, we prefer to use clip because of the technical simplicity. As for the ECMO support, we used ECMO support as a bridge to weaning the decision for partial takedown in 6 out of 14 patients who underwent partial takedown on a separate day. For the remaining 8 patients, we decided directly to perform partial takedown without previous ECMO support.

      Etiology and Prognosis after Partial Takedown

      There might be several etiologies of severe cyanosis after BCPS without pathway obstruction. One main reason is the left PA hypoplasia. In the present study, 12 patients had left PA hypoplasia, which is a good indication for partial takedown. In patients with unilateral PA hypoplasia, shunt renewal (size-up) with extensive PA reconstruction is an alternative to perform early BCPS. In early era, we adopted this strategy. However, as the results of improved Norwood procedure and HLHS became the main diagnosis, we introduced early staged Fontan completion strategy because right ventricle failure and significant tricuspid regurgitation developed frequently after placement of a larger shunt. Younger age at BCPS is also a reason to demonstrate failing BCPS physiology. Patients who demonstrated mildly elevated pulmonary pressure are also good candidates for partial takedown. However, this approach does not seem to be effective in patients with PVO. The optimal treatment for patients with PVO remains unclear, and mortality remains high even after partial takedown. Genetic/extracardiac abnormalities were identified as another risk factor. In these patients, intrinsic pulmonary vascular disease associated with disorders might influence the BCPS physiology and postoperative outcome. Furthermore, we had patients who demonstrated mediastinitis/pneumonia after BCPS. These patients developed increased pulmonary vascular resistance and/or pulmonary venous desaturation. Another reason is low cardiac output due to ventricular dysfunction. We had 1 patient who required AVV replacement after BCPS and demonstrated severe systemic ventricular dysfunction.
      When unilateral (usually right side) Glenn circulation can be maintained without SVC syndrome and an additional antegrade pulmonary blood flow in the contralateral (usually left) lung can increase the total pulmonary blood flow, partial takedown improves arterial oxygen saturation and rescues failing BCPS. If unilateral Glenn shunt could not be established due to too high pulmonary vascular resistance, SVC pressure remains high after partial takedown, and partial takedown could not rescue this situation. In this study, this was the case in patients with severe pulmonary vascular diseases with a genetic syndrome, patients with PVO, or patients with severe pneumonia. Complete takedown might be an alternative for these patients. If unilateral Glenn shunt could not establish due to too low SVC flow, partial takedown could not rescue this situation. In this study, this was the case in patients with severe AVV regurgitation and ventricular dysfunction. For these patients, heart transplantation or a new therapy such as assisted bidirectional Glenn may be more appropriate.
      • Esmaily-Moghadam M.
      • Hsia T.Y.
      • Marsden A.L.
      Modeling of Congenital Hearts Alliance (MOCHA) Investigators. The assisted bidirectional Glenn: a novel surgical approach for first-stage single-ventricle heart palliation.
      The reasons why postoperative management was so complicated in patients who underwent partial takedown on a separate day are that patients' hemodynamic parameters, such as PAP, arterial oxygen saturation, and systemic arterial pressure, consistently changed during the postoperative days. It is not easy to decide whether or not BCPS hemodynamic parameters are established or not, and when partial takedown should be performed. Certain patients demonstrated relatively low arterial oxygen saturation during the early postoperative phase, and gradually increased their arterial oxygen saturation spontaneously. Effects of ECMO support and thrombus formation are also factors influencing the postoperative course. We routinely perform pulmonary angiography through central venous catheter on postoperative day 2 or 3 to rule out the technical problem (BCPS pathway obstruction). Therefore, it is still difficult to define the clear indication and management strategy of partial takedown. Further experiences and studies with large scale cohort are necessary to establish better management strategies for the treatment of failing BCPS patients.
      In this study, patients who underwent immediate partial takedown showed better hospital survival. However, the reasons to perform partial takedown in late partial takedown group were different, so we cannot simply say that early timing to perform partial takedown is better.

      Study Limitations

      This study was limited by its retrospective, observational, and single-center design. This study was also limited by the heterogeneity of the patient cohort. Partial takedown was performed in different period after the initial BCPS. The indication for partial takedown was also different from patient to patient. Despite all efforts to conduct a large retrospective study, this study has inevitable limitations of small cohort size, no comparative group, and descriptive nature. Lack of any acceptable control group is also a significant limitation. No patients underwent complete takedown and so it is impossible to evaluate the merits or problems associated with this strategy. Another limitation was a lack of a quantifiable measurement of pulmonary blood flow. Given the recent application of this procedure, there was variable utilization of magnetic resonance imaging flow data pre- and postoperatively. Furthermore, certain patients underwent concomitant procedures on the primary vascular anomaly during preoperative catheterization and at the time of the operation, which inherently influences the outcome of this intervention. Because of the small size of cohort, results should be interpreted cautiously as only large effects could be identified. Finally, the follow-up period was not long enough to delineate the outcome after Fontan completion.

      Conclusions

      In 27 patients showing severe hypoxemia after BCPS without any stenosis at the BCPS anastomosis, partial takedown was performed to rescue the patients. There were 4 early and 7 late mortalities, and the 3-year survival was 54%. However, 10 patients underwent Fontan completion without postoperative mortality, and 6 patients were waiting for Fontan completion. Our results are encouraging in this inherently high-risk population. Future stratification of patients with intrinsic pulmonary vascular pathology and sophistication of operative and postoperative management might improve outcomes as we continue to investigate this procedure.

      Conflict of Interest Statement

      The authors reported no conflicts of interest.
      The Journal policy requires editors and reviewers to disclose conflicts of interest and to decline handling or reviewing manuscripts for which they may have a conflict of interest. The editors and reviewers of this article have no conflicts of interest.

      Supplementary Data

      Appendix E1

      Figure thumbnail fx4
      Figure E1Pulmonary artery angiogram demonstrating left pulmonary artery stenosis before bidirectional cavopulmonary shunt.
      Table E1Postoperative outcome after partial takedown (PTD)
      Patient No.DiagnosisICU stayHospital stayHospital after PTDECMOThrombusChylothoraxSVC syndromeReoperationTCPCAge at TCPCInterval after PTDOutcomeFollow-upStatus
      1HLHS615150001113.53.1Alive14.0fTCPC
      2DILV, TGA, IAA616160000010.90.5Alive12.5fTCPC
      3HLHS132020000010LD0.5
      4DORV, MS424242000010LD0.3
      5TA Ib618180000011.51.4Alive9.9TCPC
      6HLHS122929000000Alive4.5Waiting
      7HLHS163030000000LD2.0
      8HLHS1638380000011.91.7Alive8.9TCPC
      9DORV, MA716160000014.34.0Alive5.4TCPC
      10HLHS, TAPVC21010000000Alive0.7waiting
      11HLHS73434001000Alive0.7waiting
      12HLHS711110000015.95.8Alive5.9fTCPC
      13DIRV, TGA, PA611110000012.32.0Alive2.1TCPC
      14HLHS, PAPVC4444431SVC, PA, PV0110LD0.2
      15UAVSD, TGA, PA1611611581SVC0110HD0.4.
      16HLHS1616121PA0010HD0.0
      17HLHS321181131SVC1010Alive6.6Waiting
      18HLHS, TAPVC152516000000Alive0.0Waiting
      19UAVSD2543300Aorta0000LD1.6
      20HLHS7575581SVC0010LD0.2.
      21PAIVS, Ebstein4040191000115.95.5Alive5.6TCPC
      22UAVSD, DORV, PS6363401RA0000HD0.1.
      23TA Ia3955261PA11011.30.8Alive1.0fTCPC
      24TA Ib76100670SVC00111.81.5Alive1.8fTCPC
      25ccTGA, TA, IAA4646111SVC0010HD0.0.
      26TA Ic979735000000Alive1.9Waiting
      27HLHS105105420Aorta0010LD2.6
      ICU, Intensive care unit; ECMO, extracorporeal membrane oxygenation; SVC, superior vena cava; TCPC, total cavopulmonary connection; HLHS, hypoplastic left heart syndrome; fTCPC, fenestrated total cavopulmonary connection; DILV, double inlet left ventricle; TGA, transposition of the great arteries; IAA, interruption of the aorta; LD, late death; DORV, double outlet right ventricle; MS, multiple sclerosis; TA, tricuspid atresia; MA, mitral atresia; TAPVC, total anomalous pulmonary venous connection; DIRV, double inlet right ventricle; PA, pulmonary artery; PAPVC, partial anomalous pulmonary venous connection; UAVSD, unbalanced atrioventricular septal defect; PAIVS, pulmonary atresia with in intact ventricular septum; Ebstein, Ebstein anomaly; PS, pulmonary stenosis; TA, tricuspid atresia; ccTGA, congenitally corrected transposition of the great arteries.
      Table E2Characteristics of patients with regurging pulmonary arteries (PA)
      Patient No.DiagnosisStage I palliationShunt sizePA hypoplasiaLPA index pre BCPSBCPS age (mon)Shunt reoperationLPA index after PTDTCPCAge at TCPCInterval after PTD
      1HLHSNorwood5.0LPA (2.6 mm)385.0CS 4.03513.53.1
      2DILV, TGA, IAANorwood4.0LPA (3.2 mm)433.75310.90.5
      3HLHSNorwood5.0LPA (2.5 mm)275.1BT 5.0380
      4DORV, MSNorwood3.5LPA (1.2 mm)313.8BT 5.0700
      5TA Ibno2792.227111.51.4
      6HLHSNorwood3.0LPA (1.5 mm)124.6300
      7HLHSNorwood3.5LPA (1.9 mm)354.7.0
      8HLHSNorwood3.0763.18111.91.7
      9DORV, MANorwood3.5LPA (3.0 mm)294.27114.34.0
      10HLHS, TAPVCNorwood3.5865.11110
      11HLHSNorwood3.5863.6780
      12HLHSNorwood3.5LPA (2.0 mm)351.82815.95.8
      13DIRV, TGA PAPDA stent4.0LPA (3.5 mm)443.48812.32.0
      14HLHS, PAPVCNorwood3.5533.4750
      15UAVSD, TGA, PAPDA stent3.51487.53370
      16HLHSNorwood3.5664.5860
      17HLHSNorwood3.5LPA (3.0 mm)522.7BT 5.0
      Concomitant with pulmonary artery reconstruction.
      480
      18HLHS, TAPVCNorwood3.5852.8.0
      19UAVSDPAB33612.8.0
      20HLHSNorwood5.0824.3940
      21PAIVS, EbsteinMBTS3.5984.1CS 4.017015.95.5
      22UAVSD, DORV, PSMBTS3.51843.22180
      23TA IaPDA stent4.0LPA (2.7 mm)885.27411.30.8
      24TA IbPDA stent3.5662.914111.81.5
      25ccTGA, TA, IAANorwood3.5LPA (2.6 mm)724.1610
      26TA IcMBTS3.51074.11450
      27HLHSNorwood5.0863.5870
      LPA, Left pulmonary artery; BCPS, bidirectional cavopulmonary shunt; PTD, partial takedown; TCPC, total cavopulmonary connection; HLHS, hypoplastic left heart syndrome; CS, central shunt; DILV, double inlet left ventricle; TGA, transposition of the great arteries; IAA, interruption of the aorta; BT, Blalock-Taussig shunt; DORV, double outlet right ventricle; MS, multiple sclerosis; TA, tricuspid atresia; MA, mitral atresia; TAPVC, total anomalous pulmonary venous connection; DIRV, double inlet right ventricle; PAPVC, partial anomalous pulmonary venous connection; UAVSD, unbalanced atrioventricular septal defect; PDA, patent ductus arteriosus; PAB, pulmonary artery banding; PAIVS, pulmonary atresia with in intact ventricular septum; Ebstein, Ebstein anomaly; PS, pulmonary stenosis; MBTS, modified Blalock-Taussig shunt; ccTGA, congenitally corrected transposition of the great arteries.
      Concomitant with pulmonary artery reconstruction.
      Table E3Total cavopulmonary connection (TCPC) before catheterization and echocardiographic data (n = 10)
      VariableResult
      Catheterization data
       Hemoglobin (g/dL)16.0 ± 15
       Mean right pulmonary artery pressure (mm Hg)10.5 ± 2.7
       Mean left pulmonary artery pressure (mm Hg)10.0 ± 1.9
       Mean left atrial pressure (mm Hg)5.2 ± 1.5
       Transpulmonary gradient (mm Hg)5.2 ± 2.1
       Systolic ventricular pressure (mm Hg)83.7 ± 12.1
       Ventricular endo-diastolic pressure (mm Hg)7.2 ± 1.7
       Aortic oxygen saturation (%)80.9 ± 5.3
      Echocardiographic data
       Ventricular function
      Normal10 (100.0)
      Mildly impaired0 (0.0)
      Moderately impaired0 (0.0)
       Atrioventricular valve regurgitation
      None1 (10.0)
      Trivial4 (40.0)
      Mild5 (50.0)
      Moderate0 (0.0)
      Severe0 (0.0)
       (Neo) aortic insufficiency
      None8 (80.0)
      Trivíal Trivial2 (20.0)
      Mild0 (0.0)
      Values are presented as n (%) or mean ± SD.
      Table E4Variables influencing survival after partial takedown
      VariableUnivariate model
      P valueHazard ratio (95% CI)
      HLHS.8711.104 (0.3-3.6)
      UAVSD.0264.913 (1.2-19.9)
      Genetic/extracardiac anomaly.0663.083 (0.9-10.2)
      Norwood procedure as stage I.6261.395 (0.4-5.3)
      PAP.2711.092 (0.9-1.3)
      PAP >15 mm Hg.1802.850 (0.6-13.2)
      PVO.01910.982 (1.5-81.3)
      CI, Confidence interval; HLHS, hypoplastic left heart syndrome, UAVSD, unbalanced atrioventricular septal defect, PAP, pulmonary artery pressure, PVO, pulmonary venous obstruction.

      References

        • Ono M.
        • Burri M.
        • Mayr B.
        • Anderl L.
        • Strbad M.
        • Cleuziou J.
        • et al.
        Risk factors for failed Fontan procedure following stage 2 palliation.
        Ann Thorac Surg. 2021; 112: 610-618
        • Ono M.
        • Kido T.
        • Burri M.
        • Anderl L.
        • Ruf B.
        • Cleuziou J.
        • et al.
        Risk factors for thrombus formation at stage 2 palliation and its effect on long-term outcome in patients with univentricular heart.
        Semin Thorac Cardiovasc Surg. 2022; 34: 669-679
        • Kido T.
        • Ono M.
        • Anderl L.
        • Burri M.
        • Strbad M.
        • Balling G.
        • et al.
        Factors influencing length of intensive care unit stay following a bidirectional cavopulmonary shunt.
        Interact Cardiovasc Thorac Surg. 2021; 33: 124-130
        • Lee T.M.
        • Aiyagari R.
        • Hirsch J.C.
        • Ohye R.G.
        • Bove E.L.
        • Devaney E.J.
        Risk factor analysis for second-stage palliation of single ventricle anatomy.
        Ann Thorac Surg. 2012; 93: 614-618
        • Tan A.M.
        Fontan completion rate and outcomes after bidirectional cavo-pulmonary shunt.
        Eur J Cardiothorac Surg. 2010; 38: 59-65
        • Freedom R.M.
        • Nykanen D.
        • Benson L.N.
        The physiology of the bidirectional cavopulmonary connection.
        Ann Thorac Surg. 1998; 66: 664-667
        • Kido T.
        • Euringer C.
        • Burri M.
        • Vodiskar J.
        • Strbad M.
        • Cleuziou J.
        • et al.
        Impact of hypoxemia and re-interventions on clinical outcomes after bidirectional cavopulmonary shunt.
        Eur J Cardiothorac Surg. April 22, 2022; ([Epub ahead of print])https://doi.org/10.1093/ejcts/ezac266
        • Zampi J.D.
        • Hirsch-Romano J.C.
        • Armstrong A.K.
        Early cyanosis after stage II palliation for single ventricle physiology: etiologies and outcomes.
        World J Pediatr Congenit Heart Surg. 2013; 4: 367-372
        • Luo S.
        • Haranal M.
        • Deng M.X.
        • Varenbut J.
        • Runeckles K.
        • Steve Fan C.P.
        • et al.
        Low preoperative superior vena cava blood flow predicts bidirectional cavopulmonary shunt failure.
        J Thorac Cardiovasc Surg. 2020; 160: 1529-1540
        • Ono M.
        • Cleuziou J.
        • Pabst von Ohain J.
        • Beran E.
        • Burri M.
        • Strabad M.
        • et al.
        Atrioventricular valve regurgitation in patients undergoing total cavopulmonary connection: impact of valve morphology and underlying mechanisms on survival and reintervention.
        J Thorac Cardiovasc Surg. 2018; 155: 701-709
        • Schreiber C.
        • Cleuziou J.
        • Cornelsen J.K.
        • Hörer J.
        • Eicken A.
        • Lange R.
        Bidirectional cavopulmonary connection without additional pulmonary blood flow as an ideal staging for functional univentricular hearts.
        Eur J Cardiothorac Surg. 2008; 34: 550-554
        • Scheurer M.A.
        • Hill E.G.
        • Vasuki N.
        • Maurer S.
        • Graham E.M.
        • Bandisode V.
        • et al.
        Survival after bidirectional cavopulmonary anastomosis: analysis of preoperative risk factors.
        J Thorac Cardiovasc Surg. 2007; 134: 82-89
        • Alsoufi B.
        • Manlhiot C.
        • Awan A.
        • Alfadley F.
        • Al-Ahmadi M.
        • Al-Wadei A.
        • et al.
        Current outcomes of the Glenn bidirectional cavopulmonary connection for single ventricle palliation.
        Eur J Cardiothorac Surg. 2012; 42: 42-48
        • Tanoue Y.
        • Kado H.
        • Boku N.
        • Tatewaki H.
        • Nakano T.
        • Fukae K.
        • et al.
        Three hundred and thirty-three experiences with the bidirectional Glenn procedure in a single institute. Interact.
        Cardiovasc Thorac Surg. 2007; 6: 97-101
        • Alejos J.C.
        • Williams R.G.
        • Jarmakani J.M.
        • Galindo A.J.
        • Isabel-Jones J.B.
        • Drinkwater D.
        • et al.
        Factors influencing survival in patients undergoing the bidirectional Glenn anastomosis.
        Am J Cardiol. 1995; 75: 1048-1050
        • Cleveland J.D.
        • Tran S.
        • Takao C.
        • Wells W.J.
        • Starnes V.A.
        • Kumar S.R.
        Need for pulmonary arterioplasty during Glenn independently predicts inferior surgical outcome.
        Ann Thorac Surg. 2018; 106: 156-164
        • Sakamoto K.
        • Ikai A.
        • Fujimoto Y.
        • Ota N.
        Novel surgical approach ‘intrapulmonary-artery septation' for Fontan candidates with unilateral pulmonary arterial hypoplasia or pulmonary venous obstruction.
        Interact Cardiovasc Thorac Surg. 2007; 6: 150-154
        • Tachi M.
        • Murata M.
        • Ide Y.
        • Ito H.
        • Kanno K.
        • Imai K.
        • et al.
        Efficacy of the ‘intrapulmonary-artery septation' surgical approach for Fontan candidates with unilateral pulmonary arterial hypoplasia.
        Eur J Cardiothorac Surg. 2016; 49: 183-187
        • Ishidou M.
        • Ota K.
        • Watanebe K.
        • Koshiyama H.
        • Kanno K.
        • Ito H.
        • et al.
        Impact of intrapulmonary-artery septation to pulmonary vein obstruction for two-lung Fontan.
        Eur J Cardiothorac Surg. 2020; 58: 177-185
        • Casella S.L.
        • Kaza A.
        • Del Nido P.
        • Lock J.E.
        • Marshall A.C.
        Targeted increase in pulmonary blood flow in a bidirectional Glenn circulation.
        Semin Thorac Cardiovasc Surg. 2018; 30: 182-188
        • Türköz R.
        • Doğan A.
        Management for bidirectional cavopulmonary shunt failure: adding aortopulmonary shunt without takedown.
        J Thorac Cardiovasc Surg. 2021; 161: e321-e322
        • Greenberg J.W.
        • Pribble C.M.
        • Singareddy A.
        • Ta N.A.
        • Sescleifer A.M.
        • Fiore A.C.
        • et al.
        The failed bidirectional Glenn shunt: risk factors for poor outcomes and the role of early reoperation.
        World J Pediatr Congenit Heart Surg. 2021; 12: 760-764
        • Alghamdi A.A.
        Bidirectional Glenn with additional pulmonary blood flow: systematic review and evidence-based recommendations.
        J Card Surg. 2015; 30: 724-730
        • Esmaily-Moghadam M.
        • Hsia T.Y.
        • Marsden A.L.
        Modeling of Congenital Hearts Alliance (MOCHA) Investigators. The assisted bidirectional Glenn: a novel surgical approach for first-stage single-ventricle heart palliation.
        J Thorac Cardiovasc Surg. 2015; 149: 699-705