Pericardial tunnel technique in the surgical management of the vertical form of scimitar syndrome

Pericardial tunnel technique in the surgical management of the vertical form of scimitar syndrome Abstract OBJECTIVES To optimize the surgical strategy and individualized treatment for scimitar syndrome (SS) by summarizing the clinical outcomes of the pericardial tunnel technique for the vertical form of SS at a single centre. METHODS The vertical form was defined as an angle of scimitar vein (SV) insertion to the inferior vena cava (θ) ≤ 45°, whereas the horizontal form was defined as θ > 45°. Nine patients with vertical form were operated on from June 2011 to June 2017. The mean age of patients during surgery was 3.1 ± 3.63 (range 0.3–12) years. Five patients were with infantile form and 4 with childhood/adult form per Dupuis’ classification. The pericardial tunnel technique entailed attaching the SV to the right lateral pericardium and directing blood flow to the left atrium through a left atriotomy inside the pericardial tunnel. All patients had associated intracardiac anomalies repaired concomitantly; 3 patients had major collateral arteries occluded or ligated. RESULTS There was no in-hospital postoperative death or residual SV obstruction. The postoperative ventilation time was 88.3 ± 63.8 (range 36–264) h. Eight survivors were followed up for 33.4 ± 19.2 (range 2–72) months, with 1 lost to follow-up. Echocardiography demonstrated that 7 survivors had no pulmonary hypertension and 1 had mild pulmonary hypertension; none developed SV obstruction during the follow-ups. CONCLUSIONS The pericardial tunnel technique is suitable for the vertical form of SS and is a reasonable option for individualized treatment of SS. Scimitar syndrome , Congenital heart disease , Surgery , Complication INTRODUCTION Scimitar syndrome (SS) is a rare, complex congenital heart anomaly affecting approximately 0.06% of patients with congenital heart diseases, and its incidence is higher in females [1]. The major feature of SS is that all or partial right pulmonary veins drain into the inferior vena cava (IVC) through an anomalous right pulmonary vein. The morphology of this vein resembles a Turkish sabre; thus, it is termed scimitar vein (SV). SS is often associated with varying degrees of hypoplasia of the right lung and ipsilateral branch pulmonary artery, dextroposition of the heart and the right upper or middle lobe supplied by anomalous collateral arteries from the thoracic or abdominal aorta. On the basis of the clinical presentations by age, Dupuis et al. [2, 3] classified SS into 2 forms: infantile and childhood/adult. Patients with infantile form are younger than 1 year and always present with cardiac dysfunction, dyspnoea and recurrent respiratory infection. Patients with childhood/adult form are older than 1 year and presented with recurrent respiratory infection with relatively good heart function. Mild cases of SS have no obvious clinical symptoms. We found that certain SVs had different angulations on the insertion into the IVC, which we termed the ‘vertical’ and ‘horizontal’ forms. Thus, based on this unique anatomical feature of the SV, the traditional surgical technique should be modified. We summarized our experience on the pericardial tunnel technique for the vertical form of SS at our centre. PATIENTS AND METHODS Patient characteristics A total of 9 patients with SS underwent surgical repair using the pericardial tunnel technique at our centre from June 2011 to June 2017. The angle of the SV insertion to the IVC (θ) was measured. The vertical form of SS was defined as θ ≤ 45°, whereas the horizontal form was defined as θ > 45° (Fig. 1). All 9 patients in this cohort had vertical form (Fig. 2A–I). In the same timeframe, there were 5 patients with horizontal form that was repaired using another surgical technique and were excluded from this study. Figure 1: View largeDownload slide Definition of horizontal and vertical forms of scimitar vein. (A) Horizontal form with θ > 45° and (B) vertical form with θ ≤ 45°. Figure 1: View largeDownload slide Definition of horizontal and vertical forms of scimitar vein. (A) Horizontal form with θ > 45° and (B) vertical form with θ ≤ 45°. Figure 2: View largeDownload slide The preoperative scimitar vein (SV) morphology of 9 patients with vertical form. (A) SV draining into the inferior vena cava (IVC) above the diaphragm with tiny collateral artery supplying the right lung. (B–D) SV draining into the IVC above the diaphragm with a large collateral artery supplying the right lung. (E–G) SV draining into the IVC above the diaphragm with stenosis at its insertion site on the IVC. (H and I) SV draining into the IVC below the diaphragm with a tiny collateral artery supplying the right lung. Figure 2: View largeDownload slide The preoperative scimitar vein (SV) morphology of 9 patients with vertical form. (A) SV draining into the inferior vena cava (IVC) above the diaphragm with tiny collateral artery supplying the right lung. (B–D) SV draining into the IVC above the diaphragm with a large collateral artery supplying the right lung. (E–G) SV draining into the IVC above the diaphragm with stenosis at its insertion site on the IVC. (H and I) SV draining into the IVC below the diaphragm with a tiny collateral artery supplying the right lung. Figure 3: View largeDownload slide The pericardial tunnel technique for SV of vertical form. (A) SV is harvested from the IVC with its proximal end oversewn and distal end filleted open longitudinally on its medial aspect. An incision is made on the opposite site of the right lateral pericardium with redundant connective tissue on the incision edge removed and the phrenic nerve kept intact. The distal end of SV is then anastomosed to the pericardial incision. A longitudinal left atriotomy is performed posterior to the interatrial groove and extended as much as possible, with redundant atrial tissue on its edge removed. The pericardium around the left atriotomy should be kept intact to create a flap between the superior and inferior atriocaval junctions. (B) The pericardial flap is turned to the left with its anterior margin sutured onto the free wall of the right atrium anterior to the interatrial groove to create a tunnel, inside which the blood flow from SV can be directed into the LA. LA: left atrium; P: pericardium; RA: right atrium; SV: scimitar vein. Figure 3: View largeDownload slide The pericardial tunnel technique for SV of vertical form. (A) SV is harvested from the IVC with its proximal end oversewn and distal end filleted open longitudinally on its medial aspect. An incision is made on the opposite site of the right lateral pericardium with redundant connective tissue on the incision edge removed and the phrenic nerve kept intact. The distal end of SV is then anastomosed to the pericardial incision. A longitudinal left atriotomy is performed posterior to the interatrial groove and extended as much as possible, with redundant atrial tissue on its edge removed. The pericardium around the left atriotomy should be kept intact to create a flap between the superior and inferior atriocaval junctions. (B) The pericardial flap is turned to the left with its anterior margin sutured onto the free wall of the right atrium anterior to the interatrial groove to create a tunnel, inside which the blood flow from SV can be directed into the LA. LA: left atrium; P: pericardium; RA: right atrium; SV: scimitar vein. Figure 4: View largeDownload slide A postoperative computed tomography image showing the scimitar vein and pericardial tunnel of the 1st case before discharge. Figure 4: View largeDownload slide A postoperative computed tomography image showing the scimitar vein and pericardial tunnel of the 1st case before discharge. There were 4 males and 5 females, whose mean age during surgery was 3.1 ± 3.63 (range 0.3–12) years. One of the patients was older than 10 years. Their mean bodyweight was 9.6 ± 5.50 (range 3.1–21) kg. Before surgery, all patients were diagnosed based on their clinical presentations, Doppler echocardiography and cardioangiography computed tomography (CT). Five patients underwent cardiac catheterization. Two of 3 patients with a major aortopulmonary collateral artery underwent collateral artery occlusion with coil in the catheterization laboratory before surgery; the remaining subject had this collateral artery ligated during surgery. None of these 3 patients developed pulmonary ischaemia. Non-invasive pulmonary arterial pressure was determined, based on the velocity of tricuspid regurgitation (TR), as measured by Doppler echocardiography. The severity of pulmonary hypertension was defined as mild (30–50 mmHg, with TR velocity 2.5–3 m/s), moderate (50–75 mmHg, with TR velocity 3–4 m/s) or severe (>75 mmHg, with TR velocity >4 m/s). SV obstruction was suspected when the blood flow velocity of the SV was greater than 2 m/s (16 mmHg), without typical triphasic pattern of pulmonary vein, as detected by echocardiography. Table 1 shows the perioperative characteristics of these 9 patients. Table 1: Preoperative characteristics of SS patients with vertical form (n = 9) Variables  Dupuis’ classification   Total, n (%)  Infantile form (n = 5)  Childhood/ adult form (n = 4)  Gender   Male  2  2  4 (44.4)   Female  3  2  5 (55.6)  Age (years), mean ± SD  0.80 ± 0.24 (0.33–0.95)  5.98 ± 4.02 (3.8–12.0)    Qp:Qs, mean ± SDa  1.85 ± 0.21 (1.7–2.0)  1.96 ± 0.47 (1.6–2.5)    Clinical presentation   Recurrent respiratory infection  5b  3  8 (88.9)   Dyspnoea  4  1  5 (55.6)   Cardiac dysfunction  5  2  7 (77.8)  SV morphology   Drainage obstruction  3  0  3 (33.3)   Infra-diaphragm connection  2c  0  2 (22.2)  Pulmonary hypertension   Mild  1  2  3 (33.3)   Moderate  2  2  4 (44.4)   Severe  2  0  2 (22.2)  Associated anomalies   PDA  2  2  4 (44.4)   ASD  5  4  9 (100.0)   VSD  0  1  1 (11.1)   Dextroposition of the heart  5  4  9 (100.0)   Hypoplasia of the right lung  4  3  7 (77.8)   Major aortopulmonary collateral artery  3b,d  0  3 (33.3)  Variables  Dupuis’ classification   Total, n (%)  Infantile form (n = 5)  Childhood/ adult form (n = 4)  Gender   Male  2  2  4 (44.4)   Female  3  2  5 (55.6)  Age (years), mean ± SD  0.80 ± 0.24 (0.33–0.95)  5.98 ± 4.02 (3.8–12.0)    Qp:Qs, mean ± SDa  1.85 ± 0.21 (1.7–2.0)  1.96 ± 0.47 (1.6–2.5)    Clinical presentation   Recurrent respiratory infection  5b  3  8 (88.9)   Dyspnoea  4  1  5 (55.6)   Cardiac dysfunction  5  2  7 (77.8)  SV morphology   Drainage obstruction  3  0  3 (33.3)   Infra-diaphragm connection  2c  0  2 (22.2)  Pulmonary hypertension   Mild  1  2  3 (33.3)   Moderate  2  2  4 (44.4)   Severe  2  0  2 (22.2)  Associated anomalies   PDA  2  2  4 (44.4)   ASD  5  4  9 (100.0)   VSD  0  1  1 (11.1)   Dextroposition of the heart  5  4  9 (100.0)   Hypoplasia of the right lung  4  3  7 (77.8)   Major aortopulmonary collateral artery  3b,d  0  3 (33.3)  a In this study, 5 of 9 patients underwent cardiac catheterization before surgery and had data of Qp:Qs, with 2 in the group of infantile form and 3 in the group of childhood/adult form. b Three of 5 patients were admitted into the pneumology department before the operation for the treatment of pneumonia, including the 1st case of this study. They were scheduled for surgery after the pneumonia symptoms were controlled. c Both had drainage obstruction at the insertion site of SV into the IVC. d Two of 3 patients had their collateral arteries occluded with coil in the catheterization laboratory before surgery, including the 1st case of this study, and 1 of 3 patients had the collateral artery ligated during surgery. None of them developed pulmonary ischaemia. ASD: atrial septal defect; IVC: inferior vena cava; PDA: patent ductus arteriosus; SD: standard deviation; SS: scimitar syndrome; SV: scimitar vein; VSD: ventricular septal defect. Table 1: Preoperative characteristics of SS patients with vertical form (n = 9) Variables  Dupuis’ classification   Total, n (%)  Infantile form (n = 5)  Childhood/ adult form (n = 4)  Gender   Male  2  2  4 (44.4)   Female  3  2  5 (55.6)  Age (years), mean ± SD  0.80 ± 0.24 (0.33–0.95)  5.98 ± 4.02 (3.8–12.0)    Qp:Qs, mean ± SDa  1.85 ± 0.21 (1.7–2.0)  1.96 ± 0.47 (1.6–2.5)    Clinical presentation   Recurrent respiratory infection  5b  3  8 (88.9)   Dyspnoea  4  1  5 (55.6)   Cardiac dysfunction  5  2  7 (77.8)  SV morphology   Drainage obstruction  3  0  3 (33.3)   Infra-diaphragm connection  2c  0  2 (22.2)  Pulmonary hypertension   Mild  1  2  3 (33.3)   Moderate  2  2  4 (44.4)   Severe  2  0  2 (22.2)  Associated anomalies   PDA  2  2  4 (44.4)   ASD  5  4  9 (100.0)   VSD  0  1  1 (11.1)   Dextroposition of the heart  5  4  9 (100.0)   Hypoplasia of the right lung  4  3  7 (77.8)   Major aortopulmonary collateral artery  3b,d  0  3 (33.3)  Variables  Dupuis’ classification   Total, n (%)  Infantile form (n = 5)  Childhood/ adult form (n = 4)  Gender   Male  2  2  4 (44.4)   Female  3  2  5 (55.6)  Age (years), mean ± SD  0.80 ± 0.24 (0.33–0.95)  5.98 ± 4.02 (3.8–12.0)    Qp:Qs, mean ± SDa  1.85 ± 0.21 (1.7–2.0)  1.96 ± 0.47 (1.6–2.5)    Clinical presentation   Recurrent respiratory infection  5b  3  8 (88.9)   Dyspnoea  4  1  5 (55.6)   Cardiac dysfunction  5  2  7 (77.8)  SV morphology   Drainage obstruction  3  0  3 (33.3)   Infra-diaphragm connection  2c  0  2 (22.2)  Pulmonary hypertension   Mild  1  2  3 (33.3)   Moderate  2  2  4 (44.4)   Severe  2  0  2 (22.2)  Associated anomalies   PDA  2  2  4 (44.4)   ASD  5  4  9 (100.0)   VSD  0  1  1 (11.1)   Dextroposition of the heart  5  4  9 (100.0)   Hypoplasia of the right lung  4  3  7 (77.8)   Major aortopulmonary collateral artery  3b,d  0  3 (33.3)  a In this study, 5 of 9 patients underwent cardiac catheterization before surgery and had data of Qp:Qs, with 2 in the group of infantile form and 3 in the group of childhood/adult form. b Three of 5 patients were admitted into the pneumology department before the operation for the treatment of pneumonia, including the 1st case of this study. They were scheduled for surgery after the pneumonia symptoms were controlled. c Both had drainage obstruction at the insertion site of SV into the IVC. d Two of 3 patients had their collateral arteries occluded with coil in the catheterization laboratory before surgery, including the 1st case of this study, and 1 of 3 patients had the collateral artery ligated during surgery. None of them developed pulmonary ischaemia. ASD: atrial septal defect; IVC: inferior vena cava; PDA: patent ductus arteriosus; SD: standard deviation; SS: scimitar syndrome; SV: scimitar vein; VSD: ventricular septal defect. The 1st case in this study was a reoperation using the pericardial tunnel technique at our centre in 2011. This patient was admitted to the pneumology department for pneumonia before the initial operation. After pneumonia was controlled, her major collateral artery was occluded with a coil by cardiac catheterization. Then, her SV was anastomosed directly to the lateral posterior wall of the left atrium (LA) during the initial surgery. Low cardiac output and right pulmonary congestion developed after surgery. The patient could not be weaned from ventilator. The SV obstruction was confirmed by echocardiography (SV velocity 2.5 m/s, 25 mmHg, no triphasic pattern) and subsequently relieved using the pericardial tunnel technique. Surgical techniques All patients underwent surgery with cardiopulmonary bypass (CPB) via median sternotomy. After the pericardium was incised along the midline, CPB was established with aortic and bicaval cannulations. Following cross-clamping of aorta, cold blood cardioplegia was infused into the aortic root. Moderate hypothermia with rectal temperature of 28°C was applied for all patients. All associated intracardiac anomalies were repaired concomitantly. These patients were weaned from CBP per standard guidelines. The SV (n = 9) was attached to the right lateral pericardium prior to constructing a pericardial tunnel, inside which the blood from the SV was directed into the LA through a left atriotomy. After median sternotomy, the right phrenic nerve was approached via the right pleurotomy and carefully detached from the right lateral wall of pericardium by sharp and blunt dissection to keep it intact. The IVC was cannulated as low as possible. The oblique sinus of the pericardium was also kept intact to avoid postoperative haemorrhaging from the pericardial tunnel. During the cooling phase of CPB, the SV’s insertion site on the IVC and its course were inspected visually. While lungs were inflated manually by an anaesthesiologist, the exact relationship between the SV and the right lateral pericardium could be observed. Several stitches were placed on the SV and pericardium as landmarks for future incisions. After cardioplegia, a left atriotomy was performed posterior to the interatrial groove. A pericardial flap was created between the superior and inferior atriocaval junctions to create a tunnel with depth. The SV was divided at its insertion site on the IVC. The proximal end was oversewn. The distal end was filleted open longitudinally on its medial aspect. It was necessary to extend the pericardial incision, making it larger than the diameter of the SV. The pericardium and SV of paediatric patients had good elasticity and nearly the same thickness. Using a running suture technique with 7-0 polydioxanone suture (PDS, Ethicon, Johnson and Johnson; Somerville, NJ, USA)—as was used to repair the supra- or infracardiac total anomalous pulmonary venous connection—a side-to-side anastomosis was created between the distal end of the SV and the pericardial incision. The pericardial flap was turned to the left, with its anterior margin sutured onto the free wall of the right atrium anterior to the interatrial groove to create a tunnel. Lungs were reinflated to detect any torsion of the SV. To create an unobstructed SV–pericardial tunnel–left atrial pathway, the following principles should be followed: (i) the pericardial incision, SV incision and left atriotomy should be designed precisely with adequate length, same level and good alignment; (ii) a pericardial flap with sufficient but non-redundant width to ensure the appropriate size of a pericardial tunnel; (iii) a distal segment of SV with sufficient but non-redundant length to avoid any tension, kink or torsion of SV and maintain its original course as much as possible. If the pericardial flap is too narrow or if the distal segment of SV is too short, it will cause tension in the SV-to-pericardium anastomosis and secondary SV obstruction or intratunnel obstruction. If the pericardial flap is too wide or if the distal segment of SV is too long, the SV and its anastomosis to the pericardium will be kinked after the tunnel is filled, or lungs are inflated; (iv) it is unnecessary to use a tourniquet or snare around the SV, which will injure and twist this fragile vessel and complicate the placement of correct incision on it. After collateral artery is closed, there will be no excessive blood returning from the SV. By decreasing perfusion flow of CPB temporarily, combined with cardiotomy suction, the surgical field can be improved significantly and (v) manual inflation of lungs by an anaesthesiologist facilitates operator to observe the relationship between the SV and pericardium. If lungs collapse, the SV shifts from its natural position. Details on this pericardial tunnel technique are shown in Figure 3A and B. Postoperative management After the operation, all patients received mechanical ventilation and intensive care. Routine monitoring included invasive blood pressure, electrocardiogram, pulse oximetry and central venous pressure. Bronchoscopy was used for patients with prolonged mechanical ventilation (>3 days). Dopamine [5.0–7.5 μg/(kg⋅min)] and milrinone [0.5–0.75 μg/(kg⋅min)] were administrated routinely to all patients. Adrenaline [0.02–0.05 μg/(kg⋅min)] was administrated selectively for low cardiac output. Fluid balance was maintained. Following intraoperative transoesophageal echocardiography, bedside transthoracic echocardiography was performed 1–3 days after the operation. The patients underwent follow-ups 1, 3 and 6 months after discharge and then annually. Conventional follow-up surveillances consisted of Doppler echocardiography, electrocardiogram and chest X-ray. Because of the cost and concern of exposure to radiation, the cardiac catheterization and cardioangiography CT were not performed routinely in the follow-ups, unless the blood flow velocity of the SV >2 m/s (16 mmHg), without typical triphasic pattern of pulmonary vein, as detected by echocardiography. Statistical analysis Count data are expressed as numbers, frequencies and percentages. Measurement data are expressed as means ± standard deviations. RESULTS The mean CPB time was 104.8 ± 19.4 (range 77–141) min. The mean aorta cross-clamping time was 42.4 ± 16.0 (range 22–79) min. The mean postoperative mechanical ventilation time was 88.3 ± 63.8 (range 36–264) h (6 cases <3 days, 2 cases 3–7 days and 1 case >7 days). Postoperative data and complications are listed in Table 2. Table 2: Postoperative complications of SS patients with vertical form (n = 9) Complications  Dupuis’ classification   Total, n (%)  Infantile form (n = 5)  Childhood/ adult form (n = 4)  Prolonged mechanical ventilation (days)         3–7  2a  0  2 (22.2)   >7  1a,c  0  1 (11.1)  Low cardiac output      3 (33.3)   Caused by residual pulmonary hypertension  1  0  1 (11.1)   Caused by transient hypoxia  1  1  2 (22.2)  Peritoneal dialysis for renal insufficiency  1  1  2 (22.2)  Pneumonia  3a  2b  5 (55.5)  Pleural effusion  1  0  1 (11.1)  Plication of diaphragm for phrenoparalysis  1c    1 (11.1)  Complications  Dupuis’ classification   Total, n (%)  Infantile form (n = 5)  Childhood/ adult form (n = 4)  Prolonged mechanical ventilation (days)         3–7  2a  0  2 (22.2)   >7  1a,c  0  1 (11.1)  Low cardiac output      3 (33.3)   Caused by residual pulmonary hypertension  1  0  1 (11.1)   Caused by transient hypoxia  1  1  2 (22.2)  Peritoneal dialysis for renal insufficiency  1  1  2 (22.2)  Pneumonia  3a  2b  5 (55.5)  Pleural effusion  1  0  1 (11.1)  Plication of diaphragm for phrenoparalysis  1c    1 (11.1)  a These 3 patients underwent bronchoscopy with bronchoalveolar lavage taken for a microbiological test before extubation. Microorganisms detected in the bronchoalveolar lavage culture: Klebsiella pneumoniae (n = 1), Escherichia coli (n = 1) and Streptococcus pneumoniae (n = 1). b Microorganisms detected in the endotracheal secretion culture: Klebsiella pneumoniae (n = 1), negative (n = 1). c The 1st case of this study. The patient had been on a mechanical ventilator for 10 days after the reoperation using the pericardial tunnel technique. SS: scimitar syndrome. Table 2: Postoperative complications of SS patients with vertical form (n = 9) Complications  Dupuis’ classification   Total, n (%)  Infantile form (n = 5)  Childhood/ adult form (n = 4)  Prolonged mechanical ventilation (days)         3–7  2a  0  2 (22.2)   >7  1a,c  0  1 (11.1)  Low cardiac output      3 (33.3)   Caused by residual pulmonary hypertension  1  0  1 (11.1)   Caused by transient hypoxia  1  1  2 (22.2)  Peritoneal dialysis for renal insufficiency  1  1  2 (22.2)  Pneumonia  3a  2b  5 (55.5)  Pleural effusion  1  0  1 (11.1)  Plication of diaphragm for phrenoparalysis  1c    1 (11.1)  Complications  Dupuis’ classification   Total, n (%)  Infantile form (n = 5)  Childhood/ adult form (n = 4)  Prolonged mechanical ventilation (days)         3–7  2a  0  2 (22.2)   >7  1a,c  0  1 (11.1)  Low cardiac output      3 (33.3)   Caused by residual pulmonary hypertension  1  0  1 (11.1)   Caused by transient hypoxia  1  1  2 (22.2)  Peritoneal dialysis for renal insufficiency  1  1  2 (22.2)  Pneumonia  3a  2b  5 (55.5)  Pleural effusion  1  0  1 (11.1)  Plication of diaphragm for phrenoparalysis  1c    1 (11.1)  a These 3 patients underwent bronchoscopy with bronchoalveolar lavage taken for a microbiological test before extubation. Microorganisms detected in the bronchoalveolar lavage culture: Klebsiella pneumoniae (n = 1), Escherichia coli (n = 1) and Streptococcus pneumoniae (n = 1). b Microorganisms detected in the endotracheal secretion culture: Klebsiella pneumoniae (n = 1), negative (n = 1). c The 1st case of this study. The patient had been on a mechanical ventilator for 10 days after the reoperation using the pericardial tunnel technique. SS: scimitar syndrome. The sole reoperative patient underwent surgical revision on the 5th day after the initial operation of direct SV-to-left atrial anastomosis. During the reoperation, the SV was found to be of vertical form and short. There was tension on the SV and stenosis at the anastomosis. While the lungs were inflated, the SV and anastomosis were deformed. After the SV-to-left atrial anastomosis being taken down, the SV was reimplanted onto the right lateral pericardium. The oblique sinus of the pericardium was restored. An extension tunnel to the LA was created with a pericardial flap. The blood flow from the SV was directed into the LA through a left atriotomy inside tunnel. After the reoperation, her pulmonary congestion improved significantly. Because of phrenoparalysis and pneumonia, the patient was ventilator dependent. She underwent plication of diaphragm on the 7th day after the reoperation. Three days later, she was successfully weaned from ventilator. Figure 4 shows the CT image of the SV and pericardial tunnel in this patient before discharge. There was no in-hospital mortality or SV obstruction. Eight of 9 survivors were followed up after discharge, with 1 lost to follow-up. The mean follow-up time was 33.4 ± 19.2 (range 2–72) months. Echocardiography demonstrated that no SV obstruction developed during the follow-ups, and 7 patients had no pulmonary hypertension and 1 had mild pulmonary hypertension. Subsequently, the patients thrived without further symptoms of recurrent respiratory infection. They were in the New York Heart Association (NYHA) Class I. The mean left ventricular ejection fraction measured by last echocardiography was 67.6 ± 8.8% (range 57.9–80.8%). DISCUSSION Halasz first described the anomalous vein in SS as ‘scimitar-shaped’ in 1956 [4]. Dupuis et al. [2, 3] classified SS into infantile and childhood/adult forms, based on age and associated symptoms. In our study, there were 5 cases (55.6%) with infantile form. Patients with infantile form usually develop cardiac dysfunction, dyspnoea and recurrent respiratory infections. They have higher comorbidities correlated with the severity of associated defects, pulmonary hypertension and congestive heart failure [3]. The infantile form of SS has a higher surgical mortality rate [5] and rate of postoperative SV obstruction, especially for those younger than 3 months [6]. However, several groups advocated medical treatment or occlusion of collateral artery to improve symptoms and postpone surgical repair until early childhood [6, 7], QP/QS >1.5 is an indication for surgery in childhood [8]. Kirklin first completed surgical repair for SS with CPB in 1956, with the SV anastomosed to the right atrium and drained into the LA through an ASD using an intra-atrial pericardial baffle [9]. Then, Tornvall described the SV-to-left atrial anastomosis technique [10]. Both approaches remain the classical SV reimplantation techniques for surgical repair of SS. Another method created a long intra-atrial baffle from the orifice of the SV within the IVC to an ASD. This long baffle might cause intrabaffle thrombosis and obstruction of the IVC and might be difficult to construct in small infants [11]. The advantages and disadvantages of these conventional procedures remain debated. Because of the wide variation in SV anatomy, the rate of postoperative SV obstruction is 15.5–23.8% [5, 6] and that of reintervention is 11–30% [6, 12–14]. Several groups described other modified techniques for SV reimplantation to minimize postoperative complications, including SV reimplantation via anterior lateral thoracotomy without CPB [15] and interposed grafts for SV extension [16]. In 2014, Lugones and García [17] reported 1 case that underwent surgical repair for SS by construction of a pericardial tunnel. Before 2011, we used the classical technique above for SS repair but encountered postoperative problems, such as SV obstruction. We gradually realized that certain SVs had disparate courses and angulations at the insertion site on the IVC. In 2011, we attempted to combine several concepts and techniques of Senning procedure and sutureless repair for supra- or infracardiac total anomalous pulmonary venous connection as a surgical solution for a patient with residual SV obstruction after the classical direct SV-to-left atrial anastomosis. Ultimately, we successfully constructed a pericardial tunnel that was attached to the SV and relieved the residual SV obstruction. Because the preoperative condition of the 1st patient was complicated, we believed that her postoperative parameters were not attributable to the pericardial tunnel technique. Since then, we have increasingly considered SV anatomy. We classified SV into 2 anatomical forms—vertical and horizontal—based on its angulation to the IVC (Fig. 1 and 2). We found that the SVs of vertical form were always shorter than those of horizontal form, had sharper angulations to the IVC and right lateral wall of either atrium and were more distal to atrial wall. If an SV of vertical form is anastomosed directly to the right lateral wall of either atrium, the position of the anastomosis must be planned precisely in advance; otherwise, it might compromise the patency of that anastomosis and cause obstruction. When implanted more cephalad, these SVs tend to deform like a hook with kinking or torsion. However, if they are implanted more caudally, they will have significant tension. The position of anastomosis depends tremendously on surgeon’s experience and intraoperative judgement. In patients with an infradiaphragm SV-to-IVC connection, the SV is much more distal to atria, as reported in a case by Lugones and García [17], and there is always obstruction that is caused by tension after direct anastomosis. With a pericardial tunnel to which the SV of vertical form is attached, the course of the SV will be extended. Thus, the tension in the SV and anastomosis will be minimized, and the patency will be maintained well. However, for patients with horizontal form, this pericardial tunnel technique should not be the preferred procedure. SVs of horizontal form always pass through a longer course immediately above diaphragm before entering the IVC. These SVs can be easily anastomosed to either atrium with good mobility after dissection, for which some redundant length should be removed. The direct SV-to-atrium reimplantation is less likely to cause tension in anastomosis. In addition, an unnecessary pericardial tunnel might compromise the morphology of the SV and cause obstruction. Thus, we believe that the direct reimplantation is a more reasonable choice for those with horizontal form. On the basis of our understanding of 2 anatomical SV forms and our experience with the 1st case, we have preferred the classical technique for horizontal form and the pericardial tunnel technique for vertical form since 2011. Protection of phrenic nerve is important to surgical repairs for SS. Brink et al. [5] reported that the incidence of phrenic nerve palsy was 4.8% (1/21) in a group of patients whose surgical strategies included intra-atial baffle, direct reimplantation and pneumonectomy. In the multicentric study by Vida et al. [6], the incidence of phrenic nerve injury in the group of direct reimplantation (4/67, 6.0%) was significantly higher than in the group of intra-atrial baffle (1/38, 2.6%) (P = 0.04). However, Brown et al. [15] reported no incidence of phrenic nerve injury or palsy in 9 patients with mean age of 11.5 years who underwent direct reimplantation via a right anterior lateral thoracotomy without CPB. In our cohort, the incidence of phrenic never palsy was 11.1% (1/9). We do not believe that the phrenoparalysis in our 1st case was caused solely by the reoperation. We used the same protective technique as Senning procedure in this study. No phrenoparalysis occurred in subsequent patients. However, we do believe that the incidence of phrenic nerve injury has strong relationship to different surgical techniques and patient’s age. The dissection of the SV and pericardium near the right phrenic nerve while using direct reimplantation technique may be the reason of phrenic nerve injury, especially in younger patients whose phrenic nerve and diaphragm are more fragile. While using intra-atrial baffle technique, it is unnecessary to do such dissection of the SV and pericardium. However, further efforts must be made to protect the phrenic nerve for all patients. Limitations There were several limitations of this study. Because it was a retrospective study from a single centre, the selection bias might have reduced the accuracy of certain results. One of 9 (11.1%) patients was lost to follow-up, so that the incidence of postoperative pulmonary vein obstruction and mortality may be underestimated. More cases and data from longer follow-ups must be collected to obtain more accurate results and conclusions of this rare congenital heart anomaly. We will use magnetic resonance imaging as a routine surveillance for further mid-term and long-term follow-ups, because it does not use radiation and can provide more data on cardiovascular anatomy and function. This option will allow us to confirm the relationship between SV anatomy and reconstruction technique. A multicentre study is underway. CONCLUSIONS The preferred procedure is determined primarily by the SV anatomy. The pericardial tunnel technique is a favourable option for the SS patients with vertical form. ACKNOWLEDGEMENTS We are grateful to our illustrator, Jiguang Qin, for his generous help and artwork that demonstrates the surgical details of the pericardial tunnel technique. Conflictof interest: none declared. REFERENCES 1 Wang CC, Wu ET, Chen SJ, Lu F, Huang SC, Wang JK. Scimitar syndrome: incidence, treatment, and prognosis. Eur J Pediatr  2008; 167: 155– 60. Google Scholar CrossRef Search ADS PubMed  2 Dupuis C, Charaf LA, Brevière GM, Abou P, Rémy-Jardin M, Helmius G. The ‘adult’ form of the scimitar syndrome. Am J Cardiol  1992; 70: 502– 7. Google Scholar CrossRef Search ADS PubMed  3 Dupuis C, Charaf LA, Brevière GM, Abou P. ‘Infantile’ form of the scimitar syndrome with pulmonary hypertension. Am J Cardiol  1993; 71: 1326– 30. Google Scholar CrossRef Search ADS PubMed  4 Halasz NA, Halloran KH, Liebow AA. Bronchial and arterial anomalies with drainage of the right lung into the inferior vena cava. Circulation  1956; 14: 826– 46. Google Scholar CrossRef Search ADS PubMed  5 Brink J, Yong MS, d'Udekem Y, Weintraub RG, Brizard CP, Konstantinov IE. Surgery for scimitar syndrome: the Melbourne experience. Interact CardioVasc Thorac Surg  2015; 20: 31– 4. Google Scholar CrossRef Search ADS PubMed  6 Vida VL, Padalino MA, Boccuzzo G, Tarja E, Berggren H, Carrel T et al.   Scimitar syndrome: a European Congenital Heart Surgeons Association (ECHSA) multicentric study. Circulation  2010; 122: 1159– 66. Google Scholar CrossRef Search ADS PubMed  7 Korkmaz AA, Yildiz CE, Onan B, Guden M, Cetin G, Babaoglu K. Scimitar syndrome: a complex form of anomalous pulmonary venous return. J Card Surg  2011; 26: 529– 34. Google Scholar CrossRef Search ADS PubMed  8 Çiçek S, Arslan AH, Ugurlucan M, Yildiz Y, Ay S. Scimitar syndrome: the curved Turkish sabre. Semin Thorac Cardiovasc Surg Pediatr Card Surg Annu  2014; 17: 56– 61. Google Scholar CrossRef Search ADS PubMed  9 Kirklin JW, Ellis FH Jr, Wood EH. Treatment of anomalous pulmonary venous connections in association with interatrial communications. Surgery  1956; 39: 389– 98. Google Scholar PubMed  10 Tornvall SS, Jackson KH, Alvayay JC, Vargas AC, Koch W, Zarate E. Anomalous drainage of the pulmonary veins into the inferior vena cava. J Thorac Cardiovasc Surg  1961; 42: 413– 7. Google Scholar PubMed  11 Gudjonsson U, Brown JW. Scimitar syndrome. Semin Thorac Cardiovasc Surg Pediatr Card Surg Annu  2006; 9: 56– 62. Google Scholar CrossRef Search ADS   12 Vida VL, Speggiorin S, Padalino MA, Crupi G, Marcelletti C, Zannini L et al.   The scimitar syndrome: an Italian multicenter study. Ann Thorac Surg  2009; 88: 440– 4. Google Scholar CrossRef Search ADS PubMed  13 Dusenbery SM, Geva T, Seale A, Valente AM, Zhou J, Sena L et al.   Outcome predictors and implications for management of scimitar syndrome. Am Heart J  2013; 165: 770– 7. Google Scholar CrossRef Search ADS PubMed  14 Alsoufi B, Cai S, Van Arsdell GS, Williams WG, Caldarone CA, Coles JG. Outcomes after surgical treatment of children with partial anomalous pulmonary venous connection. Ann Thorac Surg  2007; 84: 2020– 6. Google Scholar CrossRef Search ADS PubMed  15 Brown JW, Ruzmetov M, Minnich DJ, Vijay P, Edwards CA, Uhlig PN et al.   Surgical management of scimitar syndrome: an alternative approach. J Thorac Cardiovasc Surg  2003; 125: 238– 45. Google Scholar CrossRef Search ADS PubMed  16 Lam TT, Reemtsen BL, Starnes VA, Wells WJ. A novel approach to the surgical correction of scimitar syndrome. J Thorac Cardiovasc Surg  2007; 133: 573– 4. Google Scholar CrossRef Search ADS PubMed  17 Lugones I, García R. A new surgical approach to scimitar syndrome. Ann Thorac Surg  2014; 97: 353– 5. Google Scholar CrossRef Search ADS PubMed  © The Author(s) 2018. Published by Oxford University Press on behalf of the European Association for Cardio-Thoracic Surgery. All rights reserved. This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices) http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Interactive CardioVascular and Thoracic Surgery Oxford University Press

Pericardial tunnel technique in the surgical management of the vertical form of scimitar syndrome

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Oxford University Press
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© The Author(s) 2018. Published by Oxford University Press on behalf of the European Association for Cardio-Thoracic Surgery. All rights reserved.
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1569-9293
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Abstract

Abstract OBJECTIVES To optimize the surgical strategy and individualized treatment for scimitar syndrome (SS) by summarizing the clinical outcomes of the pericardial tunnel technique for the vertical form of SS at a single centre. METHODS The vertical form was defined as an angle of scimitar vein (SV) insertion to the inferior vena cava (θ) ≤ 45°, whereas the horizontal form was defined as θ > 45°. Nine patients with vertical form were operated on from June 2011 to June 2017. The mean age of patients during surgery was 3.1 ± 3.63 (range 0.3–12) years. Five patients were with infantile form and 4 with childhood/adult form per Dupuis’ classification. The pericardial tunnel technique entailed attaching the SV to the right lateral pericardium and directing blood flow to the left atrium through a left atriotomy inside the pericardial tunnel. All patients had associated intracardiac anomalies repaired concomitantly; 3 patients had major collateral arteries occluded or ligated. RESULTS There was no in-hospital postoperative death or residual SV obstruction. The postoperative ventilation time was 88.3 ± 63.8 (range 36–264) h. Eight survivors were followed up for 33.4 ± 19.2 (range 2–72) months, with 1 lost to follow-up. Echocardiography demonstrated that 7 survivors had no pulmonary hypertension and 1 had mild pulmonary hypertension; none developed SV obstruction during the follow-ups. CONCLUSIONS The pericardial tunnel technique is suitable for the vertical form of SS and is a reasonable option for individualized treatment of SS. Scimitar syndrome , Congenital heart disease , Surgery , Complication INTRODUCTION Scimitar syndrome (SS) is a rare, complex congenital heart anomaly affecting approximately 0.06% of patients with congenital heart diseases, and its incidence is higher in females [1]. The major feature of SS is that all or partial right pulmonary veins drain into the inferior vena cava (IVC) through an anomalous right pulmonary vein. The morphology of this vein resembles a Turkish sabre; thus, it is termed scimitar vein (SV). SS is often associated with varying degrees of hypoplasia of the right lung and ipsilateral branch pulmonary artery, dextroposition of the heart and the right upper or middle lobe supplied by anomalous collateral arteries from the thoracic or abdominal aorta. On the basis of the clinical presentations by age, Dupuis et al. [2, 3] classified SS into 2 forms: infantile and childhood/adult. Patients with infantile form are younger than 1 year and always present with cardiac dysfunction, dyspnoea and recurrent respiratory infection. Patients with childhood/adult form are older than 1 year and presented with recurrent respiratory infection with relatively good heart function. Mild cases of SS have no obvious clinical symptoms. We found that certain SVs had different angulations on the insertion into the IVC, which we termed the ‘vertical’ and ‘horizontal’ forms. Thus, based on this unique anatomical feature of the SV, the traditional surgical technique should be modified. We summarized our experience on the pericardial tunnel technique for the vertical form of SS at our centre. PATIENTS AND METHODS Patient characteristics A total of 9 patients with SS underwent surgical repair using the pericardial tunnel technique at our centre from June 2011 to June 2017. The angle of the SV insertion to the IVC (θ) was measured. The vertical form of SS was defined as θ ≤ 45°, whereas the horizontal form was defined as θ > 45° (Fig. 1). All 9 patients in this cohort had vertical form (Fig. 2A–I). In the same timeframe, there were 5 patients with horizontal form that was repaired using another surgical technique and were excluded from this study. Figure 1: View largeDownload slide Definition of horizontal and vertical forms of scimitar vein. (A) Horizontal form with θ > 45° and (B) vertical form with θ ≤ 45°. Figure 1: View largeDownload slide Definition of horizontal and vertical forms of scimitar vein. (A) Horizontal form with θ > 45° and (B) vertical form with θ ≤ 45°. Figure 2: View largeDownload slide The preoperative scimitar vein (SV) morphology of 9 patients with vertical form. (A) SV draining into the inferior vena cava (IVC) above the diaphragm with tiny collateral artery supplying the right lung. (B–D) SV draining into the IVC above the diaphragm with a large collateral artery supplying the right lung. (E–G) SV draining into the IVC above the diaphragm with stenosis at its insertion site on the IVC. (H and I) SV draining into the IVC below the diaphragm with a tiny collateral artery supplying the right lung. Figure 2: View largeDownload slide The preoperative scimitar vein (SV) morphology of 9 patients with vertical form. (A) SV draining into the inferior vena cava (IVC) above the diaphragm with tiny collateral artery supplying the right lung. (B–D) SV draining into the IVC above the diaphragm with a large collateral artery supplying the right lung. (E–G) SV draining into the IVC above the diaphragm with stenosis at its insertion site on the IVC. (H and I) SV draining into the IVC below the diaphragm with a tiny collateral artery supplying the right lung. Figure 3: View largeDownload slide The pericardial tunnel technique for SV of vertical form. (A) SV is harvested from the IVC with its proximal end oversewn and distal end filleted open longitudinally on its medial aspect. An incision is made on the opposite site of the right lateral pericardium with redundant connective tissue on the incision edge removed and the phrenic nerve kept intact. The distal end of SV is then anastomosed to the pericardial incision. A longitudinal left atriotomy is performed posterior to the interatrial groove and extended as much as possible, with redundant atrial tissue on its edge removed. The pericardium around the left atriotomy should be kept intact to create a flap between the superior and inferior atriocaval junctions. (B) The pericardial flap is turned to the left with its anterior margin sutured onto the free wall of the right atrium anterior to the interatrial groove to create a tunnel, inside which the blood flow from SV can be directed into the LA. LA: left atrium; P: pericardium; RA: right atrium; SV: scimitar vein. Figure 3: View largeDownload slide The pericardial tunnel technique for SV of vertical form. (A) SV is harvested from the IVC with its proximal end oversewn and distal end filleted open longitudinally on its medial aspect. An incision is made on the opposite site of the right lateral pericardium with redundant connective tissue on the incision edge removed and the phrenic nerve kept intact. The distal end of SV is then anastomosed to the pericardial incision. A longitudinal left atriotomy is performed posterior to the interatrial groove and extended as much as possible, with redundant atrial tissue on its edge removed. The pericardium around the left atriotomy should be kept intact to create a flap between the superior and inferior atriocaval junctions. (B) The pericardial flap is turned to the left with its anterior margin sutured onto the free wall of the right atrium anterior to the interatrial groove to create a tunnel, inside which the blood flow from SV can be directed into the LA. LA: left atrium; P: pericardium; RA: right atrium; SV: scimitar vein. Figure 4: View largeDownload slide A postoperative computed tomography image showing the scimitar vein and pericardial tunnel of the 1st case before discharge. Figure 4: View largeDownload slide A postoperative computed tomography image showing the scimitar vein and pericardial tunnel of the 1st case before discharge. There were 4 males and 5 females, whose mean age during surgery was 3.1 ± 3.63 (range 0.3–12) years. One of the patients was older than 10 years. Their mean bodyweight was 9.6 ± 5.50 (range 3.1–21) kg. Before surgery, all patients were diagnosed based on their clinical presentations, Doppler echocardiography and cardioangiography computed tomography (CT). Five patients underwent cardiac catheterization. Two of 3 patients with a major aortopulmonary collateral artery underwent collateral artery occlusion with coil in the catheterization laboratory before surgery; the remaining subject had this collateral artery ligated during surgery. None of these 3 patients developed pulmonary ischaemia. Non-invasive pulmonary arterial pressure was determined, based on the velocity of tricuspid regurgitation (TR), as measured by Doppler echocardiography. The severity of pulmonary hypertension was defined as mild (30–50 mmHg, with TR velocity 2.5–3 m/s), moderate (50–75 mmHg, with TR velocity 3–4 m/s) or severe (>75 mmHg, with TR velocity >4 m/s). SV obstruction was suspected when the blood flow velocity of the SV was greater than 2 m/s (16 mmHg), without typical triphasic pattern of pulmonary vein, as detected by echocardiography. Table 1 shows the perioperative characteristics of these 9 patients. Table 1: Preoperative characteristics of SS patients with vertical form (n = 9) Variables  Dupuis’ classification   Total, n (%)  Infantile form (n = 5)  Childhood/ adult form (n = 4)  Gender   Male  2  2  4 (44.4)   Female  3  2  5 (55.6)  Age (years), mean ± SD  0.80 ± 0.24 (0.33–0.95)  5.98 ± 4.02 (3.8–12.0)    Qp:Qs, mean ± SDa  1.85 ± 0.21 (1.7–2.0)  1.96 ± 0.47 (1.6–2.5)    Clinical presentation   Recurrent respiratory infection  5b  3  8 (88.9)   Dyspnoea  4  1  5 (55.6)   Cardiac dysfunction  5  2  7 (77.8)  SV morphology   Drainage obstruction  3  0  3 (33.3)   Infra-diaphragm connection  2c  0  2 (22.2)  Pulmonary hypertension   Mild  1  2  3 (33.3)   Moderate  2  2  4 (44.4)   Severe  2  0  2 (22.2)  Associated anomalies   PDA  2  2  4 (44.4)   ASD  5  4  9 (100.0)   VSD  0  1  1 (11.1)   Dextroposition of the heart  5  4  9 (100.0)   Hypoplasia of the right lung  4  3  7 (77.8)   Major aortopulmonary collateral artery  3b,d  0  3 (33.3)  Variables  Dupuis’ classification   Total, n (%)  Infantile form (n = 5)  Childhood/ adult form (n = 4)  Gender   Male  2  2  4 (44.4)   Female  3  2  5 (55.6)  Age (years), mean ± SD  0.80 ± 0.24 (0.33–0.95)  5.98 ± 4.02 (3.8–12.0)    Qp:Qs, mean ± SDa  1.85 ± 0.21 (1.7–2.0)  1.96 ± 0.47 (1.6–2.5)    Clinical presentation   Recurrent respiratory infection  5b  3  8 (88.9)   Dyspnoea  4  1  5 (55.6)   Cardiac dysfunction  5  2  7 (77.8)  SV morphology   Drainage obstruction  3  0  3 (33.3)   Infra-diaphragm connection  2c  0  2 (22.2)  Pulmonary hypertension   Mild  1  2  3 (33.3)   Moderate  2  2  4 (44.4)   Severe  2  0  2 (22.2)  Associated anomalies   PDA  2  2  4 (44.4)   ASD  5  4  9 (100.0)   VSD  0  1  1 (11.1)   Dextroposition of the heart  5  4  9 (100.0)   Hypoplasia of the right lung  4  3  7 (77.8)   Major aortopulmonary collateral artery  3b,d  0  3 (33.3)  a In this study, 5 of 9 patients underwent cardiac catheterization before surgery and had data of Qp:Qs, with 2 in the group of infantile form and 3 in the group of childhood/adult form. b Three of 5 patients were admitted into the pneumology department before the operation for the treatment of pneumonia, including the 1st case of this study. They were scheduled for surgery after the pneumonia symptoms were controlled. c Both had drainage obstruction at the insertion site of SV into the IVC. d Two of 3 patients had their collateral arteries occluded with coil in the catheterization laboratory before surgery, including the 1st case of this study, and 1 of 3 patients had the collateral artery ligated during surgery. None of them developed pulmonary ischaemia. ASD: atrial septal defect; IVC: inferior vena cava; PDA: patent ductus arteriosus; SD: standard deviation; SS: scimitar syndrome; SV: scimitar vein; VSD: ventricular septal defect. Table 1: Preoperative characteristics of SS patients with vertical form (n = 9) Variables  Dupuis’ classification   Total, n (%)  Infantile form (n = 5)  Childhood/ adult form (n = 4)  Gender   Male  2  2  4 (44.4)   Female  3  2  5 (55.6)  Age (years), mean ± SD  0.80 ± 0.24 (0.33–0.95)  5.98 ± 4.02 (3.8–12.0)    Qp:Qs, mean ± SDa  1.85 ± 0.21 (1.7–2.0)  1.96 ± 0.47 (1.6–2.5)    Clinical presentation   Recurrent respiratory infection  5b  3  8 (88.9)   Dyspnoea  4  1  5 (55.6)   Cardiac dysfunction  5  2  7 (77.8)  SV morphology   Drainage obstruction  3  0  3 (33.3)   Infra-diaphragm connection  2c  0  2 (22.2)  Pulmonary hypertension   Mild  1  2  3 (33.3)   Moderate  2  2  4 (44.4)   Severe  2  0  2 (22.2)  Associated anomalies   PDA  2  2  4 (44.4)   ASD  5  4  9 (100.0)   VSD  0  1  1 (11.1)   Dextroposition of the heart  5  4  9 (100.0)   Hypoplasia of the right lung  4  3  7 (77.8)   Major aortopulmonary collateral artery  3b,d  0  3 (33.3)  Variables  Dupuis’ classification   Total, n (%)  Infantile form (n = 5)  Childhood/ adult form (n = 4)  Gender   Male  2  2  4 (44.4)   Female  3  2  5 (55.6)  Age (years), mean ± SD  0.80 ± 0.24 (0.33–0.95)  5.98 ± 4.02 (3.8–12.0)    Qp:Qs, mean ± SDa  1.85 ± 0.21 (1.7–2.0)  1.96 ± 0.47 (1.6–2.5)    Clinical presentation   Recurrent respiratory infection  5b  3  8 (88.9)   Dyspnoea  4  1  5 (55.6)   Cardiac dysfunction  5  2  7 (77.8)  SV morphology   Drainage obstruction  3  0  3 (33.3)   Infra-diaphragm connection  2c  0  2 (22.2)  Pulmonary hypertension   Mild  1  2  3 (33.3)   Moderate  2  2  4 (44.4)   Severe  2  0  2 (22.2)  Associated anomalies   PDA  2  2  4 (44.4)   ASD  5  4  9 (100.0)   VSD  0  1  1 (11.1)   Dextroposition of the heart  5  4  9 (100.0)   Hypoplasia of the right lung  4  3  7 (77.8)   Major aortopulmonary collateral artery  3b,d  0  3 (33.3)  a In this study, 5 of 9 patients underwent cardiac catheterization before surgery and had data of Qp:Qs, with 2 in the group of infantile form and 3 in the group of childhood/adult form. b Three of 5 patients were admitted into the pneumology department before the operation for the treatment of pneumonia, including the 1st case of this study. They were scheduled for surgery after the pneumonia symptoms were controlled. c Both had drainage obstruction at the insertion site of SV into the IVC. d Two of 3 patients had their collateral arteries occluded with coil in the catheterization laboratory before surgery, including the 1st case of this study, and 1 of 3 patients had the collateral artery ligated during surgery. None of them developed pulmonary ischaemia. ASD: atrial septal defect; IVC: inferior vena cava; PDA: patent ductus arteriosus; SD: standard deviation; SS: scimitar syndrome; SV: scimitar vein; VSD: ventricular septal defect. The 1st case in this study was a reoperation using the pericardial tunnel technique at our centre in 2011. This patient was admitted to the pneumology department for pneumonia before the initial operation. After pneumonia was controlled, her major collateral artery was occluded with a coil by cardiac catheterization. Then, her SV was anastomosed directly to the lateral posterior wall of the left atrium (LA) during the initial surgery. Low cardiac output and right pulmonary congestion developed after surgery. The patient could not be weaned from ventilator. The SV obstruction was confirmed by echocardiography (SV velocity 2.5 m/s, 25 mmHg, no triphasic pattern) and subsequently relieved using the pericardial tunnel technique. Surgical techniques All patients underwent surgery with cardiopulmonary bypass (CPB) via median sternotomy. After the pericardium was incised along the midline, CPB was established with aortic and bicaval cannulations. Following cross-clamping of aorta, cold blood cardioplegia was infused into the aortic root. Moderate hypothermia with rectal temperature of 28°C was applied for all patients. All associated intracardiac anomalies were repaired concomitantly. These patients were weaned from CBP per standard guidelines. The SV (n = 9) was attached to the right lateral pericardium prior to constructing a pericardial tunnel, inside which the blood from the SV was directed into the LA through a left atriotomy. After median sternotomy, the right phrenic nerve was approached via the right pleurotomy and carefully detached from the right lateral wall of pericardium by sharp and blunt dissection to keep it intact. The IVC was cannulated as low as possible. The oblique sinus of the pericardium was also kept intact to avoid postoperative haemorrhaging from the pericardial tunnel. During the cooling phase of CPB, the SV’s insertion site on the IVC and its course were inspected visually. While lungs were inflated manually by an anaesthesiologist, the exact relationship between the SV and the right lateral pericardium could be observed. Several stitches were placed on the SV and pericardium as landmarks for future incisions. After cardioplegia, a left atriotomy was performed posterior to the interatrial groove. A pericardial flap was created between the superior and inferior atriocaval junctions to create a tunnel with depth. The SV was divided at its insertion site on the IVC. The proximal end was oversewn. The distal end was filleted open longitudinally on its medial aspect. It was necessary to extend the pericardial incision, making it larger than the diameter of the SV. The pericardium and SV of paediatric patients had good elasticity and nearly the same thickness. Using a running suture technique with 7-0 polydioxanone suture (PDS, Ethicon, Johnson and Johnson; Somerville, NJ, USA)—as was used to repair the supra- or infracardiac total anomalous pulmonary venous connection—a side-to-side anastomosis was created between the distal end of the SV and the pericardial incision. The pericardial flap was turned to the left, with its anterior margin sutured onto the free wall of the right atrium anterior to the interatrial groove to create a tunnel. Lungs were reinflated to detect any torsion of the SV. To create an unobstructed SV–pericardial tunnel–left atrial pathway, the following principles should be followed: (i) the pericardial incision, SV incision and left atriotomy should be designed precisely with adequate length, same level and good alignment; (ii) a pericardial flap with sufficient but non-redundant width to ensure the appropriate size of a pericardial tunnel; (iii) a distal segment of SV with sufficient but non-redundant length to avoid any tension, kink or torsion of SV and maintain its original course as much as possible. If the pericardial flap is too narrow or if the distal segment of SV is too short, it will cause tension in the SV-to-pericardium anastomosis and secondary SV obstruction or intratunnel obstruction. If the pericardial flap is too wide or if the distal segment of SV is too long, the SV and its anastomosis to the pericardium will be kinked after the tunnel is filled, or lungs are inflated; (iv) it is unnecessary to use a tourniquet or snare around the SV, which will injure and twist this fragile vessel and complicate the placement of correct incision on it. After collateral artery is closed, there will be no excessive blood returning from the SV. By decreasing perfusion flow of CPB temporarily, combined with cardiotomy suction, the surgical field can be improved significantly and (v) manual inflation of lungs by an anaesthesiologist facilitates operator to observe the relationship between the SV and pericardium. If lungs collapse, the SV shifts from its natural position. Details on this pericardial tunnel technique are shown in Figure 3A and B. Postoperative management After the operation, all patients received mechanical ventilation and intensive care. Routine monitoring included invasive blood pressure, electrocardiogram, pulse oximetry and central venous pressure. Bronchoscopy was used for patients with prolonged mechanical ventilation (>3 days). Dopamine [5.0–7.5 μg/(kg⋅min)] and milrinone [0.5–0.75 μg/(kg⋅min)] were administrated routinely to all patients. Adrenaline [0.02–0.05 μg/(kg⋅min)] was administrated selectively for low cardiac output. Fluid balance was maintained. Following intraoperative transoesophageal echocardiography, bedside transthoracic echocardiography was performed 1–3 days after the operation. The patients underwent follow-ups 1, 3 and 6 months after discharge and then annually. Conventional follow-up surveillances consisted of Doppler echocardiography, electrocardiogram and chest X-ray. Because of the cost and concern of exposure to radiation, the cardiac catheterization and cardioangiography CT were not performed routinely in the follow-ups, unless the blood flow velocity of the SV >2 m/s (16 mmHg), without typical triphasic pattern of pulmonary vein, as detected by echocardiography. Statistical analysis Count data are expressed as numbers, frequencies and percentages. Measurement data are expressed as means ± standard deviations. RESULTS The mean CPB time was 104.8 ± 19.4 (range 77–141) min. The mean aorta cross-clamping time was 42.4 ± 16.0 (range 22–79) min. The mean postoperative mechanical ventilation time was 88.3 ± 63.8 (range 36–264) h (6 cases <3 days, 2 cases 3–7 days and 1 case >7 days). Postoperative data and complications are listed in Table 2. Table 2: Postoperative complications of SS patients with vertical form (n = 9) Complications  Dupuis’ classification   Total, n (%)  Infantile form (n = 5)  Childhood/ adult form (n = 4)  Prolonged mechanical ventilation (days)         3–7  2a  0  2 (22.2)   >7  1a,c  0  1 (11.1)  Low cardiac output      3 (33.3)   Caused by residual pulmonary hypertension  1  0  1 (11.1)   Caused by transient hypoxia  1  1  2 (22.2)  Peritoneal dialysis for renal insufficiency  1  1  2 (22.2)  Pneumonia  3a  2b  5 (55.5)  Pleural effusion  1  0  1 (11.1)  Plication of diaphragm for phrenoparalysis  1c    1 (11.1)  Complications  Dupuis’ classification   Total, n (%)  Infantile form (n = 5)  Childhood/ adult form (n = 4)  Prolonged mechanical ventilation (days)         3–7  2a  0  2 (22.2)   >7  1a,c  0  1 (11.1)  Low cardiac output      3 (33.3)   Caused by residual pulmonary hypertension  1  0  1 (11.1)   Caused by transient hypoxia  1  1  2 (22.2)  Peritoneal dialysis for renal insufficiency  1  1  2 (22.2)  Pneumonia  3a  2b  5 (55.5)  Pleural effusion  1  0  1 (11.1)  Plication of diaphragm for phrenoparalysis  1c    1 (11.1)  a These 3 patients underwent bronchoscopy with bronchoalveolar lavage taken for a microbiological test before extubation. Microorganisms detected in the bronchoalveolar lavage culture: Klebsiella pneumoniae (n = 1), Escherichia coli (n = 1) and Streptococcus pneumoniae (n = 1). b Microorganisms detected in the endotracheal secretion culture: Klebsiella pneumoniae (n = 1), negative (n = 1). c The 1st case of this study. The patient had been on a mechanical ventilator for 10 days after the reoperation using the pericardial tunnel technique. SS: scimitar syndrome. Table 2: Postoperative complications of SS patients with vertical form (n = 9) Complications  Dupuis’ classification   Total, n (%)  Infantile form (n = 5)  Childhood/ adult form (n = 4)  Prolonged mechanical ventilation (days)         3–7  2a  0  2 (22.2)   >7  1a,c  0  1 (11.1)  Low cardiac output      3 (33.3)   Caused by residual pulmonary hypertension  1  0  1 (11.1)   Caused by transient hypoxia  1  1  2 (22.2)  Peritoneal dialysis for renal insufficiency  1  1  2 (22.2)  Pneumonia  3a  2b  5 (55.5)  Pleural effusion  1  0  1 (11.1)  Plication of diaphragm for phrenoparalysis  1c    1 (11.1)  Complications  Dupuis’ classification   Total, n (%)  Infantile form (n = 5)  Childhood/ adult form (n = 4)  Prolonged mechanical ventilation (days)         3–7  2a  0  2 (22.2)   >7  1a,c  0  1 (11.1)  Low cardiac output      3 (33.3)   Caused by residual pulmonary hypertension  1  0  1 (11.1)   Caused by transient hypoxia  1  1  2 (22.2)  Peritoneal dialysis for renal insufficiency  1  1  2 (22.2)  Pneumonia  3a  2b  5 (55.5)  Pleural effusion  1  0  1 (11.1)  Plication of diaphragm for phrenoparalysis  1c    1 (11.1)  a These 3 patients underwent bronchoscopy with bronchoalveolar lavage taken for a microbiological test before extubation. Microorganisms detected in the bronchoalveolar lavage culture: Klebsiella pneumoniae (n = 1), Escherichia coli (n = 1) and Streptococcus pneumoniae (n = 1). b Microorganisms detected in the endotracheal secretion culture: Klebsiella pneumoniae (n = 1), negative (n = 1). c The 1st case of this study. The patient had been on a mechanical ventilator for 10 days after the reoperation using the pericardial tunnel technique. SS: scimitar syndrome. The sole reoperative patient underwent surgical revision on the 5th day after the initial operation of direct SV-to-left atrial anastomosis. During the reoperation, the SV was found to be of vertical form and short. There was tension on the SV and stenosis at the anastomosis. While the lungs were inflated, the SV and anastomosis were deformed. After the SV-to-left atrial anastomosis being taken down, the SV was reimplanted onto the right lateral pericardium. The oblique sinus of the pericardium was restored. An extension tunnel to the LA was created with a pericardial flap. The blood flow from the SV was directed into the LA through a left atriotomy inside tunnel. After the reoperation, her pulmonary congestion improved significantly. Because of phrenoparalysis and pneumonia, the patient was ventilator dependent. She underwent plication of diaphragm on the 7th day after the reoperation. Three days later, she was successfully weaned from ventilator. Figure 4 shows the CT image of the SV and pericardial tunnel in this patient before discharge. There was no in-hospital mortality or SV obstruction. Eight of 9 survivors were followed up after discharge, with 1 lost to follow-up. The mean follow-up time was 33.4 ± 19.2 (range 2–72) months. Echocardiography demonstrated that no SV obstruction developed during the follow-ups, and 7 patients had no pulmonary hypertension and 1 had mild pulmonary hypertension. Subsequently, the patients thrived without further symptoms of recurrent respiratory infection. They were in the New York Heart Association (NYHA) Class I. The mean left ventricular ejection fraction measured by last echocardiography was 67.6 ± 8.8% (range 57.9–80.8%). DISCUSSION Halasz first described the anomalous vein in SS as ‘scimitar-shaped’ in 1956 [4]. Dupuis et al. [2, 3] classified SS into infantile and childhood/adult forms, based on age and associated symptoms. In our study, there were 5 cases (55.6%) with infantile form. Patients with infantile form usually develop cardiac dysfunction, dyspnoea and recurrent respiratory infections. They have higher comorbidities correlated with the severity of associated defects, pulmonary hypertension and congestive heart failure [3]. The infantile form of SS has a higher surgical mortality rate [5] and rate of postoperative SV obstruction, especially for those younger than 3 months [6]. However, several groups advocated medical treatment or occlusion of collateral artery to improve symptoms and postpone surgical repair until early childhood [6, 7], QP/QS >1.5 is an indication for surgery in childhood [8]. Kirklin first completed surgical repair for SS with CPB in 1956, with the SV anastomosed to the right atrium and drained into the LA through an ASD using an intra-atrial pericardial baffle [9]. Then, Tornvall described the SV-to-left atrial anastomosis technique [10]. Both approaches remain the classical SV reimplantation techniques for surgical repair of SS. Another method created a long intra-atrial baffle from the orifice of the SV within the IVC to an ASD. This long baffle might cause intrabaffle thrombosis and obstruction of the IVC and might be difficult to construct in small infants [11]. The advantages and disadvantages of these conventional procedures remain debated. Because of the wide variation in SV anatomy, the rate of postoperative SV obstruction is 15.5–23.8% [5, 6] and that of reintervention is 11–30% [6, 12–14]. Several groups described other modified techniques for SV reimplantation to minimize postoperative complications, including SV reimplantation via anterior lateral thoracotomy without CPB [15] and interposed grafts for SV extension [16]. In 2014, Lugones and García [17] reported 1 case that underwent surgical repair for SS by construction of a pericardial tunnel. Before 2011, we used the classical technique above for SS repair but encountered postoperative problems, such as SV obstruction. We gradually realized that certain SVs had disparate courses and angulations at the insertion site on the IVC. In 2011, we attempted to combine several concepts and techniques of Senning procedure and sutureless repair for supra- or infracardiac total anomalous pulmonary venous connection as a surgical solution for a patient with residual SV obstruction after the classical direct SV-to-left atrial anastomosis. Ultimately, we successfully constructed a pericardial tunnel that was attached to the SV and relieved the residual SV obstruction. Because the preoperative condition of the 1st patient was complicated, we believed that her postoperative parameters were not attributable to the pericardial tunnel technique. Since then, we have increasingly considered SV anatomy. We classified SV into 2 anatomical forms—vertical and horizontal—based on its angulation to the IVC (Fig. 1 and 2). We found that the SVs of vertical form were always shorter than those of horizontal form, had sharper angulations to the IVC and right lateral wall of either atrium and were more distal to atrial wall. If an SV of vertical form is anastomosed directly to the right lateral wall of either atrium, the position of the anastomosis must be planned precisely in advance; otherwise, it might compromise the patency of that anastomosis and cause obstruction. When implanted more cephalad, these SVs tend to deform like a hook with kinking or torsion. However, if they are implanted more caudally, they will have significant tension. The position of anastomosis depends tremendously on surgeon’s experience and intraoperative judgement. In patients with an infradiaphragm SV-to-IVC connection, the SV is much more distal to atria, as reported in a case by Lugones and García [17], and there is always obstruction that is caused by tension after direct anastomosis. With a pericardial tunnel to which the SV of vertical form is attached, the course of the SV will be extended. Thus, the tension in the SV and anastomosis will be minimized, and the patency will be maintained well. However, for patients with horizontal form, this pericardial tunnel technique should not be the preferred procedure. SVs of horizontal form always pass through a longer course immediately above diaphragm before entering the IVC. These SVs can be easily anastomosed to either atrium with good mobility after dissection, for which some redundant length should be removed. The direct SV-to-atrium reimplantation is less likely to cause tension in anastomosis. In addition, an unnecessary pericardial tunnel might compromise the morphology of the SV and cause obstruction. Thus, we believe that the direct reimplantation is a more reasonable choice for those with horizontal form. On the basis of our understanding of 2 anatomical SV forms and our experience with the 1st case, we have preferred the classical technique for horizontal form and the pericardial tunnel technique for vertical form since 2011. Protection of phrenic nerve is important to surgical repairs for SS. Brink et al. [5] reported that the incidence of phrenic nerve palsy was 4.8% (1/21) in a group of patients whose surgical strategies included intra-atial baffle, direct reimplantation and pneumonectomy. In the multicentric study by Vida et al. [6], the incidence of phrenic nerve injury in the group of direct reimplantation (4/67, 6.0%) was significantly higher than in the group of intra-atrial baffle (1/38, 2.6%) (P = 0.04). However, Brown et al. [15] reported no incidence of phrenic nerve injury or palsy in 9 patients with mean age of 11.5 years who underwent direct reimplantation via a right anterior lateral thoracotomy without CPB. In our cohort, the incidence of phrenic never palsy was 11.1% (1/9). We do not believe that the phrenoparalysis in our 1st case was caused solely by the reoperation. We used the same protective technique as Senning procedure in this study. No phrenoparalysis occurred in subsequent patients. However, we do believe that the incidence of phrenic nerve injury has strong relationship to different surgical techniques and patient’s age. The dissection of the SV and pericardium near the right phrenic nerve while using direct reimplantation technique may be the reason of phrenic nerve injury, especially in younger patients whose phrenic nerve and diaphragm are more fragile. While using intra-atrial baffle technique, it is unnecessary to do such dissection of the SV and pericardium. However, further efforts must be made to protect the phrenic nerve for all patients. Limitations There were several limitations of this study. Because it was a retrospective study from a single centre, the selection bias might have reduced the accuracy of certain results. One of 9 (11.1%) patients was lost to follow-up, so that the incidence of postoperative pulmonary vein obstruction and mortality may be underestimated. More cases and data from longer follow-ups must be collected to obtain more accurate results and conclusions of this rare congenital heart anomaly. We will use magnetic resonance imaging as a routine surveillance for further mid-term and long-term follow-ups, because it does not use radiation and can provide more data on cardiovascular anatomy and function. This option will allow us to confirm the relationship between SV anatomy and reconstruction technique. A multicentre study is underway. CONCLUSIONS The preferred procedure is determined primarily by the SV anatomy. The pericardial tunnel technique is a favourable option for the SS patients with vertical form. ACKNOWLEDGEMENTS We are grateful to our illustrator, Jiguang Qin, for his generous help and artwork that demonstrates the surgical details of the pericardial tunnel technique. Conflictof interest: none declared. REFERENCES 1 Wang CC, Wu ET, Chen SJ, Lu F, Huang SC, Wang JK. Scimitar syndrome: incidence, treatment, and prognosis. Eur J Pediatr  2008; 167: 155– 60. Google Scholar CrossRef Search ADS PubMed  2 Dupuis C, Charaf LA, Brevière GM, Abou P, Rémy-Jardin M, Helmius G. The ‘adult’ form of the scimitar syndrome. Am J Cardiol  1992; 70: 502– 7. Google Scholar CrossRef Search ADS PubMed  3 Dupuis C, Charaf LA, Brevière GM, Abou P. ‘Infantile’ form of the scimitar syndrome with pulmonary hypertension. Am J Cardiol  1993; 71: 1326– 30. Google Scholar CrossRef Search ADS PubMed  4 Halasz NA, Halloran KH, Liebow AA. Bronchial and arterial anomalies with drainage of the right lung into the inferior vena cava. Circulation  1956; 14: 826– 46. Google Scholar CrossRef Search ADS PubMed  5 Brink J, Yong MS, d'Udekem Y, Weintraub RG, Brizard CP, Konstantinov IE. Surgery for scimitar syndrome: the Melbourne experience. Interact CardioVasc Thorac Surg  2015; 20: 31– 4. Google Scholar CrossRef Search ADS PubMed  6 Vida VL, Padalino MA, Boccuzzo G, Tarja E, Berggren H, Carrel T et al.   Scimitar syndrome: a European Congenital Heart Surgeons Association (ECHSA) multicentric study. Circulation  2010; 122: 1159– 66. Google Scholar CrossRef Search ADS PubMed  7 Korkmaz AA, Yildiz CE, Onan B, Guden M, Cetin G, Babaoglu K. Scimitar syndrome: a complex form of anomalous pulmonary venous return. J Card Surg  2011; 26: 529– 34. Google Scholar CrossRef Search ADS PubMed  8 Çiçek S, Arslan AH, Ugurlucan M, Yildiz Y, Ay S. Scimitar syndrome: the curved Turkish sabre. Semin Thorac Cardiovasc Surg Pediatr Card Surg Annu  2014; 17: 56– 61. Google Scholar CrossRef Search ADS PubMed  9 Kirklin JW, Ellis FH Jr, Wood EH. Treatment of anomalous pulmonary venous connections in association with interatrial communications. Surgery  1956; 39: 389– 98. Google Scholar PubMed  10 Tornvall SS, Jackson KH, Alvayay JC, Vargas AC, Koch W, Zarate E. Anomalous drainage of the pulmonary veins into the inferior vena cava. J Thorac Cardiovasc Surg  1961; 42: 413– 7. Google Scholar PubMed  11 Gudjonsson U, Brown JW. Scimitar syndrome. Semin Thorac Cardiovasc Surg Pediatr Card Surg Annu  2006; 9: 56– 62. Google Scholar CrossRef Search ADS   12 Vida VL, Speggiorin S, Padalino MA, Crupi G, Marcelletti C, Zannini L et al.   The scimitar syndrome: an Italian multicenter study. Ann Thorac Surg  2009; 88: 440– 4. Google Scholar CrossRef Search ADS PubMed  13 Dusenbery SM, Geva T, Seale A, Valente AM, Zhou J, Sena L et al.   Outcome predictors and implications for management of scimitar syndrome. Am Heart J  2013; 165: 770– 7. Google Scholar CrossRef Search ADS PubMed  14 Alsoufi B, Cai S, Van Arsdell GS, Williams WG, Caldarone CA, Coles JG. Outcomes after surgical treatment of children with partial anomalous pulmonary venous connection. Ann Thorac Surg  2007; 84: 2020– 6. Google Scholar CrossRef Search ADS PubMed  15 Brown JW, Ruzmetov M, Minnich DJ, Vijay P, Edwards CA, Uhlig PN et al.   Surgical management of scimitar syndrome: an alternative approach. J Thorac Cardiovasc Surg  2003; 125: 238– 45. Google Scholar CrossRef Search ADS PubMed  16 Lam TT, Reemtsen BL, Starnes VA, Wells WJ. A novel approach to the surgical correction of scimitar syndrome. J Thorac Cardiovasc Surg  2007; 133: 573– 4. Google Scholar CrossRef Search ADS PubMed  17 Lugones I, García R. A new surgical approach to scimitar syndrome. Ann Thorac Surg  2014; 97: 353– 5. Google Scholar CrossRef Search ADS PubMed  © The Author(s) 2018. Published by Oxford University Press on behalf of the European Association for Cardio-Thoracic Surgery. All rights reserved. This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices)

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Interactive CardioVascular and Thoracic SurgeryOxford University Press

Published: Mar 28, 2018

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