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Aortopulmonary collaterals in neonates with d-transposition of the great arteries – Clinical significance early after arterial switch operation
IJCA-25996; No of Pages 6 International Journal of Cardiology xxx (2017) xxx–xxx
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Aortopulmonary collaterals in neonates with d-transposition of the great arteries – Clinical significance early after arterial switch operation☆ Alexandra Wipf a,b,1, Martin Christmann a,b,⁎,1, Susanne Navarini-Meury a,b, Hitendu Dave b,c, Daniel Quandt a,b, Walter Knirsch a,b,1, Oliver Kretschmar a,b,1 a b c
Paediatric Cardiology, University Children's Hospital, Zurich, Switzerland Children's Research Center, University of Zurich, Switzerland Division of Congenital Cardiovascular Surgery, University Children's Hospital, Zurich, Switzerland
a r t i c l e
i n f o
Article history: Received 8 August 2017 Received in revised form 14 December 2017 Accepted 30 January 2018 Available online xxxx Keywords: dTGA Arterial switch operation MAPCA Cardiac catheterization
a b s t r a c t Objectives: Purpose of this study is to evaluate the clinical significance of major aortopulmonary collateral arteries (MAPCAs) during the early postoperative course after arterial switch operation (ASO) in d-transposition of the great arteries (dTGA). Methods: Clinical data of 98 patients with simple dTGA between January 2007 and December 2016 at the University Children's Hospital Zurich, Switzerland were analyzed retrospectively. Results: 37 from 98 patients (38%) required cardiac catheterization (CC) due to an early complicated postoperative course or difficult coronary transfer due to special coronary anatomy. In 15 (15%) patients, hemodynamically relevant MAPCAs were found during CC and coil embolization was performed. Patients with relevant MAPCAs had a significantly longer PICU stay (7 versus 6 days, p = 0.021), longer hospital stay (41 versus 27 days, p = 0.005), longer mechanical ventilation time (5 versus 3 days, p = 0.005), longer need for inotropic support (5 versus 4 days, p = 0.001) and delayed chest closure time (3 versus 2 days, p = 0.030) in those in whom it was left open in comparison to all other patients. In patients having CC, pre-surgery oxygen saturation was significantly lower in patients with relevant MAPCAs (58% vs 70%, p 0.019). Echocardiography had a sensitivity of 53% and a specificity of 100% in detecting relevant MAPCAs, accurately. Conclusions: MAPCAs are frequently found in dTGA patients and can be associated with lower baseline oxygen saturation and a prolonged postoperative course after ASO. Transthoracic echocardiography cannot replace CC as diagnostic tool. If significant MAPCAs are suspected, early CC should be performed for diagnostic and therapeutic reasons. © 2017 Elsevier B.V. All rights reserved.
1. Introduction Nowadays, standard surgical management for simple type of d-transposition of the great arteries (dTGA) is the arterial switch operation (ASO), if coronary anatomy and valvular morphology allow this surgical technique [1,2]. Despite good short and longterm results with ASO in patients with dTGA, enlarged bronchial arteries/major aortopulmonary collateral arteries (MAPCAs) are
☆ Funding Source: None. Financial Disclosure: All authors have no financial relationships relevant to this article to disclose. Conflict of Interest: All authors have no potential conflicts of interest to disclose. ⁎ Corresponding author at: Paediatric Cardiology, University Children's Hospital, Steinwiesstrasse 75, 8032 Zurich, Switzerland. E-mail address: [email protected] (M. Christmann). 1 Both first and both last authors contributed equally to this work.
possible findings in this patient group [2–4]. MAPCAs are often clinically irrelevant, but may cause congestive heart failure after surgical repair due to significant left-to-right shunting [4–7]. Possible symptoms of hemodynamic relevant MAPCAs are pulmonary volume overload, respiratory failure, left atrial and ventricular dilatation as well as dysfunction, failure to thrive, tachycardia or arrhythmias [6,7]. The gold standard for the diagnosis of hemodynamically significant MAPCAs after ASO is angiography during cardiac catheterization (CC). As CC after ASO is not performed on a routine basis, mostly patients with a complicated postoperative course or difficult coronary transfer due to special coronary anatomy undergo further invasive evaluation. In other case series, treatment of symptomatic MAPCAs was performed by transcatheter coil embolization of the collateral vessels [5–9]. Aim of this study was to evaluate the incidence and clinical significance of MAPCAs during the early postoperative course after ASO for surgical repair of dTGA.
https://doi.org/10.1016/j.ijcard.2018.01.132 0167-5273/© 2017 Elsevier B.V. All rights reserved.
Please cite this article as: A. Wipf, et al., Aortopulmonary collaterals in neonates with d-transposition of the great arteries – Clinical significance early after arterial switch operation, Int J Cardiol (2017), https://doi.org/10.1016/j.ijcard.2018.01.132
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A. Wipf et al. / International Journal of Cardiology xxx (2017) xxx–xxx
2. Materials and methods
category” published by L. Bergersen et al. [13], which distinguishes 4 different risk categories [1–4], as well as their “definitions for adverse event severity” (adverse event severity level 1–5) [13].
2.1. Study population In this retrospective monocentric cohort study, we analyzed clinical data of patients with simple dTGA undergoing ASO between January 2007 and December 2016 at the University Children's Hospital of Zurich, Switzerland. Simple TGA was defined by the International Pediatric and Congenital Cardiac Code of the Association for European Pediatric and Congenital Cardiology (IPCCC-AEPC) [10] ICD-10 Code Q20.3 and could be accompanied by a patent foramen ovale (PFO, ≤ 3 mm), atrial septal defect (ASD, N3 mm), persistent arterial duct (PDA), ventricular septal defect (VSD) and/or vessel and valve abnormalities like coarctation of the aorta (CoA) or pulmonary valve stenosis. Patients with other cardiac comorbidities [e.g. atrio-ventricular septal defect (AVSD) or double outlet right ventricle (DORV)] were classified as complex TGA and were not included in this study. Indications for postoperative CC were difficult intraoperative coronary transfer during ASO, signs of ischemia (ST changes or exceptionally elevated troponin levels), arrhythmia or prolonged intensive care with prolonged mechanical ventilator support and prolonged need for inotropic agents (milrinone or adrenalin). CC included hemodynamic evaluation and contrast angiography for coronary arteries and MAPCAs. MAPCAs were defined as hemodynamically relevant if injection of contrast agent into the MAPCAs was followed by a clearly visible opacification of the correspondent pulmonary veins. Two groups were created based on these findings: Patients a) with (Group I) or b) without hemodynamically relevant MAPCAs (Group II). The latter includes patients who did not undergo CC (Group II A) and patients without relevant MAPCAs in CC (Group II B) (Tables 1 and 2).
2.3. Data collection Clinical data (patients' demographics, co-morbidities, data on intraoperative and postoperative course, data on CC) were extracted from patient medical records. 2.4. Statistical analysis The data is presented as median with interquartile range (IQR) or mean ± standard deviation (SD), as appropriate. Categorical data is expressed as counts and percentages. Comparison of percentages was performed by the use of Pearson's Chi-Square test or Fishers' exact test when appropriate, those of mean values by Students' t-test and those of median values by the Mann-Whitney U test. If significant differences occurred, posthoc analysis with appropriate p-value adjustment for multiple testing was performed. Significance testing was 2-sided with the significance level set at p b 0.05. 2.5. Ethics All data was obtained primarily for medical purposes. The study design fulfills the guidelines of the Declaration of Helsinki regarding ethical principles for medical research involving human subjects. The study was approved by the institutional ethical board.
3. Results
2.2. Treatment techniques Surgical procedures were performed using moderately hypothermic cardiopulmonary bypass and cold blood cardioplegic arrest. When necessary, repeat cardioplegia by selective cannulation of the coronary buttons was performed. ASO included switching of the aorta and the pulmonary roots, coronary button transfer, obligatory ligation and transection of PDA, and closure of ASD and VSD (as indicated) [11,12]. Lecompte-maneuver (translocation of the pulmonary bifurcation anterior to the neo-aorta) was performed as a rule. Taking into account the limitations that such a retrospective data analysis involves, there were no indicators in the MAPCA group to suggest increased non-coronary blood return during extracorporeal circulation (ECC) which could be indicative of MAPCAs. No routine postoperative angiograms were performed. CC was performed under general anesthesia and mechanical ventilation. Femoral arterial vascular access was achieved via a 4 Fr introducer sheath in all patients. After hemodynamic assessment and aortic angiography, relevant MAPCAs were selectively cannulated by using a thin-walled end-hole catheter and a 0.014 in. torque wire. In those patients with MAPCAs judged to be hemodynamically relevant (Group I), micro catheters (e.g. Cantata®, COOK Medical/Bloomington/U.S.A.) were used for coil delivery using MRI-compatible coils (BALT Extrusion Spirale® embolization coil). To categorize the risk for the cardiac catheterization procedures we used the “procedure type risk
3.1. Patient characteristics 103 neonates with simple dTGA were treated with ASO including Lecompte-maneuver between January 2007 and December 2016. 5 patients were excluded from the analysis due to missing parental consent or loss of follow up. Two patients died postoperatively during hospital stay. Both had an emergency ASO, one on the first and the other one on the second day of life due to insufficient arterial oxygen saturation despite adequately sized atrial septal defect and PDA. The first patient died because of severe left coronary artery stenosis with myocardial infarction despite multiple surgical revisions at the age of 12 days (12 days after ASO, 11 days after diagnostic CC) and the other patient due to severe postoperative mitral regurgitation and heart failure at the age of 17 days (16 days postoperatively, 9 days after diagnostic CC). CC showed normal coronary arteries in this patient. Overall,
Table 1 Baseline characteristics of patients with and without relevant MAPCAs.
Numbers of patients n (%) Male n (%) GD, days (mean ± SD), n = 96 Weight, grams (median (IQR)), n = 98 Height, cm (mean ± SD), n = 96 Atrial septal with: − No atrial septal defect n (%) − PFO b 3 mm n (%) − ASD II N 3 mm n (%) VSD n (%) Coronary anatomy: n (%) − − − −
Normal LCX ex RCA Single-coronary ostium Others
Rashkind n (%) SpO2 before Rashkind (mean ± SD) SpO2 after Rashkind (median (IQR)) SpO2-difference after Rashkind (median (IQR))
Total
Patients with relevant MAPCAs in CC (Group I)
Classified as no relevant MAPCAs (Group II)
Patients without CC (Group II A)
Patients with no or no relevant MAPCAs in CC (Group II B)
p-Value *
98 (100) 70 (71) 274.69 ± 12.76 3455 (2990–3863) 50 ± 3
15 (15) 7 (47) 269.00 ± 11.95 3050 (2720–3460) 49.47 ± 2.5
83 (85) 63 (76) 275.72 ± 12.70 3500 (3000–3880) 49.81 ± 2.7
61 (62) 46 (75) 275.33 ± 13.64 3600 (3000–3910) 50 ± 3
22 (23) 17 (77) 275.82 ± 9.79 3455 (3070–3680) 49.34 ± 1.8
– 0.021 0.060 0.050 0.650 0.297
1 (1) 48 (49) 49 (50)
0 (0) 10 (67) 5 (33)
1 (1) 38 (46) 44 (53)
1 (2) 32 (52) 28 (46)
0 (0) 6 (27) 16 (73)
30 (30.6)
5 (33)
25 (30)
14 (23)
11 (50)
67 (68.4) 10 (10.2) 7 (7.1) 14 (14.3)
8 (53) 2 (13) 2 (13) 3 (20)
59 (71) 8 (10) 5 (6) 11 (13)
49 (80) 3 (5) 2 (3) 7 (12)
10 (46) 5 (23) 3 (14) 4 (18)
75 (76.5) 63 ± 16 85 (80–90) 20 (14–35)
13 (87) 58 ± 12 85 (79–90) 23 (19–36)
62 (75) 64 ± 17 85 (80–90) 20 (13−33)
49 (80) 62 ± 17 85 (80–90) 20 (13–34)
13 (59) 70 ± 15 87 (84–90) 23 (15–28)
0.770 0.385
0.509 0.205 0.786 0.339
Group I: “Patients with relevant MAPCAs in CC”; Group II: “Classified as no relevant MAPCAs”, includes Group II A (“Patients without CC”) and Group II B (“Patients with no or no relevant MAPCAs in CC”). (*) p-value calculated for the comparison of Groups I and II. n: numbers of patients; SD: standard deviation; IQR: interquartile range; GD: gestation days; PFO: persistent foramen ovale; ASD: atrial septal defect; VSD: ventricle septum defect; LCX ex RCA: left circumflex ex right coronary artery; Data shown as mean ± standard deviation, median and interquartile range (IQR) or number and percent in general study population.
Please cite this article as: A. Wipf, et al., Aortopulmonary collaterals in neonates with d-transposition of the great arteries – Clinical significance early after arterial switch operation, Int J Cardiol (2017), https://doi.org/10.1016/j.ijcard.2018.01.132
A. Wipf et al. / International Journal of Cardiology xxx (2017) xxx–xxx
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Table 2 Operative and postoperative characteristics of patients with and without relevant MAPCAs.
ECC time (median (IQR)), n = 96 ACC time (median (IQR)), n = 96 OP time (median (IQR)), n = 89 Troponin T (μg/l) (median (IQR)), n = 79 Age at OP (d) (median (IQR)), n = 98 Postop hospital stay (d) (median (IQR)), n = 96 Ventilation time (d) (median (IQR)), n = 96 Inotropic support time (d) (median (IQR)), n = 95 PICU stay (d) (median (IQR)), n = 96 Duration open thorax (d) (median (IQR)), n = 46 Total hospital stay (d) (median (IQR)), n = 96
Total
Patients with relevant MAPCAs in CC (Group I)
Classified as no relevant MAPCAs (Group II)
Patients without CC (Group II A)
Patients with no or no relevant MAPCAs in CC (Group II B)
p-Value *
172 (143–200) 111 (89–136) 262 (228–299) 5.87 (3.87–8.40) 9 (6–12) 17 (14–24) 3 (2–4) 4 (2–5) 6 (4–7) 2 (2–3) 27 (22–37)
175 (149–263) 111 (84–164) 276 (244–319) 5.3 (4.57–9.9) 9 (6–12) 24 (15–40) 5 (2–7) 5 (4–8) 7 (6–13) 3 (2–6) 41 (24–50)
170 (139–199) 111 (90–135) 261 (221–298) 5.89 (3.73–8.11) 9 (6–12) 16 (14–22) 3 (1–4) 4 (2–5) 6 (4–7) 2 (2–3) 27 (22−33)
165 (128–195) 110 (88–135) 258 (208–290) 5.61 (3.28–7.53) 9 (7–12) 15 (13−20) 2 (1–3) 4 (2–5) 5 (4–7) 2 (1–3) 27 (22−31)
193 (168–215) 120 (95–145) 287 (253–340) 8.59 (5.63–10.28) 8 (5–10) 22 (17–29) 3 (2–5) 4 (3–5) 7 (4–9) 2 (2–3) 30 (24–37)
0.126 0.273 0.474 0.187 0.862 0.001 0.005 0.001 0.021 0.030 0.005
Group I: “Patients with relevant MAPCAs in CC”; Group II: “Classified as no relevant MAPCAs”, includes Group II A (“Patients without CC”) and Group II B (“Patients with no or no relevant MAPCAs in CC”). (*) p-value calculated for the comparison of Groups I and II. n: numbers; SD: standard deviation; IQR: interquartile range; CC: cardiac catheterization; OP: operation; PICU: pediatric intensive care unit; ECC: extra corporal circulation; ACC: aortic cross clamp. Data shown as mean ± standard deviation, median and interquartile range (IQR) or number and percent in general study population.
98 patients could be included in our study, out of which 70 patients (71%) were male. Seventy five patients (77%) underwent an atrial septostomy procedure (Rashkind maneuver) within the first hours of life. Additional VSD closure was performed in 30 patients (31%). In 16 patients (16%) there was another relevant cardiac abnormality treated during the same surgery such as AV-valve reconstruction (7%), resection of coarctation of the aorta (CoA) with end-to-end anastomosis (7%), pulmonary valvuloplasty (2%) and others (2%). Thirty-one patients (32%) had coronary artery abnormalities (Table 1). The median age at time of ASO was 9 days (IQR: 6–12). Delayed secondary sternal closure was performed in 48 patients (49%). Two patients (2%) needed early redo-surgery due to relevant coarctation of the aorta after ASO, three patients (3%) underwent secondary surgical plication of the diaphragm due to paralysis. Three patients (3%) needed a surgical revision of the left coronary artery by use of a patch plasty (V. saphena magna or autologous pericardium) due to an ostial stenosis of the left coronary artery at the age of 7, 11, and 62 days, respectively. The baseline characteristics of all patients are presented in Table 1. The flow chart in Fig. 1 describes the study population concerning postoperative course and results obtained during CC. 3.2. Analysis of patients requiring cardiac catheterization 37 (37.8%) patients underwent postoperative CC due to a complicated postoperative course or difficult coronary transfer due to special coronary anatomy. Median age at catheterization was 29 days (IQR: 17–59). 20 (54%) of these 37 patients had one or more MAPCAs, of which 15 (41% of all patients with CC) were rated hemodynamically relevant and underwent transcatheter coil embolization (Fig. 2a and b). Median number of coiled MAPCAs was 3 (IQR: 2–3). Median time between surgery and catheterization was 15 days (IQR: 12–48). Patients with relevant MAPCAs had a significantly longer PICU stay (7 versus 6 days, p = 0.021), longer hospital stay until discharge (41 versus 27 days, p = 0.005), longer postoperative mechanical ventilation time (5 versus 3 days, p = 0.005), longer need for inotropic support (5 versus 4 days, p = 0.001) and delayed chest closure (3 versus 2 days, p = 0.030) in those in whom the sternum was left open (Table 2). No significant difference in early postoperative troponin T, ECC, ACC (aortic cross clamp) and surgical procedure time was seen between the two groups. Systolic blood pressure before CC was significantly lower (p = 0.038) in patients undergoing coil embolization whereas diastolic pressure and blood pressure amplitude did not differ significantly. Details are summarized in Table 2. When comparing children undergoing CC only (total n = 37, n = 15 with relevant MAPCAs, n = 22 without relevant/no MAPCAs, s. Fig. 1), we found no significant difference of sex (p 0.069), body weight (p 0.118) and height (p 0.858). Diastolic blood pressure during CC
under general anesthesia showed a trend towards lower values in the relevant MAPCA group (median 28 vs 34 mm Hg). In contrast, baseline oxygen saturation before Rashkind procedure differed significantly between the two groups (mean 58% vs 70%, p 0.019). Concerning operative and postoperative parameters we found a trend towards longer duration of inotropic support (median 5 vs 4 days, p 0.059) and towards longer hospitalisation till discharge (median 41 to 30 days, p 0.069) in the relevant MAPCA group. No significant difference for the other operative or postoperative factors was found. In the 15 patients who underwent coil embolization of MAPCAs, this resulted in complete closure of the MAPCAs in all of them. One to four MAPCAs were closed with one, two or three detachable MRIcompatible Platin coils (BALT coils™, BALT Extrusion, Montmorency, France) per MAPCA in a single patient. Mostly, MAPCAs were found arising from the descending aorta but in some cases they originated from the ascending aorta or from the vertebral or mammarian arteries. 9 patients were extubated immediately after CC and did not need readmission to the PICU. Of the remaining 6 patients, three needed ongoing intensive care treatment due to pulmonary hypertension (1 patient) or ongoing inotropic support (2 patient) and 3 patients underwent re-surgery just before or shortly after CC (diaphragmatic plication, closure of residual ASD and revascularization of the coronary artery). No major complications occurred after CC intervention. Pre-catheterization, during echocardiography, MAPCAs were suspected in 8 of the 15 patients (53%) with relevant MAPCAs. According to the risk categories of Bergersen et al. [13] the mean Bergersen Score in all patients with CC was 2.6 (IQR: 2–4) which indicates a moderate risk. The mean Adverse Event Severity Score (AES) was 1.4 (IQR: 1–3) (between none and minor). 4. Discussion This study aims to evaluate the clinical significance of MAPCAs in the early postoperative course after ASO. In a cohort of 98 neonates with dTGA, hemodynamically relevant MAPCAs could be found in a not negligible number of patients (15%). Our findings demonstrate that patients with relevant MAPCAs have a complicated and prolonged postoperative course with a significantly longer PICU stay, and with prolonged inotropic support and ventilation time. The embryological development of MAPCAs in association with dTGA is rarely described in literature to date. MAPCAs are remnants of the embryonic ventral splanchnic arteries [13]. In the first weeks of gestation, together with the onset of the formation of the normal pulmonary arterial system, these systemic-to-pulmonary collateral arteries normally start to regress as they are not preprogrammed to “survive” after birth [14,15]. When there is early underdevelopment of the pulmonary arterial system or the pulmonary valve, MAPCAs may
Please cite this article as: A. Wipf, et al., Aortopulmonary collaterals in neonates with d-transposition of the great arteries – Clinical significance early after arterial switch operation, Int J Cardiol (2017), https://doi.org/10.1016/j.ijcard.2018.01.132
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Fig. 1. Flow chart of all patients. n: numbers of patients; dTGA: d-transposition of the great arteries; LFO: loss to follow up; ASO: arterial switch operation; CC: cardiac catheterization; MAPCA: major aortopulmonary collateral artery; other findings: dilatation/stenting of pulmonary artery/aortic arch.
persist, seen especially in pulmonary atresia (PA) or Tetralogy of Fallot (ToF), thereby ensuring sufficient postnatal pulmonary blood flow [14,15]. These heart defects are characterized by reduced oxygen saturation in blood postnatally (reduced pulmonary blood flow with rightto-left shunting via VSD and/or ASD in PA and ToF, parallel circulations with reduced mixing of blood in dTGA). One explanation for the persistence or the re-opening of MAPCAs in dTGA might be either a reduced arterial partial oxygen pressure or a reduced blood flow through the pulmonary arteries both indicating a relevant oxygen deficiency. In univentricular heart defects after bidirectional Glenn anastomosis (stage 2 palliation according to Norwood), MAPCAs are often found during pre-Fontan catheterization. It has recently been shown that there was no association between collateral flow and oxygen saturations measured at time periods before the Stage 2 operation [16], questioning the assumption that cyanosis is a trigger for the development of MAPCAs in this patient group. Nevertheless, it has been shown, that acyanotic postoperative patients do not have the same burden of MAPCAs [17] and that collateral flow is responsible for a meaningful additional degree of pulmonary blood flow with the capacity to increase oxygen saturation [18]. Going along with the cyanosis theory, when looking at the neonates needing CC in our study population (Group I vs Group II B), we found lower mean oxygen saturation values before Rashkind in the relevant MAPCA group (p 0.019). Beside reduced oxygen saturation, chest wall stress and pleural inflammation, caused e.g. by prolonged ICU stay with prolonged ventilator support, provide stimuli for MAPCA growth or re-opening, which might have had an influence in our study population as well [16]. Although several case reports have addressed the relevance of MAPCAs in dTGA, it has been poorly investigated in larger studies [6,7,19]. To our knowledge, only one study from Wernovsky et al. in 1993 discussed the relevance of MAPCAs in the long-term follow-up after ASO [20].
Regarding baseline patient characteristics, we did not find any association to relevant MAPCAs (Table 1). In contrast, Wernovsky et al. [20] found an association of MAPCAs to dTGA with intact ventricular septum, without any explanation of this phenomenon. In contrast to other case reports [4,8,19], with an incidence of at least 15% of all neonates with dTGA treated by ASO in our patient cohort, we can argue that hemodynamically significant MAPCAs are not a rare finding. Several studies [4,6,21,22] analyzed a higher incidence of MAPCAs in late repair by ASO but did not define “late” and “higher” in their studies. Using our definition of significant MAPCAs, there was no difference in age at ASO between patients with and without relevant MAPCAs (median age at OP 9 days (IQR: 6–12) in patients with and without MAPCAs, p = 0.862) (Table 2). Nevertheless concerning timing of ASO it has to be taken into account that only patients with a complicated postoperative course underwent CC and that a huge number of patients have not been catheterized in whom the status of MAPCAs might be underestimated. We could also show that relevant MAPCAs have an influence on the postoperative course after ASO, with prolonged inotropic support (5 days (IQR: 4–8) versus 4 days (IQR: 2–5), p = 0.001), longer ventilation time (5 days (IQR: 2–7) versus 3 days (IQR: 1–4), p = 0.005) and PICU stay (7 days (IQR: 6–13) versus 6 (IQR: 4–7), p = 0.021) compared to dTGA patients without relevant MAPCAs. When comparing operative and postoperative parameters between patients receiving CC only (Group I vs Group II B), we only found a trend towards longer duration of inotropic support (median 5 vs 4 days, p 0.059) and towards longer hospitalisation till discharge (median 41 to 30 days, p 0.069) in the relevant MAPCA group, presumably due to the small sample size of patients with CC. Other risk factors for the prolonged postoperative course could be excluded. Nevertheless, these findings could only be evaluated retrospectively. Therefore, we unsuccessfully tried to find predicting parameters suggesting hemodynamically significant
Please cite this article as: A. Wipf, et al., Aortopulmonary collaterals in neonates with d-transposition of the great arteries – Clinical significance early after arterial switch operation, Int J Cardiol (2017), https://doi.org/10.1016/j.ijcard.2018.01.132
A. Wipf et al. / International Journal of Cardiology xxx (2017) xxx–xxx
Fig. 2. a: Angiography (aortic arch) showing MAPCAs originating from the descending aorta to both lungs. b: Closure of MAPCAs using BALT coils in the same patient.
MAPCA directly after ASO. Clinical evaluation of blood pressure did not show a significant difference in diastolic blood pressure or blood pressure amplitudes during PICU stay, whereas during CC under general anesthesia, diastolic blood pressures were lower in the relevant MAPCA group. Systolic blood pressure showed only a minor difference, which we judged to be an accidental finding. Shikata et al. [15] postoperatively measured a diastolic pressure in the femoral artery of b30 mm Hg, suggesting a diastolic steal effect of the MAPCA, as a neoaortic regurgitation had been excluded [14]. A low diastolic blood pressure or high blood pressure amplitude would be parameters clinically easy to obtain and to evaluate. As our population showed blood pressure values within normal ranges just before CC (77 ± 13/45 ± 8 mm Hg) our findings
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do not support blood pressure as a reliable parameter to detect relevant MAPCAs. With postoperative transthoracic echocardiography performed before CC, 8 relevant MAPCAs were detected/assumed and later confirmed by CC. However, 7 relevant MAPCAs detected by CC were not seen in echocardiography. These findings suggest that echocardiography does not sufficiently detect relevant MAPCAs (sensitivity 53%), while a positive echo-finding (flow in color Doppler suspicious for a collateral vessel, left atrial/left ventricle dilatation, left ventricle dysfunction or backflow in descending aorta) correlates well with a positive result in CC (specificity 100%). Therefore, we support the study of Maddali et al. [23] who stated in their case report that detection of MAPCAs can be done by echocardiography, however we advise caution, as negative echocardiographic findings do not exclude the presence of relevant MAPCAs. Even though MAPCAs might been seen in echocardiography, the relevance of MAPCAs might be underestimated, particularly if the focus of the examination is put on other details. Taking our incidence of relevant MAPCAs into account (15%), we suggest focusing more on signs of diastolic run off during echocardiography as described above in children with complicated courses after ASO and lower pre-surgery oxygen saturations. Qp:Qs calculations according to Fick are not meaningful in several MAPCA-patients, as collateral vessels enter the pulmonary circuit distally at the precapillary level, precluding shunt calculation, as already stated in Wernowsky et al. [20]. Without doubt CC is the gold standard for the diagnosis of relevant MAPCAs [5]. Single case reports [23] also described prolonged ventilation time in patients with MAPCAs after uncomplicated ASO, nevertheless they did not comment on the time in detail. Further postoperative variables such as inotropic support, duration of an open chest, PICU, or hospital stay were not analyzed in these surveys. As we stated above, all these parameters were significantly prolonged in patients with relevant MAPCAs in our study. As prediction of relevant MAPCAs by clinical findings and echocardiography might be difficult and due to the high incidence of relevant MAPCAs in our study complicating the postoperative course, the optimal time point of angiography for MAPCA detection needs to be discussed. With the analyzed parameters, we could not find a cut-off for an exact point in time for catheterization. Santoro et al. [6] stated that even selective aortic angiography could rarely detect MAPCAs before surgical repair. They assumed that local pulmonary hypoxemia as well as ductal “steal” masks the flow through these vessels, leading to vasoconstriction [6,8]. In addition, Irving et al. [8] attributed the increased appearance of MAPCAs after ASO as a result of higher left-to-right shunting with improved cardiac output [due to better LV preload postoperatively [19]]. Consequently, a routine CC before ASO would probably not help to detect MAPCAs earlier. Possibly, special hybrid aortic root injection performed routinely after ASO in the operation room might help to detect relevant MAPCAs earlier. Early detection would naturally reduce postoperative morbidity, and other interventions, and costs. In our setting, selective CC was conducted at a median age of 29 days and median time interval of 15 days after surgery. The median age at catheterization with coil embolization of patients with relevant MAPCAs was 30 days (IQR: 17–38) whereas 2 patients had late coil embolization (166 days and 414 days) due to late complications (arrhythmia and cardiorespiratory instability on long-term ventilation). Concerning the technique of occluding MAPCAs, most of the reports [4,19,20,23] used coil embolization with successful occlusion, as we did in our patient group. Only one case report described the additional use of a vascular plug for MAPCA closure [7]. The only larger study [20] examining MAPCAs in dTGA after ASO, performed CC at a median age of 11.2 months and did not mention the indication for CC. Of all 119 patients, they found relevant MAPCAs according to our definition in 55 patients and closed them in those 5 patients (9%) with markedly enlarged collateral vessels. Nevertheless, all of their patients, including the 5 in whom MAPCAs were closed, were asymptomatic without any medication. These findings lead to the assumption that significant
Please cite this article as: A. Wipf, et al., Aortopulmonary collaterals in neonates with d-transposition of the great arteries – Clinical significance early after arterial switch operation, Int J Cardiol (2017), https://doi.org/10.1016/j.ijcard.2018.01.132
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MAPCAs – even untreated – might have a rather benign short and longterm course. On the other hand, it might be possible that these vessels have a major impact to overcome the early postoperative course after ASO, which might become less important during follow-up after recovery from acute postoperative hemodynamic impairment. Our indications for CC are summarized in the methods section. As N50% of all CC revealed significant MAPCAs, we believe that our indication for CC was acceptably accurate. CCs performed were safe with no peri- and/or postinterventional complications occurring in our cohort, even though the “procedure type risk category” [13] had a mean value of 2.6. Recently, a new scoring system by the Bergersen group has been published [24] and other risk scores are available as well [25] with a more detailed risk stratification, which might be used instead in larger patient populations. The AES showed a mean of 1.4, which represents a severity level between none and minor. 4.1. Limitations The retrospective design of this study is one of the limiting factors. The long duration of the study period involved two cardiac surgery teams with changes in management that may have affected the postoperative course. However, the minor variations in surgical technique pursued are unlikely to have impacted the incidence and treatment of MAPCAs. The strategy regarding diagnosis and treatment of MAPCAs did not change in this period. There is no data assessed about long term outcome. As we did not conduct a routine CC after ASO, the prevalence of MAPCAs may be underestimated in our cohort. Though, in our observation period, none of the patients without initial CC had any corresponding clinical aggravation, even with possibly missed MAPCAs. Concerning the risk categorization for CC other scoring systems have been published recently.
[4]
[5]
[6]
[7]
[8]
[9]
[10]
[11] [12]
[13]
[14]
[15]
[16]
5. Conclusion Our study adds significant knowledge to the clinical impact of MAPCAs after ASO in patients with dTGA. Beside lower baseline saturation before surgery, chest wall stress and pleural inflammation due to prolonged ICU stay with ventilator support might be triggers for the development of these collateral vessels. With a 15% incidence rate and negative influence on the postoperative course after ASO in dTGApatients, early diagnosis of MAPCAs with cardiac catheterization is recommended, as echocardiography only has a high specificity (100%) but low sensitivity (53%) in detecting them. Echocardiography should have a special focus on signs of diastolic run-off. In the absence of other clinical parameters to identify MAPCAs, CC should be performed whenever there is a high level of clinical suspicion, even with normal echocardiography. Further research is needed to better identify patients with relevant MAPCAs and to define the optimal point in time for cardiac catheterization and embolization. Also, studies concerning the long-term outcome of patients with relevant MAPCAs and the relevance of initially insignificant MAPCAs at follow-up are needed.
[17]
[18]
[19]
[20]
[21]
[22]
[23]
[24]
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Please cite this article as: A. Wipf, et al., Aortopulmonary collaterals in neonates with d-transposition of the great arteries – Clinical significance early after arterial switch operation, Int J Cardiol (2017), https://doi.org/10.1016/j.ijcard.2018.01.132
Contents lists available at ScienceDirect
International Journal of Cardiology journal homepage: www.elsevier.com/locate/ijcard
Aortopulmonary collaterals in neonates with d-transposition of the great arteries – Clinical significance early after arterial switch operation☆ Alexandra Wipf a,b,1, Martin Christmann a,b,⁎,1, Susanne Navarini-Meury a,b, Hitendu Dave b,c, Daniel Quandt a,b, Walter Knirsch a,b,1, Oliver Kretschmar a,b,1 a b c
Paediatric Cardiology, University Children's Hospital, Zurich, Switzerland Children's Research Center, University of Zurich, Switzerland Division of Congenital Cardiovascular Surgery, University Children's Hospital, Zurich, Switzerland
a r t i c l e
i n f o
Article history: Received 8 August 2017 Received in revised form 14 December 2017 Accepted 30 January 2018 Available online xxxx Keywords: dTGA Arterial switch operation MAPCA Cardiac catheterization
a b s t r a c t Objectives: Purpose of this study is to evaluate the clinical significance of major aortopulmonary collateral arteries (MAPCAs) during the early postoperative course after arterial switch operation (ASO) in d-transposition of the great arteries (dTGA). Methods: Clinical data of 98 patients with simple dTGA between January 2007 and December 2016 at the University Children's Hospital Zurich, Switzerland were analyzed retrospectively. Results: 37 from 98 patients (38%) required cardiac catheterization (CC) due to an early complicated postoperative course or difficult coronary transfer due to special coronary anatomy. In 15 (15%) patients, hemodynamically relevant MAPCAs were found during CC and coil embolization was performed. Patients with relevant MAPCAs had a significantly longer PICU stay (7 versus 6 days, p = 0.021), longer hospital stay (41 versus 27 days, p = 0.005), longer mechanical ventilation time (5 versus 3 days, p = 0.005), longer need for inotropic support (5 versus 4 days, p = 0.001) and delayed chest closure time (3 versus 2 days, p = 0.030) in those in whom it was left open in comparison to all other patients. In patients having CC, pre-surgery oxygen saturation was significantly lower in patients with relevant MAPCAs (58% vs 70%, p 0.019). Echocardiography had a sensitivity of 53% and a specificity of 100% in detecting relevant MAPCAs, accurately. Conclusions: MAPCAs are frequently found in dTGA patients and can be associated with lower baseline oxygen saturation and a prolonged postoperative course after ASO. Transthoracic echocardiography cannot replace CC as diagnostic tool. If significant MAPCAs are suspected, early CC should be performed for diagnostic and therapeutic reasons. © 2017 Elsevier B.V. All rights reserved.
1. Introduction Nowadays, standard surgical management for simple type of d-transposition of the great arteries (dTGA) is the arterial switch operation (ASO), if coronary anatomy and valvular morphology allow this surgical technique [1,2]. Despite good short and longterm results with ASO in patients with dTGA, enlarged bronchial arteries/major aortopulmonary collateral arteries (MAPCAs) are
☆ Funding Source: None. Financial Disclosure: All authors have no financial relationships relevant to this article to disclose. Conflict of Interest: All authors have no potential conflicts of interest to disclose. ⁎ Corresponding author at: Paediatric Cardiology, University Children's Hospital, Steinwiesstrasse 75, 8032 Zurich, Switzerland. E-mail address: [email protected] (M. Christmann). 1 Both first and both last authors contributed equally to this work.
possible findings in this patient group [2–4]. MAPCAs are often clinically irrelevant, but may cause congestive heart failure after surgical repair due to significant left-to-right shunting [4–7]. Possible symptoms of hemodynamic relevant MAPCAs are pulmonary volume overload, respiratory failure, left atrial and ventricular dilatation as well as dysfunction, failure to thrive, tachycardia or arrhythmias [6,7]. The gold standard for the diagnosis of hemodynamically significant MAPCAs after ASO is angiography during cardiac catheterization (CC). As CC after ASO is not performed on a routine basis, mostly patients with a complicated postoperative course or difficult coronary transfer due to special coronary anatomy undergo further invasive evaluation. In other case series, treatment of symptomatic MAPCAs was performed by transcatheter coil embolization of the collateral vessels [5–9]. Aim of this study was to evaluate the incidence and clinical significance of MAPCAs during the early postoperative course after ASO for surgical repair of dTGA.
https://doi.org/10.1016/j.ijcard.2018.01.132 0167-5273/© 2017 Elsevier B.V. All rights reserved.
Please cite this article as: A. Wipf, et al., Aortopulmonary collaterals in neonates with d-transposition of the great arteries – Clinical significance early after arterial switch operation, Int J Cardiol (2017), https://doi.org/10.1016/j.ijcard.2018.01.132
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2. Materials and methods
category” published by L. Bergersen et al. [13], which distinguishes 4 different risk categories [1–4], as well as their “definitions for adverse event severity” (adverse event severity level 1–5) [13].
2.1. Study population In this retrospective monocentric cohort study, we analyzed clinical data of patients with simple dTGA undergoing ASO between January 2007 and December 2016 at the University Children's Hospital of Zurich, Switzerland. Simple TGA was defined by the International Pediatric and Congenital Cardiac Code of the Association for European Pediatric and Congenital Cardiology (IPCCC-AEPC) [10] ICD-10 Code Q20.3 and could be accompanied by a patent foramen ovale (PFO, ≤ 3 mm), atrial septal defect (ASD, N3 mm), persistent arterial duct (PDA), ventricular septal defect (VSD) and/or vessel and valve abnormalities like coarctation of the aorta (CoA) or pulmonary valve stenosis. Patients with other cardiac comorbidities [e.g. atrio-ventricular septal defect (AVSD) or double outlet right ventricle (DORV)] were classified as complex TGA and were not included in this study. Indications for postoperative CC were difficult intraoperative coronary transfer during ASO, signs of ischemia (ST changes or exceptionally elevated troponin levels), arrhythmia or prolonged intensive care with prolonged mechanical ventilator support and prolonged need for inotropic agents (milrinone or adrenalin). CC included hemodynamic evaluation and contrast angiography for coronary arteries and MAPCAs. MAPCAs were defined as hemodynamically relevant if injection of contrast agent into the MAPCAs was followed by a clearly visible opacification of the correspondent pulmonary veins. Two groups were created based on these findings: Patients a) with (Group I) or b) without hemodynamically relevant MAPCAs (Group II). The latter includes patients who did not undergo CC (Group II A) and patients without relevant MAPCAs in CC (Group II B) (Tables 1 and 2).
2.3. Data collection Clinical data (patients' demographics, co-morbidities, data on intraoperative and postoperative course, data on CC) were extracted from patient medical records. 2.4. Statistical analysis The data is presented as median with interquartile range (IQR) or mean ± standard deviation (SD), as appropriate. Categorical data is expressed as counts and percentages. Comparison of percentages was performed by the use of Pearson's Chi-Square test or Fishers' exact test when appropriate, those of mean values by Students' t-test and those of median values by the Mann-Whitney U test. If significant differences occurred, posthoc analysis with appropriate p-value adjustment for multiple testing was performed. Significance testing was 2-sided with the significance level set at p b 0.05. 2.5. Ethics All data was obtained primarily for medical purposes. The study design fulfills the guidelines of the Declaration of Helsinki regarding ethical principles for medical research involving human subjects. The study was approved by the institutional ethical board.
3. Results
2.2. Treatment techniques Surgical procedures were performed using moderately hypothermic cardiopulmonary bypass and cold blood cardioplegic arrest. When necessary, repeat cardioplegia by selective cannulation of the coronary buttons was performed. ASO included switching of the aorta and the pulmonary roots, coronary button transfer, obligatory ligation and transection of PDA, and closure of ASD and VSD (as indicated) [11,12]. Lecompte-maneuver (translocation of the pulmonary bifurcation anterior to the neo-aorta) was performed as a rule. Taking into account the limitations that such a retrospective data analysis involves, there were no indicators in the MAPCA group to suggest increased non-coronary blood return during extracorporeal circulation (ECC) which could be indicative of MAPCAs. No routine postoperative angiograms were performed. CC was performed under general anesthesia and mechanical ventilation. Femoral arterial vascular access was achieved via a 4 Fr introducer sheath in all patients. After hemodynamic assessment and aortic angiography, relevant MAPCAs were selectively cannulated by using a thin-walled end-hole catheter and a 0.014 in. torque wire. In those patients with MAPCAs judged to be hemodynamically relevant (Group I), micro catheters (e.g. Cantata®, COOK Medical/Bloomington/U.S.A.) were used for coil delivery using MRI-compatible coils (BALT Extrusion Spirale® embolization coil). To categorize the risk for the cardiac catheterization procedures we used the “procedure type risk
3.1. Patient characteristics 103 neonates with simple dTGA were treated with ASO including Lecompte-maneuver between January 2007 and December 2016. 5 patients were excluded from the analysis due to missing parental consent or loss of follow up. Two patients died postoperatively during hospital stay. Both had an emergency ASO, one on the first and the other one on the second day of life due to insufficient arterial oxygen saturation despite adequately sized atrial septal defect and PDA. The first patient died because of severe left coronary artery stenosis with myocardial infarction despite multiple surgical revisions at the age of 12 days (12 days after ASO, 11 days after diagnostic CC) and the other patient due to severe postoperative mitral regurgitation and heart failure at the age of 17 days (16 days postoperatively, 9 days after diagnostic CC). CC showed normal coronary arteries in this patient. Overall,
Table 1 Baseline characteristics of patients with and without relevant MAPCAs.
Numbers of patients n (%) Male n (%) GD, days (mean ± SD), n = 96 Weight, grams (median (IQR)), n = 98 Height, cm (mean ± SD), n = 96 Atrial septal with: − No atrial septal defect n (%) − PFO b 3 mm n (%) − ASD II N 3 mm n (%) VSD n (%) Coronary anatomy: n (%) − − − −
Normal LCX ex RCA Single-coronary ostium Others
Rashkind n (%) SpO2 before Rashkind (mean ± SD) SpO2 after Rashkind (median (IQR)) SpO2-difference after Rashkind (median (IQR))
Total
Patients with relevant MAPCAs in CC (Group I)
Classified as no relevant MAPCAs (Group II)
Patients without CC (Group II A)
Patients with no or no relevant MAPCAs in CC (Group II B)
p-Value *
98 (100) 70 (71) 274.69 ± 12.76 3455 (2990–3863) 50 ± 3
15 (15) 7 (47) 269.00 ± 11.95 3050 (2720–3460) 49.47 ± 2.5
83 (85) 63 (76) 275.72 ± 12.70 3500 (3000–3880) 49.81 ± 2.7
61 (62) 46 (75) 275.33 ± 13.64 3600 (3000–3910) 50 ± 3
22 (23) 17 (77) 275.82 ± 9.79 3455 (3070–3680) 49.34 ± 1.8
– 0.021 0.060 0.050 0.650 0.297
1 (1) 48 (49) 49 (50)
0 (0) 10 (67) 5 (33)
1 (1) 38 (46) 44 (53)
1 (2) 32 (52) 28 (46)
0 (0) 6 (27) 16 (73)
30 (30.6)
5 (33)
25 (30)
14 (23)
11 (50)
67 (68.4) 10 (10.2) 7 (7.1) 14 (14.3)
8 (53) 2 (13) 2 (13) 3 (20)
59 (71) 8 (10) 5 (6) 11 (13)
49 (80) 3 (5) 2 (3) 7 (12)
10 (46) 5 (23) 3 (14) 4 (18)
75 (76.5) 63 ± 16 85 (80–90) 20 (14–35)
13 (87) 58 ± 12 85 (79–90) 23 (19–36)
62 (75) 64 ± 17 85 (80–90) 20 (13−33)
49 (80) 62 ± 17 85 (80–90) 20 (13–34)
13 (59) 70 ± 15 87 (84–90) 23 (15–28)
0.770 0.385
0.509 0.205 0.786 0.339
Group I: “Patients with relevant MAPCAs in CC”; Group II: “Classified as no relevant MAPCAs”, includes Group II A (“Patients without CC”) and Group II B (“Patients with no or no relevant MAPCAs in CC”). (*) p-value calculated for the comparison of Groups I and II. n: numbers of patients; SD: standard deviation; IQR: interquartile range; GD: gestation days; PFO: persistent foramen ovale; ASD: atrial septal defect; VSD: ventricle septum defect; LCX ex RCA: left circumflex ex right coronary artery; Data shown as mean ± standard deviation, median and interquartile range (IQR) or number and percent in general study population.
Please cite this article as: A. Wipf, et al., Aortopulmonary collaterals in neonates with d-transposition of the great arteries – Clinical significance early after arterial switch operation, Int J Cardiol (2017), https://doi.org/10.1016/j.ijcard.2018.01.132
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3
Table 2 Operative and postoperative characteristics of patients with and without relevant MAPCAs.
ECC time (median (IQR)), n = 96 ACC time (median (IQR)), n = 96 OP time (median (IQR)), n = 89 Troponin T (μg/l) (median (IQR)), n = 79 Age at OP (d) (median (IQR)), n = 98 Postop hospital stay (d) (median (IQR)), n = 96 Ventilation time (d) (median (IQR)), n = 96 Inotropic support time (d) (median (IQR)), n = 95 PICU stay (d) (median (IQR)), n = 96 Duration open thorax (d) (median (IQR)), n = 46 Total hospital stay (d) (median (IQR)), n = 96
Total
Patients with relevant MAPCAs in CC (Group I)
Classified as no relevant MAPCAs (Group II)
Patients without CC (Group II A)
Patients with no or no relevant MAPCAs in CC (Group II B)
p-Value *
172 (143–200) 111 (89–136) 262 (228–299) 5.87 (3.87–8.40) 9 (6–12) 17 (14–24) 3 (2–4) 4 (2–5) 6 (4–7) 2 (2–3) 27 (22–37)
175 (149–263) 111 (84–164) 276 (244–319) 5.3 (4.57–9.9) 9 (6–12) 24 (15–40) 5 (2–7) 5 (4–8) 7 (6–13) 3 (2–6) 41 (24–50)
170 (139–199) 111 (90–135) 261 (221–298) 5.89 (3.73–8.11) 9 (6–12) 16 (14–22) 3 (1–4) 4 (2–5) 6 (4–7) 2 (2–3) 27 (22−33)
165 (128–195) 110 (88–135) 258 (208–290) 5.61 (3.28–7.53) 9 (7–12) 15 (13−20) 2 (1–3) 4 (2–5) 5 (4–7) 2 (1–3) 27 (22−31)
193 (168–215) 120 (95–145) 287 (253–340) 8.59 (5.63–10.28) 8 (5–10) 22 (17–29) 3 (2–5) 4 (3–5) 7 (4–9) 2 (2–3) 30 (24–37)
0.126 0.273 0.474 0.187 0.862 0.001 0.005 0.001 0.021 0.030 0.005
Group I: “Patients with relevant MAPCAs in CC”; Group II: “Classified as no relevant MAPCAs”, includes Group II A (“Patients without CC”) and Group II B (“Patients with no or no relevant MAPCAs in CC”). (*) p-value calculated for the comparison of Groups I and II. n: numbers; SD: standard deviation; IQR: interquartile range; CC: cardiac catheterization; OP: operation; PICU: pediatric intensive care unit; ECC: extra corporal circulation; ACC: aortic cross clamp. Data shown as mean ± standard deviation, median and interquartile range (IQR) or number and percent in general study population.
98 patients could be included in our study, out of which 70 patients (71%) were male. Seventy five patients (77%) underwent an atrial septostomy procedure (Rashkind maneuver) within the first hours of life. Additional VSD closure was performed in 30 patients (31%). In 16 patients (16%) there was another relevant cardiac abnormality treated during the same surgery such as AV-valve reconstruction (7%), resection of coarctation of the aorta (CoA) with end-to-end anastomosis (7%), pulmonary valvuloplasty (2%) and others (2%). Thirty-one patients (32%) had coronary artery abnormalities (Table 1). The median age at time of ASO was 9 days (IQR: 6–12). Delayed secondary sternal closure was performed in 48 patients (49%). Two patients (2%) needed early redo-surgery due to relevant coarctation of the aorta after ASO, three patients (3%) underwent secondary surgical plication of the diaphragm due to paralysis. Three patients (3%) needed a surgical revision of the left coronary artery by use of a patch plasty (V. saphena magna or autologous pericardium) due to an ostial stenosis of the left coronary artery at the age of 7, 11, and 62 days, respectively. The baseline characteristics of all patients are presented in Table 1. The flow chart in Fig. 1 describes the study population concerning postoperative course and results obtained during CC. 3.2. Analysis of patients requiring cardiac catheterization 37 (37.8%) patients underwent postoperative CC due to a complicated postoperative course or difficult coronary transfer due to special coronary anatomy. Median age at catheterization was 29 days (IQR: 17–59). 20 (54%) of these 37 patients had one or more MAPCAs, of which 15 (41% of all patients with CC) were rated hemodynamically relevant and underwent transcatheter coil embolization (Fig. 2a and b). Median number of coiled MAPCAs was 3 (IQR: 2–3). Median time between surgery and catheterization was 15 days (IQR: 12–48). Patients with relevant MAPCAs had a significantly longer PICU stay (7 versus 6 days, p = 0.021), longer hospital stay until discharge (41 versus 27 days, p = 0.005), longer postoperative mechanical ventilation time (5 versus 3 days, p = 0.005), longer need for inotropic support (5 versus 4 days, p = 0.001) and delayed chest closure (3 versus 2 days, p = 0.030) in those in whom the sternum was left open (Table 2). No significant difference in early postoperative troponin T, ECC, ACC (aortic cross clamp) and surgical procedure time was seen between the two groups. Systolic blood pressure before CC was significantly lower (p = 0.038) in patients undergoing coil embolization whereas diastolic pressure and blood pressure amplitude did not differ significantly. Details are summarized in Table 2. When comparing children undergoing CC only (total n = 37, n = 15 with relevant MAPCAs, n = 22 without relevant/no MAPCAs, s. Fig. 1), we found no significant difference of sex (p 0.069), body weight (p 0.118) and height (p 0.858). Diastolic blood pressure during CC
under general anesthesia showed a trend towards lower values in the relevant MAPCA group (median 28 vs 34 mm Hg). In contrast, baseline oxygen saturation before Rashkind procedure differed significantly between the two groups (mean 58% vs 70%, p 0.019). Concerning operative and postoperative parameters we found a trend towards longer duration of inotropic support (median 5 vs 4 days, p 0.059) and towards longer hospitalisation till discharge (median 41 to 30 days, p 0.069) in the relevant MAPCA group. No significant difference for the other operative or postoperative factors was found. In the 15 patients who underwent coil embolization of MAPCAs, this resulted in complete closure of the MAPCAs in all of them. One to four MAPCAs were closed with one, two or three detachable MRIcompatible Platin coils (BALT coils™, BALT Extrusion, Montmorency, France) per MAPCA in a single patient. Mostly, MAPCAs were found arising from the descending aorta but in some cases they originated from the ascending aorta or from the vertebral or mammarian arteries. 9 patients were extubated immediately after CC and did not need readmission to the PICU. Of the remaining 6 patients, three needed ongoing intensive care treatment due to pulmonary hypertension (1 patient) or ongoing inotropic support (2 patient) and 3 patients underwent re-surgery just before or shortly after CC (diaphragmatic plication, closure of residual ASD and revascularization of the coronary artery). No major complications occurred after CC intervention. Pre-catheterization, during echocardiography, MAPCAs were suspected in 8 of the 15 patients (53%) with relevant MAPCAs. According to the risk categories of Bergersen et al. [13] the mean Bergersen Score in all patients with CC was 2.6 (IQR: 2–4) which indicates a moderate risk. The mean Adverse Event Severity Score (AES) was 1.4 (IQR: 1–3) (between none and minor). 4. Discussion This study aims to evaluate the clinical significance of MAPCAs in the early postoperative course after ASO. In a cohort of 98 neonates with dTGA, hemodynamically relevant MAPCAs could be found in a not negligible number of patients (15%). Our findings demonstrate that patients with relevant MAPCAs have a complicated and prolonged postoperative course with a significantly longer PICU stay, and with prolonged inotropic support and ventilation time. The embryological development of MAPCAs in association with dTGA is rarely described in literature to date. MAPCAs are remnants of the embryonic ventral splanchnic arteries [13]. In the first weeks of gestation, together with the onset of the formation of the normal pulmonary arterial system, these systemic-to-pulmonary collateral arteries normally start to regress as they are not preprogrammed to “survive” after birth [14,15]. When there is early underdevelopment of the pulmonary arterial system or the pulmonary valve, MAPCAs may
Please cite this article as: A. Wipf, et al., Aortopulmonary collaterals in neonates with d-transposition of the great arteries – Clinical significance early after arterial switch operation, Int J Cardiol (2017), https://doi.org/10.1016/j.ijcard.2018.01.132
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Fig. 1. Flow chart of all patients. n: numbers of patients; dTGA: d-transposition of the great arteries; LFO: loss to follow up; ASO: arterial switch operation; CC: cardiac catheterization; MAPCA: major aortopulmonary collateral artery; other findings: dilatation/stenting of pulmonary artery/aortic arch.
persist, seen especially in pulmonary atresia (PA) or Tetralogy of Fallot (ToF), thereby ensuring sufficient postnatal pulmonary blood flow [14,15]. These heart defects are characterized by reduced oxygen saturation in blood postnatally (reduced pulmonary blood flow with rightto-left shunting via VSD and/or ASD in PA and ToF, parallel circulations with reduced mixing of blood in dTGA). One explanation for the persistence or the re-opening of MAPCAs in dTGA might be either a reduced arterial partial oxygen pressure or a reduced blood flow through the pulmonary arteries both indicating a relevant oxygen deficiency. In univentricular heart defects after bidirectional Glenn anastomosis (stage 2 palliation according to Norwood), MAPCAs are often found during pre-Fontan catheterization. It has recently been shown that there was no association between collateral flow and oxygen saturations measured at time periods before the Stage 2 operation [16], questioning the assumption that cyanosis is a trigger for the development of MAPCAs in this patient group. Nevertheless, it has been shown, that acyanotic postoperative patients do not have the same burden of MAPCAs [17] and that collateral flow is responsible for a meaningful additional degree of pulmonary blood flow with the capacity to increase oxygen saturation [18]. Going along with the cyanosis theory, when looking at the neonates needing CC in our study population (Group I vs Group II B), we found lower mean oxygen saturation values before Rashkind in the relevant MAPCA group (p 0.019). Beside reduced oxygen saturation, chest wall stress and pleural inflammation, caused e.g. by prolonged ICU stay with prolonged ventilator support, provide stimuli for MAPCA growth or re-opening, which might have had an influence in our study population as well [16]. Although several case reports have addressed the relevance of MAPCAs in dTGA, it has been poorly investigated in larger studies [6,7,19]. To our knowledge, only one study from Wernovsky et al. in 1993 discussed the relevance of MAPCAs in the long-term follow-up after ASO [20].
Regarding baseline patient characteristics, we did not find any association to relevant MAPCAs (Table 1). In contrast, Wernovsky et al. [20] found an association of MAPCAs to dTGA with intact ventricular septum, without any explanation of this phenomenon. In contrast to other case reports [4,8,19], with an incidence of at least 15% of all neonates with dTGA treated by ASO in our patient cohort, we can argue that hemodynamically significant MAPCAs are not a rare finding. Several studies [4,6,21,22] analyzed a higher incidence of MAPCAs in late repair by ASO but did not define “late” and “higher” in their studies. Using our definition of significant MAPCAs, there was no difference in age at ASO between patients with and without relevant MAPCAs (median age at OP 9 days (IQR: 6–12) in patients with and without MAPCAs, p = 0.862) (Table 2). Nevertheless concerning timing of ASO it has to be taken into account that only patients with a complicated postoperative course underwent CC and that a huge number of patients have not been catheterized in whom the status of MAPCAs might be underestimated. We could also show that relevant MAPCAs have an influence on the postoperative course after ASO, with prolonged inotropic support (5 days (IQR: 4–8) versus 4 days (IQR: 2–5), p = 0.001), longer ventilation time (5 days (IQR: 2–7) versus 3 days (IQR: 1–4), p = 0.005) and PICU stay (7 days (IQR: 6–13) versus 6 (IQR: 4–7), p = 0.021) compared to dTGA patients without relevant MAPCAs. When comparing operative and postoperative parameters between patients receiving CC only (Group I vs Group II B), we only found a trend towards longer duration of inotropic support (median 5 vs 4 days, p 0.059) and towards longer hospitalisation till discharge (median 41 to 30 days, p 0.069) in the relevant MAPCA group, presumably due to the small sample size of patients with CC. Other risk factors for the prolonged postoperative course could be excluded. Nevertheless, these findings could only be evaluated retrospectively. Therefore, we unsuccessfully tried to find predicting parameters suggesting hemodynamically significant
Please cite this article as: A. Wipf, et al., Aortopulmonary collaterals in neonates with d-transposition of the great arteries – Clinical significance early after arterial switch operation, Int J Cardiol (2017), https://doi.org/10.1016/j.ijcard.2018.01.132
A. Wipf et al. / International Journal of Cardiology xxx (2017) xxx–xxx
Fig. 2. a: Angiography (aortic arch) showing MAPCAs originating from the descending aorta to both lungs. b: Closure of MAPCAs using BALT coils in the same patient.
MAPCA directly after ASO. Clinical evaluation of blood pressure did not show a significant difference in diastolic blood pressure or blood pressure amplitudes during PICU stay, whereas during CC under general anesthesia, diastolic blood pressures were lower in the relevant MAPCA group. Systolic blood pressure showed only a minor difference, which we judged to be an accidental finding. Shikata et al. [15] postoperatively measured a diastolic pressure in the femoral artery of b30 mm Hg, suggesting a diastolic steal effect of the MAPCA, as a neoaortic regurgitation had been excluded [14]. A low diastolic blood pressure or high blood pressure amplitude would be parameters clinically easy to obtain and to evaluate. As our population showed blood pressure values within normal ranges just before CC (77 ± 13/45 ± 8 mm Hg) our findings
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do not support blood pressure as a reliable parameter to detect relevant MAPCAs. With postoperative transthoracic echocardiography performed before CC, 8 relevant MAPCAs were detected/assumed and later confirmed by CC. However, 7 relevant MAPCAs detected by CC were not seen in echocardiography. These findings suggest that echocardiography does not sufficiently detect relevant MAPCAs (sensitivity 53%), while a positive echo-finding (flow in color Doppler suspicious for a collateral vessel, left atrial/left ventricle dilatation, left ventricle dysfunction or backflow in descending aorta) correlates well with a positive result in CC (specificity 100%). Therefore, we support the study of Maddali et al. [23] who stated in their case report that detection of MAPCAs can be done by echocardiography, however we advise caution, as negative echocardiographic findings do not exclude the presence of relevant MAPCAs. Even though MAPCAs might been seen in echocardiography, the relevance of MAPCAs might be underestimated, particularly if the focus of the examination is put on other details. Taking our incidence of relevant MAPCAs into account (15%), we suggest focusing more on signs of diastolic run off during echocardiography as described above in children with complicated courses after ASO and lower pre-surgery oxygen saturations. Qp:Qs calculations according to Fick are not meaningful in several MAPCA-patients, as collateral vessels enter the pulmonary circuit distally at the precapillary level, precluding shunt calculation, as already stated in Wernowsky et al. [20]. Without doubt CC is the gold standard for the diagnosis of relevant MAPCAs [5]. Single case reports [23] also described prolonged ventilation time in patients with MAPCAs after uncomplicated ASO, nevertheless they did not comment on the time in detail. Further postoperative variables such as inotropic support, duration of an open chest, PICU, or hospital stay were not analyzed in these surveys. As we stated above, all these parameters were significantly prolonged in patients with relevant MAPCAs in our study. As prediction of relevant MAPCAs by clinical findings and echocardiography might be difficult and due to the high incidence of relevant MAPCAs in our study complicating the postoperative course, the optimal time point of angiography for MAPCA detection needs to be discussed. With the analyzed parameters, we could not find a cut-off for an exact point in time for catheterization. Santoro et al. [6] stated that even selective aortic angiography could rarely detect MAPCAs before surgical repair. They assumed that local pulmonary hypoxemia as well as ductal “steal” masks the flow through these vessels, leading to vasoconstriction [6,8]. In addition, Irving et al. [8] attributed the increased appearance of MAPCAs after ASO as a result of higher left-to-right shunting with improved cardiac output [due to better LV preload postoperatively [19]]. Consequently, a routine CC before ASO would probably not help to detect MAPCAs earlier. Possibly, special hybrid aortic root injection performed routinely after ASO in the operation room might help to detect relevant MAPCAs earlier. Early detection would naturally reduce postoperative morbidity, and other interventions, and costs. In our setting, selective CC was conducted at a median age of 29 days and median time interval of 15 days after surgery. The median age at catheterization with coil embolization of patients with relevant MAPCAs was 30 days (IQR: 17–38) whereas 2 patients had late coil embolization (166 days and 414 days) due to late complications (arrhythmia and cardiorespiratory instability on long-term ventilation). Concerning the technique of occluding MAPCAs, most of the reports [4,19,20,23] used coil embolization with successful occlusion, as we did in our patient group. Only one case report described the additional use of a vascular plug for MAPCA closure [7]. The only larger study [20] examining MAPCAs in dTGA after ASO, performed CC at a median age of 11.2 months and did not mention the indication for CC. Of all 119 patients, they found relevant MAPCAs according to our definition in 55 patients and closed them in those 5 patients (9%) with markedly enlarged collateral vessels. Nevertheless, all of their patients, including the 5 in whom MAPCAs were closed, were asymptomatic without any medication. These findings lead to the assumption that significant
Please cite this article as: A. Wipf, et al., Aortopulmonary collaterals in neonates with d-transposition of the great arteries – Clinical significance early after arterial switch operation, Int J Cardiol (2017), https://doi.org/10.1016/j.ijcard.2018.01.132
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MAPCAs – even untreated – might have a rather benign short and longterm course. On the other hand, it might be possible that these vessels have a major impact to overcome the early postoperative course after ASO, which might become less important during follow-up after recovery from acute postoperative hemodynamic impairment. Our indications for CC are summarized in the methods section. As N50% of all CC revealed significant MAPCAs, we believe that our indication for CC was acceptably accurate. CCs performed were safe with no peri- and/or postinterventional complications occurring in our cohort, even though the “procedure type risk category” [13] had a mean value of 2.6. Recently, a new scoring system by the Bergersen group has been published [24] and other risk scores are available as well [25] with a more detailed risk stratification, which might be used instead in larger patient populations. The AES showed a mean of 1.4, which represents a severity level between none and minor. 4.1. Limitations The retrospective design of this study is one of the limiting factors. The long duration of the study period involved two cardiac surgery teams with changes in management that may have affected the postoperative course. However, the minor variations in surgical technique pursued are unlikely to have impacted the incidence and treatment of MAPCAs. The strategy regarding diagnosis and treatment of MAPCAs did not change in this period. There is no data assessed about long term outcome. As we did not conduct a routine CC after ASO, the prevalence of MAPCAs may be underestimated in our cohort. Though, in our observation period, none of the patients without initial CC had any corresponding clinical aggravation, even with possibly missed MAPCAs. Concerning the risk categorization for CC other scoring systems have been published recently.
[4]
[5]
[6]
[7]
[8]
[9]
[10]
[11] [12]
[13]
[14]
[15]
[16]
5. Conclusion Our study adds significant knowledge to the clinical impact of MAPCAs after ASO in patients with dTGA. Beside lower baseline saturation before surgery, chest wall stress and pleural inflammation due to prolonged ICU stay with ventilator support might be triggers for the development of these collateral vessels. With a 15% incidence rate and negative influence on the postoperative course after ASO in dTGApatients, early diagnosis of MAPCAs with cardiac catheterization is recommended, as echocardiography only has a high specificity (100%) but low sensitivity (53%) in detecting them. Echocardiography should have a special focus on signs of diastolic run-off. In the absence of other clinical parameters to identify MAPCAs, CC should be performed whenever there is a high level of clinical suspicion, even with normal echocardiography. Further research is needed to better identify patients with relevant MAPCAs and to define the optimal point in time for cardiac catheterization and embolization. Also, studies concerning the long-term outcome of patients with relevant MAPCAs and the relevance of initially insignificant MAPCAs at follow-up are needed.
[17]
[18]
[19]
[20]
[21]
[22]
[23]
[24]
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Please cite this article as: A. Wipf, et al., Aortopulmonary collaterals in neonates with d-transposition of the great arteries – Clinical significance early after arterial switch operation, Int J Cardiol (2017), https://doi.org/10.1016/j.ijcard.2018.01.132