Ann Thorac Surg 2006;82:153-157
© 2006 The Society of Thoracic Surgeons
Original article: Cardiovascular
Clinical Implications of Major Aortopulmonary Collateral Arteries in Patients With Right Isomerism
Jui-Yu Hsu, MD
a
,
b
,
Jou-Kou Wang, MD, PhD
a
,
Ming-Tai Lin, MD
a
,
En-Ting Wu, MD
a
,
*
,
Sheunn-Nan Chiu, MD
a
,
Chun-An Chen, MD
a
,
Hung-Chi Lue, MD, PhD
a
,
Mei-Hwan Wu, MD, PhD
a
a Department of Pediatrics, National Taiwan University Hospital and National Taiwan University, College of Medicine, Taipei, Taiwan
b Department of Pediatrics, Buddhist Tzu-Chi General Hospital, Taipei Branch, Taipei, Taiwan
Accepted for publication February 6, 2006.
* Address correspondence to Dr Mei-Hwan Wu, Department of Pediatrics, National Taiwan University, No. 7 Chung-Shan South Road, 100 Taipei, Taiwan (Email: mhwu{at}ha.mc.ntu.edu.tw).
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Abstract
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BACKGROUND: The presence of major aortopulmonary collateral arteries (MAPCA) in patients with right isomerism may alter the prognosis, which is still unclear.
METHODS: From 1994 to 2003, 138 out of 155 patients (89%) with right isomerism had pulmonary stenosis or pulmonary atresia and constituted the study population.
RESULTS: Two groups of patients were identified, one with MAPCA and the other without. The MAPCA originating from descending thoracic aorta or aortic arch was noted in 9 patients (6.5%), with a median number of MAPCA being 3 (range, 2 to 4). Patients with MAPCA commonly had congestive heart failure (8/9, 89%) and frequent lower airway infection (6/9, 67%). In comparison with patients with MAPCA and without, the intrapericardial pulmonary artery was more frequently absent (2 of 9 vs 1 of 129, p < 0.001), and the pulmonary arterial size was smaller (McGoon ratio <1.5, 8 of 9 vs 57 of 129, p = 0.009) in the MAPCA group. The mean pulmonary arterial pressure measured was often higher than the suggested limit for Fontan circulation. Major aortopulmonary collateral arteries were addressed at a median of 6 months old (2 to 19 months old) in 5 patients. Although surgical mortality was not different for first-stage palliation and Glenn shunt in both groups, total cavopulmonary connection could only be performed in one patient with MAPCA with poor results. However, the 5-year survival of patients with and without MAPCA was not statistically different (74.1% vs 55.2%, p = 0.19).
CONCLUSIONS: The presence of MAPCA was uncommon but still noted in patients with right isomerism. It may cause heart failure and a less favorable pulmonary vasculature for a complete Fontan-type operation.
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Introduction
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Congenital systemic-to-pulmonary collateral arteries, so called major aortopulmonary collateral arteries (MAPCA), are frequently the main sources of pulmonary flow in patients with tetralogy of Fallot with pulmonary atresia [1]. The central pulmonary arteries in such patients are commonly hypoplastic or complex in morphology. On the other hand, the pulmonary segments perfused by MAPCA may be associated with pulmonary overflow or even pulmonary hypertension. The potential for late pulmonary hypertension has been reported [2]. In patients with right isomerism and complex congenital heart disease, associated pulmonary stenosis or pulmonary atresia is also common [3–5]. However, the presence of MAPCA to supply pulmonary flow in such patients has only rarely been reported [6, 7]. The prevalence and the clinical significance of MAPCA in right isomerism remain unclear still. Because the associated cardiac anomaly is usually composed of common atrium, common atrioventricular valve, dominant right ventricle, double outlet right ventricle, and restrictive pulmonary outflow, most patients with right isomerism need to receive permanent palliation by total cavopulmonary connection (TCPC), or Fontan-type operation with single ventricle circulation physiology [8–11]. In the presence of MAPCA, the morphology and pressure of the pulmonary arterial system may be less favorable for Fontan-type palliation [12, 13]. This study, based on a large patient cohort, sought to define the prevalence and the implications of MAPCA in patients with right isomerism.
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Material and Methods
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The Institutional Review Board of this institution approved this study protocol (No. 9461712127, approved 01/05/2006) and waived the individual consent for the study. From January 1994 to December 2003, there were 155 patients (88 males and 67 females) diagnosed to have right isomerism in this institution. In addition to echocardiography, ultrafast chest computed tomography (CT) and (or) cardiac catheterization was performed to define the cardiac anomaly. These findings were further proved during surgery, or autopsy if fatality. There were 138 patients (89%, 81 males and 57 females) with either pulmonary stenosis or pulmonary atresia enrolled into this study. The mean age of first visit was 1.7 years (range, 0 day to 22 years; median, 0 days). The mean length of follow-up was 3.2 years (range, 1 day to 22 years). Additional sources of pulmonary blood flow included patent ductus arteriosus (PDA) and MAPCA. Although both ductus arteriosus and MAPCA are sources of the systemic-to-pulmonary blood supply, they are considered different because they derive from different embryologic structures [14]. In this study, ductus arteriosus that persisted more than 3 days of life was defined as PDA. Some patients might have needed prostaglandin E1 infusion to keep the arterial duct open for maintaining pulmonary blood until the first palliation (shunt operation), and they were also considered as patients with PDA if the ductus arteriosus was patent before the application of prostaglandin E1. The MAPCA are abnormal branches of the aorta, most commonly arising from the descending thoracic aorta or aortic arch. The MAPCA can be conduit if they connect with pulmonary arteries, or they can supply isolated pulmonary segments.
Pulmonary arterial size was evaluated by the McGoon ratio, which is the result of the diameters of right and left pulmonary arteries divided by the diameter of descending aorta. We defined "fair" pulmonary arterial size as a McGoon ratio equal to or more than 1.5, and "poor" pulmonary arterial size as a McGoon ratio less than 1.5. The mean pulmonary artery pressure was appropriate for TCPC or Fontan operation if it was less than or equal to 15 mm Hg [15–17]. In our institution, staged operation in such patients is usually needed to achieve final Fontan circulation. A palliative intervention is needed to achieve appropriate pulmonary flow and balanced hemodynamics before a Fontan-type operation, including a systemic-to-pulmonary shunt or percutaneous transcatheter pulmonary valvuloplasty in patients with inadequate pulmonary flow, rerouting of pulmonary veins with obstruction, atrioventricular valvuloplasty with insufficiency of atrioventricular valve, and pulmonary banding with inadequate pulmonary stenosis. The MAPCA were addressed before the Glenn shunt. Unifocalization (if pulmonary segments supplied by MAPCA only) and coil embolization or surgical ligation (if dual supply of pulmonary segments by both native pulmonary arteries and MAPCA) are performed. In a staged Fontan operation, bidirectional Glenn shunt is performed at 6 months to 2 years of age, and TCPC, using either a lateral tunnel or an extracardiac conduit, is performed at 2 to 4 years of age.
Statistics
The 
2 test was used when appropriate and statistical significance was established at a p value less than 0.05. The survival curve was estimated by Kaplan-Meier analysis and log-rank regression analysis was used to examine the statistical difference between the survival curves.
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Results
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Clinical Characteristics
Among the 138 patients with right isomerism and pulmonary stenosis or atresia, MAPCA was noted in 9 (6.5%) patients (5 males and 4 females). We further divided the patients into two groups; group 1 with MAPCA and group 2 without MAPCA. In group 2 patients, PDA to supply additional pulmonary flow was noted in 74 patients. The associated intracardiac anomalies in the two groups are summarized in Table 1. Pulmonary atresia and right aortic arch were found more frequently in patients with MAPCA.
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Table 1. Intracardiac Anomalies in Patients With Right Isomerism and Pulmonary Stenosis or Atresia, Categorized by the Presence of Major Aortopulmonary Collateral Arteries (MAPCA)
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The clinical features and the pulmonary arterial morphology of the 9 patients with MAPCA were summarized in Table 2. Cyanosis was present in all patients due to the underlying complex cardiac lesions. Heart failure presented as tachypnea, poor feeding, and failure to thrive was noted in 8 (89%) and frequent lower airway infection (
3 times every year) in 6 patients (67%). Each patient had a median number of 3 MAPCA (range, 2 to 4), originating from the descending thoracic aorta or the aortic arch. Confluent intrapericardial pulmonary arteries coexisted with MAPCA in 7 patients (79%). In the remaining 2 patients (22%), the intrapericardial pulmonary arteries were absent, with all the bronchopulmonary segments supplied by the MAPCA. Absent intrapericardial pulmonary arteries were more commonly noted in patients with MAPCA than in those without MAPCA (2/9 vs 1/129, p < 0.001). The patient of group 2 who had absent intrapericardial pulmonary arteries had bilateral PDA (confirmed by the surgeon) supplying left and right extrapericardial pulmonary arteries. Poor pulmonary artery size (McGoon ratio <1.5) was found in the majority of the patients with MAPCA (8 of 9, 89%) and in only less than half of the patients without MAPCA (57 of 129, 44%, p = 0.009). Seven of the 9 patients had received cardiac catheterization. The mean pulmonary artery pressure was measured in 3 patients, with 2 of them having mean pulmonary pressure higher than the suggested limit for a Fontan-type operation.
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Table 2. Clinical Summary of the Nine Patients With Right Isomerism and Major Aortopulmonary Collateral Arteries (MAPCA)
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Interventions and Outcome
Interventions and outcomes of the 138 patients with pulmonary stenosis-atresia are detailed in Figure 1. During the first palliation, the MAPCA had been embolized (2 cases), ligated (1 case), or unifocalized (2 cases) in 5 patients at a median age of 6 months (2 to 19 months) to improve the heart failure or to rehabilitate the central pulmonary arteries. The surgical mortality rate was not decidedly different between patients with and without MAPCA for the first palliation surgery and Glenn shunt operation. However, the surgical mortality was higher in patients with MAPCA at the TCPC completion surgery. Two patients of group 2 received biventricular repair with one surgical death. None of the group 1 patients could receive biventricular repair. The overall survival for patients of group 1 was 88.9% at 1 year and 74.1% at 5 years, and for group 2 was 66.4% at 1 year and 55.2% at 5 years, respectively. The survivals were not statistically different between both groups of patients with right isomerism using log-rank regression analysis (p = 0.19) (Fig 2).
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Fig 1. Outcome of patients with right isomerism and pulmonary stenosis or atresia. (f/u = follow-up; MAPCA = major aortopulmonary collateral arteries; ns = not significant; PA = pulmonary atresia; PS = pulmonary stenosis; TCPC = total cavopulmonary connection.)
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Fig 2. The survival curves in patients with right isomerism with pulmonary obstruction (stenosis or atresia), grouped as those with major aortopulmonary collateral arteries (MAPCA) and without. Using log-rank regression analysis, there was no statistically significant difference between survivals of the two groups (p = 0.19). The numbers on the curves are the patients at risk for each time interval. (— = MAPCA [–]; · · · = MAPCA [+].)
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As to the 9 patients with MAPCA, one patient was lost to follow-up and 2 surgery-related deaths were noted. One patient died soon after the pulmonary venous rerouting plus Blalock-Taussig shunt operation. The other received TCPC at the age of 3.5 years. His preoperative pulmonary arterial size evaluated by the McGoon ratio was 2 and the mean pulmonary pressure was 10 mm Hg, but the immediate postoperative hemodynamic condition was unstable. Takedown of TCPC was performed on the second day, but he died of infection and heart failure one month later. As to the remaining 6 patients, one received a central shunt and coil embolization of the MAPCA, but the central pulmonary arterial size was inadequate for further Glenn shunt operation. One patient received Blalock-Taussig shunt and MAPCA ligation at 6 months old, and is waiting for a Glenn shunt. One patient received a central shunt only without any other further management. Two patients received bidirectional Glenn shunt and planned for TCPC, but one of them still had a residual MAPCA difficult to be managed and one had relatively high pulmonary arterial pressure (mean, 20 mm Hg). Medical therapy only, without any intervention, was chosen for one patient and he was cyanotic (systemic O2 saturation was around 80%, New York Heart Association functional class I) and was 11 years old at last follow-up.
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Comment
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The major findings of this study are the following. (1) The incidence of MAPCA in patients with right isomerism was relatively low (6.5%). (2) The presence of MAPCA is associated with less favorable pulmonary vasculature and low feasibility to complete the Fontan-type operation. (3) The survival of patients with right isomerism and MAPCA was not worse than those without MAPCA, probably due to more conservative treatment strategies without definitive palliation.
The presence of MAPCA in patients with right isomerism has only rarely been described [6, 7]. In a recent study of 164 patients who underwent surgical intervention for congenital heart disease and MAPCA, 153 (93%) patients were tetralogy of Fallot with pulmonary atresia and 5 (3%) patients were tetralogy of Fallot. The remaining 6 patients carried a variety of diagnoses, but none of them were right isomerism [18]. An autopsy study showed that abnormal arborization of the pulmonary artery was present in 3% of the 125 specimens with right isomerism [19]. We defined the incidence of MAPCA in patients with right isomerism by the imaging results of a large patient cohort. The incidence was low (6.5%), but higher than the autopsy results. Right isomerism is more prevalent in the Oriental. Whether the relatively higher incidence of MAPCA is also a racial-related difference or not remains unknown [20].
Up to the present, only two reported patients with right isomerism and MAPCA have received a successful staged operation. One patient had two ventricles and two separate atrioventricular valves and the other had a single ventricle [6, 7]. Staged unifocalization of MAPCA to recruit as many as pulmonary segments to a central pulmonary artery is a prerequisite for late total repair. Our data revealed that the presence of MAPCA in patients with right isomerism, even after intervention, was more closely associated with absent central pulmonary arteries, smaller pulmonary arterial size, and relatively higher pulmonary arterial pressure to exclude the TCPC. Patients of whom MAPCA were managed after infancy also tended to have higher pulmonary arterial pressure and smaller pulmonary arteries. None of our patients with right isomerism and MAPCA fulfilled the criteria for two-ventricle repair. Only one patient was judged suitable for TCPC after prior unifocalization, but the TCPC operation still failed. The Glenn shunt after prior palliations could be performed in about one-third of the patients. These data suggest that the chance for a complete TCPC in patients with right isomerism and MAPCA is low. But a staged operation is still feasible in selected patients and early treatment of MAPCA.
The survival for patients with right isomerism in this study was poor, but was comparable with another study [21]. Patients with MAPCA had a low chance and a very poor result for TCPC completion, but the survival was not worse than the patients without MAPCA. This could be explained by the fact that a more conservative management strategy without definitive palliation was usually adopted for patients with MAPCA, and unsatisfactory surgical results in patients with right isomerism without MAPCA.
Progressive atrioventricular valvar regurgitation is also an important prognostic factor for a Fontan-type operation [12]. In this study, the degree of atrioventricular valvar regurgitation in right isomerism with MAPCA was mostly of a mild degree and comparable with that in those without MAPCA. Although MAPCA may cause a left-to-right shunt with potentially increased loading to the atrioventricular valve, the major determinant may still depend on the structure of the papillary muscles in such patients [22].
In conclusion, the presence of MAPCA was uncommon but was still noted in patients with right isomerism, and may cause heart failure and a less favorable pulmonary vasculature for a complete Fontan-type operation. However, the surgical mortality at first palliation and Glenn shunt was similar between patients with and without MAPCA. But the chance for a TCPC completion in patients with MAPCA was low and associated with high risk. The overall survival of the patients with MAPCA was not worse than those without, probably due to more conservative surgical strategies usually adopted, and therefore most patients without definitive palliation.
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Abstract
Introduction
