Vascular compression of the airway in children
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1 PAEDIATRIC RESPIRATORY REVIEWS (2008) 9, MINI-SYMPOSIUM: IMAGING AND INTERVENTIONAL RADIOLOGY Vascular compression of the airway in children Clare A. McLaren 2, *, Martin J. Elliott 1 and Derek J. Roebuck 2 1 Department of Cardiothoracic Surgery, The Great Ormond Street Hospital for Children NHS Trust, London, WC1N 3JH, UK; 2 Department of Radiology, The Great Ormond Street Hospital for Children NHS Trust, London, WC1N 3JH, UK KEYWORDS airway compression; self-expanding stents; vascular rings; tracheomalacia Summary Congenital heart disease (CHD) is an important clinical problem. Although survival has improved over recent decades, certain children with CHD remain difficult to treat, usually because of severe co-morbidity or uncorrectable defects. Vascular compression of the airway is one such co-morbidity, occurring in approximately 1 2% of children with CHD. It may be caused by congenital anomalies of the configuration of the great vessels, enlargement of otherwise normal structures or as a result of surgery. The anatomical patterns seen in these children may be complex, and as surgical correction is usually required to relieve the compression, the pre-operative imaging assessment should be as complete as possible. Precise diagnosis and therapy are essential because chronic airway compression in childhood carries a significant morbidity and mortality. Airway stenting is currently reserved for rare occasions when surgical correction is not possible. ß 2008 Elsevier Ltd. All rights reserved. Vascular compression of the airway in children is usually caused either by congenital anomalies of the configuration of the great vessels or enlargement of otherwise normal structures (Table 1). 1 The most common congenital anomalies associated with airway compression are the vascular rings. The ring may be patent (as in double aortic arch) or alternatively be completed by an atretic arch or ligamentum arteriosum (as in right-sided aortic arch with aberrant left subclavian artery). The aortic arch and its branches and the pulmonary arteries are derived from the embryonic branchial arches. Failure of part of this complex embryological process is uncommon, but is the cause of many of the malformations that result in vascular airway compression. 1 3 An understanding of the embryology of the aortic arch and related structures is helpful for image interpretation. * Corresponding author. address: mclarc@gosh.nhs.uk (C.A. McLaren). Other vascular mechanisms of airway compression exist. The most important of these are seen in children with absent pulmonary valve syndrome, interrupted aortic arch and dilated cardiomyopathy (see below). Less common causes of vascular airway compression include pulmonary artery sling without long segment congenital tracheal stenosis and compression of the trachea by the innominate artery (brachiocephalic trunk). Symptoms at presentation are variable, ranging from dysphagia, recurrent respiratory infections and stridor to acute respiratory distress or dying spells. 2 5 Symptoms such as chest discomfort, dyspnoea, wheezing and cough are often misdiagnosed as asthma, which is much more common in older children. 6 Affected children may require mechanical ventilation and some may remain ventilatordependent, even after surgery. A combination of imaging techniques is usually required for full pre-operative assessment. Precise diagnosis and therapy are essential because chronic airway /$ see front matter ß 2008 Elsevier Ltd. All rights reserved. doi: /j.prrv
2 86 C. A. MCLAREN ET AL. Table 1 children Causes of vascular compression of the airway in Anomalies of the aorta * Double aortic arch * Interrupted aortic arch (after surgical repair) * Right-sided aortic arch With aberrant left subclavian artery With mirror-image branching and right ligamentum arteriosum * Left-sided aortic arch With aberrant right subclavian artery and right ligamentum arteriosum Right-sided descending aorta with right ligamentum arteriosum * Cervical aortic arch Absent pulmonary valve syndrome Aberrant left pulmonary artery ( pulmonary artery sling ) Acquired cardiovascular disease * Dilated cardiomyopathy * Aneurysm Ascending aorta * Ductus arteriosus compression in childhood carries a significant morbidity and mortality. 7,8 Interventional radiology is limited in what it has to offer these children. Stenting is only appropriate when surgical correction is not possible. In our practice the usual indication is a palliative setting as it allows a child to be extubated. IMAGING TECHNIQUES Different imaging approaches may be appropriate for different causes of vascular compression of the airway. The historical approach was to perform chest radiography and barium swallow (upper gastrointestinal study) to evaluate children with suspected extrinsic compression of the airway. This has now been replaced in most centres by multidetector computed tomography (MDCT) and magnetic resonance imaging (MRI). The barium swallow is probably acceptably accurate for diagnosis of a vascular ring, but does not delineate the precise anatomy required for surgical planning 3 and is usually not helpful for bronchial compression. The diagnostic imaging pathway in our centre starts with echocardiography and flexible bronchoscopy (combined with bronchography when appropriate). We usually also perform either MDCT or MRI, and occasionally both. 7,9 Thesearethemostusefulradiological techniques as they provide information about the tracheobronchial tree, the cardiovascular structures and their relationship to each other. A limitation of MDCT and MRI is that obliterated vascular segments (e.g. the ligamentum arteriosum or an atretic aortic arch) cannot be directly visualized. 4 Diagnostic catheter angiography is now obsolescent in this context and has largely been replaced by cross-sectional imaging. 3,10 Chest radiographs may show aortic arch anomalies and dilated pulmonary arteries; however, although airway compression can sometimes be seen, 11 a comprehensive assessment is not possible. Radiographs may, however, show hyperinflation, collapse or other lung pathology. Echocardiography This is essential for the evaluation of associated congenital heart disease (CHD) and usually clearly shows abnormal vascular structures. Echocardiography aids the surgeon in understanding complex three-dimensional (3D) relationships. Direct evaluation of airway compression is limited. 1 Multidetector computed tomography The development of MDCT technology has greatly extended the applications of chest CT in children. 12 Scan times for MDCT are much shorter than for MRI and spatial resolution is higher. 7 Axial MDCT data are generally sufficient to diagnose the type and severity of airway compression, but multiplanar reconstruction and 3D volume rendered images may provide further useful information. 13 Virtual bronchoscopy images can also be generated from MDCT data but rarely add diagnostic information 12 and cannot yet be used as a substitute for bronchoscopy. They serve mainly as a method of conveying some information about the airway to clinicians who are familiar with this type of view. The main disadvantage of MDCT is exposure of the patient to ionizing radiation at the age of greatest sensitivity to its carcinogenic effects. Scan parameters should be modified from adult protocols to reduce the radiation dose. This can be achieved using weight-based protocols 13 or tube current modulation techniques. When careful technique is used, the effective dose for a CT study of the chest should be <3 msv, which is comparable to 200 frontal chest radiographs. 12 Magnetic resonance imaging MRI has excellent intrinsic contrast resolution and multiplanar imaging capabilities. 13 Evaluation of cardiac anatomy and physiology with MRI is usually superior to CT. However, most MRI studies for vascular compression will be quite prolonged (>30 min), requiring sedation or general anaesthesia in young children. Sedation risks for children with a compromised airway are significant. 1,13 The scan times are often considered to be too long for haemodynamically unstable patients, 7 especially given the relative inaccessibility of the MRI scanner. 14 In practice, the increase in speed and quality of multiplanar reconstructions provided by MDCT technology means that CT is used more often than MRI in most centres. 7,15
3 VASCULAR COMPRESSION OF THE AIRWAY 87 Bronchoscopy and bronchography Cross-sectional imaging is probably much better than bronchoscopy at determining the nature of vascular compression of the airway. Current MDCT and MRI techniques do not reliably distinguish between dynamic or static narrowing. 14,15 This is a very important practical point as many children with prolonged airway compression develop secondary malacia. Although improvements in scanning technique are likely to overcome this problem, bronchoscopy and bronchography are currently the best techniques for this purpose. We usually perform these examinations at the same time, injecting isotonic non-ionic contrast (iotrolan [Isovist-240], Schering, Burgess Hill, UK) down the working channel of a flexible bronchoscope or through a separate catheter. 16 Malacia should only be assessed when the patient is breathing spontaneously. Interventional radiology The role of metal stents in the airway of children remains controversial. We prefer to restrict their use to two indications: palliation and when all other potential treatments have failed. Stenting with palliative intent may be used to allow a child to be extubated, so he/she can die at home. Our experience has been very favourable in this context, with several children surviving much longer than expected with a good quality of life, e.g. those with acquired cardiomyopathy. In other patients, however, it is sensible to be cautious. Correct stent selection is important for children with vascular compression of the airway. 16 Balloon expandable stents, such as the Palmaz stent (Cordis Europa N.V., Roden, The Netherlands), are rigid and this can lead to erosion through the wall of the airway. Self-expanding stents are much more flexible and less likely to lead to vascular erosion. 16 They are also less likely to fracture when there is severe compression, e.g. in dilated cardiomyopathy. The major problems with this type of stent are that they are difficult to remove and cannot easily be post-dilated to allow for future growth. We usually perform stent insertion under bronchographic control in an angiography suite. The advantage over rigid bronchoscopy is that the whole stent can be visualized on fluoroscopy, ensuring the it does not move during deployment and allowing the operator to position it as close as possible to a bifurcation without covering a bronchial orifice. The procedure is performed under general anaesthesia with muscle relaxation. We usually perform flexible bronchoscopy initially to confirm the diagnosis. Contrast is then injected either through the bronchoscope or through a small angle-tip catheter. When a bronchographic roadmap of the compressed area has been obtained, a guidewire is then passed into a peripheral bronchus. The stent delivery device is passed over the wire and the stent is deployed under fluoroscopic control. The stent can be repositioned during the initial part of deployment, if required. The final stent position can be checked with flexible bronchoscopy if necessary. Covered, retrievable self-expanding stents are available for use in the airway. These may be easier to deploy than silicone (Dumon) stents, but can be expected to have similar disadvantages such as stent migration and blockage caused by the covering of the stent inhibiting ciliary clearance of secretions from the lungs. It is possible that some form of absorbable stent will be available in the future, in which case the indications for stent insertion may broaden significantly. DOUBLE AORTIC ARCH Autopsy studies suggest that 3% of people have a congenital malformation of the aortic arch, but most remain undiagnosed throughout life. 3 Double aortic arch (DAA) is the most common cause of vascular compression of the airway in children. 3,4,9,17,18 DAA is defined by the presence of both left- and right-sided aortic arches, which together surround the trachea and oesophagus (Fig. 1). The right arch is usually larger ( dominant ). The left arch is usually small ( hypoplastic ) or forms a fibrous cord ( atretic segment) beyond the origin of the left common carotid or subclavian artery. 1,19 The fibrous cord tethers the patent part of the left-sided arch to the descending aorta, completing the ring. A ductal ligament may also be relevant in the creation of a ring at this point, since the ligament often connects the distal left arch to the proximal left pulmonary artery. Schlesinger et al. reviewed the MRI and CT findings of DAA with an atretic left arch. 19 They found that the fibrous cord could not be seen on imaging and that the diagnosis was made from the presence of an incomplete left arch. The descending aorta may be left- or right-sided, or may run in the midline anterior to the vertebral column. When the descending aorta is midline, the structures of the mediastinum are said to be stacked abnormally, resulting in compression between the spinal column and the sternum. 15 Children with DAA usually present in infancy, 1 with symptoms including dysphagia, stridor, wheezing and respiratory distress. 10 Surgical correction, usually by transection of the non-dominant arch, is required to relieve the airway compression. 9 It is always important to diagnose the arch anatomy before surgery because this determines the operative approach. About 30% of children have residual symptoms despite surgical treatment of DAA. 15 Although Fleck et al. found that residual symptoms may be due to persistent airway compression, some children have severe malacia of the lower trachea (extending to the carina). 15 This may develop as a secondary effect of prolonged severe extrinsic compression. In our experience, in most children this problem is self-limiting, and eventually their airway cartilage
4 88 C. A. MCLAREN ET AL. Figure 1 Persistent airway compression in a 20-month-old boy following surgery for double aortic arch. (a) 3D CT reconstruction (posterosuperior view) shows the divided left arch and surgical clips (white arrows). The right arch is indicated by a red arrow. (b) Compression is most severe where the descending aorta (arrow) crosses from right to left behind the airway. (c) Frontal bronchography shows a right-sided impression on the trachea from the right aortic arch. (d) Lateral bronchography shows posterior compression by the descending aorta (arrows). (e) 2.2-mm flexible bronchoscopy shows extrinsic compression at the level of the carina.
5 VASCULAR COMPRESSION OF THE AIRWAY 89 regains sufficient stiffness for the symptoms to resolve. Although an occasional patient requires tracheostomy during this period, we have never had to insert an airway stent in a child with DAA. Detailed studies of late respiratory function are required in this group. INTERRUPTED AORTIC ARCH Interrupted aortic arch (IAA), in which some part of the lumen of the aortic arch is discontinuous, is found in about 1% of all children with CHD. Children typically present as neonates and, if untreated, usually die by the age of 10 days. 20 In type A (30 40%) the arch is interrupted between the origin of the left subclavian artery and the ductus arteriosus. In type B (50 55%) the interruption occurs between the origins of the left common carotid artery and the left subclavian artery. Type C (interruption between the innominate artery and the left common carotid artery) is very uncommon. In all types, deoxygenated blood flows to the lower part of the body through an enlarged ductus arteriosus. Over 95% of children have associated cardiac anomalies. 20,21 Airway compression in IAA is a consequence of surgical repair rather than the malformation itself. Shortening of the arch is inherent in the procedure, in which an end-to-end anastomosis is performed between the ascending and descending aorta, irrespective of the type of IAA. This results in anterior displacement of the descending aorta, posterior displacement of the anterior aorta and consequent compression of the left main bronchus (LMB) between the aorta and the left pulmonary artery (Fig. 2). Surgical correction of this compression is technically challenging 22 and further surgery may be required as the child grows. Tracheostomy with pressure support may fail to overcome the LMB compression, and excessive continuous positive airway pressure may even damage the right lung. In some children, therefore, it may be justified to use metal airway stents, despite the risks. As noted above, balloonexpandable and self-expanding designs each have advantages and disadvantages, and the choice of stent will depend on individual clinical factors. 16,23 RIGHT-SIDED AORTIC ARCH WITH ABERRANT LEFT SUBCLAVIAN ARTERY Right-sided aortic arch (RAA) with an aberrant left subclavian artery and/or a left ligamentum arteriosum is reported in 12 25% of children with vascular rings. Most patients with these anomalies are asymptomatic. 24 There are two main patterns of origin of the great arteries to the head and upper limbs in RAA. In mirrorimage branching, a left brachiocephalic trunk (innominate artery) arises first, followed by the right common carotid and the right subclavian arteries. In RAA with aberrant left Figure 2 A 4-month-old girl with compression of the left main bronchus following surgery for interrupted aortic arch. Axial CT of the thorax showing compression in the midline by the descending aorta (arrow). Figure 3 A 5-year-old boy with a right-sided aortic arch and aberrant left subclavian artery. (a) Axial CT of the thorax showing compression of the trachea by the aberrant artery (arrow). (b) 3D volume rendered image (posterior view) shows the right-sided aortic arch (red arrow) and the aberrant left subclavian artery (white arrow) arising from the descending aorta.
6 90 C. A. MCLAREN ET AL. subclavian artery (Fig. 3) the first branch is the left common carotid, followed by the right common carotid and right subclavian arteries. The aberrant left subclavian artery arises from the descending aorta and passes behind the oesophagus. The vascular ring is completed by the left ligamentum arteriosum, which passes from the origin of the left subclavian artery to the left pulmonary artery. 1 The left subclavian artery often originates from an outpouching of the descending aorta, called a Kommerell s diverticulum. Airway compression in RAA is usually due to enlargement of the Kommerell s diverticulum, a short (tight) ligamentum arteriosum or a midline descending aorta. 24 Relief of symptoms is usually achieved by transection of the ligamentum arteriosum, 24 but it is very important also to excise the diverticulum since this can result in late compression of the oesophagus and/or trachea. Late diagnosis of this condition does occur, particularly in patients with a Kommerell s diverticulum. ABSENT PULMONARY VALVE SYNDROME Absent pulmonary valve syndrome (APVS) is characterized by the presence of enlarged pulmonary arteries and hypoplastic pulmonary valve cusps. It is most often seen in association with ventricular septal defect (VSD) and right ventricular outflow tract obstruction (RVOTO). APVS occurs in 3 6% of patients with tetralogy of Fallot, but can also be seen in isolation, with an intact ventricular septum and other congenital anomalies. 25,26 There is a strong association with DiGeorge syndrome (chromosome 22q11 deletion). 11 The characteristic pattern of compression of the lower trachea, LMB and right main bronchus or bronchus intermedius (Fig. 4) is caused by enlargement of the pulmonary arteries and left atrium. 1,11,25 The prognosis in APVS depends on the age at presentation and the severity of symptoms. Neonates and infants often present with severe cardiorespiratory compromise. 26 Mortality is between 16% and 56% in this group, with an especially poor prognosis in those infants who require mechanical ventilation. 11,25,26 Children who present later often have milder symptoms, and surgery may be performed on an elective basis, usually simply by repairing the Fallot component of the defect. 26 In small babies, there remains some controversy about which surgical technique is best to relieve the tracheobronchial compression. The usual approach involves replacement of the pulmonary artery with conduits or reduction arterioplasty. 26,27 However, the addition of the Lecompte manœuvre (transecting the aorta, allowing the pulmonary arteries to lie anterior to the reconstructed aorta) has proved successful. Any associated cardiac anomalies are corrected at the same operation If possible, airway stenting is avoided in APVS because of the risk of erosion of a pulmonary artery with fatal haemorrhage. This risk can theoretically be minimized by the use of self-expanding stents, but the potential to dilate these stents to allow for future growth is very limited. Stenting is therefore restricted to palliative indications or when all surgical options have been exhausted. Both balloon-expandable 28,29 and self-expanding stents 30 have been used. OTHER VASCULAR CAUSES OF AIRWAY COMPRESSION Pulmonary artery sling In this condition the left pulmonary artery has an anomalous course, arising from the posterior aspect of the right pulmonary artery and passing between the lower trachea and the oesophagus to enter the hilum of the left lung. There is a strong association with long segment congenital tracheal stenosis (LSCTS) with complete tracheal cartilage rings. The literature usually states that LSCTS is presentin50%ofchildrenwithpulmonaryarterysling (PAS), but in our experience the proportion is much higher than this, and a diagnosis of airway compression due to PAS without LSCTS should be treated with suspicion. 31 Non-invasive imaging is not adequate to evaluate for complete rings and good quality bronchoscopy is mandatory. The distinction is clinically important, because it seems that the prognosis is much better if the LSCTS is repaired at the same time as the left pulmonary artery is re-implanted. 31 Slide tracheoplasty is now the treatment of choice for LSCTS. Innominate artery compression Anterior compression of the trachea by the brachiocephalic trunk (innominate artery) is a controversial entity. First, this condition seems to have been over-diagnosed and possibly over-treated in the past. Second, in many patients said to have innominate artery compression (IAC) the main pathophysiological mechanism appears to be tracheomalacia rather than extrinsic compression. 32 This is particularly true in children with oesophageal atresia. Third, a large proportion of normal infants have imaging evidence of an anterior impression on the trachea at the level where it is crossed by the innominate artery. In one study, an anterior impression on the tracheal air column was seen on lateral chest radiographs in 30% of children younger than 2 years of age. 33 This finding is less common in older children. 33,34 Nevertheless, there do appear to be some children in whom arteriopexy, 35 reimplantation or even transection of the innominate artery 36 is beneficial. A high (cervical) aortic arch may also compress the trachea, but this is extremely rare.
7 VASCULAR COMPRESSION OF THE AIRWAY 91 Figure 4 Tetralogy of Fallot and absent pulmonary valve syndrome with airway compression in a 15-month-old boy. (a) CT volume rendered image shows compression of the left main bronchus (arrow). (b) Axial CT of the thorax shows severe compression of the airway between the vertebral body and the grossly enlarged pulmonary arteries. (c) Lateral bronchogram confirms severe anterior compression of the airway caused by the enlarged pulmonary arteries. (d) 2.2-mm flexible bronchoscopy shows canal compression.
8 92 C. A. MCLAREN ET AL. Figure 5 A 12-month-old girl, ventilator-dependent, with dilated cardiomyopathy. (a) 2.2-mm flexible bronchoscopy shows compression of the left main bronchus (arrow). (b) On bronchography the left main bronchus is completely occluded with no passage of contrast into the left lung. (c) A self-expanding stent has been deployed. (d) Bronchoscopy shows good position of the stent, with patency of the left main bronchus. Left-sided aortic arch with aberrant right subclavian artery This relatively common anomaly does not lead to airway compression unless there is a right-sided ligamentum arteriosum. 3 Acquired cardiovascular disease Dilated cardiomyopathy causes airway obstruction when the left atrium is sufficiently dilated to compress the LMB. This may lead to chronic infection of the left lung and progressive deterioration in the child s clinical condition. If
9 VASCULAR COMPRESSION OF THE AIRWAY 93 other treatments are unsuccessful, the insertion of a selfexpanding stent in the LMB may be effective (Fig. 5). Aneurysm of the aorta or ductus arteriosus is a very rare cause of airway compression in childhood. 37 CONCLUSION Imaging plays a crucial role in the diagnosis and treatment of vascular compression of the airway in children. In most centres, MDCT and MRI are increasingly used for the evaluation of children with suspected vascular compression, replacing barium swallow studies and catheter angiography. Although we agree with this change in imaging strategy, these techniques still have some limitations. Both MRI and MDCT are at present inadequate to differentiate reliably between dynamic airway obstruction (caused by tracheobronchomalacia) and fixed airway obstruction, as seen in extrinsic vascular compression. This is important as the presence and the severity of tracheobronchomalacia are strongly related to patient outcome. In addition, MDCT and MRI cannot yet identify complete tracheal rings. Stent insertion is only useful in selected patients with airway compression, but it may be appropriate for patients who fail all other forms of treatment. REFERENCES 1. Kussman BD, Geva T, McGowan FX. Cardiovascular causes of airway compression. Paediatr Anaesth 2004; 14: Sebening C, Jakob H, Tochtermann U et al. Vascular tracheobronchial compression syndromes experience in surgical treatment and literature review. Thorac Cardiovasc Surg 2000; 48: McLaughlin RB Jr, Wetmore RF, Tavill MA, Gaynor JW, Spray TL. Vascular anomalies causing symptomatic tracheobronchial compression. Laryngoscope 1999; 109: Woods RK, Sharp RJ, Holcomb GW 3rd et al. Vascular anomalies and tracheoesophageal compression: a single institution s 25-year experience. Ann Thorac Surg 2001; 72: discussion Shah RK, Mora BN, Bacha E et al. The presentation and management of vascular rings: an otolaryngology perspective. 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