Case 1 was presented to the pre-BSAVA satellite meeting of the Veterinary Cardiovascular Society, UK in April 2008
Corresponding author: G.J. Culshaw, Division of Veterinary Clinical Sciences, Royal (Dick) School of Veterinary Studies, The University of Edinburgh, Hospital for Small Animals, Roslin EH25 9RG, UK; e-mail: firstname.lastname@example.org.
A 7-month-old intact female Cocker Spaniel weighing 7.7 kg was presented for investigation of a heart base murmur. The dog was free from clinical signs. There was a grade IV/VI pansystolic murmur localized over the left heart base. Femoral pulses were of normal volume and character.
Routine serum biochemistry and hematology were unremarkable. Echocardiography showed increased left ventricular internal end diastolic diameter (LVIDD) at 4.2 cm (reference range, 2.3–3.4 cm1) and left ventricular internal end systolic diameter (LVIDS) at 2.8 cm (reference range, 1.4–2.4 cm1), and mildly increased left atrial (LA) to aorta (AO) ratio at 1.8 : 1 (reference range, <1.62) (Fig 1A). Spectral Doppler echocardiography showed increased aortic velocity (AV) at 1.8 m/s (reference range, 1.0–1.4 m/s3) and continuous retrograde flow in the main pulmonary artery ranging from 1.8 m/s in systole (Vs) to 1.2 m/s in diastole (VD) (Fig 1B). Color Doppler echocardiography identified the point of entry of the main shunting vessel into the proximal pulmonary artery (Fig 1C). A PDA was suspected, but not fully imaged (Fig 1A).
Selective angiography in the proximal descending aorta showed contrast opacifying a network of tortuous vessels in the dorsocaudal thorax (Fig 2A) with subsequent opacification of the left atrium. A diagnosis of a congenital left-to-right systemic to pulmonary artery vascular shunt was made. In view of the size of the vessel, number of tortuous vessels, and the increased left heart dimensions, surgical ligation of the shunting vessel was attempted.
A left thoracotomy was performed at the 5th intercostal space. Multiple tortuous vessels over the visceral surface of the lungs corresponded to those seen on angiography (Fig 3A). The point of entry of the main vessel into the pulmonary artery could not be identified, but an anomalous vessel, thought to be a bronchoesophageal artery, was observed coursing cranially toward the pulmonary artery from the descending aorta. Digital pressure on this vessel abolished the murmur audible on esophageal stethoscope. After ligation of this vessel, the tortuous vessels immediately decreased dramatically in size. Whether the anomalous vessel arose directly from the descending aorta or a dorsal intercostal artery was not determined. Routine closure was performed and the dog recovered uneventfully.
Follow-up color Doppler echocardiography 1 month postoperatively showed reduction in LVIDD to 3.2 cm and LVIDS to 2.5 cm, LA : AO to 1.5 : 1 and AV to 1.3 m/s. There was laminar flow within the pulmonary artery and no shunt was identified.
The dog continues to do well clinically 28 months later, although further echocardiography has not been performed.
A 6-year-old neutered female Labrador Retriever weighing 26.7 kg was presented for investigation of coughing, inappetence, and a left-sided murmur of 1 year duration. On auscultation, there was a grade IV/VI left apical systolic murmur.
Routine serum biochemistry and hematology analysis were unremarkable.
Color Doppler echocardiography identified increased LVIDD at 5.7 cm (reference range, 3.3–4.9 cm1), LVIDS at 4.4 cm (reference range, 2.0–3.5 cm1), and LA : AO at 1.9 : 1. There was moderate mitral valve regurgitation, mild aortic, and tricuspid insufficiency, normal AV at 1.6 m/s, and continuous turbulent flow in the pulmonary artery (velocity not recorded). A PDA was suspected, but not imaged.
Selective angiography in the proximal descending aorta showed opacification of clusters of bizarre, tortuous vessels between the aorta and pulmonary artery with simultaneous opacification of both major vessels (Fig 2B).
During a left thoracotomy at the 4th intercostal space, multiple, tortuous shunting vessels were observed in the mediastinum between the aorta and pulmonary artery. A single, large, vibrating vessel was identified arising from the aorta caudal to the ligamentum arteriosum and coursing to the pulmonary artery. The tortuous vessels appeared to communicate with the pulmonary artery branches. The large vessel was ligated. Repeat angiography postligation (Fig 2C) showed no evidence of shunting. Recovery from surgery was uneventful.
Follow-up echocardiography 6 weeks later showed a slight reduction in LVIDD (5.4 cm), LVIDS (4.0 cm), and LA : AO (1.6 : 1) with no residual shunt.
A 2-year-old intact male Bull Mastiff weighing 47 kg was presented for management of atrial fibrillation which had developed under general anesthesia for an orthopedic condition 11 months previously. The dog was receiving digoxin.1 Mild exercise intolerance was present.
On physical examination, a heart rate of 140–160 beats/min with a chaotic rhythm, multiple pulse deficits, and a left-sided grade II/VI systolic murmur were identified.
Color Doppler echocardiography showed increased LVIDD at 6.0 cm (reference range, 3.9–5.7 cm1), LVIDS at 4.4 cm (reference range, 2.4–4.2 cm1), and LA : AO at 1.8 : 1, moderate mitral insufficiency and continuous retrograde flow in the main pulmonary artery. VS was 2.3 m/s and VD was 1.5 m/s. AV was increased at 3.5 m/s. A left-to-right shunting PDA was suspected, although not identified.
An ECG confirmed atrial fibrillation. The patient was discharged and received a combination of digoxin,1 benazepril,2 and sotalol.3 Selective angiography on a separate occasion demonstrated abnormal passage of contrast from aorta to pulmonary artery, but no obvious PDA.
A left thoracotomy was performed at the 5th intercostal space. Multiple, tortuous shunting vessels were observed (Fig. 3B). A thrill was palpable within the left pulmonary artery and an abnormal vessel caudal to the ligamentum arteriosum was identified exiting the aorta on its right ventrolateral aspect. The vessel was dissected and ligated. Diastolic blood pressure rose immediately on ligation (value not recorded). Postoperative recovery was unremarkable. Ten days postoperatively, LVIDD had decreased to 4.7 cm, LVIDS to 3.9 cm, LA : AO to 1.4 : 1, and AV to 2.2 m/s. A normal interstitial lung pattern was present on thoracic radiography. Direct current cardioversion was attempted under anesthesia, and resulted in sinus rhythm for approximately 5 minutes, after which sustained atrial fibrillation recurred. Medical treatment remained unchanged. The patient was clinically well during the first 14 months postsurgery. In the next 8 months, a gradual improvement in exercise tolerance was noted by the owners.
A 4-year-old neutered male German Shepherd dog weighing 29.1 kg was presented for investigation of congestive heart failure confirmed by thoracic radiography and stabilized with furosemide,4 benazepril,2 and pimobendan.5 A grade III/VI holosystolic left heart base murmur was audible. On echocardiography there was increased LVIDD at 6.1 cm (reference range, 3.4–5.0 cm1), LVIDS at 4.4 cm (reference range, 2.1–3.6 cm1), and severely increased LA : AO at 2.6 : 1. AV was 1.3 m/s. There was continuous retrograde flow in the main pulmonary artery. VS was 3.9 m/s and VD was 2.2 m/s. An aberrant vessel was identified entering the main pulmonary artery at its bifurcation. The dog was managed conservatively for several weeks but worsened despite additional diuresis with coamilozide.6 Nonselective computed tomographic angiography (ANGIO-CT) (Fig 4) demonstrated a large, shunting vessel passing from the descending aorta on the left side, ventral to the esophagus without esophageal compression, to the right side of the trachea, and then entering the right pulmonary artery. Several small tortuous vessels originating from the aorta and entering the pulmonary artery were identified. The shunt direction of left to right was confirmed by sequential analysis of flow and density of contrast on levophase angiography in which contrast density was greater in the left heart, aorta, and shunting vessels (180 Hounsfield units) compared with the right ventricle and main pulmonary artery (100 Hounsfield units). As a result of the ANGIO-CT, a right thoracotomy was undertaken at the 4th intercostal space. Multiple tortuous mediastinal vessels were apparent. The right azygos vein was ligated to improve access to the main shunting vessels through which pulsatile flow was palpable. On ligation, there was an immediate reduction in size of the small tortuous satellite vessels except for 2 additional tortuous vessels, which were ligated individually. The dog recovered uneventfully from surgery. Congestive heart failure was managed medically. At 3 weeks postoperatively, no shunting flow into the pulmonary artery was observed on echocardiography. LVIDD (5.6 cm), LA : AO (1.3 : 1), and AV (0.8 m/s) had all decreased, but LVIDS was unchanged.
Vascular malformations involving the systemic and pulmonic circulations have been reported previously in dogs[4-7] under the nomenclature of aberrant bronchoesophageal arteries (ABAs), but this is the 1st case series to more fully elucidate their complex nature, to show they can lead to congestive heart failure, and to describe detailed imaging investigation, surgical appearance, and ligation for each dog with long-term follow-up. These malformations may have been congenital or acquired, but probably congenital at least in case 1 owing to the dog's young age.
The lungs have 2 circulations: a pulmonary circulation and a bronchial circulation. The pulmonary circulation supplies deoxygenated blood to the alveoli for gas exchange. The nutritional blood supply to the esophagus, bronchi, and lung parenchyma, and pulmonary artery vasa vasorum arises from the bronchoesophageal artery, a single artery arising from the descending aorta or the right 5th intercostal artery, that ultimately drains into bronchial veins. In all 4 cases, a large aberrant vessel appeared to arise from, or very close to, the descending aorta, caudal to the ligamentum arteriosum. Risk of hemorrhage while dissecting near the aorta made it impossible to determine whether the site of origin involved the right 5th intercostal artery in cases 1 and 2. Surgical inspection in case 3 and ANGIO-CT in case 4 showed the definitive origin of the parent vessel and an ABA was suspected.
The bronchial circulation can take part in gas exchange, but this normally only occurs during exercise or, under local neurohumoral control,[9-11] under conditions of alveolar hypoxia, lung lobe consolidation, or atelectasis. In the dog, pig, and humans,[10, 11] bronchial arterial flow can enter the pulmonary circulation either proximal to, distal to, or within the alveolar capillary bed. Substantial shunting into the pulmonary circulation may occur when there is coincidental bronchial venoconstriction. Thus, the aberrancy in this case series was that the ABA was large, entered the pulmonary circulation more proximally than usual, and was shunting into the pulmonary circulation in the absence of lung pathology at rest.
A key feature of these cases was the tortuous vessels which suggests a very complex nature to these shunts. They were easily visualized on both angiography and at surgery, and hampered surgical dissection. Visible pulsation was present in some, suggesting direct communication to pulmonary or systemic arteries. They may have been normal collateral vessels, arising from an ABA, that received far greater flow than normal or a separate network of aorta to pulmonary artery shunting vessels, as suggested on ANGIO-CT in case 4, with or without a connection to the major vessel. In case 4, there were at least 2 larger vessels in addition to the major vessel, with aortic origins that required separate ligation. These had some similarities on ANGIO-CT to major aortopulmonary collateral arteries (MAPCAs),[14, 15] embryonic vascular systemic to pulmonary circulatory connections that usually regress by birth, but can be maintained when the pulmonary circulation fails to develop as in pulmonary atresia.[15, 16] However, concurrent tortuous vessels are not usually apparent in such cases.
In cases 1–3, ligation of the major vessel resulted in immediate shrinkage of some or all of the tortuous vessels suggesting at least some communication with the major vessel distal to the point of ligation because none of these cases had angiographic or ANGIO-CT evidence of flow into the vessels from the pulmonary artery. The component of the tortuous network that was venous (deoxygenated) was not fully ascertained. Blood gas analysis and intravessel pressure measurements during surgery would have given additional information, but was not performed.
This case series shows that the term “aberrant bronchoesophageal artery” is inadequate. A single vessel connecting the aorta and pulmonary artery would be similar hemodynamically and in appearance to a PDA. In all 4 cases, the ABA coexisted with a network of closely related tortuous vessels, although the exact relationship between these vessels and the ABA was not ascertained. This case series shows that when such vessels are identified, a presumptive diagnosis of PDA would appear unlikely.
Where recorded, these cases had systolic velocity shunt flow <4 m/s, which is less than that recorded for uncomplicated PDA. This could have been because of developing pulmonary hypertension (although there was no other echocardiographic evidence for it), underestimation of the true velocity of flow owing to a suboptimal angle of incidence in the interrogating ultrasound beam, a nonrestrictive pulmonary point of entry, loss of systolic pressure as a result of diversion of flow through collateral vessels, or decreased cardiac output caused by myocardial dysfunction. The lower velocity would explain the low intensity noncontinuous murmur in all 4 dogs.
Aortic velocities in PDA are increased as result of increased left-sided stroke volume. In cases 1, 2, and 4 they were not markedly increased, possibly because of left ventricular systolic dysfunction. Postligation, there were substantial reductions in cardiac dimensions in all dogs and in aortic velocities in dogs 1 and 4. AVs remained increased in dog 3 and it is possible that the dog had mild concurrent aortic stenosis.
A PDA was originally diagnosed in 3 dogs. Thus, we agree with Fuji et al that aortopulmonic vascular malformation should be considered as an alternative diagnosis to PDA when the murmur is not continuous, less than grade V/VI, a PDA is not directly visualized, or when maximal shunt flow velocity into the pulmonary artery is <4 m/s in the absence of clinically relevant pulmonary hypertension. Selective angiography or further imaging is recommended before surgical closure of a PDA when there is any doubt regarding the diagnosis on Doppler echocardiography.
Although ABA has been reported in dogs, only 1 report describes its surgical ligation. This was performed without prior Doppler echocardiography or angiography. In other reports, surgery was not performed because of technical concerns or because the volume overload was not considered clinically relevant and could be managed medically. The volume overload changes seen, especially in cases 3 and 4, suggest that aortopulmonic vascular malformation, possibly with concurrent mild aortic stenosis, can result in hemodynamically important left-sided volume overload, tachyarrhythmias, and even left-sided congestive heart failure. Therefore, surgical occlusion should be considered. Surgery was performed in all 4 dogs rather than intravascular occlusion owing to the complex nature of the shunts and difficulty in identifying and sizing the major shunting vessel. ANGIO-CT in case 4 was extremely useful for surgical planning and led directly to a right-sided rather than left-sided thoracotomy, providing much better exposure to the area of interest. The abnormal collateral vessels did not prevent successful ligation of the major vessel, and its ligation substantially decreased flow through the tortuous vessels with only the need to ligate 2 additional vessels in dog 4. All 4 dogs recovered uneventfully and showed echocardiographic evidence of decreased volume overload, although dog 3 remained in atrial fibrillation. This dog had sufficiently long-standing atrial fibrillation that cardioversion was unlikely despite the decrease in left atrial size.[2, 17] Surgery is a viable method of occlusion of aortopulmonic vascular malformation.
Aortopulmonic vascular malformations are complex, can cause clinically relevant volume overload, and can mimic PDA even on Doppler echocardiography, although certain clinical and echocardiographic features should prompt suspicion of their presence. Diagnosis can be confirmed on selective angiography and ANGIO-CT, the latter also determining an appropriate approach. Surgical ligation is a viable method of occlusion and will decrease shunting through abnormal collateral vessels and volume loading of the heart. Resolution of congestive heart failure is possible.
Dr E. M. Welsh MRCVS, Ms Ruth Willis MRCVS, and Mr Mike Martin MRCVS for assistance with case 1.
Conflict of Interest Declaration: Geoff Culshaw's lectureship was sponsored by Boehringer Ingelheim at the time case 1 was seen.
Lanoxin; Aspen Europe GmbH, Bad Oldesloe, Germany
Fortekor; Novartis Animal Health UK Limited, Camberley, UK
Beta-Cardone; RPH Pharmaceuticals AB, Haninge, Sweden
Furosemide; Millpledge Veterinary, Retford, UK
Vetmedin; Boehringer Ingelheim Limited, Bracknell, UK
Moduret; Merck Sharp and Dohme Limited, Hoddesdon, UK