Journal of Veterinary Cardiology (2015)

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Pulmonary artery dissection in eight dogs with patent ductus arteriosus* Brian A. Scansen, DVM, MS a,*, Elaine M. Simpson, DVM a,h, ´pez-Alvarez, LltVet, MRCVS b,c, Jordi Lo William P. Thomas, DVM d, Janice M. Bright, BSN, MS, DVM e, Bryan D. Eason, DVM f, John E. Rush, DVM, MS g, Joanna Dukes-McEwan, BVMS, MVM, PhD, MRCVS b, Henry W. Green III, DVM f, Suzanne M. Cunningham, DVM g, Lance C. Visser, DVM, MS a,i, Agnieszka M. Kent, DVM, MS a,j, Karsten E. Schober, DVM, PhD a a

Department of Veterinary Clinical Sciences, The Ohio State University College of Veterinary Medicine, Columbus, OH, USA b Small Animal Teaching Hospital, School of Veterinary Science, University of Liverpool, Leahurst, Chester High Road, Neston, Cheshire, UK c Department of Clinical Science and Services, Royal Veterinary College, London, UK d Veterinary Medical Teaching Hospital, School of Veterinary Medicine, University of California-Davis, Davis, CA, USA e Department of Clinical Sciences, College of Veterinary Medicine and Biomedical Sciences, Colorado State University, Fort Collins, CO, USA f Department of Veterinary Clinical Sciences and the Veterinary Teaching Hospital, College of Veterinary Medicine, Purdue University, West Lafayette, IN, USA g Department of Clinical Sciences, Cummings School of Veterinary Medicine at Tufts University, North Grafton, MA, USA Received 12 September 2014; received in revised form 4 December 2014; accepted 5 December 2014 *

A unique aspect of the Journal of Veterinary Cardiology is the emphasis of additional web-based images permitting the detailing of procedures and diagnostics. These images can be viewed (by those readers with subscription access) by going to http://www. sciencedirect.com/science/journal/17602734. The issue to be viewed is clicked and the available PDF and image downloading is available via the Summary Plus link. The supplementary material for a given article appears at the end of the page. Downloading the videos may take several minutes. Readers will require at least Quicktime 7 (available free at http://www.apple.com/quicktime/ download/) to enjoy the content. Another means to view the material is to go to http://www.doi.org and enter the doi number unique to this paper which is indicated at the end of the manuscript. * Corresponding author. E-mail address: [email protected] (B.A. Scansen). h Dr. Simpson’s current address is: Veterinary Teaching Hospital, Colorado State University, Fort Collins, CO, USA. i Dr. Visser’s current address is: Department of Medicine & Epidemiology, School of Veterinary Medicine, University of CaliforniaDavis, Davis, CA, USA. j Dr. Kent’s current address is: Newtown Veterinary Specialists, Newtown, CT, USA. http://dx.doi.org/10.1016/j.jvc.2014.12.001 1760-2734/ª 2014 Elsevier B.V. All rights reserved.

Please cite this article in press as: Scansen BA, et al., Pulmonary artery dissection in eight dogs with patent ductus arteriosus, Journal of Veterinary Cardiology (2015), http://dx.doi.org/10.1016/j.jvc.2014.12.001

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B.A. Scansen et al. KEYWORDS Angiography; Canine; Congenital heart disease; Echocardiography

Abstract Objectives: To describe a series of dogs with pulmonary artery dissection and patent ductus arteriosus (PDA). Animals: Eight dogs. Methods: Retrospective case series. Results: Pulmonary artery dissection was diagnosed in 8 dogs, 3 were Weimaraners. Four dogs presented in left-sided congestive heart failure, 4 presented for murmur evaluation and without clinical signs, and 1 presented in right-sided congestive heart failure. In 7 dogs the dissection was first documented concurrent with a diagnosis of uncorrected PDA. In the other dog, with pulmonary valve stenosis and PDA, the dissection was observed on autopsy examination 17 months after balloon pulmonary valvuloplasty and ductal closure. Median age at presentation for the 7 dogs with antemortem diagnosis of pulmonary artery dissection was 3.5 years (range, 1.5e4 years). Three dogs had the PDA surgically ligated, 2 dogs did not undergo PDA closure, 1 dog failed transcatheter occlusion of the PDA with subsequent surgical ligation, 1 dog underwent successful transcatheter device occlusion of the PDA, and 1 dog had the PDA closed by transcatheter coil delivery 17 months prior to the diagnosis of pulmonary artery dissection. The 2 dogs that did not have the PDA closed died 1 and 3 years after diagnosis due to heart failure. Conclusions: Pulmonary artery dissection is a potential complication of PDA in dogs, the Weimaraner breed may be at increased risk, presentation is often in mature dogs, and closure of the PDA can be performed and appears to improve outcome. ª 2014 Elsevier B.V. All rights reserved.

Abbreviations ACDO PDA RVp

Amplatz Canine Duct Occluder patent ductus arteriosus right ventricular pressure

Introduction Dissection of an elastic artery, such as the aorta or pulmonary artery, is defined as a tear in the tunica intima and subsequent infiltration of blood into the vessel wall, resulting in separation of tunica intima from the tunica media.1 The incidence of aortic dissection in people is reported as 3e5 per 100,000 humans in western countries, with chronic hypertension representing the underlying cause in w75% of cases.1 In small animal medicine, sporadic case reports exist of aortic dissection in hypertensive cats,2,3 2 dogs suspected to have elastin dysplasia,4 an older dog with an aortic aneurysm,5 and in a dog secondary to tumor infiltration.6 In humans, pulmonary artery dissections appear to be rarer than aortic dissections. Fewer than 100 human cases of pulmonary artery dissection have been described, with most diagnosed postmortem.7,8 Pulmonary artery dissections in people result from chronic pulmonary hypertension in nearly all reported cases (either primary or secondary to congenital heart disease) although iatrogenic

causes (cardiac catheterization or angiography), infection, inflammatory disease, or Marfan’s syndrome have also been described as potential etiologies.8,9 Three prior descriptions of pulmonary artery dissection in the dog have all been associated with concurrent aortic dissection.6,10,11 Recently, a pulmonary artery dissection was appreciated in a dog with an anomalous vessel between the ascending aorta and main pulmonary artery.12 The aim of this case series is to describe pulmonary artery dissection in 8 dogs, each with a patent ductus arteriosus (PDA).

Animals, materials and methods Case records from 8 dogs with echocardiographic, angiographic, or autopsy diagnoses of pulmonary artery dissection were retrospectively reviewed from 7 different veterinary hospitals throughout the United States and United Kingdom. Case details, imaging findings, treatment attempted, and outcome (if available) were compiled for all dogs (Table 1).

Results Signalment and clinical presentation The signalment and clinical details for the 8 cases of this report are listed in Table 1. All of the dogs

Please cite this article in press as: Scansen BA, et al., Pulmonary artery dissection in eight dogs with patent ductus arteriosus, Journal of Veterinary Cardiology (2015), http://dx.doi.org/10.1016/j.jvc.2014.12.001

Case information from 8 dogs with pulmonary artery dissection and patent ductus arteriosus. 1

2

3

4

5

6

7

8

Breed

Boston Terrier

Weimaraner

Shih Tzu

Weimaraner

Mixed breed

Weimaraner

Bearded Collie

Gender Age at presentation (years)

Male castrated 4

Male castrated 3.5

Female spayed 1.5

Male intact 3.5

Female spayed 2.5

Female spayed 4

Female spayed 3

Weight (kg) Presenting complaint

10.9 Murmur evaluation

43.3 Labored breathing

4 Labored breathing

33.5 Labored breathing

15.2 Ascites

Cavalier King Charles spaniel Male intact 0.4; PA dissection diagnosed at 1.8 years of age 4.6 Murmur evaluation

Auscultation

Grade IV/VI left basilar continuous murmur, Grade III/VI systolic right-sided murmur Hyperkinetic

Grade V/VI left basilar continuous murmur; S3 gallop

Grade V/VI left basilar continuous murmur

Grade V/VI left basilar continuous murmur

Hyperkinetic

Hyperkinetic

Hyperkinetic

Hyperkinetic

Hyperkinetic

Hyperkinetic

Hyperkinetic

TTE, TEE, TXR, cardiac cath

TTE, TEE, TXR, cardiac cath

TTE, TEE, TXR, cardiac cath

TTE, TXR, cardiac cath, CTA L-CHF

TTE, TXR, cardiac cath

TTE, TXR, cardiac cath

TTE

TTE, TXR, cardiac cath

Femoral pulse quality Diagnostics performed Additional findings

Therapy attempted

Outcome

Overcirculation of right lung lobes on TXR None

Euthanized for L-CHF 3 years after diagnosis

23.2 16.7 Lethargy; Murmur murmur evaluation evaluation Grade III/VI left Grade IV/VI left Grade IV/VI left basilar basilar systolic basilar continuous murmur continuous murmur murmur

Grade V/VI left basilar continuous murmur

Pulmonary valve Pulmonary hypertension stenosis (severe) (estimated 61/ 41 mmHg) None Transcatheter Transcatheter Surgical ligation Surgical ligation Transcatheter Surgical ligation ACDO placed coil; balloon ACDO failed; pulmonary surgical ligation valvuloplasty successful ReCHF resolved Resolution of LV Euthanized for Died suddenly at Alive, no No PDA flow Resolution of LV with ACDO and volume overload ReCHF 1 year home 17 months symptoms 4 noted postvolume overload after diagnosis after diagnosis; after ligation; medical years after after ligation; operatively; lost PA dissection therapy; alive asymptomatic 1 surgery to follow-up alive and noted on year after and without without autopsy diagnosis; lost to symptoms 4 symptoms 4 further followmonths after years after up diagnosis surgery L-CHF

L-CHF

ReCHF; hypovascularity of left lung lobes

None

ACDO ¼ Amplatz Canine Duct Occluder; Cath ¼ catheterization; CTA ¼ computed tomography angiography; L-CHF ¼ left-sided congestive heart failure; LV ¼ left ventricle; PA ¼ pulmonary artery; PDA ¼ patent ductus arteriosus; ReCHF ¼ right-sided congestive heart failure; TEE ¼ tranesophageal echocardiography; TTE ¼ transthoracic echocardiography; TXR ¼ thoracic radiographs.

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Case number

Pulmonary artery dissection in dogs

Table 1

4 presented in this report were young to middle age. The 7 dogs diagnosed with pulmonary artery dissection at the time of presentation had a median age of 3.5 years, ranging from 1.5 to 4 years in age. Breeds affected included 3 Weimaraners, and 1 each of Boston terrier, Shih Tzu, Bearded Collie, Cavalier King Charles spaniel, and mixed breed. Reasons for cardiac evaluation were respiratory signs secondary to left-sided congestive heart failure (cases 2, 3, 4) or murmur evaluation (cases 1, 6, 7, 8). One dog presented for evaluation of ascites and right-sided congestive heart failure (case 5). The gender distribution was equal, with 4 male and 4 female. Cardiac auscultation revealed a continuous heart murmur at the left base in all cases, except the dog in right heart failure (case 5), which presented with a systolic left basilar heart murmur. In all dogs the femoral pulse quality was hyperkinetic.

Thoracic radiography Thoracic radiographs were performed in all cases, revealing left heart enlargement, pulmonary over circulation, and dilation of the main pulmonary artery segment. In 2 cases (cases 1 and 5), hypoperfusion of the left lung lobes was suspected with increased perfusion to the right lung (Fig. 1). Pulmonary edema secondary to left-sided congestive heart failure was noted in 3 cases (cases 2, 3, 4).

B.A. Scansen et al.

Echocardiographic studies Transthoracic echocardiography revealed the presence of a left-to-right shunting PDA in all dogs, except for case 5 in which the PDA was diagnosed during diagnostic catheterization. In each of the 7 dogs with antemortem diagnosis of pulmonary artery dissection, turbulent flow was noted to enter the main pulmonary artery, but not reach the pulmonary valve due to a dissecting membrane and aneurysmal false lumen (Fig. 2; Video 1). In cases 1 through 7, the membrane resulted in a variable degree of supravalvular pulmonary stenosis, which in case 5 resulted in right ventricular hypertrophy, septal flattening, right atrial dilation, and the presenting clinical signs of rightsided congestive heart failure. Antegrade flow through the true lumen of the main pulmonary artery into the branch pulmonary arteries was variably obstructed, preferentially directed toward the right branch pulmonary artery due to the dissecting membrane (Fig. 2, Video 1). In case 8, the presenting echocardiogram did not identify a dissecting membrane, rather, this dog was diagnosed with pulmonary valve stenosis characterized by a thickened, doming, and fused valve with a peak instantaneous systolic pressure gradient across the pulmonary valve of 150 mmHg. Color flow and spectral Doppler were not suggestive of pulmonary hypertension except in case 7, with peak tricuspid regurgitation velocity estimating a

Figure 1 Right lateral (A) and ventrodorsal (B) thoracic radiographs from a 4-year-old Boston terrier (case 1) with pulmonary artery dissection. Note the mild left atrial enlargement, prominence of the aortic isthmus (arrow), and increased vascularity of the right lung as compared to the left.

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Pulmonary artery dissection in dogs

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Figure 2 Right parasternal short axis echocardiographic images from 4 dogs with pulmonary artery dissection. The dissecting membrane is shown by the arrow (A, C, E, F). Panels A & B: Gray scale (A) and color Doppler (B) images from a 4-year-old Boston terrier (case 1) showing laminar flow (blue) across the pulmonary valve and left-to-right turbulent flow (green) from the patent ductus arteriosus (PDA) entering the false lumen of the pulmonary artery dissection. Panels C & D: Gray scale (C) and color Doppler (D) images from a 3-year-old Bearded Collie (case 7) showing laminar flow (blue) within the true lumen of the pulmonary artery and turbulent left-to-right flow (red-green) from the PDA entering the false lumen of the pulmonary artery dissection. Panel E: Gray scale image from a 1.5-year-old Shih Tzu (case 3) showing a large aneurysmal false lumen (FL) nearly obstructing the true lumen of the pulmonary artery. Panel F: Gray scale image from a 2.5-year-old mixed breed dog (case 5) with pulmonary artery dissection after placement of an Amplatz Canine Duct Occluder (arrowhead) into the ductal ampulla with the pulmonary artery disc within the false lumen of the pulmonary artery. Ao ¼ aortic valve; PV ¼ pulmonary valve.

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6 systolic right ventricular pressure (RVp) of at least 61 mmHg and end-diastolic pulmonary insufficiency velocity estimating a diastolic pulmonary arterial pressure of 41 mmHg. Case 7 lived at an altitude of 4984 feet, which may have contributed to the development of pulmonary hypertension in this dog. Transesophageal echocardiography was performed in 3 dogs (cases 1, 2, 3), which confirmed the ductal anatomy, dissecting membrane, and aneurysmal false lumen (Video 2).

Cardiac catheterization and angiography Cardiac catheterization and angiography were performed in all but 1 dog (case 7). Contrast injections in the descending aorta confirmed ductal flow entering the false lumen created by the dissecting membrane in cases 1 through 5 (Fig. 3, Video 3). Right ventricular selective angiography was performed in cases 1, 3, 4, 5, and 6, showing a narrowing of the contrast stream in the main pulmonary artery and around the pulmonary dissection (Fig. 3, Video 3). A mild increase in systolic RVp consistent with supravalvular stenosis was reported in case 1 (systolic RVp ¼ 37 mmHg) and case 4 (systolic RVp ¼ 35 mmHg). An Amplatz Canine Duct Occluder (ACDO) was successfully placed within the ductus of case 5, having the pulmonary artery disc deployed within the pulmonary artery false lumen, resulting in resolution of ductal flow (Videos 3 and 4). Transcatheter closure of case 2 with an ACDO was attempted, with deployment of the pulmonary arterial disc within the true lumen of the pulmonary artery in an attempt to pull the dissecting membrane adjacent to the PDA ostium. Upon release, the ACDO embolized to the right pulmonary artery. Case 8, the dog with PDA and pulmonary valve stenosis, underwent PDA occlusion with a Gianturco stainless steel coil after balloon pulmonary valvuloplasty. Computed tomography angiography was performed in case 4 to further characterize the anatomy of the branch pulmonary arteries as asymmetric size was noted on angiography with the right pulmonary artery substantially larger than the left (Fig. 4). Non-selective bolus-tracking computed tomography through the great vessels revealed a severely dilated right pulmonary artery and a membrane that separated the main pulmonary artery longitudinally. The PDA was in a normal position, but entered the false lumen of the main pulmonary artery, prior to flow exiting preferentially toward the right pulmonary artery. The left

B.A. Scansen et al. pulmonary artery was visualized and was of normal size, though no flow from the ductus entered the left pulmonary artery due to the dissecting membrane. No tapering of the PDA at the pulmonary ostium could be appreciated.

Surgery Cases 3, 4, and 6 underwent PDA ligation through a standard left lateral thoracotomy following diagnostic catheterization. Case 2 also underwent surgical ligation of the PDA following embolization of the ACDO, which was left at the embolized location within the right branch pulmonary artery. Cases 1 and 7 did not have definitive therapy for the PDA attempted and were managed medically after diagnosis of the pulmonary artery dissection.

Follow-up The PDA was successfully closed in all dogs, except cases 1 and 7. No perioperative complications from the dissection were observed, with the exception of the device embolization in case 2. Case 1 was euthanized 3 years after diagnosis for left-sided congestive heart failure, following treatment with furosemide and enalapril by the referring veterinarian. Case 2 had mild mitral insufficiency, trace tricuspid insufficiency, mild pulmonary insufficiency, and mild obstruction of the left pulmonary artery secondary to the dissecting membrane reported on echocardiography 1 month after surgical ligation with no residual flow through the ductus. The dog remains alive and without clinical signs of heart disease 4 years after surgery. Case 3 had mild flow turbulence in the main pulmonary artery around the dissecting membrane on post-operative echocardiography the day after surgery, but no flow through the PDA was appreciated and the dog was then lost to follow-up. Case 4 was tapered off all cardiac medications and the dissecting membrane was challenging to visualize on echocardiography 1 month post-operatively. Case 4 was alive and asymptomatic 4 years after surgical ligation of the PDA. Case 5 had no residual flow through the PDA, the membrane appeared torn and mobile, and a 60% reduction in the flow velocity across the supravalvular stenosis was noted on repeat echocardiography 1 month after ACDO implantation (Video 4). Case 5 had resolution of clinical signs associated with right-sided heart failure and was receiving furosemide and enalapril 4 months after PDA occlusion. Case 6 was rechecked 1 year after PDA ligation and was asymptomatic. Echocardiography showed that the dissection was still present,

Please cite this article in press as: Scansen BA, et al., Pulmonary artery dissection in eight dogs with patent ductus arteriosus, Journal of Veterinary Cardiology (2015), http://dx.doi.org/10.1016/j.jvc.2014.12.001

Pulmonary artery dissection in dogs

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Figure 3 Angiography from 2 dogs with patent ductus arteriosus (PDA) and pulmonary artery dissection. Panels A & B: Aortic (A) and right ventricular (B) angiography from a 4-year-old Boston terrier (case 1) showing ductal flow into the false lumen (FL), not reaching the pulmonary valve (PV). The FL is seen as a filling defect during right ventricular (RV) injection at the cranial aspect of the pulmonary artery, which narrows the true lumen (TL) of the pulmonary artery distal to the PV. A marker pigtail catheter is present in the esophagus to allow for calibrated measurements. Panels C & D: Similar findings in a 1.5-year-old Shih Tzu (case 3), with a larger FL and more narrowed TL creating supravalvular pulmonary stenosis.

though it was no longer causing right ventricular outflow tract obstruction. There was no residual flow through the PDA following surgical ligation and the dog was lost to follow-up after this visit. Case 7 was euthanized 1 year after diagnosis because of severe right-sided heart failure. Case 8 was rechecked 1 month after balloon pulmonary valvuloplasty and PDA occlusion, with no residual PDA

flow observed and a peak instantaneous systolic pressure gradient across the pulmonary valve of 50 mmHg. A second recheck exam 10 months after catheterization showed a peak instantaneous systolic pressure gradient across the pulmonary valve of 26 mmHg. The dog then died suddenly at home 17 months after cardiac catheterization. The dog had no signs of heart disease at the time of death.

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B.A. Scansen et al.

Figure 4 Computed tomography angiography images from a 3.5-year-old Weimaraner (case 4) with pulmonary artery dissection and a patent ductus arteriosus (PDA). Axial images in the transverse plane during peak arterial opacification progress from cranial (A) to caudal (C) through the pulmonary artery. Both the ascending aorta (AAo) and descending aorta (DAo) are opacified and contrast enters the false lumen (FL) of the dissection through PDA with flow preferentially directed to the right pulmonary artery (RPA). The true lumen of the main pulmonary artery (MPA) is seen above the pulmonary valve (PV and arrow) and flow from the right ventricle is directed preferentially through the true lumen of the MPA to the left pulmonary artery (LPA). The dissecting membrane is shown in panels A and B by arrowheads.

Autopsy findings Postmortem evaluation of case 7 was performed after the dog was euthanized for severe right-sided congestive heart failure. A large PDA was visible.

The main pulmonary artery was severely dilated and, when opened, a rent in the endothelium was present and the tunica intima was circumferentially separated from the tunica media (Fig. 5A). The pulmonary artery dissection extended from the

Figure 5 Gross pathologic images from 2 dogs with pulmonary artery dissection. Panel A is from a 4-year-old Bearded Collie examined after euthanasia for right-sided heart failure. The main pulmonary artery and right ventricle (RV) are dilated and a dissecting membrane (arrowheads) is seen within the main pulmonary artery, separating the lumen in two with a false lumen (FL) seen at the cranial aspect. The ostium (arrow) of a patent ductus arteriosus (PDA) is seen entering the FL of the pulmonary artery dissection. Similar findings are seen in panel B from a 1.8-year-old Cavalier King Charles spaniel examined after sudden death. A thickened and dysplastic pulmonary valve (PV) in this dog was consistent with the antemortem diagnosis of pulmonary valve stenosis.

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Pulmonary artery dissection in dogs sinotubular junction of the pulmonary valve throughout the length of the main pulmonary artery and into the left branch pulmonary artery. A long circumferential rent in the endothelium was also found in the descending aorta, traversing the PDA and extending the length of the thoracic aorta. There was no evidence of aortic or pulmonary arterial rupture. Lung histopathology revealed changes indicative of pulmonary vascular damage from chronic over-perfusion including pulmonary muscular and elastic arteries that were thickened by marked medial hypertrophy, intimal fibrosis, and concentric elastosis. Histopathologic pulmonary changes secondary to chronic left-sided congestive heart failure were also noted. Cystic medial degeneration with proteoglycan deposits separating and disrupting the elastin fibers were seen on histopathologic examination of the aorta. Similar findings were seen in the main pulmonary artery. Postmortem evaluation of case 8 was performed following sudden death and revealed concentric hypertrophy of the right ventricular wall with a thickened and dysplastic pulmonary valve. The free edges of the mitral valve were mildly thickened and there was a small PDA present with the coil still in the proper position in the ductal ampulla with fibrous closure of the pulmonary ductal ostium. There was moderate pulmonary artery dilation and the vessel was separated into two layers directly adjacent to the PDA and distal to the pulmonary valve, creating a false lumen and consistent with a pulmonary artery dissection. There was a small 2 mm  2 mm circular tear in the tunica intima of the pulmonary artery directly adjacent to where the ductal ampulla entered the main pulmonary artery. The false lumen extended from this tear towards the pulmonary valve and circumferentially around the main pulmonary, encompassing 30% of the vessel circumference. The dissecting aneurysm in the main pulmonary artery was not ruptured and there was no evidence of hemorrhage at the site of the dissection (Fig. 5B). There was no evidence that the pulmonary artery dissection was the cause of death on postmortem examination. Lung sections revealed moderate diffuse alveolar histiocytosis with moderate pulmonary edema. A cause of death was not identified, but was speculated to be a fatal arrhythmia.

Discussion This case series describes 8 dogs with pulmonary artery dissection, all in association with PDA. Most human cases of pulmonary artery dissection have

9 been associated with chronic pulmonary hypertension or saccular aneursyms of the pulmonary artery.7,8 As in all dogs of this report, the site of the dissection in 80% of human cases is the main pulmonary artery.7 Congenital heart disease accounts for roughly half of all reported human cases of pulmonary artery dissection,7,8 though in nearly all cases severe pulmonary hypertension (e.g., Eisenmenger’s physiology) is speculated as the underlying cause of the dissection. Congenital heart diseases reported with pulmonary artery dissection include PDA,13e20 aortopulmonary window,21 double outlet right ventricle,22 atrial septal defect,23 and ventricular septal defect.24e26 Consequences of pulmonary artery dissection in people involve rupture and bleeding into the pericardial space; however, bleeding into the lungs, mediastinum, or pleural space has been reported.8,27 The pathophysiology of pulmonary artery dissection is not fully elucidated. It is thought that dilation of the pulmonary artery, typically due to pulmonary hypertension in people, results in medial degeneration and fragmentation of the elastic fibers with subsequent weakening of the vessel wall.7,28 As degeneration and fragmentation progress, the vessel wall weakens and the increased pulmonary artery pressure and sheer stress on the vessel wall result in intimal tearing and dissection. Blood then separates the tunica intima from the tunica media, creating a dissecting membrane and predisposing to a complete tear in the vessel wall.7 While aortic dissection often leads to separation of the tunica intima from the tunica media and propagation of the dissection along the aortic length, the thin wall of the pulmonary artery in people appears less likely to dissect with an intimal flap and more likely to rupture, increasing the mortality risk for pulmonary artery dissections.21 Pulmonary artery dissection is a rare finding in veterinary medicine. Aortic rupture and dissection with extension to the pulmonary artery has been described in several horses, particularly of Friesian ancestry.29,30 Pulmonary artery dissection and rupture has also been reported in cattle with fibrillin deficiency and a syndrome comparable to the human Marfan syndrome.31 The authors are aware of 4 cases reported in the literature describing pulmonary artery dissections in dogs.6,10e12 In the first 3 cases, the pulmonary artery dissection was associated with a concurrent aortic dissection either traversing a PDA,10 spanning the ligamentum arteriosum,11 or communicating in an uncertain location.6 In the most recent report, the pulmonary artery dissection was associated with an anomalous vessel between the ascending

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10 aorta and main pulmonary artery, the embryology of which was uncertain.12 In the prior case of pulmonary artery dissection with PDA, the dissection was speculated to originate in the aorta and traversed the PDA into the main pulmonary artery.10 Given the cases described here, we speculate that the dissection described in this prior report may have instead originated in the pulmonary artery and propagated across the PDA to the aorta. The dog presented in right heart failure secondary to the supravalvular pulmonary stenosis resulting from the dissecting membrane, similar to case 5 of this report, and the diagnosis of aortic and pulmonary artery dissection was made by echocardiographic and postmortem examination.10 Similar to the cases reported here, the dog of the prior report describing PDA and pulmonary artery dissection presented at 3 years of age for labored breathing.10 The second case reported was an iatrogenic pulmonary artery dissection that occurred during cardiac catheterization.11 The dissection occurred after resistance was felt upon advancement of an aortic catheter and resulted in the dog dying suddenly during the procedure. On autopsy, the dissection extended from the intima of the aortic arch to the pulmonary artery via the ligamentum arteriosum. The third case involved a dog with an obstructive chondrosarcoma of the aortic arch in which multiple tears in the aortic intima were appreciated, as well as a periaortic hematoma that compressed the right pulmonary artery.6 An intimal tear was identified in the main pulmonary artery, though communication to the aortic dissection could not be located.6 In the dogs reported here, aortic dissections were not apparent by echocardiography, conventional angiography, or computed tomography angiography. However, case 7 did have evidence of aortic dissection on autopsy evaluation, which had not been appreciated on echocardiographic studies performed antemortem. Without postmortem evaluation of all cases, the occurrence of aortic dissection with pulmonary artery dissection in these dogs is unknown. The most recent report of pulmonary artery dissection occurred in a young dog that presented in left-sided congestive heart failure, comparable to cases 2, 3 and 4 in this series.12 The dog was diagnosed with a congenital vascular anomaly and the pulmonary artery dissection was observed on computed tomography and selective fluoroscopic angiography. This recent report utilized computed tomography and magnetic resonance angiography to characterize aneurysmal dilatation of the main

B.A. Scansen et al. pulmonary artery, as well as the pulmonary artery dissection, which closely parallels the condition described in the dogs of our series, albeit from an anomalous vessel and not a PDA. In contrast to our series, this dog was 1 year of age at the time of presentation. The dogs described in this report (excluding case 8 which did not have a dissection at presentation) presented at a mature age for PDA evaluation, with a median age of 3.5 years. This is in contrast to the typical age at presentation for dogs with PDA, reported as a median age of 5 months in a series of 520 cases.32 Sufficient time may be necessary for the pulmonary artery to dilate or undergo degenerative changes in the wall to result in dissection. Although speculative, the dissections observed in these dogs likely occurred secondary to the high velocity PDA flow, secondary pulmonary artery aneurysm, and the increased shear stress on the pulmonary arterial wall for months to years. There was also a difference in sex predilection in this series (equal number of male and female dogs affected) when compared to large series of dogs with PDA where the proportion of female to male was nearly 3:1.32 It is unknown if males carry a greater risk for pulmonary artery dissection or if the numbers in this series are too small to adequately reflect a sex bias. Three of the dogs in this series were Weimaraners, a breed not commonly associated with PDA,32 suggesting an increased risk for pulmonary artery dissection in the breed. In human medicine, pulmonary artery dissections are usually fatal and present as cardiogenic shock or sudden death.7,8 In a literature survey of pulmonary artery dissections, 63 human cases were described, though only 8 were diagnosed antemortem.7 In contrast, only case 8 was associated with sudden death in this series and the cause of death in that dog could not be directly related to the dissection, as no rupture was apparent. This contrast may reflect the different etiologies of pulmonary artery dissection in humans versus dogs. While nearly all people with pulmonary artery dissection have chronic pulmonary hypertension,7,8 this finding was only apparent in 1 of the dogs of this report. Aneurysmal dilatation of the pulmonary artery associated with PDA in these dogs may have been sufficient to dissect the arterial wall, but both elevated pulmonary arterial pressure and secondary degenerative cystic wall changes may be necessary to ultimately result in arterial rupture. Aneurysmal dilatation of the main pulmonary artery has been associated with PDA in people, though is reported to occur in only 15% of humans with

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Pulmonary artery dissection in dogs uncorrected PDA.9 While aneurysmal pulmonary artery dilatation associated with PDA has progressed to pulmonary artery dissection in people, all cases had severe pulmonary hypertension secondary to uncorrected PDA,13e20,22 which is in contrast to most of the dogs reported here. Case 8 is unique in that pulmonary artery dissection was not documented prior to sudden death and autopsy evaluation. While it is possible that the dissection was present at the time of catheterization, a review of the echocardiographic and angiographic images failed to find any evidence of a dissecting membrane at that time or in the follow-up period. It appears more likely that the dissection occurred later in life, perhaps as a result of the chronic pulmonary artery aneurysm that remained after PDA closure and balloon pulmonary valvuloplasty. The cranial aspect of the pulmonary artery was presumably weakened in this dog from PDA flow, as the dissection was localized immediately opposite the prior ductal ostium. It is also possible, however, that the dissection was created iatrogenically during the catheterization procedure, either from trauma to the arterial wall from guidewire or catheter passage or from balloon inflation during pulmonary valvuloplasty. Iatrogenic trauma to the pulmonary arterial wall resulting in hemorrhage, dissection, or rupture has been reported during pulmonary artery catheterization in people, most often during placement of a Swan-Ganz catheter for hemodynamic monitoring.33e35 Pulmonary artery dissection secondary to balloon pulmonary valvuloplasty has also been reported in a child, which was not diagnosed until 11 years after the procedure was performed.36 The 2 dogs that did not have their PDA occluded were euthanized due to progressive cardiac disease and left-sided (case 1) or right-sided (case 7) congestive heart failure. Importantly, case 1 indicates that progression of this syndrome may be consistent with pulmonary over circulation and left-sided volume overload as seen in uncorrected PDA.32 Alternatively, case 7 indicates that signs of right-sided congestive heart failure may develop in this condition comparable to dogs with pulmonary hypertension from other causes of increased vascular resistance.37 However, right-sided congestive heart failure may also develop in this condition secondary to supravalvular pulmonary artery obstruction as seen in case 5 and comparable to other causes of acquired pulmonary artery stenosis in dogs.38 Although follow-up was not available for all dogs, the outcomes for cases 1 and 7 are in contrast to the other cases with successful closure and resolution of heart failure. This difference

11 suggests that ductal closure should be advised in similar cases to reduce the risk of future complications and heart failure. Surgical ligation had the highest success, though the result of case 5 suggests that transcatheter closure of the PDA with an ACDO can also be accomplished in the setting of pulmonary artery dissection.

Conclusions Pulmonary artery dissection should be considered a potential complication of uncorrected PDA in the dog. Dogs with this complication present at a mature age and older than the typical dog diagnosed with PDA. While only 8 cases are described, the proportion of Weimaraners in this sample suggests that this breed may be at increased risk for this complication. The dogs that underwent surgical or transcatheter closure of their PDA did well post-operatively; though care should be taken when deploying an ACDO into this anatomical structure given the risk for embolization. The dogs in this report that had the PDA closed remained clinically unaffected by their pulmonary dissections for years, which is in contrast to human reports of pulmonary artery dissection in which rupture is common. However, the 2 dogs that did not undergo PDA closure died from complications related to their primary heart condition, and closure of the PDA under such circumstances is therefore advised. Last, pulmonary dissection was diagnosed 17 months after PDA closure in 1 dog, and it remains uncertain if this was a result of iatrogenic trauma or a consequence of pulmonary artery aneurysm and reduced vessel integrity from prior ductal flow.

Conflict of interest The authors declare no conflict of interest.

Acknowledgments The authors wish to thank J. Fraser McConnell BVMS, MRCVS for assistance during the acquisition of, as well as Thomas Maddox BVSc, PhD, MRCVS for his help retrieving the archived images of the computed tomography angiography of case 4. The authors gratefully acknowledge Greta M. Krafsur DVM, MS and Paula A. Schaffer DVM, MS for providing the postmortem description and photograph for case 7. Finally, the authors acknowledge Barret J. Bulmer DVM, MS for clinical contributions to

Please cite this article in press as: Scansen BA, et al., Pulmonary artery dissection in eight dogs with patent ductus arteriosus, Journal of Veterinary Cardiology (2015), http://dx.doi.org/10.1016/j.jvc.2014.12.001

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B.A. Scansen et al.

case 2, Daniel F. Hogan DVM for clinical contributions to case 5, and Adrian Boswood MA, VetMB, MRCVS and Daniel J. Brockman BVSc, CertVR for clinical contributions to case 6.

Supplementary data Supplementary data related to this article can be found at http://dx.doi.org/10.1016/j.jvc. 2014.12.001.

Video Table Video 1

Video 2

Video 3

Video 4

Compilation of transthoracic echocardiographic images from 2 dogs (cases 1 and 3) with pulmonary artery dissection and patent ductus arteriosus. An ¼ aneurysm; Ao ¼ aorta; CDI ¼ color Doppler imaging; D ¼ ductal ampulla; LA ¼ left atrium; LCLAX ¼ left cranial long axis; LPA ¼ left pulmonary artery; LV MM ¼ M-mode of left ventricle; PV ¼ pulmonary valve; RPA ¼ right pulmonary artery; RPLAX ¼ right parasternal long axis; RPSAX ¼ right parasternal short axis; RPSAX PV ¼ RPSAX at the level of the pulmonary valve; RV ¼ right ventricle; TTE ¼ transthoracic echocardiogram Tranesophageal echocardiographic (TEE) images of patent ductus arteriosus and pulmonary artery dissection from a 1.5-year-old Shih Tzu (case 3). See Video 1 for key. Compilation of angiographic images from 3 dogs (cases 1, 3, and 5) with pulmonary artery dissection and patent ductus arteriosus. ACDO ¼ Amplatz Canine Duct Occluder; LV ¼ left ventricular; RV ¼ right ventricular; RVOT ¼ right ventricular outflow tract. Post-operative transthoracic echocardiographic images from a 2.5-year-old mixed breed dog (case 5) following transcatheter ductal occlusion. See Videos 1 and 3 for key.

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Please cite this article in press as: Scansen BA, et al., Pulmonary artery dissection in eight dogs with patent ductus arteriosus, Journal of Veterinary Cardiology (2015), http://dx.doi.org/10.1016/j.jvc.2014.12.001

Pulmonary artery dissection in eight dogs with patent ductus arteriosus.

To describe a series of dogs with pulmonary artery dissection and patent ductus arteriosus (PDA)...
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