History
A 7-month-old 20-kg male Labrador Retriever was referred for investigation of a low-grade heart murmur in association with exercise intolerance.
On physical examination, the dog’s body score condition was 4/9, rectal temperature was 37.9 °C (reference range, 37.2 °C to 39.2 °C). The heart rate was 110 beats per minute (bpm; reference range, 80 to 120 beats/min) with regular rhythm and normodynamic, symmetrical, and synchronous pulses. There was a grade 2/6 systolic heart murmur over the left base. Oscillometric systolic blood pressure was 164 mm Hg (reference range, 120 to 130 mm Hg). On pulse oximeter, his oxygen saturation in room air was 100% and there was no B-lines on point-of-care ultrasound that would suggest the presence of pulmonary edema. Hematologic evaluation revealed mild neutropenia (3.460 X 109/L; reference range, 3.60 to 12.0 X 109/L) and mild anemia (PCV 0.35L/L; reference range, 0.39 to 0.55 L/L). On serum biochemistry, there was mild hypoproteinemia (49.6 g/L; reference range, 58.00 to 73.00 g/L), mildly increased alkaline phosphatase (133 U/L; reference range, 20.0 to 60.00 U/L), mildly decreased triglycerides (0.47 mmol/L; reference range, 0.57 to 1.14 mmol/L), increased creatinine kinase (348 U/L; reference range, 50.00 to 200.00 U/L), increased phosphate inorganic (2.3 mmol/L; reference range, 0.90 to 2.00 mmol/L) and mildly decreased magnesium (0.65 mmol/L; 0.69 to 1.18 mmol/L). Prothrombin and partial thromboplastin times were within reference ranges.
Echocardiography was performed (Figure 1).
Two-dimensional echocardiographic views of a 7-month-old, male Labrador Retriever with a low-grade heart murmur and clinical signs of exercise intolerance and reduced energy levels. A—Parasternal short-axis view of the heart base. B—Short-axis view at the heart base, optimized for pulmonary artery. C—Right parasternal long-axis view.
Citation: Journal of the American Veterinary Medical Association 262, 2; 10.2460/javma.23.08.0465
Diagnostic Imaging Findings and Interpretation
Echocardiography identified severe left atrial dilation (LA:Ao ratio, 2.19; reference, < 1.6:1), eccentric left ventricular and moderate mitral valve regurgitation. Systolic function was subjectively poor, and measurements of systolic function were compatible with systolic dysfunction. Interrogation of the right atrium, right ventricle and tricuspid valve was unremarkable. There was a small jet of pulmonic insufficiency that was below the threshold for pulmonary hypertension (velocity, 0.65m/s; reference, < 2.2m/s). Cardiac masses or pleural/pericardial effusions were not observed. There was a continuous, retrograde turbulent flow within the main pulmonary artery. This appeared to consist of 2 divergent jets emanating from a common source. One jet was directed toward the pulmonic valve at 2.74 m/s (systole) decreasing to 1.81 m/s (diastole). The second jet entered the left pulmonary artery directly. (Supplementary video SV1) An aortopulmonic vascular malformation with left-to-right-shunting was suspected. Because of the relatively low velocity, differentials included patent ductus arteriosus (PDA) with pulmonary hypertension, coronary artery fistula and aortopulmonary window.1–4 The divergent turbulent jets also raised the possibility of an additional main pulmonary artery dissection.1–4 Causes of mitral insufficiency included mitral valve dysplasia and mitral incompetence secondary to annular dilation caused by volume overload (Figure 2).
Two-dimensional echocardiographic views. A—Parasternal short-axis view of the heart base showing the left atrium (LA; asterisk) and the aorta (Ao; star). Increased LA:Ao ratio = 1.78. Electrocardiogram showing sinus rhythm with a heart rate of 116 beats per minute. B—Short-axis view at the heart base, optimized for pulmonary artery – demonstrating a turbulent blood flow into 2 jets, 1 into the main pulmonary artery (asterisk) and 1 into the left pulmonary artery – demonstrating a turbulent blood flow into 2 jets, 1 into the main pulmonary artery and 1 into the left pulmonary artery secondary to a left-to-right shunting structure (white arrow). Electrocardiogram showing sinus rhythm with a heart rate of 107 beats per minute. C—Right parasternal long-axis view demonstrating mitral regurgitation with color Doppler. Electrocardiogram showing sinus rhythm with a heart rate of 116 beats per minute.
Citation: Journal of the American Veterinary Medical Association 262, 2; 10.2460/javma.23.08.0465
A CT multiphase contrast angiography (angio-CT) under general anesthesia was performed for identification and characterization of the shunting vessel (Figure 3). Arising from the right side of the descending aorta at the level of the mid aspect of the seventh vertebral body, an abnormally enlarged dorsal intercostal artery was identified. It branched immediately into an equally enlarged left bronchoesophageal artery that ran cranially and tortuously along the dorsal aspect of the esophagus to form an abnormal network of small tortuous vessels surrounding the esophagus and the trachea. Arising from this network, a prominent and aberrant vessel was visible entering the left pulmonary artery at its dorsomedial wall at the level of the caudal aspect of the fourth thoracic vertebra, through an ostium of approximately 3.7 mm. On the dextro-phase post-contrast series, a jet of non-enhanced blood was present entering the contrast enhanced left pulmonary artery, confirming a left-to-right (systemic to pulmonary) direction of the shunt.
Postcontrast thoracic CT images with a 5-mm-thick slab maximum intensity projection in transverse plane at the level of T7 (A) and in sagittal reconstruction (B). Note the abnormally engorged dorsal intercostal artery arising from the right side of the aorta (arrow), as well as the dense network of paraesophageal vessels (asterisk). Window width, 714 HU; window level, 270 HU; 1-mm slice thickness. L = Left.
Citation: Journal of the American Veterinary Medical Association 262, 2; 10.2460/javma.23.08.0465
Treatment and Outcome
The patient was managed with medical and surgical treatment. Oral pimobendan was initiated preoperatively for inotropic support at 0.25 mg/kg, twice daily, 3 weeks prior surgical ligation of the shunt. A left sided lateral thoracotomy was performed at the level of the fifth intercostal space. The lateral aspect of the branch originating from a periesophageal network of tortuous vessels was identified at the entry of the pulmonary artery and a palpable thrill was felt when palpating the main branch as it joined the pulmonary artery. It was dissected free from the surrounding tissue and ligated. As it was occluded, the thrill was immediately dissipated, and the murmur no longer audible with esophageal stethoscope. There was a momentary reflex bradycardia (105 bpm to 90 bpm) and a mild increase in arterial blood pressure (SP from 120 mm Hg to 130 mm Hg) during the occlusion (possible Branham sign), that resolved, without the need for any medical intervention. Post-operative recovery was uneventful, and the patient was discharged 2 days later.
On follow-up echocardiography after 1 month, there was moderate residual mitral insufficiency, but systolic dysfunction had improved slightly after surgery. Residual left-to-right shunting could not be identified, indicating successful ligation of the shunt. The left atrial size and left ventricular (diastolic) diameters normalized after surgery, consistent with a reduction of the left-sided cardiac preload.
At 10 months post-operatively, mitral insufficiency has reduced further. Systolic function was unchanged compared to the first post-operative scan. Left atrial and ventricular sizes were still within the normal reference ranges and residual shunting was still not apparent.
Comments
Patent ductus arteriosus results in a highly characteristic continuous heart murmur over the left cranial thorax.3 Far less common are aortopulmonic or arteriopulmonic vascular malformations that clinically resemble a PDA and which have previously reported in dogs.1,2 Similar hemodynamic consequences such as left sided volume overload and reduced systolic function can make a challenge to differentiate from PDA solely by Doppler echocardiography.1
A CT scan with contrast angiography has been shown to play a determinant role in the characterization of the shunting vessels.1,4 Previous studies suggest that the volume overload seen in aortopulmonic vascular abnormalities can lead to left-sided congestive heart failure, even though these abnormalities often present as an incidental finding.1 In this clinical case there was evidence, early in the patient’s life, of volume overload. Surgical ligation should therefore be considered and was shown to be a valid method of occlusion and successful in resolution of congestive heart failure in aberrant bronchoesophageal arteries.1 Furthermore, the use of angio-CT to plan the surgical approach and a suitable site for ligation close to the main pulmonary artery entry point is validated by the lack of residual shunting and reduction in volume overload still present nearly 1 year later.
Two key features raised the suspicion that it was not a PDA causing the continuous murmur. First, the murmur intensity was relatively low, relating to a systolic shunt velocity within the main pulmonary artery < 3 m/s. Second, there was no evidence of pulmonary hypertension and bidirectional shunts, which would be expected to accompany low shunt velocities with PDA.1,5 Nevertheless, an angio-CT scan with contrast angiography was required to confirm the diagnosis and to characterize the nature of the shunting vessels, which emphasizes the importance of advanced imaging and angiography prior implementation of treatment plans.1,4
The noteworthy feature of this case was the indirect and tortuous route of the shunt. Previous reports of aortopulmonic vascular malformations or aberrant bronchoesophageal arteries identify a single parent vessel following a relatively direct course and plexuses of tortuous vessels of unclear origins. In our case, there was a clear parent dorsal intercostal artery, an intermediate network of tortuous vessels and a final, single vessel entering the main pulmonary artery.
In the dog of the present report, the 10-month follow-up has shown successful surgical ligation of the aberrant bronchoesophageal based on absence of residual flow, improved mitral regurgitation, normalization of cardiac dimensions and complete resolution of clinical signs.
In conclusion, angio-CT plays a vital role in the characterization and successful surgical planning of hemodynamically significant arteriopulmonic vascular malformations that mimic PDA.
Supplementary Materials
Supplementary materials are posted online at the journal website: avmajournals.avma.org
Acknowledgments
The authors declare no conflict of interest.
Disclosures
The authors have nothing to disclose. No AI-assisted technologies were used in the generation of this manuscript.
Funding
The authors have nothing to disclose.
References
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Yamane T, Awazu T, Fujii Y, et al. Aberrant branch of the bronchoesophageal artery resembling patent ductus arteriosus in a dog. J Vet Med Sci. 2001;63(7):819-822. doi:10.1292/jvms.63.819
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Bonagura JD, Lehmkuhl L. Congenital heart disease. In: Fox PR Sisson D Moise NS, eds. Textbook of Canine and Feline Cardiology: Principles and Clinical Practice. 2nd ed. WB Saunders; 1999:579-589.
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