Chylothorax Associated With Tricuspid Dysplasia and Atrial Septal Defect in a Bullmastiff

Introduction

Chylothorax is a potentially devastating condition characterized by accumulation of lymphatic fluid in the pleural space.^1,2 Since the advent of lymphangiography, traumatic thoracic duct rupture has been considered the most common cause of chylothorax in dogs and cats.^1–3 Many disorders may lead to increased pressure in the thoracic lymphatic vessels, thus resulting in leakage of chyle. Disorders include mediastinal masses (i.e., aortic body tumor, lymphosarcoma, thymoma, and lung lobe teratoma), fungal granulomas, venous thrombi, lung lobe torsion, and cardiac disorders associated with increased right atrial pressure (i.e., congenital cardiac anomalies, heartworm infection, cardiomyopathies, and pericardial diseases).^1,2,4–16 In many cases, chylothorax is deemed as idiopathic, since none of the above causes could be found to explain the etiology of chyle effusion.^1,2,17 Chylothorax secondary to congenital and acquired cardiac disorders has been reported in cats but is poorly documented in the dog.^1,2,12–16 To the best of the authors’ knowledge, only one dog with chylothorax associated with congenital cardiac disorder (i.e., double-chambered right ventricle with tricuspid dysplasia) has been recently described.¹⁸

The purpose of this report is to describe the diagnosis and management of chylothorax in a dog with complex congenital cardiac disorder.

Case Report

A 14-month-old, 44-kg, male bullmastiff was referred because of anorexia, lethargy, and tachypnea. Upon physical examination, the dog was dyspneic (60 breaths per minute). Oral mucous membranes were congested, with a 3-second capillary refill time. The abdomen was mildly distended, and a fluid wave was barely appreciable. Femoral pulses were weak and regular. Cardiac auscultation revealed muffled heart sounds, with a heart rate of 130 beats per minute [bpm] and a holosystolic murmur best heard over the right hemithorax. Pulmonary sounds were only appreciable in the dorsal part of the thorax. Complete blood count and serum biochemical tests were within reference ranges.

Sinus tachycardia with a heart rate of 170 bpm and deep S waves in leads II, III, and aVL were recorded on electrocardiography. Thoracic radiographs showed decreased visualization of the heart because of moderate-severe pleural effusion [Figures 1A, 1B]. Presence of fluid in the abdomen was also appreciable. Two-dimensional (2D), real-time echocardiography showed a large (10-mm diameter) atrial septal defect (ASD) involving the midportion of the atrial septum associated with a tethered septal leaflet and a redundant and elongated anterior leaflet of the tricuspid valve [Figure 2].

The following findings were seen on 2D and M-mode echocardiography: markedly enlarged right atrium and ventricle (right ventricular diastolic diameter, 40 mm); flattening of the interventricular septum toward the left ventricle; and reduced left ventricular dimension (left ventricular diastolic diameter, 37 mm; reference range, 45 to 50 mm), fractional shortening ([FS] 28%; reference range, 35% to 43%), left atrial diameter ([LA] 22 mm; reference range, 27 to 30 mm), and aortic diameter ([Ao] 19 mm; reference range, 26 to 29 mm).¹⁹

Spectral Doppler revealed a maximal velocity of regurgitant jet across the tricuspid valve of 2.63 meters per second, and color-flow Doppler displayed a wide systolic jet. Furthermore, transatrial septal blood flow having left-to-right direction during diastole and right-to-left direction during systole [Figures 3A, 3B] and trivial pulmonic insufficiency were also appreciable. Right-to-left blood flow through the ASD was confirmed with a saline contrast study [Figure 3C]. Systolic and diastolic blood flow velocities across the semilunar and atrioventricular valves, respectively, were within normal values.

Tricuspid dysplasia and ostium secundum-type ASD associated with pleural effusion and ascites were diagnosed. Thoracentesis performed in the right eighth intercostal space allowed collection of 1.5 liters of modified transudate fluid. Furosemide^a was given at a dose of 3 mg/kg per os [PO] q 12 hours. After 3 days of therapy, amelioration of respiratory signs was appreciable, and a mild amount of pleural fluid was evident on thoracic radiographs. The dog was discharged on furosemide (2 mg/kg PO q 12 hours) and enalapril^b (0.5 mg/kg PO q 12 hours) to improve cardiac sympathetic nerve terminal function.²⁰

The clinical condition of the dog was stable at control 3 months after the first examination, and the previous therapy was maintained. Ten months after first admission, the dog was reevaluated because of dyspnea and syncope. Upon physical examination, poor body condition (36 kg body weight), tachypnea (65 bpm), abdominal distension, and an arrhythmic pulse were evident. Muffled and irregular heart sounds were appreciable on cardiac auscultation.

Electrocardiography demonstrated atrial fibrillation with a ventricular rate of 180 bpm. Thoracic radiographs showed bilateral pleural effusion. No significant changes from first examination were noted on echocardiographic and echo-Doppler examinations, except for further enlargement of the right cardiac chambers (right ventricular diastolic diameter, 48 mm).

Abdominal ultrasonography showed ascites and a distended left caudal vena cava and hepatic veins. Needle thoracentesis was performed and allowed evacuation of 2 liters of milky, opaque fluid. Cytology revealed small lymphocytes, mature plasma cells, and nondegenerated neutrophils. Pleural fluid cholesterol (125 mg/dL) and triglyceride (357 mg/dL) concentrations and cholesterol/triglyceride ratio (0.35) were diagnostic of chylothorax.²¹ A presumptive diagnosis of chylothorax associated with complex congenital cardiac disease was made.

Dosage of furosemide was maintained (2 mg/kg PO q 12 hours), and spironolactone^c (2 mg/kg PO q 12 hours) and digoxin^d (0.25 mg PO q 12 hours) were added to relieve signs of congestion and reduce ventricular response to atrial fibrillation, respectively. Furthermore, rutin^e was added (100 mg/kg PO q 8 hours), and a specific lowfat diet^f was prescribed. Over the following 4 months, the dog was presented with increasing frequency for thoracentesis because of recurrence of pleural effusion and resulting dyspnea. Conservative treatment at the above dosage failed to control chylous leakage; therefore, surgical intervention was chosen.

The dog was fed with 1 mL/kg of corn oil 2 hours preoperatively to delineate the thoracic duct during surgery. A 20-gauge vialon catheter^g was placed in the left cephalic vein, and the dog was sedated with a combination of remifentanil hydrochloride^h (0.1 μg/kg per minute) and propofolⁱ (0.1 mg/kg per minute) at a constant-rate infusion (CRI). After 30 minutes, anesthesia was induced by a combination of lidocaine hydrochloride^j (1 mg/kg), propofol (2 mg/kg), and diazepam^k (0.2 mg/kg). Following orotracheal intubation, anesthesia was maintained by CRI of remifentanil hydrochloride (0.1 to 0.2 μg/kg per minute) and isoflurane^l in 100% oxygen; the lungs were mechanically ventilated using intermittent positive-pressure ventilation. Lactated Ringer’s solution was given intravenously throughout anesthesia at a dose of 10 mL/kg per hour. A two-lumen central venous catheter^m was inserted in the right jugular vein using the Seldinger technique; this was then connected to a fluid-filled line and a calibrated pressure transducer.ⁿ The measured cranial vena cava pressure ranged from 10 to 18 cm H₂O (normal range, 0 to 10 cm H₂O).

After a 10th right intercostal space thoracotomy, the mediastinum dorsal to the aorta (including the right thoracic duct and the azygous vein) was dissected, and the thoracic duct was ligated using a synthetic nonabsorbable suture of 0 silk.^o A right-sided paracostal incision was performed, and an omental pedicle flap was prepared as previously described.²² In brief, the dorsal leaf of the omentum was detached from the pancreas, and an L-shaped incision was made beginning at the caudal gastrosplenic ligament. The diaphragm was opened with a stab incision along its right dorsolateral border to carry the omentum into the thoracic cavity. The flap was then anchored over the dorsal mediastinum by simple-interrupted sutures using 3–0 polyglactin 910.^p Care was taken to advance the flap into the craniodorsal mediastinum. The incision of the diaphragm was closed using 3–0 polydioxanone.^q A 24 French thoracostomy tube^r was introduced in the pleural cavity, and a routine closure of the two surgical sites was performed. Recovery from surgery was uneventful, and the thoracic drain was removed 5 days postoperatively. The dog was discharged 7 days after surgery on furosemide (2 mg/kg PO q 12 hours), spironolactone (2 mg/kg PO q 12 hours), digoxin (0.25 mg PO q 12 hours), and enalapril (0.5 mg/kg PO q 12 hours).

The dog was reexamined 1, 3, 6, 12, and 20 months after surgery. Over this time period, the dog showed marked clinical improvement and gained 14 kg in weight without clinical signs of pleural effusion. Thoracic radiographs taken 20 months postoperatively revealed an extremely enlarged cardiac silhouette (vertebral heart score was 12), mainly involving the right side of the heart, without pleural effusion (Figures 4A, 4B). The dog is still free of clinical signs of pleural effusion (35 months postoperatively at the time of writing).

Discussion

Atrial septal defect is considered rare in dogs (comprising 0.7% to 3.7% of all congenital cardiac anomalies),²³ although it represented the second most common canine congenital heart disease in a recent French study.²⁴ Tricuspid dysplasia is considered more common (comprising 5.1% of all congenital cardiac abnormalities) than ASD.²³ The combined presence of ASD and tricuspid dysplasia has seldom been reported in the dog.^24–26

The hemodynamic consequence of tricuspid dysplasia is regurgitant blood flow into the right atrium during systole, which increases right atrial volume and pressure.²⁶ Right-sided heart failure is the end result when massive regurgitation occurs. Small ostium secundum-type ASD, the most common form of ASD, usually does not result in significant clinical abnormalities and may be hemodynamically silent.^24,25 In the absence of other cardiac abnormalities, a moderate to large ASD results in significant left-to-right blood shunting that causes right-sided cardiac overload.^25,26 When ASD occurs in conjunction with other congenital cardiac diseases that reduce the right ventricular compliance and/or increase the right-sided cardiac pressure (e.g., pulmonic stenosis and tricuspid dysplasia), reversed (right-to-left) interatrial shunting may be observed.^25–27

The dog described herein showed severe right-sided cardiac volume overload as a consequence of tricuspid dysplasia associated with large ASD. Because of the increased systolic pressure in the right atrium secondary to tricuspid regurgitation, bidirectional blood flow was observed at the level of the ASD. Increased blood pressure in the cranial vena cava due to right-sided heart failure was considered the most likely cause of chylothorax through lymphatic dilatation and hypertension.²⁸ Nevertheless, concurrent idiopathic chylothorax and congenital cardiac disease could not be excluded. Leaking of chyle from dilated but otherwise intact cranial mediastinal lymphatics is actually thought to be the most common pathophysiological mechanism of chylothorax in dogs.¹

Thoracic lymphangiectasia and chylothorax have indeed been experimentally induced in dogs by ligating the cranial vena cava.^3,28 Therefore, any impedance of the thoracic duct and/or cranial vena cava flow is a potential cause of chylothorax. Few reports of chylothorax associated with cardiovascular disorders may be found in the dog. They include chylous effusion secondary to dilated cardiomyopathy, heart base tumor, right heart failure, constrictive pericarditis, and, more recently, complex congenital cardiac disorder (i.e., double-chambered right ventricle and tricuspid dysplasia).^2,10,12,18

Management of chylothorax depends upon the inciting cause of chyle leakage. Medical options include thoracentesis or chest tube placement; dietary management (i.e., a lowfat, medium-chain triglycerides, total parenteral nutrition); use of thrombolytic substances; and administration of rutin or a somatostatin analog.¹ Surgical treatments of chylothorax include thoracic duct ligation, en bloc ligation of all structures dorsal to the aorta, thoracoscopic ligation, pericardiectomy, thoracic duct embolization, active or passive pleuroperitoneal shunting, and cisterna chyli ligation or ablation.^29–35

Studies comparing the efficacy of medical versus surgical treatment of chylothorax have not been reported to date in dogs. In the dog described here, medical therapy was unsuccessful, while surgical intervention was effective in resolving life-threatening chylothorax. Thoracic duct ligation has an overall success rate of 53% in dogs with chylothorax. ^2,29 Mediastinal omentalization is a relatively new treatment that can be used alone or after thoracic duct interruption. ³⁶ The omentum is a large mesothelial membrane with a rich vascular and lymphatic supply.^22,37 Omental peculiar white lymphoid nodules, also known as “milky spots,” have fenestrated capillaries that allow absorption of fluids from the abdomen to the omental lymphatics.^37,38 For this reason, pedunculate or free omental flaps can act as a physiological drain also in the thoracic cavity.³⁶

A surgical technique similar to that employed in the dog of this report (i.e., thoracic duct ligation and passive pleuroperitoneal shunting) was likewise effective for the resolution of chylothorax in a Labrador retriever with double-chambered right ventricle and tricuspid dysplasia.¹⁸ Partial pericardiectomy (an additional surgical option recently proposed for the treatment of idiopathic chylothorax) was not considered because of the essential role of pericardial restraint in case of dilated right-sided heart chambers.^33,39

Conclusion

Ligation of the thoracic duct and apposition of an omental pedicle flap were successful in terminating life-threatening pleural chylous effusion in a bullmastiff with severe tricuspid dysplasia and ASD. The dog remained free of clinical and radiographic signs of pleural effusion for 35 months postoperatively. Omentalization of the thorax combined with thoracic duct ligation may be a useful surgical option in dogs with chylothorax associated with right-sided congenital cardiac diseases.