Ectopic Thyroid Carcinoma Causing Right Ventricular Outflow Tract Obstruction in a Dog

Introduction

Most primary cardiac tumors in dogs are reported to be malignant. Hemangiosarcoma of the right atrium is the most common primary cardiac tumor in dogs.^1,2 Primary cardiac tumors in humans are rare; most are benign, and they are commonly located in the left side of the heart.³ Obstruction of the right ventricular outflow tract (RVOT) by a tumor originating in the heart is unusual. Only a few reports of neoplasia causing intracardiac obstruction have been published; they have involved myxoma, rhabdosarcoma, and ectopic thyroid carcinoma.^4–7 This paper reports the successful resection of an ectopic thyroid carcinoma from an unusual location within the heart.

Case Report

A 9-year-old, 40-kg, spayed female Bouvier des Flandres was presented to the Ontario Veterinary College Teaching Hospital with a 1-month history of coughing and lethargy. Diagnostic tests performed by the referring veterinarian included thoracic radiographs and an echocardiogram that revealed pleural effusion and an intracardiac mass.

On presentation, the dog was quiet, alert, and responsive; but breathing was labored. Muffled lung sounds were heard bilaterally during auscultation of the ventral part of the thorax. A grade III/VI left systolic murmur and a grade II/VI right systolic murmur were present. A complete blood count (CBC) and coagulation profile were unremarkable. A serum biochemical profile showed a mild increase in alanine transaminase (ALT; 242 U/L; reference range 19 to 107 U/L) and lipase (1387 U/L; reference range 60 to 848 U/L). Thoracic radiographs showed mild pleural effusion. Thoracocentesis yielded 460 mL of turbid, white fluid of low cellularity that was suggestive of a chylous effusion; however, a triglyceride evaluation was not initially performed to confirm this assumption. An abdominal ultrasound showed no abnormal findings. Two- and three-dimensional echocardiography revealed a 3.5 × 2.5 × 2-cm, mobile, oval mass connected by a stalk to the medial wall of the RVOT approximately 1.5 cm below the pulmonic valve. This resulted in obstruction of the RVOT during the systolic phase of each cardiac cycle, generating a pressure gradient of 100 mm Hg between the right ventricle and the main pulmonary artery. Moderate right ventricular enlargement (eccentric and concentric), severe right atrium enlargement, and poor perfusion of the left side were present. An electrocardiogram did not demonstrate arrhythmias.

Surgical resection of the mass was recommended. The thoracic approach was via resection of the right fourth rib. Rummel tourniquets were preplaced on both vena cavae and the azygos vein. A subphrenic pericardectomy was performed, releasing a large amount of chylous fluid from the pericardial sac. A 4-cm, fusiform, collagen-impregnated Dacron patch graft was sutured along the pulmonary outflow tract. Enough redundant graft was placed to allow easy partial occlusion with a tangential vascular clamp. The graft was then cut open longitudinally. Following total venous occlusion, the aorta was cross-clamped, and 60 mL of a 5°C cardioplegic solution was administered by injection into the aortic root. Cardiac standstill was followed by an incision into the RVOT pulmonary artery along the graft length. The mass was identified within the outflow tract, and the connecting stalk was transected flush with the wall of the RVOT [Figure 1].

Following removal of the mass, the heart was de-aired by removing the tourniquets. A tangential clamp was placed to isolate the graft incision. Warm blood (30 mL) was infused into the aortic root, and the aortic cross clamp was removed. The aortic root puncture was sealed with a preplaced cruciate stitch. Cardiac massage was performed, and the heart was defibrillated with 50 joules delivered directly to the epicardium. A thoracostomy tube was placed from the eighth intercostal space, and the thoracic wall was closed routinely.

The following day, the dog experienced some intrathoracic bleeding of unknown origin. A blood transfusion was administered, and the bleeding resolved without any further intervention. The dog recovered well from surgery and was discharged 5 days later, after the pleural effusion had decreased to 5 mL/kg per 24 hours and the thoracostomy tube had been removed.

The resected tissue was fixed in 10% formalin and stained with hematoxylin and eosin [Figure 2A]. The tissue was described as an oblong, fluctuant mass surrounded by a thick, vascularized capsule.

The parenchyma of the mass was composed of round to polyhedral cells embedded within a loose stroma. Sporadic follicular structures with eosinophilic proteinaceous secretion were observed; elsewhere, neoplastic cells formed elongated cords infiltrating the stroma. The stalk of the tumor seemed free of neoplastic cells within 50 μ of the resected site; however, histopathological examination of a section from the stalk area showed a blood vessel with intraluminal neoplastic cells, descending parallel to the stalk. Immunohistochemical analysis was performed for further classification of this neoplasm. Staining for chromogranin and synaptophysin was negative, which ruled out a possible neuroendocrine tumor. However, the tumor cells stained positive for thyroglobulin, which was consistent with a tumor of thyroid origin [Figure 2B]. A diagnosis of ectopic thyroid carcinoma was made.

Because of the neoplastic cells seen within the blood vessels vascularizing the mass, chemotherapy with carboplatin was recommended; but the owner declined treatment. Ultrasound of the neck to evaluate the thyroid gland, and a radioactive tracer scan to search for evidence of thyroid cancer in other ectopic sites were also recommended but declined at that time.

Six weeks following surgery, the dog was presented again with a 1-week history of coughing. On presentation, the dog was bright, alert, and responsive. Auscultation of the thorax revealed muffled lung sounds and a heart murmur. A CBC was unremarkable, and a serum biochemical profile showed mild increases of ALT and lipase. A total levorotatory thyroxine (T₄) was decreased (<13 nmol/L; reference range 13 to 50 nmol/L), but the thyroid-stimulating hormone level was normal. A free T₄ by equilibrium dialysis was at the lower end of normal (7.7 pmol/L; reference range 8 to 40 pmol/L). Thoracic radiographs confirmed the presence of marked pleural effusion. Thoracocentesis yielded 1 L of milky, viscous fluid. Cytology of the thoracic effusion showed a predominant population of nondegenerative neutrophils, consistent with chronic chylous effusion. Triglyceride concentrations were measured from the dog’s serum (0.46 mmol/L; reference range 0.2 to 1.3 mmol/L) and pleural effusion (17.44 mmol/L); both were compatible with chylothorax. Culture of the effusion was negative for bacterial growth. Ultrasound of the neck and cervical region showed no abnormalities. An echocardiogram showed no evidence of tumor regrowth and no RVOT obstruction. Mild enlargement of the right atrium was observed. Central venous pressure (CVP) was measured directly through a jugular catheter and was mildly elevated at 6 to 8 mm Hg. Two weeks later, the dog had recurrence of the cough, and 650 mL of chylous effusion was removed. The dog had frequent (a total of 13) thoracocenteses because of the reoccurrence of chylothorax. Eleven months after the diagnosis, the dog was euthanized at the request of the owner because of the nonresolving chylothorax.

Discussion

Thyroid carcinomas in dogs represent 1% of all cardiac tumors, and they are usually diagnosed postmortem. Most ectopic thyroid tumors are located at the base of the heart. Ectopic thyroid carcinoma obstructing the RVOT has been reported only twice previously in canine literature. To the authors’ knowledge, this is only the second case report of a successful removal of an ectopic thyroid carcinoma from this unique location in a dog.

Chylothorax has not been described in association with ectopic thyroid carcinoma located in the RVOT. The minimal postsurgical structural changes present on echocardiogram did not support right-sided heart failure or account for the clinical presentation of the dog. The preoperative increase in CVP from right-sided heart failure may have resulted in damage and leakage from the thoracic lymphatics. In this present case, although the obstruction was relieved and a partial pericardectomy was performed, chylous effusion was still evident following surgery. The accumulation of chylous effusion in the face of a near-normal CVP suggests persistent damage to the thoracic lymphatics. The dog was euthanized 11 months after diagnosis because of the nonresolving chylothorax. Metastatic disease was not evident on thoracic radiographs to the time of euthanasia; however, no other imaging was performed during this period.

Conclusion

Ectopic thyroid carcinoma located in the RVOT is extremely rare in dogs. A mass within this location has been removed without using extra-corporal circulation, and, based on the only other case reported in the literature, prolonged survival can potentially be obtained.