Primary peri-aortic hemangiosarcoma in a dog

Abstract

A 10-year-old intact male Norwich terrier dog was evaluated for progressive, intermittent increased respiratory effort. Thoracic radiographs, ultrasonography, and computed tomography were used to identify a caudodorsal thoracic extrapulmonary mass and the presence of pulmonary metastasis. Blood transfusion and stabilization measures were not successful and the patient died. Necropsy confirmed the origin of the mass to be the adventitial layer of the aorta and determined it to be hemangiosarcoma. This is a rare site for the primary lesion.

A 10-year-old intact male Norwich terrier dog was presented for progressive respiratory difficulty. Past medical history included cystic calculi. The results of laboratory analysis [abbreviated serum biochemistry profile, complete blood (cell) count (CBC), and urinalysis] performed approximately 1 mo prior to presentation were unremarkable except for mild hyperglycemia. The referring veterinarian also performed serologic testing for Borrelia burgdorferi, Anaplasma phagoctyophilum, Ehrlichia canis, and Dirofilaria immitis (SNAP 4Dx ELISA, Idexx Laboratories, Westbrook, Maine, USA) that revealed seropositivity for Borrelia burgdorferi. Empirical treatments with doxycycline and meloxicam were initiated with no change in condition. On physical examination, the patient was bright and alert with mild respiratory distress. Stertorous upper airway noise hindered thoracic auscultation but there was no murmur. No other abnormailities were detected on physical examination.

Case description

On presentation, the patient’s mucous membranes were pink, but pulse oximetry revealed a mild hypoxemia of 91% that increased to 96% when flow-by oxygen was provided. Thoracic radiographs revealed moderate pleural effusion (Figure 1). Approximately 6 mL of fluid obtained from an ultrasound-guided thoracocentesis was hemorrhagic and non-clotting, with a packed cell volume (PCV) of 48%, comparable to that of the peripheral circulation. Coagulation times (prothrombin time and activated partial thromboplastin time) were normal. With no history of trauma to explain the diagnosed hemothorax, the patient was admitted to the hospital for additional diagnostic testing.

Figure 1.

Right lateral radiograph of a 10-year-old male Norwich terrier dog with progressive respiratory difficulty. The scalloped lung lobes are consistent with pleural effusion. Definitive evidence of a thoracic mass is not present.

Echocardiography was performed to assess for possible cardiac causes of the effusion. No cardiac structural or functional abnormalities were detected, but pleural effusion and a caudal thoracic mass of uncertain origin were noted. The patient remained stable in hospital. The respiratory pattern was normal and supplemental oxygen was discontinued without a deterioration of signs. Two days after presentation, thoracic radiographs were repeated and the effusion was noted to be decreased in volume despite no additional removal of fluid. With less pleural fluid present, a well-marginated soft tissue mass was visible in the left caudodorsal thorax (Figure 2). This mass had a convex dorsal border and silhouetted with the diaphragm caudally on the lateral view. Abdominal ultrasonography was performed; a diffuse nonspecific hepatopathy, bilateral non-specific renal changes suggestive of chronic disease, and cystic sediment were identified. Focused thoracic ultrasound examination via a left dorsal subcostal approach was performed to further evaluate the thoracic mass identified on radiographs. The mass was hypoechoic, irregularly shaped, complex in architecture, and measured 4.2 × 3.4 × 2.6 cm. The exact origin of the mass could not be determined but the mass was adjacent to the descending aorta and moved independently of the adjacent pleural surfaces, suggesting an extrapulmonary origin.

Figure 2.

Right lateral and VD radiographs of the dog in Figure 1 taken 2 days later. A left caudodorsal thoracic mass is now visible. The cranial and left margins of the mass are rounded, displacing the lung lobe ventrally, cranially, and laterally (arrowheads). Differential diagnosis for this mass includes neoplasia, abscess or granuloma of the caudal mediastinum, including the esophagus. Other potential origins of the mass include pleura, hypaxial muscles, or less likely the lung.

Computed tomography (CT) was performed to further define the extent of the mass (Figure 3). A large, contrast-enhancing, complex mass in the left caudodorsal thorax caused ventral displacement and compression of the descending aorta and esophagus. The mass also displaced the axial margin of the left caudal lung lobe laterally. The mass abutted the left ventral vertebral bodies of T10-12, where subtle, irregular bony lysis was noted. Multiple small, 0.2 to 0.6 cm nodules were scattered throughout various lung lobes, consistent with metastatic disease. These nodules were not visible on survey radiographs. Only a small volume of bilateral pleural effusion was present on CT, consistent with the decreased volume noted on serial radiographs. The CT diagnosis was a locally extensive extra-pleural, caudal mediastinal soft tissue neoplasm with polyostotic vertebral extension and pulmonary metastatic disease.

Figure 3.

Transverse images of the caudal thorax at the level of T10 in a soft tissue (A) and bone (B) window. The images were obtained immediately after bolus IV contrast administration of iohexol. A heterogeneously contrast-enhancing soft tissue mass (*) displaces and compresses the aorta and esophagus ventrally and to the right. The mass displaces the axial margin of the left caudal lung lobe laterally. The axial margin of the left caudal lung lobe is also partially atelectatic, as evidenced by the hyperdense area of lung adjacent to the mass. In a bone window, the dorsal extent of the mass extends into a focus of bony lysis of the left ventral margin of the body of T10 (arrow). There is a small pulmonary nodule in the dorsalmost aspect of the left caudal lung lobe (arrowhead).

The patient became acutely hypotensive after the scan. Ultrasonography revealed that a large volume of pleural fluid had accumulated; thoracocentesis was repeated and the same hemorrhagic effusion was encountered, but in a much larger volume. Approximately 180 mL of fluid was removed. Other stabilization measures were attempted concurrently, including bolus infusion of canine packed red blood cells, also with no improvement. Acute hemorrhage from the mass was suspected. Given the grave prognosis and evidence to support metastatic disease, the patient was humanely euthanized.

At necropsy, the bulk of the thoracic mass surrounded the caudal segment of the descending aorta (Figure 4). Invasion into the surrounding intercostal musculature and into the 10th thoracic vertebral body (T10) was also noted. Pulmonary metastases were confirmed. Histologically, this mass and its metastases were consistent with hemangiosarcoma (HSA) (Figures 5A, B). Osteolysis of the body of T10 was noted with neoplastic infiltration (Figure 5C). No distinct aortic dissection was noted, implying that hemothorax developed due to hemorrhage directly from the mass. Hemangiosarcoma was confirmed histologically in the pulmonary nodules as well, but not in other areas more typically affected such as the right auricular appendage or the spleen, both of which were histologically devoid of neoplastic tissue.

Figure 4.

A large mass surrounds the distal segment of thoracic aorta.

Figure 5.

A — Section of an aortic branch diffusely surrounded by a densely cellular and hemorrhagic mass with extensive necrosis. Hematoxylin and eosin (H&E), 40 × Aperio scanned image. B — High magnification with details of the neoplastic morphology: fibrous septe lined by plump spindloid cells delimiting vascular spaces. C — Full thickness section of the affected vertebral body. The spinal cord is at the bottom of the figure. Above and to the left there is an extensive area of vertebral body osteolysis with neoplastic infiltration. H&E, 40× Aperio scanned image.

Discussion

Hemangiosarcoma is a malignancy of vascular endothelial origin. It accounts for approximately 2% of all tumors in dogs, with the most common primary site being the spleen. Other primary sites of disease include the right atrium/auricular appendage, pericardium, liver, muscle, lung, skin and subcutis, bone, kidney, central nervous system, peritoneum, and oral cavity. Early and aggressive metastasis is common. The mean age range of occurrence in dogs is 8 to 13 y, and German shepherd dogs show a specific breed predisposition (1–5). Hemangiosarcoma comprises 2% to 3% of canine bone tumors, including 4% to 10.5% of all vertebral bone tumors (6). Of note is that this patient exhibited an aortic lesion that extended directly into T10 with adjacent vertebrae also affected, although the aorta was considered to be the primary lesion. While speculative, the non-specific and poorly localizable pain the patient experienced may have been attributable to the lytic vertebral lesions.

A retrospective study by Brown et al (3) describes 1 dog previously noted to have a primary aortic HSA discovered at the time of necropsy, but the layer of the aorta affected by this lesion was not described. The aorta is divided histologically into 3 distinct layers: the intima including the endothelium, the media comprised primarily of smooth muscle, and the adventia comprised of fibroblasts and connective tissue. Another case report by Ranck et al describes a German shepherd dog with a mass lesion at the level of the arch of the aorta affecting the intimal layer (7). The mass showed extension into the media while causing direct intravascular metastasis and associated thromboembolic complications. This tumor most closely resembled aortic intimal angiosarcoma described in humans, and immunohistochemical staining confirmed its endothelial origin by its common expression of vimentin and CD31 by neoplastic cells. In humans, mural sarcomas of the aorta involving the media or adventitia are more common and do not show the true endothelial nature of angiosarcoma with CD31 expression. In the patient described here, immunohistochemical staining of the lesion confirmed the histogenesis of the neoplasm. Tissue samples revealed several areas that showed moderate membrano-cytoplasmic expression of factor VIII in neoplastic cells, confirming their endothelial nature (Figure 6). The lack of diffuse and intense expression of Factor VIII in neoplastic cells was hypothesized to be either secondary to poor cellular differentiation, or artifactually poor antigenic expression due to prolonged formalin fixation of the specimen.

Figure 6.

A — Neoplastic cells display granular brown cytoplasmic staining as positive expression of Factor VIII. B — Nodule of lung mestastasis shows Factor VIII cytoplasmic expression in neoplastic spindloid cells (M) and alveolar endothelium of the adjacent pulmonary parenchyma (L). H&E, 40× Aperio scanned images.

The vascular neoplasm in this case was described to be intimately associated with the adventitial layer of the descending aorta, most likely arising from the vasa vasorum of the aortic adventitia or adventitia of an adjacent aortic branch. The acute hemorrhage following CT is presumed to have originated from the mass itself as aortic dissection was not noted on macroscopic or histological examination.

Tumors arising from the aorta are very rare in the dog, especially if those arising specifically from the aortic body chemoreceptors are excluded. Most reports in veterinary medicine describe individual cases including HSA (3), melanoma (8), chondrosarcoma (9), and malignant angioendotheliomatosis (an angiotropic form of intravascular lymphoma) (10). Non-neoplastic causes of a mass effect in the area in question can include infection with Spirocerca lupi causing transmural esophageal mass lesions, and aortic aneurysm/dissection.

This report also highlights the improved visualization of thoracic structures both following removal of pleural fluid and with the use CT as previously reported (11,12).

This case report describes the radiographic, ultrasonographic, gross, histological, and immunohistochemical findings and properties of hemangiosarcoma arising from the adventitial layer of the thoracic portion of the descending aorta in a dog. This is a rare primary site for this common neoplasm of dogs. Hemangiosarcoma should be considered as a differential diagnosis for extrapulmonary masses of the caudodorsal thorax in dogs. CVJ