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Disseminated pulmonary and subcutaneous-muscular hemangiosarcoma at the left hemimandible was diagnosed postmortem in a 2-year-old Jersey bull that presented with a 7-day history of facial swelling from suspected traumatic injury. Hemangiosarcoma is uncommon in cattle and has never been reported to affect the bones of the skull.
Angiosarcome mandibulaire primaire chez un taureau. Un diagnostic post mortem d’angiosarcome sous-cutanés et musculaire de la mandibule gauche avec dissémination pulmonaire a été posé chez un taureau Jersey âgé de 2 ans. L’animal avait été présenté pour une tuméfaction faciale de 7 jours soupçonnée d’être d’origine traumatique. L’angiosarcome est rare chez les bovins et il n’avait jamais été rapporté qu’il puisse affecter les os du crâne.
(Traduit par Docteur André Blouin)
A 2-year-old Jersey bull was presented with a 1-week history of left-sided periorbital facial swelling and a 1-day history of bilateral epistaxis. The bull was group housed at a bull stud. No signs of traumatic injury had been observed and the bull was reported to be eating, drinking, and acting normally. The referring veterinarian initiated treatment with procaine penicillin G, 22 000 IU/kg bodyweight (BW), IM q12h, and aseptically aspirated blood from the mass 6 d after it was first reported. After the blood had been aspirated, the bull developed bilateral epistaxis and the mass became larger. The bull was then referred for further evaluation.
On physical examination, the bull was depressed and tachypneic (60 breaths/min; reference range: 20–40 breaths/min) with a 10- to 15-cm diameter firm, warm facial swelling on the left side of head, caudal and ventral to the eye. Also noted was left-sided exophthalmos, chemosis of the 3rd eyelid, and conjunctivitis, with mucoid ocular discharge. All cranial nerves were normal.
Clotting profile revealed normal prothrombin time (PT) of 23.4 s (control 24.5 s) and prolonged activated partial thromboplastin time (APTT) of 42.7 s (control 32.0 s). Total platelet count was 414 × 109/L (normal range: 200–800 × 109/L). Packed cell volume (PCV) was 0.19 L/L (reference range: 0.24–0.46 L/L) and serum total protein (STP) was 70 g/L (reference range: 67–75 g/L).
Ultrasonographs of the mass showed anechoic fluid, with hyperechoic tissue on the margins extending into the fluid. Cytologic examination of the anechoic fluid showed a hemodilute sample with very few cells of tissue origin. One large (approximate diameter 80 μm) connective tissue cell was noted. Endoscopic examination of the nasal passages showed active hemorrhage from the left ethmoid bone and a significant amount of blood in the pharynx and the trachea. Radiographs of the skull showed significant soft tissue swelling in the area of the left mandibular ramus and a suspected chronic left mandibular ramus fracture, with possible involvement of the zygomatic arch and maxillary bone. Osteolytic bone lesions due to infection or neoplasia could not be ruled out, base on examination of the radiographs.
Due to the decreasing ability of the eyelids to function properly and increasing pain from the swelling, the lesion was opened surgically and explored under local anesthesia. Exploration was limited, due to excessive hemorrhage, but did reveal the zygomatic arch was fractured rostrally and that the coronoid process of the mandible was also fractured. There were no bony fragments that could be elevated or removed. Due to the multiple fractures, it was presumed that the lesion was traumatic. The incision site was packed with epinephrine-soaked gauze and sutured. Broad spectrum antibiotic therapy was initiated with potassium penicillin, 22 000 IU/kg BW, IV, q6h, and ceftiofur (Naxcel; Pfizer, New York, New York, USA), 2.2 mg/kg BW, IV, q24h.
The gauze was removed 2 days later with the plan for discharge and healing by 2nd intention. However, when the gauze was removed, excessive bleeding resumed and the wound required a pressure wrap and resuturing. The PCV was reduced to 0.12 L/L. Blood transfusion was not economically feasible in this case, but intravenous fluid support was initiated with 0.9% NaCl at 60 mL/kg BW/day. Over the next 24 h, the facial swelling increased and the bull became anorectic, weak and recumbent. Due to poor prognosis, the owners elected to have the animal euthanized.
Gross pathological findings included extensive lesions of the left side of the head and the pulmonary system. There was a large, locally extensive, area of retrobulbar hemorrhage forming a mass lesion, resulting in moderate exophthalmos of the left eye. Hemorrhage was confluent both medial and lateral to the ramus of the left hemimandible, with significant lesions associated with the left coronoid process. The distal ramus of the mandible was absent and replaced by extensive nodular foci of hemorrhage, primarily on the medial aspect of the proximal remnant. On the remaining portion (base of the coronoid process) of the bone, no articular cartilage was present and trabecular bone was exposed (Figure 1). Other bony abnormalities included full thickness transverse fractures of the left zygomatic processes of the temporal and malar bones, with caudal displacement of the rostral fragment. Medullary bone was exposed and there was a full thickness fracture with a 1.5-cm gap in the temporal processes of the malar bone of the supraorbital process. There was also extensive hemorrhage within the left frontal sinus and the left nasal cavity that was confluent with the hemorrhagic mass bulging into the left retrobulbar space.
Gross pulmonary examination showed well-delineated, discrete, frequently bulging pinpoint to 4-cm red nodules scattered throughout the pleural and parenchymal surfaces of the entire lung field. Approximately 1 liter of serosanguineous fluid was present in the thorax. A localized area of right hemithorax, where the pleural surface was reddened and fibrotic, was noted midway between the costochondral junctions and the articulations with the vertebral bodies.
Histological examination of the tissues confirmed disseminated pulmonary hemangiosarcoma (HSA) and subcutaneous/muscular HSA with extensive localized infiltration, hemorrhage, and necrosis of the soft and osseous tissues at the left hemimandible with multifocal fractures. Multiple sections through the mass or muscle, subcutaneous tissue including a lymph node, and multiple nodules and areas of hemorrhage were evaluated microscopically. Several of the pieces consisted of extensive areas of chronic hemorrhage, occasionally with hematoma formation, while other samples consisted of focal areas of hemorrhage embedded within skeletal muscle. These areas of hemorrhage included irregular cords of markedly pleomorphic neoplastic endothelial cells with variable, but usually abundant, amphophilic cytoplasm; irregular ovoid nuclei with peripheral vesicular to stippled chromatin; and variable (0–3) prominent nucleoli. Mitotic figures were variable and ranged upwards to 4 per high power field (400× magnification). The cells were supported by a stroma consisting of thin bands of amorphous eosinophilic material and, frequently, line blood-filled clefts and spaces. Immunohistochemical staining was performed for factor VIII-related protein (endothelial cell marker). The neoplastic cells stained positive, indicative of endothelial cell origin.
Hemangiosarcoma is a malignant neoplasm of vascular endothelial origin that has been reported in many domesticated species (1). The neoplasm is reported to be locally invasive and to metastasize rapidly and extensively, with exception of primary HSA lesions in canine subcutaneous tissue (2). An inappropriate expression of angiogenic growth factors — vascular endothelial growth factor (VEGF), basic fibroblast growth factor (bFGF), and angiopoietin-1 (Ang-1) — has been implicated in the pathogenesis of HSA (3).
Hemangiosarcoma affects middle-aged horses, involving multiple organs, most commonly in the musculoskeletal and respiratory systems (4,5). It is less common in younger horses. In a recent retrospective study, 11 horses, aged ≤ 3 y, had cutaneous masses, leg swelling, or joint effusion. Three of the 11 animals had had masses present since birth (6).
Relatively few cases of HSA have been reported in cattle, the reports include descriptions of tumor affecting the lungs, pleura, long bones, uterine vasculature, vertebrae, skin, muscles, and extradural spinal cord (7–12). There is also a report of congenital multifocal hemangiosarcoma in a stillborn calf (13).
Treatment modalities of HSA include: surgical removal, chemotherapy, and immunotherapy. None of the modalities are 100% effective and novel therapies are being studied. Surgical removal of neoplastic tissues is the primary method of treatment for canine and feline HSA. Due to the high metastatic potential of the tumor, chemotherapy is often initiated along with surgical treatment in these cases. Immunotherapy has been shown to result in significant increases in median survival time, and further study may show further benefit from a combination of immunotherapy with chemotherapy (3). Surgical resection has been reported in equine HAS, with and without chemotherapy, with short-term success (months). Two other horses from the same retrospective study were reported to have spontaneous regression and long-term (years) survival (6). Successful long-term treatment (13 mo) has been reported in a cow with HSA affecting the external nares that was surgically resected and heat-cauterized (9). In other reports, cattle with HSA either have not been treated and were euthanized or have been diagnosed postmortem (7,11–13).
To the author’s knowledge, this is the 1st report of HSA affecting bones of the skull in a bovine animal. In our experience, most group-housed bulls that present with head swelling have lesions of traumatic origin from either direct contact with pen mates or objects in the environment, such as metal stanchions at the feed bunk. Hemangiosarcoma is an extremely rare cause of the clinical signs observed in this bull, but should have been considered in view of the chronic epistaxis, hemorrhage in the trachea, abnormal cytologic appearance of aspirated fluid, and clotting profile abnormalities.
Dr. Poulsen was clinically involved with the case, reviewed the literature, and wrote the manuscript. Dr. McSloy was clinically involved with the case and contributed to the manuscript. Dr. Perrier was a surgeon on the case and contributed to the manuscript. Dr. Prichard was the senior surgeon on the case and contributed to the manuscript. Dr. Steinberg was the pathologist on the case and contributed to the manuscript. Dr. Semrad was the senior clinician on the case and contributed to the manuscript. CVJ