Investigating the sudden death of a dog.

A 6-year-old, male, Shetland sheepdog was presented by his owner to Prairie Diagnostic Service, Inc., at the Western College of Veterinary Medicine, Saskatoon, Saskatchewan, immediately following the dog’s sudden and unexpected death. According to the owner, the dog was being managed for renal disease, but was otherwise healthy and active. Immediately prior to his death, the dog had been barking at a gas station attendant from the backseat of the owner’s car and then suddenly became quiet and died. Necropsy revealed the dog to have a normal hair coat, appropriate sized muscles, and abundant subcutaneous and visceral fat. The mucus membranes were dark blue to purple. Examine Figure 1 and formulate an appropriate morphologic diagnosis. What are the possible causes for the lesion? Figure 1 The heart, lungs, and associated tissues from a 6-year-old dog that died suddenly and unexpectedly. The pericardial sac was taut and turgid and, when opened, was found to contain approximately 100 mL of partially clotted blood. Our morphologic diagnosis was acute and severe hemo-pericardium (a form of pericardial effusion). The more common causes of hemopericardium in dogs include hemorrhage from an intrapericardial neoplasm, rupture of an atria or cardiac vessel, and so-called idiopathic pericardial hemorrhage (1). Examine Figures 2 and ​and33 and formulate an appropriate morphologic diagnosis. What are specific differential diagnoses? What ancillary diagnostic tests are available to help make a definitive diagnosis? Figure 2 The same heart, with the pericardium removed, as illustrated in Figure 1. Figure 3 A cross section of the heart base mass in a 6-year-old dog that died suddenly and unexpectedly. Attached to the base of the heart, there was a well- demarcated, firm 4 × 3 × 2 cm oval, tan mass with a smooth surface that contained numerous anastomosing blood vessels and a few small blood clots (Figure 2). The mass was embedded within the fat between the pulmonary artery and the aorta. The cut surface of the mass was multilobulated and mottled tan and dark red (Figure 3). Our morphologic diagnosis was a heart base neoplasm. Specific differential diagnoses for heart base neoplasms in dogs include an aortic body chemodectoma, ectopic thyroid gland neoplasia, ectopic parathyroid gland neoplasia (2,3) and, extremely rarely, other neoplasms (such as, hemangiosarcoma, mesothelioma, granular cell tumor, and lymphosarcoma). To pursue a definitive diagnosis, the mass, as well as portions of other tissues and organs, were placed in 10% neutral buffered formalin and processed routinely for histologic examination. Histologic examination of hematoxylin and eosin (HE anisocytosis and anisokaryosis (unequal or greater than normal variation in cell and nuclear size, respectively) including megalocytosis and megalokaryosis (abnormally large or so-called giant cells with giant nuclei); increased numbers of cells in mitosis including abnormal mitotic figures (Figure 5); and invasion of these cells through the capsule and into blood vessels and other adjacent tissues (4). Based on the appearance of the H&E stained sections, the heart base mass was believed to be a neoplasm of neuroendocrine tissue, that is, a tissue that interacts with, or has features of, both the nervous system and endocrine system. Figure 4 The histologic appearance of the heart base mass illustrated in Figure 3. Neoplastic cells were arranged in packets or nests that were supported by a fine fibrovascular stroma. Hematoxylin and eosin. Bar = 100 μm. Inset: The mass contained many ... Figure 5 The histologic appearance of the heart base mass illustrated in Figure 3. In many areas of the mass, the neoplastic cells displayed marked pleomorphism, anisocytosis, and anisokaryosis, including megalocytosis and megalokaryosis. Hematoxylin and eosin. ... To confirm this diagnosis, histologic sections of the heart base mass were also stained using the Churukian-Schenk method for the detection of amines and peptides within neurosecretory granules (3,5). Numerous neoplastic cells within the mass were found to contain argyrophilic granules (ones easily stained or impregnated with silver). Based on the location of the mass, its histologic appearance, and the presence of argyrophilic granules in the cells, the heart base neoplasm was interpreted to be an aortic body tumor or aortic body chemodectoma. Because the neoplastic cells had invaded into adjacent blood vessels and tissues, the mass was also interpreted to be malignant. Histologic evaluation of the kidneys also confirmed the presence of severe glomerulosclerosis and interstitial nephritis. As a final ancillary test, immunohistochemical evaluation of the neoplasm was performed using the avidin–biotin–peroxidase method (6) with antibodies to vimentin (a structural polypep-tide of mesenchymal cells) and cytokeratin AE1/AE3 (multiple structural proteins of epithelial cells). None of the tumor cells expressed antigens of either vimentin or multiple cytokeratins. These findings were compatible with a diagnosis of an aortic body chemodectoma (7,8) and, just as importantly, allowed for the rule out of the differential diagnoses listed above. Additional immunohistochemical testing, for example using antibodies to neuron-specific enolase (an enzyme found almost exclusively in neurons and neuroendocrine cells) or chromogranin (acidic proteins present in the secretory granules of a wide variety of endocrine and neuroendocrine cells) (2,3,9,10), could have been employed to further support the diagnosis, but were not thought to be necessary, not readily available, or both. The aortic bodies are paraganglion: a relatively small collection of neuroendocrine cells that originate from neurocrest ectoderm. The 2 types of paraganglia, sympathetic and parasympathetic, contain both catecholamine- and peptide-producing cells. Aortic bodies are located, as their name would suggest, in the aortic arch at the bifurcation of the subclavian artery. The carotid bodies are closely related chemoreceptor organs, in terms of origin and function, that are located at the bifurcation of the common carotid artery. Together, these chemoreceptor organs monitor the partial pressures of oxygen and carbon dioxide (PO2 and PCO2, respectively) and hydrogen ion concentration, or acidity (pH), of arterial blood and have input to the midbrain for the regulation of respiration and circulation (2,3,7,11). Neoplasms of paraganglia are generically referred to as para-gangliomas. However, 2 terms, pheochoromocytoma and chemodectoma, have come to be associated with neoplasms of specific paraganglia, the adrenal medullae and the aortic and carotid bodies, respectively (2,3). Chemodectomas have been reported in a variety of domestic animals, but the neoplasm appears to develop most commonly in dogs (2,7,12,13). Of relevance in this case, were the findings of a retrospective postmortem study conducted at the Faculty of Veterinary Medicine, University of Montreal, in which chemodectomas were found to be the second most frequently diagnosed primary intrapericardial neoplasm in dogs (13). The etiology of chemodectomas is uncertain. However, in 1975, a veterinarian and epidemiologist with the National Cancer Institute in Maryland published the findings of a retrospective study in which dogs of bulldog ancestry (boxers, Boston terriers, and English bulldogs), were found to be at higher risk of developing chemodectomas. While the author suggested that this higher risk represented a familial (genetic) predisposition, he also hypothesized that the predisposition might be aggravated by chronic hypoxia in brachycepahalic breeds of dogs (14). This hypothesis was based on work that described carotid body hyperplasia in several animal species, including dogs, and humans that were subject to the chronic hypoxia associated with living at high altitude as well as an increased incidence of chemodectomas in humans living at high altitude compared with those living at sea level (2,15).

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