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CASE I – 654 (AFIP 2739123)
Signalment: Adult male Dall's porpoise (Phocoenoides dalli)
History: The porpoise was found dead and washed ashore at Gabriola Pass, British Columbia, Canada.
Gross Pathology: The animal presented in good flesh. There was approximately 0.5 L of dark red fluid within the thoracic cavity and the mediastinal lymph nodes were enlarged, mucoid and pale. The right lung was moderately enlarged, firm, and homogeneously dark red-black with numerous firm nodules on cut surface. A small number of adhesions were apparent between the visceral pleura and pericardium. There was a large volume (1.0-1.5 L) of serosanguinous ascites. The glandular compartment of the stomach featured multiple erosions and occasional hemorrhagic ulcers. The distal small intestine contained a moderate amount of melena. No ingesta or feces were noted within the gastrointestinal tract.
Laboratory Results: Pooled samples of lung and liver were negative by polymerase chain reaction for dolphin morbillivirus. Trace mineral analysis of the liver and kidney was normal.
Contributor’s Diagnoses and Comment: 1. Lung: Pneumonia, moderate, multifocal, granulomatous, with florid intralesional fungal elements compatible with Cryptococcus neoformans.
2. Lung, bronchiole: Bronchiolitis, moderate, diffuse, erosive, subacute with intralesional nematode parasites.
Immediately below and elevating the visceral pleura, as well as extending deep into and affecting up to 80% of the sectioned parenchyma, there are multifocal to coalescing, well-delineated aggregates of extracellular, 5-15 m m diameter spherical, elliptical, and oval yeast forms with a prominent, 2-4 m m wide, clear to slightly amphophilic capsule. These organisms have finely stippled to homogenous basophilic cytoplasm and occasional narrow-based budding. Multifocally, there are septal and alveolar accumulations of degenerate and viable macrophages and lymphocytes with fewer collagen fibers and neutrophils. Similar yeast lakes were apparent within the mediastinal lymph node.
Eccentrically, within the distal limit of sectioned lung lobe and involving an intermediate-size airway, there is marked dilation of the lumen. Adjacent to the eroded, ulcerated, attenuated and occasionally hyperplastic respiratory epithelia, there are numerous cross and tangential sections of nematode parasites. Extending across the airway wall, and infiltrating a short distance into the adjacent interstitium, there are moderate accumulations of lymphocytes, fewer plasma cells, eosinophils, multinucleate giant cells and neutrophils with variable amounts of dispersed, karyorrhectic debris. A small number of parasitic larvae are localized within terminal bronchioles and the adjoining compressed alveolar spaces. Multifocally, involving the airway and terminal bronchioles, there is mild to moderate smooth muscle hypertrophy.
Dall's porpoises (Phocoenoides dalli) have been reported throughout the eastern rim of the Pacific ocean, from as far north as the Pribilof Islands, Alaska, and south to San Francisco, California. They are considered among the most abundant and frequently encountered cetaceans off the British Columbia coast. As part of an ongoing collaboration with the Canadian Department of Fisheries and Oceans to monitor the cause of death of these animals, a postmortem examination was performed on a recently stranded porpoise and representative tissues were submitted to the Animal Health Center.
Based on the morphology of the yeast, a diagnosis of pulmonary cryptococcosis was made. These organisms are cosmopolitan, ubiquitous within nature, and particularly abundant in areas contaminated by pigeon excreta. This yeast is considered non-contagious, with infection generally acquired through inhalation or ingestion. Although infection with this pathogen has been reported in a captive 7-year-old Atlantic bottlenose dolphin (Tursiops truncatus) and an adult female Pacific white-sided dolphin (Lagenorhynchus obliquidens), this case is believed to be the first in a wild cetacean, and is a sentinel case in a Dall's porpoise. Within six months of receiving this case, an adult female harbour porpoise (Phocoena phocoena) was presented from Tofino, British Columbia with a similar diagnosis of pulmonary cryptococcosis and lymphatic dissemination. This animal was also negative for morbillivirus by polymerase chain reaction.
Although this pathogen is capable of infecting immunocompetent animals, cryptococcosis is more commonly recognized in immunocompromised or severely debilitated hosts. Close evaluation of submitted tissues from both animals failed to reveal any underlying or predisposing conditions. The pulmonary nematodes noted within most of the sections are likely Halocercus spp. and are considered an incidental finding in this animal.
AFIP Diagnoses: 1. Lung: Pneumonia, granulomatous, multifocal, moderate, with numerous encapsulated yeast, etiology consistent with Cryptococcus sp., Dall’s porpoise (Phocoenoides dalli), cetacean.
2. Lung: Bronchiolitis, granulomatous and eosinophilic, focal, moderate, with bronchiectasis and many intraluminal metastrongyles.
Conference Comment: Cryptococcal infections are acquired most commonly via inhalation, resulting in a primary pulmonary focus that may later disseminate hematogenously. For unexplained reasons, C. neoformans is extremely neurotropic and often disseminates to a cerebromeningeal location where it forms expansile, intracranial mucoid cysts that may mimic a neoplasm in its clinical presentation.
T-lymphocyte activated macrophages are thought to be necessary for clearing and preventing progressive infection, but often the host inflammatory reaction is minimal. The thick, mucopolysaccharide capsule is thought to interfere with antigen presentation and allow the yeast to escape cell-mediated destruction.
Cryptococcus is the only pathogenic fungus that has a mucinous capsule. The cell walls of Blastomyces dermatitidis and Rhinosporidium seeberi may also stain positively for mucin, but these unencapsulated organisms can be distinguished histomorphologically.
Cetacean lung morphology differs from that of land mammals. Cartilage rings, present down to the small terminal airways, are thought to aid in the re-inflation of collapsed lung parenchyma following deep dives. Capillaries are present on both sides of alveolar septa and probably aid in more efficient blood-gas exchange. Mineralization is frequently seen in the subepithelial connective tissue of small airways in dolphins; its cause is unknown. Pulmonary metastrongyles, as pointed out by the contributor, also are frequently seen and are usually clinically insignificant. Unfortunately, because of tissue section variability, the intrabronchiolar nematodes were not present on all slides.
Contributor: British Columbia Ministry of Agriculture, Abbotsford Agricultural Centre, 1767 Angus Campbell Road, Abbotsford, BC, Canada V3G 2M3
References: 1. Chandler FW, Watts JC: Cryptococcosis. In: Pathologic Diagnosis of Fungal Infections, pp. 161-174. American Society of Clinical Pathologists Press, Chicago, IL, 1987
2. Migaki G, Gunnels RD, Casey HW: Pulmonary cryptococcosis in an Atlantic bottlenose dolphin (Tursiops truncatus). Lab An Sci 28(5):603-607, 1978
3. Murnane RD, Kinsel MJ, Briggs MB: Subacute and fulminating pulmonary cryptococcosis with dissemination in an Atlantic bottlenose dolphin. Int Assoc Aq Anim Med Proc 29:43-44, 1998
CASE II – 98:8006 (AFIP 2674855)
Signalment: Five juvenile male and female ring-necked pheasants (Phasianus colchicus)
History: The flock consists of 810 birds that are raised on the ground. The flock was treated with neomycin for two days prior to the submission of five birds for necropsy. Fifty birds had died in the previous six days. Clinical signs consisted of weakness, lethargy, and death within twenty-four hours.
Gross Pathology: The birds were thin and had mildly to moderately thickened and opaque crops. The ceca were enlarged and contained cores. The spleens were enlarged also. One bird had a roundworm attached to the mucosa of the distal trachea.
Laboratory Results: No significant clinical pathology or microbiology.
Contributor’s Diagnosis and Comment: 1. Lung: Diffuse marked histiocytosis with numerous intrahistiocytic, Gram positive bacilli.
2. Spleen: Diffuse marked reticuloendothelial proliferation with lymphoid depletion and numerous intrahistiocytic, Gram positive bacilli.
Microscopically there are numerous mononuclear cells containing many intracytoplasmic, blue, rod-shaped organisms within the vasculature of most body organs. These organisms stain Gram positive with a Brown and Brenn stain. Transmission electron microscopy performed at the AFIP revealed histiocytes packed with clusters of pleomorphic bacilli that have thick, electron dense cell walls consistent with Gram positive bacteria. The histological findings are most consistent with peracute erysipelas septicemia.
A Gram positive bacillus, Erysipelothrix rhusiopathiae causes erysipelas, a worldwide disease that affects many mammalian and avian species. The bacillus can survive in soil for long periods of time. The route of entry is generally considered to occur through breaks in the skin or mucous membranes.
Turkeys are the most commonly affected of birds in which erysipelas causes acute septicemia with high mortality. Pheasants are less commonly affected and, although the disease can produce an acute septicemia, many infections are subclinical. The pheasants in this case may have been predisposed to the more severe septicemic form due to debilitation from concurrent multiple parasitic infections (Capillaria spp. infection of the crop, Heterakis spp. infection of the cecum, and Syngamus trachea infection of the trachea). Additionally, the pheasants had multifocal ulcerative typhlitis caused by Clostridium colinum, which may have provided the entry portal for the erysipelas bacterium.
Erysipelas is a zoonotic disease, called erysipeloid in humans. It generally takes the form of localized skin lesions, but occasionally progresses to septicemia and fatal infection.
AFIP Diagnoses: 1. Spleen: Splenitis, histiocytic, diffuse, moderate, with numerous intrahistiocytic bacilli, and lymphoid depletion, ring-necked pheasant (Phasianus colchicus), avian.
2. Lung: Pneumonia, interstitial, histiocytic, diffuse, moderate, with numerous intrahistiocytic and intramonocytic bacilli.
Conference Comment: The mechanism by which the many different strains of E. rhusiopathiae cause disease is not completely clear. Although the enzyme neuraminidase appears to be associated with virulence, is has not been shown to have toxic activity and must be present in large quantities, as might be present in septicemic conditions, to be active in pathogenesis. The ability to produce various virulence factors, such as specific capsular attachment factors or adhesins, and stress proteins also may be important.
Erysipelas is also a sporadic disease of swine and small cetaceans. The deaths of a 14-year-old beluga whale mother (Delphinapterus leucas), in December 1999, and a young male Pacific white-sided dolphin (Lagenorhynchus obliquidens) almost 5 years previously, at the Shedd Aquarium in Chicago, Illinois, were confirmed to have been caused by acute Erysipelothrix rhusiopathiae septicemia. The source of the infections was believed to be surface slime on the fish fed to them. Although periodic bacterial culture sampling of the frozen fish it stocks was instituted following the first death at the Shedd Aquarium, E. rhusiopathiae has not been isolated. Neither the whale nor the dolphin was believed to have been immunosuppressed. Other cetaceans and pinnipeds managed in the same water system, to include a nursing calf of the beluga mother, were not affected.
Contributor: University of Connecticut, Department of Pathobiology, 61 North Eagleville Rd, U-89, Storrs, CT 06269
References: 1. Bricker JM, Saif YM: Erysipelas. In: Diseases of Poultry, ed. Calnek BW, 10th ed., pp. 302-313. Iowa State University Press, Ames, Iowa, 1997
2. Milne EM, Windsor RS, Rogerson F, Pennycott TW: Concurrent infection with enteric protozoa and Erysipelothrix rhusiopathiae in chicken and pheasant flocks. Veterinary Record 141: 340-341, 1997
3. Kinsel MJ, Boehm JR, Harris B, Murnane RD: Fatal Erysipelothrix rhusiopathiae septicemia in a captive Pacific white-sided dolphin (Lagenorhyncus obliquidens). J Zoo Wildlife Med 28:494-497, 1997
CASE III – S3129/99 (AFIP 2741725)
Signalment: 25-year-old, male Pacific walrus, Odobenus rosmarus divergens Illiger.
History: This walrus had been kept in the Hannover Zoological Garden since it was 6 months old. It was fed a standard fish diet (approximately 20 to 40 kg of fresh high quality fish per day, with 80% mackerel) supplemented with vitamins, minerals and trace elements. The animal had a history of recurrent corneal opacities throughout the last couple of years. Three months before the animal died, ocular lesions were treated with a virustatic and gentamycin for 2 weeks. The lesions healed well, but the animal refused to eat approximately one week after treatment and lost significant weight over a six-week period (body weight dropped from 1.4 tons to 1.13 tons). The animal showed recurrent colic-like abdominal pain. Butylscopolamine and metamizole were administered to reduce the pain. Twelve hours later, multiple cutaneous vesicles and shallow ulcerations were observed. Despite intensive treatment, the walrus became less and less active and its general condition deteriorated until it died.
Gross Pathology: Multiple cutaneous ulcerations and three small corneal ulcers of the right eye were found. There was a severe pulpitis and radiculitis of the upper right canine tooth. The reduced amount of body fat present indicated a moderate nutritional status. The lungs were congested and edematous, the right cardiac ventricle was moderately dilated, and the liver was severely congested.
Laboratory Results: None reported.
Contributor’s Diagnosis and Comment: 1. Heart, cardiac arteries: Severe atherosclerosis with lipid, cholesterol and mineral deposits, foamy macrophages, proliferation of smooth muscle cells and deposits of collagen and other extracellular matrix proteins, causing severe vascular occlusion.
Heart: Multifocal chronic myocardial degeneration and scarring.
In all small and medium-sized myocardial arteries there is extensive intimal thickening, variably composed of numerous needle-shaped lipid (cholesterol) crystals, enhanced deposits of extracellular matrix, dystrophic calcification, proliferated fibroblasts and smooth muscle cells, and foamy macrophages. The intima is lined with a single layer of endothelial cells, some of which appear mildly swollen. The vascular lumen is severely reduced in most arteries to between 10% and 30% of their original size. Special stains for lipid (not submitted) revealed large amounts of extracellular lipid deposits in the swollen intima and within macrophages in small and medium-sized arteries, as well as in small veins often associated with mineral deposits. Similar intimal lipid deposits were found in a few small renal arteries without proliferation of connective tissue or mineral deposition. No vascular changes were evident in other organs.
Death of the presented walrus was most likely due to cardiac failure as a sequel to the severe atherosclerosis of myocardial vessels that led to multiple myocardial infarctions. The morphological features of the lesions, as described above, include typical characteristics of atherosclerosis in other mammals and man, (e.g., subintimal lipid plaques, needle-shaped cholesterin crystals, proliferation of and phagocytosis by media smooth muscle cells, and multifocal dystrophic mineralization of the lesions).
Manipulations during treatment of the ocular lesions caused stress to the animal. The myocardial and vascular alterations may have induced additional myocardial infarctions. Thus, the colic observed 5 days prior to death, and interpreted as abdominal pain, was most likely a cardiac infarction. The severe vascular and myocardial changes may explain the animal’s deteriorating general condition and final circulatory failure.
Concerning the pathogenesis of atherosclerosis in this animal, several aspects may have been contributory, to include the progressed age and dietary components. The fish diet has to be reconsidered carefully, since there are no precise data available on the physiological diet of feral walruses. Several unique characteristics of apolipoprotein E have been detected in seals, sea lions and walruses that make it distinct from humans, and even cetaceans including dolphins and whales. The possibility of infection with chlamydia, which is thought to contribute to the pathogenesis of human atherosclerosis, was excluded in the heart and liver through immunohistochemistry and PCR.
AFIP Diagnoses: 1. Heart, coronary arteries: Atherosclerosis, moderate to severe, characterized by intimal foam cells, cholesterol clefts, fibrosis, mineralization, and luminal attenuation, Pacific walrus (Odobenus rosmarus divergens), pinniped.
2. Heart, myocardium: Replacement fibrosis, multifocally extensive.
Conference Comment: In humans, major risk factors for atherosclerosis that can be modified are hypercholesterolemia, hypertension, cigarette smoking, and diabetes mellitus. High dietary intake of cholesterol and saturated fats increases blood cholesterol. The “reaction to injury hypothesis” proposes that endothelial injury, possibly caused by hyperlipidemia, initiates a cascade of increased endothelial permeability, intimal lipid accumulation, platelet and monocyte adhesion, migration of smooth muscle cells into the intima, smooth muscle proliferation, synthesis of extracellular matrix components, and accumulation of lipid in macrophages, smooth muscle cells, and extracellularly. This leads to evolution of the atherosclerotic plaque. Ultimately, plaques may cause myocardial infarcts, cerebral infarcts or other major clinical effects.
It is thought that the paradoxically low incidence of ischemic heart disease in Greenland Eskimos, despite high dietary fat consumption, may be due to the high content of omega-3 fatty acids in their fish-based diets. Omega-3 fatty acids lower plasma low density lipoproteins (the major atherogenic lipoprotein moiety), increase vasodilation, increase high density lipoprotein (the protective lipoprotein believed to remove cholesterol from plaques), and reduce platelet aggregation.
Whether or not the fish-based diets fed to captive walruses may contribute to the development of atherosclerotic lesions warrants further investigation. We have seen another case of advanced atherosclerosis in a captive walrus. In the wild, walruses are believed to feed mainly on benthic invertebrates, such as molluscs, echinoderms and crustaceans, often consuming up to 45 kg per day.
Contributor: Institut für Pathologie, Tierärztliche Hochschule Hannover, Bunteweg 17 30559 Hannover, Germany
References: 1. Gruber AD, Peters M, Knieriem A, Wohlsein P: Atherosclerosis with cardiac failure in a Pacific walrus (Odobenus rosmarus divergens Illiger). Proc Eur Assoc Zoo Wildlife Vet, 3rd Scientific Meeting, 31 May–4 June, Paris, France, 2000
2. Schoen FJ, Cotran RS: Blood vessels. In: Robbins Pathologic Basis of Disease, ed. Cotran RS, Kumar V, Collins T, 6th ed., pp. 498-509. WB Saunders, Co., Philadelphia, PA, 1999
CASE IV – F-13457 (AFIP 2739653)
Signalment: 16-year-old male, castrated, Siamese, Felis catus, feline.
History: A 2-cm in diameter, firm, nodular mass adjacent to the maxillary premolars was noticed by the owners. The mass was subsequently removed and submitted for histologic examination.
Gross Pathology: None reported.
Laboratory Results: None reported.
Contributor’s Diagnoses and Comment: 1. Focal, nodular amyloidosis, gingiva, Siamese cat
2. Extramedullary plasmacytoma, gingiva, Siamese cat
Beneath the mildly hyperplastic gingival mucosa are variably-sized, relatively well-defined deposits of acellular, amorphous, pale eosinophilic material which reacts with Congo red staining and appears apple-green under polarized light (interpreted as amyloid). In some areas, amyloid forms well-demarcated lakes that compress the surrounding submucosa, while in other areas multinucleated giant cells surround smaller deposits. Macrophages often contain large amounts of intra-cytoplasmic amyloid. Aggregates of pleomorphic plasmacytoid neoplastic cells admixed with a few small lymphocytes and occasional neutrophils are scattered throughout the sections. The neoplastic cells have moderate amounts of pale, often basophilic cytoplasm, and dark round, often eccentrically located nuclei with stippled chromatin. There is marked anisokaryosis. Binucleate and multinucleate cells are common among the neoplastic cell population. Mitotic figures are rare at approximately 1 per 10 hpf (40X). Tumor cells and amyloid extend to the deep and lateral margins of the sections examined. Sections were also treated with acidified potassium permanganate, bleached with oxalic acid, and stained with Congo red. In these sections, amyloid showed positive Congo red staining, suggesting that it was AL type (amyloid light chain).
AL type amyloid is derived from plasma cells and contains immunoglobulin light chains. Amyloidosis is relatively rare in cats. Carothers (1989) reported a plasmacytoma involving the digit, with associated amyloidosis. Otherwise, no other reports of nodular amyloidosis involving the skin or oral cavity could be found. Extramedullary plasmacytomas in dogs are relatively common tumors that have often been associated with nodular amyloidosis.
Familial amyloidosis has recently been reported in Siamese cats. The main gross findings in affected cats include enlarged, pale livers with subcapsular hemorrhages, and enlarged spleens. The amyloid type in these cases was a unique AA (amyloid-associated) non-immunoglobulin protein synthesized in the liver.
In this case, the differential diagnosis for the nodular gingival lesion should include chronic plasmacytic gingivitis. However, because of the relatively anaplastic histologic appearance of the plasma cell population, and the presence of AL amyloid, this diagnosis was considered less likely.
AFIP Diagnosis: Stratified squamous epithelium overlying fibrous connective tissue and skeletal muscle (gingiva per contributor): Plasmacytoma, with abundant amyloid, Siamese cat, feline.
Conference Comment: Although the precursors of amyloid proteins have been well studied, some aspects of amyloid deposition remain unclear. Chronic inflammatory states often elevate serum AA levels, but monocyte-derived enzymes can degrade these circulating proteins to soluble end products, resulting in a lack of amyloid deposition. It is thought that amyloidosis results from incomplete degradation due to an enzyme defect, thus forming insoluble AA molecules. Alternatively, the AA molecules may be resistant to monocyte degradation due to a molecular structural mutation. Similar mechanisms of defective degradation of the immunoglobulin light chains, or resistance to proteolysis, are postulated for amyloid of the AL type. Tissue macrophages are believed to be involved in the conversion of the precursor proteins into the amyloid fibrils.
Contributor: Atlantic Veterinary College, University of Prince Edward Island, Department of Pathology and Microbiology, 550 University Avenue, Charlottetown, PEI, Canada, C1A 4P3
References: 1. Carothers MA, Johnson GC, DiBartola SP, Liepnicks J, Benson MD: Extramedullary plasmacytoma and immunoglobulin-associated amyloidosis in a cat. J Am Vet Med Assoc 195(11):1593-1597, 1989
2. Cotran RS, Kumar V, Collins T: Diseases of immunity. In: Robbins Pathologic Basis of Disease, 6th ed., pp. 251-257. WB Saunders Co., Philadelphia, PA, 1999
3. Niewold TA, van der Linde-Sipman JS, Murphy C, Tooten PC, Gruys E: Familial amyloidosis in cats: Siamese and Abyssinian AA proteins differ in primary sequence and pattern disposition. Amyloid 6(3):205-209, 1999
4. van der Linde-Sipman JS, Niewold TA, Tooten PCJ, de Neijs-Backer
M, Gruys E: Generalized AA-amyloidosis in Siamese and Oriental
cats. Vet Immuno Immunopathol 56:1-10, 1997
*Sponsored by the American Veterinary Medical Association, the American College of Veterinary Pathologists and the C. L. Davis Foundation.
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