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CASE I – 41197 (AFIP 2741455)
Signalment: 2.5-year-old, male East African pygmy falcon (Polihierax semitorquatus castanotus).
History: This falcon was presented to the veterinary hospital due to weight loss noted at a routine weighing. During the period of hospitalization (approximately 3 weeks) the falcon became increasingly lethargic and anorectic and continued to lose weight despite supplemental (forced) feeding and fluid administration. In addition to supportive care, the bird was treated with antibiotic and antifungal medications. Despite treatment, the falcon died.
Gross Pathology: The bird was in poor body condition with 36% weight loss, no fat stores and decreased pectoral muscle mass. The left cerebral hemisphere was pale tan/yellow and soft.
Laboratory Results: Persistently elevated CPK and LDH. Immunohistochemistry performed on formalin-fixed, paraffin embedded brain and lung was positive for Sarcocystis sp. Immunoperoxidase for Toxoplasma gondii on the same samples was negative.
Contributor’s Diagnoses and Comment: 1. Brain: severe, multifocally extensive, chronic, necrotizing encephalitis with intralesional protozoa (Etiology: Sarcocystis sp.).
2. Skeletal muscle, myofibers: severe parasitism (protozoal cysts) with mild multifocal myositis (Etiology: Sarcocystis sp.).
Sarcocytis species have a two-host predator-prey life cycle. Carnivores are generally the definitive host of the parasite and herbivores are the intermediate host. However, many species of carnivores may also serve as intermediate hosts, as demonstrated in this falcon. Three forms of infection with Sarcocystis have been described in avian intermediate hosts: visceral, muscular, and nervous. This case demonstrated both the muscular and nervous forms (not all slides contained skeletal muscle sections). The tissue response to the infection in the brain ranged from minimal (as seen in many of the submitted sections) to severe necrosis and perivascular mononuclear infiltration. As is common with muscle cysts, there was mild to no tissue reaction. We have also seen the fatal visceral (pulmonary) form of sarcocystosis in this species of bird. The species of Sarcocystis was not identified in this case. Sarcocystis falcatula is considered a likely possibility as several avian species (including other raptors) have been identified as intermediate hosts for S. falcatula. The opossum (Didelphis virginiana) is the definitive host for S. falcatula.
AFIP Diagnoses: 1. Skeletal muscle: Sarcocysts, numerous, with multifocal myofiber degeneration and necrosis, East African pygmy falcon (Polihierax semitorquatus castanotus), avian.
2. Brain: Encephalitis, lymphoplasmacytic and heterophilic, necrotizing, multifocal, moderate, with gliosis and many coccidian organisms.
Conference Comment: Sarcocystosis has an obligatory two-host life cycle. The muscle phase in the intermediate host was once thought to be a relatively asymptomatic infection. It is now known that occasionally schizogony during the asexual phase may cause severe muscle lesions with segmental hyaline change and degeneration of muscle fibers.
Muscle diseases characterized by degeneration and necrosis will result in elevations of several serum enzymes. Creatine kinase (CK) can be found primarily in the cytosol of skeletal and cardiac muscle and the brain. Of the three isoenzymes, CK1 is found in brain, peripheral nerves, cerebrospinal fluid and viscera, but cannot be detected in serum, even in neurological disease. CK2 is found in cardiac muscle and minute amounts may be found in skeletal muscle. CK3 is found in skeletal and cardiac muscle. CK is considered the most sensitive indicator of muscle injury and its values increase and return to normal quickly. Lactate dehydrogenase (LDH) has five isoenzymes and can be found in many tissues, although muscle, liver and erythrocytes usually account for most of the increase in levels. LDH1 is the principal isoenzyme in cardiac muscle and LDH5 is found in skeletal muscle and erythrocytes. Alanine aminotransferase (ALT), while considered nearly liver-specific in the dog and cat, is not useful for detecting liver disease in horses, ruminants and pigs. It increases moderately in muscle disease in ruminants and pigs.
Conference participants noted evidence of endopolygeny in the brain sections, characterized by multiple zoites radiating off a central organism. This is a distinctive features of some apicomplexans; Toxoplasma gondii does not replicate by this process.
Contributor: Zoological Society of San Diego, Department of Pathology, P.O. Box 120551, San Diego CA, 92112-0551
References: 1. Aguilar RF, Shaw DP, Dubey JP, Redig P: Sarcocystis-associated encephalitis in an immature northern goshawk (Accipiter gentilis atricapillus). J Zoo Wildl Med 22(4):466-469, 1991
2. Dubey JP, Porter SL, Hattel AL, Kradel DC, Topper MJ, Johnson L: Sarcocystis-associated clinical encephalitis in a golden eagle (Aquila chrysaetos). J Zoo Wildl Med 22(2):233-236, 1991
3. Dubey JP, Speer CA, Fayer R: Sarcocystosis of animals and man, pp. 1-13. CRC Press, Boca Raton, FL, 1989
4. Duncan JR, Prasse KW, Mahaffey EA: Muscle. In: Veterinary Laboratory Medicine: Clinical Pathology, 3rd ed., pp. 184-187. Iowa State University Press, Ames, IA, 1994
5. Hulland TJ: Muscle and tendon. In: Pathology of Domestic Animals, ed. Jubb KVF, Kennedy PC, Palmer N, 4th ed., vol. 1, pp. 256-259. Academic Press, San Diego, CA, 1993
CASE II – 97/00-638 (AFIP 2747840)
Signalment: 18-month-old, female crossbred bovine (Bos indicus).
History: This animal originated from a group of ±80 animals necropsied as part of an eradication campaign. The animal had a history of coughing and was emaciated with exaggerated costo-abdominal breathing.
Gross Pathology: At necropsy, the animal was in fair condition. A sequestrum measuring ±60 mm in diameter was present in the ventral part of the left diaphragmatic lung lobe. On cut surface a well-developed fibrous connective tissue capsule surrounded the necrotic contents. The pleura adjacent to the sequestrum was diffusely thickened and there were multiple fibrous attachments between the parietal and visceral pleura. The remaining lung lobes were unaffected.
Laboratory Results: Mycoplasma mycoides subspecies mycoides was isolated from the affected lung tissue and identified by using the indirect fluorescent antibody test on lung impression smears. The serum tested positive with the complement fixation test, as well as a competitive enzyme-linked immunosorbent assay (cELISA).
Contributor’s Diagnosis and Comment: Lung: Pneumonia, necrotizing and granulomatous, diffuse, severe with vasculitis and lymphangitis associated with thrombosis, infarction and dilatation of interstitial septa.
Etiology: Mycoplasma mycoides subsp. mycoides (lungsickness).
An outbreak of contagious bovine pleuropneumonia (CBPP) was confirmed in Botswana in 1995 after being absent from the country for more than half a century. The disease has since been eradicated from Botswana. Currently the presence of CBPP in parts of Southern Africa severely restricts economic development and the proper utilization of agricultural land.
The causative organism has a low resistance to adverse environmental factors and only survives outside the host for up to 3 days in tropical areas and up to 2 weeks in temperate zones. Natural transmission of CBPP occurs by droplet infection, either from cattle with clinical disease or from sub-clinical carriers. Direct contact of susceptible with diseased animals appears to be mandatory for transmission.
During the course of the disease, pulmonary sequestra may develop in animals that recover from the clinical disease and persists for many months. Sequestra are comprised of necrotic tissue that becomes encapsulated by fibrous connective tissue in which viable organisms may occur for up to 12 months or longer. It is suspected that immuno-incompetence resulting from stress may induce the capsule of a sequestrum to breakdown and thus allow new foci of active pneumonia to develop in surrounding lung tissue with the result that the animal is, once again, infective. Clinically recovered animals are, therefore, mainly responsible for the spreading of disease under such circumstances.
The level of susceptibility of animals in a given herd varies considerably between individuals. Ten to 16% of cattle may be resistant, and as few as 8% of the herd may develop clinical signs. Survivors in an outbreak have a substantial degree of resistance.
The pathogenesis of CBPP is poorly understood. Infection via the respiratory tract causes bronchiolitis and pneumonia. The carbohydrate galactan, a major antigen present in M. mycoides mycoides SC (small colony), has profound physiological effects similar to those of the endotoxins of Gram-negative bacteria.
At necropsy, the most characteristic lesions occur in the lungs and thoracic cavity. During the acute stage of the disease, there is often uni- or bilateral pleural effusion. The yellowish-grey, clear, or turbid fluid contains pieces of fibrin and may exceed 10 liters. This is generally accompanied by a localized or diffuse pronounced fibrinous pleuritis. Pneumonic areas are characterized by marbling, caused by the intermingling of lobules which show varying stages of grey or red hepatization, and relatively unaffected lobules. The marbling is accentuated by distension of interlobular septa and interstitium surrounding vessels and airways by a serofibrinous exudate.
Multiple thrombi are found along the course of the lymphatics in the interlobular septa, with subsequent irregular lymphangiectasia that often imparts a “beaded” appearance to the septa. Infarcts of varying size are frequently present in the affected lung tissue as a result of thrombosis of inter- or intralobular arteries and are manifested as well-demarcated areas of necrosis. Infarcts subsequently become sequestered from the adjacent parenchyma by granulation tissue and are referred to as sequestra. In chronic cases, one or more sequestra are usually present in the lungs. Secondary bacterial infection of sequestra frequently occurs. In animals that recover, previous infarcts are represented by fibrous scars.
A serofibrinous polyarthritis and tenosynovitis, affecting particularly the carpus and tarsus, are a common lesion in affected calves.
Diagnosis of CBPP is confirmed by either isolation of the causative organism, indirect fluorescent antibody testing on lung impression smears, or by means of polymerase chain reaction (PCR).
Acute CBPP must be differentiated from pneumonic pasteurellosis, mainly caused by Manheimia (Pasteurella) haemolytica, and hemorrhagic septicemia caused by Pasteurella multocida types B and E. The sequestra in chronic cases of the disease must be differentiated from the lesions associated with actinobacillosis, echinococcus cysts, foreign body pneumonia, and pneumonia caused by various fungi.
AFIP Diagnosis: Lung: Pneumonia, fibrinonecrotic, chronic, diffuse, severe, with peribronchiolar lymphoid hyperplasia and marked septal and alveolar edema, crossbred cow (Bos indicus), bovine.
Conference Comment: The implication of mycoplasmas as a primary pathogenic agent in many diseases is difficult due to their ubiquitous nature, especially in the respiratory tract. Additionally, the more virulent strains are often the most difficult to culture. Firm cellular adhesion of Mycoplasma mycoides mycoides SC to mucous membrane epithelial cells is central to their pathogenicity and ability to resist elimination by mucous secretions. The chain of pathogenic events leading to the commonly seen vasculitis is still speculative, but the ensuing thrombosis it can cause is central to the development of sequestra. The fact that many animals may remain serologically positive without showing overt disease is a clinical pattern consistent with the chronic nature of most mycoplasmal infections.
Contributor: Onderstepoort Veterinary Institute, P.O. Box 12502, Onderstepoort, South Africa, 0110
References: 1. Amanfu W, Masupu KV, Adom EK, Raborokgwe MV, Bashiruddin JB: An outbreak of contagious bovine pleuropneumonia in Ngamiland district of Northwestern Botswana. Vet Rec 143:46-48, 1998
2. Henton MM, Potts AD, Prozesky L, Marais SJF: Chronic Mycoplasma mycoides mycoides SC; comparison of bacterial and serologic results. In: Proceedings of the ARC-Onderstepoort, OIE International Congress with WHO-cosponsorship on Anthrax, Brucellosis, CBPP, Clostridial and Mycobacterial diseases, pp. 208-225. Berg-en-Dal, Kruger National Park, 9-15 August, 1998
3. Prozesky L, Henton MM, Dungu-Kimbenga B, Bosman AM, Potts A, Amanfu W, Thiaucourt F, Nyange JF, Masupu KV: Diagnosis of contagious bovine pleuropneumonia. A comparison of macro- and microscopical lesions, bacterial isolation, complement fixation test, ELISA and polymerase chain reaction. In: Proceedings of the ARC-Onderstepoort, OIE International Congress with WHO-cosponsorship on Anthrax, Brucellosis, CBPP, Clostridial and Mycobacterial diseases, p. 207. Berg-en-Dal, Kruger National Park, 9-15 August, 1998
4. Schneider HP, van der Lugt JJ, Hübschle OJB: Contagious bovine pleuropneumonia. In: Infectious Diseases of Livestock with Special Reference to Southern Africa, vol. 2, pp. 1485-1494. Oxford University Press, New York, NY, 1994
CASE III – 00-991 (AFIP 2737307)
Signalment: Juvenile, sex unknown, Eastern gray squirrel (Sciurus carolinensis)
History: This juvenile gray squirrel was rescued from a cat. At presentation it had generalized thickening of the skin, including swollen paws and had difficulty walking. It was euthanized because of bilateral corneal ulcers.
Gross Pathology: The 161.5 g squirrel had generalized thickening of the skin with many folds, multifocal crusting and alopecia. Facial skin was diffusely thickened, including the eyelids, giving a distorted profile to the face. The feet were enlarged. The lung had disseminated white firm nodules.
Laboratory Results: A suspension of a skin nodule (from another gray squirrel, 00-1137, found in the same vicinity as 00-991) was negatively stained with phosphotungstic acid, sprayed on a Formbar carbon coated grid and examined by TEM. The electron micrograph (018331), at 20,000X, demonstrates some of the numerous “brick-shaped” particles about 350 nm in greatest dimension, consistent with large orthopoxvirus particles (scale bar=250 nm).
Contributor’s Diagnosis and Comment: The skin has marked parakeratotic/ orthokeratotic hyperkeratosis and acanthosis with numerous, epidermal, intracytoplasmic, magenta inclusion bodies of varying diameter; inclusions usually have a thin, blue-black rim. The subjacent dermis is expanded by primitive fibroblasts (fibroma, fibromatosis) which occasionally have similar intracytoplasmic inclusions. The kidney has generalized dilation of tubules and multifocal interstitial edema and fibromatosis; a very occasional inclusion body like those in the skin is present in the cytoplasm of interstitial fibroblasts. Transitional epithelium in some sections contains numerous cytoplasmic inclusion bodies.
The pulmonary nodules seen grossly consisted of multifocal, coalescing, alveolar accumulations of large, round cells with foamy cytoplasm and intracytoplasmic inclusions like those in the skin.
Squirrel pox is not only associated with a prominent epidermal hyperkeratosis and dermal fibromatosis but may be associated with fibromatosis in various organs including the kidney, liver, lung, intestine and lymph nodes. The generalized distention of renal tubules with atrophied epithelia in this case is thought to be associated with multifocal interstitial fibromatosis that was quite prominent in some regions. Renal papillary tubular adenomas have also been associated with squirrel pox.
Note: The amount of dermal and renal fibromatosis varied throughout the slide set so this response in some slides will be more prominent than in others.
AFIP Diagnoses: 1. Haired skin: Dermatitis, lymphohistiocytic and neutrophilic, chronic, diffuse, moderate, with marked epidermal and follicular epithelial hyperplasia, dermal mesenchymal cell proliferation, epithelial ballooning degeneration, and numerous epithelial and mesenchymal eosinophilic intracytoplasmic inclusion bodies, Eastern gray squirrel (Sciurus carolinensis), rodent.
2. Kidney: Tubular dilatation, diffuse, moderate, with multifocal interstitial mesenchymal proliferation, epithelial ballooning degeneration, and epithelial and mesenchymal eosinophilic intracytoplasmic inclusion bodies.
Conference Comment: The large family of host-specific DNA poxviruses can cause cutaneous and systemic lesions in many animal species. Experimentally transmitted by mosquitoes, squirrel poxvirus is a member of the Leporipoxvirus genus that also includes Shope fibroma and myxoma viruses of rabbits. Immune competence is believed to play a role in the development of lesions since only juvenile squirrels develop multiple fibromas of lung, liver or kidney, in addition to the cutaneous tumors seen in adults.
Skin and multi-organ tumors often involve proliferation of both epithelial and mesenchymal cells. Hydropic or ballooning degeneration of epithelial cells is classic, and the eosinophilic intracytoplasmic inclusion bodies can be found in both populations of cells.
An interesting comment by the moderator concerned the decimation of the red squirrel (Sciurus vulgaris) population in the United Kingdom caused by the introduction of the North American Eastern gray squirrel (Sciurus carolinensis). In addition to the gray squirrel being stronger and more efficient at food gathering, it may also be an asymptomatic carrier of a parapoxvirus that can be fatal to red squirrels.
Contributor: University of Tennessee, College of Veterinary Medicine, Department of Pathology, Room A201, Knoxville, TN 37901-1071
References: 1. Hirth RS, Wyand DS, Osborne AD, Burke CN: Epidermal changes caused by squirrel poxvirus. J Am Vet Med Assoc 155:1120-1125, 1969
2. King JM, Woolf A, Shively JN: Naturally occurring squirrel fibroma with involvement of internal organs. J Wildl Dis 8:321-324, 1972
3. Melton NN, Flyger V, Jacobson ER, Dutta SK, Sacchi ED: Systemic phycomycosis and multiple fibromas in a gray squirrel (Sciurus carolinensis). J Wildl Dis 17:89-95, 1981
4. O’Connor DJ, Diters RW, Nielsen SW: Poxvirus and multiple tumors in an Eastern gray squirrel. J Am Vet Med Assoc 177:792-795, 1980
CASE IV – 133369 (AFIP 2740569)
Signalment: 12-year-old, female green conure
History: The bird was housed with another conure and allowed to fly freely within the house. Feed included seed mix, fruits and vegetables, and pasta. The bird had a history of chronic sneezing that was attributed clinically to an upper respiratory infection. The bird died acutely after one day of increased sneezing and was presented for necropsy.
Gross Pathology: There was a 1.6 x 1.4 cm well-demarcated transmural thickening at the junction of the proventriculus and esophagus. The lesion was uniformly white-tan and its mucosal surface was soft and papillary. There was fine granular white discoloration of the adjacent esophageal mucosa. No other gross lesions were noted.
Laboratory Results: None given.
Contributor’s Diagnosis and Comment: Esophageal-proventricular junction: Basaloid squamous cell carcinoma with superficial bacterial and fungal colonization, green conure, avian.
The most striking features of this papillary, infiltrative, transmural malignancy at the junction between the esophagus and proventriculus is its prominent basal cell component and the presence of florid papillary hyperkeratosis. The mass is covered by thick spires of lamellar keratin with ghost cells. Thick fronds and trabeculae of primarily basaloid and, less frequently, stratified squamous, keratinized epithelial cells are supported by a moderately dense fibrovascular stroma. Neoplastic epithelial cells exhibit moderate anisocytosis, anisokaryosis and >10 mitotic forms per HPF. Cells contain oval to indented, heterochromatic nuclei, rare nucleoli, and variable amounts of pale eosinophilic cytoplasm. Cords of neoplastic cells multifocally dissect the muscularis externa. The keratin layer contains cellular debris, moderate infiltrates of heterophils and gram-positive bacterial cocci, rods and filamentous forms. Surface colonization by fungal yeast-like cells (3-6 m m diameter), pseudohyphae, and poorly septate hyphae (3-5 m m wide) are present. Hyphae have roughly parallel walls and rare oval budding forms (blastoconidia) that are consistent with Candida spp., and considered to be not clinically significant. The mucosal epithelium of the adjacent crop was markedly and diffusely hyperplastic and hyperkeratotic (orthokeratotic). In some sections, the esophagus is abutted by segments of thoracic air sac that contain mild, multifocal, primarily lymphoplasmacytic submucosal infiltrates.
Reported epithelial neoplasms of the avian esophagus and crop include papilloma, squamous plaque (epithelioma) and squamous cell carcinoma. Avian esophageal squamous cell carcinoma (SCC) has been rarely reported and may grossly have a “cauliflower” surface. Histologically, lesions are similar in appearance and invasiveness to mammalian SCC. Local invasion is common and metastasis is rare. Squamous plaques are described as hyperplastic, +/- dysplastic thickenings of squamous epithelium that may also undergo neoplastic transformation. Papillomas are the most common avian esophageal neoplasms and have a typical appearance. Mucosal papillomatous proliferations are seen throughout the gastrointestinal tract of psittacine birds as part of the disease complex known as internal papillomatous disease (IPD) or internal papillomatous disease of parrots (IPP). The cloaca is usually among the sites affected, although the oral cavity, lacrimal system, esophagus and stomach also may be involved. No etiologic agent has been identified, although papilloma virus and Pacheco’s disease virus, a herpesvirus, have been investigated. Malignant transformation of these lesions has not been recognized, although such transformation can be seen in cases of human papillomaviral infections.
Esophageal neoplasms are extremely rare in dogs and cats; they account for less than 1% of all malignancies and less than 5% of all gastrointestinal tumors. Most are metastatic. Primary canine esophageal neoplasms include Spirocerca lupi-associated sarcoma, squamous cell carcinoma, undifferentiated carcinoma and leiomyoma. Viral oropharyngeal papillomas rarely may extend into the proximal esophagus. In cats, squamous cell carcinomas are the most common neoplasms with others rarely encountered. Feline esophageal SCC usually presents as a variably annular and sometimes nodular or ulcerated mass in the middle third of the esophagus at the level of the heart base. Esophageal SCC in both species tends to be locally invasive and rarely will metastasize.
In horses, esophageal SCC is rare. SCC of the non-glandular portion of the stomach is uncommon, and some cases of gastric SCC may result from malignant transformation of areas of glandular stomach that have undergone squamous metaplasia. In domestic swine, carcinoma of the non-glandular stomach is not reported. Papillomas and SCC of the bovine esophagus are well-recognized, while they are rare in small ruminants.
In humans, basaloid squamous cell carcinoma (BSCC) is an uncommon variant of SCC that may occur in the esophagus. BSCC is characterized by a growth pattern of solid cords of neoplastic cells with regions of squamous differentiation and frequent confluent (comedo type) necrosis surrounded by a fibrous stroma. Such neoplasms demonstrate occasional ribbon-like growth or pseudoglandular or cribriform displays. The behavior and prognosis are similar to that of typical SCC.
Significant geographic variation in frequency of esophageal neoplasia has been reported in humans, chickens, cats and cattle. Ingestion of mycotoxins, nitrosamines and other carcinogens (including bracken fern in cattle) has been investigated as a possible cause (or cofactor in cases of papillomaviral infection of humans and cattle). It has been proposed that these agents induce hyperplasia of squamous epithelium, immunosuppression, and subsequent malignant transformation. Mold-contaminated grain has been implicated as a likely source of exposure. Chronic esophagitis has also been implicated as a possible etiology.
AFIP Diagnosis: Esophagus, adjacent to proventriculus: Squamous cell carcinoma, green conure, avian.
Conference Comment: Although “basaloid” squamous cell carcinoma is not a diagnosis that has been routinely used in veterinary medicine, the term is certainly descriptive of this neoplasm's appearance.
Contributor: Angell Memorial Animal Hospital, Department of Pathology, 350 S. Huntington Avenue, Boston MA 02130
References: 1. Gualtieri M, Monzeglio MG, DiGiancamillo M: Oesophageal squamous cell carcinoma in two cats. J Small Anim Pract 40:79-83, 1999
2. Graham DL: Internal papillomatous disease: a pathologist’s view of cloacal papillomas–and then some! Proc Assoc Avian Vet, pp. 141-143. Chicago, 1991
3. Head KW: Tumors of the alimentary tract: tumors of the esophagus and esophageal region of the stomach. In: Tumors in Domestic Animals, ed. Moulton JE, 3rd ed., pp. 381-91. University California Press, Berkeley, CA, 1990
4. Latimer KS: Oncology: digestive system. In: Avian Medicine: Principles and Applications, ed. Ritchie BW, Harrison GJ, Harrison LR, pp. 655-656. Wingers Publishing, Inc., Lake Worth, FL, 1994
5. Murtaugh RJ, Ringler DJ, Petrak ML: Squamous cell carcinoma of the esophagus in an Amazon parrot. J Am Vet Med Assoc 188:872-873, 1986
6. Sarbia M, Verreet P, Bittinger F, Dutkowski P, Heep H, Willers
R, Gabbert H: Basaloid squamous cell carcinoma of the esophagus.
Cancer 79(10):1871-1878, 1997
*Sponsored by the American Veterinary Medical Association, the American College of Veterinary Pathologists and the C. L. Davis Foundation.
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