History

A 4-week-old 1.0-kg (2.2-lb) female red panda (Ailurus fulgens) cub that had died at a zoo was submitted to the University of Tennessee College of Veterinary Medicine for necropsy. Information regarding clinical findings and treatment was provided by the submitting veterinarian. Prior to death, zoo veterinarians had removed the red panda cub from the mother because it developed an ulcerated tail lesion. The tail lesion was clinically suggestive of ringworm infection. The panda cub was hospitalized, and treatment with clotrimazole, itraconazole, and amoxicillin-clavulanic acid was initiated. Samples of skin and hair were collected for bacterial and fungal cultures before drug treatment initiation. An attempt to collect urine was made via urinary bladder catheterization 2 days before the panda cub's death. The following day, the panda cub developed a distended abdomen and anorexia and a stomach tube was used for administration of a feeding formula. The panda cub died after 2 days of hospitalization.

Clinical and Gross Findings

At necropsy, the panda cub had little to no subcutaneous, epicardial, mesenteric, or perirenal fat. A circumferential, 1-cm-deep, alopecic scaly lesion was present at the tail base. A focally extensive necrotizing and ulcerative area along the lateral surface of the tail was evident. This lesion measured approximately 3 × 2 × 1 cm. The edges of the lesion were raised and uneven with thickening, scaling, and alopecia of the adjacent skin. An alopecic scaly, circumferential, swollen lesion was present on the distal portion of the tail (Figure 1). Examination of the ulcerative tail base lesion under a Wood's lamp during necropsy revealed minimal fluorescence along the margins of the lesions. Skin samples were collected during necropsy for fungal culture.

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Photograph of tail lesions of a 4-week-old female red panda (Ailurus fulgens) that was initially treated for ringworm infection but subsequently died. The tail hairs were clipped prior to obtaining the photograph. Notice the circumferential tail-base lesion and the necrotizing and ulcerative lesion along the lateral surface of the tail and an alopecic scaly and swollen lesion on the distal portion of the tail.

Citation: Journal of the American Veterinary Medical Association 240, 8; 10.2460/javma.240.8.953

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The lungs had a mottled to multifocal pattern of alternating pink and red discoloration. The urinary bladder was empty, and a small 2 × 2 × 1-mm blood clot was attached to the mid-dorsal serosal surface. Within the abdominal cavity, 40 mL of serosanguineous fluid was present. Although a visible defect in the wall of the urinary bladder was not observed during gross examination, urinary bladder rupture and uroabdomen were suspected. The history of urinary bladder catheterization was provided by the submitting veterinarian after the necropsy, and it was concluded that the clinical procedure could have been the cause of the urinary bladder lesion. The likely cause of death was uroabdomen.

Formulate differential diagnoses from the history, clinical and gross findings, and Figure 1—then turn the page →

Histopathologic and Microbiological Findings

Sections of lungs, urinary bladder, kidneys, esophagus, trachea, skin from tail, pancreas, small intestine, and large intestine were examined histologically. Examination of sections of haired skin from the tail-base lesion revealed epidermal hyperplasia and parakeratosis with accompanying serocellular and neutrophilic crust formation. The dermis was expanded by perifollicular inflammatory infiltrates of macrophages and lymphocytes, a few neutrophils, and occasional plasma cells that extended diffusely into the deeper dermis. There were ruptured hair follicles in the mid and deep regions of the dermis. Free hair shafts were surrounded by an inflammatory infiltrate consisting of neutrophils and epithelioid macrophages; these cells formed multifocal to coalescing pyogranulomas (Figure 2). Large numbers of arthrospores and fungal hyphae were present in the hair shafts (endothrix), the follicular lumen (ectrothrix), and the hair follicular epithelium (Figure 3). In sections stained with Gomori methenamine silver stain, there were myriad arthrospores and fewer hyphae in the hair follicles and hair shafts and within the pyogranulomas. Arthrospores were round (up to 4 μm in diameter) to oval (4 × 2 μm). Hyphae were approximately 4 μm wide, septate, and parallel walled with occasional acute angle branching.

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Photomicrograph of a section of skin from the tail of the red panda cub in Figure 1. The section was obtained from the area of the distal tail lesion. Notice the multiple deep areas of furunculosis. Cartilage is evident in the lower left corner of the image. H&E stain; bar = 600 μm.

Citation: Journal of the American Veterinary Medical Association 240, 8; 10.2460/javma.240.8.953

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Photomicrographs of sections of skin from the tail of the red panda cub in Figure 1. A—Numerous arthrospores are visible in hair follicles and hair shafts. Mixed inflammatory infiltrates surround affected hair follicles. H&E stain; bar = 200 μm. B—Following Gomori methenamine silver staining, arthrospores and very few hyphae appear darkly stained. Bar = 200 μm.

Citation: Journal of the American Veterinary Medical Association 240, 8; 10.2460/javma.240.8.953

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Fungal culture of the skin samples collected during necropsy yielded a pure culture of a fungal organism that was mature in 8 days. The fungus grew on Sab-ouraud dextrose agar with added gentamicin and on a selective medium for the isolation of pathogenic fungi.^a A brownish-yellow powdered fungus that was brown on the reverse side of the plates containing Sabouraud dextrose agar with added gentamicin or the selective medium was observed. Microscopic examination of a transparent tape preparation with lactophenol aniline blue stain revealed that the fungus had numerous large cigar-shaped microconidia with ≤ 6 segments. Macroconidia had thin walls and rounded ends. Hyphae were septate, and no other fungal elements were observed. The fungal organism was identified as Microsporum gypseum. The results of bacterial and fungal cultures of samples of hair and skin collected from the panda cub during hospitalization were reported after the necropsy; M gypseum was isolated from the hairs, and Streptococcus-like organisms, Escherichia coli, and Proteus mirabilis were isolated from the aerobic bacterial culture of skin. No anaerobic organisms were isolated.

Sections of lung tissue had evidence of diffuse marked subacute histiocytic and neutrophilic bronchointerstitial pneumonia with intralesional granular to homogeneous eosinophilic material that was interpreted as aspirated liquid material. This histopathologic lesion in the lungs was most consistent with moderate aspiration pneumonia and was not grossly extensive; however, it might have had some role in the death of this already compromised patient. The urinary bladder had diffuse edema and hemorrhage on the serosa and in the submucosa and a focally extensive area of necrosis and hemorrhage of the muscular wall at the edge of the histologic section. Although bladder rupture was grossly suspected, a full-thickness perforation was not confirmed during histologic examination, possibly because of sectioning artifact, but the lesions detected were consistent with bladder rupture. No important histologic findings were observed in the other organs examined.

Morphologic Diagnosis

Severe chronic diffuse pyogranulomatous dermatitis with folliculitis, furunculosis, and intralesional dermatophytes (consistent with M gypseum).

Comments

For the panda cub of this report, clinical evidence was suggestive of ringworm infection, and results of gross and histologic examinations and fungal culture of the tail lesions and skin from the tail were consistent with M gypseum infection. Dermatophytosis is a superficial fungal infection, which is generally confined to the keratin layers of the skin, hair, and nails but occasionally can involve deeper tissues.¹ The nodular form of dermatophytosis due to furunculosis is also known as kerion, and the subcutaneous form is called dermatophyte pseudomycetoma.^1–3 Dermatophytosis affects humans and other animals, and the infection is caused by fungi of the genera Microsporum, Trichophyton, or Epidermophyton. These fungi can be classified as anthropophagic species (ie, those that are primarily adapted to humans and rarely infect other animals); zoophilic species (ie, those that are primarily adapted to nonhuman animals and typically cause less inflammation in their adapted host than do other species [eg, Microsporum canis in cats]); and geophilic species (ie, those that normally inhabit the soil and may cause infections in humans and other animals). Dermatophytosis in healthy individuals is usually self-limiting. Impaired T-cell function has been associated with chronic or recurrent dermatophyte infections; however, even apparently healthy animals can have persistent infections.¹

Microsporum canis, M gypseum, and Trichophyton mentagrophytes cause most infections in nonhuman animals.¹ Microsporum gypseum is a geophilic dermatophyte, and it is commonly isolated from deep skin lesions in dogs.^2,4,5 Young red pandas appear to be predisposed to infection with M gypseum.⁶ Dermatophytosis in red panda cubs from the Knoxville Zoo has been described, and M gypseum has been the only organism isolated via culture from most cases.⁶ The median age of affected red panda cubs is 8.5 weeks, and the lesions develop on the extremities, tail, muzzle, and ears.⁶ Tail lesions develop in approximately 40% of affected cubs, and pandas with severe disease commonly have ulcerative lesions on either the base or tip of the tail.⁶ Lesions in dogs attributable to M gypseum are most often observed on the face and limbs.^4,5 Microsporum gypseum infections of the skin on the tail of a 7-month-old panther kitten⁷ and on the tail of a 2-month-old cat have been described.⁸ Red pandas with focal lesions typically recover with topical or systemic treatment. However, red pandas with tail lesions generally develop highly inflammatory kerions, which rapidly expand and usually require partial tail amputation or result in marked fibrosis.⁶ The severity of the tail lesions is attributed in part to the limited blood supply to this region.⁶

The natural habitat of M gypseum is the soil, especially rich garden soil, where it decomposes keratinous debris. Dogs are exposed to it by digging in contaminated soils.^1,4 Usually kerion dermatophytosis is most often associated with geophilic dermatophytes such as M gypseum. These organisms are maladapted to the skin of humans or other animals; consequently, inflammation of the skin caused by colonization with these organisms can be severe.³ The incidence of M gypseum infection varies seasonally, being more common in summer and autumn and more common in humid tropical and subtropical areas.⁵ Most cases among red panda cubs have been reported during the months of July, August, and September⁶; the red panda cub of this report developed skin lesions in mid-July.

Dermatophytosis due to M gypseum should always be included in the differential diagnosis of focal or multifocal skin lesions in red panda cubs, especially when skin lesions are localized on the tail, limbs, or face. Both topical and systemic antifungal treatments are recommended for red pandas with dermatophytosis.⁶