ABSTRACT

Thirty-three North American zoos currently holding tapirs (Tapirus spp.) were surveyed for the occurrence of vesicular skin disease in those animals. Nineteen (58%) zoos responded and of those, 7 (37%) indicated that they had tapirs with histories suggestive of vesicular skin disease. From the 7 zoos with affected tapirs, 27 animals (18 T. indicus, 9 T. terrestris) experiencing a total of 116 episodes of skin disease were identified. Forty-eight percent (13) of the animals experienced more than one episode (mean 4.3 episodes per animal, range 1-24 episodes), and the mean duration of veterinary attention required per episode was 11.5 days (range 1-64 days). Previously affected females were 3.2 times more likely to suffer multiple episodes than previously affected males. The mean duration between episodes in repeatedly affected animals was 208 days (range 12 days-4.6 yrs). During 1991 the incidence rate was 0.36. The mean age of onset of the disease was 4.4 yrs (range 0.3-10.9 yrs). The lesions typically were characterized by coalescing hemorrhagic vesicles and bullae with 80% of the cases having lesions distributed along the dorsal midline. No fatalities have been attributed to this disease and all affected animals appear to recover fully regardless of the treatments given. No causal factors or effective treatments were noted.



INTRODUCTION

A 4 yr old female lowland tapir (Tapirus terrestris) at the Nashville Zoo was examined because of skin lesions occurring over the dorsal cervical and lumbosacral regions. The lesions consisted of coalescing hemorrhagic vesicles which ruptured and sloughed releasing serosanguinous fluid and leaving areas of exposed dermis. Digital pressure applied to affected areas of the skin yielded a positive Nikolsky's sign. The animal's appetite and attitude were normal, but it was noted that the tapir would collapse on all four legs when its head was manually elevated. The tapir's medical record indicated that two similar incidents had occurred within the previous year. Diagnostic evaluation at this time consisted of a complete blood count, serum biochemical profile, bacterial cultures of skin lesions, viral isolation attempts on vesicle fluid and skin biopsies, electron microscopy of vesicle fluid, and histopathology of affected skin. No etiologic agent was identified. After approximately one week the formation of new vesicles had stopped and older lesions began healing.

Anecdotal reports of other tapirs of different species with similar skin lesions prompted a survey of American and Canadian zoos holding Tapirus spp. in order to better define the disease in the various tapir species, reveal contributing factors, and compile diagnostic information relating to the disease.

For the purposes of this report, a case was defined as the occurrence of cervical or truncal, nonpruritic, hemorrhagic vesicular or bullous skin lesions. Descriptors such as "blisters," "peeling skin," "ulcers," and "flaking/rash" were considered compatible with the case definition if other factors (e.g., clinical course, distribution, tendency to reoccur) were described and consistent with other cases.



RESULTS

Questionnaires were sent to 33 zoological parks housing tapirs in the United States and Canada and 19 (58%) responded. Of the responding zoos, 7 (37%) had animals with histories of skin disease which met the criteria for vesicular skin disease. In total, 116 episodes of vesicular skin disease were documented in 27 animals (18 T. indicus, 9 T. terrestris) giving an average of 4.3 episodes per affected animal (range 1-24). Nearly half of the affected animals (13) experienced more than one episode and females were more likely to suffer multiple episodes than males. The relative risk for recurrence for affected females compared to affected males was 3.2. The average duration between episodes was 204 days (range 12 days-4.6 years) and there was no significant seasonal variation associated with the development of lesions detected. During 1991 there were 19 new episodes of vesicular skin disease at responding zoos giving an incidence rate of 0.36 for the year.

The disease typically first occurred in young adults (mean age of onset 4.4 yrs), but very young and aged animals were affected as well (range 0.3-10.9 yrs). Veterinary attention was required for an average of 11.5 days but ranged from 1 to 64 days.

Common descriptors used by veterinarians in documenting this disease included, "vesicles," "blisters"/"blood blisters," peeling epidermis/skin," "sweating blood," "flaking skin," and "ulcers." Eighty percent of the cases had lesions distributed over the dorsal midline. The cranial cervical region behind the ears, interscapular region, and lumbosacral region were all common sites of lesions. Concomitant unexplained neuromuscular abnormalities including hind limb ataxia, tetraparesis, collapse, or other lameness were described during 17 episodes. Most animals maintained a normal attitude and appetite during the course of the disease and there were no associated mortalities.

Diagnostic and therapeutic approaches varied considerably. Diagnostic tests including skin biopsy, cytology, CBC, serum biochemical profile, bacterial and fungal cultures, virus isolation, and serology were performed. No causative agent was identified. Therapeutic regimens focused on debridement of necrotic epidermis and the application of topical antimicrobials. In some cases systemic antibiotics, nonsteroidal antiinflammatory agents, systemic corticosteroids, topical sunscreens, topical antimicrobial/corticosteroid combinations, or moisturizing or protective agents were used. None of these therapeutic regimens appeared to dramatically alter the course of the disease and all cases appear to have resolved completely.



DISCUSSION

Histological evaluation of the of several full thickness skin biopsies from the Nashville Zoo's lowland tapir revealed multiple vesicles which were predominantly subepidermal and contained abundant fibrin, neutrophils, and eosinophils. The epithelium had severe spongiosis as well as superficial to transepidermal necrosis. Subcorneal pustules and abundant emigrating neutrophils, eosinophils, and red blood cells were present in viable epithelium. Hair follicles were unaffected. Along the superficial dermis, underlying the vesicles, was a narrow zone of collagen necrosis and a mild neutrophillic and eosinophilic infiltrate. There was severe perivascular edema surrounding dermal vessels and regionally severe hemorrhage in the superficial dermis. No microorganisms were identified within the lesions or on electron microscopy performed on vesicle fluid. Based on these findings, a histopathological diagnosis of subacute multifocal subepidermal vesicular dermatitis was made.

The primary differential diagnoses based on the histopathologic findings alone included erythema multiforme (vesicobullous form), toxic epidermal necrolysis, bullous skin diseases (bullous pemphigoid, lupus erythematosis, epidermolysis bullosa), dermatitis herpetiformis, and drug eruption.

Erythema multiforme (EM) is an acute, self-limiting cutaneous reaction pattern, of unknown pathogenesis and numerous etiologies. In humans, roughly 50% of EM cases are attributed to drug hypersensitivity, infection (viral, mycoplasmal, bacterial, fungal), pregnancy, neoplasia, contact reactions, sunlight, cold, or collagen-vascular disorders. The remaining 50% are classified as idiopathic (Scott 1984). Individual cell necrosis of keratinocytes (apoptosis) is a prominent feature of EM (Gross 1992), but areas of confluent epidermal necrosis may occur (vesicobullous form) (Scott 1991). Typically, EM is self-limiting, bilaterally symmetrical and asymptomatic (Scott 1991). Resolution generally occurs within 3 months (Scott 1988).

Toxic epidermal necrolysis (TEN) may have similar histopathological lesions to the vesicobullous form of EM, but tends to be more widespread and is usually associated with recent dnug administration. In TEN, unlike EM, there is no inflammatory component to the lesions initially and the patients tend to be painful and systemically ill (Gross 1992, Scott 1983).

The bullous skin diseases may resemble the lesions seen in this animal, however these diseases tend to have epidermal necrosis focused at the basal layer (Gross 1992, Scott 1988). IgG and complement components may be visualized at the basement membrane zone using direct immunofluorescence. These diseases are usually progressive without treatment and are often associated with signs of systemic illness (Schmeitzel 1991).

The histopathological findings in this animal's case are similar to those seen in dermatitis herpetiformis (DH). The diagnosis (DH) in animals is controversial (Ackerman 1984). In humans, the disease has been associated with gluten-sensitive enteropathy and the deposition of IgA along the dermal-epidermal junction. Elimination of gluten from the diet results in resolution of the skin lesions (Hall 1992).

It may be that vesicular skin disease is a common reaction pattern to a multitude of diseases in tapirs. A similar, but distinct, dermatological condition has been recognized in some captive Baird's tapirs (T. bairdii) (Dr. C. Miller, per. comm. 1993). In Baird's tapirs, the lesions tend to be more laterally oriented over the neck and trunk and are intensely pruritic. In these animals the lesions begin as vesicles but fill with a purulent exudate then rupture. In one animal these lesions appeared consistent with Staphylococcal folliculitis histologically. One zoo noted that coronary band vesicles were observed commonly in their Malayan tapirs, but that they had not seen lesions elsewhere (Dr. C. Miller, per. comm. 1993).

The vesicular skin disease seen in black rhinoceroses (Diceros bicornis) more closely resembles superficial necrolytic dermatitis (SND), than the disease seen in tapirs (Dr. L. Munson, per. comm. 1993). With SND, parakeratosis, edema and necrosis of keratinocytes with superficial clefting, and basal cell layer hyperplasia result in the characteristic "pink-white-blue" appearance seen in histologic sections (Miller 1990, Gross 1990). Unlike the skin disease of tapirs, the skin lesions in black rhinoceroses tend to be located over pressure points, ears, tail, feet, and coronary bands.

Future investigations will focus on attempts to demonstrate an immune component to this disease. Histological samples will be stained for immunoglobulin deposition. The presence and location of immunoglobulins will aid in the differentiation of the bullous skin diseases as well as DH. Serum will be collected during the acute and recovery phases and screened for specific antibody titers. If possible, cerebrospinal fluid analysis and titers will be performed on animals with neurological signs.



ACKNOWLEDGEMENTS

We would like to extend our appreciation to the zoos who took the time to complete our survey or send in medical records or clinical summaries. Drs. Kris Petrini and Don Janssen provided photographs of affected Malayan tapirs and Dr. Chris Miller provided photographs of both Baird's and Malayan tapirs.



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