History
An 8-year-old castrated male llama was evaluated because of skin disease that had waxed and waned in severity over the last few years. The owner had been treating the llama's affected skin areas with topical applications of a liberal amount of 20% zinc oxide ointmenta twice a week for > 1 year with no apparent effect. An unrelated 13-year-old female llama within the herd had similar, although more subtle, skin lesions. There were 17 llamas in the herd.
Clinical and Gross Findings
On physical examination, the male llama was weak and had a body condition score of 2 of 5. Rectal temperature was 39°C (102.2°F; reference range, 37.5° to 38.9°C [99.5° to 102.0°F]). Heart rate and respiration rate were considered normal. Large, locally extensive areas of thick, coalescing crusts were present in sparsely haired areas of skin of the axillary, inguinal, and perineal areas and around the muzzle (Figure 1). The crusts were firm and moist and could be manipulated away from the skin. When the crusts were removed, the underlying skin was moist and red and had a foul odor. Within the affected areas, there were scattered small pustules. Punch biopsy specimens of affected skin were obtained and submitted for histologic examination and routine aerobic microbial culture on blood agar plates.b
Photograph of a llama that was evaluated because of skin disease that had waxed and waned in severity over the last few years. Coalescing crusts are present over the skin of the muzzle. Photograph courtesy of Sue Cornell, Osage Llamas, Fayetteville, Ark.
Citation: Journal of the American Veterinary Medical Association 234, 8; 10.2460/javma.234.8.1013
Photograph of a llama that was evaluated because of skin disease that had waxed and waned in severity over the last few years. Coalescing crusts are present over the skin of the muzzle. Photograph courtesy of Sue Cornell, Osage Llamas, Fayetteville, Ark.
Citation: Journal of the American Veterinary Medical Association 234, 8; 10.2460/javma.234.8.1013
Photograph of a llama that was evaluated because of skin disease that had waxed and waned in severity over the last few years. Coalescing crusts are present over the skin of the muzzle. Photograph courtesy of Sue Cornell, Osage Llamas, Fayetteville, Ark.
Citation: Journal of the American Veterinary Medical Association 234, 8; 10.2460/javma.234.8.1013
Formulate differential diagnoses from the history, clinical findings, and Figure 1—then turn the page →
Histopathologic Findings
Histologic examination of punch biopsy specimens obtained from the axillary region revealed marked orthokeratotic to parakeratotic hyperkeratosis with thick serocellular crusts composed of layered degenerate neutrophils, small numbers of RBCs, and myriad yeast organisms (Figure 2). The yeast organisms were 5 to 7 μm in diameter; approximately 5- to 7-μm-diameter pseudohyphae with nonparallel walls were also evident (Figure 3). The underlying epidermis was moderately to markedly hyperplastic with multifocal areas of spongiosis, neutrophil exocytosis, and large intraepidermal pustules composed of degenerate neutrophils. Within the underlying dermis, there was a marked, multifocal perivascular infiltrate of neutrophils, macrophages, lymphocytes, and plasma cells. A pure culture of Candida albicans was obtained from the submitted fresh skin samples.
Photomicrograph of a section of a punch biopsy specimen obtained from the axilla of the llama in Figure 1. Notice the large serocellular crusts that are composed of neutrophils and cellular debris. The underlying epidermis is moderately hyperplastic with orthokeratotic to parakeratotic hyperkeratosis. There is a moderate mixed dermal inflammatory infiltrate. H&E stain; bar = 200 μm.
Citation: Journal of the American Veterinary Medical Association 234, 8; 10.2460/javma.234.8.1013
Photomicrograph of a section of a punch biopsy specimen obtained from the axilla of the llama in Figure 1. Notice the large serocellular crusts that are composed of neutrophils and cellular debris. The underlying epidermis is moderately hyperplastic with orthokeratotic to parakeratotic hyperkeratosis. There is a moderate mixed dermal inflammatory infiltrate. H&E stain; bar = 200 μm.
Citation: Journal of the American Veterinary Medical Association 234, 8; 10.2460/javma.234.8.1013
Photomicrograph of a section of a punch biopsy specimen obtained from the axilla of the llama in Figure 1. Notice the large serocellular crusts that are composed of neutrophils and cellular debris. The underlying epidermis is moderately hyperplastic with orthokeratotic to parakeratotic hyperkeratosis. There is a moderate mixed dermal inflammatory infiltrate. H&E stain; bar = 200 μm.
Citation: Journal of the American Veterinary Medical Association 234, 8; 10.2460/javma.234.8.1013
Photomicrograph of a section of a serocellular crust within a punch biopsy specimen obtained from the axilla of the llama in Figure 1. Yeast forms (arrowheads) and pseudohyphae (arrows) are evident within the crust. Gomori methenamine silver stain; bar = 100 μm.
Citation: Journal of the American Veterinary Medical Association 234, 8; 10.2460/javma.234.8.1013
Photomicrograph of a section of a serocellular crust within a punch biopsy specimen obtained from the axilla of the llama in Figure 1. Yeast forms (arrowheads) and pseudohyphae (arrows) are evident within the crust. Gomori methenamine silver stain; bar = 100 μm.
Citation: Journal of the American Veterinary Medical Association 234, 8; 10.2460/javma.234.8.1013
Photomicrograph of a section of a serocellular crust within a punch biopsy specimen obtained from the axilla of the llama in Figure 1. Yeast forms (arrowheads) and pseudohyphae (arrows) are evident within the crust. Gomori methenamine silver stain; bar = 100 μm.
Citation: Journal of the American Veterinary Medical Association 234, 8; 10.2460/javma.234.8.1013
Morphologic Diagnosis
Severe, diffuse suppurative dermatitis with serocellular crusting, epidermal hyperplasia, and intralesional yeast and pseudohyphae in haired skin of the axilla.
Comments
Causes of dermatologic disorders in camelids include ectoparasites, cutaneous fungal infection, bacterial dermatitis, immune-mediated disease, zinc-responsive dermatosis, and idiopathic nasal and perioral hyperkeratotic and inflammatory dermatosis (munge).1,2 Differential diagnoses for pustular dermatoses in camelids include autoimmune diseases and infectious dermatitis. The presence of yeast and pseudohyphae within the section of tissue obtained from the axilla of the llama of this report is characteristic of C albicans infection. Fungal dermatitis attributable to Malassezia spp is a common problem in domestic animals, but Malassezia organisms do not form pseudohyphae.3 The morphology of the yeast organisms and growth of C albicans from affected skin confirmed infection with this organism.
Autoimmune disease in camelids includes pemphigus foliaceus and pemphigus vulgaris.1,2 Pemphigus foliaceus is characterized histologically by subcorneal epidermal pustules that are composed of nondegenerate and degenerate neutrophils with acantholytic keratinocytes.4 Pemphigus vulgaris is characterized histologically by suprabasalar clefting with vesicle formation, few acantholytic keratinocytes, and minimal inflammatory cells.4 The neutrophils in the pustules associated with infectious dermatitis are more likely to be degenerate than those in the pustules associated with autoimmune disease.4 Infectious organisms may or may not be present within examined tissue sections. It can be difficult to differentiate autoimmune disease from an infectious disease in some instances, particularly if infectious organisms are not present within the sections that are examined histologically. In the llama of this report, the abundance of yeast organisms embedded within dense serocellular crusts composed of degenerate neutrophils favored the diagnosis of an infectious pustular dermatitis.
To our knowledge, there are limited reports1,2 of fungal dermatitis in camelids in the veterinary medical literature; among those reports, the most common fungal dermatitis is dermatophytosis. Infection with dermatophytes results in alopecia and scaling (ie, the typical ringworm lesion). Infections with Coccidioides immitis and Conidiobolus coronatus in camelids have also been reported.1,2,5 Clinical signs of those infections included pustular or nodular skin lesions; the diagnoses were made on the basis of findings of fungal culture of skin samples.
Candida albicans is a common microbial inhabitant of the respiratory, alimentary, and genital tracts.3,4 In a variety of species, C albicans can be associated with cutaneous, systemic, and localized infections.3 To our knowledge, there is only 1 report6 of infection with a Candida sp in an alpaca; the camelid had a mixed pulmonary infection with an Aspergillus sp, but there were no cutaneous signs of infection. In domestic mammals and humans, cutaneous infection with Candida spp is rare and often associated with underlying immune suppression.7–9
At the initial evaluation, the llama of this report had signs of depression suggestive of systemic illness. However, evidence of immune suppression was not documented by the referring veterinarian. The llama was treated with daily topical application of nystatinc and chlorhexidine acetated ointments to the affected skin regions. Following treatment for 60 days, the llama fully recovered with regrowth of hair within the affected regions. The female llama with similar, albeit less severe, clinical signs was treated similarly and responded completely to treatment.
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