key: cord-257943-fippk9p4
authors: Palmeiro, Brian S.; Roberts, Helen
title: Clinical Approach to Dermatologic Disease in Exotic Animals
date: 2013-07-17
journal: Vet Clin North Am Exot Anim Pract
DOI: 10.1016/j.cvex.2013.05.003
sha: 
doc_id: 257943
cord_uid: fippk9p4

Skin disease is an extremely common presenting complaint to the exotic animal practitioner. A systematic diagnostic approach is necessary in these cases to achieve a diagnosis and formulate an effective treatment plan. In all exotic species, husbandry plays a central role in the pathogenesis of cutaneous disease, so a thorough evaluation of the husbandry is critical for successful management. The clinical approach to skin disease in exotic animal patients is reviewed with specific focus on structure and function of the skin, diagnostic testing, and differential diagnoses for commonly encountered cutaneous diseases.

Skin disease is an extremely common presenting complaint to the exotic animal practitioner. A systematic diagnostic approach is necessary in these cases to achieve the appropriate diagnosis and formulate an effective treatment plan. In all exotic species, husbandry plays a central role in the pathogenesis of cutaneous disease, so a thorough evaluation of the husbandry is critical for successful management. There are vast differences in the structure and function of the skin in exotic species; an understanding of these unique properties is important when treating skin disease in exotic pets. This article focuses on the clinical approach to skin disease in exotic pets including structure and function of the skin, appropriate diagnostic testing, and differential diagnoses for commonly encountered cutaneous diseases. study of dermatologic lesions in reptiles found that from 29% to 64% (dependent on institution and reptile group) of the cases had underlying husbandry-related deficiencies. 1 

Reptile skin is modified into scales and composed of a three-layered epidermis and a dermis that typically is aglandular. [2] [3] [4] The three layers of the epidermis are (1) stratum corneum (six to eight cell layers, heavily keratinized); (2) stratum intermedium; and (3) stratum germinativum (deepest). [2] [3] [4] Two types of keratins compose the stratum corneum. 4 The softer more flexible a-keratins are elastic and pliable and form the suture/hinges and spaces between scales. 4 The b-keratins (unique to birds and reptiles) compose the hard horny scale. 4 The skin is protected by scales produced by the stratum germinativum; scales are separated by scale pockets. 2 The keratinized layers of chelonians are modified into scutes. 5 The scales or scutes of chelonians and some lizards (plated and girdled lizards, skinks, and crocodilians) are underlain by dermal bony plates referred to as osteoderms or osteoscutes. [2] [3] [4] [5] In tortoises, the stratum corneum produces the shell, which consists of the carapace (dorsal) and plastron (ventral); the keratinized scutes cover osteoderms that fuse with the vertebrae and sternebrae. [2] [3] [4] Chromatophores (pigment cells) are found in the dermis and melanocytes are present within the stratum germinativum. 3 Reptiles shed their skin at regular intervals in a process called ecdysis. The skin of lizards and chelonians shed in several smaller pieces, whereas snakes typically shed their entire skin as one piece. 4 Chelonians and crocodilians shed their epidermis continuously, whereas lizards and snakes shed their epidermis periodically. 5 

A detailed clinical history is important in all cases of reptile skin disease; important husbandry-related questions include those pertaining to diet, substrate and housing, lighting, heating, humidity, and temperature.

Common findings during clinical examination of reptiles with dermatologic disease include abrasions, erosions, ulcers, wounds, swellings, pustules, blisters/vesicles/ bullae, crusts, dysecdysis, petechial and ecchymoses, discoloration, macroparasites, and edema. In some cases, cutaneous changes can be secondary to systemic disease; petechia and ecchymoses are commonly seen with septicemia and ventral edema may be seen with renal or liver disease. 3 In one study, 47% of all reptiles with confirmed or suspected cases of sepsis had petechiae, with the highest association seen in chelonians (82%). 1 Commonly used dermatologic diagnostic tests in reptiles include the following 2-5 : 

Most useful for swellings and growths 8. Clinicopathologic evaluation including complete blood count (CBC) and biochemistry analysis 9. Radiographs are useful when assessing damaged osteoderms and for the presence of bony changes associated with secondary nutritional hyperparathyroidism or other internal disease

See Table 1 for a review of common differential diagnoses for dermatologic diseases in reptiles, including bacterial dermatitis, shell rot, bacterial ulcerative dermatitis, snake mite, and secondary nutritional hyperparathyroidism (Figs. [1] [2] [3] [4] [5] .

The thin, relatively unprotected skin of amphibians combined with the significant diversity of amphibian habitats and their biphasic life cycles render them particularly susceptible to a wide range of infectious and noninfectious cutaneous diseases.

Amphibians belong to three distinct Orders: Anura (frogs); Caudata (salamanders); and Gymnophiona (caecilians). The skin of amphibians is clinically the most important organ system of amphibians and varies depending on the life stage (premetamorphosis or postmetamorphosis); habitat (generally divided into aquatic or terrestrial); and the species. 6 The skin functions in osmoregulation, gas respiration, and water absorption. 6, 7 Amphibian epidermis is typically thin; keratinized; and consists of the stratum corneum, stratum granulosum, stratum spinosum, and the stratum basale. [7] [8] [9] [10] [11] Modifications of amphibian skin include the presence of dermal scales (caecilians); folds and grooves for increased surface area (salamanders); partial ossification of the cranial skin and adherence to the skull (bufonids); a specialized highly vascularized ventral dermal organ for water absorption ("drinking patch" in anurans); and the presence of dermal bones (some anurans). 10, 12 The stratum corneum is typically shed in one piece at regular intervals and consumed (dermatophagy) unless the animal is ill. 6, 11, 13 The skin of anurans is loosely adhered to the body and can become edematous in disease states. 11 Two key features separate adult caecilians and anurans from their larval form: the epidermis is keratinized in adults and the dermis contains a variety of dermal glands. 7, 9, 11 Mucus, produced by mucous glands and epithelial cells, aids in respiration, prevents evaporative water loss, contains antibacterial and antifungal properties, can be defensive noxious or contain toxic chemicals, may act as pheromones, and can aid in reproduction. 12, [14] [15] [16] [17] Dermatologic Examination and Diagnostic Testing A thorough history and dermatologic examination are important when evaluating any case of amphibian skin disease. Husbandry-related factors often underlie the development of many skin diseases in amphibians. Important questions to consider include recent introductions into the collection; diet; and tank setup including filtration, aeration, water quality, and temperature. During examination, it is important to always handle amphibians with rinsed gloves to avoid damaging their skin and prevent cutaneous absorption of potentially toxic glandular secretions. [18] [19] [20] Many amphibian skin diseases can have a similar appearance with cutaneous hyperemia and discoloration, dermal papules and nodules, ulceration, hemorrhages, edema, and excess mucus being the most common findings. 21 Clinical Approach to Dermatologic Disease Commonly used dermatologic diagnostic tests in amphibians include the following:

1. Skin scraping 8, 10, 13 Using a coverslip, blunt scalpel blade, or edge of a glass slide, gently scrape over the surface of the skin Samples taken from lesions may be more diagnostic Place the sample on a slide If needed, wet the slide with physiologic saline for a wet mount preparation Examine immediately using lowest power objective first Shed skin can also be examined as a wet mount preparation Samples can also be dried and stained for later examination 2. Impression or swab smears, fine-needle aspirates 6, 8, 13 Typically these samples are air dried and stained Less traumatic than skin scrapings 3. Bacterial culture 10, 13, 22, 23 

Gentle irrigation of the lesion with sterile physiologic saline or getting a deep sample can reduce contamination of normal surface microflora and environmental bacteria Dermal glandular secretions and normal microflora may inhibit bacterial growth because of antibacterial properties Swabs can be moistened with sterile saline or transport media to minimize skin damage and maximize recovery of bacteria Optimal temperature for sample growth is 35 C/95 F Most isolates are gram-negative bacteria but gram-positive and mycobacterial infections also occur 4. Fungal cultures 24, 25 Tissue sections can be placed directly onto fungal culture media Sabouraud dextrose agar media is a good choice for most fungal isolates Culture at room temperature 5. Polymerase chain reaction (PCR) of skin swabs [26] [27] [28] [29] Consult laboratory for availability; verification of positive results; type of PCR (conventional, Taqman, real-time, and so forth); use of negative and positive controls; sample collection and swab type; and shipping details Avoid cross- 

See Table 2 for a review of common differential diagnoses for dermatologic diseases in amphibians.

Cutaneous disease is an extremely common presenting complaint to the fish veterinarian. Many owners notice abnormalities in the integumentary system as the first sign of disease in their pet fish. In addition, the skin is an extremely common target for many infectious diseases of ornamental fish. The skin of fish provides a protective barrier against infection, osmotic pressure, and injury. Disruptions of the skin can result in osmotic disturbance, disruption of internal homeostasis, morbidity, and mortality. 

The skin can be divided histologically into the cuticle, epidermis, dermis, and subcutis. The cuticle (outermost layer) is approximately 1 mm thick and contains mucus, sloughed cells, and cellular debris. It has antimicrobial properties mediated by antibodies (IgM), free fatty acids, and lysozymes. 30, 31 This layer is commonly referred to as the "slime coat" by aquarium hobbyists because of its high concentration of mucus. This layer is usually lost during routine processing for histopathology. Together with the cuticle, the epidermis produces a waterproof barrier. The epidermis is a nonkeratinizing (most species) stratified squamous epithelium that contains 3 to 20 cell layers. 30, 31 It contains many mucus-producing goblet cells and, in some species, club cells that secrete an "alarm substance" when the skin is damaged. Unlike mammals, epidermal cells are not keratinized and are capable of mitotic division in all layers; however, division most commonly occurs in cells adjacent to the basement membrane where the epidermis junctions with the dermis. 30, 31 The upper dermis contains collagen and reticulin and forms a supportive network; the deeper dermis contains more compact collagen and provides the main structural strength to the skin. 30, 31 Scales are flexible bony plates that develop in scale pockets in the dermis; they are not shed regularly. 30, 31 As scales emerge they are covered by a layer of epidermis, and often overlap one another, providing structural support and protection. Two main types (ctenoid and cycloid scales) are described that differ in surface sculpture. 30, 31 Ultrastructurally, scales contain collagen fibers interspersed with an organic matrix in which hydroxyapatite crystals are deposited. 30, 31 Some fish are scaleless and histologically have a thicker epidermis. Chromatophores (pigment cells) are present in the dermis and include melanophores; xanthophores (yellow); erythrophores (orange-red); leucophores (white); and iridophores (reflective/iridescent/silver). The pigments consist mainly of carotenoids. The subcutis contains connective tissue and fat and is highly vascular; bacterial disease can spread rapidly along this layer. 30, 31 Dermatologic Examination and Diagnostic Testing

The diagnostic approach to a fish with dermatologic disease should include a complete history, direct observation of the fish in its aquarium or pond, dermatologic examination, complete water quality, skin scrapings, and a gill biopsy. As with other species, historical evaluation is extremely important. Because infectious disease is very common in pet fish, questions pertaining to quarantine protocol, most recent fish introduction, and number of fish affected are extremely important. Husbandry-related questions (water changes, filtration, tank or pond setup, water quality testing, and so forth) are extremely important because many diseases in fish are related to poor husbandry and water quality. The owner should be questioned regarding prior treatments because many fish hobbyists attempt numerous overthe-counter remedies before consulting with a veterinarian.

Direct observation is best performed in the home aquarium or pond. Isolation is often an early indication of disease in schooling fish. Other signs that can be seen during direct observation include piping (gasping for air at the surface) and flashing (a sign of pruritus in which the fish rubs against objects in the aquarium or pond). The skin and fins can also be evaluated for abnormalities.

During the dermatologic examination, the skin, fins, and scales should be evaluated thoroughly. Some fish require sedation for this procedure. Latex gloves should be worn to protect the cuticle. Abnormalities that are commonly seen on the dermatologic examination include skin discolorations; erythema; frayed and irregular fins; erosions and ulcerations; petechial and ecchymoses; edema and raised scales; macroparasites (anchor worm, fish lice); papules and nodules; excess mucus production; scale loss; and white-to-gray irregular patches. 30 Commonly used dermatologic diagnostic tests in fish include the following:

1. Water quality evaluation a. Poor water quality is the most common cause of morbidity and mortality in pet fish b. Poor water quality is the most common underlying cause of immunosuppression and opportunistic infections in pet fish c. Parameters that should be monitored include temperature, pH, ammonia, salinity, nitrite, nitrate, dissolved oxygen, and alkalinity 3 2. Skin scrapings and gill biopsy a. Skin scrapings i. If there are lesions on the skin, a coverslip should be dragged across lesional skin in a head-to-tail direction, collecting mucus on the coverslip. The coverslip is then placed onto a slide with a drop of tank water. Some fish require sedation for this procedure. Sedation may reduce the number of ectoparasites found on skin scrapings. ii. When there are no obvious lesions on the skin, sites commonly sampled include just caudal to the pectoral fin, operculum, and the ventrum. Samples should be taken from two to three different sites; when possible, several fish should be sampled. b. Gill biopsy i. Gill is epithelial tissue and many ectoparasites affect the gills and skin. Occasionally, ectoparasites are found only on the gills. ii. Typically requires sedation iii. The operculum is lifted and a small snip of distal gill lamellae is taken (usually with iris scissors) and placed onto a slide with a drop of tank or pond water to examine. c. Skin scrapings and gill biopsies are examined under the microscope; superior results are obtained with the condenser down. Most parasites can be seen on Â4 or Â10 magnification. However, with some smaller parasites, such as Ichythobodo, and bacteria, such as Flavobacterium columnare, Â40 magnification is required. 3. Bacterial culture and sensitivity a. Tissue biopsy for culture sampling is preferred over superficial swabbing of ulcerative lesions 4. Histopathology 5. Clinical pathology (complete blood count, biochemistry panel) 6. Viral testing a. Koi herpes virus serology and PCR 7. Necropsy

See Table 3 for a review of common differential diagnoses for dermatologic diseases in fish, including Gyrodactylus and ulcerative bacterial dermatitis (Figs. 6 and 7) .

Cutaneous disease is extremely common in pet birds; assessing the skin can be difficult given the variation in species presenting to the avian practitioner. Avian Clinical Approach to Dermatologic Disease 

Avian skin is composed of an epidermis and dermis; the skin is thicker in nonfeathered areas. The layers of the epidermis include the stratum germinativum and the stratum corneum. 33 The stratum germinativum (bottom most layer) produces cells that mature to form the keratinized stratum corneum and can be divided into three distinct layers:

(1) the stratum basale, (2) the stratum intermedium, and (3) the stratum transitivum. The cells show signs of keratinization in the stratum transitivum. 33 Feathers are formed from feather follicles in the dermis. The dermis is thicker than the epidermis and contains structurally supportive collagen, blood vessels, fat, nerves and neuroreceptors, feather follicles, and associated smooth muscle. 32, 33 Avian skin is aglandular with the exception of the uropygial (or preen) glands; the pericloacal glands (secrete mucus); and the sebaceous glands of the ear canal. 32, 33 The uropygial gland is a holocrine gland found at the base of the tail that secretes a liposebaceous material important in protecting and waterproofing feathers; it is spread through the feathers in a process called preening that is also necessary for interlocking of feather barbules. 32, 33 Feathers are arranged into tracts known as pterylae that are separated by featherless areas of skin called apteria. [32] [33] [34] Table 4 illustrates the common feather types and their properties. The calamus is the part of the feather that attaches to the follicle. [32] [33] [34] The main shaft of the feather is called the rachis; where the rachis meets the calamus is a pulp cap referred to as the superior umbilicus. [32] [33] [34] There may be a smaller feather attached to the superior umbilicus that is referred to as the after feather. [32] [33] [34] Projections from the rachis are referred to as barbs, which bear projections called barbules. [32] [33] [34] Most barbules contain hooks called barbicels that hold the barbs and barbules together. [32] [33] [34] Molting occurs when the growth of a new feather in the follicle forces out the older feather; all feathers of adult birds are replaced regularly during molting. Most species of pet birds molt once to twice yearly. 32, 33 Dermatologic Examination and Diagnostic Testing A thorough history and dermatologic examination are important when evaluating any case of avian skin disease. Dermatologic examination in birds should include evaluation of feathers, skin, beak and cere, ears, legs and claws, preen gland, and cloaca. Common findings during clinical examination of birds with skin disease include feather abnormalities (broken or absent feathers, dystrophic and discolored feathers); scaling; crusting; ulceration; redness; and nodules and masses. Commonly used dermatologic diagnostic tests in pet birds include the following:

1. Feather pulp cytology 32, 33 Feather pulp cytology is collected from a freshly plucked feather and used to assess for the presence of folliculitis. The calamus can be removed from the feather and contents smeared onto a microscope slide. Possible findings include bacteria, inflammatory cells, viral inclusion bodies, and dermatophytes. 2. Gross and microscopic examination of feathers 32, 33 Evaluate for overall condition, ectoparasites, fret marks and stress bars, evidence of self-trauma 3. Feather preparation with potassium hydroxide 33 To improve mite identification, the calamus of the feather can be placed into a 10% potassium hydroxide solution, gently heated, and then centrifuged, followed by microscopic examination of the sediment 4. Acetate tape impressions Used to detect ectoparasites, yeast, and bacterial infections. Feather dander and keratinaceous debris is very abundant on these samples and in some cases can be difficult to differentiate from bacteria and yeast.

For moist, exudative, or crusted lesions, direct slide impressions are often used For drier lesions, direct impressions can be attempted but acetate tape impressions may be preferred. Alternatively, a moistened swab can be used to collect a sample and contents rolled onto a slide. 6. Skin scrapings 7. Culture and sensitivity (bacterial, fungal)

Calamus and feather plucking, sterile tissue biopsy, or superficial swabs 8. Biopsy

Avian skin is much thinner than dogs and cats. In some cases, it is easier to biopsy the skin with a scalpel compared with a punch biopsy. If a punch biopsy is to be performed, a technique has been described where acetate tape is placed over the biopsy site to maintain the structure of the skin. 35 9 . Clinical pathology evaluation including complete blood count and biochemistry panel and heavy metal testing 32, 33 Systemic diseases can cause cutaneous changes including feather picking Testing for lead and zinc levels may be needed in some cases 10. Crop washes 33 Can identify Trichomonas or Candida, which can present in birds that feather pluck over the crop area 11. Fecal examination Certain intestinal parasites may result in feather plucking 32,33 12. Intradermal allergy testing Codeine phosphate at 1:100,000 wt/vol preferred over histamine as a positive control in birds 36 Further research is needed to evaluate appropriate protocols for intradermal allergy testing in pet birds and establish correct allergen dilutions and thresholds 13. Viral testing including PCR for polyoma virus and psittacine beak and feather disease 32, 33 Common Differential Diagnoses for Cutaneous Diseases See Table 5 for a review of common differential diagnoses for dermatologic diseases in pet birds, including feather picking (Fig. 8) . Clinical Approach to Dermatologic Disease

The skin is a common site of disease in small mammals and a very common presenting complaint to the exotic animal practitioner. Parasites, bacterial infections, and husbandry-and environmental-related conditions are most commonly seen.

The basic structure and function of exotic small mammal skin is very similar to that of the dog and cat. Relevant differences are discussed. The skin is divided into a fourlayered avascular epidermis (stratum corneum, stratum granulosum, stratum spinosum, stratum basale) and the underlying, structurally supportive, collagenous, and vascular dermis. The subcutis is below the dermis and consists of connective tissue and fat. In rodents, brown fat is located between the scapulae, in the ventral neck, and in the axillary and inguinal regions; it is more prominent in smaller rodents, rabbits, and ferrets and less so in guinea pigs and chinchillas. 37 Fig. 10 . Gyropus ovalis from a guinea pig. Fig. 11 . Cystic ovarian disease resulting in symmetric noninflammatory flank alopecia. Hairs can be divided into primary (guard) hairs; secondary (undercoat) hairs; and tactile hairs. 37 The number of hairs per follicle varies with the species, breed, age, and other external factors; chinchillas have as many as 60 hairs per follicle, producing the characteristic dense soft coat. 37 The keratinized hair consists of the innermost medulla, pigmented cortex, and outermost cuticle. Primary hairs are associated with sebaceous glands, apocrine sweat glands, and an arrector pili muscle. Rodents and ferrets have no epitrichial (apocrine) sweat glands. 37 Secondary hairs are typically only accompanied by sebaceous glands. 37 The rat and mouse tail is very sparsely haired. In interfollicular regions, there is surface parakeratosis and no stratum granulosum, whereas follicular ostia contain the typical orthokeratosis and stratum granulosum; these changes give the tail its characteristic scaly appearance. 37 The footpads are areas of specialized thickened epidermis with underlying shockabsorbing fat deposits. Atrichial (eccrine) sweat glands are located only in the footpad. Rabbits lack foot pads, but instead have coarse fur on their distal limbs. Sebaceous scent glands are a common feature in many small mammal species and are important in scent marking and communication. Hamsters have large darkly pigmented glands on their flanks, more prominent in males. 37 Gerbils have large oval-shaped yellowish hairless scent glands on the ventrum. 37 Guinea pigs have a large gland over the rump that can secrete an oily substance, especially in boars. 37 Rabbits have sebaceous scent glands on the chin (mental gland) that is used for territorial marking, anal glands, and androgen-dependent inguinal scent glands. 37 Ferrets have active sebaceous glands throughout their skin that results in their typical musky odor and greasy coat; they also have two prominent perianal scent glands. 37 As with other exotic species, a thorough questioning and evaluation of the husbandry is critical for successful diagnosis and treatment of small mammal dermatoses. Important questions include those pertaining to the environment and husbandry (type of housing, indoor or outdoor, substrate or bedding, diet, and so forth), and more targeted questions pertaining to skin disease. In small mammals, it is important to know whether the condition is pruritic and whether any other animals are affected.

A thorough dermatologic examination is necessary in all patients with skin disease. Common lesions include hairloss, erythema, scaling, crusting, excoriations, erosions, and ulcers. Restraint to obtain quality diagnostic samples from small mammal skin can be challenging in some cases, so anesthesia or sedation may be needed.

Commonly used dermatologic diagnostic tests in small mammals include the following:

For moist, exudative, or crusted lesions, direct slide impressions are often used 

For drier lesions, direct impressions can be attempted but acetate tape impressions may be preferred. Alternatively, a moistened swab can be used to collect a sample and contents rolled onto a slide. 2. Skin scrapings a. Very useful for detection of ectoparasites b. Given the thin skin of many exotic patients, some practitioners prefer to use scraping spatulas to perform skin scrapings 3. Bacterial culture and sensitivity 4. Fungal culture 5. Wood lamp a. Limited usefulness in small mammals given that Trichophyton mentagrophytes is the most common dermatophyte isolate in clinical cases 6. Trichogram a. Useful to evaluate hair structure b. Evaluation for broken or fractured hair ends that would help determine whether hair loss is traumatic. Evaluate for ectoparasites. c. Evaluation for evidence of dermatophytosis (fungal hyphae/ectothrix spores) 7. Acetate tape impression a. Useful for collection of surface-dwelling mites, such as Cheyletiella and Myobia 8. Skin biopsies for histopathology 9. Clinical pathology testing including complete blood count and biochemistry panel 10. Testing for adrenal disease in ferrets

See Table 6 for a review of common differential diagnoses for dermatologic diseases in rabbits, including Cheyletiella parasitivorax (Fig. 9) . See Table 7 for a review of common differential diagnoses for dermatologic diseases in guinea pigs, including Gyropus ovalis and noninflammatory flank alopecia (Figs. 10 and 11 ). See Table 8 for a review of common differential diagnoses for dermatologic diseases in gerbils and hamsters, including demodicosis, (Demodex aurati and Demodex criceti, [Fig. 12] ). See Table 9 for a review of common differential diagnoses for dermatologic diseases in mice and rats, including Myobia musculi and Polyplax spinulosa (Figs. 13 and 14) . See Table 10 for a review of common differential diagnoses for dermatologic diseases Fig. 15 . Alopecia in a ferret with hyperadrenocorticism. in ferrets, including alopecia (Fig. 15 ). See Table 11 for a review of common differential diagnoses for dermatologic diseases in chinchillas.

Skin disease is an extremely common presenting complaint to the exotic animal practitioner. These cases may be challenging because dermatologic diseases are often multifactorial and many have underlying husbandry or environmental deficiencies that must be identified. A thorough diagnostic evaluation is critical for successful management of exotic animal cutaneous disease.

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