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Llama Dermatology
Llama Medicine
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Llama Dermatology Rod A. W. Rosychuk, DVM*
Very little information concerning llama dermatology is available in the veterinary literature. Whereas most existing published data are related to ectoparasitism, we now recognize that the llama is susceptible to a wide variety of other dermatopathies. We only have begun to describe various clinical syndromes and hastily would point out that the etiologies and pathogenesis for many of these skin diseases remain speculative and their therapies somewhat empiric. A major goal of this article is to share our early experiences with various llama dermatopathies in the hope it will provide a stimulus for further studies.
GROSS ANATOMY AND PHYSIOLOGY Although llama fiber commonly is referred to as wool or fleece, it is unlike true wool fiber, which is fine, tightly crimped and usually nonmedullated. Llama fiber properly is defined as hair. 25 Llamas generally have two types of hair fiber. Primary or guard hairs usually are long (5 to 30 cm), straight, and account for approximately 20 per cent of the coat.24 They range in diameter from 10 to 150 microns and the majority are medullated. They likely contribute most to the prevention of mechanical injury to the skin and the shedding of water. Secondary or undercoat hairs are short, crimped, and range in diameter from 10 to 40 microns. Most secondary hairs also are medullated. 15.24 The undercoat is suggested to contribute primarily to the insulating qualities of the coat. 25 The overall texture of the llama coat varies from very soft to coarse, and the contrast between guard hair and undercoat may be pronounced or subtle. Llamas occasionally are subdivided into either long-haired (lanuda) or short-haired (pelada) types. In both, the face itself usually is covered with very short hairs. The long-haired types generally have a long, thick coat that may cover the entire head, neck, *Diplomate, American College of Veterinary Internal Medicine; Assistant Professor, Department of Clinical Sciences, Colorado State UniverSity College of Veterinary Medicine, Fort Collins, Colorado
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and body. The short-haired types generally have much less hair, which is most obvious over the head, neck, and distal extremities. 25 Partial shedding of primarily the undercoat occurs each year but is most noticeable every second year. The shedding process produces a thin spot or "break" in the retained hair unless the animal is shorn each year. 24 Hair fiber quality is noted to decrease after about 10 years of age. 25 Hair fiber characteristics apparently are highly heritable and comparatively easy to breed for. Llama breeders who have selected for a longer, more uniform fleece with longer secondary hairs, have found that these animals do not shed out normally except perhaps at the neck, where the guard hairs and undercoat remain very distinguishable. 25 The rate and quality of fiber production likely are affected by changes in environmental temperature, moisture, and light exposure. 25 Vegetable matter, including foxtails, other weed seeds, hay, dirt, and dust frequently are found within the coat - a testament to the llama's desire to roll on the ground and take "dirt baths." Basic recommendations given to optimize coat condition include the feeding of higher protein diets, the provision of readily available sulfur blocks, the inclusion of adequate copper and zinc in the diet, and the avoidance of sudden dietary changes (Johnson L, personal communication, 1988). Stress should be minimized. Llamas ideally should be groomed regularly, but not excessively. Attempts also should be made to minimize contamination of the coat with excessive vegetable debris and, especially, plastic baling twine fibers. Skin thickness varies considerably, being thickest over the dorsal cervical area (where it may be in excess of 10 mm) and the ventral cervical and dorsal thoracic regions. This increased thickness primarily is caused by the presence of larger amounts of dense collagen within the dermis. Skin over the dorsal lumbar, ventral abdominal, axillary, inguinal, medial, and caudal thigh regions comparatively is quite thin (approximately 2 to 3 mm). An alopecic, hyperpigmented, thick callus-like plate of varying sizes normally is present over the ventral thoracic region and likely serves a protective function. Alopecic, thickened, hyperkeratotic, hyperpigmented callus-like areas also are found over the anterior aspect of the carpi and, occasionally, over the anterolateral aspect of the stifles. Linear, alopecic, hyperkeratotic areas also are located on each side of the metatarsal bone. These structures likely represent vestigial metatarsal bones much like the chestnuts found on the inside of front and rear limbs of the horse. A linear line of marked hyperkeratosis also is found extending down the length of the dorsal interdigital spaces on all four feet. Although it has been suggested that this may represent a glandular area, important in territorial marking, histologic examination of the region has failed to reveal such glandular material. The purpose of this structure, if any, is unknown. The thick foot pad essentially is comparable to that of most carnivores. There are only two digits, each with its own toenail. These nails normally grow constantly and with normal exercise usually will wear even with the foot pad. Toenails allowed to grow excessively will result
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in toe curling, which often is difficult, if not impossible, to resolve. Where adequate wearing of the nail is not possible, regular trimming is indicated. There are some crooked toes that appear to be a heritable trait (Johnson L, personal communication, 1988).
MICROSCOPIC ANATOMY AND PHYSIOLOGY The epidermis of the llama varies in thickness from two to four cells in heavily haired areas (cervical, dorsal, and lateral thorax) to three to five cells in less densely haired areas (axillae, inguinal regions, medial and caudal thighs, perineum). A mild degree of orthokeratotic hyperkeratosis appears to be quite normal and especially is evident over the dorsal cervical, thoracic, and lumbar regions. The histological appearance of the callus-like areas over the ventral thorax, anterior carpi, and lateral stifles; the alopecic hyperkeratotic areas over the metatarsal bones; and the hyperkeratotic areas in the interdigital spaces all are similar. Orthokeratotic hyperkeratosis is marked. There is marked epidermal hyperplasia and rete ridge formation. Sebaceous and apocrine glands are found in variable numbers but generally are very small and sparse in areas that are heavily haired (entire cervical region, dorsal thoracic and lumbar regions, lateral thorax) and quite large and numerous in the lightly haired regions (axillae, inguinal regions, medial and caudolateral thighs). Very large aggregates of sebaceous glands are noted in the perineal and perianal regions. Llamas are known to sweat significantly in association with exposure to increased ambient temperatures 1 ,8 and following the intravenous administration of adrenalin. 1 The major sites for effective water vapor loss appear to be over the ventral, relatively hairless areas of the body where apocrine glands are most numerous and evaporative cooling can occur more readily. Perhaps the most unique species variation noted to occur within normal llama skin is the presence of a very prominent vascular plexus in the superficial dermis. This vascular plexus occasionally is so extensive it becomes the predominant structure in the superficial dermis. Similar vascular structures also are present in the alpaca and have been described in the guanaco. 3 Their function is unknown but may be related to thermal regulation. 3 Vessel walls in these vascular plexi frequently are thick and surrounded by slightly increased numbers of lymphocytes and macrophages. Small numbers of eosinophils also may be present. To the uninitiated, these findings often are interpreted as representing mild chronic inflammatory changes, but apparently this number of perivascular cells is quite normal in the llama. They have been present in the skin biopsies of all the normal llamas we have looked at to date. When interpreting llama skin biopsies, it is important to recall that mild orthokeratotic hyperkeratosis, a prominent superficial dermal vascular plexus, and mild perivascular accumulation of inflammatory cells
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likely are normal. When interpreting the size and numbers of sebaceous glands (for example, especially when assessing the presence of a possible endocrinopathy), the region from which the biopsy has been taken also must be taken into consideration.
SELECTED LLAMA SKIN DISEASES Ectoparasites
Sarcoptic Mange. Sarcoptic mange or "sarna," as it is called in South America, is caused by Sacroptes scabii, var. auchenidae, and has been well described in the camilidae, (llama, alpaca, vicuna, and guanaco I3 ). Although sarcoptic mange once was quite common in North American llamas, its incidence appears to be decreasing significantly, perhaps because of the routine practice of worming with ivermectin, a therapy of choice for this form of mange. The scabies mite spends its entire life on the host, burrowing within the epidermis of the skin. The life cycle (from egg to adult) is completed in about 7 to 14 days.9 Under ideal conditions, the mite can survive off the host for only a few days.23 The presence of the mite provokes an inflammatory response that initially produces a papular dermatitis. Many of the more obvious cutaneous changes, such as crusting, thickening, and hyperpigmentation, however, are a product of the moderate to severe pruritus that is characteristic of the disease. Sarcoptic mange is communicable readily to other llamas, with transmission occurring primarily through direct contact, the use of communal dusting areas, or contact with fomites such as bedding, grooming tools, and clothing. 23 It is interesting to note that some llamas appear to be quite resistant to infestation. 14 Although communicability to other species is uncommon, transmission to sheep, horses, and humans has been reported. 2,17 The disease has been suggested to be most active in cold, wet weather and more dormant in summer. 23 Affected llamas initially develop a pruritic, papular, erythematous dermatitis over the inguinal, axillary, ventral abdominal, perineal, and distal extremity areas. Affected regions gradually become alopecic, crusted, thickened, and hyperpigmented. The problem can become more generalized, involving the dorsal and lateral abdomen and thorax and facial regions. Lesions in the more heavily haired regions may appear as heavy scaling. Severely affected individuals have been known to die, likely because of secondary bacterial infections and general debilitation. 14 Differential diagnoses include chorioptic mange, an irritant dermatitis associated with lying on abrasive surfaces (for example, alfalfa stems) in damp cold weather, idiopathic hyperkeratosis (zinc-responsive dermatoses), and inhalant or food allergies. Diagnosis is based on skin scrapings. Scrapings should be deep, retrieving large amounts of debris. Mites and mite· eggs usually are present in large numbers. Material from the scraping may be placed on
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a slide and covered with 10 per cent KOH to "clear" the hairs and facilitate observation of the mites. The clearing process generally takes 10 to 20 minutes at room temperature. On occasion, scrapings may be negative even in the severely affected individual. 23 When sarcoptic mange is suspected but mites are not found, the diagnosis is confirmed by assessing response to trial treatment. Skin biopsies show variable degrees of epidermal hyperplasia, hyperkeratosis, and subacute and chronic inflammatory changes in the dermis. Eosinophils usually are present in large numbers. Mites may be seen. Many therapies for sarcoptic mange in the camilidae have been reviewed. 2,9,14,23 Most recently, the therapy of choice is the ivermectin formulated for bovine use (Ivomec-AGVET, Merck, Sharp, & Dohme, Rahway, NJ) 0.2 mg per kg given subcutaneously and repeated in 10 to 14 days. Parenteral administration appears to be more effective than oral dosing. Pruritus should be reduced significantly within 10 days and there should be good evidence of hair regrowth within 30 days.14 A lack of response to this therapy likely would rule out a diagnosis of sarcoptic mange. The author's alternative therapy of choice is 2 to 3 per cent lime sulfur applied as a spray or dip once weekly for 4 weeks. Lime sulfur will discolor light coats. Affected animals ideally should be isolated and treated into remission. Especially with tenacious or recurrent problems or where isolation of affected individuals is not possible, all in-contact animals should be treated. Chorioptic Mange. The history and physical findings associated with Chorioptes bovis infestations in the llama and alpaca are similar to those described for sarcoptic mange lO but chorioptic mange is encountered less commonly. Pruritic lesions generally are found over the distal extremities, ventrum, and base of the tail. Pruritus, however, is less severe than with sarcoptic mange and, indeed, may be quite mild. Mention has been made of a Chorioptes-infested young llama who initially was presented for head shaking. 4 It has been suggested that chorioptic mange may not be as responsive to ivermectin therapy as sarcoptic mange because the chorioptic mite lives on the surface of the skin and does not burrow into the epidermis. For this reason, the lack of response to a trial ivermectin therapy should not rule out this form of mange. Differential diagnoses are as for sarcoptic mange. Diagnosis is made by skin scrapings (mites generally are found readily) and response to therapy. Although ivermectin formulated for bovine use (Ivomec-AGVET, 0.2 mg/kg subcutaneously and repeated in 2 weeks) occasionally may be effective, our therapy of choice at this time has been 2 to 3 per cent lime sulfur dips or sprays applied once weekly for 4 weeks. Crotoxyphos {0.25 per cent applied as a total body dip or spray at least twice at 10 to 14 day intervals apparently has been effective in the cow, goat, sheep, and horse. 22 The author, however, has no experience with this medication in camelids. Pediculosis. Louse infestations are quite common in llamas. Both biting louse (Damalinia breviceps) and sucking louse (Microthoreis cameli) infestations are noted, 5 with biting lice being most common.
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Mixed infestations occasionally are encountered. Clinically significant louse infestations are most common during the winter. Louse infestations usually are pruritic, which often results in patchy hair loss. The coat often becomes dry and scaly and the llama may appear unthrifty. Lice generally are found in heavily wooled areas. Differential diagnoses would include sarcoptic and chorioptic mange, allergies, and dermatophytosis. Diagnosis is based on history, physical examination, and the demonstration of lice. Highest concentrations of lice are reported to be found along the dorsal midline and the sides and dorsum of the tailhead region. 6 The lice, which are about 2 mm in length, are seen best by parting the hairs and directly examining the skin. The mites themselves may look like pieces of scale. The type of louse infestation (biting versus sucking) ideally should be determined using a hand magnifying lens because this may help determine the therapy to be used. Treatment recommendations include powdering with a 50 per cent wettable powder of methoxychlor (Morlate) or a 5 per cent carbaryl dust (Sevin). 6 The wool should be parted, then dusted down to the skin; "move an inch or so away and repeat the operation until the heavily wooled areas are covered thoroughly."7 I vermectin therapy has been suggested to be effective against sucking lice, but not biting lice. 6 The ivermectin formulated for bovine use is given and repeated in 10 to 14 days (0.2 mg per kg IvomecAGVET subcutaneously). All in-contact animals should be treated. Other therapies noted to be effective include fenthion (Tiguvon, Bayvet Div. of Cutter Labs., Shawnee, KS) pour-on (use swine dilution; do not use Spotton) and Ectrin spray (Johnson L, personal communication, 1988). Prevention should involve the treatment of all new llamas brought into the environment. Environmental therapy using products like the Ectrin spray also may be indicated in refractory or recurrent cases. Demodicosis Demodicosis appears to be rare in camelids. Its clinical presentation appears similar to that observed in cattle and goats. 18 Singular or multiple asymptomatic papules or nodules are noted, especially over the face, neck, and brisket area. Exudation and crusting may be seen, especially when lesions are infected secondarily. Differential diagnoses include bacterial folliculitis, dermatophilosis, and dermatophytosis. Diagnosis is based on history, physical findings, skin scrapings, and skin biopsy. Papular lesions should be squeezed and then scraped deeply. Nodular lesions should be incised and the caseous contents examined microscopically. Mites will be present in large numbers. Skin biopsies will show markedly dilated follicles filled with demodectic mange mites and variable degrees of associated perifolliculitis, folliculitis, furunculosis, and/or pyogranulomatous inflammation. Therapy, if necessary, simply may involve manual expression of the lesion followed by infusion of Lugol's iodine. Other therapies to be considered include infusion of rotenone in alcohol (1: 3) as used in goats 18 or the generalized total body therapies reportedly used in
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goats, cattle, and sheep.Is Although the author has no experience with ivermectin therapy for this disease in llamas, its failure in the treatment of demodicosis in other species would suggest that it likely will not be effective. Infectious Dermatoses
Bacterial Folliculitis and Furunculosis. Bacterial skin infections generally have been presented as variable pruritic (most commonly nonpruritic) focal asymmetrical areas of hair loss, crusting, and exudation. They primarily have been noted over the head and/or distal extremities. Differential diagnoses include sarcoptic/chorioptic mange, dermatophytosis, dermatophilosis, and idiopathic hyperkeratosis (zincresponsive dermatosis). Diagnosis is based on skin biopsy and response to therapy. Skin biopsies show variable degrees of folliculitis, perifolliculitis, and furunculosis. InHammatory cell accumulations consist of admixtures of neutrophils, lymphocytes, macrophages, and eosinophils. An epidermitis and/ or diffuse accumulation of inHammatory cells within the dermis may be present. To date, limited cultures have been done from affected individuals. Staphylococcus intermedius has been retrieved most consistently from lesions. For more focal lesions, therapy has involved clipping, cleansing, and the topical application of antibacterial preparations (for example, iodophors). More generalized involvement may require systemic therapy. Empirically, penicillin (22,000 IU per kg subcutaneously twice daily for 7 to 10 days) or trimethoprim-sulfadiazine (10 mg per kg of combined product diluted to 12 per cent and given subcutaneously twice daily) has worked well. Otherwise, parenteral antibiotics should be chosen on the basis of culture and sensitivity testing. Dermatophilosis. Dermatophilosis caused by Dermatophilus congolensis is noted to occur in the llama. It most commonly is seen in warm, moist climates during the rainy season. Lesions most frequently are seen over the back, sides, and distal extremities. Maceration and skin irritation associated with the accumulation of vegetable material in the dense coat likely predispose animals to the truncal lesions. Lesions usually are not painful but may be pruritic, and consist of heavy exudate mixed with matted hairs. Peeling the hairs and crust away usually leaves an erosion covered with purulent debris. Differential diagnoses include dermatophytosis and bacterial folliculitis and furunculosis. Diagnosis is based on direct smears of purulent material or saline-soaked and broken up crusts, which may be stained with Diff-Quik, new methylene blue, or Gram's stain. Dermatophilus congolensis also may grow well on blood agar. I9 The author has no personal experience with skin biopsies from affected llamas but would assume they would be similar to those described in other species. I9 Therapy would include clipping and cleansing, followed by the use of topical disinfectants (such as iodophors, 2 to 5 per cent lime sulfur or 0.5 per cent zinc sulfate) applied once daily for 3 to 5 days and then weekly until healing has occurred. I9 Unfortunately, all of these products may stain the hair. Although the author has no personal experience
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with systemic therapy, a combination of penicillin and streptomycin as used in cattle, sheep, and goats (5,000 IU per kg procaine penicillin G and 5 mg per kg streptomycin daily for 4 days)19 could be tried. Affected individuals should be moved to dry, clean environments. Dennatophytosis. Dermatophytosis or ringworm in llamas, in our clinic, has been associated most commonly with Trichophyton verrucosum, Microsporum nanum, and Microsporum gypseum. Dermatophytosis appears to be more common in confined animals, especially during the winter months. Skin lesions consist of variable-sized focal areas of hair loss and crusting. Lesions have been noted most commonly over the distal extremities, face, and perineum. They are variably pruritic. Differential diagnoses include bacterial folliculitis and furunculosis, dermatophilosis, and idiopathic hyperkeratosis (zinc-responsive dermatosis). Diagnosis is based on KOH preparations, fungal culture, and skin biopsy. KOH preparations, in our hands, rarely are positive. Our experience with skin biopsies is limited but findings have included orthokeratotic hyperkeratosis, folliculitis, perifolliculitis, a perivascular dermatitis, and diffuse accumulations of mononuclear inflammatory cells within the dermis. Fungal organisms are seen only occasionally on H & E or with special stains. Therapy usually begins with clipping affected areas (where possible) and discarding the hairs. Topical therapy may include iodophors, 2 to 3 per cent lime sulfur, 3 per cent captan, or 0.5 per cent sodium hypochloride. 20 For very focal lesions, anyone of these therapies can be applied to the region once or twice daily until the lesions are resolved. For more generalized problems, the author's topical therapy of choice is 3 per cent captan applied once daily for 5 days, then twice weekly until the lesions resolve. The author has no experience with systemic griseofulvin therapy in the llama. Its expense and questionable efficacy in other large animal species make its use controversial. If it were to be considered, a dosage regimen similar to that used in sheep and goats (10 mg per kg per day per orally) would seem appropriate. 2o Adjunctive therapies include maintenance of good nutrition and the provision of a clean, dry, and sunny environment. Coccidioidomycosis (Valley Fever). Coccidioidomycosis has been described in new-world camelids that reside or have spent time in the Southwestern United States where coccidiodes is endemic. The causative organism, Coccidioides immitis, usually is inhaled. Clinical signs depend on the organ system involved (for example, respiratory, central nervous system). A cutaneous form of the disease has been described in association with systemic involvement and also may be present as the only apparent site of involvement. 11 Skin lesions are papular, plaquelike, or nodular. They may be exudative and crusty. Lesions are found most commonly over the perineum, face, and limbs. 11 Differential diagnoses include dermatophilosis, dermatophytosis, and idiopathic hyperkeratosis (zinc-responsive dermatosis). Diagnosis of the cutaneous form of the disease is based on history, physical findings, cytological examination of exudate from the lesions, or skin biopsy. Cytological examination is performed best by examining cuta-
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neous exudates in a wet mount of 10 per cent potassium hydroxide under subdued microscopic lighting. The highly refractile doublewalled spherules that contain endospores are typical. Histological examination of tissues also may show the characteristic spherules. There apparently is no successful therapy for coccidiodomycosis in llamas at this time. Contagious Viral Pustular Dennatitis. Contagious viral pustular dermatitis, also known as contagious ecthyma, sore mouth, or orf has been recognized in camelids 12,16 and, specifically, in the llama (Johnson L, personal communication, 1988). This contagious disease is caused by a papovavirus in sheep and goats and likely is transmitted to camelids via contact. Lesions usually are noted at the mucocutaneous junctions and are raised, alopecic, often erythematous, and, frequently, painful. The disease usually resolves spontaneously within 10 to 14 days. Allergies
Steroid-responsive Pruritic Dennatoses of Suspect Allergic Origin. The author has seen and consulted on a number of llamas whose skin disease was characterized by generalized pruritus without significant skin lesions, or with variable degrees of hair loss, and dermatitis induced by self trauma. There appears to be no sex or age predilection, although younger animals (1 to 3 years) appear to be affected more commonly. The problem may be either seasonal or nonseasonal. The primary differential diagnoses usually have included sarcoptic and chorioptic mange, pediculosis, and dermatophytosis. Skin scrapings, fungal cultures, and fecal examinations have been negative. There has been- no response to insecticide therapy. Skin biopsies have shown minimal changes. They have included orthokeratotic hyperkeratosis with variable degrees of a mononuclear perivascular dermatitis. Eosinophils often have been present in slightly increased numbers. Response to systemic steroids has been prompt. Based on experience with similar syndromes in other species, this pattern of disease would suggest the presence of an allergic disorder. Seasonal problems (for example, summer) might suggest inhalant allergies, perhaps to environmental pollens or molds. Nonseasonal problems may suggest allergies to dust and/or molds or foods. To date, trial food restriction (for example, discontinuation of supplements, use of one hay source at a time) to assess possible food allergies and intradermal skin testing to evaluate for inhalant allergies have not been employed for diagnostic purposes. Problem cases have been treated with oral prednisone, 0.5 to 1 mg per kg per day initially, gradually decreasing to the lowest every-other-day dose required to control the symptomatology. Alopecic Disorders
Alopecia Affecting the Bridge of the Nose. A focal alopecia noted primarily over the mid-dorsal region of the bridge of the nose is noted quite commonly in the llama. Skin in affected areas may be normal or variably scaly, hyperpigmented, and thickened. Black-pigmented indi-
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viduals may be predisposed. This alopecia most frequently is self-induced by rubbing the nose area. Although this simply may be a vice in some individuals, it usually is most prominent during the warmer summer months and may be a response to fly irritation. Differential diagnoses include dermatophytosis and idiopathic hyperkeratosis (zinc-responsive dermatosis). Skin biopsies reveal only mild epidermal hyperplasia and orthokeratotic hyperkeratosis. There usually are minimal to no inflammatory changes. Therapy usually is not required, although if flies are incriminated in the pathogenesis, fly repellants should be considered. Idiopathic Cervical Alopecia. An acquired alopecia involving primarily the undercoat has been noted to occur in the cervical/shoulder regions of llamas. Age of onset usually is about 24 months, although this syndrome has been reported to develop in animals as old as 6 to 8 years. There is no apparent sex predilection; both neutered and intact males have been affected. Diet and management practices do not appear to playa role. The alopecia is nonpruritic and unassociated with other skin changes. Affected individuals otherwise are normal systemically. The alopecia generally begins in the spring. Although regrowth often occurs, it may take as long as 6 months to see first evidence of this and affected areas usually do not return to full coat. Diagnostics to date have included skin scrapings, fungal cultures, and skin biopsies but they have failed to reveal a cause for the problem. Skin biopsies have not shown evidence to support the presence of an endocrinopathy. Breeders have commented that certain of their llamas may develop the hair loss every 2 years. Others believe that this is an inherited trait. At present, we are considering this a normal, genetically determined shedding pattern. Epithelial Neoplasia
Papillomatosis. Papillomas or warts are noted to occur in llamas. They are raised, usually verrucus, lesions that are found singly or on a random distribution over the less haired areas of the body (face, legs, perineum, and brisket). As in other species, llama papillomas likely are caused by a papovavirus and probably can be transmitted by direct contact or fomite contact. Diagnosis is by history, physical examination, and skin biopsy. Skin biopsies have been characterized by both epithelial and dermal fibrous tissue proliferation. Papillomas in llamas usually resolve spontaneously, but this process may take several months. Idiopathic Dermatoses
Idiopathic Hyperkeratosis (Zinc-responsive Dennatosis). Idiopathic hyperkeratosis is an apparently common skin disorder of llamas. It usually is recognized first in 1 to 2 year old llamas but age of onset is variable. Both sexes may be affected, although males appear to be somewhat over-represented. Only one or a few individuals in a herd may be affected. The disease has developed in spite of the fact that dietary zinc concentrations appear to be adequate. Lesions are noted
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most commonly over the ventral abdomen, inguinal region, medial thighs, and axilla. They initially are papular, progressing to raised alopecic plaques with a dry adherent scale. Larger areas of involvement often give the skin a diffusely thickened appearance and feel. The lesions usually do not appear inflammatory. As the disease progresses, there may be involvement of the face (especially bridge of the nose) and distal extremities. These lesions usually are asymptomatic (nonpruritic) although, on occasion, mild pruritus may be noted. They do not appear to resolve spontaneously. There is no systemic symptomatology. Differential diagnoses include sarcoptic and chorioptic mange, dermatophytosis, and dermatophilosis. Diagnosis is made by history, physical examination, and skin biopsies. Skin biopsies show a marked epithelial and follicular orthokeratotic hyperkeratosis. A mild to moderate perivascular dermatitis, characterized by increases in lymphocytes, macrophages, and eosinophils, may be seen. Quite empirically, this problem has been treated most successfully with oral zinc supplementation. Daily zinc therapy (for example 1 g zinc sulfate or 0.5 g zinc oxide per day) generally is necessary to achieve and maintain remission. Because dietary calcium is noted to potentially bind zinc and prevent its absorption from the gastrointestinal tract, some recommend minimizing calcium supplementation and discontinuing the use of alfalfa hay. The use of an organic complex of zinc in the form of zinc methionine theoretically may be a more benencial supplement because of its more effective absorption, independent of calcium content of the diet. Improvement in the skin lesions usually occurs gradually over 2 to 3 months. Daily maintenance therapy is required to maintain remission. At present, it is not known whether this syndrome represents a true zinc denciency. It, instead, may be a keratinizing disorder that is benented by superphysiologic systemic zinc concentrations, wherein the zinc is helping to normalize keratinization or reduce inflammation. Although the histological nndings in this syndrome do not include the parakeratotic hyperkeratosis usually associated with zinc-responsive dermatoses, others have noted that zinc-responsive dermatoses in some cattle, sheep, and goats may show only orthokeratotic hyperkeratosis. 21 Others also have recognized zinc-responsive dermatoses to occur in sheep and goats where the condition has not been associated with dietary denciency and affected individuals have required constant therapy to maintain remission. 21 To date, no good data exist on serum or hair zinc concentrations in affected llamas, although, in other species, it is noted that these concentrations are not sufficiently accurate to be of general diagnostic value. 21 SUMMARY
As llamas become more common in North America, veterinarians will be called on ever more frequently to deal with their dermatologic
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problems. Adherence to the basic tenets of the thorough dermatologic work up, including history, physical examination, skin scrapings, cytological examinations, fungal culture, skin biopsies, and assessing response to judiciously chosen trial therapies will offer the best opportunity of arriving at proper diagnoses. Special attention must be paid to the fact that llama skin bears some histological differences that may prove confusing to the uninitiated. A mild degree of hyperkeratosis, a prominent vascular plexus in the superficial dermis that is associated with mild perivascular mononuclear cell accumulations, and regional differences in sebaceous gland size and numbers, all are considered normal findings. Ectoparasites, including sarcoptic mange, chorioptic mange, and pediculosis, appear to be the most common causes of pruritus in the llama. Although ivermectin therapy would appear to be very effective for the treatment of scabies and, indeed, may work well against sucking lice, chorioptic mange and biting lice usually do not respond to this medication. Corticosteroids can be used to treat pruritus in the llama nonspecifically, using the anti-inflammatory dosages established in other species. These drugs are used most appropriately for the management of the allergies that we suspect occur in this species, until better alternative therapies can be developed. Variably pruritic focal areas of alopecia, exudation, and crusting suggest differential diagnoses including bacterial folliculitis and furunculosis, dermatophilosis, dermatophytosis, and coccidiomycosis. The diagnosis of bacterial problems often is made by assessing response to antibiotic therapy. Topical disinfectants and/or systemic penicillin or trimethoprim-sulfadiazine are indicated. Dermatophilosis is treated by cleaning and drying the leasions, applying topical antibiotics, and, occasionally, using parenteral penicillin and streptomycin. Dermatophytosis usually is treated with topical antibiotics only. Captan is one of several therapies of choice. There is no therapy presently available for coccidioidomycosis in the llama. Perhaps most perplexing is the fact that one of the most common dermatopathies seen in the llama is an idiopathic keratinizing disorder that, in some cases, is responsive to zinc supplementation. We have no real idea of the pathogenesis of this problem and recognize that some affected animals will not respond to supplementation. Questions regarding this disease and several others that we are beginning to recognize emphasize the fact that we have only begun to scratch the surface in llama dermatology - the bulk of our work lies ahead.
REFERENCES 1. Allen TE, Bligh TE: A comparative study of the temporal patterns of cutaneous water vapor loss from some domesticated mammals with epitrichial sweat glands. Comp Biochem Physiol 31:347 -363, 1969 2. Alvarado J, Astrom RG: An investigation into remedies of sarna (sarcoptic mange) of alpacas in Peru. Expl Agric 2:245-254, 1966
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3. Everts W: Comparative functional anatomical study of the skin of several South American mammals (En Alemain). Z Wiss Zool 185:319-360, 1973 4. Fowler ME: Llama care questions and answers. 3L-Llama 22:7, 1979 5. Fowler ME: Llama medicine. In Workshop Proceedings. Santa Cruz, California, 1984, pp 77 -96 6. Fowler ME: Llama care-questions and answers. 3-L Llama 24:11-12,50,1984 7. Fowler ME: Llama care-questions and answers. 3-L Llama 27:46, 1985 8. Fowler ME: Thermal stress in llamas. 3-L Llama, May/June: 17 -20, 1985 9. Fowler ME: Parasitic diseases of camelids. In Fowler ME (ed): Zoo and Wild Animal Medicine. Philadelphia, WB Saunders, 1986, pp 974 10. Fowler ME: Llama care. Llama 2:12, 1988 11. Fowler ME: Medicine and Surgery of South American Camelids. Ames, Iowa State University Press, 1989, in press 12. Hartwig J: Contagious ecthyma of sheep. Tierarztliche Praxis 8:435-438, 1989 13. Kraft H: Considerations of sarcoptic mange in camelids. Betrachtungen zur Sacroptesraude der Cameliden BMIW 69:365 - 366, 1956 14. Kress PJ: Use of ivermectin for treatment of scabies in llamas. Llama World 3: 18-19, 1983 15. Langley KD, Kennedy RA Jr: The identification of specialty fibers (mohair, cashmere, camel hair, alpaca, and angora rabbit). Textile Res J 51:703-709, 1981 16. McConnell T: Basic llama tips worth knowing. 3L-Llama 26:48, 52, 1985 17. Mellanby K: Sarcoptic mange in the alpaca. Transactions of the Royal SOciety Tropical Medicine and Hygiene 40:359, 1946 18. Scott DW: Large Animal Dermatology. Philadelphia, WB Saunders, 1988, pp 226-230 19. Scott DW: Large Animal Dermatology. Philadelphia, WB Saunders, 1988, pp 144-146 20. Scott DW: Large Animal Dermatology. Philadelphia, WB Saunders, 1988, pp 179-182 21. Scott DW: Large Animal Dermatology. Philadelphia, WB Saunders, 1988, pp 365-367 22. Scott DW: Large Animal Dermatology. Philadelphia, WB Saunders, 1988, p 225 23. Sharpnack E: Sarcoptic mange in llamas. Llama World, Spring:18, 1982 24. Torrey S: Llama wool. The Llama Newsletter 2:1-5, 1981 25. Walker LB: Breeding and selling of wool to use. Part 1: Wool Series. Llama 1: 57 -61, 1987 26. Young E: Chorioptic mange in the alpaca. Lama pacos. S Afr Vet Med Assoc J 37:475,1966 Department of Clinical Sciences Colorado State University College of Veterinary Medicine Fort Collins, CO 80523
0749-0720/89 $0.00
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Llama Dermatology Rod A. W. Rosychuk, DVM*
Very little information concerning llama dermatology is available in the veterinary literature. Whereas most existing published data are related to ectoparasitism, we now recognize that the llama is susceptible to a wide variety of other dermatopathies. We only have begun to describe various clinical syndromes and hastily would point out that the etiologies and pathogenesis for many of these skin diseases remain speculative and their therapies somewhat empiric. A major goal of this article is to share our early experiences with various llama dermatopathies in the hope it will provide a stimulus for further studies.
GROSS ANATOMY AND PHYSIOLOGY Although llama fiber commonly is referred to as wool or fleece, it is unlike true wool fiber, which is fine, tightly crimped and usually nonmedullated. Llama fiber properly is defined as hair. 25 Llamas generally have two types of hair fiber. Primary or guard hairs usually are long (5 to 30 cm), straight, and account for approximately 20 per cent of the coat.24 They range in diameter from 10 to 150 microns and the majority are medullated. They likely contribute most to the prevention of mechanical injury to the skin and the shedding of water. Secondary or undercoat hairs are short, crimped, and range in diameter from 10 to 40 microns. Most secondary hairs also are medullated. 15.24 The undercoat is suggested to contribute primarily to the insulating qualities of the coat. 25 The overall texture of the llama coat varies from very soft to coarse, and the contrast between guard hair and undercoat may be pronounced or subtle. Llamas occasionally are subdivided into either long-haired (lanuda) or short-haired (pelada) types. In both, the face itself usually is covered with very short hairs. The long-haired types generally have a long, thick coat that may cover the entire head, neck, *Diplomate, American College of Veterinary Internal Medicine; Assistant Professor, Department of Clinical Sciences, Colorado State UniverSity College of Veterinary Medicine, Fort Collins, Colorado
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and body. The short-haired types generally have much less hair, which is most obvious over the head, neck, and distal extremities. 25 Partial shedding of primarily the undercoat occurs each year but is most noticeable every second year. The shedding process produces a thin spot or "break" in the retained hair unless the animal is shorn each year. 24 Hair fiber quality is noted to decrease after about 10 years of age. 25 Hair fiber characteristics apparently are highly heritable and comparatively easy to breed for. Llama breeders who have selected for a longer, more uniform fleece with longer secondary hairs, have found that these animals do not shed out normally except perhaps at the neck, where the guard hairs and undercoat remain very distinguishable. 25 The rate and quality of fiber production likely are affected by changes in environmental temperature, moisture, and light exposure. 25 Vegetable matter, including foxtails, other weed seeds, hay, dirt, and dust frequently are found within the coat - a testament to the llama's desire to roll on the ground and take "dirt baths." Basic recommendations given to optimize coat condition include the feeding of higher protein diets, the provision of readily available sulfur blocks, the inclusion of adequate copper and zinc in the diet, and the avoidance of sudden dietary changes (Johnson L, personal communication, 1988). Stress should be minimized. Llamas ideally should be groomed regularly, but not excessively. Attempts also should be made to minimize contamination of the coat with excessive vegetable debris and, especially, plastic baling twine fibers. Skin thickness varies considerably, being thickest over the dorsal cervical area (where it may be in excess of 10 mm) and the ventral cervical and dorsal thoracic regions. This increased thickness primarily is caused by the presence of larger amounts of dense collagen within the dermis. Skin over the dorsal lumbar, ventral abdominal, axillary, inguinal, medial, and caudal thigh regions comparatively is quite thin (approximately 2 to 3 mm). An alopecic, hyperpigmented, thick callus-like plate of varying sizes normally is present over the ventral thoracic region and likely serves a protective function. Alopecic, thickened, hyperkeratotic, hyperpigmented callus-like areas also are found over the anterior aspect of the carpi and, occasionally, over the anterolateral aspect of the stifles. Linear, alopecic, hyperkeratotic areas also are located on each side of the metatarsal bone. These structures likely represent vestigial metatarsal bones much like the chestnuts found on the inside of front and rear limbs of the horse. A linear line of marked hyperkeratosis also is found extending down the length of the dorsal interdigital spaces on all four feet. Although it has been suggested that this may represent a glandular area, important in territorial marking, histologic examination of the region has failed to reveal such glandular material. The purpose of this structure, if any, is unknown. The thick foot pad essentially is comparable to that of most carnivores. There are only two digits, each with its own toenail. These nails normally grow constantly and with normal exercise usually will wear even with the foot pad. Toenails allowed to grow excessively will result
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in toe curling, which often is difficult, if not impossible, to resolve. Where adequate wearing of the nail is not possible, regular trimming is indicated. There are some crooked toes that appear to be a heritable trait (Johnson L, personal communication, 1988).
MICROSCOPIC ANATOMY AND PHYSIOLOGY The epidermis of the llama varies in thickness from two to four cells in heavily haired areas (cervical, dorsal, and lateral thorax) to three to five cells in less densely haired areas (axillae, inguinal regions, medial and caudal thighs, perineum). A mild degree of orthokeratotic hyperkeratosis appears to be quite normal and especially is evident over the dorsal cervical, thoracic, and lumbar regions. The histological appearance of the callus-like areas over the ventral thorax, anterior carpi, and lateral stifles; the alopecic hyperkeratotic areas over the metatarsal bones; and the hyperkeratotic areas in the interdigital spaces all are similar. Orthokeratotic hyperkeratosis is marked. There is marked epidermal hyperplasia and rete ridge formation. Sebaceous and apocrine glands are found in variable numbers but generally are very small and sparse in areas that are heavily haired (entire cervical region, dorsal thoracic and lumbar regions, lateral thorax) and quite large and numerous in the lightly haired regions (axillae, inguinal regions, medial and caudolateral thighs). Very large aggregates of sebaceous glands are noted in the perineal and perianal regions. Llamas are known to sweat significantly in association with exposure to increased ambient temperatures 1 ,8 and following the intravenous administration of adrenalin. 1 The major sites for effective water vapor loss appear to be over the ventral, relatively hairless areas of the body where apocrine glands are most numerous and evaporative cooling can occur more readily. Perhaps the most unique species variation noted to occur within normal llama skin is the presence of a very prominent vascular plexus in the superficial dermis. This vascular plexus occasionally is so extensive it becomes the predominant structure in the superficial dermis. Similar vascular structures also are present in the alpaca and have been described in the guanaco. 3 Their function is unknown but may be related to thermal regulation. 3 Vessel walls in these vascular plexi frequently are thick and surrounded by slightly increased numbers of lymphocytes and macrophages. Small numbers of eosinophils also may be present. To the uninitiated, these findings often are interpreted as representing mild chronic inflammatory changes, but apparently this number of perivascular cells is quite normal in the llama. They have been present in the skin biopsies of all the normal llamas we have looked at to date. When interpreting llama skin biopsies, it is important to recall that mild orthokeratotic hyperkeratosis, a prominent superficial dermal vascular plexus, and mild perivascular accumulation of inflammatory cells
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likely are normal. When interpreting the size and numbers of sebaceous glands (for example, especially when assessing the presence of a possible endocrinopathy), the region from which the biopsy has been taken also must be taken into consideration.
SELECTED LLAMA SKIN DISEASES Ectoparasites
Sarcoptic Mange. Sarcoptic mange or "sarna," as it is called in South America, is caused by Sacroptes scabii, var. auchenidae, and has been well described in the camilidae, (llama, alpaca, vicuna, and guanaco I3 ). Although sarcoptic mange once was quite common in North American llamas, its incidence appears to be decreasing significantly, perhaps because of the routine practice of worming with ivermectin, a therapy of choice for this form of mange. The scabies mite spends its entire life on the host, burrowing within the epidermis of the skin. The life cycle (from egg to adult) is completed in about 7 to 14 days.9 Under ideal conditions, the mite can survive off the host for only a few days.23 The presence of the mite provokes an inflammatory response that initially produces a papular dermatitis. Many of the more obvious cutaneous changes, such as crusting, thickening, and hyperpigmentation, however, are a product of the moderate to severe pruritus that is characteristic of the disease. Sarcoptic mange is communicable readily to other llamas, with transmission occurring primarily through direct contact, the use of communal dusting areas, or contact with fomites such as bedding, grooming tools, and clothing. 23 It is interesting to note that some llamas appear to be quite resistant to infestation. 14 Although communicability to other species is uncommon, transmission to sheep, horses, and humans has been reported. 2,17 The disease has been suggested to be most active in cold, wet weather and more dormant in summer. 23 Affected llamas initially develop a pruritic, papular, erythematous dermatitis over the inguinal, axillary, ventral abdominal, perineal, and distal extremity areas. Affected regions gradually become alopecic, crusted, thickened, and hyperpigmented. The problem can become more generalized, involving the dorsal and lateral abdomen and thorax and facial regions. Lesions in the more heavily haired regions may appear as heavy scaling. Severely affected individuals have been known to die, likely because of secondary bacterial infections and general debilitation. 14 Differential diagnoses include chorioptic mange, an irritant dermatitis associated with lying on abrasive surfaces (for example, alfalfa stems) in damp cold weather, idiopathic hyperkeratosis (zinc-responsive dermatoses), and inhalant or food allergies. Diagnosis is based on skin scrapings. Scrapings should be deep, retrieving large amounts of debris. Mites and mite· eggs usually are present in large numbers. Material from the scraping may be placed on
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a slide and covered with 10 per cent KOH to "clear" the hairs and facilitate observation of the mites. The clearing process generally takes 10 to 20 minutes at room temperature. On occasion, scrapings may be negative even in the severely affected individual. 23 When sarcoptic mange is suspected but mites are not found, the diagnosis is confirmed by assessing response to trial treatment. Skin biopsies show variable degrees of epidermal hyperplasia, hyperkeratosis, and subacute and chronic inflammatory changes in the dermis. Eosinophils usually are present in large numbers. Mites may be seen. Many therapies for sarcoptic mange in the camilidae have been reviewed. 2,9,14,23 Most recently, the therapy of choice is the ivermectin formulated for bovine use (Ivomec-AGVET, Merck, Sharp, & Dohme, Rahway, NJ) 0.2 mg per kg given subcutaneously and repeated in 10 to 14 days. Parenteral administration appears to be more effective than oral dosing. Pruritus should be reduced significantly within 10 days and there should be good evidence of hair regrowth within 30 days.14 A lack of response to this therapy likely would rule out a diagnosis of sarcoptic mange. The author's alternative therapy of choice is 2 to 3 per cent lime sulfur applied as a spray or dip once weekly for 4 weeks. Lime sulfur will discolor light coats. Affected animals ideally should be isolated and treated into remission. Especially with tenacious or recurrent problems or where isolation of affected individuals is not possible, all in-contact animals should be treated. Chorioptic Mange. The history and physical findings associated with Chorioptes bovis infestations in the llama and alpaca are similar to those described for sarcoptic mange lO but chorioptic mange is encountered less commonly. Pruritic lesions generally are found over the distal extremities, ventrum, and base of the tail. Pruritus, however, is less severe than with sarcoptic mange and, indeed, may be quite mild. Mention has been made of a Chorioptes-infested young llama who initially was presented for head shaking. 4 It has been suggested that chorioptic mange may not be as responsive to ivermectin therapy as sarcoptic mange because the chorioptic mite lives on the surface of the skin and does not burrow into the epidermis. For this reason, the lack of response to a trial ivermectin therapy should not rule out this form of mange. Differential diagnoses are as for sarcoptic mange. Diagnosis is made by skin scrapings (mites generally are found readily) and response to therapy. Although ivermectin formulated for bovine use (Ivomec-AGVET, 0.2 mg/kg subcutaneously and repeated in 2 weeks) occasionally may be effective, our therapy of choice at this time has been 2 to 3 per cent lime sulfur dips or sprays applied once weekly for 4 weeks. Crotoxyphos {0.25 per cent applied as a total body dip or spray at least twice at 10 to 14 day intervals apparently has been effective in the cow, goat, sheep, and horse. 22 The author, however, has no experience with this medication in camelids. Pediculosis. Louse infestations are quite common in llamas. Both biting louse (Damalinia breviceps) and sucking louse (Microthoreis cameli) infestations are noted, 5 with biting lice being most common.
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Mixed infestations occasionally are encountered. Clinically significant louse infestations are most common during the winter. Louse infestations usually are pruritic, which often results in patchy hair loss. The coat often becomes dry and scaly and the llama may appear unthrifty. Lice generally are found in heavily wooled areas. Differential diagnoses would include sarcoptic and chorioptic mange, allergies, and dermatophytosis. Diagnosis is based on history, physical examination, and the demonstration of lice. Highest concentrations of lice are reported to be found along the dorsal midline and the sides and dorsum of the tailhead region. 6 The lice, which are about 2 mm in length, are seen best by parting the hairs and directly examining the skin. The mites themselves may look like pieces of scale. The type of louse infestation (biting versus sucking) ideally should be determined using a hand magnifying lens because this may help determine the therapy to be used. Treatment recommendations include powdering with a 50 per cent wettable powder of methoxychlor (Morlate) or a 5 per cent carbaryl dust (Sevin). 6 The wool should be parted, then dusted down to the skin; "move an inch or so away and repeat the operation until the heavily wooled areas are covered thoroughly."7 I vermectin therapy has been suggested to be effective against sucking lice, but not biting lice. 6 The ivermectin formulated for bovine use is given and repeated in 10 to 14 days (0.2 mg per kg IvomecAGVET subcutaneously). All in-contact animals should be treated. Other therapies noted to be effective include fenthion (Tiguvon, Bayvet Div. of Cutter Labs., Shawnee, KS) pour-on (use swine dilution; do not use Spotton) and Ectrin spray (Johnson L, personal communication, 1988). Prevention should involve the treatment of all new llamas brought into the environment. Environmental therapy using products like the Ectrin spray also may be indicated in refractory or recurrent cases. Demodicosis Demodicosis appears to be rare in camelids. Its clinical presentation appears similar to that observed in cattle and goats. 18 Singular or multiple asymptomatic papules or nodules are noted, especially over the face, neck, and brisket area. Exudation and crusting may be seen, especially when lesions are infected secondarily. Differential diagnoses include bacterial folliculitis, dermatophilosis, and dermatophytosis. Diagnosis is based on history, physical findings, skin scrapings, and skin biopsy. Papular lesions should be squeezed and then scraped deeply. Nodular lesions should be incised and the caseous contents examined microscopically. Mites will be present in large numbers. Skin biopsies will show markedly dilated follicles filled with demodectic mange mites and variable degrees of associated perifolliculitis, folliculitis, furunculosis, and/or pyogranulomatous inflammation. Therapy, if necessary, simply may involve manual expression of the lesion followed by infusion of Lugol's iodine. Other therapies to be considered include infusion of rotenone in alcohol (1: 3) as used in goats 18 or the generalized total body therapies reportedly used in
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goats, cattle, and sheep.Is Although the author has no experience with ivermectin therapy for this disease in llamas, its failure in the treatment of demodicosis in other species would suggest that it likely will not be effective. Infectious Dermatoses
Bacterial Folliculitis and Furunculosis. Bacterial skin infections generally have been presented as variable pruritic (most commonly nonpruritic) focal asymmetrical areas of hair loss, crusting, and exudation. They primarily have been noted over the head and/or distal extremities. Differential diagnoses include sarcoptic/chorioptic mange, dermatophytosis, dermatophilosis, and idiopathic hyperkeratosis (zincresponsive dermatosis). Diagnosis is based on skin biopsy and response to therapy. Skin biopsies show variable degrees of folliculitis, perifolliculitis, and furunculosis. InHammatory cell accumulations consist of admixtures of neutrophils, lymphocytes, macrophages, and eosinophils. An epidermitis and/ or diffuse accumulation of inHammatory cells within the dermis may be present. To date, limited cultures have been done from affected individuals. Staphylococcus intermedius has been retrieved most consistently from lesions. For more focal lesions, therapy has involved clipping, cleansing, and the topical application of antibacterial preparations (for example, iodophors). More generalized involvement may require systemic therapy. Empirically, penicillin (22,000 IU per kg subcutaneously twice daily for 7 to 10 days) or trimethoprim-sulfadiazine (10 mg per kg of combined product diluted to 12 per cent and given subcutaneously twice daily) has worked well. Otherwise, parenteral antibiotics should be chosen on the basis of culture and sensitivity testing. Dermatophilosis. Dermatophilosis caused by Dermatophilus congolensis is noted to occur in the llama. It most commonly is seen in warm, moist climates during the rainy season. Lesions most frequently are seen over the back, sides, and distal extremities. Maceration and skin irritation associated with the accumulation of vegetable material in the dense coat likely predispose animals to the truncal lesions. Lesions usually are not painful but may be pruritic, and consist of heavy exudate mixed with matted hairs. Peeling the hairs and crust away usually leaves an erosion covered with purulent debris. Differential diagnoses include dermatophytosis and bacterial folliculitis and furunculosis. Diagnosis is based on direct smears of purulent material or saline-soaked and broken up crusts, which may be stained with Diff-Quik, new methylene blue, or Gram's stain. Dermatophilus congolensis also may grow well on blood agar. I9 The author has no personal experience with skin biopsies from affected llamas but would assume they would be similar to those described in other species. I9 Therapy would include clipping and cleansing, followed by the use of topical disinfectants (such as iodophors, 2 to 5 per cent lime sulfur or 0.5 per cent zinc sulfate) applied once daily for 3 to 5 days and then weekly until healing has occurred. I9 Unfortunately, all of these products may stain the hair. Although the author has no personal experience
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with systemic therapy, a combination of penicillin and streptomycin as used in cattle, sheep, and goats (5,000 IU per kg procaine penicillin G and 5 mg per kg streptomycin daily for 4 days)19 could be tried. Affected individuals should be moved to dry, clean environments. Dennatophytosis. Dermatophytosis or ringworm in llamas, in our clinic, has been associated most commonly with Trichophyton verrucosum, Microsporum nanum, and Microsporum gypseum. Dermatophytosis appears to be more common in confined animals, especially during the winter months. Skin lesions consist of variable-sized focal areas of hair loss and crusting. Lesions have been noted most commonly over the distal extremities, face, and perineum. They are variably pruritic. Differential diagnoses include bacterial folliculitis and furunculosis, dermatophilosis, and idiopathic hyperkeratosis (zinc-responsive dermatosis). Diagnosis is based on KOH preparations, fungal culture, and skin biopsy. KOH preparations, in our hands, rarely are positive. Our experience with skin biopsies is limited but findings have included orthokeratotic hyperkeratosis, folliculitis, perifolliculitis, a perivascular dermatitis, and diffuse accumulations of mononuclear inflammatory cells within the dermis. Fungal organisms are seen only occasionally on H & E or with special stains. Therapy usually begins with clipping affected areas (where possible) and discarding the hairs. Topical therapy may include iodophors, 2 to 3 per cent lime sulfur, 3 per cent captan, or 0.5 per cent sodium hypochloride. 20 For very focal lesions, anyone of these therapies can be applied to the region once or twice daily until the lesions are resolved. For more generalized problems, the author's topical therapy of choice is 3 per cent captan applied once daily for 5 days, then twice weekly until the lesions resolve. The author has no experience with systemic griseofulvin therapy in the llama. Its expense and questionable efficacy in other large animal species make its use controversial. If it were to be considered, a dosage regimen similar to that used in sheep and goats (10 mg per kg per day per orally) would seem appropriate. 2o Adjunctive therapies include maintenance of good nutrition and the provision of a clean, dry, and sunny environment. Coccidioidomycosis (Valley Fever). Coccidioidomycosis has been described in new-world camelids that reside or have spent time in the Southwestern United States where coccidiodes is endemic. The causative organism, Coccidioides immitis, usually is inhaled. Clinical signs depend on the organ system involved (for example, respiratory, central nervous system). A cutaneous form of the disease has been described in association with systemic involvement and also may be present as the only apparent site of involvement. 11 Skin lesions are papular, plaquelike, or nodular. They may be exudative and crusty. Lesions are found most commonly over the perineum, face, and limbs. 11 Differential diagnoses include dermatophilosis, dermatophytosis, and idiopathic hyperkeratosis (zinc-responsive dermatosis). Diagnosis of the cutaneous form of the disease is based on history, physical findings, cytological examination of exudate from the lesions, or skin biopsy. Cytological examination is performed best by examining cuta-
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neous exudates in a wet mount of 10 per cent potassium hydroxide under subdued microscopic lighting. The highly refractile doublewalled spherules that contain endospores are typical. Histological examination of tissues also may show the characteristic spherules. There apparently is no successful therapy for coccidiodomycosis in llamas at this time. Contagious Viral Pustular Dennatitis. Contagious viral pustular dermatitis, also known as contagious ecthyma, sore mouth, or orf has been recognized in camelids 12,16 and, specifically, in the llama (Johnson L, personal communication, 1988). This contagious disease is caused by a papovavirus in sheep and goats and likely is transmitted to camelids via contact. Lesions usually are noted at the mucocutaneous junctions and are raised, alopecic, often erythematous, and, frequently, painful. The disease usually resolves spontaneously within 10 to 14 days. Allergies
Steroid-responsive Pruritic Dennatoses of Suspect Allergic Origin. The author has seen and consulted on a number of llamas whose skin disease was characterized by generalized pruritus without significant skin lesions, or with variable degrees of hair loss, and dermatitis induced by self trauma. There appears to be no sex or age predilection, although younger animals (1 to 3 years) appear to be affected more commonly. The problem may be either seasonal or nonseasonal. The primary differential diagnoses usually have included sarcoptic and chorioptic mange, pediculosis, and dermatophytosis. Skin scrapings, fungal cultures, and fecal examinations have been negative. There has been- no response to insecticide therapy. Skin biopsies have shown minimal changes. They have included orthokeratotic hyperkeratosis with variable degrees of a mononuclear perivascular dermatitis. Eosinophils often have been present in slightly increased numbers. Response to systemic steroids has been prompt. Based on experience with similar syndromes in other species, this pattern of disease would suggest the presence of an allergic disorder. Seasonal problems (for example, summer) might suggest inhalant allergies, perhaps to environmental pollens or molds. Nonseasonal problems may suggest allergies to dust and/or molds or foods. To date, trial food restriction (for example, discontinuation of supplements, use of one hay source at a time) to assess possible food allergies and intradermal skin testing to evaluate for inhalant allergies have not been employed for diagnostic purposes. Problem cases have been treated with oral prednisone, 0.5 to 1 mg per kg per day initially, gradually decreasing to the lowest every-other-day dose required to control the symptomatology. Alopecic Disorders
Alopecia Affecting the Bridge of the Nose. A focal alopecia noted primarily over the mid-dorsal region of the bridge of the nose is noted quite commonly in the llama. Skin in affected areas may be normal or variably scaly, hyperpigmented, and thickened. Black-pigmented indi-
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viduals may be predisposed. This alopecia most frequently is self-induced by rubbing the nose area. Although this simply may be a vice in some individuals, it usually is most prominent during the warmer summer months and may be a response to fly irritation. Differential diagnoses include dermatophytosis and idiopathic hyperkeratosis (zinc-responsive dermatosis). Skin biopsies reveal only mild epidermal hyperplasia and orthokeratotic hyperkeratosis. There usually are minimal to no inflammatory changes. Therapy usually is not required, although if flies are incriminated in the pathogenesis, fly repellants should be considered. Idiopathic Cervical Alopecia. An acquired alopecia involving primarily the undercoat has been noted to occur in the cervical/shoulder regions of llamas. Age of onset usually is about 24 months, although this syndrome has been reported to develop in animals as old as 6 to 8 years. There is no apparent sex predilection; both neutered and intact males have been affected. Diet and management practices do not appear to playa role. The alopecia is nonpruritic and unassociated with other skin changes. Affected individuals otherwise are normal systemically. The alopecia generally begins in the spring. Although regrowth often occurs, it may take as long as 6 months to see first evidence of this and affected areas usually do not return to full coat. Diagnostics to date have included skin scrapings, fungal cultures, and skin biopsies but they have failed to reveal a cause for the problem. Skin biopsies have not shown evidence to support the presence of an endocrinopathy. Breeders have commented that certain of their llamas may develop the hair loss every 2 years. Others believe that this is an inherited trait. At present, we are considering this a normal, genetically determined shedding pattern. Epithelial Neoplasia
Papillomatosis. Papillomas or warts are noted to occur in llamas. They are raised, usually verrucus, lesions that are found singly or on a random distribution over the less haired areas of the body (face, legs, perineum, and brisket). As in other species, llama papillomas likely are caused by a papovavirus and probably can be transmitted by direct contact or fomite contact. Diagnosis is by history, physical examination, and skin biopsy. Skin biopsies have been characterized by both epithelial and dermal fibrous tissue proliferation. Papillomas in llamas usually resolve spontaneously, but this process may take several months. Idiopathic Dermatoses
Idiopathic Hyperkeratosis (Zinc-responsive Dennatosis). Idiopathic hyperkeratosis is an apparently common skin disorder of llamas. It usually is recognized first in 1 to 2 year old llamas but age of onset is variable. Both sexes may be affected, although males appear to be somewhat over-represented. Only one or a few individuals in a herd may be affected. The disease has developed in spite of the fact that dietary zinc concentrations appear to be adequate. Lesions are noted
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most commonly over the ventral abdomen, inguinal region, medial thighs, and axilla. They initially are papular, progressing to raised alopecic plaques with a dry adherent scale. Larger areas of involvement often give the skin a diffusely thickened appearance and feel. The lesions usually do not appear inflammatory. As the disease progresses, there may be involvement of the face (especially bridge of the nose) and distal extremities. These lesions usually are asymptomatic (nonpruritic) although, on occasion, mild pruritus may be noted. They do not appear to resolve spontaneously. There is no systemic symptomatology. Differential diagnoses include sarcoptic and chorioptic mange, dermatophytosis, and dermatophilosis. Diagnosis is made by history, physical examination, and skin biopsies. Skin biopsies show a marked epithelial and follicular orthokeratotic hyperkeratosis. A mild to moderate perivascular dermatitis, characterized by increases in lymphocytes, macrophages, and eosinophils, may be seen. Quite empirically, this problem has been treated most successfully with oral zinc supplementation. Daily zinc therapy (for example 1 g zinc sulfate or 0.5 g zinc oxide per day) generally is necessary to achieve and maintain remission. Because dietary calcium is noted to potentially bind zinc and prevent its absorption from the gastrointestinal tract, some recommend minimizing calcium supplementation and discontinuing the use of alfalfa hay. The use of an organic complex of zinc in the form of zinc methionine theoretically may be a more benencial supplement because of its more effective absorption, independent of calcium content of the diet. Improvement in the skin lesions usually occurs gradually over 2 to 3 months. Daily maintenance therapy is required to maintain remission. At present, it is not known whether this syndrome represents a true zinc denciency. It, instead, may be a keratinizing disorder that is benented by superphysiologic systemic zinc concentrations, wherein the zinc is helping to normalize keratinization or reduce inflammation. Although the histological nndings in this syndrome do not include the parakeratotic hyperkeratosis usually associated with zinc-responsive dermatoses, others have noted that zinc-responsive dermatoses in some cattle, sheep, and goats may show only orthokeratotic hyperkeratosis. 21 Others also have recognized zinc-responsive dermatoses to occur in sheep and goats where the condition has not been associated with dietary denciency and affected individuals have required constant therapy to maintain remission. 21 To date, no good data exist on serum or hair zinc concentrations in affected llamas, although, in other species, it is noted that these concentrations are not sufficiently accurate to be of general diagnostic value. 21 SUMMARY
As llamas become more common in North America, veterinarians will be called on ever more frequently to deal with their dermatologic
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problems. Adherence to the basic tenets of the thorough dermatologic work up, including history, physical examination, skin scrapings, cytological examinations, fungal culture, skin biopsies, and assessing response to judiciously chosen trial therapies will offer the best opportunity of arriving at proper diagnoses. Special attention must be paid to the fact that llama skin bears some histological differences that may prove confusing to the uninitiated. A mild degree of hyperkeratosis, a prominent vascular plexus in the superficial dermis that is associated with mild perivascular mononuclear cell accumulations, and regional differences in sebaceous gland size and numbers, all are considered normal findings. Ectoparasites, including sarcoptic mange, chorioptic mange, and pediculosis, appear to be the most common causes of pruritus in the llama. Although ivermectin therapy would appear to be very effective for the treatment of scabies and, indeed, may work well against sucking lice, chorioptic mange and biting lice usually do not respond to this medication. Corticosteroids can be used to treat pruritus in the llama nonspecifically, using the anti-inflammatory dosages established in other species. These drugs are used most appropriately for the management of the allergies that we suspect occur in this species, until better alternative therapies can be developed. Variably pruritic focal areas of alopecia, exudation, and crusting suggest differential diagnoses including bacterial folliculitis and furunculosis, dermatophilosis, dermatophytosis, and coccidiomycosis. The diagnosis of bacterial problems often is made by assessing response to antibiotic therapy. Topical disinfectants and/or systemic penicillin or trimethoprim-sulfadiazine are indicated. Dermatophilosis is treated by cleaning and drying the leasions, applying topical antibiotics, and, occasionally, using parenteral penicillin and streptomycin. Dermatophytosis usually is treated with topical antibiotics only. Captan is one of several therapies of choice. There is no therapy presently available for coccidioidomycosis in the llama. Perhaps most perplexing is the fact that one of the most common dermatopathies seen in the llama is an idiopathic keratinizing disorder that, in some cases, is responsive to zinc supplementation. We have no real idea of the pathogenesis of this problem and recognize that some affected animals will not respond to supplementation. Questions regarding this disease and several others that we are beginning to recognize emphasize the fact that we have only begun to scratch the surface in llama dermatology - the bulk of our work lies ahead.
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3. Everts W: Comparative functional anatomical study of the skin of several South American mammals (En Alemain). Z Wiss Zool 185:319-360, 1973 4. Fowler ME: Llama care questions and answers. 3L-Llama 22:7, 1979 5. Fowler ME: Llama medicine. In Workshop Proceedings. Santa Cruz, California, 1984, pp 77 -96 6. Fowler ME: Llama care-questions and answers. 3-L Llama 24:11-12,50,1984 7. Fowler ME: Llama care-questions and answers. 3-L Llama 27:46, 1985 8. Fowler ME: Thermal stress in llamas. 3-L Llama, May/June: 17 -20, 1985 9. Fowler ME: Parasitic diseases of camelids. In Fowler ME (ed): Zoo and Wild Animal Medicine. Philadelphia, WB Saunders, 1986, pp 974 10. Fowler ME: Llama care. Llama 2:12, 1988 11. Fowler ME: Medicine and Surgery of South American Camelids. Ames, Iowa State University Press, 1989, in press 12. Hartwig J: Contagious ecthyma of sheep. Tierarztliche Praxis 8:435-438, 1989 13. Kraft H: Considerations of sarcoptic mange in camelids. Betrachtungen zur Sacroptesraude der Cameliden BMIW 69:365 - 366, 1956 14. Kress PJ: Use of ivermectin for treatment of scabies in llamas. Llama World 3: 18-19, 1983 15. Langley KD, Kennedy RA Jr: The identification of specialty fibers (mohair, cashmere, camel hair, alpaca, and angora rabbit). Textile Res J 51:703-709, 1981 16. McConnell T: Basic llama tips worth knowing. 3L-Llama 26:48, 52, 1985 17. Mellanby K: Sarcoptic mange in the alpaca. Transactions of the Royal SOciety Tropical Medicine and Hygiene 40:359, 1946 18. Scott DW: Large Animal Dermatology. Philadelphia, WB Saunders, 1988, pp 226-230 19. Scott DW: Large Animal Dermatology. Philadelphia, WB Saunders, 1988, pp 144-146 20. Scott DW: Large Animal Dermatology. Philadelphia, WB Saunders, 1988, pp 179-182 21. Scott DW: Large Animal Dermatology. Philadelphia, WB Saunders, 1988, pp 365-367 22. Scott DW: Large Animal Dermatology. Philadelphia, WB Saunders, 1988, p 225 23. Sharpnack E: Sarcoptic mange in llamas. Llama World, Spring:18, 1982 24. Torrey S: Llama wool. The Llama Newsletter 2:1-5, 1981 25. Walker LB: Breeding and selling of wool to use. Part 1: Wool Series. Llama 1: 57 -61, 1987 26. Young E: Chorioptic mange in the alpaca. Lama pacos. S Afr Vet Med Assoc J 37:475,1966 Department of Clinical Sciences Colorado State University College of Veterinary Medicine Fort Collins, CO 80523