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Pathologic Changes in Otitis Externa
Diseases of the Ear Canal
0195-5616/88 $0.00
+ .20
Pathologic Changes in Otitis Externa
Lois Roth, DVM, PhD*
Otitis externa is a common clinical disorder of cats and dogs. Initial inflammatory lesions may appear innocuous and, therefore, are frequently overlooked or inadequately treated, permitting the development of secondary infections and other complications. Histologic examination of tissue from the external ear canal is rarely included as part of the evaluation of an animal with otitis externa, because useful information is usually obtained from less invasive procedures, specifically cytologic evaluation of skin scrapings or exudates. Rather, it is a procedure of last resort, employed when other tests or therapeutic regimens have not yielded diagnostic results. By this time, lesions associated with superimposed infections or changes associated with medication may mask the primary lesion, making a definitive diagnosis difficult to achieve. Otitic lesions must be evaluated in the context of the whole animal. Accurate historical and clinical assessments are important aids to the pathologist attempting to reach an accurate diagnosis. Primary lesions of the pinna, with or without involvement of the external ear canal, may be an extension of a more generalized dermato logic problem or may specifically involve the ear because of its unique gross and histologic characteristics. 2 • 3
UNDERLYING LESIONS OF OTITIS EXTERNA Parasitic Otitis Externa Parasite-induced otitis is considered to be among the most common primary causes of otitis externa. 4 • 6 It is attributed to infestations with fleas, as well as several species of mites and ticks. Otodectes cynotis, the ear mite of carnivores, is usually implicated in cats, and is probably quite common in dogs, although reports of incidence vary. 4 • 6 • 10 In most cases, the earliest lesions are not detected. Experimental observation suggests that these consist of erythema and a slightly moist and greasy texture to the skin. 10 *Diplomate, American College of Veterinary Pathologists; Department of Pathobiology, Virginia Maryland Regional College of Veterinary Medicine, Virginia Polytechnic Institute and State University, Blacksburg, Virginia Veterinary Clinics of North America: Small Animal Practice-Val. 18, No. 4, July 1988
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Histologic observations include minimal nonsuppurative dermatitis, engorgement of superficial vessels, and hyperplasia of ceruminous and seba· ceous glands. With increasing chronicity, the gross changes become more obvious and the histologic alterations more severe. The gross lesion is characterized by the accumulation of moist, friable, reddish brown debris that is somewhat adherent to the underlying epithelium. Variable numbers of mites are found between this layer of exudate and the epithelium, which is hyperemic and may be multifocally eroded or ulcerated. 6 The number of mites seen does not correlate well with the severity of the lesion, as hypersensitivity responses are suspected to play a significant role. 6 The histologic lesions in uncomplicated cases a~;e indicative of a chronic, severely irritating injury. Because the mites do not burrow into the epidermis, they are rarely included in histologic specimens, unless the exudate is examined. Typical lesions include epidermal hyperplasia with hyperkeratosis and acanthosis, marked hyperplasia and hypertrophy of sebaceous and ceruminous glands, atrophy of hair follicles, and a diffuse cellular infiltrate consisting primarily of mast cells and macrophages, with fewer numbers of lymphocytes and plasma cells. Neutrophils and eosinophils are less common, particularly in cats, but they are abundant in cases complicated by secondary infections. Primary lesions are most often confined to the pinna and external auditory meatus, but may extend to involve the skin of the head if the infestation is severe. Other lesions included moderate enlargement of regional lymph nodes due to reactive hyperplasia. Demodex spp., the follicular mite, is a species-specific mite that is found in small numbers in hair follicles of most normal dogs and cats, without clinically evident disease. In overt clinical demodicosis, lesions may be distributed generally or localized to the feet or the head, including the pinnae. Alopecia and hyperemia with papules characterize the gross lesions. Crusts and excoriations are indicative of secondary infections caused by self-induced trauma. The histologic lesion is diagnostic. Hair follicles that are devoid of hair shafts become dilated with mites and excess keratin debris (Fig. 1). Frequently, adnexal structures are displaced and compressed by the swollen follicles. Eventually, the glands become atrophic. The inflammatory infiltrate is minimal unless affected hair follicles rupture, releasing keratin and mites into the dermis. The resulting inflammatory lesion is usually characterized as a severe, pyogranulomatous dermatitis and is thought primarily to be a response to the keratin released into the dermis. Neutrophils, plasma cells, lymphocytes, macrophages, and multinucleated, foreign body-type giant cells are typically present within the lesion. Notoedric mange, caused by Notoedres cati, is a less common cause of otitis externa in cats. 6 • 7 The disease is sometimes referred to as feline scabies, because the mites burrow into the epidermis as do the mites Sarcoptes scabei var. canis, which may cause similar otic lesions in dogs. Gross lesions, characterized by hyperemia and alopecia with yellowish brown, tightly adherent crusts are typically found on the margins of the pinnae, the nose, and face, but they may also be found in other locations. Scabies in dogs and cats is associated with severe pruritus, and secondary
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Figure l. Hair follicles are devoid of hair shafts and dilated with mites and keratin debris (arrows) in this cat with demodectic mange (X 500).
lesions due to self-induced trauma are usually present. Microscopic examination of deep skin scrapings often yields a definitive diagnosis, as mites are usually nume rous. As part of the life cycle, the female mite burrows into the epidermis to lay eggs, causing the dog or cat to scratch continually at its ears, producing excoriations. The epidermis becomes hyperplastic in response to the burrowing mites, with moderate to marked hyperkeratosis and acanthosis. Mites are often present in histologic sections (Fig. 2). The dermal inflammatory infiltrate consists of neutrophils, eosinophils, lymphocytes, and plasma cells and is a response to the trauma as well as to the mites. The spinous ear tick, Otobius megnini, is occasionally associated with otitis externa in cats and dogs in the southwestern United States. 4 • 7 Adults live in the cracks and crevices of the environment, whereas larvae live within the external ear canal, feeding on epithelial cells, blood, and other tissue fluids . Larvae are relatively large (0.8 to 1.0 em in length) and may be seen grossly, associated with localized areas of hyperemia and accumulations of small brownish yellow crusts. The histologic lesion is characterized by focal edema, hemorrhage, and accumulations of mast cells and eosinophils. This lesion is not specific for Otobius megnini, but the focal/multifocal distribution along with the type of inflammatory cells present suggests a parasitic etiology. Otitis externa is occasionally associated with other ectoparasites, such as fleas or biting flies. Flea-induced otitis externa is usually an extension of generalized cutaneous infestations. Uncomplicated gross lesions typically consist of small, multifocal, hyperemic foci. Fleas may be observed in most cases by carefully searching among the hairs of the pinna. The histologic lesion is characterized by de rmal edema and multifocal aggregates of eosinophils and mast cells in the superficial dermis. Because the lesions
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Figure 2. Sarcoptic mange mites are present within the acanthotic and hyperkeratotic epidermis of the pinna (X 500).
are pruritic, self-induced traumatic lesions are common. Lesions are more severe in animals that are hypersensitive to flea saliva, and it is often more difficult to demonstrate fleas. Gross lesions consist of coalescing foci of hyperemia, again with secondary lesions of self-induced trauma. Histologic lesions are characterized by edema and hyperemia, along with an infiltrate of eosinophils and mast cells. In addition, accumulations of plasma cells and lymphocytes are present in the dermis. These cells, along with eosinophils, may be found around vessels in the deeper dermis. Fly bite otitis/dermatitis usually afflicts dogs and cats living in a rural environment, as the offending fly, Stomoxys calcitrans, lives in manure piles or piles of straw. These biting flies attack the ears and face, inserting their labia and probosces through the epidermis to obtain blood. This causes severely irritating punctate to coalescing lesions characterized by reddish brown crusts and hyperemia. The histologic lesion is not specific and consists of dermal and epidermal edema, slight hemorrhage, and small accumulations of eosinophils and neutrophils. On rare occasions, fortuitous histologic sections may contain the thin tract made by the fly's mouth parts in the epidermis. Hypersensitivity Disorders Lesions attributed to hypersensitivity disorders involve the ears exclusively, or more commonly are seen as a component of more generalized dermatologic disorders . The otitic lesions are frequently pruritic and are often complicated by self-induced trauma with secondary bacterial infections. Atopy, food hypersensitivity, and contact allergic dermatitis have been implicated as causes of otitis externa. 1• 3 • 4 • 6 Atopy is more frequently associated with otitis externa than are the other two disorders. 4 The gross appearance of affected ears is not specific, but may become
PATHOLOG IC CHANGES IN OTITIS EXTERNA
759
Figure 3. Allergic otitis exlerna in a dog with food hypersensitivity. There is slight perivascular edema, and vessels are surrounded by aggregates of plasma cells and eosinophils (X 500).
more meaningful when viewed in combination with a complete physical examination and accurate history. In cases of allergic otitis externa, the pinnae of the ears are slightly to moderately swollen, moderately to severely hyperemic, and slightly warm. Both ears are usually involved. Histologically, there is a variable amount of diffuse edema, which is often most pronounced around blood vessels. The characteristic cellular infiltrate depends, in part, on the duration of the lesion. Early on, eosinophils and mast cells surround blood vessels and are found among adnexal structures and as discrete aggregates within the dermis . In more chronic lesions, lymphocytes and plasma cells are more common components of perivascular aggregates and diffuse dermal infiltrates (Fig. 3). Smaller accumulations of eosinophils are still found, and may be more numerous if the offending antigen has not been removed from the animal's environment. Contact allergic dermatitis that is confined to the ears is a rare condition. A complete history will greatly contribute to achieving an accurate diagnosis, because the most common cause of this condition is medications, especially neomycin, that are used to treat otitis externa. 4 Contact allergic otitis exte rna should be suspected if otic lesions do not resolve or become more severe following the initiation of topical medications. Immune-Mediated Otitis Externa As in other conditions, immune-mediated otitis externa is rarely an isolated e ntity; it is usually associated with more widely distributed cuta-
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ROTH
neous lesions. A complete physical examination is necessary because the distribution of lesions is an important consideration in immune-mediated diseases. 5 • 6 • 9 Immune-mediated diseases that usually involve the face and head, including the pinnae, are pemphigus foliaceous and pemphigus erythematosus. These two diseases rarely involve mucocutaneous junctions or mucous membranes. 9 Gross lesions include hyperemia, scales, crusts, and erosions. Although the lesions of pemphigus foliaceous initially involve the face, head, and neck, lesions gradually spread to involve the entire body. 5 · 9 Pemphigus erythematosus is suspected to be an abortive form of p~mphigus foliaceous, with lesions remaining confined to the face, head, and neck. 9 The severity of the individual lesions in these two entities is similar. The histologic findings are -also indistinguishable. Characteristic lesions include acantholysis, with blister and cleft formation in the superficial epidermis. Blisters contain aggregates of neutrophils and/or eosinophils and, importantly, numerous acantholytic cells. 5 · 8 These clefts or blisters are located within or just beneath the stratum granulosum, and cells of this layer typically adhere to the roof of the blisters. Involvement of hair follicles is an important diagnostic feature. 9 Nonspecific lesions include epithelial hyperplasia due to acanthosis, hyperkeratosis, parakeratosis, epidermal and dermal edema, hyperemia, and a heterogeneous inflammatory cell infiltrate within the dermis. Immunofluorescent staining techniques often demonstrate autoantibody, usually immunoglobulin G, and complement deposited in the intercellular spaces of the stratified squamous epithelium. 9 Dermatomyositis (previously known as epidermolysis bullosa simplex) is a rare, genetically transmitted, blistering disorder of unknown cause that has been reported in Collie dogs. 8 Lesions often involve the pinnae, face, tail, and the skin over bony prominences. 8· 9 Bullae that result from innocuous frictional trauma become focal erosions and ulcers that may be painful. The characteristic histologic lesion is one of liquefactive degeneration of the basal epithelium with blister formation that leaves the basement membrane intact. 9 Immunologic testing yields negative results. 8 Foreign Body (Mechanical) Otitis
A variety of foreign bodies can cause otitis externa, including plant awns, sand, gravel, inspissated otic medications, and children's toys or small household items. Neoplastic masses, both polypoid and sessile, act as endogenous foreign bodies, causing irritation of the external ear canal resulting in otitis externa. Foreign bodies cause discomfort and pain by their presence in the external ear canal. The condition is usually unilateral. The astute owner may notice an acute onset of head shaking and scratching, particularly at one ear. Larger foreign bodies may be seen by the owner, but often require the expertise of the veterinarian for safe removal. Smaller foreign bodies or gritty material is frequently overlooked by the owner. Initially, the foreign material causes localized hyperemia. Erosions or foci of ulceration may develop if the material remains for days or weeks. Material such as plant awns may become embedded in the epithelium early on, inciting a pyogranulomatous inflammatory response. Lesions are usually
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Figure 4. Pyogranulomatous otitis externa associated with embedded fragments of plant material in a cat ( x 1000).
compounded by self-induced trauma. The histologic appearance of early, uncomplicated lesions is characterized by hyperemia, edema, and occasionally, hemorrhage. When the foreign material causes erosion or ulceration from pressure, or fragments of the agent become embedded in the epithelium and/or dermis, the cellular infiltrate becomes more severe and consists of neutrophils, macrophages, multinucleated giant cells, plasma cells, and lymphocytes. Foreign material, especially plant awns, may be found in histologic sections (Fig. 4). Miscellaneous Causes of Otitis Externa Otitis externa may occur in dogs and cats with systemic endocrine disorders. Ovarian imbalance, hypothyroidism, and feminization-associated Sertoli cell tumor have been associated with otitis externa. These disorders are often manifested by generalized cutaneous changes, particularly alopecia or seborrhea, although in some animals cutaneous lesions are limited to the ears. 4 The pathogenesis of endocrine-associated otitis externa has not been defined. It is suspected that hormonal imbalances alter the secretions of sebaceous and ceruminous glands in the ears and disrupt the normal keratinization process. The abnormal accumulation of glandular secretions mixed with keratin debris results in irritation and otitis externa. Bacterial or fungal infections are common sequelae. Frequent exposure to water during swimming or bathing may be a predisposing factor in the development of otitis externa. 4 Some water is retained in the external ear canal, which causes softening of the epidermis and predisposes to secondary bacterial or fungal infections. Initially, the pinna may be slightly reddened and have a soft, moist texture. The histologic lesion is characterized by epidermal edema, epithelial degeneration, and
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Figure 5. Epithelial hyperplasia of the ear canal of a dog with chronic otitis externa. There is a focal accumulation of inflammatory cells in the superficial dermis (X 500).
hyperemia. Inflammatory cell infiltrates are not present until secondary infections occur. Solar dermatitis is a condition that most frequently involves the pinnae of white cats. Lesions result following long-term, repeated exposure to the sun. The earliest observable lesion is hyperemia that usually begins at the tips and margins of the pinna. The pinnae feel slightly thickened. This is considered a preneoplastic change and usually will become progressively more severe with time. Nonhealing, ulcerative, crusting lesions are the next observable change and are followed by overt proliferative, neoplastic lesions. Early histologic lesions consist of hyperemia and epithelial hyperplasia. Epithelial growth continues to become more pronounced, eventually breaking through the basement membrane and resulting in squamous cell carcinoma. SECONDARY LESIONS OF OTITIS EXTERNA The secondary lesions of otitis externa are due to chronic irritation, secondary bacterial or fungal infections, or a combination of these factors. Chronic irritation without a severe inflammatory component is characterized by epithelial hyperplasia with hyperkeratosis and acanthosis (Fig. 5). Rete pegs are often thickened and extend more deeply than normal. There may be dermal fibrosis . Ceruminous and sebaceous glands that were originally hyperplastic become degenerative. Individual cells swell and become vacuolated (Fig. 6). This is followed by cellular shrinkage and glandular collapse. Aggregates of plasma cells and lymphocytes are variable in number and size and may be observed among atrophic glandular structures, among surrounding vessels , and in the superficial dermis. The lack of a significant
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Figure 6 .• Ballooning degeneration of sebaceous glands in a dog with chronic otitis externa ( X 500).
inflammatory reaction at this stage does not rule out a primary inflammatory etiology. The reaction indicates attempts of the ear canal to heal. Unfortunately, the healing process may have some deleterious effects, including stenosis of the external auditory canal due to scarring. The role of bacterial or fungal infections in otitis externa is controversial. 2-4. 6 Bacteria most often isolated from inflamed ear canals include Streptococcus spp., Staphylococcus intermedius, Pseudomonas spp., and Pasteurella multocida. 4 • 6 The yeast Pityrosporum canis as well as the common fungal agents Trichophyton spp., Microsporum spp., and Candida spp. have been reported as isolates from ear canals of animals with otitis externa. 2 • 4 All of these organisms are ubiquitous, and many of them comprise the small heterogeneous population of microorganisms that normally inhabit the skin of the pinna and external ear canal of cats and dogs. When the normal ecology of the ear canal is disrupted by any one of a wide variety of causes, these organisms take advantage of the abnormal environment and invade the damaged tissue and proliferate, causing secondary infections that contribute to the ongoing inflammatory process. Affected ears have usually been chronically inflamed, causing the animal long-term discomfort and pain. The pinnae are often held in an abnormal position; normally erect pinnae appear droopy, and normally floppy ears are held slightly away from the head. A foul, slightly musty odor can often be detected. Some believe that the odor is characteristic of the organism that is primarily involved. On gross examination, one may see an exudate that
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varies from dark red, to brown, to pale tan, and varies from being serous to viscous in consistency. Scales, crusts, erosions, and ulcers are usually present. The histologic lesions are variable, depending upon duration and severity. In the early stages, the inflammatory infiltrate is predominately neutrophilic, with bacterial colonies scattered throughout the dermis and epidermis. Sebaceous and ceruminous glands become hyperplastic at first, in response to the irritation. Degenerative changes, followed by atrophy, occur as the lesion progresses. The suppurative nature of the infiltrate changes with time. Neutrophils become less numerous, and plasma cells and lymphocytes become more conspicuous. Ultimately, there is proliferation of connective tissue with scarring and the inflammatory nature of the lesion is no longer obvious. In rare cases of severe, chronic otitis externa, resolution of the lesion does not occur, because either the insult to the ears continues or the defense mechanisms of the animal cannot stop the infection from extending by local invasion. Involvement of the tympanic membrane is characterized by opacity and eventual sclerosis, or the tympanic membrane may rupture, allowing the infection to extend to the middle and inner ear. Inflammatory polyps are occasionally observed in cats with chronic otitis externa, but these occur more commonly as sequelae to otitis media or otitis interna.
REFERENCES l. Chamberlain KW: Atopic dermatitis. Vet Clin North Am 4:29, 1974 2. Fernando SDA: Certain histopathologic features of the external auditory meatus of the cat and dog with otitis externa. Am J Vet Res 28:278, 1967 3. Fraser G: Factors predisposing to canine external otitis. Vet Rec 73:55, 1961 4. Griffin CE: Otitis externa. Compend Contin Ed Pract Vet 3:741, 1981 5. Manning TO, Scott DW, Smith CA, et al: Pemphigus diseases in the feline: Seven case reports and discussion. J Am Anim Hosp Assoc 18:433, 1982 6. Scott DW: External ear disorders. J Am Anim Hosp Assoc 16:426, 1980 7. Scott DW: Parasitic disorders. JAm Anim Hosp Assoc 16:365, 1980 8. Scott DW: Schultz RD: Epidermolysis bullosa simplex in the collie dog. J Am Vet Med Assoc 171:721, 1977 9. Scott DW, Wolfe MJ, Smith CA, et al: The comparative pathology of nonviral bullous skin diseases in domestic animals. Vet Pathol17:257, 1980 10. Weisbroth SH, Powell MD, Roth L, et al: Immunopathology of naturally occurring otodectic otacariasis in the domestic cat. JAm Vet Med Assoc 165:1088, 1974
Department of Pathobiology Virginia-Maryland Regional College of Veterinary Medicine Virginia Polytechnic Institute and State University Blacksburg, Virginia 24061
0195-5616/88 $0.00
+ .20
Pathologic Changes in Otitis Externa
Lois Roth, DVM, PhD*
Otitis externa is a common clinical disorder of cats and dogs. Initial inflammatory lesions may appear innocuous and, therefore, are frequently overlooked or inadequately treated, permitting the development of secondary infections and other complications. Histologic examination of tissue from the external ear canal is rarely included as part of the evaluation of an animal with otitis externa, because useful information is usually obtained from less invasive procedures, specifically cytologic evaluation of skin scrapings or exudates. Rather, it is a procedure of last resort, employed when other tests or therapeutic regimens have not yielded diagnostic results. By this time, lesions associated with superimposed infections or changes associated with medication may mask the primary lesion, making a definitive diagnosis difficult to achieve. Otitic lesions must be evaluated in the context of the whole animal. Accurate historical and clinical assessments are important aids to the pathologist attempting to reach an accurate diagnosis. Primary lesions of the pinna, with or without involvement of the external ear canal, may be an extension of a more generalized dermato logic problem or may specifically involve the ear because of its unique gross and histologic characteristics. 2 • 3
UNDERLYING LESIONS OF OTITIS EXTERNA Parasitic Otitis Externa Parasite-induced otitis is considered to be among the most common primary causes of otitis externa. 4 • 6 It is attributed to infestations with fleas, as well as several species of mites and ticks. Otodectes cynotis, the ear mite of carnivores, is usually implicated in cats, and is probably quite common in dogs, although reports of incidence vary. 4 • 6 • 10 In most cases, the earliest lesions are not detected. Experimental observation suggests that these consist of erythema and a slightly moist and greasy texture to the skin. 10 *Diplomate, American College of Veterinary Pathologists; Department of Pathobiology, Virginia Maryland Regional College of Veterinary Medicine, Virginia Polytechnic Institute and State University, Blacksburg, Virginia Veterinary Clinics of North America: Small Animal Practice-Val. 18, No. 4, July 1988
755
756
LOIS ROTH
Histologic observations include minimal nonsuppurative dermatitis, engorgement of superficial vessels, and hyperplasia of ceruminous and seba· ceous glands. With increasing chronicity, the gross changes become more obvious and the histologic alterations more severe. The gross lesion is characterized by the accumulation of moist, friable, reddish brown debris that is somewhat adherent to the underlying epithelium. Variable numbers of mites are found between this layer of exudate and the epithelium, which is hyperemic and may be multifocally eroded or ulcerated. 6 The number of mites seen does not correlate well with the severity of the lesion, as hypersensitivity responses are suspected to play a significant role. 6 The histologic lesions in uncomplicated cases a~;e indicative of a chronic, severely irritating injury. Because the mites do not burrow into the epidermis, they are rarely included in histologic specimens, unless the exudate is examined. Typical lesions include epidermal hyperplasia with hyperkeratosis and acanthosis, marked hyperplasia and hypertrophy of sebaceous and ceruminous glands, atrophy of hair follicles, and a diffuse cellular infiltrate consisting primarily of mast cells and macrophages, with fewer numbers of lymphocytes and plasma cells. Neutrophils and eosinophils are less common, particularly in cats, but they are abundant in cases complicated by secondary infections. Primary lesions are most often confined to the pinna and external auditory meatus, but may extend to involve the skin of the head if the infestation is severe. Other lesions included moderate enlargement of regional lymph nodes due to reactive hyperplasia. Demodex spp., the follicular mite, is a species-specific mite that is found in small numbers in hair follicles of most normal dogs and cats, without clinically evident disease. In overt clinical demodicosis, lesions may be distributed generally or localized to the feet or the head, including the pinnae. Alopecia and hyperemia with papules characterize the gross lesions. Crusts and excoriations are indicative of secondary infections caused by self-induced trauma. The histologic lesion is diagnostic. Hair follicles that are devoid of hair shafts become dilated with mites and excess keratin debris (Fig. 1). Frequently, adnexal structures are displaced and compressed by the swollen follicles. Eventually, the glands become atrophic. The inflammatory infiltrate is minimal unless affected hair follicles rupture, releasing keratin and mites into the dermis. The resulting inflammatory lesion is usually characterized as a severe, pyogranulomatous dermatitis and is thought primarily to be a response to the keratin released into the dermis. Neutrophils, plasma cells, lymphocytes, macrophages, and multinucleated, foreign body-type giant cells are typically present within the lesion. Notoedric mange, caused by Notoedres cati, is a less common cause of otitis externa in cats. 6 • 7 The disease is sometimes referred to as feline scabies, because the mites burrow into the epidermis as do the mites Sarcoptes scabei var. canis, which may cause similar otic lesions in dogs. Gross lesions, characterized by hyperemia and alopecia with yellowish brown, tightly adherent crusts are typically found on the margins of the pinnae, the nose, and face, but they may also be found in other locations. Scabies in dogs and cats is associated with severe pruritus, and secondary
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Figure l. Hair follicles are devoid of hair shafts and dilated with mites and keratin debris (arrows) in this cat with demodectic mange (X 500).
lesions due to self-induced trauma are usually present. Microscopic examination of deep skin scrapings often yields a definitive diagnosis, as mites are usually nume rous. As part of the life cycle, the female mite burrows into the epidermis to lay eggs, causing the dog or cat to scratch continually at its ears, producing excoriations. The epidermis becomes hyperplastic in response to the burrowing mites, with moderate to marked hyperkeratosis and acanthosis. Mites are often present in histologic sections (Fig. 2). The dermal inflammatory infiltrate consists of neutrophils, eosinophils, lymphocytes, and plasma cells and is a response to the trauma as well as to the mites. The spinous ear tick, Otobius megnini, is occasionally associated with otitis externa in cats and dogs in the southwestern United States. 4 • 7 Adults live in the cracks and crevices of the environment, whereas larvae live within the external ear canal, feeding on epithelial cells, blood, and other tissue fluids . Larvae are relatively large (0.8 to 1.0 em in length) and may be seen grossly, associated with localized areas of hyperemia and accumulations of small brownish yellow crusts. The histologic lesion is characterized by focal edema, hemorrhage, and accumulations of mast cells and eosinophils. This lesion is not specific for Otobius megnini, but the focal/multifocal distribution along with the type of inflammatory cells present suggests a parasitic etiology. Otitis externa is occasionally associated with other ectoparasites, such as fleas or biting flies. Flea-induced otitis externa is usually an extension of generalized cutaneous infestations. Uncomplicated gross lesions typically consist of small, multifocal, hyperemic foci. Fleas may be observed in most cases by carefully searching among the hairs of the pinna. The histologic lesion is characterized by de rmal edema and multifocal aggregates of eosinophils and mast cells in the superficial dermis. Because the lesions
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Figure 2. Sarcoptic mange mites are present within the acanthotic and hyperkeratotic epidermis of the pinna (X 500).
are pruritic, self-induced traumatic lesions are common. Lesions are more severe in animals that are hypersensitive to flea saliva, and it is often more difficult to demonstrate fleas. Gross lesions consist of coalescing foci of hyperemia, again with secondary lesions of self-induced trauma. Histologic lesions are characterized by edema and hyperemia, along with an infiltrate of eosinophils and mast cells. In addition, accumulations of plasma cells and lymphocytes are present in the dermis. These cells, along with eosinophils, may be found around vessels in the deeper dermis. Fly bite otitis/dermatitis usually afflicts dogs and cats living in a rural environment, as the offending fly, Stomoxys calcitrans, lives in manure piles or piles of straw. These biting flies attack the ears and face, inserting their labia and probosces through the epidermis to obtain blood. This causes severely irritating punctate to coalescing lesions characterized by reddish brown crusts and hyperemia. The histologic lesion is not specific and consists of dermal and epidermal edema, slight hemorrhage, and small accumulations of eosinophils and neutrophils. On rare occasions, fortuitous histologic sections may contain the thin tract made by the fly's mouth parts in the epidermis. Hypersensitivity Disorders Lesions attributed to hypersensitivity disorders involve the ears exclusively, or more commonly are seen as a component of more generalized dermatologic disorders . The otitic lesions are frequently pruritic and are often complicated by self-induced trauma with secondary bacterial infections. Atopy, food hypersensitivity, and contact allergic dermatitis have been implicated as causes of otitis externa. 1• 3 • 4 • 6 Atopy is more frequently associated with otitis externa than are the other two disorders. 4 The gross appearance of affected ears is not specific, but may become
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Figure 3. Allergic otitis exlerna in a dog with food hypersensitivity. There is slight perivascular edema, and vessels are surrounded by aggregates of plasma cells and eosinophils (X 500).
more meaningful when viewed in combination with a complete physical examination and accurate history. In cases of allergic otitis externa, the pinnae of the ears are slightly to moderately swollen, moderately to severely hyperemic, and slightly warm. Both ears are usually involved. Histologically, there is a variable amount of diffuse edema, which is often most pronounced around blood vessels. The characteristic cellular infiltrate depends, in part, on the duration of the lesion. Early on, eosinophils and mast cells surround blood vessels and are found among adnexal structures and as discrete aggregates within the dermis . In more chronic lesions, lymphocytes and plasma cells are more common components of perivascular aggregates and diffuse dermal infiltrates (Fig. 3). Smaller accumulations of eosinophils are still found, and may be more numerous if the offending antigen has not been removed from the animal's environment. Contact allergic dermatitis that is confined to the ears is a rare condition. A complete history will greatly contribute to achieving an accurate diagnosis, because the most common cause of this condition is medications, especially neomycin, that are used to treat otitis externa. 4 Contact allergic otitis exte rna should be suspected if otic lesions do not resolve or become more severe following the initiation of topical medications. Immune-Mediated Otitis Externa As in other conditions, immune-mediated otitis externa is rarely an isolated e ntity; it is usually associated with more widely distributed cuta-
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ROTH
neous lesions. A complete physical examination is necessary because the distribution of lesions is an important consideration in immune-mediated diseases. 5 • 6 • 9 Immune-mediated diseases that usually involve the face and head, including the pinnae, are pemphigus foliaceous and pemphigus erythematosus. These two diseases rarely involve mucocutaneous junctions or mucous membranes. 9 Gross lesions include hyperemia, scales, crusts, and erosions. Although the lesions of pemphigus foliaceous initially involve the face, head, and neck, lesions gradually spread to involve the entire body. 5 · 9 Pemphigus erythematosus is suspected to be an abortive form of p~mphigus foliaceous, with lesions remaining confined to the face, head, and neck. 9 The severity of the individual lesions in these two entities is similar. The histologic findings are -also indistinguishable. Characteristic lesions include acantholysis, with blister and cleft formation in the superficial epidermis. Blisters contain aggregates of neutrophils and/or eosinophils and, importantly, numerous acantholytic cells. 5 · 8 These clefts or blisters are located within or just beneath the stratum granulosum, and cells of this layer typically adhere to the roof of the blisters. Involvement of hair follicles is an important diagnostic feature. 9 Nonspecific lesions include epithelial hyperplasia due to acanthosis, hyperkeratosis, parakeratosis, epidermal and dermal edema, hyperemia, and a heterogeneous inflammatory cell infiltrate within the dermis. Immunofluorescent staining techniques often demonstrate autoantibody, usually immunoglobulin G, and complement deposited in the intercellular spaces of the stratified squamous epithelium. 9 Dermatomyositis (previously known as epidermolysis bullosa simplex) is a rare, genetically transmitted, blistering disorder of unknown cause that has been reported in Collie dogs. 8 Lesions often involve the pinnae, face, tail, and the skin over bony prominences. 8· 9 Bullae that result from innocuous frictional trauma become focal erosions and ulcers that may be painful. The characteristic histologic lesion is one of liquefactive degeneration of the basal epithelium with blister formation that leaves the basement membrane intact. 9 Immunologic testing yields negative results. 8 Foreign Body (Mechanical) Otitis
A variety of foreign bodies can cause otitis externa, including plant awns, sand, gravel, inspissated otic medications, and children's toys or small household items. Neoplastic masses, both polypoid and sessile, act as endogenous foreign bodies, causing irritation of the external ear canal resulting in otitis externa. Foreign bodies cause discomfort and pain by their presence in the external ear canal. The condition is usually unilateral. The astute owner may notice an acute onset of head shaking and scratching, particularly at one ear. Larger foreign bodies may be seen by the owner, but often require the expertise of the veterinarian for safe removal. Smaller foreign bodies or gritty material is frequently overlooked by the owner. Initially, the foreign material causes localized hyperemia. Erosions or foci of ulceration may develop if the material remains for days or weeks. Material such as plant awns may become embedded in the epithelium early on, inciting a pyogranulomatous inflammatory response. Lesions are usually
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Figure 4. Pyogranulomatous otitis externa associated with embedded fragments of plant material in a cat ( x 1000).
compounded by self-induced trauma. The histologic appearance of early, uncomplicated lesions is characterized by hyperemia, edema, and occasionally, hemorrhage. When the foreign material causes erosion or ulceration from pressure, or fragments of the agent become embedded in the epithelium and/or dermis, the cellular infiltrate becomes more severe and consists of neutrophils, macrophages, multinucleated giant cells, plasma cells, and lymphocytes. Foreign material, especially plant awns, may be found in histologic sections (Fig. 4). Miscellaneous Causes of Otitis Externa Otitis externa may occur in dogs and cats with systemic endocrine disorders. Ovarian imbalance, hypothyroidism, and feminization-associated Sertoli cell tumor have been associated with otitis externa. These disorders are often manifested by generalized cutaneous changes, particularly alopecia or seborrhea, although in some animals cutaneous lesions are limited to the ears. 4 The pathogenesis of endocrine-associated otitis externa has not been defined. It is suspected that hormonal imbalances alter the secretions of sebaceous and ceruminous glands in the ears and disrupt the normal keratinization process. The abnormal accumulation of glandular secretions mixed with keratin debris results in irritation and otitis externa. Bacterial or fungal infections are common sequelae. Frequent exposure to water during swimming or bathing may be a predisposing factor in the development of otitis externa. 4 Some water is retained in the external ear canal, which causes softening of the epidermis and predisposes to secondary bacterial or fungal infections. Initially, the pinna may be slightly reddened and have a soft, moist texture. The histologic lesion is characterized by epidermal edema, epithelial degeneration, and
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Figure 5. Epithelial hyperplasia of the ear canal of a dog with chronic otitis externa. There is a focal accumulation of inflammatory cells in the superficial dermis (X 500).
hyperemia. Inflammatory cell infiltrates are not present until secondary infections occur. Solar dermatitis is a condition that most frequently involves the pinnae of white cats. Lesions result following long-term, repeated exposure to the sun. The earliest observable lesion is hyperemia that usually begins at the tips and margins of the pinna. The pinnae feel slightly thickened. This is considered a preneoplastic change and usually will become progressively more severe with time. Nonhealing, ulcerative, crusting lesions are the next observable change and are followed by overt proliferative, neoplastic lesions. Early histologic lesions consist of hyperemia and epithelial hyperplasia. Epithelial growth continues to become more pronounced, eventually breaking through the basement membrane and resulting in squamous cell carcinoma. SECONDARY LESIONS OF OTITIS EXTERNA The secondary lesions of otitis externa are due to chronic irritation, secondary bacterial or fungal infections, or a combination of these factors. Chronic irritation without a severe inflammatory component is characterized by epithelial hyperplasia with hyperkeratosis and acanthosis (Fig. 5). Rete pegs are often thickened and extend more deeply than normal. There may be dermal fibrosis . Ceruminous and sebaceous glands that were originally hyperplastic become degenerative. Individual cells swell and become vacuolated (Fig. 6). This is followed by cellular shrinkage and glandular collapse. Aggregates of plasma cells and lymphocytes are variable in number and size and may be observed among atrophic glandular structures, among surrounding vessels , and in the superficial dermis. The lack of a significant
PATHOLOGIC CHANGES IN OTITIS EXTERNA
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Figure 6 .• Ballooning degeneration of sebaceous glands in a dog with chronic otitis externa ( X 500).
inflammatory reaction at this stage does not rule out a primary inflammatory etiology. The reaction indicates attempts of the ear canal to heal. Unfortunately, the healing process may have some deleterious effects, including stenosis of the external auditory canal due to scarring. The role of bacterial or fungal infections in otitis externa is controversial. 2-4. 6 Bacteria most often isolated from inflamed ear canals include Streptococcus spp., Staphylococcus intermedius, Pseudomonas spp., and Pasteurella multocida. 4 • 6 The yeast Pityrosporum canis as well as the common fungal agents Trichophyton spp., Microsporum spp., and Candida spp. have been reported as isolates from ear canals of animals with otitis externa. 2 • 4 All of these organisms are ubiquitous, and many of them comprise the small heterogeneous population of microorganisms that normally inhabit the skin of the pinna and external ear canal of cats and dogs. When the normal ecology of the ear canal is disrupted by any one of a wide variety of causes, these organisms take advantage of the abnormal environment and invade the damaged tissue and proliferate, causing secondary infections that contribute to the ongoing inflammatory process. Affected ears have usually been chronically inflamed, causing the animal long-term discomfort and pain. The pinnae are often held in an abnormal position; normally erect pinnae appear droopy, and normally floppy ears are held slightly away from the head. A foul, slightly musty odor can often be detected. Some believe that the odor is characteristic of the organism that is primarily involved. On gross examination, one may see an exudate that
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varies from dark red, to brown, to pale tan, and varies from being serous to viscous in consistency. Scales, crusts, erosions, and ulcers are usually present. The histologic lesions are variable, depending upon duration and severity. In the early stages, the inflammatory infiltrate is predominately neutrophilic, with bacterial colonies scattered throughout the dermis and epidermis. Sebaceous and ceruminous glands become hyperplastic at first, in response to the irritation. Degenerative changes, followed by atrophy, occur as the lesion progresses. The suppurative nature of the infiltrate changes with time. Neutrophils become less numerous, and plasma cells and lymphocytes become more conspicuous. Ultimately, there is proliferation of connective tissue with scarring and the inflammatory nature of the lesion is no longer obvious. In rare cases of severe, chronic otitis externa, resolution of the lesion does not occur, because either the insult to the ears continues or the defense mechanisms of the animal cannot stop the infection from extending by local invasion. Involvement of the tympanic membrane is characterized by opacity and eventual sclerosis, or the tympanic membrane may rupture, allowing the infection to extend to the middle and inner ear. Inflammatory polyps are occasionally observed in cats with chronic otitis externa, but these occur more commonly as sequelae to otitis media or otitis interna.
REFERENCES l. Chamberlain KW: Atopic dermatitis. Vet Clin North Am 4:29, 1974 2. Fernando SDA: Certain histopathologic features of the external auditory meatus of the cat and dog with otitis externa. Am J Vet Res 28:278, 1967 3. Fraser G: Factors predisposing to canine external otitis. Vet Rec 73:55, 1961 4. Griffin CE: Otitis externa. Compend Contin Ed Pract Vet 3:741, 1981 5. Manning TO, Scott DW, Smith CA, et al: Pemphigus diseases in the feline: Seven case reports and discussion. J Am Anim Hosp Assoc 18:433, 1982 6. Scott DW: External ear disorders. J Am Anim Hosp Assoc 16:426, 1980 7. Scott DW: Parasitic disorders. JAm Anim Hosp Assoc 16:365, 1980 8. Scott DW: Schultz RD: Epidermolysis bullosa simplex in the collie dog. J Am Vet Med Assoc 171:721, 1977 9. Scott DW, Wolfe MJ, Smith CA, et al: The comparative pathology of nonviral bullous skin diseases in domestic animals. Vet Pathol17:257, 1980 10. Weisbroth SH, Powell MD, Roth L, et al: Immunopathology of naturally occurring otodectic otacariasis in the domestic cat. JAm Vet Med Assoc 165:1088, 1974
Department of Pathobiology Virginia-Maryland Regional College of Veterinary Medicine Virginia Polytechnic Institute and State University Blacksburg, Virginia 24061