Retrospective Study- The Presence of Malassezia in Feline Skin Biopsies. a Clinicopathological Study (Pages 7–14)

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© 2002 Blackwell Science Ltd 7

Veterinary Dermatology 2002, 13, 7–14

sBlackwellScienceLtd

Retrospective study: the presence of Malassezia in feline skinbiopsies. A clinicopathological study

ELIZABETH A. MAULDIN,* DANIEL O. MORRIS* and MICHAEL H. GOLDSCHMIDT†

Departments of *Clinical Studies and †Pathobiology, Veterinary Hospital of the University of Pennsylvania,

3850 Spruce St. Philadelphia, PA 19104, USA

(Received 26 December 2000; accepted 1 June 2001)

Abstract Malassezia spp. dermatitis, a rare disorder in cats, has previously been associated with immune sup-

pression and internal malignancies. This study evaluates the presence and importance of Malassezia spp. in feline

biopsy specimens submitted for histopathological examination. Five hundred and fifty haematoxylin and eosin-

stained skin biopsy specimens received for histopathological examination between January 1999 and November

2000 were reviewed. Fifteen (2.7%) submissions contained Malassezia organisms in the stratum corneum of the

epidermis or follicular infundibulum. Eleven of 15 cats presented with an acute onset of multifocal to generalized

skin lesions. All 11 cats were euthanized or died within 2 months of the onset of clinical signs. Seven cats had

dermatopathological changes and clinical signs supportive of paraneoplastic alopecia, and three cats had aninterface dermatitis suggestive of erythema multiforme or thymoma-associated dermatosis. Histopathological

changes were nonspecific in one cat that was euthanized 2 weeks following onset of severe pruritus and alopecia.

In three cats, Malassezia spp. were found in localized sites (two chin, one footpads) and appeared inconsequential

to their overall health status. One cat had Malassezia spp. in association with cutaneous demodicosis. These

findings suggest that Malassezia yeast in dermatopathological specimens from multifocal or generalized lesions

should prompt a thorough clinical work-up for internal neoplasia.

Keywords: alopecia, carcinoma, feline, Malassezia, pancreas, paraneoplastic, thymoma.

INTRODUCTION

Malassezia dermatitis is a commonly diagnosed der-

matopathy in dogs. The overgrowth of Malassezia pachy-

dermatis on the skin of dogs has been associated with

allergic disease, cornification defects and the corticos-

teroids or antibiotics used to treat these disorders. Most

dogs respond well to treatment if an underlying disorder

is identified and addressed.1–8 In cats, the association

between Malassezia and allergic disorders is not estab-

lished and far fewer cases of Malassezia infection have

been documented. Veterinary practitioners occasionally

encounter cats with waxy otitis externa or refractorychin acne due to Malassezia.1–3,9–11 However, cutane-

ous infections beyond these sites are quite rare. Cats

can harbour Malassezia organisms within the auditory

canal, anus and skin. Malassezia organisms of several

species have been cultured from normal and abnormal

feline skin.12–14 Cats with feline immunodeficiency

virus and diabetes mellitus could be predisposed to

developing Malassezia infection.11 A recent study

showed that Malassezia yeast could be cultured more

commonly from retroviral-infected cats than from

normal cats.15

GeneralizedMalassezia dermatitis in the cat is extremelyrare. A causal relationship between the overgrowth of

Malassezia organisms and the development of seborrheic

dermatitis was proposed in an abstract at the 1994

American College of Veterinary Dermatology meeting

in Charleston, South Carolina. The two cats cited had

generalized exfoliative and greasy erythroderma, which

responded to antifungal therapy. However, relapses were

frequent and required repeated therapy. No predispos-

ing disorders were identified and the histopathological

changes were nonspecific. Malassezia overgrowth has

since been reported in cats with thymoma-associated

dermatoses (TAD) and paraneoplastic alopecia (PA).

16,17

Cats with TAD develop a generalized exfoliative

inflammatory skin condition that occurs secondary

to a benign intrathoracic tumour. Specific interface

dermatopathological changes can be suggestive of

the disorder, although demonstration of a thymoma is

required for a definitive diagnosis.16,18 Feline paraneo-

plastic alopecia is a well-recognized condition that occurs

secondary to pancreatic or bile duct carcinoma. The

histopathological changes are characterized by profound

and diffuse follicular atrophy.17,19–22 Both disorders are

severely debilitating and most animals are euthanized.16–22

Cats have recovered only when the underlying neoplasm

was surgically excised.16,22

At the University of Pennsylvania we had observed

that the presence of Malassezia organisms in biopsy

specimens seemed to correlate with histopathological

Correspondence: Elizabeth A. Mauldin, Department of Clinical

Studies, Veterinary Hospital of the University of Pennsylvania, 3850

Spruce Street, Philadelphia, PA 19104, USA. Fax: 215 898 0719,

E-mail: [email protected]





© 2002 Blackwell Science Ltd, Veterinary Dermatology, 13, 7–14

Malassezia in feline skin biopsies 9

changes indicative of internal disease. Thus, we decided

to undertake a retrospective review of all feline skin

biopsy submissions over a 2-year period to verify this

observation.

MATERIALS AND METHODS

A computer search for feline skin biopsy submissions

coded as ‘dermatitis or dermatosis’ submitted to the

Out-Patient Diagnostic Service of the Laboratory of

Pathology and Toxicology, University of Pennsylvania,

School of Veterinary Medicine from January 1999 to

November 2000 was reviewed. For inclusion in this study

the cases must have been interpreted as dermatosis or

dermatitis on the written report and must have been

taken as surgical or post mortem sample from anywhere

on the skin except the external ear canal. The external

ear canal was excluded from the study based on the

commonality of Malassezia organisms at this site. Five

hundred and fifty cases met these criteria. Hematoxylin

and eosin-stained slides from all cases were reviewed by

a board-certified veterinary pathologist (EAM) for the

presence of Malassezia organisms, without knowledge

of prior histopathological diagnoses. Yeast were classi-

fied as Malassezia based on size (3–6 µm diameter), shape

(oval to ellipsoidal or ‘peanut’ shaped) and broad-based

unipolar budding of daughter cells.2,5 The medical

histories of all cases with Malassezia were reviewed

and follow-up information was obtained from the

referring veterinarians.

RESULTS

Fifteen of 550 (2.7%) cases contained Malassezia yeast

in the stratum corneum of the epidermis (14/15) or

follicular infundibulum (2/15). Yeast were readily

identifiable in areas of mild to severe orthokeratotic

and parakeratotic hyperkeratosis.

Three groups of animals were identified from the

histopathological and clinical results. Individual cases

are listed in Table 1. All cats except cat 13, an Abyssinian,

were Domestic Short Hair or Long Hair cats. Cats ingroup 1 and group 2 had multifocal to generalized skin

lesions and a shortened lifespan. All cats in groups 1 and

2 were euthanized or died naturally within 2 months of

the onset of clinical signs. Group 1 (7/15 cases) contained

cats with histological and clinical features diagnostic

of or highly consistent with paraneoplastic alopecia

(PA). Group 2 (4/15) contained the remaining cats with

multifocal to generalized skin lesions. Group 3 (4/15

cases) included animals with lesions from focal sites

(chin, footpad). One cat had demodicosis with lesions

confined to the head and neck. Three cats from group

3 were alive at the time of data collection.

Group 1

Group 1 ranged in age from 7 to 15 years (mean,

12 years; median, 13 years). None of the cats were

pure-bred animals. The dermatological lesions were fairly

uniform within this group. All cats were presented for

an acute onset of skin lesions of 2–6 weeks’ duration.

A dramatic loss of body weight, inappetance and/or

vomiting and diarrhoea developed with the onset of skin

lesions. Hair was easily epilated in large tufts leaving

behind areas of complete alopecia with a smooth sheen

to the epidermis. Lesions were primarily found on the

ventrum, particularly the ventral abdomen, but alsoinvolved the ventral neck, thorax and medial hindlimbs

(Fig. 1). Several cats had footpad hyperkeratosis.

All cases except cat 7 (no treatment) received various

antibiotics, and /or corticosteroids with no improvement.

Cat 1 was the only case that received treatment for the

igure 1. Cat 1, paraneoplastic alopecia; severe symmetrical alopecia and erythema on ventrum and limbs (Courtesy of Dr Jean Greek,

verland Park, KS).



10 Elizabeth A. Mauldin et al.


Malassezia infection (ketoconazole 50 mg orally once

a day) but continued to deteriorate and was euthanized

2 weeks after presentation to the referral dermatologist.

An abdominal ultrasonographic examination performed

on cat 5 showed a mass in the pancreas and multiple

masses in the liver. All cats were euthanized 3–8 weeks

following the onset of clinical signs. Cats 1, 4, 6 and 7

tested negative for FELV and FIV. Cat 3 tested negative

for FELV. Cats 2 and 5 were not tested.

All cats in group 1 had histopathological features

characteristic of paraneoplastic alopecia, which has been

described previously.18,20–23 Briefly, hair follicles were

profoundly and uniformly atrophied. Normal sebaceous

and epitrichial sweat glands were either orphaned ororientated adjacent to the remnants of hairless telogen

follicles. The epidermis was mildly to moderately hyper-

plastic. The stratum corneum was either absent or

hyperkeratotic with parakeratosis and alternating areas

of laminated orthokeratosis. Malassezia organisms were

found randomly in medium (5–15) to large groups (> 15)

among the corneocytes and intermittently admixed with

bacterial cocci (Fig. 2). In cat 6, the dermis was focally

fibrotic. In cat 7, the follicular atrophy was patchy and

irregular. Dermal inflammatory infiltrates were sparse

in all skin biopsy specimens. The dermatopathological

findings in cat 2 were particularly intriguing. The dermiscontained profoundly atrophied hair follicles and orph-

aned adnexae consistent with paraneoplastic alopecia.

In addition, features of superficial necrolytic dermatitis

(SND) with areas of marked epidermal parakeratosis,

a zone of pallor (intracellular oedema) in the upper layers

of the stratum spinosum, and basal cell hyperplasia were

seen (Fig. 3).24

Additional pathological findings included an

ultrasound-guided liver biopsy from cat 7, which con-

tained metastatic pancreatic carcinoma. Post mortem

histologic specimens from cat 2 revealed acute hepato-

cellular swelling and necrosis, and intestinal lympho-

sarcoma. Post mortem specimens from cats 1, 2 and 5confirmed the presence of pancreatic tumours (Fig. 4).

Cat 5 had massive hepatic metastases. Cats 3, 4 and 6

were euthanized because of the severity of the clinical

signs and skin condition without additional imaging or

post mortem examinations.

Group 2

The cats in group 2 were slightly younger than those in

group 1 (mean 9 years; median 9.5 years). None of the

cats were pure-bred animals. Cats 8, 9 and 10 had anacute onset of a severe, fairly generalized skin disease with

abundant crusting, scale and erosions. Cat 9 presented

with inflammation of the ears, which progressed to the

Figure 2. Cat 7, paraneoplastic alopecia; Extreme atrophy of telogen

stage follicles with orphaned epitrichial sebaceous glands and

epidermal hyperplasia (H&E, bar = 48 µm) Inset: hyperkeratosis

with Malassezia in stratum corneum (H&E, bar = 9.5 µm). Figure 3. Cat 2, superficial necrolytic dermatitis; marked epidermal

parakeratosis, a zone of pallor in the upper layers of the stratum

spinosum and basal cell hyperplasia (H&E, bar = 55 µm).

Figure 4. Cat 8, interface dermatitis; multifocal keratinocyte

necrosis in all levels of epidermis and severe hyperkeratosis (H&E,

bar = 63 µm).





neck, head and body over a 4-week period. Cats 8 and

9 had no additional diagnostics. Cat 10 had a normal

thoracic radiograph. Cat 11 developed the skin disorder

while receiving amoxicillin for an upper respiratory tract

infection. Cats 9, 10 and 11 were euthanized 4 weeks

after the onset of clinical signs, whereas cat 8 was euth-

anized within 8 weeks of onset (precise date unknown).Cats 8, 10 and 11 tested negative for FELV and FIV,

and cat 9 tested negative for FELV.

In group 2, three cases (8, 9, 10) had interface dermatitis

(Fig. 4). In all cases, the epidermis was hyperplastic and

covered by a markedly thickened and laminated corneal

layer, which varied from orthokeratotic to parakeratotic.

Individually necrotic keratinocytes were randomly dis-

tributed within all layers of the epidermis. Intracellular

oedema was multifocally noted within basilar kerati-

nocytes in the epidermis and outer root sheath of hair

follicles. A mild pleocellular inflammatory cell infiltrate

was present at the dermoepidermal interface. Large

collections of Malassezia were typically clumped in

groups between nucleate or anucleate corneocytes. In

case 11 the epidermis was moderately hyperplastic and

contained areas of hyperpigmentation with aggregates

of melanophages, due to pigmentary incontinence,

in the dermis. The superficial dermis in one section

contained a perivascular to interstitial infiltration of

eosinophils, mast cells and few plasma cells.

A definitive diagnosis could not be established for

any of the cases in group 2. Differentials for the cats

with interface dermatitis included thymoma-associated

dermatosis, erythema multiforme, drug eruption or

graft vs. host disease.24

Group 3

Cats in group 3 had localized lesions. The age range

was most variable in this group (mean, 7.4; median,

5.3). The skin lesions in these cats did not have the

degree of severity or poor outcome associated with

groups 1 and 2. In two cases, Malassezia were found

within lesions on the chin. Case 13 had chin acne. Very

few (< 5) yeast were located within the infundibulum

of one dilated hair follicle. Clinical information on

response to therapy was not available. Case 14 had

scattered yeast within the stratum corneum overlying aneoplasm (squamous cell carcinoma in situ) on the

chin. This cat was euthanized after 6 months because

the owner could not manage the lesion. The Malas-

sezia were found on review of the biopsy. This cat was

considerably older (17 years) than the others. Case 12

had scattered Malassezia within the stratum corneum

of hyperkeratotic footpads. Clinically, this cat had

diabetes mellitus and recurrent urinary tract infections

due to Enterococcus and Candida. The cat was reported

to have ulcers on the footpads but none were evident

in the histological section. The cat was treated with

oral itraconazole (10 mg kg –1, once daily) for fungal

cystitis. The footpads improved but the cat developedmarkedly elevated liver enzymes (alanine aminotrans-

ferase 2125 IU L –1, alkaline phosphatase 288 IU L –1)

3 weeks after initiation of treatment.

Case 15 had cutaneous demodicosis. All mites were

found in cross-section in the follicular infundibulum

(probable Demodex cati ). No mites were found within

the stratum corneum. Minimal inflammation was located

in the superficial dermis. The epidermis was minimally

hyperplastic. Large numbers of Malassezia (> 15/40×

field) were found within orthokeratin of the stratumcorneum. This cat had been treated with several repositol

steroid injections for facial pruritus before the his-

topathological diagnosis of demodicosis.

Case 15 tested negative for FELV and FIV, and case

13 was negative for FELV. The retroviral status of cases

12 and 14 was unknown.

DISCUSSION

Recent interest in canine Malassezia dermatitis has led

to a dramatic increase in research into the clinical and

immunological manifestations of this disorder. In con-

trast, few studies have reported the incidence or signi-

ficance of Malassezia in the cat. This may be due to the

rarity of the disease in the cat compared with the dog.

In this study, we found Malassezia in very few of the

feline biopsies (2.7%) submitted over a 23-month period.

In general, the diagnostic pathology service may be

a better estimation of skin disease in a cat population

than a clinical referral practice. Eleven of the biopsies

in our series were from veterinarians in general practice.

Two were submitted from board-certified veterinary

dermatologists in private practice, and only two were

seen at the Veterinary Hospital of the University of Pennsylvania. In this study, Malassezia was not found

in association with feline allergic disorders. The authors

estimate that at least 75% of the 550 skin biopsies

reviewed had eosinophilic dermatitides suspicious of

allergic disease. This differs slightly from a previous

histological study, which found Malassezia in 3 of 338

feline skin biopsies − two with eosinophilic granuloma

complex and one case of lichenoid dermatitis.25 The

authors recognize that biopsies with few organisms could

have been overlooked during the histopathological review.

However, neither study demonstrates a propensity of

Malassezia infection in cats with allergic disease. Thisis in sharp contrast to the dog in which M. pachydermatis

infection typically occurs in association with atopy or

other allergic disorders.1–8 Perhaps, the failure to detect

yeast in allergic cats was a result of the sampling tech-

nique. Histopathology is an insensitive method to detect

yeast organisms because of the processing of the tissue

and loss of stratum corneum. Smaller populations of

yeast may be more readily identified with tape stripping

or impression smears.25,26

In this study, the presence of Malassezia was not

associated with retroviral infections. None of the 11/15

cats tested for FIV and/or FELV were positive. This

finding contrasts a recent study, which showed thatMalassezia could be recovered more readily from

cats with retroviral infections than normal cats.15 How-

ever, this study did not document skin lesions in cats





seropositive for FELV or FIV, and it is not known if

these cats are truly at greater risk of developing clinical

signs. One cat in our study had diabetes mellitus and

recurrent urinary tract infections. These infections

were attributed to uncontrolled diabetes but no history

of retroviral testing was found in the medical record.

This cat, included in group 3, was alive 18 months afterskin biopsy.

It is very unlikely that the presence of Malassezia

had any direct effect on the lifespan of the affected cats.

However, the yeast organisms could serve as a harbinger

of a more serious disorder. The obvious limitation of

this study is the use of retrospective biopsy material.

Overall, group 2 cats had the most poorly documented

skin conditions. We speculate from the histopatholog-

ical changes that three of these cats could have TAD,

erythema multiforme or a drug reaction but this cannot

be proven. Furthermore, cat 4 could have represented

a cutaneous drug reaction or the Malassezia-associated

seborrheic dermatitis described in a previous abstract.

We feel more confident that the cats in group 1 suffered

from paraneoplastic alopecia. The clinical presentations

(dramatic weight loss, increased liver enzymes and com-

plete alopecia on ventrum with a sheen to the epidermis)

and histopathological changes were consistent and uni-

form. Four of the seven cats had confirmed neoplasia.

All cases had profound and diffuse follicular atrophy.

However, regardless of the diagnosis, all cats in groups

1 and 2 were dead within 2 months of clinical presen-

tation because of intractable skin disease and/or weight

loss and gastrointestinal signs.

There were no histopathological changes specific forMalassezia infection, and histopathological findings

varied with the underlying disorder. Hyperkeratosis

was the only change common to all biopsies. The

organism appears therefore to proliferate under condi-

tions that cause increased production of keratin. This

study also revealed one of very few cases of hepato-

cutaneous syndrome (superficial necrolytic dermatitis,

metabolic epidermal necrosis or necrolytic migratory

erythema) reported in cats. This cat had pathological

changes in the liver suggestive of an acute toxic

hepatopathy. Although this disorder has been well-

documented in dogs, particularly Terrier breeds, onlytwo cases have been reported in the cat.28,29 Interest-

ingly, one case was an 11-year-old cat with pancreatic

carcinoma. The second case was cited in a review on

thymic pathology and involved a cat with generalized

crusting and histological features of superficial necro-

lytic dermatitis. The only abnormality reported on post

mortem was thymic amyloidosis.29 Perhaps these cats

had paraneoplastic dermatoses similar to our cases in

groups 1 and 2.

Malassezia yeast were identified in a small percentage

of feline skin biopsies submitted for routine histopatho-

logical interpretation. Of those, 73% cats were euthanized

or died within 2 months. Finding yeast organisms inhistopathological specimens from cats with generalized

skin disease should prompt the clinician to rule out an

associated internal disease.

ACKNOWLEDGEMENTS

The authors thank Drs Jean Greek and James Jeffers

and the many veterinarians in private practice for their

case submissions and assistance.

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Résumé La dermatite à Malassezia spp. est rare chez le chat, et a été rapportée dans cette espèce en association

avec un immunodéficit et des tumeurs internes. Cette étude s’est intéressée à évaluer la présence et l’importance

de Malassezia spp. dans des prélèvements biopsiques soumis pour examen histopathologique. Cinq cent cin-

quante biopsies, reçues pour examen histopathologique entre janvier 1999 et novembre 2000, ont été évaluées.

Quinze (2.7%) contenaient des Malassezia dans la couche cornée de l’épiderme ou dans l’infundibulum follicu-

laire. Onze des 15 chats étaient présentés pour des lésions cutanées, d’apparition brutale, multifocales ou

généralisées. Les 11 chats ont été euthanasiés ou sont morts 2 mois après l’apparition des signes cliniques. Sept

chats présentaient des modifications histologiques et des signes cliniques évocateurs d’une alopécie paranéoplasi-

que et trois chats présentaient une dermatite d’interface évoquant un érythème polymorphe ou une dermatite

exfoliative associée à un thymome. Les lésions histologiques étaient peu spécifiques dans un cas, qui a été eutha-nasié 2 semaines après un épisode de prurit sévère et d’alopécie. Pour trois chats, les levures ont été retrouvées

sur des zones localisées (deux fois au niveau du menton, une fois sur les coussinets) sans implication clinique.

Un chat présentait à la fois des Malassezia spp. et une démodécie cutanée. Ces observations suggèrent que la

présence de levures Malassezia à l’examen histopathologique de lésions multifocales ou généralisées doit s’accom-

pagner d’une recherche approfondie de tumeur interne.

Resumen La dermatitis por Malassezia spp., una presentación infrecuente en gatos, se ha asociado previamente

a inmunosupresión y a procesos malignos internos. Este estudio evalua la presencia e importancia de Malassezia

spp. en las muestras de biopsia cutánea remitidas para examen histopatológico. Se revisaron quinientas cincuenta

muestras de biopsia cutánea teñidas con hematoxilina/eosina, remitidas para estudio histopatológico entre enero

de 1999 y noviembre de 2000. Quince muestras (2.7%) contenían organismos de Malassezia en el estrato córneo

de la epidermis o el infundíbulo folicular. Once de 15 gatos presentaban con lesiones de forma aguda de dis-

tribución multifocal a generalizada. Los 11 gatos fueron eutanasiados o murieron durante los 2 meses siguientesal inicio de los síntomas clínicos. Siete gatos tenían cambios dermatopatológicos y síntomas clínicos que apoy-

aban una alopecia paraneoplásica, y tres gatos tenían una dermatitis de la unión dermo-epidérmica sugestiva

de eritema multiforme o dermatosis asociada a timoma. Los cambios histopatológicos fueron inespecíficos en

un gato que fue eutanasiado 2 semanas después del inicio de prurito intenso y alopecia. En tres gatos, se encon-

traron Malassezia spp. en áreas localizadas (dos barbillas, una almohadilla) y parecían no tener consecuencias

en su salud general. Un gato tenía Malassezia spp. asociada demodicosis cutánea. Estos hallazgos sugieren que

la presencia de la levadura Malassezia en muestras dermatopatológicas de lesiones multifocales o generalizadas,

debería mover a realizar una analítica completa para investigar una posible neoplasia interna.

Zusammenfassung Fünfhundertundfünfzig mit Hämatoxylin und Eosin gefärbte Hautbiopsieproben, die

zwischen Januar 1999 und November 2000 eingereicht wurden, wurden untersucht. Fünfzehn (2.7%) eingereichte

Proben enthielten Malassezia Organismen im Stratum corneum der Epidermis oder im follikulären Infundibu-

lum. Elf dieser 15 Katzen wurden mit akuten, multifokalen bis generalisierten Hautläsionen vorgestellt. Alle 11

Katzen wurden euthanasiert oder starben innerhalb von 2 Monaten nach Beginn der klinischen Symptomatik.

Sieben Katzen hatten dermatopathologische Veränderungen und Symptome, die mit paraneoplastischer Alope-

zie in Einklang standen und 3 Katzen hatten eine auf Erythema multiforme oder Thymom-assoziierte Dermatitis

hindeutende Entzündung der dermo-epidermalen Grenzzone. Bei einer Katze, die 2 Wochen nach Beginn von





hochgradigem Juckreiz und Alopezie euthanasiert wurde, waren die histopathologischen Veränderungen nicht

diagnostisch. Bei drei Katzen wurden Malassezia spp. lokalisiert gefunden (2 am Kinn, eine am Fussballen) und

schienen den Gesundheitszustand nicht zu beeinflussen. Eine Katze hatte Malassezia spp. assoziiert mit

Demodikose. Diese Befunde deuten darauf hin, dass Malassezia Hefen in dermatopathologischen Proben von

multifokalen oder generalisierten Läsionen eine gründliche diagnostische Aufarbeitung für internal Neoplasien

prompt sollten.

Documents

Retrospective Study- The Presence of Malassezia in Feline Skin Biopsies. a Clinicopathological Study (Pages 7–14)