Malassezia dermatitis: an opportunist attacks and a host responds
Daniel O. Morris, DVM, Diplomate, ACVD
Asst. Professor and Chief of Dermatology & Allergy
University of Pennsylvania, Philadelphia, PA USA
Background: Yeast of the genus Malassezia (formerly Pityrosporum) are lipophilic,
non-mycelial, unipolar fungi that occur as commensal organisms on the skin of
vertebrates. The two originally described species, M. pachydermatis and M. furfur, have
been studied extensively as animal and human opportunistic pathogens, respectively.
The now well-established association between M. pachydermatis and canine and feline
dermatoses requires a working knowledge of the host/pathogen relationship by all
veterinarians, but especially by veterinary dermatologists.1-4
Microbiology/Ecology: The genus Malassezia is now described to consist of seven
lipid-dependent (M. furfur, M. sympodialis, M. globosa, M. obtusa, M. restricta, M.
sloofiae, M equi) and one non-lipid-dependent species (M. pachydermatis).5,6 The latter,
while not exhibiting an absolute requirement for lipid, is still enhanced by the addition of
lipid substrates to the culture media. Lipophilic organisms exhibit the unique capability
of utilizing lipid as a source of carbon. Malassezia yeasts are characterized by a thick,
multilayered cell wall and the production of blastoconidia by repetitive monopolar (or
sympodial) budding. This gives them the appearance of unshelled peanuts. M.
pachydermatis is easily cultured from the non-inflamed skin of normal dogs but is quite
difficult to demonstrate by cytological techniques (direct impression smear, cotton-tip
swab, dry skin scrapings) of these same normal dogs.7 The yeast has also been localized
to the distal hair shaft, where it may occur as a commensal, but its presence in the hair
follicle infundibulum is rare.8 The yeast is best cultured at 37oC on lipid-enhanced
Saubaraud’s dextrose/glucose media at 5% CO2, although microaerophilic conditions are
not mandatory.9 Optimum growth is typically achieved by 72 hours, when individual
colonies can be counted (prior to confluence). Techniques to obtain culture samples will
vary according to purpose. For quantitative cultures, the tape-strip method, detergent
scrub method, or contact plate method can be applied.7,10,11 These allow estimation of the
number of colony-forming organism per unit of skin surface area. A sterile swab of the
skin surface or ear canal exudates is also quite successful in isolating the organism. Since
the yeast is a commensal on normal skin, a positive culture result cannot necessarily be
equated with “infection”.
The genus Malassezia can be speciated by either phenotypic and biochemical
characteristics12, or by molecular mechanisms.13 Such laboratory tests are germane to the
epidemiological study of yeast species and strains, especially in zoonotic outbreaks. In
regards to zoonosis, M. pachydermatis is known to cause life-threatening fungemia in
immunocompromised human infants and adults, and the point source of some infections
have been traced to pet-owning health care workers.14,15 A large epidemiological study
of normal dogs, atopic dogs with Malassezia dermatitis (MD) and their respective owners
is currently being conducted by the author. Paired isolates from dogs and their human
companions will be characterized by pulsed-field gel electrophoresis (“genetic
fingerprinting”) to search for concordance of genetic identity. Even at the sub-species
level, various strains are becoming recognized that could potentially behave in clinically
distinct manners.16,17a
Clinical manifestations of Malassezia overgrowth: While isolated from species as
diverse as the rhinoceros and ferret,17b clinical disease manifestations have been studied
in relatively few species. In dogs, cats, and human beings, Malassezia yeast contribute to
the pathogenesis of several disease states, including seborrheic dermatitis, atopic
dermatitis (AD), endocrine/metabolic diseases, and disorders of cornification.
Occurrence of several Malassezia spp. from normal horses and domestic ruminants
(cattle, sheep, and goats) has been reported, and lipid-dependent species were isolated
more frequently (42%) than M. pachydermatis (3%).18 Occurrence in the external ear
canals of normal swine is also known, and a single strain was shown to have colonized a
herd of pigs on one isolated farm.19
In dogs, the role of M. pachydermatis in the atopic dermatitis phenotype has been
well described clinically and to some degree, immunologically (see below). The
inflamed skin and ear canals of dogs with AD often harbor increased numbers of yeast
(compared to the skin of normal dogs), and specific antifungal therapy will ameliorate a
large portion of the pruritus experienced by many of these dogs. Malassezia overgrowth
is also associated with primary (idiopathic) seborrhea of dogs (especially in Basset
hounds, Cocker spaniels, Dachshunds, and West Highland White terriers).2,3,20 A
correlation with recent antibiotic treatment has also be documented.2
M. pachydermatis is commonly associated with otitis externa. Protein profiling of
M. pachydermatis isolates from dogs has shown that there is generally no difference
between strains of epidermal versus otic origin.21 There appears to be an increased
incidence of Malassezia overgrowth in dogs with allergic and seborrheic otitis,
endocrinopathies, and iatrogenic immunosuppression. However, it is also commonly
seen in general practice occurring in otherwise normal dogs, but after swimming or
bathing (ie, water trapping or “swimmer’s ear”).
While rare, it has also been reported that M. pachydermatis can promote oral
pathology (stomatitis, pharyngitis, tonsillitis).22 Occurrence in the oral cavity is
considered to be normal,23 but oral cavity populations actually decreased in a group of
seborrheic Basset hounds that were being treated with topical antifungal shampoos for
Malassezia dermatitis.24 This suggests either that oral populations reflect direct transfer
of cutaneous inhabitants to the oral cavity during licking, or that transfer of the antifungal
from the hair coat to the oral cavity was therapeutic.
While a definitive relationship between Malassezia yeast and atopic dermatitis
has not been described in cats, it has been reported to be associated with feline chin acne,
otitis externa, and pruritic/inflammatory dermatoses.25,26a Certainly, it is a known
commensal of feline skin.26b In a recent review of 550 feline skin biopsies, Malassezia
spp. were most commonly associated with feline paraneoplastic alopecia and thymomaassociated dermatosis/erythema multiforme.27 All cats with histology consistent with
these underlying systemic diseases had died within 8 weeks of skin biopsy sampling. In
contrast to a prior report,28 there were no biopsy samples in this series in which the yeast
were associated with an inflammatory reaction pattern typical of feline allergic skin
disease. As this report was a retrospective study of archived biopsy specimens, it did not
evaluate the cytological status of the same cats. Still, it is recommended that cats with
Malassezia dermatitis be evaluated for internal/systemic diseases, especially when the
clinical picture is not suggestive of allergic dermatitis.
While anecdotal reports have suggested a role for Malassezia on avian skin
(especially in association with feather picking in Psittacine birds), a pilot study which
evaluated feather follicles and feather pulp cytologically, histologically, and by culture
failed to reveal any yeast.29 A larger scale study in which normal and picking Psittacines
are sampled by tape-strip cytology and tape-strip quantitative culture techniques is
currently under way within the author’s clinical group at the University of Pennsylvania.
Pathogen-dependent immunological factors: In dogs, as in human beings, Malassezia
yeast are known to produce allergens which, upon percutaneous absorption, contribute to
the inflammatory reaction in the skin via a Type-1 hypersensitivity response (see host
immunological responses below). The yeast are also capable of fixing complement
through the alternate pathway, which may result in inflammation via the production of
anapylatoxins (C3a, C4a, C5a).30 This mechanism is a non-specific reaction and should
be capable of occurring in any animal with yeast over-growth and compromised stratum
corneum barrier function. Perhaps this is the case in non-atopic animals with dermatitis
secondary to Malassezia overgrowth. Dermatologists commonly observe highly
inflammatory Malassezia infections occurring in cases of zinc-responsive dermatosis,
generic dog food dermatosis, cutaneous T-cell lymphoma, and canine Cushing’s disease
in which allergic diseases are absent.a
Studies of human keratinocytes, incubated with different Malassezia species,
indicate that cytokine production is provoked by the yeast, and that different species
induce heterogenous responses. Interestingly, the species Malassezia furfur, a normal
commensal of human skin, did not induce inflammatory cytokines, while M. pachydermatis and other “non human” species did.31
Pathogen virulence factors: Several virulence factors also contribute to the ability of
the yeast to survive and proliferate on the skin. Adherence to corneocytes is thought to
play an important role in the colonization and infection of the skin by the yeast. It is
known that M. pachydermatis is capable of adhering to canine corneocytes via trypsinsensitive proteins or glycoproteins and mannosyl-bearing carbohydrate ligands on yeast
cell walls.32,33 Knowing the specific adherence factors might allow intervention by use of
ligand inhibitors. However, marked variability between yeast strains may limit
identification of a universal inhibitor.33 In otic infections, adherence to corneocytes
appears to be mediated through lipid ligands rather than carbohydrate moieties.34 In
human skin, adherence of M. furfur is increased by elevated skin temperature (as would
be the case with inflammatory dermatoses), and is not hindered by concurrent
Staphylococcal colonization.35
Malassezia yeast are also capable of hydrolyzing lipids to free fatty acids in the
sebum film. FFA’s are inhibitory to other microorganisms and therefore may help
protect the yeast from competition.36 Production of proteinase, chondroiton-sulphatase,
phospholipase, and hyaluronidase by M. pachydermatis isolates from dogs37 may serve as
a
ACVD/AAVD roundtable on Malassezia dermatitis; 1998, San Antonio, TX
mediators of keratin invasion or (as in the case of proteinase) mediate the sensation of
pruritus which is provoked at free nerve endings in the skin.
Although an initial report38 suggested that M. pachydermatis may promote
epidermal hyperplasia (a well known histological feature of Malassezia dermatitis39), a
recent study argues against this theory, as yeast culture supernatants and yeast cell
extracts failed to stimulate cultured canine corneocytes.40
Host factors -- skin surface microclimate: In dogs, cats, and human beings, Malassezia
yeast colonize the skin during the immediate perinatal period.41-43a In a canine study,
yeast was present as early as 3 days after birth, colonizing the lips, nailbeds, and external
ear canals of 22 Rottweiler puppies (39.4% of tape-strip samples). In a Devon Rex
cattery in Western Australia, waxy paronychial exudates loaded with yeast were
identified within several hours of birth in kittens. b In dogs and cats, it is apparent that
alterations in the skin’s surface microclimate contribute to susceptibility to overgrowth of
Malassezia yeast. The yeast colonizes moist areas of the skin and mucosa of normal dogs
in higher numbers than in more densely haired areas.7 In human beings, increased M.
furfur numbers are directly correlated with increased sebum film at the skin surface (i.e.,
head and neck).43b Increased M. pachydermatis numbers on seborrheic canine and
feline skin is the veterinary homologue. The ear canals, which express a higher
temperature and humidity than the skin, are a very favorable environment for yeast
growth, and the lipid-rich cerumen is also supportive.44 In fact, the propensity for yeast
to be the etiological agent (as opposed to bacteria) in otitis externa appears to depend
more upon the fatty acid composition of the canal than the pinnal shape. Even though the
incidence of otitis externa in general is significantly higher in dogs with pendulous
pinnae than in those with erect pinnae, there is no statistical difference between these
morphological types in the occurrence rate of yeast otitis specifically.45
It has been shown experimentally that the addition of sterile saline to the canine
ear canal can result in Malassezia otitis without predisposing inflammation.46 Similarly,
the author has noted a higher incidence of primary Malassezia otitis and pododermatitis
(in otherwise normal dogs) living in a humid coastal climate than in dogs living in more
arid and temperate climates.
Host factors -- immunological responses: In human beings with atopic dermatitis,
hypersensitivity to Malassezia furfur (formerly Pityrosporum ovale and P. orbiculare)
has been confirmed by several independent groups, utilizing intradermal allergy testing47
as well as skin prick testing,48-51 the atopy patch test,49,52 and in-vitro demonstration of
anti-Malassezia furfur IgE by ELISA and RAST techniques.48,53-58 Furthermore, the cellmediated immune response to M. furfur has also been investigated, where both the
peripheral blood mononuclear cell (PBMC) response and the in-situ (dermal) lymphocyte
response to yeast extracts have been characterized in-vitro in patients with AD.48,59-62 In
addition, the cytokine profiles of the responding lymphocytes have been reported in some
of these studies. Both the PBMC and in situ populations, when isolated from AD
patients, show increased blastogenic responses. However, human beings with seborrheic
dermatitis do not show an altered PBMC response to Malassezia furfur when compared
to normal subjects.63
b
Personal communication: Dr. Mandy Burrows, Murdoch University, Perth, W.A.
The canine immune response has been characterized in a similar fashion, albeit in
more limited studies. Type-1 hypersensitivity responses (wheal and flare) to M.
pachydermatis have been demonstrated after intradermal injection.4,64,65 However,
delayed reactions were absent in most atopic dogs.4,64 In seborrheic Basset hounds,
which often show marked Malassezia overgrowth without an atopic constitution,
immediate reactivity to M. pachydermatis extracts is not significant compared to normal
Bassets. This lack of immediate hypersensitivity, along with the blunted cell-mediated
response noted in seborrheic Bassets (see below) may indicate an overtly different
pathomechanism for MD associated with seborrheic dermatitis.66 Atopy patch testing
utilizing yeast extracts has not yet been reported in dogs.
Recently, anti-Malassezia IgE and IgG has been described in a population of
atopic dogs.67 Passive transfer of cutaneous anaphylaxis by the serum of atopic dogs
with MD (performed in the author’s laboratory) confirms that canine anti-Malassezia IgE
is pathogenic in-vivo.68 Another group has characterized several major allergens of M.
pachydermatis recognized by canine serum (via Western Blot analysis).69 A major
allergen is an allergenic epitope recognized by at least 50% of an allergic population.
Currently, 9 allergens of M furfur recognized by IgE from the sera of atopic humans have
been characterized.70-73
The PBMC responses of normal dogs, atopic dogs with MD, atopic dogs with
Malassezia otitis, and atopic dogs free of yeast infections have been compared. Atopic
dogs with MD had an increased lymphocyte blastogenic response to crude M. pachydermatis extract as compared with clinically normal dogs and dogs with Malassezia
otitis. However, atopic control dogs did not differ significantly in their responses when
compared with the responses of dogs with MD or Malassezia otitis.74 These atopic dogs
with MD also had a significantly increased CD4:CD8 ratio versus normal dogs, while
atopic dogs without MD were not different from normal dogs.74 The PBMC response of
atopics with MD contrasts to seborrheic Basset hounds with high M. pachydermatis
counts on the skin: these dogs had significantly lower PBMC reactivity to M.
pachydermatis extract than did clinically normal Basset hounds, suggesting an impaired
cell-mediated immune response to the yeast in seborrheic dermatitis.75 These findings,
considered in parallel, support a role for T-cell hyper-responsiveness to M.
pachydermatis as part of the atopic paradigm in dogs.
One odd caveat, mentioned in the study of PBMC response by atopic dogs,
occurred in the Malassezia otitis group. The decreased PBMC activity to M.
pachydermatis extracts in the otitis group (vs. atopic controls and atopics with MD) may
suggest that the waxy microenvironment of the external ear canal provides a protective
effect against T-cell/antigen interaction.74
A role for superantigens in canine MD has also been hypothesized. Superantigens
are microbial products capable of binding a large repertoire of T-cell receptors that share
common V regions without regard for other binding determinants. This allows
activation of as much as 5-30% of the entire T-cell population.76 A role for Malassezia
superantigens has now been ruled out in human atopic dermatitis.77 Similar studies are
planned for canine T-cells in the author’s laboratory.
Future therapies: For the time being, the clinical manifestations of Malassezia
dermatitis must be dealt with using topical and systemic antifungal agents.26,78 It is the
author’s hope that immunotherapy may palliate the hyper-responsiveness of atopics to
Malassezia allergens. Such studies, if done properly, will require double-masked,
placebo-controlled clinical trials that last a minimum of 12 to 18 months. It is already
known that M. furfur and M. pachydermatis express some of the same major allergens
(for human beings) in common.79 If it is found that allergic dogs and humans recognize
the same common allergens of Malassezia sp. yeast, recombinant allergens would be the
purest products for utilization in IDT and immunotherapy protocols. For the immediate
future, Greer Laboratories has recently introduced an M. pachydermatis allergen for IDT
and immunotherapy. It will be necessary to characterize the host immune response to the
extract itself, as well as to the major M. pachydermatis allergens, whether or not this
commercial extract is clinically useful as an immunotherapeutic.
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