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Abstract
Forty-four nodular and noninvasive cutaneous fungal
granulomas were identified in 34 horses over a 14.5year period. Cutaneous fungal granulomas were most
common in young horses (mean age 6.1 4.2 years;
range 119 years). There was no apparent breed or sex
bias. Granulomas were either single or multiple, and
most often occurred in the skin of the head and neck.
The characteristic histological finding was a nodular
dermal mass with a mean diameter of 7.3 mm (range
2.5 20 mm) and an intact overlying epithelium. Lesions
most often exhibited intense lymphocytic inflammation,
with admixed pyogranulomatous inflammation associated with a small to moderate number of fungal
elements. Causative fungi were both pigmented and
nonpigmented organisms of variable morphology.
Penetrating plant material was identified in three
cases. Granulomas caused by nonpigmented fungi
were most common in horses from wet regions. Both
pigmented and nonpigmented fungi were found in
granulomas from horses in dry regions. Cutaneous
fungal granulomas occurred in February through
November, with peaks in April and July. No correlation
of yearly incidence with annual average temperature
or rainfall was detected. This study confirms that
equine cutaneous fungal granuloma is relatively
common in horses in the Pacific Northwest. Morphology
of causative fungi was variable, but the signalment,
266
Introduction
Cutaneous fungal infections involving skin tissue rather
than hair shafts occur in animals and in people.13 Causative
fungi are ubiquitous saprophytic organisms that include
pigmented (dematiaceous) and nonpigmented species.13
Cutaneous fungal disease in the horse can be an invasive,
ulcerative and progressive infection including pythiosis
(caused by Pythium spp.; not a true fungus, but often
included in the spectrum of mycotic disease),3 zygomycosis
(caused by various fungi in the orders Mucorales and Entomophthorales) and sporotrichosis (caused by Sporothrix
schenckii).37 However, it can also occur as nodular, nonprogressive lesions3,4,6,7 caused by numerous opportunistic
fungi.3 Pigmented fungi reported to cause nodular nonprogressive cutaneous lesions in horses include Alternaria
alternata,8,9 Madurella mycetomatis,10 Curvularia verruculosa,3 Bipolaris speciferum,3,11 Cladosporium species,3
and Exserohilum rostratum.3 Nonpigmented fungi reported
to cause localized fungal infections in horses include
Pseudallescheria boydii,3,12 Aspergillus versicolor,3,13
Alternaria tenuis,14 and Scedosporium apiospermum.15
The terminology used to define cutaneous mycoses and
to classify causative fungi is often confusing and has often
been changed.3 In the current classification scheme of
nonprogressive cutaneous mycoses, chromomycosis refers
to infection by pigmented fungi and includes infections
with both hyphal and yeast forms (phaeohyphomycosis)
and infections with fungi growing primarily as yeast forms
(chromoblastomycosis).13 Hyalohyphomycosis refers to
lesions caused by nonpigmented fungi forming hyphae.1,3
Eumycotic mycetoma (maduromycosis) refers to cutaneous infection by either pigmented or nonpigmented fungi
with characteristic tissue grains (granules) composed of
fungal hyphae and degenerate cells.3,6 Eumycotic mycetomas are typically ulcerated, with persistent discharge from
tract lesions; however, horses with cutaneous eumycotic
mycetoma do not always have draining tracts.3 Nodular
cutaneous fungal infection caused by Alternaria species in
horses has also been described as Alternaria dermatitis.3
Cutaneous fungal infections in horses have been
reported in many geographical areas, but previous reports
of nonprogressive fungal granulomas describe only a
single case or only a small number of cases.823 Equine
cutaneous nodular fungal infection has been reported to be
rare, comprising less than 0.5% of skin biopsy submissions.3
2006 The Authors. Journal compilation 2006 European Society of Veterinary Dermatology. 17; 266272
Lymphoid
predominant
Predominantly pyogranulomatous
Eosinophils
Grains
Plant material
Single
Multiple
Mean size (mm)
Mean horse age (year)
Dry climate
Wet climate
Pigmented
fungi
Unpigmented
fungi
15
26
1
1
0
1
15
5
7.4
5.3
7
4
2
1
1
2
6
4
7.2
6.5
6
17
Histopathological analysis
Microscopic sections stained with haematoxylin and eosin (H&E) and
with periodic acid-Schiff (PAS) and/or Grocotts methenamine-silver
(GMS) for fungus were examined. The lesion size for all lesions was
determined by measuring with a microscope ruler the maximum
diameter of the lesion. The nature of the inflammatory response, microscopic feature of the fungi present, and the presence or absence of
associated plant material were recorded.
Statistical analysis
The mean age and standard deviation were calculated for all horses.
The mean age of horses with single and multiple lesions, the mean
age of horses with granulomas caused by pigmented and nonpigmented fungi, and the mean diameter of lesions with pigmented
and nonpigmented fungi were compared using the Students t-test.
A P < 0.05 was considered significant. All statistical analyses were
performed using Microsoft Excel Data Analysis.
Results
One to two fungal lesions were submitted from each horse
and a total of 44 lesions from 34 horses were examined.
The characteristics of the lesions, ages of horses studied,
and climate where horses resided are summarized in
Table 1. Breeds were quarter horse (13), paint (5), crossbred
(3), thoroughbred (2), Arabian (2), Morgan (1), Norwegian
Fjord (1), appaloosa (1), haflinger (1), Friesian (1), Rocky
Mountain horse (1), and Lipizzan (1). Breed was not specified for two horses. There were 14 males and 16 females.
Sex was not specified in four cases. The age of 28 horses
was recorded. The overall mean age was 6.1 4.2 years
(range 119 years). The mean age for horses with multiple
lesions (4.8 3.6 years; range 211 years) was less than
that of horses with single lesions (6.9 4.7 years; range
119 years), but this difference was not significant
(P > 0.05). The mean age of horses with lesions associated
with pigmented fungi (5.3 2.9 years; range 119 years)
was not significantly different (P > 0.05) than the mean
age of horses with nonpigmented fungi lesions (6.5
4.7 years; range 212 years). Nineteen of 28 horses were
6 years of age or younger.
Twenty-one horses had single granulomas and eight
horses had multiple granulomas. Five additional horses
were reported to have multiple skin masses but only one
was examined histologically. Multiple granulomas were
associated with a similar type of fungus in all but one horse.
This horse had developed two lesions 6 months apart, and
one contained pigmented hyphae and one contained
nonpigmented hyphae.
The location of lesions was recorded in 29 horses.
Fungal granulomas were most commonly identified on
the head, including the lips and ears (14 lesions) and neck
(8 lesions). Less common locations were the shoulder
region (3 lesions), thorax or flank (3 lesions), leg (3 lesions),
and tail (1 lesion). Two horses with granulomas caused by
pigmented fungi were described as having generalized
skin nodules and the location was not recorded for seven
lesions. Draining tracts were not described in any case.
Granulomas caused by nonpigmented fungi were most
common on the head and neck (19/23 lesions). No site
predilection was found for granulomas caused by pigmented fungi. Lesions had been present from less than
1 week to 1.5 years prior to excision. No fungi were isolated from the one sample submitted for fungal culture.
Thirty-three horses were from Oregon and one was from
California. The month of development of fungal granuloma
was reported in 32 Oregon horses (Fig. 1). Fungal granulomas developed from February through November. Peak
months were April (five cases) and July (seven cases).
Five of six lesions occurring in February, October, or
November were in horses from dry climates.
Fungal granulomas occurred in 21 horses living in
western Oregon, an area with high average annual rainfall,
and in 12 horses living in central and eastern Oregon, areas
with low average annual rainfall (Table 1). Granulomas
2006 The Authors. Journal compilation 2006 European Society of Veterinary Dermatology.
267
Valentine et al.
Discussion
All lesions identified were localized, nodular, dermal
masses consisting primarily of inflammatory cells, frequently
with very few fungal elements. An intense lymphocytic
response was typical, and lymphocytic inflammation
formed the majority of the nodule in all but three lesions.
The three exceptions were early lesions removed soon
after development. The intensity of the lymphocytic
response was such that, until small foci of pyogranulomatous inflammation, multinucleate giant cells and
fungal elements were identified, a diagnosis of pseudolymphoma25 was often considered. Ulceration or other
alteration of the overlying skin was rare. Causative fungi
were either pigmented or nonpigmented. Tissue grains
were identified in only one of 44 lesions. Eosinophilic
inflammation, a characteristic of equine pythiosis,36 was
uncommon, and was seen only in early lesions, in one
case associated with embedded plant material.
Cutaneous fungal granulomas in horses are thought to
be most often caused by penetrating plant material or
by secondary infection of traumatized skin.3,4 There was
no history of wounds prior to granuloma formation in the
horses studied, but plant material was present in three
cases. Associated skin was not extensively ulcerated and
the plant material occurred as single fragments, deep
within the inflammatory lesions, suggesting that it was
not introduced secondarily through areas of ulceration.
The common occurrence of lesions on the head, neck, and
shoulder, supports introduction of fungi associated with
penetrating plant material, as might occur when horses
2006 The Authors. Journal compilation 2006 European Society of Veterinary Dermatology.
Figure 2. Microscopic appearance of equine cutaneous fungal granulomas. (a) Skin; horse, fungal granuloma (phaeohyphomycosis). Discrete
dermal nodular mass composed primarily of lymphocytes. There are small foci of pigmented fungi forming hyphae and yeast surrounded by a thin
rim of neutrophils, macrophages, and multinucleate giant cells. The overlying epidermis is intact. H&E. Bar = 200 m. (b) Skin; horse, fungal
granuloma (chromoblastomycosis). Pigmented fungi forming yeast bodies within a multinucleate macrophage. There is a thin rim of surrounding
neutrophils. H&E. Bar = 40 m. (c) Skin; horse, fungal granuloma (hyalohyphomycosis). Fragments of nonpigmented fungi, primarily round to oval
chlamydoconidia, with an associated granulomatous inflammatory response. H&E. Bar = 40 m. Inset: Higher magnification of irregularly septate
and branching nonpigmented fungal hyphae. Periodic acid-Schiff stain. Bar = 15 m. (d) Skin; horse, fungal granuloma (phaeohyphomycosis).
Irregularly septate and branching pigmented hyphae with an associated pyogranulomatous inflammatory response. H&E. Bar = 60 m. Inset:
Higher magnification of the causative fungi. Grocotts methenamine-silver (GMS) stain. Bar = 10 m. (e) Skin; horse, fungal granuloma (eumycotic
mycetoma; maduromycosis). Tissue grain composed of masses of indistinct thin nonpigmented fungal hyphae with associated amorphous
acellular eosinophilic material. There is surrounding pyogranulomatous inflammation. H&E. Bar = 75 m. Inset: Fungal hyphae within the grain
are faintly stained with GMS stain. Bar = 15 m. (f) Skin; horse, fungal granuloma (phaeohyphomycosis). A large plant fragment is present with
surface pigmented fungal hyphae. There is intense surrounding neutrophilic inflammation. H&E. Bar = 100 m. Inset: Higher magnification of the
fungal hyphae growing on and within the plant material (arrows). GMS stain. Bar = 50 m.
2006 The Authors. Journal compilation 2006 European Society of Veterinary Dermatology.
269
Valentine et al.
2006 The Authors. Journal compilation 2006 European Society of Veterinary Dermatology.
Acknowledgements
The authors thank Dr. Christiane Lhr for assistance with
the literature search.
16.
17.
References
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Journal 1981; 13: 2359.
8. Cabanes FJ, Abarca L, Bragulat MR et al. Phaeohyphomycosis
caused by Alternaria alternata in a mare. Journal of Medical and
Veterinary Mycology 1988; 26: 35965.
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phaeohyphomycosis in five horses associated with Alternaria
alternata infection. Veterinary Record 2001; 148: 556.
10. Van Amstel SR, Ross M, van den Bergh SS. Maduromycosis
(Madurella mycetomatis) in a horse. Journal of the South African
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11. Kaplan W, Chandler FW, Ajello L et al. Equine phaeohyphomycosis
caused by Drechslera spicifera. Canadian Veterinary Journal
1975; 16: 2058.
12. McEntee M. Eumycotic mycetoma: review and report of a
cutaneous lesion caused by Pseudallescheria boydii in a horse.
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13. Keegan KG, Dillavou CL, Turnquist SE et al. Subcutaneous
mycetoma-like granuloma in a horse caused by Aspergillus
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Rsum Quarante quatre granulomes fongiques nodulaires et non invasifs ont t identifis chez 34
chevaux sur une priode de 14.5 ans. Les granulomes cutans fongiques taient plus frquents chez des
chevaux jeunes (moyenne de 6.1 4.2 ans; variation 119 ans). Aucune prdisposition raciale ou sexuelle
na t note. Les granulomes taient uniques ou multiples, et le plus souvent localiss la peau de la face
et du cou. Les modifications histopathologiques typiques taient une masse nodulaire dermique dun
diamtre de 7.3 mm (variation 2.5 20 mm) et un pithlium intact. Les lsions prsentaient le plus souvent
une inflammation lymphocytaire massive, avec des lments fongiques en faible nombre. Les champignons
en cause taient la fois pigments ou non pigments, et dune morphologie variable. Des morceaux de
vgtaux ont galement t identifis dans trois cas. Les granulomes dus des champignons non
pigments taient les plus frquents chez les chevaux vivant en climat humide. En revanche, des granulomes champignons non pigments et champignons pigments ont t retrouvs chez les chevaux
vivant en climat sec. Les lsions taient retrouves entre fvrier et novembre, avec un pic en avril et en
juillet. Aucune corrlation na cependant pu tre retrouve pour la temprature et le nombre de jours de
pluie. Cette tude confirme que les granulomes fongiques sont relativement frquents chez le cheval dans
le nord ouest du Pacifique. La morphologie des champignons tait variable, mais lanamnse, les signes
2006 The Authors. Journal compilation 2006 European Society of Veterinary Dermatology.
271
Valentine et al.
cliniques et histopathologiques taient relativement semblables. La chirurgie dxrse a permis dans tous
les cas la gurison.
Resumen Cuarenta y cuatro granulomas fngicos cutneos nodulares y no invasivos se identificaron
en 34 caballos durante un perodo de 14.5 aos. Los granulomas fngicos cutneos fueron ms comunes
en caballos jovenes (edad media 6.1 4.2 aos; rango de 119). No se observ una aparente preferencia
basada en gnero o raza. Los granulomas fueron solitarios o mltiples, y la mayoria de ellos ocurrieron en
la piel de la cabeza y del cuello. El hallazgo histolgico ms caraterstico se defini como una masa nodular
drmica con un dimetro medio de 7.3 mm (rango 2.520 mm) y un revestimiento epitelial intacto. Las
lesiones a menudo presentaron una infiltracin linfocitaria intensa, mezclada con inflamacin piogranulomatosa asociada con un nmero de pequeo a moderado de elementos fngicos. Los hongos causantes
fueron tanto organismos pigmentados como no pigmentados de morfologa variable. Material vegetal
insertado en la herida se identific en tres casos. Los granulomas originados por hongos no pigmentados
fueron ms comunes en los caballos de regiones hmedas. Tanto hongos pigmentados como no pigmentados
se hallaron en los granulomas de caballos procedentes de regiones secas. Los granulomas ocurrieron de
Febrero a Noviembre, con picos en Abril y Julio. No se apreci ninguna correlacin entre la incidencia anual
de granulomas con la temperatura media ni con la pluviosidad. Este estudio confirma que el granuloma
equino fngico cutneo es relativamente comn en caballos del Pacfico Noroeste en los EEUU. La morfologa
del agente causal fue variable, pero la resea, historia clnica, as como las caractersticas clnicas e histolgicas
fueron muy similares. La excisin quirrgica result ser curativa.
Zusammenfassung Vierundvierzig nodulre und nichtinvasive kutane Pilzgranulome wurden bei 34
Pferden ber einen Zeitraum von 14.5 Jahren identifiziert. Kutane Pilzgranulome waren am hufigsten bei
jungen Pferden (Durchschnittsalter 6.1 4.2 Jahre; Spannweite 119 Jahre). Es bestand kein aufflliger
Rassen- oder Geschlechtsunterschied. Die Granulome traten entweder einzeln oder multipel auf und
kamen am hufigsten in der Haut des Gesichts und Halses vor. Der charakteristische histologische Befund
war eine nodulre dermale Masse mit einem durchschnittlichen Durchmesser von 7.3 mm (Spannweite
2.5 20 mm) und einem intakten bergelagerten Epithel. Die Vernderungen zeigten am hufigsten eine
massive lymphozytre Entzndung, mit Beimischung einer pyogranulomatsen Entzndung, die mit einer
kleinen bis moderaten Anzahl von Pilzelementen assoziiert war. Die Erreger waren sowohl pigmentierte als
auch unpigmentierte Pilz-Organismen von variabler Morphologie. Durchdringendes Pflanzenmaterial wurde
in drei Fllen identifiziert. Granulome aufgrund von nichtpigmentierten Pilzen kamen am hufigsten
bei Pferden aus nassen Regionen vor. Sowohl pigmentierte als auch unpigmentierte Pilze wurden in
Granulomen von Pferden aus trockenen Gegenden gefunden. Die kutanen Pilzgranulome kamen von
Februar bis November vor, mit Hchstwerten im April und Juli. Es konnte keine Korrelation festgestellt
werden zwischen der jhrlichen Hufigkeit und der durchschnittlichen Jahrestemperatur bzw. Niederschlag.
Diese Studie besttigt, dass equine kutane Pilzgranulome relativ hufig bei Pferden im pazifischen Nordwesten auftreten. Die Morphologie der verursachenden Pilze war variabel, aber Signalement, die Anamnese,
die klinischen und allgemeinen histologischen Charakteristika waren sehr hnlich. Chirurgische Entfernung
war heilend.
272
2006 The Authors. Journal compilation 2006 European Society of Veterinary Dermatology.