Seasonal 4-year investigation into the role of the alpine

marmot (Marmota marmota) as a carrier of zoophilic

dermatophytes

M.G. GALLO*, P. LANFRANCHI$, G. POGLAYEN%, S. CALDEROLA§, A. MENZANO*, E. FERROGLIO* &

A. PEANO*

*Dipartimento di Produzioni Animali, Epidemiologia ed Ecologia, Sezione Parassitologia e Malattie Parassitarie, Grugliasco,Turin, $Dipartimento di Patologia Animale, Igiene e Sanita Pubblica, Sezione di Patologia Generale e Parassitologia, Milan and%Dipartimento di Sanita Pubblica Veterinaria, Sezione di Parassitologia e Malattie Parassitarie, Messina, Italy, and §ResearchInstitute for Wildlife Ecology, Veterinary Faculty, Vienna, Austria

Two hundred and six samples of alpine marmot (Mamota marmota) hair (148 from

adults and 58 from young subjects), 102 soil samples from the entrances to the

burrows of the above individuals and 20 control specimens (obtained from

adjoining areas away from the burrow systems where the rodents are not usually

present) were examined from May 1994 to September 1997. Seventy-five isolates

belonging to six species of dermatophytes were found in 69 of the 206 hair samples

examined (33.5%). Two species were zoophilic, Microsporum canis (7.8%) and

Trichophyton mentagrophytes (11.2.%), and four geophilic, Microsporum cookei

(2%), M. gypseum (5.8%), Trichophyton ajelloi (3.9%) and T. terrestre (5.8%). The

prevalence of each species in the hair samples did not change significantly

according to year, season (chi-squared test [limit significance: P B/0.05] gives no

significant values [P�/0.05] both in year and in season comparison) or age/sex

(adult versus juvenile: P�/ 0.1; male versus female: P�/0.8) of the marmot.

Twenty-three of the 102 soil samples (22.5%) were positive for dermatophytes

found in the hair of marmots from the same burrow systems.

Five of the 20 control soil samples (25%) were positive for dermatophytes. One

isolate of M. gypseum , three of T. terrestre and one of T. mentagrophytes were

obtained.

Compared with other free-ranging rodent hosts studied in Europe, this

mycoflora is characterized by the presence and relatively high prevalence of M.

canis, frequently reported in symptomatic and asymptomatic cats, dogs and fur

animals. M. canis has not been isolated in other rodents in the wild. However, it

has recently been reported in asymptomatic foxes (Vulpes vulpes) from northern

Italy. The close link between V. vulpes and M. marmota , with the former

representing the most important mammal predator of the latter in the Alps (only

a fraction of the predator’s attacks result in the death of the rodent) may have

favoured the adaptation of M. canis to this rodent host. The stable character of the

The procedures followed during this study conform to the current

laws regulating such research in Switzerland.

Correspondence: Maria Grazia Gallo, Dipartimento di Produzioni

Animali, Epidemiologia ed Ecologia, Sezione Parassitologia e

Malattie Parassitarie, Via Leonardo da Vinci 44, I-10095

Grugliasco, Torino, Italy. Tel: �/39 0116 709001; Fax �/39 0116

709000; E-mail: mariagrazia.gallo@unito.it

Received 15 April 2004; Accepted 3 August 2004

– 2005 ISHAM DOI: 10.1080/13693780400008282

Medical Mycology June 2005, 43, 373�/379

Med

Myc

ol D

ownl

oade

d fr

om in

form

ahea

lthca

re.c

om b

y R

adbo

ud U

nive

rsite

it N

ijmeg

en o

n 12

/17/

14Fo

r pe

rson

al u

se o

nly.

M. canis/M. marmota relationship (no seasonally or annually related difference in

the prevalence of this dermatophyte has been found) suggests the inclusion of the

alpine marmot in the reservoir of this zoophilic pathogenic agent. In this situation,

hibernation in labyrinthine burrow systems, where temperature and moisture

ranges are quite uniform the whole year round, may favour the viability of M. canis

arthroconidia, whose survival in mountain habitat might otherwise be compro-

mised. This seems to be confirmed by the fact that the fungus has never been found

in the control samples collected at a distance of 300 m from the outer edge of the

sampled burrow systems.

Keywords alpine marmot, dermatophytes, burrow soil, Microsporum canis,

zoonotic agents

Introduction

Surveys on keratinophilic fungi have been carried out

examining many wild species in several European

countries [1�/7]. Most of them deal with rodents or

foxes, observed both as affected animals or carriers of

these fungi [1�/3,6,8,9,11,12]. Some authors also point

out the zoonotic aspect revealed by their studies [6,11�/

17]. Until now only two surveys have referred to the

alpine marmot as a carrier of keratinophilic fungi

[17,18]. However, neither of these studies, both carried

out in the Italian Alps, investigates marmot hair, but

only the soil outside the entrance to the animals’

burrows. Marmots are a very common inhabitant of

the Alps and they share their environment both with

wild animals (especially foxes, small mammals and

ungulates) and domestic ones (such as cattle, sheep and

sheepdogs).

Moreover, the marmot’s home range is often found

in tourist resorts where the marmots have, to some

extent, adapted fairly well to man [19], making

indirect contact between marmots and humans possi-

ble. The alpine marmot is a very social species [20]

which spends 6 months of the year in hibernation in

complex, labyrinthine burrow systems, creating a soil

substrate enriched in keratinic particles, which Man-

tovani has called ‘animalized soil’ [21]. Here the

temperature and moisture ranges are quite uniform

all the year round [22] and most probably suitable for

the survival and circulation of fungi such as derma-

tophytes.

The aim of the present survey, therefore, is to

investigate the presence and the epidemiological role

played by alpine marmot colonies in the diffusion of

dermatophyte fungi, with particular reference to zoo-

philic dermatophyte fungi.

Materials and methods

Habitat and field of research

This survey was carried out in Bivio, a winter tourist

resort in the Engandine region of the Canton of

Graubunden in the Rhaetian Alps of eastern Switzer-

land (46828?N/9841?E).

The study field was a rectangular, south-facing area

of a roughly 5 ha pasture from 1950 to 2000 m above

sea level. The climate and vegetation are typical of the

high alpine habitat. From November until the end of

April, the area is mostly covered by snow. In summer,

the area is populated by livestock, especially cattle and

sheep, with man present to tend the livestock. Roe deer

live in this territory the whole year round, while red

deer, ibex and chamois are found only in spring. Fox

and small mammals are also present.

The socio-economic implications of mountain live-

stock rearing in the area studied provided the oppor-

tunity for the present investigation. The damage caused

by marmot activity to high-value pastures led the

Game and Fishing Inspectorate of the Canton of

Graubunden to initiate a culling programme as part

of its Regional Pest Control Project. No animal

selection was made, as culling applied to all marmots

found within range of fire. According to the data listed

on individual cards, all animals were of normal weight

and healthy. None was found to be affected by

dermatophytosis. A multidisciplinary project was car-

ried out on the marmots culled.

Hair samples

From 1994 to 1997, 206 hair samples were collected in

spring (May), summer (July) and autumn (September)

from the marmots culled.

– 2005 ISHAM, Medical Mycology, 43, 373�/379

374 Gallo et al.

Med

Myc

ol D

ownl

oade

d fr

om in

form

ahea

lthca

re.c

om b

y R

adbo

ud U

nive

rsite

it N

ijmeg

en o

n 12

/17/

14Fo

r pe

rson

al u

se o

nly.

The age of the marmots was calculated by dental

eruption and body dimensions following Ratti [23] anddivided into two age classes: juvenile (B/12 months old)

and adult (]/12 months old). In total, 206 hair samples

were collected, 148 samples from adults (78 male, 70

female) and 58 from young subjects.

The marmots were brushed before any other body

examination was carried out, to avoid contamination.

The procedure was essentially the same as that

described by Mackenzie [24]. Each animal was brushedall over using a sterilized plastic hair brush measuring 8

cm in diameter. None of the marmots showed clinical

signs of dermatophyte infection. The brushes were sent

to the mycological laboratory of the Department of

Animal Production of the University of Turin, Italy,

where each of them was pressed into a Petri dish

containing Sabouraud’s dextrose agar supplemented

with chloramphenicol (0.05 g/l) and cycloheximide (0.5g/l). The hairs left on the brush were inoculated on a

second agar plate using sterile forceps as described by

Okafor and Gugnani [25]. All the plates were incubated

at 288C and examined daily for 45 days.

Soil samples

In 102 cases, the marmots were culled at the entrance totheir burrows and a soil sample was collected from in

front of the burrow entrances. Twenty control speci-

mens were obtained by sampling soil from adjoining

areas 300 m away from the outer edge of the burrow

systems where the rodents are not usually present. (The

Alpine marmot does not usually move more than

200�/250 m from its burrow system.) Each soil speci-

men, weighing 100 g, was taken by scooping the top 2cm of surface soil likely to be rich in organic matter and

put directly into a paper bag to keep the soil dry and to

avoid dermatophyte growth before laboratory culture.

These specimens were each divided into five sub-

samples, each weighing 20 g, which were placed in a

sterile 10-cm diameter Petri dish and processed by

Vanbreuseghem’s method [26] using short pieces

(7�/12 mm) of horse hair as keratinic bait. Thisprocedure was modified by the addition of horse hair

powder obtained from ground sterile hair; 0.5 g was

uniformly mixed with the contents of each Petri dish

while a further 0.5 g was sprinkled on the surface of the

samples to increase the amount of keratinous material

available for the keratinophilic fungi.

The samples were moistened with sterile distilled

water, incubated at 288C and kept moistened as needed.The inoculated dishes were examined three times a

week for 2 months. When the hair fragments showed

good fungal growth, they were microscopically exam-

ined for preliminary morphological identification. Sub-

sequently, the pieces of positive hair were transferred toSabouraud’s dextrose agar medium supplemented with

chloramphenicol (0.05 g/l) and cycloheximide (0.5 g/l),

and kept at 288C for 45 days to obtain pure cultures for

identification.

Fungus identification

Fungus identification was carried out both on hair and

soil samples by observing the macroscopic and micro-

scopic features of the tallus, the colony characteristics

and the asexual reproductive structures (macro- and

microconidia). When needed, slide culture technique

was employed to facilitate detailed observations ofmicroscopic morphology. Each isolate was identified

following the analytical keys given by Rebell and Taplin

[27] and de Hoog et al . [28].

Statistical analyses

Differences between categorical data were compared by

the chi-squared test (limit significance: P�/0.05), when

necessary by kappa statistics and general agreement

(McNemar test) with a 95% confidence interval.

Results

In total, 75 isolates of dermatophytes were cultured

from 69 (33.5%) of the 206 marmot hair samples

examined. Of the six species identified, two were

zoophilic: Microsporum canis (7.8%) and Trichophyton

mentagrophytes (11.2%), and four geophilic:

Microsporum gypseum (5.8%), M. cookei (1.9%),

Trichophyton terrestre (5.8%) and T. ajelloi (3.9%)(Table 1).

Infection was monospecific in 63 positive samples

(91.3%) while the following associations were observed

in the remaining six samples: T. mentagrophytes�/

M. gypseum (two samples each); and T.

mentagrophytes�/M. canis ; M. gypseum�/T. ajelloi ;

Table 1 Presence of dermatophyte fungi and their prevalence in 206

marmot hair samples collected at Bivio, Canton of Graubunden,

Switzerland, during a 4-year investigation (1994�/97)

Species No. isolates Prevalence (%)

Microsporum canis 16 7.8

Microsporum cookei 4 1.9

Microsporum gypseum 12 5.8

Trichophyton ajelloi 8 3.9

Trichophyton mentagrophytes 23 11.2

Trichophyton terrestre 12 5.8

– 2005 ISHAM, Medical Mycology, 43, 373�/379

Alpine marmot as a carrier of zoophilic dermatophytes 375

Med

Myc

ol D

ownl

oade

d fr

om in

form

ahea

lthca

re.c

om b

y R

adbo

ud U

nive

rsite

it N

ijmeg

en o

n 12

/17/

14Fo

r pe

rson

al u

se o

nly.

M. cookei�/T. terrestre ; M. canis�/T. ajelloi (one

sample each). In addition, four strains of Chrysospor-

ium spp. were obtained.

The prevalence of positive hair samples did not

change according to year or season (Table 2; chi-

squared limit of significance: PB/0.05), host age

(36.5% of positive adults versus 25.9% of positive

juveniles: P�/ 0.1) or sex (35.0% of positive males

versus 37.1% of positive females: P�/ 0.8).

Dermatophytes were isolated from 23 of the 102 soilsamples (22.5%) collected from the entrances to the

burrows. The same six species identified in the hair

samples were found: M. canis, T. mentagrophytes and

T. terrestre each with six samples (5.9%), M. cookei

with three (2.9%) and T. ajelloi with one (0.9%). A

single dermatophyte species was present in 22 positive

samples (95.6%), while the association T. menta-

grophytes�/T. terrestre was observed in one sample.Eight isolates of Chrysosporium spp. were also ob-

tained.

The prevalence of dermatophytes in contaminated

soil samples decreased in summer for all the species

found, except for M. canis which remained unchanged

(Table 3). Application of the chi-squared test shows

that the summer decrease of dermatophyte fungi in the

soil is due to the decrease of geophilic fungi (zoophilicversus geophilic fungi: P�/0.005), whereas the presence

of a dermatophyte species both in hair and in the soil

from the corresponding burrow was significantly

and positively correlated for M. canis (P B/0.01),

M. gypseum (P B/0.01) and T. terrestre (P�/0.01). No

correlation was found for T. mentagrophytes and

Chrysosporium spp. Data regarding M. cookei and T.

ajelloi were deemed insufficient for a statistical check.Moreover, the correlation between all dermatophytes

harboured in the marmot hair and those found in the

soil collected from the entrance to the corresponding

burrows was calculated using kappa statistics and

general agreement. Whereas the first test indicates

borderline intermediate values (kappa: 0.38, CI�/0.18

and 0.59) [29], the second gives significant values(McNemar test: P�/0.0011).

Five of the 20 control soil samples (25%) were

positive for dermatophytes. One isolate of M. gypseum ,

three of T. terrestre and one of T. mentagrophytes were

obtained.

Discussion

Dermatophytes, both geophilic (M. cookei , M. gyp-

seum , T. terrestre, T. ajelloi ) and zoophilic (M. canis

and T. mentagrophytes ) were found on the fur of

Marmota marmota . M. cookei and T. ajelloi were

occasional findings, whereas M. canis, M. gypseum,

T. mentagrophytes and T. terrestre were repeatedlyfound in fur cohorts from different seasons and years.

T. mentagrophytes, T. terrestre and M. gypseum were

found in the marmot hair, in the burrow soil and in the

samples taken from the control areas. Some remarks

are worth making about these findings.

The presence of zoophilic T. mentagrophytes, whose

recognized carriers are rodents, was to be expected.

Besides marmot, other sympatric rodent hosts maycontribute to the persistence of this fungus in the

habitat studied, including the control areas, for exam-

ple Apodemus sylvaticus and Clethrionomys glareolus.

These two hosts have frequently been implicated in the

spread of T. mentagrophytes elsewhere [6].

Similarly, it is likely that these rodents participate in

the spread of T. terrestre [6,11], whose possibilities of

isolation, it would seem, are influenced little by soilcomposition [30,31], unlike some other geophilic der-

matophytes, for example M. gypseum [32]. This may

explain why T. terrestre is found to be as prevalent in

the control soil as in the marmot fur and environment.

The presence of domestic and wild ungulates may

play a fairly important role, as they enrich the soil with

organic matter. Such a habitat is particularly favourable

Table 2 Yearly and seasonal dermatophyte-positive samples, and their prevalence (%), obtained from hair of 206 culled marmots at Bivio,

Canton of Graubunden, Switzerland, during a 4-year investigation (1994�/1997)

Year No. samples

examined

Positive

samples (%)

Season No. samples

examined

Positive

samples (%)

1994 46 15 (32.6) Spring 63 22 (34.9)

1995 40 13 (32.5) Summer 93 30 (32.2)

1996 64 22 (34.3) Autumn 50 23 (46.0)

1997 56 19 (33.9)

Chi-squared test gives no significant values (P �/0.05) both in year and in season comparison.

– 2005 ISHAM, Medical Mycology, 43, 373�/379

376 Gallo et al.

Med

Myc

ol D

ownl

oade

d fr

om in

form

ahea

lthca

re.c

om b

y R

adbo

ud U

nive

rsite

it N

ijmeg

en o

n 12

/17/

14Fo

r pe

rson

al u

se o

nly.

for M. gypseum [32] and justifies its presence also in the

samples taken from the control areas.Compared with other studies of European free-

ranging rodents, the mycotic flora obtained in this

survey is characterized by the presence and relatively

high prevalence of M. canis. This species is usually

reported world-wide in symptomatic and asymptomatic

cats, dogs and fur animals [33�/36] as well as in

synanthropic species (Rattus rattus, Rattus norvegicus

and Mus musculus) within heavily anthropogenic areas[36]. M. canis has not been isolated in other free-

ranging small mammals [3,4,6,10,12] nor in wild boar

in Europe [8], but it has been reported in asymptomatic

wild foxes (Vulpes vulpes ) in northern Italy [8,9]. The

close ecological link between V. vulpes and M. mar-

mota , with the former representing the most important

mammal predator of the latter in those alpine areas

where the two share the same territory, [37,38] mayhave favoured the apparent adaptation of M. canis to

this rodent host. As only a fraction of the predator’s

attacks result in the death of the rodent, M. canis may

be transferred to the marmot hair. In addition, a fox

explores the entrances to marmot burrows and may

shed M. canis arthroconidia during its search.

Previously, M. canis had been isolated in soil samples

collected from four out of 15 M. marmota burrowsystems surveyed in the western Italian Alps [18], while

a similar investigation carried out in the central Italian

Alps had yielded negative results [17].

The steady character of the M. canis/M. marmota

association in this 4-year survey suggests the inclusion

of the alpine marmot among the reservoirs of this

pathogenic dermatophyte. Indeed, should a mere spill-

over of M. canis from other reservoirs have occurred,an age-related (adults versus juveniles) and/or season-

related prevalence (spring [just after emergence from a

6-month hibernation] versus summer/autumn) would

probably have arisen. Further evidence of the adapta-

tion of M. canis to this new rodent host is afforded by

its unchanged seasonal presence in soil samples col-

lected in the burrow systems as opposed to its absence

in the soil obtained from outside the marmot colonies,where other hosts, including man, might spread the

dermatophyte. [Unchanged seasonal presence of course

refers to the waking moments of the marmot’s life

cycle, excluding winter when all rodent activity stops as

the animal hibernates in burrows under a deep layer of

snow.]

Obviously, man and his pets may be suspected as the

original source for the past introduction of M. canis

into the marmot environment. For a long time, Bivio

has been a tourist resort and the anthropic impact is

quite noticeable, also in the neighbourhood of the areaTa

ble

3S

easo

na

lis

ola

tes

an

dth

eir

pre

va

len

ce(%

)o

fd

erm

ato

phy

tes

fro

mso

ilsa

mp

les

coll

ecte

do

uts

ide

the

entr

an

ces

tom

arm

ot

bu

rro

ws,

atB

ivio

,C

an

ton

of

Gra

ub

un

den

,S

wit

zerl

an

d,

du

rin

ga

4-y

ear

inves

tig

atio

n(1

99

4�/9

7)

Sea

son

Zo

op

hil

icd

erm

ato

phy

tes

Geo

ph

ilic

der

mato

phy

tes

No

.sa

mp

les

exa

min

ed

Mic

rosp

oru

mca

nis

Tri

cho

phy

ton

men

tag

rop

hyte

sM

.co

ok

eiM

.gy

pse

um

T.

aje

llo

iT

.te

rres

tre

Sp

rin

g1

(4.3

)2

(8.7

)0

1(4

.3)

1(4

.3)

2(8

.7)

23

Su

mm

er3

(6.5

)0

00

01

(2.2

)4

6

Au

tum

n2

(6.0

)3

(9.0

)3

(2.9

)2

(6.0

)0

2(6

.0)

33

To

tal

6(5

.9)

5(4

.9)

3(2

.9)

3(2

.9)

1(1

.0)

5(4

.9)

10

2

Ch

i-sq

uare

dte

stsh

ow

ssi

gn

ific

an

tvalu

esin

sum

mer

com

pari

son

of

zoo

ph

ilic

ver

sus

geo

ph

ilic

der

mato

phyte

s(P

�/0

.00

5).

– 2005 ISHAM, Medical Mycology, 43, 373�/379

Alpine marmot as a carrier of zoophilic dermatophytes 377

Med

Myc

ol D

ownl

oade

d fr

om in

form

ahea

lthca

re.c

om b

y R

adbo

ud U

nive

rsite

it N

ijmeg

en o

n 12

/17/

14Fo

r pe

rson

al u

se o

nly.

studied, due to the presence of many footpaths, much

used by hikers, and a busy road. Nevertheless, it isimportant to emphasize that M. canis was found only

in marmot settlements, never in the control areas away

from the rodents’ environment, where, on the contrary,

man, dog and cat are present. Therefore, in our

opinion, M. canis nowadays seems fully adapted to

the wild environment of the marmot.

Burrow systems probably play a key role in the

preservation of M. canis arthroconidia. First, theburrow microclimate varies little during the course of

the year, particularly in winter when the internal

temperature never drops below 08C [22], thereby

avoiding the damage caused by the sudden, extreme

temperature and moisture variations [39] typical of an

alpine environment. Furthermore, as marmot spends

around 80% of its life in the burrows [40], in particular

during the hibernation period, a keratin-enrichedmedium is created which is important for the preserva-

tion of the fungus [41].

The presence of two zoophilic dermatophytes (M.

canis and T. mentagrophytes ) and of M. gypseum

(geophilic with parasitic aptitude) both on the marmot

hair and in the burrow soil suggests that gamekeepers,

veterinarians and anyone who may come into contact

with the rodent should take all precautions necessary toavoid infection from any arthroconidia present.

Acknowledgements

We thank a sponsor who wishes to remain anonymous,

for financing part of this project.The authors thank the management and game-

keepers of the Game and Fishing Inspectorate, Canton

of Graubunden, Switzerland, for the use of their

facilities and for their collaboration during field work.

We also thank the former Director, P. Ratti, the leading

spirit of the project, U. Bruns, F. Frey-Roos and M.

Giacometti for their co-operation in collecting samples.

References

1 English MP. Ringworm in wild mammals. J Zool 1967; 153: 556�/

561.

2 Alteras I, Nesterov V, Ciolofan I. The occurrence of dermato-

phytes in wild animals from Rumania. Sabouraudia 1966; 4: 215�/

218.

3 Otcenasek M, Hubalec Z, Sixl W. Survey of dermatophytes on

hair of small mammals from Austria. Folia Parasitologica

(Praha) 1980; 27: 83�/87.

4 Poglayen G, Tamperi MP, Mantovani AL, Bacchi-Reggiani G.

Ricerca di dermatofiti in ruminanti selvatici in Italia. Arch Sclavo

1981; 123: 225�/226.

5 Mantovani A, Morganti L, Battelli G, et al . The role of wild

animals in the ecology of dermatophytes and relates fungi. Folia

Parasitologica (Praha) 1982; 20: 279�/283.

6 Chabasse D, Guiguen G, Couatamanac’h A, et al . Contribution a

la connaissance de la flore keratinophile isolee des petites

mammiferes sauvages et du lapin de Garenne en France. Discus-

sion sur les especes fongiques rencontrees. Ann Parasitol Hum

Comp 1987; 62: 357�/368.

7 Mancianti F, Mignone W, Papini R. Keratinophylic fungi from

coats of wild boars in Italy. J Wildlife Dis 1997; 33: 167�/169.

8 Gallo MG, Gagliardo D, Cabeli P. Flora micotica del mantello

della volpe (Vulpes vulpes ) in Piemonte. Parassitologia 1990;

32(Suppl.): 114�/115.

9 Mancianti F, Papini R, Poli A. Mycological survey from coats of

red foxes in Italy. J Mycol Med 1993; 3: 109�/111.

10 Otcenasek M, Dvorak J. The isolation of Trichophyton terrestre

and other keratinophylic fungi from small mammals in South

Western Moravia. Sabouraudia 1962; 2: 111�/113.

11 Mariat F, Chatelain J, Rouffaud MA. Study of the contamination

by dermatophytes of population of small mammals in Alsace.

Mycopathologia 1976; 58: 71�/78.

12 Banaszkiewicz H. A study on fungi in the fur of small rodents

from the environs of Warsaw. Mycosen 1985; 28: 520�/523.

13 LaTouche CJ. The importance of the animal reservoir of infection

in the epidemiology of animal-type ringworm in man. Vet Rec

1955; 67: 666�/669.

14 Kaplan W, George LK, Ajello L. Recent developments in animals

ringworm and their public health implications. Ann NY Acad Sci

1958; 70: 636�/648.

15 English MP, Bayley JA. Dermatophytes in a population of bank-

voles and woodmice. Mycopathologia 1978; 66: 67�/71.

16 Arrese JE, Martalo O, Pierard-Franchimont C, Pierard GE.

Urban and rural mycozoonoses. Rev Med Liege 2000; 55: 998�/

1002.

17 Battelli G, Bianchedi M, Frigo W, et al . Survey of keratinophilic

fungi in alpine marmot (Marmota marmota ) burrow soil and

adjoining soils. Sabouraudia 1978; 16: 83�/86.

18 Gallo MG, Bassano B, Milan F. Dermatophytes in Alpine

marmots (Marmota marmota ) burrows soil from Western Alps.

In: Bassano B, Durio P, Gallo Orsi U, Macchi E, eds. Proceedings

of the First International Symposium on Alpine Marmot ( Mar-

mota marmota) and on genus Marmota, 28�/30 October 1991, S.

Vincent, Aosta, Italy. Turin: Desk Top Pre-Press Color Type

Setting, 1992: 199�/202.

19 Neuhaus P, Mainini B, Ingold P. Human impact on marmot

behaviour. In: Bassano B, Durio P, Gallo Orsi U, Macchi E, eds.

Proceedings of the First International Symposium on Alpine

Marmot ( Marmota marmota) and on genus Marmota, 28�/30

October 1991, S. Vincent, Aosta, Italy. Turin: Desk Top Pre-Press

Color Type Setting, 1992: 165�/169.

20 Armitage KB. Social organisation and fitness strategies of

marmots. In: Bassano B, Durio P, Gallo Orsi U, Macchi E, eds.

Proceedings of the First International Symposium on Alpine

Marmot ( Marmota marmota) and on genus Marmota, 28�/30

October 1991, S. Vincent, Aosta, Italy. Turin: Desk Top Pre-Press

Color Type Setting, 1992: 89�/94.

21 Mantovani A. The role of animals in the epidemiology of the

mycoses. Mycopathologia 1979; 65: 61�/66.

22 Lenti D. Distribuzione degli insediamenti e stima della densita di

marmotta alpina (Marmota marmota L.): i metodi d’indagine per

zone campione. In: Spagnesi M, Toso S, eds. Atti del I Convegno

Nazionale dei Biologi della Selvaggina (Suppl Ricerche Biologia

Selvaggina) , 28�/30 January 1998, Bologna, Italy. Savignano al

Panaro-Modena: Tipolitografia F.G 1988; 14: 353�/364.

23 Ratti P. Beitrag zur Kenntnis des Alpenmurmeltieres. Schweiz

Arch Tierheilk 1970; 112: 283�/295.

– 2005 ISHAM, Medical Mycology, 43, 373�/379

378 Gallo et al.

Med

Myc

ol D

ownl

oade

d fr

om in

form

ahea

lthca

re.c

om b

y R

adbo

ud U

nive

rsite

it N

ijmeg

en o

n 12

/17/

14Fo

r pe

rson

al u

se o

nly.

24 Mackenzie DWR. ‘Hairbrush diagnosis’ in detection and eradica-

tion of non fluorescen scalp-ringworm. Br Med J 1963; 2: 363�/

365.

25 Okafor JI, Gugnani H. Dermatophytes and other keratinophilic

fungi associated with hairs of Rodents in Nigeria. Mycosen 1981;

24: 616�/620.

26 Vanbreuseghem R. Technique biologique pour l’isolement des

dermatophytes du soil. Ann Soc Belge Med Trop 1952; 32: 173�/

178.

27 Rebell G, Taplin D. Dermatophytes �/ Their Recognition and

Identification , 2nd edn. Coral Gables, Florida: University of

Miami Press, 1974.

28 De Hoog GS, Guarro J, Gene J, Figueras MJ. Atlas of Clinical

Fungi , 2nd edn. Utrecht, The Netherlands/Reus, Spain: Central-

bureau voor Schimmelcultures/Universitat Rovira i Virgili, 2000.

29 Landis JR, Kock GG. The measurement of observer agreement

for categorial data. Biometrics 1977; 33: 159�/174.

30 Otcenasek M. Ecology of the dematophytes. Mycopathologia

1978; 65: 67�/72.

31 Alteras I, Evolceanu R. A ten year survey of Romanian soil

screening for keratinophylic fungi (1958�/1967). Mycopath Mycol

Appl 1969; 38: 151�/159.

32 Sommerville D, Marples MJ. The effects of soil enrichment on the

isolation of keratinophylic fungi from soil samples. Sabouraudia

1967; 6: 70�/76.

33 Moriello KA, DeBoer DJ. Fungal flora of the haircoat of cats

with and without dermatophytosis. J Med Vet Mycol 1991; 29:

285�/292.

34 Kwon-Chung KJ, Bennett JKE. Medical Mycology, 1st edn.

Philadelphia/London: Lea & Febiger, 1992.

35 Foil CS. Dermatophytosis. In: Griffin CE, Kwochka KW,

MacDonald JM, (eds.) Current Veterinary Dermatology: The

Science and Art of Therapy. St Louis, MO: Mosby Year Book,

1993: 22�/33.

36 Mantovani A, Morganti L. Dermatozoonoses in Italy. Vet Sci

Comm 1977; 1�/2: 171�/177.

37 Chiesura Corona M. Observation on distribution and abundance

of Alpine marmot (Marmota marmota L) in the territory of

Belluno (south-eastern Alps). In: Bassano B, Durio P, Gallo

Orsi U, Macchi E, eds. Proceedings of the First International

Symposium on Alpine Marmot ( Marmota marmota) and on

genus Marmota, 28�/30 October 1991, S. Vincent, Aosta,

Italy. Turin: Desk Top Pre-Press Color Type Setting, 1992: 117�/

121.

38 Calderola S. Indagine sui parassiti intestinali della marmotta

alpina (Marmota marmota ). Tesi di laurea. Veterinary Faculty,

University of Bologna, Bologna, Italy, 1994.

39 Alteras MD. On the long-term survival of keratinophilic fungi in

non-sterile soil. Mycopathologia 1971; 44: 177�/181.

40 Svendsen GE. Behavioural and environmental factors in the

spatial distribution and population dynamics of a yellow-bellied

Marmot population. Ecology 1974; 55: 760�/771.

41 Ajello L. Present day concept of the dermatophytes. Mycopathol

Mycol Appl 1962; 17: 315�/324.

– 2005 ISHAM, Medical Mycology, 43, 373�/379

Alpine marmot as a carrier of zoophilic dermatophytes 379

Med

Myc

ol D

ownl

oade

d fr

om in

form

ahea

lthca

re.c

om b

y R

adbo

ud U

nive

rsite

it N

ijmeg

en o

n 12

/17/

14Fo

r pe

rson

al u

se o

nly.