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Veterinary Dermatology 2005, 16, 385 391

Adherence of Staphylococcus intermedius to corneocytes of healthy


and atopic dogs: effect of pyoderma, pruritus score, treatment and
gender

Blackwell Publishing Ltd

CHRISI SIMOU*, KEITH L. THODAY*, PETER J. FORSYTHE and PETER B. HILL*


*The University of Edinburgh, Dermatology Unit, Division of Veterinary Clinical Studies, The Hospital for
Small Animals, The Royal (Dick) School of Veterinary Studies, Easter Bush Veterinary Centre, Roslin,
Midlothian, Scotland and, Veterinary Dermatology Referrals, Dunlop, Ayrshire, Scotland
(Received 25 May 2005; accepted 10 July 2005)

Abstract Staphylococcal pyoderma occurs commonly in atopic dogs. Some studies have suggested that adherence of staphylococci to corneocytes of atopic dogs and humans is higher than to corneocytes of healthy individuals. This hypothesis and possible differences resulting from the presence or absence of pyoderma, the severity
of pruritus or the effect of treatment or gender, were studied. Adherent bacteria (Staphylococcus intermedius) were
quantified by computerized image analysis on corneocytes collected from healthy or atopic dogs using doublesided adhesive tape. The adherence of S. intermedius to the corneocytes of atopic dogs was significantly greater
than to those of healthy dogs (P = 0.005). Furthermore, adherence was significantly greater in dogs with high
levels of pruritus compared to those with low scores. No significant differences were found between atopic dogs
with no history of pyoderma, atopic dogs with a history of pyoderma and atopic dogs with pyoderma at the time
of sampling (P = 0.068), suggesting that factors other than adherence are necessary for clinical pyoderma to
develop. Treatment did not generally influence the adherence of S. intermedius to corneocytes of atopic dogs and
there was no gender difference in adherence in either healthy or atopic dogs.

IN TRO D U CT I ON
Canine atopic dermatitis has been defined as a genetically predisposed, inflammatory and pruritic allergic
skin disease with characteristic clinical features, most
commonly associated with IgE antibodies to environmental allergens.1 It has traditionally been classified as
a type I hypersensitivity reaction, although the precise
pathogenesis has still to be elucidated. Numerous other
factors are known to be involved, including defective
epidermal barrier function,2 processing of allergens
by epidermal Langerhans cells,3,4 polarization of Tlymphocyte cytokine responses,4 enhanced production
of IgE,5 increased releasability of cutaneous mast cells4
and susceptibility to secondary bacterial and yeast
infections.6
Pyoderma, pyotraumatic dermatitis or acral lick
dermatitis can be found in up to 68% of atopic dogs.7
Many different factors seem to affect the pathogenesis
of pyoderma on atopic skin. It is likely that the hypersensitivity reaction influences, in some way, the cutaneous defence mechanisms. It has been suggested that
atopic dermatitis can lead to alterations in the epidermal

barrier, which allows staphylococcal antigens to


penetrate into the dermis.8 Another possibility is that
serum constituents pass to the skin surface and become
growth factors for the cutaneous flora. In addition,
atopic dermatitis results in changes in the microclimate
of the skin. For example, many atopic dogs suffer from
hyperhidrosis and the rise in the amount of sweat
increases humidity.9 Moreover, ingredients in sweat can
act as a source of nutrients for bacteria and therefore
enhance their proliferation.8,10 It is well-established
that atopic dogs and humans carry higher loads of
staphylococci than healthy individuals.10,11
Other studies have suggested that adherence of
staphylococci to corneocytes of atopic dogs and humans
is higher than to corneocytes of healthy individuals
and that this may predispose allergic skin to secondary
infection.12,13 The aim of this study was to examine this
hypothesis and to study any possible differences resulting
from the presence or absence of pyoderma, the severity
of pruritus and the effect of treatment or gender.

M AT E R IA L S A N D M E T H O D S
Dogs

Correspondence: Dr PB Hill. E-mail: peter.hill@bris.ac.uk.


Present address: Division of Companion Animal Studies, University
of Bristol, Langford, Bristol, UK.
Funding
Chrisi Simou was funded by the Triandafillidis Foundation
2005 European Society of Veterinary Dermatology

Eighteen healthy dogs presented to the Royal (Dick)


School of Veterinary Studies for elective surgical procedures were used for collection of corneocytes. None
had any history or physical signs of skin disease. They
comprised four cross-breeds, one greyhound, two rough
385

386

C Simou et al.

Table 1. Clinical details of the atopic dogs sampled


Dog Breed

Age (years) Sex

Diagnosis

PS

Treatment

1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41

2
2
2
2
3
2
6.5
2
2
9
7.5
3
6
4
3
7
4
2.5
3
2
2.5
4
4
3
3.5
3
5
2.5
1
3
5
8
3
3
4
5
1.5
5
1
3
3

Atopic dermatitis, pyoderma


Atopic dermatitis, pyoderma
Atopic dermatitis, pyoderma
Atopic dermatitis, history of pyoderma
Atopic dermatitis
Atopic dermatitis, history of pyoderma
Atopic dermatitis, pyoderma
Atopic dermatitis, pyoderma
Atopic dermatitis, history of pyoderma
Atopic dermatitis, history of pyoderma
Atopic dermatitis, pyoderma
Atopic dermatitis
Atopic dermatitis, pyoderma
Atopic dermatitis, pyoderma
Atopic dermatitis
Atopic dermatitis, pyoderma
Atopic dermatitis, pyoderma
Atopic dermatitis
Atopic dermatitis, pyoderma
Atopic dermatitis
Atopic dermatitis history of pyoderma
Atopic dermatitis, history of pyoderma
Atopic dermatitis, history of pyoderma
Atopic dermatitis, history of pyoderma
Atopic dermatitis, history of pyoderma
Atopic dermatitis, pyoderma
Atopic dermatitis, pyoderma
Atopic dermatitis, history of pyoderma
Atopic dermatitis, history of pyoderma
Atopic dermatitis, pyoderma
Atopic dermatitis, pyoderma
Atopic dermatitis, pyoderma
Atopic dermatitis, pyoderma
Atopic dermatitis, pyoderma
Atopic dermatitis
Atopic dermatitis, history of pyoderma
Atopic dermatitis, pyoderma
Atopic dermatitis, history of pyoderma
Atopic dermatitis, pyoderma
Atopic dermatitis, history of pyoderma
Atopic dermatitis

3
5
3
2
2
4
ND
4
3
5
5
2
3
3
3
3
2
0
3
0
1
1
0
1
4
4
3
4
4
3
4
4
4
4
3
1
1
1
3
0
1

Antibiotics glucocorticoids
None
None
Immunotherapy
Immunotherapy
None
Immunotherapy
Antibiotics
Immunotherapy, topical glucocorticoids
None
Immunotherapy, topical glucocorticoids
Immunotherapy
Antibiotics, immunotherapy
None
Immunotherapy
None
None
Topical glucocorticoids
Antibiotics, immunotherapy
Topical glucocorticoids
Immunotherapy glucocorticoids
Immunotherapy
Antibiotics
Antibiotics
None
Antibiotics
None
None
Topical glucocorticoids
None
Antibiotics
None
Topical glucocorticoids
Immunotherapy
None
None
Antibiotics
Glucocorticoids, immunotherapy
None
Immunotherapy, topical glucocorticoids
Immunotherapy

Boxer
Staffordshire bull terrier
Labrador retriever
Golden retriever
Labrador retriever
Labrador retriever
Labrador retriever
Labrador retriever
Jack russell terrier
German shepherd dog
West highland white terrier
Labrador retriever
Border terrier
Labrador retriever
West highland white terrier
Dachshund
Labrador retriever
Weimeraner
Labrador retriever
Springer spaniel
Flat-coated retriever
Newfoundland
West highland white terrier
Golden retriever
West highland white terrier
Cross-breed
Labrador retriever
West highland white terrier
Staffordshire bull terrier
German shepherd dog
West highland white terrier
Staffordshire bull terrier
West highland white terrier
Border terrier
Boxer
Cavalier king charles spaniel
Boxer
West highland white terrier
Newfoundland
Staffordshire bull terrier
West highland white terrier

M
M
F
FN
MN
F
M
MN
M
M
FN
MN
MN
MN
MN
FN
FN
FN
M
FN
M
MN
MN
MN
FN
MN
MN
F
F
FN
F
F
FN
MN
M
FN
FN
M
MN
MN
FN

F, female; FN, female ovariohysterectomized;


M, male; MN, male castrated;
ND, not determined;
PS, pruritus score (see text for details of scoring system);
y, years;
Antibiotics, receiving antibiotic therapy with cephalexin at the time of corneocyte collection;
History of pyoderma, had pyoderma in the past but not affected at the time of corneocyte collection;
Pyoderma, evidence of bacterial skin disease at the time of corneocyte collection;
Glucocorticoids, receiving glucocorticoids at the time of corneocyte collection;
Immunotherapy, receiving allergen specific immunotherapy at the time of corneocyte collection.

collies, one Border collie, four Labrador retriever crosses,


one German shepherd dog, three lurchers, one Great
Dane and one springer spaniel. They ranged in age
from 7 months to 7 years with two being of unknown
age. Ten dogs were intact female and eight dogs were
male (seven entire and one castrated).
Corneocytes were also collected from 41 dogs with
atopic dermatitis, presented to the Dermatology Unit
of the Royal (Dick) School of Veterinary Studies with
or without pyoderma. The breed, age, sex, diagnoses,
pruritus score (see succeeding discussions) and therapy
at the time of sampling, are shown in Table 1.

Diagnostic criteria
The diagnosis of atopic dermatitis was made by
members of the dermatology service based on consistent
history and physical signs, and one or more positive
reactions in an intradermal allergy test or allergenspecific IgE enzyme-linked immunosorbent assay
(ELISA). In addition, other concurrent diseases were
eliminated as follows: ectoparasite infestations (by skin
scrapings and application of selamectin (Stronghold,
Pfizer, Sandwich, UK)), yeast infection (by the examination of stained tape strips) and food intolerance (by
a 6-week restricted diet trial).

2005 European Society of Veterinary Dermatology, Veterinary Dermatology, 16, 385 391

Bacterial adherence in atopic dermatitis

387

Grade 0: Normal dog: the dog does not itch more than before the disease began.
Grade 1: Occasional episodes of itching (small increase in itch compared with before the disease began).
Grade 2: More frequent episodes of itching, but the itching stops when the dog is sleeping, eating, playing or is otherwise distracted.
Grade 3: Regular episodes of itching are seen when the dog is awake. The dog occasionally wakes up because of itching, but the itching stops
when the dog is eating or playing or exercising or is otherwise distracted.
Grade 4: Prolonged episodes of itching are seen. The dog regularly wakes up because of itching, or itches in its sleep. The itching can also been
seen when the dog is eating or playing or exercising or is otherwise distracted.
Grade 5: Almost continuous itching, which does not stop when the dog is distracted, even in the consulting room (the dog needs to be physically
restrained from itching).

The owner assessed the level of pruritus objectively


using a 05 behaviour-based pruritus score (PS)
developed at the Royal (Dick) School of Veterinary
Studies.14 (see box)
The diagnostic criteria used for the diagnosis of
pyoderma were clinical signs (the presence of a maculopapular eruption, pustules and/or epidermal collarettes)
and cytological examination of relevant samples
(presence of degenerate neutrophils and phagocytosed
cocci).

Collection of corneocytes
Corneocytes collected from atopic dogs were taken
from skin without lesions. Previous studies in our
laboratory had shown that the difference in staphylococcal adherence to corneocytes taken from various
anatomical sites was significant only between the head/
neck and the dorsum.15 Thus, the samples were taken
from the trunk (either the ventral abdomen or the
lateral thorax). Corneocytes from healthy dogs were
collected from the ventral abdomen.
Initially, the skin sites were clipped and surface
debris and most indigenous bacteria were removed by
serial application of four strips of single adhesive tape
(Cellux, Sellotape GB Ltd, Dunstable UK).15,16 To
collect the corneocytes, a 2 cm2 piece of clear doublesided adhesive tape (Tropical Tape Super Grip, USA)
was used. One side of the tape was mounted onto a clean
glass microscope slide (Premium microscope slides, BDH,
UK) and the other was applied 10 times to the clean skin
surface using the same force on each occasion. The
samples were always collected by the same investigator
(CS) in a standard manner to reduce variability. Three
slides of corneocytes were collected from each dog.
Storage of corneocytes at 80 C, 4 C or room
temperature for up to 5 months does not significantly
reduce or increase staphylococcal adherence.17 Thus,
all corneocytes collected were stored at 4 C for a
maximum of up to 5 months. The adherence assay for
all samples was conducted in one day.

Bacterial isolates
An isolate of S. intermedius from a clinical case of canine
bacterial pyoderma (M 732, 99) was used. Bacterial
suspensions were prepared using the technique previously described by Forsythe et al.15 Briefly, for each
assay, organisms stored at 70 C on cryobank beads
(Mast, Bootle, UK) were inoculated onto horse blood
agar and incubated for 24 h at 37 C. An individual
colony was then subcultured on horse blood agar for

a further 24 h. Bacterial colonies were harvested from


the agar plate and placed in a sterile tube containing
1 mol L1 sterile phosphate buffered saline (PBS), pH 7.2.
The bacteria were washed by vortex mixing for 60 s
using a Rotamixer (Camlab Ltd, Cambridge, UK) and
then centrifuged for 3 min at 3000 r.p.m. using a
Centrifugette 4206 centrifuge (Camlab Ltd, Cambridge,
UK). The resulting supernatant was discarded, a further
34 mL of PBS was added to the tube and the process
repeated. The bacteria were subjected to three washes
in total and then resuspended in 1 mol L1 PBS by further
vortex mixing for at least 2 min. The optimal concentration of staphylococcal suspensions for adherence
studies was previously established as 3 108 per mL.15
This density corresponds to an optical density (OD)
of 0.289 when measured by a spectrophotometer
(Colorimeter 257, Ciba Corning Diagnostics, Halstead,
UK) at a wavelength of 600 nm. Therefore, bacterial
suspensions were diluted in PBS to an OD of 0.289.

Adherence assay
The corneocyte-covered slides were placed in moisture
chambers consisting of 30 30 cm flat plastic trays
with well-fitting lids and lined by paper towel moistened
with water. 300 L of bacterial suspension was then
pipetted onto the centre of each piece of corneocytecovered tape to form a meniscus. The slide chambers
were incubated for 90 min at 37 C. Subsequently, all slides
were rinsed with 1 mol L1 PBS, to remove nonadherent
bacteria and finally were stained with 0.5% crystal
violet (Crystal violet for microscopical staining, Gurr
Certistain, BDH, VWR International Ltd, UK) for
90 s. Two slides from each dog were incubated with
S. intermedius and one from each dog acted as a negative
control (incubated with 300 L of PBS alone).

Quantification of adherence
The quantification of adherent bacteria was performed
by means of a previously validated computerized image
analysis technique.15 The same person performed the
analysis each time and was blinded to the identity of
the samples. Briefly, the analysed fields were randomly
selected by moving the microscope stage in a standard
direction and to a standard distance after each image
acquisition. A chosen field was rejected if the corneocytes were not confluent, if there were objects other than
corneocytes on the field (hair, artefacts) or if it was not
possible to bring the entire field into sharp focus.15
Previous studies showed that acquisition of 15 fields
from each duplicate slide yielded acceptable coefficients

2005 European Society of Veterinary Dermatology, Veterinary Dermatology, 16, 385391

388

C Simou et al.

of variation of approximately 10%.15 Therefore, 15


images of oil-immersion fields (1000) of each of the
three slides collected from each dog were acquired with
a JVC TK-C1381 colour video camera attached to a
Leica Laburlux S conventional compound microscope
(Leica Microsystems UK Ltd, Milton Keynes, UK).
Video microscopy images were digitized by a Power
Macintosh 7100/80 computer fitted with an AV digitizer
(Apple Computer, California, USA). Images viewed
on the computer screen were captured and analysed
using Object-Image 1.62 an image analysis software
program freely available from http://simon.bio.uva.nl/
object-image.html.
The software calculated the percentage area covered
by staphylococci that were adherent to a confluent layer
of corneocytes within a constant defined area of the
captured field. For each field, the percentage bacterial
coverage (termed percentage adherence), was calculated, and the mean percentage adherence figure was
determined by calculating the mean of the percentage
bacterial coverage of all 15 fields analysed on each
slide. Overall percentage adherence was determined by
subtracting the percentage adherence of the control
slide from the mean of the duplicates.

Statistical analysis
The results of the mean percentage adherence values
were compared by and Students t-test was used
to compare pairs of adherence values from corneocytes
of healthy and atopic dogs. A P value of < 0.05 was
considered significant.

R ESU LTS
Adherence to corneocytes from atopic and healthy
dogs
A comparison of the two groups is shown in Fig. 1. There
was a significant increase in adherence of S. intermedius

Figure 2. Percentage adherence of Staphylococcus intermedius to


corneocytes in relation to pyoderma status. The bottom of the box
represents the first quartile (Q1); and the top the third quartile (Q3).
The whiskers define the range of the data and the line within the box
is the median. N = number of dogs in each group. No significant
differences were found among groups (P = 0.068).
= mean, * = outlier

organisms to the corneocytes of atopic dogs compared


with those from healthy dogs (P = 0.005).

Percentage adherence of S. intermedius to


corneocytes of healthy dogs, atopic dogs with no
history of pyoderma, atopic dogs with a past history
of pyoderma and atopic dogs with active pyoderma
at the time of sampling
Differences in the percentage adherence of S. intermedius
to corneocytes of healthy and atopic dogs subdivided
based on their pyoderma status are shown in Fig. 2.
Group comparison by analysis of variance showed no
significant differences (P = 0.068). Comparison of the
three atopic groups by analysis of variance also showed
no significant differences (P = 0.731).

Percentage adherence of S. intermedius to


corneocytes of atopic dogs according to pruritus
level
The percentage adherence of S. intermedius to corneocytes of atopic dogs in relation to pruritus level is shown
in Fig. 3. The analysis is based on data from 40 dogs
(the pruritus score of one dog was not determined).
Comparison by analysis of variance demonstrated a
significant difference between groups (P = 0.004).
Subanalysis by Students t-test showed no difference
between the dogs with pruritus score (PS) of 23 and
45 (P = 0.422). However, there was a significant
difference between the dogs with PS of 01 and 23
(P = 0.003) and between the dogs with PS of 01 and
45 (P = 0.025).

Figure 1. Adherence of Staphylococcus intermedius to corneocytes


of healthy and atopic dogs. The bottom of the box represents the first
quartile (Q1); and the top the third quartile (Q3). The whiskers
define the range of the data and the line within the box is the median.
N = number of dogs in each group. Adherence in the atopic group
was significantly higher than in the healthy group (P = 0.005).
= mean, * = outlier

Percentage adherence of S. intermedius to


corneocytes of atopic dogs receiving various kinds
of treatment
There was no significant difference in the percentage
adherence of S. intermedius to corneocytes of atopic
dogs that were receiving any kind of treatment compared

2005 European Society of Veterinary Dermatology, Veterinary Dermatology, 16, 385 391

Bacterial adherence in atopic dermatitis

Figure 3. Percentage adherence of Staphylococcus intermedius to


corneocytes of atopic dogs with different degrees of pruritus, as
indicated by the pruritus score. (N = 40). The bottom of the box
represents the first quartile (Q1); and the top the third quartile (Q3).
The whiskers define the range of the data and the line within the box
is the median. N = number of dogs in each group. Adherence in dogs
with PSs of 23 or 4 5 were significantly higher than in dogs with
scores of 01 (P = 0.003 and 0.025 respectively).
= mean

to those that were not at the time of sampling (P =


0.989). In addition, comparison of dogs treated with
or without topical or systemic glucocorticoids and
comparison of dogs treated with or without allergenspecific immunotherapy did not reveal significant
differences (P = 0.968 and 0.942 respectively).

Percentage adherence of S. intermedius to


corneocytes of male and female dogs
There were no significant differences in adherence
between male and female healthy dogs (P = 0.724), or
male and female atopic dogs, regardless of neutering
status (P = 0.446).

D ISCU SSION
The results of this study show that the adherence of
S. intermedius to corneocytes of atopic dogs is significantly greater than to corneocytes of healthy dogs. This
supports previous results that also showed increased
adhesion of S. intermedius to corneocytes of atopic dogs
compared with healthy and with seborrhoeic (but nonatopic) dogs.13 Greater adherence of Staphylococcus aureus
to corneocytes of atopic humans has also been reported.12
The most likely explanation for this phenomenon is
that atopic dermatitis in some way alters the cutaneous
receptors for staphylococci and this is one contributing
factor for the high incidence of pyoderma in both atopic
dogs and atopic humans. This could involve changes in
the number, the nature, or the position of the receptors.
In both humans and dogs, a greater expression of
intercellular adhesion molecule 1 (ICAM-1) has been
demonstrated in atopic disease.7 Moreover, immunohistochemical staining reveals a different pattern of
distribution of fibronectin in atopic human skin, but
canine skin has yet to be studied. In healthy human
skin, fibronectin is present in the epidermal basement

389

membrane and in the dermis and it also occurs in the


stratum corneum of human atopics.18 Cho et al.,19
using a murine model, have shown that the adherence
of S. aureus to the skin is enhanced by a T helper 2
lymphocyte (Th2) response and that this binding is
mediated by fibronectin.
Although adherence was greater in atopic dogs
compared to healthy dogs, there was no significant
difference between atopic dogs that had concurrent
pyoderma, those with a history of pyoderma and those
with no pyoderma. Hence, development of pyoderma
would seem to depend on other factors. However, it is
not known whether some of the dogs in the present
study had previous skin infections that were unobserved
or whether they were going to develop subsequent
pyoderma.
The finding of significant differences between dogs
with high and low pruritus scores raises a series of complex questions that require further study. A number of
possible explanations may be responsible for this finding. First, it may indicate that atopic dogs with a low
degree of pruritus are similar to healthy dogs in terms
of their staphylococcal adherence receptor expression,
whereas more severe pruritus is associated with upregulation. However, this finding needs to be interpreted with caution because the degree of pruritus does
not always reflect the severity of the underlying atopic
dermatitis. Often, dogs that are intensely pruritic suffer
from secondary infections with bacteria or yeast. What
is clear, however, is that more severe pruritus, whether
caused by the atopic dermatitis alone or a combination
of atopic dermatitis and secondary infection, results
in an increase in adherence of S. intermedius to canine
corneocytes. It is interesting to note that the presence
of bacterial infection per se did not appear to alter
adherence.
A second possibility is that there is an effect of treatment that was not uncovered by the analysis performed
in this study. Because atopic dermatitis is often treated
by combination therapy involving both systemic and
topical agents, it was not possible to investigate the
effects of individual therapies on adherence. There was
no apparent effect of glucocorticoids or immunotherapy
on adherence but it is possible that some other aspect
of the therapeutic regime could have decreased adherence in dogs that were under stable control and had low
pruritus scores. However, it has been shown in previous
studies that the carriage of S. intermedius did not differ
between healthy dogs and atopic dogs that were
receiving prednisolone and were in clinical remission.20
Moreover, in a study in humans, the recovery rate of
S. aureus from atopic individuals did not change with
the use of topical steroids.21
A third possibility would be that self-trauma to the
epidermis in more pruritic dogs resulted in greater
adherence, either by exposing lower layers of the
epidermis or allowing adhesins such as fibronectin to
reach the surface. However, corneocytes in this study
were collected from grossly normal areas on the ventral
abdomen, which tends to preclude this possibility.

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C Simou et al.

Clearly, the relationship between the level of pruritus


and bacterial adherence warrants further investigation.
As this study was performed using cases of atopic
dermatitis that presented to a dermatology clinic, it
was not possible to age-, breed- and sex-match the
study animals and the controls. To the authors knowledge, the effect of age on adherence in dogs has not
been studied. However, a previous study has shown
that adherence differs between breeds.15 Boxers and
Bull terriers were shown to have higher adherence
values than spaniels and hounds.15 As the atopic group
in this study contained boxers and bull terriers, it could
be argued that this may have affected the results.
However, analysis of the individual adherence values
for these breeds in this study did not reveal values that
were consistently higher than other breeds in the group
(data not shown). The lack of a significant effect in
terms of gender was not surprising because canine
atopic dermatitis does not have a clear predilection
for either sex. Some studies show sex predilection for
females22 and others show no sex predilection.2326
In order to allow the number of animals in this study
to be investigated, and to minimize variations as a result
of differences between different strains of S. intermedius,
only one strain was used throughout these experiments.
It is therefore impossible to draw general conclusions
about the adherence of different strains of S. intermedius.
Different strains of Staphylococcus epidermidis have been
shown to differ in the production of biofilm.27 In another
study, although no difference was detected between the
adherence of S. intermedius strains that were isolated from
pyoderma cases and others isolated from healthy dogs,
significant variation was noticed among individual
isolates within the groups.28 Therefore, further studies
are required to investigate the effect of strain differences
on the results reported in this study.

7.

8.

9.

10.

11.

12.

13.

14.

15.

16.

17.

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Rsum Les pyodermites bactriennes sont frquentes chez les chiens atopiques. Certaines tudes ont suggr
que ladhrence des staphylocoques aux cornocytes des chiens comme des humains atopiques est suprieures
celle observe chez les individaux normaux. Cette hypothse, ainsi que de possibles diffrences lies la prsence
ou labsence de pyodermite, la svrit du prurit, ou leffet du traitement ou du sexe ont t tudies ici.
Ladhrence des bactries (Staphylococcus intermedius) a t quantifie avec laide dun ordinateur, sur des
cornocytes obtenus de chiens atopiques ou sains par la technique de la cellophane adhsive. Ladhrence de
S. intermedius aux cornocytes des chiens atopiques tait significativement suprieure celle des chiens sains
(P = 0.005). En outre, ladhrence tait significativement suprieure chez les chiens degr lev de prurit par
rapport ceux prurit faible. Aucune diffrence significative na t observe entre les chiens atopiques avec une
histoire de pyodermite et les chiens atopiques prsentant une pyodermite au moment des prlvements
(P = 0.068), suggrant que dautres facteurs que ladhrence sont ncessaires pour le dveloppement de linfection bactrienne. Le traitement na en gnral pas influenc ladhrence de S. intermedius aux cornocytes des
chiens atopiques, et il nexistait pas de diffrence en fonction du sexe, ni chez les chiens sains, ni chez les chiens
atopiques.
Resumen La pioderma producida por estafilococos ocurre generalmente en perros atpicos. Algunos estudios
han sugerido que la adherencia de Staphylococci a corneocitos de perros y humanos atpicos es mayor que la
adherencia a corneocitos de individuos sanos. Estudiamos esta hiptesis, as como las posibles diferencias debido
a la presencia o ausencia de pioderma, la severidad del prurito, o los efectos del tratamiento o del gnero (machos
o hembras). La adherencia de la bacteria (Staphylococcus intermedius) se cuantific mediante anlisis de imagen
computerizado en corneocitos obtenidos de perros sanos o atpicos utilizando cinta adhesiva de doble cara. La
adherencia de S. intermedius a corneocitos de perros atpicos fue significativamente mayor que la adherencia a
corneocitos de perros sanos (P = 0.005). Adems la adherencia fue significativamente mayor en perros con nivel
ms elevado de prurito, comparada con perros con menores niveles de prurito. No encontramos diferencias
significativas entre perros atpicos sin historia de pioderma, perros atpicos con historia de pioderma y perros
atpicos con pioderma en el momento del muestreo (P = 0.068), lo cual sugiere que factores diferentes a la adherencia de las bacterias son necesarios para desarrollar la forma clnica de pioderma. El tratamiento generalmente
no afect a la adherencia de S. intermedius a los corneocitos de los perros atpicos y no hubo diferencias debidas
al gnero en la adherencia perros sanos o atpicos.
Zusammenfassung Eine Staphylokokken-Pyodermie tritt bei atopischen Hunden hufig auf. Einige Studien
haben angedeutet, dass das Anhaften der Staphylokokken an den Korneozyten von atopischen Hunden und
Menschen grer ist, als an den Korneozyten von gesunden Individuen. Diese Hypothese und mgliche Unterschiede aufgrund der An- oder Abwesenheit einer Pyodermie, der Strke des Pruritus, sowie der Auswirkung einer
Behandlung oder des Geschlechts, wurden untersucht. Anhaftende Bakterien (Staphylococcus intermedius)
wurden mittels computergesttzter Bildanalyse auf Korneozyten, die von gesunden und atopischen Hunden
mittels doppelseitigem Klebestreifen gesammelt wurden, quantitativ bestimmt. Das Anhaften von Staphylococcus
intermedius an Korneozyten von atopischen Hunden war signifikant grer als an denen von gesunden Hunden
(P = 0.005). Auerdem war das Anhaften bei Hunden mit strkerem Pruritus im Vergleich zu solchen mit
geringerem Juckreiz grer. Keine signifikanten Unterschiede wurden zwischen atopischen Hunden ohne
Vorbericht einer Pyodermie, atopischen Hunden mit dem Vorbericht einer Pyodermie und atopischen Hunden
mit einer Pyodermie zum Zeitpunkt der Probenentnahme festgestellt (P = 0.068). Dieses Ergebnis deutet darauf
hin, dass fr die Entstehung einer klinischen Pyodermie neben dem Anhaften auch andere Faktoren notwendig
sind. Im Allgemeinen wurde das Anhaften der S. intermedius an den Korneozyten von atopischen Hunden durch
eine Behandlung nicht beeinflusst und es bestand beim Anhaften weder bei gesunden noch bei atopischen
Hunden ein Geschlechtsunterschied.

2005 European Society of Veterinary Dermatology, Veterinary Dermatology, 16, 385391

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