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Veterinary Dermatology 2005, 16, 156161

Species specificity in the adherence of staphylococci to canine


and human corneocytes: a preliminary study

Blackwell Publishing, Ltd.

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


*The University of Edinburgh, Division of Veterinary Clinical Studies, Dermatology Unit, The Hospital for
Small Animals, The Royal (Dick) School of Veterinary Studies, Easter Bush Veterinary Centre, Roslin,
Midlothian, Scotland, UK Veterinary Dermatology Referrals, Lugton Farm, Aiket Road, Dunlop, Ayrshire,
Scotland, UK
(Received 3 November 2004; accepted 28 March 2005)

Abstract Staphylococcal pyoderma is rarely contagious between dogs and humans, or humans and dogs. This
study investigated the hypothesis that there are species differences in adherence of Staphylococcus intermedius
(the most common isolate from dogs) and Staphylococcus aureus (the most common isolate from humans) to
canine and human corneocytes. Sheets of corneocytes were collected from the ventral abdomen of 10 dogs and
the medial forearm of 10 humans (all healthy and without any history or physical signs of skin disease) using
double-sided tape. Staphylococcus intermedius from a case of canine bacterial pyoderma and a human strain of
S. aureus were prepared in phosphate buffered saline (PBS) and applied in duplicate, respectively, to the canine
and human corneocyte-covered tapes using PBS as negative control. After incubation, rinsing, and staining with
crystal violet, quantification of the adherent bacteria was carried out blindly by computerized image analysis.
Staphylococcus intermedius was found to adhere significantly more to canine corneocytes than S. aureus
(P = 0.0006), whereas S. aureus showed greater adherence to human corneocytes than S. intermedius
(P < 0.0001). In addition, the pattern of adherence differed between the two organisms, with S. intermedius adhering to the entire surface and S. aureus adhering mainly to the periphery of both canine and human corneocytes.
Preference for adherence to these two hosts may explain, in part, why S. intermedius and S. aureus are uncommonly
isolated from human and canine skin infections, respectively.

I N TRO D U CT ION
Bacterial pyoderma is one of the most frequently
diagnosed skin conditions of dogs1 and, in the USA, is
the second most common skin disorder after flea bite
hypersensitivity.1 Bacterial skin disease is also common
in humans.2 The most common pathogenic staphylococcal isolate from dogs is Staphylococcus intermedius,
whereas in humans it is Staphylococcus aureus.37 Staphylococcus intermedius infections are rarely transmitted
between dogs, probably because underlying factors
are required for the infection to become established.
Owners of affected dogs commonly ask veterinary surgeons if there is any risk of transmission of infection to
members of their families. Typically, this does not
occur but the reasons for this lack of contagion are not
known. One possibility involves differences in the process
of bacterial adherence between species of staphylococci.
Bacterial adherence is the measurable union between
a bacterium and a substratum in which energy is
required to achieve dissociation.8 Adherence is the
Presented as a Free Communication at the 19th Annual Congress of
the European Society of Veterinary DermatologyEuropean College
of Veterinary Dermatology, Tenerife, 2003.
Chrisi Simou was funded by the Triandafillidis Foundation.
Correspondence: K. L. Thoday. E-mail: k.l.thoday@ed.ac.uk.
Present address: The University of Athens, School of Biology,
Panepistimioupoli, Athens, Greece.
156

first, and essential stage of any infection and in the skin


involves interaction between adhesins on the bacterial
surface and receptors on various skin components,
including corneocytes.2,9
In this study, we explored the hypothesis that differences
in adherence of S. intermedius and S. aureus to canine
and human corneocytes might explain the apparent
lack of contagion of bacterial pyoderma between dogs
and humans.

M AT E R IA L S A N D M E T H O D S
Canine and human subjects
Ten healthy dogs and 10 healthy humans were sampled.
The dogs either belonged to staff members of the Royal
(Dick) School of Veterinary Studies or presented to the
School for elective surgical procedures. The dogs
comprised four cross-breeds, two lurchers, one Labrador
retriever, one Dalmatian, one Border collie and one
Great Dane, and ranged in age between 10 months and
9 years. Six dogs were female (five entire and one ovariohysterectomized) and four were male (two entire and
two castrated). The human volunteers comprised six
women and four men with ages ranging from 25 to
40 years. All the dogs and humans were healthy with
no history or physical signs of dermatological disease
and none had received recent antibacterial agents
either systemically or topically.
2005 European Society of Veterinary Dermatology

Staphylococcal adherence in dogs and humans

Collection of corneocytes
Corneocytes were collected from the ventral abdomen
of the dogs and the medial forearm of the humans. Initially, the canine skin sites were prepared by removal
of hair with Oster clippers (Oster Professional Products,
TN, USA), and removal of surface debris and most
indigenous bacteria by serial application of four strips
of single adhesive tape (Cellux, Sellotape GB Ltd,
Dunstable, UK).10,11 To collect the corneocytes from
both dogs and humans, a 2-cm2 piece of clear doublesided adhesive tape (Tropical Tape Super Grip, London,
UK) was used. One side of the tape was mounted onto
a clean glass microscope slide (Premium microscope
slides, BDH, VWR International Ltd, Poole, UK) and
the other was applied 10 times to the clean skin surface
using the same force on each occasion. The same investigator collected the samples in a standard manner in
order to reduce sampling variability. Six samples were
collected from each dog and human, with samples
from one dog and one human being taken and subsequently processed on the same day.

Bacterial isolates
An isolate of S. intermedius from a clinical case of canine
bacterial pyoderma (M732/99) and a human strain of
S. aureus (NCTC 6571) were compared. Bacterial suspensions were prepared using the technique from our
laboratories previously described by Forsythe et al . 11
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 onto horse
blood agar for a further 24 h. Bacterial colonies were
harvested from the agar plate and placed into a sterile
tube containing 1 M 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 were then centrifuged for 3 min at
3000 r.p.m. using a Centrifugette 4206 centrifuge (Camlab
Ltd). 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 re-suspended in 1 M PBS by further
vortex mixing for at least 2 min. Previous studies in our
laboratories have established that the optimal concentration of staphylococcal suspensions for adherence
studies is 3 108 per mL.11 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, throughout these studies, 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. Three hundred L of bacterial
suspension was then pipetted onto the centre of each
piece of corneocyte-covered tape, to form a meniscus.

157

The slide chambers were incubated for 90 min at 37 C.


Subsequently, all slides were rinsed with 1 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, Poole, UK) for 90 s. For each dog or
human, the six collected samples were divided into
two groups of three. Two from each group were
incubated with S. intermedius or S. aureus, respectively,
and one sample in each group 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 computerized image analysis technique
as previously validated and used in our laboratories.11
The same person performed the analysis each time and
was blinded to the identity of the samples. Briefly, the
analysed fields were selected in a random way 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.11
Our previous studies have shown that acquisition of
15 fields from each duplicate slide yielded acceptable
coefficients of variation of approximately 10%.11
Therefore, in this study 15 images of oil-immersion
fields (1000) of each slide 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).
Live 24-bit super-VHS colour PAL video was digitized
using a Power Macintosh 7100/80 fitted with an AV
digitiser (Apple Computer, CA, USA). Image acquisition and processing were performed using ObjectImage 1.62, a public domain software package, available from the Internet by anonymous FTP 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 defined area of the captured field. The defined area remained constant
throughout the study. 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. The overall percentage adherence was determined by subtracting the percentage adherence of the
control slide from the mean of the duplicates. Previous
studies using this methodology have shown that the
mean surface area of S. intermedius organisms (0.42
m2) and S. aureus organisms (0.37 m2) are so similar
that corrections for bacterial size are not required.12

Statistical analysis
Statistical analyses were carried out using GRAPHPAD PRISM version 3.00 for Windows (GraphPad

2005 European Society of Veterinary Dermatology, Veterinary Dermatology, 16, 156161

158

C Simou et al.

Figure 1. Representative photomicrographs showing the adherence


of Staphylococcus intermedius and Staphylococcus aureus to canine
and human corneocytes. (a) S. intermedius adherent to canine
corneocytes; (b) S. intermedius adherent to human corneocytes;
(c) S. aureus adherent to human corneocytes; (d) S. aureus adherent
to canine corneocytes. S. intermedius adheres in a diffuse pattern,
whereas S. aureus adheres in a peripheral distribution. Crystal
violet stain 1000 original magnification. Bar = 10 m.

Software, San Diego CA, USA; http://www.graphpad.com). The results of the mean percentage adherence amongst the four groups (two organisms and two
species) were compared by . For subanalysis, the
adherence of the two species of staphylococci to corneocytes from the same individual was compared by
paired Students t-test, whereas the adherence of the
same species of staphylococcus to corneocytes from
dogs and humans was compared by unpaired Students
t-test. A P-value of < 0.05 was considered to be significant in each case.

R ESU LTS
Representative photomicrographs of staphylococcal
adherence to canine and human corneocytes are shown
in Fig. 1. Staphylococcus intermedius clearly adhered
to canine corneocytes in larger numbers than S. aureus,

Figure 2. Percentage adherence of Staphylococcus intermedius and


Staphylococcus aureus to canine and human corneocytes. The
bottom of the box represents the first quartile (Q1); the top of the
box represents the third quartile (Q3). The whiskers define the range
of the data and the line within the box is the median. = mean,
* = outlier. Statistical differences between the groups are described
in the text.

whereas S. aureus clearly showed greater adherence to


human corneocytes than S. intermedius. In addition,
the pattern of adherence differed between the two
organisms, with S. intermedius adhering to the entire
surface of both canine and human corneocytes (Fig. 1a,b)
and S. aureus adhering mainly to the periphery (Fig. 1c,d).
The mean percentage adherence values from the 10
experiments are shown in Table 1 and illustrated in
Fig. 2. The statistical differences between the four
groups were highly significant (P < 0.0001). Staphylococcus intermedius showed significantly greater adherence to canine corneocytes than S. aureus (P = 0.0006),
and S. aureus showed significantly greater adherence to
human corneocytes than S. intermedius (P < 0.0001).
In addition, the mean percentage adherence of S. intermedius to canine corneocytes was significantly greater
than its adherence to human corneocytes (P < 0.0001)
and the mean percentage adherence of S. aureus to
human corneocytes was significantly greater than its
adherence to canine corneocytes (P < 0.0001). The
mean adherence of S. intermedius to canine corneocytes did not differ significantly from the mean adherence of S. aureus to human corneocytes (P = 0.956).

Table 1. Mean percentage adherence of Staphylococcus intermedius and Staphylococcus aureus to canine and human corneocytes in 10
individual experiments
Experiment

Canine corneocytes
S. intermedius (%)

Canine corneocytes
S. aureus (%)

Human corneocytes
S. aureus (%)

Human corneocytes
S. intermedius (%)

1
2
3
4
5
6
7
8
9
10

7.37
4.41
8.54
9.51
10.94
13.19
6.15
6.39
14.02
13.05

4.05
1.34
8.54
3.04
4.06
1.75
1.42
2.9
3.89
3.3

10.93
9.75
6.74
4.85
10.82
10.89
6.47
10.59
12.06
11.2

1.4
1.24
1.35
1.72
0.6
2.18
0.68
1.7
1.58
2.21

2005 European Society of Veterinary Dermatology, Veterinary Dermatology, 16, 156161

Staphylococcal adherence in dogs and humans

D ISCU SSION
Why certain bacteria more commonly infect the skin of
particular species is still speculative. Noble provided
good evidence that different staphylococcal species
have evolved together with their hosts. 13 Moreover,
a recent study of S. intermedius isolates from the skin
of different phylogenetic groups within the Canidae
indicated host specificity and co-evolution within the
animal hosts, even among different strains of
S. intermedius.14
Staphylococcus intermedius is now regarded as a
resident organism on/in the majority of dogs.15 It can
be cultured commonly from the oropharynx, nares and
anal ring of healthy dogs with approximate frequencies
of isolation of 46%, 64% and 60%, respectively.16,17
Lloyd has descriptively termed S. intermedius a
nomad, disseminating from resident sites to secondarily infect existing cutaneous lesions.4
The natural host of S. aureus is humans and it colonizes the nasal passage of up to 40% of healthy adults,
but rarely other body sites in the absence of pre-existing
dermatoses.18 However, Waldvogel reported rectal,
peri-anal and vaginal carriage.19 He considered that the
organism was transferred from these sites to the skin and
that pre-existing lesions are necessary for the infection to
develop and spread. In one study, bacterial cultures
from 60 patients that presented with impetigo in a private
practice were virtually all S. aureus (59 people), with
pure group A beta-haemolytic Streptococcus being
recovered from only one patient.20
Host-adapted species of staphylococci may transiently colonize other species when contact between
hosts is frequent, or infection (rather than mere carriage)
is present.18 Despite this, transmission of S. intermedius
from dogs to humans appears to be rare. In a study of
nasal carriage in the staff of a veterinary school, only
one of 144 persons (0.69%) carried S. intermedius as
part of the nasopharyngeal flora.21 Likewise, the transmission of S. aureus to dogs is very uncommon. In
a study involving 210 dogs with pyoderma, of 201
isolates that were coagulase-positive, 197 (98.01%) were
S. intermedius, three (1.49%) were S. aureus and one
(0.5%) was Staphylococcus hyicus.22
In this study, we have shown that adherence of
S. intermedius and S. aureus to canine and human
corneocytes is highly species-specific. The adherence of
S. intermedius to canine corneocytes was far higher than
that of S. aureus, a finding supporting the results of a
smaller study by Saijonmaa-Koulumies and Lloyd.23
This may explain why the carriage and infection rate by
S. aureus is so low in dogs. Likewise, the adherence of
S. aureus to human corneocytes was far higher than
that of S. intermedius. However, there was no significant difference in the mean adherence of S. intermedius
and S. aureus to canine and human corneocytes,
respectively. As bacterial adherence is the essential
first step in the development of clinical infections,
and the corneocytes are the first physical defensive
barrier against infection, these findings provide one

159

explanation for why skin infections in dogs are rarely transmitted to humans. As adherence of staphylococci is
believed to involve one or more specific adhesinreceptor
interactions,11,24 these findings suggest the existence
of different molecules on the surface of the corneocytes of these two species and/or on the bacterial
surface.
Another important observation from this study is
the different adherence patterns on the corneocytes.
Staphylococcus intermedius adhered more diffusely to
the entire surface of canine and human corneocytes
whereas S. aureus mainly adhered to the periphery of
corneocytes from both species. Previous authors have
commented on the adhesion patterns of S. intermedius
and S. aureus to corneocytes but have not compared
them.2527 It is possible that these findings could be the
result of a different distribution of adhesion molecules
on the corneocytes surfaces.
In the present study, adherence of staphylococci was
compared between corneocytes taken from the ventral
abdomen of dogs and the medial forearm of humans.
In dogs, while differences in adhesion were not found
between cells harvested from the limb, axilla and groin,
significant differences were shown between the head
and neck compared with the dorsum.11 Further studies
are required to compare staphyloccal adherence
between the same and other sites on dogs and humans.
In this preliminary study, the adherence to corneocytes of only one strain of each of S. intermedius and
S. aureus was investigated. There is considerable variation in both the number of binding sites and the affinity
of binding between some strains of S. aureus. Variations in binding between strains of S. aureus have been
shown to, for example, collagen,28 and fibronectin.2931
Further extensive studies are required to investigate
and elucidate possible differences in adherence between
strains of S. intermedius.
Staphylococcal skin infections are rarely transmitted
between dogs. Staphylococcus intermedius is not a particularly virulent organism,32 and the failure to detect
differences in pathogenicity of S. intermedius has
suggested that host factors, such as poorly developed
epidermal defences, are important.33 However, the
specific reasons are unknown. Although speciesspecific adherence of staphylococci is, perhaps, not
unlikely, the lack of transmission of S. intermedius
infection between in-contact dogs cannot be explained
by the possibility of species-specific adherence. Further
studies are needed to investigate this phenomenon.
In summary, this study has demonstrated clear host
specificity in the adherence of staphylococci to corneocytes from humans and dogs, a finding that may subsequently help to explain the lack of cross-infection
between the two species. Further studies are needed to
see whether the differences in adherence demonstrated
are maintained when corneocytes from the same sites
of dogs and humans and when different strains of
staphylococci are compared. In addition, further
exploration of the precise mechanisms responsible for
the phenomenon of adherence might reveal potential

2005 European Society of Veterinary Dermatology, Veterinary Dermatology, 16, 156161

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C Simou et al.

targets for prophylactic and therapeutic targeting of


both canine and human staphylococcal infections.

ACKN OWLEDGE ME NT S
The authors are grateful to Dr Jeremy Brown for his
advice on the use of the computerized image analysis
facilities and to Dr Darren Shaw for helpful comments
on statistical analysis.
Ms Lorna Hume provided excellent technical
assistance.

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Rsum les pyodermites bactriennes sont rarement contagieuses entre les chiens et les hommes. Cette tude
sest intresse lhypothse que des diffrences dadhsion aux cornocytes existent entre les espces S. intermedius
(rencontre le plus souvent chez le chien et S aureus (la plus souvent rencontre chez lhumain). Des cornocytes
ont t prlevs de labdomen ventral de 10 chiens et de lavant-bras de 10 humains (tous sains et sans pass
pathologique de dermatose) en utilisant du scotch double face. Une souche de S. intermedius obtenue dun cas
de pyodermite canine et une souche de S. aureus ont t prpares dans un phosphate buffered saline (PBS) et
ont t appliques en double sur les cultures, en utilisant le PBS comme contrle ngatif. Aprs incubation, rinage
et coloration au cristal violet, une quantification des bactries adhrentes a t ralise en aveugle par ordinateur.
S. intermedius adhrait significativement plus aux cornocytes canins que S. aureus (P = 0.0006), alors que
S. aureus adhrait plus aux cornocytes humains que S. intermedius (P < 0.0001). En outre, le type ddhrence
variait pour les 2 organismes, S. intermedius adhrant toute la surface et S. aureus adhrant surtout la
priphrie. Les prfrences dadhsion pour les deux htes pourraient expliquer, en partie, pourquoi S. intermedius
et S. aureus sont peu frquemment isols en cas dinfection humaine et canine respectivement.
Resumen La pioderma estafiloccica raramente es contagiosa entre perros y humanos o entre humanos y
perros. Este estudio investig la hiptesis que existen diferencias entre especies en la adherencia de S. intermedius
(el aislamiento ms frecuente en perros) y S. aureus (el aislamiento ms frecuente en humanos) a corneocitos caninos
y humanos. Se recogieron laminas de corneocitos de reas ventrales del abdomen de 10 perros y del antebrazo
medial de 10 humanos (todos normales y sin historia o signos fsicos de enfermedad cutnea) utilizando una cinta
adhesiva de doble cara. Se prepararon en suero salino tamponado con fosfato (PBS) S. intermedius de un caso
de Hypoderma canina bacteriana y una cepa humana de S. aureus y se aplicaron por duplicado respectivamente
a cintas adhesivas cubiertas de corneocitos caninos y humanos utilizando PBS como control negativo. Despus
de la incubacin, se enjuagaron y tieron con cristal de violeta, se realizo una cuantificacin ciega de las bacterias
adheridas, mediante un anlisis computerizada de imgenes. Se observ que el S. intermedius se adhera de forma
significativamente superior a los corneocitos caninos que el S. aureus (P = 0.0006), mientras que S. aureus mostr
mayor adherencia a corneocitos humanos que S. intermedius (P < 0.0001). Adems, el patrn de adherencia
difera entre los dos organismos, con el S. intermedius mostrando mayor adherencia a toda la superficie y S. aureus
principalmente a la periferia tanto de los corneocitos caninos como humanos. La preferencia de adherencia de
estos dos huspedes podra explicar, en parte, por qu S. intermedius y S. aureus raramente de aslan de infecciones
cutneas humanas y caninas, respectivamente.

Zusammenfassung Pyodermie durch Staphylokokken ist nur selten von Hunden auf Menschen oder von
Menschen auf Hunde bertragbar. Diese Studie untersucht die Hypothese, da es Speziesunterschiede hinsichtlich
der Adhsion an canine oder humane Korneozyten zwischen S. intermedius (dem hufigsten Isolat bei Hunden)
und S. aureus (dem hufigsten Isolat bei Menschen) gibt. Vom ventralen Abdomen von 10 Hunden und vom
medialen Unterarm von 10 Menschen (alle gesund und ohne irgendeine Vorgeschichte oder irgendwelche
krperlichen Anzeichen einer Hauterkrankung) wurden Korneozytenverbnde unter Verwendung von doppelseitigem Klebeband gesammelt. S. intermedius von einem Fall mit einer caninen bakteriellen Pyodermie und ein
humaer Stamm von S. aureus wurden mit Phospat-gepufferter Kochsalzlsung (PBS) vorbereitet und gleichzeitig
auf mit caninen beziehungsweise humanen Korneozyten bedeckten Klebestreifen mit PBS als Negativkontrolle
verabreicht. Nach Inkubation, Splen und Frben mit Kristallviolet wurde verblindet eine Quntifikation der
anheftenden Bakterien durch computerisierte Bildanalyse ausgefhrt. S. intermedius heftete sich signifikant
strker an canine Korneozyten als an S. aureus (P = 0.0006) an, wogegen S. aureus eine strkere Adhsion an
humane Korneozyten als S. intermedius (P < 0.0001) zeigte. Zustzlich unterschied sich das Adhsionsmuster
der zwei Organismen, wobei S. intermedius sich an die gesamte Oberflche whrend S. aureus sich mehr an die
Peripherie sowohl caniner als auch humaner Korneozyten anheftete. Die Bevorzugung der Anheftung an diese
zwei Wirte kann teilweise erklren, warum S. intermedius und S. aureus so selten von human, beziehungsweise
caninen Hautinfektionen isoliert werden.

2005 European Society of Veterinary Dermatology, Veterinary Dermatology, 16, 156161