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fm Page 171 Thursday, April 26, 2001 4:56 PM

Veterinary Dermatology 2001, 12, 171175

Antimicrobial activity of enrofloxacin against Staphylococcus

intermedius strains isolated from canine pyodermas

Blackwell Science, Ltd

JEAN-PIERRE GANIRE,* CHRISTINE MDAILLE, AGNS LIMET,

NATHALIE RUVOEN* and GENEVIVE ANDR-FONTAINE*
*Unit de Pathologie Infectieuse, Ecole Nationale Vtrinaire, BP 40706, 44307 Nantes Cedex 03, France
Vebiotel, 41 bis, avenue Aristide Briand, 94110 Arcueil, France
Bayer Pharma Division Sant Animale, 13 rue Jean Jaurs, 92807 Puteaux, France
(Received 25 July 2000; accepted 4 October 2000)

Abstract This study examined and compared the minimal inhibition concentrations (MICs) of enrofloxacin
against 393 Staphylococcus intermedius strains isolated in France from canine pyodermas during three different
years, 1995 (174 isolates), 1997 (101 isolates) and 1999 (118 isolates). The MICs of enrofloxacin against these
strains ranged from 0.063 to 64 mg L1, with MIC50 and MIC90 equal to 0.125 and 0.25 mg L1, respectively. Two
resistant strains were found, but only among isolates collected in 1999. The data show that resistance to enrofloxacin among S. intermedius strains is still rare in dogs, but the selection in vitro of variants in which the MICs
were increased 4 16-fold after 10 serial passages in subinhibitory concentrations of enrofloxacin suggests that
inappropriate use might favour the development of resistant strains in vivo.
Keywords: dog, enrofloxacin, MIC, pyoderma, resistance induction, Staphylococcus intermedius.

INTRODUCTION
Enrofloxacin is a fluoroquinolone developed exclusively for use in veterinary medicine, in companion and
food-producing animals. Like other third-generation
quinolones, this antibiotic exhibits bactericidal activity
against a broad spectrum of gram-negative and grampositive bacteria. In dogs, enrofloxacin is indicated for
the treatment of various infections, including canine
pyodermas.
Pyoderma is a commonly encountered disease in
dogs and its treatment usually involves antibiotic therapy. Staphylococcus intermedius, a coagulase positive,
gram-positive coccus, is the main pathogenic bacterial
species responsible for canine pyodermas.1,2,3,4
Staphylococcus intermedius is increasingly reported
to be resistant to many antibiotics3,514 and failures in
treatments cause problems in small animal practice.
Enrofloxacin, has shown good clinical efficacy in pyodermas6,1520 and is an alternative to treatment with
those antibiotics. However, high quinolone usage and
a nonappropriate dosage regimen in dogs may increase
the risk of resistant strain selection. A survey of the
trend of the susceptibility of canine S. intermedius
strains to enrofloxacin is therefore warranted.
This study examines and compares the minimal inhibition concentrations (MICs) of enrofloxacin against
S. intermedius strains isolated in France from canine
pyodermas during three different years, 1995, 1997 and

Correspondence: Jean-Pierre Ganire. Tel.: +33-2-68-76-90, Fax:

+33-2-68-76-94, E-mail: ganiere@vet-nantes.fr
2001 Blackwell Science Ltd

1999, respectively. We also report the experimental

induction of resistance of S. intermedius to enrofloxacin in vitro.

MATERIALS AND METHODS

Bacterial strains
A total of 393 field S. intermedius strains isolated from
clinical cases of canine pyoderma was tested in this
study. One hundred and seventy-four and 101 strains
were isolated during two multicentre field trials conducted in France in 1995 and 1997, respectively. The
118 strains tested in 1999 were collected from several
French veterinary clinical laboratories.
The strains were identified as S. intermedius using
standard microbiological procedures and differentiated in particular from S. aureus by lack of betahaemolysis on sheep blood agar, lack of colony pigment, lack of acid production from d-mannitol and
negative reaction for Voges-Proskauer test. The strains
were stored at 80 C until required.
Determination of MIC of enrofloxacin
Enrofloxacin was supplied by Bayer AG (Leverkusen,
Germany). MICs were determined using a twofold
serial dilution method in Mueller-Hinton agar
(Biomrieux, Marcy-LEtoile, France), performed
according to the recommendations of the French Society of Microbiology.21 The strains were subcultured in
Mueller-Hinton broth and 104 colony-forming units
(c.f.u.) per spot were spread onto agar plates using a
multipoint inoculator. A reference strain (S. aureus
171

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172

J.-P. Ganire et al.

ATCC 25923) was systematically included in assays.

The MIC was defined as the lowest concentration of
enrofloxacin that inhibited visible growth on agar after
incubation for 18 h at 37 C. MIC50 and MIC90 were
defined as the lowest concentration that inhibited the
visible growth of 50 and 90% of the tested strains,
respectively.
Induction of resistant variants to enrofloxacin
Ten serial passages were carried out with five susceptible strains (strains isolated in 1995) in subinhibitory
concentrations of enrofloxacin. After control of the
MIC, each strain was streaked onto Mueller-Hinton
agar plates containing between half and four times the
MIC of enrofloxacin per mL (MIC0) of the wild
strain.22,23 The plates were incubated at 37 C for 48 h.
For each subsequent passage, colonies were collected
from the plate containing the highest concentration of
enrofloxacin and subcultured onto another set of
plates in which the antibiotic concentrations were
adjusted according to the new MICs. Bacterial samples
from the fifth and tenth passages were subcultured
onto agar without antibiotics and then tested for their
MIC vs. their wild-types.
Statistical analyses
The proportions of susceptible or resistant strains
between the three study periods were compared using
the chi-squared test. Differences were considered significant at P < 0.05.

RESULTS
MICs of enrofloxacin
Results are shown in Fig. 1 and Table 1. According to
the susceptibility and resistance breakpoints, a strain is
considered susceptible when the MIC is 0.5 mg L1
and resistant when the MIC is 4 mg L1.
The MICs of enrofloxacin against the strains isolated in 1995 and 1997 ranged from 0.063 to 1 mg L1,
and 98.8 and 98%, respectively, of these strains were

Table 1. Minimum inhibitory concentrations (MIC, mg L1) of

enrofloxacin against 393 field strains of Staphylococcus intermedius
isolated from canine pyodermas
MIC (mg L1)

Year of
isolation

Number
of isolates

50%

90%

Range

1995
1997
1999

174
101
118

0.125
0.125
0.125

0.25
0.125
0.125

0.0631
0.0631
0.06364

Total

393

0.125

0.25

0.06364

Table 2. Susceptibility of five Staphylococcus intermedius strains to

enrofloxacin before (MIC0) and after 5 (MICfifth) and 10 (MICtenth)
serial passages in subinhibitory concentrations of enrofloxacin
(mg L1)

Strain 95B17
Strain 95B182
Strain 95B192
Strain 95B208
Strain 95B210

MIC0

MICfifth

MICtenth

0.063
0.25
0.25
0.25
0.25

0.5
0.5
0.5
1
1

1
2
1
1
2

susceptible. Only four strains (two in 1995 and two in

1997) were intermediate, with MICs equal to 1 mg L1.
None of the strains showed any resistance.
The MICs against the strains tested in 1999 ranged
from 0.063 to 64 mgL1, and 98.3% of the isolates were
susceptible. One strain had an intermediate MIC
(2 mg L1) and one strain was resistant (MIC =
64 mg L1).
MIC50, equal to 0.125 mg L1, was identical for the
three periods. MIC90 was 0.25 mg L1 against the isolates tested in 1995, but 0.125 mg L1 during 1997 and 1999.
The MIC90 overall was 0.25 mg L1.
Induction of resistant variants
Results are shown in Table 2. The five strains were initially susceptible; one had a lower MIC (0.063 mg L1)
than the others whose MIC values corresponded to
MIC90 (0.25 mg L1). At the fifth passage, MICs of

Figure 1. Distribution of the minimum

inhibitory concentrations (MIC, mg L1) of
enrofloxacin against 393 field strains of
Staphylococcus intermedius isolated in 1995,
1997 and 1999 from canine pyodermas.
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Antimicrobial activity of enrofloxacin

enrofloxacin increased by a factor of 28. At the end of
the 10 serial passages, MICs were increased 416-fold
and reached 12 mg L1.

DISCUSSION
Over and above elimination of predisposing factors
and avoidance of corticosteroids,8,16 successful therapy
of canine pyodermas due to S. intermedius requires the
use of an appropriate antibiotic given at an effective
dosage and sufficient duration of treatment. Pharmacodynamic and pharmacokinetic parameters of enrofloxacin have already been established in the dog,2426
and the available data allow us to optimize the use
of this antibiotic according to the MICs against
S. intermedius. In general, these MICs range from 0.2
to 1 mg L1,24 and considering that the resistance
breakpoint for enrofloxacin corresponds to a MIC
4 mg L1, it is important to have updated data on the
susceptibility trend of isolates and the occurrence of
resistant strains.
Resistance to fluoroquinolones develops by chromosomal mutations. It is mediated by target changes
(DNA gyrase and/or topoisomerase IV) and/or reduced intracellular accumulation.27 In S. aureus,28,29
gyrA-mediated resistance is probably the most important mechanism of resistance to quinolones, generally associated with a mutation in parC (DNA
topoisomerase IV subunit A). An efflux pump (norA
in norfloxacin resistance) is also incriminated in staphylococcal resistance. The mechanisms of resistance
in S. intermedius are not yet known, but there are some
data that suggest that they are certainly similar to those
described for S. aureus.30
Several reports have mentioned the isolation of
S. intermedius strains resistant to fluoroquinolones in
canine skin and/or ear infections, but with occurrences
often < 1%.6,9,12,13,15,3032 Moreover, in these studies,
intermediate strains were often grouped as resistant.
Fluoroquinolones were authorized and marketed
in France for use in small animal practice in 1995 for
marbofloxacin and 1996 for enrofloxacin. However,
flumequin was already used in dogs. In our study,
no resistance to enrofloxacin was detected among the
174 isolates collected in France in 1995. Other studies
performed on isolates collected over the period 1989
95 in several European countries10,11,33 showed identical data, and Stegemann et al. reported the isolation of
only one enrofloxacin-resistant strain (MIC = 8 mg L1)
among a total of 160 isolates from dogs with skin and
ear infections collected in 1993 and 1994 in Germany.25
Despite the increasing use of fluoroquinolones in
dogs since 1995, none of the strains collected in 1997
was resistant to enrofloxacin, and paradoxically, if
MIC50 remained stable (equal to 0.125 mg L1 as in
1995), MIC90 decreased significantly in 1997 from 0.25
to 0.125 mg L1.
In 1999, MIC90 remained equal to 0.125 mg L1, but
two isolates had a MIC 2 mg L1. The first, isolated

173

from a dog treated with a fluoroquinolone for a chronic

skin infection of the labial region, appeared to have
intermediate values for enrofloxacin (MIC = 2 mg L1).
But, when we tested this strain against marbofloxacin and danofloxacin (results not shown), we revealed
(with a MIC = 4 mg L1 for these two antibiotics) a
low level of resistance against fluoroquinolones.
However, this isolate did not have any associated resistance to other antibiotics such as amoxicillin and
cephalexin, gentamicin, doxycycline, lincomycin and
clindamycin (results not shown). The second strain,
isolated from a dog with a chronic skin infection of
the ear and treated with several antibiotics including
a fluoroquinolone, appeared to have a high level of
resistance, with a MIC = 64 mg L1 for enrofloxacin
and 32 mg L1 for marbofloxacin and danofloxacin
(results not shown). This strain was also resistant to
lincomycin and clindamycin, but was susceptible to
amoxicilin, cephalexin, gentamicin and doxycycline
(results not shown). The histories of these two cases
were not detailed, but it was possible to think that the
conditions of treatment might favour the selection
of resistant strains, particularly if the bacteria were
exposed to subinhibitory antibiotical concentrations.
Selective pressure in vitro was frequently used to
determine whether it would give rise to resistance patterns similar to those encountered under field conditions and to investigate the mechanisms involved. In
our study, S. intermedius strains showed a 416-fold
decrease in susceptibility after 10 passages in subinhibitory concentrations of enrofloxacin. We failed to select
resistant variants with MIC values 4 mg L1. However, a higher number of serial passages may have
allowed MICs of that level to be obtained. We selected
only intermediate variants with MICs of 12 mg L1.
Nevertheless, the increased MIC of enrofloxacin suggests that inappropriate use in the field might favour
the development of intermediate or resistant strains
in vivo. In dogs, therapy of severe pyodermas often
requires treatment for periods of several months, and
the length of treatment might also favour the development of resistant strains. Carlotti et al. recently
reported one case of failure of treatment with marbofloxacin in a dog with deep pyoderma, in which a resistant strain of S. intermedius was cultured at day 28,
whereas no resistance to marbofloxacin had been
observed at day 0.7 Scott recently reported the isolation of resistant strains from three dogs with recurrent deep pyoderma; in all three cases, the dogs had
previously received multiple antibiotics, including
enrofloxacin.32 In our study, the two resistant strains
were also isolated from animals treated previously with
fluoroquinolones.
It is not surprising that fluoroquinolone resistance
was revealed in our study. Similar observations have
been reported in the UK, where four resistant strains
were identified over the period 199698 (one in 1996,
two in 1997 and one in 1998) among 429 isolates.30
However, the very low occurrence of resistant strains
and the level of MICs recorded in our study confirm the
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J.-P. Ganire et al.

interest of enrofloxacin in the treatment of infections

caused by S. intermedius. Like other third-generation
fluoroquinolones, enrofloxacin remains the antibiotic
of choice for antimicrobial therapy in mixed infections,
in recurrent pyoderma, in chronic, deep pyoderma
with extensive scar tissue, or when canine pyodermas
have been refractory to first-line antibiotics.34 However, bacterial isolation for antibiotic susceptibility
testing and a review of the clinical response to therapy
may be appropriate because of the possible occurrence
of resistant strains, particularly when long-term treatment is required. Moreover, enrofloxacin should be
avoided for chronic low-dose or pulse-dose.

14.

15.

16.
17.
18.

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Rsum Cette tude sest intresse valuer et comparer les concentrations inhibitrices minimales (MICs)
de lenrofloxacine sur 393 souches de Staphylococcus intermedius isoles en France partir de cas de pyodermites
canines pendant trois annes diffrentes, 1995 (174 isolats), 1997 (101 isolats) et 1999 (118 isolats). Les MICs de
lenrofloxacine contre ces souches variaient entre 0.063 et 64 mg L1, avec des MIC50 et MIC90 de 0.125 et
0.25 mg L1, respectivement. Deux souches rsistantes ont t observes, mais seulement parmi les souches de
1999. Ces donnes montrent que la rsistance de S. intermedius lenrofloxacine est rare. La slection in vitro de
souches pour lesquelles les MICs taient augmentes 4-16 fois aprs 10 expositions conscutives des concentrations subinhibitrices denrofloxacine suggre quune utilisation inapproprie de cette molcule pourrait
favoriser le dveloppement de souches rsistantes in vivo. [Ganire, J.-P., Mdaille, C., Limet, A., Ruvoen N.,
Andr-Fontaine, G. Antimicrobial activity of enrofloxacin against Staphylococcus intermedius strains isolated
from canine pyodermas. (Effet antibactrien de lenrofloxacine sur des souches de Staphylococcus intermedius
isoles partir de pyodermites canines.) Veterinary Dermatology 12: 171175.]
Resumen Este estudio examin y compar las concentraciones inhibitorias mnimas (CIMs) de la enrofloxacina
contra 393 cepas de Staphylococcus intermedius aisladas en Francia de piodermas caninas durante tres aos diferentes, 1995 (174 aislamientos), 1997 (101 aislamientos) y 1999 (118 aislamientos). Las CIMs de enrofloxacina
contra estas cepas oscilaron entre 0.063 y 64 mg L1, con CIM50 y CIM90 igual a 0.125 y 0.25 mg L1, respectivamente. Se encontraron dos cepas resistentes, pero slo en aislamientos recogidos en 1999. Estos datos muestran
que la resistencia a la enrofloxacina entre las cepas de S. intermedius sigue siendo infrecuente en perros, pero la
seleccin in vitro de variantes, en las que las CIMs se encontraban incrementadas entre 4 y 16 veces despus de
10 pases seriados en concentraciones subinhibitorias de enrofloxacina, sugiere que el uso inadecuado de este
frmaco podra favorecer el desarrollo de cepas resistentes in vivo. [Ganire, J.-P., Mdaille, C., Limet, A., Ruvoen N.,
Andr-Fontaine, G. Antimicrobial activity of enrofloxacin against Staphylococcus intermedius strains isolated from
canine pyodermas. (Actividad antimicrobiana de la enrofloxacina contra cepas de Staphylococcus intermedius
aisladas de piodermas caninas.) Veterinary Dermatology 12: 171175.]
Zusammenfassung Diese Studie berprfte und verglich die minimalen Hemmkonzentrationen (minimal
inhibition concentrations = MICs) von Enrofloxacin gegen 393 Staphylococcus intermedius-Stmme, die in
Frankreich von Hundepyodermien in den Jahren 1995 (174 Isolate), 1997 (101 Isolate) und 1999 (118 Isolate)
isoliert wurden. Die MICs von Enrofloxacin gegen diese Stmme reichte von 0,063 bis 64 mg L1, mit MIC50 und
MIC90 von 0,125 und 0,25 mg L1. Zwei resistente Stmme wurden gefunden, beide von 1999. Diese Daten zeigen,
dass Enrofloxacin-Resistenz bei S.-intermedius-Stmmen beim Hund noch selten ist, aber die in vitro Auswahl
der Varianten, bei denen die MICs nach10 Serienpassagen mit subinhibitorischen Konzentrationen von
Enrofloxacin 4-16-fach erhht waren, deutet darauf hin, dass unsachgemsser Gebrauch die Entwicklung resistenter Stmme in vivo erleichtern knnte. [Ganire, J.-P., Mdaille, C., Limet, A., Ruvoen N., Andr-Fontaine, G.
Antimicrobial activity of enrofloxacin against Staphylococcus intermedius strains isolated from canine pyodermas.
(Antimikrobielle Aktivitt von Enrofloxacin gegen von Hundepyodermien isolierte Staphylococcus intermedius
Stmme.) Veterinary Dermatology 12: 171175.]

2001 Blackwell Science Ltd, Veterinary Dermatology, 12, 171175