DOI: 10.1111/j.1365-3164.2009.00842.

Species distribution and antimicrobial susceptibility

of staphylococci isolated from canine otitis externa

Bruno Penna, Renato Varges, Luciana Medeiros, microorganisms are not routinely cultured from the nor-
Gabriel M. Martins, Rodrigo R. Martins and mal ear canal, Pseudomonas aeruginosa, Proteus mirabi-
Walter Lilenbaum lis, Klebsiella pneumoniae and Escherichia coli are also
contributors to the pathogenesis of otitis.1
Laboratório de Bacteriologia Veterinária, Instituto Biomédico, The delineation of S. intermedius species was useful
Universidade Federal Fluminense, Niterói, RJ, Brazil because it separated them from S. aureus thereby avoid-
Correspondence: Walter Lilenbaum, Laboratório de Bacteriologia ing an epidemiologically important source of confusion.4
Veterinária, Instituto Biomédico, Rua Prof. Hernani Mello, 101 sala More recently, strains of S. intermedius found in the dog
309, Niterói, RJ, CEP 24210-130, Brazil. E-mail: [email protected]
and identified by traditional means are classified as
Conflict of Interest
No conflicts of interest have been declared.
S. pseudintermedius, unless shown by genomic investi-
Sources of Funding gation to belong to other related species.4 Although this
CAPES, FAPERJ and FLAP, from Brazil. coagulase-positive species is the most frequent Staphylo-
coccus species isolated from dogs, other species of
staphylococci have been reported, including the
Abstract coagulase-positive species S. aureus and S. schleiferi
The diversity of species of the genus Staphylococcus coagulans, as well as the coagulase-negative species
sp. and the antimicrobial resistance of isolates S. epidermidis, S. schleiferi schleiferi, S. simulans and
from 151 unmedicated dogs of both sexes with a S. saprophyticus.5–8
clinical diagnosis of otitis were recorded. Ninety-one Since members of this Staphylococcus genus have a
isolates of Staphylococcus spp. were identified by high frequency of conjugation and constantly acquire plas-
biochemical reactions and tested for susceptibility to mids containing genes that codify for antimicrobial resis-
15 antimicrobials. Coagulase-positive species were tance,9,10 knowledge of their resistance patterns to
most common; S. pseudintermedius (38.4%), antimicrobial drugs requires frequent updating. Empirical
S. schleiferi schleiferi (15.4%), S. aureus (14.3%), treatments without the assistance of antimicrobial sus-
S. epidermidis (11%), S. simulans (11%), S. schleiferi ceptibility test data may result in therapeutic failure and
coagulans (8.8%) and S. saprophyticus (1.1%). All the the selection of multiresistant strains.8
isolates showed resistance to at least one drug and The purpose of the present study was to evaluate the
89% were multiresistant. Amoxicillin combined with diversity of species and to determine the antimicrobial
clavulanic acid and oxacillin were the most effective, resistance of Staphylococcus spp. isolates obtained from
while resistance was widely observed for neomycin dogs with otitis externa.
and erythromycin. The results highlight the recogni-
tion and the potential need for bacterial culture with
species identification and antimicrobial susceptibility Materials and methods
tests for appropriate antimicrobial therapy.
Samples
Accepted 21 July 2009 This was a prospective study. Samples were obtained from 151 adult
(1–8 years) dogs of both sexes diagnosed with otitis externa but
unmedicated for at least 15 days. A sterile cotton swab was used to
collect samples of ear exudates. The cotton swabs were inoculated
in Brain Heart Infusion broth (Difco, Franklin Lakes, NJ, USA) and
Introduction incubated at 37 C. Only one sample from each dog was studied,
even if both ears presented with clinical signs.
Canine otitis externa is one of the most common dis-
eases encountered in veterinary practice and is estimated Inclusion criteria
to affect between 5% and 20% of dogs.1 Infectious otitis Dogs included had to present with clinical signs in at least one ear.
externa commonly occurs as a secondary complication of Signs of otitis externa included local pain, pruritus, erythema, ear dis-
primary factors that initiate inflammation within ears, charge and desquamation. Ears were screened with cytological for
evidence of cocci and subsequent pure cultures of staphylococci-like
such as atopic dermatitis, cutaneous adverse reactions to
bacteria as seen on Gram stain of cultured colonies were included.
food, foreign bodies, ectoparasites, metabolic diseases,
keratinization abnormalities, and autoimmune diseases.2
Bacteriological culture
The most common pathogens in the aetiology of otitis If growth occurred after 24 or 48 h, smears were made, Gram
include members of the Staphylococcus genus, mainly stained and examined microscopically. Samples containing both
S. pseudintermedius, which is often present in low gram-positive and gram-negative bacteria were not considered
numbers in healthy ears.1,3 Although gram-negative for this study, since on those mixed cultures the exact role of

292 ª 2009 The Authors. Journal compilation ª 2009 ESVD and ACVD, Veterinary Dermatology, 21, 292–296.
 Staphylococcus in canine otitis externa

staphylococci as agents of the infection cannot be determined. erythromycin (15 lg), mupirocin (5 lg), bacitracin (10 lg) and chl-
Samples with morphologies compatible with Staphylococcus spp. oramphenicol (30 lg) were also tested. After measuring the antimi-
were transferred to tryptic soy agar, 5% sheep blood agar and manni- crobial zone diameters and following the National Committee for
tol salt agar (Merck, Darmstadt, Germany). Methodology for isolation Clinical Laboratory Standards13, the isolates were categorized as sen-
of anaerobic bacteria was not employed, since staphylococci are fac- sitive or resistant to the drug. Intermediate susceptibility was
ultative aerobes. Isolates in pure culture were identified on the basis regarded as resistant. A breakpoint for multiresistance has not yet
of colony morphology, Gram staining, pigment production, haemoly- well been standardized and varies among researchers.8,15 In the
sis on 5% bovine blood agar and biochemical reactions, including present study, multiresistance was defined as resistance to three or
catalase activity test, resistance to Bacitracin 0.04 U, acid production more antimicrobial classes.
in Hugh-Leifson’s OF base medium, tube coagulase test, acetoin
production, urease, novobiocin resistance, deoxyribonuclease test,
ornithine and arginine utilization and aerobic fermentation of sucrose, Results
D-mannose, D-cellobiose, D-xylose, L-arabinose, raffinose, D-trehalose,
maltose and D-mannitol. Staphylococcus species were classified
Ninety-one of the 151 samples yielded Staphylococcus
according to reference methods.11–13 spp. in pure culture, representing 60.3% of the total iso-
lates. Since these samples were inoculated on an enrich-
Susceptibility tests ment medium before plating, the assessment of colony
All the staphylococci isolates were tested for susceptibility to antimi- numbers from the clinical samples was not possible.
crobial agents by the agar disc diffusion method on Mueller Hinton Among these 91 isolates, the coagulase-positive staphy-
Agar (Difco).14 Fifteen of the most commonly used antibiotics in our lococci (CoPS) were the most frequently isolated, while
local geographic area were included in this study, using commercial coagulase-negative staphylococci (CoNS) were isolated
discs containing plasma concentrations of the drugs. Aminoglyco-
from 35 samples (38.5%). No more than one species of
sides were represented by gentamicin (10 lg), neomycin (30 lg) and
amikacin (30 lg), fluoroquinolones were represented by ciprofloxacin
staphylococci was cultured from an affected ear
(5 lg) and enrofloxacin (5 lg). Penicillins were represented by the (Table 1).
amoxicillin–clavulanic acid combination – AMC (10 lg), amoxicillin All the isolates were resistant to at least one drug, and
(10 lg) and oxacillin (1 lg). Cephalosporins were represented by multiresistance was common, both with CoPS and CoNS.
cefalexin (30 lg) and cefadroxil (30 lg). Nitrofurantoin (300 lg), One isolate of S. aureus, one of S. pseudintermedius and
one of S. simulans were resistant to all tested classes of
antimicrobial agents (Table 1).
Table 1. Distribution of multiresistant strains of different staphylo- Resistance to aminoglycosides was frequently
coccal species from 151 unmedicated dogs with otitis externa from observed; neomycin and gentamicin were the less effec-
Rio de Janeiro, Brazil tive drugs of this class, while amikacin was only some-
Species MI ⁄ TI % what more effective. Although oxacillin was the most
CoPS 49 ⁄ 56 87.5 effective antibiotic of the study, overall resistance to the
S. pseudintermedius 33 ⁄ 35 85.7 penicillins as a group was very common and mainly direc-
S. aureus 13 ⁄ 13 100 ted to amoxicillin. Nevertheless, when it was combined
S. schleiferi coagulans 6⁄8 75 with clavulanic acid, the number of resistant isolates
CoNS 33 ⁄ 35 94.3 dropped considerably. Overall resistance to the cephalo-
S. epidermidis 10 ⁄ 10 100
sporin class was not frequent, and resistance to the two
S. simulans 9 ⁄ 10 90
S. schleiferi schleiferi 13 ⁄ 14 92.8 tested drugs was almost the same. Resistance to the
S. saprophyticus 1⁄1 100 fluoroquinolones as a group could be detected mainly
Total 82 ⁄ 91 90.1 directed to either ciprofloxacin or enrofloxacin, while a
CoPS, coagulase-positive staphylococci; CoNS, coagulase-negative great proportion of resistant isolates could be observed to
staphylococci; MI, number of multiresistant isolates; TI, number of erythromycin, bacitracin, chloramphenicol and mupirocin
total isolates. (Table 2).

Table 2. Antimicrobial susceptibility of seven staphylococci species from 151 unmedicated dogs with otitis externa from Rio de Janeiro, Brazil
Antimicrobial resistance (%)

AMC AMI AMO BAC CFD CFE CIP CLO ENO ERI GEN MUP NEO NIT OXA
S. pseudintermedius 14.3 48.6 71.4 54.3 22.8 25.7 45.7 51.4 48.6 80 54.3 37.1 91.4 22.8 14.3
S. aureus 23.1 46.1 69.2 92.3 30.8 30.8 53.8 53.8 53.8 84.6 84.6 46.1 84.6 53.8 15.4
S. schleiferi coagulans 12.5 25 25 62.5 12.5 12.5 25 0 12.5 75 62.5 37.5 87.5 50 12.5
S. schleiferi schleiferi 21.4 71.4 92.8 50 21.4 28.6 57.1 57.1 42.8 92.8 85.7 78.6 100 42.8 14.2
S. epidermidis 0 60 70 60 30 20 30 70 20 90 60 40 90 40 0
S. simulans 30 40 80 70 50 50 60 80 80 100 70 60 80 50 30
S. saprophyticus 0 0 0 0 0 0 0 100 0 100 0 100 0 100 0
Overall resistance 16.5 50.5 70.3 61.5 29.7 28.6 46.1 53.8 45.1 85.7 65.9 48.4 87.9 38.5 11.8
Numbers and percentages in each column under ‘antimicrobial resistance’ represent proportions of isolates that were resistant to each antibiotic.
The rates of resistance of each staphylococci isolated in the study to each antimicrobial agent are shown. Percentages indicate frequencies of
resistant isolates to each antimicrobial agent in the period of the study. AMC, amoxicillin + clavulanic acid; AMO, amoxicillin; OXA, oxidizing; CFD,
cefadroxil; CFE, cefalexin; CIP, ciprofloxacin; ENO, enrofloxacin; CLO, chloramphenicol; AMI, amikacin; GEN, gentamicin; NEO, neomycin; BAC,
bacitracin; ERI, erythromycin; MUP, mupirocin; NIT, nitrofurantoin.

ª 2009 The Authors. Journal compilation ª 2009 ESVD and ACVD, Veterinary Dermatology, 21, 292–296. 293
Penna et al.

ously been reported in staphylococcal strains of canine

Discussion
origin in various countries.25,26
Although staphylococci are members of the normal flora The cephalosporins were associated with the lowest
of the ear, the fact that they were obtained in pure culture incidence of resistance. Resistance to the tested drugs
from dogs who met the inclusion criteria indicates their of this class was very similar, ranging from 28.6% to
importance in the pathogenesis of otitis, a conclusion 29.7%. Only one S. pseudintermedius isolate was resis-
which supports previous findings.5 In a similar population tant to cefadroxil and susceptible to cefalexin. This sug-
of dogs from Rio de Janeiro, Brazil, with clinical signs of gests that the resistance mechanism for both drugs is
canine otitis externa, 67.7% of the isolates were mem- the same, since the majority of the isolates when resis-
bers of this genus. Other studies have also reported a tant to one cephalosporin drug were also resistant to the
high frequency of staphylococci isolates, varying from other. Cefalexin is the most frequently used systemic
36.3% in Canada16, 39.5% in France17 to 48.3% in antibiotic in veterinary dermatology, and it has been
Japan.18 reported that resistance of S. pseudintermedius to
The high prevalence of CoPS also agrees with other cefalexin is unusual, except for meticillin-resistant
studies16,17, and the predominance of S. pseudintermedi- strains17,18, a finding that contrasts to the present find-
us over S. aureus and S. schleiferi coagulans was not ings where only 50% (13 ⁄ 26) of the staphylococci iso-
unexpected, since this species (previously known as lates that were resistant to cefalexin were also resistant
S. intermedius) is known as the major staphylococcal to oxacillin.
species in canine infections.1,3,17,19 It is well known that In relation to aminoglycosides, gentamicin was a very
CoNS constitute a major component of the normal micro- efficient drug for the treatment of canine otitis externa in
flora of human beings, dogs and cats.20 Nevertheless, 197727, with resistance seen in only 5.6% of the isolates.
they can initiate opportunistic infections such as otitis and It was reported as 3.7% in 199828 and as 15.9% in 2000.5
have been reported in other otitis externa studies.5,17 This is in contrast to the 65.9% of resistant isolates
Some 38% of the isolates in this study were CoNS. Other observed in this study. Although it could be argued that
studies evaluating canine otitis externa have reported these resistance rates may vary with geographic areas, it
lower incidences of these species.1,3,7 The predisposing is important to note that the 15.9% resistance in the
factors that may have resulted in the higher incidence of 2000 study5 was generated in the same geographic area.
these opportunistic bacteria in the current study are not This suggests misuse and ⁄ or the excessive use of this
known. drug for the treatment of canine otitis in Brazil. A very
Antimicrobial resistance was common, and all isolates high rate of resistance was also seen for neomycin
were resistant to at least one antimicrobial drug. The (87.9%), a very common antibiotic in otic products. This
degree of multiresistance was much higher than in previ- may also be a result of widespread and possibly indis-
ous studies7,17,18,21–23 and supports the view8,10 that criminate or inappropriate use. Based on these results,
rapid development and spread of antimicrobial resistance the empiric use of aminoglycosides for routinely treating
of this genus is indeed occurring in our local environment. canine otitis externa must be questioned in this geo-
This could be because the antimicrobial agents tested in graphic area.
this study are commonly encountered in the principal for- Other studies have reported resistance to erythromy-
mulations available for otitis externa treatment and over- cin, a member of the macrolides group, varying from
usage may be leading to the selection of resistant strains 7.8% in Japan, 10% in Australia to 21% in the USA.29 All
of staphylococci of canine origin. are much lower than the 85.7% observed in the present
The production of the enzyme b-lactamase is the major study. Staphylococcus pseudintermedius isolates have
mechanism by which staphylococci acquire resistance.9 been reported as increasingly more resistant to macro-
Therefore, the high incidence of resistance to amoxicillin lides30,31, which also may be explained by their increased
observed in the present study was not surprising, since it use in canine clinical practice.
has recently been demonstrated16 that up to 62% the iso- Resistance to the individual fluoroquinolones was
lates of the S. pseudintermedius strains of canine origin very similar, ranging from 45.1% to 46.1%. The rapid
from France were b-lactamase producers. When com- introduction of these drugs into companion animal
pared to a previous Brazilian study in 20005, where much practice and the increasing use of new quinolones
lower resistance rate (41.2%) was observed in a similar over the past 10 years has led to increasing resis-
population, it would appear that resistance to penicillins tance.18,22 Resistance to quinolones develops by chro-
may have increased substantially. When combined with mosomal mutations and is mediated by target changes
clavulanic acid, the AMC was one of the most efficacious (DNA gyrase and ⁄ or topoisomerase IV) and ⁄ or reduced
antimicrobials tested. intracellular accumulation with an efflux pump.17 To
An increase in local resistance was also noted with avoid increasing resistance problems, fluoroquinolones
respect to oxacillin. Although resistance to oxacillin is still should not be used as first-line choices in the manage-
lower than that associated with other drugs, it would ment of staphylococcal otitis externa. Their use should
appear to have been increasing in recent years. In 2000, be reserved for those cases supported by culture and
our group reported resistance in only 4.6% of isolates.5 In sensitivity data.
a retrospective study conducted in the USA, it was noted It is important to point out that the samples processed
that the resistance to oxacillin in the period of 2001 to in the present study were provided by clinical practitio-
2005 had substantially increased in clinical samples of ners. Therefore, it is possible that some of these animals
canine origin.24 Meticillin ⁄ oxacillin resistance has previ- had been treated with antimicrobial agents prior to the

294 ª 2009 The Authors. Journal compilation ª 2009 ESVD and ACVD, Veterinary Dermatology, 21, 292–296.
 Staphylococcus in canine otitis externa

collection of the study samples. This could contribute to a 10. Morris DO, Rook KA, Shofer FS et al. Screening of Staphylococ-
higher resistance rate amongst these isolates. cus aureus, Staphylococcus intermedius and Staphylococcus
schleiferi isolates obtained from small companion animals for
It is important to note that the in vitro resistance of
antimicrobial resistance: a retrospective review of 749 isolates
these drugs may not be accurate reflections of in vivo (2003–04). Veterinary Dermatology 2006; 17: 332–7.
efficacy, especially when they are used as topical medica- 11. Bannerman TL. Staphylococcus, Micrococcus, and other cata-
tions in ears. The Kirby Bauer (KB) test system utilizes lase-positive cocci that grow aerobically. In: Murray PR, Barron
low concentrations of drugs, as would be associated with EJ, Pfaller MA et al., eds. Manual of Clinical Microbiology, 8th
plasma concentrations when the drugs are used paren- edn. Washington, DC: ASM Press, 2003: 84–404.
terally. The topical use of some of these drugs allows for 12. Mac Faddin JF. Biochemical Tests for Identification of Medical
Bacteria. Baltimore, MD: Williams & Wilkins Company, 1997.
the attainment of much higher local drug concentrations
13. Holt JG, Krieg NR, Sneath PHA et al. Staphylococcus spp. In:
which may exceed the minimum inhibitory concentra- Holt JG, ed. Bergey’s Manual of Determinative Bacteriology, 9th
tions of apparently resistant drugs as defined by the KB edn. Baltimore, MD: Williams & Wilkins, 1994: 544–51.
system. 14. Anonymous. Performance Standards for Antimicrobial Suscepti-
In conclusion, the antimicrobial resistance of staphylo- bility Testing, 9th edn. Approved Standard Document. Villanova,
coccal isolates from cases of canine otitis externa appear PA: National Committee for Clinical Laboratory Standards (USA),
to be increasing worldwide, especially in Brazil. This may 2008.
15. Hariharan H, Coles M, Poole D et al. Update on antimicrobial
be the product of widespread and ⁄ or indiscriminate or
susceptibilities of bacterial isolates from canine and feline otitis
inappropriate use. The present study highlights the possi- externa. Canadian Veterinary Journal 2006; 47: 253–5.
ble importance of CoNS in the pathogenesis of canine oti- 16. Prescott JF, Hanna WJB, Smith RR et al. Antimicrobial drug use
tis externa. These data would also argue for the early and resistance in dogs. Canadian Veterinary Journal 2002; 43:
consideration of culture and sensitivity testing in the man- 107–16.
agement of cases of otitis externa that are not responding 17. Ganiere JP, Medaille C, Mangion C. Antimicrobial drug suscepti-
bility of Staphylococcus intermedius clinical isolates from canine
to empiric therapy.
pyoderma. Journal of Veterinary Medicine 2005; 52: 25–31.
18. Yamashita K, Shimizu A, Kawano J et al. Isolation and character-
Acknowledgements ization of staphylococci from external auditory meatus of dogs
with or without otitis externa with special reference to Staphylo-
This study was funded by CAPES, FAPERJ and FLAP, coccus schleiferi subsp. coagulans Isolates. Journal of Veterinary
from Brazil. WL is a research fellow of CNPq. The authors Medical Science 2005; 67: 263–8.
also much appreciate the contributions of M. Giambiagi 19. Biberstein EL, Jang SS, Hirsh DC. Species distribution of coagu-
lase-positive staphylococci in animals. Journal of Clinical Microbi-
de Marval and the practitioner collaboration.
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20. Lilenbaum W, Nunes ELC, Azevedo MAI. Prevalence and antimi-
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Résumé La diversité des espèces du genre Staphylococcus sp. et leur résistance antimicrobienne ont
été déterminées à partir d’échantillons de 151 chiens mâles ou femelles, non traités, atteints d’otite. Les
réactions biochimiques ont permis d’identifier 91 souches de Staphylococcus spp. et de tester leur suscep-
tibilité vis-à-vis de 15 antimicrobiens. Les espèces coagulases positives étaient les plus fréquentes;
S. pseudintermedius (38.4%), S. schleiferi schleiferi (15.4%), S. aureus (14.3%), S. epidermidis (11%),
S. simulans (11%), S. schleiferi coagulans (8.8%) et S. saprophyticus (1.1%). Tous les échantillons ont
révélé une résistance à au moins un antimicrobien et 89% étaient multirésistants. L’amoxicilline combinée
à l’acide clavulanique et l’oxacilline étaient les plus actifs alors que la résistance était largement observée
pour la néomycine et l’érythromycine. Ces résultats ont révélé la nécessité d’effectuer une culture bactéri-
enne pour identifier les bactéries et effectuer des tests de susceptibilité antimicrobienne afin de mettre en
place une thérapie antimicrobienne adaptée.

Resumen Se anotaron la diversidad de especies del genero Staphyloccus sp. y la resistencia antimicrobi-
ana de aislados de 151 perros no medicados de ambos sexos con diagnostico clı́nico de otitis. Se identifica-
ron 91 aislados de Staphylococcus spp. mediante reacciones bioquı́micas y se probaron para
susceptibilidad a 15 antimicrobianos. Las especies coagulasa positivas fueron mas comunes; S. pseudin-
termedius (38,4%), S. schleiferi schleiferi (15,4%), S. aureus (14,3%), S. epidermidis (11%), S. simulans
(11%), S. schleiferi coagulans (8.8%) y S. saprophyticus (1,1%). Todos los aislados mostraron resistencia
al menos a un compuesto y 89% eran multiresistentes. La combinación amoxicilina-ácido clavulánico y la
oxacilina fueron los más efectivos, mientras que se observó alto grado de resistencia a neomicina y eritr-
omicina. Estos resultados remarcan el reconocimiento y necesidad de cultivo bacteriano con identificación
de especies y susceptibilidad antimicrobiana para establecer el tratamiento adecuado.

Zusammenfassung Die Vielfalt der Spezies der Gattung Staphylococcus spp. und die antimikrobielle Re-
sistenz der Isolate von 151 unbehandelten Hunden beider Geschlechter mit der klinischen Diagnose einer
Otitis wurde erfasst. Einundneunzig Isolate von Staphylococcus spp. wurden mittels biochemischer Reak-
tionen identifiziert und ihre Empfänglichkeit auf 15 Antimikrobiotika getestet. Die häufigsten Spezies waren
Koagulase-positiv; S. pseudointermedius (38,4%), S. schleiferi schleiferi (15,4%), S. aureus (14,3%), S. epi-
dermidis (11%), S. simulans (11%), S. schleiferi coagulans (8,8%) und S. saprophyticus (1,1%). Alle Isolate
waren zumindest gegenüber einem Wirkstoff resistent und 89% waren multiresistent. Amoxicillin in Kom-
bination mit Clavulansäure und Oxacillin waren die effektivsten Wirkstoffe, während gegen Neomycin und
Erythromycin weitgehend eine Resistenz vorlag. Diese Ergebnisse verdeutlichen die Wichtigkeit und die
mögliche Notwendigkeit einer Bakterienkultur zur Identifizierung der Spezies, sowie von Antibiogrammen
zur passenden antimikrobiellen Therapie.

296 ª 2009 The Authors. Journal compilation ª 2009 ESVD and ACVD, Veterinary Dermatology, 21, 292–296.