CVJ / VOL 49 / OCTOBER 2008
Antimicrobial resistance and prevalence of canine uropathogens at the
Western College of Veterinary Medicine Veterinary Teaching Hospital,
Katherine R. Ball, Joseph E. Rubin, M. Chirino-Trejo, Patricia M. Dowling
Abstract — Between January 2002 and June 2007, uropathogens were isolated from 473 of 1557 canine urine
samples submitted to Prairie Diagnostic Services from the Western College of Veterinary Medicine Veterinary
Teaching Hospital. Culture and susceptibility results were analyzed, retrospectively, to estimate the prevalence of
common bacterial uropathogens in dogs with urinary tract infections and to identify changes in antimicrobial
resistance. The most common pathogens identified were Escherichia coli, Staphylococcus intermedius, Enterococcus
spp., and Proteus spp. Antimicrobial resistance increased during the study period, particularly among recurrent
E. coli isolates. Using the formula to help select rational antimicrobial therapy (FRAT), bacterial isolates were most
likely to be susceptible to gentamicin, fluoroquinolones, amoxicillin-clavulanic acid, and groups 4 and 5 (third gen-
Résumé — Résistance aux antimicrobiens et prévalence des pathogènes urinaires canins à l’hôpital
d’enseignement vétérinaire du Western College of Veterinary Medicine. Entre janvier 2002 et juin 2007, des
pathogènes urinaires ont été isolés de 473 des 1557 échantillons d’urine de chiens soumis au Prairie Diagnostic
Services du Western College of Veterinary Medicine Veterinary Teaching Hospital. Les résultats des cultures et des
susceptibilités ont été analysés rétrospectivement afin d’estimer la prévalence des bactéries uropathogènes courantes
du chien atteint d’infection du tractus urinaire et d’identifier des modifications de la résistance aux antimicrobiens.
Les pathogènes identifiés les plus courants étaient Escherichia coli, Staphylococcus intermedius, Enterococcus spp. et
Proteus spp. La résistance aux antimicrobiens a augmenté au cours de la période d’étude, particulièrement parmi
les isolats d’E. coli récurrents. Selon une formule visant à aider à choisir une thérapie antimicrobienne rationnelle
(FTAR), les isolats bactériens avaient plus de chances d’être susceptibles à la gentamycine, aux fluoroquinolones,
à l’amoxicilline-acide clavulanique et aux céphalosporines de groupes 4 et 5 (3ième génération).
(Traduit par Docteur André Blouin)
Can Vet J 2008;49:985–990
and affects approximately 14% of dogs presented for veterinary
care (1). Uropathogenic strains of Escherichia coli are the most
common cause of UTIs in both humans and dogs, and strains
of this species are often abundant in the gastrointestinal tract
at the time of infection (2,3). In contrast to most intestinal
acterial urinary tract infection (UTI) is one of the most
commonly diagnosed infectious diseases in canine practice
strains of E. coli, uropathogenic strains possess virulence fac-
tors which facilitate survival and persistence in the urinary
tract (3). The risk of UTI recurrence is increased when highly
pathogenic bacteria or underlying problems (such as, anatomic
abnormalities, neoplasia, diabetes mellitus) are present (4,5).
Microbiological culture and susceptibility testing is the corner-
stone of UTI diagnosis and the results are used by veterinarians
to select antimicrobial therapy (6). Susceptibility results from
specific populations are used to select empirical therapy and to
monitor trends in antimicrobial resistance (5,7). Antimicrobial
resistance in uropathogens complicates therapy in dogs and is
also a public health concern because these pathogens may be
The epidemiology of human uropathogens varies significantly
by region and care setting (10). Given the many other similari-
ties between human and canine UTIs, there is likely regional
and population-specific variation in the epidemiology of canine
uropathogens (8,9). The prevalence of fluoroquinolone resis-
tance in canine uropathogens is increasing in the United States,
Department of Veterinary Biomedical Sciences (Ball, Dowling),
Department of Veterinary Microbiology (Rubin, Chirino-
Trejo), Western College of Veterinary Medicine, University of
Saskatchewan, 52 Campus Drive, Saskatoon, Saskatchewan
Address all correspondence to Dr. Katherine R. Ball; e-mail:
Drs. Katherine R. Ball and Joseph E. Rubin were supported by
Interprovincial Graduate Student Fellowships.
CVJ / VOL 49 / OCTOBER 2008
but only limited information is available about antimicrobial
resistance trends in Canadian isolates (11,12).
Multi-drug resistance was observed in canine urinary isolates
from an intensive care unit at the Ontario Veterinary College
teaching hospital (13); however, the population of that study
may not be representative of the general population of dogs in
other areas, such as western Canada. The objectives of this study
were to estimate the prevalence of uropathogens in dogs with
urinary tract infections at the Western College of Veterinary
Medicine Veterinary Teaching Hospital (WCVM-VTH), to
apply the formula to help select rational antimicrobial therapy
(FRAT) developed by Blondeau and Tillotson (7), and to
identify changes in antimicrobial resistance among canine uro-
pathogens over a 5-year period,
Materials and methods
Records were obtained from Prairie Diagnostic Services (PDS)
for all canine urine samples that had been submitted by the
WCVM-VTH between January 2002 and June 2007 for culture
and susceptibility testing. During this period, urine samples were
plated on Columbia agar supplemented with 5% sheep blood
and on MacConkey agar (Becton Dickinson and Company,
Sparks, Maryland, USA) upon receipt. Each plate was divided
in half such that each sample could be applied twice (1 mL and
10 mL) for quantitative analysis. Blood agar plates were incu-
bated with 5% CO2 while MacConkey agar plates were incu-
bated aerobically. All samples were incubated at 37°C for 18 to
24 h until adequate growth was present. Identification was based
on colony type and morphology, Gram staining characteristics,
and standard biochemical tests. Antimicrobial susceptibility was
determined by the Kirby-Bauer disk diffusion method. Zones
of growth inhibition were interpreted according to Clinical and
Laboratory Standards Institute (CLSI) guidelines. Anaerobic
cultures were performed when hematuria was evident or if
requested by the attending veterinarian.
Statistical analysis was performed using a commercial statisti-
cal software package (SPSS 12.0 for Windows, SPSS, Chicago,
Illinois, USA). The mean was taken from the ages recorded
from all submissions for each dog to produce a single measure of
age. Numbers of antimicrobials to which isolates were resistant
were compared with the Kruskal-Wallis test, with alpha set to
0.05. Post-hoc analysis was performed by the Mann-Whitney
U-test with Bonferroni’s correction. Recurrent isolates were
excluded from all analyses except for recurrent E. coli isolates,
which were analyzed separately. Analyses of the number of
antimicrobials to which isolates were resistant included results
reported for amoxicillin-clavulanic acid, ampicillin, cephalo-
thin, ceftiofur, chloramphenicol, clindamycin, enrofloxacin,
gentamicin, tetracycline, and trimethoprim-sulfamethoxazole.
Change in resistance to individual antimicrobial drugs over
time was evaluated using simple logistic regression with year as
a continuous variable. The relationship between sex, age, and
resistance to individual antimicrobial drugs was evaluated by
logistic regression with backward stepwise variable entry and
evaluation by likelihood ratio. The same approach was used to
examine the relationship between sex, age, and mixed infections
(defined as more than 1 species isolated from 1 urine sample)
and the relationship between sex, age, resistance, and recurrent
The impact factors for individual antimicrobial drugs were
calculated using susceptibility data for E. coli, Enterococcus
spp., Staphylococcus intermedius, Streptococcus canis, Proteus
spp., Staphylococcus spp., Streptococcus spp., Enterobacter spp.,
Pseudomonas spp., and Klebsiella pneumoniae isolates and the
formula to help select rational antimicrobial therapy (FRAT,
Equation 1) (7).
FS = S PPathogen (i) 3 SAntimicrobial 3 100
The impact factor is FS, PPathogen (i) is the prevalence of pathogen
i, and SAntimicrobial is the proportion of pathogen i isolates suscep-
tible to the antimicrobial in question. Anaerobes, fungal species,
and bacterial isolates of minor species (prevalence , 3.1%) were
excluded from this consideration, as susceptibility data were
available for only a small proportion of these isolates. To allow
comparison of impact factors between years, prevalence values
used in the equation were calculated after exclusion of fungal
species and minor bacterial isolates.
Between January 2002 and June 2007, 1557 urine samples
from 1149 dogs were submitted to PDS by the WCVM-VTH
Table 1. Isolates from canine urine samples submitted by
WCVM-VTH for culture and susceptibility testing, 2002–2007
a Minor species included Acinetobacter spp., Bacillus spp., Bacteroides spp.,
Citrobacter spp., Clostridium spp., Corynebacterium spp., Lactobacillus spp.,
Morganella morganii, and Pasteurella multocida
Table 2. Bacteria isolated from dogs with recurrent urinary tract
Species Percent of recurrent infections (n)
n — number of dogs
CVJ / VOL 49 / OCTOBER 2008
for culture and susceptibility testing. Of these samples, 1 to 14
were submitted from each dog, with a median of 1 submission
per dog. The mean age of the dogs ranged from 2 mo to 18.7 y,
with a median of 8 y; age was not reported for 1.13% of the
dogs. Urine samples were submitted from 492 spayed females
(42.8%), 157 intact females (13.7%), 347 castrated males
(30.2%), and 153 intact males (13.3%).
A positive bacterial culture was obtained from 473 samples
from 361 dogs. Of these samples, 4 (0.85%) yielded 3 different
bacterial species, 39 samples (8.25%) yielded 2 species, and the
remainder yielded a single bacterial species. The prevalence of
bacterial species differed between mixed infections and cases
where the pathogen was isolated in pure culture (Table 1). There
was no significant association between mixed infections, age,
and sex. One hundred and twelve isolates were from cases where
the same bacterial species was cultured on more than 1 occasion
(referred to as recurrent pathogens). Escherichia coli was the
most common recurrent pathogen, followed by S. intermedius,
Enterococcus spp., and Proteus spp. (Table 2). Escherichia coli
was isolated more than once from 17.3% of all cases where it
had ever been isolated. This recurrence rate was higher than
the rates observed for S. intermedius (10.5%), Enterococcus spp.
(6.7%), and Proteus spp. (10.7%). There was no significant
association between recurrent infection by E. coli, S. intermedius,
Enterococcus spp., or Proteus spp. and age or sex.
The number of antimicrobials to which recurrent E. coli
isolates were resistant increased significantly during the study
period (P = 0.010), specifically between 2003 and 2007
(P , 0.001). There was no significant change in the number of
antimicrobials to which nonrecurrent E. coli, Enterococcus spp.,
S. intermedius, and Proteus spp. isolates were resistant (Table 3).
Gentamicin, enrofloxacin (indicator for veterinary fluoroquino-
lones), amoxicillin-clavulanic acid, and ceftiofur (indicator for
groups 4 and 5 cephalosporins, also classified as 3rd generation)
had the highest cumulative antimicrobial impact factors, reflect-
ing the high frequency of in vitro susceptibility to these drugs
among the bacterial isolates (Table 4). Antimicrobial impact
factors decreased for all antimicrobials between 2002 and 2007
except for tetracycline and trimethoprim-sulfamethoxazole, in
which the impact factors increased (Table 4).
Of the 267 E. coli isolates, 73 (27.3 %) were from dogs
with recurrent E. coli infections (defined here as more than
one positive E. coli culture result during the study period).
Recurrence among E. coli was associated with resistance to
increasing numbers of antimicrobials [odds ratio (OR) 1.22,
95% confidence interval (CI) 1.03–1.45]. There was no sig-
nificant association of recurrence and antimicrobial resistance
for S. intermedius, Enterococcus spp., and Proteus spp. There was
no significant effect of sex on the number of antimicrobials to
which nonrecurrent E. coli, S. intermedius, Enterococcus spp., and
Proteus spp. isolates were resistant. Resistance to cephalothin,
indicating resistance to group 1 and group 2 (first generation)
cephalosporins, increased among nonrecurrent Enterococcus
spp. (Table 5). Among S. intermedius, resistance to ampicillin
increased over the study period (Table 5). Resistance to cepha-
lothin, chloramphenicol, and gentamicin increased among
recurrent E. coli isolates (Table 5). Resistance to cephalothin
decreased among nonrecurrent E. coli (Table 5). There was no
significant increase in resistance to any individual antimicrobial
drug among Proteus spp. isolates. Recurrent E. coli isolates were
more likely to be resistant to chloramphenicol (OR = 6.65;
95% CI = 1.96–22.54) and gentamicin (OR = 4.59; 95%
CI = 1.05–20.07) than isolates from dogs with a single E. coli
isolate. Escherichia coli isolates that were resistant to gentamicin
were resistant to between 5 and 10 antimicrobials, and those that
were resistant to trimethoprim-sulfamethoxazole were resistant
to between 3 and 10 antimicrobials. Chloramphenicol-resistant
E. coli were resistant to between 3 and 10 antimicrobials.
Escherichia coli, Staphylococcus spp., Proteus spp., Klebsiella spp.,
and Enterococcus spp., have been reported as the most com-
mon canine uropathogens, composing 44.1%, 11.6%, 9.3%,
9.1%, and 8.0% of microbial isolates, respectively (14). Other
Table 3. Mean (standard error) number of antimicrobials to which bacterial isolates from canine urine
samples were resistant, by year
Species 2002 2003 2004 2005 2006 2007
All E. coli
E. coli (recurrent)a
E. coli (single positive culture) 1.36 (0.17) 1.50 (0.24) 1.67 (0.26) 1.73 (0.26) 1.36 (0.17) 1.05 (0.08)
S. intermedius 1.00 (0.32) 0.95 (0.27) 0.88 (0.45) 0.64 (0.15) 1.00 (0.22) 1.20 (0.49)
Enterococcus spp. 2.17 (0.48) 3.14 (0.99) 5.29 (0.97) 2.86 (0.59) 3.41 (0.45) 5.43 (0.30)
Proteus spp. 3.20 (0.20) 3.00 (0.82) 3.33 (0.33) 3.75 (0.48) 3.55 (0.43) 4.25 (1.25)
1.68 (0.20) 1.49 (0.16) 2.12 (0.23) 1.74 (0.18) 2.04 (0.18) 2.74 (0.35)
1.45 (0.18) 1.37 (0.16) 1.67 (0.21) 1.74 (0.24) 1.55 (0.20) 2.09 (0.43)
1.71 (0.56) 1.15 (0.15) 1.64 (0.36) 1.83 (0.65) 2.08 (0.61) 4.00 (1.01)
a Denotes significant change in resistance during the study period (P , 0.05) based on analysis by Kruskal-Wallis test
Table 4. Antimicrobial impact factors calculated using FRAT for
the 10 most prevalent bacterial species isolated from canine urine
samples submitted from the WCVM-VTH
a Includes prevalence and resistance data from all years (2002–2007)
CVJ / VOL 49 / OCTOBER 2008
studies have had similar results for E. coli and Staphylococcus
spp. prevalence, but for Proteus spp. the prevalence fluctuates
between 18% and 35.2% (15–18). The differences in prevalence
between our study and previous reports are likely attributable to
the WCVM-VTH being a predominantly primary care hospital.
Compared to referral cases, primary care cases are less likely to
have been treated on multiple occasions, producing different
selection pressures for uropathogens. A primary care caseload
likely includes a smaller proportion of cases with secondary
UTIs such as catheter-associated infections compared with a
referral caseload. The nature of the caseload may also partially
account for the lower frequency of mixed infections in our study
compared with previous reports (14). Additionally, geographical
factors may contribute to the differences in the prevalence of
bacterial uropathogens (10). Unlike findings in a previous study
where mixed infections were more common in females, there was
no significant association between sex and prevalence of mixed
infections in our study population (14).
Isolation of the same bacterial species on more than 1 occa-
sion can result from re-infection (2 infections separated by a
period where the pathogen is eradicated from the urinary tract)
or persistent infection (where the pathogen is not eradicated).
Although these processes were indistinguishable from each other
in this study, E. coli is over-represented in cases where multiple
positive cultures revealed the same organism. Genetic analysis
would allow distinction to be made between persistence and
Uropathogenic E. coli possess multiple adaptations for survival
and persistence in the urinary tract. These adaptations facilitate
their invasion into transitional epithelial cells, where they can
either enter a latent state within membrane-bound vesicles or
reproduce and establish biofilm-like intracellular bacterial com-
munities free within the cytoplasm (19,20). Bacteria later emerge
from the intracellular communities and, by assuming a filamen-
tous form, can bridge between epithelial cells without entering
the urine (21,22). Some of the intracellular bacteria also emerge
from the epithelial cells into the urine (21,22). The normal
host defense of exfoliating infected epithelial cells disseminates
E. coli in the environment and exposes deeper layers of tissue for
invasion by bacteria in the urine (23). Neutrophil recruitment
disrupts the integrity of the epithelium, which may also con-
tribute to deeper penetration of the infection (23). While these
mechanisms for survival in the urinary tract have been studied
extensively in mouse models of human disease, their role in
canine E. coli UTIs remains unclear. However, there is remark-
able genetic similarity between uropathogenic E. coli isolated
from humans and dogs (3). Because uropathogenic E. coli can
survive and multiply within epithelial cells, urine samples can
produce negative culture results despite ongoing infection, and
infection can persist despite the presence of bactericidal con-
centrations of antimicrobial drugs in urine (21,24). Therefore,
therapeutic efficacy likely depends on achieving appropriate
antimicrobial concentrations within the uroepithelium.
With the exception of decreased resistance to group 1 and
group 2 (first generation) cephalosporins among nonrecurrent
E. coli, antimicrobial resistance increased over the study period.
While fluoroquinolone resistance increased among E. coli isolates
Table 5. Odds ratios (95% confidence intervals) for increasing resistance to individual antimicrobials by year
E. coli (nonrecurrent)
E. coli (recurrent)
Recurrent isolates were excluded from analysis except where stated
NR — cases where too few resistant organisms were observed to allow analysis (, 1/y)
R — cases where too few nonresistant organisms were observed to allow analysis (, 1/y)
a A statistically significant change in resistance with year modeled as a continuous variable
CVJ / VOL 49 / OCTOBER 2008
in a previous study, no change was observed in the present study
(based on resistance to enrofloxacin) (12). Gentamicin and
chloramphenicol are not commonly used to treat bacterial
UTIs in dogs so the increased resistance of recurrent E. coli
to these antimicrobials is likely attributable to co-selection, as
these isolates were resistant to multiple antimicrobials (data
not shown). Co-selection for antimicrobial resistance may be
facilitated by the presence of class 1 integrons. These genetic
elements facilitate the uptake and maintenance of gene cas-
settes coding for antimicrobial resistance (25,26). Co-selection
of antimicrobial resistance occurs when multiple gene cassettes
are included in the integron, such that exposure to any drug to
which the bacterium is resistant selects for all resistance genes
present (25). Class 1 integrons containing chloramphenicol and
gentamicin resistance genes have been reported in uropathogenic
and other E. coli strains isolated from humans and animals
(27–30). Further study is needed to determine the role of class
1 integrons in disseminating antimicrobial resistance in canine
uropathogenic E. coli isolates.
Laboratory culture and susceptibility results are often used
for monitoring antimicrobial resistance, but there is inherent
bias to this approach (31). Samples tend to be submitted from
animals with more severe clinical signs. In some cases, urine
may not be submitted for culture and susceptibility testing
until initial antimicrobial therapy (based on urinalysis results
and Gram staining) has failed. This case selection bias may over-
estimate antimicrobial resistance. However, case selection bias
is counterbalanced by the limited sensitivity of disk diffusion
testing to changes in resistance. Because the results are reported
as categorical data, changes are observed at only one breakpoint
representing the transition between “intermediate” and “resis-
tant” (permitting classification as “not resistant” and “resistant”).
Consequently, shifts in minimum inhibitory concentrations are
not apparent unless they occur around the breakpoint.
Prudent use of antimicrobials is an important step in reduc-
ing the emergence of antimicrobial resistance. In the context
of canine UTIs, prudent use includes considering likely patho-
gens and their susceptibility patterns when choosing empirical
treatment. Antimicrobial impact factors calculated using FRAT
reflect the probability that a pathogen randomly selected from
the study population is susceptible to a particular antimicrobial
on disk diffusion testing. Based on these factors, canine UTIs
are likely to be susceptible to a number of antimicrobials.
However, the antimicrobial impact factors should not be used
alone to select empirical therapy. The impact factors are based
on in vitro susceptibility data, which does not necessarily reflect
clinical efficacy for antimicrobials that achieve substantially
higher concentrations in urine than what is evaluated in vitro
or in cases involving intracellular infection. In the present study,
gentamicin, enrofloxacin and amoxicillin-clavulanic acid had
cumulative impact factors between 90 and 94. Small differences
in impact factors are likely of little clinical significance, so other
factors including pharmacokinetics, antimicrobial use strategies
to reduce the emergence of resistance, drug safety profile, cost
and convenience of administration must be considered when
choosing empirical therapy. However, impact factors decreased
between 2002 and 2007 for all antimicrobials except tetracycline
and trimethoprim-sulfamethoxazole, consistent with increasing
prevalence of antimicrobial resistance. Culture and susceptibility
testing for individual cases remains the best instrument for guid-
ing treatment decisions, especially for recurrent infections.
Increasing antimicrobial resistance is a growing concern in
both human and veterinary medicine. Because pathogens iso-
lated from recurrent infections are more resistant and resistance
is increasing over time, appropriate management of recur-
rent infections is critical to control antimicrobial resistance.
Underlying anatomic or metabolic problems should be identified
and addressed whenever possible. Novel treatment strategies
should address the virulence mechanisms of uropathogenic
E. coli which facilitate persistent infection.
Dr. Ball conducted the literature review, performed the statistical
analysis, and wrote the initial manuscript. Dr. Rubin assisted in
writing the Materials and Methods section and contributed to
the Discussion. Dr. Dowling provided the initial ideas for this
project and assisted with interpretation of results, and assisted
with manuscript editing. Dr. Chirino-Trejo assised with inter-
pretation of results.
The authors thank Brian Chelack and Prairie Diagnostic Services
for providing culture and susceptibility data.
1. Ling GV. Therapeutic strategies involving antimicrobial treatment of
the canine urinary tract. J Am Vet Med Assoc 1984;185:1162–1164.
2. Low DA, Braaten BA, Ling GV, Johnson DL, Ruby AL. Isolation and
comparison of Escherichia coli strains from canine and human patients
with urinary tract infections. Infect Immun 1988;56:2601–2609.
3. Johnson JR, Kaster N, Kuskowski MA, Ling GV. Identification of uro-
virulence traits in Escherichia coli by comparison of urinary and rectal
E. coli isolates from dogs with urinary tract infection. J Clin Microbiol
4. Drazenovich N, Ling GV, Foley J. Molecular investigation of Escherichia
coli strains associated with apparently persistent urinary tract infection
in dogs. J Vet Intern Med 2004;18:301–306.
5. Seguin MA, Vaden SL, Altier C, Stone E, Levine JF. Persistent urinary
tract infections and reinfections in 100 dogs (1989–1999). J Vet Intern
6. Bartges JW. Diagnosis of urinary tract infections. Vet Clin North Am
Small Anim Pract 2004;34:923–933.
7. Blondeau JM, Tillotson GS. Formula to help select rational antimicrobial
therapy (FRAT): Its application to community- and hospital-acquired
urinary tract infections. Int J Antimicrob Agents 1999;12:145–150.
8. Johnson JR, Clabots C. Sharing of virulent Escherichia coli clones among
household members of a woman with acute cystitis. Clin Infect Dis
2006;43:E101–E108. Epub 2006 Oct 10.
9. Kurazono H, Nakano M, Yamamoto S, et al. Distribution of the usp
gene in uropathogenic Escherichia coli isolated from companion animals
and correlation with serotypes and size-variations of the pathogenicity
island. Microbiol Immunol 2003;47:797–802.
10. Zhanel GG, Hisanaga TL, Laing NM, et al. Antibiotic resistance in out-
patient urinary isolates: Final results from the North American Urinary
Tract Infection Collaborative Alliance (NAUTICA). Int J Antimicrob
11. Cooke CL, Singer RS, Jang SS, Hirsh DC. Enrofloxacin resistance in
Escherichia coli isolated from dogs with urinary tract infections. J Am
Vet Med Assoc 2002;220:190–192.
12. Cohn LA, Gary AT, Fales WH, Madsen RW. Trends in fluoroquinolone
resistance of bacteria isolated from canine urinary tracts. J Vet Diagn
13. Ogeer-Gyles J, Mathews K, Weese JS, Prescott JF, Boerlin P. Evaluation
of catheter-associated urinary tract infections and multi-drug-resistant
990 Download full-text
CVJ / VOL 49 / OCTOBER 2008
Escherichia coli isolates from the urine of dogs with indwelling urinary
catheters. J Am Vet Med Assoc 2006;229:1584–1590.
14. Ling GV, Norris CR, Franti CE, et al. Interrelations of organism preva-
lence, specimen collection method, and host age, sex, and breed among
8,354 canine urinary tract infections (1969–1995). J Vet Intern Med
15. Féria CP, Correia JD, Machado J, Vidal R, Gonçalves J. Urinary tract
infection in dogs. Analysis of 419 urocultures carried out in Portugal.
Adv Exp Med Biol 2000;485:301–304.
16. Bush BM. A review of the aetiology and consequences of urinary tract
infections in the dog. Br Vet J 1976;132:632–641.
17. Wooley RE, Blue JL. Quantitative and bacteriological studies of urine
specimens from canine and feline urinary tract infections. J Clin
18. Wierup M. Bacteriological examination of urine specimens from non-
catheterized and catheterized dogs with symptoms of urinary tract
infection. Nord Vet Med 1978;30:318–323.
19. Kau AL, Hunstad DA, Hultgren SJ. Interaction of uropathogenic
Escherichia coli with host uroepithelium. Curr Opin Microbiol
20. Garofalo CK, Hooton TM, Martin SM, et al. Escherichia coli from
urine of female patients with urinary tract infections is competent for
intra cellular bacterial community formation. Infect Immun 2007;75:
21. Mulvey MA, Schilling JD, Hultgren SJ. Establishment of a persistent
Escherichia coli reservoir during the acute phase of a bladder infection.
Infect Immun 2001;69:4572–4579.
22. Justice SS, Hung C, Theriot JA, et al. Differentiation and developmental
pathways of uropathogenic Escherichia coli in urinary tract pathogenesis.
Proc Natl Acad Sci U S A 2004;101:1333–1338.
23. Bower JM, Eto DS, Mulvey MA. Covert operations of uropathogenic
Escherichia coli within the urinary tract. Traffic 2005;6:18–31.
24. Schilling JD, Lorenz RG, Hultgren SJ. Effect of trimethoprim-
sulfamethoxazole on recurrent bacteriuria and bacterial persistence
in mice infected with uropathogenic Escherichia coli. Infect Immun
25. Ploy MC, Lambert T, Couty JP, Denis F. Integrons: An antibiotic
resistance gene capture and expression system. Clin Chem Lab Med
26. Solberg OD, Ajiboye RM, Riley LW. Origin of class 1 and 2 integrons
and gene cassettes in a population-based sample of uropathogenic
Escherichia coli. J Clin Microbiol 2006;44:1347–1351.
27. Cocchi S, Grasselli E, Gutacker M, Benagli C, Convert M, Piffaretti JC.
Distribution and characterization of integrons in Escherichia coli strains
of animal and human origin. Fems Immunol Med Microbiol 2007;50:
28. Martinez-Freijo P, Fluit AC, Schmitz FJ, Grek VSC, Verhoef J, Jones ME.
Class I integrons in Gram-negative isolates from different European hos-
pitals and association with decreased susceptibility to multiple antibiotic
compounds. J Antimicrob Chemothe 1998;42:689–696.
29. Kim TE, Jeong YW, Cho SH, Kim SJ, Kwon HJ. Chronological study of
antibiotic resistances and their relevant genes in Korean avian pathogenic
Escherichia coli isolates. J Clin Microbiol 2007;45:3309–3315.
30. Du XD, Shen ZQ, Wu BB, Xia SC, Shen JZ. Characterization of
class 1 integrons-mediated antibiotic resistance among calf pathogenic
Escherichia coli. FEMS Microbiol Lett 2005;245:295–298.
31. Hillier S, Bell J, Heginbothom M, et al. When do general practitioners
request urine specimens for microbiology analysis? The applicability
of antibiotic resistance surveillance based on routinely collected data.
J Antimicrob Chemother 2006;58:1303–1306.