Eur J Clin Microbiol Infect Dis (2000) 19 : 112–117 Q Springer-Verlag 2000

Article

Antibiotic Susceptibility of Bacterial Strains Isolated from

Patients with Community-Acquired Urinary Tract
Infections in France

F.W. Goldstein, the Multicentre Study Group

Abstract The aim of this study was to determine the distribution and antibiotic
susceptibility patterns of bacterial strains isolated from adults with community-
acquired urinary tract infections (UTI) in France. From December 1996 to March
1997, each of 15 private laboratories in France consecutively collected about 80 non-
duplicate strains isolated from adult outpatients with UTI, including patients
receiving care at home, and tested their susceptibility by the disk diffusion test. A
total of 1160 strains were collected: 1031 gram-negative bacilli, including Escherichia
coli (np865), Proteus mirabilis (np68) and Klebsiella spp. (np40), and 129 gram-
positive cocci, including Staphylococcus aureus (np16), other staphylococci (np25),
group B streptococci (np25) and enterococci (np63). In the case of 430 bacterial
isolates, the patients had either been hospitalised in the last 6 months or received
antibiotic treatment in the last 3 months. The antibiotic susceptibility rates for
Escherichia coli were: amoxicillin (58.7%), amoxicillin-clavulanic acid (63.3%), ticar-
cillin (61.4%), cephalothin (66.8%) cefuroxime (77.6%), cefixime (83.6%), cefo-
taxime (99.8%), ceftazidime (99%), nalidixic acid (91.9%), norfloxacin (96.6%),
ofloxacin (96.3%), ciprofloxacin (98.3%), cotrimoxazole (78.2%), fosfomycin
(99.1%) and gentamicin (98.4%). Of the Enterobacteriaceae, five strains produced an
extended-spectrum beta-lactamase. Methicillin resistance was detected in nine
Staphylococcus aureus isolates. The most important findings were two extended-
spectrum, beta-lactamase-producing and three methicillin-resistant Staphylococcus
aureus strains isolated from patients who had not been hospitalised in the last 6
months or taken antibiotics in the last 3 months. The findings indicate that these
strains can spread within the community; therefore, monitoring antibiotic suscepti-
bility of bacteria isolated in the community appears to be mandatory.

Introduction France. However, in most of these studies the bacterial

Recently, several study groups have reported on the
antibiotic susceptibility rates for Enterobacteriaceae or
bacteria isolated from urinary tract infections (UTI) in
F.W. Goldstein
Laboratoire de Microbiologie, Hôpital Saint-Joseph,
185 rue Raymond Losserand, 75674 Paris Cedex 14, France
The Multicentre Study Group: J. Gojon (Annecy),
P. Braquemart (Caen), JL. Mounard (Chamalières), L. Martin
(Le Mans), JC. Herbaut (Lille), Y Ph. Germain (Nancy),
P. Diesnis (Nice), V. Napoly (Paris), R. Mesnard (Rennes),
S. Grelat and Y. Loubat (Saint Vallier), T. Porcher (Saintes),
M. Shuh (Strasbourg), M.P. Goubert (Toulouse), P. Laudat
(Tours), and Ph. Corteel (Versailles)
isolates were recovered in hospitals [1–6], the suscepti-
bility of community-acquired isolates being docu-
mented in only a few studies [7–10].
Bacteria causing community-acquired infections have
developed resistance to many antimicrobial agents,
highlighting the need for regular surveys of bacterial
resistance in the community [8, 9]. The aim of this study
was thus to determine the distribution and suscepti-
bility pattern of bacteria isolated in 15 private laborato-
ries from adult outpatients with urinary tract infections
in France over a 4-month period, and to establish the
effects of previous antibiotic use or hospitalisation on
rates of bacterial resistance.
 113

Materials and Methods
Collection of Bacterial Strains. A total of 1160 non-duplicate
gram-negative and gram-positive bacteria (about 80 isolates per
centre) isolated from patients with urinary tract infections in the
period from December 1996 to March 1997 in the 15 participating
centres were collected for the study. A colony count of 610 5 cfu/
ml in the presence of 610 4 leukocytes/ml was considered signifi-
cant. Only strains isolated from outpatients, including patients
receiving care at home, were used in the study, strains isolated
from patients in private care centres or nursing homes being
excluded.
Susceptibility Testing. All centres performed disk diffusion
susceptibility testing as follows: Enterobacteriaceae were tested on
Mueller-Hinton agar at 37 7C against amoxicillin, amoxicillin-
clavulanic acid, ticarcillin, cephalothin, cefuroxime, cefixime,
cefotaxime, ceftazidime, nalidixic acid, norfloxacin, ofloxacin,
ciprofloxacin, cotrimoxazole, fosfomycin and gentamicin.
Extended-spectrum beta-lactamases (ESBL) in gram-negative
bacilli were detected by the double-diffusion method, which
revealed a synergistic effect between amoxicillin-clavulanic acid
and either cefotaxime or ceftazidime.
Three strains were used as controls: Escherichia coli ATCC 25922
(wild strain), Escherichia coli RM3346 (cephalosporinase
producer) and Klebsiella pneumoniae CF-104 (TEM-3 producer)
and subjected to susceptibility testing once every 2 weeks.
All cefotaxime-resistant bacteria, ESBL producers, oxacillin-
resistant staphylococci and amoxicillin-resistant streptococci were
sent by participant laboratories to St. Joseph Hospital, Paris, for
confirmation of test results, likewise about 10% of the susceptible
gram-negative bacilli and gram-positive cocci selected at
random.
All patients were asked to state their age, sex, whether they had
received any antibiotics during the previous 3 months, whether
they had been hospitalised during the previous 6 months, whether
they had received care at home and whether they had had an
indwelling urinary catheter.
Statistical Analysis. A two-tailed Fisher’s exact test was used to
compare susceptibility rates between groups of patients. As many
tests were performed, a P value of 0.005 was used to determine
statistical significance.

Staphylococci were tested on Mueller-Hinton agar against peni- Results

cillin G, oxacillin, amoxicillin-clavulanic acid, cephalothin and
cefotaxime at 30 7C, and against ofloxacin, cotrimoxazole, fosfo-
mycin, gentamicin and erythromycin at 37 7C. Streptococci were
tested against penicillin G, oxacillin, amoxicillin, cephalothin,
cefotaxime, fosfomycin, gentamicin (500 mg high-concentration
disk), kanamycin (1000 mg high-concentration disk) and ofloxacin
on Mueller-Hinton agar supplemented with 5% horse blood and
incubated at 37 7C in ambient air. The antibiotics tested were
available either in the community or in hospitals only (cefta-
zidime, cefotaxime). The disks and Mueller-Hinton agar plates
were obtained from Sanofi Diagnostics Pasteur (France).
Bacteria were classified as susceptible, intermediate or resistant
in accordance with the criteria of the Antibiogram Committee of
the French Society for Microbiology [11]. Isolates producing an
ESBL were never classified as susceptible to cephalosporins,
whatever the inhibition zone diameter [11].
Distribution of Clinical Isolates. A total of 1160
bacteria were collected from patients during the study
(Table 1). Patients’ ages ranged from 18 to 98 years.
More strains were isolated from patients under 65 years
of age (736; 63.4%) than from patients aged 65 years or
over (424; 36.6%). Likewise, more strains were isolated
from women (894; 77%) than from men (242; 21%); no
data was available for 31 (2%) patients. Altogether,
1120 (97%) strains were isolated from outpatients and
only 34 (3%) from outpatients receiving home care. Of
the strains, 999 (86%) were isolated from patients who
had not been hospitalised during the previous 6 months
and 800 (69%) from patients who had not received any

Table 1 Distribution of microorganisms isolated according to risk factors

Microorganism Total no. No. (%) of isolates

of isolates
Patients with Patients previously Patients without
prior exposure hospitalised risk factors
to antibiotics

Escherichia coli 865 200 (64.3) 58 (49) 588 (78.6)

Proteus mirabilis 68 27 (8.7) 9 (7.5) 39 (5.2)
Klebsiella pneumoniae 24 11 (3.5) 4 (3.4) 12 (1.6)
Klebsiella oxytoca 16 3 (1) 1 (0.8) 13 (1.7)
Citrobacter diversus 9 1 (0.3) 0 7 (0.9)
Indole-positive Proteus a 13 2 (0.7 3 (2.5) 6 (0.8)
Group 3 b 19 9 (2.8) 6 (5) 9 (1.2)
Proteus spp. 3 0 0 3 (0.4)
Non-fermentative bacilli c 14 9 (2.8) 9 (7.5) 4 (0.5)
Staphylococcus aureus 16 6 (2) 6 (5) 6 (0.8)
Other staphylococci 25 9 (2.8) 3 (2.5) 15 (2)
Streptococcus agalactiae 25 3 (1) 0 21 (3)
Group D streptococci and enterococci 63 31 (10) 20 (16.8) 25 (3.3)
Total 1160 311 (100) 119 (100) 748 (100)
a c
Proteus vulgaris, Morganella morganii and Providencia stuartii Pseudomonas aeruginosa, Pseudomonas fluorescens, Stenotro-
b
Hafnia alvei, Enterobacter cloacae, Enterobacter aerogenes, phomonas maltophilia and Acinetobacter baumannii
Enterobacter agglomerans, Citrobacter freundii, Serratia
marcescens and Serratia liquefacien
114

Table 2 Susceptibility of gram-negative bacilli to antibiotics

Organism Percent of isolates susceptible to stated antibiotic (breakpoint [11])

(no.
isolated) AMX AMC TIC CF CXM CFM CTX CAZ NAL NOR OFX CIP SXT FOS GM
(p21– (p21– (p22– (p18– (p22– (p25– (p21– (p21– (p20– (p22– (p21– (p22– (p16– (p14– (p16–
~14) ~14) ~18) ~12) ~15) ~22) ~15) ~15) ~15) ~19) ~16) ~19) ~20) ~14) ~14)

Isolates from all patients

Escheri- 58.7 63.3 61.4 66.8 77.6 83.6 99.8 99 91.9 96.6 96.3 98.3 78.2 99.1 98.4
chia coli
(865)
Proteus 72 82.3 77.9 89.7 97 100 98.5 98.5 70.6 91.1 88.2 91.1 83.8 83.6 97
mirabilis
(68)
Klebsiella 0 87.5 0 85 77.5 95 97.5 95 85 90 90 97.5 87.5 65 100
spp. (40)
Other 6.9 31 43.1 27.5 36.2 53.4 74.1 84.4 56.9 72.4 68.9 79.3 58.6 65.5 82.7
GNB (58)
All GNB 54.4 63.7 59 66.8 76.6 83.4 98.1 98 88.2 94.6 93.9 96.8 77.9 94.9 97.5
(1031)
Isolates from patients without risk factors
Escheri- 65.4 68.7 68.2 70 80.1 84.8 99.8 99.3 93.7 97.4 96.9 98.9 83.8 99.1 99.4
chia coli
(588)
Proteus 76.9 82 84.6 94.8 100 100 100 100 76.9 94.8 92.3 94.8 87.1 86.8 97.4
mirabilis
(39)
Klebsiella 8 92 0 92 84 100 100 100 92 100 100 100 92 68 100
spp. (25)
Other 13.7 51.7 44.8 41.3 48.2 68.9 86.2 93.1 72.4 86.2 82.7 89.6 75.8 65.5 96.5
GNB (29)
All GNB 61.5 69.6 65.6 71 80 85.6 99.2 99.1 91.7 96.9 96.1 98.3 83.9 95.8 99.2
(681)
Isolates from patients with at least one risk factor
Escheri- 42.4 50.6 45 58 71.8 80 99.5 98.2 86.5 93.9 93.9 96.5 65.3 99.1 95.6
chia coli
(231)
Proteus 67.8 85.7 71.4 85.7 92.8 100 96.4 96.4 64.2 89.2 85.7 89.2 78.5 78.5 96.4
mirabilis
(28)
Klebsiella 0 80 0 73.3 66.6 86.6 93.3 86.6 73.3 73.3 73.3 93.3 80 60 100
spp. (15)
Other 0 3.8 42.3 7.6 23 30.7 57.6 73 34.6 53.8 50 65.3 38.4 65.3 65.3
GNB (26)
All GNB 39 51.3 45 57 69.3 78 95.3 95.3 79.3 89 88.3 93 65 92.3 93.3
(300)

GNB, gram-negative bacilli; AMX, amoxicillin; AMC, amoxicillin- acin; CIP, ciprofloxacin; SXT, cotrimoxazole; FOS, fosfomycin; GM,
clavulanic acid; TIC, ticarcillin; CXM, cefuroxime; CFM, cefixime; gentamicin
CTX, cefotaxime; NAL, nalidixic acid; NOR, norfloxacin; OFX, oflox-

antibiotics during the previous 3 months, whereas 119
(10%) of the strains were from patients who had been
hospitalised during the previous 6 months and 311
(27%) were from patients who had received at least
one antibiotic during the previous 3 months (Table 1).
A few strains (46; 4%) were isolated from patients with
a urinary catheter. Data on any previous hospitalisation
and/or antibiotic treatment was not available for 4% of
the patients.
The antibiotics most frequently taken by the patients
during the previous 3 months were beta-lactams (32%)
and fluoroquinolones (24.3%). Penicillins and amoxi-
cillin-clavulanic acid represented 78.5% of the beta-
lactams and norfloxacin represented 60.9% of the
quinolones.
In Vitro Antibiotic Susceptibility. The antibiotic
susceptibility rates for gram-negative bacilli (GNB) are
presented in Table 2. Beta-lactams, cefotaxime and
ceftazidime were the most active agents, 98% of GNB
being susceptible to them. Cefixime and cefuroxime
were less active, 83.4% and 76.6% of strains, respec-
tively, being susceptible. The rate of resistance to
amoxicillin and amoxicillin-clavulanic acid was 45.6%
and 36.3%, respectively. Of the 1031 GNB tested,
93.9% were susceptible to ofloxacin, 96.8% to cipro-
floxacin and 88.2% to nalidixic acid. Gentamicin and
fosfomycin were also very active, 97.5% and 94.9% of
strains, respectively, being susceptible. Cotrimoxazole
was less active, 77.9% of strains being susceptible.
The rate of susceptibility of Escherichia coli to several
antibiotics decreased in isolates from patients who had
 115

been hospitalised and/or who had previously received
antibiotics (Table 2). A significant difference
(P~0.005) was observed in susceptibility to amoxicillin,
amoxicillin-clavulanic acid, ticarcillin, nalidixic acid,
cotrimoxazole and gentamicin of Escherichia coli
isolates from patients with at least one risk factor
(previous hospitalisation or prior exposure to antibio-
tics) compared with patients without these risk factors.
The susceptibility rates were similar for strains isolated
from patients over and under 65 years of age, and for
strains isolated from men and women (data not
shown).
Proteus mirabilis was more susceptible than Escherichia
coli, more than 80% of strains being susceptible to most
antibiotics. The rate of susceptibility of Klebsiella spp.
to cefotaxime and ceftazidime was 97.5% and 95%
respectively. Resistance to cefotaxime in one Klebsiella
pneumoniae isolate was due to the production of
ESBL. Over 80% of Klebsiella spp. isolates were
susceptible to quinolones. Fosfomycin was less active
than the other agents tested, only 65% of strains being
susceptible.
ESBL synthesis was detected in two Escherichia coli
isolates, one Proteus mirabilis isolate, one Klebsiella
pneumoniae isolate and one Enterobacter aerogenes
isolate. One Escherichia coli isolate and one Entero-
bacter aerogenes isolate were obtained from patients
who had not been hospitalised during the previous 6
months and who had not received antibiotics during the
previous 3 months. In the case of the other three
strains, patients had previously been hospitalised and/
or received antibiotics.
The susceptibility rates of all gram-positive cocci are
presented in Table 3. Results are not shown for
patients who had previously been hospitalised or
received antibiotics because of the low number of
isolates.
Methicillin resistance was detected in 9 of 17 Staphylo-
coccus aureus isolates. Only five of these isolates were
from patients who had previously been hospitalised. In
the case of three strains, neither hospitalisation nor
antibiotic intake was reported.
Of the 25 Streptococcus agalactiae isolates tested, 48%
were highly resistant to kanamycin according to the
criteria of the Antibiogram Committee of the French
Society for Microbiology. High-level resistance to
kanamycin was also detected in 55.5% of group D
streptococci and enterococci strains, while 17.5% of
these strains were highly resistant to gentamicin.
Discussion
This study reveals the distribution of bacterial species
isolated from patients with both complicated and
uncomplicated community-acquired urinary tract infec-
tions in France and their antibiotic susceptibility
patterns in relation to previous hospitalisation and/or
antibiotic therapy. It should be emphasised that these
data do not represent the true prevalence of commu-
nity-acquired infections but only those infections in
which the physician responsible sought the assistance of
a laboratory, as in cases of severe infection or treat-
ment failure.
Escherichia coli represented 74.6% of the strains
isolated in our study. This is consistent with the find-
ings of previous studies in which Escherichia coli was
the predominant pathogen isolated from patients with
UTI, especially in the community [10, 12]. The
frequency of Escherichia coli was lower in men (58.7%)
than in women (78.7%). When patients had recently
been hospitalised or taken antibiotics, the frequency of
Escherichia coli was also lower (48.7% and 64%,
respectively). De Mouy et al. [D. De Mouy et al., 17th
Interdisciplinary Meeting on Anti-Infectious Chemo-
therapy, Paris, 1997, Abstract 298] also found a 10-20%

Table 3 Susceptibility of gram-positive cocci to antibiotics

Organism Percent of isolates susceptible to stated antibiotic (breakpoint [11])

(no. isolated)
P AMX OXA CF AMC CTX OFX SXT FOS GM E
(p29– (p21– (p20– (p18– (p21– (p21– (p22– (p21– (p14– (p16– (p22–
~8) ~14) ~20) ~12) ~14) ~15) ~16) ~14) ~14) ~14) ~17)

S. aureus (17) 0 ND 47 47 47 47 23.5 100 70.6 88.2 50

Coagulase-negative staphylococci 36 ND 62.5 62.5 62.5 62.5 58.3 88 45.8 87.5 54.2
(24)
S. agalactiae (25) 36 100 4 100 ND 96 16 ND 88
Group D streptococci and 1.6 93.6 6.3 ND 11.1 ND 55.5
enterococci a (63)
a
Group D streptococci and enterococci: Streptococcus spp., P, penicillin; AMX, amoxicillin; AMC, amoxicillin-clavulanic
Streptococcus bovis, Enterococcus faecalis, Enterococcus. spp. acid; CF, cephalothin; CTX, cefotaxime; SXT, cotrimoxazole;
FOS, fosfomycin; GM, gentamicin; E, erythromycin; ND, not
determined
116
decrease in the frequency of Escherichia coli when
patients had one of these two risk factors.
The frequency of other species was below 6%, Proteus
mirabilis being the most common organism. Prior
hospitalisation was associated with a marked increase
in the frequency of enterococci and non-fermentative
bacilli. This is consistent with the previously reported
finding that these pathogens are more frequently
encountered in hospitals than in the community [12].
Of the antibiotics frequently used in the community,
fluoroquinolones were very active against Escherichia
coli, more than 90% of strains being susceptible. These
results are consistent with those of other community-
based studies [7, 9, 13, 15].
Amoxicillin-clavulanic acid, another antibiotic fre-
quently used in the community, was less active against
Escherichia coli, 63.3% of strains being susceptible. In
our previous community-based study [8], Escherichia
coli isolates were more susceptible to amoxicillin and
amoxicillin-clavulanic acid, the susceptibility rates
being 63.6% versus 58.7% and 89.7% versus 63.3%,
respectively. These results show there is a decrease in
susceptibility to amoxicillin-clavulanic acid. In a survey
of the susceptibility of Enterobacteriaceae to antibiotics
used in the community, Weber et al. [7] documented a
decrease in the rate of susceptibility to amoxicillin-
clavulanic acid between 1990 and 1993 from 82.4% to
68.1%. Similarly, De Mouy et al. [9] showed a signifi-
cant decrease in the rate of susceptibility to this anti-
biotic of Escherichia coli isolated from patients with
community-acquired UTI from 94% to 71% between
1990 and 1995.
The rates of susceptibility of Escherichia coli to cefo-
taxime, ceftazidime, fosfomycin and gentamicin in our
study were over 95%. These results are consistent with
those of other studies conducted in the general popula-
tion in France [5, 9, 10, 13]. We found that more than
15% of Escherichia coli were not susceptible to
cefixime. Similar findings have recently been published
by Schito et al. [14] for Escherichia coli and Proteus
mirabilis strains isolated from hospitalised patients with
UTI in Italy.
Escherichia coli strains isolated from patients who had
previously been hospitalised and/or taken antibiotics
were less susceptible to most of the antibiotics tested,
especially amoxicillin, amoxicillin-clavulanic acid, ticar-
cillin, cotrimoxazole, gentamicin and nalidixic acid; this
is consistent with the results obtained by Weber et al.
[15]. The rate of susceptibility of Escherichia coli to
cefotaxime, ceftazidime, fosfomycin and fluoroquino-
lones was the same, irrespective of whether the strains
were isolated from patients who had previously been
hospitalised and/or received antibiotics.
Proteus mirabilis appeared to be more susceptible to
penicillins (whether or not they were combined with
clavulanate) than Escherichia coli. Similar results have
been reported elsewhere [F.W. Goldstein et al.; 15th
Interdisciplinary Meeting on Anti-Infectious Chemo-
therapy, Paris, 1995, Abstract 362]. Klebsiella spp. are
rarely encountered in cases of community-acquired
UTI and exhibited good susceptibility to most antibio-
tics tested in our study except penicillins and fosfo-
mycin. However, a larger number of strains would need
to be tested to confirm these results.
Five ESBL-producing strains were isolated from among
the Enterobacteriaceae during the study. Two of these
strains were isolated in the same centre from patients
who had not been hospitalised in the last 6 months or
taken antibiotics in the last 3 months. Nine methicillin-
resistant Staphylococcus aureus (MRSA) strains were
also isolated during the study period and, surprisingly,
three of these strains were isolated from three different
patients without either of the risk factors. This is an
important finding, since it indicates that infection with
these strains, which are usually found in hospitals, is
now being acquired in the community in France.
However, we cannot exclude the possibility that some
relevant data was not reported by the respective
patients. ESBL were not found in a previous commu-
nity-based study [8].
Steinberg et al. [16] reported that MRSA caused 18.5%
of cases of community-acquired bacteraemia in the
period from 1990 to 1993 in the USA, most of these
infections occurring in patients who had recently been
hospitalised or were nursing home residents. All
patients with community-acquired MRSA bacteraemia
had regular contact with health care institutions.
However, Layton et al. [17] recently reported that 22%
of patients with community-acquired MRSA whom
they studied had no discernible risk factors, which is in
accordance with our results. These findings suggest an
increase in community acquisition of MRSA, probably
resulting from patient-to-patient transmission. Thus, in
addition to their role in nosocomial infections, ESBL
and methicillin-resistant Staphylococcus aureus are
emerging as problem pathogens in community-acquired
infection.
The results of this large multicentre study, in which
more than 1160 strains isolated in the community were
tested, show that the third-generation cephalosporins,
fluoroquinolones, fosfomycin and gentamicin still
exhibit good activity against Enterobacteriaceae, the
organisms most frequently isolated in cases of UTI.
The results also reveal that multiresistant nosocomial
strains (BLSE-producers, MRSA) are now being
encountered in the community in France. This might be
due to the fact that some patients carry resistant strains
acquired in hospital and that these strains are spread to
other individuals in the community, although it cannot

be concluded from the low number of MRSA isolated
that MRSA are now generally spreading in the commu-
nity. Thus, the need to monitor antibiotic resistance in
cases of community-acquired UTI appears to be
mandatory.
Acknowledgements This study was supported by Hoechst
Marion Roussel, Paris, France. We thank N. Moniot-Ville and C.
Dib for logistic assistance.
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