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Journal of Clinical Microbiology, April 2000, p. 1703-1705, Vol. 38, No. 4
0095-1137/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
Aerococcus urinae in Urinary Tract
Infections
Qing
Zhang,1
Christopher
Kwoh,2
Silvia
Attorri,1 and
Jill E.
Clarridge III1,3,4,*
Department of
Pathology1 and Department of
Microbiology and Immunology,3 Baylor College of
Medicine, Baylor College of
Medicine,2 and Pathology and Laboratory
Medicine Service, Veterans Affairs Medical
Center,4 Houston, Texas
Received 8 November 1999/Returned for modification 31 December
1999/Accepted 21 January 2000
 |
ABSTRACT |
Aerococcus urinae is a rarely reported pathogen,
possibly due to difficulties in the identification of the organism.
A. urinae is a gram-positive coccus that grows in pairs and
clusters, produces alpha-hemolysis on blood agar, and is negative for
catalase and pyrrolidonyl aminopeptidase. Some of these characteristics
and its being absent from the databases of most commercial
identification systems could allow A. urinae to be
misidentified as a streptococcus, enterococcus, or staphylococcus. We
report two cases of urinary tract infection (UTI) caused by A. urinae and characterize these isolates by morphology, biochemical
testing, whole-cell fatty acid analysis, 16S rRNA gene sequencing, and
antibiotic susceptibilities. Most patients infected with A. urinae are elderly males with predisposing conditions who present
initially with UTI. Because A. urinae is resistant to
sulfonamides, treatment could be inappropriate, with infections
resulting in serious complications, including death. It is important
for the clinician and the microbiologist to consider A. urinae a potential pathogen and proceed with thorough
microbiological identification.
| |
CASE REPORTS |
Case 1.
An 80-year-old
male with preexisting coronary artery disease, left-sided hemiparesis
(the residual effect of a stroke), and multiinfarct dementia was
admitted to the hospital for altered mental status. The patient
developed slowly worsening urinary symptoms, including nocturia and
frequency, over the 3 weeks prior to admission.
On admission the patient was afebrile with normal vital signs. The
physical examination was unremarkable except that a marked disorientation to place and time and a left-sided hemiparesis (the
residual effect of a previous stroke) were observed. Urinalysis showed
white blood cells (WBCs) too numerous to count, 8 red blood cells/high
power field (HPF), many bacteria, a specific gravity of 1.017, and a pH
of 5.0, with negative results for protein, ketones, and bilirubin. The
patient had a serum WBC count of 6.6 (64% neutrophils, 19%
lymphocytes, 9% monocytes, 7% eosinophils, and 1% basophils) and a
hemoglobin and a hematocrit of 10.6 g/dl and 31.5%, respectively.
Serum chemistries including electrolytes, glucose, liver, renal, and
thyroid function tests were all reported as normal. Chest X-ray was
normal except for an elevated right hemidiaphragm. Computed tomogram of
the head revealed a previous infarct in the distribution of the right
middle cerebral artery as well as hypodensity consistent with diffuse
small vessel disease. The patient was treated empirically with
intravenous ciprofloxacin for presumed urinary tract infection (UTI).
Urine cultures grew >105 CFU of Aerococcus
urinae, the only isolate, per ml. His urinary symptoms resolved
and his mental status improved by hospital day 3. The patient was
discharged, having had oral ciprofloxacin prescribed. Results of
repeated urinalysis after discharge were normal.
Case 2.
A 58-year-old white male with adequately treated
hypothyroidism presented at the Veterans Affairs Medical Center
outpatient clinic with several days of dysuria, increased urinary
frequency, and nocturia. He was afebrile at the time, with normal vital
signs and a large, tender prostate on physical exam. Urinalysis
revealed 4 to 6 WBCs/HPF, no bacteria, trace amounts of leukocyte
esterase, and negative results for nitrites, protein, ketones,
bilirubin, and blood. He was diagnosed clinically with prostatitis and
treated with tetracycline due to a history of ciprofloxacin allergy.
The patient developed a rash and discontinued the antibiotic after 2 days of treatment. He returned to the clinic 2 weeks later, still
complaining of urinary symptoms, and was febrile at 100.1°F. A second
urinalysis demonstrated 20 to 30 WBCs/HPF, 1 to 3 red blood cells/HPF,
a moderate level of leukocyte esterase, and negative urine chemistries.
The urine culture on the second urine sample later grew
>105 CFU of A. urinae, the only isolate, per
ml. The patient was lost to follow-up.
Microbiology. We compared two strains of
A. urinae from the present cases and two blood isolates of
Aerococcus viridans from our stock for growth on Trypticase
soy agar with 5% sheep
blood, with incubation at 35°C in three
different atmospheres.
At 24 h, the diameters of colonies of
A. urinae grown in ambient
air, air plus 8%
CO
2, or anaerobic conditions were 0.1, 0.5, or
0.5 mm,
respectively. At 48 h all colonies were larger, but at
24 h,
A. viridans grew to 0.7- and 1-mm diameters in air and in
air plus 8% CO
2, respectively, and showed no growth under
anaerobic
conditions.
A. viridans growth in anaerobic
conditions was barely
visible at 48 h. The colonies of both
species produce alpha-hemolytic
reactions on blood
agar.
The two
A. urinae strains are catalase negative and
pyrrolidonyl aminopeptidase (PYR) test negative. Biochemical
identification
was performed by the API 20 Strep system
(bioMeriéux, Marcy l'Etoile,
France), the Rapid CB Plus
system (Remel, Lenexa, Kans.), and
an automated identification system
(Vitek 120; bioMeriéux, Hazelwood,
Mo.) according to the
manufacturers' instructions. The results
shown in Table
1 are consistent with the results
reported by
Christensen et al. (
4). The API biotype number
(3442300) is
appropriate for
A. urinae but is not in the
code book. The Vitek
gave a unique code number (52025410000 or
50025410200) that is
also not in the code book. The whole-cell fatty
acid (CFA) analysis
was performed on isolates grown on blood agar
plates for 48 h
at 35°C in 8% CO
2 (Hewlett-Packard
HP 5890 II microbial identification
system [MIDI, Inc., Newark,
Del.]), which gave no match or called
the isolate
Streptococcus
equinus at a 0.291 similarity index.
The major CFAs were
hexadecanoic acid (16:0) (24%), octadecenoic
acid (18:1 omega 9 cis)
(21%), octadecanoic acid (18:0) (17.5%),
hexadecenoic acid (16:1
omega 9 cis) (12%). However,
A. viridans was correctly
named by all these biochemical identification systems.
The nucleotide
sequences of 16S rRNA were determined (MicroSeq
16S rRNA gene kit;
Perkin-Elmer Applied Biosystems, Foster City,
Calif.). The two isolates
were identified as
A. urinae by 16S
rRNA gene sequencing,
with a 0.2 to 0.4% difference from the type
strain.
A. urinae demonstrated a 7 to 8% difference from
A. viridans,
which indicates a genetic diversity similar to that
found among
other well-described genera and does not support Facklam
and Elliott's
assertion that these organisms, which they call
Aerococcus-like
organisms, belong in a separate genus
(
6).
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TABLE 1.
Biochemical results of the present clinical isolates
compared with the literature values for A. urinae and
A. viridans (adapted from references 1, 2, 4, 5,
6, and 7)
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|
Antibiotic susceptibility was tested by the disk diffusion method using
Mueller-Hinton blood agar, and the MICs were determined
by E-test.
National Committee for Clinical Laboratory Standards
guidelines for
Staphylococcus spp. were used for susceptibility
testing
(
11). Our strains of
A. urinae are resistant to
trimethoprim-sulfamethoxazole
and gentamicin but susceptible to
penicillin (Table
2).
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TABLE 2.
Antibiotic susceptibilities of present isolates, together
with those of A. urinae and A. viridans (adapted
from references 3, 4,
and 10)a
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|
Discussion.
There are currently three described species of the
genus Aerococcus: A. viridans, Aerococcus
christensenii, and A. urinae. A. viridans is more
commonly isolated from blood and has been associated with granulocytic
bacteremia (9) and endocarditis (12). The
recently characterized species A. christensenii
(5) has not been reported as a human pathogen. A. urinae, previously known as Aerococcus-like organism,
is an uncommon pathogen. Previous reports from European countries
indicate that it is associated with UTI (4), bacteremia
(3), sepsis (2), and potentially fatal
endocarditis (2, 7, 10, 13). The main features of our two
cases and previously reported cases are summarized in Table
3. One report described a total of 63 cases of A. urinae infection; however, little clinical
information was available (4). The single case reports are
summarized. Similar to our patients, the other patients are elderly
males with a median age of 73 and have underlying predisposing
conditions, such as prostatic diseases, diabetes mellitus, and
alcoholism. All patients had confirmed UTIs or symptoms typical of UTI.
When these patients were treated with antibiotics effective against
A. urinae, as in cases 1, 6, and 8, the infection resolved
and the patients recovered fully. On the other hand, as in cases 3, 4, 5, and 7, when A. urinae was not recognized or correct
antibiotic treatment was delayed, simple UTI progressed to systemic
infection, including endocarditis and sepsis. Thus, it is important to
consider A. urinae a potential pathogen in UTIs especially
for patients with predisposing factors who are unresponsive to
sulfonamides. If not recognized by the clinician and microbiologist,
A. urinae infection can cause serious complications.
The laboratory diagnosis of
A. urinae can be difficult. The
presumptive identification of aerobic gram-positive alpha-hemolytic
cocci and the decision on whether to more fully identify the isolates
are frequently based on Gram stain, colony appearance, and catalase
reaction. Because
A. urinae is catalase negative, it could
be
mistaken for alpha-hemolytic streptococci or enterococci that
are
more common urine isolates. At 24 h the colony morphology
resembles that of an alpha-hemolytic streptococcus or lactobacillus;
at
48 h it is similar to that of an enterococcus. The Gram stain
should be differential, as
A. urinae forms pairs, tetrads,
and
clusters. However, since
A. urinae shows smaller cocci
and fewer
tetrads than
A. viridans does, it could be
confused with pediococci
or densely packed streptococci or
enterococci.
We characterized our isolates by macroscopic and microscopic
appearance, biochemical profiles, CFA analysis, 16S rRNA gene
sequencing analysis, and antibiotic
susceptibilities.
However, according to our study and previous reports (
3,
4,
5,
6), the most important routine tests are detection
of leucine
arylamidase,
-glucuronidase, PYR, hydrolysis of hippurate
(Table
1),
and antibiotic susceptibility patterns (Table
2).
Rapid PYR testing is
useful for distinguishing between
A. viridans or enterococci
(both PYR positive) and
A. urinae (PYR negative).
A Gram
stain should be carefully examined for the characteristic
arrangement
in clusters and tetrads to rule out lactobacillus
and other
streptococcus. Pediococci are PYR negative and have
a Gram stain
morphology similar to that of
A. urinae; however,
they
differ in their resistance to vancomycin and in their positive
bile
esculin test result. Other newly described genera that are
rarely
encountered in the clinical laboratory can be differentiated
by the
characteristics listed in Table
1 (
6).
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Pathology and
Laboratory Medicine Service (113), Veterans Affairs Medical Center,
2002 Holcombe Blvd., Houston, TX 77030. Phone: (713) 794-7336. Fax: (713) 794-7657. E-mail: jillc{at}bcm.tmc.edu.
| |
REFERENCES |
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Urosepticemia and fatal endocarditis caused by Aerococcus-like organisms.
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Journal of Clinical Microbiology, April 2000, p. 1703-1705, Vol. 38, No. 4
0095-1137/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
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