1. health and fitness
2. disease

Prostatic Diseases and Male Voiding
Dysfunction
Incidence of Acute Prostatitis
Caused by Extended-spectrum
␤-Lactamase-producing Escherichia
coli After Transrectal Prostate Biopsy
Ender Özden, Yakup Bostanci, Kamil Y. Yakupoglu, Ekrem Akdeniz, Ali F. Yılmaz,
Necla Tulek, and Saban Sarıkaya
OBJECTIVES
METHODS
RESULTS
CONCLUSIONS
To study the clinical and bacteriologic picture of acute prostatitis caused by extendedspectrum ␤-lactamase (ESBL)-producing Escherichia coli after transrectal ultrasound-guided
prostate biopsy.
The retrospective data from 1339 patients who had undergone transrectal ultrasound-guided
biopsy from November 2003 to June 2008 were reviewed. An automatic biopsy gun with an
18-gauge needle was used to obtain 10-core biopsies for first biopsies and ⱖ12-core for repeat
biopsies. These patients had received 500 mg ciprofloxacin orally twice daily for 5 days,
beginning 24 hours before biopsy. All biopsies were performed as outpatient procedures.
Of the 1339 patients, 28 (2.1%) had acute bacterial prostatitis detected after transrectal
ultrasound-guided prostate biopsy. Acute prostatitis occurred after the first biopsy in 15 patients
(1.3%) and after repeat biopsy in 13 (6.8%). The patients had developed infective symptoms a
mean of 3 days after transrectal ultrasound-guided prostate biopsy. Of the 28 patients, 17 (61%)
had positive urine and/or blood cultures, including E. coli in 14. Of the 14 patients, 6 had acute
prostatitis caused by ESBL-producing E. coli. Bacteria isolated from urine were tested for drug
susceptibility to a wide range of antibiotics. All patients with ESBL-producing E. coli were
treated with imipenem. The bacteria detected in these urine cultures were resistant to ciprofloxacin, ceftriaxone, sulbactam/ampicillin, and cefazolin. Imipenem and piperacillin-tazobactam
were the most active agents against ESBL-producing E. coli. ESBL-producing isolates had a
significant reduction in activity for most antimicrobial agents, including fluoroquinolones and
amikacin.
The prompt initiation of effective antimicrobial treatment is essential in patients with ESBLproducing E. coli, and empirical decisions must be determined by knowledge of the local
distribution of pathogens and their susceptibility. UROLOGY 74: 119 –124, 2009. © 2009 Elsevier Inc.
T
ransrectal ultrasound (TRUS)-guided needle biopsy of the prostate is generally accepted as the
standard procedure to diagnose prostate cancer.
The risks and complications of TRUS-guided biopsy are
well documented. Some of these complications are minor, such as hematuria and hemospermia, but some complications are clinically significant, including urinary
tract infection and sepsis. The most serious complication
From the Departments of Urology and Department of Infectious Disease, Ondokuz
Mayıs University Faculty of Medicine, Samsun, Turkey
Reprint requests: Ender Özden, M.D., Department of Urology, Ondokuz Mayıs
University Faculty of Medicine, 55200 Kurupelit, Samsun, Turkey. E-mail:
[email protected]
Submitted: November 15, 2008, accepted (with revisions): December 15, 2008
© 2009 Elsevier Inc.
All Rights Reserved
of TRUS-guided biopsy is bacterial sepsis. After biopsy,
the reported incidence of bacteremia is 16%-73% and
bacteriuria is 36%-44%. Most often, the bacteria diagnosed in either the urine or blood are Escherichia coli.1,2
Antibiotic prophylaxis with various drug protocols before
biopsy has generally been accepted to reduce the infection-related complications. Several studies have shown
that fluoroquinolone derivatives are effective in lowering
the incidence of infectious complications.3-5 However,
some studies have reported patients developing fluoroquinolone-resistant infections after prostate biopsy.6,7
Because fluoroquinolones have a broad spectrum, the
increase in the use of these drugs has led to resistance.
One of the mechanisms of resistance is the activity of
extended-spectrum ␤-lactamases.
0090-4295/09/$34.00
doi:10.1016/j.urology.2008.12.067
119
ESBLs are enzymes that mediate resistance to extendedspectrum (third-generation) cephalosporins (eg, ceftazidime, cefotaxime, and ceftriaxone) and monobactams
(eg, aztreonam) but do not affect carbapenems (eg, meropenem, imipenem, and ertapenem). E. coli and Klebsiella
pneumoniae are potentially ESBL-producing microorganisms. ESBLs are often plasmid mediated.8
The presence of an ESBL-producing organism in severe infections can result in treatment failure if one of
these classes of drugs is used, even in cases in which the
minimal inhibitory concentration of the cephalosporin
chosen for treatment is in the susceptible range.9 We
studied the clinical picture of acute prostatitis caused by
ESBL-producing E. coli after transrectal prostate biopsy,
evaluated the urine and blood culture results, and reviewed the treatment protocol for acute prostatitis.
Table 1. Patient characteristics
Characteristic
Total
First Biopsy
Repeat
Biopsy
Patients (n)
1339
1149 (85.8) 190 (14.2)
Mean age (y)
65 ⫾ 8.4 65.3 ⫾ 8.5 62.7 ⫾ 7.2
Median PSA
9.7
9.6
10.7
(ng/mL)
Prostatitis
Patients (n)*
28 (2.1)
15 (1.3)
13 (6.8)
Mean age (y) 60.4 ⫾ 10.4 62.4 ⫾ 11 58.1 ⫾ 9.5
Median PSA
5.9
6.1
8.4
(ng/mL)
Interval since
biopsy (d)
Mean
3.1
3.6
2.6
Range
1-7
1-7
1-5
PSA, prostate-specific antigen.
Data in parentheses are percentages.
* Significant difference (P ⬍ .05), ␹2 test was used for statistical
analysis.
MATERIAL AND METHODS
A retrospective evaluation was performed of the records of all
patients who had undergone TRUS-guided biopsy at Ondokuz
Mayis University Hospital from November 2003 to June 2008.
A total of 1339 patients underwent TRUS-guided biopsy. The
indications for biopsy were generally prostate-specific antigen
elevation and/or abnormal digital rectal examination findings.
All prostate biopsies were performed transrectally under ultrasound guidance. An automatic biopsy gun with an 18-gauge
needle was used to obtain 10-core biopsies for the first biopsies
and ⱖ12 cores for repeat biopsies. None of the patients had
received an enema or parenteral injections of an antibiotic
before biopsy. These patients received 500 mg ciprofloxacin
orally twice daily for 5 days, beginning 24 hours before biopsy.
All biopsies were performed as outpatient procedures.
The data of all patients with acute prostatitis occurring
within 7 days after biopsy were reviewed. The clinical diagnosis
of acute prostatitis was determined by a body temperature
⬎38°C, leukocytes in the urine sediment, and clinical findings
on digital rectal examination. Before initiating the antibiotic
treatment, samples of urine for aerobic and blood for both
aerobic and anaerobic cultures were obtained for bacterial evaluation. All organisms isolated from urine or blood cultures were
tested for antibiotic susceptibility. The minimal inhibitory concentration was measured by the broth microdilution method,
using the Clinical and Laboratory Standards Institute criteria,
and drug susceptibility was determined according to the breakpoint minimal inhibitory concentration established by the
Clinical and Laboratory Standards Institute.
Statistical analysis was performed using the ␹2 test and Fisher’s
exact test. P ⬍ .05 was considered significant.
RESULTS
From November 2003 to June 2008, 1587 biopsy procedures performed in 1339 patients. Of the 1339 patients,
1149 underwent a first biopsy and 190 underwent repeat
biopsies. Tables 1 and 2 list the patient demographics,
clinical manifestations of the infective complications,
and bacteria types. Clinically, none of the patients were
suspected of having a urinary tract infection or acute
prostatitis before biopsy. Of the 1339 patients, 28 (2.1%)
120
Table 2. Bacteriologic findings of patient urine
Finding
% (n)
Positive culture
E. coli
Quinolone resistance
ESBL(⫹) E. coli
Quinolone resistance
ESBL(⫹) E. coli
In first biopsy
In repeat biopsy
61 (17)
82 (14)
93 (13)
43 (6)
100 (6)
66.7 (4)
33.3 (2)
ESBL, extended-spectrum ␤-lactamase.
were detected with acute bacterial prostatitis after prostate biopsy. Acute prostatitis occurred after the first biopsy in 15 patients (1.3%) and after repeat biopsy in 13
patients (6.8%). None of the patients in the repeat
biopsy group had developed acute prostatitis after their
first biopsy. The difference was significant between the 2
groups (P ⫽ .001). The mean age of the patients who
developed prostatitis was 60.4 ⫾ 10.4 years. The patients
developed infective symptoms within a mean of 3 days after
prostate biopsy. All patients presented with a temperature
⬎38°C, and 18 (64%) had leukocytosis, defined as ⬎10 000
cells/mL, were hospitalized, and received intravenous antibiotics. Of the 28 patients, 15 received ceftriaxone, 8 received fluoroquinolone, and 5 received sulbactam ampicillin/gentamicin combination as their initial treatment. No
cases of septic shock or death occurred.
Of the 28 patients, 17 (61%) had positive urine cultures, including E. coli in 14 (82%), Enterobacter cloacae
in 1, Pseudomonas aeruginosa in 1, and Flavobacterium
specium in 1. Of the 14 patients with E. coli in urine, 2
had ESBL-producing E. coli in their blood culture, with
the same drug susceptibility pattern seen.
Of the 17 patients, 13 (76.5%) harbored fluoroquinolone-resistant pathogens, including E. coli in 10, Enterobacter cloacae in 1, Pseudomonas aeruginosa in 1, and
Flavobacterium specium in 1. Thus, the overall incidence
of fluoroquinolone resistance was 1% (13/1339 patients).
UROLOGY 74 (1), 2009
Table 3. Drug susceptibility of ESBL-producing Echerichia coli isolated from urine and blood cultures
Antibiotics
Gentamicin
Piperacillin-tazobactam
Imipenem
Patient 1
Patient 2
Patient 3
Patient 4
Patient 5
Patient 6
R
S
S
S
R
S
S
S
S
S
S
S
S
S
S
R
S
S
ESBL, extended-spectrum ␤-lactamase; S, susceptible; R, resistant.
All ESBL-producing E. coli were resistant to ampicillin, sulbactam-ampicillin, amikacin, cefepime, ceftriaxone, ciprofloxacin.
Drug susceptibility was same in urine and blood samples in all cases.
Table 4. Susceptibility patterns of ESBL-producing Escherichia coli compared with non-ESBL-producing E. coli
Antibiotics
Ampicillin
SAM
Cefazolin
Gentamicin
Amikacin
Piperacillintazobactam
Cefepime
Ceftriaxone
Ciprofloxacin
Imipenem
Nitrofurantoin
Susceptibility
ESBL-Producing
E. coli
E. coli (n)
(n)
0 (0)
0 (0)
0 (0)
4 (66.6)
0 (0)
5 (83.3)
1 (12.5)
0 (0)
8 (100)
4 (50)
5 (62.5)
6 (75)
0 (0)
0 (0)
0 (0)
6 (100)
5 (83.3)
8 (100)
7 (87.5)
1 (12.5)
8 (100)
3 (37.5)
P Value*
.571
1000
.001
.471
.028
.615
.001
.001
.571
1000
.121
Data in parentheses are percentages.
* Fisher’s exact test.
Of these patients, 11 had no positive urine or blood
culture and were treated with ceftriaxone or ciprofloxacin
uneventfully.
During the study period, 6 of 14 patients had acute
prostatitis caused by ESBL-producing E. coli. The bacteria
isolated from urine were tested for drug susceptibility to a
wide range of antibiotics. These results are listed in Table 3.
All patients with ESBL-producing E. coli were treated
with imipenem. The bacteria detected in these urine
cultures were resistant to ciprofloxacin, ceftriaxone, sulbactam/ampicillin, and cefazolin. Imipenem and piperacillin-tazobactam were the most active agents against
ESBL-producing E. coli.
ESBL-producing E. coli were compared with the nonESBL-producing E. coli strains. ESBL-producing isolates
had a significant reduction in activity for most antimicrobial agents, including fluoroquinolones, amikacin, cefazolin, ceftriaxone, and cefepime (Table 4).
COMMENT
The introduction of antibiotic prophylaxis before transrectal ultrasound-guided prostate biopsy has significantly
decreased the urinary tract infection rate. However, no
reference standard is available for preparing a patient
before prostate biopsy, especially regarding the use of
antibiotics. Fluoroquinolones are the most frequently
used antibiotics for prophylaxis before transrectal prostate biopsy. Kapoor et al.5 noted that using ciprofloxacin
before transrectal prostate biopsy significantly reduced
UROLOGY 74 (1), 2009
the infection rates compared with the placebo group in
their randomized, double-blind, controlled study. In an
randomized controlled study, no clinically or statistically
significant difference was observed between 1-day and
3-day antibiotic prophylaxis regimens.10 The European
Association of Urology and American Urology Association guidelines recommend antibiotic prophylaxis for
⬍72 or 24 hours, respectively.11,12
In addition to reducing the infection rate, it also
supplied a cost-effective approach, which led us to use
fluoroquinolones for antibiotic prophylaxis. Enemas were
not given before biopsy in our protocol, because no
consensus has been reached with regard to the effect of
enemas before biopsy on the transrectal prostate biopsy
complication rate.13,14
After TRUS-guided biopsy, when the patients presented with infective symptoms, blood and urine cultures
were obtained. In our series of 1339 patients, the overall
incidence of infective complications was 2.1% (28/1339),
and 17 of 28 (61%) cases had positive urine cultures.
This result is consistent with the reported rates7,15,16
However, the increase in the rate of fluoroquinoloneresistant E. coli poses a problem. The fluoroquinolone
resistance rate in E. coli-associated urinary tract infection
has been reported to be about 10%-20% in different
studies.17,18 Recent data have shown that fluoroquinoloneresistant infections after prostate biopsy are also increasing. Tal et al.15 reported that the causative pathogen in
urinary tract infections after transrectal prostate biopsy
was mainly E. coli with complete resistance to fluoroquinolones. Otrock et al.16 also noted that 50% of patients hospitalized with clinical urinary tract infections
after transrectal prostate biopsy were infected with fluoroquinolone-resistant E. coli. Feliciano et al.7 demonstrated an increase in postbiopsy infections (1.7%-4.8%)
and fluoroquinolone resistance in the 2 years after biopsy
in a study of 1273 patients.
Fluoroquinolone resistance was observed in 93% of
patients infected with E. coli in our patient cohort. One
of the possible causes of the increasing resistance to
fluoroquinolones is the previous wide use of these drugs.
Also, some studies have reported on the development of
quinolone-resistant strains of E. coli in the stool of patients receiving fluoroquinolone prophylaxis.19 Shigehara
et al.6 considered that the previous use of levofloxacin
might cause bacterial selection in the rectum, and E. coli
resistant to levofloxacin might then appear in the rectum
for a certain period.
121
In our study, a greater rate of acute prostatitis was
observed in the repeat biopsy group compared with patients who had undergone prostate biopsy for the first
time (6.8% vs 1.3%, respectively). The difference in this
complication rate was statistically significant. These findings have indicated that the previous use of an extended
course of broad-spectrum antibiotics for prophylaxis is
probably counterproductive, and, as Shigehara et al.6
indicated, fluoroquinolone-resistant strains might be
more frequently found in the rectum of repeat biopsy
patients than in those undergoing first biopsy. These
findings might suggest that the antibiotic prophylaxis
regimen should be revised by using a shorter period of
fluoroquinolones or parenteral administration of different
groups of antibiotics before repeat biopsy.
In addition to the fluoroquinolone-resistant strains of
E. coli, many studies have addressed the emergence of
ESBL-producing E. coli. No such report after transrectal
prostate biopsy has been published. Our results demonstrated that 43% of E. coli are ESBL producing. This high
ESBL frequency might have been caused by the excessive
use of broad-spectrum antibiotics in our hospital. A number of case-control studies have consistently shown that
previous use of third-generation cephalosporins and the
previous use of fluoroquinolones remain as independent
risk factors for infections caused by ESBL-producing organisms. Kanafani et al.20 reported that the most notable
risk factor for acquiring infections with ESBL-producing
organisms was antibiotic consumption within 30 days of
infection with an odds ratio of 7. Lautenbach et al.21
have also shown that the previous use fluoroquinolone
increased the risk of ESBL-producing E. coli and K.
pneumonia infections.21
The importance of the accurate identification of ESBLproducing microorganisms should be emphasized. Patients with bacteremia caused by ESBL-producing E. coli
strains had greater mortality rates than those with bacteremia caused by non-ESBL-producing strains. Hyle et
al.22 found a significant association between inadequate
initial antibiotic treatment and mortality, but only for
nonurinary ESBL-producing bacteria. A recent report
confirmed these findings, suggesting that inadequate initial antimicrobial therapy is an independent risk factor
for mortality in patients with bacteremia caused by
ESBL-producing microorganisms.22 Similarly, Melzer and
Petersen23 noted that the risk of death was fourfold
greater among patients with undefined sites of infection
compared with patients with urinary tract infections. In
contrast, Skippen et al.24 found no difference in the
overall mortality rate between those with ESBL-producing and those with non-ESBL-producing pathogen-related infections. These discordant results might have
been because of small or unpowered studies or a failure to
adequately adjust for the severity of underlying disease.
We did not observe septic shock or mortality in patients
with ESBL-producing E. coli infections in our series.
122
Our study had some potential limitations. First, although the total number of patients in our study was one
of the largest reported to date, the sample size of the
groups was limited because of the low incidence of acute
prostatitis after TRUS-guided biopsy. These data should
also be analyzed using larger cohort studies. Second,
because our predictor variables were obtained from clinical chart review, they were inherently incomplete. However, we tried to include the most complete patientspecific information. We showed that previous use of
fluoroquinolones was associated with ESBL-producing infections. Third, the lack of a molecular analysis of the
ESBL strains made it difficult to determine the relatedness of the bacterial isolates; therefore, we could not
assess the risk of cross-contamination in patients who
required frequent visits to healthcare providers.
CONCLUSIONS
To our knowledge, this is the first report to emphasize
that we will encounter ESBL-producing E. coli more
frequently in patients with acute prostatitis after transrectal prostate biopsy. The high frequency of multiple
antibiotic resistance among ESBL-producing strains
greatly limits the possibilities of administering an adequate empirical antibiotic regimen to these patients.
However, blanket use of broad-spectrum antibiotics is
likely to result in the additional emergence of resistance.
Thus, efforts to optimize the initial therapy must be
balanced by efforts to promote the judicious use of antimicrobial agents. Theoretically, in the clinical setting,
using a carbapenem is the only way to ensure that an
effective empirical antibiotic therapy is administered to a
patient suspected of having a possible ESBL-producing E.
coli infection. However, this practice is not in accordance
with rational antibiotic use. One should remember the
possibility of an ESBL-producing microorganism in the patient with acute prostatitis after transrectal prostate biopsy.
We suggest restricting the use of carbapenems to those with
proven infection caused by ESBL-producing pathogens.
The prompt initiation of effective antimicrobial treatment is essential in patients with ESBL-producing E. coli
infections, and empirical decisions must be based on
knowledge of the local distribution of pathogens and
their drug susceptibility.
References
1. Crawford ED, Haynes AL Jr, Story MW, et al. Prevention of
urinary tract infection and sepsis following transrectal prostatic
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2. Lindert KA, Kabalin JN, Terris MK. Bacteremia and bacteriuria
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3. Aron M, Rajeev TP, Gupta NP. Antibiotic prophylaxis for transrectal needle biopsy of the prostate: a randomized controlled study.
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4. Sieber PR, Rommel FM, Agusta VE, et al. Antibiotic prophylaxis
in ultrasound guided transrectal prostate biopsy. J Urol. 1997;157:
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5. Kapoor DA, Klimberg IW, Malek GH, et al. Single-dose oral
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6. Shigehara K, Miyagi T, Nakashima T, et al. Acute bacterial prostatitis after transrectal prostate needle biopsy: clinical analysis.
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UROLOGY 74 (1), 2009
EDITORIAL COMMENT
This is an excellent clinical review of a large number of patients
who underwent transrectal ultrasound-guided prostate biopsy
(TRUS-BP) during an almost 5-year period. All patients received ciprofloxacin, 500 mg twice daily for 5 days, starting 24
hours before the procedure. All patients underwent a minimum
of a 12-core biopsy. The authors reviewed the infectious complications and noted that these occurred in 28 of 1339 patients
(2.1%). A slightly greater (and statistically significant) incidence was found in patients undergoing repeat biopsy (6.8%) vs
an initial biopsy (1.3%). Most of the patients (61%) had
Escherichia coli as the cause of the infection, with 13 of 17
(76.5%) caused by extended-spectrum ␤-lactamase (ESBL)producing bacteria. Of these, 10 of 17 (58.9%) were due to
ESBL-producing E. coli. These infections were resistant to fluoroquinolone antibiotics.
There are 2 import facets to this study: the high level of safety
in regard to patients undergoing TRUS-BP, and the increasing
incidence of ESBL-producing bacteria. Other studies have documented the safety of this common office-based procedure.
Generally, the incidence of acute prostatitis after TRUS-BP
is about 0.25%-3%.1-4 Given this, the clinician must keep in
mind that infections occurring after TRUS-BP might be due
to resistant strains that do not respond to fluoroquinolones.2,3 Hence, the clinician should consider selecting an
alternative nonfluoroquinolone antibiotic in this scenario.
This study also serves to support that, in general, patients
with acute bacterial prostatitis that does not respond to a
fluoroquinolone antibiotic should be switched to an alternative if they do not improve clinically within several days of
the initial treatment.
No overall consensus has been reached on the antibiotic
prophylaxis for TRUS-BP in the published data.2 Studies
have ranged from a single dose of a long-acting fluoroquinolone to several days of an antibiotic after biopsy. Recently,
the American Urological Association issued guidelines on
antibiotic prophylaxis for urologic surgery in general.5 Included were recommendations suggesting a fluoroquinolone
or second- or third-generation cephalosporin for ⱕ24 hours
for TRUS-BP. No clinical benefit appears to exist for extending
coverage for ⬎24 hours and probably only increases the risk of
ESBL-producing bacteria. Additionally, several studies have
shown that a cleansing enema is not required or recommended
before biopsy.3 Some have theorized the high incidence of
infectious complications after repeat TRUS-BP might be due to
the development of ESBL-producing bacteria that reside within
the colon after initial biopsy.
If we continue to use fluoroquinolones as the mainstay of
antibiotic prophylaxis for TRUS-BP, we will continue to see an
increasing emergence of ESBL-producing bacteria. This could
translate into more post-TRUS-BP prostatitis and other infectious complications. Clinicians must be aware of this and should
promptly initiate an alternative antibiotic determined by their
local distribution of pathogens and susceptibility. Many have
suggested using either a second- or third-generation cephalosporin or carbapenem (if the patient is at high risk or has a poor
clinical response).2,4 Fortunately, this procedure has stood the
test of time and has shown itself to be highly safe with a low
incidence of overall complications.
123