Transrectal ultrasound guide prostate biopsies in patients taking aspirin for cardiovascular disease- a meta-analysis

1. Transfusion and Apheresis Science 45 (2011) 275–280
Contents lists available at SciVerse ScienceDirect
Transfusion and Apheresis Science
journal homepage: www.elsevier.com/ locate/ transci
Transrectal ultrasound-guided prostate biopsies in patients taking
aspirin for cardiovascular disease: A meta-analysis
Luca Carmignani a, Stefano Picozzi a,⇑, Giorgio Bozzini a, Ercole Negri b, Cristian Ricci c,
Maddalena Gaeta d, Marco Pavesi e
a Urology Department, University of Milan, IRCCS Policlinico San Donato, San Donato Milanese, Italy
b Urology Department, University of Milan, Istituto Clinico Villa Aprica, Como, Italy
c Biometry and Clinical Epidemiology Unit, IRCCS Policlinico San Donato, San Donato Milanese, Italy
d Department of Preventive, Occupational and Community Medicine, University of Pavia, Pavia, Italy
e Polispecialistic Anaesthesia Unit, IRCCS Policlinico San Donato, San Donato Milanese, Italy
a r t i c l e i n f o
Keywords:
Prostate
Cancer
Prostate cancer
Biopsy
Vascular disease
Myocardial infarction
Cardiovascular disease
Aspirin
a b s t r a c t
Introduction: The management of anti-platelet therapy in the peri-operative period is a
source of great concern. The dilemma is between whether to stop these agents peri-oper-atively
in order to reduce the risk of bleeding complications, or to continue them in order
not to compromise the protection they afford against the risk of cardiovascular events.
Materials and methods: The aim of this systematic review and meta-analysis was to under-stand
whether continued aspirin therapy is a risk factor for bleeding complications after
ultrasound-guided biopsy of the prostate. A bibliographic search covering the period from
January 1990 to May 2011 was conducted in PubMed, MEDLINE and EMBASE. We also
included our own series in the analysis.
Results: A total of 3218 participants were included. Haematuria was statistically more fre-quent
(P = 0.001) among patients taking aspirin than in the control group with an odds
ratio estimate of 1.36 [1.13; 1.64]. This increased risk was, however, due to minor bleeding.
The occurrence of rectal bleeding and haematospermia was not statistically increased
(P = 0.33 and P = 0.24, respectively) in patients taking aspirin compared to in the control
group with odds ratios estimate of 1.24 [0.80;1.93] and 1.52 [0.75; 3.08], respectively.
Discussion: There is limited information of the relationship between continued use of aspi-rin
and haemorrhagic complications after transrectal ultrasound-guided biopsy of the
prostate. This is the first comprehensive analysis on this topic.
Conclusion: Continued use of aspirin does not increase the risk of overall bleeding or mod-erate
and severe haematuria after prostatic biopsy, and thus stopping aspirin before such
biopsies is unnecessary.
2011 Elsevier Ltd. All rights reserved.
1. Introduction
With an increasingly elderly population requiring surgi-cal
procedures and the growing indications for potentially
lifelong use of anti-platelet agents, the management of
anti-platelet therapy in the peri-operative period is a
source of great concern.
Anti-platelet agents are prescribed widely for primary
and secondary prevention of coronary artery and cerebro-vascular
disease in patients with acute coronary syndrome,
myocardial infarction, transient ischaemic attacks/stroke,
severe carotid artery stenosis and peripheral vascular dis-ease.
They are also used after percutaneous vascular inter-ventions
with positioning of endovascular stents and in
high-risk patients with multiple cardiovascular risk factors
⇑ Corresponding author. Address: Urology Department, IRCCS Policli-nico
San Donato, Via Morandi 30, San Donato Milanese, 20097 Milan,
Italy. Tel./fax: +39 02 52774329.
E-mail address: stepico@tin.it (S. Picozzi).
1473-0502/$ - see front matter 2011 Elsevier Ltd. All rights reserved.
doi:10.1016/j.transci.2011.10.008

2. 276 L. Carmignani et al. / Transfusion and Apheresis Science 45 (2011) 275–280
(e.g. diabetes mellitus, cigarette smoking, hypercholestero-laemia,
hypertension). According to a meta-analysis of
several randomised studies, secondary prevention with
low-dose aspirin reduces the risk of stroke and myocardial
infarction by about one-third, and, most important, the risk
of cardiovascular death by about one-sixth [1].
Thus, the practice of routine peri-procedural
withdrawal of anti-aggregant therapy in patients with
known cardiovascular disease could have disastrous conse-quences.
The dilemma is between whether to stop these
agents peri-operatively in order to reduce the risk of bleed-ing
complications, or to continue them in order not to
compromise the protection they afford against the risk of
cardiovascular events. Since the published information on
the management of anti-platelet agents before prostatic
biopsy is limited and conflicting, we conducted a system-atic
review on this issue.
2. Materials and methods
The aim of this systematic review and meta-analysis
was to understand whether continued anti-aggregant
therapy is a risk factor for bleeding complications after
ultrasound (US)-guided biopsy of the prostate. Clinical out-comes
of interest were the rates of haematuria, rectal
bleeding and haematospermia. We also qualitatively eval-uated
the occurrence of mild, moderate and severe bleed-ing
complications. The results analysed were drawn from
our own series of patients and published cohorts.
2.1. Our series
Our series consisted of 477 patients who underwent
transrectal ultrasound (TRUS)-guided prostate biopsy in
urology units of various referral hospitals between January
2008 and March 2011 and who were enrolled in a study ap-proved
by the local ethical committee. All patients gave
written informed consent to their participation in the study.
The indications for performing prostatic biopsy were
those stated in the EAU 2007 guidelines: presence of an
abnormal finding, suspicious of a neoplastic lesion, on dig-ital
rectal examination; total prostate-specific antigen
(PSA) higher than 4 ng/ml (or greater than 2.5 ng/ml in
cases with a positive family history) and/or presence of
suspicious lesions on ultrasound examination of the pros-tate
[2].
Immunosuppressed patients, patients who had already
undergone a previous prostatic biopsy or previous radical
prostatectomy (biopsy of the anastomosis) and patients
on dual anti-platelet therapy because of cardiovascular
disease were excluded from the study.
As part of the work up for the prostatic biopsy, all pa-tients
had undergone blood tests including a full blood
count and a coagulation screen, with assays of the pro-thrombin
time and activated partial thromboplastin time.
Treatment in patients receiving anti-platelet therapy with
acetylsalicylic acid was not suspended or integrated.
Of the 477 patients who entered this study, 459 (96.2%)
completed the telephone interview and 136 patients were
taking anti-platelet drugs.
Preparation for the procedure consisted of an enema the
evening prior to the biopsy and antibiotic prophylaxis with
fluoroquinolones starting on the morning of the biopsy and
continued for three more days [3,4].
The TRUS-guided biopsy of the prostate was carried out
using disposable 18 G needles. The ultrasound equipment
used was an Esaote MyLab 40 with a Transrectal Micro
Convex Array probe with a curvature radius of 10 mm
and frequency of 9.4 MHz.
The anaesthesia was also administered under ultra-sound
guidance and consisted of two injections of 5 ml
lidocaine 1% into the angle between the bladder and pros-tate,
one on each side. Fourteen samples were taken,
according to the scheme described by Gore et al. [5].
Following the procedure, the patients were observed for
2 h until they had micturated in order to evaluate the onset
of any early complications (urinary retention, haematuria,
rectal bleeding). Furthermore, in cases in which rectal
bleeding occurred, the rectum was explored.
Bleeding complications were evaluated by direct
observation for the first few hours after the biopsy and
by telephone interview on the 3rd and 7th days and
1 month post-procedure and included:
urethral bleeding: loss of blood from the external
urethral meatus independently of micturition;
rectal bleeding: bleeding from the rectum;
haematuria: macroscopically evident blood in the
urine.
2.2. Meta-analysis
2.2.1. Search strategy
Studies were identified by searching electronic
databases and scanning reference lists of articles. A
bibliographic search covering the period from
January 1990 to May 2011 was conducted in PubMed,
MEDLINE and EMBASE. Additional hand searches of the
reference lists of included studies, reviews, meta-analy-ses
and guidelines on the management of anti-aggregant
therapy during US-guided prostate biopsy were
performed. The searches were restricted to publications
in English.
2.2.2. Study selection
Identified studies were reviewed and selected if they
reported bleeding complications in patients taking anti-platelets
agents who underwent US-guided biopsy of the
prostate. Inclusion or exclusion of studies was performed
hierarchically based first on the title of the report, then
on the abstract, and finally on the contents of the full text.
A study was accepted for inclusion on the basis of agree-ment
of two investigators (SP and CR); any disagreement
on study inclusion was resolved by consulting a third
investigator (LC). Database searches yielded 42 references.
Exclusion of irrelevant references left six references
describing studies. This analysis is based on the four
studies that fulfilled the predefined inclusion criteria
[6–9]. All these studies dealt with TRUS-guided biopsy of
the prostate in patients taking aspirin as an anti-aggregant
agent.

3. 2.2.3. Study classification
L. Carmignani et al. / Transfusion and Apheresis Science 45 (2011) 275–280 277
Studies were classified according to the Cochrane Inter-vention
Meta-analysis Handbook into non-randomised
comparative studies (including non-randomised, con-trolled
trials, retrospective cohort studies and historically
controlled trials) and into randomised clinical trials.
2.2.4. Data extraction and quality assessment
One author (SP) extracted the data from included stud-ies
and entered them into the data extraction form. A sec-ond
author (CR) checked the extracted data to ensure data
quality. Disagreements were resolved by discussion be-tween
the two review authors; if no agreement could be
reached, it was planned that a third author would decide
(LC). The quality of studies was scored using the methods
of the US Preventive Services Task Force [10,11].
The US Preventive Services Task Force classifies a study
as ‘‘good’’ if it evaluates relevant available screening tests,
uses a credible reference standard, interprets the reference
standard independently of the screening test, shows reli-ability
of the test assessed, has few or handles indetermi-nate
results in a reasonable manner and includes a large
number of patients (more than 100 broad-spectrum cases);
as ‘‘fair’’ if it evaluates relevant available screening tests,
uses reasonable although not best standards, interprets
the reference standard independently of the screening test,
has a moderate sample size (50–100 subjects) and a ‘‘med-ium’’
spectrum of patients; and as ‘‘poor’’ if it has a fatal
flaw such as using an inappropriate reference standard,
administering a screening test improperly, biased ascer-tainment
of a reference standard, and has a very small
sample size or very narrow selected spectrum of patients.
2.2.5. Statistical analysis
An overall quantitative evaluation was made of all the
studies included. Both the fixed and the random effect mod-els
were used on bleeding complications according to the
heterogeneity reported by the I2 statistic [12]. In this
meta-analysis the fixed effect model was used if the I2 statis-tic
was lower than 50%. Publication bias and small study ef-fect
were qualitatively evaluated by visual inspection of
funnel plots.
All analyses were performed using RevMan 5 (Review
Manager, version 5.0; Copenhagen, Denmark: The Nordic
Cochrane Centre, The Cochrane Collaboration, 2008).
3. Results
3.1. Analysis of the databases
Table 1 summarises the characteristics of the studies in-cluded
in this analysis. A total of 3218 participants were in-cluded
in the four published studies [6–9] and our series.
The number of participants in each trial ranged from 200
to 1811. Of the four published studies, two were from the
UK, while Italy and Greece provided one each; all these stud-ies
were published after 2003. For each study we recorded
the author, year of publication, the number of patients en-rolled,
the number of evaluated patients, the biopsy proto-col,
the size of the biopsy needle, the use of an anaesthetic
technique (local or cream peri-prostatic injection), length
of follow-up, the number of patients taking aspirin, the
number of controls, their mean age, mean prostate volume,
mean PSA, the number of biopsy cores, the number of pa-tients
with haematuria (as a total and also divided by the
severity of the symptom into mild, moderate and severe),
the number of patients with rectal bleeding (again as a total
and divided by the severity of the symptom in mild, moder-ate
and severe), the number of patients with haematosper-mia
and the reported duration of each complication.
The total number of patients subjected to prostate
biopsy who were taking aspirin was 776, with the number
of aspirin recipients ranging from 36 to 387 in the various
studies (Table 2). The mean age of patients, reported in
four studies, was 67.3 years. The average volume of the
prostate, reported in three studies, was 48.87 ml. The mean
total PSA, reported in three studies, was 7.96 ng/ml. The
average number of biopsies, reported in four studies, was
Table 1
General data extracted from the studies, listed by first author and year of publication.
Authors, year [Ref.] Nation Type Period Total patients, no. Patients entering in the study, no. Follow-up (days)
Maan et al., 2003 [11] UK Prospective NR 200 177 30
Giannarini et al., 2007 [12] Italy Prospective 2005–2006 200 130 14
Halliwell et al., 2008 [13] UK Prospective NR 1811 1740 30
Kariotis et al., 2010 [14] Greece Prospective 2007–2008 530 434 7
Carmignani et al., 2011 Italy Prospective 2008–2010 477 449 30
NR: not reported.
Table 2
Bleeding complications in patients subjected to prostate biopsy who were taking aspirin (haematuria, rectal bleeding and haematospermia).
Authors, year ASA, no. Haematuria % Rectal bleeding, no. % Haematospermia, no. %
Kariotis et al., 2010 152 98 65.4 51 33.5 91/101 90.1
Halliwell et al., 2008 387 279 72.1 82 21.2 66 17.1
Giannarini et al., 2007 65 33 51 20 31 22/56 40
Maan et al., 2003 36 20 56 0 0 4 11
Carmignani et al., 2011 136 33 24.6 14 10.2 62/72 86.1

4. 278 L. Carmignani et al. / Transfusion and Apheresis Science 45 (2011) 275–280
Table 3
Bleeding complications in patients subjected to prostate biopsy who were not receiving aspirin therapy (haematuria, rectal bleeding and haematospermia).
Authors, year Control, no. Haematuria % Rectal bleeding, no. % Haematospermia, no. %
Kariotis et al., 2010 282 171 60.6 73 25.9 159/183 86.9
Halliwell et al., 2008 731 444 60.7 95 13 154 21.1
Giannarini et al., 2007 65 31 48 18 28 23/54 42
Maan et al., 2003 141 83 59 31 22 40 29
Carmignani et al., 2011 313 69 22 36 11 95/140 67.8
10.7. Haematuria after prostate biopsy occurred in a total
of 463 patients with its frequency in the studies ranging
between 24.6% and 72.1% (mean 53.82%) (Table 2). Three
studies described the degree of this complication as mild,
moderate and severe which occurred in 319, 87 and 4 pa-tients,
respectively. Rectal bleeding developed in a total of
167 patients with its frequency in the various studies rang-ing
between 0% and 33.5% (mean 19.18%) (Table 2). Two
studies described the degree of this complication as mild,
moderate and severe which occurred in 70, 24 and 0 pa-tients,
respectively. Haematospermia occurred in a total
of 245 patients with a frequency ranging between 11.0%
and 90.1% (mean 48.86%) (Table 2).
There were 1530 control patients who underwent pros-tate
biopsy and were not receiving aspirin therapy, with
the number of control patients in the studies ranging from
65 to 731 (Table 3). The mean age of control patients, re-ported
in four studies, was 64.6 years. The mean volume
of the prostate in control patients, reported in three stud-ies,
was 49.4 ml. The mean total PSA, reported in three
studies, was 7.53 ng/ml. The average number of biopsies,
reported in four studies, was 10.7. Haematuria developed
after prostate biopsy in a total of 798 control patients with
the frequency of this complication ranging between 22%
and 60.7% (mean 50.06%) in the various studies. In three
studies haematuria was classified as mild, moderate and
severe and occurred in 573, 110 and 1 of the control pa-tients,
respectively. Rectal bleeding was reported in a total
of 253 control patients, with a frequency varying between
11.0% and 28% (mean 10.01%). Two studies describe the de-gree
of this complication as mild, moderate and severe and
reported that it occurred in 111, 17 and 2 control patients,
respectively. Haematospermia developed in a total of 471
patients, with a frequency varying between 29.0% and
86.9% (mean 49.36%).
3.2. Analysis of the outcomes
We found that aspirin had an overall significant effect of
increasing haematuria: the fixed effect model applied to
haematuria (Fig. 1 panel A) showed a significantly higher
odds ratio for the aspirin group (odds ratio estimate = 1.36
[1.13; 1.64]), indicating an increased risk of bleeding of
about 30%. The other two outcomes, rectal bleeding and
haematospermia, did not show a statistically significant
association with aspiring treatment (Fig. 1 panel B and C).
3.3. Heterogeneity evaluation among studies
All the included studies belonged to the general design
of the analysis and between 200 and 1811 patients were
included. Heterogeneity among studies was relevant for
rectal bleeding and haematospermia, being about 60%,
but not for haematuria. For rectal bleeding the heterogene-ity
was mostly attributable to the study of Maan, in which
no rectal bleeding occurred in any of the aspirin-treated
patients. If this study was excluded the heterogeneity re-sulted
in a I2 of 29% having a fixed effect odds ratio esti-mate
of 1.48 [1.18; 1.86].
3.4. Publication and small study bias assessment
None of the comparisons performed revealed a relevant
publication or small study bias. With regards to rectal
bleeding, the study by Maan et al. could be considered an
outlier both because no events were described in the aspi-rin
group and because of the small sample size. Excluding
this study led to an even smaller publication bias.
4. Discussion
Anti-platelet or anti-aggregant agents are members of a
class of pharmaceuticals that decrease platelet aggregation
and inhibit thrombus formation. They are effective in the
arterial circulation, where anticoagulants have little effect.
Anti-platelet agents are classified into three categories: cy-clo-
oxygenase inhibitors (e.g. aspirin), thienopyridines
(e.g. ticlopidine, clopidogrel, prasugrel) and platelet GP-IIb–
IIIa inhibitors (e.g. eptifibatide, tirofiban, abciximab).
Aspirin exerts its anti-platelet effects by inhibiting cy-clo-
oxygenase 1 (COX-1), thus irreversibly inhibiting the
synthesis of thromboxane A2 and prostacyclin (PGI2).
The inhibition of COX-1 is irreversible and lasts the whole
of the platelet’s circulating lifespan (around 7 days). The
long-term benefit of aspirin is a relative risk reduction of
recurrent vascular events of 38% after myocardial infarc-tion
and 25% after stroke [13].
Severe haemorrhagic complications after TRUS-guided
biopsy of the prostate are rare, but mild haemorrhagic
complications, such as haematuria, haematospermia and
rectal bleeding, are very common. The lack of a uniform
policy concerning the management of aspirin before
TRUS-guided biopsy was clearly exposed by Connor and
Wingate who surveyed over 500 biopsy centres in the UK
and found a wide variation in practice; 52% of radiologists
and 27% of urologists taking biopsies preferred that the pa-tients
stopped aspirin before the biopsy [14]. Using a ques-tionnaire
mailed to 450 consultant urological surgeons in
the UK, with the aim of establishing practices and proto-cols
for managing aspirin or aspirin-like drugs before pros-tate
biopsy, Masood et al. found that 65% did not routinely
stop aspirin before prostate biopsy, while 35% stopped

5. L. Carmignani et al. / Transfusion and Apheresis Science 45 (2011) 275–280 279
Fig. 1. (Panel A) The fixed effect model applied to haematuria; (panel B) the fixed effect model applied to rectal bleeding; and (panel C) the fixed effect
model applied to haematospermia.
aspirin at various times before prostate biopsies (52%
1 week before, 41% 2 weeks before and 6% 2 weeks be-fore)
[15]. Among the urological surgeons who routinely
stopped aspirin use in their patients, the median time for
restarting aspirin was 2 (range 0–10) days after the biopsy
procedure. The authors also reported that a third of the
respondents stated that they would routinely stop aspirin
and would cancel a procedure if the patient had inadver-tently
not stopped aspirin or aspirin-like drugs.
Clinicians must stratify patients in relation to the
different risks of bleeding, as well as the different risks of
thrombosis. Given the vast number of patients on oral
anti-aggregant therapy for cardiovascular prevention, to-gether
with the aging population, this problem of reconcil-ing
these risks has emerged in recent years. As illustrated
by the available investigations on the urological manage-ment
of peri-procedural aspirin use, there are different
points of view on how to resolve the dilemma. Although
the risk of coronary thrombosis largely outweighs the risk
of surgical haemorrhage, this issue has not yet been clearly
evaluated in urological patients because, in many in-stances,
the risk of bleeding might be exceedingly danger-ous
during urological surgery [16].
General and specific guidelines on this topic are currently
inconsistent and new studies and meta-analyses are
needed. This is well evidenced by the lack of standardised
practice in the peri-operative management of aspirin in
other surgical specialities. Doctors are unsure how to pre-vent
aspirin-induced bleeding complications and
hazardous events, such as stroke, myocardial infarction or
even cardiovascular death. One multi-study analysis con-cluded
that aspirin use did not cause clinically relevant
bleeding complications in cardiovascular, vascular and
orthopaedic surgery, or during epidural anaesthesia
although most of the studies included in the analysis
reported an increase in clinically irrelevant bleeding
induced by aspirin [1].
The relation between aspirin use and the incidence of
bleeding complications after TRUS biopsy of the prostate
was first analysed by Rodríguez and Terris [17]. They pro-spectively
studied 128 patients and found that none of
the haemorrhagic complications was related to previous
aspirin or non-steroidal anti-inflammatory drug use, so
they concluded that recent use of aspirin or non-steroidal
anti-inflammatory drugs is not an absolute contraindica-tion
to this procedure. Likewise, in 1999, Herget et al. found
no evidence of an association between the use of aspirin
and post-biopsy bleeding complications [18]. Following
these preliminary studies, only four recent studies have
been published in the literature [6–9]. Through this meta-analysis
we wanted to clearly determine, for the first time,
the role of aspirin in increasing the frequency of bleeding
complications and to establish a landmark on this topic.
Our findings seem to confirm those previously reported
in other surgical specialties: aspirin only increased the rate
of haematuria, in a mild form, which resolved in a mean of
2–3 days after the procedure. Rectal bleeding and haemat-ospermia
were not statistically associated with the use of

6. 280 L. Carmignani et al. / Transfusion and Apheresis Science 45 (2011) 275–280
aspirin, although we noted that haematospermia in
patients taking aspirin was prolonged, lasting a mean of
10 days.
One limitation of this analysis is related to the non-homogeneity
in the method of recording and quantifying
bleeding complications. Furthermore, the rate of haemato-spermia
has to be calculated from the number of sexually
active patients who engaged in sexual activity after the
procedure and not from the overall number of patients in-cluded
in the studies. Another issue that can be considered
a limitation is due to the absence of published data regard-ing
the number of patients who suffer from a cardiovascu-lar
event related to peri-procedural aspirin withdrawal.
Thus, the exact incidence of cardiovascular events after
aspirin cessation remains uncertain.
5. Conclusion
In conclusion, the results of this analysis suggest that
continued use of aspirin does not increase the risk of over-all
bleeding or moderate and severe haematuria after pros-tatic
biopsy, and thus stopping aspirin before such biopsies
is unnecessary.
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