Patterns of Repeat Prostate Biopsy in Contemporary
Clinical Practice
Nitya E. Abraham, Neil Mendhiratta and Samir S. Taneja*,†
From the Division of Urologic Oncology, Department of Urology, New York University School of Medicine, New York, New York
Abbreviations
and Acronyms
ASAP ¼ atypical small acinar
proliferation
CaP ¼ prostate cancer
DRE ¼ digital rectal examination
GS ¼ Gleason score
HGPIN ¼ high grade prostatic
intraepithelial neoplasia
MRI ¼ magnetic resonance
imaging
PSA ¼ prostate specific antigen
mp-MRI ¼ multiparametric MRI
TRUS ¼ transrectal ultrasound
UCSF-CAPRA ¼ University of
California-San Francisco Cancer of
the Prostate Risk Assessment
Accepted for publication October 15, 2014.
Study received local institutional review
board approval.
* Correspondence: Division of Urologic
Oncology, Department of Urology, New York
University Langone Medical Center, 150 East
32nd St., Suite 200, New York, New York 10016
(telephone: 646-825-6321; FAX: 646-825-6399;
e-mail: samir.taneja@nyumc.org).
† Financial interest and/or other relationship
with Hitachi-Aloka, Healthtronics, Elsevier, Trod
and Steba Biotech.
0022-5347/15/1934-1178/0
1178 j www.jurology.com
THE JOURNAL OF UROLOGY®
© 2015 by AMERICAN UROLOGICAL ASSOCIATION EDUCATION AND RESEARCH, INC.
Purpose: The objectives of this study were to 1) describe the patterns of repeat
prostate biopsy in men with a previous negative biopsy and 2) identify predictors
of prostate cancer diagnosis on repeat biopsy in these men.
Materials and Methods: From a university faculty group practice we identified
1,837 men who underwent prostate biopsy between January 1, 1995 and January
1, 2010. Characteristics of repeat biopsy were examined, including the indication
for biopsy, the number of repeat biopsies performed, the number of cores ob-
tained and total prostate specific antigen before biopsy. Features of prostate
cancer diagnosed on repeat biopsy were examined, including Gleason score,
number of positive cores, percent of tumor and treatment choice. Multivariable
logistic regression was done to identify prostate cancer predictors.
Results: Initial biopsy was negative in 1,213 men. In 255 men a total of 798
repeat biopsies were performed. Of the 63 men diagnosed with prostate cancer
Gleason score was 6 or less in 33 (52%), 7 in 22 (35%) and 8e9 in 8 (13%). When
categorized by Epstein criteria, the rate of clinically insignificant cancer diag-
nosis decreased substantially by the third and fourth repeat biopsies. Repeat
biopsy in men older than 70 years, biopsies including more than 20 cores and the
fourth repeat biopsy were associated with an increased likelihood of prostate
cancer diagnosis.
Conclusions: In men selected for multiple repeat biopsies clinically significant
cancer is found at each sampling round. Given the continued likelihood of cancer
detection even by the fifth biopsy, early consideration of saturation or image
guided biopsy may be warranted in the repeat biopsy population.
Key Words: prostate, prostatic neoplasms, biopsy,
magnetic resonance imaging, diagnosis
CONTEMPORARY systematic biopsy Previous studies show a decrease in
technique relies on sampling effi- the CaP diagnosis rate with each
ciency for cancer detection. As such, repeat biopsy whether using serial
the risk of missing cancer on initial sextant biopsy3,4 or extended core
prostate biopsy due to sampling error sampling.5
is substantial, often resulting in the Currently with the exception of
need for repeat biopsy upon continued men found to have ASAP on initial
suspicion of CaP. While sampling ef- biopsy there is no clear consensus on
ficiency can be improved by increased the indications or techniques of
sampling, the cancer detection rate repeat biopsy. Urologists typically
on repeat biopsy varies highly.1,2 rely on clinical judgment to determine
http://dx.doi.org/10.1016/j.juro.2014.10.084
Vol. 193, 1178-1184, April 2015
Printed in U.S.A.
 PATTERNS OF REPEAT PROSTATE BIOPSY IN CONTEMPORARY PRACTICE
the need for repeat sampling and on personal pref-
erence to determine the biopsy approach. Collec-
tively the variable cancer detection rate of repeat
biopsy and the absence of clear guidelines on in-
dications lead to the potential for excessive repeat
biopsies, subsequently escalating biopsy related
complications and cost.
We performed this study to evaluate the fre-
quency, indications and outcomes of repeat prostate
biopsy in a single institution, academic urologi-
cal practice.
MATERIALS AND METHODS
After receiving local institutional review board approval
we queried the billing records of a single university fac-
ulty group practice to identify men with no previous
diagnosis of CaP who underwent prostate biopsy between
January 1, 1995 and January 1, 2010. Cases after 2010
were excluded from analysis after integrating MRI guided
strategies for prostate biopsy into our institutional clinical
practice algorithms. Men were identified by the ICD-9
code 55700 in the billing database. At the time that
ICD-9 code 185 was added to the record men were docu-
mented as diagnosed with CaP and, thus, excluded from
additional analysis. Of men with an initial negative bi-
opsy those without a subsequent 55700 code were
assumed not to have undergone additional biopsy and
were also excluded.
Clinical characteristics at repeat biopsy were exam-
ined, including biopsy indication, total PSA, PSA density
and PSA velocity before biopsy. Biopsy characteristics
were also recorded, including number of repeat biopsies
performed, interval between biopsies and number of cores
obtained. Features of CaP diagnosed on repeat biopsy
Figure 1.
1179
were investigated, including GS, number of positive cores,
percent of tumor involvement, treatment choice and
radical prostatectomy pathology if the patient was treated
with surgery.
We used multivariable logistic regression to identify
factors associated with CaP detection. The primary
dependent variable was CaP diagnosis. Covariates
potentially associated with the CaP diagnosis included
age at biopsy, reason for biopsy, TRUS volume, prebiopsy
PSA, number of previous biopsies and total number of
biopsy cores. Analysis was done with StataÒ 11.0. All
hypotheses were 2-tailed and the critical a level was 0.05.
RESULTS
During the study period 1,837 men underwent a
total of 2,430 prostate biopsies. Initial biopsy was
negative in 1,213 men. The treating urologist
selected 255 men for repeat biopsy, in whom a total
of 798 biopsies were performed during the study
period (fig. 1). The remaining 958 men with nega-
tive biopsy were believed to have no clinical indi-
cation for rebiopsy or they did not return for
followup care. Of 255 men selected for rebiopsy
140 (55%) underwent 2 or more repeat biopsies,
including 5 or more in 18 (6.3%) (table 1).
Prebiopsy PSA was 4 or less, 4.1 to 10 and greater
than 10 ng/ml in 126 (16%), 443 (56%) and 151
biopsies (19%), respectively (table 1). Most repeat
biopsies involved extended sampling (12 or more
cores), including 107 (42%), 68 (50%), 50 (63%) and
24 (65%) on biopsies 2, 3, 4 and 5, respectively.
The most common indication for biopsy in the
repeat biopsy population was increasing/increased
1180 PATTERNS OF REPEAT PROSTATE BIOPSY IN CONTEMPORARY PRACTICE

Table 1. Rebiopsy characteristics diagnosis. Most repeat biopsies performed due to

No./Total No. (%) increasing/increased PSA (226 of 290 or 77.9%),
HGPIN (85 of 118 or 72.0%) and PSA plus HGPIN
No. rebiopsies (255 pts): 798
1 115 (45.1)
(45 of 55 or 81.8%) were done 12 months or longer
2 59 (23.9) after the prior biopsy (fig. 3).
3 35 (13.7) CaP was found in 63 repeat biopsies (8%), HGPIN
4 28 (11.0)
5 of Greater 18 (6.3)
was found in 140 (18%) and ASAP was found in 50
Biopsy reason: 798 (6%). A decreasing CaP diagnosis rate was observed
Increasing/increased PSA 508 (63.6) on serial repeat biopsy. The detection rate was 25 of
HGPIN 118 (14.8)
Increasing/increased PSA þ HGPIN 55 (6.9)
250 (10%), 15 of 137 (11%), 8 of 80 (10%) and 11 of 44
ASAP 45 (5.6) diagnoses (25%) on repeat biopsies 1, 2, 3, 4 and 5,
Abnormal DRE 20 (2.5) respectively (fig. 1). Five men were diagnosed with
Missing 52 (6.5)
Pts diagnosed with CaP 63 (24.8)
CaP on repeat biopsy 5 or greater.
Ca pos biopsies by biopsy reason: Of men diagnosed with CaP on repeat biopsy 33
Increasing/increased PSA 32/508 (6.3) (52%), 22 (35%) and 8 (13%) were diagnosed with GS
HGPIN 9/118 (7.6)
Increasing/increased þ HGPIN 11/55 (20)
6 or less, 7 and 8e9 disease, respectively (table 2).
ASAP 9/45 (20) Only 1 core was positive in 30 biopsies (48%). Total
Abnormal DRE 0/20 tumor involvement was 5% or less in 37 biopsies
Missing 2/52 (3.8)
Greater than 12 cores (biopsy No.):
(59%). When categorized into clinically insignificant
1 23/250 (9.2) cancer by Epstein criteria (PSA density less than
2 107/250 (42.8) 0.15 ng/ml, GS 6 or less, 2 or fewer positive cores
3 68/137 (49.6)
4 50/80 (62.5)
and 50% or less involvement in a single core) and
5 24/44 (54.5) UCSF-CAPRA (score 2 or greater based on age, PSA
Prebiopsy PSA (ng/ml): at diagnosis, GS, clinical stage and percent of biopsy
0e4 ng/ml 126 (15.8)
Greater than 4e10 443 (55.5)
core involved with cancer),6 the rate of clinically
Greater than 10 151 (18.9) insignificant cancer diagnosis decreased substan-
Missing 78 (9.8) tially by the third and fourth rebiopsies (fig. 1).
Surgery was performed in 20 men diagnosed with
CaP. In 6 of these men (30%) tumor volume was 5%
or less (table 3). GS was 6 in 9 patients (45%), 7 in
PSA (508 biopsies or 64%) followed by HGPIN (118 10 (50%) and 8 in 1 (5%).
or 15%), combined increasing/increased PSA and Multivariable analysis revealed that CaP was
HGPIN history (55 or 7%), ASAP (45 or 6%) and significantly more likely to be diagnosed in men
abnormal DRE (20 or 3%) (fig. 2). Median time to older than 70 years, biopsies including 20 cores or
repeat biopsy was 12.8 months (IQR 0e32.4). Of the more and on repeat biopsy 4 (table 4). CaP was
45 rebiopsies performed after ASAP was identified significantly less likely to be identified in biopsies of
33 (73.3%) were done within 6 months of the initial a prostate with a TRUS volume of greater than 50 cc.

Figure 2. Indication for 798 biopsies. Red bars indicate CaP. Blue
bars indicate no CaP. Figure 3. Time to repeat biopsy by indication
 PATTERNS OF REPEAT PROSTATE BIOPSY IN CONTEMPORARY PRACTICE 1181

Table 2. CaP features diagnosed on 63 rebiopsies Table 4. Multivariable analysis of CaP detection predictors

No. (%) OR (95% CI)

Clinical stage: Age at biopsy (vs 40e60):
T1c 40 (63.5) 61e70 1.41 (0.65e3.06)
T2a 6 (9.5) Greater than 70 5.62 (2.52e12.5)*
Missing 17 (27.0) No. previous biopsies (vs 1):
GS: 2 0.80 (0.37 e1.72)
6 or Less 33 (52.4) 3 1.04 (0.41e2.64)
7 22 (34.9) 4 2.98 (1.13e7.82)*
8e9 8 (12.6) 5 or Greater 1.46 (0.44e4.86)
No. pos cores: Biopsy reason (vs increasing/increased PSA):
1 30 (47.6) ASAP 1.77 (0.68e4.66)
2 15 (23.8) HGPIN 0.54 (0.21e1.37)
3 or Greater 16 (25.4) PSA þ HGPIN 1.78 (0.76e4.14)
Missing 2 (3.2) Prebiopsy ng/ml PSA (vs less than 4):
% CaP cores: 4e10 1.52 (0.52e4.41)
5 or Less 37 (58.7) Greater than 10 1.19 (0.34e4.19)
10 12 (19.1) TRUS cc vol (vs less than 30):
Greater than 10 14 (22.2) 31e49 0.78 (0.31e1.95)
Max % CaP/1 core: 50 or Greater 0.25 (0.09e0.73)*
5 or Less 21 (33.0) No. biopsy cores (vs 12 or less):
6e50 24 (38.1) 13e20 1.72 (0.89e3.30)
Greater than 50 15 (23.8) Greater than 20 3.77 (1.46e9.73)*
Missing 3 (4.7)
CaP laterality: * p <0.05.
Unilat 53 (84.1)
Bilat 10 (15.9)
No. prediagnosis rebiopsies:
best indication for repeat biopsy.7 When biopsy is
1 25 (39.7) repeated, a minimum of 14 cores should be obtained,
2 15 (23.8) including 12 lateral cores and 2 anterior apical
3 8 (12.7)
4 or Greater 15 (23.8)
cores. If cancer is not diagnosed on repeat biopsy
CaP treatment: and suspicion persists, saturation biopsy should
Radical retropubic prostatectomy 20 (31.7) be performed.
External radiotherapy/brachytherapy 17 (27.0)
Active surveillance 6 (9.5)
Terris described indications for repeat biopsy as
High intensity focused ultrasound 2 (3.2) 1) a change in PSA, 2) HGPIN and 3) ASAP.8 In
Watchful waiting 2 (3.2) regard to the PSA change a value of greater than
Unknown 16 (25.4)
10 ng/ml was believed to be an indication for repeat
biopsy. However, in men with PSA 4 to 10 ng/ml
additional parameters would suggest repeat biopsy,
DISCUSSION including percent free PSA less than 25%, PSA
Clinicians have yet to find the balance between density greater than 0.15 ng/ml/cm3 and PSA ve-
avoiding the morbidity of repetitive prostate biopsy locity greater than 0.75 ng/ml per year. The rate of
while still identifying clinically significant CaP in cancer diagnosis on repeat biopsy after identifying
men with an initial negative prostate biopsy and HGPIN was 23% and, thus, immediate rebiopsy was
persistent suspicion for CaP. Recommendations on probably not necessary. On the other hand, a cancer
when to repeat prostate biopsy have been reported diagnosis rate after identifying ASAP of 40% to 50%
in the literature. Presti recommended repeat biopsy justifies immediate repeat biopsy. Terris recom-
if initial sampling was inadequate (ie sextant mended that in patients with high suspicion for
biopsy) using a low free-to-total PSA ratio as the cancer biopsy should be repeated within 2 to 6
weeks but those not at high risk can undergo biopsy
Table 3. CaP features in 20 prostatectomy specimens in 3 to 6 months. Biopsy should include 14 cores. If
No. 1 No. Greater Than 1 repeat biopsy is still negative, additional biopsy
Rebiopsy (%) Rebiopsy (%) should include 4 to 6 transition zone biopsies or a
GS: 7 13 saturation technique.
6 2 (28.6) 7 (53.8) The NCCN (National Comprehensive Cancer
7 5 (71.4) 5 (38.5) NetworkÒ) recommends followup based on PSA and
8 0 1 (7.7)
% Tumor vol: DRE findings if initial biopsy is negative with the
5 or Less 2 (28.6) 4 (30.8) decision to repeat biopsy individualized based on
10 2 (28.6) 3 (23.1) risk stratification factors and/or biomarkers such as
Greater than 10 2 (28.6) 5 (38.5)
Missing 1 (14.3) 1 (7.7) PCA3 and percent free PSA, which may improve
Pathological stage: specificity.9 Men with ASAP should undergo
T2 5 (71.4) 9 (69.2) extended pattern rebiopsy within 3 to 6 months
T3 2 (28.6) 4 (30.8)
and men with HGPIN should be considered for
1182 PATTERNS OF REPEAT PROSTATE BIOPSY IN CONTEMPORARY PRACTICE
rebiopsy at 6 months. New commercially available
serum biomarkers, including the PHI (Prostate
Health Index)10 and the 4-kallikrein panel,11 may
further refine the decision for repeat biopsy in the
future.
In this retrospective cohort study the practice
patterns of multiple providers in a university
faculty group practice were generally in line with
recommendations in the literature. Of biopsies done
due to ASAP 78% were performed within 6 months.
Of biopsies performed due to HGPIN 46% were done
after 1 to 3 years with 26% done after more than
3 years. Repeat biopsies usually involved extended
sampling with about 50% or more of rebiopsies
including more than 12 cores. Of biopsies 82% were
performed at a prebiopsy PSA of 4 ng/ml or higher.
Notably men chosen to undergo repeat biopsy
continued to undergo multiple biopsies, that is 29%
of this cohort underwent 4 or more biopsies.
The CaP diagnosis rate generally decreases with
repeat biopsies, as reported by Roehl et al.12 In that
series 34% of men were diagnosed with cancer on
initial biopsy, followed by 10% on biopsies 2, 3 and 4.
Prior research showed that CaP diagnosed on
repeat biopsy is often of lower grade, stage and
volume.5,13e16 Keetch et al reported a 34% CaP
diagnosis rate on biopsy 1 followed by 19%, 8% and
7% on biopsies 2, 3 and 4, respectively.3 In the Eu-
ropean Prostate Cancer Detection Study the CaP
diagnosis rate was 22%, 10%, 5% and 4% on biopsies
1, 2, 3 and 4, respectively.4 The diagnosis rate
increased to 30% to 34% when rebiopsy was per-
formed with a saturation technique (14 to
45 cores).2,17 However, the initial biopsy technique
used in these studies was sextant sampling so that
many cancers were likely missed due to inadequate
initial sampling.
More contemporary series using extended initial
biopsy sampling showed higher cancer detection
rates. The CaP diagnosis rate was 57%, 23% and
21% on the initial, second and third or more pros-
tate biopsies.5 Likewise our study differs from the
observations of the REDUCE (Reduction by Dutas-
teride of Prostate Cancer Events), in which the
cancer detection rate was higher on repeat biopsy.18
We suspect that this relates to the inclusion of men
with 6-core as well as 12-core sampling (mean 8.8)
on initial biopsy in REDUCE compared to our study,
in which almost all men underwent a minimum
12-core sample.
About 50% of men diagnosed with CaP in this
cohort had GS 6 or less cancer, 5% or less tumor
involvement of cores and only 1 positive core.
However, when categorized as low risk cancer based
on the UCSF-CAPRA score, the rate of low risk
cancer diagnosis decreased with each consecutive
biopsy. In fact, 12.6% of the repeat biopsy cohort
was diagnosed with GS 8 or 9 disease. On multi-
variable analysis the CaP diagnosis rate was higher
on the fourth repeat biopsy. This trend likely did not
persist for the fifth or more rebiopsy due to small
numbers. More than 20 biopsy cores was associated
with a higher likelihood of a CaP diagnosis. These
findings show that increased sampling leads to
increased identification of CaP.
The implications of these findings are twofold. 1)
High risk CaP is still diagnosed, thus, warranting
repeat biopsy. Tan et al similarly found that 14% of
men diagnosed with CaP after 2 more prior biopsies
had GS 8e10 disease.5 The likelihood of finding
high grade disease missed on initial biopsy likely
relates to the quality of sampling on initial biopsy.
2) When performing repeat biopsy, a clear risk is the
detection of clinically insignificant or indolent can-
cer. Increased sampling through repetitive biopsy
likely increases this risk. Balancing the risk of
missed clinically significant cancer against the risk
of finding clinically insignificant cancer is the
greatest challenge of repeat biopsy.
A fundamental problem of repeat biopsy tech-
nique is the use of techniques similar to those of the
initial biopsy. This risks missing cancer in regions
outside the template. Adopting early saturation bi-
opsy in the setting of a negative first biopsy may
preclude the need for multiple repeat biopsies. In
this study men chosen for repeat biopsy subse-
quently underwent multiple repeat biopsies. Nine
men underwent as many as 7 biopsies each.
Taira et al used transperineal template guided
mapping biopsy on initial and repeat biopsy, and
diagnosed CaP at a rate of 75.9%, 55.5%, 41.7% and
34.4% on the first, second, third and fourth biopsy,
respectively.19 The CaP diagnosis rates on repeat
biopsy are lower but still substantial. Using satu-
ration biopsy on the first repeat biopsy CaP may be
diagnosed earlier because of improved sampling but
the risk of clinically insignificant cancer detection is
not decreased. Likewise a number of serum
markers, including PCA3, PHI,10 free PSA and the
4-kallekrein score,11 could be used to select men
who would benefit from rebiopsy. While such tests
are believed to predict cancer, use must be combined
with refined methods of biopsy to maximize the
likelihood of cancer detection.
MRI of the prostate is a rapidly emerging,
noninvasive imaging modality that can accurately
identify CaP foci in the gland and facilitate targeted
sampling of disease in the initial and repeat biopsy
populations.20 Target lesions are identified by mp-
MRI, which is an integration of anatomical and
functional MRI sequences including T2-weighted,
diffusion weighted and dynamic contrast enhanced
images.21 Targeted biopsy using mp-MRI demon-
strated increased rates of clinically significant and
 PATTERNS OF REPEAT PROSTATE BIOPSY IN CONTEMPORARY PRACTICE 1183

overall cancer detection in patients with at least
1 prior negative biopsy22e24 as well as an increased
cancer detection rate in patients with up to 4 pre-
vious negative biopsies.25 Also, mpMRI before
biopsy allows for increased detection of tumors in
the anterior prostate, which can be missed on
standard TRUS guided biopsy.26 Negative mpMRI
has a negative predictive value of up to 85% and
95% for 0.2 and 0.5 cc tumor foci, respectively.27
Platforms for computer assisted MRI-ultrasound
fusion have further improved the ability to accu-
rately biopsy suspicious lesions identified on
mpMRI and reveal an increased percent of cancer
detected per core compared to systematic biopsy.28
Given the selective ability of mpMRI to identify
clinically significant disease, MRI targeted biopsy
may be a means to decrease the need for multiple
repeat biopsies. However, the significant added
costs of multisequence MRI and the operation of a
real-time MRI-ultrasound fusion platform must be
considered when evaluating the overall usefulness
of an imaging targeted approach. Ultimately the
indications for mpMRI and its use in conjunction
with serum biomarkers and genetic methods of
candidate selection must be further evaluated.
Our study has several strengths. This was a large
cohort of men who underwent mostly 12-core repeat
biopsy, unlike most of the earlier literature, which
examined the outcomes of repeat sextant biopsy. It
is now widely agreed on that sextant biopsy is
inadequate to sample the prostate. The biopsy pat-
terns of multiple providers in a group practice were
examined, making our results more representative
of general practice.
Study limitations include its retrospective nature
and the potential for institutional bias in the selec-
tion of repeat biopsy candidates. The reasons why
men with an initial negative biopsy did not subse-
quently undergo repeat biopsy are unknown. Finally,
some men may have been referred to our institution
after undergoing prior prostate biopsies. Thus, the
number of repeat biopsies may be underestimated.
CONCLUSIONS
Men selected for repeat biopsy due to clinical sus-
picion often undergo multiple repeat biopsies. In our
study selection for repeat biopsy indicated a 1:3
likelihood of 3 repeat biopsies and a 1:7 likelihood of
4 repeat biopsies. Clinically significant cancer was
identified at each successive biopsy round. Given
the continued likelihood of cancer detection even by
biopsy 5, early consideration of saturation tech-
niques or MRI guided targeted biopsy may improve
sampling efficiency and obviate the need for multi-
ple repeat biopsies.

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