Yonago Acta medica 2014;57:53–58

Original Article

The Efficacy of Target Biopsy of Suspected Cancer Lesions Detected by Magnetic
Resonance Imaging and/or Transrectal Ultrasonography during Initial Prostate
Biopsies: Comparison of Outcomes between Two Physicians
Hideto Iwamoto, Tetsuya Yumioka, Noriya Yamaguchi, Seiya Inoue, Toshihiko Masago, Shuichi Morizane, Akihisa
Yao, Masashi Honda, Takehiro Sejima and Atsushi Takenaka
Division of Urology, Department of Surgery, School of Medicine, Tottori University Faculty of Medicine, Yonago, Tottori 683-8504, Japan

ABSTRACTThe efficacy of adding target prostatebiopsy (PBx) of suspected cancer lesions identified onmagnetic resonance imaging (MRI) and/or transrectal
ultrasonography (TRUS) to initial systematic PBx was
evaluated. Moreover, the outcomes were compared between 2 physicians.
Methods We retrospectively investigated 238 patients who underwent first-time PBx in our hospital.
All patients were examined with prostate MRI before
PBx. Fourteen systematic biopsies were obtained in all
patients. When a suspected lesion was present on MRI
and/or TRUS, the lesion was the target of target PBx.
Results The overall detection rate of prostate cancer(PCa) was 45% (106/238). With target PBx, the PCa
detection rate was 32% overall, while that of suspectedlesions seen only on MRI was 32%, that of suspected lesions seen only on TRUS was 8% and that of suspectedlesions seen on both MRI and TRUS was 52%. The
same tendency was shown for each physician. Comparing systematic PBx and target PBx, the overall rate ofGleason score (GS) upgrading with target PBx was 13%.
The rate of PCa detected only by systematic PBx was
95%. There was no significant difference between the 2physicians.
Conclusion In initial PBx, the addition of target PBxof suspected cancer lesions detected by MRI and/or
TRUS to systematic PBx might not be useful to improvethe cancer detection rate. However, it may enable moreaccurate risk classification and detection of minute cancers with a high GS.

prove this situation. However, no dramatic improvementof the cancer detection rate has been achieved. Accordingly, the best methodology for PBx remains controversial.
On the other hand, progress in imaging modalities,
for example magnetic resonance imaging (MRI) andtransrectal ultrasonography (TRUS), has been remarkable in recent years. MRI has developed particularly
rapidly in the past 20 years, along with the managementof localized PCa. A high diagnostic accuracy has beenreported using various groups of patients and protocols.
Many reports have suggested that the rate of PCa detection was improved by combining MRI findings with a
PBx.3–6 However, there are also reports that deny theusefulness of MRI in PBx.7, 8 Currently, as the methodology of PBx has progressed, the detection rate of the
MRI/US fusion biopsy system has been reported.9, 10
However, since such systems are very expensive, at the
moment, use of this approach has not become widespread.
Although past studies have focused on methodologies of PBx, to the best of our knowledge, no papers
have examined the difference in outcomes with different operators who performed the PBx using the same
methodology and instrument. Therefore, the aim wasto evaluate the efficacy of the addition of target PBx ofsuspected cancer lesions detected by MRI and/or TRUS
to a systematic, 14-core, transrectal ultrasound-guided
PBx. Moreover, the outcomes of the PBx performed by 2
physicians who used the same methodology and instruments were compared.

Key words

MATERIALS AND METHODS

Backgroundmagnetic resonance image; prostate cancer; target prostate biopsy; transrectal ultrasonography

Patients

This study was approved by the Ethics Committee of
Tottori University, Japan, and all patients provided their

The pathological diagnosis of prostate cancer (PCa) isbased on the use of ultrasonography-guided prostatebiopsy (PBx). Based on recent systematic reviews, 10
to 12 cores are generally taken because they show better efficacy for cancer detection than 6 cores.1 However,the cancer detection rate of PBx has traditionally been
fraught with poor sensitivity, around 50%.2 Many methodologies, techniques and approaches are used to im-

Corresponding author: Hideto Iwamoto
gakkoura@med.tottori-u.ac.jp
Received 2013 December 9
Accepted 2014 January 6
Abbreviations: ADC, apparent diffusion coefficient; DWI, diffusion-weighted imaging; GS, Gleason score; MRI, magnetic resonance imaging; PBx, prostate biopsy; PCa, prostate cancer; PSA,
prostate-specific antigen; PSAD, PSA density; TRUS, transrectal
ultrasound53

H. Iwamoto et al.

written, informed consent. A total of 333 patients withelevated prostate-specific antigen (PSA) who underwent
first-time PBx at the Department of Urology, Tottori
University Hospital, between November 2010 and February 2013, were retrospectively investigated. Patients
whose PSA level was less than 4 ng/mL or more than 30
ng/mL and who underwent 1 or more previous PBx procedures were excluded. Thus, 238 patients were includedin the final analysis. All patients were examined withprostate MRI before undergoing PBx. All PBx procedures were performed within 4 weeks after MRI.

Fig. 1. Transrectal prostate biopsy was performed as follows.
Fourteen systematic biopsies (8, peripheral zone; 4, transitionalzone; 2, apex) were obtained in all patients. When a suspected lesion was present on MRI and/or TRUS, it was targeted for biopsy,
in addition to the systematic biopsy. MRI, magnetic resonance image; TRUS, transrectal ultrasound.

MRI protocol

In our hospital, we used a 1.5-T (Achieva, Philips
Healthcare, Best, Netherlands) or a 3.0-T (MAGNETOM
skyra, Siemens, Munich, Germany) magnetic resonance imaging (MRI) system. All patients underwent
diffusion-weighted imaging (DWI), apparent diffusion
coefficient (ADC) mapping and dynamic imaging, inaddition to the imaging sequences as part of a routine
prostate MRI protocol. T2-weighted images (T2WI)
were acquired in 3 orthogonal planes (axial, sagittal andcoronal). All images were reviewed by radiologists blindto the PSA data. Lesions were defined as suspectedcancer lesions on MRI if 2 or more of the following 4
findings were present: i) low-intensity on T2WI; ii) highintensity on DWI; iii) low-intensity on the ADC map
and iv) enhancement in the early phase but washed out
on dynamic imaging.

pected cancer lesion on TRUS was left to each operator’s
discretion. Fourteen systematic biopsies (8, peripheral
zone; 4, transitional zone; 2, apex) were obtained in all
patients. The systematic biopsy was performed independently of the location of the suspected lesion on MRI
and/or TRUS. When a suspected lesion was present on
MRI and/or TRUS, that lesion was made a target PBx in
addition to the systematic biopsy. If the suspected lesion
on MRI could not be identified on TRUS, the target PBx
was performed using only anatomical landmarks (shapeof the prostate, position of the verumontanum, distancefrom the apex or the prostate base, presence of a benign
cyst or calcification nearby, etc.). In target PBx, on principle, 1 core was taken from 1 suspected lesion (Fig. 1).

Transrectal PBx protocol

Statistical analyses

All biopsies were obtained under TRUS guidance using
a medical ultrasonography scanner (Nemio XG, Toshiba, Tokyo, Japan). PBx was performed by 2 physicians,
Physician X, a urologist in his 6th year, and Physician Y,a urologist in his 5th year, using the same methodology
and instruments, under caudal anesthesia with an 18-G
biopsy needle (BARD Max-Core Disposable Core Biopsy Instrument, Tempe, AZ). Lesions were defined assuspected cancer lesions on TRUS if low-echoic lesions
were identified by the operators. The judgment of a sus-

All statistical analyses were performed using PASW
statistics 18 (SPSS, Chicago, IL). Statistical analysis was
performed with the chi-square test for continuous variables. Fisher’s exact test was used to compare categorical variables. P-values of less than 0.05 were consideredsignificant.
RESULTS
Patients’ characteristics

The characteristics of the patients in each physician’s

Table 1. Patients’ characteristics
		
Patients characteristics
OverallComparison between 2 physicians
Physician X
Physician Y

P value

Number of patients
Age, mean [range], year
PSA, mean [range], ng/mL
Prostate volume, mean [range], mL
PSAD, mean [range], ng/mL/mL
Number of patients with target PBx (%)

137		
69.6 [42–86]
9.03 [3.27–24.63]
45.6 [14–231]
0.23 [0.04–0.83]
104 (76%)

0.40
0.12
0.84
0.26
0.29

238		
69.2 [39–93]
9.60 [3.27–29.63]
45.8 [14–231]
0.25 [0.04–1.34]
188 (79%)

PBx, prostate biopsy; PSA, prostate-specific antigen; PSAD, PSA density.

54

101
68.5 [39–93]
10.57 [3.48–29.63]
46.3 [14–158]
0.28 [0.07–1.34]
84 (83%)

The efficacy of target prostate biopsy
Table 2. The overall PBx outcome including both patients with and without target PBx
		PCa detection ratio
OverallComparison between 2 physicians
Physician X
Physician Y

P value

Number of patients
PCa (%)
Low GS (%)
Moderate GS (%)
High GS (%)
PCa with MRI suspicion (%)
PCa with TRUS suspicion (%)

137
55/137 (40%)
10/ 55 (19%)
21/ 55 (38%)
24/ 55 (43%)
43/ 76 (57%)
39/ 95 (41%)

–
0.11
0.62
0.65
0.88
0.91
0.02*

238
106/ 238 (45%)
21/ 106 (20%)
36/ 106 (37%)
47/ 106 (43%)
89/ 155 (58%)
66/ 138 (48%)

101
51/101 (50%)
11/ 51 (22%)
17/ 51 (34%)
23/ 51 (44%)
46/ 79 (58%)
27/ 43 (62%)

GS, Gleason score; MRI, magnetic resonance imaging; PBx, prostate biopsy; PCa, prostate cancer; TRUS, transrectal ultrasonography.
Table 3. The cancer detection rate of target PBx by imaging modality
		Image modality in target PBx
OverallComparison between 2 physicians
Physician X
Physician Y

P value

Number of patients (%)
Total (%)
Only on MRI (%)
Only on TRUS (%)
On both MRI and TRUS (%)

104/137 (76%)
27/104 (26%)
4/ 17 (24%)
3/ 50 (6%)
22/ 51 (43%)

–
0.04*
0.42
0.39
0.001**

188/ 238 (79%)
61/ 188 (32%)
23/ 73 (32%)
6/ 76 (8%)
38/ 73 (52%)

84/101 (83%)
34/ 84 (40%)
19/ 56 (34%)
3/ 26 (11%)
16/ 22 (73%)

MRI, magnetic resonance imaging; PBx, prostate biopsy; TRUS, transrectal ultrasonography.

group are summarized in Table 1. Physician X’s grouphad 137 patients, and Physician Y’s group had 101 patients. The baseline characteristics of the patients in eachgroup showed no significant differences in age, PSA levels, prostate volume, PSA density (PSAD) and the rateof patients with target PBx.

with suspected lesions on imaging modalities. Especiallyin patients with suspected lesions on MRI, the increasein the cancer detection rate was the highest in all groups,
approximately 60%. However, the cancer detection rateof patients with a suspected lesion on TRUS was lower
and showed a significant difference between the 2 physician groups (P = 0.02).

The overall PBx outcome

The overall outcomes of PBx are presented in Table 2.
The overall detection rate of PCa including both patientswith and without target PBx was 45% (106/238), and
43% (47/106) of PCa patients was diagnosed as having
a high Gleason score (GS) (4 + 4 = 8 or more). There
were no significant differences between the 2 physician groups. The overall detection rate in patients withsuspected lesions on MRI was 58% (89/155), while thaton TRUS was 48% (66/138). (This was not related towhether PCa was identified with the target PBx.) In allgroups, the cancer detection rate was higher in patients

Target PBx outcome

The outcomes of target PBx are presented in Table 3.
Of a total of 238 patients, 188 (79%) underwent target
PBx. The overall detection rate of PCa with target PBx
was 32% (61/188). If the overall detection rate for each
imaging modalities was compared, that of patients witha suspected lesion only on MRI was 32% (23/73), that ofpatients with a suspected lesion only on TRUS was 8%(6/76) and that of patients with a suspected lesion seen
on both MRI and TRUS was 52% (38/73). However, if
more than 1 suspected lesion were found in a prostate,
they were counted respectively. The detecTable 4. The rate of GS upgrading by the addition of target PBx totion rate was highest if the suspected lesion
systematic PBx
appeared on both MRI and TRUS, while that		
Comparison between 2 physiciansof a lesion seen only on TRUS was the lowOverall Physician X Physician Y P value
est. As for the outcome in each physician’sgroup, the same overall tendency was seen.
GS upgraded in target PBx
8 / 612 / 276 / 34
0.22
(%)
(13%)
(7%)
(17%)
However, the total detection rate of target
3		
1		
2		
–
Low Moderate GS
PBx (P = 0.04) and the detection rate with
0		
0		
0		
–
Moderate High GS
a suspected lesion seen on both MRI and
2		
1		
1		
–
0 Moderate GS
TRUS (P = 0.001) were significantly different
3		
0		
3		
–
0 High GS
between the physician groups.
GS, Gleason score; PBx, prostate biopsy.

55

H. Iwamoto et al.

Fig. 2. The detection rate was investigated according to the site from which PCa was detected. The overall rate of PCa detected only bysystematic PBx, which therefore did not need target PBx, was 95%. Furthermore, PCa was also detected from one lobe contralateral tothe other with a suspected cancer lesion on MRI or TRUS in approximately 20% of patients (18/89). PBx, prostate biopsy; PCa, prostatecancer; MRI, magnetic resonance imaging; TRUS, transrectal ultrasonography.

Comparison of systematic PBx and target PBx

the physicians’ groups.
Interestingly enough, in the 89 PCa patients withtarget PBx (Fig. 2; B + C + D), PCa was detected also
in one lobe contralateral to the other lobe that had a suspected cancer lesion on MRI or TRUS in approximately
20% (18/89). Of the 18 patients, 5 (28%) were diagnosed
with high GS (4 + 4 = 8 or more), and in 3 of the 5 patients, target PBx did not detect PCa.

In the cases in which PCa was detected by both systematic PBx and target PBx, the overall rate of GS upgrading with target PBx as compared with systematic PBx
was 13%. There was no significant difference between
the 2 physicians’ groups. Interestingly, in some cases
PCa was detected only by target PBx but not by systematic PBx, including PCa with a high GS (4 + 4 = 8 ormore) (Table 4).
Furthermore, the detection rate was investigated according to the site at which PCa was detected (Fig. 2).
The rate of PCa detection with only systematic PBx,
which did not need target PBx to detect PCa, was 95%
on the whole, 98% in physician X’s group and 92% inphysician Y’s group (Fig. 2; A + B + C). There was no
significant difference between the 2 physicians’ groups.
However, the detection rate of PCa which was detectable
only by a target PBx was significantly different between

DISCUSSION
Urologists have been continuing to explore the optimal
methodologies to improve the detection rate of PCa with
PBx. The addition of anterior directed biopsy cores,11
saturation biopsy templates12, 13 and transperineal template-guided biopsy14 has been attempted. Although allof these methodologies added some diagnostic usefulness, some reports denied the usefulness of these methodologies. The reason the PCa detection rate does not
56

The efficacy of target prostate biopsy

improve dramatically is probably related to the fact thatthese methodologies ultimately remain dependent on
random sampling.
On the other hand, the MRI/US fusion PBx system
has appeared as a more advanced method of PBx. Pint
et al. reported that PCa was detected in 12 of 43 (27.9%),
26 of 39 (66.7%) and 17 of 19 (89.5%) patients with low,
moderate and high suspicion on MRI, respectively. Theysuggested that their methodology might be useful in focal therapy for PCa.9 Moreover, they reported in theircurrent study that the diagnostic yield of MRI/US fusion
PBx was not affected by the increased number of priornegative PBx procedures, especially for the detectionof high-grade PCa.10 Certainly, their outcome of fusion
PBx exceeded that of the past methodology. However,this system is not likely to immediately spread worldwide because the system is very expensive, and focal
therapy is not standard therapy worldwide. Therefore,
the methodology adopted in the present study was themost common and economical, since it uses the mostwidely available imaging modalities, TRUS and MRI.
In the present study, the overall detection rate ofPCa, including both patients with and without target
PBx, was almost equivalent to past studies. In patientswith a suspected lesion on the imaging modalities,
especially MRI, there was a tendency for the rate ofcancer detection to be higher. However, the detection
rate of patients with a suspected lesion on TRUS wassignificantly different between the 2 physician groups.
This was thought to be due to variation in judging theimaging findings on TRUS between the 2 physicians.
Evaluated exclusively on the outcome of target PBx, theoverall rate of cancer detection (32%) was not as high as
we had expected; the cancer detection rate of target PBxof a suspected lesion seen only on TRUS was very low(8%). This suggests that the evaluation of imaging findings on TRUS was poorly reproducible. Interestingly, thecancer detection rate of target PBx of a suspected lesion
on both MRI and TRUS was increased in all groups,
and that of Physician Y’s group was higher (73%). However, there was a significant difference between the 2physician groups, likely due to the difference in the hit
probability to the suspected lesion in target PBx between
the 2 physicians and the small number of patients inthis study. Comparing the outcomes of systematic PBx
and target PBx, the GS was upgraded in 13% of cancer
patients; thus, more accurate risk classification was obtained in approximately 1 in 10 patients by performing atarget PBx. It was found that minute cancer with a highGS, which was detectable only by a target PBx, was notuncommon. Furthermore, in the evaluation according to
the site from which PCa was detected, since 95% of theoverall patients in whom PCa was detected did not needtarget PBx, it must be said that target PBx was not usefulin terms of improvement of cancer detection. Shigemura
et al.7 reported that, by using the PBx methodology asin the present study, only 1 of the 96 patients (1.04%)
with additional cores based on MRI findings had acancer-positive core that would have been missed by thestandard 12-core PBx, suggesting that additional PBx
could be omitted. Singh et al.8 also stated that 3-T MRItargeted PBx showed similar PCa detection comparedto systematic PBx. The present outcome supports these
conclusions. Moreover, it was also confirmed that theoverall cancer detection rate was not affected by the difference in physicians. However, the hit probability of target PBx was significantly different between the two physicians, although the cancer detection rate of target PBx
was not so high as to suggest the usefulness of target
PBx. PCa was also detected in approximately 20% fromone lobe without a suspected cancer lesion contralateral
to the other lobe with a suspected cancer lesion on MRI
or TRUS; although the probability was low, patients witha high GS PCa were included. Summarizing the above
data, although the probability of PCa in a suspected lesion identified on imaging, especially MRI, is high, owing to the lack of reproducibility and the difference in hit
probability of the suspected lesion between physiciansin target PBx without using an MRI/US fusion system,
there is a limit to the improvement of the cancer detection rate.
Then the question becomes, “Is the target PBx without using MRI/US fusion system completely meaningless?” as Shigemura said.7 Certainly, target PBx without
using an MRI/US fusion system might not be usefulfrom the perspective of improving the cancer detection rate. However, it can be immediately implemented
in many institutions and may facilitate more accurate
staging with detection of minute cancer with a high GS.
Therefore, target PBx of a suspected cancer lesion seen
on both MRI and TRUS should be carried out, since theprobability of the existence of cancer is expected to behigh.
Furthermore, an ink mark was placed on the rectal,
prostatic fascia side of the biopsy cores to estimate thedistance of the cancer lesion from the prostatic fascia.
This information was used to determine the nervesparing policy more oncologically in robotic-assisted
laparoscopic radical prostatectomy, sparing as muchnerve as possible while maintaining the radical cure of
the cancer. Such small efforts do not improve the cancer
detection rate, but may improve treatment outcomes.
This study has several limitations. Without theevaluation of whole mount prostatectomy specimens, the57

H. Iwamoto et al.

difference in accuracy between target PBx and systematic PBx cannot be determined. The MRI system, 1.5T or 3.0-T, was not unified because some of the patients
who visited our hospital from distant places underwent
MRI at another hospital. The cancer detection rate oftarget PBx might be better if more cores were obtained
from the suspected lesion. However, because the complication rate may increase with the core number, theprinciple of taking only one core from a suspected lesion
was adopted. There were no serious complications that
resulted in the need to extend the duration of scheduled
hospitalization (data not shown).
In conclusion, the addition of target PBx of suspected cancer lesions detected by MRI and/or TRUS to asystematic 14-core initial PBx might not be useful fromthe perspective of improving the cancer detection rate
regardless of operator differences. However, it can be
immediately implemented in many institutions and may
make it possible to achieve more accurate risk classification with detection of minute cancer with a high GS.
Moreover, by adding a little ingenuity as ink application,
it may be useful for determination of treatment policy.

5 Lee SH, Chung MS, Kim JH, Oh YT, Rha KH, Chung
BH. Magnetic resonance imaging targeted biopsy in men
with previously negative prostate biopsy results. J Endourol.
2012;26:787-91. PMID: 22122555.
6 Lattouf JB, Grubb RL 3rd, Lee SJ, Bjurlin MA, Albert P,
Singh AK, et al. Magnetic resonance imaging-directed transrectal ultrasonography-guided biopsies in patients at risk of
prostate cancer. BJU Int. 2007;99:1041-6. PMID: 17437438.
7 Shigemura K, Motoyama S, Yamashita M. Do additionalcores from MRI cancer-suspicious lesions to systematic 12core transrectal prostate biopsy give better cancer detection?
Urol Int. 2012;88:145-9. PMID: 22301885.
8 Singh AK, Krieger A, Lattouf JB, Guion P, Grubb RL 3rd,
Albert PS, et al. Patient selection determines the prostate cancer yield of dynamic contrast-enhanced magnetic resonanceimaging-guided transrectal biopsies in a closed 3-Tesla scanner. BJU Int. 2008;101:181-5. PMID: 17922874.
9 Pinto PA, Chung PH, Rastinehad AR, Baccala AA Jr, Kruecker J, Benjamin CJ, et al. Magnetic resonance imaging/ultrasound fusion guided prostate biopsy improves cancer detection
following transrectal ultrasound biopsy and correlates withmultiparametric magnetic resonance imaging. J Urol. 2011;
186:1281-5. PMID: 21849184.
10 Vourganti S, Rastinehad A, Yerram NK, Nix J, Volkin D,
Hoang A, et al. Multiparametric magnetic resonance imaging
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2012;188:2152-7. PMID: 23083875.
11 Chon CH, Lai FC, McNeal JE, Presti JC Jr. Use of extended
systematic sampling in patients with a prior negative prostateneedle biopsy. J Urol. 2002;167:2457-60. PMID: 11992057.
12 Zaytoun OM, Moussa AS, Gao T, Fareed K, Jones JS. Officebased transrectal saturation biopsy improves prostate cancer
detection compared to extended biopsy in the repeat biopsy
population. J Urol. 2011;186:850-4. PMID: 21788047.
13 Stewart CS, Leibovich BC, Weaver AL, Lieber MM. Prostatecancer diagnosis using a saturation needle biopsy techniqueafter previous negative sextant biopsies. J Urol. 2001;166:8691.
14 Pinkstaff DM, Igel TC, Petrou SP, Broderick GA, Wehle MJ,
Young PR. Systematic transperineal ultrasound-guided template biopsy of the prostate: three-year experience. Urology.
2005;65:735-9. PMID: 15833518.

The authors declare no conflict of interest.
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