Outcomes and Trends of Prostate Biopsy for Prostate
Cancer in Chinese Men from 2003 to 2011
Rong Na1,2,3., Haowen Jiang1,3., Seong-Tae Kim2, Yishuo Wu1,3, Shijun Tong1,3, Limin Zhang1,3,
Jianfeng Xu1,2,3, Yinghao Sun4, Qiang Ding1,3*
1Department of Urology, Huashan Hospital, Fudan University, Shanghai, China, 2Center for Cancer Genomics, Wake Forest University School of Medicine, Winston-Salem,
North Carolina, United States of America, 3Fudan Institute of Urology, Huashan Hospital, Fudan University, Shanghai, China, 4Department of Urology, Changhai Hospital,
Background: Prostate-specific antigen (PSA) screening is growing in popularity in China, but its impact on biopsy
characteristics and outcomes are poorly understood.
Objective: Our objective was to characterize prostate biopsy outcomes and trends in Chinese men over a 10-year period,
since the increasing use of PSA tests.
Methods: All men (n=1,650) who underwent prostate biopsy for PCa at Huashan Hospital, Shanghai, China from 2003–2011
were evaluated. Demographic and clinical information was collected for each patient, including age, digital rectal
examination (DRE), transrectal ultrasound (prostate volume and nodule), total prostate-specific antigen (tPSA) levels and
free PSA ratio (fPSA/tPSA) prior to biopsy. Prostate biopsy was performed using six cores before October 2007 or ten cores
thereafter. Logistic regression and multivariate analysis were used to evaluate our data.
Results: The overall positive rate of prostate biopsy for PCa was 47% and the rate decreased significantly over the years
from 74% in 2003 to 33% in 2011 (P-trend=0.004) . Age at diagnosis was slightly increased (P-trend=0.04) while fPSA/tPSA
was significantly decreased (P-trend=1.11610-5). A statistically significant trend was not observed for tPSA levels, prostate
volume, or proportion of positive nodule. The model including multiple demographic and clinical variables (i.e., age, DRE,
tPSA, fPSA/tPSA and transrectal ultrasound results) (AUC=0.93) statistically outperformed models that included only PSA
(AUC=0.85) or fPSA/tPSA (AUC=0.66) to predict PCa risks (P,0.05). Similar results were observed in a subgroup of men
whose tPSA levels were lower than 20 ng/mL (AUC=0.87, vs. AUC of tPSA =0.62, P,0.05).
Conclusions: Detection rates of PCa and high-grade PCa among men that underwent prostate biopsy at the institution has
decreased significantly in the past 10 years, likely due to increasing use of PSA tests. Predictive performance of demographic
and clinical variables of PCa was excellent. These variables should be used in clinics to determine the need for prostate
Citation: Na R, Jiang H, Kim S-T, Wu Y, Tong S, et al. (2012) Outcomes and Trends of Prostate Biopsy for Prostate Cancer in Chinese Men from 2003 to 2011. PLoS
ONE 7(11): e49914. doi:10.1371/journal.pone.0049914
Editor: Zoran Culig, Innsbruck Medical University, Austria
Received July 23, 2012; Accepted October 15, 2012; Published November 26, 2012
Copyright: ? 2012 Na et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted
use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: The authors have no support or funding to report.
Competing Interests: The authors have declared that no competing interests exist.
* E-mail: firstname.lastname@example.org
. These authors contributed equally to this work.
In the past two decades, prostate cancer (PCa) has become one of
the most prevalent malignant tumors in western countries, and is the
second leading cause of cancer death in men . In China, the
incidence of PCa has risen significantly in recent years, however,
prostate-specific antigen (PSA) screening is not common and the
majority of Chinese patients are found to have high grade PCa at
in China. PSA testing was provided based on clinician’s experience.
For example, PSA testing prior to 2007 was only offered to Chinese
men highly suspected of having PCa. Specifically, clinician’s recom-
mended testing if a patient had urinary tract symptoms, a positive
digital rectal exam (DRE) or positive transrectal ultrasound. While
urology guidelines in China after 2007 recommended annual PSA
testing for men over 55 years, testing was selectively provided, most
commonly due to lack of insurance coverage. Because PSA testing is
not routine in China, limited data was available to set tPSA thresholds
for prostate biopsy. In this study, our objective was to characterize
prostate biopsy outcomes and trends in Chinese men over a 10-year
period, since the introduction of PSA tests in China.
Materials and Methods
2.1 Patient population
Our study included all patients (n=1,650) who underwent
prostate biopsy for PCa during 2003 to 2011 at Huashan Hospital,
PLOS ONE | www.plosone.org1November 2012 | Volume 7 | Issue 11 | e49914
Fudan University in Shanghai, China (Table 1). As a tertiary
health institute, Huashan Hospital provides a highly technical level
of medical health care and research, especially for cancer, special
clinical procedures, and other uncommon and severe diseases.
Although most tertiary health institutes like Huashan Hospital are
located in metropolitan areas of China, patients from all over the
country seek their services. Before October 2007, standard
indications were not available for prostate biopsy in China.
However, after that, the indications for prostate biopsy in our
institution were: (1) tPSA.4.0 ng/mL (not the first elevated PSA,
but the PSA after weeks of surveillance and confirmation; in
addition, the patient should meet standard criteria, i.e. no
ejaculation and no manipulations such as catheterization, cystos-
copy or transurethral resection, and no urinary tract infections) (2)
tPSA,4.0 ng/mL, with suspicious fPSA/tPSA (,0.16) or PSAD
(.0.15); (3) Positive findings from DRE, with any level of tPSA; (4)
Positive findings from imaging techniques, such as transrectal
ultrasound and magnetic resonance imaging (MRI), with any level
2.2 Sample collection
All patients underwent transrectal ultrasound guided transper-
ineal prostate biopsy and had 6 core biopsies before Oct. 2007 or
10 core biopsies after Oct. 2007. All specimens were diagnosed by
doctors in the Pathology Department of Huashan Hospital. Blood
samples were collected on the day before biopsy and prior to any
manipulations (e.g. DRE, transrectal ultrasound) that may have
caused a transient increase of biomarkers. The samples were
temporarily stored in a serum tube and sent immediately to the
Department of Clinical Laboratory. We used the same method to
measure tPSA and fPSA. Written informed consent was obtained
from each patient for their participation and so that their
information could be stored in the hospital database and used
for research. The study was approved by the Institutional Review
Board of Huashan Hospital, Fudan University, Shanghai China.
2.3 Statistic analysis
Univariate and multivariate logistic regression models were used
to predict PCa and high grade PCa. Demographic and clinical
variables used in the models included age, logarithm of tPSA,
fPSA/tPSA, logarithm of prostate volume, result of DRE, and
result of transrectal ultrasound. The predictive performance for
each model (different combinations of the variables above) was
measured using the area under the receiver operating curve
(AUC). Statistical analyses were implemented using PROC
LOGISTIC in SAS 9.2 (SAS Institute, Cary, NC).
A total of 774 out of the 1,650 (47%) patients that underwent
biopsies were diagnosed with PCa (PCa group). The total positive
rate of biopsy was 47% and significantly decreased over the study
period (Ptrend=0.004, Table 1). The mean age of all men was 71.24
years. Patients with PCa (72.96 years) were older than patients
with other diseases (non-PCa group) (69.76 years, p,0.001). Age
at diagnosis was increased slightly from 71.65 years in 2003 to
74.72 years in 2011 (Ptrend=0.04, Table 1).
Compared to the non-PCa group, the PCa group had much
higher tPSA levels (mean: 53.61 ng/mL vs. 11.9 ng/mL,
p,0.001) and lower fPSA/tPSA levels (mean: 0.15 vs. 0.19,
p,0.001). There was a significant decrease in fPSA/tPSA levels
(Ptrend=1.1161025, Table 1) and the percentage of tPSA levels for
PCa patients with levels over 20 ng/mL (Ptrend=2.2661025,
Fig. 1), while no statistically significant change in trend for
Table 1. Characteristic table of prostate biopsies performed from 2003–2011 in Huashan Hospital, Shanghai, China.
No. of biopsies
Gleason score$8 (%)
Age of entire group (SD) (Yr)
Age of PCa group (SD) (Yr)
Age of non-PCa group (SD) (Yr)
tPSAu (SD) (ng/mL)
Prostate Volumeu (SD) (mL)
*No Data about Gleason Scores was available in 2003.
Ten Years Outcomes of Prostate Biopsy in China
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patients with tPSA levels under 20 ng/mL (Ptrend=0.47, Table 1)
was observed. The overall positive prostate biopsy rates were
14.8% for tPSA,10 ng/mL, 27.4% for tPSA$10 ng/mL and
,20 ng/mL, and 75.8% for tPSA$20 ng/mL. We observed a
similar trend for high-grade PCa (Gleason Score$8).
Among 774 PCa patients, 670 patients had complete Gleason
score information. Most of them had biopsies from 2004 to 2011
(Only 3 out of 58 men (43 PCa) in 2003 had the information of
Gleason Score). The majority of patients had Gleason scores $8
(Mean: 43.58% for Gleason Score$8, 38.81% for Gleason
Score=7, 17.61% for Gleason Score#6), the percentage of
patients with Gleason scores$8 decreased from 50% in 2004 to
27% in 2011 (Ptrend=2.0861027, Table 1, Fig. 2). This suggests
that men have been getting diagnosed with PCa at earlier stages
during the past ten years.
We first performed univariate analysis to test the association
between PCa and each variable (age, tPSA, fPSA/tPSA, volume,
nodule, DRE) (Table 2). A comparison of prostate volumes by
(Mean=43.06 mL) had significantly (p,0.001) smaller prostate
volumes than those of the non-PCa group (Mean=54.3 mL). In
addition, the PCa group (Mean=81.24%) was twice as likely
(p,0.001) to have one or more nodules than the non-PCa group
(Mean=40.58%). Also, the PCa group had a 5-fold higher
percentage for abnormal DRE (PCa 56.85% vs. non-PCa 10.43%,
p,0.001). The AUCs ranged from 0.610 for the model with age
only to 0.847 for the model with tPSA only.
Next, we stratified our data into three groups, a group with all
men (entire group), a group of men with tPSA,10 ng/mL
(tPSA,10 ng/mL group) and a group of men with tPSA,20 ng/
mL (tPSA,20 ng/mL group), calculating AUC by using tPSA
only (as shown before, tPSA itself performed well in predicting
PCa) and two types of multivariate models (model 1: modeling by
using 5 variables of age, logarithm of tPSA, logarithm of prostate
volume, result of DRE, result of transrectal ultrasound; model 2:
added fPSA/tPSA besides the five variables). The multivariate
models increased the prediction value for both PCa and high
grade PCa. In the tPSA,10 ng/mL group, multivariate models
didn’t perform better comparing with tPSA only, probably
because the number of the high-grade PCa samples was too
small. By using tPSA only, we got significant different AUCs, with
0.85 in the entire group, 0.62 (P,0.05) in the tPSA,20 ng/mL
group and 0.57 (P,0.05) in the tPSA,10 ng/mL group, which
showed a decrease of AUCs when we adjusted the tPSA threshold
to a lower level. We observed similar results by using multivariate
models, with 0.93, 0.86 (P,0.05) and 0.87 (P,0.05) by model 1,
and with 0.93, 0.87 (P,0.05) and 0.87 (P,0.05) by model 2 in the
entire, tPSA,20 ng/mL and tPSA,10 ng/mL groups respec-
tively. However, multivariate models predicted almost equally for
PCa in the tPSA,20 ng/mL and tPSA,10 ng/mL groups when
using these models (Table 3). Generally, multivariate models had
better prediction utility than tPSA only for PCa (P,0.05). When
predicting high-grade PCa (Gleason Score$8), multivariate
models outperformed the model that only used tPSA in the entire
group and tPSA,20 ng/mL group (P,0.05), but performed
equally in the tPSA,10 ng/mL group (P.0.05) (Table 3).
The total risk of PCa at our institute was 47% (positive rate of
prostate biopsy). We calculated the risk at different PSA levels.
The risk of PCa ranged from 4.7% to 14.8% with the tPSA level
from 4 ng/mL to 10 ng/mL. Men with tPSA levels of 20 ng/mL
had a risk of 22.4% (Fig. 3). We also evaluated the sensitivity and
specificity at different cutoff PSA levels (Table 4.). We found that
when the cutoff value was 4 ng/mL, the sensitivity was 99.7%,
and the specificity was 4.4%. When the cutoff value was 10 ng/
mL, the sensitivity would be 92.4%, while the specificity rose to
37.3%. If we increase the cutoff value to 20 ng/mL, the sensitivity
decreases to 74.3%, however, the specificity raises to 79.4%.
To the best of our knowledge, this is the first retrospective study
to evaluate the prevalence and trend of biopsy use for PCa after
the increasing use of PSA screening in a Chinese population. We
also evaluated the predictive performance of variables for PCa and
Most studies conducted in western countries had positive
detection rates ,35%, much lower than the rates (47%) we
observed in our study. However, some of the previous studies had
large populations and were based on randomized screening trials
[2–5]. In addition, most of those studies used tPSA levels of
1.25 ng/mL–2.5 ng/mL as their cutoff values to perform prostate
biopsy, compared with the cutoff value of tPSA.4 ng/mL used in
our study. Therefore, the detection rates reported in those studies
are not comparable to our study. One the other hand, there are a
few studies that used single institute cohorts including New York
Presbyterian Hospital (Weill Medical College of Cornell Univer-
sity, New York, NY), Cleveland Clinic (Cleveland Clinic, Cleve-
land, OH, USA) and Durham VA (Durham VA Medical Center,
Durham, NC, USA). The detection rates from those studies were
Figure 1. The percentage of tPSA levels over 20 ng/mL in PCa
patients. There was a significant decrease in the percentage of tPSA
levels over 20 ng/mL in PCa patients from 2003 to 2010
Figure 2. Trends of Gleason Score # #6, =7, $ $8 Groups over the
years. The percentage of $8 group trend to go downwards from 50%
in 2004 to 27% in 2011 (Ptrend=2.0861027).
Ten Years Outcomes of Prostate Biopsy in China
PLOS ONE | www.plosone.org3 November 2012 | Volume 7 | Issue 11 | e49914
31%, 39% and 47% respectively, which were more comparable to
ours [4–7]. The positive rate of prostate biopsy has decreased over
the years at our institute. Zhu et al. (2009) observed similar
findings in a Chinese population . This may be due to the fact
that PSA testing was not popular in China during earlier years and
patients were more likely to be biopsied because they were
experiencing other symptoms (e.g. hematuria, dysuria). Therefore,
they observed higher detection rates of PCa and dropped
thereafter due to widespread use of PSA test.
According to results from studies conducted in western
countries, the risk for developing PCa varies from 15% (Goteborg
cohort) to 40% (SABOR cohort) when a tPSA threshold of 4 ng/
mL is used . Our study showed that only 4.7% of men with a
tPSA level of 4 ng/mL were diagnosed with PCa, much lower
than rates in western countries. Even men with a tPSA level of
10 ng/mL had lower risk (14.8%) than men that participated in
western studies. In addition, according to our data, although the
sensitivity for tPSA=10 ng/mL was 92.4%, lower (P,0.05) than
that for 4 ng/mL (99.7%), the specificity for tPSA=10 ng/mL
(37.3%) was much higher (P,0.05) than that for tPSA=4 ng/mL
(4.4%). Using a cutoff value of 4 ng/mL for prostate biopsy will
cause a large number of men to undergo unnecessary prostate
biopsies. Thus, we believe that using a cutoff value of tPSA.4 ng/
mL for prostate biopsy in China is not appropriate. We suggest
that when using tPSA.4 ng/mL as cutoff value for prostate
biopsy, fPSA/tPSA, PSAD or other clinical information should be
comprehensively considered before a new cutoff value is set up
based on further prospective and larger population studies.
The tPSA levels at diagnosis for Chinese men were much higher
than levels for men in western countries. Our tPSA level at
diagnosis fluctuated from 28.6 ng/mL to 50.9 ng/mL (median),
while in western trials the median ranged from 11.8 ng/mL to
6.3 ng/L . We also found that the percentage of patients with
Gleason scores .8 was 43.58%, much higher than those of studies
from western countries, which ranged from 2% (Goteborg cohort)
to 21% (Tyrol cohort ) . Overall, the downward trend of high-
grade PCa percentages shows that there are benefits to PSA
The SEER database documented a decline in age at diagnosis
from 72 to 69.4 yr from 1990 to 1994 due to the increasing use of
PSA testing and increased ability of early detection of serum PSA
. However, our data showed a different result with a slight
increase of age at diagnosis from 2003 to 2011 (Table 1). This may
be due to the fact that, with the increasing use of PSA testing,
clinicians were more likely to monitor or use active surveillance of
PSA levels instead of performing prostate biopsies with initial
abnormal PSA results.
Table 2. Univariate analysis (testing the association between each variable and PCa).
PCa72.94(8.30) 53.61(3.55)0.15(0.13)43.06(1.62) 81.2456.85
non-PCa69.76(8.69)11.9(2.22) 0.19(0.12) 54.3(1.57) 40.5810.43
P-value (PCa vs. non-
2.02E-13 6.05E-852.56E-062.81E-201.69E-51 2.65E-81
OR(95%CI) 1.05 (1.03–1.06) 4.81 (4.11–5.63)0.08 (0.03–0.23)0.34 (0.27–0.43) 6.34 (4.99–8.06) 12.9 (9.89–16.7)
AUC0.6100.847 0.6630.645 0.703 0.751
uThe tPSA and fPSA values are antilogarithmic when calculating P-value, OR and AUC.
Table 3. Performance of tPSA only and Multivariate model for predicting PCa and high grade PCa in different stratification.
High Grade PCa (Gleason
AUC (Area Under the Curve)
Total men (PCa: 774 vs. non-PCa: 876) (High grade PCa: 290)tPSA only0.850.62
*Multivariate Model 1 0.930.66
**Multivariate Model 20.93 0.67
Men with tPSA,20 ng/mL (PCa:198 vs. non-PCa: 692) (High
grade PCa: 58)
tPSA only0.62 0.54
Multivariate Model 10.86 0.63
Multivariate Model 20.870.63
Men with tPSA,10 ng/mL (PCa:59 vs. non-PCa:325) (High
grade PCa: 18)
tPSA only 0.57 0.92
Multivariate Model 1 0.870.87
Multivariate Model 2 0.870.94
*Multivariate Model 1: Modeling by using 5 variables: age, logarithm of tPSA, logarithm of prostate volume, result of DRE, result of transrectal ultrasound.
**Multivariate Model 2: Modeling by using 6 variables: age, logarithm of tPSA, fPSA/tPSA, logarithm of prostate volume, result of DRE, result of transrectal ultrasound.
-The tPSA and fPSA values are antilogarithmic when calculating AUC.
Ten Years Outcomes of Prostate Biopsy in China
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Studies in the tPSA era have demonstrated a fall in PSA levels at
diagnosis . The median tPSA level at the time of diagnosis
decreased from 11.8 ng/mL in 1990 to 6.3 ng/mL in 1998 .
The levels of tPSA over the years didn’t show a significant trend,
however, because of the significant decrease of percentage of
patients with tPSA.20 ng/mL, we can still conclude that PSA
screening had benefits over the years.
We would like to point out that there were two notable changes in
the clinical parameters during the study period. First, we obtained 6
cores for prostate biopsy before Oct. 2007 and 10 cores thereafter. Up
to a 40% increase in detection rates of PCa were reported in some of
not observe a significant difference between detection rates based on
6-core biopsy and 10-core biopsy (Chi-square test, P=0.976). Thus,
the number of cores was not included in our multivariate analysis.
Second, the International Society of Urological Pathology modified
the Gleason scoring system in 2005, thereby introducing some
potential bias [23–27]. However, this had limited effects on our study
as only 8.7% of our study population were graded using the old
Gleason score system before 2005. More importantly, our analysis of
high-grade PCa was defined as Gleason score $8, and men in this
category were least affected by the new scoring system [23–27].
Although retrospective, our study presents a good depiction of
PCa prevalence and the trends of prostate biopsy in Chinese men.
Some of the limitations of this study include the lack of family
history and that study participants were recruited from a single
institution. Although most tertiary health institutes like Huashan
Hospital are located in metropolitan areas of China, patients from
all over the country seek their services.
Detection rates of PCa and high-grade PCa among men that
underwent prostate biopsy in China have decreased significantly in
the last 10 years. This trend is likely due to the increasing use of
PSA testing. Significant differences in positive prostate biopsy rates
were found between western countries and China. Predictive
performance of demographic and clinical variables of PCa was
excellent. These variables should be used in clinics to determine
the need for prostate biopsy. Furthermore, the cutoff value of
4 ng/mL for prostate biopsy in China is not appropriate, and
should be considered in further studies.
Conceived and designed the experiments: RN YS QD JX. Performed the
experiments: RN HJ. Analyzed the data: STK ST JX. Contributed
reagents/materials/analysis tools: YW LZ. Wrote the paper: RN.
Figure 3. Probability of having prostate cancer with increasing PSA in biopsy population. The probability of having prostate cancer when
undertaking prostate biopsy is raised from nearly 0% with tPSA,1.0 ng/mL to nearly 31% with tPSA=50 ng/mL according to our study population.
This figure can be use to predict the probability with tPSA level in the future.
Table 4. Different sensitivities and specificities in different
tPSA cutoff level.
Sensitivity (%) Specificity (%)
Cutoff tPSA value (ng/mL)499.7 4.4
Ten Years Outcomes of Prostate Biopsy in China
PLOS ONE | www.plosone.org5 November 2012 | Volume 7 | Issue 11 | e49914
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