Stesura Seveso


81Archivio Italiano di Urologia e Andrologia 2014; 86, 2

ORIGINAL PAPER

Evaluation of various active surveillance protocols 
in prostate cancer

Kayhan Yılmaz 1, Tahir Karadeniz 2, Orkunt Özkaptan 3, Oğuz Yilanoglu 4

1 Antalya Korkuteli State Hospital, Turkey;
2 Medicana Hospital Group Istanbul, Turkey;
3 Kastamonu State Hospital;
4 Hatay Dörtyol State Hospital, Turkey.

Objective: This study aims to investi-
gate whether pathology results obtained

by radical retropubic prostatectomy (RRP) were correlat-
ed with active surveillance (AS) criteria defined by Klotz,
Soloway and D’Amico. 
Materials and Methods: In our clinic we evaluated 211
patients with diagnosis of localized prostate cancer who
underwent RRP between 2007 and 2012. AS criteria
defined by Soloway (cT ≤ T2, PSA ≤ 15 ng/dl, Gleason
≤ 6), Klotz (cT1c-T2a; if age ≥ 70 PSA ≤ 15 ng/dl, if age
< 70 PSA ≤ 10 ng/dl; if age ≥ 70 Gleason ≤ 7(3+4), if age
< 70 Gleason ≤ 6) and D’Amico (cT1c-T2a, PSA ≤ 10
ng/dl, Gleason ≤ 6) were used in our study. Pathological
stages and Gleason scores were evaluated with coherence
to AS protocols, mis-staging rates, biochemical recur-
rence (BC) of the mis-staged patients and death due to
prostate cancer Data was analyzed using NCSS 2007 &
PASS 2008 Statistical Software (Utah, USA). Chi square
test and Mann-Whitney U test were applied for analyzing
qualitative data. Significance was determined as p < 0.05.
Results: 137 (64.9%) patients were coherent with
Soloway AS criteria, 118 (55.9%) with Klotz AS criteria
and 108 (51.1%) with D’Amico AS criteria.
Histopathological results of the patients grouped accord-
ing to Soloway, Klotz and D’Amico AS protocols showed
high stage prostate cancer in 40 (29.2%), 32 (27%) and
27 (24.9%) patients, respectively. High grade prostate
cancer rates in Soloway, Klotz, D’Amico groups were 55
(40.2%), 46 (38%) and 39 (36.1%); respectively.
Misstaging rates of Soloway, Klotz and D’Amico AS
 protocols were determined as 65 (47.4%), 54 (45.5%)
and 46 (42.5%), respectively. In the Soloway group BC
rate was 21.9% in those with high stages. Relation
between BC and high stage was found to be statistically
significant (p < 0.05).
Conclusion: Misstaging rates were relatively high in the
three groups and there was no difference between the
three groups in BC rates. Randomized studies with
 adequate follow up are needed.

Key WORDS: Active surveillance; Prostate cancer; Radical
prostatectomy.

Submitted 23 August 2013; Accepted 5 October 2013

Summary

No conflict of interest declared.

INTRODUCTION
Prostate cancer is a multifaceted disease in which genet-
ic and environmental factors play an important role.
Studies show that prostate cancer is the most common
cancer in man over 50 years age and is shown to be the
second most reason for death due to cancer (1-3). 
Currently prostate cancer has various treatment options
according to the stage and clinical course of the disease
such as radical retropubic prostatectomy (RRP), bra chy -
therapy, external radiotherapy, hormone therapy and
chemotherapy.  Although there has been an increase in
the early diagnosis and treatment rates in prostate cancer,
there has been no significant decrease in mortality. This
fact gives rise to the thought that clinically insignificant
disease is being treated excessively and active follow up
of these patients should be preferred instead of radical
treatment. Active surveillance which was first described
by Coo et al. (4, 5) aims to postpone radical treatment
and prevent redundant early treatment. 
Active surveillance in prostate cancer has become popu-
lar in the last decade (6, 7). Patients who are adequate for
active surveillance are determined with criteria; appro-
priate prostate specific antigen (PSA) level, clinical stage
and Gleason score in the biopsy (8). However, there is no
sufficient randomized data available for supporting these
criteria. 
In our study, we retrospectively investigated patients
diagnosed as having localized prostate cancer in which
RRP was performed in relation to three different active
surveillance criteria as established by Klotz, Soloway and
D’Amico. We evaluated whether the pathology results
obtained from the RRP specimens were correlated with
these three active surveillance criteria.

MATERIALS AND METHODS
We evaluated 211 patients with localized prostate cancer
diagnosis in which RRP was performed between 2007
and 2012 in Okmeydanı Training and Research Hospital/
Istanbul. Patients who underwent previous hormono the -
rapy and/or 5-alfa reductase inhibitor or pelvic radio-
therapy were excluded from the study.
Clinical stages were determined using 2002 TMN classifi-

DOI: 10.4081/aiua.2014.2.81



Archivio Italiano di Urologia e Andrologia 2014; 86, 2

K. Yılmaz, T.Karadeniz, O. Özkaptan, O. Yilanoglu

82

cation. All the RRP operations were performed by the same
urologist and all biopsy and RRP specimens were evaluat-
ed by the same pathologist. Since positive biopsy core
number and tumor percentage were not present in most of
the biopsy pathology results, these active surveillance crite-
ria were not included in the study. The active surveillance
criteria defined by Soloway (cT ≤ T2, PSA ≤ 15 ng/dl, biop-
sy Gleason score ≤ 6), Klotz (T1c-T2a; if age ≥ 70 PSA ≤ 15
ng/dl, if age < 70 PSA ≤ 10 ng/dl; if age ≥ 70 biopsy Gleason
score ≤ 7 (3 + 4), if age < 70 biopsy Gleason score ≤ 6) and
D’Amico (clinical stage T1c-T2a, PSA ≤ 10 ng/dl, biopsy
Gleason score ≤ 6) were used in our study. Patients appro-
priated for the three active sur-
veillance protocols were deter-
mined by retrospectively exami-
nation of the preoperative PSA
value, clinical stage and biopsy
Gleason score (Table 1).
Pathological stages and RRP spec-
imen Gleason scores were evalu-
ated with coherence to active sur-
veillance protocols, misstaging
rates, biochemical recurrence of
the misstaged patients and death
due to prostate cancer.
The data of the study there ana-
lyzed using NCSS (Number
Cruncher Statistical System) 2007
& PASS 2008 Statistical Software
(Utah, USA). In addition to
descriptive statistical analyses
(mean, standard deviation), chi
square test was used for analyz-
ing qualitative data and in order
to analyze qualitative data in
cases of abnormal distribution
Mann-Whitney U test was
applied. Significance was deter-
mined at the level of p < 0.05.

RESULTS
We evaluated 211 patients who
underwent RRP according to total
PSA, clinical stage and biopsy
Gleason scores as active surveil-
lance criteria. Active surveillance
criteria defined by D’amico, Solo -
way and Klotz were shown in
Table 1. 137 (64.9%) of the pa -
tients were coherent with Solo way
active surveillance criteria (9),
118 (55.9%) with Klotz active
surveillance criteria (7) and 108
(51.1%) with D’amico active sur-
veillance (10) criteria (Table 1).
The clinical features found coher-
ent with active surveillance proto-
cols were compared to final
pathology results. The pathology
results that showed high grade
prostate cancer, Gleason score

sum ≥ 7) (17), extracapsular extension (ECI), seminal vesi-
cle (SVI) and/or lymph node involvement (LNI) were stud-
ied and misstaging rates were determined (Table 2).
The histopathological results of the patients grouped
according to Soloway active surveillance protocol showed
high stage prostate cancer in 40 patients (29.2%). ECI,
SVI, LNI was observed in 32 (23.3%), 7 (5.1%) and 1
(0.7%) patient, respectively. High grade prostate cancer
was observed in 55 (40.2%) patients. Of the 118 patients
classified in the Klotz active surveillance protocol 32
(27%) had high stage prostate cancer. ECI, SVI and LNI
were found in 26 (22%), 5 (4.2%) and 1 (0.8%), respec-

Selection criteria All patients Soloway Klotz D’Amico
and Coleman

Clinical stage - ≤ T2 T1c-T2a T1c-T2a

PSA - ≤ 15 If age ≥ 70 ≤ 15 ≤ 10
If age < 70  ≤ 10

Biopsy gleason score - ≤ 6 If age ≥ 70 ≤ 7 (3+4)
If  age < 70 ≤ 6 ≤ 6 ≤ 6

Patients coherent 211 (%100) 137 (%64,9) 118 (%55,9) 108 (%51,1)
with the criteria

Table 1.

Criteria for active surveillance protocols.

ECI Extracapsular extension. SVI Seminal Vesicle Involvement. LNI Lymph Nod Involvement.

All cases Soloway Klotz D’Amico
(n = 211) (n = 137) (n = 118) (n = 108)
Min-max Min-max Min-max Min-max

(Mean ± SD) (Mean ± SD) (Mean ± SD) (Mean ± SD)
Diagnosis age 44-79 44-79 44-79 44-79 

(63,10 ± 64) (62,87 ± 7,24) (63,43 ± 64) (62,61 ± 7,19)
Preoperative PSA 1,20-93 1,20-15 1,20-14 10-1,20 

(14,12 ± 14,68) (7,19 ± 2,92) (6,59 ± 6,17) (6,15 ± 2,05)
n (%) n (%) n (%) n (%)

Clinical stage T1c 89 (%42,2) 74 (%54) 65 (%55,1) 61 (%56,5)
T2a 89 (%42,2) 55 (%40,1) 51 (%43,2) 47 (%43,5)
T2b 33 (%15,6) 8 (%5,8) 2 (%1,7) -

Preoperative 2-6 171 (%81) 137 (%100) 117 (%99,2) 108 (%100)
gleason score 7 (3+4) 28 (%13,3) - 1 (%0,8) -

7 (4+3) 5 (%2,4) - - -
8-10 7 (%3,3) - - -

ECI 76 (%36) 32 (%23,4) 26 (%22) 22 (%20,3)
SVI 33 (%15,6) 7 (%5,1) 5 (%4,2) 5 (%4,6)
LNI 9 (%4,3) 1 (%0,7) 1 (%0,8) -
Pathological 2-6 105 (%49,8) 82 (%59,9) 72 (%61) 69 (%63,9)
gleason score 7 (3+4) 68 (%32,2) 43 (%31,4) 36 (%30,5) 32 (%29,6)

7 (4+3) 25 (%11,8) 9 (%6,6) 9 (%7,6) 6 (%5,6)
8-10 13 (%6,2) 3 (%2,2) 1 (%0,8) 1 (%0,9)

Pathological stage pT0 1 (%0,5) 1 (%0,7) 1 (%0,8) 1 (%0,9)
pT2a 47 (%-22,3) 36 (%26,3) 35 (%29,7) 33 (%30,6)
pT2b 73 (%34,6) 57 (%41,6) 46 (%39) 42 (%38,9)
pT2c 13 (%6,2) 12 (%8,8) 10 (%8,5) 10 (%9,3)
pT3a 44 (%20,9) 25 (%18,2) 21 (%17,8) 17 (%15,7)
pT3b 30 (%14,2) 7 (%5,1) 5 (%4,2) 5 (%4,6)
pT4a 3 (%1,4) - - -

Misstaging (*)
Number (%) - 65 (%47,4) 54 (%45,7) 46 (%42,5)
%95 CI - 40.4-54.4 38.9-54.1 34.6-50.2

Table 2.

Pathology results and misstaging rates of RRP.



tively. High grade prostate cancer was present in 46
(38%) patients. Patients classified according to D’Amico
active surveillance criteria comprised 27 (24.9%) high
stage prostate cancer patients. ECI, SVI rates were 22
(20.3%) and 5 (4.6%); respectively. In this group 39
(36.1%) patient were categorized as high grade cancer.
Patients diagnosed as organ confined disease on digital
rectal examination had local advanced disease in the
prostatectomy pathology result with rates of 21.3% in
the group classified by Soloway criteria, 22.8% in the
group according Klotz and 23.3% in the group according
D’Amico. Misstaged patients and misstaging rates of
Soloway, Klotz and D’Amico active surveillance protocols
were determined as 65 (47.4%), 54 (45.7%), 46
(42.5%); respectively (Table 2). 
Average follow up periods were 63 months in the Soloway
group, 63 months in the Klotz group and 61 months in the
D’Amico group. Time until recurrence was 9-48 in the
three groups. Total numbers of patients in which bio-
chemical recurrence was detected were 16 (11.6%) in the
Soloway group, 13 (11%), in the Klotz group, 11 (10.2%)
D’Amico group and the period until recurrence in each

group was 21, 24 and 25 months, respectively. There was
no difference in term of biochemical recurrence rates
between the three groups (p > 0.05). In the Soloway group
biochemical recurrence rate was obtained to be 21.9% in
those with high stages. The relation between biochemical
recurrence and high stage was found to be statistically sig-
nificant for Solowoy group (p < 0.05) (Tables 3, 4). No sta-
tistically significant difference was shown between bio-
chemical recurrence rates and high stages according to
D’Amico and Klotz criteria (p > 0.05). High Gleason grade
(≥ 7 in the prostatectomy specimen) had higher biochem-
ical recurrence values, but this analysis did not reach sig-
nificance (p > 0.05).
There was no statistically significant difference between
recurrence and death rates according to misstaging status
(p > 0.05). In the Soloway and Klotz groups two deaths
due prostate cancer per group and in the D’Amico group
one death due prostate cancer were reported. 
Deaths due to prostate cancer were only among mis-
staged patients in the three groups. Statistical analysis
was not performed because of the low number of exitus
patients (Table 4).

DISCUSSION
After the description of active surveil-
lance by Coo et a.l, it became more
popular for clinicians in the last ten
years (4, 6, 7). Mortality rates of
prostate cancer did not decrease
despite early diagnosis and treatment
of the disease within this period. This
fact led clinicians to come to the opin-
ion that clinically insignificant disease
is being treated excessively.
Our study was performed to evaluate
the credibility of various criteria
groups used for the selection of active
surveillance patients in order to esti-
mate pathological stage. Misstaging
rates of our study for the groups
formed according to D’Amico, Klotz
and Soloway active surveillance crite-
ria were found to be 42.4%, 45.7%
and 47.4%, respectively. With regard
to our results D’Amico active surveil-
lance protocol had the most firm
patient selection criteria with lower
misstaging rates compared to the
other groups. In a study by Marc et al.,
2837 patients who underwent RRP
were evaluated retrospectively. 
Patients with appropriate clinical fea-
tures for separate active surveillance
protocols had a misstaging rate
between 26-35% according to their
pathological features (11). Nazareno et
al. evaluated 4308 patients treated
with RRP in five separate active sur-
veillance protocols including D’Amico
and Klotz retrospectively. Pathology
reports of patients in groups appropri-

83Archivio Italiano di Urologia e Andrologia 2014; 86, 2

Evaluation of various active surveillance protocols in prostate cancer

Chi square test and Fisher’s exact was used.

Soloway Klotz D’Amico
Follow up period Min-max 13-120 13-118 13-118
(month) Mean ± SD 63,93 ± 32,26 63,93 ± 31,68 61,75 ± 31,92
Time until recurrence Min-max 9-48 9-48 9-48

Mean ± SD 21,87 ± 12,19 24,17 ± 12,87 25,10 ± 13,79
n (%) n (%) n (%)

Recurrence Number (%) 16 (7,3%) 13 (11%) 11 (10.2%)
%95 CI 13.1-19.1 10,3-18.9 9,4-18,0

Death Number (%) 10 (7,3%) 8 (6,8%) 7 (6,5%)
%95 CI 3.7-10.9 3.0-10.6 2.6-10.4

Cause of death Prostate cancer 2 (1,4%) 2 (1,6%) 1 (0,9%)
Other 8 (5,9%) 6 (5,2%) 6 (5,6%)

Table 3.

Follow up periods, recurrence and exitus rates distribution in the groups.

Misstaging
Present n (%) Absent n (%) P

Soloway group
Recurrence 10 (%15,4) 6 (%8,3) 0,199
Death 6 (%9,2) 4 (%5,6) 0,409
Cause of death Prostate 2 (%33,3) 0 (%0) -

Other 4 (%66,7) 4 (%100)
Klotz group
Recurrence 9 (%16,7) 4 (%6,3) 0,072
Death 5 (%9,3) 3 (%4,7) 0,467
Cause of death Prostate 2 (%40,0) 0 (%0) -

Other 3 (%60,0) 3 (%100)
D’Amico group
Recurrence 7 (%15,2) 4 (%6,5) 0,136
Death 4 (%8,7) 3 (%4,8) 0,456
Cause of death Prostate 1 (%25,0) 0 (%0) -

Other 3 (%75,0) 3 (%100)

Table 4.

Recurrence and death rates according to misstaging status in the groups.



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K. Yılmaz, T.Karadeniz, O. Özkaptan, O. Yilanoglu

84

ate for active surveillance were investigated and high
stage and/or high Gleason scores were detected in the
range 39-56%. According to active surveillance criteria
recommended by this study group (PSA < 4 ng/ml, cT1
and Gleason score < 7), the misstaging rate (7.2%) was
found to be statistically significantly decreased. However,
the patients’ ratio appropriate for active surveillance was
found to be decreased to 6.9% (12) and this rate seemed
to be low. In fact in our study the rate of patients suitable
for Soloway, Klotz, D’Amico active surveillance protocols
were 64.9%, 55.9%, 51.2%, respectively.
Most important reason for misstaging was determined to
be low prostate cancer grade in the biopsy results. The
misstaging rate in the biopsy grades with regard to
prostatectomy specimen grade were 36.1%, 38.9% and
40.1%, respectively. Supporting our finding, Dall’Era et
al. established in their study that the most important rea-
son for changing from active surveillance to radical treat-
ment was the increase in the Gleason grades in prostate
biopsies repeated periodically and this ratio was report-
ed to be 38% (13). In another study performed by Carter
et al. this ratio was found to be 30% (14). In the light of
these findings we believe that if tumor grade is detected
more accurately at the beginning, approximately 30% of
patients could be treated with active surveillance proto-
cols instead of RRP without losing the chance of cure. 
Several studies have determined that the sensitivity of
digital rectal examination is low in the diagnosis and
staging of prostate cancer (15-17). In our study patients
with organ confined disease on digital rectal examination
had local advanced disease in the prostatectomy pathol-
ogy results with the rates 21.3%, 22.8%, and 23.3%
according to Soloway, Klotz and D’Amico active surveil-
lance groups, respectively. In agreement with this results
the evaluation of the propriety of patients for active sur-
veillance showed that there was a misstaging rate of
21.3%-23.3% with digital rectal examination and 36.1-
40.1% with Gleason grade. In our study digital rectal
examination was found to detect whether the disease is
limited to the organ better than grade, however misstag-
ing rates were very high. 
The final point in active surveillance is not pathological
stage, but biochemical recurrence, metastasis and cancer
related death. While radical prostatectomy can cure the
disease without affecting the quality of life when per-
formed by experienced surgeons, it is still debated
whether one should risk this chance with active surveil-
lance (18). Warlick et al. compared 38 patients who under-
went radical prostatectomy following active surveillance
with 150 patients with similar characteristics in which
radical prostatectomy was performed immediately. This
study indicated that postponing prostate cancer surgery
didn’t risk the chance of cure, however the evident differ-
ence between the patient population in the groups
decreases the credibility of the study (19). In contrast, the
Toronto active surveillance study followed 299 patients
and they performed radical prostatectomy in 24 patients
which showed progression; in 14 (14%) pT3 and in two
(8%) N1 was detected and these rates are high (20). This
indicated the risk of losing the chance for curative treat-
ment after active surveillance (21-23). 
Also the PRIAS (Prostate Cancer Research International:

Active Surveillance) study reported undesired pathological
results in 29% of the patients in which radical surgery was
performed following a period of 1.3 years: pT3-4 disease
and /or Gleason score ≥ 4+3 (24). John Hopkins reported
that the 10 year disease free rate of 23% patients in which
RRP was performed due to grade progression in the con-
trol biopsy was lesser than 75% (25). However, this rate
was not statistically significantly different than patients
who have similar clinical features and were operated on
with radical surgery within three months (25).
In our study the average follow up periods were 61-63
months in three groups. Biochemical recurrences and
rates were 16 (11.6%) in the Soloway group, 13 (11%),
in the Klotz group, and 11 (10.2%) D’Amico group and
the period until recurrence in each group was 21, 24 and
25 months, respectively. In comparing the three active
surveillance groups in our study according to biochemi-
cal recurrence, no statistically difference was noted.
Statistical significance (p < 0.05) between biochemical
recurrence and high stage was remarkable in the Soloway
group. Although there was no statistically significant dif-
ference in biochemical recurrence rates in high stages
according to D’Amico and Klotz criteria, high values of
biochemical recurrence in high stage were observed.
When evaluating the relationship between Gleason
grades in RRP pathologies and biochemical recurrence,
patients with high Gleason grades had higher biochemi-
cal recurrence values, however this analysis was not sta-
tistically significant (p > 0.05). In comparing the bio-
chemical recurrence values of misstaged patients and
patients who met the criteria in three active surveillance
groups, no statistically significant difference (p > 0.05)
was found, however biochemical recurrence rates were
higher in misstaged patients. About death due to prostate
cancer there were two deaths due to prostate cancer in
the Soloway and Klotz group and one death in the
D’Amico group. This result was remarkable because all
these patients were among the misstaged patients. 

CONCLUSION
All these findings show that there are serious problems in
the selection of active surveillance patients. Also, there is
no consensus in the follow up of active surveillance
patient. Consequently the controversial status of active
surveillance may result in various mood disorders in
patients, and this psychological aspect should not be
underestimated. After evaluating all the study results, it is
evident that the data on radical surgery results following
active surveillance in low risk prostate cancer patients are
insufficient. At least one fourth of the pathological data are
consistent with the need of treatment and it is unknown
how this rate will change with longer surveillance periods
and how this will affect the patient  prognosis. Thus, there
is no current data that postponing active treatment in
these patients decreases the chance of cure. Since there are
not sufficient randomized studies with adequate follow up
periods, active surveillance should only be recommended
to a well selected patient group and the patient should be
informed about the inconsistencies about active surveil-
lance and all the treatment options should be explained,
and the decision should be up to the patient. 



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85Archivio Italiano di Urologia e Andrologia 2014; 86, 2

Evaluation of various active surveillance protocols in prostate cancer

Correspondence
Kayhan Yılmaz, MD
kayhany@gmail.com
Aşağı Pazar mah. Hastane cad. no 71 Korkuteli Antalya, Turkey

Tahir Karadeniz, MD
karadeniz@gmail.com
Director of Medicana Hospital Group
Beylikdüzü cad. No:3 Beylikdüzü, Istanbul, Turkey  

Orkunt Özkaptan, MD
orkunt79@gmail.com
Fellow in Heilbronn Urology Clinic
Tatlipinar caddesi yunus apt no 11 d3 Fatih Istanbul, Turkey

Oğuz Yilanoglu, MD
oyilanoglu@yahoo.com
Yilanoglu, Istasyon Cd. 31600 Dörtyol Hatay, Turkey