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Original Article: Clinical Investigation
Salvage partial brachytherapy for prostate cancer recurrence afterprimary brachytherapyHiroshi Sasaki,1 Masahito Kido,1 Kenta Miki,1 Hidetoshi Kuruma,1 Hiroyuki Takahashi,2 Manabu Aoki3
and Shin Egawa1
Departments of 1Urology, 2Pathology and 3Radiology, Jikei University School of Medicine, Tokyo, Japan
Abbreviations & AcronymsADT = androgendeprivation therapyAnt = anteriorBCR = biochemicalrecurrenceCT = computedtomographyCTV = clinical targetvolumeDW = diffusion-weightedEBRT = external beamradiotherapyLDR-BT = low-dose ratebrachytherapyLt SV = left seminal vesicleMRI = magnetic resonanceimagingNA = not availablePSA = prostate-specificantigenPSADT = prostate-specificantigen doubling timeRec = recoveryRt SV = right seminalvesicleSal BT = salvage regionallow-dose-ratebrachytherapyT2W = T2-weightedTx = treatment
Correspondence: HiroshiSasaki M.D., Department ofUrology, Jikei University Schoolof Medicine, 3-25-8Nishi-Shimbashi, Minato-ku,Tokyo 105-8461, Japan. Email:[email protected]
Received 2 July 2013; accepted17 November 2013.Online publication 23 December2013
Objectives: To characterize local recurrence of prostate cancer and to assess the effect ofsalvage partial brachytherapy after primary 125-iodine low-dose rate brachytherapy with orwithout external beam radiotherapy in Japanese men.Methods: Between 2003 and 2010, a total of 616 consecutive patients underwent low-dose rate brachytherapy-based therapy for clinically localized prostate cancer at Jikei Univer-sity Hospital in Tokyo, Japan. Biochemical recurrence occurred in 45 (7.3%) patients at amedian of 30 months (range 11–93 months). A total of 20 patients subsequently underwenttransperineal template prostatic biopsy; of those, eight had positive cores at the base of theprostate or at the seminal vesicles. These eight patients had underdosed areas identified atinitial low-dose rate brachytherapy corresponding to the positive biopsy sites. All were con-firmed to have only localized recurrence, and seven underwent salvage partial low-dose ratebrachytherapy.Results: Median prostate-specific antigen nadir level in the eight patients with biopsy-proven local recurrence after initial low-dose rate brachytherapy was 0.75 ng/mL (range0.39–2.06). The seven retreated patients tolerated the salvage partial low-dose ratebrachytherapy well, and showed a decrease in prostate-specific antigen level at follow up.Two patients later developed biochemical and clinical progression at 11 and 13 months,respectively. Prostate-specific antigen level continued to be low in the remaining five patients.No significant genitourinary or gastrointestinal toxicity was encountered.Conclusions: Salvage partial low-dose rate brachytherapy for biopsy-proven localizedprostate cancer recurrence appears rational, technically feasible and safe. Optimal patientselection is of utmost importance for long-term success. Larger studies with longer follow upare warranted.
Key words: local recurrence, prostate cancer, salvage partial brachytherapy.
Introduction
Selection of ideal treatment for localized prostate cancer recurrence after definitive radiotherapyis controversial, owing to the lack of evidence based on randomized controlled trials. Accordingto guidelines from the National Comprehensive Cancer Network, local salvage therapy should beconsidered for patients with solitary local recurrence. Such therapy includes radical prostatec-tomy, cryosurgery and brachytherapy, and some authorities also recommend salvage high-intensity focused ultrasound. However, because of the toxicities associated with these modalities,physicians often choose palliative treatment with ADT instead.1,2 Potentially curative treatment isthus withheld from many patients.
Salvage LDR-BT can be a useful treatment option for localized prostate cancer.3–7 However,conventional salvage LDR-BT, with re-implantation of the entire prostate,2 might be associatedwith serious adverse events. Gastrointestinal or genitourinary grade ≥3 toxicity has been reportedin up to 47% of patients, and can develop prostatic urethral fistulas requiring surgical repair, ifproper dosimetric constraints are not applied.2,7 Salvage LDR-BT of the entire gland can besuboptimal if inappropriately applied.
Localized persistence of prostate cancer after radiotherapy might result from radioresistantcell clones in the primary tumor. However, such persistence can more often be the result ofinhomogeneous dosimetric distribution of irradiation within the prostate, so that the tumor doesnot incur uniformly lethal damage.2,7,8 In such cases, underdosed regions or “cold spots” wouldbe expected to correspond to areas of local recurrence.8 The target volume could then be definedbased on the initial dosimetric record, coupled with information from template-style biopsy
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International Journal of Urology (2014) 21, 572–577 doi: 10.1111/iju.12373
572 © 2013 The Japanese Urological Association
mapping. We carried out the present study to test this hypoth-esis, in order to better define the safety and technical feasibilityof salvage partial LDR-BT for undertreated areas.
Methods
Patients
Between October 2003 and April 2010, 616 Japanese patientsunderwent LDR-BT for localized prostate cancer at JikeiUniversity Hospital. LDR-BT was administered using anultrasound-guided technique with a Mick applicator as previ-ously described.9 LDR-BT monotherapy was administered in167 low-risk, 124 intermediate-risk and two high-risk patientsas defined by D’Amico’s risk stratification. A total of 17patients in the intermediate-risk and nine patients in the high-risk group received trimodality therapy consisting of LDR-BT,ADT, and EBRT. A total of 90 patients enrolled in theSHIP0804 randomized controlled trial for intermediate-riskprostate cancer had 3-month neoadjuvant ADT before LDR-BT; none of them received EBRT. An additional 43 patientsfrom the SHIP0804 study received 9-month adjuvant ADT.9
BCR was defined as a PSA increase of >2 ng/mL above thePSA nadir level (Phoenix definition).10 A total of 45 patients(7.3%) developed BCR after initial LDR-BT at a median of30 months (range 11–93 months). Patients with BCR within24 months had significant clinical progression or continuousincreasing PSA levels, thus minimizing the possibility of PSAbounce phenomenon. Admittedly, this diagnosis is primarilymade based on clinical judgment, as there are no solid diagnos-tic criteria available to exclude this possibility, especiallyduring the early phase after LDR-BT. A total of 20 patientssubsequently underwent template transperineal biopsy toconfirm local recurrence as described by Satoh et al.11 A total of22 tissue cores were obtained in general from the prostate; 16from the mid-prostate to the base including seminal vesicles,and six cores from the distal half of the gland. All histology wasreviewed by one pathologist (HT). The remaining patients didnot undergo prostatic biopsy after BCR, either because distantmetastases were diagnosed (n = 19) or because the patientrefused the procedure (n = 6). These latter patients are currentlyfollowed without further treatment.
Patients with positive biopsy results were further evaluatedwith the use of CT, MRI (T2W and DW at 1.5T, beginning in2007) and bone scintigraphy to exclude the possibility ofdistant metastases. Local recurrence and its location within theprostate were visually evaluated using DW imaging.
Eight patients had positive cores at the base of the prostate orthe seminal vesicles (Table 1). Those eight patients were con-firmed to have localized recurrence only. All eight patients hadunderdosed areas identified at initial LDR-BT, and those areascorresponded to the positive biopsy sites. Seven of the eightpatients underwent salvage partial LDR-BT using 125-iodinewith real-time transrectal ultrasound-guided transperinealloading. The eighth patient opted for surveillance.
Median follow up after initial LDR-BT for these eightpatients with isolated local recurrence was 88.5 months(range 36–108 months). No patients received ADT after initialLDR-BT before BCR. Seven patients had been initially treatedwith 144 Gy 125-iodine LDR-BT monotherapy, and the
Tab
le1
Dem
ogra
phi
csof
pat
ient
sat
pre
sent
atio
nw
hola
ter
dev
elop
edlo
calr
ecur
renc
eaf
ter
125-
iod
ine
LDR
-BT-
bas
edra
dio
ther
apy
Patie
nts
Age
(yea
rs)
PSA
(ng/
mL)
Stag
eB
iop
syG
leas
on
scor
e
Bio
psy
core
sno
.
pos
itive
/tot
al
Ris
kst
ratifi
catio
nSo
urce
Pro
stat
ic
volu
me
(cc)
V10
0D
90P
SAna
dir
afte
rin
itial
BT
168
11.7
T1c
3+
4=
74/
6In
term
edia
teI-1
2530
.086
.813
5.9
1.20
264
9.5
T1c
3+
3=
65/
6Lo
wI-1
2511
.784
.612
4.7
0.72
368
34.0
T1c
3+
4=
72/
6H
igh
I-125
EBRT
28.8
99.1
–
113.
0
–
0.48
469
7.9
T1c
3+
3=
61/
6Lo
wI-1
2538
.089
.014
2.3
0.78
569
13.8
T1c
3+
4=
75/
6In
term
edia
teI-1
2541
.887
.113
4.8
2.06
666
14.8
T2a
4+
3=
73/
8In
term
edia
teI-1
2530
.798
.118
9.9
0.39
769
6.8
T1c
3+
3=
62/
8Lo
wI-1
2531
.089
.814
3.3
1.69
869
12.2
T2a
4+
3=
73/
8In
term
edia
teI-1
2519
.794
.812
3.9
0.49
Med
ian
68.5
12.0
30.4
89.0
†13
5.9†
0.75
†Pat
ient
no.3
excl
uded
.
Salvage partial brachytherapy
© 2013 The Japanese Urological Association 573
remaining patient had undergone combined modality therapywith partial-dose 110 Gy 125-iodine implantation and 45 Gy ofEBRT. Median follow up after salvage partial LDR-BT forthese seven patients with isolated local recurrence was27 months (range 3–62 months).
Defining CTV at salvage partialprostate brachytherapy
Salvage partial LDR-BT was designed to deliver 144 Gy torecurrent regions, defined as sites of positive biopsy corre-sponding to underdosed areas at initial LDR-BT. The term“underdosed” was understood to mean that the area receivedless than the prescribed dose of radioactivity. As fusion imagingwas not available, the CTV was manually delineated as aregion of local recurrence with biopsy positivity and initialunderdosage according to the MRI imaging and the initial CTdosimetry. The treatment was deliberately designed to reducerectal and urinary morbidity by positioning needles away fromthe urethra and rectal wall. Regions with sufficient coverageduring initial LDR-BT were carefully avoided. The dose wasprescribed to the isodose line covering the CTV. The planningtarget volume included the CTV plus a 5-mm margin (5-mmposterior margin). Prostatic MRI showed no abnormalitiesoutside the targeted area.
Patient follow up
All patients underwent a CT scan for post-implant dosimetry1 month after salvage partial LDR-BT. Post-treatment followup was quarterly for the first 2 years and semiannually there-after, with PSA measurement and rectal examination at eachvisit. Toxicities were recorded using Common Toxicity Criteriaversion 3.0. Written informed consent was obtained from allpatients. Multiple imaging studies, including chest X-ray, CTscan (chest, abdomen), bone scintigraphy and pelvic MRI, werecarried out in cases of BCR (Phoenix definition) to search forclinical recurrence.
Results
Characteristics of isolated local recurrenttumors after initial LDR-BT and/or EBRT
Eight patients were histologically confirmed to have isolatedlocal recurrence of prostate cancer (Table 1). The median timeto BCR was 58.5 months. The median initial PSA was12.0 ng/mL (range 6.8–34.0). At initial LDR-BT, median D90and median V100 were 135.9 Gy (range 123.9–189.9) and89.0% (range 84.6–98.1), respectively. Median nadir PSA levelafter initial LDR-BT was 0.75 ng/mL (range 0.39–2.06).Median PSA level at the time of BCR was 3.66 ng/mL (range2.88–4.39). Of the 12 patients with negative biopsy, fourpatients had declined PSA over a median period of 21.5 monthsafter biopsy (from a median of 3.58 to 0.63 ng/mL). Theremaining patients still sustain rising PSA trend at last followup. The median time to BCR in these 12 patients with negativebiopsy was 26.0 months, and that for four patients with declin-ing PSA after biopsy was 22.5 months, respectively. Positivebiopsy sites were in the anterior base in five patients, posteriorbase in one patient and seminal vesicles in two patients. Theseregions corresponded precisely to the underdosed area at
dosimetry 1 month after initial LDR-BT. No anatomical vari-ations, such as protruding median lobe, were observed in any ofthese cases. The number of positive cores ranged from 1 to 3(median 2), located exclusively in the base (6 patients) andseminal vesicles (2 patients). The maximum cancer lengthranged from 1 to 14 mm (median 7 mm). Only a mild radiationeffect was noted histologically, as defined by Crook et al.12
Assigned Gleason scores were 6–7. MRI was carried out in sixpatients after histological confirmation of recurrence. In five ofthose six patients, MRI findings showed local recurrence ofprostate cancer at the base and/or seminal vesicle (Table 2).These tumors typically appeared as low-intensity lesions onT2WI and high-intensity lesions on DWI, ranging from 10 to18 mm in size. All of these lesions were located in underdosedareas with positive biopsy.
Quality assessment of salvage partial LDR-BT
The median number of seeds for salvage partial LDR-BT was50 (range 20–70). The activity of seeds was 0.29–0.33 mCi perseed. All patients tolerated the procedure well and showeddecreased PSA (median 14.5% at 7 months) (Fig. 1). Twopatients later developed biochemical and clinical progression at11 and 13 months after salvage partial LDR-BT, respectively.The PSA response persisted in the remaining patients. Time toBCR after the initial LDR-BT in the two patients who devel-oped clinical progression was shorter (18 and 27 months,respectively) than in the other five patients. The median PSADTbefore BCR was calculated as log × 2 / the slope of the logPSA line (the difference in the 2 log PSA value divided by thetime between readings in months). For these patients, themedian PSADT before BCR was 13.2 months (range 8.4–32.3 months). The PSADT was 8.4 and 13.3 months, respec-tively, for the two patients with disease progression. Nosignificant genitourinary or gastrointestinal toxicity was noted.
Case presentation
A 69-year-old man with Gleason score 6, T1cN0M0 prostatecancer (patient no. 4 in Tables 1,2) had undergone initialLDR-BT in August 2004. A CT scan 4 weeks after the implantshowed D90 to be 142.3 Gy and V100 to be 89.0%, and showedan underdosed area at the anterior base of the prostate (Fig. 2a).The PSA nadir after LDR-BT was 0.78 ng/mL. BCR was diag-nosed in April 2011; the PSA level was 4.18 ng/mL, and onepositive core was detected at the right anterior base of theprostate. On MRI, the recurrent tumor appeared as a low-intensity lesion on T2WI, and a high-intensity lesion on DWI atthe base (Fig. 2b,c). Salvage partial LDR-BT was carried out inSeptember 2011. The well-defined cold area was re-implantedwith 50 seeds of 125-iodine (Fig. 2d). The post-salvage PSAlevel remained low at 0.06 ng/mL 13 months later. No signifi-cant genitourinary or gastrointestinal toxicity was noted.
Discussion
Optimal patient selection is critical for the success of salvagetherapy after definitive radiotherapy. Identification of candi-dates has been proposed on the basis of pretreatment clinicaland pathological factors, as well as on post-treatment PSAkinetics, such as PSADT.13,14 Stock et al. have analyzed patterns
H SASAKI ET AL.
574 © 2013 The Japanese Urological Association
of failure after LDR-BT for localized prostate cancer,13 andsuggested that time to BCR, Gleason score and PSADT were allpredictive of distant metastases.13 Local therapy should be indi-cated for those with the highest probability of purely localizedrecurrence. Lee et al. reported that ideal candidates for salvagelocal therapy meet the following criteria: (i) low risk at initialtreatment and prediagnostic PSA velocity <2 ng/mL during theyear before diagnosis; (ii) BCR occurred more than 3 yearsafter treatment, PSADT at the time of recurrence >12 monthsand low absolute PSA value before initiating salvage localtherapy (<1 ng/mL).14
Accurate diagnosis of local recurrence can sometimes beconfounded by the well-known PSA bounce phenomenon afterradiotherapy.15 BCR was diagnosed in 45 men at a median of30 months after initial LDR-BT in the present study. Of the 20patients who agreed to have prostatic biopsy, eight were diag-nosed with isolated local recurrence of prostate cancer. Inter-estingly, four patients with negative biopsy later showeddeclined PSA, suggesting the possibility of PSA bounce. Diag-nosis of BCR and indication of biopsy need to be furtherrefined.
Seven of those eight with positive biopsy subsequentlyunderwent salvage partial LDR-RT. Two of those patients laterdeveloped distant metastases. Both had less time to BCR and ashorter PSADT than any of the other five patients. The use ofsystemic therapy, such as simultaneous ADT, or some investi-gational protocol-based therapy might be an option for suchpatients with peculiar PSA kinetics. Awareness and more timelydiagnosis should maximize treatment efficacy for better diseasecontrol.
Of the several available options, salvage partial LDR-BTcould be the treatment of choice for certain patients with BCR.In the present study, the prostatic base was the most commonregion for biopsy positivity (6/8 patients). This region is oftenunderdosed and thus undertreated.8 Difficulty in identifying anddelineating the boundary between prostate and seminal vesi-cles, especially in cases of median lobe protrusion, could leadto planning errors that account for this tendency. Appropriateseed placement at the base of the gland can also be technicallychallenging. In the present study, for eight patients, according
Tab
le2
Clin
icop
atho
logi
calfi
ndin
gsof
pat
ient
sw
ithlo
calr
ecur
renc
eaf
ter
125-
iod
ine
LDR
-BT-
bas
edra
dio
ther
apy
Patie
nts
PSA
atB
CR
(ng/
mL)
Tim
eto
BC
R
(mon
ths)
PSA
DT
(mon
ths)
MR
Ifind
ing
T2W
and
DW
Bio
psy
core
sno
.
pos
itive
/tot
al
Bio
psy
pos
itive
loca
tion
Bio
psy
Gle
ason
scor
e
Bio
psy
max
imum
canc
er
leng
th(m
m)
Txaf
ter
BC
R
Tim
eto
sal
BT
afte
r
initi
alB
T
(mon
ths)
SalB
T,
num
ber
ofse
eds
Rec
afte
r
salB
T
Follo
wup
afte
rsa
lBT
(mon
ths)
PSA
atla
st
follo
wup
(ng/
mL)
13.
9060
13.1
–1/
12R
tSV
3+
31
SalB
T70
30–
382.
12
22.
8818
8.4
NA
2/22
Ant
bas
e3
+4
8Sa
lBT
3120
+(1
3m
)62
4.6†
33.
1065
18.4
+1/
23A
ntb
ase
4+
37
SalB
T82
6514
0.35
44.
1880
10.3
+1/
22A
ntb
ase
3+
47
SalB
T85
50–
130.
06
54.
3927
13.3
NA
3/22
Post
bas
e4
+3
14Sa
lBT
3030
+(1
1m
)54
0.11
†
63.
4157
16.4
+1/
22Lt
SV3
+4
6Sa
lBT
6050
–27
0.14
73.
9270
32.3
+2/
22A
ntb
ase
3+
35
SalB
T82
70–
30.
70
83.
1336
9.0
+2/
22A
ntb
ase
4+
38
Surv
eilla
nce
––
––
–
Med
ian
3.66
58.5
13.2
770
5027
†Pat
ient
no.2
and
no.5
wer
egi
ven
horm
one
ther
apy
afte
rth
ere
curr
ence
afte
rsa
lvag
ep
artia
lLD
R-B
T.
0
2
4
6
8
10
12
14
16
0 10 20 30 40
PSA
(ng/
mL)
Time after salvage regional LDR-BT (months)
Fig. 1 Changes of PSA with time after salvage regional LDR-BT. , Pt1; ,
Pt2; , Pt3; , Pt4; , Pt5; , Pt6; , Pt7.
Salvage partial brachytherapy
© 2013 The Japanese Urological Association 575
to Table 2, the median time to BCR was 58.5 months, which ismuch more in keeping with local failure. Six of the eightpatients with local recurrence were treated when we were stillrelatively inexperienced with this procedure (<150 cases). Thisre-emphasizes the importance of initial treatment, which shouldbe carried out with care. The development of a practical real-time dosimetry system should improve dose distribution byidentifying isodose holes intraoperatively, so that more seedscan be added immediately in the affected regions.16
Two patients were diagnosed with tumor recurrence in theseminal vesicles (patient no. 1 and 6). As seminal vesicles hadnot been included in the target volume at the initial LDR-BT,salvage partial LDR-BT was thought to offer a second chance
for a cure. Seeds were successfully placed with no sign ofmigration, possibly because of desmoplasia in the surroundingtissue. PSA decreased after the procedure. An intraprostatic“cold spot” at the base beside the urethra was noted in patientno. 3, despite the successful dosimetry of V100 and D90 valuesof LDR-BT. Time to BCR was 65 months after initial LDR-BT.The cause is not readily certain; however, EBRT coveragemight have been suboptimal for this high-risk disease.
Because all tumors were diagnosed in the underdosed areas,undertreatment was thought to be the primary cause of recur-rence. However, aggressive radioresistant clones in the primarycancer can give rise to longer-term tumor recurrence(radiorecurrence). Correct and timely identification of localrecurrence is ideal for establishing effective treatment strat-egies. Multiparametric MRI techniques, which include T2WI,DWI, dynamic contrast enhanced imaging and MR spectros-copy, are expected to encourage efficient diagnosis of locallyrecurrent prostate cancer after EBRT.17–19 These techniquesmight prove clinically useful by identifying individual localizedfoci within the prostate to facilitate focal salvage therapy.20
After radiotherapy, the prostate generally shows low signalintensity in T2-weighted images because of fibrotic changes inthe gland.21 In the present study, with the use of T2WI and DWIMRI, five out of six patients showed positive findings indica-tive of local recurrence, corresponding to positive biopsy/underdosed areas. More effective imaging technology is clearlyrequired for thorough evaluation of the prostate outside theunderdosed area. With better imaging options, template typetransperineal biopsy mapping to localize disease might becomeunnecessary in the future.
The present study had several limitations. First, this studywas carried out in a single institution and was small in size, asonly a fraction of the patients with BCR had prostatic biopsy.Second, the appropriateness of salvage partial therapy has notyet been established. Though biopsy-positive underdosed areaswere targeted in the present study, we do not know if this formof targeting can provide a robust response or can be applied toradiorecurrent lesions previously covered with sufficientdosage at initial LDR-BT. Further collaborative work is war-ranted in order to establish a logical approach to the treatmentof recurrent tumors after radiotherapy.
In conclusion, seven patients underwent salvage partialLDR-BT. At a median follow up of 27 months, PSA levelsremained under control in five (71.4%). Salvage partialLDR-BT for biopsy-proven localized prostate cancerrecurrence with the corresponding underdosed area is a rationaland practical approach for local control of the disease.
Acknowledgment
This study was supported in part by a SHIP0804 grant(NCT00664456).
Conflict of interest
None declared.
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(a)
(b)
(d)
(c)
Fig. 2 A case of local recurrence of prostate cancer after primary 125-iodine
LDR-BT (patient no. 4 in Tables 1,2). (a) The dosimetry on CT-imaged axial slices of
the prostatic gland after initial LDR-BT (light green line showing prescribed dose,
144 Gy, red line showing contouring of the prostate, yellow arrows showing
underdosed area). (b) Axial T2WI of MRI after BCR, the recurrent tumor appears
as a low-intensity lesion (arrow). (c) DWI of MRI, the recurrent tumor appears as
a high-intensity lesion (arrow). (d) The dosimetry on CT-imaged axial slices of the
prostatic gland after salvage.
H SASAKI ET AL.
576 © 2013 The Japanese Urological Association
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© 2013 The Japanese Urological Association 577