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Japanese Journal of Clinical Oncology Advance Access originally published online on July 11, 2008
Japanese Journal of Clinical Oncology 2008 38(7):474-479; doi:10.1093/jjco/hyn056
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© The Author (2008). Published by Oxford University Press. All rights reserved

Comparison of the Outcome and Morbidity for Localized or Locally Advanced Prostate Cancer Treated by High-dose-rate Brachytherapy Plus External Beam Radiotherapy (EBRT) Versus EBRT Alone

Fu-Min Fang1, Yu-Ming Wang1, Chong-Jong Wang1, Hsuan-Ying Huang2 and Po-Hui Chiang3

1 Department of Radiation Oncology, Chang Gung Memorial Hospital, Kaohsiung Medical Center, Chang Gung University College of Medicine, Niao Sung Hsian, Kaohsiung Hsien
2 Department of Pathology, Chang Gung Memorial Hospital, Kaohsiung Medical Center, Chang Gung University College of Medicine, Niao Sung Hsian
3 Department of Urology, Chang Gung Memorial Hospital, Kaohsiung Medical Center, Chang Gung University College of Medicine, Niao Sung Hsian, Kaohsiung Hsien, Taiwan

For reprints and all correspondence: Po-Hui Chiang, Department of Urology, Chang Gung Memorial Hospital, Kaohsiung Medical Center, 123 Ta-Pei Road, Niao Sung Hsian, Kaohsiung Hsien, Taiwan. E-mail: fang2569{at}adm.cgmh.org.tw

Received March 27, 2008; accepted June 3, 2008


   Abstract
TOP
 Abstract
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 References
 
Objective: To compare the survival, gastrointestinal (GI) and genitourinary (GU) toxicity for localized or locally advanced prostate cancer treated by high-dose-rate-brachytherapy (HDR-BT) plus external beam radiotherapy (EBRT) versus EBRT alone at a single institute in Taiwan.

Methods: Eighty-eight patients with T1c–T3b prostate cancer consecutively treated by EBRT alone (33 patients) or HDR-BT+EBRT (55 patients) were studied. The median dose of EBRT was 70.2 Gy in the EBRT group and 50.4 Gy in the HDR-BT group. HDR-BT was performed 2–3 weeks before EBRT, with 12.6 Gy in three fractions over 24 h.

Results: Five patients (15.2%) in the EBRT group and seven (12.7%) in the HDR-BT group developed a biochemical relapse. The 5-year actuarial biochemical relapse-free survival rates were 65.0% in the EBRT group and 66.7% in the HDR-BT group (P = 0.76). The 5-year actuarial likelihood of late ≥Grade 2 and ≥Grade 3 GI toxicity in the EBRT versus HDR-BT group was 62.8 versus 7.7% (P < 0.001) and 19.6 versus 0% (P = 0.001), respectively. In a multivariate analysis, the only predictor for late GI toxicity was the mode of RT. The 5-year actuarial likelihood of late ≥Grade 2 and ≥Grade 3 GU toxicity in the EBRT versus HDR-BT group was 14.8 versus 15.9% (P = 0.86) and 3.6 versus 8.5% (P = 0.40), respectively.

Conclusions: The addition of HDR-BT before EBRT with a reduced dose from the EBRT produces a comparable survival outcome and GU toxicity but a significantly less GI toxicity for prostate cancer patients.

Key Words: high-dose-rate brachytherapy • external beam radiotherapy • prostate cancer


   INTRODUCTION
TOP
 Abstract
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 References
 
With the increasing use of a high-fat diet, population aging and cancer screening by prostate-specific antigen (PSA), the incidence of adenocarcinoma of the prostate has rapidly increased in past 10 years in Taiwan (1). The standard curative treatment of localized prostate cancer used to be radical prostatectomy, with radiotherapy (RT) usually being limited to the elderly or cases with locally advanced tumors. However, with the expanding evidence of the competitive results of RT versus surgery being reported in the literature (2–5), the choice of external beam RT (EBRT) or brachytherapy (BT) as a reliable treatment strategy for the disease has been increasing in this country (1,7,8).

High-dose-rate-BT (HDR-BT) applies advanced technology to the delivery of iridium192 and technically allowing the user to modulate the radiation intensity by controlling the time and position of the radioisotope (5,6). At the Department of Radiation Oncology in Kaohsiung Chang Gung Memorial Hospital, a Tertiary Medical Center in Taiwan, we treated patients with localized or locally advanced prostate cancer either by EBRT alone or HDR-BT+EBRT. In this study, we retrospectively analyzed the survival outcome, gastrointestinal (GI) and genitourinary (GU) toxicities, and their prognostic factors for these patients.


   MATERIALS AND METHODS
TOP
 Abstract
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 CONCLUSION
 References
 
From January 1998 to June 2003, there were 88 consecutive patients with pathologically proven T1c–T3b adenocarcinoma of the prostate curatively treated by EBRT alone (33 patients) or HDR-BT+EBRT (55 patients) in the department. The choice of HDR-BT or not was non-randomized, but mostly followed the patients’ preference, the suitability of epidural anesthesia, and the referring urologists’ capability of doing the procedure of prostate implantation. The hospital’s review board approved the study. According to the classification by D’Amico et al. (9), the distributions of low, intermediate and high-risk features were six (18.2%), four (12.1%) and 23 (79.7%), respectively, in the EBRT group, and nine (16.4%), 12 (21.8%) and 34 (61.8%), respectively, in the HDR-BT group. Sixty-two (70.5%) patients received hormonal therapy as neoadjuvant, concurrent and/or adjuvant treatment. The decision to use androgen ablation was mostly taken in patients with high-risk features. Androgen deprivation in the form of luteinising-hormone releasing hormone agonist and/or anti-androgen was used. The duration of hormone therapy was not consistent in the cohort, with a median month of 19 months (range: 1–47 months). As shown in Table 1, there was no statistically significant difference in the distributions of age, Gleason score, clinical stage, baseline PSA, risk features or the use of hormone therapy between the two groups. The only exception was that 21 (63.6%) patients in the EBRT group versus 15 (27.3%) patients in the HDR group had been treated with transurethral prostatectomy (TURP).


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  		Table 1. Characteristics of patients treated by EBRT alone versus HDR-BT+EBRT

 
For EBRT, the immobilization for prostate cancer patients was in a supine position by a thermoplastic cast, without special instructions for bladder or bowel filling. The treatment target and organs at risk, such as the rectum and bladder, were delineated on the CT images performed on the CT simulator. The treatment target arbitrarily included 0–5 mm around the prostate and seminal vesicles. Additional 1.5 cm expansions in all directions of the volume were made to yield the planning target volume to overcome the uncertainty in immobilization of patients and beam placements. All patients were treated with a rectangular four field technique by 10 or 15 MV photon beam. The treatment planning system (Pinnacle, Miwaki) was used for dose calculation, and the treatment plans were delivered in a linear accelerator (10 or 15 MV X-rays) equipped with multi-leaf collimators. The dose/fractionation regimen was 45.0–54.0 Gy with 1.8 Gy per fraction at the isocenter, 5 days a week, for both groups. For patients treated by EBRT alone, a coned down boost excluding the seminal vesicle (except 11 cases with clinically suspected T3b stage) was followed to a total dose of 64.8–70.2 Gy in T1–T2 cases and 72.0–75.6 Gy in T3 cases, respectively. The treatment fields and isodose distributions of the target, rectum and bladder in one patient were demonstrated in Fig. 1.


Figure 1
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  		Figure 1. The (a) anterior–posterior and (b) right-lateral fields and (c, d) the isodose distributions of two axial planes in one patient with T2 stage prostate carcinoma irradiated by a rectangular four-field technique. B, Bladder; P, Prostate; R, Rectum; S, Seminal vesicle.

 
The detailed procedures of HDR-BT have been described previously (8). Briefly, after placed in a lithotomy position with epidural anesthesia, the patients were inserted with multiple 20- or 18-cm long closed-end, 1.9-mm diameter needles by using a perineal template. After the procedure in the operation room, the patients were transferred to the Department of Radiation Oncology, and a CT scan was used to identify the actual needle positions within the prostate tissue. Basically, the tips of the needles should be into at least 0.5 cm of the bladder mucosal wall. The Plato BT Planning System (Nucletron, Netherlands) was used for the treatment planning. The treatment target covered the whole prostate with 0–5 mm margin. After delineating the target as well as the critical structures such as the urethra, bladder and rectum, an optimal iridium192 source distribution plan was devised for the individual patient. Fifty-two patients (96%) were given 4.2 Gy per fraction at the 100% isodose curve. The urethral dose line was limited to below 125% of the maximal prescribed dose. Treatments were delivered in three fractions over a 2-day period, and the needles were removed immediately after the last treatment. At the commencement of the technique, some modifications of the prescribed dose to 4.0 Gy per fraction were carried out in three patients for the unsatisfactory dose distribution. The EBRT was initiated 2–3 weeks after the completion of HDR-BT.

The median follow-up was 58 months (range, 5–84 months) in the EBRT group and 56 months (range, 8 to 82 months) in the HDR-BT group, respectively. Disease status and late complications were determined as of the time of analysis in June 2007. Biochemical relapse was defined according to the updated American Society for Therapeutic Radiology and Oncology consensus: a Nadir+2 with ‘at call’ dating (10). Acute and late treatment complications, graded according to the morbidity grading system of the Radiation Therapy Oncology Group/European Organization for Research and Treatment of Cancer criteria (11). Time-adjusted rates of the appearance of the late complications and biochemical relapse-free survival were calculated using the Kaplan–Meier method. The log-rank test was used to analyze the differences between multiple survival curves or time-adjusted incidence rates. The Cox proportional hazards regression model was used for multivariate analysis. The software, Microsoft SPSS-12.0, was used for data processing.


   RESULTS
TOP
 Abstract
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 CONCLUSION
 References
 
Biochemical Relapse-free Survival
Five patients (15.2%) in the EBRT group and seven patients (12.7%) in the HDR-BT group developed a PSA relapse, with corresponding 5-year actuarial biochemical relapse-free survival rates 65.0 and 66.7%, respectively (P = 0.76) (Fig. 2a). In multivariate analysis, risk features were found to be significant prognostic factors on biochemical relapse-free survival (Table 2). The 5-year actuarial biochemical relapse-free survival rates were 52.2% in patients with high-risk features, compared with 93.3 and 93.8% in patients with low- and intermediate-risk features (P = 0.001).


Figure 2
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  		Figure 2. Comparisons of (a) biochemical relapse-free survival, (b) late ≥Grade 2 GI toxicity and (c) late ≥Grade 2 GU toxicity for prostate cancer patients treated by three dimensional conformal radiotherapy (3DCRT) alone versus HDR-BT+3DCRT. EBRT, external beam radiotherapy; HDR-BT, high-dose-rate brachytherapy.

 

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  		Table 2. Cox regression analysis of variables affecting biochemical relapse-free survival

 
GI Toxicity
Fourteen patients (42%) in the EBRT group, compared with seven patients (13%) in the HDR-BT group had acute Grade 2 GI toxicity (P = 0.004). Thirteen patients (39%) in the EBRT group and four patients (7%) in the HDR-BT group experienced late Grade 2 GI toxicity (rectal bleeding), which required conservative medication such as cortisone enemas. Six patients (19%) in the EBRT group versus no patients in the HDR-BT group had late Grade 3 GI toxicity, which required blood transfusion or minor surgical intervention. The 5-year actuarial likelihood of developing late ≥Grade 2 and ≥Grade 3 GI toxicity in the EBRT group versus the HDR-BT group was 62.8 versus 7.7% (P < 0.001, Fig. 2b) and 19.6 versus 0% (P = 0.001), respectively. No late Grade 4 GI toxicity was observed in either group.

As shown in Table 3, the only predictor for late ≥Grade 2 GI toxicity was the mode of RT (EBRT versus HDR-BT). In this Cox regression model, patients treated with HDR-BT had 9.7 times (95% CI: 2.9–32.3) lower probability to develop late ≥Grade 2 GI toxicity, whereas the AJCC stage, risk features, prior TURP, hemorrhoids, age and hormone therapy had no significant impact on this endpoint.


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  		Table 3. Cox regression analysis of variables affecting late Grade 2 or higher gastrointestinal toxicity

 
GU Toxicity
Nine patients (27.3%) in the EBRT compared with 17 patients (30.9%) in the HDR-BT group had acute Grade 2 GU toxicity (P = 0.75). Acute urinary retention caused by urethral stricture (Grade 3) occurred in one patient (1.8%) after HDR-BT and necessitated urethrotomy. No Grade 3 acute GU toxicity was observed in the EBRT group. Two patients in the EBRT group developed late Grade 3 GU toxicity (radiation cystitis with gross hematuria) 3 years after irradiation, and four patients in the HDR-BT group developed late Grade 3 GU toxicity, including one radiation cystitis and three urethral stricture. No late Grade 4 GU toxicity was observed in either group. The 5-year actuarial likelihood of developing late ≥Grade 2 and ≥Grade 3 GU toxicity in the EBRT group versus the HDR-BT group was 14.8 versus 15.9% (P = 0.86) and 7.2 versus 8.6% (P = 0.78), respectively (Fig. 2c). As concerns the 37 patients with prior TURP, the 5-year actuarial likelihood of developing late ≥Grade 2 and ≥Grade 3 GU toxicity in the EBRT group versus the HDR-BT group was 14.7 versus 15.4% (P = 0.97) and 5.3 versus 7.0% (P = 0.70), respectively (Fig. 3).


Figure 3
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  		Figure 3. Comparisons of late ≥Grade 2 GU toxicity for prostate cancer patients treated by prior transurethral prostatectomy followed by 3DCRT alone (n = 21) versus HDR-BT+3DCRT (n = 15).

 

   DISCUSSION
TOP
 Abstract
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
CONCLUSION
 References
 
BT is well established as a treatment modality for localized prostate cancer and has advantages over EBRT when there are uncertainties of organ motion during protracted multiple fractionations. For locally advanced disease, however, there are concerns when using BT as a monotherapy, as it may not give an adequate dose to the peri-prostatic tissue with the risk of microscopic tumor spread. In this setting, BT may be optimally used as a boost to the prostate in combination with EBRT. In the current study, the addition of HDR-BT before EBRT with a reduced dose of the EBRT was observed to produce comparable survival outcomes and GU toxicity, but a significant therapeutic benefit in reducing both acute and late GI toxicity.

This result was supported by two recently published reports. Soumarova et al. observed the combination of EBRT with HDR-BT resulted in a lower acute GI toxicity but a comparable GU toxicity than EBRT alone (12). Hoskin et al. compared the regimen of hypofractionated EBRT with 55 Gy in 20 fractions with that of 35.75 Gy in 13 fractions followed by a HDR-BT boost of 17 Gy in two fractions, and observed that a dose escalation by HDR-BT in combination with EBRT resulted in an improved biochemical relapse-free survival compared with EBRT alone with less acute rectal toxicity and improved quality-of-life (13).

The explanation of high late GI toxicity in those treated by EBRT alone was that a conventional rectangular four field technique to irradiate the prostate and seminal vesicle with additional 1.5 cm expansions in all directions might easily cause the inevitable overlap of radiation target with the anterior rectal wall (see Fig. 1). The volume of the rectum receiving a high radiation dose was observed to be a determining factor for the occurrence of late rectal toxicity (14,15). The dose gradient between prostate and rectum was observed to be steeper in HDR-BT than that in EBRT, which might explain the lower rectal toxicity if the boost phase was performed by HDR-BT. More detailed analysis of the dose-volume histogram and complication data will allow us to test the models of these normal tissue complication probabilities in our patients. Such analysis might help us to assess the relative contributions of EBRT and/or HDR-BT in the complications. Eventually, we could use these data to tailor the dose prescription of each modality for the individual patient. Some models in predicting rectal toxicity have been attempted in prostate cancer treated with EBRT (16,17). However, a model to fit both EBRT and BT, which produce different biological effects in normal tissues, has not been well established yet, but this is needed if the complications contributed by EBRT and HDR-BT are to be compared.

A history of TURP remains an important consideration when evaluating a patient for BT. TURP defect was regarded as a relative contraindication for permanent seed implantation, because no dose will be given in the area of defect. The study by Zelefsky et al. showed that the presence of a TURP defect posed a 25% overall risk of urinary incontinence at 6 years, for permanent seed implantation (18). Under this background, many published studies of HDR-BT in prostate cancer have excluded patients with prior TURP and patients with such condition were usually recommended to receive EBRT alone. In contrast, a recent report by Peddada et al. showed low GI and GU morbidities for patients treated with TURP followed by HDR-BT+EBRT (19). For the 37 patients with prior TURP in our study, we also observed the late GU toxicity was comparable for patients treated by EBRT alone versus HDR-RT+EBRT.

Other than the dosimetric effects, some variables such as pre-treatment existing diabetes or hemorrhoids, or the use of hormone therapy have been reported to be associated factors for the development of late radiation toxicity in prostate cancer patients (20,21). Put into multivariate analysis, these confounding variables did not reveal to be significantly correlated with the GI or GU toxicity in our patients either treated with EBRT alone or EBRT+HDR-BT.


   CONCLUSION
TOP
 Abstract
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
References
 
We may not make a conclusive suggestion of which RT modality is more advantageous than the others simply from our results and limited reports in literature, unless a randomized, multi-institutional and prospective trial can prove it. However, for a single academic institution capable of performing some of the various RT modalities, we conclude that the addition of HDR-BT before EBRT with a reduced dose from the external beams reduced the GI toxicity without compromising biochemical relapse-free survival or GU toxicity.

Conflict of interest statement

None declared.


   References
TOP
 Abstract
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 References
 
1 Republic of China Department of Health. Cancer Registry Annual Report. (2003) Taipei, Taiwan, Republic of China: Department of Health, Executive Yuan.

2 Peschel RE, Colberg JW. Surgery, brachytherapy, and external-beam radiotherapy for early prostate cancer. Lancet Oncol (2003) 4:233–41.[CrossRef][Web of Science][Medline]

3 Dearnaley DP, Khoo VS, Norman AR, Meyer L, Nahum A, Tait D, et al. Comparison of radiation side-effects of conformal and conventional radiotherapy in prostate cancer: a randomized trial. Lancet (1999) 353:267–72.[CrossRef][Web of Science][Medline]

4 Zelefsky MJ, Wallner KE, Ling CC, Raben A, Hollister T, Wolfe T, et al. Comparison of the 5-year outcome and morbidity of three-dimensional conformal radiotherapy versus transperineal permanent iodine-125 implantation for early-stage prostatic cancer. J Clin Oncol (1999) 17:517–22.[Abstract/Free Full Text]

5 Mate TP, Gottesman JE, Hatton J, Gribble M, Van Hollebeke L. High dose-rate afterloading 192Iridium prostate brachytherapy: feasibility report. Int J Radiat Oncol Biol Phys (1998) 41:525–33.[CrossRef][Web of Science][Medline]

6 Akimoto T, Katoh H, Noda SE, Ito K, Yamamoto T, Kashiwagi B, et al. Acute genitourinary toxicity after high dose rate (HDR) brachytherapy combined with hypofractionated external-beam radiation therapy for localized prostate cancer: second analysis to determine the correlation between the urethral dose in HDR brachytherapy and the severity of acute genitourinary toxicity. Int J Radiat Oncol Biol Phys (2005) 63:472–8.[Web of Science][Medline]

7 Chen YC, Chuang CK, Hsieh ML, Chen WC, Fan KH, Yeh CY, et al. High-dose-rate brachytherapy plus external beam radiotherapy for T1 to t3 prostate cancer: an experience in Taiwan. Urology (2007) 70:101–5.[Web of Science][Medline]

8 Chiang PH, Fang FM, Wang CJ, Yu TJ, Chuang YC, Wang HJ. High-dose rate iridum-192 brachytherapy and external beam radiation therapy for prostate cancer with or without androgen ablation. Int J Urol (2004) 11:152–8.[CrossRef][Web of Science][Medline]

9 D’Amico AV, Desjardin A, Chung A, Chen MH. Assessment of outcome prediction models for localized prostate cancer in patients managed with external beam radiation therapy. Semin Urol Oncol (1998) 16:153–9.[Medline]

10 Roach M III, Hanks G, Thames H Jr, Schellhammer P, Shipley WU, Sokol GH, et al. Defining biochemical failure following radiotherapy with or without hormone therapy in men with clinically localized prostate cancer: recommendations of the RTOG-ASTRO Phoenix Consensus Conference. Int J Radiat Oncol Biol Phys (2006) 65:965–74.[CrossRef][Web of Science][Medline]

11 Rubin P, Constine LS, Fajardo LF, Phillips TL, Wassweman TH. RTOG Late Effects Working Group. Overview. Late Effects of Normal Tissue (LENT) scoring system. Int J Radiat Oncol Biol Phys (1995) 31:1041–2.[CrossRef][Web of Science][Medline]

12 Soumarová R, Homola L, Perková H, Stursa M. Three-dimensional conformal external beam radiotherapy versus the combination of external radiotherapy with high-dose rate brachytherapy in localized carcinoma of the prostate: comparison of acute toxicity. Tumori (2007) 93:37–44.[Web of Science][Medline]

13 Hoskin PJ, Motohashi K, Bownes P, Bryant L, Ostler. High dose rate brachytherapy in combination with external beam radiotherapy in the radical treatment of prostate cancer: initial results of a randomized phase three trial. Radiother Oncol (2007) 84:114–20.[CrossRef][Web of Science][Medline]

14 Storey MR, Pollack A, Zagars G, Smith L, Antolak J, Rosen I. Complications from radiotherapy dose escalation in prostate cancer: preliminary results of a randomized trial. Int J Radiat Oncol Biol Phys (2000) 48:635–42.[CrossRef][Web of Science][Medline]

15 Wachter S, Gerstner N, Goldner G, Pötzi R, Wambersie A, Pötter R. Rectal sequelae after conformal radiotherapy of prostate cancer: dose-volume histograms as predictive factors. Radiother Oncol (2001) 59:65–70.[CrossRef][Web of Science][Medline]

16 Tucker SL, Cheung R, Dong L, Liu HH, Thames HD, Huang EH, et al. Dose-volume response analyses of late rectal bleeding after radiotherapy for prostate cancer. Int J Radiat Oncol Biol Phys (2004) 59:353–65.[Web of Science][Medline]

17 Peters ST, Hoogeman MS, Heemsbergen WD, Hart AA, Hoogeman MS, Lebesque JV. Rectal bleeding, fecal incontinence, and high stool frequency after conformal radiotherapy for prostate cancer: normal tissue complication probability modeling. Int J Radiat Oncol Biol Phys (2006) 66:11–9.[Web of Science][Medline]

18 Zelefsky MJ, Lyass O, Fuks Z, Wolfe T, Burman C, Ling CC, et al. Predictors of improved outcome for patients with localized prostate cancer treated with neoadjuvant androgen ablation therapy and three-dimensional conformal radiotherapy. J Clin Oncol (1998) 16:3380–5.[Abstract]

19 Peddada AV, Jennings SB, Faricy PO, Walsh RA, White GA, Monroe AT. Low morbidity following high dose rate brachytherapy in the setting of prior transurethral prostate resection. J Urol (2007) 178:1963–7.[CrossRef][Web of Science][Medline]

20 Herold DM, Hanlon AL, Hanks GE. Diabetes mellitus: a predictor for late morbidity. Int J Radiat Oncol Biol Phys (1999) 43:473–4.[Web of Science][Medline]

21 Vavassori V, Fiorino C, Rancati T, Magli A, Fellin G, Baccolini M, et al. Predictors for rectal and intestinal acute toxicity during prostate cancer high-dose 3D-CRT: results of a prospective multicenter study. Int J Radiat Oncol Biol Phys (2007) 67:1401–10.[Web of Science][Medline]


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