failure (FBF) rates were calculated using the Phoenix definition.
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1 . JOURNAL COMPILATION 2009 BJU INTERNATIONAL Urological Oncology GLEASON SCORES 8 10 PROSTATE CANCER TREATED WITH TRIMODAL THERAPY STOCK et al. BJUI BJU INTERNATIONAL Outcomes for patients with high-grade prostate cancer treated with a combination of brachytherapy, external beam radiotherapy and hormonal therapy Richard G. Stock, Jamie A. Cesaretti, Simon J. Hall* and Nelson N. Stone* Departments of Radiation Oncology and *Urology, Mount Sinai School of Medicine, New York, NY, USA Accepted for publication 18 March 2009 Study Type Therapy (case series) Level of Evidence 4 OBJECTIVE To assess the outcomes for patients with Gleason score 8 10 prostate cancer treated with brachytherapy, external beam radiotherapy (EBRT) and hormonal therapy (HT). PATIENTS AND METHODS In all, 181 patients with Gleason scores 8 10 prostate cancer were treated from 1994 to 2006 with a 103 Pd implant (prescription dose 100 Gy), 45 Gy of EBRT and 9 months of HT. The median (range) follow-up was 65 (24 150) months; freedom from biochemical failure (FBF) rates were calculated using the Phoenix definition. RESULTS The 8-year actuarial FBF, freedom from distant metastases, prostate-cancer specific survival and overall survival were 73%, 80%, 87% and 79%, respectively. The pretreatment prostate-specific antigen (PSA) level significantly affected FBF, with 8-year rates of 72%, 82% and 58% for patients with PSA level of 10, >10 20 and >20 ng/ ml, respectively (P = 06). The PSA level had no significant effect on rates of distant metastases. The Gleason score had the most significant affect on FBF in a multivariate analysis, and was the only factor to significantly affect rates of distant metastases; the 8-year FBF rates were 84%, 55% and 30% for scores of 8, 9 and 10, respectively (P = 03). The corresponding freedom from distant metastases and prostate-cancer specific survival rates were 86%, 76%, 30% (P < 01) and 92%, 80%, 62.5% (P = 03), respectively. CONCLUSIONS The 8-year outcomes after this regimen showed favourable biochemical and distant control, as well disease-specific survival rates for patients with Gleason scores of This treatment approach should be considered as a viable option for this subset of patients with high-risk disease. KEYWORDS prostate cancer, Gleason score 8 10, brachytherapy, external beam radiotherapy, hormonal therapy INTRODUCTION The Gleason scoring system for grading prostate cancer has been shown to be a highly significant predictor of treatment outcomes. Gleason scores of 8 10 represent a more aggressive form of the disease and are used to classify patients as high risk, by the National Cancer Care Network (available at High-grade cancer poses an increased risk for both biochemical and distant failure. Standard therapy for this disease, radical prostatectomy (RP) and conventional external beam radiotherapy (EBRT), have resulted in suboptimal biochemical control rates. EBRT using conventional doses and techniques has yielded biochemical disease-free survival rates of 5 23% at up to 10 years after treatment [1 4]. The reported biochemical control rates after RP for patients with Gleason scores of 8 10 are 27 39% [5 8]. The cause for these high failure rates might be the presence of microscopic systemic disease or poor local disease control. For RP, findings of positive margins on the pathological specimen or extraprostatic disease can be seen as surrogates for inadequate local control. In one large series, the likelihood of obtaining negative margins and organconfined disease was only 21% for patients with Gleason scores of 8 10 [9]. For conventional EBRT the best method for assessing local control is a prostate biopsy after treatment; reported positive biopsy rates are 18 62% [10 13], and the rate was 64% for high-grade cancers in a series by Dugan et al. [11]. To address some of the limitations of more standard therapies, a combined approach using hormonal therapy (HT), EBRT and lowdose rate prostate brachytherapy was developed to treat patients with locally advanced prostate cancer, with the goal of enhancing local control [14]. Treatment outcomes after this regimen for patients with Gleason scores of 8 10 are reported to determine whether this treatment can maximize local tumour eradication, and in doing so improve biochemical freedom from failure (FBF), reduce distant metastases and enhance prostate cancer-specific survival (CSS). In addition, the effect of several JOURNAL COMPILATION 2009 BJU INTERNATIONAL 104, doi: /j x x 1631
2 STOCK ET AL. disease- and treatment-related factors on outcomes were tested to determine potential prognostic subgroups. PATIENTS AND METHODS In all, 181 patients with prostate cancer and biopsy Gleason scores of 8 10 were treated with combined therapy between 1994 and 2006 at Mount Sinai Medical Center in New York. The median (range) age of the patients was 69 (39 88) years. All patients were staged using the American Joint Committee on Cancer/International Union Against Cancer TNM classification [15]. The presenting disease characteristics are shown in Table 1. All patients had negative CT findings and bone scans. Bilateral seminal vesicle biopsies were taken in 116 patients and 29 had positive results; 31 patients had laparoscopic pelvic lymph node dissections and three had positive nodes. Patients were treated with a combination of HT, prostate brachytherapy and EBRT; the typical sequence was 3 months of HT with an LHRH agonist (±an antiandrogen) followed by a brachytherapy implant of the prostate (±seminal vesicles). Two months latter, EBRT was delivered with concomitant HT. The recommended total duration of HT was 9 months; the actual time on HT was 9 months in 163 patients, 1 year in seven and 2 years in 11. The actual time on HT was dictated by the referring urologist s discretion or patient compliance. The isotope 103 Pd was used in all patients; since 1998, the prescription dose for 103 Pd has been 100 Gy (National Institute of Standards and Technology 99). In the earlier years of the study, lower implant doses were used with higher EBRT doses. The median (range) of implant prescription doses was 100 (63 100) Gy, and of EBRT dose was 45 ( ) Gy, all given in 1.8-Gy fractions. EBRT doses were 41.4 Gy in 3%, 45 Gy in 81% and >45 Gy in 16%. Three-dimensional conformal and intensity-modulated techniques were used to deliver the EBRT. The fields included the prostate and seminal vesicles, plus margin and pelvic nodes for those with positive nodes. CT-based dosimetry was done at 1 month after implantation; the dose delivered to 90% of the prostate (D90) values were calculated using the dose volume histogram. All doses were converted to biologically effective doses (BED), which were calculated using the total EBRT dose as well as the D90 of the implants. The α/β ratio used for these calculations was 2.0. Details of these equations were described previously [16]. The mean (range) BED for the treatments ranged was 206 ( ) Gy 2. All patients were followed at 6-month intervals after treatment; the median (range) follow-up was 65 (24 150) months. The biochemical control rates were calculated using the Phoenix definition [17]. The PSA doubling time was calculated using first-order kinetics. Distant metastasis was defined as radiographic or pathologically determined evidence of disease outside the pelvis, which included bone, visceral organ, or nodal disease. Prostate-cancer specific death was defined as a patient dying with the presence of metastatic disease. Survival curves were calculated using the actuarial methods of Kaplan and Meier, with differences in survival rates assessed using the log-rank test. For the multivariate analysis we used Cox regression [18]. RESULTS The overall 8-year actuarial FBF at 8 years was 73% (Fig. 1a); in the 36 patients with a biochemical failure, the median (range) time to PSA failure was 33 ( ) months, with 53% failing within 3 years and 83% within 5 years. The median (range) PSA doubling time was 2.7 ( ) months; doubling times were 3 months in 56%, >3 6 months in 13%, >6 10 months in 9% and >10 months in 22%. In patients with no biochemical failure, the last follow-up PSA levels were 0.1 ng/ml in 83%, > ng/ ml in 9% and > ng/ml in 8%. As patients were given HT as part of their initial treatment, testosterone levels after treatment were measured, and were available for 137 patients; the median (range) highest levels was 384 (10 869) ng/dl. Metastatic disease developed in 22 patients and the 8-year freedom from distant metastases rate was 80% (Fig. 1b). The rates of prostate CSS and overall survival at 8 years were 87% (Fig. 1c) and 79%, respectively. In patients with biochemical failure, the rate of remaining free of metastatic disease, prostate CSS and overall survival at 8 years were 30.5%, 53% and 51%, respectively. The effect of prognostic factors on FBF and freedom from distant metastasis (FDM) were TABLE 1 The disease characteristics at presentation Variable n (%) PSA, ng/ml Median (mean, range) 9 (14, ) (55) > (27) >20 33 (18) Gleason score (67) 9 53 (29) 10 8 (4) Clinical T classification T1b 1 (0.5) T1c 33 (18) T2a 20 (11) T2b 57 (31) T2c 43 (24) T3 27 (15) tested using univariate analysis (Table 2); this showed that pretreatment PSA level and Gleason score significantly affected FBF rates but only Gleason score affected the rates of FDM (Fig. 1d). Table 2 also lists the FBF and FDM analysed by staging and treatmentrelated factors. In addition, patients were divided into two groups based on time of treatment to reflect a potential shift in less aggressive disease over time; group 1 (91 patients) were treated before 20 June 2001 and group 2 (90 patients) after that date. There was no significant difference between the 8-year FBF rates for the two groups, at 71% vs 85%, respectively (P = 0.5). Notably, testosterone levels after treatment did not significantly affect FBF or FDM rates. One of the three patients with positive nodes developed a biochemical failure and has not yet developed distant metastases. The only staging or treatment-related factor to significantly affect either FBF or FDM rates was seminal vesicle status. Having a negative seminal vesicle biopsy was associated with a FBF rate of 86.5% at 8 years (P = 4). Multivariate analysis showed that only Gleason score and initial PSA level significantly affected the development of biochemical failure (Table 3). Only Gleason score affected distant metastases rates and so a multivariate analysis was not done for this endpoint. As the Gleason score was the only factor to significantly affect distant metastases rates, its effects on prostate CSS and overall survival were also analysed. The Gleason score significantly affected prostate 1632 JOURNAL COMPILATION 2009 BJU INTERNATIONAL
3 GLEASON SCORES 8 10 PROSTATE CANCER TREATED WITH TRIMODAL THERAPY TABLE 2 The effect of disease-related prognostic factors, staging and treatment, on biochemical failure and distant metastases FIG. 1. Freedom from (a) biochemical failure; (b) developing distant metastases; and (c) prostate CSS; and (d) effect of Gleason score on biochemical failure, and (e) on distant metastases. a b Factor FBF FDM 8-year rates, % PSA, mg/ml > > P Gleason score P 03 <01 Clinical T classification T2b T2c P Seminal vesicle biopsy status not done negative positive P Laparoscopic lymph-node status not done done P Testosterone level after treatment, ng/dl > P BED, Gy > P Duration of HT, months > P percent free from biochemical failure c prostate cancer specific survival e percent free from distant metastases 1 years No. at risk years No. at risk P < 01 Score = 10 Score = 8 Score = percent free from distant metastases d percent free from biochemical failure 1 years No. at risk P = 03 Score = 8 Score = 10 Score = Factor P Exp B (95% CI) Gleason score (8, 9, 10) < ( ) PSA ( 10, >10 20, >20) ( ) Seminal vesicle status ( ) BED ( 205, 205) ( ) CSS, with 8-year rates of 92%, 80% and 63% for scores of 8, 9 and 10, respectively (P = 03); it did not significantly affect overall survival, with rates of 85%, 71% and 63%, respectively (P = 0.14). DISCUSSION TABLE 3 Cox regression analysis of factors potentially affecting biochemical failure The encouraging results of this combined approach are derived from two recent advances in prostate RT, dose escalation and the use of HT. The current regimen used both neoadjuvant and concurrent HT. The cytoreductive and synergistic qualities of HT given with RT have been well documented in the laboratory [19]. Numerous randomized controlled trials also reported the benefit of adding HT to RT. An update of the Radiation Therapy and Oncology Group (RTOG) 8610 trials showed an improvement in local control (42% vs 30%), biochemical disease-free survival (24% vs 10%) and cause-specific mortality (23% vs 31%), and a reduction in distant metastases (34% vs 45%) for 4 months of HT and Gy of EBRT vs EBRT JOURNAL COMPILATION 2009 BJU INTERNATIONAL 1633
4 STOCK ET AL. alone [4]. An update of RTOG showed a 10-year local failure rate for RT and adjuvant HT of 23% vs 38% for the RT-alone arm. The 10-year distant metastases rates and diseasespecific mortality were 24% vs 39% and 16% vs 22%, both in favour of the adjuvant HT arm [20]. With a median follow-up of 66 months, the European Organisation for Research and Treatment of Cancer (EORTC) reported both an improvement in 5-year disease-specific survival, 94% vs 79%, and overall survival, at 78% vs 62%, for RT and 3 years of adjuvant HT vs RT alone [21]. Other prospective trials have also shown an advantage to adding HT to RT or to a longer duration of HT [22 24]. Although the use of HT has not been studied in a prospective randomized fashion with brachytherapy, in one study by Merrick et al. [25], HT improved the 10-year biochemical relapse-free survival when added to combined brachytherapy and EBRT over combined therapy alone for high-risk prostate cancer. The use of 9 months of HT in the present regimen was chosen to provide both neoadjuvant therapy for 3 months before brachytherapy, as well as concurrent HT given during the life of the implant and through the course of EBRT. In addition to the effects of HT the current treatment benefited from dose escalation, achieved by combing low-dose rate brachytherapy with EBRT. The importance of dose escalation, especially in high-risk disease, has been well documented. A recent report of the long-term results of the MD Anderson randomized trial of dose escalation, in which 51% of patients had Gleason scores of 7, reported an improvement in FBF of 78% for doses of 78 Gy, vs 59% for the 70-Gy arm (P = 04) [26]. In another randomized trial, reported by Zeitman et al. [27], 70.2 Gy of conventional-dose RT was compared to 79.2 Gy delivered with combined photons and protons (8% of patients had Gleason scores of 8 10). The FBF rate was 78.8% at 5 years for the conventional arm, vs 91.3% for the highdose arm (P < 01). Although the present regimen did not involve a planned dose escalation, and the present analysis did not show a dose-response relation between the range of delivered doses, the overall doses were very high. The combination of brachytherapy and EBRT resulted in very high BEDs (median 206, range Gy 2 ). This dose is much higher than 81 Gy (associated BED of 155), a common prescription dose of intensity-modulated RT. Our inability to show a dose-response relation between the lower TABLE 4 Biochemical control rates after RP or conventional-dose RT for patients with Gleason scores of 8 10 Reference N patients Dose, Gy Years after treatment Rate, % After RP [30] (PSA 20 ng/ml) 19 (PSA > 20 ng/ml) [6] [7] [5] [8] [9] After RT [1] [3] [2] [31] (Gleason score 7 10) [4] [21] (high-risk) and higher range of doses was probably because all of the doses were above the threshold for a significant response. A previous report showed that the most significant dose threshold was at a BED of 150 Gy 2 [16]. The results of this combined therapy at 8 years are promising, with a FBF rate of 73%, FDM rate of 80%, prostate CSS of 87% and overall survival of 79%. One limitation of the study is that the 8-year outcomes are reported and the median follow-up is only 65 months. Some of the other limitations of the present study arise because it was retrospective. Although most patients were treated uniformly, there was some variation in terms of staging procedures and duration of HT used. This was due, in part, to different urologists being involved in the care of these patients. The effects of these variations were taken into account by analysing the effect of both the duration of HT and the use and results of both node dissection and seminal vesicle biopsy, in both univariate and multivariate analysis. Neither of these factors had a significant effect on biochemical control in the multivariate analysis. The range seen in BED values is mostly due to inherent inaccuracies in the implant procedure itself, and the resulting variation in dosimetry results after implantation. The variation in EBRT dose stems mainly from the policy of adjusting these doses based on the final dosimetric outcome of the implant. Despite these adjustments the vast majority of patients (81%) received the same EBRT dose of 45 Gy given in 25 fractions. The overall outcomes after this therapy are supported by other series of combined brachytherapy and EBRT; these series report biochemical control rates for patients with Gleason scores of 8 10 of 58 89% [25,28,29]. Overall, the biochemical control rates for this high-risk group of patients compare favourably to more standard therapies. Table 4 [1 9,21,30,31] lists biochemical control rates after RP and conventional-dose EBRT for patients with Gleason scores of The outcomes reported above highlight two important prognostic factors among patients with Gleason score 8 10 disease, i.e. pretreatment PSA level and Gleason score. Using biochemical failure as an endpoint, there were significant differences among patients with PSA levels of 10, >10 20 and >20 ng/ml, with corresponding 8-year FBF rates of 72%, 82% and 58%. This effect retained significance in the multivariate analysis. A similar finding was reported by Grossfeld et al. [30] who showed that patients with Gleason scores of 8 10 treated with RP fared better if their initial PSA level was <20 ng/ml (5-year FBF of 38%) than those with a PSA level of >20 ng/ml (5-year FBF of 16%). Manoharan et al. [32] similarly reported a 5-years FBF of 60% for patients with a PSA level of <20 ng/ml, vs 10% for those with a level of >20 ng/ml after RP JOURNAL COMPILATION 2009 BJU INTERNATIONAL
5 GLEASON SCORES 8 10 PROSTATE CANCER TREATED WITH TRIMODAL THERAPY In the present analysis, the most significant predictor of both biochemical failure and developing distant metastases was the Gleason score. Patients with Gleason scores of 8 10 had FBF rates of 84%, 55% and 30%, respectively. Very similar results were reported by Dattoli et al. [28], treating patients with Gleason score of 8 10 with combined lowdose rate brachytherapy and EBRT. In that series, the 10-year FBF for patients with scores of 8 was 85%, vs 56% for those with scores of 9. Serni et al. [33] reported that patients with a score of 8 had a 5-year FBF rate of 72%, vs 38% for those with a score of 9, after RP. In the present analysis the Gleason score was the only factor to significantly affect the development of distant metastases. Those with Gleason scores of 9 and 10 had a 24% and 70% rate, respectively, of developing metastatic disease by 8 years. Based on these findings, the Gleason score would appear to be the best surrogate for the inherent biological aggressiveness of these high-grade cancers. The effect of Gleason score on FBF and developing metastatic disease translated into a significant effect on prostate CSS. Future investigations must be done for those patients with scores of 9 10, to develop better systemic approaches to combine with local therapy. In conclusion, the treatment regimen of combined HT, low-dose rate brachytherapy and EBRT was designed to improve cancer control rates. The 8-year outcomes after this regimen show favourable FBF, FDM and disease-specific survival rates for patients with Gleason scores of This treatment approach should be considered as a viable option for this subset of patients with highrisk prostate cancer. CONFLICT OF INTEREST Jamie A. Cesaretti is a consultant for BARD; Nelson N. Stone is the owner of Prologics and a consultant for Nihon-Mediphysics and B&K Medical. 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Philadelphia: JB Lippincott, 1992: Stock RG, Stone NN, Cesaretti JA, Rosenstein BA. Biologically effective dose values for prostate brachytherapy: effects on PSA failure and post treatment biopsy results. Int J Radiat Oncol Biol Phys 2006; 64: Roach M3rd,Hanks G, Thames H et al. Defining biochemical failure following radiotherapy with or without hormonal therapy in men with clinically localized prostate cancer; recommendations of the RTOG-ASTRO Phoenix Consensus Conference. Int J Radiat Oncol Biol Phys 2006; 65: Nrusis MJ. SPSS 1 Guide to Data Analysis. Upper Saddle River, NJ; Prentice Hall, Zeitman AL, Prince EA, Nakfoor BM, Park JJ. Androgen deprivation and radiation therapy: sequencing studies using the Shionogi in vivo tumor system. Int J Radiat Oncol Biol Phys 1997; 38: Pilpich MV, Winter K, Lawton CA et al. 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6 STOCK ET AL. suppression and radiation vs radiation alone for prostate cancer: a randomized trial. JAMA 2008; 299: Horwitz EM, Bae K, Hanks GE et al. Ten- year follow-up of Radiation Therapy Oncology Group Protocol 92 02: a phase III trial of the duration of elective androgen deprivation in locally advanced prostate cancer. J Clin Oncol 2008; 26: Denham JW, Steigler A, Lamb DS et al. Short-term androgen deprivation and radiotherapy for locally advanced prostate cancer: results from the Transtasman radiation Oncology group randomised controlled trial. Lancet Oncol 2005; 6: Merrick GS, Butler WM, Wallner KE et al. Androgen deprivation therapy does not impact cause specific survival or overall survival in high risk prostate cancer managed with brachytherapy and supplemental external beam. Int J Radiat Oncol Biol Phys 2007; 68: Kuban DA, Tucker SL, Dong L et al. Long-term results of the M.D. Anderson randomized dose-escalation trial for prostate cancer. Int J Radiat Oncol Biol Phys 2008; 70: Zeitman AL, DeSilvio ML, Slater JD et al. comparison of conventional-dose versus high dose conformal radiation therapy in clinically localized adenocarcinoma of the prostate: a randomized controlled trial. JAMA 2005; 294: Dattoli M, Wallner K, True L, Cash J. Long-term outcomes after treatment with brachytherapy and supplemental conformal radiation for prostate cancer patients having intermediate and highrisk features. Cancer 2007; 110: Sylvester JE, Grimm PD, Blasko JC et al. 15-year biochemical relapse free survival in clinical stage T1 T3 prostate cancer following combined external beam radiotherapy and brachytherapy; Seattle experience. Int J Radiat Oncol Biol Phys 2007; 67: Grossfeld GD, Latini DM, Lubeck DP, Mehta SS, Carroll PR. Predicting recurrence after radical prostatectomy for patients with high risk prostate cancer. J Urol 2003; 169: Pollack A, Hanlon AL, Horwitz EM, Feigenberg SJ, Uzzo RG, Hanks GE. Prostate cancer radiotherapy dose response: an update of the Fox Chase experience. J Urol 2004; 171: Manoharan M, Bird VG, Kim SS, Civantos F, Soloway MS. Outcome after radical prostatectomy with a pretreatment prostate biopsy Gleason score of 8. BJU Int 2003; 92: Serni S, Masieri L, Minervini A, Lapini A, Nesi G, Carini M. Cancer progression after anterograde radical prostate for pathologic Gleason score 8 10 and influence of concomitant variables. Urology 2006; 67: Correspondence: Richard G. Stock, Professor and Chairman, Department of Radiation Oncology, Mount Sinai School of Medicine, New York, NY 10029, USA. Richard.stock@mountsinai.org Abbreviations: RP, radical prostatectomy; (EB)RT, (external beam) radiotherapy; HT, hormone therapy; CSS, cancer-specific survival; FBF, freedom from biochemical failure; FDM, freedom from distant metastases; RTOG, Radiation Therapy and Oncology Group; BED, biologically effective dose; EORTC, European Organisation for Research and Treatment of Cancer JOURNAL COMPILATION 2009 BJU INTERNATIONAL
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