Monotherapy with Carbon Ion Radiation for Localized Prostate Cancer

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1 Japanese Journal of Clinical Oncology Advance Access published May 30, 2006 Monotherapy with Carbon Ion Radiation for Localized Prostate Cancer Jun Shimazaki 1, Koichiro Akakura 1, Hiroyoshi Suzuki 1, Tomohiko Ichikawa 1, Hiroshi Tsuji 2, Hitoshi Ishikawa 2, Masaoki Harada 3 and Hirohiko Tsujii 2 1 Department of Urology, Graduate School of Medicine, Chiba University, 2 Research Center for Charged Particle Therapy, National Institute of Radiological Sciences, Chiba 3 Department of Surgical Pathology, Kanagawa Cancer Center, Yokohama, Japan Received December 24, 2005; accepted February 13, 2006 Jpn J Clin Oncol doi: /jjco/hyl030 Background: Radiation treatment for localized prostate cancer has become a prominent choice of monotherapy, and carbon ion beam is a powerful means for this purpose. Methods: In total, 37 patients with localized prostate cancer were treated by monotherapy with carbon ion radiation and the outcome, more than 4 years later, was followed. Results: PSA relapse-free survival was overall 85%, 5 years after radiation, and 96% in lowrisk patients. Local control was mostly achieved, and no cancer-specific death was obtained. Except in cases of relapse, 1.0 ng/ml or less of PSA was shown in 78%, 3 years after radiation. Half of biopsy specimens out of 12 cases revealed non-viable or no cancer cells after a rather short time from treatment. Conclusion: Monotherapy with carbon ion radiation may be an excellent treatment for localized prostate cancer with low risk. Key words: prostate cancer localized stage radiotherapy carbon ion radiation INTRODUCTION Recently the incidence of prostate cancer has been increasing in Japan, and more than half of the patients are organ-confined or in locally advanced stages. For these patients, radiation therapy is one of the curative strategy, and many radiological techniques are being used. Carbon ion radiation may be a powerful means of radiotherapy for prostate cancer, because it shows a Bragg peak in the human body and gives a high dose of radiation energy to the prostate without adverse effects to the surrounding tissues. The Heavy Ion Medical Accelerator in Chiba (HIMAC) was built at the National Institute of Radiological Sciences, and treatment was initiated with carbon ion radiation for many kinds of solid tumors (1,2). Treatment for prostate cancer by HIMAC started in 1995 and 400 patients have been treated to date. The patients were divided into either low-risk group [T1b,c and T2ab, Gleason score 56, and PSA (prostate-specific antigen) 520 ng/ml] or high-risk group (T2c,T3, Gleason score =7, and/or PSA >20), supplemented without or with hormone therapy, respectively. Results of first (96 cases) and second (273 cases) series were reported (3,4). For reprints and all correspondence: Jun Shimazaki, Department of Urology, Graduate School of Medicine, Chiba University, Chuo-ku, Chiba-shi , Japan. shimajun@opal.famille.ne.jp Of these patients, 37 received monotherapy with carbon ion radiation between April 1998 and December Based on these studies, a possibility has arisen to establish the carbon ion radiation as a new independent treatment. Studying the effect for >4 years, we present this report which describes the outcomes of these 37 patients. PATIENTS AND METHODS The clinical records of 37 patients who received monotherapy were examined by mid Carbon ion radiation was performed according to the method previously described as the routine technique (4). Briefly, 60 GyE (first Phase I/II clinical trial) 66GyE (second Phase I/II clinical trial) in 20 fractions were irradiated to the entire prostate and most parts of the seminal vesicle with one anterior posterior port and a pair of lateral ports. After radiation, these patients were observed without any additional therapy for prostate cancer until clinical relapse was evident. Staging was performed according to TNM 2002 (5). Pre-treatment biopsy was performed with 6 8 cores via rectal or perineal approaches. After radiation, sample tissues were taken for biopsy from suitable portions in some patients, and radiation effects were graded as follows: positive residual tumor without any treatment effect (Oa) or with degeneration but none of them are non-viable (Ob), less than one-half (1) or more than one-half (2) of residual # 2006 Foundation for Promotion of Cancer Research

2 Page 2 of 5 Carbon ion radiotherapy tumor are non-viable, only non-viable tumor cells are observed (3a) and no tumor cells and/or tissues are detected (3b) according to the Japanese General Rule for Clinical and Pathological Studies on Prostate Cancer (6). PSA value was expressed as ng/ml of total PSA. During follow-up, PSA was measured every 2 3 months, and images (CT or MRI of the pelvic area) were taken every year. PSA relapse was determined by ASTRO criteria (7). Definition of PSA relapse was not a prerequisite with other objective findings. After PSA relapse, findings of the prostate and pelvic lymph nodes were examined with digital rectal examination and images for detection of clinically local relapse. PSA doubling time at relapse was calculated by log e 2 divided by the slope which was obtained from the least square method on three or more points. The histological grade and radiation effect were examined by one central pathologist (M.H.). Analysis of morbidity was performed according to Radiation Therapy Oncology Group / European Organization for Research and Treatment of Cancer Scoring System. Survival curve was constructed using the Kaplan Meier method. RESULTS Patients characteristics are shown in Table 1. Seven cases showed =7 of Gleason score alone, and one was >20 of PSA alone, but the other factors fitted the criteria of low risk. Two cases exceeded low-risk category of Gleason score and PSA, but they were enrolled because of low stage. Therefore, there were 27 low-risk patients. Of 37 patients, PSA relapse was found in 6. PSA relapse-free survival is shown in Fig. 1, and the rate at 5 years was 85%. In low-risk patients, PSA relapse-free survival at 5 years was 96%. No clinically local relapse occurred, thus the local control rate was 100% throughout the observation period (>4 years). Three patients died (hepatocellular carcinoma, malignant lymphoma and unknown cause but with a negative biopsy after radiation). These three cases did not show PSA relapse with signs of clinical relapse of prostate cancer. Therefore, cause-specific survival was regarded as 100% at 5 years after radiation. After radiation, PSA was gradually decreased except in relapse cases (Fig.2). There was no PSA bounce following radiation. After treatment, patients with <0.5 ml of PSA were 11, 46, 42% at 1, 2 and 3 years, respectively, and those with <1 ng/ml of PSA were 37, 73, 78% at 1, 2 and 3 years, respectively, without values at PSA relapse and thereafter. Moreover, except in one patient (3%), PSA of others was <1.5 ng/ml at 3 years. The clinical courses of PSA relapse patients are shown in Table 2. Case nos 1 3 and 5 revealed long durations between the start of treatment and PSA relapse [ave. 46 months ( )], and their PSA doubling time at relapse was rather long [ave. 16 months ( )]. After relapse, these patients showed a very slow increase in PSA. No adjuvant treatment was delivered to cases 1, 2 and 5 until now, but case 3 received hormone therapy because of the biopsy finding, which showed definitely viable residual cancer tissues after radiation Table 1. Patients characteristics and radiation dose Age (years) Stage T1b T1c T2ab >76 5 PSA* (ng/ml) Gleason score =8 2 > Unknown 1 Radiation doses (GyE) *Total PSA. Figure 1. Total PSA relapse-free survival rate for 37 patients. (Table 3). Conversely, case nos 4 and 6 showed a short doubling time and distant metastasis appeared 7 and 16 months after PSA relapse, respectively, regardless of no signs of clinically local relapse. They were treated with hormone therapy and control of the cancer was achieved currently. Post-radiation biopsy was performed in 12 patients (Table 3). Six biopsy specimens of 12 cases revealed therapeutic effects of grade 3a or 3b (no viable tumor or no residual tumor). Of the other six cases, one case (Tables 2 and 3, no.3) with pretreatment Gleason score 6 showed PSA relapse 28 months after radiation. The other five cases revealed only a small volume of degenerative residual tumor cells and/or tissues with only a scarce amount of viable cells, but three cases

3 Jpn J Clin Oncol Page 3 of PSA (ng/ml) subsequently showed PSA relapse (Tables 2 and 3, nos 1, 2 and 4). In some cases, Gleason score of the remaining cancer cells after radiation showed upgrading. Apparently the time of biopsy after radiation or the radiation doses did not affect any significant histological effects, partly attributable to the rather short period between radiation and examination. Slight morbidity on the urinary system was frequently noticed, but no adverse effects of Grade 3 or worse were experienced during or after radiation (Table 4). DISCUSSION 10 Photon therapy for the treatment of localized prostate cancer was initiated during the 1960s, and has widely been performed worldwide since then. A multi-institutional pooled analysis of external beam radiation therapy delivered to 1765 patients with 5 0 Start 6mo 12mo 18mo 24mo 30mo 36mo Figure 2. Total PSA values determined before treatment (Start) and at indicated time (months) after carbon ion radiation. Values at PSA relapse and thereafter from three relapse cases (nos 2, 3, and 6 in Table 2) were excluded. Table 2. Cases of total PSA relapse Case no. Stage Gleason score* PSA (ng/ml)** Duration (months) PSA doubling time (months) # Start Nadir Relapse Start Nadir Nadir Relapse 1 T2ab T2ab T1c Outcome 4 T2ab Distant metastasis 5 T1c T1c Distant metastasis *On the pre-treatment biopsy. **Total PSA, Start; before radiation, Nadir; mostly reduced level, Relapse; at PSA relapse # at PSA relapse. T1b, T1c and T2 at six US medical centers between 1985 and 1995 reported 65.8% of PSA relapse-free survival at 5 years (8). Patients with T1 T2 were treated with 68.4 Gy of conventional external beam radiation, and PSA relapse-free survival at 5 years was 62% (9). Similar survival at 5 years was reported in Japan (10). To improve survival with external beam radiotherapy, an increased dose was administered to patients with T1 T2, and the 5 years PSA relapse-free survival with =72 Gy was 81% in comparison with 51% with <72 Gy (11). Radiation with 78 Gy was beneficial for patients with >10 ng/ml of pre-treatment PSA but no significant dose response was obtained from low-risk patients (12). This suggests that cancer control for low-risk patients is achieved with an adequate dose in proper fractions; therefore, 66 GyE/20 fractions of carbon ion radiation has been established in our system (4). This hypofractionated radiation gave an excellent

4 Page 4 of 5 Carbon ion radiotherapy Table 3. Histological findings after radiation Case no.* Stage Gleason score** PSA (ng/ml) Start z Radiation dose (GyE) Post-radiation biopsy Months PSA # Effect (grade) Gleason score 1 T2ab (1/4) y 2 T2ab T1c (2/6) 4 T2ab T1c b 8 T1b b 9 T1c a (1/8) 10 T2ab (1/8)small volume { 11 T2ab b 12 T1b (3/12)small volume 13 T1c b 14 T2ab a (1/3)small volume *Case nos 1 4 are the same as in Table 2. Nos 5 and 6 in Table 2 did not receive post-radiation biopsy. **On the pre-treatment biopsy. z Total PSA determined before radiation. # Determined at biopsy. y Gleason score (number of cancer tissues/total chips examined). { Very few viable cancer cells. Table 4. Incidence of acute and late radiation morbidity Bladder/urethra effect and the results showed overall 85% of PSA relapse-free survival at 5 years, and 96% in low-risk patients. Of six PSA relapse cases (Table 2), four cases were not indicated in lowrisk category (PSA = 20 and/or Gleason score 56); therefore, 40% of high-risk patients subsequently experienced PSA relapse. In spite of two cases showing histologically incomplete radiation effect (Table 3, no.3 and 10), all revealed no clinically local signs of relapse. Therefore, carbon ion radiation may be a highly effective treatment for localized prostate cancer. In this sense, both radiation therapy and radical prostatectomy reveal similar PSA relapse-free rates for low-risk patients such as those with stage T1 T2ab, Gleason score 56 and PSA 510 ng/ml (13,14). For high-risk patients, additional managements might be necessary before and/or after radiation therapy. It has been reported that nadir PSA after radiation influences subsequent outcome. Patients with T1 T2 and 1 2 ng/ml of PSA 5 years after radiation revealed 10 20% incidence of subsequent PSA relapse after 10 years, in contrast with >60% of subsequent PSA relapse in patients with >2 ng/ml of PSA (15). Patients with 1 ng/ml or less of PSA 5 years after Rectum Acute Late Acute Late Grade 1 Grade 2 Grade 1 Grade 2 Grade 1 Grade 2 Grade 1 Grade 2 Number of cases Rate (%) 14% 38% 3% 11% radiation may reveal 71 78% of disease-free survival subsequently (16). As PSA level gradually decreases after radiation, the exact value of nadir PSA is difficult to determine because of fluctuation over a short period. However, low PSA level after radiation may indicate low PSA relapse rate in the present cases. PSA doubling time at relapse after radiation therapy was reported to be a reliable marker for discriminating between slow and fast progressions, and a cut-off value of 3 months was proposed (17). Criteria for PSA relapse were defined by ASTRO (7,18) in which three consecutive increases in PSA constitutes definition. Two relapse cases in the present report showed short PSA doubling time at relapse, and they turned out to have bone metastatic disease. In the other four relapse cases, their PSA showed a very slow increase and their courses seem to be mild progression. If other criteria of PSA relapse, for example nadir + 2 ng/ml which indicates 0.68 of sensitivity for relapse, were applied (19,20), none of these cases might be defined as PSA relapse. Although PSA relapse indicates a turning point of progression, other factors are needed to predict outcome. Calculation of doubling time is

5 Jpn J Clin Oncol Page 5 of 5 one way to more reliably predict the subsequent course after PSA relapse. Radiation delivered to prostate induces various histological changes in both non-malignant and malignant cells, and shows diverse effects even within a single biopsy specimen (21). There is no universal evaluation system for histological effects in post-radiation biopsy specimens. A grading system of radiation-induced histological effects has been proposed, based on separately graded nuclear and cytoplasmic changes each classified on a three-point scale (no effect to heavily damaged), and the least reactive point was used to determine biopsy failure (22). In contrast, the Japanese rule for histological effect of treatment in prostate cancer classifies according to the proportional amount of non-viable tumor cells and/or tissues, which show nuclear pyknosis, karyorrhexis and karyolysis within all of residual tumor cells and/or tissues (6). Applying this grading system to the 12 cases of post-radiation biopsy specimens, significant degenerative effects of carbon ion radiation were observed in most cases. Patients with incomplete radiation effect experienced subsequent PSA relapse, but it is not clear whether a small volume of the residual tumor cells and/or tissues participated in the relapse. This suggests that histological findings are indeed one of the prognostic factors. Although we cannot exclude the possibility that biopsy specimens were taken from an inadequate area, the course of PSA after radiation supports an outcome without relapse in most of the present cases until now (23). An upgrading in Gleason score has been reported in residual tumor tissues, as was noticed in the present cases. It is disputable whether upgrading is a profile of radio-resistant cells or represents radiation effect. Grading the histological pattern after radiation with the Gleason system may be different from that of untreated structure. Further histological examination will confirm the effect of monotherapy with carbon ion radiation for patients with low-risk prostate cancer. In conclusion, risk assessment of patients is the first step in applying monotherapy with carbon ion radiation, and lowrisk patients appear to be the appropriate candidates for this treatment. Acknowledgment The authors deeply thank the Working Group on Genitourinary Tumors, National Institute of Radiological Sciences, for their kind support. References 1. Kanai T, Endo M, Minohara S, Miyahara N, Koyama-Ito H, Tomura H, et al. Biophysical characteristics of HIMAC clinical irradiation system for heavyion radiation therapy. Int J Radiat Oncol Biol Phys 1999;44: Tsujii H, Mizoe JE, Kameda T, Baba M, Kato S, Kato H, et al. Overview of clinical experiences on carbon ion radiotherapy at NIRS. Radiother Oncol 2004;73(Suppl. 2):S Akakura K, Tsujii H, Morita S, Tsujii H, Yagishita T, Isaka S, et al. Phase I/II clinical trials of carbon ion therapy for prostate cancer. Prostate 2004;58: Tsuji H, Yanagi T, Ishikawa H, Kemada T, Mizoe J-E, Kanai T, et al. Hypofractionated radiotherapy with carbon ion beams for prostate cancer. Int J Radiat Oncol Biol Phys 2005;63: Sobin LH, Wittekind Ch (eds). TNM Classification of Malignant Tumours. UICC, 6th edn. New York: Wiley-Liss General Rule for Clinical and Pathological Studies on Prostate Cancer, 3rd edn. Kanehara Pub Inc.: Tokyo American Society for Therapeutic Radiology and Oncology Consensus Panel. Consensus statement: guidelines for PSA following radiation therapy. Int J Radiat Oncol Biol Phys 1997;37: Shipley WU, Thames HD, Sandler HM, Hanks GE, Zietman AL, Perez CA, et al. Radiation therapy for clinically localized prostate cancer. JAMA 1999;281: Zietman AL, Chung CS, Coen JJ, Shipley WU. 10 Year outcome for men with localized prostate cancer treated with external radiation therapy: results of a cohort study. J Urol 2004;171: Takahashi A, Yanase M, Masumori N, Sasamura H, Oda T, Tanaka T, et al. External beam radiation monotherapy for locally advanced prostate cancer. Jpn J Clin Oncol 2003;33: Kupelian PA, Potters L, Khuntia D, Ciezki JP, Reddy C, Reuther AM, et al. Radical prostatectomy, external beam radiotherapy <72 Gy, external beam radiotherapy 572 Gy, permanent seed implantation, or combined seeds/ external beam radiotherapy for stage T1-T2 prostate cancer. Int J Radiat Oncol Biol Phys 2004;58: Pollack A, Zagars GK, Starkschall G, Antolak JA, Lee JJ, Huang E, et al. Prostate cancer radiation dose response: Results of the M.D.Anderson phase III randomized trial. Int J Radiat Oncol Biol Phys 2002;53: Klein EA, Kupelian PA. Localized prostate cancer: radiation or surgery? Urol Clin N Am 2003;30: D Amico AV, Whittington R, Malkowicz B, Schultz D, Blank K, Broderick GA, et al. Biochemical outcome after radical prostatectomy, external beam radiation therapy, or interstitial radiation therapy for clinically localized prostate cancer. JAMA 1998;280: Kavadi VS, Zagars GK, Pollack A. Serum prostate-specific antigen after radiation therapy for clinically localized prostate cancer: Prognostic implications. Int J Radiat Oncol Biol Phys 1994;30: Yock TL, Zietman AL, Shipley WU, Thakral HK, Coen JJ. Long-term durability of PSA failure-free survival after radiotherapy for localized prostate cancer. Int J Radiat Oncol Biol Phys 2002;54: D Amico AV, Moul JW, Carroll PR, Sun L, Lubeck D, Chen M-H. Surrogate end point for prostate cancer-specific mortality after radical prostatectomy or radiation therapy. J Natl Cancer Inst 2003;95: Hanlon AL, Hanks GE. Scrutiny of the ASTRO consensus definition of biochemical failure in irradiated prostate cancer patients demonstrates its usefulness and robustness. Int J Radiat Oncol Biol Phys 2000;46: Kuban DA, Thames HD, Levy LB. Radiation for prostate cancer: Use of biochemical failure as an endpoint following radiotherapy. World J Urol 2003;21: Vicini FA, Kestin LL, Martinez AA. The correlation of serial prostate specific antigen measurements with clinical outcome after external beam radiation therapy of patients for prostate carcinoma. Cancer 2000;88: Cheng L, Cheville JC, Bostwick DG. Diagnosis of prostate cancer in needle biopsies after radiation therapy. Am J Surg Pathol 1999;23: Crook JM, Bahadur YA, Robertson SJ, Perry GA, Esche BA. Evaluation of radiation effect, tumor differentiation, and prostate specific antigen staining in sequential prostate biopsies after external beam radiotherapy for patients with prostate carcinoma. Cancer 1997;79: Crook J, Malone S, Perry G, Bahadur Y, Robertson S, Abdolell M. Postradiotherapy prostate biopsies: What do they really mean? Results for 498 patients. Int J Radiat Oncol Biol Phys 2000;48:

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