european urology 50 (2006)
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1 european urology 50 (2006) available at journal homepage: Prostate Cancer Duration of Testosterone Suppression after a 9.45 mg Implant of the GnRH-Analogue Buserelin in Patients with Localised Carcinoma of the Prostate A 12-Month Follow-up Study Bill Pettersson a, *, Eberhard Varenhorst a, Anssi Petas b,jürgen Sandow c a Department of Urology, Faculty of Health Sciences University Hospital, Linköping, Sweden b Department of Urology, Helsinki University Central Hospital, Helsinki, Finland c Sanofi-Aventis Pharma, Hoechst Industry Park, Frankfurt, Germany Article info Article history: Accepted March 1, 2006 Published online ahead of print on March 27, 2006 Keywords: Prostate cancer Neoadjuvant endocrine therapy GnRH-analogue Buserelin Radiation Testosterone Hot flushes Potency Abstract Objectives: (1) To determine the duration of androgen deprivation after a single buserelin implant 9.45 mg in the neoadjuvant setting in combination with curative radiation therapy of carcinoma of the prostate, and (2) to evaluate the time to recovery of gonadal function, and the incidence and duration of hypogonadal symptoms. Methods: We prospectively evaluated 21 men with carcinoma of the prostate who received one implant of 9.45 mg buserelin subcutaneously. Release of buserelin, changes in serum testosterone concentration, hot flushing and sexual function over a 12-month study period were recorded. Results: Testosterone was suppressed below the castration limit (0.58 ng/ ml = 2 nmol/l) for 224 days (range, ). The mean time to first return of testosterone above the castration limit was 246 days (range, ); 50% of pre-treatment value was reached after 285 days (range, ). The prevalence of hot flushing was 19 of 21 patients (90%) at 12 weeks. At the end of the study period, serum testosterone had reached 80% (range, 33% 166%) of pre-treatment concentration, sexual interest was present in 52%, erection was possible in 60%, and hot flushing remained in 24%. Conclusion: A single injection of 3-month buserelin implant 9.45 mg suppresses serum testosterone below the castration limit for at least 6 months. Testosterone secretion recovers by 8 12 months. Hypogonadal symptoms decreased with the restoration of serum testosterone secretion. These data are clinically relevant regarding the dose schedule for buserelin and the patient information provided. # 2006 European Association of Urology. Published by Elsevier B.V. All rights reserved. * Corresponding author. Urologiska Kliniken Östergötland, Universitetssjukhuset, S Linköping, Sweden. Tel ; Fax: address: bill.petersson@lio.se (B. Pettersson) /$ see back matter # 2006 European Association of Urology. Published by Elsevier B.V. All rights reserved. doi: /j.eururo
2 484 european urology 50 (2006) Introduction Long-acting gonadotropin-releasing hormone (GnRH)-analogues such as buserelin, goserelin and leuprolide have an established place in the treatment of prostate cancer [1]. They are given as repeated injections for long-term treatment in advanced disease and as single dose neoadjuvant hormonal therapy in men with localised or locally advanced disease undergoing curative external beam radiation or brachytherapy. Neoadjuvant therapy is based on temporary and reversible androgen deprivation [2]. The rationale behind neoadjuvant hormonal therapy is to decrease tumour volume, thereby reducing exposure of normal tissue to radiation, and thus diminishing radiation-related side effects and increasing sensitivity to radiation therapy [3,4]. The disadvantages of neo-adjuvant androgen suppression are side effects of androgen deficiency such as hot flushing, and decreased libido and potency [5]. The use of temporary androgen deprivation has become widespread, but as yet there is a need for more evidence on which to base recommendations regarding duration of androgen deprivation and information given to the patient about the expected duration of side effects. In many studies, authors have selected arbitrarily 3 4 months or more of androgen deprivation using goserelin or leuprolide [4,6]. In a randomised study, 6 months of androgen deprivation therapy improved the outcome of patients with locally advanced prostate cancer more than 3 months of treatment did [7]. On the other hand, long-term androgen deprivation therapy may increase the risk for developing hormone-refractory prostate cancer [8,9]. Our knowledge concerning recovery from temporary androgen deprivation therapy is limited. Few patient series describe the time to recovery of testosterone levels after injection of a 3-month preparation of leuprolide or goserelin [10 15]. Time to recovery after a single subcutaneous implant of 9.45 mg buserelin has not been investigated. We performed this study to provide the information required when using this implant in the neoadjuvant setting or when deciding upon the optimal interval between injections in long-term androgen deprivation treatment, and to improve patient information about the anticipated time required for recovery from hypogonadal symptoms. 2. Material and methods Twenty-one men (average age, 66 years [range, 53 80]) with histopathologically proven carcinoma of the prostate were included in this study. According to the TNM-classification, there were one T1a, nine T1c, three T2 and eight T3 tumours. In seven cases, no regional lymph node metastasis was found at regional lymph node exploration (N0). In 14 patients regional lymph nodes were not assessed (Nx). No distant metastases were found in 20 patients, and distant metastases were not assessed in one. With regards to the grade of malignancy, there were two G1, 14 G2, and five G3. The patients were consecutively recruited from the Department of Urology, University Hospital of Linköping (n = 11), and the Department of Urology, University Hospital of Helsinki (n = 10), when the decision was made to perform radiation therapy preceded by neoadjuvant hormonal treatment. In these patients, the mean concentration of serum prostate specific antigen at diagnosis was 17.8 mg/l (range, mg/l). A single implant of 9.45 mg buserelin (equivalent to buserelin acetate 9.9 mg) was injected subcutaneously, and the initial rise in testosterone was neutralised by 50 mg bicalutamide given orally once daily for 28 days. Radiation therapy was started 3 months later. Thirteen patients received external radiation therapy (70 Gy), and 8 patients received brachytherapy (20 Gy) combined with external radiation therapy (50 Gy) Blood and urine sampling Venous blood samples were obtained between 8:00 and 10:00 am, and 24-hour urine samples were collected at the screening visit, after implant injection, at week 2 and at 4-week intervals from week 4 until week 52 after injection. Serum and urine samples were stored at 20 8C pending analysis. Analyses of buserelin and testosterone using established and validated methods were carried out at a central laboratory (Sanofi Aventis Pharma, Frankfurt, Germany) Symptoms of androgen deprivation Evaluation of hot flushing was done the day before implantation and after 12, 24, 36 and 52 weeks of treatment. Patients were asked to grade the number of hot flushes during the previous week as 0, 1 3, 4 10 or more then 10 per 24 hours. They also were asked about the severity in terms of no flushes, have flushes but not distressed, slightly distressed or greatly distressed. These data were documented in a box questionnaire modified from a previously used and evaluated questionnaire [16]. Sexual function, libido and potency were evaluated by means of self-assessment questionnaires on the day before implantation and after 12, 24, 36 and 52 weeks of treatment. Four levels of sexual desire were queried. Penile erection was described by using a 6-grade scale, and the ability to ejaculate was assessed by the patient choosing one of 6 alternatives. These data were documented in a box questionnaire modified from a previously used and evaluated questionnaire [17] Methods of analysis Serum testosterone concentration was measured with the commercially available, validated, coated tube radioimmune assay DSL 4000 purchased from Diagnostic Systems
3 european urology 50 (2006) Laboratories, Inc (Webster, TX, USA). The detection limit in serum is 0.08 ng/ml; the normal range for total testosterone in adult males is ng/ml. Serum PSA and urine creatinine concentrations were determined by routine laboratory methods. The serum and urine concentrations of buserelin were measured by a specific radioimmunoassay technique [16]. The detection limit for buserelin in serum and urine was 0.05 mg/l. Urinary excretion of buserelin was standardised for creatinine excretion, as described previously [18,19]. The rate of buserelin release (mg/ 24 hours) was calculated from the amount excreted in the urine over 24 hours Ethics The study was approved by the local ethics committees at the universities of Helsinki and Linköping Data handling and statistics All variables for buserelin and testosterone time-action profiles were analysed descriptively. For each subject, the duration of buserelin release at therapeutic concentrations was determined by the number of days with release of buserelin above the minimum therapeutic rate required for testosterone suppression. From previous study results, the minimum therapeutic release rate for testosterone suppression was estimated to be 5 mg/d [20]. The pre-defined serum testosterone castration limit was 0.58 ng/ml (=2 nmol/l). Serum testosterone data were analysed to give the number of days from implant injection until the castration limit was reached, to return to castration limit and to return to 50% of baseline concentration before treatment, as well as the final testosterone level after 12 months. All patients completed the study. 3. Results 3.1. Buserelin release and serum testosterone Testosterone suppression was maintained by a therapeutic buserelin release rate of 5 mg per 24 hours. The relationship between buserelin release and serum testosterone concentration is shown in Fig. 1. The therapeutic release rate after a single injection of one buserelin implant 9.45 mg was maintained for an average period of 230 days (range, ). The mean serum testosterone concentration before treatment was 4.62 ng/ml (range, ) and had returned to 3.37 ng/ml (range, ) by 12 months. Serum testosterone below the castration limit (0.58 ng/ml) was achieved after 224 days (range, ), had started to increase above the castration limit by 230 days (range, ) and reached 50% of the pretreatment concentration by 285 days (range, ). At 12 months, the serum testosterone had reached 80% (range, 33% 166%) of the concentration before implantation. The patients data are shown in Tables 1 and Hot flushing Four of 21 patients already had hot flushing before starting treatment. At 3 months, 19 patients (90%) experienced hot flushes. The prevalence of hot flushing thereafter decreased: 16 (76%) at 6 months and 13 (62%) at 8 months. Six men reported hot Fig. 1 Rate of buserelin release (mg/24 hours) and serum testosterone concentration during a 12-month neoadjuvant treatment period for prostate cancer (one buserelin implant 9.45 mg). Means and standard error for 21 patients. Testosterone castration limit 0.58 ng/ml. =2 nmol/l. (Conversion factor to SI units: ng/ml 3.47 = nmol/l.)
4 486 european urology 50 (2006) Table 1 Testosterone suppression over 12 months after one buserelin implant 9.45 mg in 21 patients a Patient no. Age (yr) Serum testosterone (ng/ml) Before treatment Nadir After 12 months % of initial value Mean Range a Means, range (minimum to maximum); initial value = serum testosterone before treatment. Table 2 Recovery from testosterone suppression and duration of therapeutic release (days) after one buserelin implant 9.45 mg and remaining symptoms of androgen deficiency in 21 patients () after 12 months Patient no. Duration of therapeutic buserelin release (d) No. of days until above castration limit Testosterone level No. of days to reach 50% baseline value Symptoms of androgen deficiency after 12 months Libido absent Erection absent Ejaculation absent Hot flushing present Mean Range
5 european urology 50 (2006) flushing at night. During the 12-month follow-up period, 11 patients had up to three hot flushes per 24 hours, 8 had 4 10, and 2 more than 10. Of those who reported hot flushing, 12 were at the most slightly distressed and three were greatly distressed at 3 months. At the end of the study, hot flushing had disappeared in 17 patients and remained disturbing in two patients (Table 2) Sexual function, libido and potency Before starting treatment, five men felt no desire for sexual activity; five felt the desire for sexual activity rarely ; 9, sometimes and two, frequently. At 6 months, 16 men felt no desire for sexual activity and four felt desire to only some degree (one answer missing). At 12 months, 18 men felt the desire for sexual activity. Low testosterone explained the absence of sexual interest in two patients. Before starting treatment, seven men were unable to gain sufficient penile erection, whereas the remaining 14 patients had various degrees of erection. After 6 months, 18 men could not gain erection. At the end of 12 months, 12 had various degrees of erection, and eight could not gain erection (one answer missing). Before starting treatment, six of 21 men were unable to ejaculate. After 8 months, 17 men had no ejaculation; by the end of 12 months, the ability to ejaculate was absent in nine of 20 patients (Table 2). 4. Discussion Medical castration today usually is achieved by administering long-acting GnRH-analogues, which has been demonstrated to be as effective as surgical castration [21,22]. However there is no generally accepted upper castration limit for testosterone after androgen deprivation therapy. Recently a value around 0.2 ng/ml or 0.69 nmol/l was defined, but studies comparing clinical outcome with different castration limits are lacking [23]. In buserelin and goserelin implants, the active hormone is dispersed homogeneously in cylindrical rods of biodegradable co-polymer [20]. GnRH implants are fully effective in initiating and maintaining medical castration once the therapeutic release rate is achieved. Duration of fully effective testosterone suppression depends on the dose injected. Evidence of duration of buserelin implant 9.45 mg was provided first by a single-dose study with a follow-up of 4 months [20]. The study established a dose-interval of 3 months in repeateddose treatment of prostate cancer. Neo-adjuvant androgen treatment requires a predictable period of androgen deprivation. The optimum dose of GnRH-analogue therefore has been discussed by several authors. In the case of the 3- month preparation of the GnRH-analogue leuprolide, the duration of castration levels of testosterone was twice as long as that suggested by the product description, which led to hypogonadal symptoms such as hot flushing lasting more than 1 year after a single injection [10]. A similar delay in testosterone recovery was noted with the 3-month goserelin depot preparation used as neoadjuvant hormone treatment before radical prostatectomy [11,12]. The authors concluded that a 1-month preparation should be used instead of the 3-month preparation in the neoadjuvant setting when prompt testosterone recovery is desirable [12]. The same conclusion was reached on the basis of a study of 267 patients treated with goserelin 3-month depot after a single injection or one injection every 3 months over 3 years. The median time to testosterone recovery was 10 months, but only 53% of the patients had testosterone levels recorded before medical castration. The release of the GnRH-analogue (leuprolide or goserelin) in serum or urine was not measured in any of these studies [10 15]. The buserelin 3-month implant has been documented (not published) as maintaining castration levels of testosterone for at least 16 weeks (112 days), but information is still lacking about the total duration of androgen suppression after one single injection [20]. The present study provides information about buserelin release, the relationship between buserelin release and testosterone suppression, time required for recovery of testosterone secretion and symptoms of gonadal deficiency. This prospective, open, non-controlled two-centre study on buserelin, 9.45 mg, 3-month implant with a follow-up of 12 months confirms that testosterone is suppressed fully by a buserelin release rate of 5 mg/24 hours [19]. Release at this rate was maintained for 230 days whereas testosterone was suppressed fully for 224 days. Time to return to 50% of baseline testosterone levels was about 10 months. At these testosterone concentrations, the symptoms of androgen deficiency were disappearing. On the basis of an arbitrary lower normal limit of 2 ng/ml for serum testosterone, four patients had low testosterone with symptoms of androgen deficiency (patients 2, 6, 8, 19 in Table 2) at 12 months, whereas another 10 patients had symptoms of androgen deficiency in the presence of normal testosterone levels (patients 3, 4, 9, 10, 11, 12, 17, 18, 20 and 21 in Table 2). The results from this 3-month buserelin implant study support previous conclusions regarding the other two GnRH-analogues, goserelin and leuprolide,
6 488 european urology 50 (2006) showing that castration testosterone levels are maintained for a considerably longer time than the nominal dose interval for repeated-dose treatment for prostate cancer. To explain the long duration of suppression, we determined the release rate of buserelin, which was found to be closely related to testosterone suppression. There was individual variability in the duration of testosterone suppression, which lasted for a considerably longer time than indicated by the nominal dose interval. The patient with the shortest therapeutic buserelin release did not have the shortest period with testosterone below castration level. The long time required for return to 50% of pre-treatment testosterone secretion explains the prolonged hypogonadism symptoms (hot flushing, decreased libido and potency). We confirm the previously published observation that symptoms of androgen deficiency may persist after the return of testosterone secretion to normal [12]. 5. Conclusion Our findings show that the 3-month GnRH buserelin implant has a substantially longer duration than has been documented previously. The choice of a 2- month instead of a 3-month GnRH implant in the neoadjuvant setting may be considered when shortening of the duration of hypogonadal symptoms is desired. However this approach has not yet been tested clinically. In patients with advanced disease receiving repeated-dose treatment with 3-month buserelin, it would seem possible to extend the dose interval, provided that serum testosterone is monitored and the next implant is given when the testosterone level lies above the castration limit. The reduction in treatment cost could be substantial. Conflict of interest statement Funding for this study was provided by Sanofi- Aventis Pharma, Frankfurt, Germany. Acknowledgements We thank Marianne Jern and Merja Rignell for assisting with the patients, and Birgit Krauss for performing the laboratory analyses. References [1] Cook T, Sheridan WP. Development of GnRH antagonists for prostate cancer: new approaches of treatment. Oncologist 2000;5: [2] Lee HHK, Warde P, Jewett MAS. Neoadjuvant hormonal therapy in carcinoma of the prostate. BJU Int 1998;83: [3] Forman JD, Kumar R, Haas G, Montie J, Porter AT, Mesina CF. Neoadjuvant hormonal downsizing of localised carcinoma of the prostate: effects on the volume of normal tissue irradiation. Cancer Invest 1995;13:8 15. [4] Shearer RJ, Davies HJ, Gelister JSK, Dearnaley DP. Hormonal cytoreduction and radiotherapy for carcinoma of the prostate. Br J Urol 1992;69: [5] Potosky AL, Knopf K, CleggLX, et al. Quality-of-life outcomes after primary androgen deprivation therapy: Results from the prostate cancer outcomes group. J Clin Oncol 2002;19: [6] Pilepich MV, Krall JM, Al-Sarraf M, et al. Androgen deprivation with radiation therapy compared with radiation therapy alone for locally advanced prostatic carcinoma: a randomized comparative trial of the radiation therapy oncology group. Urology 1995;45: [7] Denham JW, Steigler A, Lamb DS, et al. Short-term androgen deprivation and radiotherapy for locally advanced prostate cancer: results from the Trans-Tasman Radiation Oncology Group randomised controlled trial. Lancet Oncol 2005;6: [8] Paule B. Reappraisal of the concept of hormone therapy in metastatic prostate cancer and implications for treatment. Eur Urol 2005;47: [9] Hirano D, Okada Y, Minei S, Minei S, Takimoto Y, Nemoto N. Neuroendocrine differentiation in hormone refractory prostate cancer following androgen deprivation therapy. Eur Urol 2004;45: [10] Oefelein MG. Time to normalization of serum testosterone after 3-month luteinizing hormone-releasing hormone agonist administered in the neoadjuvant setting: implications for dosing schedule and neoadjuvant study consideration. J Urol 1998;160: [11] Nejat RJ, Rashid HH, Bagiella E, Katz AE, Nenson MC. A prospective analysis of time to normalisation of serum testosterone after withdrawal of androgen deprivation therapy. J Urol 2000;164: [12] Dearnaley DP, Norman AR, Shahidi M. Re: Time to normalization of serum testosterone after 3-month luteinizing hormone-releasing hormone agonist administered in the neoadjuvant setting: implications for dosing schedule and neoadjuvant study consideration (letter; comment). J Urol 1999;162:170. [13] Pickles T, Agranovich A, Berthelet E, et al. Testosterone recovery following prolonged adjuvant androgen ablation for prostate carcinoma. Cancer 2002;94: [14] Meinhardt W, Horenblas S. Re: Time to normalization of serum testosterone after 3-month luteinizing hormonereleasing hormone agonist administered in the neoadjuvant setting: implications for dosing schedule and neoadjuvant study consideration (letter; comment). J Urol 1999; 162: [15] Gulley JL, Figg WD, Steinberg SM, Carter J, Hussain MH, Dahut WL. A prospective analysis of the time to normalisation of serum androgens following 6 months of androgen deprivation therapy in patients on a randomized
7 european urology 50 (2006) phase III clinical trial using limited hormonal therapy. J Urol 2005;173: [16] Spetz AC, Hammar M, Lindberg B, Spangberg A, Varenhorst E, the Scandinavian prostate cancer group-5 trial study. Prospective evaluation of hot flashes during treatment with parenteral estrogen or complete androgen ablation for metastatic carcinoma of the prostate. J Urol 2001;166: [17] Wijma C, Varenhorst E, Hjertberg H, et al. Patienten kan bestämma själv: medicinsk eller kirurgisk behandling (summary in English). [Prostate cancer study: patients may choose for themselves between medical or surgical treatment.]. Läkartidningen 1992;89: [18] Blom JHM, Hirdes Wh. Schroeder FH, et al. Pharmacokinetics and endocrine effects of the LHRH analogue buserelin after subcutaneous implantation of a slow release preparation in prostatic cancer patients. Urol Res 1989; 17:43 6. [19] Sandow J, Seidel G, Rechenberg W, Jerabek-Sandow G, Krauss B. Implants and other controlled release systems for long-term LHRH agonist administration. In: Filicori M, Flamigni C, editors. Treatment with GnRH analogues: controversies and perspectives. London: Parthenon Publishing; p [20] Suprefact Depot product information. Available at: %20Depot%20implant%209.45%20mg%20ENG.pdf# search= suprefact%20depot. [21] Griffiths K. Is there a best castration? Cancer 1993;72: [22] Aus G, Abbou CC, Bolla M, et al. EAU guidelines on prostate cancer. Eur Urol 2005;48: [23] Tombal B, Berges R. How good do current LHRH agonists control testosterone? Can this be improved with Eligard 1?. Eur Urol Suppl 2005;4(8):30 6.
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