Intravesical Gemcitabine: State of the Art
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1 european urology supplements 6 (2007) available at journal homepage: Intravesical Gemcitabine: State of the Art Paolo Gontero *, Alessandro Tizzani Urologia 1, Università degli Studi di Torino, Italy Article info Keywords: Superficial bladder cancer BCG refractory Gemcitabine Intravesical Abstract Intravesical gemcitabine has been tested in several phase 1 studies. The 2000-mg dose of gemcitabine in 50 or 100 ml normal saline when administered intravesically for up to 2 h once a week for 6 wk has unremarkable systemic and local side effects; therefore, this schedule should be considered the most convenient. Phase 2 studies have assessed the activity of intravesical gemcitabine on a marker lesion in intermediate-risk superficial bladder cancers (SBCs), showing complete responses in up to 60% of cases. Few attempts have been made to test the activity of intravesical gemcitabine in highrisk SBC, achieving unexpected complete responses in carcinoma in situ refractory to Bacillus Calmette-Guérin. Initial trials have also documented clinically relevant responses in prophylaxis. The current level of evidence indicates that gemcitabine possesses clinical activity, but further confirmation is awaited from additional exploratory phase 2 and, preferably, phase 3 trials. # 2007 Published by Elsevier B.V. on behalf of European Association of Urology. * Corresponding author. Ricercatore in Urologia Università di Torino, Urologia 1, Ospedale Molinette, Torino, C.so Dogliotti, 14, Italy. Tel ; Fax: ; mobile phone: address: paolo.gontero@unito.it (P. Gontero). 1. Introduction According to the European Association of Urology guidelines [1], superficial bladder cancer (SBC) at intermediate risk should be preferably managed with prophylactic intravesical chemotherapy, leaving Bacillus Calmette-Guérin (BCG) immunotherapy as a second option in case of treatment failure. By contrast, BCG has become the standard treatment for high-risk SBC, with radical surgery remaining the sole valid alternative for any persistent or recurrent disease [2 9]. A potential limiting factor on the currently available intravesical agents concerns the side effect burden, particularly for BCG. In a recent review on the complications of intravesical therapies, BCGinduced, low urinary symptoms vary considerably between different series, from a minimum of 27% up to 90% of cases [10]. Similarly, systemic side effects of BCG like fever has been described in up to 17% of cases in one series [10], leading to stopping of the treatment in 10% of patients [11]. Chemotherapeutic agents, usually better tolerated than BCG, have provoked chemical cystitis in one of four patients in one series [10]. These limitations in tolerability for the most widely used intravesical agents across all risk categories of SBC have promoted the need for alternative therapies. A new treatment option should combine a good safety profile together with proven efficacy. These criteria are particularly true /$ see front matter # 2007 Published by Elsevier B.V. on behalf of European Association of Urology. doi: /j.eursup
2 810 european urology supplements 6 (2007) for intermediate-risk SBC in which the primary treatment end point resides in the prevention of recurrence for an otherwise good prognosis disease. 2. Rationale for intravesical administration Gemcitabine (2 0,2 0 -difluorodeoxycytidine [dfdc]) is a deoxycytidine analogue with a broad spectrum of antitumour activity. After being transported into the cell, it is phosphorylated and incorporated into the DNA and RNA, which cause inhibition of cell growth and trigger apoptosis [12]. Gemcitabine is then deactivated by deamination into 2 0,2 0 -difluorodeoxyuridine (dfdu) and transported out of the cell. When given systemically, gemcitabine has shown significant activity as a single agent against invasive bladder cancers, yielding response rates of 27 38% [13 14]. Gemcitabine has a molecular weight of 299 D, lower than that of commonly used intravesical chemotherapeutic agents such as mitomycin C (389 D) and doxorubicin (589 D). Its lower molecular weight may enable gemcitabine to penetrate the bladder mucosa with beneficial effects in the treatment of early invasive bladder cancers (T1 disease). At the same time the molecular weight is high enough to prevent significant systemic absorption in an intact bladder. Its pharmacokinetic properties also make gemcitabine an ideal candidate for regional therapy. When given intravenously, it is rapidly deaminated into the inactive metabolite, thus resulting in a high total body clearance. In an in vitro study, gemcitabine sensitivity was compared with adriamicin, epirubicin, and mitomycin C for relative potency on cell cultures of transitional cell carcinoma [15]. Gemcitabine at 10 mg/ml resulted in a more robust cytotoxic activity (90% lethality in all cell lines) than the other chemotherapeutic agents. Preclinical animal studies have been performed with the specific aims of assessing organ-specific toxicity and identifying the possible systemic absorption of gemcitabine following intravesical administration. These studies, albeit limited by the use of an animal model, have proven the absence of bladder-specific toxicity as well as negligible systemic absorption even at high doses of 50 mg/kg (equivalent to around 3150 mg/m 2 in humans) in rabbits [16] and at 350 mg (equivalent to 1000 mg/m 2 in humans) in dogs [17]. 3. Pharmacokinetics and tolerability The pharmacokinetic and safety profile of gemcitabine has been assessed for three different treatment schedules (twice weekly for 6 wk, once weekly for 6 wk, and one single instillation immediately after transurethral resection [TUR], respectively) and for doses escalating from 500 to 2000 mg diluted in 50 or 100 ml of saline solution (maximum drug concentration of 40 mg/ml). In the biweekly treatment scheme, gemcitabine was detectable in plasma at only the 2000 mg/100 ml concentration, with one of six patients developing grade 3 thrombocytopenia and neutropenia) [18]. When administered once a week for 6 wk, gemcitabine was detectable in plasma at low concentrations (1 mmol/l) in only the four patients receiving 2000 mg [19] and occasionally (1 patient) at 1000 mg [20]. Otherwise plasma concentrations were always below the detection limit [21]. Finally, early postoperative instillation produced measurable plasma concentrations (4.5 and 6.1 mmol/l, respectively) in only the two patients with suspected bladder perforation [22]. Pharmacokinetic data have thus shown systemic absorption of intravesical gemcitabine at up to a 40 mg/ml concentration (2000 mg in 50 ml is minimal and transient across all three different schedules. Table 1 lists systemic and local side effects recorded for different escalating doses in phase 1 studies. Local toxicity was generally described as minimal and rapidly self-resolving. With the possible exception of three cases of grade 3 urinary frequency (one in the study by Laufer [19] at 2000 mg and the other two reported by Dalbagni [18] following 1000 and 1500 mg administrations, respectively), genitourinary side effects were usually confined to the grade 1 toxicity level. Notably, this latter study was the only one to employ a buffered solution. Whether increase in the ph of the drug may result in fewer side effects without affecting its activity remains to be elucidated. A study is currently underway at our institution to assess possible changes in intratumoral concentration of gemcitabine and its metabolites according to different types of intravesical administration of the standard 2000 mg dose: 20 versus 40 mg/dl, 1-h versus 2-h intravesical exposure, and buffered versus unbuffered solution. 4. Activity on SBC marker lesions Marker lesion studies have been specifically designed in SBC to test the ablative activity of a given drug on a single papillary marker lesion. At the same time, these phase 2 trials allow assessment of the incidence and severity of early side effects in relatively few patients [23,24]. Current intravesical
3 Table 1 Toxicity according to three different treatment schemes and escalating doses Treatment schedule Indwell time (h) Reference paper Patients Dose level/toxicity * Twice weekly 6wk 1 [18] N =18 N =3 N =6 N =3 N = mg in 100 ml 1 G1 nausea 4 G2 urinary frequency 1 G2 urinary frequency 1 G2 hematuria 1 G3 urinary frequency 1 G3 urinary frequency 1 G2 asthenia 3 G2 hematuria 1 G2hematuria 1 G2 nausea 1 G2 asthenia 1 G2 UTI 1 G2 vomiting 1 G3 thrombocytopenia and neutropenia Once weekly for 6 wk 2 [19] N =15 N =3 N =3 N =3 N =6 ** mg in 50 or 100 ml 1 G1 thrombocytopenia, 1 G1 leukopenia 1 G1 dysuria 1 G1 leukopenia 1 G1 dysuria 1 G1 hematuria 3 G1 hematuria 2 G1 hematuria 1 G2 frequency 1 G1 dysuria 1 G1 frequency 1 G1 incontinence 3 G1 hematuria 2 G1 hematuria 1 G1 bladder spasm 1 G1 fatigue 2 G1 fatigue/headache 1 G1 fatigue 1 G2 proteinuria 2 G1 chills 1 G1 arthralgia 1 G1 pruritus 3 G1 fatigue 1 G3 frequency *** 1 G1 dizziness 2 G1 headache 2 G1 myalgia 1 G1 nausea 1 G3 urine retention 1 G1 arthralgia 2 [21] N =12 N =3 N =3 N =3 N =3 None None None 1 G1 dysuria 1 [20] N =10 N =3 N =4 N =3 ****, 1 G1 myelosuppression **** **** Early single (within 2 3 h 1 [20] N =10 N =5 N =5 from TUR) mg in 100 ml 2 G1 hypogastric discomfort 1 G1 bladder spasms 2 G1 liver toxicity G, grade of toxicity; TUR, transurethral resection. * Toxicity was graded according to the National Cancer Institute-Common Toxicity Criteria, version 2.0. ** The 2000 dosage was diluted in 50 ml in 4 patients and in 100 ml in 2 patients. *** The 2000 dosage was diluted in 100 ml; the patients discontinued treatment because of toxicity. **** Seven of 10 patients experienced G1 and transient toxicity including dysuria in 4 cases, and headache, fatigue, and heavy legs in 3. The paper does not specify at what dose level each side effect occurred. european urology supplements 6 (2007)
4 812 european urology supplements 6 (2007) agents, namely mitomycin C, epirubicin, and BCG have all been tested in marker lesions studies with a complete response (ie, complete disappearance of the marker lesion) in 40 60% of cases [25 29]. These findings constitute the reference value of activity for any new intravesical agent. The ablative efficacy of intravesical gemcitabine on a marker lesion tumour has been investigated by several authors. Eradication of a marker lesion peaked 66.6% in a peer-reviewed abstract presented by Calais da Silva FM [30], followed by 56% in another phase 2 study [31]. Lower levels of chemoresection, 46.4% [32] and 22% [33], were reported in two additional studies in which multiple marker lesions were left. Finally Gardmark et al [34] observed complete remissions of a marker lesions, increasing from 10% with a single dose up to 40% with the standard regiment of once weekly for 6 wk. Taken together these data fare well in comparison with previous similar studies on BCG and other chemotherapeutic agents, and indicate that gemcitabine is active on SBC. 5. Clinical evidence on prophylaxis and chemoresection Intravesical gemcitabine has been tested in several phase 2 studies that explored its clinical utility for intermediate- and high-risk SBC. Notably, the available series included a significant proportion of patients relapsing after BCG or chemotherapies, with only a minority being treatment naïve. The reason for this new drug to be conceived primarily as a second-line treatment, despite its favorable safety profile, is not known. It is likely that cost issues may have played a role Intermediate-risk SBC: prophylaxis and chemoresection Phase 2 studies do not allow any firm conclusion on drug efficacy, but clinically relevant information can be extrapolated. This is the case for the study by Bartoletti and the Tuscani Urology Group [35], in which a mixed series of intermediate- and high-risk SBCs were treated with 6 weekly instillations. The most interesting result was achieved in the subgroup of patients with recurrent SBC previously treated with BCG, in whom a 75% 1-yr recurrencefree interval was observed. Since a maximum of 45% probability of 1-yr recurrence had been considered acceptable in the statistical design, the authors concluded that the drug had reached a good level of clinical activity. Table 2 Current studies addressing the utility of gemcitabine in clinical practice Schedule Patients (N) Category of SBC Toxicity CR (N [%]) Outcome Author Drug concentration: indwell time NA 74.6% recurrence-free at a median follow-up of 12 mo [35] 40 mg/ml: 1 h Weekly for 6 wk 118 Intermediate and high risk Urgency 12%; 2 patients withdrew from treatment 14%; 8 patients suspended treatment NA 70.5% recurrence-free at a median follow-up of 20 mo [36] 40 mg/ml: 1 h Weekly for 8 wk 73 Intermediate risk; recurring after previous treatment 13/28 (46.4) Median recurrence-free interval of 9.1 mo 9 of 34 (26%); mild and transient local toxicity; 1 G3 leukopenia; 6 patients discontinued 34 Unresected 2 cm; low to intermediate risk [32] 40 mg/ml: 1 h Weekly for 4 wk before TUR SBC, superficial bladder cancer; CR, complete response (complete disappearance of the marker lesion with negative urine cytology and biopsy); NA, not applicable; TUR, transurethral resection.
5 european urology supplements 6 (2007) A favorable profile in prophylaxis was confirmed in another phase 2, single-arm, multicentric Italian experience [36]. Seventy-three SBCs recurring after BCG (N = 13) or mitomycin C (N = 25) or both (N = 39) received 8 weekly instillations of 2000 mg gemcitabine. Treatment was discontinued in 8 patients for toxicity and 68 were evaluable. At a median follow-up of 20 mo, 46 of 68 (70.5%) patients were recurrence free. The recent study of Maffezzini et al [32] is peculiar in that it proposes a new clinical application of intravesical chemotherapy. Thirty-four low- to intermediate-risk SBCs with solitary or multiple lesions less than 2 cm received 4 weekly instillations of gemcitabine 2000 mg in a neoadjuvant setting (ie, before undertaking a TUR). In this perspective, the marker lesion concept, out of a speculative definition of the drug activity, was applied, with a more clinical intent in mind. The 46% response rate is therefore intriguing and opens the view to the use of neoadjuvant gemcitabine as minimally invasive treatment in place of TUR. This treatment modality may prove useful in selected patients such as elderly patients unfit for anesthesia. Follow-up data were also favorable for treatment responders, with a 53% 1-yr recurrence rate. Eighty percent of nonresponders to neoadjuvant treatment experienced recurrence (following TUR) at 1 yr. These latter data cannot be compared with previous studies because the neoadjuvant setting is not a way to achieve prophylaxis of recurrences in that the drug is administered before the TUR. In contrast with the Maffezzini et al study, a recent pilot study failed to demonstrate significant activity of gemcitabine in the chemoresection of a selected group of primary low-risk SBC with lesions up to 2 cm [37]. Table 2 summarizes the current most relevant studies addressing the utility of gemcitabine in clinical practice. 6. Conclusion Intravesical gemcitabine has so far demonstrated an excellent safety profile and minimal toxicity at concentrations up to 40 mg/ml. Instillation times of 1 and 2 h have been tested with excellent tolerability, although a few patients may not be able to retain the drug in the bladder for more than 1 h, particularly when bladder compliance is reduced by a mild chemical cystitis. The standard scheme of weekly instillations of gemcitabine for 6 wk as an induction course has shown an excellent safety profile and should be adopted when designing a treatment protocol on intermediate-risk SBC. Drug administration can be carried out as early as the third hour postoperatively, with no remarkable toxicity provided no major bladder perforation has occurred. The question remains as to whether a more-intense scheme (such as a 6-instillation course twice a week for 3 wk or even a 12-instillation course biweekly for 6 wk) maybemoreappropriateforhigh-risksbc. The clinical role of the drug has so far been confined to phase 2 studies enrolling intermediateand/or high-risk SBC recurring after previous therapies. The current level of evidence indicates that gemcitabine possesses clinical activity, but further confirmation is awaited from additional exploratory phase 2 and, preferably, phase 3 trials. However gemcitabine s use as second-line treatment for intermediate-risk SBC has been recently approved in some countries (Italy) in an attempt to provide the clinician with a safe therapeutic tool while more consistent data on its efficacy is awaited. Conflicts of interest Paolo Gontero has been lecturing to sponsored symposia organized by Lilly. References [1] Oosterlinck W, Lobel B, Jakse G, et al. Guidelines on bladder cancer. European Association of Urology (EAU) Working Group on Oncological Urology. Eur Urol 2002;41: [2] Lamm DL. Intravesical therapy for superficial bladder cancer: slow but steady progress. J Clin Oncol 2003;21: [3] Huncharek M, Kupelnick B. Impact of intravesical chemotherapy versus BCG immunotherapy on recurrence of superficial transitional cell carcinoma of the bladder: metaanalytic reevaluation. Am J Clin Oncol 2003;26: [4] Sylvester RJ, van der Mejden AP, Lamm DL. Intravesical bacillus Calmette-Guerin reduces the risk of progression in patients with superficial bladder cancer: a meta-analysis of the published results of randomized clinical trials. J Urol 2002;168: [5] Bohle A, Bock PR. Intravesical bacille Calmette-Guérin versus mitomycin C in superficial bladder cancer: formal meta-analysis of comparative studies on tumor progression. Urology 2004;63: [6] Bohle A, Jocham D, Bock PR. Intravesical Bacillus Calmette-Guerin versus mitomycin C for superficial bladder cancer: a formal meta-analysis of comparative studies on recurrence and toxicity. J Urol 2003;169:90 5. [7] Shelley MD, Court JB, Kynaston H, Wilt TJ, Coles B, Mason M. Intravesical bacillus Calmette-Guerin versus
6 814 european urology supplements 6 (2007) mitomycin C for Ta and T1 bladder cancer. Cochrane Database Syst Rev 2003:CD [8] Huncharek M, Kupelnick B. The influence of intravesical therapy on progression of superficial transitional cell carcinoma of the bladder: a metaanalytic comparison of chemotherapy versus bacilli Calmette-Guerin immunotherapy. Am J Clin Oncol 2004;27: [9] Joudi FN, Smith BJ, O Donnell MA, Konety BR. The impact of age on the response of patients with superficial bladder cancer to intravesical immunotherapy. J Urol 2006;175: [10] Koya MP, Simon MA, Soloway MS. Complications of intravesical therapy for urothelial cancer of the bladder. J Urol 2006;175: [11] van der Meijden AP, Sylvester RJ, Oosterlinck W, et al. Maintenance bacillus Calmette-Guerin for Ta T1 bladder tumors is not associated with increased toxicity: results from a European Organisation for Research and Treatment of Cancer Genito-Urinary Group Phase III Trial. Eur Urol 2003;44: [12] Bergman AM, Pinedo HM, Peters GJ. Determinants of resistance to 2 0,2 0 -difluorodeoxycytidine (gemcitabine). Drug Resist Updat 2002;5: [13] Stadler WM, Kuzel T, Roth B, Raghavan D, Dorr FA. Phase II study of single-agent gemcitabine in previously untreated patients with metastatic urothelial cancer. J Clin Oncol 1997;15: [14] Lorusso V, Pollera CF, Antimi M, et al. A phase II study of gemcitabine in patients with transitional cell carcinoma of the urinary tract previously treated with platinum. Italian Co-operative Group on Bladder Cancer. Eur J Cancer 1998;34: [15] Odonnel MA, Evanoff D, Luo Y. Studies on Gemcitabine as an intravesical agent for superficial bladder cancer. J Urol 2003;4(Suppl):508. [16] Matera M, Costantino G, Clementi G, et al. Experimental study on the toxicity and the local and systemic tolerability of gemcitabine after topical treatment of the rabbit bladder. Oncol Rep 2004;11: [17] Witjes JA, Vriesema JL, van der Heijden AG, et al. Pharmacokinetics of intravesical gemcitabine: a preclinical study in pigs. Eur Urol 2003;44: [18] Dalbagni G, Russo P, Sheinfeld J, et al. Phase I trial of intravesical gemcitabine in bacillus Calmette-Guerinrefractory transitional-cell carcinoma of the bladder. J Clin Oncol 2002;20: [19] Laufer M, Ramalingam S, Schoenberg MP, et al. Intravesical gemcitabine therapy for superficial transitional cell carcinoma of the bladder: a phase I and pharmacokinetic study. J Clin Oncol 2003;21: [20] Witjes JA, van der Heijden AG, Vriesema JL, et al. Intravesical gemcitabine: a phase 1 and pharmacokinetic study. Eur Urol 2004;45: [21] De Berardinis E, Antonini G, Peters GJ, et al. Intravesical administration of gemcitabine in superficial bladder cancer: a phase I study with pharmacodynamic evaluation. BJU Int 2004;93: [22] Palou J, Carcas A, Segarra J, et al. Phase I pharmacokinetic study of a single intravesical instillation of gemcitabine administered immediately after transurethral resection plus multiple random biopsies in patients with superficial bladder cancer. J Urol 2004;172: [23] Hall RR. Transurethral resection for transitional cell carcinoma. Problems Urol 1992;6: [24] Van der Meijden APM, Hall RR, Pavone Macaluso M, et al. Marker tumour response to the sequential combination of intravesical therapy with mitomycin C and BCG-RIVM in multiple superficial bladder tumours. Report from the European Organization for Research and Treatment on Cancer-Genitourinary Group (EORTC 30897). Eur Urol 1996;29: [25] Calais da Silva F, Denis L, Bono A, et al. Intravesical chemoresection with 4 0 -epi-doxorubicin in patients with superficial bladder tumors. Eur Urol 1988;14: [26] Van der Meijden A, Hall RR, Pavone Macaluso M, et al. Marker tumour response to the sequential combination of intravesical therapy with mitomycin-c and BCG-RIVM in multiple superficial bladder tumours. Eur Urol 1996;29: [27] Popert RJM, Goodall J, Coptcoat MJ, et al. Superficial bladder cancer: the response of a marker tumour to a single intravesical instillation of epirubicin. Br J Urol 1994;74: [28] Fellows G, Parmar M, Grigor R, et al. Marker tumour response to Evans and Pasteur BCG in multiple recurrent pta, pt1 bladder tumours: report from the Medical Research Council Subgroup on Superficial Bladder Cancer (Urological Cancer Working Party). Br J Urol 1994;73: [29] Mack D, Holtl W, Bassi P, et al. The ablative effect of quarter dose BCG on a papillary lesion of the bladder. J Urol 2001;165: [30] Calais da Silva FM, Calais da Silva FE. Phase 2 study 2000mg of intravesical gemcitabine in marker lesions. Eur Urol Suppl 2005;4(3):222 (abstract no. 877). [31] Gontero P, Casetta G, Maso G, et al. Phase II study to investigate the ablative efficacy of intravesical administration of gemcitabine in intermediate-risk superficial bladder cancer (SBC). Eur Urol 2004;46: [32] Maffezzini M, Campodonico F, Canepa G, Capponi G, Fontana V. Short-schedule intravesical gemcitabine with ablative intent in recurrent Ta T1, G1 G2, low- or intermediate-risk, transitional cell carcinoma of the bladder. Eur Urol 2007;51: [33] Serretta V, Galuffo A, Pavone C, Allegro R, Pavone- Macaluso M. Gemcitabine in intravesical treatment of Ta-T1 transitional cell carcinoma of the bladder: phase I-II study on marker lesion. Urology 2005;65: [34] Gardmark T, Carringer M, Beckman E, Malmstrom PU, members of the Intravesical Gemcitabine Study Group. Randomized phase II marker lesion study evaluating effect of scheduling on response to intravesical gemcitabine in recurrent Stage Ta urothelial cell carcinoma of the bladder. Urology 2005;66: [35] Bartoletti R, Cai T, Gacci M, et al. Intravesical gemcitabine therapy for superficial transitional cell carcinoma: results of a phase II prospective multicenter study. Urology 2005;66:
7 european urology supplements 6 (2007) [36] Conti G, the AURO (Associazione Urologi Ospedalieri) Group. Prospective phase II study on intravesical gemcitabine in intermediate risk SBC recurring after previous intravescial therapy. Arch Ital Urol Androl 2005, Abst 241. [37] Brausi M, Giussani L, Altieri V, et al. Phase II marker lesion study of 6-week intravesical gemcitabine instillation in patients with low risk non muscle invasive bladder tumours. Eur Urol Suppl 2007;6:59 (abstract no. 148).
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