Continued Progress in the Treatment of Advanced Renal Cell Carcinoma: An Update on the Role of Sunitinib

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1 european urology supplements 7 (2008) available at journal homepage: Continued Progress in the Treatment of Advanced Renal Cell Carcinoma: An Update on the Role of Sunitinib Peter Mulders * Department of Urology, Radboud University Nijmegen, Medical Centre, PO Box 9101, 6500 HB Nijmegen, The Netherlands Article info Keywords: Multi-targeted Renal cell carcinoma Sunitinib Tyrosine kinase inhibitor This paper summarizes a presentation at a Pfizersponsored satellite symposium at the European Association of Urology Congress, March 27, Abstract Context: Renal cell carcinoma (RCC) constitutes approximately 2 3% of all cancers worldwide. Approximately a third of patients diagnosed with RCC present with metastatic disease (mrcc) and in about a third of patients with localized disease, RCC recurs following treatment. Metastatic renal cell carcinoma (mrcc) is associated with poor survival rates, and until recently, cytokines were the only treatment options for mrcc. Objective: The rationale for the use of targeted agents in mrcc is reviewed, and the key challenges to optimizing treatment are discussed. Evidence acquisition: Clinical data on the safety and efficacy of targeted agents in mrcc, practical therapy management, and patient stratification strategies are reviewed. Evidence synthesis: The development of targeted agents, including sunitinib, sorafenib, temsirolimus, and bevacizumab (given with interferon-a [IFN-a]) has dramatically changed the outlook for patients with mrcc and improved survival rates. Sunitinib has demonstrated clinical efficacy for mrcc in phase 2 and phase 3 trials and in an expanded-access study. Sunitinib is now a reference standard of care for the first-line treatment of patients with mrcc. As with the other targeted agents, sunitinib treatment is associated with a particular profile of adverse events (AE). Management of AEs is critical, as tolerability can affect adherence to therapy and limit clinical benefit. The development of practical strategies to support the optimal use of targeted agents is essential. In addition, prognostic factors such as tumor histology affect treatment outcome. Patient stratification into risk groups based on prognostic factors allows optimal treatment selection. A treatment algorithm, based on patient stratification and the available clinical data for the targeted agents, may facilitate the optimal choice of treatment for patients with mrcc. Conclusions: This supplement reviews the clinical data from sunitinib studies in mrcc as well as practical therapy-management strategies and presents a treatment algorithm for mrcc. Finally, experience from the clinic is presented. # 2008 Published by Elsevier B.V. on behalf of European Association of Urology. * Tel ; Fax: address: P.Mulders@uro.umcn.nl /$ see front matter # 2008 Published by Elsevier B.V. on behalf of European Association of Urology. doi: /j.eursup

2 580 european urology supplements 7 (2008) Introduction The past few years have seen much activity centered on the development of novel anticancer therapies that target specific components of the pathways implicated in tumor growth and angiogenesis. Marketing authorizations have been granted in several different tumor types, for example, the humanized monoclonal antibody bevacizumab (Avastin; Gentech, San Francisco, CA, USA), licensed for the treatment of metastatic colorectal cancer in conjunction with chemotherapy and for the treatment of metastatic nonsquamous non small-cell lung cancer. In some instances, these therapies have become the new standard of care. The development of such therapies has transformed the manner in which cancer patients are treated and as such, targeted therapies may represent the future of cancer treatment. The management and treatment of metastatic renal cell carcinoma (mrcc) has evolved considerably with the recent development and introduction of targeted therapies. The outlook for patients with this historically treatment-insensitive tumor has substantially improved. The rationale for the use of targeted treatments in mrcc is reviewed below, along with a discussion of key challenges faced when optimizing mrcc treatment for individual patients. 2. Renal cell carcinoma epidemiology and histologic classification Worldwide, >200,000 patients are diagnosed with renal cell carcinoma (RCC) each year, accounting for approximately 2% of all cancers; the incidences are highest in North America, Australasia, and Europe [1]. In the European Union, there were >63,000 new cases of RCC and 26,000 deaths in 2006 [2]. US statistics show an increase in the incidence of RCC over the period in both men and women, accompanied by a smaller but significant reduction in RCC-related mortality [3]. RCC is more common in men than in women (ratio: 1.5:1), and incidence generally increases with age, with a median age at diagnosis of about 65 yr [3]. The majority of patients with RCC initially present with localized disease, for which surgery is the primary treatment option. However, 20 30% of patients are diagnosed with metastatic disease [3,4], and a high proportion of patients with localized disease subsequently develop metastases, despite undergoing nephrectomy with curative intent [5 7]. Prior to the advent of targeted therapies, the overall 5-yr survival rate from mrcc was approximately 10% [3]. RCC can be divided into five main histologic subtypes, of which clear-cell is the most common (approximately 75 85% of cases) [4]. Other subtypes include papillary (or chromophilic; 12 14% of cases), chromophobic (4 6%), oncocytic (2 4%), and collecting duct (1%) [4]. These RCC subtypes vary in their biologic behavior and response to treatment, leading to varying survival among patients with tumors of differing histology [8 10]. For example, in a retrospective analysis of studies carried out in patients with histopathologically confirmed RCC in Iceland, patients with chromophobic RCC had significantly longer 5-yr survival rate than those with papillary and clear-cell RCC (84.6% vs 66.5% and 54.9%, respectively; p < 0.001) [9]. However, in matched case-control series of patients who had undergone radical or partial nephrectomy, median survival in collecting duct carcinoma was similar to clear-cell RCC (4.9 yr vs 5.4 yr), despite the patients with collecting duct carcinoma presenting with more advanced-stage and aggressive disease [11]. 3. Historical treatment recommendations for metastatic renal cell carcinoma Overall, mrcc has proved extremely resistant to radiotherapy, chemotherapy, and hormonal therapy [12 14]. Until recently, the only treatments available were the cytokines, interferon-a (IFN-a), and interleukin-2 (IL-2). However, these agents provide survival benefits in a limited patient population, such as those with either a World Health Organization (WHO) status 0 1 or an Eastern Cooperative Oncology Group performance status (ECOG PS) of 0 1 (one metastatic site and clear-cell histology), and are associated with considerable toxicity, particularly in high doses [15 19]. Indeed, the updated European Association of Urology (EAU) guidelines on RCC state that only selected patients with mrcc with a good risk profile and clear-cell histology derive clinical benefit from treatment with IL-2 or IFN-a (grade B recommendation) [19]. Furthermore, combinations of cytokines, with or without additional chemotherapy, do not improve overall survival compared with monotherapy (grade A recommendation). 4. Rationale for targeted treatments The development of sporadic, clear-cell RCC has been linked in up to 65% of cases with biallelic

3 european urology supplements 7 (2008) inactivation of the von Hippel-Lindau (VHL) gene by deletion, mutation, or methylation [20 26]. Restoring VHL function in VHL / RCC lines prevents their ability to form tumors in nude mouse models, suggesting that VHL acts as a tumor suppressor [27]. The VHL protein targets the a-subunit of hypoxiainducible factor 1 (HIF-1a), a molecule that regulates cellular responses to hypoxia, for proteolysis [28,29]. In the absence of VHL, HIF-1a accumulates and activates the transcription of several genes, including vascular endothelial growth factor (VEGF) and platelet-derived growth factor (PDGF) [30]. These serve as agonists for their respective receptor tyrosine kinases, VEGF receptor (VEGFR) and PDGF receptor (PDGFR). Overexpression of VEGFR and PDGFR as well as other receptor tyrosine kinases is implicated in tumor angiogenesis and growth [31,32]. There is, therefore, a sound rationale for targeting the VEGF/VEGFR and PDGF/PDGFR systems in RCC. Activity of HIF-1a is also regulated by other growth-factor and cell-adhesion pathways [33]. Binding of growth factors increases levels of HIF- 1a through the phosphatidylinositol 3-kinase/Akt/ mammalian target of rapamycin (mtor) signal transduction pathway as well as the Ras/Raf/mitogen activated protein kinase pathway [33]. Thus, both of these pathways are also potential targets in RCC. Increased understanding of the genetics and biology of RCC has led to the development of several targeted agents, including sunitinib (Sutent; Pfizer Oncology, New York, NY, USA). Initial studies in the preclinical setting showed that sunitinib, a novel receptor tyrosine kinase inhibitor, targeted the VEGF, PDGF, stem cell factor (KIT), FLT3 and RET receptor tyrosine kinases [34 37] and demonstrated antitumor and antiangiogenic activity. Phase 1 studies in a broad range of solid tumors indicated sunitinib activity in patients with solid tumors, including RCC [38]. On the basis of the phase 1 results, two phase 2 studies were carried out in patients with mrcc who had failed prior cytokine treatment [39,40]. The promising efficacy results obtained in these two studies led to conditional approval for sunitinib for the treatment of advanced RCC. The subsequent pivotal phase 3 study, demonstrating superior clinical efficacy for sunitinib as compared to IFN-a in treatment-naïve patients, resulted in sunitinib approval in the first-line setting for the treatment of advanced and metastatic RCC [41]. Sunitinib activity has also been examined in a broader population of patients, including those ineligible for participation in the clinical trials, in an expanded-access study [42]. 5. Current treatment recommendations for metastatic renal cell carcinoma In addition to sunitinib, targeted therapies for mrcc approved in Europe include the oral multitargeted receptor tyrosine kinase inhibitor sorafenib (Nexavar; Bayer HealthCare Pharmaceuticals, Leverkusen, Germany); the mtor kinase inhibitor temsirolimus (Torisel; Wyeth, Collegeville, PA, USA); and the VEGF-targeted monoclonal antibody bevacizumab (Avastin), which is given in combination with IFN-a. As mentioned previously, the efficacy of sunitinib has been demonstrated in a phase 3 randomized trial in the first-line setting, where sunitinib treatment resulted in median progression-free survival more than double that observed with IFN-a (11 mo vs 5 mo, respectively; p < ) [41,43,44]. Recent presentation of the final overall survival (OS) data from the phase 3 study confirmed sunitinib benefit in the firstline treatment of patients with mrcc [44]. Sunitinib resulted in median OS of >2 yr (26.4 mo, 95% confidence interval [CI]: ), which was substantially longer than that observed for IFN-a (21.8 mo, 95% CI: ; hazard ratio [HR] 0.821, 95% CI: ; p = [log-rank test]; p = [Wilcoxon test]) [44]. As such, sunitinib is now considered a reference standard of care in this setting. In this supplement, we review recent advances in the treatment of mrcc, focusing on the rationale for the use of receptor tyrosine kinase inhibitors. We review the available clinical data supporting their efficacy in mrcc and examine the practical management of targeted therapies to optimize treatment outcomes. Patient selection and the prognostic factors affecting clinical outcomes are discussed, and a potential treatment algorithm is described in the context of different patient profiles and characteristics. In the first article, Professor Joaquim Bellmunt examines the efficacy data from key clinical trials with sunitinib in mrcc as well as the ongoing expanded-access study, which involves a heterogeneous population of patients that includes subgroups of concern (patients with brain metastases, aged 65 yr, with non clear-cell histology and PS 2) not previously studied. The expanded-access study provides a valuable insight into the real-life clinical profile of sunitinib in an uncontrolled setting across a broad range of patients. All the targeted therapies in mrcc discussed above are associated with adverse events (AEs). The adverse event profile observed with targeted therapies differs from that observed with conventional chemotherapy or immunotherapy. Therapy-management approaches, encompassing early identifi-

4 582 european urology supplements 7 (2008) cation of AEs and the development of management strategies to limit their impact, is a continuing challenge for clinicians involved in the care of patients with mrcc. The safety profile of sunitinib is well defined and broadly consistent in all patient subgroups with mrcc, with AEs manageable according to standard medical intervention or dose modification. Sunitinib safety data, along with practical therapy-management strategies, are discussed in the second article by Dr Jan Roigas. The ability to select patients most likely to benefit from a given treatment is critical to optimal medical care and to support the best use of available resources. Risk groups for patients with mrcc, based on prognostic variables, were developed some years ago and continue to be relevant in the era of targeted therapy. Patient-stratification strategies, along with recommendations for the optimal use of sunitinib and other targeted therapies in mrcc, are reviewed in the third article in this issue by Dr Jean-Jacques Patard. Finally, case reports of interest are presented to highlight the practical use of targeted agents, including strategies to maximize clinical benefit while managing AEs. The case studies describe treatment of two patients with mrcc, each stratified into the intermediate and poor Memorial Sloan- Kettering Cancer Center (MSKCC) risk categories, respectively. The first patient developed multiple soft-tissue and lung metastases following nephrectomy, whereas the second presented with synchronous liver metastases. Both patients were treated with sunitinib, and the case studies, described by Professor Vincenzo Ficarra, confirm the efficacy of sunitinib in the treatment of patients stratified into different MSKCC risk groups. 6. Conclusions The treatment of patients with mrcc has advanced considerably over the past few years and looks set to change further as clinicians refine strategies for deriving maximum benefit from newly available targeted agents. This supplement provides an update on the most recent efficacy data from sunitinib clinical studies and describes strategies for patient management, including recommendations for the optimal use of sunitinib and other targeted therapies in mrcc. Conflicts of interest Peter Mulders is an advisor for Pfizer Inc., Bayer Pharmaceuticals, Gen-Probe, and Antigenics; has received honoraria from AstraZeneca, Bayer Pharmaceuticals, Pfizer Inc., and Novartis; and has received research funding from Bayer Pharmaceuticals and AstraZeneca. Funding support Pfizer Inc. provided funding for editorial assistance. Acknowledgments The author acknowledges ACUMED (Tytherington, UK) for providing editorial assistance for this paper. References [1] Parkin DM, Bray F, Ferlay J, Pisani P. Global cancer statistics, CA Cancer J Clin 2005;55: [2] Ferlay J, Autier P, Boniol M, et al. Estimates of the cancer incidence and mortality in Europe in Ann Oncol 2007;18: [3] Ries LAG, Melbert D, Krapcho M, et al, eds. SEER Cancer Statistics Review, National Cancer Institute Web site. Available at: _2004/. Accessed June 25, [4] Motzer RJ, Bander NH, Nanus DM. Renal-cell carcinoma. N Engl J Med 1996;335: [5] Antonelli A, Cozzoli A, Zani D, et al. The follow-up management of non-metastatic renal cell carcinoma: definition of a surveillance protocol. BJU Int 2007;99: [6] Janzen NK, Kim HL, Figlin RA, Belldegrun AS. Surveillance after radical or partial nephrectomy for localized renal cell carcinoma and management of recurrent disease. Urol Clin North Am 2003;30: [7] Rabinovitch RA, Zelefsky MJ, Gaynor JJ, Fuks Z. Patterns of failure following surgical resection of renal cell carcinoma: implications for adjuvant local and systemic therapy. J Clin Oncol 1994;12: [8] Cheville JC, Lohse CM, Zincke H, Weaver AL, Blute ML. Comparisons of outcome and prognostic features among histologic subtypes of renal cell carcinoma. Am J Surg Pathol 2003;27: [9] Gudbjartsson T, Hardarson S, Petursdottir V, Thoroddsen A, Magnusson J, Einarsson GV. Histological subtyping and nuclear grading of renal cell carcinoma and their implications for survival: a retrospective nation-wide study of 629 patients. Eur Urol 2005;48: [10] Upton MP, Parker RA, Youmans A, McDermott DF, Atkins MB. Histologic predictors of renal cell carcinoma response to interleukin-2-based therapy. J Immunother 2005;28: [11] Karakiewicz PI, Trinh Q-D, Rioux-Leclercq N, et al. Collecting duct renal cell carcinoma: a matched analysis of 41 cases. Eur Urol 2007;52:

5 european urology supplements 7 (2008) [12] Godley P, Taylor M. Renal cell carcinoma. Curr Opin Oncol 2001;13: [13] Lilleby W, Fossa SD. Chemotherapy in metastatic renal cell cancer. World J Urol 2005;23: [14] Rohrmann K, Staehler M, Haseke N, et al. Immunotherapy in metastatic renal cell carcinoma. World J Urol 2005; 23: [15] Coppin C, Porzsolt F, Awa A, et al. Immunotherapy for advanced renal cell cancer. Cochrane Database of Systematic Reviews;2005. Abstract CD [16] McDermott DF, Regan MM, Clark JI, et al. Randomized phase III trial of high-dose interleukin-2 versus subcutaneous interleukin-2 and interferon in patients with metastatic renal cell carcinoma. J Clin Oncol 2005;23: [17] Negrier S, Escudier B, Lasset C, et al. Recombinant human interleukin-2, recombinant human interferon alfa-2a, or both in metastatic renal-cell carcinoma. Groupe Francais d Immunotherapie. N Engl J Med 1998;338: [18] Negrier S, Perol D, Ravaud A, et al. Do cytokines improve survival in patients with metastatic renal cell carcinoma (MRCC) of intermediate prognosis? Results of the prospective randomized PERCY Quattro trial [abstract]. J Clin Oncol 2005;23(Suppl 16S):380S. [19] Ljungberg B, Hanbury DC, Kuczyk MA, et al. Renal cell carcinoma guideline. Eur Urol 2007;51: [20] Clifford SC, Prowse AH, Affara NA, Buys CH, Maher ER. Inactivation of the von Hippel-Lindau (VHL) tumour suppressor gene and allelic losses at chromosome arm 3p in primary renal cell carcinoma: evidence for a VHL-independent pathway in clear cell renal tumourigenesis. Genes Chromosomes Cancer 1998;22: [21] Foster K, Prowse A, van den Berg A, et al. Somatic mutations of the von Hippel-Lindau disease tumour suppressor gene in non-familial clear cell renal carcinoma. Hum Mol Genet 1994;3: [22] Gnarra JR, Tory K, Weng Y, et al. Mutations of the VHL tumour suppressor gene in renal carcinoma. Nat Genet 1994;7: [23] Herman JG, Latif F, Weng Y, et al. Silencing of the VHL tumor-suppressor gene by DNA methylation in renal carcinoma. Proc Natl Acad Sci U S A 1994;91: [24] Kim WY, Kaelin WG. Role of VHL gene mutation in human cancer. J Clin Oncol 2004;22: [25] Na X, Wu G, Ryan CK, et al. Overproduction of vascular endothelial growth factor related to von Hippel-Lindau tumor suppressor gene mutations and hypoxia-inducible factor-1 alpha expression in renal cell carcinomas. J Urol 2003;170: [26] Rini BI, Small EJ. Biology and clinical development of vascular endothelial growth factor-targeted therapy in renal cell carcinoma. J Clin Oncol 2005;23: [27] Iliopoulos O, Levy AP, Jiang C, Kaelin Jr WG, Goldberg MA. Negative regulation of hypoxia-inducible genes by the von Hippel-Lindau protein. Proc Natl Acad Sci U S A 1996;93: [28] Cockman ME, Masson N, Mole DR, et al. Hypoxia inducible factor-alpha binding and ubiquitylation by the von Hippel-Lindau tumor suppressor protein. J Biol Chem 2000;275: [29] Maxwell PH, Wiesener MS, Chang GW, et al. The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 1999;399: [30] Kaelin Jr WG. The von Hippel-Lindau tumor suppressor gene and kidney cancer. Clin Cancer Res 2004;10:6290S 5S. [31] Krause DS, Van Etten RA. Tyrosine kinases as targets for cancer therapy. N Engl J Med 2005;353: [32] Kawai Y, Sakano S, Korenaga Y, Eguchi S, Naito K. Associations of single nucleotide polymorphisms in the vascular endothelial growth factor gene with the characteristics and prognosis of renal cell carcinomas. Eur Urol 2007;52: [33] Motzer R, Bukowski R. Targeted therapy for metastatic renal cell carcinoma. J Clin Oncol 2006;24: [34] Abrams TJ, Lee LB, Murray LJ, Pryer NK, Cherrington JM. SU11248 inhibits KIT and platelet-derived growth factor receptor beta in preclinical models of human small cell lung cancer. Mol Cancer Ther 2003;2: [35] Kim DW, Jo YS, Jung HS, et al. An orally administered multitarget tyrosine kinase inhibitor, SU11248, is a novel potent inhibitor of thyroid oncogenic RET/papillary thyroid cancer kinases. J Clin Endocrinol Metab 2006;91: [36] Mendel DB, Laird AD, Xin X, et al. In vivo antitumor activity of SU11248, a novel tyrosine kinase inhibitor targeting vascular endothelial growth factor and platelet-derived growth factor receptors: determination of a pharmacokinetic/pharmacodynamic relationship. Clin Cancer Res 2003;9: [37] O Farrell AM, Abrams TJ, Yuen HA, et al. SU11248 is a novel FLT3 tyrosine kinase inhibitor with potent activity in vitro and in vivo. Blood 2003;101: [38] Faivre S, Delbaldo C, Vera K, et al. Safety, pharmacokinetic, and antitumor activity of SU11248, a novel oral multitarget tyrosine kinase inhibitor, in patients with cancer. J Clin Oncol 2006;24: [39] Motzer RJ, Michaelson MD, Redman BG, et al. Activity of SU11248, a multitargeted inhibitor of vascular endothelial growth factor receptor and platelet-derived growth factor receptor, in patients with metastatic renal cell carcinoma. J Clin Oncol 2006;24: [40] Motzer RJ, Rini BI, Bukowski RM, et al. Sunitinib in patients with metastatic renal cell carcinoma. JAMA 2006;295: [41] Motzer RJ, Hutson TE, Tomczak P, et al. Sunitinib versus interferon alfa in metastatic renal-cell carcinoma. N Engl J Med 2007;356: [42] Gore M, Szczylik C, Porta C, et al. Sunitinib in metastatic renal cell carcinoma (mrcc): preliminary assessment of safety and efficacy in an expanded access trial with subpopulation analysis [abstract]. Eur J Cancer Suppl 2007;5:299.

6 584 european urology supplements 7 (2008) [43] Motzer RJ, Figlin R, Hutson TE, et al. Sunitinib versus interferon-alfa (IFNa) as first-line treatment of metastatic renal cell carcinoma (mrcc): updated results and analysis of prognostic factors [abstract]. J Clin Oncol 2007;25(Suppl), abstract [44] Figlin RA, Hutson TE, Tomczak P, et al. Overall survival with sunitinib versus interferon (IFN)-alfa as first-line treatment of metastatic renal cell carcinoma (mrcc). J Clin Oncol 2008;26(Suppl), Oral presentation (abstract 5024).

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