New and emerging therapies for bone metastases in genitourinary cancers

European Urology

Volumn 63, Issue 2, 2013, Pages 309-320

  Saylor, Philip J ^a   Armstrong, Andrew J ^b   Fizazi, Karim ^c   Freedland, Stephen ^d   Saad, Fred ^e   Smith, Matthew R ^a   Tombal, Bertrand ^f   Pienta, Kenneth ^g  

^a MASSACHUSETTS GENERAL HOSPITAL CANCER CENTER   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

^c INSTITUT GUSTAVE ROUSSY   (France)

^d DUKE UNIVERSITY   (United States)

^e CENTRE HOSPITALIER DE L UNIVERSITÉ DE MONTRÉAL   (Canada)

^f CLINIQUES UNIVERSITAIRES SAINT LUC   (Belgium)

^g UNIVERSITY OF MICHIGAN COMPREHENSIVE CANCER CENTER   (United States)

Author keywords

Bladder cancer; Bone metastases; Denosumab; Prostate cancer; Radium 223; Urothelial cancer; Zoledronic acid

Indexed keywords

ABIRATERONE; BISPHOSPHONIC ACID DERIVATIVE; CABOZANTINIB; CLODRONIC ACID; DASATINIB; DENOSUMAB; DOCETAXEL; ENZALUTAMIDE; ETIDRONIC ACID RE 186; LEXIDRONAM SAMARIUM SM 153; MITOXANTRONE; PAMIDRONIC ACID; PLACEBO; RADIOPHARMACEUTICAL AGENT; RADIUM 223; STRONTIUM 89; UNCLASSIFIED DRUG; ZOLEDRONIC ACID;

ANDROGEN DEPRIVATION THERAPY; BLADDER CANCER; BONE MARROW SUPPRESSION; BONE METASTASIS; CANCER INCIDENCE; CANCER PAIN; CANCER PALLIATIVE THERAPY; CANCER SURVIVAL; CANCER THERAPY; CASTRATION RESISTANT PROSTATE CANCER; DRUG APPROVAL; DRUG EFFICACY; DRUG POTENCY; DRUG SAFETY; FEVER; FLU LIKE SYNDROME; HUMAN; HYPOCALCEMIA; IC 50; JAW OSTEONECROSIS; KIDNEY CARCINOMA; MALAISE; MOLECULARLY TARGETED THERAPY; MYALGIA; NEPHROTOXICITY; NEUTROPENIA; OVERALL SURVIVAL; PATHOLOGIC FRACTURE; PATHOPHYSIOLOGY; PATIENT CARE; PHASE 3 CLINICAL TRIAL (TOPIC); PREVALENCE; PRIORITY JOURNAL; PROSTATE CANCER; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; SPINAL CORD COMPRESSION; SYSTEMIC THERAPY; THROMBOCYTOPENIA; TRANSITIONAL CELL CARCINOMA; UROGENITAL TRACT CANCER;

ANTIBODIES, MONOCLONAL, HUMANIZED; BONE DENSITY CONSERVATION AGENTS; BONE NEOPLASMS; CARCINOMA; DIPHOSPHONATES; FEMALE; HUMANS; IMIDAZOLES; KIDNEY NEOPLASMS; MALE; PROSPECTIVE STUDIES; PROSTATIC NEOPLASMS; RADIOPHARMACEUTICALS; RADIUM; RANDOMIZED CONTROLLED TRIALS AS TOPIC; RANK LIGAND; URINARY BLADDER NEOPLASMS; UROGENITAL NEOPLASMS; UROTHELIUM;

EID: 84871918834     PISSN: 03022838     EISSN: 18737560     Source Type: Journal    
DOI: 10.1016/j.eururo.2012.10.007     Document Type: Review

References (80)

1. F.E. Lecouvet, D. Geukens, and A. Stainier Magnetic resonance imaging of the axial skeleton for detecting bone metastases in patients with high-risk prostate cancer: diagnostic and cost-effectiveness and comparison with current detection strategies J Clin Oncol 25 2007 3281 3287 (Pubitemid 47325613)
2. H.I. Scher, S. Halabi, and I. Tannock Design and end points of clinical trials for patients with progressive prostate cancer and castrate levels of testosterone: recommendations of the Prostate Cancer Clinical Trials Working Group J Clin Oncol 26 2008 1148 1159
3. F. Saad, D.M. Gleason, and R. Murray A randomized, placebo-controlled trial of zoledronic acid in patients with hormone-refractory metastatic prostate carcinoma J Natl Cancer Inst 94 2002 1458 1468
4. F. Saad, D.M. Gleason, and R. Murray Long-term efficacy of zoledronic acid for the prevention of skeletal complications in patients with metastatic hormone-refractory prostate cancer J Natl Cancer Inst 96 2004 879 882 (Pubitemid 38807610)
5. J. Zekri, N. Ahmed, R.E. Coleman, and B.W. Hancock The skeletal metastatic complications of renal cell carcinoma Int J Oncol 19 2001 379 382
6. R.J. Motzer, B. Escudier, and S. Oudard Efficacy of everolimus in advanced renal cell carcinoma: a double-blind, randomised, placebo-controlled phase III trial Lancet 372 2008 449 456
7. R.J. Motzer, T.E. Hutson, and P. Tomczak Sunitinib versus interferon alfa in metastatic renal-cell carcinoma N Engl J Med 356 2007 115 124 (Pubitemid 46089672)
8. A. Lipton, A. Colombo-Berra, R.M. Bukowski, L. Rosen, M. Zheng, and G. Urbanowitz Skeletal complications in patients with bone metastases from renal cell carcinoma and therapeutic benefits of zoledronic acid Clin Cancer Res 10 2004 6397S-403S
9. A. Lipton, M. Zheng, and J. Seaman Zoledronic acid delays the onset of skeletal-related events and progression of skeletal disease in patients with advanced renal cell carcinoma Cancer 98 2003 962 969 (Pubitemid 37022096)
10. J. Bellmunt, T.K. Choueiri, and R. Fougeray Prognostic factors in patients with advanced transitional cell carcinoma of the urothelial tract experiencing treatment failure with platinum-containing regimens J Clin Oncol 28 2010 1850 1855
11. M.S. Zaghloul, R. Boutrus, H. El-Hossieny, Y.A. Kader, I. El-Attar, and M. Nazmy A prospective, randomized, placebo-controlled trial of zoledronic acid in bony metastatic bladder cancer Int J Clin Oncol 15 2010 382 389
12. W.J. Boyle, W.S. Simonet, and D.L. Lacey Osteoclast differentiation and activation Nature 423 2003 337 342 (Pubitemid 40852708)
13. P.V. Hauschka, A.E. Mavrakos, M.D. Iafrati, S.E. Doleman, and M. Klagsbrun Growth factors in bone matrix. Isolation of multiple types by affinity chromatography on heparin-Sepharose J Biol Chem 261 1986 12665 12674 (Pubitemid 17204223)
14. H. Kodama, M. Nose, S. Niida, and A. Yamasaki Essential role of macrophage colony-stimulating factor in the osteoclast differentiation supported by stromal cells J Exp Med 173 1991 1291 1294
15. Y.Y. Kong, H. Yoshida, and I. Sarosi OPGL is a key regulator of osteoclastogenesis, lymphocyte development and lymph-node organogenesis Nature 397 1999 315 323
16. D.L. Lacey, E. Timms, and H.L. Tan Osteoprotegerin ligand is a cytokine that regulates osteoclast differentiation and activation Cell 93 1998 165 176 (Pubitemid 28180851)
17. R.J. Cook, R. Coleman, and J. Brown Markers of bone metabolism and survival in men with hormone-refractory metastatic prostate cancer Clin Cancer Res 12 2006 3361 3367
18. L. Costa, L.M. Demers, and A. Gouveia-Oliveira Prospective evaluation of the peptide-bound collagen type I cross-links N-telopeptide and C-telopeptide in predicting bone metastases status J Clin Oncol 20 2002 850 856 (Pubitemid 34111395)
19. R.E. Coleman, P. Major, and A. Lipton Predictive value of bone resorption and formation markers in cancer patients with bone metastases receiving the bisphosphonate zoledronic acid J Clin Oncol 23 2005 4925 4935 (Pubitemid 46223998)
20. J.E. Brown, R.J. Cook, and P. Major Bone turnover markers as predictors of skeletal complications in prostate cancer, lung cancer, and other solid tumors J Natl Cancer Inst 97 2005 59 69
21. J.E. Brown, C.S. Thomson, S.P. Ellis, S.A. Gutcher, O.P. Purohit, and R.E. Coleman Bone resorption predicts for skeletal complications in metastatic bone disease Br J Cancer 89 2003 2031 2037 (Pubitemid 38030899)
22. S. Rajpar, C. Massard, and A. Laplanche Urinary N-telopeptide (uNTx) is an independent prognostic factor for overall survival in patients with bone metastases from castration-resistant prostate cancer Ann Oncol 21 2010 1864 1869
23. K. Fizazi, M. Carducci, and M. Smith Denosumab versus zoledronic acid for treatment of bone metastases in men with castration-resistant prostate cancer: a randomised, double-blind study Lancet 377 2011 813 822
24. D.M. Anderson, E. Maraskovsky, and W.L. Billingsley A homologue of the TNF receptor and its ligand enhance T-cell growth and dendritic-cell function Nature 390 1997 175 179 (Pubitemid 27507987)
25. M.F. Bachmann, B.R. Wong, R. Josien, R.M. Steinman, A. Oxenius, and Y. Choi TRANCE, a tumor necrosis factor family member critical for CD40 ligand-independent T helper cell activation J Exp Med 189 1999 1025 1031 (Pubitemid 29169819)
26. N.B. Watts, C. Roux, and J.F. Modlin Infections in postmenopausal women with osteoporosis treated with denosumab or placebo: coincidence or causal association? Osteoporos Int 23 2012 327 337
27. S.R. Cummings, J. San Martin, and M.R. McClung Denosumab for prevention of fractures in postmenopausal women with osteoporosis N Engl J Med 361 2009 756 765
28. A.T. Stopeck, A. Lipton, and J.J. Body Denosumab compared with zoledronic acid for the treatment of bone metastases in patients with advanced breast cancer: a randomized, double-blind study J Clin Oncol 28 2010 5132 5139
29. D.H. Henry, L. Costa, and F. Goldwasser Randomized, double-blind study of denosumab versus zoledronic acid in the treatment of bone metastases in patients with advanced cancer (excluding breast and prostate cancer) or multiple myeloma J Clin Oncol 29 2010 1125 1132
30. F.M. Paes, and A.N. Serafini Systemic metabolic radiopharmaceutical therapy in the treatment of metastatic bone pain Semin Nucl Med 40 2010 89 104
31. C. Parker, D. Heinrich, and J.M. O'Sullivan Overall survival benefit and safety profile of radium-223 chloride, a first-in-class alpha-pharmaceutical: results from a phase III randomized trial (ALSYMPCA) in patients with castration-resistant prostate cancer (CRPC) with bone metastases [abstract] J Clin Oncol 30 Suppl 5 2012
32. J.S. de Bono, C.J. Logothetis, and A. Molina Abiraterone and increased survival in metastatic prostate cancer N Engl J Med 364 2011 1995 2005
33. H.I. Scher, K. Fizazi, and F. Saad Increased survival with enzalutamide in prostate cancer after chemotherapy N Engl J Med 367 2012 1187 1197
34. A.O. Sartor, D. Heinrich, and S.I. Helle Radium-223 chloride impact on skeletal-related events in patients with castration-resistant prostate cancer (CRPC) with bone metastases: a phase III randomized trial (ALSYMPCA) [abstract] J Clin Oncol 30 Suppl 5 2012
35. D.P. Dearnaley, M.D. Mason, M.K. Parmar, K. Sanders, and M.R. Sydes Adjuvant therapy with oral sodium clodronate in locally advanced and metastatic prostate cancer: long-term overall survival results from the MRC PR04 and PR05 randomised controlled trials Lancet Oncol 10 2009 872 876
36. D.P. Dearnaley, M.R. Sydes, and M.D. Mason A double-blind, placebo-controlled, randomized trial of oral sodium clodronate for metastatic prostate cancer (MRC PR05 Trial) J Natl Cancer Inst 95 2003 1300 1311 (Pubitemid 37160863)
37. M.D. Mason, M.R. Sydes, and J. Glaholm Oral sodium clodronate for nonmetastatic prostate cancer - results of a randomized double-blind placebo-controlled trial: Medical Research Council PR04 (ISRCTN61384873) J Natl Cancer Inst 99 2007 765 776 (Pubitemid 47073523)
38. M.R. Smith, F. Kabbinavar, and F. Saad Natural history of rising serum prostate-specific antigen in men with castrate nonmetastatic prostate cancer J Clin Oncol 23 2005 2918 2925 (Pubitemid 46224110)
39. Wirth M, Tammela T, Debruyne F, et al. Effectiveness of zoledronic acid for the prevention of bone metastases in high-risk prostate cancer patients. A randomised, open label, multicenter study of the European Association of Urology (EAU) in cooperation with the Scandinavian Prostate Cancer Group (SPCG) and the Arbeitsgemeinschaft Urologische Onkologie (AUO). A report of the ZEUS study [abstract 184]. Presented at: American Society of Clinical Oncology Genitourinary Cancers Symposium; February 14-16, 2008; San Francisco, CA, USA.
40. M.R. Smith, F. Saad, and R. Coleman Denosumab and bone-metastasis-free survival in men with castration-resistant prostate cancer: results of a phase 3, randomised, placebo-controlled trial Lancet 379 2011 39 46
41. F. Saad, M. Smith, and N. Shore Effect of denosumab on prolonging bone-metastasis free survival (BMFS) in men with nonmetastatic castrate-resistant prostate cancer (CRPC) presenting with aggressive PSA kinetics [abstract] J Clin Oncol 30 Suppl 2012
42. S. Halabi, E.J. Small, and P.W. Kantoff Prognostic model for predicting survival in men with hormone-refractory metastatic prostate cancer J Clin Oncol 21 2003 1232 1237 (Pubitemid 46606398)
43. A.J. Armstrong, E.S. Garrett-Mayer, Y.C. Yang, R. de Wit, I.F. Tannock, and M. Eisenberger A contemporary prognostic nomogram for men with hormone-refractory metastatic prostate cancer: a TAX327 study analysis Clin Cancer Res 13 2007 6396 6403 (Pubitemid 350075029)
44. A.J. Armstrong, E. Garrett-Mayer, R. de Wit, I. Tannock, and M. Eisenberger Prediction of survival following first-line chemotherapy in men with castration-resistant metastatic prostate cancer Clin Cancer Res 16 2010 203 211
45. K. Fizazi, A. Lipton, and X. Mariette Randomized phase II trial of denosumab in patients with bone metastases from prostate cancer, breast cancer, or other neoplasms after intravenous bisphosphonates J Clin Oncol 27 2009 1564 1571
46. K. Fizazi, L. Bosserman, G. Gao, T. Skacel, and R. Markus Denosumab treatment of prostate cancer with bone metastases and increased urine N-telopeptide levels after therapy with intravenous bisphosphonates: results of a randomized phase II trial J Urol 182 2009 509 515 discussion 515-6
47. S.M. Tu, R.E. Millikan, and B. Mengistu Bone-targeted therapy for advanced androgen-independent carcinoma of the prostate: a randomised phase II trial Lancet 357 2001 336 341 (Pubitemid 32128538)
48. K. Fizazi, P. Beuzeboc, and J. Lumbroso Phase II trial of consolidation docetaxel and samarium-153 in patients with bone metastases from castration-resistant prostate cancer J Clin Oncol 27 2009 2429 2435
49. C. Parker, S. Nilsson, and D. Heinrich Updated analysis of the phase III, double-blind, randomized, multinational study of radium-223 chloride in castration-resistant prostate cancer (CRPC) patients with bone metastases (ALSYMPCA) [abstract] J Clin Oncol 30 Suppl 2012
50. D. Tong, L. Gillick, and F.R. Hendrickson The palliation of symptomatic osseous metastases: final results of the Study by the Radiation Therapy Oncology Group Cancer 50 1982 893 899 (Pubitemid 12047122)
51. B. Jeremic Single fraction external beam radiation therapy in the treatment of localized metastatic bone pain. A review J Pain Symptom Manage 22 2001 1048 1058 (Pubitemid 33152691)
52. F. Saad, and A. Lipton SRC kinase inhibition: targeting bone metastases and tumor growth in prostate and breast cancer Cancer Treat Rev 36 2010 177 184
53. K. Fizazi The role of Src in prostate cancer Ann Oncol 18 2007 1765 1773 (Pubitemid 350119560)
54. E.Y. Yu, G. Wilding, and E. Posadas Phase II study of dasatinib in patients with metastatic castration-resistant prostate cancer Clin Cancer Res 15 2009 7421 7428
55. E.Y. Yu, C. Massard, and M.E. Gross Once-daily dasatinib: expansion of phase II study evaluating safety and efficacy of dasatinib in patients with metastatic castration-resistant prostate cancer Urology 77 2011 1166 1171
56. J.C. Araujo, P. Mathew, and A.J. Armstrong Dasatinib combined with docetaxel for castration-resistant prostate cancer: results from a phase 1-2 study Cancer 118 2012 63 71
57. F.M. Yakes, J. Chen, and J. Tan Cabozantinib (XL184), a novel MET and VEGFR2 inhibitor, simultaneously suppresses metastasis, angiogenesis, and tumor growth Mol Cancer Ther 10 2011 2298 2308
58. M. Hussain, M.R. Smith, and C. Sweeney Cabozantinib (XL184) in metastatic castration-resistant prostate cancer (mCRPC): results from a phase II randomized discontinuation trial [abstract] J Clin Oncol 29 Suppl 2011
59. D.C. Smith, M.R. Smith, and E.J. Small Phase II study of XL184 in a cohort of patients (pts) with castration-resistant prostate cancer (CRPC) and measurable soft tissue disease [abstract] J Clin Oncol 29 Suppl 7 2011
60. W.K. Kelly, S. Halabi, and M. Carducci Randomized, double-blind, placebo-controlled phase III trial comparing docetaxel and prednisone with or without bevacizumab in men with metastatic castration-resistant prostate cancer: CALGB 90401 J Clin Oncol 30 2012 1534 1540
61. M.D. Michaelson, S. Oudard, and Y. Ou Randomized, placebo-controlled, phase III trial of sunitinib in combination with prednisone (SU + P) versus prednisone (P) alone in men with progressive castration-resistant prostate cancer (mCRPC) [abstract] J Clin Oncol 29 Suppl 2011
62. M.S. Gordon, C.S. Sweeney, and D.S. Mendelson Safety, pharmacokinetics, and pharmacodynamics of AMG 102, a fully human hepatocyte growth factor-neutralizing monoclonal antibody, in a first-in-human study of patients with advanced solid tumors Clin Cancer Res 16 2010 699 710
63. C.J. Ryan, M. Rosenthal, and S. Ng A multicenter, randomized phase II study of rilotumumab (R) (AMG 102) or placebo (Pbo) plus mitoxantrone (M) and prednisone (P) in patients (pts) with previously treated castrate-resistant prostate cancer (CRPC) [abstract] J Clin Oncol 30 Suppl 5 2012
64. L.S. Rosen, D. Gordon, and S. Tchekmedyian Zoledronic acid versus placebo in the treatment of skeletal metastases in patients with lung cancer and other solid tumors: a phase III, double-blind, randomized trial - the Zoledronic Acid Lung Cancer and Other Solid Tumors Study Group J Clin Oncol 21 2003 3150 3157 (Pubitemid 46606297)
65. E. Woodward, S. Jagdev, and L. McParland Skeletal complications and survival in renal cancer patients with bone metastases Bone 48 2011 160 166
66. J. Ferlay, D.M. Parkin, and E. Steliarova-Foucher Estimates of cancer incidence and mortality in Europe in 2008 Eur J Cancer 46 2010 765 781
67. R. Siegel, D. Naishadham, and A. Jemal Cancer statistics, 2012 CA Cancer J Clin 62 2012 10 29
68. R.E. Marx Pamidronate (Aredia) and zoledronate (Zometa) induced avascular necrosis of the jaws: a growing epidemic J Oral Maxillofac Surg 61 2003 1115 1117 (Pubitemid 37064711)
69. S.L. Ruggiero, B. Mehrotra, T.J. Rosenberg, and S.L. Engroff Osteonecrosis of the jaws associated with the use of bisphosphonates: a review of 63 cases J Oral Maxillofac Surg 62 2004 527 534 (Pubitemid 38542516)
70. A.O. Hoff, B.B. Toth, and K. Altundag Frequency and risk factors associated with osteonecrosis of the jaw in cancer patients treated with intravenous bisphosphonates J Bone Miner Res 23 2008 826 836 (Pubitemid 351768801)
71. F. Saad, J.E. Brown, and C. Van Poznak Incidence, risk factors, and outcomes of osteonecrosis of the jaw: integrated analysis from three blinded active-controlled phase III trials in cancer patients with bone metastases Ann Oncol 23 2011 1341 1347
72. AAOMS American Association of Oral and Maxillofacial Surgeons position paper on bisphosphonate-related osteonecrosis of the jaws J Oral Maxillofac Surg 65 2007 369 376
73. M.A. Dimopoulos, E. Kastritis, and C. Bamia Reduction of osteonecrosis of the jaw (ONJ) after implementation of preventive measures in patients with multiple myeloma treated with zoledronic acid Ann Oncol 20 2009 117 120
74. B.J. Edwards, J.W. Hellstein, P.L. Jacobsen, S. Kaltman, A. Mariotti, C.A. Migliorati American Dental Association Council on Scientific Affairs Expert Panel on Bisphosphonate-Associated Osteonecrosis of the Jaw Updated recommendations for managing the care of patients receiving oral bisphosphonate therapy: an advisory statement from the American Dental Association Council on Scientific Affairs J Am Dent Assoc 139 2008 1674 1677
75. C.I. Ripamonti, M. Maniezzo, and T. Campa Decreased occurrence of osteonecrosis of the jaw after implementation of dental preventive measures in solid tumour patients with bone metastases treated with bisphosphonates. The experience of the National Cancer Institute of Milan Ann Oncol 20 2009 137 145
76. S.L. Ruggiero, T.B. Dodson, L.A. Assael, R. Landesberg, R.E. Marx, and B. Mehrotra American Association of Oral and Maxillofacial Surgeons position paper on bisphosphonate-related osteonecrosis of the jaws - 2009 update J Oral Maxillofac Surg 67 Suppl 5 2009 2 12
77. G.S. Markowitz, P.L. Fine, and J.I. Stack Toxic acute tubular necrosis following treatment with zoledronate (Zometa) Kidney Int 64 2003 281 289 (Pubitemid 36714182)
78. Zometa [package insert]. Basel, Switzerland: Novartis International AG; 2009.
79. D.S. Ernst, I.F. Tannock, and E.W. Winquist Randomized, double-blind, controlled trial of mitoxantrone/prednisone and clodronate versus mitoxantrone/prednisone and placebo in patients with hormone-refractory prostate cancer and pain J Clin Oncol 21 2003 3335 3342 (Pubitemid 46613484)
80. E.J. Small, M.R. Smith, J.J. Seaman, S. Petrone, and M.O. Kowalski Combined analysis of two multicenter, randomized, placebo-controlled studies of pamidronate disodium for the palliation of bone pain in men with metastatic prostate cancer J Clin Oncol 21 2003 4277 4284 (Pubitemid 46621802)