Systemic therapy for non-clear cell renal cell carcinomas: A systematic review and meta-analysis

European Urology

Volumn 67, Issue 4, 2015, Pages 740-749

  Vera Badillo, Francisco E ^a   Templeton, Arnoud J ^a   Duran, Ignacio ^b   Ocana, Alberto ^c   De Gouveia, Paulo ^a   Aneja, Priya ^a   Knox, Jennifer J ^a   Tannock, Ian F ^a   Escudier, Bernard ^d   Amir, Eitan ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b HOSPITAL UNIVERSITARIO VIRGEN DEL ROCÍO   (Spain)

^c HOSPITAL GENERAL UNIVERSITARIO DE ALBACETE   (Spain)

^d INSTITUT GUSTAVE ROUSSY   (France)

Author keywords

Non clear renal cell carcinoma; Systemic therapy

Indexed keywords

ANTINEOPLASTIC AGENT;

CANCER THERAPY; HUMAN; KIDNEY CARCINOMA; META ANALYSIS; NON CLEAR CELL RENAL CELL CARCINOMA; OVERALL SURVIVAL; PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; REVIEW; SYSTEMATIC REVIEW; SYSTEMIC THERAPY; TREATMENT OUTCOME; ADENOCARCINOMA, CLEAR CELL; ADULT; AGED; CARCINOMA, RENAL CELL; CLASSIFICATION; DISEASE COURSE; DISEASE FREE SURVIVAL; FEMALE; MALE; MIDDLE AGED; PATHOLOGY;

ADENOCARCINOMA, CLEAR CELL; ADULT; AGED; ANTINEOPLASTIC AGENTS; CARCINOMA, RENAL CELL; DISEASE PROGRESSION; DISEASE-FREE SURVIVAL; FEMALE; HUMANS; MALE; MIDDLE AGED; TREATMENT OUTCOME;

EID: 84923145728     PISSN: 03022838     EISSN: 18737560     Source Type: Journal    
DOI: 10.1016/j.eururo.2014.05.010     Document Type: Review

References (76)

1. K.T. Mai, H. Faraji, and D. Desantis Renal cell carcinoma with mixed features of papillary and clear cell cytomorphology: a fluorescent in situ hybridization study Virchows Arch 456 2010 77 84
2. J.N. Eble, K. Togashi, and P. Pisani WHO histological classification of tumours of the kidney J.N. Eble, G. Sauter, J.I. Epstein, I.A. Sesterhenn, Pathology and genetics of tumours of the urinary system and male genital organs 2004 IARC Press Lyon, France 9 11
3. Tickoo SK, RVE, Westfall DE, Vankalakunti M. Kidney tumors and tumor-like conditions. In: Amin MB, McKenney JK, Tickoo SK, et al., editors. Diagnostic pathology: genitourinary. Manitoba, Canada: AMIRSYS; 2010. p. 1-2-247.
4. A. Lopez-Beltran, J.C. Carrasco, and L. Cheng 2009 update on the classification of renal epithelial tumors in adults Int J Urol 16 2009 432 443
5. A.R. Golshayan, S. George, and D.Y. Heng Metastatic sarcomatoid renal cell carcinoma treated with vascular endothelial growth factor-targeted therapy J Clin Oncol 27 2009 235 241
6. R.J. Motzer, J. Bacik, and T. Mariani Treatment outcome and survival associated with metastatic renal cell carcinoma of non-clear-cell histology J Clin Oncol 20 2002 2376 2381
7. L.E. Moore, M.L. Nickerson, and P. Brennan Von Hippel-Lindau (VHL) inactivation in sporadic clear cell renal cancer: associations with germline VHL polymorphisms and etiologic risk factors PLoS Genet 7 2011 e1002312
8. B.J. Ljungberg, J. Jacobsen, and S.H. Rudolfsson Different vascular endothelial growth factor (VEGF), VEGF-receptor 1 and -2 mRNA expression profiles between clear cell and papillary renal cell carcinoma BJU Int 98 2006 661 667
9. K. Inoue, T. Karashima, and M. Chikazawa Overexpression of c-met proto-oncogene associated with chromophilic renal cell carcinoma with papillary growth Virchows Arch 433 1998 511 515
10. P. Sweeney, A.K. El-Naggar, S.H. Lin, and L.L. Pisters Biological significance of c-met over expression in papillary renal cell carcinoma J Urol 168 2002 51 55
11. T.R. Hartman, E. Nicolas, and A. Klein-Szanto The role of the Birt-Hogg-Dubé protein in mTOR activation and renal tumorigenesis Oncogene 28 2009 1594 1604
12. J.R. Gnarra, K. Tory, and Y. Weng Mutations of the VHL tumour suppressor gene in renal carcinoma Nat Genet 7 1994 85 90
13. B.I. Rini, S.C. Campbell, and B. Escudier Renal cell carcinoma Lancet 373 2009 1119 1132
14. B. Escudier, A. Pluzanska, and P. Koralewski Bevacizumab plus interferon alfa-2a for treatment of metastatic renal cell carcinoma: a randomised, double-blind phase III trial Lancet 370 2007 2103 2111
15. 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
16. C.N. Sternberg, I.D. Davis, and J. Mardiak Pazopanib in locally advanced or metastatic renal cell carcinoma: results of a randomized phase III trial J Clin Oncol 28 2010 1061 1068
17. G. Hudes, M. Carducci, and P. Tomczak Temsirolimus, interferon alfa, or both for advanced renal-cell carcinoma N Engl J Med 356 2007 2271 2281
18. B. Escudier, T. Eisen, and W.M. Stadler Sorafenib in advanced clear-cell renal-cell carcinoma N Engl J Med 356 2007 125 134
19. B.I. Rini, B. Escudier, and P. Tomczak Comparative effectiveness of axitinib versus sorafenib in advanced renal cell carcinoma (AXIS): a randomised phase 3 trial Lancet 378 2011 1931 1939
20. 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
21. R.J. Motzer, C. Porta, and N.J. Vogelzang Dovitinib versus sorafenib for third-line targeted treatment of patients with metastatic renal cell carcinoma: an open-label, randomised phase 3 trial Lancet Oncol 15 2014 286 296
22. A. Liberati, D.G. Altman, and J. Tetzlaff The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration PLoS Med 6 2009 e1000100
23. Chapter 9: analysing data and undertaking meta-analyses J.J. Deeks, J.P.T. Higgins, D.G. Altman, J.P.T. Higgins, and S. Green Cochrane handbook for systematic reviews of interventions, version 5.1.0 (updated March 2011) 2011 Cochrane Collaboration London, UK
24. J.P. Dutcher, P. de Souza, and D. McDermott Effect of temsirolimus versus interferon-alpha on outcome of patients with advanced renal cell carcinoma of different tumor histologies Med Oncol 26 2009 202 209
25. C.L. Cowey, C. Amin, and R.S. Pruthi Neoadjuvant clinical trial with sorafenib for patients with stage II or higher renal cell carcinoma J Clin Oncol 28 2010 1502 1507
26. B. Rini, J. Garcia, and P. Elson The effect of sunitinib on primary renal cell carcinoma and facilitation of subsequent surgery J Urol 187 2012 1548 1554
27. R. Passalacqua, C. Buzio, and S. Buti Phase III, randomised, multicentre trial of maintenance immunotherapy with low-dose interleukin-2 and interferon-alpha for metastatic renal cell cancer Cancer Immunol Immunother 59 2010 553 561
28. A.M. Molina, S.K. Tickoo, and N. Ishill Sarcomatoid-variant renal cell carcinoma: treatment outcome and survival in advanced disease Am J Clin Oncol 34 2011 454 459
29. C. Kwak, Y.H. Park, and C.W. Jeong Sarcomatoid differentiation as a prognostic factor for immunotherapy in metastatic renal cell carcinoma J Surg Oncol 95 2007 317 323
30. N.B. Haas, X. Lin, and J. Manola A phase II trial of doxorubicin and gemcitabine in renal cell carcinoma with sarcomatoid features: ECOG 8802 Med Oncol 29 2012 761 767
31. B. Escudier, J.P. Droz, and F. Rolland Doxorubicin and ifosfamide in patients with metastatic sarcomatoid renal cell carcinoma: a phase II study of the genitourinary group of the French Federation of Cancer Centers J Urol 168 2002 959 961
32. M. Staehler, N. Haseke, and A. Roosen Sorafenib after combination therapy with gemcitabine plus doxorubicine in patients with sarcomatoid renal cell carcinoma: a prospective evaluation Eur J Med Res 15 2010 287 291
33. R.J. Motzer, Barrios, C.H. Carlos, and T.M. Kim Record-3: Phase II randomized trial comparing sequential first-line everolimus (EVE) and second-line sunitinib (SUN) versus first-line SUN and second-line EVE in patients with metastatic renal cell carcinoma (mRCC) [abstract 4504] J Clin Oncol 31 Suppl 2013
34. L. Schmidt, F.M. Duh, and F. Chen Germline and somatic mutations in the tyrosine kinase domain of the MET proto-oncogene in papillary renal carcinomas Nat Genet 16 1997 68 73
35. R. Srinivasan, D.P. Bottaro, and T.K. Choueiri Correlation of germline MET mutation with response to the dual Met/VEGFR-2 inhibitor foretinib in patients with sporadic and hereditary papillary renal cell carcinoma: results from a multicenter phase II study (MET111644) [abstract 372] J Clin Oncol 30 Suppl 5 2012
36. T.K. Choueiri, U.N. Vaishampayan, and J.E. Rosenberg A phase II and biomarker study (MET111644) of the dual Met/VEGFR-2 inhibitor foretinib in patients with sporadic and hereditary papillary renal cell carcinoma: final efficacy, safety, and PD results [abstract 355] J Clin Oncol 30 Suppl 5 2012
37. S. Negrier, D. Perol, and A. Ravaud Medroxyprogesterone, interferon alfa-2a, interleukin 2, or combination of both cytokines in patients with metastatic renal carcinoma of intermediate prognosis: results of a randomized controlled trial Cancer 110 2007 2468 2477
38. D.C. Cho, J.A. Sosman, and M. Sznol Clinical activity, safety, and biomarkers of MPDL3280A, an engineered PD-L1 antibody in patients with metastatic renal cell carcinoma (mRCC) [abstract 4504] J Clin Oncol 31 Suppl 2013
39. M.E. Gore, C. Szczylik, and C. Porta Safety and efficacy of sunitinib for metastatic renal-cell carcinoma: an expanded-access trial Lancet Oncol 10 2009 757 763
40. H.S. Kim, M.H. Hong, and K. Kim Sunitinib for Asian patients with advanced renal cell carcinoma: a comparable efficacy with different toxicity profiles Oncology 80 2011 395 405
41. W.M. Stadler, R. Figlin, and D. McDermott Safety and efficacy results of the advanced renal cell carcinoma sorafenib expanded access program in North America Cancer 116 2010 1272 1280
42. E. Chung, E. Posadas, and K. Kasza A phase II trial of gemcitabine, capecitabine, and bevacizumab in metastatic renal carcinoma Am J Clin Oncol 34 2011 150 154
43. G. Di Lorenzo, G. Carteni, and R. Autorino Phase II study of sorafenib in patients with sunitinib-refractory metastatic renal cell cancer J Clin Oncol 27 2009 4469 4474
44. J. Gollob, W.K. Rathmell, and T. Richmond Phase II trial of sorafenib plus interferon alfa-2b as first- or second-line therapy in patients with metastatic renal cell cancer J Clin Oncol 25 2007 3288 3295
45. R.J. Motzer, M. Michaelson, and B. Redman 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 24 2006 16 24
46. G. Procopio, E. Verzoni, and S. Bracarda Sorafenib with interleukin-2 vs sorafenib alone in metastatic renal cell carcinoma: the ROSORC trial Brit J Cancer 104 2011 1256 1261
47. I. Yildiz, F. Sen, and M. Basaran Response rates and adverse effects of continuous once-daily sunitinib in patients with advanced renal cell carcinoma: a single-center study in Turkey Jpn J Clin Oncol 41 2011 1380 1387
48. J. Busch, C. Seidel, and C. Kempkensteffen Sequence therapy in patients with metastatic renal cell carcinoma: comparison of common targeted treatment options following failure of receptor tyrosine kinase inhibitors Eur Urol 60 2011 1163 1170
49. G. Di Lorenzo, C. Buonerba, and P. Federico Third-line sorafenib after sequential therapy with sunitinib and mTOR inhibitors in metastatic renal cell carcinoma Eur Urol 58 2010 906 911
50. C. Yoo, J.E. Kim, and J.-L. Lee The efficacy and safety of sunitinib in Korean patients with advanced renal cell carcinoma: high incidence of toxicity leads to frequent dose reduction Jpn J Clin Oncol 40 2010 980 985
51. Y. Koh, H.Y. Lim, and J.H. Ahn Phase II trial of everolimus for the treatment of nonclear-cell renal cell carcinoma Ann Oncol 24 2013 1026 1031
52. J.L. Lee, J.H. Ahn, and H.Y. Lim Multicenter phase II study of sunitinib in patients with non-clear cell renal cell carcinoma Ann Oncol 23 2012 2108 2114
53. A.M. Molina, D.R. Feldman, and M.S. Ginsberg Phase II trial of sunitinib in patients with metastatic non-clear cell renal cell carcinoma Invest New Drugs 30 2012 335 340
54. N.M. Tannir, E. Plimack, and C. Ng A phase 2 trial of sunitinib in patients with advanced non-clear cell renal cell carcinoma Eur Urol 62 2012 1013 1019
55. T.K. Choueiri, A. Plantade, and P. Elson Efficacy of sunitinib and sorafenib in metastatic papillary and chromophobe renal cell carcinoma J Clin Oncol 26 2008 127 131
56. M. Krzyzanowska, I. Tannock, and G. Lockwood A phase II trial of continuous low-dose oral cyclophosphamide and celecoxib in patients with renal cell carcinoma Cancer Chemother Pharmacol 60 2007 135 141
57. S. Marur, J. Eliason, and L. Heilbrun Phase II trial of capecitabine and weekly docetaxel in metastatic renal cell carcinoma Urology 72 2008 898 902
58. S. Naito, M. Eto, and N. Shinohara Multicenter phase II trial of S-1 in patients with cytokine-refractory metastatic renal cell carcinoma J Clin Oncol 28 2010 5022 5029
59. S. Naito, T. Tsukamoto, and M. Usami An early phase II trial of S-1 in Japanese patients with cytokine-refractory metastatic renal cell carcinoma Cancer Chemother Pharmacol 66 2010 1065 1070
60. L. Pagliaro, C. Perez, S. Tu, and D.D. Daliani Phase II study of capecitabine single-agent therapy in patients with metastatic renal cell carcinoma Urol Oncol 24 2006 487 491
61. W.M. Stadler, S. Halabi, and B. Rini A phase II study of gemcitabine and capecitabine in metastatic renal cancer: a report of Cancer and Leukemia Group B Protocol 90008 Cancer 107 2006 1273 1279
62. P.J. Van Veldhuizen, M. Hussey, and P.N. Lara Jr. A phase II study of gemcitabine and capecitabine in patients with advanced renal cell cancer: Southwest Oncology Group Study S0312 Am J Clin Oncol 32 2009 453 459
63. J. Waters, C. Moss, and L. Pyle Phase II clinical trial of capecitabine and gemcitabine chemotherapy in patients with metastatic renal carcinoma Br J Cancer 91 2004 1763 1768
64. F. Zustovich, G. Cartei, and D. Pastorelli A phase II study of gemcitabine at fixed infusion rate of 10 mg/m2/min with or without immunotherapy in advanced renal cancer Anticancer Res 27 2007 4461 4464
65. S. Buti, M. Brighenti, and C. Bongiovanni Role of chemotherapy with gemcitabine plus 5-fluorouracil and chemoimmunotherapy in metastatic renal cell cancer (mRCC) J Immunother 30 2007 780 786
66. K. Bylow, M. Atkins, and E. Posadas Phase II trial of carboplatin and paclitaxel in papillary renal cell carcinoma Clin Genitourin Cancer 7 2009 39 42
67. S. Oudard, E. Banu, and A. Vieillefond Prospective multicenter phase II study of gemcitabine plus platinum salt for metastatic collecting duct carcinoma: results of a GETUG (Groupe d'Etudes des Tumeurs Uro-Génitales) study J Urol 177 2007 1698 1702
68. S.L. Richey, P. Tamboli, and C.S. Ng Phase II trial of pemetrexed plus gemcitabine in patients with locally advanced and metastatic nonclear cell renal cell carcinoma Am J Clin Oncol 36 2013 450 454
69. I. Tsimafeyeu, L. Demidov, and G. Kharkevich Phase II, multicenter, uncontrolled trial of single-agent capecitabine in patients with non-clear cell metastatic renal cell carcinoma Am J Clin Oncol 35 2012 251 254
70. A.S. Artz, K. Van Besien, and T. Zimmerman Long-term follow-up of nonmyeloablative allogeneic stem cell transplantation for renal cell carcinoma: the University of Chicago experience Bone Marrow Transplant 35 2005 253 260
71. M. Bregni, A. Dodero, and J. Peccatori Nonmyeloablative conditioning followed by hematopoietic cell allografting and donor lymphocyte infusions for patients with metastatic renal and breast cancer Blood 99 2002 4234 4236
72. R. Childs, A. Chernoff, and N. Contentin Regression of metastatic renal-cell carcinoma after nonmyeloablative allogeneic peripheral-blood stem-cell transplantation N Engl J Med 343 2000 750 758
73. B. Rini, T. Zimmerman, and W.M. Stadler Allogeneic stem-cell transplantation of renal cell cancer after nonmyeloablative chemotherapy: feasibility, engraftment, and clinical results J Clin Oncol 20 2002 2017 2024
74. H. Akaza, T. Tsukamoto, and T. Onishi A low-dose combination therapy of interleukin-2 and interferon-alpha is effective for lung metastasis of renal cell carcinoma: a multicenter open study Int J Clin Oncol 11 2006 434 440
75. H. Akaza, T. Tsukamoto, and T. Fujioka Combined immunotherapy with low-dose IL-2 plus IFN-alpha for metastatic renal cell carcinoma: survival benefit for selected patients with lung metastasis and serum sodium level Jpn J Clin Oncol 41 2011 1023 1030
76. H. Miyake, I. Hara, and I. Sakai Clinical outcome of combined immunotherapy with low-dose interleukin-2 and interferon-alpha for Japanese patients with metastatic renal cell carcinoma who had undergone radical nephrectomy: a preliminary report Int J Clin Oncol 10 2005 338 341