Incidence and risk of hemorrhagic events with vascular endothelial growth factor receptor tyrosine-kinase inhibitors: An up-to-date meta-analysis of 27 randomized controlled trials

Annals of Oncology

Volumn 24, Issue 12, 2013, Pages 2943-2952

  Qi, W X ^a   Tang, L N ^a   Sun, Y J ^a   He, A N ^a   Lin, F ^a   Shen, Z ^a   Yao, Y ^a  

^a SHANGHAI JIAO TONG UNIVERSITY   (China)

Author keywords

Cancer; Hemorrhagic events; Meta analysis; VEGFR TKIs

Indexed keywords

ALPHA INTERFERON; AXITINIB; CAPECITABINE; CARBOPLATIN; DACARBAZINE; DOCETAXEL; DOXORUBICIN; ERLOTINIB; GEFITINIB; GEMCITABINE; PACLITAXEL; PAZOPANIB; PEMETREXED; PLACEBO; REGORAFENIB; SORAFENIB; SUNITINIB; VANDETANIB;

BLEEDING; BRAIN HEMORRHAGE; BREAST CANCER; BREAST METASTASIS; CANCER PATIENT; CONFIDENCE INTERVAL; DISEASE ASSOCIATION; DISEASE CLASSIFICATION; EPISTAXIS; GASTROINTESTINAL HEMORRHAGE; GASTROINTESTINAL STROMAL TUMOR; HEMOPTYSIS; HUMAN; INCIDENCE; KIDNEY CARCINOMA; LIVER CELL CARCINOMA; LUNG HEMORRHAGE; LUNG NON SMALL CELL CANCER; LUNG SMALL CELL CANCER; MELANOMA; META ANALYSIS; METASTATIC COLORECTAL CANCER; PANCREAS CANCER; PANCREATIC NEUROENDOCRINE TUMOR; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; RISK FACTOR; SUBDURAL HEMATOMA; SYSTEMATIC REVIEW; THYROID CANCER; UPPER GASTROINTESTINAL BLEEDING;

CANCER; HEMORRHAGIC EVENTS; META-ANALYSIS; VEGFR-TKIS;

ANTINEOPLASTIC AGENTS; HEMORRHAGE; HUMANS; INCIDENCE; NEOPLASMS; PROTEIN KINASE INHIBITORS; RANDOMIZED CONTROLLED TRIALS AS TOPIC; RECEPTORS, VASCULAR ENDOTHELIAL GROWTH FACTOR; RISK FACTORS;

EID: 84888793629     PISSN: 09237534     EISSN: 15698041     Source Type: Journal    
DOI: 10.1093/annonc/mdt292     Document Type: Review

References (51)

1. Yap TA, Carden CP, Kaye SB. Beyond chemotherapy: targeted therapies in ovarian cancer. Nat Rev Cancer 2009; 9: 167-181.
2. Folkman J. Role of angiogenesis in tumor growth and metastasis. Semin Oncol, Edition Elsevier 2002; 29: 15-18.
3. Zetter PBR. Angiogenesis and tumor metastasis. Annu Rev Med 1998; 49:407-424.
4. Llovet JM, Ricci S, Mazzaferro V et al. Sorafenib in advanced hepatocellular carcinoma. N Engl J Med 2008; 359: 378-390.
5. van der Graaf WT, Blay JY, Chawla SP et al. Pazopanib for metastatic soft-tissue sarcoma (PALETTE): a randomised, double-blind, placebo-controlled phase 3 trial. Lancet 2012; 379: 1879-1886.
6. Sternberg CN, Davis ID, Mardiak J et al. Pazopanib in locally advanced or metastatic renal cell carcinoma: results of a randomized phase III trial. J Clin Oncol 2010; 28: 1061-1068.
7. Raymond E, Dahan L, Raoul JL et al. Sunitinib malate for the treatment of pancreatic neuroendocrine tumors. N Engl J Med 2011; 364: 501-513.
8. Goodman VL, Rock EP, Dagher R et al. Approval summary: sunitinib for the treatment of imatinib refractory or intolerant gastrointestinal stromal tumors and advanced renal cell carcinoma. Clin Cancer Res 2007; 13: 1367-1373.
9. Nosov DA, Esteves B, Lipatov ON et al. Antitumor activity and safety of tivozanib (AV-951) in a phase II randomized discontinuation trial in patients with renal cell carcinoma. J Clin Oncol 2012; 30: 1678-1685.
10. Kurzrock R, Sherman SI, Ball DW et al. Activity of XL184 (Cabozantinib), an oral tyrosine kinase inhibitor, in patients with medullary thyroid cancer. J Clin Oncol 2011; 29: 2660-2666.
11. Grothey A, Van Cutsem E, Sobrero A et al. Regorafenib monotherapy for previously treated metastatic colorectal cancer (CORRECT): an international, multicentre, randomised, placebo-controlled, phase 3 trial. Lancet 2013; 381: 303-312.
12. Demetri GD, Reichardt P, Kang YK et al. Efficacy and safety of regorafenib for advanced gastrointestinal stromal tumours after failure of imatinib and sunitinib (GRID): an international, multicentre, randomised, placebo-controlled, phase 3 trial. Lancet 2013; 381: 295-302.
13. Duffy A, Wilkerson J, Greten TF. Hemorrhagic events in hepatocellular carcinoma patients treated with anti-angiogenic therapies. Hepatology 2012; 57:1068-1077.
14. Elice F, Rodeghiero F. Side effects of anti-angiogenic drugs. Thromb Res 2012; 129: S50-S53.
15. Hang XF, Xu WS, Wang JX et al. Risk of high-grade bleeding in patients with cancer treated with bevacizumab: a meta-analysis of randomized controlled trials. Eur J Clin Pharmacol 2011; 67: 613-623.
16. Hapani S, Sher A, Chu D et al Increased risk of serious hemorrhage with bevacizumab in cancer patients: a meta-analysis. Oncology 2010; 79: 27-38.
17. Je Y, Schutz FA, Choueiri TK. Risk of bleeding with vascular endothelial growth factor receptor tyrosine-kinase inhibitors sunitinib and sorafenib: a systematic review and meta-analysis of clinical trials. Lancet Oncol 2009; 10: 967-974.
18. Kumar R, Knick VB, Rudolph SK et al. Pharmacokinetic-pharmacodynamic correlation from mouse to human with pazopanib, a multikinase angiogenesis inhibitor with potent antitumor and antiangiogenic activity. Mol Cancer Ther 2007; 6: 2012-2021.
19. Qi WX, Tang LN, He AN et al. The role of vandetanib in the second-line treatment for advanced non-small-cell-lung cancer: a meta-analysis of four randomized controlled trials. Lung 2011; 189: 437-443.
20. Leboulleux S, Bastholt L, Krause T et al. Vandetanib in locally advanced or metastatic differentiated thyroid cancer: a randomised, double-blind, phase 2 trial. Lancet Oncol 2012; 13: 897-905.
21. de Boer RH, Arrieta O, Yang CH et al. Vandetanib plus pemetrexed for the secondline treatment of advanced non-small-cell lung cancer: a randomized, double-blind phase III trial. J Clin Oncol 2011; 29: 1067-1074.
22. Wells SA, Jr, Robinson BG, Gagel RF et al. Vandetanib in patients with locally advanced or metastatic medullary thyroid cancer: a randomized, double-blind phase III trial. J Clin Oncol 2012; 30: 134-141.
23. Moher D, Pham B, Jones A et al. Does quality of reports of randomised trials affect estimates of intervention efficacy reported in meta-analyses?. Lancet 1998; 352:609-613.
24. NCI, Cancer Therapy Evaluation Program. CTC v 2.0 and common terminology criteria for adverse events criteria V3.0 (CTCAE). Available at: http://ctep.cancer. gov/protocolDevelopment/electronic_applications/ctc.htm (Jan 27 2013, date last accessed).
25. Robins J, Greenland S, Breslow NE. A general estimator for the variance of the Mantel-Haenszel odds ratio. Am J Epidemiol 1986; 124: 719-723.
26. Zintzaras E, Ioannidis JP. Heterogeneity testing in meta-analysis of genome searches. Genet Epidemiol 2005; 28: 123-137.
27. Moher D, Liberati A, TetzlaffJ et al. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med 2009; 6:e1000097.
28. Scagliotti GV, Krzakowski M, Szczesna A et al. Sunitinib plus erlotinib versus placebo plus erlotinib in patients with previously treated advanced non-small-cell lung cancer: a phase III trial. J Clin Oncol 2012; 30: 2070-2078.
29. Natale RB, Thongprasert S, Greco FA et al. Phase III trial of vandetanib compared with erlotinib in patients with previously treated advanced non-small-cell lung cancer. J Clin Oncol 2011; 29: 1059-1066.
30. Herbst RS, Sun Y, Eberhardt WE et al. Vandetanib plus docetaxel versus docetaxel as second-line treatment for patients with advanced non-small-cell lung cancer (ZODIAC):a double-blind, randomised, phase 3 trial. Lancet Oncol 2010; 11: 619-626.
31. Natale RB, Bodkin D, Govindan R et al. Vandetanib versus gefitinib in patients with advanced non-small-cell lung cancer: results from a two-part, double-blind, randomized phase ii study. J Clin Oncol 2009; 27: 2523-2529.
32. Heymach JV, Johnson BE, Prager D et al. Randomized, placebo-controlled phase II study of vandetanib plus docetaxel in previously treated non small-cell lung cancer. J Clin Oncol 2007; 25: 4270-4277.
33. Heymach JV, Paz-Ares L, De Braud F et al. Randomized phase II study of vandetanib alone or with paclitaxel and carboplatin as first-line treatment for advanced non-small-cell lung cancer. J Clin Oncol 2008; 26: 5407-5415.
34. Bergh J, Bondarenko IM, Lichinitser MR et al. First-line treatment of advanced breast cancer with sunitinib in combination with docetaxel versus docetaxel alone:results of a prospective, randomized phase III study. J Clin Oncol 2012; 30:921-929.
35. Wildiers H, Fontaine C, Vuylsteke P et al. Multicenter phase II randomized trial evaluating antiangiogenic therapy with sunitinib as consolidation after objective response to taxane chemotherapy in women with HER2-negative metastatic breast cancer. Breast Cancer Res Treat 2010; 123: 463-469.
36. Barrios CH, Liu MC, Lee SC et al. Phase III randomized trial of sunitinib versus capecitabine in patients with previously treated HER2-negative advanced breast cancer. Breast Cancer Res Treat 2010; 121: 121-131.
37. Rugo HS, Stopeck AT, Joy AA et al. Randomized, placebo-controlled, double-blind, phase II study of axitinib plus docetaxel versus docetaxel plus placebo in patients with metastatic breast cancer. J Clin Oncol 2011; 29: 2459-2465.
38. Motzer RJ, Hutson TE, Tomczak P et al. Sunitinib versus interferon alfa in metastatic renal-cell carcinoma. N Engl J Med 2007; 356: 115-124.
39. Escudier B, Eisen T, Stadler WM et al. Sorafenib in advanced clear-cell renal-cell carcinoma. N Engl J Med 2007; 356: 125-134.
40. Hsu C, Yang TS, Huo TI et al. Vandetanib in patients with inoperable hepatocellular carcinoma: a phase II, randomized, double-blind, placebo-controlled study. J Hepatol 2012; 56: 1097-1103.
41. Abou-Alfa GK, Johnson P, Knox JJ et al. Doxorubicin plus sorafenib versus doxorubicin alone in patients with advanced hepatocellular carcinoma: a randomized trial. JAMA 2010; 304: 2154-2160.
42. Cheng AL, Kang YK, Chen Z et al. Efficacy and safety of sorafenib in patients in the Asia-Pacific region with advanced hepatocellular carcinoma: a phase III randomised, double-blind, placebo-controlled trial. Lancet Oncol 2009; 10: 25-34.
43. Hauschild A, Agarwala SS, Trefzer U et al. Results of a phase III, randomized, placebo-controlled study of sorafenib in combination with carboplatin and paclitaxel as second-line treatment in patients with unresectable stage III or stage IV melanoma. J Clin Oncol 2009; 27: 2823-2830.
44. McDermott DF, Sosman JA, Gonzalez R et al. Double-blind randomized phase II study of the combination of sorafenib and dacarbazine in patients with advanced melanoma: a report from the 11715 study group. J Clin Oncol 2008; 26:2178-2185.
45. Kindler HL, Ioka T, Richel DJ et al. Axitinib plus gemcitabine versus placebo plus gemcitabine in patients with advanced pancreatic adenocarcinoma: a double-blind randomised phase 3 study. Lancet Oncol 2011; 12: 256-262.
46. Spano JP, Chodkiewicz C, Maurel J et al. Efficacy of gemcitabine plus axitinib compared with gemcitabine alone in patients with advanced pancreatic cancer: an open-label randomised phase II study. Lancet 2008; 371: 2101-2108.
47. Demetri GD, van Oosterom AT, Garrett CR et al. Efficacy and safety of sunitinib in patients with advanced gastrointestinal stromal tumour after failure of imatinib: a randomised controlled trial. Lancet 2006; 368: 1329-1338.
48. Arnold AM, Seymour L, Smylie M et al. Phase II study of vandetanib or placebo in small-cell lung cancer patients after complete or partial response to induction chemotherapy with or without radiation therapy: National Cancer Institute of Canada Clinical Trials Group Study BR.20. J Clin Oncol 2007; 25: 4278-4284.
49. Sherwood LM, Parris EE, Folkman J. Tumor angiogenesis: therapeutic implications. New England Journal of Medicine 1971; 285: 1182-1186.
50. Folkman J. Angiogenesis in cancer, vascular, rheumatoid and other disease. Nature medicine 1995; 1: 27-30.
51. Bennett CL, Silver SM, Djulbegovic B et al. Venous thromboembolism and mortality associated with recombinant erythropoietin and darbepoetin administration for the treatment of cancer-associated anemia. JAMA 2008; 299: 914-924.