Where Are Anti-Angiogenic Agents Positioned Within Cancer Care Guidelines?
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- Olivia Snow
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1 Introduction Additionally, other anti-angiogenic drugs, including sorafenib, sunitinib, axitinib, pazopanib, vandetanib, The development and subsequent use of drugs for treating cancer cabozantinib, and nintedanib have been approved for use in requires thorough vetting through a series of clinical trials designed other forms of cancer. These drugs have not been FDA to understand the activity and effects of the drug within patients. approved for use in lung cancer, ovarian cancer, colorectal Several anti-angiogenic agents have been vetted by this process cancer, or glioma and are not within the scope of this and approved by US Food and Drug Administration (FDA) to treat program. The European Union has approved nintedanib for various cancers within the last 15 years. use in combination with chemotherapy for treating locally The first anti-angiogenic drug was bevacizumab. It has been tested advanced, metastatic or locally recurrent NSCLC of in various clinical trials across multiple cancer indications, including adenocarcinoma tumor histology after first-line treatment. colorectal cancer, lung cancer, ovarian cancer and glioblastoma. The results of these clinical trials have shown promise by improving patient outcomes. Bevacizumab is a humanized murine monoclonal antibody against vascular endothelial growth factor- A (VEGF-A, or VEGF). VEGF is required for the development of new blood vessels. VEGF has been found in many solid cancers. Bevacizumab is approved for use as first-line treatment for metastatic colorectal cancer (mcrc) in combination with chemotherapy, as second line treatment for mcrc that progressed on a first-line bevacizumab-containing treatment, and as first-line treatment of unresectable, locally advanced, recurrent, or metastatic non-squamous non-small cell lung cancer (NSCLC) in combination with chemotherapy. It is also approved for use in combination with chemotherapy for treating recurrent, platinum-resistant ovarian cancer, and as a single agent for use in previously treated, progressive glioblastoma. Additionally, bevacizumab is approved in combination with interferon-alpha for treating metastatic renal cell carcinoma and in combination with chemotherapy for treating persistent, recurrent, or metastatic cervical cancer. More recently approved anti-angiogenic agents include ziv-aflibercept, regorafenib, and ramucirumab. Ziv-aflibercept is approved for use in combination with 5-fluorouracil, leucovorin, and irinotecan (FOLFIRI) to treat patients with mcrc that is resistant to, or has progressed following, treatment with an oxaliplatin-containing regimen. Regorafenib is approved for advanced mcrc that has progressed or recurred after being treated with fluoropyrimidine-, oxaliplatin-, and irinotecan-based chemotherapy, an anti-vegf therapy, and an anti-epidermal growth factor receptor (EGFR) therapy if KRAS is wild type. It is also approved for treating locally advanced, unresectable or metastatic gastrointestinal stromal tumors that have been treated with imatinib mesylate or sunitinib malate. Ramucirumab in combination with docetaxel is approved for treating platinum-resistant metastatic NSCLC. It is approved for use in combination with FOLFIRI for treating patients with mcrc whose disease has progressed on a first-line regimen containing bevacizumab, oxaliplatin, and fluoropyrimidine. Ramucirumab is also indicated for use as a single agent or in combination with paclitaxel for treatment of patients with advanced or metastatic gastric or gastroesophageal junction adenocarcinoma whose disease has progressed while on or after fluoropyrimidine- or platinum-containing chemotherapy. A Brief History of Anti-Angiogenic Agents Entering the Standard of Care In the early 1970s, Dr. Judah Folkman first proposed the concept that blocking the growth of new blood vessels (angiogenesis) associated with tumor growth may be a therapeutic approach for treating solid tumors.1,2 After studies showed that tumor cells released a tumor angiogenesis factor that stimulated endothelial cell proliferation, Folkman hypothesized that using an antibody against tumor angiogenesis factor would be a potential cancer therapy.2 Subsequent research went on to identify numerous endogenous pro-angiogenic factors, including placental growth factor, basic fibroblast growth factor, and vascular endothelial growth factor (VEGF) family; and endogenous angiogenesis inhibitors, including endostatin, angiostatin, and thorombospondin. Due to its role in neovascularization, VEGF emerged as a potential target for cancer treatments. Using immunohistochemistry, the expression of VEGF and its receptors was found in many cancers, and correlations between VEGF expression and prognosis have been reported for several cancers, including colorectal and lung.3 A monoclonal antibody specific for VEGF was developed and early experiments showed that the antibody inhibited tumor growth by targeting tumor angiogenesis, not by inhibiting the tumor cell growth directly.4 Bevacizumab Bevacizumab is a humanized murine monoclonal antibody that targets VEGF. In 1997, patients with sarcoma, renal cell carcinoma, breast cancer, or lung cancer were enrolled in a phase 1 trial, which established the linear pharmacokinetic profile of bevacizumab and its half-life of 21 days. A phase 1b trial evaluated bevacizumab in combination with standard cytotoxic chemotherapy and resulted in no significant effect on cytotoxic adverse event rates.5 Multiple phase 2 trials subsequently commenced. High or low dose bevacizumab in combination with first-line standard chemotherapy was evaluated in two separate trials in patients with advanced NSCLC or mcrc. In another trial, patients with IL-2 refractory renal cell cancer were treated
2 with single agent high or low dose bevacizumab vs placebo bevacizumab.6-8 By , results from these trials varied but showed promise. Lung cancer patients treated with carboplatin and paclitaxel with the higher dose of 15 mg/kg bevacizumab did not experience any significant increase in toxicity, as compared to patients who received only chemotherapy, and had slightly longer survival (17.7 months versus 14.9 months). However, major bleeding events (hemoptysis or hematemesis) occurred in six patients with centrally located tumors close to major blood vessels who were treated with bevacizumab; four events were fatal, four occurred in patients with squamous histology, and five had cavitation or necrosis at baseline or with bevacizumab treatment.6 Time to disease progression was significantly longer in renal cancer patients who received the higher bevacizumab dose (10 mg/kg) than the lower dose (3 mg/kg).7 In contrast, patients with metastatic colorectal cancer treated with lower dose of bevacizumab (5 mg/kg) had a higher objective response rate than patients treated with either a high dose (10 mg/kg) of bevacizumab or a placebo (40%, 24%, 17% respectively).8 The data from the first phase 3 trial of first-line irinotecan, fluorouracil, and leucovorin (IFL) with or without bevacizumab (5 mg/kg) to treat patients with mcrc was reported in This data showed that the addition of bevacizumab to first-line chemotherapy treatment resulted in significantly longer median survival (20.3 months vs 15.6 months) and progression free survival (PFS) (10.6 months vs 6.2 months) for patients with mcrc.9 In 2004, the FDA approved the use of bevacizumab for first-line treatment of mcrc.10 The results from phase 3 Eastern Cooperative Group s Trial E3200 showed that the addition of bevacizumab to treatment with oxaliplatin, fluorouracil, and leucovorin (FOLFOX4) extended both overall survival (OS) (12.9 months vs 10.8 months) and PFS (7.3 months vs 4.7 months) in mcrc patients with previously treated with irinotecan and a fluoropyrimidine.11 On the basis of these data, the FDA granted a labeling extension in June 2006 for use of bevacizumab with intravenous 5-fluorourcil-based chemotherapy for second-line treatment of mcrc.10 In 2006, the results of the phase 3 E4599 trial of paclitaxel and carboplatin with or without bevacizumab to treat patients with NSCLC were reported. This data also showed a statistically significant increase in median OS, PFS, and response rate for the patients receiving chemotherapy with bevacizumab. Patients with squamous histology, mixed cell tumors with predominant squamous cell histology, or gross hemoptysis were specifically excluded from this trial.12 FDA approval was granted in April 2006 for the use of bevacizumab in the treatment of NSCLC;10 however, bevacizumab should not be administered to patients who had a recent history of hemoptysis of greater than or equal to ½ teaspoon of red blood.13 Data from two studies on the use of bevacizumab as a single agent for the treatment of patients suffering from recurrent glioblastoma multiforme (GBM) were submitted to the FDA for accelerated approval. In 2009, an independent radiologic review granted approval based on the objective response rates from these studies.14 Although a meta-analysis of randomized control trials studying the addition of bevacizumab to standard therapy for patients with GBM demonstrated a statistically significant improvement in PFS, there was no improvement in OS.15 Evaluating bevacizumab in combination with chemotherapy, the AURELIA trial was the first randomized phase 3 trial for platinum-resistant ovarian cancer.16 Median PFS was 6.7 months for patients treated with bevacizumab in combination with chemotherapy, whereas PFS was 3.4 months for patients receiving only chemotherapy; however, no significant effect was found on OS. On the basis of these data, bevacizumab in combination with chemotherapy was approved in the setting of platinum-resistant recurrent ovarian cancer in The subsequent phase 3 OCEANS trial examined the use of chemotherapy with and without bevacizumab in platinum-sensitive recurrent ovarian cancer, and reported significant improvement in median PFS (12.4 months and 8.4 months, respectively) at the time of final PFS analysis.17 However, OS on final analysis with a median follow-up of 58.2 months was not significantly different between treatment groups.18 Two additional phase 3 clinical trials were performed on the use of bevacizumab for the treatment of chemotherapy-naïve patients. GOG-218 enrolled patients with stage III (incompletely resectable) or stage IV ovarian cancer after debulking surgery. The addition of bevacizumab to chemotherapy treatment and its use as maintenance treatment extended median PFS (14.1 months bevacizumab throughout vs 10.3 months chemotherapy alone).19 ICON7 enrolled patients with new diagnosed high-risk early stage or advanced ovarian cancer. Results indicated that front-line bevacizumab plus chemotherapy improved PFS20 but had no effect on OS.21 Additional Anti-Angiogenic Agents Ziv-aflibercept is a recombinant fusion protein that inhibits angiogenesis by acting as a soluble decoy receptor, preventing VEGF pathway activation. Ziv-aflibercept plus FOLFIRI was approved by the FDA in 2012 for the treatment of mcrc patients who were resistant to or who had progressed following an oxaliplatin-containing regimen based on the result of the phase 3 VELOUR clinical trial showed that ziv-aflibercept plus FOLFIRI provided improvements in OS and PFS.22 Regorafenib is a multikinase inhibitor approved by the FDA in 2012 for treatment of previously treated mcrc after a phase 3 CORRECT clinical trial revealed that treatment with single agent regorafenib versus best supportive care for patients with previously treated mcrc resulted in an increased median OS.23 Ramucirumab is a fully human monoclonal antibody that blocks VEGF signaling by targeting the VEGFR2. The phase 3
3 RAISE clinical trial identified a modest improvement in PFS when used in combination with FOLFIRI in patients with metastatic colorectal cancer whose disease progressed after first-line treatment with fluoropyrimidine/oxaliplatin/ bevacizumab.24 Ramucirumab plus FOLFIRI was approved for the treatment of second line mcrc in In 2014, the FDA-approved ramucirumab in combination with docetaxel for the treatment of patients with metastatic NSCLC with disease progression on or after platinum-based chemotherapy. The approval was based upon the phase 3 REVEL study in which the combination of ramucirumab plus docetaxel versus docetaxel alone showed a statistically significant improvement in median OS.25 How are Anti-Angiogenic Agents Typically Used According to Guideline-Based Care? For NSCLC, bevacizumab 15 mg/kg IV in combination with carboplatin/paclitaxel every 3 weeks is approved for first-line treatment for unresectable, locally advanced, recurrent, or metastatic disease.13 For mcrc, the dose of bevacizumab 5 mg/kg IV every 2 weeks in combination with bolus-5-fu/leucovorin/irinotecan (IFL) is approved for use in first-line treatment. A dose of 10 mg/kg IV every 2 weeks is approved for use in combination with FOLFOX4. Bevacizumab 5 mg/kg IV every 2 weeks or 7.5 mg/kg IV every 3 weeks is approved for use in combination with fluoropyrimidine-based chemotherapy for patients who progressed on a first-line bevacizumab-containing regimen.13 For ovarian cancer, bevacizumab 10 mg/kg IV every 2 weeks plus paclitaxel, pegylated lipsosomal doxorubicin, or topotecan (weekly); or 15 mg/kg IV with topotecan every 3 weeks is approved for women with platinum-resistant ovarian cancer and who had received no more than two chemotherapy regimens.13 For platinum-sensitive, recurrent ovarian cancer, the recommended dose is bevacizumab 15 mg/kg every 3 weeks in combination with carboplatin and paclitaxel for 6 to 8 cycles, followed by continued use of single agent bevacizumab 15 mg/kg every 3 weeks until disease progression. Alternatively, 15 mg/kg every 3 weeks plus carboplatin and gemcitabine for 6 to 10 cycles, followed by single agent bevacizumab 15 mg/kg every 3 weeks until disease progression. For adult patients with recurrent glioblastoma, bevacizumab 10 mg/kg IV every 2 weeks is approved for use as a single agent.13 For mcrc that was previously treated with oxaliplatin, 4 mg/kg IV ziv-aflibercept every 2 weeks in combination with FOLFIRI is approved. When ziv-aflibercept is used, patient should receive the ziv-aflibercept IV before they receive chemotherapy. 26 For colorectal cancer, 160 mg regorafenib orally, once daily for the first 21 days of each 28 day cycle is approved for use in patients whose cancer has spread to other parts of the body and have previously received treatment.27 For second-line metastatic NSCLC, the FDA has approved ramucirumab 10m/kg IV on day 1 of a 21-day cycle prior to docetaxel administration. For second line metastatic colon cancer, ramucirumab is approved at 8 mg/kg IV on day 1 of a 14-day cycle prior to FOLFIRI administration.28
4 References 1. Folkman J. Anti-angiogenesis: New Concept for Therapy of Solid Tumors. Ann Surg. 1972;175(3): Folkman J. Tumor Angiogenesis: Therapeutic Implications. N Engl J Med. 1971;285(21): Nishida N, Yano H, Nishida T, Kamura T, Kojiro M. Angiogenesis in Cancer. Vasc Health Risk Manag. 2006;2(3): Kim KJ, Li B, Winer J, et al. Inhibition of vascular endothelial growth factor-induced angiogenesis suppresses tumour growth in vivo. Nature. 1993;362(6423): Midgley R, Kerr D. Bevacizumab-Current Status and Future Directions. Ann Oncol. 2005;16(7): Johnson DH, Fehrenbacher L, Novotny WF, et al. Randomized phase II trial comparing bevacizumab plus carboplatin and paclitaxel with carboplatin and paclitaxel alone in previously untreated locally advanced or metastatic non-small-cell lung cancer. J Clin Oncol. 2004;22(11): Yang JC, Haworth L, Sherry RM, et al. A randomized trial of bevacizumab, an anti-vascular endothelial growth factor antibody, for metastatic renal cancer. N Engl J Med. 2003;349(5): Khasraw M, Ameratunga MS, Grant R, Wheeler H, Pavlakis N. Antiangiogenic therapy for high-grade glioma. Cochrane Database Syst Rev. 2014(9):Cd Pujade-Lauraine E, Hilpert F, Weber B, et al. Bevacizumab combined with chemotherapy for platinum-resistant recurrent ovarian cancer: The AURELIA open-label randomized phase III trial. J Clin Oncol. 2014;32(13): Aghajanian C, Blank SV, Goff BA, et al. OCEANS: a randomized, double-blind, placebo-controlled phase III trial of chemotherapy with or without bevacizumab in patients with platinum-sensitive recurrent epithelial ovarian, primary peritoneal, or fallopian tube cancer. J Clin Oncol. 2012;30(17): Aghajanian C, Goff B, Nycum LR, Wang YV, Husain A, Blank SV. Final overall survival and safety analysis of OCEANS, a phase 3 trial of chemotherapy with or without bevacizumab in patients with platinum-sensitive recurrent ovarian cancer. Gynecologic oncology. 2015;139(1): Burger RA, Brady MF, Bookman MA, et al. Incorporation of bevacizumab in the primary treatment of ovarian cancer. N Engl J Med. 2011;365(26): Perren TJ, Swart AM, Pfisterer J, et al. A phase 3 trial of bevacizumab in ovarian cancer. N Engl J Med. 2011;365(26): Kabbinavar F, Hurwitz HI, Fehrenbacher L, et al. Phase II, randomized trial comparing bevacizumab plus fluorouracil (FU)/leucovorin (LV) with FU/LV alone in patients with metastatic colorectal cancer. J Clin Oncol. 2003;21(1): Oza AM, Cook AD, Pfisterer J, et al. Standard chemotherapy with or without bevacizumab for women with newly diagnosed ovarian cancer (ICON7): overall survival results of a phase 3 randomised trial. Lancet Oncol. 2015;16(8): Hurwitz H, Fehrenbacher L, Novotny W, et al. Bevacizumab plus irinotecan, fluorouracil, and leucovorin for metastatic colorectal cancer. N Engl J Med. 2004;350(23): Van Cutsem E, Tabernero J, Lakomy R, et al. Addition of aflibercept to fluorouracil, leucovorin, and irinotecan improves survival in a phase III randomized trial in patients with metastatic colorectal cancer previously treated with an oxaliplatin-based regimen. J Clin Oncol. 2012;30(28): FDA Approval of Bevacizumab. Accessed January 18, Giantonio BJ, Catalano PJ, Meropol NJ, et al. Bevacizumab in combination with oxaliplatin, fluorouracil, and leucovorin (FOLFOX4) for previously treated metastatic colorectal cancer: results from the Eastern Cooperative Oncology Group Study E3200. J Clin Oncol. 2007;25(12): Sandler A, Gray R, Perry MC, et al. Paclitaxel-carboplatin alone or with bevacizumab for non-small-cell lung cancer. N Engl J Med. 2006;355(24): Avastin Package Insert. In: Genetech I, ed. South San Francisco, CA Cohen MH, Shen YL, Keegan P, Pazdur R. FDA drug approval summary: bevacizumab (Avastin) as treatment of recurrent glioblastoma multiforme. Oncologist. 2009;14(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(9863): Tabernero J, Yoshino T, Cohn AL, et al. Ramucirumab versus placebo in combination with second-line FOLFIRI in patients with metastatic colorectal carcinoma that progressed during or after first-line therapy with bevacizumab, oxaliplatin, and a fluoropyrimidine (RAISE): a randomised, double-blind, multicentre, phase III study. Lancet Oncol. 2015;16(5): Garon EB, Ciuleanu TE, Arrieta O, et al. Ramucirumab plus docetaxel versus placebo plus docetaxel for second-line treatment of stage IV non-small-cell lung cancer after disease progression on platinum-based therapy (REVEL): a multicentre, double-blind, randomised
5 phase 3 trial. Lancet. 2014;384(9944): Zaltrap package insert. In: Sanofi-Aventis U.S. L, ed Stivarga Package Insert. In: Inc. BHP, ed CYRAMZA Package Insert. In: Company ELa, ed 2016.
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