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Gastrointest Cancer Res. 2012 Sep-Oct; 5(5): 155–160.
PMCID: PMC3481147

A Phase 2 Trial of Ixabepilone Plus Cetuximab in First-Line Treatment of Metastatic Pancreatic Cancer



The aim of this phase 2 study was to evaluate the safety and efficacy of ixabepilone plus cetuximab in patients with advanced pancreatic cancer.


Eligible patients had advanced pancreatic adenocarcinoma that was metastatic or not amenable to resection, a Karnofsky performance status ≥70%, and no prior therapy for advanced disease. Patients received ixabepilone 32 mg/m2 (3-hour IV infusion) every 3 weeks and cetuximab 250 mg/m2 (1-hour IV infusion) weekly. The primary efficacy end point was the 6-month survival rate. Secondary end points included tumor response rate, overall survival, progression-free survival, and tolerability.


A total of 54 patients were enrolled on this study. The 6-month survival rate was 57% (31/54: 95% CI: 43–71%) with a median overall survival of 7.6 months (95% CI: 5.5–12.2 months). Patients who developed acneiform rash (n = 36) had a median survival of 8.8 months, compared with 2.6 months for those without rash (n = 18). Of 31 patients with measurable disease (defined as response-evaluable), 4 had confirmed partial responses and an additional 24 had stable disease. The combination was generally well-tolerated with the most common grade 3/4 hematological toxicities being leucopenia (39%) and neutropenia (33%). The most common grade 3/4 nonhematologic toxicity was fatigue (17%).


The combination of ixabepilone and cetuximab was active and had acceptable toxicity. The efficacy results are similar to single-agent ixabepilone and gemcitabine-based combination therapies in patients with advanced pancreatic cancer. Exploratory analyses suggest a trend toward improved survival for patients who experienced rash.

Pancreatic cancer is the 10th most common malignancy in the United States and the fourth leading cause of cancer death among both men and women. In 2010, an estimated 43,140 new cases of pancreatic cancer will be diagnosed, and an estimated 36,800 deaths will result from the disease.1 The median survival for patients with metastatic pancreatic cancer is 3 to 6 months; therefore, the major goal of treating patients with advanced pancreatic cancer is the palliation of symptoms.2 Currently, gemcitabine-based therapy is considered a standard for the first-line treatment of advanced and metastatic pancreatic cancer. Single-agent gemcitabine was FDA approved based on its superiority to bolus 5-fluorouracil in clinical benefit response.3 In addition, median overall survival (OS) of 5.7 vs. 4.4 months favored gemcitabine.

No clear improvement in survival has been demonstrated in randomized phase 3 trials with gemcitabine combinations, despite higher response rates with combination therapy.47 In 1 study, a marginal improvement in OS was seen when erlotinib was added to gemcitabine.4 Because the outcome in advanced pancreatic cancer remains poor, there is an unmet need for more effective systemic approaches. More recently, a combination of 5-fluorouracil, leucovorin, oxaliplatin, and irinotecan (FOLFIRINOX) was shown to be superior to gemcitabine alone (median OS 10.5 compared to 6.9 months) in patients with metastatic pancreatic cancer with favorable performance status and normal organ function.8

Ixabepilone (IXEMPRA) is a semisynthetic epothilone B analog with clinical activity in multiple solid tumors.9 Although ixabepilone is a microtubule-stabilizing drug, its binding to β-tubulin differs from that of taxanes, which may explain why ixabepilone is less susceptible to common mechanisms of taxane resistance, such as overexpression of βIII-tubulin.10 Preclinical data demonstrated that single-agent ixabepilone had antitumor activity against a broad range of human tumor xenograft models, including the pancreatic tumors,11 supporting its clinical development. In a phase 2 Southwest Oncology Group study in patients with advanced pancreatic cancer, first-line treatment with ixabepilone resulted in an estimated 6-month survival rate of 60% and median OS of 7.2 months. Confirmed partial responses were achieved by 5 (8.9%) of 56 evaluable patients, and unconfirmed responses in an additional 7 (12.5%) patients. Ixabepilone was generally well tolerated, with neutropenia and nausea/vomiting as the most frequent toxicities.12 These encouraging results indicated that further evaluation of ixabepilone for advanced pancreatic cancer as an alternative to gemcitabine was warranted.

Cetuximab is a monoclonal antibody directed against the epidermal growth factor receptor (EGFR), with activity against a range of solid tumors. In preclinical studies, cetuximab inhibited the survival of BxPC-3 human pancreatic cancer cells in vitro and tumor xenografts in vivo.13 Despite evidence of promising preclinical and phase 2 clinical activity,14 the addition of cetuximab to gemcitabine in a more recent phase 3 trial of patients with advanced pancreatic cancer failed to provide a clinically significant advantage with respect to OS, progression-free survival (PFS), or response compared with gemcitabine alone.15 These data were unavailable at the time of trial design for this study.

Preclinical and clinical activity of ixabepilone as a single agent in pancreatic cancer is encouraging.1112 However, ixabepilone demonstrates therapeutic synergy with various targeted therapies, suggesting that its greatest antineoplastic activity is achieved in combination.16 Synergistic antitumor activity of ixabepilone and cetuximab has been demonstrated in GEO human colon and L2987 human lung carcinoma xenografts,17 providing a biologic rationale for this combination in the treatment of cancer. Based on this evidence, the present study was designed to evaluate the safety and efficacy of ixabepilone plus cetuximab in patients with advanced pancreatic cancer. Studies in patients with pancreatic adenocarcinoma have shown a 6-month survival rate of approximately 50% or better for drugs or combinations considered to be active.4,12,14 Therefore, the primary objective was to determine the effect of the combination on the 6-month survival rate, with additional efficacy parameters and safety evaluated as secondary objectives.


Study Design

This open-label, multicenter, single-arm, phase 2 study, was designed to assess the safety and efficacy of ixabepilone plus cetuximab in patients with locally advanced pancreatic adenocarcinoma that was not surgically resectable or in patients with distant metastatic disease. The study was conducted in accordance with ethical principles originating in the Declaration of Helsinki and in compliance with Good Clinical Practice and all local regulatory requirements. The study was approved by the Institutional Review Board/Independent Ethics Committee at each site before that site enrolled any patients. All patients provided written informed consent.

Ixabepilone was administered at a dose of 32 mg/m2 via 3-hour IV infusion on day 1 of a 3-week cycle, with cetuximab at an initial loading dose of 400 mg/m2 via 2-hour IV infusion and then weekly at 250 mg/m2 via 1-hour infusion. On days when both drugs were to be administered, ixabepilone was administered before cetuximab. All patients were premedicated before each dose of ixabepilone with an oral H1 antihistamine (diphenhydramine 50 mg or equivalent) and H2 antihistamine (ranitidine 150–300 mg or equivalent) to prevent hypersensitivity reactions. Patients continued to receive treatment with ixabepilone plus cetuximab until disease progression or unacceptable toxicity.

The primary objective was rate of survival at 6 months. Secondary end points were objective tumor response rate (ORR), as defined by Response Evaluation Criteria in Solid Tumors (RECIST) guidelines, PFS, OS, duration of response, time to response, and the safety and tolerability of ixabepilone plus cetuximab in all patients that received at least 1 dose of study drug(s).


Men and women aged ≥18 years were eligible for inclusion if they had histologic or cytologic confirmation of pancreatic adenocarcinoma that was locally advanced (unresectable) or metastatic. Patients were required to have measurable disease according to RECIST and had not previously received chemotherapy, immunotherapy, or radiation therapy for advanced pancreatic cancer. Prior adjuvant therapy was allowed if completed ≥6 months earlier. Additional eligibility criteria included adequate recovery from recent surgery (≥1 week after minor surgery or ≥4 weeks after major surgery), Karnofsky performance status of 70% to 100%, and adequate hematologic and hepatic function, including serum creatinine <2 mg/dL. Women of childbearing potential were eligible if they used an adequate method of contraception and were not pregnant or breastfeeding. Patients with serious, uncontrolled medical conditions or who planned to receive any other type of concurrent anticancer treatment were excluded. Patients were also excluded if they had grade 2 or higher peripheral neuropathy, brain and/or leptomeningeal metastases, psychiatric disorders or conditions rendering the patient incapable of protocol compliance; a second malignancy (excluding nonmelanoma skin cancer or carcinoma in situ of the cervix) or known human immunodeficiency viral infection. Prior treatment with an epothilone or epothilone analog, cetuximab, or any other therapy targeting the EGF pathway or the concomitant use of strong CYP3A4 inhibitors was not permitted.

Criteria for Continued Treatment

Treatment with ixabepilone was repeated every 21 days, provided the absolute neutrophil count was ≥1,500 cells/mm3, platelets ≥100,000 cells/mm3, and all treatment-related nonhematologic toxicity attributable to ixabepilone had resolved to lower than grade 2 (except for alopecia or grade 2 fatigue for which resolution was not required and diarrhea for which grade 2 was allowed). Treatment with cetuximab was repeated each week if acne-form rash and diarrhea were grade 2 or lower, and all grade 3 to 4 nonhematologic toxicities attributable to cetuximab had resolved to less than grade 2 (except for anorexia, alopecia, neuropathy, and grade 2 fatigue, for which resolution was not required). If retreatment criteria were not met, treatment with ixabepilone or cetuximab was delayed up to a maximum of 4 weeks. Patients who could not meet retreatment criteria for 1 drug discontinued that drug but were allowed to continue treatment with the other. Upon retreatment, doses of ixabepilone and cetuximab were modified based on tolerability, with a maximum of 2 dose reductions allowed per study drug. Once a dose had been reduced, re-escalation was not permitted.

Patients who had hypersensitivity reactions despite premedication with oral antihistamines in the first cycle received IV premedication with dexamethasone 20 mg, diphenhydramine 50 mg, and ranitidine 50 mg (or their equivalents) approximately 30 to 45 minutes before subsequent doses. Surface area (BSA) was determined at screening, and was recalculated prior to each dose of study drug only when body weight varied by >10% from the last BSA determination.

Efficacy Assessments

All patients who received at least 1 dose of study drug were followed up for survival. Patients were evaluated for tumor responses every 6 weeks. Spiral CT scans with contrast were the preferred imaging modality unless the contrast material was contraindicated. Once a tumor was measured at baseline, all subsequent assessments used the same imaging or assessment method, whenever possible. Objective tumor responses were defined according to RECIST guidelines and were considered confirmed if noted on 2 evaluations at least 4 weeks apart. Patients meeting these assessment criteria were defined as response evaluable. Patients who discontinued treatment for reasons other than disease progression were followed every 6 weeks until criteria for progression were met.

Cytological or histological tumor tissue samples, when available, were evaluated for EGFR expression by immunohistochemistry using the DAKO EGFR pharmDx assay, although EGFR expression was not used as an eligibility criterion.

Safety Assessments

Adverse events were monitored continuously during treatment and evaluated according to the National Cancer Institute's CTCAE, version 3.0. Physical examinations, including neurological assessment, performance status, and evaluation of baseline signs and symptoms, were performed before treatment and then every 3 weeks during treatment. Vital signs were monitored before the dose was administered, every 30 minutes during infusions, at the end of each infusion, and for cetuximab, at 1 hour after infusion. A 12-lead electrocardiogram was recorded at baseline and then as clinically indicated. Complete blood counts including differential were monitored weekly, and serum chemistry was monitored every 3 weeks.

Statistical Analysis

The 6-month survival rate, calculated from the date of the first dose of study treatment, and its exact 2-sided 95% confidence interval (CI) were determined for all treated patients and also estimated using the Kaplan-Meier product limit method.

The study was testing the null hypothesis that the true 6-month survival rate was ≤50% vs. the alternative that the true 6-month survival rate was ≥70%. In order to have 81% power to reject the null hypothesis if the expected 6-month survival rate is 70% at the 2-sided, α = 0.05 level with the exact test, a total of 52 treated patients had to be accrued. With 52 treated patients, the maximum width of the 95% CI is 28% given that the expected 6-month survival rate is within the 50% to 70% range.

ORR and its exact 2-sided 95% CI were determined by the proportion of response-evaluable patients with a best response of partial response (PR) or complete response. Time to response was summarized descriptively for all patients with an objective response, and the duration of response was estimated using the Kaplan-Meier product limit method. PFS and OS were also analyzed by the Kaplan-Meier method for all treated patients. Each time-based variable was summarized by median and 2-sided CI using the method of Brookmeyer and Crowley.18 Safety parameters were analyzed using descriptive statistics for all treated patients.


Patients and Exposure to Study Drugs

Fifty-four patients were enrolled at 9 study sites. The median age was 63 years (range 47–84 years), and 22 (40.7%) were aged ≥65 years. The majority (64.8%) of patients were male and most had metastatic disease (92.6%) (Table 1). Patients received a median of 4 cycles of ixabepilone (range, 1–21 cycles) and 12 weekly infusions of cetuximab (range, 1–58 infusions). The median cumulative dose of ixabepilone was 127.7 mg/m2, with a median dose intensity of 10.6 mg/m2/week. For cetuximab, median cumulative dose and dose intensity was 3,140 mg/m2 and 249 mg/m2/week, respectively.

Table 1.
Demographic and baseline clinical characteristics


Overall, 31 patients survived to the 6-month milestone. The 6-month survival rate (primary efficacy measure) for this study was therefore 57% (31/54 patients; 95% CI: 43–71%) and median OS (n = 54) was 7.6 months (95% CI: 5.5–12.2 months; Figure 1). The Kaplan-Meier estimate (n = 54) for 6-month survival was 62% (95% CI: 48.8–75.1%) with subsequent analyses estimating the 12-month survival rate as 40% (95% CI: 27–54%). At the time of the data cut-off, disease progression had occurred in 49 of the 54 patients, with median PFS of 3.9 months (95% CI: 2.6–4.4 months; Figure 1).

Figure 1.
Overall survival, including 6-month survival rate (top) and progression-free survival (bottom).

Of the response evaluable patients (n = 31), 4 (12.9%) achieved PRs and an additional 24 (77.4%) patients had stable disease (Table 2). Therefore, 28 (90.3%) of the 31 response-evaluable patients had disease control with study treatment. In the context of the total study population, 7.4% (4/54 patients) achieved PR, and 51.9% (28/54 patients) had disease control. Of those patients who achieved PR, the median duration of response was 5.7 months (95% CI: 2.8–6.3 months). Median time to response (n = 4) was 8.8 weeks.

Table 2.
Responses to treatment with ixabepilone plus cetuximab

Tissue samples were available for 13 treated patients, of whom 11 were EGFR positive and 2 were EGFR negative. Among the 13 patients, 2 EGFR-positive patients and 1 EGFR-negative patient achieved survival >6 months.

Subsequent analyses revealed that patients who developed rash on-study (n = 36) achieved a greater OS rate (median 8.8 months, [95% CI: 6.5–15.4 months]) compared with those without rash (n = 18; median 2.6 months, [95% CI: 1.3–11.8 months]; Figure 2). Time to rash was not recorded.

Figure 2.
Overall survival by acneiform rash (n = 54).


The adverse event profile was consistent with prior clinical trials of ixabepilone or cetuximab (Table 3). The most common grade 3/4 hematological toxicities were leukopenia (39%) and neutropenia (33%); including 8 patients with grade 4 neutropenia and 4 patients with grade 4 leukopenia. Two patients had febrile neutropenia. All other hematological toxicities were grade 1 or 2 except for 2 patients (4%) with grade 3 anemia.

Table 3.
Adverse events

Nonhematologic toxicities were generally mild or moderate (ie, grade 1 or 2). The most common grade 3/4 nonhematological toxicities were fatigue/asthenia (n = 10; all grade 3 except for 1 patient with grade 4), hypomagnesemia (n = 4), diarrhea (n = 3), vomiting (n = 3), peripheral neuropathy (n = 3), and hypersensitivity (n = 3). Overall, there were 5 hypersensitivity reactions related to ixabepilone and 3 related to cetuximab.

Acne-form dermatitis, an adverse event associated with cetuximab and other EGFR blockers, occurred in 29 patients (53.7%), with only 1 occurrence of grade 3.

Ixabepilone was discontinued due to toxicity by 7 (13.0%) patients, most commonly for peripheral neuropathy (n = 3) or hypersensitivity (n = 2). Twelve patients (22.2%) required dose reductions, most commonly for neutropenia (n = 5), fatigue (n = 3), or liver enzyme elevations (n = 3). Cetuximab was discontinued due to toxicity in 4 (7.4%) patients, including 3 patients for hypersensitivity and 1 patient due to hypomagnesemia. Six patients required dose reductions (11.1%), most commonly for hypomagnesemia (n = 4) or hypertension (n = 2).


The combination of ixabepilone plus cetuximab was generally well tolerated by patients with advanced pancreatic cancer. However, the study failed to reject the null hypothesis and meet its primary end point. Moreover, the efficacy of ixabepilone plus cetuximab in the present study (6-month survival rate of 57% with a median survival of 7.6 months and confirmed PR in 13% of patients) was comparable with that previously reported for single-agent ixabepilone (estimated 6-month survival of 60% with a median survival of 7.2 months and confirmed PR in 9% of patients).12 The efficacy results achieved with single agent ixabepilone and the ixabepilone/cetuximab combination appear comparable to those reported with gemcitabine-based therapy in contemporary phase 2 and 3 trials.5,7,14,19

Despite the disappointing results in this phase 2 trial, the potential for ixabepilone plus cetuximab to provide additional clinical benefit in subgroups of pancreatic cancer patients should be explored. Potential molecular predictors, including BRAF, KRAS, or tubulin mutation status were not included as part of this clinical trial. In addition, clinical indicators such as smoking status, as recently reported for erlotinib, may also be important in patient selection for EGFR inhibitors in pancreatic cancer.20

The efficacy results in patients with rash (at any grade) in this study support the findings of multiple other trials of EGFR-targeted therapies, whereby a higher grade of rash correlated with improved outcome (although severe rash is not necessary to achieve a positive outcome). The etiology and clinical significance of this association remain to be determined; however, the association has been postulated to arise from variations in drug absorption or metabolism, or genetic variability affecting the expression of EGFR in both germline and tumor cells.21

Grade 3/4 peripheral neuropathy was reported in 3/54 (5.6%) patients within this study compared with 9/60 (15%) with single agent ixabepilone in a similar patient population.12 It was anticipated that a starting dose of 32 mg/m2 would result in a lower rate of treatment-related adverse events and in particular, peripheral neuropathy. In the single-agent trial of ixabepilone, the drug was administered at a dose of 40 mg/m2. The starting dose of 32 mg/m2 in the current study was based on pooled safety data from different patient populations, suggesting that there is a direct correlation between the starting dose of ixabepilone and the rate and severity of adverse events. Last, ixabepilone 32 mg/m2 administered second-line as a 3-hour infusion every 3 weeks was shown to be clinically active in a phase 2 trial in patients with non–small-cell lung cancer whose tumors had failed first-line, platinum-based chemotherapy.22

In conclusion, the combination of ixabepilone and cetuximab is feasible and has acceptable toxicity. Although the study did not meet its primary end point, the efficacy results are similar to gemcitabine-based combination therapies and single-agent ixabepilone in patients with advanced pancreatic cancer. An understanding of the efficacy of ixabepilone plus cetuximab in enriched populations of pancreatic cancer patients selected by potential molecular or clinical predictors remains to be fully investigated. It is unlikely that this drug combination will be explored further in patients with advanced pancreatic cancer.


The authors take full responsibility for the content of this publication and confirm that it reflects their viewpoint and scientific expertise. They also wish to acknowledge StemScientific, funded by Bristol-Myers Squibb, for providing writing and editorial support.


This work was supported by Bristol-Myers Squibb.

Disclosures of Potential Conflicts of Interest

Mark Zalupski received research funding from Bristol-Myers Squibb to perform this study. Remigiusz Kaleta, M. Brent McHenry, and Ovidiu C. Trifan are employees and stockholders of Bristol-Myers Squibb. All remaining authors have declared no conflicts of interest.


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