Journal of Clinical Oncology, Vol 22, No 7 (April 1), 2004: pp. 1209-1214
© 2004 American Society of Clinical Oncology.
DOI: 10.1200/JCO.2004.11.037
Survival of Patients With Advanced Colorectal Cancer Improves With the Availability of Fluorouracil-Leucovorin, Irinotecan, and Oxaliplatin in the Course of Treatment
Axel Grothey,
Daniel Sargent,
Richard M. Goldberg,
Hans-Joachim Schmoll
From the Divisions of Medical Oncology and Biostatistics, Mayo Clinic, Rochester, MN; Division of Oncology, University of North Carolina, Chapel Hill, NC; and Department of Hematology/Oncology, University of Halle, Halle, Germany
Address reprint requests to Axel Grothey, MD, Division of Medical Oncology, Mayo Clinic, 200 First St SW, Rochester, MN 55905; e-mail: grothey.axel{at}mayo.edu
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ABSTRACT
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PURPOSE: Fluorouracil (FU)-leucovorin (LV), irinotecan, and oxaliplatin administered alone or in combination have proven effective in the treatment of advanced colorectal cancer (CRC). Combination protocols using FU-LV with either irinotecan or oxaliplatin are currently regarded as standard first-line therapies in this disease. However, the importance of the availability of all three active cytotoxic agents, FU-LV, irinotecan, and oxaliplatin, on overall survival (OS) has not yet been evaluated.
MATERIALS AND METHODS: We analyzed data from seven recently published phase III trials in advanced CRC to correlate the percentage of patients receiving second-line therapy and the percentage of patients receiving all three agents with the reported median OS, using a weighted analysis.
RESULTS: The reported median OS is significantly correlated with the percentage of patients who received all three drugs in the course of their disease (P = .0008) but not with the percentage of patients who received any second-line therapy (P = .19). In addition, the use of combination protocols as first-line therapy was associated with a significant improvement in median survival of 3.5 months (95% CI, 1.27 to 5.73 months; P = .0083).
CONCLUSION: Our results support the strategy of making these three active drugs available to all patients with advanced CRC who are candidates for such therapy to maximize OS. In addition, our findings suggest that, with the availability of effective salvage options, OS should no longer be regarded as the most appropriate end point by which to assess the efficacy of a palliative first-line treatment in CRC.
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INTRODUCTION
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Colorectal cancer (CRC) is the third most common cause of cancer deaths for both men and women in the United States and Europe and is the second most common lethal cancer overall. In the last 10 years, several new cytotoxic agents with activity as single agents have widened the spectrum of therapeutic options in advanced CRC.1 In particular, chemotherapy protocols including irinotecan and oxaliplatin alone or coupled with fluorouracil (FU)-leucovorin (LV) have been extensively studied in phase II and III trials, both as first- and second-line therapies.
The median survival for patients with advanced disease treated with FU-LV without effective salvage therapy has been consistently reported as 11 to 13 months by a variety of investigators.2,3 This was confirmed recently in several large trials using FU-LV (or capecitabine) without effective salvage therapy, which again reported a consistent median overall survival (OS) of 12 to 13 months.4,5 The positive impact of irinotecan as a second-line therapy on OS was demonstrated in two pivotal multicenter randomized phase III studies conducted in FU-LV-refractory patients with advanced CRC.6,7 Several phase III trials investigating combination regimens with FU-LV plus irinotecan or oxaliplatin as first-line therapy have achieved OS of 14.8 to 21.5 months, suggesting that combining these agents is advantageous.1 On the basis of the finding of improved OS demonstrated in two phase III trials,8,9 FU-LV-irinotecan (IFL) was approved as first-line therapy of advanced CRC by the United States Food and Drug Administration in 2000, replacing FU-LV as the standard of care. The IFL (Saltz) regimen, in which FU is delivered as a bolus, emerged as standard therapy in the United States, whereas in Europe, clinicians have tended to favor regimens in which FU is delivered as a 1- to 2-day infusion in conjunction with irinotecan. Recent results of the Intergroup trial N9741 demonstrated the superiority of an oxaliplatin-based first-line therapy over the IFL protocol in terms of efficacy (response rate, progression-free survival, and OS) and safety.10
It is intriguing and of great clinical interest that the recently published phase III trials using combination protocols as first-line therapy of advanced CRC have shown substantial variations in the reported median OS, with a range of 14.8 to 21.5 months.3,8-13 It is unlikely that differences in patient selection or factors unrelated to the actual treatment strategy caused this variation because of the large number of patients enrolled onto each of these trials and the fact that all trials were conducted within a relatively short time frame. However, although it is conceivable and even likely that effective salvage therapies have an impact on patient OS and, thus, contributed to the differences in OS observed, the impact of serial therapies has yet not been systematically assessed in clinical trials. Therefore, our analysis was undertaken to investigate the influence of active salvage therapies on the reported median OS in CRC in recent clinical trials and, in particular, the impact of the availability of all three active cytotoxic agents, FU-LV, irinotecan, and oxaliplatin, in the course of the treatment.
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MATERIALS AND METHODS
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We reviewed the data from seven recently published or presented phase III trials in CRC. For each trial, the percentage of patients receiving any second-line therapy and the percentage of patients treated with all three active drugs (FU-LV, irinotecan, and oxaliplatin) in the course of their disease were recorded. The order in which the drugs were administered was not specified, so individuals could be exposed to any agent as either first- or second-line therapy. The data were taken from published articles or, if a full report had not yet been published, from presentations at American Society of Clinical Oncology meetings with updates and revalidation of the number of patients receiving second-line therapies made by the authors of the trial12 that was conducted under their supervision. In addition, we abstracted information on patient median OS from each trial. A test for heterogeneity between regimens with monotherapy versus combination initial therapy was performed. Subsequently, only those treatment arms containing an irinotecan- or oxaliplatin-based combination as a first-line therapy were included for the following reasons: (1) the test for heterogeneity indicated a survival advantage for combination initial therapy, (2) combination initial therapy has become standard of care, and (3) reliable and comparable data on patients receiving all three agents in the course of their treatment were available only on those arms. This resulted in the inclusion of 10 treatment arms from the seven trials. We did not include secondary surgery as a treatment modality in our analysis because this was not an end point in any of the studies and, thus, was not consistently recorded and analyzed. Table 1 summarizes the design of the trials used in our analysis. The goal of the analysis was to correlate both the percentage of patients receiving second-line therapy and the percentage of patients receiving all three agents with the reported median OS. For analysis, the Spearman rank correlation test was supplemented by simple linear regression. As a sensitivity analysis, a weighted regression was used, with weights proportional to the trial's sample size. P values reported are based on the weighted regression models, with P < .05 used to denote statistical significance.
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RESULTS
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A test for heterogeneity between regimens that used combination versus monotherapy as the initial treatment indicated significant heterogeneity between these two approaches (P = .01). Specifically, patients treated with a combination therapy as first-line treatment had a predicted 3.5 months improvement in median survival (95% CI, 1.27 to 5.73 months). We subsequently focused on the 10 first-line combination therapy regimens. As illustrated in Table 2 and Figure 1, the percentage of patients who were treated with FU-LV and irinotecan and oxaliplatin at some point in their disease showed a strong correlation with the reported median OS. This correlation was statistically significant (P = .0008). Thus, studies in which a high percentage of patients had access to all three active cytotoxic drugs in the course of their treatment showed the longest OS. The reported median OS did not show a significant correlation with the percentage of patients receiving any, that is, not necessarily irinotecan- or oxaliplatin-based, second-line treatment (P = .19).
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Table 2. Correlation Between Percentage of Patients Receiving FU-LV and Irinotecan and Oxaliplatin in the Course of Their Disease or Any Second-Line Therapy and the Reported Median OS
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Fig 1. Regression plot and relationship between percentage of patients (pts) receiving fluorouracil (FU)-leucovorin (LV), irinotecan, and oxaliplatin (3 drugs) in the course of their disease and the reported median overall survival (OS). Mathematical equitation of regression (based on a weighted model [solid line]): median OS (months) = 14.09 + 0.09 x (% patients with three drugs). First-line therapies: circles, infusional FU-LV + oxaliplatin; squares, infusional FU-LV + irinotecan; diamonds, bolus FU-LV + irinotecan; and triangle, irinotecan + oxaliplatin. Pts, patients.
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DISCUSSION
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The positive correlation between treatment with FU-LV, irinotecan, and oxaliplatin and improvement in patient OS is striking. This finding suggests that it is important to make all drugs that have well-demonstrated clinical activity in CRC (in particular, FU-LV, irinotecan, and oxaliplatin) available to all patients with advanced CRC to guarantee maximal benefit of systemic therapy for OS. The results indicate that the percentage of patients receiving all three active drugs (FU-LV, irinotecan, and oxaliplatin) is more important than the overall percentage of patients receiving any second-line therapy in influencing patient OS. This suggests that the specific second-line therapy patients receive does impact median survival; for maximum benefit in terms of OS, patients with oxaliplatin-based first-line chemotherapy need irinotecan-based second-line therapy and vice versa. Thus, effective salvage therapies might indeed compensate for a less-active first-line therapy.
We recognize that the nature of the analysis conducted raises a question of inherent bias. Specifically, one could argue that patients who live longer have greater opportunity to be treated with all three active drugs. Patients with poorer performance status and, thus, shorter life expectancy might have been excluded from irinotecan- or oxaliplatin-based second-line therapy. In addition, our analysis did not specifically distinguish between whether the one missing active drug was given as second- or third-line therapy. However, at the time the studies were conducted, not all drugs, in particular, oxaliplatin, were available for all patients enrolled onto the trials. It is of interest in this context that more recent trials, in which patients were more likely to have access to all three active drugs, in particular, oxaliplatin, were associated with a longer median OS. It seems unlikely that reasons unrelated to the use of oxaliplatin, such as changes in general oncologic practice, could have accounted for this effect. It is also unlikely that the percentage of patients in poor performance status after first-line therapy differed greatly between the phase III trials. Furthermore, the fact that not any kind but only specific second-line therapies were significantly correlated with median OS in our analysis argues against this point because a high percentage of patients in all trials (52% to 81.3%) lived long enough to have the chance to receive second-line treatment of any kind.
Our findings further indicate a significant advantage in OS if combination chemotherapy is used first-line. Regimens that used combination versus monotherapy as the initial treatment were associated with a predicted 3.5-month improvement in median survival (P = .0083; 95% CI, 1.27 to 5.73 months). This finding of our informal pooled analysis could be useful to further support the use of combination protocols as first-line therapy as the optimal treatment strategy for patients with advanced CRC. In addition and in accordance with our general hypothesis, the percentage of patients receiving all three drugs in the course of their treatment is higher if irinotecan- or oxaliplatin-based combination protocols are used as first-line options because, as is clear from Table 2, only 50% to 80% of patients can receive effective salvage therapies after failure of first-line treatments.
The importance of effective second-line therapies for OS in advanced CRC was first highlighted by the pivotal phase III trials using irinotecan as a salvage option in patients who had experienced failure on or progressed after first-line FU-LV treatment. In both trials, a significant prolongation of OS was achieved with second-line irinotecan versus best supportive care7 or infusional FU-LV.6 The value of active salvage therapies for the prognosis of patients with CRC is further supported by the results of the study recently presented by Tournigand et al,13 which tried to assess the optimal sequence of treatment protocols (biweekly infusional plus bolus FU-LV plus oxaliplatin [FOLFOX] followed by biweekly infusional plus bolus FU-LV plus irinotecan [FOLFIRI] v FOLFIRI followed by FOLFOX). The obligatory cross over within the study led to a high rate of patients who received FU-LV and oxaliplatin and irinotecan. This study has reported the longest median OS in a phase III study on advanced CRC so far. Interestingly, median OS did not differ significantly between the two sequences studied, although the sample size for this trial was relatively small by modern standards. However, the importance of the high percentage of cross over for patient survival in the Tournigand et al13 study is illustrated by the results of Intergroup trial N974110 in which a smaller proportion of patients receiving IFL as first-line therapy had second-line access to oxaliplatin, which, at the time of the study, was not approved in the United States. In contrast, patients receiving FOLFOX upfront had a much greater opportunity to receive irinotecan-based therapy. The efficacy of oxaliplatin-based therapy as second-line treatment in patients with CRC who had progressed on or relapsed within 6 months of first-line therapy with the IFL protocol has recently been demonstrated in a phase III trial of 463 patients. The combination protocol of oxaliplatin plus infusional (+ bolus) FU-LV was superior to oxaliplatin monotherapy and to infusional FU-LV alone in terms of response rate (9.9% v 1.3% v 0%, respectively) and progression-free survival (4.6 v 1.6 v 2.7 months, respectively).14 The data led to the registration of oxaliplatin in combination with infusional FU-LV as second-line therapy in advanced CRC in the United States.
A possible alternative explanation for these findings is that, as time has progressed and trials have included multiple agents, the advances that have been observed in median survival are the result of better patient selection, improvements in supportive care, or earlier detection of advanced disease. We find this explanation unlikely for two reasons. First, the median survival for patients with advanced CRC remained highly consistent at approximately 12 months for many years before the introduction of irinotecan and oxaliplatin. This consistent median survival was also observed in recently published phase III trials on oral fluoropyrimidines4,5,15,16 and a trial comparing continuous versus intermittent FU-LV or raltitrexed in advanced CRC17 with limited access to irinotecan- or oxaliplatin-based protocols as second-line therapy. Second, the median survival times for the FU-LV control arms that had low rates of second-line treatment in the studies included in this analysis were again approximately 12 to 13 months (12.6 months for the Saltz et al9 trial and 12.9 months for the FU-LV arm of N9741,18 which, however, only included 61 patients). We recognize that this study was not conducted as a formal meta-analysis because individual patient data was not obtained and only the reported median OS were used for analysis and, therefore, should be viewed as hypothesis generating. However, given the recent nature of many of these studies and the delays that are inherent in the processes of data collection, clean-up, analysis, and eventual publication, we feel that this less formal analysis still provides valuable information for the practitioner. A detailed assessment of the influence of prognostic or predictive factors on OS has to be reserved for future studies or a meta-analysis of all presently available clinical trials.
Our results suggest that the use of all three active drugs in advanced CRC produces the longest OS. Because sequential treatment with all three agents cannot be guaranteed for 100% of patients, one might consider the use of a triple-combination protocol as first-line therapy. The safety and efficacy of this approach has been assessed in several phase II trials. Triple-combination protocols using FU-LV plus irinotecan plus oxaliplatin have consistently resulted in high response rates of 57% to 78% in patients with previously untreated advanced CRC.19-22 Reliable data on progression-free survival and OS are still lacking, although an encouraging median OS of 22.5 months was reported in one trial.21 We caution against extrapolating from our regression model for a predicted median OS if 100% of patients received all three drugs because this is outside the range of our data and because concurrent (as opposed to sequential) administration of all three agents might yield different outcomes. The ability of first-line triple combinations to achieve or improve on the OS associated with dual-combination protocols as first-line therapy can only be assessed in a phase III trial.
On the basis of these results, we would propose that OS may no longer be the appropriate parameter and primary end point to assess the contribution of a new agent to the efficacy of first-line therapy in advanced CRC. Our analysis supports previous reports that second- and presumably third-line treatments can have a substantial impact on OS. It is not realistic to assume that sequential steps of therapies can be predefined in a phase III protocol because of differences in the availability of drugs, the experience of the investigators, and reimbursement issues. Therefore, other parameters, such as progression-free survival, time to treatment failure, and 60-day mortality, should be used in addition to OS to evaluate efficacy and clinical usefulness of first-line protocols. Our analysis could not address the question of the best sequence of treatment options (ie, whether an irinotecan- or oxaliplatin-based protocol should be preferred as first-line therapy). Current data do not definitively suggest the superiority of one sequence over the other, at least in terms of efficacy. This question can only be answered by future randomized trials comparing different sequential treatment strategies.
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Authors' Disclosures of Potential Conflicts of Interest
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The following authors or their immediate family members have indicated a financial interest. No conflict exists for drugs or devices used in a study if they are not being evaluated as part of the investigation. Acted as a consultant within the last 2 years: Axel Grothey, Sanofi-Synthelabo; Hans-Joachim Schmoll, Sanofi-Synthelabo; Richard M. Goldberg, Sanofi-Synthelabo, Pharmacia. Received more than $2,000 a year from a company for either of the last 2 years: Axel Grothey, Sanofi-Synthelabo, Aventis; Richard M. Goldberg, Sanofi-Synthelabo, Pharmacia; Hans-Joachim Schmoll, Sanofi-Synthelabo.
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NOTES
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Supported in part by Public Health Services grant No. CA-25224 from the National Cancer Institute to the Mayo Clinic in support of the North Central Cancer Treatment Group.
Authors' disclosures of potential conflicts of interest are found at the end of this article.
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Submitted November 8, 2002;
accepted January 23, 2004.
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July 10, 2005;
23(20):
4553 - 4560.
[Abstract]
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F. F. Kabbinavar, J. Hambleton, R. D. Mass, H. I. Hurwitz, E. Bergsland, and S. Sarkar
Combined Analysis of Efficacy: The Addition of Bevacizumab to Fluorouracil/Leucovorin Improves Survival for Patients With Metastatic Colorectal Cancer
J. Clin. Oncol.,
June 1, 2005;
23(16):
3706 - 3712.
[Abstract]
[Full Text]
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A. Venook
Critical Evaluation of Current Treatments in Metastatic Colorectal Cancer
Oncologist,
April 1, 2005;
10(4):
250 - 261.
[Abstract]
[Full Text]
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J. A. Meyerhardt and R. J. Mayer
Systemic Therapy for Colorectal Cancer
N. Engl. J. Med.,
February 3, 2005;
352(5):
476 - 487.
[Full Text]
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G. Masi, G. Allegrini, S. Cupini, L. Marcucci, E. Cerri, I. Brunetti, E. Fontana, S. Ricci, M. Andreuccetti, and A. Falcone
First-line treatment of metastatic colorectal cancer with irinotecan, oxaliplatin and 5-fluorouracil/leucovorin (FOLFOXIRI): results of a phase II study with a simplified biweekly schedule
Ann. Onc.,
December 1, 2004;
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1766 - 1772.
[Abstract]
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R. H. J. Mathijssen, F. A. de Jong, R. H. N. van Schaik, E. R. Lepper, L. E. Friberg, T. Rietveld, P. de Bruijn, W. J. Graveland, W. D. Figg, J. Verweij, et al.
Prediction of Irinotecan Pharmacokinetics by Use of Cytochrome P450 3A4 Phenotyping Probes
J Natl Cancer Inst,
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96(21):
1585 - 1592.
[Abstract]
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C. J. A. Punt
New options and old dilemmas in the treatment of patients with advanced colorectal cancer
Ann. Onc.,
October 1, 2004;
15(10):
1453 - 1459.
[Abstract]
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R. Chan and D. J. Kerr
Can we individualise chemotherapy for colorectal cancer?
Ann. Onc.,
July 1, 2004;
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996 - 999.
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TOP
ABSTRACT
INTRODUCTION
