Vol. 26 No. 3 September 2003 Journal of Pain and Symptom Management 849
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1 Vol. 26 No. 3 September 2003 Journal of Pain and Symptom Management 849 Original Article Amifostine, in a Reduced Dose, Protects Against Severe Diarrhea Associated with Weekly Fluorouracil and Folinic Acid Chemotherapy in Advanced Colorectal Cancer: A Pilot Study Nicolas Tsavaris, MD, Christos Kosmas, MD, Maria Vadiaka, MD, Dimitris Zonios, MD, Efstathios Papalambros, MD, Nikitas Papantoniou, MD, Heraklis Margaris, MD, George Zografos, MD, Sofia Rokana, BSc, George Retalis, MD, BSc, and Christos Koufos, MD Department of Pathophysiology (N.T., C.K., M.V., D.Z., S.R., G.R., C.K.), Laikon General Hospital, University of Athens; First Surgical Unit (E.P., N.P.), University of Athens School of Medicine; and 3rd Surgical Unit, G. Genimatas General Hospital (H.M., G.Z.), Athens, Greece Abstract Fifty-two consecutive patients with advanced colorectal cancer who developed persistent diarrhea following chemotherapy with 5-fluorouracil despite dose reduction were treated with amifostine 800, 500 or 150 mg/m 2. The administered dose of 5-fluorouracil was significantly greater during amifostine treatment. Amifostine 800 mg/m 2 was associated with complete elimination of diarrhea, but 76.3% of patients developed infusion-related hypotension. At a dose of 500 mg/m 2, diarrhea was significantly reduced and milder compared with baseline and the incidence of hypotension was 54.2%. At the lowest dose of amifostine, 17.1% of patients developed Grade 1 diarrhea, a significant reduction over baseline, and hypotension occurred in 25.2% of patients. Treatment with amifostine also improved mucositis but had no effect on the relatively mild nausea and vomiting due to 5- fluorouracil. In this study, amifostine reduced the incidence and severity of diarrhea associated with 5-fluorouracil in patients with advanced colorectal cancer, with acceptable efficacy at a reduced dose that offered better tolerability. J Pain Symptom Manage 2003;26: U.S. Cancer Pain Relief Committee. Published by Elsevier Inc. All rights reserved. Key Words Amifostine, 5-Fluorouracil, folinic acid, colorectal cancer Address reprint requests to: Nicolas Tsavaris, MD, Department of Pathophysiology, Athens University School of Medicine, Laikon General Hospital, Athens, Greece. Accepted for publication: January 18, U.S. Cancer Pain Relief Committee Published by Elsevier Inc. All rights reserved. Introduction 5-Fluorouracil (5-FU) is associated with a relatively high risk of gastrointestinal toxicity and myelotoxicity; the incidence and severity of symptoms vary according to the dose, schedule and the route of administration. 1 Epithelial /03/$ see front matter doi: /s (03)
2 850 Tsavaris et al. Vol. 26 No. 3 September 2003 ulceration may occur throughout the gastrointestinal tract, causing mucositis, pharyngitis, dysphagia, esophagitis, gastritis, colitis, or proctitis. Diarrhea may be watery or bloody, and the combination of nausea, vomiting, and profuse diarrhea can lead to profound dehydration and/or hypotension. There is also an increased risk of overwhelming sepsis if the granulocyte nadir coincides with diarrhea. 2 The occurrence of gastrointestinal toxicity, even if mild, indicates the need to withhold treatment; after recovery, subsequent doses should be reduced to avoid recurrence. 2 Diarrhea, therefore, not only adversely affects patients well being but may also impair treatment outcomes by limiting the administered dose of 5-FU. Treatment options for diarrhea associated with 5-FU are limited. Diphenoxylate or loperamide may help control mild diarrhea and the somatostatin analogue octreotide is more effective in controlling more severe and refractory symptoms. 3 6 Furthermore, these drugs are useful only after the onset of diarrhea whereas prevention of symptoms would be a preferable strategy. Amifostine (WR-2721), an aminothiol compound, selectively protects normal but not tumor tissues from the cytotoxic effects of radiation therapy and chemotherapy, and may offer a new option for the management of gastrointestinal toxicity associated with 5-FU. In preclinical and Phase II-III clinical studies, amifostine substantially reduced the incidence and severity of a range of adverse effects associated with chemotherapy, such as mucositis and myelosuppression However, it is also associated with adverse effects of its own, including hypotension, nausea, vomiting, chills and dizziness, and these often indicate the need for dose reduction. We therefore evaluated the efficacy and tolerability of lower doses of amifostine in patients who developed serious diarrhea and myelotoxicity during treatment with 5-FU and calcium folinate. Methods Patients were recruited consecutively from those attending Laikon General Hospital. Eligible patients had advanced metastatic or stage Dukes B 2 or C colorectal cancer and developed serious Grade 3 and 4 or persistent Grade 2 diarrhea (WHO) 11 while undergoing adjuvant chemotherapy with 5-FU 500 mg/m 2 plus calcium folinate mg/m 2 weekly. Treatment was interrupted for the management of diarrhea with anti-diarrheal agents (diphenoxylate, loperamide or octreotide); patients with severe diarrhea were hospitalized. In case of Grade 2 or 3/4 diarrhea, chemotherapy was initially continued by decreasing the dose of 5-FU by 10 20%. When diarrhea recurred, the first 18 patients (Group I) continued treatment with the initial dose of 5-FU and calcium folinate plus amifostine 800 mg/m 2 weekly. The dose was subsequently lowered to 500 mg/m 2 weekly (Group II, n = 16) and then to 150 mg/m 2 weekly (Group III, n = 18). Toxicity was evaluated according to WHO criteria. 11 Amifostine toxicity was defined as infusionrelated hypotension. The primary endpoints were the proportion of 5-FU/calcium folinate doses associated with diarrhea or amifostine toxicity. Secondary endpoints were chemotherapy-related adverse effects such as mucositis, anorexia, nausea and vomiting reported by patients and hematological toxicity. Continuous outcomes were compared using the paired t-test (comparisons with baseline) or the independent sample t-test (betweengroups); these tests were also applied to the proportions of doses with Grade 1 diarrhea or associated with amifostine toxicity after an initial transformation using the inverse sine transformation. 12 Changes in hematological parameters were analyzed as dichotomous (binary) variables decrease or increase. For paired comparisons the McNemar test was used, while for independent comparisons Pearson s chi-square (with Fisher s P-value where appropriate) was used. Results The study population comprised 52 patients; their baseline characteristics are summarized in Table 1. The mean number of cycles of 5-FU and calcium folinate administered prior to treatment with amifostine was and median 9 (range, 5 17). The incidence of diarrhea per 5-FU treatment cycle during the baseline phase (for all 52 patients entering the study) is listed by severity in Table 2. All patients
3 Vol. 26 No. 3 September 2003 Amifostine and Chemotherapy-Associated Diarrhea 851 Table 1 Patient Characteristics Number of patients 52 Advanced disease 25 Stage Dukes B2 and C 27 Age (median) 62 Range Sex Male 36 Female 16 Performance status (Karnofsky) Primary site Colon 40 Rectum 12 Grade of differentiation I 0 II 43 III 9 Number of metastatic sites and 4 3 Site of metastases Liver 28 Lymph nodes 11 Lung 4 Abdominal 7 Pelvis 5 received diphenoxylate or loperamide to control diarrhea; 12 were also treated with octreotide until the resolution of diarrhea and 7 were admitted for rehydration therapy. Compared with baseline, all doses of amifostine significantly reduced the incidence of diarrhea (P for each group; Fig.1) and mucositis (P 0.04); in addition, symptoms were milder. There were no differences between the groups in severity of diarrhea or mucositis. The incidence and severity of nausea and vomiting were unchanged compared with baseline (Table 2). The incidence of hypotension associated with amifostine was dose-related (Fig. 2). Patients in Groups I and II experienced similar protection against diarrhea and mucositis but the incidence of amifostine-related adverse effects was significantly lower in Group II (Table 3). In Group III, the incidence of Grade 1 diarrhea was 17.1%, significantly greater than in Group 1 (0%; P ) or Group II (5.8%, P 0.015) but there were no differences between the groups in the incidence of more severe diarrhea (Table 2). The incidence of adverse effects associated with amifostine was significantly lower in Group III than in either Group I or Group II (Table 3). There was a statistically significant difference in the mean administered doses of 5-FU between patients prior to treatment with amifostine (445 mg/m 2 ) and subsequently ( mg/m 2 ; P 0.04 for all groups) (Tables 3). There was no significant difference between the mean 5-FU doses during treatment with amifostine. Amifostine also reduced the incidence and severity of hematological toxicity. Hemoglobin decreased in 92% of patients prior to treatment with amifostine, compared with 55% of patients during treatment with amifostine at all doses. It should be stressed that erythropoietin was not administered for the management of anemia, and patients with hemoglobin levels 8 g/dl were transfused. The mean reduction in hemoglobin before treatment with amifostine was gr%, significantly more than in Group I ( gr%; P 0.04), Group II ( gr%; P 0.04) or Group III Table 2 Incidence of Diarrhea, Mucositis, and Nausea and Vomiting at Baseline and During Treatment with Amifostine (proportion of 5-FU treatment cycles affected) for All 52 Patients Entering the Study Therapy Groups Baseline I II III Baseline I II III Baseline I II III Number of Cycles Degree (WHO) 11 Diarrhea a (%) Mucositis b (%) Nausea & Vomiting c (%) a P for all groups vs. baseline. b P 0.04 for all groups vs. baseline. c P 0.98, P 0.98, P 1.0 vs. baseline.
4 852 Tsavaris et al. Vol. 26 No. 3 September 2003 Fig. 1. Percentage of 5-FU treatment cycles associated with diarrhea. Baseline vs. Groups I, II, III, P ; Group I vs. Group II, P 0.95; Group I vs. Group III, P 0.15; Group II vs. Group III, P ( gr%; P 0.05). Moreover, the platelet count was significantly higher during treatment with amifostine 800 mg/m 2 than at baseline (baseline, 82% of patients, mean decrease /mm /mm 3 ;Group I, 17% of patients, mean decrease / mm /mm 3 )(P 0.04). No other differences in hematological parameters (e.g., in white cells and neutrophils) were statistically significant. Discussion This study demonstrates that amifostine reduces the incidence and severity of diarrhea and mucositis associated with chemotherapy with 5-FU and calcium folinate in patients with advanced colorectal cancer, despite the use of decreased doses of 5-FU. Furthermore, it shows that amifostine is equally effective but better tolerated at a dose of 500 mg/m 2 than at the dose currently used to protect against hematological toxicity associated with other treatment regimens. Even the lowest dose in this study (150 mg/m 2 ) conferred clinically important protection against the adverse effects of chemotherapy, with only a relatively modest increase in the risk of mild Grade 1 diarrhea, a level that could be considered clinically acceptable. 5-FU is a long-established cytotoxic agent that remains a drug of choice for the treatment of gastrointestinal malignancies. However, its adverse effects are often dose-limiting. Amifostine appears to offer protection against these adverse effects and permits the use of higher doses of 5-FU. Amifostine is a broad spectrum, selective cytoprotective agent that reduces the adverse effects of various chemotherapy regimens involving alkylating agents, platinums, taxanes and anthracyclines. 8,13,14 Effective doses of amifostine Fig. 2. Incidence of infusion-related hypotension due to amifostine. Baseline vs. Groups I, II, III, P 0.001; Group I vs. Group II, P 0.06; Group I vs. Group III, P 0.02; Group II vs. Group III, P 0.04.
5 Vol. 26 No. 3 September 2003 Amifostine and Chemotherapy-Associated Diarrhea 853 Table 3 Weekly Doses of 5-FU and Amifostine, Mean and Median Dose of 5-FU, and the Proportion of 5-FU Doses Associated with Amifostine Toxicity Doses of Amifostine 5-FU (mg/m 2 ) Adverese Effects of Group n 5-FU LV (mg/m 2 ) Mean Median Amifostine (%) Baseline I a II a b III a c,d a P 0.04 vs. baseline. b P 0.04 vs. Group I. c P 0.02 vs Group I. d P 0.04 vs. Group II. appear to be in the range of mg/m 2 when it is used in conjunction with chemotherapy and in the range of mg/m 2 when it is used in conjunction with radiotherapy. It affords not only protection from myelotoxicity, but also against other chemotherapy-related toxicities, such as nephrotoxicity, cardiotoxicity, gastrointestinal and mucosal toxicity, and peripheral neurotoxicity In the present study, we started using amifostine at a dose comparable to that indicated to protect against the hematological toxicity of cisplatin (800 mg/m 2 ). This was associated with a high incidence of adverse effects (76.3% in Group I), though there was complete resolution of severe (Grade 3 4) or persistent (Grade 1 2) 5-FU-related diarrhea. To improve the tolerability of amifostine, we reduced the dose substantially, first to 500 mg/m 2 (the dose typically used in the treatment of myelodysplastic syndromes, then to 150 mg/m 2 (selected as a potentially minimally effective dose that might also offer cost savings). Although we did not observe the same degree of protection against diarrhea using these lower doses, the response was clinically satisfactory and there was a significant reduction in the incidence and severity of diarrhea. This study shows that 20% of the usual dose of amifostine is still capable of offering an adequate degree of cytoprotection against diarrhea and mucositis associated with 5-FU. Although nausea and vomiting was not reduced, this was usually mild and clinically insignificant. There was also evidence that amifostine reduced the incidence and severity of anemia and thrombocytopenia 20 but it was difficult to assess the significance of these findings in patients who, after an average of nine weekly doses of 5-FU, were already suffering from some degree of mild myelosuppression. As there was not a parallel non-treatment randomized control group, the findings and conclusions of the present study should not be regarded as definitive. Many potential biases can overestimate the benefit from sequential amifostine treatment at different dose levels. Some of these could be: (i) augmentation of the severity of diarrhea/mucositis and anemia with prolonged 5-FU LV treatment in some patients, (ii) disease-associated worsening of performance status and subsequent impaired tolerance of treatment, and (iii) sequential and non-random assignment of patients with Grade II-IV toxicity to the 3 amifostine dose levels. In conclusion, the present study demonstrates that amifostine is able to reduce the incidence and severity of diarrhea associated with 5-FU. Efficacy appears clinically acceptable at a relatively low dose that offers superior tolerability. Further randomized studies are now required to determine the optimal dose of amifostine versus no treatment for this indication. References 1. Pinedo HM, Peters GF. Fluorouracil: biochemistry and pharmacology. J Clin Oncol 1988;6: Ardalan B, Luis R, Jaime M, et al. Biomodulation of fluorouracil in colorectal cancer. Cancer Invest 1998;16: Cascinu S, Fedeli A, Fedeli SL, et al. Octreotide versus loperamide in the treatment of fluorouracilinduced diarrhea: a randomized trial. J Clin Oncol 1993;11: Mahood DJ, Kose AM, Loprinzi CL, et al. Inhibition of fluorouracil-induced stomatitis by oral cryotherapy. J Clin Oncol 1991;9:
6 854 Tsavaris et al. Vol. 26 No. 3 September Grem JL. 5-Fluoropyrimidines. In: Chabner BA, Longo DL, eds. Cancer chemotherapy and biotherapy: principles and practice. 2nd ed. Philadelphia: Lippincott-Raven, 1996: Ardalan B, Singh G, Silberman HA. Randomized phase I and phase II study of short-term infusion of high-dose fluorouracil with or without N-(phosphonacetyl)-L-aspartic acid in patients with advanced pancreatic and colorectal cancer. J Clin Oncol 1988;6: Alberts DS, Bleyer WA. Future Development of amifostine in cancer treatment. Semin Oncol 1996; 23: Martens-Lobenhoffer J, Fuhlroth J, Ridwelski K. Influence of the administration of amifostine on the pharmacokinetics of 5-fluorouracil in patients with metastatic colorectal carcinoma. Int J Clin Pharmacol 2000;38: Van Laar JA, van der Wilt CL, Treskes M, et al. Effect of WR-2721 on the toxicity and antitumor activity of the combination of carboplatin and 5-fluorouracil. Cancer Chemother Pharmocol 1992;31: Wasserman TH, Phillips TL, Ross G, et al. Differential protection against cytotoxic chemotherapeutic effects on bone marrow CFUs by Wr Cancer Clin Trials 1981;4: Miller A, Hoogstraten B, Staquet M, et al. Reporting results of cancer treatment. Cancer 1981; 47: Armitage P, Berry G. Statistical Methods in Medical Research, 2nd ed. Oxford: Blackwell, Bukowski RM. The need for cytoprotecion. Eur J Cancer 1966;32A:S2 S Mabro M, Faivre S, Raymond E. A risk-benefit assessment of amifostine in cytoprotection. Drug Safety 1999;21: Fahlke J, Ridwelski K, Lippert H. High-dose therapy with combined 5-fluorouracil and folinic acid with and without amifostine in the treatment of patients with metastatic colorectal carcinoma. Int J Colorectal Disease 1999;14: Kurbacher CM, Mallmann PK. Chemoprotection in anti-cancer therapy: the emerging role of amifostine (WR-2721). Anticancer Res 1998;18: Ng TY, Ngan HY, Cheng DK, et al. The effect of amifostine on the in vitro cytotoxicity of chemotherapeutic agents in three epithelial ovarian carcinoma cell lines. Gynecol Oncol 1999;75: Hospers GA, Eisenhauer EA, de Vries EG. The sulfhydryl containing compounds WR-2721 and glutathione as radio- and chemoprotective agents. A review, indications for use and prospects. Br J Cancer 1999;80: Poplin EA, LoRusso P, Lokich JJ, et al. Randomized clinical trial of mitomycin-c with or without pretreatment with WR-2721 in patients with advanced colorectal cancer. Cancer Chemother Pharmocol 1994;33: Budd GT. Amifostine and chemotherapy-related thrombocytopenia. Anticancer Res 1996;23:49 52.
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