Oncologist. The. Gastrointestinal Cancer. Phase II Study of 5-fluorouracil, Doxorubicin, and Mitomycin C for Metastatic Small Bowel Adenocarcinoma
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1 The Oncologist Gastrointestinal Cancer Phase II Study of 5-fluorouracil, Doxorubicin, and Mitomycin C for Metastatic Small Bowel Adenocarcinoma MICHAEL K. GIBSON, a CHRISTINA A. HOLCROFT, b,c LARRY K. KVOLS, d,e DANIEL HALLER f a Division of Medical Oncology, The Sidney Kimmel Comprehensive Cancer Center at Johns Hopkins, Baltimore, Maryland, USA; b Dana Farber Cancer Institute, Department of Biostatistics, Boston, Massachusetts, USA; c Work Environment Department, University of Massachusetts, Lowell, Massachusetts, USA; d Mayo Clinic, Rochester, Minnesota, USA; e Moffitt Cancer Center, Tampa, Florida, USA; f University of Pennsylvania, Philadelphia, Pennsylvania, USA ABSTRACT Background. Small bowel adenocarcinoma is a rare gastrointestinal malignancy that is treated primarily with surgery. Even with optimal resection, however, survival is poor and recurrences are common. Response rates to palliative combination chemotherapy are low, and the median duration of survival for metastatic disease is less than 1 year. This study aimed to document the response rate and survival time for patients with advanced small bowel adenocarcinoma who were not surgically curable and were treated with a regimen of 5-fluorouracil (5-FU), mitomycin C (Mutamycin ; Bristol-Myers Squibb; Princeton, NJ), and doxorubicin (Adriamycin ; Bedford Laboratories; Bedford, OH), the FAM regimen. Methods. This multi-institutional study was performed by the Eastern Cooperative Oncology Group (ECOG). Between November, 1983 and December, 1985, 39 patients with advanced or recurrent disease were enrolled. Chemotherapy was given as follows: 5-FU, 600 mg/m 2 on days 1, 8, 29 and 36; mitomycin C, 10 mg/m 2 on day 1; and doxorubicin, 30 mg/m 2 on days 1 and 29. Eligibility criteria included an ECOG performance Key Words. Chemotherapy Small bowel Adenocarcinoma status score of 0-2, measurable disease, and adequate baseline organ function. Prior chemotherapy was allowed. Response was measured by examination and imaging techniques. Survival time and time to progression were evaluated by the method of Kaplan and Meier, and these outcomes were stratified by clinical and laboratory covariates. Results. Of the 39 evaluated patients, 38 were eligible and 36 were evaluable for response. Grade 3-5 toxicities were experienced by a total of 26 patients (20 grade 3, 5 grade 4, 1 grade 5). The most common adverse events were neutropenia and vomiting. Responses were seen in a total of seven patients (2 complete responses, 5 partial responses), for a response rate of 18.4% (95% confidence interval of 7.8%-34.4%). The median survival time was 8 months. Conclusions. The FAM regimen was active and tolerable for patients with advanced small bowel adenocarcinoma; however, the results were no better than those seen with other chemotherapy combinations. The Oncologist 2005;10: Correspondence: Michael K. Gibson, M.D., The Sidney Kimmel Comprehensive Cancer Center at Johns Hopkins, Bunting- Blaustein Cancer Research Building, Room 345, 1650 Orleans Street, Baltimore, Maryland , USA. Telephone: ; Fax: ; gibsomi@jhmi.edu Received September 8, 2004; accepted for publication October 22, AlphaMed Press /2005/$12.00/0 The Oncologist 2005;10:
2 133 Chemotherapy for Small Bowel Carcinoma INTRODUCTION Small bowel adenocarcinoma is an uncommon neoplasm that remains difficult to cure. It comprises a small fraction of all gastrointestinal (GI) malignancies (~1%) with an annual incidence of approximately 3,000 cases. With complete surgical resection, only 20%-25% of patients are cured. Inadequately resected or recurrent disease is incurable, and most regimens of chemotherapy achieve low response rates with minimal prolongation of survival [1-3]. Given the rarity of this tumor, prospective evaluations of the efficacy of chemotherapy are rare, and most information is derived from descriptive studies that include retrospective analyses, case reports, and case series. Single and multiple agent regimens are empirically translated from experience with gastric and colorectal cancers. Previously tested regimens include 5-fluorouracil (5-FU) alone or in combination with doxorubicin (Adriamycin ; Bedford Laboratories; Bedford, OH), mitomycin C (Mutamycin ; Bristol-Myers Squibb; Princeton, NJ), cisplatin (Platinol ; Bristol-Myers Squibb), and carmustine (BCNU ; Bristol-Myers Squibb) [4]. One combination of these drugs, 5-FU, doxorubicin, and mitomycin C (the FAM regimen) demonstrated encouraging activity in gastric cancer [5]. Given the activity and safety of the FAM regimen for other GI malignancies as well as the need for better treatment of advanced small bowel adenocarcinoma, the Eastern Cooperative Oncology Group (ECOG) performed a phase II study of the FAM regimen in small bowel adenocarcinoma. MATERIALS AND METHODS Patient Selection Eligible patients required the following inclusion criteria: biopsy-proven, noncarcinoid adenocarcinoma of the small bowel (duodenum, jejunum, ileum, ampulla of Vater); disease incurable by surgery (R2 resection, recurrent or primary metastatic); measurable disease by computerized tomography scan or hepatomegaly; adequate time from prior therapy (2 weeks for biopsy, 3 weeks for surgery, 4 weeks for radiotherapy or chemotherapy); no prior treatment with the FAM regimen; adequate hematologic, liver, and renal functions; no active heart disease; and no concurrent malignancy (other than CIN or basal cell or squamous cell cancer of the skin). All patients provided appropriate informed consent at the participating institution. A total of 39 patients was enrolled, 38 were eligible and 36 were evaluable for response. Treatment Chemotherapy consisted of 5-FU, 600 mg/m 2 on days 1, 8, 29, and 36; mitomycin C, 10 mg/m 2 on day 1; and doxorubicin, 30 mg/m 2 on days 1 and 29. A cycle duration was 8 weeks. A single dose escalation of each drug by 10% was allowed if the patient met the following criteria during cycle 1: WBC nadir >4,000 cells/ml, platelet nadir >200,000 cells/ml, and hemoglobin nadir >10 g/dl. ECOG toxicity criteria were used to assess adverse reactions. Each drug was decreased by 25% for platelet nadirs of 25,001 50,000 and WBC nadirs of 1,001 2,000 and by 50% for platelet nadirs <25,000 and WBC nadirs <1,000. Additional dose modification included: an additional 10% reduction in mitomycin C for hemoglobin nadirs <10 g/dl; a 25% reduction in 5-FU and doxorubicin for stomatitis or severe diarrhea (>5 stools/day); and a 25% reduction in doxorubicin for total bilirubin >2 mg/dl. Doxorubicin was discontinued in the setting of cardiotoxicity. In order to receive a subsequent cycle of chemotherapy, the following hematologic values were required: WBC >3,000 cells/ml and platelet count >100,000 cells/ml. Treatment was continued until toxicity or progression of disease. Measurement of Effect A complete response (CR) was defined as the absence of any clinically detectable tumor mass. A partial response (PR) was defined as a 50% or greater reduction in the product of the longest perpendicular diameters of the most clearly measurable area of the primary indicator lesion. With hepatomegaly, a PR was defined as a >30 % decrease in the sum of the liver measurements below the xyphoid process and below each costal margin at the midclavicular lines. Other areas of malignant disease must not have increased, and no new disease must have appeared. ECOG performance status (PS) score must not have decreased and weight loss must not have exceeded 10% of the pretreament dry body weight. Disease progression was defined as a greater than 25% increase in the product of the longest perpendicular diameters of any measurable indicator lesion, a >25% increase in the sum of liver measurements, the appearance of new areas of tumor, any decrease in PS score, or weight loss >10%. Stable disease was defined as disease that was measurable but that did not fulfill any of the above criteria. Statistical Methods A confidence interval (CI) for the response rate was calculated with Atkinson and Brown s method for a two-stage phase II trial [6]. Probability estimates of survival time and time to progression were obtained from the Kaplan-Meier method [7]. The log-rank test identified differences in stratified survival curves.
3 Gibson, Holcroft, Kvols et al. 134 RESULTS Of 39 patients evaluated for enrollment, 38 were eligible and 36 were evaluable for response. Characteristics of all evaluated patients are listed in Table 1. Gender favored men, and most patients where Caucasian. In concordance with the epidemiology of small bowel adenocarcinoma, most tumors occurred in a proximal location, including 17 in the duodenum and four at the ampulla of Vater. PS scores varied from 0-2, and age ranged broadly from years. Treatment was somewhat toxic but generally tolerated. Adverse reactions are categorized in Table 2. As expected, the most common toxicity was hematologic, with one patient dying from grade 5 toxicity, most likely sepsis on day 15 of cycle 1 of chemotherapy. Five additional grade 4 hematologic toxicities were seen and included: fevers with WBC nadirs of 100, 500, 600, and 900 cells/ml on days 10, 12, 17, and 15 of cycle 1 of chemotherapy, respectively. A total of 26 patients experienced a severe or worse toxicity, with GI events making up most of the remainder. A range of mild and moderate toxicities were seen that included, primarily, vomiting, diarrhea, other GI symptoms, and alopecia. A total of 36 patients were evaluable for response, and these responses are listed in Table 3. Of the seven responses, two were CRs and five were PRs. Four patients achieved stable disease. The observed response rate (CR + PR) using all eligible patients (intention-to-treat analysis) was 18.4% (95% CI = 7.8% 34.4%). Survival time and time to progression were roughly similar. Survival was calculated as the number of days elapsed Table 2. Toxicity profile Table 1. Patient characteristics Characteristic Frequency Sex (n) Male 27 Female 11 Race (n) Caucasian 35 African American 2 Other 1 Location of primary (n) Duodenum 17 Jejunum 12 Ileum 5 Ampulla of Vater 4 ECOG PS score (n) Age (years) Minimum 38 Maximum 80 Median 63 between study entry and death. At the time of analysis, all 38 eligible patients were dead. The Kaplan-Meier survival curve is presented in Figure 1. Survival time stratified by clinical characteristics is presented in Table 4. The median survival time of all patients was 8 months, with 13% surviving for 2 years. Only PS score correlated with survival Toxicity Mild Moderate Severe Life threatening Lethal Vomiting Diarrhea Other GI 5 5 Infection 1 2 Bleeding Skin/mucous membrane 4 5 Neurologic 4 6 Respiratory 1 Genitourinary 5 1 Blood Liver Fever 1 Alopecia 8 5 Other * 3 1 Worse toxicity experienced * One case of grade 3 mouth soreness, agitation and edginess, and grade 1 alopecia; two cases of grade 2 fever and chills; one case of grade 2 alopecia and local toxicity.
4 135 Chemotherapy for Small Bowel Carcinoma Table 3. Response rates Status n (%) Complete response 2 (5%) Partial response 5 (13%) Stable disease 4 (11%) Disease progression 25 (66%) Not evaluable for response 2 (5%) (p = 0.02 by log-rank test), demonstrating worse outcome in patients with poorer PS scores. There was a nonsignificant trend toward worse survival for patients older than 65 years. In the time-to-progression analysis, the date of progression for most patients was defined as the relapse date or the date of death if relapse did not occur. The data listed in Table 5 include information for four patients for whom progression was not observed. One of these died while in PR of unrelated causes, one was stable at 3 months but then was censored when lost to additional follow-up, one was administratively removed from the study, and one died of unrelated causes and was censored at the date of death. The median time to progression of 5 months was only 3 months shorter than the median survival time. Only age demonstrated a trend toward significance as a predictor of time to progression. DISCUSSION At the time of initiation of this phase II, multi-institutional study, few treatment options for advanced small bowel Table 4. Overall survival stratified by clinical characteristics Probability Group All patients / / Months adenocarcinoma existed, and the overall experience with chemotherapy was limited. The MD Anderson experience with 14 patients treated between 1950 and 1980 provided perhaps the largest single aggregation of patients [4]. In that study, 21 chemotherapy regimens were given to patients with unresectable and recurrent disease. Objective tumor shrinkage occurred in three patients (response rate [RR] = 21.4%), all of whom received a combination that contained 5-FU. One responding patient received 5-FU, doxorubicin, and mitomycin C (the FAM regimen). The median survival time of all patients was 9 months. Similar results were documented by Ourial and Adams [8]. The current study prospectively evaluated the efficacy of FAM chemotherapy in 39 patients with advanced small 40 Time interval /6 3/4 (n events/n at risk) / /1 Figure 1. Kaplan-Meier survival analysis of overall survival plotted as the probability of surviving versus time from study entry. Characteristic n Median survival (months) 2-year survival (%) Log-rank test (p value) All patients Sex Male Female Race Caucasian African American Other Location Duodenum Jejunum Ileum Ampulla of Vater ECOG PS score Age <65 years years
5 Gibson, Holcroft, Kvols et al. 136 Table 5. Progression-free survival (PFS) stratified by clinical characteristics Characteristic n Median PFS (months) 1-year PFS (%) Log-rank test (p value) All patients Sex Male Female Race Caucasian African American Other Location Duodenum Jejunum Ileum Ampulla of Vater ECOG PS score Age <65 years years bowel adenocarcinoma. This largest single study to date of chemotherapy in this disease included a representative sample of patients, suggesting that the results can be generalized [9,10]. Toxicities were manageable, and accrual goals were reached; however, the studied combination did not achieve a response rate or survival duration greater than historical controls. As such, while this regimen has activity in small bowel adenocarcinoma, it does not represent an improvement over prior approaches and cannot be advocated for future study or general use. It does, however, document that small bowel adenocarcinomas are chemotherapy sensitive and are likely treatable with regimens defined for gastric adenocarcinomas. Tremendous progress in the treatment of advanced GI malignancies has occurred since this phase II study concluded. Although most experience is with colorectal, gastric, and esophageal cancers, additional reports of treatments for advanced small bowel adenocarcinoma do exist. Crowley et al. [11] reported the Royal Marsden experience of using infusional 5-FU as a single agent or in combination with cisplatin and epirubicin (Ellence ; Pharmacia and Upjohn; Portage, MI), the ECF regimen [10]. Of the eight patients assessable for response, one achieved a CR and two achieved PRs (RR = 37%), with a median overall survival time of 13 months. A more recent publication described the use of single-agent irinotecan (Camptosar ; Pfizer Pharmaceuticals; New York, NY) in three patients with advanced disease [12]. Two patients achieved PRs with palliation of symptoms. While treatments for advanced GI malignancies continue to advance, objectively evaluated chemotherapy options for small bowel adenocarcinoma remain limited. This lack of data will likely continue given the rarity of this disease. Until additional multi-institutional studies are done, it is likely that practitioners will continue to translate regimens developed for other upper GI malignancies for use in small bowel adenocarcinoma. REFERENCES 1 Chow JS, Chen CC, Ahsan H et al. A population-based study of the incidence of malignant small bowel tumours: SEER, Int J Epidemiol 1996;25: Kummar S, Ciesielski TE, Fogarasi MC. Management of small bowel adenocarcinoma. Oncology (Huntingt) 2002;16: ; discussion 1370, Neugut AI, Marvin MR, Rella VA et al. An overview of adenocarcinoma of the small intestine. Oncology (Huntingt) 1997;11: ; discussion 545, Jigyasu D, Bedikian AY, Stroehlein JR. Chemotherapy for primary adenocarcinoma of the small bowel. Cancer 1984;53: MacDonald JS, Woolley PV, Smythe T et al. 5-fluorouracil, adriamycin, and mitomycin-c (FAM) combination chemotherapy in the treatment of advanced gastric cancer. Cancer 1979;44: Atkinson EN, Brown BW. Confidence limits for probability of response in multistage Phase II clinical trials. Biometrics 1985;41:
6 137 Chemotherapy for Small Bowel Carcinoma 7 Kaplan E, Meier P. Nonparametric estimation from incomplete observations. J Am Stat Assoc 1958;53: Ouriel K, Adams JT. Adenocarcinoma of the small intestine. Am J Surg 1984;147: Talamonti MS, Goetz LH, Rao S et al. Primary cancers of the small bowel: analysis of prognostic factors and results of surgical management. Arch Surg 2002;137: ; discussion Severson RK, Schenk M, Gurney JG et al. Increasing incidence of adenocarcinomas and carcinoid tumors of the small intestine in adults. Cancer Epidemiol Biomarkers Prev 1996;5: Crawley C, Ross P, Norman A et al. The Royal Marsden experience of a small bowel adenocarcinoma treated with protracted venous infusion 5-fluorouracil. Br J Cancer 1998;78: Polyzos A, Kouraklis G, Giannopoulos A et al. Irinotecan as salvage chemotherapy for advanced small bowel adenocarcinoma: a series of three patients. J Chemother 2003;15:
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