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Journal of Clinical Oncology, Vol 19, Issue 5 (March), 2001: 1320-1325
© 2001 American Society for Clinical Oncology

Phase II Trial of Paclitaxel and Carboplatin in Metastatic Small-Cell Lung Cancer: A Groupe Français de Pneumo-Cancérologie Study

By P. Thomas, O. Castelnau, D. Paillotin, H. Léna, G. Robinet, J. F. Muir, P. Delaval, S. Gouva, P. Balmes, F. Blanchon, D. Perdu, R. Poirier, P. Pommier de Santi, C. Penot-Ragon, J. P. Kleisbauer

From the Service d’Oncologie Respiratoire and Pharmacie, Hôpital Sainte-Marguerite, Marseille; Service d’Oncologie Thoracique, Hôpital Morvan, Brest; and Services de Pneumologie, Hôpital Bois-Guillaume, Bois Guillaume, Hôpital de Pontchaillou, Rennes, Hôpital Gaston Doumergues, Nîmes, Hôpital Saint-Faron, Meaux, Hôpital Maison Blanche, Reims, Centre Hospitalier Général, Aix en Provence, and Centre Hospitalier Général, La Seyne sur Mer, France.

Address reprint requests to Thomas Pascal, MD, Service d’Oncologie Respiratoire, Département des Maladies Respiratoires, Hôpital Ste-Marguerite, 270 Bd Ste-Marguerite, 13 009 Marseille, France; email: pnthomas{at}ap-hm.fr


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
PURPOSE: To evaluate the efficacy and safety of paclitaxel and carboplatin in the treatment of previously untreated patients with metastatic small-cell lung cancer (SCLC).

PATIENTS AND METHODS: Eligible patients were aged 18 to 75 years with an Eastern Cooperative Oncology Group (ECOG) score <= 2 and life expectancy >= 12 weeks. Paclitaxel (200 mg/m2) was infused over 3 hours, before carboplatin (area under the curve [AUC] 6; Calvert formula) infused over 1 hour, once every 3 weeks for six cycles maximum. Prednisolone, dexchlorpheniramine, and ranitidine were standard premedication. Response to treatment was assessed every two cycles, and nonresponding patients were withdrawn from the trial to receive standard chemotherapy.

RESULTS: Of the 50 patients entering the study, 48 and 46 patients were assessable for toxicity and response, respectively. The overall response rate was 65%, with complete responses in three patients. Five patients had stable disease (11%) and 11 patients experienced progressive disease (24%). Median survival was 38 weeks, and median duration of response was 20 weeks. One-year survival was 22.5%. For a total of 232 cycles, grade 3 and 4 toxicity was 33% for neutropenia, 3.5% for thrombocytopenia, and 4% for anemia. Four patients had neutropenic fever (one toxic death). Nonhematologic toxicity was mainly grade 1 and 2 paresthesia (21% of patients); grade 3 myalgia/arthralgia was observed in 6.5% of patients.

CONCLUSION: First-line chemotherapy with paclitaxel and carboplatin in metastatic SCLC achieved a response rate and survival similar to standard regimens. With 1-day administration and a tolerable toxicity profile, this combination merits further investigation.


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
DESPITE THE efficacy of various chemotherapy regimens against small-cell lung cancer (SCLC), in terms of response, the survival of patients with extensive disease remains poor. With standard first-line treatments, such as platinum and etoposide or cyclophosphamide, doxorubicin, and etoposide (CDE), objective response rates of 60% to 80% are observed in extensive SCLC, with a median survival generally ranging from 7 to 10 months.1,2

In previous phase II studies, paclitaxel as single-agent therapy has demonstrated activity against extensive SCLC. As first-line treatment, a 24-hour infusion of paclitaxel 250 mg/m2 with granulocyte colony-stimulating factor (G-CSF) support produced response rates of 34%3 and 68%.4 Similar results were obtained with shorter infusions, over 3 hours, and were more convenient and induced less toxicity.5 At the time we initiated this study, the combination of carboplatin and paclitaxel had been tested in several phase II trials concerning non–small-cell lung cancer (NSCLC), and the feasibility of this treatment was well known. Various regimens were tested, and we selected that used in two of these studies, involving a short infusion (over 1 to 3 hours) of paclitaxel 175 to 225 mg/m2 and carboplatin area under the concentration-time curve (AUC) 6.6,7 Recently, the efficacy and favorable toxicity profile of this schedule in the treatment of NSCLC was confirmed in a large randomized study.8 After these various trials, we decided to investigate the efficacy and toxicity of the paclitaxel and carboplatin combination as first-line treatment in metastatic SCLC. Since this combination had never before been tested in that situation, an adaptation of the design of the Eastern Cooperative Oncology Group (ECOG) trial9 for testing new drugs in untreated patients with extensive SCLC was used: evaluation of response to therapy before every cycle by chest radiography, with measurement of all targets every two cycles, and, in the absence of response, administration of a standard salvage chemotherapy.


   PATIENTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Eligibility
This multicenter phase II study was initiated in February 1997. Eligible patients were between 18 and 75 years of age, had an ECOG performance status of <= 2 and a life expectancy of >= 12 weeks, and were required to have histologically or cytologically proven SCLC, never treated. Patients had to have metastatic disease; asymptomatic brain metastases were allowed. The following laboratory values were required: WBC count of >= 4 x 109/L, with neutrophils >= 2 x 109/L, platelets >= 150 x 109/L , hemoglobin >= 10 g/dL, total bilirubin <= 1.25 times the upper limit of the institutional normal range, and creatinine concentration 180 µmol/L or less.

In addition, patients were required to have at least one bidimensionally measurable target lesion, >= 2 x 2 cm on computed tomographic (CT) scan. Bone metastases and pleural or peritoneal effusions were not considered to be measurable lesions. Patients were excluded from the trial for any of the following reasons: active uncontrolled infection or fever greater than 38.3°C, unstable coronary cardiac disease, psychiatric disorders, previous malignant disease (except in situ carcinoma of the cervix or adequately treated basal or squamous cell carcinoma of the skin), or brain metastasis as the sole metastatic site. All patients were required to provide written informed consent, and the protocol was approved by the institutional ethics committee.

Pretreatment and Follow-Up Evaluations
Before enrollment, a full medical history was taken and patients underwent a physical examination, with assessment of performance status. Laboratory investigations included complete blood count (CBC) and differential blood count, and assays of electrolytes, glucose, calcium, albumin, transaminases, alkaline phosphatases, total bilirubin, and creatinine. An ECG was also recorded. A chest radiograph, bronchoscopy, CT scan of the chest and the head, abdominal CT scan or ultrasonography, and bone scintigraphy had to be obtained within the month preceding entry into the study. Bone marrow biopsy was not mandatory. A panel of pathologists reviewed all biopsy or cytology material for confirmation of the cytohistologic diagnosis.

Throughout the study, all patients had weekly CBCs. Before drug administration, every 21 days, patients were reviewed for cancer-related symptoms and treatment-related toxicities and underwent a clinical examination. On these occasions, all laboratory tests were also repeated, as were the chest radiograph and ECG. Toxicity was graded according to standard World Health Organization (WHO) criteria. Responses were assessed after two, four, and six cycles, according to WHO criteria.10 The imaging tests were performed in the week preceding the third and the fifth cycles and 1 month after the sixth cycle, and could also be repeated at any other time if clinically indicated, for example, to confirm a clinical or radiologic progression. Patients with no objective response after two cycles of chemotherapy were withdrawn from the trial, and a new treatment could be given at the discretion of the investigator. At any time, patients with progressive disease were also withdrawn, and received a salvage therapy. For all patients, the results of the imaging tests were reviewed by a panel, for staging and response evaluation. Follow-up visits were conducted every month.

Treatment Program
Paclitaxel 200 mg/m2 dissolved in 500 mL of 0.9% saline was first administered intravenously (IV) over 3 hours. Then, 125 mL of 0.9% saline was given to wash the vein, and carboplatin dissolved in 500 mL of 0.9% saline was infused IV over 1 hour. Carboplatin (Paraplatin, Bristol-Myers Squibb, Puteaux, France) was given at a dose designed to give an AUC of 6 mg/mL/min, using the formula developed by Calvert et al11: dose = target - AUC x (GFR + 25), where GFR is the glomerular filtration rate. The GFR was calculated using the formula of Cockcroft and Gault.12 Before every cycle, patients were premedicated with prednisolone 60 mg orally on the evening before the day of chemotherapy and on the morning of that day. Thirty minutes before the start of paclitaxel infusion, dexchlorpheniramine 5 mg and ranitidine 50 mg were given IV. The antiemetic regimen was at the discretion of each investigator.

Both drugs were given every 3 weeks, with a maximum of six cycles. At day 21, if neutrophils were <= 1,500 x 109/L or platelets were <= 100 x 109/L, chemotherapy was delayed until recovery, with a maximum delay of 2 weeks. If patients had not recovered by this time, they were withdrawn from the study on the grounds of hematologic toxicity. The dose of paclitaxel was reduced by 25 mg/m2 in the event of grade 4 neutropenia for more than 7 days, febrile neutropenia, grade 4 anemia, or grade 2 peripheral neuropathy. The carboplatin AUC target was lowered from 6 mg/mL/min to 5 mg/mL/min in the event of grade 4 thrombocytopenia or any grade of thrombocytopenia with clinical bleeding, and for grade 2 peripheral neuropathy.

Radiotherapy as supportive care was administered if it did not interfere with measurable disease or marrow reserve. Growth factors were not used as prophylaxis, but could be used with curative intent in the event of febrile neutropenia.

Statistical Analysis
The sample size was calculated to detect a response rate of 30% ± 15% with an alpha = 0.05. Standard WHO response criteria were used. Response duration was measured from the time response was first documented to the time progression was documented. All patients were assessable for toxicity. Response was considered assessable only for patients who received at least one course of chemotherapy.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Demographics
A total of 50 patients from nine institutions were entered onto this study, from February 1997 to November 1998. Forty-eight patients were assessable for toxicity, one patient experienced medullar chord compression before the first cycle of chemotherapy, and one patient was lost to follow-up after the first cycle. Response was assessed for 46 patients, excluding four ineligible patients (one with symptomatic brain metastasis, two with the brain as sole metastatic site, and one with medullar chord compression before treatment). The characteristics of the patients are listed in Table 1.


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  		Table 1. Patients and Disease Characteristics
 
Drug Delivery
A total of 232 cycles were administered. Twenty-six patients received the total of six courses. Details of the number of courses and doses of carboplatin and paclitaxel administered are given in Table 2.


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  		Table 2. Number of Cycles and Drug Delivery (eligible patients)
 
Secondary to hematologic toxicity, delays in chemotherapy were observed for seven patients: a 1-week delay for six of these, and one patient with two cycles delayed by 2 weeks. One patient was withdrawn from the study because the hematologic toxicity failed to resolve within 2 weeks. No dose reduction secondary to high-grade hematologic toxicity or neuropathy was needed, so all the patients received 100% of the planned dose of carboplatin or paclitaxel.

Response
Among the 46 patients assessable for response, there were three complete responses and 27 partial responses, giving an overall response rate of 65% (95% confidence interval [CI], 51% to 80%). The objective response rates as a function of different prognostic factors (PS, organ involved by metastasis, weight loss) were not significantly different ({chi}2 test) ( Table 3). Five patients experienced disease stabilization (11%), including two patients with no change after two cycles of chemotherapy and three patients with a nonconfirmed partial response after two cycles. Eleven patients were considered to have progressive disease (24%), including two patients with early progression before the second course of chemotherapy (clinical and radiologic progression on chest radiograph); one patient decided to stop treatment after the first chemotherapy course; four patients were in progression on the basis of imaging results after two or three cycles of chemotherapy; and four partial responders after two cycles were in progression after four or five cycles (Table 2).


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  		Table 3. Response Rate
 
With the exception of the patient who decided to stop the treatment after the first course, all the patients with progressive disease or stabilization received other chemotherapy. None of these patients received radiotherapy for "supportive care only."

The median survival was 38 weeks (range, 1 to 90 weeks) ( Fig 1). The 1-year survival rate was 22.5% (95% CI, 11% to 37%). The median duration of response (WHO criteria10) was 20 weeks (range, 4 to 73 weeks) ( Fig 2).



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  		Fig 1. Kaplan-Meier overall survival curve.

 


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  		Fig 2. Kaplan-Meier duration-of-response curve.

 
Toxicity
The major toxicity was hematologic ( Table 4), with neutropenia WHO grade 3 or 4 observed in 33% of the 232 cycles. Thrombocytopenia grade 3 was observed in 3% of cycles, one grade 4 (0.5% of cycles) was observed, and platelet transfusions were never used. Four patients presented febrile neutropenia, in one of whom it was fatal.


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  		Table 4. Hematologic Toxicity for all Cycles (n = 232)
 
Nonhematologic toxicity ( Table 5) consisted mainly of transient alopecia, and low-grade (1 and 2) peripheral neuropathy in 21% of the patients. Severe myalgia and arthralgia (grade 3) were observed in 6.5% of the patients, as early as the first cycle in two patients. These adverse effects were only partially improved by prolonged corticosteroid and analgesic therapy and, despite objective response, the treatment was stopped after two and three cycles of chemotherapy, respectively. In one patient, also a responder, grade 3 myalgia was observed only after five cycles of treatment, without any pain before. As a result of this toxicity, the sixth cycle of chemotherapy was not administered.


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  		Table 5. Nonhematologic Toxicity for 48 Patients
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
With an objective response rate of 65% among patients with metastatic SCLC, and a median survival of 9.5 months, the combination of carboplatin AUC 6 and paclitaxel 200 mg/m2 infused over 3 hours seems to be as effective as the standard regimens. All the patients had metastatic disease, a subgroup of extensive disease13 with the worst prognosis. With repeated evaluations every two cycles, and administration of standard chemotherapy in the absence of response, the results obtained using this new combination are similar to those achieved by conventional treatment.

In several studies reported by cooperative groups, the median survival for extensive SCLC ranged from 7 to 10 months with classic chemotherapy, such as cisplatin and etoposide or cyclophosphamide, doxorubicin, and vincristine.1,14 Median survival was not increased by alternating these regimens with non–cross-resistant drugs, or high-dose chemotherapy. Two recent studies of the paclitaxel and carboplatin combination as first-line treatment of SCLC gave similar results. For Deppermann et al,15 using paclitaxel 200 mg/m2 and carboplatin AUC 6 every 3 weeks, the objective response rate was 64% among 75 patients with extensive SCLC, with a median survival of 53 weeks and a 51% 1-year survival rate. According to the staging system described by Wolf and Havemann13 used in this trial, the response rate was 61% for the 48 patients with distant metastases. Zarogoulidis et al,16 using a 28-day regimen combining paclitaxel 175 mg/m2 and carboplatin AUC 6, obtained an objective response rate of 57.7% in 78 patients with SCLC. The median survival time was 10.4 months for the 52 patients with extensive disease.

According to Hainsworth et al,17 adding paclitaxel at full dose (135 mg/m2 then 200 mg/m2) to a derivative of a standard regimen, carboplatin (AUC 5 then 6) and oral etoposide, the median survival among the 32 patients with extensive SCLC reached 10 months, with an overall response rate of 84%. With this regimen, the hematologic toxicities were substantial; grade 3 or 4 leukopenia was observed in 71% of the patients (38% of the cycles) and high-grade thrombocytopenia in 8% (3.5% of the cycles). This was considered to be a tolerable toxicity profile, so the efficacy of this three-drug regimen led to a randomized trial versus a standard carboplatin and IV etoposide regimen.

As second-line treatment, the paclitaxel and carboplatin combination is also effective. This was evaluated in the treatment of SCLC patients resistant to CDE.18 The regimen used was carboplatin AUC 7 and paclitaxel 175 mg/m2 (3-hour infusion). The toxicity was mainly hematologic, but tolerable for these pretreated patients. Among 34 patients, of whom 16 presented initially with limited disease, the objective response rate was 73.5%, with a median survival of 31 weeks. This response rate is unusually high for a second-line treatment in resistant SCLC, permitting the conclusion that CDE and paclitaxel and carboplatin are non–cross-resistant regimens.

In our study, as in the trial reported by Deppermann,15 using the same dose of cytostatics, hematologic toxicity of this carboplatin-paclitaxel regimen without G-CSF was frequently observed, but tolerable. Febrile neutropenia was seen in four patients only. Delays in chemotherapy administration were observed for 15% of 48 patients, with only one patient withdrawn from the study because of lasting grade 2 neutropenia, six weeks after the second cycle. With a 3-hour paclitaxel infusion, only grade 1 and 2 peripheral neuropathy were observed in 21% of the patients. This is consistent with previous studies.

As the demarcation line between limited and extensive disease is sometimes unclear, depending on local practices, the inclusion of only metastatic disease gives a more homogeneous population, but one with the worst prognosis for never-treated SCLC. For this population, the efficacy and toxicity profile of the paclitaxel and carboplatin combination seems promising. This chemotherapy can easily be administered during a single day, on an outpatient basis, in contrast to the standard regimen with IV etoposide, imposing 3 days of treatment. This reduction in treatment duration counterbalances the high cost of paclitaxel. Considering the results achieved by the carboplatin and paclitaxel combination as first-line treatment in SCLC, a randomized study comparing this combination to standard regimens would be useful, with quality-of-life and cost-effectiveness evaluations. In view of the conclusions of Groen and al,18 demonstrating that CDE and paclitaxel and carboplatin are not cross-resistant, it might also be interesting to study the efficacy of a regimen alternating these two combinations.


   ACKNOWLEDGMENTS
 
We thank Bristol-Myers Squibb France for supplying paclitaxel for this trial.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
1. Roth BJ, Johnson DH, Einhorn LH, et al: Randomized study of cyclophosphamide, doxorubicin, and vincristine versus etoposide and cisplatin versus alternation of these two regimens in extensive small-cell lung cancer: A phase III trial of the Southeastern Cancer Study Group. J Clin Oncol 10: 282-291, 1992[Abstract]

2. Fukuoka M, Furuse K, Saijo N, et al: Randomized trial of cyclophosphamide, doxorubicin and vincristine versus cisplatin and etoposide versus alternation of these regimens in small cell lung cancer. J Natl Cancer Inst 83: 855-861, 1991[Abstract/Free Full Text]

3. Ettinger DS, Finkelstein DM, Sarma RP, et al: Phase II study of paclitaxel in patients with extensive-disease small-cell lung cancer: An Eastern Cooperative Oncology Group study. J Clin Oncol 13: 1430-1435, 1995[Abstract]

4. Kirschling RJ, Jung SH, Jett JR, et al: A phase II trial of Taxol and G-CSF in previously untreated patients with extensive-stage small-cell lung cancer. Proc Am Soc Clin Oncol 13: 326a, 1994 (abstr 1076)

5. Bunn PA: Defining the role of paclitaxel in lung cancer: Summary of recent studies and implications for future directions. Semin Oncol 24: 153-162, 1997 (suppl 12)[Medline]

6. Hainsworth JD, Thompson DS, Urba WJ, et al: One hour paclitaxel plus carboplatin in advanced non-small cell lung cancer (NSCLC): Preliminary results of a multi-institutional phase II study. Proc Am Soc Clin Oncol 15: 379a, 1996 (abstr 1131)

7. Vafai D, Israel V, Zaretsky S, et al: Phase I/II trial of combination carboplatin and Taxol in non-small cell lung cancer (NSCLC). Proc Am Soc Clin Oncol 14: 352a, 1995 (abstr 1067)

8. Kelly K, Crowley J, Bunn PA, et al: Randomized phase III trial of paclitaxel plus carboplatin (PC) versus vinorelbine plus cisplatin (VC) in untreated non-small cell lung cancer (NSCLC): A Southwest Oncology Group (SWOG) trial. Proc Am Soc Clin Oncol 18: 461a, 1999 (abstr 1777)

9. Ettinger DS, Finkelstein DM, Abeloff MD, et al: Justification for evaluating new anticancer drugs in selected untreated patients with extensive-stage small cell lung cancer. An Eastern Cooperative Oncology Group study. J Natl Cancer Inst 84: 1077-1084, 1992[Abstract/Free Full Text]

10. Miller AB, Hoogstraten B, Staquet M, et al: Reporting results of cancer treatment. Cancer 47: 207-214, 1981[Medline]

11. Calvert AH, Newell DR, Gumbrell LA, et al: Carboplatin dosage: Prospective evaluation of a simple formula based on renal function. J Clin Oncol 7: 1748-1756, 1989[Abstract]

12. Cockcroft DW, Gault MH: Prediction of creatinine clearance from serum creatinine. Nephron 16: 31-41, 1976[Medline]

13. Wolf K, Havemann K: Chemotherapy and combined chemotherapy procedures in bronchial carcinoma. Internist 35: 740-750, 1994[Medline]

14. Ihde DC, Mulshine JL, Kramer BS, et al: Prospective randomized comparison of high-dose and standard-dose etoposide and cisplatin chemotherapy in patients with extensive-stage small cell lung cancer. J Clin Oncol 12: 2022-2034, 1996[Abstract/Free Full Text]

15. Deppermann KM, Serke M, Oehm C, et al: Paclitaxel and carboplatin in advanced SCLC: A phase II study. Proc Am Soc Clin Oncol 18: 482a, 1999 (abstr 1860)

16. Zarogoulidis K, Kontiakiotis T, Hatziapostoulou P, et al: Pacli- taxel (P) in combination with carboplatin (C) in the treatment of SCLC patients (a phase II study). Lung Cancer 29: 53, 2000 (suppl 1, abstr 171)

17. Hainsworth JD, Gray JR, Stroup SL, et al: Paclitaxel, carboplatin, and extended-schedule etoposide in the treatment of small-cell lung cancer: Comparison of sequential phase II trials using different dose-intensities. J Clin Oncol 15: 3464-3470, 1997[Abstract/Free Full Text]

18. Groen HJM, Fokkema E, Biesma B, et al: Paclitaxel and carboplatin in the treatment of small-cell lung cancer patients resistant to cyclophosphamide, doxorubicin, and etoposide: A non-cross-resistant schedule. J Clin Oncol 17: 927-932, 1999.[Abstract/Free Full Text]

Submitted July 31, 2000; accepted November 14, 2000.


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