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Preoperative Chemotherapy Followed by Surgery Compared With Primary Surgery in Resectable Stage I (Except T1N0), II, and IIIa Non–Small-Cell Lung Cancer

From the J Minjoz University Hospital, Besançon; Tenon University Hospital, Paris; St Louis University Hospital; St Antoine University Hospital; Hôtel Dieu Univesity Hospital; and Bichat University Hospital, Paris; Michalon University Hospital, Grenoble; University Hospital, Strasbourg; General Hospital, Briey; General Hospital, Belfort; Bretonneau University Hospital, Tours; A. Morvan University Hospital, Brest; General Hospital, Metz; University Hospital, Clermont-Ferrand; General Hospital, Le Mans; University Hospital, Dijon; Claude Bernard Clinic, Ermont; General Hospital, St-Brieuc; General Hospital, Verdun; General Hospital, St Germain-en-Laye; General Hospital, Meaux; Charles Nicolle University Hospital, Rouen; and Asta Medica, Mérignac, France.

Address reprint requests to A. Depierre, MD, Chest Disease Department, J. Minjoz University Hospital, 25030 Besançon Cedex, France; email: pneumo-depierre{at}ufc-chu.univ-fcomte.fr

	ABSTRACT

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION REFERENCES

 
PURPOSE: To evaluate whether preoperative chemotherapy (PCT) could improve survival in resectable stage I (except T1N0), II, and IIIA non–small-cell lung cancer (NSCLC).

PATIENTS AND METHODS: A randomized trial compared PCT to primary surgery (PRS). PCT consisted of two cycles of mitomycin (6 mg/m², day 1), ifosfamide (1.5 g/m², days 1 to 3) and cisplatin (30 mg/m², days 1 to 3), and two additional postoperative cycles for responding patients. In both arms, patients with pT3 or pN2 disease received thoracic radiotherapy.

RESULTS: Three hundred fifty-five eligible patients were randomized. Overall response to PCT was 64%. There were two preoperative toxic deaths. Postoperative mortality was 6.7% in the PCT arm and 4.5% in the PRS arm (P = .38). Median survival was 37 months (95% confidence interval [CI], 26.7 to 48.3) for PCT and 26.0 months (95% CI, 19.8 to 33.6) for PRS (P = .15). Survival differences between both arms increased from 3.8% (95% CI, 1.3% to 25.1%) at 1 year to 8.6% (95% CI, 2.64% to 24.4%) at 4 years. A quantitative interaction between N status and treatment was observed, with benefit confined to N0 to N1 disease (relative risk [RR], 0.68; 95% CI, 0.49 to 0.96; P = .027). After a nonsignificant excess of deaths during treatment, the effect of PCT was significantly favorable on survival (RR, 0.74; 95% CI, 0.56 to 0.99; P = .044). Disease-free survival time was significantly longer in the PCT arm (P = .033).

CONCLUSION: Although impressive differences in median, 3-year, and 4-year survival were observed, they were not statistically significant, except for stage I and II disease.

	INTRODUCTION

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION REFERENCES

 
LUNG CANCER IS the most frequent cancer in men in the United States and Europe.¹ Surgery remains the best therapy for cure in non–small-cell lung cancer (NSCLC).² The concept of preoperative chemotherapy (PCT) was born from the hypothesis that drug resistance appears as a result of genetic changes. Thus, the best efficacy of chemotherapy should be obtained with small tumor burdens.³ PCT, studied in more than 30 phase II studies, has proven to be feasible at the expense of mild postoperative morbidity and mortality, with higher response rates than in more advanced disease and an increase in median survival when compared with historical controls who only received surgery.⁴ In all these studies, only patients with stage IIIa tumors were included. Taking into account that the 5-year survival rate is approximately 50% in T2N0 tumors and less than 50% in stage II disease,⁵ we undertook in 1991 a multicenter randomized trial to compare PCT plus surgery with primary surgery (PRS) in stage I (except T1N0), II, and IIIa resectable NSCLC.

	PATIENTS AND METHODS

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION REFERENCES

 
Eligibility Criteria
Patients were eligible if they had a stage I (except for T1N0), II, or IIIa⁵ histologically proven NSCLC. They had to be 75 years old or less, have operable status, and have a World Health Organization performance status of 2 or less.⁶ Their tumor had to be judged resectable before any chemotherapy was administered. Patients could not have received any prior cancer treatment. This investigation was approved by the Human Investigations Committee of Besançon, France, and signed informed consent was obtained from all patients. Eligibility criteria were reviewed by an internal expert committee.

Preinclusion investigations consisted of chest x-ray, thoracic computed tomographic (CT) scan with sections on adrenal glands, fiberoptic bronchoscopy, CT scan or ultrasound of the liver, brain CT scan, blood cell count, serum creatinine, and bilirubin. Hilar and mediastinal nodes 1 cm or greater in size in their short axis diameter on CT scan were considered to be involved with the disease. Mediastinoscopy was permitted but not routinely performed.

Treatment
Patients were randomized to either undergo PRS or to receive two cycles of chemotherapy 3 weeks apart before surgery. Patients randomly assigned to PRS had to be operated on during the first week. In the PCT arm, surgery was planned during the seventh week. The extent of pulmonary resection was decided before randomization, and the surgeon was not permitted to perform a lesser procedure even if, after chemotherapy, the lesion was judged to be less extensive at thoracotomy. Mediastinal node dissection and node sampling were left to the discretion of the surgeon.

PCT consisted of mitomycin (6 mg/m² on day 1), ifosfamide (1.5 g/m² on days 1 to 3), and cisplatin (30 mg/m² on days 1 to 3). Mesna, standard hydration, and antiemetics were given. In patients with febrile neutropenia during cycle 1, an absolute granulocyte count lower than 0.5 x 10⁹/L on day 21, a platelet count lower than 75 x 10⁹/L on day 21, and/or evidence of progressive disease, the second cycle was not delivered, and surgery was performed earlier. Doses of mitomycin and ifosfamide were reduced by 50% for an absolute granulocyte count between 0.5 and 1 x 10⁹/L or a platelet count between 75 and 100 x 10⁹/L. In case of serum creatinine greater than or equal to 150 µmol/L, cisplatin was omitted. In patients with a clinical partial response or a pathologic complete response, two postoperative cycles were delivered on weeks 10 and 13.

In both arms, patients with a pT3 or pN2 disease and/or those who received incomplete surgery received thoracic radiotherapy 3 weeks after either surgery or postoperative chemotherapy by parallel opposed anterior and posterior fields. Patients received 40 Gy delivered in 2-Gy daily fractions 5 days per week. An additional dose of 20 Gy in 10 fractions was delivered on the T3 or N2 site by appropriate oblique fields.

Response
Before each cycle, a chest x-ray was performed, and progressive disease suspected on chest x-ray had to be confirmed by a thoracic CT scan. Response was assessed according to the World Health Organization criteria⁶ by chest CT scan and fiberoptic bronchoscopy before surgery and by pathologic analysis of surgical specimens.

Follow-Up
Follow-up procedures included physical examination and chest x-ray every 3 months and fiberoptic bronchoscopy and chest CT scan every 6 months for the first 2 years. From the third to the seventh years, follow-up consisted of a chest x-ray every 6 months and a fiberoptic bronchoscopy and chest CT scan every year.

Statistical Analysis
Primary end point was overall survival from randomization. Secondary end points were disease-free survival, response rate, and toxicity of PCT. The study was designed to test the hypothesis that the 2-year survival rate would be 45% in the PRS arm and 60% in the PCT arm. Assuming a one-sided test with a type I error rate of 0.05 and a power of 0.90, these survival rates would mean 174 deaths on study.

Randomization of patients was centralized, performed by phone, and stratified by center. Baseline comparisons of patients in both arms used the ² or the Fisher’s exact tests. Survival time was that elapsed from the date of randomization until death or November 1, 2000. Postoperative treatment deaths were defined as deaths by a complication that occurred during the 30 postoperative days, whatever the date of death. Disease-free survival was calculated from the date of randomization to the date of surgery for patients who did not have a complete resection to the date of recurrence for patients whose cancer recurred and to the date of death or to November 1, 2000, when no recurrence occurred, and death was considered an event. Overall and disease-free survival were estimated using the Kaplan-Meier method.⁷ Survival and disease-free survival were compared by the logrank test.⁸ A multivariate survival analysis was performed using a Cox proportional hazards model,⁹ checking for nonproportional hazards by plots of log (-log{S(t)}) against log(t), as well as estimates of instantaneous risk over time in both arms. Variables included in the model were those that were significant in the univariate analysis. As hazards were not proportional over time in the two arms, influence of PCT on survival was separately analyzed before and after the whole treatment termination (5 months) by including a time-dependent variable in the Cox model. Risks for locoregional and distant recurrence were estimated using the Cox model.

	RESULTS

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From June 1991 to July 1997, 373 patients were enrolled, 187 patients onto the PCT arm and 186 patients onto the PRS arm. Eight patients on the PCT arm and 10 on the PRS arm were found to be ineligible. Reasons for ineligibility included stage IV disease (two patients), T4 disease (six), N3 disease (two), missing consent (two), other histology (two), previous cancer (two), performance status more than 2 (one), and inoperability for a functional reason (one). Thus, a total of 179 patients in the PCT arm and 176 in the PRS arm remained in the analysis. However, a 12% (95% CI, 2.4% to 21.6%) excess of N2 disease was observed in the PCT group, but the difference was not statistically significant (P = .065). Main patient characteristics were close in the two treatment arms (Table 1).

Of the 337 PCT cycles performed, reported toxicity was as follows: grade 4 leukopenia in 21 cycles, grade 4 thrombocytopenia in 10 cycles, grade 3 to 4 nausea and vomiting in 20 cycles, and grade 3 alopecia in 26 patients. One case of pulmonary hypertension possibly caused by mitomycin was observed. Two toxic deaths were registered (one caused by massive hemoptysis and one caused by neutropenic sepsis).

Of the 179 eligible patients in the PCT arm, 171 were assessable for response. Eight were not assessable (five patient refusals of PCT and/or surgery, two toxic deaths, one death by intercurrent disease). Among the 179 eligible patients, 19 pathologic complete responses (11%) and 95 partial responses (53%) were observed, for an overall response rate of 64%. Progressive disease was observed in 10 cases. Sites of progression were locoregional in six cases and distant metastases in four (bone, cervical nodes, adrenal gland, and subcutaneous). Forty-seven patients (26.8%) achieved disease stabilization.

Surgery
Surgery was performed in 167 patients of the PCT arm, although 12 patients did not receive surgery because of metastatic progression (four patients), death (one by intercurrent disease, one by hemoptysis, one by neutropenic sepsis), mediastinal involvement at mediastinoscopy (one), patient refusal (three), and respiratory insufficiency (one) (Table 2). Among the 176 patients assigned to the PRS arm, 171 were operated on. Surgery was not performed in five patients because of immediate metastatic progression. Four patients had an exploratory thoracotomy in the PCT arm because of involvement of the right main bronchus (one patient), of the left atrium (one), of the pericardium (one), and of the aortic arch (one). Thoracotomy was exploratory in five patients of the PRS arm because of involvement of the pericardium and/or parietal pleura (two), bulky mediastinal involvement (one), involvement of the main pulmonary artery and of the aortic arch (one), and of the left atrium (one). Lobectomies or bilobectomies were performed in 144 cases, and pneumonectomies were performed in 185 cases. Numbers of lobectomies and pneumonectomies were not different between the two arms (P = .30). One hundred fifty-four patients (92%) underwent complete resection in the PCT arm, and 149 (86%) underwent complete resection in the PRS arm. Of the 296 data available, 120 patients had a complete lymph node dissection, and 121 underwent a systematic sampling (Table 3). No difference in mediastinal lymph node dissection was observed between the two arms. Pathologic N status was unknown in six patients: the five patients who did not undergo the operation and one patient lost to follow-up and operated on in a nonparticipating center. In the PRS arm, 92 (73%) of the 120 patients considered to have a cN0 or a cN1 disease were found to have a pN0 to pN1 tumor, and 28 (56%) of the 50 patients considered to have cN2 disease actually had pN2 (Table 4). The total number of treatment-related deaths after surgery was sixteen in the PCT arm and nine in the PRS arm, and the difference was not significant (P = .16). There was a nonsignificant excess of morbidity in the PCT arm during the 30 postoperative days (Table 5). Fistula and empyema were observed after pneumonectomy in eight cases and after lobectomy in seven cases.

Radiotherapy was delivered in 41 patients on the PCT arm and in 72 on the PRS arm. Pulmonary toxicity was infrequent, observed in only three patients (two on the PCT arm and one on the PRS arm). Indications for thoracic radiotherapy are detailed in Table 6.

View larger version (12K): [in this window] [in a new window]   Fig 1. Overall survival by treatment arm: arm A, PRS; arm B, PCT + surgery.

View larger version (18K): [in this window] [in a new window]   Fig 2. Overall survival by treatment arm and by nodal status.

Of the 303 patients whose disease has been completely resected, recurrence occurred in 56 patients of the PCT arm and in 75 patients in the PRS arm. After adjustment for stage, the RR of recurrence in the PCT arm was 0.74 (95% CI, 0.57 to 0.95; P = .001). Recurrences were distant in 25 patients on the PCT arm and in 42 on the PRS arm and both thoracic and distant in 10 patients from both groups. The risk of distant recurrence was significantly lower in the PCT arm (RR, 0.54; 95% CI, 0.33 to 0.88; P = .01). The risk of locoregional recurrence was not significantly different between the two arms, with a RR of locoregional recurrence of 0.83 (95% CI, 0.46 to 1.49; P = .52) Survival after recurrence was similar in the two arms, with a median at 6.2 months (95% CI, 3.5 to 8.3) in the PCT arm and 9.5 months (95% CI, 6.4 to 12.6) in the PRS arm (P = .12).

Second Cancers
At the reference date of November 1, 2000, 34 patients had developed a second cancer, 15 on the PCT arm and 19 on the PRS arm. The main involved sites were lungs (nine patients), head and neck (eight), and colon (four).

	DISCUSSION

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION REFERENCES

 
This trial demonstrates a delayed benefit of PCT on survival with a time-treatment interaction, as well as an interaction with stage, with a positive effect of PCT on survival in stage I and II NSCLC patients. There was a significant increase in disease-free survival in the PCT arm. A perioperative toxicity was responsible for a nonstatistically significant excess of deaths in the PCT arm. The absolute difference in survival increased from 1 to 4 years of follow-up. Beyond 4 years, the number of patients at risk decreased dramatically.

One hundred eighty-five patients (82%) underwent pneumonectomies. This high number of pneumonectomies can be explained by two facts: the absence of T1N0 tumors in the inclusion criteria, which account for the majority of lobectomies in surgical series and the proportion of stage IIIA disease that required pneumonectomy in most cases (especially in N2).^10-12

The postoperative lethal toxicity rate was 0% in the studies by Roth et al¹³ and Pass et al,¹⁴ 6.6% in the study by Rosell et al,¹⁵ and 7.8% in ours. The postoperative mortality rate of the present trial is similar to that reported in the numerous phase II studies published on PCT.¹⁶ The most frequently observed complications are empyemas and fistulae, which may be prevented by special surgical procedures. Minimizing treatment-related deaths is an important goal, and physicians should be careful with the choice of chemotherapy regimens in this setting of preoperative treatment. Nowadays, new chemotherapy regimens might be less toxic than the one we chose for this trial.^17,18

To our knowledge, the efficacy of PCT in early stages has never been evaluated in phase III trials. The lack of efficacy of PCT in stage IIIa disease observed in our study conflicts with the results of the three previously published phase III trials. The Rosell et al¹⁵ trial assigned 60 patients with stage IIIa disease to have surgery plus radiotherapy or preoperative chemotherapy, surgery, and radiotherapy. Drugs were the same ones used in our trial (mitomycin, ifosfamide, and cisplatin), but dosages were lower. Patients in the PCT arm had a significant gain in survival, which was stable at the analysis performed 7 years after enrollment.¹⁹ However, the small number of patients in each arm precludes any definitive conclusion.^20,21 Moreover, median survival of the control arm (8 months) was poor, comparable to that observed in stage IV disease treated with chemotherapy. Roth et al¹³ randomly assigned 60 patients with a stage IIIa disease to directly undergo surgery or to receive PCT before surgery. Chemotherapy consisted of cyclophosphamide, etoposide, and cisplatin. In this study, the response rate was low (35%). The gain in overall survival for the preoperative arm was significant, with a P value of less than .008. The long-term analysis²² of the study by Roth et al,¹³ with a median time of follow-up of 82 months, showed an important decrease in the survival difference between the two arms. In these two trials, early stopping rules were applied after interim analyses. The third trial, reported by Pass et al,¹⁴ also included a small number of patients and was only published as an interim analysis. Increased survival was observed in the PCT arm (median survival, 28.5 months v 15.6 months), but the difference was not statistically significant.

In our study, the lack of efficacy of PCT in stage IIIa patients may have been related to several factors. First, the results are usually less favorable in studies that include a larger number of patients. Second, efficacy of chemotherapy might be poorer in bulky disease than in earlier stages. In stage IIIa disease, local recurrences seem to arrive as soon as distant metastases. PCT may be mainly active on micrometastases and not on locoregional lymphatic spread. This was already shown in a trial that compared induction chemotherapy followed by radiotherapy to radiotherapy alone in stage III NSCLC, in which chemotherapy decreased the probability of metastatic occurrence without any effect on locoregional control.²³

In conclusion, this large phase III trial focuses on the interest of chemotherapy in the preoperative setting. The evolution of survival curves over time suggests that the results might become more demonstrative in favor of PCT as the number of patients at risk increases. Preoperative chemotherapy seems to be more beneficial in early stages than in stage IIIA NSCLC. This assertion, based on a subset analysis, needs to be confirmed by the other phase III studies, which are ongoing in various countries. Therefore, testing of new strategies in the future should separately study stage I to II and stage IIIA NSCLC, with possible evaluation of chemotherapy and radiation therapy before surgery in stage IIIA because of the high risk of local and distant recurrence, continuing to evaluate various perioperative chemotherapy schedules in stages I and II, and minimizing treatment-related toxicity.

APPENDIX
The following investigators participated in this study: Gilles Adam, MD, General Hospital, Bourges; Thierry Beyssens, MD, General Hospital, Saintes; François Blanchon, MD, General Hospital, Meaux; Bonnefoy, MD, General Hospital, Jonzac; Denis Braun, MD, General Hospital, Briey; Jeanne Marie Bréchot, MD, Hôtel-Dieu University Hospital, Paris; Jean-Luc Breton, MD, General Hospital, Belfort; Daniel Coëtmeur, MD, General Hospital, Saint-Brieux; Bruno Coudert, MD, Anti-Cancer Center, Dijon; Philippe David, MD, General Hospital, Elbeuf; Didier Debieuvre, MD, General Hospital, Vesoul; Alain Depierre, MD, University Hospital, Besançon; Michel Desjobert, MD, General Hospital, Laval; Pascal Foucher, MD, University Hospital, Dijon; Michel Grivaux, MD, General Hospital, Meaux; Sylvie Gouva, MD, University Hospital, Brest; Jean-Pierre Gury, MD, General Hospital, Vesoul; Bernard Hamel, MD, General Hospital, Orléans; Henri Janicot, MD, University Hospital, Clermont-Ferrand; Eric Kelkel, MD, General Hospital, Chambéry; Jean Lahourcade, MD, General Hospital, Pontarlier; François-Xavier Lebas, MD, General Hospital, Le Mans; Bernard Lebeau, MD, Saint-Antoine University Hospital, Paris; Pascal Leclerc, MD, General Hospital, Sartrouville; Etienne Lemarié, MD, University Hospital, Tours; Hervé Léna, MD, University Hospital, Rennes; Marie-Christine Level, MD, General Hospital, Verdun; Pascal-André Maignan, MD, General Hospital, Boulogne sur Mer; Yves Martinet, MD, University Hospital, Nancy; Bernard Milleron, MD, Tenon University Hospital, Paris; Michel Montchâtre, MD, General Hospital, Ermont; Denis Moro-Sibilot, MD, University Hospital, Grenoble; Nadine Paillot, MD, General Hospital, Metz; Dominique Paillotin, MD, University Hospital, Rouen; Marie-Lise Paquin, MD, General Hospital, Pontarlier; Elisabeth Quoix, MD, University Hospital, Strasbourg; Véronique Reboulet, MD, General Hospital, Dole; Jean-Michel Rodier, MD, Bichat University Hospital, Paris; Vincent Tack, MD, General Hospital, Calais; Philippe Terrioux, MD, Meaux; Luc Thiberville, MD, University Hospital, Rouen; Eric Watrigant, MD, General Hospital, Tourcoing; Virginie Westeel, MD, University Hospital, Besançon; Gérard Zalcman, MD, Curie Anti-Cancer Institute, Paris; and Jean-Marc Zipper, MD, General Hospital, Mulhouse, France.

	ACKNOWLEDGMENTS

 
Supported in part by grant no. 542 from Asta Medica, Mérignac, France.

We thank B. Depierre for her technical collaboration.

	NOTES

 
Presented in part at the Thirty-Fifth Annual Meeting of the American Society of Clinical Oncology, Atlanta, GA, May 15-18, 1999.

	REFERENCES

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Submitted August 17, 2000; accepted August 24, 2001.

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