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a Department of Thoracic Surgery, Hôtel Dieu Hospital, AP-HP, Paris, France
c Department of Pathology, Hôtel Dieu Hospital, AP-HP, Paris, France
b JE2492 Institut National de la Santé et de Recherche Médicale (INSERM), University Paris-Sud, Paris, France
d Faculty of Medicine Paris-Descartes, Paris, France
Accepted for publication January 17, 2008.
* Address correspondence to Dr Alifano, Unité de Chirurgie Thoracique, Hôtel Dieu, 1, Place du parvis Notre-Dame, Paris, Cedex 75181, France (Email: marcoalifano{at}yahoo.com).
Presented at the Forty-fourth Annual Meeting of The Society of Thoracic Surgeons, Fort Lauderdale, FL, Jan 28–30, 2008.
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Abstract |
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Methods: Records of patients who underwent pneumonectomy after chemotherapy for non-small cell lung cancer in a single institution in a 6-year period were reviewed retrospectively.
Results: One hundred eighteen patients had pneumonectomy after chemotherapy. Indications for preoperative chemotherapy were N2 disease, 74; potentially resectable T4 disease, 17; doubtful resectability, 18; stage IV disease (nodule on another ipsilateral lobe), 4; and participation in a randomized trial on induction chemotherapy in initial stages, 5. Chemotherapy protocols were platinum-based. Imaging reevaluation showed complete, partial, minor response, and disease stability in 0, 24, 39, and 55 patients, respectively. Operative mortality was 5.9% (7 of 118), consisting of 4 of 54 after pneumonectomy, and 3 of 64 after left pneumonectomy. Bronchopleural fistula caused one death. No factor among those evaluated (sex, age, comorbidities, forced expiratory volume in 1 second, symptoms, side and location of tumor; indication for operation, number of cycles, and response to chemotherapy; extent of resection, TNM status, pathologic stage) predicted postoperative death. Median and overall 5-year survival was 22 months and 23.7%, respectively. At univariate analysis, pathologic stage, T status, and the occurrence of postoperative complications influenced 5-year survival. At multivariate analysis, T status (p = 0.0054), the occurrence of postoperative complications (p = 0.0015), and clinical response to induction chemotherapy (p = 0.028) were identified as independent predictors of 5-year survival.
Conclusions: Pneumonectomy after chemotherapy has acceptable mortality. Long-term results are encouraging.
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Introduction |
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Neoadjuvant chemotherapy has the theoretic advantage of possible administration to a larger number of candidates because a significant percentage of patients are not sufficiently fit to tolerate chemotherapy after surgical intervention, especially those who have a complicated postoperative course. Furthermore, it has been hypothesized that induction chemotherapy could be more effective than postoperative chemotherapy because of earlier action on possible infraclinic metastatic disease [4, 7]. Finally, some reports underline the possibility of resection after chemotherapy of disease previously considered too locally advanced to be resectable [8].
The morbidity and mortality of surgical intervention after induction chemotherapy are largely variable according to different authors' experiences; with respect to pneumonectomy, some authors reported quite acceptable results [9, 10]. According to others, however, the figures were excessively high [11, 12], especially after right-side procedures, and the question of considering whether this operation is acceptable has been raised [7]. On the other hand, results on long-term survival of pneumonectomy after neoadjuvant chemotherapy are relatively scarce. Hence, we undertook a retrospective review of our experience with 118 patients treated by pneumonectomy after chemotherapy to study morbidity, mortality, and long-term survival.
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Material and Methods |
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We retrospectively reviewed the clinical records of all the patients who underwent pneumonectomy after induction chemotherapy for NSCLC in a 6-year period in our institution (between November 2000, when our surgical team moved to the Hôtel-Dieu Hospital, Paris, France, and May 2006). For all the patients, preoperative evaluation included clinical history, physical examination, routine blood tests, electrocardiography, lung function tests, and perfusion lung scan.
The lung cancer staging protocol included chest roentgenogram, fiberoptic bronchoscopy, and thoracic, upper abdominal, and cerebral computed tomography (CT) scan. Isotopic bone scan was performed in the presence of bone pain or abnormalities in serum calcium or alkaline phosphatase. Almost all the patients with clinical suspicion of N2 disease (short axis <1 cm) underwent mediastinal staging by either transbronchial needle aspiration or by mediastinoscopy/anterior mediastinotomy. In rare cases the disease was staged N2 on the basis of CT and positron emission tomography (PET) scan without histologic confirmation because of the presence of bulky homolateral lymph nodes. After completion of chemotherapy, a complete restaging was performed, including thoracic, upper abdominal and cerebral CT scan, whereas redo mediastinoscopy was never used.
Clinical response to chemotherapy was defined as suggested by Roth and colleagues [3]:
Disease was considered stable if the variation in the sum of the products of two diameters of disease was between –25% and +25%. Beyond the latter threshold, disease was considered progressive and surgical intervention was denied.
Resection was considered functionally possible if the predictive postoperative forced expiratory volume in 1 second (FEV1), calculated on the basis of spirometry and isotopic scan, was 40% or greater of predicted FEV1 and provided that no major hypoxemia (<60 mm Hg) or hypercapnia (> 46 mm Hg) existed, whereas it was contraindicated if the predicted postoperative FEV1 was 30% or less. Patients with FEV1 values between 30% and 40% were considered at relatively high risk, and a definitive decision was based on an evaluation that included predictive postoperative FEV1, PO 2, PCO 2, age, associated comorbidities, and results of exercise tests (stair climbing and 6-minute walking).
Pneumonectomy was decided only if more economic resections (including sleeve lobectomies) were not adequate in dealing radically with the disease. Furthermore, in the presence of a nodule in another lobe accompanying the primary tumor, our general policy was lobectomy and wedge resection of the nodule, if technically feasible and oncologically was adequate (these patients are not included in this study); otherwise, we performed pneumonectomy.
Pain control was achieved by intrathecal morphine administration, followed by continuous patient-controlled intravenous analgesia with morphinic drugs. Intravenous proparacetamol was also administered. Supplemental subcutaneous morphinic drugs were administered to achieve a numeric analog score constantly at 4 or less (range, 1 to 10) at rest.
Patients were admitted to the intensive care unit (ICU) for 48 hours because ICU surveillance is legally mandatory in France in patients with intrathecal analgesia and were transferred to the surgical ward in the absence of complications. In patients with symptoms suggestive of postoperative pneumonia, samples for bacteriology by protected distal brushing were obtained before the initiation of any antibiotic treatment [13].
Our thoracic surgical department is a tertiary referral center, and patients who undergo operations are referred by the pneumology departments of many different hospitals, which then care for induction and adjuvant treatments; thus, no uniform protocol was used.
Operative mortality was calculated by accounting for all the deaths occurring within 30 days from the operation or during the hospitalization. Correlation between death and potential risk factors was assessed by 
2 or the Fisher exact test for categoric variables and the t test or U test for continuous variables.
Follow-up information was obtained by direct telephone interview with patients or, in case of deaths, with families. Referring physicians were also contacted to confirm data obtained from patients or the family interview. Overall survival rates (including noncancer-related deaths) were calculated by the Kaplan-Meier method and compared by the log-rank test. All the variables showing a possible correlation with survival (p < 0.1) were entered in a multivariate analysis (Cox proportional hazard model) to identify independent prognostic factors. Results were considered significant at a value of p < 0.05.
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Results |
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The mean patient age was 56.3 ± 9.7 years, and 24 were older than 65. The right lung was affected in 54 patients and the left lung in 64. Eight patients had major cardiovascular comorbidities (ischemic myocardial disease). Symptoms related to disease were present in 87 patients (73.7%), whereas in the remaining 21 cases, the lung cancer was discovered on chest roentgenograms performed for other reasons. Initial fiberoptic bronchoscopy results were normal in 21 patients, but abnormalities were recorded in the remaining patients, including intraluminal tumor in 47, mucosal infiltration in 22, and extrinsic compression in 28. The mean preoperative FEV1 was 81% ± 16.9%; 56 patients (47.4%) had a FEV1 of less than 80%.
Before induction therapy, 33 patients underwent PET scans. The PET was repeated before operation in 9 patients: no modification in uptake of either tumor or mediastinal nodes was observed in 5 patients; mediastinal uptake completely disappeared in 1 patient, although the uptake of primary tumor was unchanged; whereas in the remaining 3 patients, a diminution in the standardized uptake value was observed of mediastinal nodes in 1 and of both mediastinal nodes and primary tumor in 2.
Induction Therapy
The mean indication for preoperative chemotherapy was N2 disease in 74 patients, which was histologically proved before chemotherapy in 62 and affirmed on the basis of hyperfixation of huge mediastinal nodes at PET scan in the rest. Induction chemotherapy was administered because of T4 disease that was considered as potentially resectable in 17 patients; whereas in 18 patients, doubts existed about the resectability of the primary tumor. Chemotherapy was administered in 4 patients because of stage IV disease (nodule on another ipsilateral lobe). The remaining 5 patients had stage I or II disease but underwent induction chemotherapy because they participated in a randomized study evaluating preoperative chemotherapy in the initial stages.
Five patients underwent a single cycle of preoperative chemotherapy, which was discontinued because of poor tolerance; two, three, and four cycles were administered in 52, 37, and 12 patients, respectively. In 12 patients who were initially considered definitively inoperable, six cycles of chemotherapy were administered before they were referred for surgical intervention. All chemotherapy protocols were platinum-based. The associated drugs, dose, and schedule were extremely variable (Table 1) because different pulmonologists and oncologists referred the patients.
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Imaging reevaluation after induction therapy showed no complete response. Partial and minor responses were observed in 24 and 39 patients, respectively, with a 55.1% rate of objective response. Disease stability was observed in 55 patients. Operations took place 3 to 5 weeks after the completion of preoperative chemotherapy.
Surgical and Pathologic Data
Patients underwent 64 left pneumonectomies and 54 right pneumonectomies. Intrapericardial dissection was necessary in 78 patients (66.1%). The bronchial stump was closed by mechanical stapler in 97 patients and by interrupted sutures with absorbable monofilament in 15. The resection in the remaining 6 patients was extended to the carina and the anastomosis was done with absorbable monofilament, as previously described [14]. Full nodal dissection was done in all patients. The bronchial suture was protected in 56 patients by a pleural flap in 31 or a muscular flap in 25, consisting of serratus anterior in 14 and intercostal in 11.
Histologic types were squamous cell in 56 patients, adenocarcinoma in 34, and large cell carcinomas in 28 cases. One patient had a pathologic complete response, defined as the absence of viable tumor in all the examined slides. For the others, postchemotherapy pathologic staging was Ia, Ib, IIa, IIb, IIIa, IIIb, and IV in 4, 18, 1, 9, 52, 25, and 8 patients, respectively.
Outcome
No patients died intraoperatively. Seven patients (5.93%) died postoperatively: 4 patients died after right pneumonectomy (7.4%), and 3 died after left pneumonectomy (4.6%, p = 0.82). Bronchopleural fistula was responsible for death in 1 patient, who eventually experienced contralateral lung pneumonia and respiratory failure. Empyema without fistula, as assessed by fiberoptic bronchoscopy and negativity of detection of inhaled nitrous oxide in the pleural space [15], and septic shock was responsible for death in another patient. Postoperative pneumonia and acute respiratory distress (with no infection identified) was responsible for two other deaths. Two patients died of intractable cardiogenic shock. A single patient had rhabdomyolysis with renal failure complicated with cardiogenic shock and death.
No factor among those evaluated, including sex, age, comorbidities, symptoms, side, location, indication for chemotherapy, number of cycles, response to chemotherapy, FEV1, extent of resection, TNM status, or pathologic stage, could be identified as associated with postoperative death at univariate analysis (all p > 0.1); so multivariate analysis was not performed.
Other complications not responsible for deaths occurred in 28 patients, including postoperative pneumonia in 8, supraventricular arrhythmias in 15, hemothorax requiring reexploration in 2, pulmonary embolism in 1, empyema without fistula in 1, hypernatremia in 1, rhabdomyolysis without renal failure in 2, and delirium tremens in 1. After hospital discharge, 6 more patients died within 3 months, for a 90-day mortality of 11.01%.
Median follow-up was 21 months (range, 7 to 77 months). At the completion of the study (December 2007), 37 patients were alive and 81 were dead. Median survival was 22 months; 3- and 5-year overall survival was 37.9% and 23.7% (Fig 1). These figures were 40.3% and 25.1% in 30-day operative survivors. Five-year survival was 30.1% in patients with stage 0 to IIIa (Fig 2).
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Among the 37 surviving patients, possible dyspnea could be graded in 30 patients according to the New York Heart Association (NYHA) functional class: scores were 0, I, II, III, and IV in 13, 12, 3, and 2 patients, respectively.
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Comment |
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The question of whether pneumonectomy after chemotherapy for NSCLC is acceptable has been raised by several published studies that showed a very high mortality rate. In 1993, a report from the Fox Chase Cancer Center in Philadelphia on complications after induction treatment showed that of the 7 patients treated by pneumonectomy after chemoradiotherapy, adult respiratory distress syndrome (ARDS) occurred in 5, with two deaths, and one additional death was secondary to bronchopleural fistula [11]. In 2001 a retrospective study of morbidity after neoadjuvant chemotherapy from the Memorial Sloan-Kettering Cancer Center in New York [12], showed that pneumonectomy had an overall mortality rate of 11.3% (11 of 97), but a rate of 23.9% in case of right pneumonectomy was observed. More recently Doddoli and colleagues [8] published a retrospective study on 100 consecutive pneumonectomies after chemotherapy and reported 30-day and 90-day mortality rates of 12% and 21%, retrospectively. Respiratory failure (sometimes associated with ARDS) and empyema (with or without fistula) were the leading causes of deaths in all these studies. Because of these results, pneumonectomy (especially on the right side) after chemotherapy is often considered a dangerous operation and it has been recently suggested that patients who still require pneumonectomy after induction therapy may be better served by definitive chemoradiotherapy [7].
The experience of other authors is quite different: Leo and colleagues [9] found a 3% mortality rate of pneumonectomy after chemotherapy, whereas Stamatis and colleagues [10] reported a figure of 7.2% in case of pneumonectomy after induction chemoradiotherapy. Of note, these authors found an 8% rate of bronchopleural fistula. Similarly, in the multicenter study from France by Brouchet and colleagues, mortality of pneumonectomy after chemotherapy was 3.5% after right-sided operation and 8.5% after a left-sided procedure [16].
In our single-institution study of 118 consecutive patients, 30-day and 90-day mortality were 5.93% and 11.01%, percentages that compare quite favorably with available data. In agreement with others, we were not able to identify factors predicting operative mortality; it is possible that the low number of events renders this assessment statistically difficult. As observed by authors who reported similar results [9], we did not observe an increased mortality rate after right pneumonectomy. Careful attention to limit intraoperative barotrauma, early extubation policy, limitation of total fluid administration, and strategies for early detection of postoperative pneumonia are probably responsible for the relative low incidence of postoperative respiratory complications, which in turn may be responsible for death in these fragile patients. On the other hand, surgical techniques include avoiding devascularization of bronchial stump and its protection with flaps of viable tissue to minimize the risk of bronchopleural fistula: 1 patient in our series experienced this complication, which unfortunately, was rapidly lethal in spite of prompt drainage.
In our experience, a pathologic complete response was observed in a single patient. This result is in total agreement with the extremely low rate of pathologic complete response observed in the randomized trials on neoadjuvant chemotherapy of Rosell [2], Roth [3], and Depierre [4] and their associates, all of them including about 50% pneumonectomies. Of note in the study of Doddoli and colleagues [8] dealing with 100 consecutive pneumonectomies after induction treatments, the rate of pathologic complete response was higher (8%), but 30 patients also received preoperative radiotherapy, a percentage significantly more important compared with our series. In our experience, only 4 patients had preoperative radiotherapy on mediastinal nodes and all had initially bulky mediastinal nodes. This reflects the attitude of medical oncologists and pneumologists referring patients to our surgical center of performing preoperative chemotherapy rather than chemoradiotherapy as induction treatment in patients in whom secondary operation is initially planned.
Long-term results are quite encouraging in this subset of patients with locally advanced lung cancer, as the overall 5-year survival rate was 23.7%. If patients with stages IIIB/IV are excluded from the analysis, 5-year survival rate was 30.1%, whereas this figure was 44.7% in patients with stages I and II.
Few studies have specifically evaluated the long-term outcome of patients treated by pneumonectomy after chemotherapy. Doddoli and colleagues [8] reported a 5-year survival rate of 25% among the patients who live beyond 90 postoperative days, a value similar to the value of 26.3% in the same subset of patients in our study. There are also few data about outcome of pneumonectomy after induction chemotherapy in the randomized studies evaluating the value of preoperative chemotherapy, the total number of patients is quite limited and, in particular, in the studies by Pass [17], Rosell [2], and Roth [3] and their associates, and the number of pneumonectomies is even more exiguous. On the other hand, the study from Depierre and colleagues [4] included a greater number of subjects, and half of them received pneumonectomy—87 patients underwent neoadjuvant chemotherapy and pneumonectomy—but data about long-term outcome were not reported according to the type of resection.
At univariate analysis in our study, the pT value and stage of disease statistically influenced 5-year survival. The pN variable, pathologic downstaging of N2 disease (in patients who had induction chemotherapy for this reason), and clinical response to induction chemotherapy in all the patients were associated with a trend toward increased survival, not reaching significance, probably because of lack of power. At multivariate analysis, T status, the occurrence of postoperative complications, and clinical response to induction chemotherapy were independent predictors of 5-year survival. These results are in agreement with previous experience on lung resection (including also pneumonectomy) after induction chemotherapy: the Leuven lung cancer group [18] found that low pathologic T stage and downstaging of mediastinal nodes were independent prognostic factors and also in the prospective study of Depierre and colleagues [4], only stage was an independent prognostic factor. On the other hand, in the retrospective study by Takeda and colleagues [19], response to chemotherapy and treatment-induced complications had no effect on survival, whereas both pathologic T and N factors were independent prognostic factors. These discrepancies are probably explained by the heterogeneity in type and schedules of chemotherapy, assessment of response, possibly administered adjuvant chemotherapy or radiotherapy, or both, as well as ethnic differences.
In conclusion, pneumonectomy after chemotherapy in our experience is a relatively safe procedure with an acceptable rate of operative morbidity and mortality. Long-term results are encouraging in this subset of patients with locally advanced lung cancer.
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Discussion |
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DR ALIFANO: No, we do not use steroids in preventing ARDS. We only use careful intraoperative fluid administration, and avoid barotrauma at maximum during surgery. Furthermore, we have a policy of strong suspicion of postoperative pneumonia, with aggressive management if pneumonia is suspected, in order to promptly start adequate and targeted treatment.
DR MICHAEL J. LIPTAY (Chicago, IL): I notice that only 4 of your patients underwent radiotherapy in addition to chemotherapy. Do you think that could explain the low bronchopleural fistula rate that you have seen and very reasonable perioperative mortality? Secondly, did you record 90-day mortality as well as in-hospital or 30-day mortality?
DR ALIFANO: Only 4 patients had preoperative mediastinal radiotherapy: 1 had 45 Gy, another 60 Gy, and the remaining 2 had 65 Gy, but there was no mortality among them. I can't exclude that the small percentage of induction radiotherapy may justify our very low rate of BPF.
DR LIPTAY: And the 90 days, longer follow-up?
DR ALIFANO: We had an 11% mortality rate at the 90-day follow-up, but none of these deaths were attributable to late bronchopleural fistula, but mainly to sudden death, pneumonia, and pulmonary embolism.
DR MALCOLM M. DECAMP (Boston, MA): One striking result that I saw from your survival curves is that patients who had N2 or N3 disease had survival under 20%: 15%, 16%, 17%. Would you reconsider your treatment algorithm now and consider alternative ways to restage the mediastinum and/or suggest that perhaps you could achieve that kind of survival by adding radiation and not the morbidity of pneumonectomy for those patients who have mediastinal nodal involvement after chemotherapy?
DR ALIFANO: After chemotherapy, we did not perform a restaging mediastinoscopy, but based our decision on clinical staging.
DR DECAMP: Right, but your survival in the patients who pathologically had N2 or N3 disease was not very good. It was 16% at 5 years.
DR ALIFANO: With respect to nodal stage, I can show you a supplementary slide. This is the probability of survival in N0-1 or N2 patients. Effectively, patients with N2 disease had a trend toward worse prognosis as compared to N0 or N1 patients, but this difference was not significant. We have no N3 patients in our series. Stage IIIB was because of the T4 factor. As you can see, N2 patients had a trend to worse prognosis, but 5-year survival was 18.5%, which is not a bad result in these kind of patients.
DR DECAMP: No, but it would probably be the patient population that you could target to have a better result. You have identified clearly that N2 disease following a pneumonectomy is a marker for poor outcome. So that would be an opportunity if you could identify those patients prior to the resection to more optimize their therapy, different chemotherapy, adding radiation, so that they had a survival benefit that went up. I know it is not statistically significant to the statistician, but it is pretty depressing to the patient.
DR ALIFANO: I agree. Maybe further studies will be necessary.
DR JEAN DESLAURIERS (Sainte-Foy, Quebec, Canada): How many patients had N0-N1 disease that underwent induction treatments?
DR ALIFANO: There were approximately 70 N2 patients.
DR DESLAURIERS: Am I right in numbering 55 patients with N2 disease who underwent induction chemotherapy and 63 patients with N0–N1 disease?
DR ALIFANO: Approximately.
DR DESLAURIERS: So several patients with non-N2 disease had induction chemotherapy and were included in the series.
DR ALIFANO: As I stated, N2 disease was the cause of induction chemotherapy in 74 out of 118 cases.
DR DESLAURIERS: That means that in 30% of cases, patients with non N2 disease had induction chemotherapy.
DR ALIFANO: Approximately, as there was some degree of pathologic downstaging. Numbers in this slide refer to pathologic stage, not to initial stage.
DR DESLAURIERS: This is probably one of the reasons why the results appear better than in the previous paper.
DR ALIFANO: Yes. I agree.
DR DESLAURIERS: Induction chemotherapy for N2 disease followed by pneumonectomy is a bad combination. I noticed that in your series, there were three or four patients who died of a respiratory event more than 30 days postoperatively. Did these events start soon post-op and the patients died later or were they "De Novo" events that occurred once the patient had returned home?
DR ALIFANO: They had late respiratory or cardiac events and eventually they died.
DR DESLAURIERS: So these events did not start early post-op and the patient died from them later than 30 days. They were new events.
DR ALIFANO: With respect to 90-day mortality, all the patients had been discharged and the event leading to late death occurred thereafter.
DR DESLAURIERS: This is an important question because we see more and more often patients with respiratory complications such as ARDS where the event occurs within 7–10 days of the surgery and yet the patients die more than 30 days post-op. Perhaps the terminology regarding post-operative mortality should be revised.
DR ALIFANO: No. I simplified when speaking about in-hospital mortality. 30-day mortality was all the mortality occurring during the same hospitalization of surgery or within 30 days from it.
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