J Thorac Cardiovasc Surg 1999;117:1095-1101
© 1999 Mosby, Inc.
COMPLETION PNEUMONECTOMY: EXPERIENCE IN EIGHTY PATIENTS
J. F. Regnard, MD,
P. Icard, MD,
P. Magdeleinat, MD,
B. Jauffret, MD,
E. Farés, MD,
P. Levasseur, MD
From the Department of Thoracic Surgery, Marie Lannelongue Hospital, Le Plessis Robinson, France.
Received for publication Nov 4, 1998. Revisions requested Jan 12, 1999. Revisions received Feb 15, 1999. Accepted for publication Feb 19, 1999.
Address for reprints: J. F. Regnard, MD, Service de Chirurgie Thoracique et Vasculaire, Centre Chirurgical Marie Lannelongue, 133 avenue de la résistance, Le Plessis Robinson, 92350 France.
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Abstract
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Objective: Because completion pneumonectomy is a procedure reputed to place patients at risk, we reviewed our results with the objective of identifying factors that influence complications and survival.
Methods: In a 25-year period, 80 completion pneumonectomies were performed after first operations for 17 cases of benign disease and 63 cases of lung cancer (89% stages I and II), with 7 of the latter patients receiving postoperative radiotherapy. Completion pneumonectomy was performed in 18 cases of benign disease and 62 cases of lung cancer: 28 second primary cancers, 26 recurrent cancers, 3 metastases, and 5 primary cancers in patients previously operated on for benign disease.
Results: No intraoperative deaths occurred. Postoperative mortality rates were 5% for the entire series, 6.4% for patients operated on for cancer, and 0% for patients operated on for benign diseases. Patients previously irradiated and those operated on for infectious disease were at risk for postoperative empyema and fistula formation. In the cancer treatment group the actuarial 5-year survival was 36%, without significant difference between patients with recurrent and second primary lung cancers. The actuarial 5-year survivals were 51% for patients with stage I disease, 42% for patients with stage II disease, and 18% for patients with stage IIIA disease (P < .05).
Conclusions: Completion pneumonectomy can be performed with an acceptable operative mortality rate and offers a second chance for cure to patients with cancer. Patients previously irradiated and those requiring completion pneumonectomy for infectious benign disease are at risk for postoperative complications. (J Thorac Cardiovasc Surg 1999;117:1095-101)
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Introduction
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Completion pneumonectomy is an operation reputed to pose difficulties in both the intraoperative and postoperative periods, with greater risks of death and of complications than are associated with standard pneumonectomy.
1-7 Extensive experience is rare, and series exceeding 50 patients are exceptional. 2,3 We reviewed our results of 80 consecutive completion pneumonectomies with the objective of determining factors that influence immediate results and long-term survival.
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Patients and methods
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Eighty consecutive patients underwent a completion pneumonectomy in our department between 1972 and 1997. Of these patients 72 (90%) were operated on in the last 15 years. The ratio of completion pneumonectomies to standard pneumonectomies was around 5% during the same period. There were 74 men and 6 women, with an average age of 58 years (range 18-84 years). Twelve patients (15%) had previous pulmonary insufficiency, cardiovascular disorders, or both; 12 patients (15%) had already been treated for another extrathoracic cancer.
First operation
The initial surgical procedure was a lobectomy in 71 cases, a bilobectomy in 6 cases, and a segmentectomy in 3 cases. These first operations were performed for various infectious diseases in 18 cases (bronchiectasis in 8 cases, tuberculosis in 8 cases, and lung abscess in 2 cases), for a benign tumor in 1 case, and for primary lung cancers in 61 cases. Three of the patients with chronic infectious disease underwent a thoracoplasty at the end of the operation. Among the 61 cases of primary lung cancers there were 37 squamous cell carcinomas, 16 adenocarcinomas, 4 poorly differentiated large cell carcinomas, 2 mixed squamous cell carcinomas and adenocarcinomas, and 2 bronchioloalveolar carcinomas. According to the TNM classification for lung cancers 8 most patients had localized cancers: 35 patients (58%) had stage I disease, 19 (31%) had stage II disease, 5 (8%) had stage IIIA disease, and 2 (3%) had stage IIIB disease. Seven of these 61 patients (11%) underwent an incomplete initial resection, with a neoplastic bronchial margin found on definitive histologic examination. Five of these 7 patients were operated on at another hospital and underwent completion pneumonectomy in our department after intervals of 7, 11, 21, 21, and 22 months. Among the 2 patients initially operated on in our department, 1 underwent an immediate reoperation whereas the other initially received adjuvant postoperative radiotherapy. The latter patient required a completion pneumonectomy 8 months later for recurrence. During the postoperative period after the first operation, 7 patients (all with stage III disease) received adjuvant radiotherapy (in 2 cases associated with chemotherapy) and 4 patients received chemotherapy. The mean dose of the delivered radiotherapy was 58 Gy (range 45-65 Gy).
Second operation
Completion pneumonectomy was performed in 18 cases for a benign lesion and in 62 cases for a malignant tumor. The indications for completion pneumonectomy among the 18 patients with benign disease were chronic infected bronchiectasis destroying the remaining lobe in 12 cases and complications directly linked to the first surgical procedure in 6 cases. There were 3 cases of bronchial anastomotic strictures (1 after sleeve lobectomy and 2 after standard lobectomy) and 3 cases of bronchovascular fistulas, which required urgent reoperation. These 3 cases of bronchovascular fistulas occurred in patients who had undergone standard lobectomies. In the group of 61 patients with cancerous disease a second primary lung cancer or a local recurrence was defined according to the criteria defined by Martini and Melamed 9: a local recurrence was defined as a second malignant tumor with the same cell type occurring in the same anatomic site within 2 years of the first operation and a second primary lung cancer was defined as a second malignant tumor when the cell type was different or when a tumor with same cell type occurred in a different anatomic site more than 2 years after the first cancer in the absence of residual tumor after the first operation. According to these criteria, completion pneumonectomies were performed for a second primary cancer in 28 cases (44%), for a local recurrence of the first cancer in 26 cases (41%), for a probable metastasis of the first primary lung cancer in 3 cases, and for a primary lung cancer in the 5 remaining cases of patients who had previously been operated on for benign disease. Completion pneumonectomy was performed on average 17 months (1-46 months) after the initial surgical procedure in cases of local recurrence, 34 months (7-58 months) after the initial surgical procedure in cases of metastasis, 67 months (12-131 months) after the initial surgical procedure in cases of second primary cancer, and 124 months (3-408 months) in cases of benign recurrent lesions.
Preoperative evaluation included assessment of cardiac, renal, and respiratory function. The selection criteria for completion pneumonectomy were the same as those for standard pneumonectomy, mainly a predicted postpneumonectomy forced expiratory volume in 1 second greater 33% of the theoretic values. The mean preoperative forced expiratory volume in 1 second was 66% ± 14% (33%-88%) and the mean perfusion of the operated side found on a lung scintiscan was 29% (5%-33%). In the group with malignant disease assessment of mediastinal lymph nodes was done by computed tomographic scan, and mediastinoscopy with biopsy was performed in response to any suspicion of N2 disease (mean diameter >1.5 cm) to avoid surgery in cases of bulky N2 disease.
Surgical procedure
Forty-six completion pneumonectomies were performed on the right side and 34 were performed on the left side. Extrapleural dissection was generally performed in any area with dense adhesions and obliteration of the pleural space. The hilar dissection was systematically undertaken by first opening the pericardium to control the pulmonary artery and veins. The bronchial stump was kept short, and excessive peribronchial dissection was avoided to preserve vascularization. Bronchial closure was done with staplers in 60 cases and with interrupted sutures (absorbable 3-0 polyglactin Vicryl sutures; Ethicon, Inc, Somerville, NJ) in 20 cases. The line of bronchial closure was always covered with adjacent fascial, pleural, or mediastinal tissues when available. In 5 of the patients who had received postoperative radiotherapy after the initial surgical procedure and in 1 patient who underwent a completion pneumonectomy for infected lesions, a serratus anterior muscle flap was performed to reinforce the bronchial stump closure. The space was drained by a clamped chest tube, which was left in place for equilibration and removed 48 hours after the operation.
In the 62 patients who underwent completion pneumonectomy for cancerous disease, histologic examination showed a squamous cell carcinoma in 38 cases (61%), an adenocarcinoma in 19 cases (31%), a mixed adenocarcinoma and squamous cell carcinoma in 1 case, and an undifferentiated large cell carcinoma in 3 cases. The stages of these resected tumors were as follows: stage I in 28 cases (45%), stage II in 8 cases (13%), stage IIIA in 24 cases (39%), and stage IIIB in 2 cases (3%). In the postoperative period 17 patients received radiotherapy, 1 patient received chemotherapy, and 1 patient received both treatments.
Statistical analysis
Information was gathered from the files of patients followed up in our institution or was obtained from the referring pulmonary physicians. Follow-up of at least 2 years, with a mean duration of 48 months, was completed at the end of 1997 for all patients. Clinical data (duration of the operation, side of the pneumonectomy, level of blood loss, and use of transfusions) were analyzed as factors influencing postoperative complications (simple recovery vs empyema or bronchopleural fistula). The patients were divided into 3 subgroups: those with cancers who received adjuvant radiotherapy after the first operation, those with cancers who did not receive radiotherapy, and those with benign disease. The Student t test and the 
2 test were used for group comparisons with univariate analysis. Survival was calculated from the time of completion pneumonectomy according to an actuarial method derived from the Kaplan-Meier analysis. 10 Stage of cancer was analyzed as a predictor of survival. Survivals were compared between subgroups with the log rank test. When appropriate, confidence intervals (CIs) are given.
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Results
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No intraoperative deaths occurred. Although a hilar dissection was systematically undertaken by first opening the pericardium to control the pulmonary artery and veins, this precaution did not avoid 3 operative vascular injuries, all of which were immediately controlled. The median duration of the surgical procedure was 3 hours and 30 minutes (2-6 hours, 25%-75% CI 3-4 hours). The median perioperative blood loss was 950 mL (250-2500 mL, 25%-75% CI 300-2000 mL), necessitating blood transfusions during the hospitalization in 52 cases (66%) with a median of 3 units of packed cells per patient (2-14 units, 25%-75% CI 1-5 units).
The overall postoperative mortality rate was 5%, with all 4 deaths occurring among the patients with cancerous disease. There were 1 lethal pulmonary embolus, 1 lethal infection of the remaining lung, and 2 lethal bronchopleural fistulas with empyemas. These 2 fistulas occurred in the group of patients who had received radiotherapy after the initial operation. In 1 of these 2 cases a serratus anterior flap had been performed but failed to prevent the occurrence of a bronchopleural fistula. The overall postoperative mortality rates were 6.4% (4/62) for patients with cancerous disease and 0% for patients with benign disease. In the group of patients who underwent completion pneumonectomy for lung cancer, the mortality rates were 28% (2/7) among those who had received radiotherapy after the initial operation and 3.2% (2/55) among those who had not (P = .18).
Postoperative recovery was uneventful in 60 cases (75%). Twenty patients (25%) sustained nonlethal postoperative complications, as shown in Table I. The significant factors related to postoperative morbidity were preliminary radiotherapy and indication of completion pneumonectomy for benign disease. In fact, among patients operated on for cancerous disease preliminary radiotherapy was significantly related to higher rates of postoperative empyema (42.8% vs 7.2%, P = .05) and of bronchopleural fistula (28.6% vs 0%, P = .02). Three bronchopleural fistulas occurred in this select group, and 2 resulted in death (Table I). On the other hand, the side of the pneumonectomy, the duration of the operation, the level of blood loss, the need for red blood cell transfusions, and the stage of cancer were not significant predictive factors for postoperative complications.
Empyema was frequent among patients undergoing completion pneumonectomy for benign disease (27.7%) but did not result in any deaths. There was no difference in bronchopleural fistula occurrence between patients who had a hand-sewn bronchial closure and those who had a staple closure.
Actuarial survival curves are presented in Figs. 1 and 2.The actuarial 5-year survival was 70% for patients who underwent completion pneumonectomy for benign disease. The actuarial 5-year survival was 36% for patients who underwent completion pneumonectomy for cancerous disease, without any difference in survival between patients with recurrent cancers and those with second primary cancers ( P = .75; Fig. 2).As indicated in Fig. 3, the prognosis was significantly influenced by the stage of the cancer. The actuarial 5-year survivals were 51% (95% CI 31%-71%) for patients with stage I disease, 42% (95% CI 25%-75%) for patients with stage II disease, and 18% (95% CI 2%-38%) for patients with stage IIIA disease. There was no significant difference in survival between patients with stage I and stage II disease (P = .8), whereas there was a significant difference between patients with stage I and stage IIIA disease (P = .03) and between patients with stage II and stage IIIA disease (P = .05). Both patients with stage IIIB disease died within 3 years after the operation.
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Fig. 1 Actuarial survival of patients undergoing completion pneumonectomy either for primary lung cancer or for benign disease. Numbers in parentheses indicate patients at risk.
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Fig. 2 Actuarial survival of patients with stage I, stage II, and stage IIIA lung cancers undergoing completion pneumonectomy. Numbers in parentheses indicate patients at risk.
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Fig. 3 Comparison of survival between patients undergoing completion pneumonectomy for second cancer with those undergoing completion pneumonectomy for recurrent cancer. Numbers in parentheses indicate patients at risk.
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Discussion
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Our results show that completion pneumonectomy may be performed with an acceptable postoperative mortality rate, offering some chance of long-term survival for patients with lung cancers and giving them a second chance for cure. Our indications for completion pneumonectomy were mainly occurrence of lung cancer, either recurrence of the primary lung cancer previously resected or a second primary lung cancer. In almost a quarter of our cases, however, completion pneumonectomy was indicated for benign lesions, most often for infected and destroyed lobes but sometimes also for complications related to the first resection, either bronchovascular fistula or bronchial stenosis.
Perioperative risk and precautions
There were no intraoperative deaths in our series, despite the reported risk, 2 especially among patients with previous radiotherapy. However, dense adhesions and extrapleural dissection resulted in greater blood loss (median 950 mL), with a need for transfusion in 66% of the patients. Radiotherapy significantly increases the density of fibrosis, especially in the apex of the lung. Technical factors aiding in dissection include initial intrapericardial control of the vessels (which may be sometimes very difficult because of a near to total obliteration of the intrapericardial space), and the "bronchus first" technique that may facilitate the control of vessels on the right side.
Postoperative mortality rate
The overall mortality rate was 5%, 6.4% among patients undergoing resection for malignancy and 0% among patients undergoing resection for benign disease. These results compare favorably with those in reported series (Table II). As indicated in Tables II and III, some series have shown higher mortality rates for benign disease 2,4,7 and for completion pneumonectomy after initial bronchial sleeve resection. 11 In contrast to McGovern and colleagues, 2 we did not observe any difference in postoperative mortality rate between patients with second primary cancers and recurrent cancers, and our 5% overall mortality rate is close to that seen for standard pneumonectomy in our institution and in the literature. 12,13
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Table II. Operative mortality rates and 5-year survivals after completion pneumonectomy for malignant disease according to the literature
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Table III. Operative mortality and major complication rates after completion pneumonectomy for benign disease according to the literature
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Postoperative complications
Preoperative radiotherapy increases the bronchopleural fistula rate after lung resections. 14,15 We especially saw major postoperative complications among patients who received adjuvant radiotherapy after the initial resection. To prevent bronchopleural fistula formation, reinforcement of the stump (with muscle, pericardial fat, pleura, or omentum) is recommended. As we reported previously, 16 we favor a muscle flap. As with Arnold and Pairolero, 17 the serratus anterior muscle is the first choice, but other flaps such as the latissimus dorsi flap 5,18 or the omental flap 19 may also be used. In this study the use of a serratus anterior muscle flap failed to avoid the occurrence of 1 fistula among the patients previously irradiated. Despite this precaution, these patients thus remain at risk for major complications. Not surprisingly, in our series empyema was more frequent after completion pneumonectomy for infectious disease than for lung cancer (28.6% and 11.3%, respectively). McGovern and colleagues 2 reported similar rates (20.6% and 10.6%, respectively). In contrast to McGovern and colleagues, 2 however, who reported a higher rate of bronchopleural fistulas among patients who underwent completion pneumonectomy for benign disease than among those operated on for cancer (17.2% vs 5.5%), we did not observe any statistical difference between these groups (5.5% and 3.1%, respectively). The potential risk factors for development of empyema and bronchopleural fistula after completion pneumonectomy for infectious disease are presumably the same as after standard pneumonectomy: poor general condition, sputum revealing mycobacteria, perioperative polymicrobial contamination of the lung, and Aspergillus species infection. u2,5,20-23 In these situations immediate muscle transposition could also be a good option to prevent the occurrence of a bronchopleural fistula.
Long-term survival among patients with cancer
In our study we found an overall 5-year survival among patients with cancer of 36%, despite the fact that 45% of the patients had stage III disease. Completion pneumonectomy undoubtedly offers a second chance for cure to patients with cancer. The prognosis was closely dependent on the stage of cancer (Fig. 2
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In this series we did not find any difference in survival between patients with second cancers and with recurrent cancers, in contrast to 2 other studies 2,3 that reported a better survival after completion pneumonectomy among patients with second primary cancers. The distinction between a second primary cancer and recurrent cancer is of only academic importance, however, if the tumor can be radically resected. These results support the need to carefully follow up patients with lung cancer after initial resection, because 45% of patients in our series underwent completion pneumonectomy for an advanced stage III cancer. Patients with a first resected low stage (stage I or II) cancer obviously may benefit the most from the follow-up because they are the best candidates for a second curative procedure. Efforts should be made to focus the follow-up on these patients, who are at risk for development of a second new primary cancer and sometimes a recurrence. The prognosis after completion pneumonectomy for lung cancer is relatively close to the commonly accepted norms for standard primary resection for equal stages of cancer. 24
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Conclusion
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This series demonstrates the feasibility and benefits of completion pneumonectomy for patients with new primary or recurrent lung cancers, with postoperative mortality rates and survivals that are comparable to those associated with standard pneumonectomy. Patients who received adjuvant radiotherapy after the first resection are at risk for bronchopleural fistula formation, which should be prevented by covering the bronchial closure with a muscle flap. Empyema was more frequent after completion pneumonectomy for infectious disease but did not result in any deaths. Intensive follow-up of patients previously operated on for a low stage cancer is recommended to give these patients a second chance for cure in cases of new primary or recurrent cancers.
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Abstract
Introduction
