141 Ann Thorac Surg , Aug Copyright by The Society of Thoracic Surgeons

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1 Completion Pneumonectomy: Indications, Complications, and Results Eilis M. McGovern, M.B.B.Ch., Victor F. Trastek, M.D., Peter C. Pairolero, M.D., and W. Spencer Payne, M.D. ABSTRACT From 958 through 985, a total of consecutive patients had completion pneumonectomy (CP). Indications for pulmonary resection resulting in CP were lung cancer (LC) in 64 patients, pulmonary metastases (PM) in 20, and benign lung disease (BLD) in 29. Operative mortality was 2.4% (4 deaths) but varied according to the indication for CP. Mortality was 9.4% for LC, 0% for PM, and 27.6% for BLD. Forty-three patients (8.%) had major complications (26 of 64 with LC, 40.6%; of 20 with PM, 5.0%; and 6 of 29 with BLD, 55.2%). Five-year actuarial survival for patients with LC was 26.4% but vaned according to stage. Five-year survival for patients with PM was 40.8% and with BLD was 27.2%. We conclude that CP for BLD carries marked operative mortality and morbidity, usually due to intense reaction around hilar structures and concurrent active infection or fistula. In contrast, CP for LC and PM can be performed with low mortality, acceptable morbidity, and gratifying long-term survival. Sequential unilateral pulmonary resection leading to pneumonectomy is uncommon. The last pulmonary resection in the sequence has been termed completion pneumonectomy (Fig ). Little information regarding this procedure is available in the literature, and indications, morbidity, and mortality are not well defined. Nonetheless, thoracic surgeons are asked to evaluate patients for this procedure. To develop guidelines, a retrospective review of patients who had completion pneumonectomy was undertaken. Patients and Methods The records of all patients who had completion pneumonectomy at the Mayo Clinic between January, 958, and December, 985, were reviewed; there were consecutive patients. The records of these patients were analyzed for indication for operation, type of pulmonary resection performed, operative findings, pulmonary pathology, complications, and long-term results. Survival probabilities were calculated by the Kaplan-Meier actuarial method [l] using the date of completion pneumonectomy as the starting date and including deaths from all causes. Operating mortality included all From the Section of General Thoracic Surgery, Department of Surgery, Mayo Clinic and Mayo Foundation, Rochester, MN. Presented at the Thmty-fourth Annual Meeting of the Southern Thoracic Surgical Association, Boca Raton, FL, Nov 5-7, 987. Address reprint requests to Dr. Trastek, 200 First St SW, Rochester, MN deaths occuning within 0 days of completion pneumonectomy and all deaths occurring beyond 0 days but during the same hospitalization. Expected survival curves were based on deaths from all causes from West- North Central United States 970 life-table data and were matched for age and sex. All patients with lung cancer were staged by the TNM (tumor, node, metastasis) classification system of the American Joint Committee for Cancer and End-Results Reporting [2]. Results Initial Pulmonary Resections There were 79 male and 4 female patients. Ages ranged from 6 to 8 years, with an average age of 59.9 years. Indication for initial lung operation was lung cancer in 75 patients, pulmonary metastases in 20, and benign lung disease in 8 (Table ). Bilobectomy was performed in 4 patients, lobectomy in 69, segmentectomy in 5, wedge resection in 7, and various combinations of these procedures in 8. The resection was on the right in 57 patients and on the left in 54; 2 had bilateral pulmonary wedge resection performed through a median sternotomy for pulmonary metastases. Fifty-eight lung cancer patients were postsurgically classified as Stage I, 2 as Stage, and 4 as Stage. One patient could not be staged. Eleven patients had multiple staged pulmonary resections before completion pneumonectomy. Seven patients had 2 prior pulmonary resections, had, and had 4. The indication for these interim procedures was pulmonary metastases in 9 patients, alveolar cell carcinoma in l, and radiationinduced bronchopleural fistula in. Nineteen patients received adjuvant therapy for their pulmonary disease before completion pneumonectomy; 8 received chemotherapy, 7 received radiation therapy, and 4 received both. Completion Pneumonectomy The median interval between the first pulmonary resection and completion pneumonectomy was 2.2 years and ranged from 0 days to 28.4 years. There was frequent crossover in operative indication from the initial pulmonary resection to completion pneumonectomy (Fig 2). Seventeen patients whose initial indication was lung cancer had no evidence of recurrence but subsequently required completion pneumonectomy for benign lung disease. Similarly, in 2 patients with initial pulmonary metastases, a new primary lung cancer later developed. Conversely, in 6 patients with initial benign lung disease, cancer developed (primary lung cancer in 4, and pulmonary metastases in 2). Consequently, the final in- 4 Ann Thorac Surg , Aug 988. Copyright by The Society of Thoracic Surgeons

2 42 The Annals of Thoracic Surgery Vol 46 No 2 August 988 A Fig. Sequential unilateral pulmonary resection leading to completion pneumonectomy in 2-year-old man with resected osteogenic sarcoma of distal right femur. (A) Posteroanterior chest roentgenogram demonstrating bilateral pulmona y metastases. (B) Posteroanterior chest roentgenogram following sternotomy for resection of bilateral pulmonary metastases demonstrating large left hilar mass and loss of volume in left lung. (0 Posteroanterior chest roentgenogram following completion pneumonectomy. Table. Indications for Initial Pulmonary Resection C dication for completion pneumonectomy was lung cancer in 64 patients, pulmonary metastases in 20, and benign lung disease in 29 (Table 2). The 64 patients with lung cancer were postsurgically reclassified as Stage I in 28, Stage I in 6, and Stage I in 0. Twenty-six of these patients exhibited new primary lung cancer, 6 of whom had no evidence of prior lung cancer. Cancer developed in a total of 0 patients (89.4%). During the time frame of this study, 79 patients had lung cancer, 20 had pulmonary metastases, and 2 had both (see Fig 2). Indication for completion pneumonectomy in the 29 patients with benign lung disease was a complication of the initial pulmonary resection in 6 patients (bronchopleural fistula in and bronchial stenosis in ), persistent lung disease in 5 (bronchiectasis in, hemoptysis in, and lung abscess in l), aspergilloma in, radiation necrosis in, and other causes in 2 (see Table 2). These indications were in contrast to those observed in the Indication Lung cancer (N = 75) Squamous cell 45 Adenocarcinoma 4 Large cell Small cell Alveolar cell 9 Car cin o i d Pulmonary metastases (N = 20) Colodrectum 5 Osteogenic sarcoma Soft tissue sarcoma 2 Breast 2 Other carcinomdsarcoma 8 Benign lung disease (N = 8) Lung abscess Bronchiectasis Granuloma Chronic pneumonitis Hem o p ty s i s Aspergillosis Tuberculosis No. of Patients

3 4 McGovern et a Pneumonectomy, Complications, Lung Cancer, Metastatic Cancer Table 2. Indications for Completion Pneumonectomy ~~ ~ Indication Lung cancer (N = 64) New primary (N = 26) squamous 20 Adenocarcinoma 2 Large cell 2 Alveolar cell Adenosquamous Local recurrence (N = 8) Squamous 8 Adenocarcinoma 0 Alveolar cell 8 Carcinoid 2 Pulmonary metastases (N = 20) Osteogenic 5 Soft tissue sarcoma 2 Colodrectum 4 Breast 2 Other caranomakarcoma 7 Benign conditions (N = 29) Bronchopleural fistula Bronchial stenosis Bronchiectasis Aspergilloma Radiation necrosis Hemopty sis Lung abscess Foreign body Hilar mass No. of Patients Total remaining 84 patients, in whom cancer was the indication in all. The pulmonary resection performed at completion pneumonectomy was lobectomy in 58 patients, bilobectomy in 8, and a combination of wedge resection and lobectomy in 7 patients. Completion pneumonectomy was on the right in 58 patients and on the left in 55. Eighteen patients had concomitant procedures, including intrathoracic transportation of extrathoracic skeletal Lung cancer Pulmonary metastases Benign lung disease Initial resection Completion pneumonectomy Fig 2. Indication for pulmonary resection demonstrating crossover from initial resection to completion pneumonectomy. muscle in 0, chest wall resection in 7, and open pleural window in. Hospitalization averaged 4.8 days and ranged from 6 to 50 days. Seventy-four complications, including both intraoperative and postoperative, occurred in 4 patients (8.%; Table ). Of patients with benign lung disease, 55.2% (6 of 29) had complications compared with 40.6% (26 of 64) for those with lung cancer and only 5.0% ( of 20) for those with pulmonary metastases (p < 0.002). There were 4 operative deaths (operative mortality, 2.4%). Six of these deaths occurred intraoperatively, all from hilar bleeding. All 6 patients had prior lung cancer, 4 of whom received adjuvant radiation therapy. Indication for completion pneumonectomy in these 6 patients was benign lung disease in 4 and lung cancer in 2. The remaining 8 deaths occurred from 2 to 54 days postoperatively. Cause of postoperative death was multisystem failure in 6 patients, bleeding from a contralateral aspergilloma in, and respiratory aspiration in. The indication for completion pneumonectomy in these 8 postoperative deaths was benign lung disease in 4 and lung cancer in 4. None of these 8 patients had radiation therapy. The mortality for the patients with benign lung disease was 27.6% compared with 9.4% for patients with lung cancer and 0% for patients with pulmonary metastases (p < 0.0). The average age in patients with pulmonary metastasis was 45.4 years as compared with 58. years for patients with benign conditions and 65.2 years for patients with recurrent lung cancer. Table. Complication by Indication for Completion Pneumonectomy Lung Cancer Benign Lung Disease Pulmonary Metastases Variable (N = 64) (N = 29) (N = 20) No. of patients 26 6 Total complications 42 Cardiac dysrhythmia Respiratory failure 8 6 Empyema Hemorrhage Fistula Sepsis 2 0 Myocardial infarction 2 0 Wound infection 2 0 Stroke 2 0 0

4 44 The Annals of Thoracic Surgery Vol 46 No 2 August 988 Table 4. Follow-up Status of 95 Patients who had Completion Pneumonectomy Variable Lung Cancer Benign Lung Disease Pulmonary Metastases (N = 57) (N = 9) (N = 9) Alive 2 7 Without cancer With cancer 2 Unknown 0 Dead Cancer 4 0 Pneumonia 2 0 Myocardial infarction Ruptured aorta 0 Suicide 0 0 cn Intestinal bleeding 0 0 Stroke 0 0 Unknown Expected survival Observed survival I I I I I I I I I I Fig. Overall probability of survival (death from any cause) of patients undergoing completion pneumonectomy compared with expected sunrival matched for age and sex. Zero time on the abscissa represents the day of completion pneumonectomy. Fig 5. Probability of survival (death from any cause) in 64 patients with lung cancer undergoing completion pneumonectomy by postsurgical stage. Zero time on the abscissa represents the day of completion pneumonectomy. Stage I Stage II I I I, Stage Local recurrence 0 I I I I Fig 4. Probability of survival (death from any cause) of patients undergoing completion pneumonectomy by indication. Zero time on the abscissa represents the day of the completion pneumonectomy. (BC = benign condition; LC = lung cancer; PM = pulmonary metastases.) Follow-up Follow-up was complete in 95 of the 99 operative survivors (96.0%) and ranged from 4 days to 5.5 years, with a mean of 2.4 years. Two patients with benign lung disease were lost to follow-up at 0 and 4 days postoperatively, with lung cancer at 0 days and with pulmonary metastases at 6 days. At follow-up, 0 patients were alive, 24 without any evidence of cancer, 4 with known cancer, and 2 unknown (Table 4). Cause of death was cancer in 47 patients and unknown in 8. Five-year actuarial survival for all patients under- 0 I I I I 0 I Fig 6. Probability of survival (death from any cause) following completion pneumonectomy of 26 patients with new primary lung cancer compared with 8 patients with locally recurrent lung cancer. Zero time on the abscissa represents the day of completion pneumonectomy. going completion pneumonectomy was 28.4% (Fig ) and varied according to the indication for operation. Five-year survival for the 64 patients with lung cancer was 26.4%; pulmonary metastases, 40.8%; and benign lung conditions, 27.2% (Fig 4). Survival of patients with lung cancer was largely stage dependent (Fig 5), and at 5 years was 42.% for patients with Stage I disease, 20.0% for Stage, and.8% for Stage HI (p < 0.0). Five-year survival for patients with new primary lung cancer was 45.5% compared with only 4.8% (Fig 6) for patients with locally recurrent cancer (p < 0.02).

5 45 McGovem et a Pneumonectomy, Complications, Lung Cancer, Metastatic Cancer Comment Multiple staged pulmonary resection resulting in pneumonectomy is uncommon, and we have not been able to find any report in the literature specifically addressing indications, morbidity, and mortality associated with completion pneumonedomy. Completion pneumonectomy, however, has been reported as treatment for recurrent lung cancer [, 4. In our series, mortality and morbidity clearly varied with the indication for completion pneumonectomy. Lung cancer patients had a mortality of 9.4%, which was similar to the 6.2% mortality for routine pneumonectomy reported by the Lung Cancer Study Group in 98 [5] and the 4.% observed by Jensik and colleagues [4] in 98 for completion pneumonectomy for recurrent lung cancer. In contrast, there was no mortality in our patients who had completion pneumonectomy for pulmonary metastases. Undoubtedly a younger age, better pulmonary and cardiac reserve, a Mum free of inflammation, fibrosis, or tumor, and the absence of infection in the pleural space contributed to this more favorable outcome. The most surprising finding was observed in patients with benign lung disease who had a mortality for completion pneumonectomy of 27.6%. These patients differed substantially from patients with either lung cancer or pulmonary metastases in that the indication for completion pneumonectomy was either a complication of the initial lung resection (fistula, stenosis) or adjuvant radiation therapy (necrosis, fistula) or persistence of residual pulmonary disease (aspergilloma, bronchiectasis, lung abscess). In 26 of the 29 patients with benign lung disease, extensive hilar inflammatory reaction was identified at operation. There were 2 major causes of hospital mortality in our patients: hemorrhage and multisystem failure. Uncontrollable hemorrhage was responsible for all 6 intraoperative deaths. Five of the 6 patients had either benign lung disease (4 patients) or radiation therapy (4 patients), or both, following their initial pulmonary resection, both of which were implicated in the formation of ligneous reaction in the hilus. In all 6 intraoperative deaths, the pericardium was opened to control the great vessels, but the pericardial cavity was obliterated in the 4 patients who had had prior radiation therapy. In the 6 patients dying of multisystem failure, either sepsis (empyema, pneumonia, peritonitis) or respiratory failure could be implicated. In 2 of these patients, the indication for completion pneumonectomy was bronchopleural fistula that had persisted since the initial pulmonary resection. Two hospital deaths were coincidental to operation and not directly attributed to completion pneumonectomy. One patient bled from an aspergilloma in the contralateral lung on the second postoperative day, and the second, who was recovering well, inexplicably aspirated and died on the th postoperative day. Complications following pneumonectomy are not uncommon. The frequency of complications varied significantly in our patients according to the indication for completion pneumonectomy and occurred in over half of all patients with benign lung disease, but in only 5% of patients with pulmonary metastases. Complications related to infection were more common in patients with benign lung disease and did not occur in patients with pulmonary metastases. Infection complications were most commonly postpneumonectomy empyema and bronchopleural fistula. In the future, open pleural drainage and muscle transposition to reinforce a closed bronchial stump and obliterate pleural space at the time of completion pneumonectomy could potentially reduce these complications [6]. The association of cardiac dysrhythmia with pneumonectomy has been well documented [7]. In our series, cardiac dysrhythmia was the most common complication and occurred overall in 7.7% of patients. This figure is similar to the 22% incidence noted by Krowka and associates [7] in 26 consecutive patients undergoing pneumonectomy. Cardiac dysrhythmia occurred in 25.0% of our patients with lung cancer, in.8% of our patients with benign lung disease, and in none of our patients with pulmonary metastases. Why dysrhythrnia should be highest in patients with lung cancer and absent in patients with pulmonary metastases is uncertain, but this pattern is probably related to an older age, stronger smoking history, and the presence of both coronary artery disease and chronic obstructive lung disease. An overall 5-year actuarial survival of 28.4% for patients undergoing completion pneumonectomy is encouraging considering that 0 patients (89.4%) in this study had cancer. The 5-year survival for the 64 patients with lung cancer at the time of completion pneumonectomy was 26.4%. Although postsurgical staging of lung cancer in these 64 patients is arbitrary since 58 had had prior lung cancer, survival data do correlate with staging and were 42.% for patients with Stage I disease, 20% for Stage, and.8% for Stage. The classification of lung cancer into new primary cancer and local recurrence is also controversial, but again, the survival data in this study correlate with the survival reported by Pairolero and associates [8]. Five-year survival was 45.5% in our patients considered to have new primary lung cancer, but only 4.8% in those with locally recurrent cancer. The 40.8% five-year survival in our patients with pulmonary metastases is as expected. Five-year survival for patients undergoing resection of pulmonary metastases at our institution has been reported to vary from 27 to 8% [9-. In contrast, a 5-year survival of only 27.2% for patients with a benign lung condition appears poor. However, this less than expected survival is better understood when one considers that the indication for completion pneumonectomy in many patients with benign lung condition was a life-threatening complication of the initial pulmonary resection and that 27.6% (8 of 29) of the deaths occurred as a complication of completion pneumonectomy. Furthermore, of the late deaths in patients with benign lung disease were due to prior lung cancer.

6 46 The Annals of Thoracic Surgery Vol 46 No 2 August 988 Completion pneumonectomy can only be performed under circumstances in which there is sufficient pulmonary reserve to tolerate loss of the remaining ipsilateral lung and in which the patient's general condition will tolerate the surgical intervention. Moreover, the risk of completion pneumonectomy must be balanced by the benefits of long-term survival. It is interesting in this regard that patients undergoing completion pneumonectomy for benign lung disease have increased operative risk. Much of this risk is the major threat of uncontrollable intraoperative bleeding imposed by an attending inflammatory process that destroys tissue dissection planes about the root of the lung. Time-honored principles for intrapericardial vascular control are all too often frustrated by pericardial obliteration. Additionally, preexisting active pleuropneumonic sepsis places the pneumonectomy space in serious jeopardy. Empyema, bronchial stump dehiscence, respiratory insufficiency, and multisystem failure are common causes of postoperative morbidity and mortality. Meticulous hilar dissection, open pleural drainage, and muscle transposition to reinforce the closed bronchial stump and obliterate pleural space could all contribute to reducing these infection complications in the future. In contrast, patients undergoing completion pneumonectomy for lung cancer and pulmonary metastases tolerate the procedure with no more risk than others who undergo pneumonectomy in a single stage. Longterm survival of these patients undergoing completion pneumonectomy for various types of malignancy is sufficiently satisfactory to justify the risk, true whether the completion pneumonectomy is performed for primary lung cancer, local residual lung cancer, or pulmo- nary metastases from a controlled, remote primary cancer. References Kaplan EL, Meier I? Nonparametric estimation from incomplete observation. J Am Stat Assoc 5:457, 958 American Joint Committee for Cancer Staging and End- Results Reporting: Manual for Staging of Cancer. Chicago, American Joint Committee, 977, 74 pp Gabler A, Liebig S: Reoperation for bronchial carcinoma. Thorax 5:668, 980 Jensik RJ, Faber LP, Kittle CF, Meng RL SuMval following resection for second primary bronchogenic carcinoma. J Thorac Cardiovasc Surg 82:658, 98 Ginsburg RJ, Hill LD, Eagan RT, et al: Modem thlrty day operative mortality for surgical resections in lung cancer. J Thorac Cardiovasc Surg 86654, 98 Pairolero PC, Amold PG, Piehler JM: Intrathoracic transposition of extrathoracic skeletal muscle. J Thorac Cardiovasc Surg 86509, 98 Krowka MJ, Pairolero PC, Trastek VF, et al: Cardiac dysrhythmia following pneumonectomy: cliical correlates and prognostic significance. Chest 9:490, 987 Pairolero PC, Williams DE, Bergstralh EJ, et ai: Postsurgical stage I bronchogenic carcinoma: morbid implications of recurrent disease. Ann Thorac Surg 8:, 984 Creagan ET, Fleming TR, Edmonson JH, Pairolero PC Pulmonary resection for metastatic osteogenic sarcoma. Cancer M908, 979 Jett JR, Hollinger CG, Zinmeister AR, Pairolero PC: Pulmonary resection of metastatic renal cell carcinoma. Chest &Q: 442,98 Manse JK, Zmsmeister AR, Pairolero PC, Jett JR Pulmonary resection of metastatic colarectal adenocarcinoma: a ten year experience. Chest 89:09, 986