CURRENT REVIEW
Current Morbidity, Mortality, and Survival After Bronchoplastic Procedures for Malignancy Mark Tedder, MD, Mark P. Anstadt, MD, Stephen D. Tedder, BS, and James E. Lowe, MD Department of Surgery, Duke University Medical Center, Durham, North Carolina
The number of patients reported to have undergone bronchoplastic procedures has increased nearly fourfold in the past decade. These techniques represent excellent surgical therapy for patients with benign endobronchial lesions, traumatic airway disruptions, or tumors of lowgrade malignant potential, and for select patients with surgically resectable lung cancer. Eighty-nine percent of bronchoplastic procedures are performed for malignancy. We reviewed 1,915 bronchoplastic procedures for carcinoma reported over the past 12 years to determine the incidence of complications and survival. Complications included local recurrence (10.3%), 30-day mortality
(7.5%), pneumonia (6.7%), atelectasis (5.4%), benign stricture or stenosis (5.0%), bronchopleural fistulas (3.5%), empyema (2.8%), bronchovascular fistulas (2.6%),and pulmonary embolism (1.9%).Results were further stratified into sleeve lobectomy and sleeve pneumonectomy groups. Five-year survivals for stage I, 11, and I11 carcinoma were 63%,37%, and 21%, respectively. Sleeve lobectomy for carcinoma extends surgical therapy to select patients with complication rates comparable to pneumonectomy and long-term survival similar to that for conventional resections. (Ann Thorac Surg 1992;54:387-91)
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data regarding postoperative complications, 30-day mortality, and long-term survival. Complication rates were calculated only from reports that explicitly stated the presence or absence of each specific complication. Both early and late complications with special reference to bronchoplastic techniques were determined, including atelectasis, pneumonia, local recurrence, benign stricture or stenosis, empyema, bronchopleural and bronchovascular fistulas, pulmonary embolism, and early death. Complication rates were stratified for sleeve lobectomy and sleeve pneumonectomy. Complication rates for both sleeve lobectomy and pneumonectomy are discussed, because sleeve lobectomy for bronchogenic carcinoma is most commonly performed as an alternative to pneumonectomy. In contrast to complications, 5-year survival frequently was reported by stage of disease. Because there is a marked discrepancy in 5-year survival between preoperative and surgical staging [4], the method of staging was noted for each report that presented survival data by stage of disease.
he number of bronchoplastic procedures reported in the past decade has increased nearly fourfold [ 11. These techniques represent the ideal surgical therapy for large airway injuries, benign strictures, benign endobronchial tumors, and tumors of low-grade malignant potential such as bronchial carcinoids. Conservative resections also extend surgical therapy to those patients who cannot tolerate pneumonectomy because of limited pulmonary function. The most common indication for these procedures is bronchogenic carcinoma (89% of patients [2]). Bronchoplastic procedures are appropriate for approximately 5% to 8% of patients with a resectable pulmonary malignancy [ 11. Although bronchoplastic techniques have been applied to upper and lower lobe lesions in both the right and left lungs, sleeve lobectomy for carcinoma is most often performed for squamous cell carcinoma localized to the right upper lobe orifice [ 3 ] .In such patients, a sleeve lobectomy with regional lymph node dissection achieves the same surgical margins as a pneumonectomy and preserves the middle and lower lobes. Although bronchoplastic procedures have generally been considered safe, a comprehensive review of postoperative complications would help to confirm this. Therefore, recent series of patients with bronchogenic carcinoma treated by bronchoplastic procedures were reviewed to determine the incidence of short-term and long-term complications.
Material and Methods Series of bronchoplastic procedures reported over the past 12 years were reviewed for ones that provided adequate Address reprint requests to Dr Lowe, Department o f Surgery, Duke University Medical Center, PO Box 3954, Durham, NC 27710.
0 1992 by The Society of Thoracic Surgeons
Results Reviewing bronchoplastic procedures for carcinoma over the past 12 years yielded the morbidity, mortality, and 5-year survival of 1,915 patients. The associated morbidity and mortality are summarized in Tables 1 and 2, and complication rates for sleeve lobectomy and sleeve pneumonectomy are presented in Table 3 .
Morbidity The most common postoperative complication was local recurrence (10.3%).However, this occurred in as many as 38.6% of patients [5]. The local recurrence rate was higher 0003-4975/92/$5.00
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Table 1. Complications and Early Mortality in 1,915 Patients After Bronchoplastic Procedures for Malignancf Complication
Local recurrence Thirty-day mortality Pneumonia Atelectasis Benign stricturektenosis Bronchopleural fistula Empyema Bronchovascular fistula Pulmonary embolism a
No. of Patients
Incidence (%)
110/1064 143/1915 32/481 33/614 481966 42/1186 171599 16/615 13/672
10.3 7.5 6.7 5.4 5.0 3.5 2.8 2.6 1.9
Data are taken from references [2, 5-28]
Table 3 . Complications and Early Mortality After Sleeve Lobectomy" and Sleeve Pneumonectomy" for Malignancy Complication Local recurrence Pneumonia Thirty-day mortality Atelectasis
Benign stricturelstenosis Bronchopleural fistula Bronchovascular fistula Pulmonary embolus
Empyema a
for patients treated by sleeve lobectomy (12.5%) than those treated by sleeve pneumonectomy (4.2%). Postoperative pneumonia was the second most frequent complication, reported in 6.7% (1.4% to 21.1%) of patients (see Table 1). The incidence of postoperative pneumonia was frequently stratified by procedure, and was 9.9% for sleeve lobectomy and 16.7% for sleeve pneumonectomy. However, the failure of several large series to separate complications into procedure-related groups explains the apparent inconsistency between overall and stratified complication rates. Atelectasis complicated 5.4% of bronchoplastic procedures for carcinoma, and represented the third most common complication (see Table 1). The incidence after sleeve lobectomy was 5.2%. Atelectasis occurred only slightly more often than benign stricture or stenosis, which was documented in 5.0% (0% to 18%)[6-17, 29-32] of patients (see Table 1).Sleeve lobectomy was associated with a 4.8% incidence of stricture or stenosis (see Table 3). The cause was either technical ("kink' stenosis) or related to suture granuloma formation. Bronchopleural fistula represented the next most common complication, occurring in 3.5% of patients (see Table I). The incidence was 3.0% after sleeve lobectomy and 10.1% after sleeve pneumonectomy (see Table 3). Other serious complications included empyema (2.8%), bronchovascular fistula (2.6%),and pulmonary embolism (1.9%). Infrequent complications included dysrhythmias
Table 2 , Early Mortalitf After Bronchoplastic Procedures for Mali~nancy~ Cause
Respiratory failure Cardiac event Pneumonia Pulmonary embolus Bronchopleural fistula Bronchovascular fistula Empyema
Number of Patients
Incidence (%)
19/91 18/91 14/91 13/91 8/91 5/91 2/91
20.9 19.8 15.4 14.3 8.8 5.5 2.2
30-day mortality in the 911143 patients (64%) where the cause of death was explicitly stated. Data are taken from references 12, 5-28].
Sleeve
Sleeve
Lobectomy
Pneumonectomy
12.5% (84/673) 9.9% (14/141) 5.5% (62/1125) 5.2% (20/383) 4.8% (331694) 3.0% (171565) 2.5% (12/475) 2.3% (10/436) 2.0% (61294)
4.2% (3/72) 16.7% (12172) 20.9% (29/139)
... ... 10.1% (14/139) 2.9% (1134) 2.1% (2/93) 8.6% (8193)
Data are taken from references [2, 5 8 ,10, 12-15, 18-20, 22, 251.
I,Data are taken from references (7, 26281.
[6, 10, 331, cerebrovascular accident [7, 181, recurrent laryngeal nerve palsy [lo], deep venous thrombosis [lo], chylothorax [30], colonic perforation [30], cecal volvulus [30], tension pneumothorax [9], and agranulocytosis [ 191.
Mortality The 30-day mortality for bronchoplastic techniques performed for malignancy was 7.5% (see Table 1).The causes of death were specified in 64% (91/143)of early deaths and are summarized in Table 2. The incidence was 5.5% for sleeve lobectomy and 20.9% for sleeve pneumonectomy (see Table 3). More than 20% of early deaths were attributed to respiratory failure (see Table 2). Cardiac events lead to 19.8% of the early deaths and consisted of myocardial infarction, congestive heart failure, and malignant ventricular dysrhythmias. Pulmonary embolism caused 14.3% of the early deaths. Bronchopleural and bronchovascular fistulas represented 8.8% and 5.5% of the early deaths, respectively. Two patients died of empyema in the early postoperative period [8, 151. Faber and colleagues [29] reported a patient who could not be ventilated adequately during the procedure and died intraoperatively . Pulmonary artery thrombosis [7, 181, pulmonary infarction [33], tension pneumothorax [9], gastrointestinal hemorrhage [8, 301, cerebrovascular accident [7, 161, sepsis [20], colonic perforation [15], adult respiratory distress syndrome [19,29], agranulocytosis [ 191, and "shock' after decortication for postoperative hemothorax [13] were rare causes of early mortality.
Survival In this review, the 5-year survival of patients undergoing sleeve lobectomy for bronchogenic carcinoma was 40% (245/614) [ 5 7 , 14, 211. Sleeve lobectomy for stage I, 11, and I11 disease yielded 63%, 37%, and 21% 5-year survivals, respectively. Approximately one-third of patients were staged preoperatively. Absence of nodal involvement was associated with a 60% 5-year survival [lo, 14, 20-221.
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Comment Bronchoplastic procedures for benign lesions are rarely associated with serious morbidity [2, 6, 7, 20, 34-39]. In addition, 96% of patients with bronchial carcinoids treated by such techniques survive 5 years [l].Because the published results of conservative resections for benign pathology are uniformly excellent, this review focused on results of bronchoplastic techniques performed for bronchogenic carcinoma. Nearly 75% of all bronchoplastic procedures for pulmonary malignancy have been reported in the past decade [l]. This review has attempted to objectively summarize current complication rates reported during the past 12 years. When calculating the incidence of a complication, reports that did not explicitly state the absence of that complication were deleted. It is important to realize that most authors did not report the absence of complications; therefore, the incidence of complications may be overestimated. The most common complication was local recurrence. Local recurrence represents an unfortunate and serious problem after both standard pulmonary resections and bronchoplastic procedures. Regrettably, most authors did not define local recurrence. Some authors only considered tumor at the suture line as local recurrence, whereas others included subsequent malignancy in intrathoracic lymph nodes or pulmonary sites remote from the initial resection. Therefore, the true ramifications of the 10.3% incidence of local recurrence in this review are less clear. A possible explanation for suture line recurrence may be lung preservation at the expense of adequate bronchial margins. Paulson and associates [30] recommend that patients undergoing bronchial resection have margins of at least 1.5 to 2.0 cm. Frozen sections of the resected specimen should minimize the risk of an incomplete resection. Local recurrence after a sleeve lobectomy in patients without evidence of extensive nodal or metastatic disease may require completion pneumonectomy [ 11-13, 18, 291. Both variable follow-up and incomplete initial resection limit the accuracy in reporting recurrence rates. There is an inherent potential for postoperative pneumonia in patients treated by conservative resections. For example, a compromised bronchial anastomosis, regardless of cause, may increase the chance of subsequent pneumonia. This may result from atelectasis or an impaired ability to clear secretions. The incidence of postoperative pneumonia in this review was 6.7%. Atelectasis has been reported to be the most common complication after bronchoplastic procedures [2]. Technical errors in bronchial approximation, lymphatic interruption, local postoperative bronchial edema, and partial or complete denervation of the remaining lung may potentially contribute to atelectasis, and are unique to these resections [21]. Although this review only noted a 5.4% incidence of postoperative atelectasis, the variability of published reports (2% to 20%) [2, 6, 8-11, 18, 19, 21, 231 may be explained by various definitions and diligence in reporting. Intraoperative creation of an optimal bronchial anastomosis, perioperative attention to pulmonary hy-
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giene, and early ambulation all serve to minimize postoperative atelectasis and pneumonia. Although the cumulative incidence of benign stricture or stenosis including suture granuloma formation was 5.0%, the occurrence of suture granulomas has markedly diminished with the decreased use of silk for the bronchial anastomosis [6]. Absorbable suture is considered superior by many surgeons to nonabsorbable monofilament material [40]. Furthermore, strict attention must be given to bronchial stump alignment to minimize kinking and tension at the anastomosis. The treatment of benign strictures or stenoses by bronchoscopic dilation or bronchoscopic suture excision usually yields acceptable results 16, 9, 11, 23, 30, 311. Laser excision has been used succes fully in patients in whom strictures develop from granulation tissue [41]. Occasionally, early revision of the bronchial anastomosis is necessary [6, 7, 291, and it is preferred over a late completion pneumonectomy . Like benign strictures and stenoses, bronchopleural fistulas cause substantial morbil’ ity; in this review they occurred in 3.5% of patients. I his compares favorably with the 3.7% incidence (18148, ) reported after pneumonectomy [42]. Collective series of conventional pulmonary resections have documented similar bronchopleural fistula complication rates (2.7% to 4.39: ) [43, 441. Bronchopleural fistulas may result from ischemia at the bronchial anastomosis. Accordingly, bronchial dissection and orientation for reanastomosis must be performed with minimal disruption of vascular supply. It is currently accepted that pleural flaps do not augment perfusion at the bronchial anastomosis and, therefore, do not assist in win. preventing bronchopleural fistulas of ischemic However, most surgeons cover the bronchial anastoi As with tissue to provide a physical barrier to the deveiopment of bronchopleural as well as bronchovascular fistulas. Another potentially fatal complication of bronchoplastic techniques is bronchovascular fistula. These patients typically are seen with massive hemoptysis. Vogt-Moykopf and associates [24] noted 7 patients who died of “acute pulmonary hemorrhage.” Ayabe and co-workers [9] also reported a patient who died on the first postoperative day of ”bleeding.” This patient experienced a segmental resection of the left pulmonary artery in combination with a left upper sleeve lobectomy. Two additional deaths were reported by Keszler [19]: in 1 patient a concomitant pulmonary artery resection was performed; in the other, ”reliable tissues” did not separate the pulmonary artery from the bronchial anastomosis. These additional deaths may represent bronchovascular fistulas and suggest that the incidence is greater than the 2.6% found in this review. Mortality after this complication was 100%whenever the outcome was explicitly stated [5, 9, 14, 18, 20, 25, 451. The most important method of prevention is tissue coverage of the bronchial anastomosis. This is most commonly performed using a pleural flap; however, the use of free pericardium has also been reported [6]. This complication represents a potential drawback to sleeve resections. 01
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In addition to bronchovascular and bronchopleural fistulas, empyema also complicates bronchoplastic procedures. Although sleeve resection leaves a substantially smaller pleural space than pneumonectomy, the incidence of postoperative empyema in patients treated by sleeve lobectomy was similar to that for pneumonectomy (2.0% versus 1%to 3% [43], respectively). Distinct from the aforementioned bronchial, parenchymal, and pleural complications is the incidence of pulmonary embolism. Although the actual incidence of pulmonary embolism is difficult to assess, it was documented in 13 of 672 patients (1.9%), comprised 14.3% of early deaths, and was universally fatal. The 30-day mortality of 7.5% is similar to that of other reported series [2]. The marked disparity between the early mortalities for sleeve lobectomy (5.5%) and sleeve pneumonectomy (20.9%) serves to emphasize the point that sleeve pneumonectomy should be reserved for the rare surgical candidate with tumor confined to the carina or tracheobronchial angle. Sleeve lobectomy for carcinoma is frequently employed as an alternative to, and is technically more demanding- than, pneumonectomy; however, in this review, the 30-day mortality for sleeve lobectomy was 5.5%. This compares favorably with the 6.2% early mortality after pneumonectomy reported by the Lung Cancer Study Group [47]. Five-year survivals for patients with stage I, 11, and 111 disease were 63%, 37%, and 21%, respectively. When one corrects for the percentage of patients staged preoperatively in this review, the predicted 5-year survivals for conventional procedures would be 58%, 37%, and 22% for stage I, 11, and 111 disease, respectively [4]. In addition, the 5-year survival for NO disease in this review (60%) is similar to that for conventional resections (63%)[4]. These data confirm that in appropriately selected patients survival is not compromised by conservative resections. With comparable long-term survival, sleeve lobectomy has the potential advantage over conventional resections of preserving lung function. Pulmonary function after sleeve lobectomy has been reported infrequently. Wood and associates [48] noted maximal impairment in oxygen uptake 3 days postoperatively from sleeve lobectomy relative to lobectomy in an experimental model. However, 28 days postoperatively, the groups had comparable oxygen uptake. Rees and Paneth [32] noted minimal differences in pulmonary function tests of 6 patients who underwent sleeve lobectomy for malignancy. Deslauriers and colleagues [21] noted no functional pulmonary loss after sleeve lobectomy for carcinoma in 15 patients; they attributed this to the resection of impaired lung, cessation of smoking, and improved postoperative pulmonary hygiene. The role of radiation therapy before sleeve lobectomy for carcinoma has been disputed. Paulson [49], Bennett [MI, and Ungar [22] and their respective associates recommend preoperative irradiation and reported 5-year survivals as high as 52% (patient population not defined). However, the only double-blind study designed to address this issue concluded that preoperative radiation therapy did not prolong survival [50]. Because Faber [50]
Ann Thorac Surg 1992;54:387-91
found that patients treated with preoperative irradiation experienced no increase in complications, he recommended considering radiation therapy in the patient with impaired pulmonary function and a large bulky central tumor. Patients with central tumors may be candidates for sleeve pneumonectomies, which are associated with a 30-day mortality of 20.9% (29/139) [7, 26281 and a higher complication rate (see Table 3) than either sleeve lobectomy or pneumonectomy. In particular, postoperative pneumonia (16.7%), bronchopleural fistula (10.1%), and empyema (8.6%) are relatively common. This group of patients represented 63% (12/19) of all patients who died of respiratory failure. With such a high morbidity and mortality, it appears that this procedure should be limited to patients with large tumors isolated to the carina or tracheobronchial angle, with adequate cardiopulmonary reserve, and who are in otherwise good health. In summary, review of all clinical data available for bronchogenic carcinoma treated by sleeve lobectomy shows a similar morbidity and mortality to that of pneumonectomy, with preservation of lung function. In addition, when stratified by stage, long-term survival of patients treated by sleeve lobectomy is comparable with the accepted survivals for conventional resections. Therefore, sleeve lobectomy represents a safe and effective therapy for select patients with pulmonary malignancy.
References 1. Lowe JE, Sabiston DC Jr. Bronchoplastic techniques in the surgical management of benign and malignant pulmonary lesions. In: Sabiston DC Jr, Spencer FC, eds. Surgery of the chest. Philadelphia: W.B. Saunders, 1990577. 2. Lowe JE, Bridgman AH, Sabiston DC Jr. The role of bronchoplastic procedures in the surgical management of benign and malignant pulmonan/ lesions. J Thorac Cardiovasc Surg 1982;83:227-34.' Urschel HC. Razzuk MA. Bronchoplastic procedures. In: 3. Glenn WWL, Baue AE, Geha AS, Hammodd GL, Laks H, eds. Thoracic and cardiovascular surgery. East Norwalk, CT: Appleton-Century-Crofts, 1983:431. 4. Mountain CF. A new international staging system for lung cancer. Chest 1986;89(Suppl4):225~-33~. 5. Weisel RD, Cooper JD, Delarue NC, Therman TE, Todd TRJ, Pearson FG. Sleeve lobectomy for carcinoma of the lung. J rhorac Cardiovasc Surg 1979;78:839-49. 6. Frist WH, Mathisen DJ, Hilgenberg AD, Grillo HC. Bronchial sleeve resection with and without pulmonary resection. J rhorac Cardiovasc Surg 1987;93:35G7. 7. Watanabe Y, Shimizu J, Oda M, et al. Results in 104 patients undergoing bronchoplastic procedures for bronchial lesions. Ann Thorac Surg 1990;50:607-14. 8. Robinson CLN, Holmes D, Jamieson WRE. Lobectomy and bronchoplasty for cancer. Can J Surg 1981;24:196-7. 9. Ayabe H, Nakamura Y, Miura T, Kugimiya T, Koga Y, Tsuji Y. Bronchoplasty for bronchogenic carcinoma. World J Surg 1982;6:433-9. 10. Firmin RK, Azariades M, Lennox SC, Lincoln JCR, Paneth M. Sleeve lobectomy (lobectomy and bronchoplasty) for bronchial carcinoma. Ann Thorac Surg 1983;35:442-9. 11 Belli L, Meroni A, Rondinara G, Beati CA. Bronchoplastic procedures and pulmonary artery reconstruction in the treatment of bronchogenic cancer. J Thorac Cardiovasc Surg 1985;90:167-71. 12 Vanderhoeft P. Bronchoplastic lobectomies for advanced
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carcinoma: functional changes and survival. Acta Chir Belg 1978;4:293-302. Shaw KM, Luke DA. Lobectomy with sleeve resection of the bronchus for malignant disease of the lung and the influence of the suture material used for the bronchial repair. Thorac Cardiovasc Surg 1979;27325-9. Sartori F, Binda R, Spreafico G, et al. Sleeve lobectomy in the treatment of bronchogenic carcinoma. Int Surg 1986;71: 233-6. Roder OC, Christensen JB, Andersen C, Andersen K, Oxhoj H. Bronchoplastic procedures for bronchial carcinoma. Scand J Thorac Cardiovasc Surg 1987;21:109-11. Maeda M, Nanjo 5,Nakamura K, Nakamoto K. Tracheobronchoplasty for lung cancer. Int Surg 1986;71:221-8. Naruke T. Bronchoplastic and bronchovascular procedures of the tracheobronchial tree in the management of primary lung cancer. Chest 1989;96:53S-65. Bennett WF, Smith RA. A twenty-year analysis of the results of sleeve resection for primary bronchogenic carcinoma. J Thorac Cardiovasc Surg 1978;76:840-5. Keszler P. Sleeve resection and other bronchoplasties in the surgery of bronchogenic tumors. Int Surg 1986;71:229-32. Van Den Bosch JMM, Bergstein PGM, Laros CD, Gelissen HJ, van Riempst S, Wagenaar SS. Lobectomy with sleeve resection in the treatment of tumors of the bronchus. Chest 1981;80:154-7. Deslauriers J, Gaulin P, Beaulieu M, Piraux M, Bernier R, Lormier Y. Long-term clinical and functional results of sleeve lobectomy for primary lung cancer. J Thorac Cardiovasc Surg 1986;92:871-9. Ungar 1, Gyeney 1, Sherer E, Szarvas 1. Sleeve lobectomy: an alternative to pneumonectomy in the treatment of bronchial carcinoma. Thorac Cardiovasc Surg 1981;29:41-6. Cataldo I, Bedini AV, Lequaglie C, Ongari M, Valente M, Ravasi G. Late results after sleeve or wedge lobectomies for non-small cell lung carcinoma. Tumori 1988;74:71-3. Vogt-Moykopf I, Fritz T, Meyer G, Bulzerbruck H, Daskos G. Bronchoplastic and angioplastic operation in bronchial carcinoma: long-term results of a retrospective analysis from 1973 to 1983. lnt Surg 1986;71:211-20. Kittle CF. Atypical resections of the lung: bronchoplasties, sleeve resections, and segmentectomiestheir evolution and present status. Curr Probl Surg 1989;63-131. Deslauriers J, Beaulieu M, McClish A. Tracheal-sleeve pneumonectomy. In: Shields TW, ed. General thoracic surgery. 3rd ed. Philadelphia: Lea & Febiger, 1989:382-7. Jensik RJ, Faber LP, Kittle CF, Miley RW, Thatcher WC, El-Baz N. Survival in patients undergoing tracheal sleeve pneumonectomy for bronchogenic carcinoma. J Thorac Cardiovasc Surg 1982;84:489-96. Dartevelle PG, Khalife J, Chapelier A, et al. Tracheal sleeve pneumonectomy for bronchogenic carcinoma: report of 55 cases. Ann Thorac Surg 1988;46:6%72. Faber LP, Jensik RJ, Kittle CF. Results of sleeve lobectomy for bronchogenic carcinoma in 101 patients. Ann Thorac Surg 1984;37279-85. Paulson DL, Urschel HC Jr, McNamara JJ, Shaw RR. Bronchoplastic procedures for bronchogenic carcinoma. J Thorac Cardiovasc Surg 1970;59:3848. Jensik RJ, Faber LP, Milloy FJ, Amato JJ. Sleeve lobectomy for carcinoma. J Thorac Cardiovasc Surg 1972;64:400-12.
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32. Rees GM, Paneth M. Lobectomy with sleeve resection in the treatment of bronchial tumors. Thorax 1970;25:160-4. 33. Deslauriers J, Beaulieu M, Benazera A, McClish A. Sleeve pneumonectomy for bronchogenic carcinoma. Ann Thorac Surg 1979;28:465-74. 34. Jensik RJ, Faber LP, Brown CM, Kittle CF. Bronchoplastic and conservative resectional procedures for bronchial adenoma. J Thorac Cardiovasc Surg 1974;68:556. 35. Okike J, Bernatz PE, Payne WS, Woolner LB, Leonard PF. Bronchoplastic procedures in the treatment of carcinoid tumors of the tracheobronchial tree. J Thorac Cardiovasc Surg 1978;76:281. 36. Salminen US, Halttunen P, Miettinen M, Mattila S. Bronchoplastic procedures in the treatment of endobronchial carcinoid tumors. Scand J Thorac Cardiovasc Surg 1990;24:27-32. 37. Todd TR, Cooper JD, Weissberg D, Delarue N, Pearson FG. Bronchial carcinoid tumors. J Thorac Cardiovasc Surg 1980; 79:532-6. 38. Toledo J, Roca R, Anton ]A, Martin de Nicolas JL, Varela G, Yuste P. Conservative and bronchoplastic resection for bronchial carcinoid tumours. Eur J Cardiothorac Surg 1989;3: 288-91. 39. Hurt R. Benign tumours of the bronchus and trachea. Ann R Coll Surg Engl 1984;66:22. 40. Hsieh CM, Tomita M, Ayabe H, Kawahara K, Hasegawa H, Yoshida R. Influence of suture on bronchial anastomosis in growing puppies. J Thorac Cardiovasc Surg 1988;95: 998-1002. 41. Wolfe WG, Sabiston DC Jr. Management of benign and malignant lesions of the trachea and bronchi with the neodymium-yttrium-aluminum-garnet laser. J Thorac Cardiovasc Surg 1986;91:40-5. 42. Vester SR, Faber LP, Kittle CF, Warren WH, Jensik RJ. Bronchopleural fistula after stapled closure of the bronchus. Ann Thorac Surg 1991;52:1253-8. 43. Hankins JR, Miller JE, Attar 5,Satterfield JR, McLaughlin IS. Bronchopleural fistula: thirteen-year experience with 77 cases. J Thorac Cardiovasc Surg 1978;76:755-62. 44. Williams NS, Lewis CT. Bronchopleural fistula: a review of 86 cases. Br J Surg 1976;63:520-2. 45. Nagasaki F, Flehinger BJ, Martini N. Complications of surgery in the treatment of carcinoma of the lung. Chest 1982;82:25-9. 46. Shields TW. Carcinoma of the lung. In: Shields TW, ed. General thoracic surgery. 3rd ed. Philadelphia: Lea & Febiger, 1989:368. 47. Ginsberg RJ, Hill LD, Eagan RT, et al. Modern thirty-day operative mortality for surgical resections in lung cancer. J Thorac Cardiovasc Surg 1983;86:6548. 48. Wood PB, Gilday D, Ilves R, Rae 5,Pearson FG. A comparison of gas exchange after simple lobectomy and lobectomy with sleeve resection in dogs. J Thorac Cardiovasc Surg 1974;68:64&53. 49. Jensik RJ. Preoperative irradiation and bronchopulmonary sleeve resection for lung cancer. Surg Clin North Am 1966; 46345-59. 50. Faber LP. Results of surgical trearment of stage 111 lung carcinoma with carinal proximity-the role of sleeve lobectomy versus pneumonectomy and the role of sleeve pneumonectomy. Surg Clin North Am 1987;67:1001-14.
Current Morbidity, Mortality, and Survival After Bronchoplastic Procedures for Malignancy Mark Tedder, MD, Mark P. Anstadt, MD, Stephen D. Tedder, BS, and James E. Lowe, MD Department of Surgery, Duke University Medical Center, Durham, North Carolina
The number of patients reported to have undergone bronchoplastic procedures has increased nearly fourfold in the past decade. These techniques represent excellent surgical therapy for patients with benign endobronchial lesions, traumatic airway disruptions, or tumors of lowgrade malignant potential, and for select patients with surgically resectable lung cancer. Eighty-nine percent of bronchoplastic procedures are performed for malignancy. We reviewed 1,915 bronchoplastic procedures for carcinoma reported over the past 12 years to determine the incidence of complications and survival. Complications included local recurrence (10.3%), 30-day mortality
(7.5%), pneumonia (6.7%), atelectasis (5.4%), benign stricture or stenosis (5.0%), bronchopleural fistulas (3.5%), empyema (2.8%), bronchovascular fistulas (2.6%),and pulmonary embolism (1.9%).Results were further stratified into sleeve lobectomy and sleeve pneumonectomy groups. Five-year survivals for stage I, 11, and I11 carcinoma were 63%,37%, and 21%, respectively. Sleeve lobectomy for carcinoma extends surgical therapy to select patients with complication rates comparable to pneumonectomy and long-term survival similar to that for conventional resections. (Ann Thorac Surg 1992;54:387-91)
T
data regarding postoperative complications, 30-day mortality, and long-term survival. Complication rates were calculated only from reports that explicitly stated the presence or absence of each specific complication. Both early and late complications with special reference to bronchoplastic techniques were determined, including atelectasis, pneumonia, local recurrence, benign stricture or stenosis, empyema, bronchopleural and bronchovascular fistulas, pulmonary embolism, and early death. Complication rates were stratified for sleeve lobectomy and sleeve pneumonectomy. Complication rates for both sleeve lobectomy and pneumonectomy are discussed, because sleeve lobectomy for bronchogenic carcinoma is most commonly performed as an alternative to pneumonectomy. In contrast to complications, 5-year survival frequently was reported by stage of disease. Because there is a marked discrepancy in 5-year survival between preoperative and surgical staging [4], the method of staging was noted for each report that presented survival data by stage of disease.
he number of bronchoplastic procedures reported in the past decade has increased nearly fourfold [ 11. These techniques represent the ideal surgical therapy for large airway injuries, benign strictures, benign endobronchial tumors, and tumors of low-grade malignant potential such as bronchial carcinoids. Conservative resections also extend surgical therapy to those patients who cannot tolerate pneumonectomy because of limited pulmonary function. The most common indication for these procedures is bronchogenic carcinoma (89% of patients [2]). Bronchoplastic procedures are appropriate for approximately 5% to 8% of patients with a resectable pulmonary malignancy [ 11. Although bronchoplastic techniques have been applied to upper and lower lobe lesions in both the right and left lungs, sleeve lobectomy for carcinoma is most often performed for squamous cell carcinoma localized to the right upper lobe orifice [ 3 ] .In such patients, a sleeve lobectomy with regional lymph node dissection achieves the same surgical margins as a pneumonectomy and preserves the middle and lower lobes. Although bronchoplastic procedures have generally been considered safe, a comprehensive review of postoperative complications would help to confirm this. Therefore, recent series of patients with bronchogenic carcinoma treated by bronchoplastic procedures were reviewed to determine the incidence of short-term and long-term complications.
Material and Methods Series of bronchoplastic procedures reported over the past 12 years were reviewed for ones that provided adequate Address reprint requests to Dr Lowe, Department o f Surgery, Duke University Medical Center, PO Box 3954, Durham, NC 27710.
0 1992 by The Society of Thoracic Surgeons
Results Reviewing bronchoplastic procedures for carcinoma over the past 12 years yielded the morbidity, mortality, and 5-year survival of 1,915 patients. The associated morbidity and mortality are summarized in Tables 1 and 2, and complication rates for sleeve lobectomy and sleeve pneumonectomy are presented in Table 3 .
Morbidity The most common postoperative complication was local recurrence (10.3%).However, this occurred in as many as 38.6% of patients [5]. The local recurrence rate was higher 0003-4975/92/$5.00
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Table 1. Complications and Early Mortality in 1,915 Patients After Bronchoplastic Procedures for Malignancf Complication
Local recurrence Thirty-day mortality Pneumonia Atelectasis Benign stricturektenosis Bronchopleural fistula Empyema Bronchovascular fistula Pulmonary embolism a
No. of Patients
Incidence (%)
110/1064 143/1915 32/481 33/614 481966 42/1186 171599 16/615 13/672
10.3 7.5 6.7 5.4 5.0 3.5 2.8 2.6 1.9
Data are taken from references [2, 5-28]
Table 3 . Complications and Early Mortality After Sleeve Lobectomy" and Sleeve Pneumonectomy" for Malignancy Complication Local recurrence Pneumonia Thirty-day mortality Atelectasis
Benign stricturelstenosis Bronchopleural fistula Bronchovascular fistula Pulmonary embolus
Empyema a
for patients treated by sleeve lobectomy (12.5%) than those treated by sleeve pneumonectomy (4.2%). Postoperative pneumonia was the second most frequent complication, reported in 6.7% (1.4% to 21.1%) of patients (see Table 1). The incidence of postoperative pneumonia was frequently stratified by procedure, and was 9.9% for sleeve lobectomy and 16.7% for sleeve pneumonectomy. However, the failure of several large series to separate complications into procedure-related groups explains the apparent inconsistency between overall and stratified complication rates. Atelectasis complicated 5.4% of bronchoplastic procedures for carcinoma, and represented the third most common complication (see Table 1). The incidence after sleeve lobectomy was 5.2%. Atelectasis occurred only slightly more often than benign stricture or stenosis, which was documented in 5.0% (0% to 18%)[6-17, 29-32] of patients (see Table 1).Sleeve lobectomy was associated with a 4.8% incidence of stricture or stenosis (see Table 3). The cause was either technical ("kink' stenosis) or related to suture granuloma formation. Bronchopleural fistula represented the next most common complication, occurring in 3.5% of patients (see Table I). The incidence was 3.0% after sleeve lobectomy and 10.1% after sleeve pneumonectomy (see Table 3). Other serious complications included empyema (2.8%), bronchovascular fistula (2.6%),and pulmonary embolism (1.9%). Infrequent complications included dysrhythmias
Table 2 , Early Mortalitf After Bronchoplastic Procedures for Mali~nancy~ Cause
Respiratory failure Cardiac event Pneumonia Pulmonary embolus Bronchopleural fistula Bronchovascular fistula Empyema
Number of Patients
Incidence (%)
19/91 18/91 14/91 13/91 8/91 5/91 2/91
20.9 19.8 15.4 14.3 8.8 5.5 2.2
30-day mortality in the 911143 patients (64%) where the cause of death was explicitly stated. Data are taken from references 12, 5-28].
Sleeve
Sleeve
Lobectomy
Pneumonectomy
12.5% (84/673) 9.9% (14/141) 5.5% (62/1125) 5.2% (20/383) 4.8% (331694) 3.0% (171565) 2.5% (12/475) 2.3% (10/436) 2.0% (61294)
4.2% (3/72) 16.7% (12172) 20.9% (29/139)
... ... 10.1% (14/139) 2.9% (1134) 2.1% (2/93) 8.6% (8193)
Data are taken from references [2, 5 8 ,10, 12-15, 18-20, 22, 251.
I,Data are taken from references (7, 26281.
[6, 10, 331, cerebrovascular accident [7, 181, recurrent laryngeal nerve palsy [lo], deep venous thrombosis [lo], chylothorax [30], colonic perforation [30], cecal volvulus [30], tension pneumothorax [9], and agranulocytosis [ 191.
Mortality The 30-day mortality for bronchoplastic techniques performed for malignancy was 7.5% (see Table 1).The causes of death were specified in 64% (91/143)of early deaths and are summarized in Table 2. The incidence was 5.5% for sleeve lobectomy and 20.9% for sleeve pneumonectomy (see Table 3). More than 20% of early deaths were attributed to respiratory failure (see Table 2). Cardiac events lead to 19.8% of the early deaths and consisted of myocardial infarction, congestive heart failure, and malignant ventricular dysrhythmias. Pulmonary embolism caused 14.3% of the early deaths. Bronchopleural and bronchovascular fistulas represented 8.8% and 5.5% of the early deaths, respectively. Two patients died of empyema in the early postoperative period [8, 151. Faber and colleagues [29] reported a patient who could not be ventilated adequately during the procedure and died intraoperatively . Pulmonary artery thrombosis [7, 181, pulmonary infarction [33], tension pneumothorax [9], gastrointestinal hemorrhage [8, 301, cerebrovascular accident [7, 161, sepsis [20], colonic perforation [15], adult respiratory distress syndrome [19,29], agranulocytosis [ 191, and "shock' after decortication for postoperative hemothorax [13] were rare causes of early mortality.
Survival In this review, the 5-year survival of patients undergoing sleeve lobectomy for bronchogenic carcinoma was 40% (245/614) [ 5 7 , 14, 211. Sleeve lobectomy for stage I, 11, and I11 disease yielded 63%, 37%, and 21% 5-year survivals, respectively. Approximately one-third of patients were staged preoperatively. Absence of nodal involvement was associated with a 60% 5-year survival [lo, 14, 20-221.
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Comment Bronchoplastic procedures for benign lesions are rarely associated with serious morbidity [2, 6, 7, 20, 34-39]. In addition, 96% of patients with bronchial carcinoids treated by such techniques survive 5 years [l].Because the published results of conservative resections for benign pathology are uniformly excellent, this review focused on results of bronchoplastic techniques performed for bronchogenic carcinoma. Nearly 75% of all bronchoplastic procedures for pulmonary malignancy have been reported in the past decade [l]. This review has attempted to objectively summarize current complication rates reported during the past 12 years. When calculating the incidence of a complication, reports that did not explicitly state the absence of that complication were deleted. It is important to realize that most authors did not report the absence of complications; therefore, the incidence of complications may be overestimated. The most common complication was local recurrence. Local recurrence represents an unfortunate and serious problem after both standard pulmonary resections and bronchoplastic procedures. Regrettably, most authors did not define local recurrence. Some authors only considered tumor at the suture line as local recurrence, whereas others included subsequent malignancy in intrathoracic lymph nodes or pulmonary sites remote from the initial resection. Therefore, the true ramifications of the 10.3% incidence of local recurrence in this review are less clear. A possible explanation for suture line recurrence may be lung preservation at the expense of adequate bronchial margins. Paulson and associates [30] recommend that patients undergoing bronchial resection have margins of at least 1.5 to 2.0 cm. Frozen sections of the resected specimen should minimize the risk of an incomplete resection. Local recurrence after a sleeve lobectomy in patients without evidence of extensive nodal or metastatic disease may require completion pneumonectomy [ 11-13, 18, 291. Both variable follow-up and incomplete initial resection limit the accuracy in reporting recurrence rates. There is an inherent potential for postoperative pneumonia in patients treated by conservative resections. For example, a compromised bronchial anastomosis, regardless of cause, may increase the chance of subsequent pneumonia. This may result from atelectasis or an impaired ability to clear secretions. The incidence of postoperative pneumonia in this review was 6.7%. Atelectasis has been reported to be the most common complication after bronchoplastic procedures [2]. Technical errors in bronchial approximation, lymphatic interruption, local postoperative bronchial edema, and partial or complete denervation of the remaining lung may potentially contribute to atelectasis, and are unique to these resections [21]. Although this review only noted a 5.4% incidence of postoperative atelectasis, the variability of published reports (2% to 20%) [2, 6, 8-11, 18, 19, 21, 231 may be explained by various definitions and diligence in reporting. Intraoperative creation of an optimal bronchial anastomosis, perioperative attention to pulmonary hy-
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giene, and early ambulation all serve to minimize postoperative atelectasis and pneumonia. Although the cumulative incidence of benign stricture or stenosis including suture granuloma formation was 5.0%, the occurrence of suture granulomas has markedly diminished with the decreased use of silk for the bronchial anastomosis [6]. Absorbable suture is considered superior by many surgeons to nonabsorbable monofilament material [40]. Furthermore, strict attention must be given to bronchial stump alignment to minimize kinking and tension at the anastomosis. The treatment of benign strictures or stenoses by bronchoscopic dilation or bronchoscopic suture excision usually yields acceptable results 16, 9, 11, 23, 30, 311. Laser excision has been used succes fully in patients in whom strictures develop from granulation tissue [41]. Occasionally, early revision of the bronchial anastomosis is necessary [6, 7, 291, and it is preferred over a late completion pneumonectomy . Like benign strictures and stenoses, bronchopleural fistulas cause substantial morbil’ ity; in this review they occurred in 3.5% of patients. I his compares favorably with the 3.7% incidence (18148, ) reported after pneumonectomy [42]. Collective series of conventional pulmonary resections have documented similar bronchopleural fistula complication rates (2.7% to 4.39: ) [43, 441. Bronchopleural fistulas may result from ischemia at the bronchial anastomosis. Accordingly, bronchial dissection and orientation for reanastomosis must be performed with minimal disruption of vascular supply. It is currently accepted that pleural flaps do not augment perfusion at the bronchial anastomosis and, therefore, do not assist in win. preventing bronchopleural fistulas of ischemic However, most surgeons cover the bronchial anastoi As with tissue to provide a physical barrier to the deveiopment of bronchopleural as well as bronchovascular fistulas. Another potentially fatal complication of bronchoplastic techniques is bronchovascular fistula. These patients typically are seen with massive hemoptysis. Vogt-Moykopf and associates [24] noted 7 patients who died of “acute pulmonary hemorrhage.” Ayabe and co-workers [9] also reported a patient who died on the first postoperative day of ”bleeding.” This patient experienced a segmental resection of the left pulmonary artery in combination with a left upper sleeve lobectomy. Two additional deaths were reported by Keszler [19]: in 1 patient a concomitant pulmonary artery resection was performed; in the other, ”reliable tissues” did not separate the pulmonary artery from the bronchial anastomosis. These additional deaths may represent bronchovascular fistulas and suggest that the incidence is greater than the 2.6% found in this review. Mortality after this complication was 100%whenever the outcome was explicitly stated [5, 9, 14, 18, 20, 25, 451. The most important method of prevention is tissue coverage of the bronchial anastomosis. This is most commonly performed using a pleural flap; however, the use of free pericardium has also been reported [6]. This complication represents a potential drawback to sleeve resections. 01
9
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In addition to bronchovascular and bronchopleural fistulas, empyema also complicates bronchoplastic procedures. Although sleeve resection leaves a substantially smaller pleural space than pneumonectomy, the incidence of postoperative empyema in patients treated by sleeve lobectomy was similar to that for pneumonectomy (2.0% versus 1%to 3% [43], respectively). Distinct from the aforementioned bronchial, parenchymal, and pleural complications is the incidence of pulmonary embolism. Although the actual incidence of pulmonary embolism is difficult to assess, it was documented in 13 of 672 patients (1.9%), comprised 14.3% of early deaths, and was universally fatal. The 30-day mortality of 7.5% is similar to that of other reported series [2]. The marked disparity between the early mortalities for sleeve lobectomy (5.5%) and sleeve pneumonectomy (20.9%) serves to emphasize the point that sleeve pneumonectomy should be reserved for the rare surgical candidate with tumor confined to the carina or tracheobronchial angle. Sleeve lobectomy for carcinoma is frequently employed as an alternative to, and is technically more demanding- than, pneumonectomy; however, in this review, the 30-day mortality for sleeve lobectomy was 5.5%. This compares favorably with the 6.2% early mortality after pneumonectomy reported by the Lung Cancer Study Group [47]. Five-year survivals for patients with stage I, 11, and 111 disease were 63%, 37%, and 21%, respectively. When one corrects for the percentage of patients staged preoperatively in this review, the predicted 5-year survivals for conventional procedures would be 58%, 37%, and 22% for stage I, 11, and 111 disease, respectively [4]. In addition, the 5-year survival for NO disease in this review (60%) is similar to that for conventional resections (63%)[4]. These data confirm that in appropriately selected patients survival is not compromised by conservative resections. With comparable long-term survival, sleeve lobectomy has the potential advantage over conventional resections of preserving lung function. Pulmonary function after sleeve lobectomy has been reported infrequently. Wood and associates [48] noted maximal impairment in oxygen uptake 3 days postoperatively from sleeve lobectomy relative to lobectomy in an experimental model. However, 28 days postoperatively, the groups had comparable oxygen uptake. Rees and Paneth [32] noted minimal differences in pulmonary function tests of 6 patients who underwent sleeve lobectomy for malignancy. Deslauriers and colleagues [21] noted no functional pulmonary loss after sleeve lobectomy for carcinoma in 15 patients; they attributed this to the resection of impaired lung, cessation of smoking, and improved postoperative pulmonary hygiene. The role of radiation therapy before sleeve lobectomy for carcinoma has been disputed. Paulson [49], Bennett [MI, and Ungar [22] and their respective associates recommend preoperative irradiation and reported 5-year survivals as high as 52% (patient population not defined). However, the only double-blind study designed to address this issue concluded that preoperative radiation therapy did not prolong survival [50]. Because Faber [50]
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found that patients treated with preoperative irradiation experienced no increase in complications, he recommended considering radiation therapy in the patient with impaired pulmonary function and a large bulky central tumor. Patients with central tumors may be candidates for sleeve pneumonectomies, which are associated with a 30-day mortality of 20.9% (29/139) [7, 26281 and a higher complication rate (see Table 3) than either sleeve lobectomy or pneumonectomy. In particular, postoperative pneumonia (16.7%), bronchopleural fistula (10.1%), and empyema (8.6%) are relatively common. This group of patients represented 63% (12/19) of all patients who died of respiratory failure. With such a high morbidity and mortality, it appears that this procedure should be limited to patients with large tumors isolated to the carina or tracheobronchial angle, with adequate cardiopulmonary reserve, and who are in otherwise good health. In summary, review of all clinical data available for bronchogenic carcinoma treated by sleeve lobectomy shows a similar morbidity and mortality to that of pneumonectomy, with preservation of lung function. In addition, when stratified by stage, long-term survival of patients treated by sleeve lobectomy is comparable with the accepted survivals for conventional resections. Therefore, sleeve lobectomy represents a safe and effective therapy for select patients with pulmonary malignancy.
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