Bronchopleural Fistula After Stapled Closure of Bronchus S. Russell Vester, MD, L. Penfield Faber, MD, C. Frederick Kittle, MD, William H. Warren, MD, and Robert J. Jensik, MD Rush-Presbyterian-St. Luke‘s Medical Center, Chicago, Illinois
The incidence of bronchopleural fistula after stapling among 2,243 pulmonary resections at the RushPresbyterian-St. Luke’s Medical Center has been reviewed. There were 35 fistulas in 1,773 stapled and in 470 sutured bronchi (segmentectomy, 2; lobectomy, 1; bilobectomy, 9; and pneumonectomy, 23). We have found that the stapler is expedient and simple to use, and that
it produces a hermetic and uniform closure. The stapler is contraindicated when the bronchus is thickened, inflamed, or of insufficient length. The overall incidence of bronchopleural fistula was 1.6%. Approximately two thirds of the patients with bronchopleural fistula had preoperative radiation therapy or chemotherapy or both. (Ann Thorac Surg 1991;52:1253-8)
ated on for bronchogenic carcinoma, 1 for mesothelioma (an extrapleural pneumonectomy), and 1 for an aspergilloma (a superior segmentectomy with part of the posterior basal segment in a patient who had previously had a right upper lobectomy). Of the 33 patients with carcinoma, 21 had squamous cell, 9 adenocarcinoma, 2 small cell carcinoma, and 1 large cell carcinoma. Fourteen of the 33 patients with carcinoma received radiation therapy only preoperatively, an additional 6 were given both irradiation and chemotherapy, and 13 had no preoperative treatment. Preoperative radiation therapy or chemotherapy was given because of clinical stage I11 disease. The most frequent time for development of these bronchopleural fistulas postoperatively was between 10 and 15 days, with a mean of 44 days and a range from 7 to 210 days. There were 23 fistulas in the 506 pneumonectomy patients (4.5%), 20 in 489 (4.1%) who were stapled and 3 in 17 (17.6%)who were sutured. However, comparison is not appropriate as suturing was done in most instances when stapling was contraindicated. There were 10 fistulas in the 965 bilobectomy and lobectomy patients, 8 of which were stapled and 2 sutured, and 2 fistulas in the 319 segmentectomy patients, both stapled (Table 2). The fistulas in the segmentectomies were bronchial, not parenchymal leaks. When the incidence of bronchopleural fistulas was analyzed according to tumor stage, history, type of resection, and whether or not preoperative radiation therapy or chemotherapy was given, no statistically significant relationships using the x2 test were found (Table 3). Of the 23 bronchopleural fistulas after pneumonectomy, 17 occurred on the right and six on the left. Of the pneumonectomy patients in whom bronchopleural fistulas developed, 15 had preoperative irradiation and 5 received chemotherapy also. In patients who received preoperative irradiation, a
lthough pulmonary resections have become frequent and standard procedures, the occasional occurrence of bronchopleural fistula postoperatively continues to be an important complication that deserves further scrutiny and attention. The best method of bronchial closure is still a controversial topic that evokes many different opinions.
Data and Results We have reviewed the records of 2,243 patients undergoing pulmonary resection at the Rush-Presbyterian-St. Luke’s Medical Center from December 1, 1970, through June 30, 1989, to investigate the incidence of bronchopleural fistula after stapling. The procedures done are shown in Table 1. The majority of the resections were done for neoplastic diseases. The TA-30 or the TA-55 (Auto Suture Co, United States Surgical Corp, Norwalk, CT) was used for bronchial stapling in 1,773 patients. For a pneumonectomy or a lobectomy, staples with a leg length of 4.8 mm and a closed height of 2.0 mm were used; for smaller bronchi, staples with a leg length of 3.5 mm and a closed height of 1.5 mm were used. In 470 patients suture of the bronchus was done because the bronchus was grossly thickened, inflammatory changes were noted, or there was insufficient length of bronchus or margin of normal tissue from the tumor to allow application of the stapler. The pulmonary artery was stapled in 443 instances and the pulmonary vein in 1,738 with no complications. Bronchopleural fistula developed postoperatively in 35 of the 2,243 patients (1.6%). Fistulas developed in 30 of the 1,773 patients in the stapled group (1.7%)and 5 of the 470 in the sutured group (1.1%).The diagnosis of bronchopleural fistula was established in these patients by clinical and radiologic findings and usually confirmed by bronchoscopy. Thirty-three of these patients were operPresented at the Twenty-seventh Annual Meeting of The Society of Thoracic Surgeons, San Francisco, CA, Feb 18-20, 1991. Address reprint requests to Dr Faber, 1725 West Harrison St, Chicago, IL 60612.
0 1991 by The Society of Thoracic Surgeons
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Table 1. Method of Bronchial Closure in 2,243 Pulmonay Resections Resection
650 1,087 506 2,243
319 965 489 1,773
331 122 17 470
Lobectomylbilobectomy Pneumonectomy Total
significantly longer time (average, 48 days) elapsed before the diagnosis of bronchopleural fistula than in the other patients (average, 18 days). The data regarding bronchopleural fistula pertaining to time of diagnosis were analyzed using the Mann-Whitney U test (normal approximation) and that pertaining to the risk of fistula, by Fisher’s Exact test.
Comment The technique of bronchial stump closure and prevention of bronchopleural fistula have been of primary concern since the beginning of pulmonary resections. Many clinical efforts and experimental studies have been made regarding this subject. Meyer [l]recommended the inversion technique similar to that in appendectomy. The cartilage is first crushed or removed before placement of the inversion sutures (Fig 1). Several years later Sweet  advised the use of single interrupted sutures of “medium silk,” placing them over the end of the bronchus and burying the stump beneath a pleural flap; he thought the use of mattress sutures illogical. In a series of 80 lobectomies and 61 pneumonectomies using this method he found only one instance of bronchial fistula (Fig 2). In an attempt to decrease the incidence of bronchopleural fistula and the associated mortality and to simplify lung resections, the Russians Gorkin and Strekopytov developed various mechanical stapling devices in 1957 . The clinical application of bronchial stapling in several thousand patients was reported first by Amosov and Berezovsky , who thought it superior to conventional
Table 2. Bronchopleural Fistulas According to Type of Resection Procedure Segmentectomy Lobectomy Bilobectomy RUL and RML RML and RLL
Pneumonectomy Right Left Total RLL = right lower lobe; upper lobe.
2 1 9 4 5 23 17 6 35
2 1 7 4 3 20 15 5 30
right middle lobe;
... ... 3 2 1 5 RUL
hand suturing because of expediency, simplicity, decreased surgical trauma, and the ability to produce a hermetic approximation of the tissues. The original design, the UKB stapler, placed a single row of metal sutures parallel to the axis of the bronchus. The subsequent instrument, the UKL, placed two staggered rows of sutures perpendicular to the bronchial axis. The Russian stapler was brought to the United States by Ravitch [5, 61 and subsequently underwent several technological improvements (United States Surgical Corp, Norwalk, CT). The initial report by Ravitch and associates  described 139 pulmonary resections with three bronchopleural fistulas (two occurring in diabetic patients and one in a patient with active tuberculosis) using the Russian UKB stapler. With the newly developed American staplers (TA-30 and the TA-55), Kirksey and co-workers  reported on 147 pulmonary resections; there was only one bronchopleural fistula and two bronchial air leaks that healed spontaneously. During the same year, Dart and colleagues  wrote about their experiences using both the Russian and American staplers in 493 patients. With the Russian stapler there were eight bronchopleural fistulas, but there were none with the American stapler. Some spoke enthusiastically about the advantages of the stapling instrument for bronchial closure [9-131, whereas others resisted this new technology [ 14-16]. Experimentally, Scott and associates  studied bronchial healing after closure with silk, catgut, and the stapling device. They concluded: “. . . stumps closed with the automatic stapling device (TA-30) showed the best healing with a minimal degree of inflammation. These findings correlated well with leakage pressures.” The next year Scott and associates  extended their studies to include nylon sutures and measured the collagen levels. Again, the bronchi that were stapled proved superior in collagen levels, had the least inflammatory reaction, and withstood the greatest pressures before disruption. Scott and associates commented: ”These results have clinical relevance to the selection of suture materials for stump closures.” Lynn [191 reviewed the incidence of bronchopleural fistula after resection for tuberculosis in numerous collected series in the United States, Great Britain, Canada, and France between 1951 and 1958, and found it to be 6.7% (see also Table 4). The results of bronchial closure vary from surgeon to surgeon [20-231, and the cause of bronchial fistula is multifactorial. Numerous studies indicate that the causes of bronchial fistula include devitalization and devascularization by excessive dissection, peribronchial infection related to nonabsorbable suture, residual bronchial disease, poor approximation of the mucosa, the length of the stump, and the surgeon’s experience [24-261. To avoid the complication of bronchopleural fistula, we consciously dissect as little of the peribronchial tissue as possible to maintain vascularity of the closed stump. A uniform and rapid closure of the bronchus can be accomplished by use of the stapling technique, but familiarity with the instrumentation and awareness of con-
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Table 3. Bronchopleural Fistulas: Type of Resection, Cell Type, Stage, Preoperative Therapy, Time of Onset, and Closure Surgical
Resection Segmentectomy Lobectomy
1 2 3 4 5 6 7 8 9 10 11 12
Squamous Aspergilloma Squam ous Large cell Squamous Adeno Squam ous Adeno
13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35
Squamous Squamous Squamous Adeno Squamous Squamous Squamous Squamous Adeno Squamous Adeno Squamous Adeno Adeno Squamous Meso Adeno Adeno Squamous Squamous Squamous Squamous
... RT RT No No No No RT RT RT/Chemo No
I1 I I
I1 I IV" 111 I I I
Squamous SCC Squamous
RT RT No
I11 I1 111 I11 0 I11 0 I I 0 I I 111 111 I11
RT/Chemo RT RT RT No
RT/Chemo RT No RT RT No RT No RT
... IVb IVb I1 0 111 111 111
Brain metastasis previously resected. Adeno = adenocarcinoma;
Time of Onset
RT/Chemo RT/Chemo No No
17 14 46 14 20 10 27 10 155 79 70 14
Staple Staple Staple Staple Staple Staple Staple Staple Staple Suture Suture Staple
39 7 11 63 47 11 74 210 15 16 14 35 13 21 141 170 21 22 13 42 57 12 21
Staple Suture Staple Staple Staple Staple Staple Staple Staple Staple Suture Staple Staple Staple Staple Staple Staple Suture Staple Staple Staple Staple Staple
Pleural or distant metastases. =
traindications to its use must be present. Various stapling guns are available, and the surgeon must be familiar with their advantages and disadvantages. Use of the proper size of staple is extremely important. Closure of the anvil to the indicated mark provides a constant space (1.5 mm or 2.0 mm) between the jaws for bronchial approximation. The leg length of the staple determines the tension of the bronchial approximation. If the bronchus is large or particularly thick, a smaller staple will pull through the bronchial wall, and the compressed closure further compromises blood supply to the cut ends
small cell carcinoma
of the bronchus. We use the staple with a 4.8-mm leg length for all pneumonectomies and the majority of lobectomies. In an adolescent or small female patient in whom the lobar bronchus is small, we will use the staple with a 3.5-mm leg length. The smaller segmental bronchus is routinely closed with the staple with a 3.5-mm leg length. Proper positioning of the stapler with the jaws perpendicular to the long axis of the bronchus and parallel to the mucous membrane is obligatory. This should be done without excessive bronchial traction to avoid inclusion of the proximal airway in the stapler. The distal bronchus is
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of knife transection and suture is done when there is a question as to the proximal extent of the cancer. We recommend closure with interrupted monofilament absorbable sutures. A thickened and inflamed bronchus is a relative contraindication to use of the stapler. We do not advise two applications of the staples to close a pneumonectomy stump. This technique creates a longer length of devascularized tissue and would only enhance formation of a fistula. The use of additional absorbable
Fig 1 . Method of bronchial closure as described by Meyer in 1909. He emphasized removing the cartilage, ligating the mncosa, and inverting the stump.
firmly grasped between the thumb and forefinger to flatten the cartilage rings and to avoid bending over of the cartilage wall. We believe this is important in pneumonectomy; obviously it is difficult to do when performing a lobectomy. The bronchus is transected while the jaws are still approximated and flush with the jaw on the distal bronchial side. After transection of the bronchus the specimen is examined grossly and by frozen section for evidence of pathology, particularly with a neoplasm. After stapling, the closed bronchus is tested for air leaks at 20 cm H,O of airway pressure. When small air leaks are identified where the staples have cut through the cartilage, these can be closed with interrupted 4-0 absorbable sutures. We make every attempt to achieve complete pneumostasis. The right pneumonectomy stump is covered with available tissue such as pleura, mediastinal fat pad, pericardium, or an intercostal muscle flap. We do not routinely cover the left pneumonectomy stump because it retracts into the mediastinum. The surgeon should be aware of contraindications to closing the bronchus by the stapling technique. If the cancer is close to the bronchial orifice as observed by bronchoscopy or external appearance and a larger resettion cannot be done, we do not use a stapler. In this instance the bronchus is transected by knife and both the proximal and distal margins are inspected. The technique
of bronchial closure advocated by Sweet 121. He emphasized simple over-and-over sutures, a minimal amount of trauma and dissection (top), and coverage of the stump (bottom). (Reprinted from Sweet RH. Thoracic surgey. Philadelphia: W.B. Saunders, 1950:148-9, by permission.)
Fig 2. Method
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Table 4 . Bronchopleural Fistula After Pneumonectomf Study Schaefer et al, 1977  Verain et al, 1979  Forrester-Wood, 1980  Lawrence et al, 1982  Vester et al, 1991 (present study) Total a
10185 (10.6) 5/33 (15.1) 251225 (11.1) 3/45 (6.6) 3/17 (18.2)
7/111 (6.3) 1/33 (5.3) 61225 (2.7) 2/37 (3.9) 16/307 (5.2)
Numbers in parentheses are percentages.
sutures to reinforce an already airtight suture line requires the surgeon’s judgment. The placement of these sutures will further compromise blood supply. When performing a lobectomy, care must be taken to avoid compromise of the adjacent lobar or main bronchus. If the stapling device is placed too far proximal, narrowing of the bronchus may occur with resultant narrowing of the airway. This is most likely to occur with a left upper lobectomy. Although not statistically significant, the incidence of bronchial fistula after pneumonectomy appears greater in those patients who have had preoperative irradiation or chemotherapy. Fifteen of the 20 pneumonectomy fistulas were in patients who had received preoperative irradiation, and 5 also received combination chemotherapy. Radiation affects the blood supply; grossly at operation there is increased perihilar fibrosis. After preoperative treatment for stage I11 neoplasms we make every attempt to preserve bronchial blood supply during subcarinal and mediastinal lymph node dissection. There are disadvantages to use of the stapler, which include its occasionally cumbersome insertion and application. Closure of the stapling gun can crush the bronchial tissues, and with a thickened bronchus the stapling technique is contraindicated with the presently available staples. Despite the occurrence of an occasional fistula after bronchial closure by the stapling technique, the stapling technique remains our choice for bronchial closure. The closure is precise, expedient, uniform, and airtight.
References Meyer W. Pneumonectomy with aid of differential air pressure. JAMA 1909;53:197%87. Sweet RH. Closure of the bronchial stump following lobectomy or pneumonectomy. Surgery 1945;18:824. Ananyev MG, Antoshina NV, Gritsman YY. Apparatus for suturing tissues with tantalum staples. Eksp Khir 1957;2:28. Amosov NM, Berezovsky KK. Pulmonary resection with mechanical suture. J Thorac Cardiovasc Surg 1961;41:325-5.
5. Ravitch MM, Steichen FM, Fishbein RH, Knowles PW, Weil P. Clinical experiences with the Soviet mechanical bronchus stapler (UKB-25).J Thorac Cardiovasc Surg 1964;47446-54. 6. Steichen FM, Ravitch MM. Stapling in Surgery. Chicago: Year Book Medical, 1984:%78, 364-87. 7. Kirksey TD, Arnold HS, Calhoon JH, Hood RM. Techniques of uulmonarv resection. Tradition and travail. Ann Thorac Su& 1970;9:525-34. 8. Dart CH Jr, Scott SM, Takaro T. Six-year clinical experience using automatic stapling devices for lung resections. Ann Thorac Surg 1970;9:53550. 9. Goldman A. An evaluation of automatic suture with UKL-60 and UKL-40 devices by pulmonary resection. Dis Chest 1964;46:29-36. 10. Konrad RM, Tarbiat S. Die Insuffizienzquote nach Verwendung des Klammernaht-Geraetes beim Bronchusverschluss. Thoraxchir Vask Chir 1971;19:17941. 11. Hood RM, Kirksey TD, Calhoon JH, Arnold HS, Tate RS. The use of automatic stapling devices in pulmonary resection. Ann Thorac Surg 1973;16:8598. 12. Jensik RJ. Discussion of Hood et a1 [ll]. Ann Thorac Surg 1973;16:96-7. 13. Harrison RW. Discussion of Hood et a1 [ll].Ann Thorac Surg 1973;16:97. 14. Overholt RH, Langer L. The technique of pulmonary resection. Springfield, IL: Charles C. Thomas, 1949. 15. Overholt RH. Discussion of Dart et a1 . Ann Thorac Surg 1970;9:54&9. 16. Sabot IA. Discussion of Dart et a1 [S]. Ann Thorac Surg 1970;9:549. 17. Scott RN, Faraci RP, Goodman DG, Militano TC, Geelhoed GW, Chretien PB. The role of inflammation in bronchial stump healing. Ann Surg 1975;181:381-5. 18. Scott RN, Faraci RP, Hough A, Chretien PB. Bronchial stump closure techniques following pneumonectomy: a serial comparative study. Ann Surg 1976;184:20!%11. 19. Lynn RB. The bronchus stump. J Thorac Surg 1958;36:7&5. 20. Schaefer G, Demischew M. Closure of bronchial stump: suturing or stapling? Zentrabl Chir 1977;102:662. 21. Verain C, Cayot M, Virard H, et al. Etude comparative des modes de suture automatique et manuelle en chirurgie pulmonaire-a propas de 132 resections. Ann Chir 1979;33: 147. 22. Forrester-Wood CP. Bronchopleural fistula following pneumonectomy for carcinoma of the bronchus. J Thorac Cardiovasc Surg 1980;80:406-9. 23. Lawrence GH, Ristroph R, Wood JA, et al. Methods for avoiding a dire surgical complication: bronchopleural fistula after pulmonary resection. Am J Surg 1982;144:136-44.. 24. Taffel M. Repair of tracheal and bronchial defects with free fascia grafts. Surgery 1940;8:56-71. 25. Bjork VO. Suture material and technique for bronchial closure and bronchial anastomosis. J Thorac Surg 1956;32:22-7. 26. Kaplan DK, Whyte RI, Donnelly RD. Pulmonary resection using automatic stapling devices. Eur J Cardiothorac Surg 1987;1:152.
DISCUSSION D R WILLARD A. FRY (Evanston, IL): My experience in stapling bronchi for segmental resection in small people, particularly women, is that the stapled stump will sometimes leak around the 3.5-mm staples, which are the smallest of the standard bronchial
closure staples. I have consequently over recent years simply sutured those small segmental bronchi; it only takes a few sutures. But I wonder if the 30 V might not be an acceptable staple closure for such small bronchi.
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BRONCHOPLEURAL FISTULA AFTER STAPLING
DR VESTER: We have rarely used the vascular staples for bronchial closure. We also have had a similar experience of a slight tear in the bronchial closure caused by the large staple, and these small defects do require the placement of interrupted sutures. Our experience with staple or suture closure of a segmental bronchus has always been individual surgeon preference and, as you have stated, it is frequently easier to close a smaller bronchus with sutures. DR JOEL D. COOPER (St. Louis, MO): I have not been in the habit of using the stapler on the airway. I was heavily influenced by Michael Perlman, who is the head of the institute in Moscow, where they have, as you pointed out, invented the staplers. What impressed me is when I asked him 8 or 9 years ago if he used the staplers and he said, “On the vessels always, on the bronchus never, except very supple bronchus or in children.” And I think the point to be made is that the stapler can be used safely, but there are some circumstances under which perhaps it cannot. I honestly believe that the incidence of leakage with stapler is every bit as high as with manual closure. People do not report their bad results with staplers; they only report their good results. My main concern is particularly related to right pneumonectomy, where, if it is close to the trachea, you have a very strong strut on the medial aspect, which is the canna. It is one of the points that Dr Perlman made as well. You pointed out that an advantage of the stapler is the uniform application of the device, but I would argue that that is one of the disadvantages if you are working on an airway, which is nonuniform in terms of its elasticity and thickness. Under what circumstances do you think the stapler should be avoided? DR VESTER There are very definite contraindications to the use of the stapling technique for bronchial closure, and a surgeon must always keep these in mind. Preresection bronchoscopy by the thoracic surgeon is mandatory to permit the opportunity to visualize the mucosa of the bronchus to be transected, as well as the exact location of the cancer. We believe that serious endobronchial mucosal inflammation or severe bronchitis is a contraindication to stapling. When the cancer is in close proximity to the area of bronchial transection either by endoscopic visualization or palpation at the time of thoracotomy, the staple instrument is not used. In this instance, the bronchus is sharply transected with a knife and both the proximal and distal margins can be inspected. As you have pointed out, a substantially thickened bronchus or a bronchus in which a ring of cartilage could not be approximated satisfactorily would be a contraindication to stapling. In this situation, the bronchus is crushed by closure of the anvil and the staples tend to pull through with a resultant fistula. This requires careful selection and judgment by the surgeon as to whether to staple or hand suture the bronchus.
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When performing a pneumonectomy, we make every attempt to flatten the membrane against the cartilage so that we do not fold over the end of the lateral bronchial wall. Any time the surgeon believes that the bronchus is too thick for stapling or it is calcified, then stapling is not indicated. DR THOMAS W. RICE (Cleveland, OH): Have you been able to categorize the bronchopleural fistulas into those resulting from V closure staplers versus those resulting from parallel closure staples? DR VESTER: I am sorry, I do not know what you mean by V closure. DR RICE: There was a stapler that had a V closure of the jaws, and the incidence of bronchopleural fistula was increased with that instrument. DR VESTER: You are absolutely correct in stating that this type of staple cartridge was associated with a higher incidence of bronchopleural fistula. It was related to the fact that there was not a uniform application of compressive pressure on the bronchus just before the instrument was fired. We immediately recognized the defect with this type of device and never used it. We have always used the original TA-30 and TA-55 stapling instruments for their advantages of reliability and reproducible results. DR STEVEN W. GUYTON (Seattle, WA): I am sorry I did not get here for your presentation of data, but I think the sweeping conclusions that you make are not supported by the data that I got out of the abstract. What I see in the abstract is that you have fewer leaks with segmentectomy with suture closure than with staple closure, and it seems like the staple closure should be applied selectively rather than as a sweeping statement. DR VESTER We have reviewed our experience with staple closure of the bronchus and are reporting the incidence of bronchial fistula after pneumonectomy, lobectomy, and segmentectomy. A true comparison of staple closure versus suture closure of a bronchus would require a randomized, prospective study, and this review is retrospective. Suture closure after pneumonectomy and lobectomy was accomplished primarily in those patients in whom the use of the stapling technique was contraindicated and incidence of fistula cannot be compared. The closure of the segmental bronchus was primarily at the discretion of the operating surgeon, and there was no statistical difference in incidence of fistula after staple or suture closure of the smaller bronchi. Selectivity is always appropriate when applying any surgical technique.