- Email: [email protected]
HEALING OF THE BRONCHIAL STUMP AFTER PULMONARY RESECTION
HEALING OF THE BRONCHIAL STUMP AFTER P U L M O N A R Y RESECTION Daniel E. Smith, M.D., Anthony F. Karish, M.D., Jesse P. Chapman, and Timothy
Takaro, M.D., Oteen and Asheville,
M.D.,
N. C.
T
HE problem of bronchial stump healing after pulmonary resection has al ways been of lively interest to thoracic surgeons because of the strong natural tendency for this springy, tubular, cartilagenous-muscular structure to re-open, and the seriousness of the resulting morbidity to the patient. The variety of methods of bronchial closure advocated and of materials used attest to the fact that bronchial healing continues to be a problem of primary im portance and that a ready solution is not yet at hand. The approximation of the two walls of a severed bronchus and the healing process, whereby an air tight closure is attained, has been extensively studied by numerous investigators and most thoroughly by Reinhoff in 1943.1 Bronchopleural fistulas still occur, but the incidence is reportedly less with the Russian stapling device described as early as 1954. Lushnikov 2 listed eight fistulas in 350 pulmonary resections in bronchi closed with the stapling device. Amosov3"0 described the use of the stapling device and in several articles listed almost 3,000 pulmonary resections with a fistula rate of about 2 per cent. The interest in the stapling device arises from the ease and rapidity of closing a severed bronchus, the minimal reaction to tantalum or steel staples, and the close approximation of the bronchial wall whereby the severed ends of the bronchus are united by earlier fibroblastic proliferation. The stapling apparatus consists of a shaft with hooked ends (Pig. 1), and a stapling magazine which slides along the shaft and a screw which regulates the distance between the magazine and the hook. The hook houses the matrix for bending the staples and the magazine houses the extruding apparatus op erated by the handle near the screw. The apparatus is placed around the bron chus as close to the bifurcation as possible. The screw is then tightened and the bronchus is stapled by pressure applied to the handle. The parallel arrangement of staples with respect to the bronchial axis provides a hermetic union of the suture and does not disturb the blood circulation of the distal ends of the severed bronchi. From Veterans Administration Hospital, Oteen, N. C, and Western North Carolina Sani tarium, Asheville, N. C. Received for publication April 29, 1963.
548
Vol. 46, No. 4 October, 1963
H E A L I N G OF BRONCHIAL STUMP
549
METHOD
The healing process was studied in 40 animals after pneumonectomy: Ten bronchi were closed with end-on silk sutures, ten were closed with tantalum staples with the use of the Russian bronchus stapling device, UKB-25, and ten were closed with horizontal mattress sutures as originally described by Rienhoff.1 None of the sutured bronchi were covered with pleura in a deliberate attempt to leave the bronchus free from closure by adjacent tissue of the mediastinum. The fourth group consisted of bronchial closure reinforced with Teflon felt in an attempt to add substance to the suture line and to promote earlier union between the severed ends of the bronchus. At intervals of 16 days to 9 months, photoendoscopy, bronchograms with magnification technique, and gross surgical pathology of autopsy specimens defined the type and extent of bronchial heal ing. Subsequent histological studies compared the reaction to suture material, type of healing, and the contribution of associated adjacent mediastinal struc tures.
Fig;. 1.—Russian stapling device, UKB-25. RESULTS
Photoendoscopic observation of the healing bronchus 17 to 20 days after closure usually revealed an intact suture line, irrespective of method of closure. Occasionally a suture granuloma (Pig. 2) in a sutured bronchus was seen as a fold of fibrous tissue covered with mucous membrane and red granulation tissue. The presence of suture or staples was variable. In the stapled bronchus, the membranous portion of the bronchus approximated the cartilage and formed a convex line with the contour of the bronchus and several glistening staples were seen embedded in the mucous membrane (Fig. 3). The numerous bronchoscopic examinations did not contribute significantly to the over-all classification of the healing process of the bronchus. The bronchograms showed the parting of the bronchial walls very well. The staples were usually well aligned. Occasionally, a puckering at the cut end,
550
SMITH ET AL.
J. Thoracic and Cardiovas. Surg.
with gross distortion of the bronchial stump, was seen. Radiopaque material appeared a short distance beyond the original line of closure. By direct inspection of the internal surface of the autopsy specimen, breaks in continuity of bronchial mucous membrane, fibrous bands, irregular openings in the bronchus, and, in some instances, complete separation of the bronchial walls at the point of suture were seen (Pig. 4). In many instances, sutures or staples were loose and attached on one side of the lumen. Longitudinal sections of the intact stump provided a view of the bronchus which could be classified into one of three types (Pig. 5.) : 1. The bronchus is healed with intact opposed bronchial walls, and mucous membrane is intact over the entire surface—this is termed primary healing.
Fig. 2.—Suture granuloma of bronchus. Fig-. 3.—Stapled bronchus.
2. The bronchial walls are partially separated but filled with fibrous tissue, granulation tissue, and irregular ridges covered with bronchial epithelium. The inner surface of the bronchus is incompletely covered with epithelium. This is referred to as partial disruption. 3. There is complete disruption of the bronchial walls and the bronchial lumen is occluded by suture material, bronchial fragments, mediastinal pleura, lymph nodes, and inflammatory fibrous plug. Each type of healing was seen in every group, irrespective of the suture used to approximate the walls of the bronchus. The frequency of the types in each group is illustrated in Table I. This gross surgical classification was ap plied during histological study of the bronchus.
Vol. 46, No. 4
H E A L I N G OF BRONCHIAL STUMP
October, 1963
551
Histological study of "primary healing" shows close coaptation of the bronchial walls and continuity of bronchial epithelium (Fig. 6). The walls of the bronchus show infiltration of lymphocytes and occasional leukocytes. Mild edema is evident. The bronchial cuff distal to the point of suture is infiltrated with fibrous tissue, the cartilage is intact. The stapled bronchus shows the same response, although with less cellular infiltration and a greater fragmentation of the cartilage. This histological picture is evident as early as 17 days after bronchial suture. In the bronchus with partial disruption, the bronchial walls are wider apart, the inflammatory response is greater, and micro-abscesses are seen where
Fig. 4.—Autopsy specimen, open-end view of stapled bronchus.
r
Fig. 5.—Composite which shows, left to right, primary healing, partial disruption, and complete disruption. TABLE T Y P E OP CLOSURE
Mattress sutures Silk sutures Staples Staples (Teflon)
|
PRIMARY H E A L I N G
4 3 5 3
|
I PARTIAL DISRUPTION
2 4 3 3
|
DISRUPTION
4 3 2 2 (3 B P F )
552
SMITH ET
AL.
J. Thoracic and Cardiovas. Surg.
sutures are extruded into the lumen (Fig. 7). This type occurred in 40 per cent of bronchi. The bronchial epithelium is usually interrupted and metaplasia is seen. Leukocytes and lymphocytes permeate the entire thickness of the wall of the bronchus. There is a larger mass of fibrous tissue which covers the ends of the bronchi and seals it off from the pleural space. Between the point of suture and the cut end of the bronchus, a pocket or "cleft" may be seen. It varies in size and inflammatory reaction and is incompletely lined with bronchial epi thelium. This is the usual histological picture of the bronchus at 2 to 3 months after suture. It occurred more frequently in the silk-sutured bronchus.
Pig. 6.—Close coaptation of the primary healed bronchus.
The widely separated bronchus, which is termed "complete disruption," may occur as early as 4 weeks, although usually it is evident after 4 to 5 months (Pig. 8). The ultimate pattern was illustrated in four of ten bronchi closed with mattress sutures, three of ten silk-sutured and two of ten stapled bronchi. The sutures have cut through the lumen and the widely separated bronchial walls are bridged by a thin membrane composed of flattened bronchial epithelial cells and varying submucosal fibrous tissue. Inflammatory response varies; it is usu ally intense during early healing and less marked as late as 5 to 6 months after suture. The end of the bronchus is sealed by mediastinal tissue, lymph nodes, etc. Of the stapled bronchi reinforced with Teflon on the membranous portion of the bronchus, three bronchopleural fistulas were evident and erosion of the
Vol. 46, No. 4 October. 1963
H E A L I N G OF BRONCHIAL STUMP
553
r^jfS Jift^&t'
»?'•*
£-'
Z r ^>-rhfe^ ^ a.'
Fig. 7.—Partial disruption which shows inflammatory reaction and extrusion of debris into lumen to "seal" the open bronchus.
Fig. 8.—Complete disruption-separation of bronchial walls and marked inflammatory
554
SMITH ET
AL.
J. Thoracic and Cardiovas. Surg.
mucous membrane occurred in four other instances. It would appear that foreign material is not well tolerated by the bronchus. The clinical portion of the study involved the tabulation of each pulmonary resection, lobectomy or pneumonectomy for tuberculosis, carcinoma, lung ab scess, and bronchiectasis. Routine preoperative attention was given, with par ticular emphasis to sputum volume, appropriate antibiotics, and adequate tracheobronchial toilet. Bronchoscopy and bronchograms were done when indi cated for evaluation of disease, with attention directed to the redness of bron chial mucosa at the proposed site of resection. The bronchial mucous membrane was rendered as clean as possible. Each pulmonary resection was recorded on the day of operation as to diagnosis, type of bronchial closure, extent of disease, pleural and adventitial coverage of the stump, and contamination of the pleural space. The postoperative observation recorded early expansion of the lung, per sistent air leak, and bronchoscopic appearance of the bronchial closure. Post operative bronchoscopy was done, when indicated, for retention of secretions, or for possible suture granuloma or fistula as indicated by postoperative hemoptysis. The follow-up period varied from 18 months for the earlier resec tions to 9 months for the later resections. In 101 patients, the bronchus was closed with metallic sutures by means of the mechanical stapling device; in 73 patients several different techniques of manual suturing were used. No ran domization or alternation of cases was done. It became evident, apparently be cause of the ease of mechanical suturing, that the bronchi of patients with more extensive disease were stapled. Bronchial healing was evaluated according to disease and method of closure. The analysis of one hundred and seventy-four pulmonary resections constitutes the basis of this report. One hundred and two resections were done for pul monary tuberculosis, of which ninety-three were lobectomies and nine were pneumonectomies. Fifty-one per cent of the patients had positive smears or cul tures at the time of pulmonary resection. Three patients had bisegmental re sections and are included in the lobectomy group. Four patients with atypical acid-fast bacilli are included in this group. Bronchopleural fistulas occurred in five of seventeen bronchi which were stapled after pneumonectomy (Table I I ) . In 2 patients, previous partial re sections for tuberculosis had been done on the side of the pneumonectomy, and, in 2, technical errors in the use of the device were apparent. All patients responded favorably to additional surgical management, and there were no fatalities in this group. There were no bronchopleural fistulas among the thir teen manually sutured bronchi following pneumonectomy. Fistulas were noted in two of sixty manually sutured bronchi after lobectomy; and in one of eightyfour stapled bronchi (Table I I I ) . The inflammatory process surrounding the bronchopleural fistula after right upper lobectomy for lung abscess responded to antibiotics and bronchial aerosol? without residual suture granuloma. Photoendoscopic examination revealed a smaller opening, less purulent secrel^n, and a more healthy appearance of the bronchial mucous membrane. Drainage of surrounding abscesses into the bronchus occurred with regression of the infec tion in contrast to the troublesome granuloma of the sutured stump which
Vol. 46, No. 4 October, 1963
555
H E A L I N G OF BRONCHIAL STUMP
requires endoscopic suture removal to overcome the infection. Histological exami nation of specimens revealed endobronchial tuberculosis of 2 patients treated by completion pneumonectomy in whom fistula occurred. Carcinoma of the bronchial stump was found on the autopsy specimen of one patient who died of recurrent disease. One patient required secondary thoracotomy for active intrathoracic bleeding. A bronchial artery was found actively bleeding between two adequately closed staples. TABLE I I .
PNEUMONECTOMY
NO. BRONCHI
NO. BRONCHOPLEUEAL FISTULAS
Tuberculous Sutured Stapled Nontuberculous Sutured Stapled
10 11
TABLE I I I .
LOBECTOMY
NO. BRONCHI
Tuberculous Sutured Stapled Nontuberculous Sutured Stapled
NO. BRONCHOPLEURAL FISTULAS
32 61 93
(1.7%)
28 23 51
(3.9%)
DISCUSSION
Observation of bronchi closed by different methods illustrates a tremendous propensity of the bronchus to heal despite changes in intrabronchial pressure with coughing, the spring-like action of cartilage, and the presence of infection. Interesting is the observation that many bronchi separate or avulse from the sutures and yet remain closed through the interposition of an inflammatory response and coverage of the cut ends of the bronchus with tissue derived from the mediastinum. The fact, pointed out by Rienhoff, that opening of the bron chus occurs followed by healing was verified by the dog experiments in each of four methods of closure. More important is the time factor in which it is observed that at 17 to 20 days the continuity of the bronchus is dependent on the closure, and at least 50 per cent of these bronchi will subsequently separate and actually heal by secondary intention. It would seem from this observation that the preser vation of the blood supply, close approximation of the severed ends of the bron-
SMITH ET AL.
556
J. Thoracic and Cardiovas. Surg.
chus, and covering the bronchial stump are more important than the type of material used to suture the bronchus. Considerable emphasis has been placed by Savchenko7 on an air-tight closure, early rapid healing by the tenth day, and preservation of blood supply to distal ends of the severed bronchus. As observed in this work, the staples do cut through the membranous portion of the bronchus. However, a healing by secondary intention has by this time oc curred, in which the peribronchial tissue plays a significant part. This was pointed out by Quinby and Morse in 1911.8 A new material and method for the closure of a bronchus has been added; the method of healing, the histology of different types of healing, and the end result of bronchial closure have not changed. The evaluation of the clinical material illustrates the mechanical ease of the stapling device in a loosely dissected bronchus. The endoscopic appearance suggests a cleaner wound as being conducive to healing. Histologically, the stapled bronchus shows less inflammatory response. With the initial technical errors overcome, more of the larger bronchi should be closed with fewer bronchopleural fistulas, particularly in patients who undergo pneumonectomy. SUMMARY
1. The use of the Russian stapling device has been described. 2. The healed bronchus in the dog has been classified into the following categories: primary healing, partial disruption, and disruption according to gross pathology and histological pattern. 3. In 101 patients the bronchus was closed with metallic staples by means of the mechanical stapling device. Small bronchopleural fistulas occurred in five of seventeen bronchi which were stapled after pneumonectomy. Fistulas were noted in two of sixty manually sutured bronchi, and in one of eighty-four stapled bronchi after lobectomy. 4. Since technical errors and more severe disease were prominent in the bronchial closures by means of stapling, in which fistulas later developed, fur ther trial of bronchial closure with the use of the stapling device seems to be in order. REFERENCES 1. Eienhoff, W. F., Jr., Gannon, J., Jr., and Sherman, I.: Closure of the Bronchus Following Pneumonectomy, Ann. Surg. 116: 481-531, 1942. 2. Lushnikov, B. S.: Mechanical Tantalum Suturing of the Bronchus and Trachea, Grudn. Khir. 1: 64-71, 1959. 3. Amosov, N. M.: Pulmonary Resection With Mechanical Bronchial Suturing, Tuberkulozis (Budapest) 13: 353-357, 1950. 4. Amosov, N. M., and Berezovski, K. K.: Development of Pulmonary Surgery in the Ukraine, Grudn. Khir. 3 : 72-77, 1961. 5. Amosov, N. M., Berezovski, K. K., and Zabroda, G. S.: Results of 100 Pulmonary Resec tions With the TJKL-60, Eksp. Khir. 3 : 3-7, 1958. 6. Amosov, N . M., and Dedkov, I. P . : On Bilateral Lung Resections, Khirurgiia 35: 19-24, 1959. 7. Androsov, P. I., Potekhina, L. A., Savchenko, E. D., Strekopytov, A. A., Tliakova, L. S., and Sheinber: A New Method for Suturing the Bronchial Stump, Khirurgiia, No. 8: 66-70, 1955. 8. Quinby, W. C . and Morse, G. W.: Experimental Pneumonectomy and Application to Man, Boston M. & S. J . 165: 121, 1911.
Takaro, M.D., Oteen and Asheville,
M.D.,
N. C.
T
HE problem of bronchial stump healing after pulmonary resection has al ways been of lively interest to thoracic surgeons because of the strong natural tendency for this springy, tubular, cartilagenous-muscular structure to re-open, and the seriousness of the resulting morbidity to the patient. The variety of methods of bronchial closure advocated and of materials used attest to the fact that bronchial healing continues to be a problem of primary im portance and that a ready solution is not yet at hand. The approximation of the two walls of a severed bronchus and the healing process, whereby an air tight closure is attained, has been extensively studied by numerous investigators and most thoroughly by Reinhoff in 1943.1 Bronchopleural fistulas still occur, but the incidence is reportedly less with the Russian stapling device described as early as 1954. Lushnikov 2 listed eight fistulas in 350 pulmonary resections in bronchi closed with the stapling device. Amosov3"0 described the use of the stapling device and in several articles listed almost 3,000 pulmonary resections with a fistula rate of about 2 per cent. The interest in the stapling device arises from the ease and rapidity of closing a severed bronchus, the minimal reaction to tantalum or steel staples, and the close approximation of the bronchial wall whereby the severed ends of the bronchus are united by earlier fibroblastic proliferation. The stapling apparatus consists of a shaft with hooked ends (Pig. 1), and a stapling magazine which slides along the shaft and a screw which regulates the distance between the magazine and the hook. The hook houses the matrix for bending the staples and the magazine houses the extruding apparatus op erated by the handle near the screw. The apparatus is placed around the bron chus as close to the bifurcation as possible. The screw is then tightened and the bronchus is stapled by pressure applied to the handle. The parallel arrangement of staples with respect to the bronchial axis provides a hermetic union of the suture and does not disturb the blood circulation of the distal ends of the severed bronchi. From Veterans Administration Hospital, Oteen, N. C, and Western North Carolina Sani tarium, Asheville, N. C. Received for publication April 29, 1963.
548
Vol. 46, No. 4 October, 1963
H E A L I N G OF BRONCHIAL STUMP
549
METHOD
The healing process was studied in 40 animals after pneumonectomy: Ten bronchi were closed with end-on silk sutures, ten were closed with tantalum staples with the use of the Russian bronchus stapling device, UKB-25, and ten were closed with horizontal mattress sutures as originally described by Rienhoff.1 None of the sutured bronchi were covered with pleura in a deliberate attempt to leave the bronchus free from closure by adjacent tissue of the mediastinum. The fourth group consisted of bronchial closure reinforced with Teflon felt in an attempt to add substance to the suture line and to promote earlier union between the severed ends of the bronchus. At intervals of 16 days to 9 months, photoendoscopy, bronchograms with magnification technique, and gross surgical pathology of autopsy specimens defined the type and extent of bronchial heal ing. Subsequent histological studies compared the reaction to suture material, type of healing, and the contribution of associated adjacent mediastinal struc tures.
Fig;. 1.—Russian stapling device, UKB-25. RESULTS
Photoendoscopic observation of the healing bronchus 17 to 20 days after closure usually revealed an intact suture line, irrespective of method of closure. Occasionally a suture granuloma (Pig. 2) in a sutured bronchus was seen as a fold of fibrous tissue covered with mucous membrane and red granulation tissue. The presence of suture or staples was variable. In the stapled bronchus, the membranous portion of the bronchus approximated the cartilage and formed a convex line with the contour of the bronchus and several glistening staples were seen embedded in the mucous membrane (Fig. 3). The numerous bronchoscopic examinations did not contribute significantly to the over-all classification of the healing process of the bronchus. The bronchograms showed the parting of the bronchial walls very well. The staples were usually well aligned. Occasionally, a puckering at the cut end,
550
SMITH ET AL.
J. Thoracic and Cardiovas. Surg.
with gross distortion of the bronchial stump, was seen. Radiopaque material appeared a short distance beyond the original line of closure. By direct inspection of the internal surface of the autopsy specimen, breaks in continuity of bronchial mucous membrane, fibrous bands, irregular openings in the bronchus, and, in some instances, complete separation of the bronchial walls at the point of suture were seen (Pig. 4). In many instances, sutures or staples were loose and attached on one side of the lumen. Longitudinal sections of the intact stump provided a view of the bronchus which could be classified into one of three types (Pig. 5.) : 1. The bronchus is healed with intact opposed bronchial walls, and mucous membrane is intact over the entire surface—this is termed primary healing.
Fig. 2.—Suture granuloma of bronchus. Fig-. 3.—Stapled bronchus.
2. The bronchial walls are partially separated but filled with fibrous tissue, granulation tissue, and irregular ridges covered with bronchial epithelium. The inner surface of the bronchus is incompletely covered with epithelium. This is referred to as partial disruption. 3. There is complete disruption of the bronchial walls and the bronchial lumen is occluded by suture material, bronchial fragments, mediastinal pleura, lymph nodes, and inflammatory fibrous plug. Each type of healing was seen in every group, irrespective of the suture used to approximate the walls of the bronchus. The frequency of the types in each group is illustrated in Table I. This gross surgical classification was ap plied during histological study of the bronchus.
Vol. 46, No. 4
H E A L I N G OF BRONCHIAL STUMP
October, 1963
551
Histological study of "primary healing" shows close coaptation of the bronchial walls and continuity of bronchial epithelium (Fig. 6). The walls of the bronchus show infiltration of lymphocytes and occasional leukocytes. Mild edema is evident. The bronchial cuff distal to the point of suture is infiltrated with fibrous tissue, the cartilage is intact. The stapled bronchus shows the same response, although with less cellular infiltration and a greater fragmentation of the cartilage. This histological picture is evident as early as 17 days after bronchial suture. In the bronchus with partial disruption, the bronchial walls are wider apart, the inflammatory response is greater, and micro-abscesses are seen where
Fig. 4.—Autopsy specimen, open-end view of stapled bronchus.
r
Fig. 5.—Composite which shows, left to right, primary healing, partial disruption, and complete disruption. TABLE T Y P E OP CLOSURE
Mattress sutures Silk sutures Staples Staples (Teflon)
|
PRIMARY H E A L I N G
4 3 5 3
|
I PARTIAL DISRUPTION
2 4 3 3
|
DISRUPTION
4 3 2 2 (3 B P F )
552
SMITH ET
AL.
J. Thoracic and Cardiovas. Surg.
sutures are extruded into the lumen (Fig. 7). This type occurred in 40 per cent of bronchi. The bronchial epithelium is usually interrupted and metaplasia is seen. Leukocytes and lymphocytes permeate the entire thickness of the wall of the bronchus. There is a larger mass of fibrous tissue which covers the ends of the bronchi and seals it off from the pleural space. Between the point of suture and the cut end of the bronchus, a pocket or "cleft" may be seen. It varies in size and inflammatory reaction and is incompletely lined with bronchial epi thelium. This is the usual histological picture of the bronchus at 2 to 3 months after suture. It occurred more frequently in the silk-sutured bronchus.
Pig. 6.—Close coaptation of the primary healed bronchus.
The widely separated bronchus, which is termed "complete disruption," may occur as early as 4 weeks, although usually it is evident after 4 to 5 months (Pig. 8). The ultimate pattern was illustrated in four of ten bronchi closed with mattress sutures, three of ten silk-sutured and two of ten stapled bronchi. The sutures have cut through the lumen and the widely separated bronchial walls are bridged by a thin membrane composed of flattened bronchial epithelial cells and varying submucosal fibrous tissue. Inflammatory response varies; it is usu ally intense during early healing and less marked as late as 5 to 6 months after suture. The end of the bronchus is sealed by mediastinal tissue, lymph nodes, etc. Of the stapled bronchi reinforced with Teflon on the membranous portion of the bronchus, three bronchopleural fistulas were evident and erosion of the
Vol. 46, No. 4 October. 1963
H E A L I N G OF BRONCHIAL STUMP
553
r^jfS Jift^&t'
»?'•*
£-'
Z r ^>-rhfe^ ^ a.'
Fig. 7.—Partial disruption which shows inflammatory reaction and extrusion of debris into lumen to "seal" the open bronchus.
Fig. 8.—Complete disruption-separation of bronchial walls and marked inflammatory
554
SMITH ET
AL.
J. Thoracic and Cardiovas. Surg.
mucous membrane occurred in four other instances. It would appear that foreign material is not well tolerated by the bronchus. The clinical portion of the study involved the tabulation of each pulmonary resection, lobectomy or pneumonectomy for tuberculosis, carcinoma, lung ab scess, and bronchiectasis. Routine preoperative attention was given, with par ticular emphasis to sputum volume, appropriate antibiotics, and adequate tracheobronchial toilet. Bronchoscopy and bronchograms were done when indi cated for evaluation of disease, with attention directed to the redness of bron chial mucosa at the proposed site of resection. The bronchial mucous membrane was rendered as clean as possible. Each pulmonary resection was recorded on the day of operation as to diagnosis, type of bronchial closure, extent of disease, pleural and adventitial coverage of the stump, and contamination of the pleural space. The postoperative observation recorded early expansion of the lung, per sistent air leak, and bronchoscopic appearance of the bronchial closure. Post operative bronchoscopy was done, when indicated, for retention of secretions, or for possible suture granuloma or fistula as indicated by postoperative hemoptysis. The follow-up period varied from 18 months for the earlier resec tions to 9 months for the later resections. In 101 patients, the bronchus was closed with metallic sutures by means of the mechanical stapling device; in 73 patients several different techniques of manual suturing were used. No ran domization or alternation of cases was done. It became evident, apparently be cause of the ease of mechanical suturing, that the bronchi of patients with more extensive disease were stapled. Bronchial healing was evaluated according to disease and method of closure. The analysis of one hundred and seventy-four pulmonary resections constitutes the basis of this report. One hundred and two resections were done for pul monary tuberculosis, of which ninety-three were lobectomies and nine were pneumonectomies. Fifty-one per cent of the patients had positive smears or cul tures at the time of pulmonary resection. Three patients had bisegmental re sections and are included in the lobectomy group. Four patients with atypical acid-fast bacilli are included in this group. Bronchopleural fistulas occurred in five of seventeen bronchi which were stapled after pneumonectomy (Table I I ) . In 2 patients, previous partial re sections for tuberculosis had been done on the side of the pneumonectomy, and, in 2, technical errors in the use of the device were apparent. All patients responded favorably to additional surgical management, and there were no fatalities in this group. There were no bronchopleural fistulas among the thir teen manually sutured bronchi following pneumonectomy. Fistulas were noted in two of sixty manually sutured bronchi after lobectomy; and in one of eightyfour stapled bronchi (Table I I I ) . The inflammatory process surrounding the bronchopleural fistula after right upper lobectomy for lung abscess responded to antibiotics and bronchial aerosol? without residual suture granuloma. Photoendoscopic examination revealed a smaller opening, less purulent secrel^n, and a more healthy appearance of the bronchial mucous membrane. Drainage of surrounding abscesses into the bronchus occurred with regression of the infec tion in contrast to the troublesome granuloma of the sutured stump which
Vol. 46, No. 4 October, 1963
555
H E A L I N G OF BRONCHIAL STUMP
requires endoscopic suture removal to overcome the infection. Histological exami nation of specimens revealed endobronchial tuberculosis of 2 patients treated by completion pneumonectomy in whom fistula occurred. Carcinoma of the bronchial stump was found on the autopsy specimen of one patient who died of recurrent disease. One patient required secondary thoracotomy for active intrathoracic bleeding. A bronchial artery was found actively bleeding between two adequately closed staples. TABLE I I .
PNEUMONECTOMY
NO. BRONCHI
NO. BRONCHOPLEUEAL FISTULAS
Tuberculous Sutured Stapled Nontuberculous Sutured Stapled
10 11
TABLE I I I .
LOBECTOMY
NO. BRONCHI
Tuberculous Sutured Stapled Nontuberculous Sutured Stapled
NO. BRONCHOPLEURAL FISTULAS
32 61 93
(1.7%)
28 23 51
(3.9%)
DISCUSSION
Observation of bronchi closed by different methods illustrates a tremendous propensity of the bronchus to heal despite changes in intrabronchial pressure with coughing, the spring-like action of cartilage, and the presence of infection. Interesting is the observation that many bronchi separate or avulse from the sutures and yet remain closed through the interposition of an inflammatory response and coverage of the cut ends of the bronchus with tissue derived from the mediastinum. The fact, pointed out by Rienhoff, that opening of the bron chus occurs followed by healing was verified by the dog experiments in each of four methods of closure. More important is the time factor in which it is observed that at 17 to 20 days the continuity of the bronchus is dependent on the closure, and at least 50 per cent of these bronchi will subsequently separate and actually heal by secondary intention. It would seem from this observation that the preser vation of the blood supply, close approximation of the severed ends of the bron-
SMITH ET AL.
556
J. Thoracic and Cardiovas. Surg.
chus, and covering the bronchial stump are more important than the type of material used to suture the bronchus. Considerable emphasis has been placed by Savchenko7 on an air-tight closure, early rapid healing by the tenth day, and preservation of blood supply to distal ends of the severed bronchus. As observed in this work, the staples do cut through the membranous portion of the bronchus. However, a healing by secondary intention has by this time oc curred, in which the peribronchial tissue plays a significant part. This was pointed out by Quinby and Morse in 1911.8 A new material and method for the closure of a bronchus has been added; the method of healing, the histology of different types of healing, and the end result of bronchial closure have not changed. The evaluation of the clinical material illustrates the mechanical ease of the stapling device in a loosely dissected bronchus. The endoscopic appearance suggests a cleaner wound as being conducive to healing. Histologically, the stapled bronchus shows less inflammatory response. With the initial technical errors overcome, more of the larger bronchi should be closed with fewer bronchopleural fistulas, particularly in patients who undergo pneumonectomy. SUMMARY
1. The use of the Russian stapling device has been described. 2. The healed bronchus in the dog has been classified into the following categories: primary healing, partial disruption, and disruption according to gross pathology and histological pattern. 3. In 101 patients the bronchus was closed with metallic staples by means of the mechanical stapling device. Small bronchopleural fistulas occurred in five of seventeen bronchi which were stapled after pneumonectomy. Fistulas were noted in two of sixty manually sutured bronchi, and in one of eighty-four stapled bronchi after lobectomy. 4. Since technical errors and more severe disease were prominent in the bronchial closures by means of stapling, in which fistulas later developed, fur ther trial of bronchial closure with the use of the stapling device seems to be in order. REFERENCES 1. Eienhoff, W. F., Jr., Gannon, J., Jr., and Sherman, I.: Closure of the Bronchus Following Pneumonectomy, Ann. Surg. 116: 481-531, 1942. 2. Lushnikov, B. S.: Mechanical Tantalum Suturing of the Bronchus and Trachea, Grudn. Khir. 1: 64-71, 1959. 3. Amosov, N. M.: Pulmonary Resection With Mechanical Bronchial Suturing, Tuberkulozis (Budapest) 13: 353-357, 1950. 4. Amosov, N. M., and Berezovski, K. K.: Development of Pulmonary Surgery in the Ukraine, Grudn. Khir. 3 : 72-77, 1961. 5. Amosov, N. M., Berezovski, K. K., and Zabroda, G. S.: Results of 100 Pulmonary Resec tions With the TJKL-60, Eksp. Khir. 3 : 3-7, 1958. 6. Amosov, N . M., and Dedkov, I. P . : On Bilateral Lung Resections, Khirurgiia 35: 19-24, 1959. 7. Androsov, P. I., Potekhina, L. A., Savchenko, E. D., Strekopytov, A. A., Tliakova, L. S., and Sheinber: A New Method for Suturing the Bronchial Stump, Khirurgiia, No. 8: 66-70, 1955. 8. Quinby, W. C . and Morse, G. W.: Experimental Pneumonectomy and Application to Man, Boston M. & S. J . 165: 121, 1911.