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THE RESULTS OF RAISING THE RESECTABILITY RATE IN OPERATIONS FOR LUNG CARCINOMA
THE RESULTS OF RAISING THE RESECTABILITY RATE I N OPERATIONS FOR L U N G CARCINOMA R. Abbey Smith, M.Ch., F.R.C.S., Warwick, Warwickshire,
England
I
N the period from 1951 through 1963, a policy of removing the tumor by some form of resection in every patient suffering from lung carcinoma, considered resectable before operation, has been followed. Some 600 patients have been personally explored and the tumor removed from 568 patients, a resectability rate of 95 per cent. In analyzing the results, the classification suggested by Chamberlain, McNeill, Parnassa, and Edsall 1 will be followed. The operation will be described as "standard" when the specimen consisted of lung and mediastinal lymph nodes; "extended" when complete resection required removal of extrapleural structures invaded by carcinoma, and "noncurative" when inaccessible car cinoma could not be removed (in this type of resection, therefore, carcinomatous tissue remained in the thorax after the conclusion of the operation). The re sults of the extended and noncurative types of operation will be considered, especially in those patients operated upon more than 5 years previously. It is not possible to detail the indications for operation in each patient. No clear sign of inoperability existed in any patient and each, therefore, was explored. Allocation into one of the three types of resection has not always been easy, although most fall naturally into the classification mentioned. It can be said of a number that whereas at the initial examination of the hilum at operation it seemed inevitable that some inaccessible extension of tumor could not be resected (a noncurative resection), after a wide dissection, com plete removal was achieved by inclusion of some extrapulmonary structure (an extended resection). Approximately 33 per cent of all resections were extended or noncurative. It might be asked, if the principle of cutting across the tumor to effect removal is accepted, why any lesion need be considered nonresectable. Experience has shown that in three circumstances the patient's prospects cannot be improved by continuing with resection. First, when the preoperative assessment suggests that only lobeetomy rather than pneumoneetomy will be tolerable. In 39 patients over the age of 62 years in whom the local extent of
Prom the King Edward VII Memorial Chest Hospital, Hertford Hill, Nr. Warwick, War wickshire, England. Sponsored by J. Maxwell Chamberlain, M.D., New York, N. Y. Read at the Forty-fourth Annual Meeting of the American Association for Thoracic Surgery, Montreal, Quebec, Canada, April 27, 28, and 29, 1964. 418
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the tumor made pneumonectomy necessary, the average postoperative survival was, if one patient is excluded, only 6 months. Lobectomy when possible has always been the operation of choice in the older patient, and the disappointing results of pneumonectomy in patients over 62 years of age in this series is a measure of the local extent of the tumor rather than the ability of a 62-year-old patient to withstand a standard pneumonectomy. The second reason for abandon ing resection is the presence of widespread lymph gland invasion by encephaloid, undifferentiated carcinoma which cannot be totally removed. Finally, invasion of the chest wall which cannot be included as part of an extended resection—in the sternum or vertebral column, for example. No patient with residual tumor on the chest wall at the conclusion of operation has lived 2 years. Table I shows the patients operated upon more than 5 years previously. The follow-up of each of these patients is known; none has been lost to followup and 'each has been seen and examined clinically and radiologically at reg ular intervals. Only 4 patients from the entire group of 600 patients have moved outside the area of a personal follow-up. The radiological check of these 4 has continued. The cause of death in only one patient, who died 9 years after a noncurative resection from hemoptysis, is in real doubt. Table II shows the postoperative deaths after 56 noncurative resections carried out before 1958. This figure of 21.6 per cent is high; many of these patients had extensive penetration of the mediastinum, more severe than the lesion treatable by an extended resection. The figure has been significantly reduced by a number of factors. At the present day the hospital mortality for the 600 patients is 6.5 per cent and for the extended and noncurative resection group it is less than 10 per cent. TABLE I . PERIOD 1951-1958
Total operations Resections Without resection Hospital deaths 5-year survivors
TABLE I I .
12
302
HOSPITAL D E A T H S
CAUSE OF DEATH
|
288 14 26 62
(56
95.4% 4.6% 8.6% 20.5%
NONCURATIVE
PATIENTS
|
RESECTIONS) DAY OF DEATH
Superior vena cava involvement
3
At operation Dayl Dayl
Bronchopleural fistula
3
Day 6 Day 12 Day 12
Cardiorespiratory failure
5
Dayl Day 2 Day 2 Day 12 Day 28
Hemorrhage from peptic ulcer
1
Day 15
420
ABBEY SMITH
J. Thoracic and Cardiovas. Surg.
The causes of hospital death in the pre-1958 period fall under three main headings, namely, bronchopleural fistula, damage to the superior vena cava, and cardiorespiratory failure. An attempt has been made to reduce the incidence of bronchopleural fistula due to the inclusion of tumor tissue in the bronchial stump in left-sided pneumonectomy, by suture of the trachea after mobilization of the aortic arch, and detachment of the main bronchus, including a portion of trachea. By standard pneumonectomy an endobronchial carcinoma of the orifice of the left main bronchus must be considered inoperable, or if it is resected by a standard procedure, inclusion of tumor in the suture line cannot be avoided. In some circumstances, resection of the superior vena cava at the time of an extended pneumonectomy may be necessary. A technique has been described elsewhere.2
Pig. 1.—George O.: 69 years of age. The patient was unfit for pneumonectomy because of respiratory insufficiency. Fig. 2.—Roentgenogram of George O. made after sleeve resection of left upper lobe and 3.5 cm. segment of main pulmonary artery. Patient was well in third year.
The hospital mortality from cardiorespiratory deaths has been reduced by preoperative selection of patients, by leaving tumor on or in the atrial wall rather than attempting its complete removal, and by avoiding pneumonectomy in the patient over the arbitrary age of 62 years. This may necessitate a modified form of sleeve resection of the bronchus, or Teflon patch closure of the bronchial stump following lower lobectomy where the bronchus has had to be sectioned so close to the upper lobe as to prevent closure by conventional methods, or a combined sleeve resection of bronchus and segment of pulmonary artery (Figs. 1 and 2).
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These four variants of the extended operation-supra-aortic division of the left main bronchus, resection of the superior vena eava with pneumonectomy, Teflon patch closure of the lower lobe stump, and combined sleeve resection of left upper lobe and pulmonary artery have been carried out on 14 patients with no mortality or morbidity. They have contributed something to the re duction in hospital mortality of resection for locally advanced carcinoma. Only the first of these methods has not already been described. Technique of supra-aortic closure of trachea for carcinoma of the left main bronchus involving the trachea. The patient is placed in the prone (Overholt) position on the operating table after intubation of the right main bronchus with a suitable endobronchial cuffed tube. The fifth left rib is resected. If the situation of the tumor in the left main bronchus is so proximal as to make conventional left pneumonectomy impracticable, the aortic arch and left subclavian artery are mobilized by division of at least two pairs of intercostal arteries; a tape is placed around the arch and the arch is retracted toward the operator. The esophagus and the thoracic duct are retracted medially. An ex posure of the lower end of the trachea, the carina, and the origin of the left main bronchus is obtained. The lower end of the left lateral wall of the trachea is cut away at the origin of the left main bronchus; the transection is completed to the carina. No clamp is necessary as the right main bronchus is blocked off by the cuffed tube through which anesthesia is maintained. The trachea is sutured with interrupted thread sutures. The left main bronchus containing the tumor is delivered below the aortic arch and the tape retracting the aortic arch is removed. The severed left main bronchus is clamped to prevent leakage and the operation is completed as a conventional pneumonectomy. In most patients, however, in whom this operation has been carried out, the tumor has been adherent to the superior pulmonary vein. The vein has been divided intrapericardially on the atrial wall and the atrial wall sutured, because of the impossibility of division of this vein outside the pericardium. Figs. 3 through 7 demonstrate the operation. RESULTS
Deaths.—The hospital mortality rate for extended and noncurative resec tion is now less than 10 per cent. In the survivors we have regarded the period of total incapacity and the terminal illness to be shorter and less of an emo-
TABLE
I I I . DEATHS
PATIENTS SURVIVING RESECTION
3 YR.
3 YEARS OR MORE AFTER
DEATHS CARCINOMA
5 Non12 curative Extended 15 7 Standard 89 23 •Cause of death uncertain in this patient.
OTHER CAUSES
RESECTION DEATHS PROM CARCINOMA I N RELATION TO YEARS SINCE OPERATION
0
3-4 4
0 6
6 14
|
5-12 1* 1 9
422
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Fig. 3.—William W.: 42 years of age. Squamous cell carcinoma at origin of left main bronchus. Empyema present. Fig. 4.—Tracheogram of William W. made after extended pneumonectomy with supraaortic suture of trachea. Patient has returned to former occupation.
Fig. 5.—Helen M. 49 years of age. Polypoid squamous cell carcinoma in origin of left main bronchus. Fig. 6.—Tracheogram of Helen M. made after extended pneumonectomy with supra-aortic suture of trachea. Patient has returned to former occupation.
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tional and physical strain in patients undergoing resection than in the group in which resection was not possible. A striking feature of the cause of late death in this follow-up is seen in Table III, which shows the death rate from lung carcinoma more than 3 years after successful operation. In all but 3 of the patients who died of lung car cinoma (shown in Table I I I ) , the first evidence of extension of the disease was in the lung or mediastinum, although the autopsy rate was not sufficiently high to state that these were the only sites of tumor at death.
I »
Pig. 7.—Operative sketch of supra-aortic pneumonectomy with patient in Overholt position. The arch and esophagus are retracted and the suture lines on the trachea and atrial wall are shown.
After 12 noncurative operations performed 3 or more years previously, 5 patients died of lung carcinoma. After 15 extended operations, 7 patients died of lung carcinoma, and after 89 standard operations, 23 died of lung carcinoma and 6 from other causes. Thus, of the 116 patients who survived for more than 3 years, 35 died of lung carcinoma; or from a total of 41 deaths, 35 were due to lung carcinoma (81 per cent). This high carcinoma death rate cannot be wholly due to the proportion of operations in which the tumor was incompletely removed, because it can be seen that the death rate from car cinoma following standard operations (23 out of 41 deaths) is 56 per cent. Nine patients died of carcinoma between the fifth and twelfth years after op eration. Another patient is alive with recurrence in the opposite lung 8 years after operation. Whether these represent second, primary, or recurrent tumors is outside the scope of this paper.
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Age at the time of resection will presumably influence the cause of death. A series of patients of the average age of 50 at the time of resection may show a higher postoperative carcinoma death rate than a series of the average age of 65, because the life expectancy is reduced in the older series and death is more likely from other causes. The average age at operation in this series was 54 years. The roentgenograms of 3 patients with lung carcinoma in the ninth, tenth, and eleventh postoperative years are shown (Figs. 8 to 10). Conclusions from an examination of the mode of death in Table I I I are that exposure to factors predisposing to carcinoma (smoking) should be pro hibited after operation, and that some form of long-term eytotoxie therapy might help to reduce the number of late manifestations of the disease, or delay the onset of signs of the disease for a longer period. Thompson4 has not observed death from metastases after the tenth postoperative year. Survival.—Of the patients surviving extended and noncurative resection, 2 were, it was thought, made worse by operation: one because of a leak from the esophagus into the pneumonectomy space which required tube drainage, the other from gross respiratory insufficiency. One half of the survivors were able for a time to return to some form of work. Table I I I shows that 27 pa tients were alive at the end of 3 years after operation (12 noncurative and 15 extended resections)—evidence of the short-term benefit from the operation. The long-term results are shown in Table IV. TABLE IV.
62
SURVIVORS FROM
TYPE OF OPERATION
Noncurative Extended Standard Totals
288
EESECTIONS: LENGTH OP OPERATION
NUMBER OPERATED UPON
56 47 185 288
OF SURVIVAL RELATED TO
TYPE
TIME INTERVAL SINCE OPERATION
5-7 YR. 2 3 27 32
|
8-12 YR. 4 2 24 30
Six patients of 56 who had noncurative resections lived more than 5 years; 3 had residual tumor on the atrial wall. One of the 6 died 9 years after opera tion. The residual tumor was in the bronchus stump and the cause of death was unproved (Table I I I ) . Five out of 47 patients with extended resections lived more than 5 years. One of these died from recurrence in the eleventh post operative year. At operation, an involved portion of the diaphragm was resected with the lung (see Fig. 10). The figure for survival from extended resection resembles that described by Price Thomas.3 He reported the cases of 7 patients from 60 similar opera tions, with 4 still living at the time of reporting. The present series thus adds to the evidence that extended operation is worth while. That 6 of 56 patients who had noncurative resections survived 5 years (approximately 10 per cent) places this operation in the same category. It should be noted that of the 11 5-year survivors of extended and noncurative resection, 9 are alive and well at the time of reporting.
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Fig. 8.—Carcinoma right upper lobe, ninth year after left upper lobectomy. Caval ob struction developed and the patient died 5 months after first evidence of fresh tumor. Fig. 9.—Carcinoma right lower lobe, tenth year after left pneumonectomy. Patient died 9 months after first evidence of fresh tumor.
Fig. 10.—Carcinoma left lower lobe and carina, eleventh year after extended right pneumonec tomy. Stridor developed and patient died 7 months after first evidence of fresh tumor.
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These results strongly support the view expressed by Chamberlain and others 1 that the biologic behavior of bronchogenic carcinoma is often para doxical; it may become extensive and invasive locally without detectable sys temic dissemination, and such lesions deserve an extended surgical effort to accomplish complete removal. Stated in round figures, this series may be summarized in this way. From every 100 patients explored the tumor was removed in 96 patients, by an ex tended or noncurative resection in 30, and of these 30 patients, 3 will survive 5 years. Of the remaining 66 patients treated by a standard operation, 18 will live for 5 years. Table IV shows the 5-year survival rate for standard resection in this series to be 27.5 per cent (51 survivors from 185 resections). A final analysis of the statistics shows that at operation 33 per cent of resections are noncurative or extended; at 3 years, 23 per cent of survivors have had these types of resection (27 patients from a total of 116 resections survived 3 years, Table I I I ) , and, at 5 years, 17 per cent of survivors have had these types of resection (11 patients from a total of 62 who survived 5 years, Table I V ) . These are significant percentages of the total survivors. Every described cell type of lung carcinoma, except alveolar cell, is rep resented in our late survivors of extended and noncurative resection. Factors other than cell type therefore influence the decision to attempt resection. These are: a young patient with few symptoms, a hard, circumscribed tumor pref erably endobronchial and not associated with obvious hilar gland metastases. If residual tumor must be left, the prognosis improves if the tumor is situated on the vascular structures or heart rather than in the bronchial stump, chest wall, or inaccessible lymph glands. I am greatly indebted to the Research Committee of the Birmingham Regional Hospital Board for their assistance, and to the Wellcome Trust for a Wellcome Research Travel Grant enabling certain aspects of this study t o continue. REFERENCES 1. Chamberlain, J . M., McNeill, T. M., Parnassa, P., and Edsall, J . R.: Bronchogenic Car cinoma:
An Aggressive
Surgical Attitude, J .
THORACIC & CARDIOVAS. SURG. 38:
727, 1959. 2. Smith, R. A . : Surgery in the Treatment of Locally Advanced Lung Carcinoma, Thorax 18: 21, 1963. 3. Thomas, C. P . : Conservative and Extensive Resection for Carcinoma of the Lung, Ann. Roy. Coll. Surgeons 24: 345, 1959. 4. Thompson, V. C.: The Present Position Relating to Cancer of the Lung, (Symposium by the Thoracic Society), Thorax 15: 1, 1960.
DISCUSSION DR. RICHARD A. RASMUSSEN, Grand Rapids, Mich.—It is a pleasure to discuss Mr. Smith's paper in which he has presented an aggressive approach to the surgical treat ment of carcinoma of the lung. We have heard Dr. Clagett and others advocate lobectomy as being equally as good as pneumonectomy in the properly selected case. Others here un doubtedly agree with this policy. I expect Mr. Smith accepts this, too. The resection rate of 96 per cent is very high. I t would seem that a policy of resection in nearly every ease would require careful
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preoperative selection in order to achieve this high resection rate and a hospital mortality of about 7 per cent. I t is suggested that some patients might be denied surgical exploration and possibly a lesser, curative or palliative, resection if such a rigid attitude is observed. I would further suggest that exploratory thoracotomy is necessary to obtain the diagnosis and to determine resectability. I should like to know what per cent of Mr. Smith's total patients who were seen were treated surgically. I assume his criteria of inoperability are essentially those which most of us accept; namely, recurrent or phrenic nerve paralysis, positive mediastinal lymph nodes, usually, local extension to vital structures, distant metastasis, or bloody pleural effusion. With regard to incomplete removal of tumor, I believe these factors should be men tioned: for diagnosis this certainly is acceptable; excision of an abscess distal to an ob structing lesion; to relieve symptoms caused by local extension to the chest wall; or for mechanical reasons such as removal of a large tumor mass prior to irradiation. These pro cedures should be utilized with discretion because the complications are more frequent than with complete clean resections. I should like to ask whether or not Mr. Smith uses irradiation therapy routinely. Our experience, as reported in 1963, (Choice of Operation in the Treatment of Bronchogenic Carcinoma by R. A. Rasmussen, M.D., C. E. Basinger, M.D., R. W. Harrison, M.D., and R. H. Meade, M.D., Grand Rapids, Michigan, and read before American College of Chest Physicians a t Atlantic City, June 1963) consisted of 813 proved cases of bronchogenic carcinoma of which we considered 398 of the patients or 49 per cent, to be operable. Re section was accomplished in 209 or 52.5 per cent of those considered operable. The 189, or 47.5 per cent, explored but not resected, resulted in a 9 per cent mortality. A resection in this group, especially the older individual, would have resulted in an even higher mortality and morbidity. We have an unknown result in 1 per cent of our operable cases. Our over-all surgical (30 day) mortality is 10 per cent. We have a 35.8 per cent 3-year survival after resection. Six of our explored, but not resected, patients have lived over 3 years with the disease. This emphasizes the frequent slow growth of bronchogenic carcinoma. The change in policy toward type of resection is apparent during the interval be tween 1947 and 1963. Pneumonectomy was emphasized prior to 1956. Lobectomy or even a lesser resection (partial lobectomy or excision) was often done after that date. This was because of an attempt to extend resection to the poorer risk patient. There were 325 pa tients of the 398 operable cases who were over 50 years of age; 42 of these were over 70 years of age. I n general, with comparable age groups, I would suggest that with the more radical or aggressive surgical policy the higher the mortality and morbidity will be.
DR. J E A N MATHEY, Paris, France.—One word to thank you very much because I am very glad to be here at your meeting and to learn many, many things. Secondly, I ask you to excuse me because I speak English very poorly, and it is difficult to understand me. On the matter of carcinoma, my statistics are very small. I have two targets when operating. One is to keep a good, functional ventilation, and the second is to do correct carcinogenic operations. [Slide] Here you see the evolution of the procedures from 1944 to 1963. This shows that for certain lobectomy was done with resection of the main bronchus and an end-to-end bronchial anastomosis. From 1959 to 1963, you see the pneumonectomies are just half the total resections. [Slide] The group of partial resections is growing, because in certain cases it is pos sible to do the easiest operation, an upper right lobectomy with resection and anastomosis of the main bronchus. I n this case we have done a resection of the lower and middle lobe and of the main bronchus, and end-to-side anastomosis of the upper lobe bronchus with the trachea was done. I n 2 cases there was an invasion of the lower part of the trachea, and it was neces sary, with a right pneumonectomy, to do a tracheal resection. In the 2 cases it was necessary
428
ABBEY SMITH
J. Thoracic and Cardiovas. Surg.
to remove 4 cm. of the trachea and to do the bronchial anastomosis with the trachea. One of these patients died 10 months after the operation. The other was operated upon in August, 1960, and he is still living after 3 years. I hope he will live for 5 years, but I don't know. Another thing is the question of vascular and arterial invasion. [Slide] I n one case the patient had had an artificial pneumothorax several years pre viously on the right side. There were tuberculous lesions and also a carcinoma of the left upper bronchus. On functional examination pneumonectomy was impossible. [Slide] My program was to do a resection of the left upper lobe with a bronchial anastomosis and resection of the bronchus, but unfortunately, or fortunately, I don't know which, there was also an invasion of the left pulmonary artery, and it was necessary to resect and remove the extrapericardial segment of the artery and to cut just above the artery at the apex of the lower lobe. Anastomosis was very easy. From a functional point of view the result was good. [Slide] Here you can see after the operation the angiography and the good result with the circulation. I t was also good for the ventilation. During the winter this patient was in the mountains skiing, and during the summer he was in the Mediterranean and was doing deep diving and fishing. DR. J O H N MAXWELL CHAMBERLAIN, New York, N. Y.—Mr. Smith has provided us with a very exciting presentation. He obviously is a "cancer hater" and a most courageous man. I think that goes for Dr. Mathey as well. My residents and younger surgeons often ask, "How do you determine resectability?" I think from Mr. Smith's presentation we can say that resectability is probably a state of mind combined with a certain amount of experience and skill. He has shown us that the resectability rate is almost 100 per cent in his hands. A cross-section of the literature in the United States reports the resectability rate as low as 33% per cent. The average is somewhere around 55 to 60 per cent. Before this Association in 1959 we talked about our extended efforts to perform re section in these difficult cases, and I can report to you now that our figures are somewhat similar to Mr. Abbey Smith's. Of those extended efforts, 15 per cent of the patients are 5-year cures. There is just one technical point I might suggest to a large audience of thoracic sur geons. In case it becomes necessary to resect the superior vena cava (at least if the invasion by the tumor is in the middle third) it is possible to mobilize the right pulmonary artery all the way to its origin, and then it may be used as a graft instead of a prosthesis. We have done this in one case. The graft was successful, but during the technical procedure it was necessary to occlude the superior vena cava entirely for 15 minutes, and the patient later died of cerebral complications. I would like to ask Mr. Abbey Smith how he feels about complete occlusion of the superior vena cava, and how long it can be occluded safely. The surgeon at the operating table has a critical decision to make. When he takes a patient to the operating room, he accepts a great obligation. The decision to close the patient as nonreseetable is a most serious one. I think Mr. Abbey Smith has given us a target at which we should all aim. MR. ABBEY SMITH (Closing) .—There is very little I have to add to what I have already said. I think if there is any misunderstanding about what those who take a radical approach to carcinoma try and achieve, the misunderstanding is that we attempt to resect too many advanced lesions. I think certainly all I try to do, having selected the patient before operation, is in every case to remove the tumor. My selection is really before opera tion rather than at operation. Dr. Rasmussen mentioned the number of patients on whom we operate. We operate upon only 1 in 12 patients who die of lung carcinoma, and of these 12 only 3 are submitted for a surgical opinion.
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Dr. Chamberlain's method of superior vena caval replacement is obviously important. He mentioned the time the superior vena cava can be occluded. I n the 4 patients in whom we used the method of vena caval occlusion with pneumonectomy, we occluded the vena cava for 20 minutes in each of these 4 patients without any evidence of cerebral damage; but there again, these patients were very carefully selected before operation. None of the 4 was over 55 years of age. Finally, may I thank you again and through you the members of the Association, your Program Committee, and Dr. Maxwell Chamberlain, for the very great privilege of reading this paper today.
England
I
N the period from 1951 through 1963, a policy of removing the tumor by some form of resection in every patient suffering from lung carcinoma, considered resectable before operation, has been followed. Some 600 patients have been personally explored and the tumor removed from 568 patients, a resectability rate of 95 per cent. In analyzing the results, the classification suggested by Chamberlain, McNeill, Parnassa, and Edsall 1 will be followed. The operation will be described as "standard" when the specimen consisted of lung and mediastinal lymph nodes; "extended" when complete resection required removal of extrapleural structures invaded by carcinoma, and "noncurative" when inaccessible car cinoma could not be removed (in this type of resection, therefore, carcinomatous tissue remained in the thorax after the conclusion of the operation). The re sults of the extended and noncurative types of operation will be considered, especially in those patients operated upon more than 5 years previously. It is not possible to detail the indications for operation in each patient. No clear sign of inoperability existed in any patient and each, therefore, was explored. Allocation into one of the three types of resection has not always been easy, although most fall naturally into the classification mentioned. It can be said of a number that whereas at the initial examination of the hilum at operation it seemed inevitable that some inaccessible extension of tumor could not be resected (a noncurative resection), after a wide dissection, com plete removal was achieved by inclusion of some extrapulmonary structure (an extended resection). Approximately 33 per cent of all resections were extended or noncurative. It might be asked, if the principle of cutting across the tumor to effect removal is accepted, why any lesion need be considered nonresectable. Experience has shown that in three circumstances the patient's prospects cannot be improved by continuing with resection. First, when the preoperative assessment suggests that only lobeetomy rather than pneumoneetomy will be tolerable. In 39 patients over the age of 62 years in whom the local extent of
Prom the King Edward VII Memorial Chest Hospital, Hertford Hill, Nr. Warwick, War wickshire, England. Sponsored by J. Maxwell Chamberlain, M.D., New York, N. Y. Read at the Forty-fourth Annual Meeting of the American Association for Thoracic Surgery, Montreal, Quebec, Canada, April 27, 28, and 29, 1964. 418
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the tumor made pneumonectomy necessary, the average postoperative survival was, if one patient is excluded, only 6 months. Lobectomy when possible has always been the operation of choice in the older patient, and the disappointing results of pneumonectomy in patients over 62 years of age in this series is a measure of the local extent of the tumor rather than the ability of a 62-year-old patient to withstand a standard pneumonectomy. The second reason for abandon ing resection is the presence of widespread lymph gland invasion by encephaloid, undifferentiated carcinoma which cannot be totally removed. Finally, invasion of the chest wall which cannot be included as part of an extended resection—in the sternum or vertebral column, for example. No patient with residual tumor on the chest wall at the conclusion of operation has lived 2 years. Table I shows the patients operated upon more than 5 years previously. The follow-up of each of these patients is known; none has been lost to followup and 'each has been seen and examined clinically and radiologically at reg ular intervals. Only 4 patients from the entire group of 600 patients have moved outside the area of a personal follow-up. The radiological check of these 4 has continued. The cause of death in only one patient, who died 9 years after a noncurative resection from hemoptysis, is in real doubt. Table II shows the postoperative deaths after 56 noncurative resections carried out before 1958. This figure of 21.6 per cent is high; many of these patients had extensive penetration of the mediastinum, more severe than the lesion treatable by an extended resection. The figure has been significantly reduced by a number of factors. At the present day the hospital mortality for the 600 patients is 6.5 per cent and for the extended and noncurative resection group it is less than 10 per cent. TABLE I . PERIOD 1951-1958
Total operations Resections Without resection Hospital deaths 5-year survivors
TABLE I I .
12
302
HOSPITAL D E A T H S
CAUSE OF DEATH
|
288 14 26 62
(56
95.4% 4.6% 8.6% 20.5%
NONCURATIVE
PATIENTS
|
RESECTIONS) DAY OF DEATH
Superior vena cava involvement
3
At operation Dayl Dayl
Bronchopleural fistula
3
Day 6 Day 12 Day 12
Cardiorespiratory failure
5
Dayl Day 2 Day 2 Day 12 Day 28
Hemorrhage from peptic ulcer
1
Day 15
420
ABBEY SMITH
J. Thoracic and Cardiovas. Surg.
The causes of hospital death in the pre-1958 period fall under three main headings, namely, bronchopleural fistula, damage to the superior vena cava, and cardiorespiratory failure. An attempt has been made to reduce the incidence of bronchopleural fistula due to the inclusion of tumor tissue in the bronchial stump in left-sided pneumonectomy, by suture of the trachea after mobilization of the aortic arch, and detachment of the main bronchus, including a portion of trachea. By standard pneumonectomy an endobronchial carcinoma of the orifice of the left main bronchus must be considered inoperable, or if it is resected by a standard procedure, inclusion of tumor in the suture line cannot be avoided. In some circumstances, resection of the superior vena cava at the time of an extended pneumonectomy may be necessary. A technique has been described elsewhere.2
Pig. 1.—George O.: 69 years of age. The patient was unfit for pneumonectomy because of respiratory insufficiency. Fig. 2.—Roentgenogram of George O. made after sleeve resection of left upper lobe and 3.5 cm. segment of main pulmonary artery. Patient was well in third year.
The hospital mortality from cardiorespiratory deaths has been reduced by preoperative selection of patients, by leaving tumor on or in the atrial wall rather than attempting its complete removal, and by avoiding pneumonectomy in the patient over the arbitrary age of 62 years. This may necessitate a modified form of sleeve resection of the bronchus, or Teflon patch closure of the bronchial stump following lower lobectomy where the bronchus has had to be sectioned so close to the upper lobe as to prevent closure by conventional methods, or a combined sleeve resection of bronchus and segment of pulmonary artery (Figs. 1 and 2).
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These four variants of the extended operation-supra-aortic division of the left main bronchus, resection of the superior vena eava with pneumonectomy, Teflon patch closure of the lower lobe stump, and combined sleeve resection of left upper lobe and pulmonary artery have been carried out on 14 patients with no mortality or morbidity. They have contributed something to the re duction in hospital mortality of resection for locally advanced carcinoma. Only the first of these methods has not already been described. Technique of supra-aortic closure of trachea for carcinoma of the left main bronchus involving the trachea. The patient is placed in the prone (Overholt) position on the operating table after intubation of the right main bronchus with a suitable endobronchial cuffed tube. The fifth left rib is resected. If the situation of the tumor in the left main bronchus is so proximal as to make conventional left pneumonectomy impracticable, the aortic arch and left subclavian artery are mobilized by division of at least two pairs of intercostal arteries; a tape is placed around the arch and the arch is retracted toward the operator. The esophagus and the thoracic duct are retracted medially. An ex posure of the lower end of the trachea, the carina, and the origin of the left main bronchus is obtained. The lower end of the left lateral wall of the trachea is cut away at the origin of the left main bronchus; the transection is completed to the carina. No clamp is necessary as the right main bronchus is blocked off by the cuffed tube through which anesthesia is maintained. The trachea is sutured with interrupted thread sutures. The left main bronchus containing the tumor is delivered below the aortic arch and the tape retracting the aortic arch is removed. The severed left main bronchus is clamped to prevent leakage and the operation is completed as a conventional pneumonectomy. In most patients, however, in whom this operation has been carried out, the tumor has been adherent to the superior pulmonary vein. The vein has been divided intrapericardially on the atrial wall and the atrial wall sutured, because of the impossibility of division of this vein outside the pericardium. Figs. 3 through 7 demonstrate the operation. RESULTS
Deaths.—The hospital mortality rate for extended and noncurative resec tion is now less than 10 per cent. In the survivors we have regarded the period of total incapacity and the terminal illness to be shorter and less of an emo-
TABLE
I I I . DEATHS
PATIENTS SURVIVING RESECTION
3 YR.
3 YEARS OR MORE AFTER
DEATHS CARCINOMA
5 Non12 curative Extended 15 7 Standard 89 23 •Cause of death uncertain in this patient.
OTHER CAUSES
RESECTION DEATHS PROM CARCINOMA I N RELATION TO YEARS SINCE OPERATION
0
3-4 4
0 6
6 14
|
5-12 1* 1 9
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Fig. 3.—William W.: 42 years of age. Squamous cell carcinoma at origin of left main bronchus. Empyema present. Fig. 4.—Tracheogram of William W. made after extended pneumonectomy with supraaortic suture of trachea. Patient has returned to former occupation.
Fig. 5.—Helen M. 49 years of age. Polypoid squamous cell carcinoma in origin of left main bronchus. Fig. 6.—Tracheogram of Helen M. made after extended pneumonectomy with supra-aortic suture of trachea. Patient has returned to former occupation.
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tional and physical strain in patients undergoing resection than in the group in which resection was not possible. A striking feature of the cause of late death in this follow-up is seen in Table III, which shows the death rate from lung carcinoma more than 3 years after successful operation. In all but 3 of the patients who died of lung car cinoma (shown in Table I I I ) , the first evidence of extension of the disease was in the lung or mediastinum, although the autopsy rate was not sufficiently high to state that these were the only sites of tumor at death.
I »
Pig. 7.—Operative sketch of supra-aortic pneumonectomy with patient in Overholt position. The arch and esophagus are retracted and the suture lines on the trachea and atrial wall are shown.
After 12 noncurative operations performed 3 or more years previously, 5 patients died of lung carcinoma. After 15 extended operations, 7 patients died of lung carcinoma, and after 89 standard operations, 23 died of lung carcinoma and 6 from other causes. Thus, of the 116 patients who survived for more than 3 years, 35 died of lung carcinoma; or from a total of 41 deaths, 35 were due to lung carcinoma (81 per cent). This high carcinoma death rate cannot be wholly due to the proportion of operations in which the tumor was incompletely removed, because it can be seen that the death rate from car cinoma following standard operations (23 out of 41 deaths) is 56 per cent. Nine patients died of carcinoma between the fifth and twelfth years after op eration. Another patient is alive with recurrence in the opposite lung 8 years after operation. Whether these represent second, primary, or recurrent tumors is outside the scope of this paper.
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Age at the time of resection will presumably influence the cause of death. A series of patients of the average age of 50 at the time of resection may show a higher postoperative carcinoma death rate than a series of the average age of 65, because the life expectancy is reduced in the older series and death is more likely from other causes. The average age at operation in this series was 54 years. The roentgenograms of 3 patients with lung carcinoma in the ninth, tenth, and eleventh postoperative years are shown (Figs. 8 to 10). Conclusions from an examination of the mode of death in Table I I I are that exposure to factors predisposing to carcinoma (smoking) should be pro hibited after operation, and that some form of long-term eytotoxie therapy might help to reduce the number of late manifestations of the disease, or delay the onset of signs of the disease for a longer period. Thompson4 has not observed death from metastases after the tenth postoperative year. Survival.—Of the patients surviving extended and noncurative resection, 2 were, it was thought, made worse by operation: one because of a leak from the esophagus into the pneumonectomy space which required tube drainage, the other from gross respiratory insufficiency. One half of the survivors were able for a time to return to some form of work. Table I I I shows that 27 pa tients were alive at the end of 3 years after operation (12 noncurative and 15 extended resections)—evidence of the short-term benefit from the operation. The long-term results are shown in Table IV. TABLE IV.
62
SURVIVORS FROM
TYPE OF OPERATION
Noncurative Extended Standard Totals
288
EESECTIONS: LENGTH OP OPERATION
NUMBER OPERATED UPON
56 47 185 288
OF SURVIVAL RELATED TO
TYPE
TIME INTERVAL SINCE OPERATION
5-7 YR. 2 3 27 32
|
8-12 YR. 4 2 24 30
Six patients of 56 who had noncurative resections lived more than 5 years; 3 had residual tumor on the atrial wall. One of the 6 died 9 years after opera tion. The residual tumor was in the bronchus stump and the cause of death was unproved (Table I I I ) . Five out of 47 patients with extended resections lived more than 5 years. One of these died from recurrence in the eleventh post operative year. At operation, an involved portion of the diaphragm was resected with the lung (see Fig. 10). The figure for survival from extended resection resembles that described by Price Thomas.3 He reported the cases of 7 patients from 60 similar opera tions, with 4 still living at the time of reporting. The present series thus adds to the evidence that extended operation is worth while. That 6 of 56 patients who had noncurative resections survived 5 years (approximately 10 per cent) places this operation in the same category. It should be noted that of the 11 5-year survivors of extended and noncurative resection, 9 are alive and well at the time of reporting.
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Fig. 8.—Carcinoma right upper lobe, ninth year after left upper lobectomy. Caval ob struction developed and the patient died 5 months after first evidence of fresh tumor. Fig. 9.—Carcinoma right lower lobe, tenth year after left pneumonectomy. Patient died 9 months after first evidence of fresh tumor.
Fig. 10.—Carcinoma left lower lobe and carina, eleventh year after extended right pneumonec tomy. Stridor developed and patient died 7 months after first evidence of fresh tumor.
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These results strongly support the view expressed by Chamberlain and others 1 that the biologic behavior of bronchogenic carcinoma is often para doxical; it may become extensive and invasive locally without detectable sys temic dissemination, and such lesions deserve an extended surgical effort to accomplish complete removal. Stated in round figures, this series may be summarized in this way. From every 100 patients explored the tumor was removed in 96 patients, by an ex tended or noncurative resection in 30, and of these 30 patients, 3 will survive 5 years. Of the remaining 66 patients treated by a standard operation, 18 will live for 5 years. Table IV shows the 5-year survival rate for standard resection in this series to be 27.5 per cent (51 survivors from 185 resections). A final analysis of the statistics shows that at operation 33 per cent of resections are noncurative or extended; at 3 years, 23 per cent of survivors have had these types of resection (27 patients from a total of 116 resections survived 3 years, Table I I I ) , and, at 5 years, 17 per cent of survivors have had these types of resection (11 patients from a total of 62 who survived 5 years, Table I V ) . These are significant percentages of the total survivors. Every described cell type of lung carcinoma, except alveolar cell, is rep resented in our late survivors of extended and noncurative resection. Factors other than cell type therefore influence the decision to attempt resection. These are: a young patient with few symptoms, a hard, circumscribed tumor pref erably endobronchial and not associated with obvious hilar gland metastases. If residual tumor must be left, the prognosis improves if the tumor is situated on the vascular structures or heart rather than in the bronchial stump, chest wall, or inaccessible lymph glands. I am greatly indebted to the Research Committee of the Birmingham Regional Hospital Board for their assistance, and to the Wellcome Trust for a Wellcome Research Travel Grant enabling certain aspects of this study t o continue. REFERENCES 1. Chamberlain, J . M., McNeill, T. M., Parnassa, P., and Edsall, J . R.: Bronchogenic Car cinoma:
An Aggressive
Surgical Attitude, J .
THORACIC & CARDIOVAS. SURG. 38:
727, 1959. 2. Smith, R. A . : Surgery in the Treatment of Locally Advanced Lung Carcinoma, Thorax 18: 21, 1963. 3. Thomas, C. P . : Conservative and Extensive Resection for Carcinoma of the Lung, Ann. Roy. Coll. Surgeons 24: 345, 1959. 4. Thompson, V. C.: The Present Position Relating to Cancer of the Lung, (Symposium by the Thoracic Society), Thorax 15: 1, 1960.
DISCUSSION DR. RICHARD A. RASMUSSEN, Grand Rapids, Mich.—It is a pleasure to discuss Mr. Smith's paper in which he has presented an aggressive approach to the surgical treat ment of carcinoma of the lung. We have heard Dr. Clagett and others advocate lobectomy as being equally as good as pneumonectomy in the properly selected case. Others here un doubtedly agree with this policy. I expect Mr. Smith accepts this, too. The resection rate of 96 per cent is very high. I t would seem that a policy of resection in nearly every ease would require careful
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preoperative selection in order to achieve this high resection rate and a hospital mortality of about 7 per cent. I t is suggested that some patients might be denied surgical exploration and possibly a lesser, curative or palliative, resection if such a rigid attitude is observed. I would further suggest that exploratory thoracotomy is necessary to obtain the diagnosis and to determine resectability. I should like to know what per cent of Mr. Smith's total patients who were seen were treated surgically. I assume his criteria of inoperability are essentially those which most of us accept; namely, recurrent or phrenic nerve paralysis, positive mediastinal lymph nodes, usually, local extension to vital structures, distant metastasis, or bloody pleural effusion. With regard to incomplete removal of tumor, I believe these factors should be men tioned: for diagnosis this certainly is acceptable; excision of an abscess distal to an ob structing lesion; to relieve symptoms caused by local extension to the chest wall; or for mechanical reasons such as removal of a large tumor mass prior to irradiation. These pro cedures should be utilized with discretion because the complications are more frequent than with complete clean resections. I should like to ask whether or not Mr. Smith uses irradiation therapy routinely. Our experience, as reported in 1963, (Choice of Operation in the Treatment of Bronchogenic Carcinoma by R. A. Rasmussen, M.D., C. E. Basinger, M.D., R. W. Harrison, M.D., and R. H. Meade, M.D., Grand Rapids, Michigan, and read before American College of Chest Physicians a t Atlantic City, June 1963) consisted of 813 proved cases of bronchogenic carcinoma of which we considered 398 of the patients or 49 per cent, to be operable. Re section was accomplished in 209 or 52.5 per cent of those considered operable. The 189, or 47.5 per cent, explored but not resected, resulted in a 9 per cent mortality. A resection in this group, especially the older individual, would have resulted in an even higher mortality and morbidity. We have an unknown result in 1 per cent of our operable cases. Our over-all surgical (30 day) mortality is 10 per cent. We have a 35.8 per cent 3-year survival after resection. Six of our explored, but not resected, patients have lived over 3 years with the disease. This emphasizes the frequent slow growth of bronchogenic carcinoma. The change in policy toward type of resection is apparent during the interval be tween 1947 and 1963. Pneumonectomy was emphasized prior to 1956. Lobectomy or even a lesser resection (partial lobectomy or excision) was often done after that date. This was because of an attempt to extend resection to the poorer risk patient. There were 325 pa tients of the 398 operable cases who were over 50 years of age; 42 of these were over 70 years of age. I n general, with comparable age groups, I would suggest that with the more radical or aggressive surgical policy the higher the mortality and morbidity will be.
DR. J E A N MATHEY, Paris, France.—One word to thank you very much because I am very glad to be here at your meeting and to learn many, many things. Secondly, I ask you to excuse me because I speak English very poorly, and it is difficult to understand me. On the matter of carcinoma, my statistics are very small. I have two targets when operating. One is to keep a good, functional ventilation, and the second is to do correct carcinogenic operations. [Slide] Here you see the evolution of the procedures from 1944 to 1963. This shows that for certain lobectomy was done with resection of the main bronchus and an end-to-end bronchial anastomosis. From 1959 to 1963, you see the pneumonectomies are just half the total resections. [Slide] The group of partial resections is growing, because in certain cases it is pos sible to do the easiest operation, an upper right lobectomy with resection and anastomosis of the main bronchus. I n this case we have done a resection of the lower and middle lobe and of the main bronchus, and end-to-side anastomosis of the upper lobe bronchus with the trachea was done. I n 2 cases there was an invasion of the lower part of the trachea, and it was neces sary, with a right pneumonectomy, to do a tracheal resection. In the 2 cases it was necessary
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to remove 4 cm. of the trachea and to do the bronchial anastomosis with the trachea. One of these patients died 10 months after the operation. The other was operated upon in August, 1960, and he is still living after 3 years. I hope he will live for 5 years, but I don't know. Another thing is the question of vascular and arterial invasion. [Slide] I n one case the patient had had an artificial pneumothorax several years pre viously on the right side. There were tuberculous lesions and also a carcinoma of the left upper bronchus. On functional examination pneumonectomy was impossible. [Slide] My program was to do a resection of the left upper lobe with a bronchial anastomosis and resection of the bronchus, but unfortunately, or fortunately, I don't know which, there was also an invasion of the left pulmonary artery, and it was necessary to resect and remove the extrapericardial segment of the artery and to cut just above the artery at the apex of the lower lobe. Anastomosis was very easy. From a functional point of view the result was good. [Slide] Here you can see after the operation the angiography and the good result with the circulation. I t was also good for the ventilation. During the winter this patient was in the mountains skiing, and during the summer he was in the Mediterranean and was doing deep diving and fishing. DR. J O H N MAXWELL CHAMBERLAIN, New York, N. Y.—Mr. Smith has provided us with a very exciting presentation. He obviously is a "cancer hater" and a most courageous man. I think that goes for Dr. Mathey as well. My residents and younger surgeons often ask, "How do you determine resectability?" I think from Mr. Smith's presentation we can say that resectability is probably a state of mind combined with a certain amount of experience and skill. He has shown us that the resectability rate is almost 100 per cent in his hands. A cross-section of the literature in the United States reports the resectability rate as low as 33% per cent. The average is somewhere around 55 to 60 per cent. Before this Association in 1959 we talked about our extended efforts to perform re section in these difficult cases, and I can report to you now that our figures are somewhat similar to Mr. Abbey Smith's. Of those extended efforts, 15 per cent of the patients are 5-year cures. There is just one technical point I might suggest to a large audience of thoracic sur geons. In case it becomes necessary to resect the superior vena cava (at least if the invasion by the tumor is in the middle third) it is possible to mobilize the right pulmonary artery all the way to its origin, and then it may be used as a graft instead of a prosthesis. We have done this in one case. The graft was successful, but during the technical procedure it was necessary to occlude the superior vena cava entirely for 15 minutes, and the patient later died of cerebral complications. I would like to ask Mr. Abbey Smith how he feels about complete occlusion of the superior vena cava, and how long it can be occluded safely. The surgeon at the operating table has a critical decision to make. When he takes a patient to the operating room, he accepts a great obligation. The decision to close the patient as nonreseetable is a most serious one. I think Mr. Abbey Smith has given us a target at which we should all aim. MR. ABBEY SMITH (Closing) .—There is very little I have to add to what I have already said. I think if there is any misunderstanding about what those who take a radical approach to carcinoma try and achieve, the misunderstanding is that we attempt to resect too many advanced lesions. I think certainly all I try to do, having selected the patient before operation, is in every case to remove the tumor. My selection is really before opera tion rather than at operation. Dr. Rasmussen mentioned the number of patients on whom we operate. We operate upon only 1 in 12 patients who die of lung carcinoma, and of these 12 only 3 are submitted for a surgical opinion.
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Dr. Chamberlain's method of superior vena caval replacement is obviously important. He mentioned the time the superior vena cava can be occluded. I n the 4 patients in whom we used the method of vena caval occlusion with pneumonectomy, we occluded the vena cava for 20 minutes in each of these 4 patients without any evidence of cerebral damage; but there again, these patients were very carefully selected before operation. None of the 4 was over 55 years of age. Finally, may I thank you again and through you the members of the Association, your Program Committee, and Dr. Maxwell Chamberlain, for the very great privilege of reading this paper today.