Tracheal Tumors: Surgical Management Hermes C. Grillo, M.D.

ABSTRACT In a 15-year period, 63 patients with primary tracheal tumors were seen. Twenty-eight patients with primary tumors and 8 with secondary tumors of the trachea were treated by resection with single-stage reconstruction. There were 24 cylindrical resections of trachea, 2 lateral resections of trachea, and 10 carinal reconstructions. Thirty-five additional patients with primary tracheal tumors were managed by staged reconstruction, irradiation, or no treatment. The most common primary lesion was squamous cell carcinoma and the second, adenoid cystic carcinoma. Benign primary tumors and low-grade malignant tumors obtained excellent palliation and usually cure. Surgical removal of squamous cell carcinoma and adenoid cystic carcinoma, usually with adjunctive irradiation, provided good palliation or the probability of cure. Resection of selected secondary tumors provided longterm palliation.

Resection and primary reconstruction of the trachea and carina have been utilized to any degree only since 1962, when the techniques of anatomical mobilization were applied to extend the possibilities of the procedures. Primary tracheal tumors that are surgically removable, even by present techniques, are rare in any single institution [2, 10, 13, 14, 16, 181, and few secondary tumors involving the trachea seem amenable to potentially curative resection. As a result, the accumulation of experience in the treatment of specific lesions has been slow. A further problem in the statement of results is the notoriously prolonged and insidious course of adenoid cystic carcinoma, which may require 15 or more years of follow-up for reasonable certainty of cure. From November, 1962 through 1977, 36 patients with primary or secondary tumors in the trachea underwent From the General Thoracic Surgical Unit of the Massachusetts General Hospital and the Department of Surgery of the Harvard Medical School, Boston, MA. Presented at the Fourteenth Annual Meeting of The Society of Thoracic Surgeons, Jan 23-25, 1978, Orlando, FL. Address reprint requests to Dr. Grillo, Massachusetts General Hospital, Boston, MA 02114.

tracheal resection and primary reconstruction at Massachusetts General Hospital. Although the number of patients in any single subcategory is small, this report may be instructive in its discussion of the problems of such approaches. Follow-up has been brief for many of the patients, but some trends have appeared.

Material From 1940 to 1962, before resection and primary reconstruction were used, 27 patients with primary tracheal tumors were seen. In the following 15 years, covered by this report, 63 additional patients were treated. (The increase in numbers reflects my interest in the problem rather than an upsurge in occurrence.) The histological distribution of the lesions was consistent. Squamous cell carcinoma primary in the trachea was most common; 42 patients out of the 90 seen had this cell type. Excluded are extensions of squamous cell carcinoma of the larynx, esophagus, and lung. The second most common primary tracheal tumor was adenoid cystic carcinoma, 29 patients. It was formerly called by the mistakenly benign sounding term cylindroma. Ten patients had tumors of varying malignancy, including chondrosarcoma, carcinosarcoma, carcinoid, spindle cell sarcoma, adenosquamous carcinoma, adenocarcinoma, and monocytic leukemia. Nine patients demonstrated benign primary tumors, including chondroma, chondroblastoma, squamous papilloma, granular cell tumor, hemangioma, and fibroma. Twenty-three of the 63 patients with primary tracheal tumors seen in the 15-year period covered by this study did not undergo resection. Three of them had specialized problems, which it seemed best to handle conservatively. One child had juvenile papillomas, which were treated cryosurgically with the expectation of regression. One suffered from extensive squamous papillomas with atypism, which were too extensive for resection. A third had probable congenital hemangiomatous involve-

112 0003-4975/78/0026-0204$01.50 @ 1978 by Hermes C. Grillo

113

Grillo: Tracheal Tumors

ment of the entire mediastinum and neck with one element present in the tracheal lumen. Four patients with adenoid cystic carcinoma were not accepted as candidates for surgical resection. In 1 the lesion extended submucosally to the takeoff of the upper lobe on both right and left sides and was manifestly beyond surgical resection. Two others had pulmonary metastases; palliative resection would have required laryngectomy in 1 of them. Irradiation of the local lesions was therefore utilized. A fourth patient had what appeared to be a resectable lesion, but he had received high-dose irradiation for the initial appearance of the same lesion many years before. The balance of the patients who did not undergo resection had extensive squamous cell carcinoma. In the majority, the lesion either was too extensive along the length of the trachea or had extended too deep into the mediastinal structures to be considered for surgical resection. Three had had extensive irradiation long before they were seen by me, and 2 had undergone previous attempts at resection elsewhere, with recurrence. One additional patient with adenoid cystic carcinoma and l with recurrence were explored, but both were found to have extensive mediastinal invasion. Irradiation was subsequently given. The remaining 40 patients underwent one type or another of surgical resection. During the same period, 16 patients with secondary tracheal tumors underwent various attempts at surgical extirpation. In total, there were 56 patients who underwent resection of either primary or secondary tracheal tumors. From this group 36 patients were selected to have primary resection and reconstruction, and this report focuses on these 36 patients. However, since one of the principal purposes of this paper is to analyze the techniques and results of surgical treatment of neoplasms affecting the trachea, patients with secondary tumors are mentioned. Of the 56 patients, 10 had tumors involving the larynx that were too extensive for partial laryngectomy. Laryngotracheal extirpations were done with varying amounts of adjacent tissue in attempts at cure. Two of these patients had adenoid cystic carcinoma, and a third had an unusual mixture of adenoid cystic carcinoma, adenocarcinoma, and squamous cell

carcinoma. A fourth patient had a primary squamous cell carcinoma in the lower third of the trachea, which appeared contemporaneously with primary carcinoma of the larynx. Six patients with primary carcinoma of the thyroid, larynx, or esophagus underwent various types of cervical exenterations, including resection of the larynx, thyroid, and in some cases esophagus or lower pharynx as well as the upper trachea. The reconstructive procedures sometimes included colon transplants for esophageal reconstruction. Ten patients-2 with primary squamous cell carcinoma of the trachea, 5 with very extensive adenoid cystic carcinoma of the trachea, 1 who had had prior resection for granular cell tumor of the trachea elsewhere with subsequent necrosis of the trachea, and 2 with extensive invasion by thyroid carcinoma-could not have primary reconstruction. Instead, radical extirpation of the tumors was performed with attempts at staged reconstruction by a variety of techniques. Excluding these 20 patients, there were 36 patients who underwent resection of tumors with primary reconstruction. Thirty-four had either cylindrical resection or carinal resection with suture anastomoses. Two had simple lateral resection of the trachea (window resection) and primary repair. These numbers emphasize the relatively small group of patients with primary neoplastic lesions of the upper airway that are resectable with primary reconstruction, even by present-day extended techniques. In contrast, more than 200 patients with benign stenotic lesions of the trachea, chiefly due to postintubation injuries, underwent reconstruction during the same period. The 36 patients reported on had a wide geographic distribution, and follow-up was necessarily largely by mail or telephone. Satisfactory communication was made with either the patient or his physician or both in every instance. When possible, roentgenograms were reviewed and the patients were seen by us. Table 1 summarizes the management of patients in the 15-year period from late 1962 through 1977. Ten of the patients in whom resection and primary reconstruction were possible had sauamous cell carcinoma. 9 had adenoid cvs1

114 The Annals of Thoracic Surgery Vol 26 NO 2 August 1978

Table 1. Management of Tracheal Tumors at Massachusetts General Hospital” (2962-1977) Primary Tumors

Treatment

Resection and anastomosis Trachea Cylindrical

Squamous Cell Carcinoma

Adenoid Cystic Carcinoma

Other

Tumors

Total

Secondary

Lateral Carina Resection for ”staged”

8 0 2 2

3 0 6 5

8 0 1 1

5 2 1 2

24 2 10 10

Laryngo tracheal

1

2

1

6

10

0

2 4

0 3

1 . . .b

3 21

reconstruction

resection Exploration only Irradiation, tracheostomy,

14

or no treatment “The text is primarily concerned with treatment by resection and primary anastomosis. Total experience during this period is indicated in the table. bThe number of secondary tumors involving trachea not treated surgically cannot be stated.

tic carcinoma, and 9 had other primary tracheal tumors. These 9 tumors included 3 carcinoids and 1 each of squamous papilloma, carcinosarcoma, chondrosarcoma, chondroma, chondroblastoma, and spindle cell sarcoma. Most of the patients with squamous cell carcinoma involving the canna were not considered to be resectable. Adenoid cystic carcinoma was overall more common at the carina. The only other primary tumor of the trachea involving the carina in this ”surgical” group was a malignant carcinoid tumor. The only secondary tumor that involved the carina and was selected for resection was a recurrent carcinoid adenoma in a left main bronchial stump in a patient who had undergone pneumonectomy 8 years previously. Both lateral resections were for secondary tumors, 1 a recurrent carcinoma of the thyroid and the other a carcinoma of the esophagus. Thus, there were 24 cylindrical resections of the trachea, 2 window resections, and 10 resections of the carina. One patient with a low-grade spindle cell sarcoma of atypical variety had undergone bronchoscopic resection previously, and a tracheotomy with local excision and curettage of the tumor on two other occasions. One pa-

tient with adenoid cystic carcinoma of the carina had undergone a wedge resection of the carina 3 years before. Another with carcinoid adenoma had undergone exploratory thoracotomy in another city. Three patients with recurrent thyroid carcinoma invading the trachea had undergone partial thyroidectomy -1 at 1, 1 at 6, and 1 at 13 years prior to the recurrence. The last had received more than 7,000 rads at intervals following the original resection because of known residual tumor on the trachea. One other patient with squamous cell carcinoma had received 3,000 rads shortly before being referred for surgical treatment. Two patients with primary cancer of esophagus received 4,500 rads as part of a treatment program prior to extended resection.

Methods Tumors of the upper half of the trachea are approached through an anterior exposure. If the tumor is extensive, the patient is positioned with the right side of the thorax elevated from the surface of the table. The right arm is abducted at the shoulder and the elbow is flexed to allow for a field that includes the skin from the tip of the chin to the lateral costal arch and

115 Grillo: Tracheal Tumors

extends from the posterior axillary line on the right to the left anterior axillary line. An inflatable bag is placed beneath the shoulders so that reversible hyperextension of the neck may be easily obtained. After the neck is extended, the table is tilted so that the patient lies with the sternum horizontal with the floor. After gentle induction of anesthesia without respiratory paralysis [4], bronchoscopy is performed if it has not previously been done. Biopsy specimens are obtained for frozen section, if histological definition is not already available. Biopsies are advisable beyond the visible gross limits of adenoid cystic carcinoma since submucosal spread is common. Regardless of how obstructive a tumor is, a small endotracheal tube can usually be passed beside it in the area where the tracheal wall is not involved. Such a lesion is only rarely circumferential. If necessary, a bronchoscope may be insinuated as a gentle dilator and an airway then passed. Occasionally, tumors that infiltrate both right and left main bronchi may present special problems. Careful bronchoscopic removal of part of the tumor can provide a tentative airway. In general, I try not to disturb the tumor in order to avoid troublesome bleeding. If additional working space is required, a vertical extension is made from the collar incision through the upper sternum to a point just below the sternal angle. Full sternotomy is very rarely required. If carinal mobilization should become necessary, the incision can be extended into the right fourth interspace through the field described. Tumors of the lower half of the trachea and carina are best approached through a transthoracic incision. While benign strictures of the lowest part of the trachea may be corrected through the anterior approach, the type of dissection required for total removal of the tumor requires a wider exposure. Posterolateral thoracotomy provides much better access than does the partial trapdoor incision I initially used [5,12]. In most patients with tumors of the lower trachea, the operative field includes the neck as well, in case laryngeal release is required. The right arm is positioned so that it may be swung back and forth in the field. Certain problems may require special incisions or variations. One patient with a large

tumor at the junction of the carina and left main bronchus extending down to the takeoff of the left upper lobe bronchus had removal through a left thoracotomy with mobilization of the aortic arch. Carinal resection and left pneumonectomy with anastomosis between the right main bronchus and the trachea was accomplished from the left side. The detailed techniques of resection and anastomosis were described previously [6-91. It must be remembered that considerable mobility of the trachea is obtained by cervical flexion, whether the surgeon is operating through the cervical, mediastinal, or thoracic route. Especially in young patients, the cervical trachea can be delivered into the thorax by flexion. The anterior surface of the entire trachea is usually exposed. The actual technique of dissection, however, depends on the conditions of each individual tumor. In contrast to the technique for approaching benign lesions, dissection for tumor must remain distant from the tumor. Therefore, in 5 patients with upper tracheal tumors not of thyroid origin, hemithyroidectomy was done. In 1 of these patients a recurrent nerve was deliberately sacrificed because of intimate involvement by the tumor. Two patients with primary thyroid lesions underwent thyroidectomy, which included sacrificing a paralyzed nerve in 1patient and en bloc removal of strap muscles in both. In such instances, adjacent lymph nodes are removed with the tracheal specimen to an extent that must compromise between radical removal of all regional nodes and preservation of the blood supply of the portion of the airway that will remain. Great care must be taken not to devascularize the trachea by excessive lateral dissection [ll, 191. Also, in contrast with resection for benign disease in which the dissection is kept close to the trachea and no attempt is made to dissect the recurrent nerves out of the dense scar surrounding the trachea, in dissection for tumor the recurrent nerves are usually identified and spared if possible. Of the 26 patients in this series undergoing either cylindrical resection of the trachea or window resection, 9 were operated on through the cervical route, 6 through the cervicomediastinal route, and 11 by the transthoracic route. Six patients required cricothyroid anastomoses.

116 The Annals of Thoracic Surgery Vol 26 No 2 August 1978

Various anterior and lateral portions of cricoid cartilage were beveled obliquely for adequate margins above tumors located high in the trachea. If the recurrent laryngeal nerve is to be preserved in such high resections, it must often be dissected to its point of entry into the larynx posteriorly. The 10 patients who underwent carinal reconstruction were approached through the thorax. The degree of intrathoracic mobilization accomplished varied with the extent of resection. In most instances in which the

Fig 1 . Modes of reconstruction used i n this series. ( A ) Following carinal resection without removal o f a long segment of trachea, reconstruction was done by trachea to bronchial end-to-end anastomosis with lateral implantation of either the right or the left main bronchus into the devolved lower trachea. Three patients underwent such reconstructions. ( B ) Carinal resection with a longer tracheal resection was repaired by direct suture of the trachea of the right main bronchus with anastomosis of the left main bronchus to the bronchus intermedius. T w o such reconstructions were performed. ( C ) In 1 patient an adenoid cystic carcinoma of the tracheobronchial angle extending down to the right upper lobe orifice was removed as shown. W i t h plastic reconstruction of the tracheal defect, implantation of the bronchus intermedius was accomplished.

A

transthoracic route was employed, the pulmonary ligament was divided and some freeing of the carina was accomplished. In a number of the more extensive resections, the right hilar structures were fully dissected, though care was taken to attempt to preserve bronchial blood supply distally. Laryngeal release proved to be a useful adjunct in 4 patients. In this series, release was required in patients in whom the approach had been transthoracic and was accomplished through a second independent transverse incision high in the neck over the upper larynx. A thyrohyoid release was used initially [l]:In the latter part of the series a suprahYoid was preferentially used because of a diminished incidence if difficulty in swallowing [15]. Laryngeal release is an extremely useful adjunct, but its routine use is unnecessary. The effectiveness of resection must be checked by frozen section from the margins of resection, Particularly in the treatment of adenoid cystic carcinoma. This may present one of the most difficult aspects of this type of surgery. In a number Of the patients in whom complex reconstructions were attempted, ex-

117 Grillo: Tracheal Tumors

tended resection was necessitated by the finding of tumor at initial resection margins. Further resection then made it impossible to effect primary reconstruction. I have found it all but impossible to plan precisely the type of reconstruction to employ following carinal resection. Much depends on the exact disposition of the resection. Figure 1 shows several of the reconstructive approaches used in this series. Following removal of the tumor the surgeon exerts gentle tension through lateral traction sutures at all the di-

vided ends of trachea and bronchi to determine which will come together with minimum tension. The greatest problem arises when long segments of the left main bronchus must be resected. It may be difficult to bring the remaining sections across the midline to the airway on the right side, especially if a large amount of lower trachea has also been resected. I did not find it possible in this series to reconstruct the carina by suturing the right and left main bronchi together and then advancing the trachea to this point. Binding the two main bronchi to-

(

C

118 The Annals of Thoracic Surgery

A

Vol 26

No 2 August 1978

B

D '

Fig 2 . Reconstruction following carinal resection with pneumonectomy. (A) Right pneumonectomy. ( B ) Carinal resection with anastomosis of the right lung to the trachea performed through the right chest. Left pneumonectomy was done because the left rnain bronchus had insufficient length for implantation into the reconstructed righ t-sided airway. ( C ) Carinal resection and left pneumonectomy were necessary because of the extent of the tumor. This procedure was done through the left chest. ( D ) "Carinal" resection for a recurrent stump tumor following prior left pneumonectomy for carcinoid adenoma. This procedure was performed through the right chest while ventilation was maintained in the residual lung.

gether at such a low level beneath the aortic arch usually makes it impossible for the trachea to reach, unless only a minimal tracheal resection has been done. More often, the trachea is devolved to reach the left main bronchus and the right bronchus is implanted into the side of the trachea. If the major resection is in the lower trachea on the right side, the primary end-toend anastomosis is made between the trachea and right main bronchus with lateral implantation of the unshortened left main bronchus. Although pneumonectomy (Fig 2 ) and limited carinal resection were accomplished from the left,

reconstruction with salvage of the lung is difficult from the left side when the carina is involved because of the aortic arch. Even a resection of left main bronchus for a mucoepidermoid cancer in which the carinal spur had to be removed for margin was preferentially done through the right chest. Lengths of resection for primary reconstruction were 2 cm or less in 5 patients, between 2 and 4 cm in 20, and between 4 and 6 cm in 7. Four of the long resections were in patients with carinal tumors. The procedures are carried out under assisted ventilation, without respiratory paralysis [41. Cardiopulmonary bypass is unnecessary even for relatively complex reconstructions. In an exceedingly complex reconstruction in which much manipulation of the right lung is required, intrapulmonary hemorrhage is predictable if heparinization is used. Indeed, this occurred in 1patient with a carinal tumor involving the right upper lobe bronchus and with compression of the left pulmonary artery by tumor, who had undergone left lower lobectomy previously. The patient failed to survive

119 Grillo: Tracheal Tumors

the bypass because of hemorrhage into the residual middle and lower lobe on the right. Such a patient would now be handled with double intubation of both the right and left main bronchi and alternate ventilation. Bypass was used in 1 other patient only for a brief phase of the operation when a segment of involved main pulmonary artery was excised and repaired. After operation the patient is expected to breathe spontaneously. Occasionally, a brief period of ventilation may be required. Tracheostomy is usually avoided. Secretions are cleared by physiotherapy; flexible bronchoscopy may also be used. Raising secretions is most difficult in those patients who have undergone carinal reconstruction. When laryngeal compromise results from complex upper tracheal reconstruction, a small endotracheal tube may be necessary for a few days. It is placed either with the cuff deflated or in such a way that the cuff does not rest on the anastomosis. The tube is removed as early as possible. In those patients who have sufficient length of cervical trachea remaining between the anastomosis and the innominate artery, a tiny tracheostomy tube may be placed for security. If it is thought that a tracheostomy may be required because of such transient laryngeal

compromise and if there is insufficient distance between the level of anastomosis and the sternal notch, tissue is carefully sutured over the anastomosis above and over the innominate artery below. A small area of the trachea is identified for tracheostomy, and the patient is maintained with a small endotracheal tube. After four or five days, if the airway is still not adequate, a small tracheostomy tube can generally be safely inserted with very careful technique at the predetermined locus. Tracheostomy was used in 4 patients in this series.

Results The results in this series must be considered predictors. First, the series includes all of my experience with tracheal resection and reconstruction for tumors. The limits of the field have been explored gradually, and some of the operative and management techniques have evolved from the earlier experiences. Second, a longer time must pass before a definitive statement can be made about final results for many of the patients (Table 2).

Deaths There were 5 hospital deaths among the 36 patients. All were directly related to the surgical

Table 2 . Results from Primary Resection and Anastomosis of Tumors lnvolving the Trachea (1962-1977)

Outcome Postoperative deaths Alive without disease

Alive with disease Dead without disease Dead with disease

Squamous Cell Carcinoma

Adenoid Cystic Carcinoma

2

Other Tumors J

13 yr 7 mo 7yr 7mo 2yr 5mo 1 yr 11 mo 10 mo

15 yr 1 mo 7yr3mo 5yr8mo 4yr3mo 1yr5mo 1yr3mo

1yr 6mo

5yr8mo 1yr6mo

15 yr 1 mo 8 Y' 7yr 3mo 3yr 6mo 2yr 9mo 2yr 5mo 1 yr 10 mo 1yr 1mo

...

2 Yr

...

..

2yr 8mo

...

..

Secondary Tumors 1

4yr4mo 10 mo

...

8 Y'

6yr6mo 3yr6mo 2 Yr 6 mo

120 The Annals of Thoracic Surgery Vol 26 No 2 August 1978

procedure. Two patients who died had undergone cylindrical resection of the trachea. One of them had received high-dosage irradiation many years before for residual thyroid carcinoma. The divided trachea necrotized and anastomotic separation followed. Attempt at resuture and eventually even mediastinal tracheostomy failed. Since that time, no other patients who have undergone high-dose irradiation in the remote past have been considered candidates for resection. A nonspecific pneumonia and pulmonary insufficiency developed in a patient who underwent transthoracic resection of the lower trachea for squamous cell carcinoma early in the series. Three patients who underwent carinal reconstruction died after the operation. One who appeared to be doing well died of sudden hemorrhage into the trachea on the tenth postoperative day. In this patient a pedicled pleural flap had not been placed between the suture line and the adjacent pulmonary artery as is usually done. The presence of a low-grade fever for a number of days suggested the possibility of a local abscess that eroded into the artery. A postmortem examination was not done. Another patient who had undergone extensive carinal reconstruction probably had a closure with excessive tension. Partial separation and pneumonia occurred. The third patient had extended resection of the trachea, right main bronchus, and most of the left main bronchus for adenoid cystic carcinoma. Anastomosis of the residual distal stump of the left main bronchus could not be made to the remaining airway on the right, and left pneumonectomy was done. Pulmonary insufficiency developed in the manipulated right lung. All 3 patients had malignant lesions-1 squamous cell carcinoma, 1 adenoid cystic carcinoma, and 1 invasive and metastasizing carcinoid tumor.

Complications The most common complication following the procedure was the late appearance of granulations at the suture line. During the period covered by this series, most of the reconstructions were done with nonabsorbable sutures. Eight of the surviving 31 patients required one or more bronchoscopies for removal of granula-

tions and sutures. In most patients the problem was minimal and was solved by a single bronchoscopy. One patient whose airway had been reduced to 3 mm by a slowly growing chondroblastoma was operated on at a time when he was still taking high doses of prednisone for a mistaken diagnosis of asthma. Partial stenosis of the anastomosis developed. At the time of writing, the patient was functioning normally except that he could not engage in strenuous exercise. Reresection will be done if the symptoms progress. One patient who underwent extended resection of a supracarinal tumor had a partial separation that resulted in stenosis. Reresection was done with adjunctive laryngeal release. Two patients had difficulties with recurrent laryngeal nerves. In 1 the right recurrent nerve was deliberately sacrificed because of its involvement in tumor; the left recurrent nerve was inadvertently injured. The patient gradually recovered a very satisfactory spoken voice and even was able to sing at a later period. A second patient had partial removal of the cricoid on one side to provide added margin above a tumor. A "sluggish" vocal cord resulted; it was asymptomatic at the time of writing. One patient who underwent extensive resection of the trachea could swallow only when the neck was in the flexed position. This probably results from the fact that ordinarily laryngeal closure is obtained when the larynx rises during swallowing. If the neck is extended, the larynx cannot rise high enough for swallowing to occur.

Survival and Recurrence The number of patients in each group is too small to predict much about the completeness of cure. Of those patients with squamous cell carcinoma, 5 are alive and without known disease at periods ranging from 10 months to more than 13% years after operation. Three have been followed for more than 2 years. An additional patient had recurrent tracheal disease 1% years following resection. This patient also had a squamous cell carcinoma on the base of the tongue and squamous cell carcinoma of both

121 Grillo: Tracheal Tumors

main bronchi. All tumors have been treated with irradiation. Another patient died 2 years after operation from either a myocardial infarction or a pulmonary embolism without known recurrence. One final patient with squamous cell carcinoma died of the disease 2 years 8 months following resection. He had had positive lymph nodes at the time of resection and received a subsequent course of palliative irradiation when recurrence was discovered. One of the 5 patients without disease received 3,000 rads preoperatively in another institution, and 1 was given 5,000 rads postoperatively because of the closeness of the margins. Six patients with adenoid cystic carcinoma are living without known disease at periods ranging from 1 year 3 months to just over 15 years following resection. One of these patients was given 5,000 rads postoperatively because of the finding of positive subcarinal lymph nodes. Three others were irradiated in the same dose range because of the closeness of the resection margin to the tumor. Two of these had upper tracheal lesions and the third had a carinal lesion. In none of these patients could the resection be extended without further drastic losses of either larynx or lung. Two additional patients are alive 1year 5 months and 5 years 8 months, respectively, following resection. The patient with the longer survival was found to have bilateral pulmonary metastases a year ago; they were surgically cropped. The second patient has bony metastases, which have been irradiated. Eight patients who had resections for primary tracheal tumors other than squamous cell or adenoid cystic carcinoma are living, for periods ranging from just over l year to just over 15 years, without known recurrences. The tumors involved were 1squamous papilloma, 2 carcinoid tumors, 1 carcinosarcoma, 1 spindle cell sarcoma, 1 chondroma, 1 chondrosarcoma, and 1chondroblastoma. As might be expected, the group with secondary tumors has not done well in terms Of cure. A patient with carinal recurrence of a carcinoid tumor following a left pneumonectomy 8 years Dreviouslv had no residual disease 4 years 4 r-months following resection of the lower trachea and right main bronchus. Another patient with

papillary carcinoma of the thyroid invading the trachea underwent total thyroidectomy and tracheal resection in continuity 10 months before this writing and is doing well. Five other patients who underwent palliative resection died of their disease, however. Palliation was obtained for respectable periods in all except 1 patient who died only 6 months following esophagectomy for irradiated esophageal carcinoma with adjacent window resection of trachea. He experienced massive gastrointestinal bleeding at another hospital. Residual carcinoma was found in the subcarinal lymph nodes at postmortem examination. A second patient with carcinoma of the upper esophagus who had a concurrent resection of the cervical trachea following irradiation died of tumor remote from the operative site 3% years after resection. Two additional patients operated on for recurrent carcinoma of the thyroid obstructing the trachea lived for 6Y2 years and 8 years, respectively, following tracheal resection and reconstruction. Each of them died of recurrent d i s e a s e 1 of bony and the other of mediastinal metastases.

Laryngotracheal Resection and Staged Reconstruction The primary purpose of this paper is to discuss the management of patients with tracheal tumors in whom resection and anastomosis are possible. Laryngotrachiectomy was done in a few patients whose primary tumors involved both trachea and adjacent larynx. One with adenoid cystic carcinoma has remained free of disease for more than 4 years. In a second, airway palliation has been obtained but metastases are growing slowly in both lungs. Another patient, with squamous cell carcinoma of the trachea, had a second primary carcinoma of the larynx. Recurrences were treated with radical neck dissections later. Ultimately he died of hemorrhage from erosion of the aortic arch from sepsis around the mediastinal tracheostomy site 4 years 8 months after the original operation. A fourth patient, with a carcinoma of compound histology, died of metastatic disease 2 years following resection. Variable palliation was obtained from similar complex exenteration procedures in other carcinomas involving

122 The Annals of Thoracic Surgery Vol 26 No 2 August 1978

the trachea secondarily. These are not discussed further here. The attempt to remove the trachea with or without the canna in patients who had primary tumors so extensive that a primary reconstruction could not be done proved to be, in general, disastrous. Two patients were operated on in this fashion for primary squamous cell carcinoma and 5, for adenoid cystic carcinoma. One of the latter procedures was done in a desperate attempt to save a patient who had airway obstruction following an unsuccessful resection elsewhere. In all of these patients, various types of cutaneous interpositions were placed after resection of the upper sternum. The attempt was made to complete an intrathoracic reconstruction in the hope of establishing continuity later with the larynx through means of a splinted skin tube. Concerning the 2 patients with squamous cell carcinoma, 1 died of innominate artery hemorrhage postoperatively, and the other lived for 2l/2 years but could never have a skin tube completed because of recurring stenosis at the lower end. Of the 5 with adenoid cystic carcinoma, 1 died following cardiopulmonary bypass and 3 died of various complications in the postoperative period. The other lived for a good many months but needed constant attention for a stenosis of one of the three anastomoses in the carinal region. Skin tube reconstruction was successfully accomplished in 2 patients. One patient had had necrosis following removal of the lower trachea for granular cell tumor, done at another institution, and 1 had had removal of a papillary carcinoma of the thyroid [5]. This patient had recurrent carcinoma 21/2 years later, but the airway had functioned well until then. The first patient continued to do well 4% years later. It is clear that this type of staged reconstruction carries too high a risk to be employed electively. At the present time, patients with extensive disease might better be treated by irradiation or even by the attempted use of a prosthetic device. It remains difficult to predict the extent of resection necessary in advance of the procedure. Although predictions are generally possible for most lesions, they cannot be made for adenoid cystic carcinoma. In this lesion, what

seems to be a grossly clear margin of resection is insidious in its microscopic appearance.

Comment We are still in the process of collecting data on the most effective way to treat both primary and secondary tumors involving the trachea. The goal of the surgeon is twofold: the relief of airway obstruction in the most effective way possible and the achievement of cure. Before the methods of extended tracheal resection with reconstruction were developed, the risks were prohibitive and the techniques undependable. There are still few data on which to base firm conclusions. In 1974, Eschapasse [3] published a collected series of 152 patients with primary tracheal tumors treated by twelve French and two Soviet groups. In this series there were 32 cylindrical resections of the trachea with primary anastomosis and 18 carinal reconstructions. In this same series, Perelman [3] from Moscow reported on 15 cylindrical and 10 carinal resections. He also performed 3 window resections and the French groups, 19. There were 18 early postoperative deaths in this series of 162 operations. The highest mortality was in patients with squamous cell carcinoma. The long-term results were, as expected, best with benign tumors and with carcinoid tumors. Patients with adenoid cystic carcinoma demonstrated prolonged survival but also late recurrences. The poorest results were seen in patients with squamous cell carcinoma. Pearson and associates [17] reported on 14 patients with adenoid cystic carcinoma treated by circumferential resection of the trachea and on 2 treated by lateral resection. Five of the 14 underwent primary anastomosis, 6 were treated by prosthetic replacement, and 3 were treated by laryngotrachiectomy. Eight were alive and free of tumor 2 to 18 years later. Houston and coworkers [14l, reporting a 30-year experience, listed 3 patients with squamous cell carcinoma who had undergone tracheal resection and 7 with adenoid cystic carcinoma. Of 5 surgical survivors, 3 had had lateral resections, 1 had had a laryngotrachiectomy, and only 1 had had a segmental resection. Another patient with mucoepidermoid carcinoma who underwent

123 Grillo: Tracheal Tumors

segmental resection was alive 4% years later. There are few additional reports of any large number of tracheal tumors treated aggressively by surgical means. In light of the data available in 1962 and later, I believe that squamous cell and adenoid cystic carcinoma of the trachea are best resected if it appears that a procedure can encompass the tumor and still permit primary repair. Irradiation alone has rarely given more than 1 to 2 years of respite in squamous cell carcinoma. It has provided 5 to 7 years of remission in adenoid cystic carcinoma, but ultimately recurrence seems to be the rule. Since I now have followed a number of patients with squamous cell carcinoma and adenoid cystic carcinoma of the trachea treated by resection who have survived for much longer periods without recurrence, I think the possibility of cure by resection alone or by resection with irradiation is very good. At present, I use the combined treatment in patients in whom the margins are limited or in whom microscopic tumor is found in the margins or lymph nodes. Equally unclear is the efficacy of preoperative irradiation. Pearson and colleagues [17] employed it on a trial basis in the treatment of adenoid cystic carcinoma. Surgical resection is clearly the treatment of choice for most other primary tumors of the trachea, whether benign in character or of low-grade malignancy. While I continue to think that tracheal reconstruction, because of its magnitude and particularly in the carinal region, should be restricted in application to secondary tumors, it clearly has a place in the palliation of selected patients. This seems to be especially true for slowly growing tumors of the thyroid. Although cure is rare, the length of remission and the quality of life provided seemed to justify this approach. Eschapasse [3] presents the view that tracheal resection and reconstruction should be done in patients with adenoid cystic carcinoma that is locally resectable, even in the presence of pulmonary metastases. The prolonged course in such patients would seem to justify this approach. I prefer not to proceed, however, if laryngeal resection is required. It remains to be seen whether aggres-

sive cropping of pulmonary metastases will have value. This study points to the following three conclusions: (1) Resection of benign primary tumors of the trachea and low-grade malignant tumors of the trachea appears to offer excellent palliation and high probability of cure. (2) Resection and reconstruction when possible in a single stage appear to offer the best palliation and chance for cure in squamous cell carcinoma and adenoid cystic carcinoma of the trachea. Adjunctive irradiation is probably indicated. (3) Tracheal resection and reconstruction for secondary tumors involving the trachea may provide good palliation in carefully selected patients, chiefly in those with low-grade thyroid carcinoma.

References 1. Dedo HH, Fishman NH: Laryngeal release and

sleeve resection for tracheal stenosis. Ann Otol Rhino1 Laryngol 78:285, 1969 2. Dor V, Kreitmann P, Arnaud A, et al: Resection etendue de la trachee pour tumeur et stenose. Presse Med 79:1843, 1971 3. Eschapasse H: Les tumeurs tracheales primitives. Traitement chirurgical. Rev Fr Malad Resp 2:425, 1974 4. Geffin B, Bland J, Grillo HC: Anesthetic management of tracheal resection and reconstruction. Anesth Analg 48:884, 1969 5. Grillo HC: Circumferential resection and reconstruction of mediastinal and cervical trachea. Ann Surg 162:374, 1965 6. Grillo HC: Surgery of the trachea. Current Probl Surg, July, 1970 7. Grillo HC: Benign and malignant disease of the trachea, in Textbook of General Thoracic Surgery. Edited by TW Shields. Philadelphia, Lea & Febiger, 1972 8. Grillo HC: Reconstruction of the trachea. Experience in 100 consecutive cases. Thorax 28:667,1973 9. Grillo HC: Congenital lesions, neoplasms and injuries of the trachea, in Gibbon’s Surgery of the Chest. Third edition. Edited by DC Sabiston Jr, FC Spencer. Philadelphia, Saunders, 1976 10. Grillo HC: Tracheal tumors, in Rhoads’ Textbook of Surgery. Fifth edition. Edited by J Hardy. Philadelphia, Lippincott, 1977 11. Grillo HC: Tracheal blood supply (editorial). Ann Thorac Surg 24:99, 1977 12. Grillo HC, Bendixen HH, Gephart T: Resection of the carina and lower trachea. Ann Surg 158:889, 1963

124 The Annals of Thoracic Surgery Vol 26

No 2 August 1978

tion. In stark contrast, 4 of the 7 patients undergoing prosthetic reconstruction died after operation of erosion of the innominate artery by the abrasive, rigid prosthesis. Six of these prosthetic reconstructions were done before 1970, and the seventh was done in 1977. In the latest reconstruction, resection of the entire trachea and larynx except for about 1 cm of the distal trachea was necessary, and we deliberately resected the innominate artery at the time of operation to avoid the complication of tracheoinnominate fistula. Of special interest to us is the group of 19 patients who underwent segmental resection of the trachea for adenoid cystic carcinoma. There was an unusual preponderance of this cell type in our series. Nine of these 19 patients are dead. There were 4 operative deaths because of tracheoinnominate fistula following prosthetic reconstruction. Three patients died of local recurrence, but it should be noted that palliation was achieved for noteworthy periods of time, death occurring 2, 4, and 8l/2 years after resection. One patient died of cerebral metastases 14 months after resection of the primary tumor, and 1 patient Discussion died of heart disease 12 years following resection and DR. F. GRIFFITH PEARSON (Toronto, Ont, Canada): We was clinically free of recurrent tumor at that time. have heard a classic paper on primary tumors of the Ten of the 19 patients with adenoid cystic carcinoma trachea. Dr. Grillo’s efforts over the years in the field are still living. Nine are clinically free of disease, of tracheal surgery have made it possible for many of with very long periods of survival in some instances, us to extend our indications for surgical resection in and 1 is alive 6 years after resection with bilateral patients with tracheal tumors. As Dr. Grillo stated, pulmonary metastases. Although a chest roentgenothese tumors are rare and no one individual or in- gram of this patient shows a veritable snowstorm on stitution accumulates a very large experience. Dr. both sides, she i s asymptomatic. Those of us who Grillo has discussed the most extensive group of pa- have seen this type of metastatic disease with tients managed in a single institution anywhere in adenoid cystic carcinoma recognize the very slow the world, and I will support the points he has made progress that occurs when the lung is involved. by reviewing briefly our own hospital experience. I again emphasize the observations and concluThis experience is similar in almost every way to his. sions that Dr. Grillo has made. Nearly all primary During a 27-year period we have seen 41 pa- tumors of the trachea are malignant, adenoid cystic tients with primary tracheal tumors, and all but 3 carcinoma and squamous cell carcinoma are the most were malignant. Adenoid cystic carcinoma and common cell types, and, if they can be resected and squamous cell carcinoma were the most common cell reconstructed primarily, there is a very reasonable types. Thirty tracheal resections were done in 29 pa- prospect for long-term survival with a low operative tients, and the types of resection include all of those mortality and postoperative morbidity. reviewed by Dr. Grillo. In 13 patients, we were able to achieve a stage I resection of the trachea with pri- DR. ROBERT JENSIK (Chicago, IL): Dr. Grillo is to be mary anastomosis. There were 5 carinal resections commended on this superb series of patients, and I and 3 tracheal resections that also required laryngec- offer my personal congratulations for the results he tomy. Two lateral resections were done by Dr. F. G. has achieved in some of the very long resections. Kergin in the early 1950s. In 7 resections and in com- Our series at Rush-Presbyterian-St. Luke’s Medical plex reconstructions we used a prosthesis of heavy Center is more modest. It consisted of 5 tracheal resections; 1 for mucoepidermoid carcinoma, 1 for Marlex mesh. It is evident that the operative mortality and mor- fibrous histiocytoma, and 3 for adenoid cystic carbidity will be low if a single-stage reconstruction cinoma. with autogenous tissue can be achieved. In the 23 All patients survived resection and anastomosis. patients managed by primary reconstruction with However the 18-year and 14-year survivors who had autogenous tissue, there were no operative or post- adenoid cystic carcinoma support the overall good operative deaths and no major complication de- prognosis in this pathological group as described by veloped at the site of the anastomosis or reconstruc- Dr. Grillo and by Dr. Pearson.

13. Hajdu S1, Huvos AG, Goodner IT, et al: Carcinoma of the trachea. Clinico-pathologic study of 41 cases. Cancer 25:1448, 1970 14. Houston H, Payne W, Harrison E: Primary cancers of the trachea. Arch Surg 2:132, 1969 15. Montgomery WW: Suprahyoid release for tracheal stenosis. Arch Otolaryngol 99955, 1974 16. Pearson FG: Techniques in the surgery of the trachea, in Surgery of the Lung, The Coventry Conference. Edited by RE Smith, WG Williams. Norwich, England, Page Bros Ltd, 1974 17. Pearson FG, Thompson DW, Weissberg D, et al: Adenoid cystic carcinoma of the trachea. Experience with 16 patients managed by tracheal resection. Ann Thorac Surg 18:16, 1974 18. Perelman MI: Surgery of the Trachea. Moscow, .Mir, 1976 ‘19. Salassa.JR, Pearson B, Payne WS: Growth and microscopic blood supply of the trachea. Ann Thorac Surg 23:100, 1977

125 Grillo: Tracheal Tumors

Our most recent resection was an adenoid cystic lesion involving approximately 6 cm of trachea extending upward from the carina. Despite laryngeal release and right hilar mobilization, it was impossible to approximate the membranous portion of the trachea. The cartilaginous portion was approximated and an endotracheal tube was advanced into the left main bronchus. We used a pericardial graft, which measured 2% by 5 cm. The graft was approximated to the posterior defect and was sutured superiorly, laterally to either side of the trachea, and inferiorly. I would like to ask Dr. Grillo if he has ever utilized free pericardial grafts in this fashion. DR. HAWLEY H . SEILER (Tampa, FL): I thought it would be of some interest to report the long-term survival of a patient with malignant sarcoma involving the cervical trachea and the technique used in the pre-Grillo era. Twenty-five years ago, in January, 1953, I saw a 3-year-old girl with severe stridor. Immediate tracheostomy was required as a lifesaving procedure. We then were able to establish a diagnosis and subsequently proceed with excision of the entire cervical trachea. We used as a replacement a Gebauer dermal graft, which was in vogue at that time, especially in certain bronchoplastic procedures. As expected, the graft became stenosed, and for several years it was necessary to dilate it periodically. When the family moved to the Chicago area, the patient was seen by Dr. Paul Hollinger, an outstanding bronchoesophagologist. He continued dilatation for another 4 or 5 years. Eventually, the patient recov-

ered completely and has remained well, with no evidence of recurrence of the sarcoma. DR. GRILLO: Dr. Pearson presented some extraordinarily interesting data. I wish he would present them as a paper in more detail. His comment about the patient with asymptomatic adenoid cystic pulmonary metastases is of interest. Dr. Eschapasse from Toulouse has proposed that we should resect the trachea for adenoid cystic carcinoma even in patients with pulmonary metastases. I have not resected the primary tumor in 2 patients with pulmonary metastases since both would have required laryngotracheoectomy. This seemed a little drastic for palliation only. In patients in whom margins are close or nodes are positive, I use postoperative irradiation. Later, one such patient had bilateral pulmonary metastases. His surgeon in Ohio did a bilateral thoracotomy and removed the metastases. Presently, the patient is free of metastases, but they may recur. I shall be very interested to see the results of preoperative irradiation, but it will take many years to collect comparative series at the low incidence rate. None of 4 patients with adenoid cystic carcinoma irradiated after operation have had local recurrence to date. I think 3 out of 5 with squamous cell lesions had recurrence. Dr. Jensik, in answer to your question, I have not used pericardium to reconstruct the trachea. Many years ago a surgeon in our hospital used pericardium to reinforce a Marlex mesh patch after lateral resection. It worked beautifully initially, but the tumor recurred locally in about 2 years.