Anterior transcervical-thoracic approach for radical resection of lung tumors invading the thoracic inlet

General Thoracic Surgery

Anterior transcervical-thoracic approach for radical resection of lung tumors invading the thoracic inlet We describe an original anterior transcervical-thoracic approach required for a safe exposure and radical resection of non-small-cell lung cancer that has invaded the cervical structures of the thoracic inlet. Through a large L-shaped anterior cervical incision, after the removal of the internal half of the clavicle, the following steps may be performed: (1) dissection or resection of the subclavian vein; (2) section of the anterior scalenus muscle and resection of the cervical portion of the phrenic nerve, if invaded; (3) exposure of the subclavian and vertebral arteries; (4) dissection of the brachial plexus up to the spinal foramen; (5) section of invaded ribs; and (6) en bloc removal of chest wall and lung tumor, either directly or through an extension of the cervical incision into the deItopectoral groove. An additional posterior thoracotomy may be required for resection of the chest wall below the second rib. Between 1980 and 1991, 29 patients underwent radical en bloc resection of the inlet tumor, chest wall (ribs 1 and 2), and underlying lung, either through the anterior transcervical approach alone (n = 9) or with an additional posterior thoracotomy (n = 20). The inferior root of the brachial plexus, either alone (n = 11) or with the phrenic nerve (n = 4), was involved and resected in 15 patients (52 %). Twelve patients (41%) had a vascular involvement that included the subclavian artery alone (n = 3); subclavian artery and subclavian vein (n = 3); subclavian artery, subclavian vein, and vertebral artery (n = 2); subclavian artery and vertebral artery (n = 1); subclavian vein alone (n = 1); vertebral artery alone (n = 1), or subclavian artery and vertebral artery (n = 1). The subclavian artery was revascularized either with a prosthetic replacement (n = 7) or an end-to-end anastomosis (n = 2), and the median graft patency was 18.5 months (range, 6 to more than 73 months); only 1 patient had postradiotherapy graft occlusion in the revascularized artery 6 months after operation. We performed 14 wedge resections, 14 lobectomies, and 1 pneumonectomy. There were no operative or hospital deaths. Postoperative radiotherapy (median, 56 Gy) was given to 25 (86%) patients, either alone (n = 14) or in combination with adjuvant systemic chemotherapy (n = 11). With a median follow-up time of 2.5 years, overall 2- and 5-year survivals were 50% and 31 %, respectively. This transcervical-thoracic approach affords a safe exposure and radical resection of non-small-cell lung cancer involving the thoracic inlet and results in encouraging long-term survival. (J THORAe CARDIOVASC SURG 1993;105:1025-34)

Philippe G. Dartevelle, MD, Alain R. Chapelier, MD, Paolo Macchiarini, MD, Bernard Lenot, MD, Jacques Cerrina, MD, Francois Le Roy Ladurie, MD, Francois J. F. Parquin, MD, and Denise Lafont, MD, Le Plessis-Robinson, France Sponsored by Jean Deslauriers, MD, Sainte-Fay, Quebec, Canada

From the Department of Thoracic and Vascular Surgery and HeartLung Transplantation, H6pital Marie-Lannelongue, Paris-Sud University, Le Plessis Robinson, France. Read at the Seventy-second Annual Meeting of The American Association for Thoracic Surgery, Los Angeles, Calif., April 26-29, 1992.

Address for reprints: Philippe Dartevelle, MD, Department of Thoracic and Vascular Surgery and Heart-Lung Transplantation, H6pital Marie-Lannelongue, Paris-Sud University, 133 Avenue de la Resistance, 92350 Plessis Robinson, France. Copyright

1993 by Mosby-Year Book, Inc.

0022-5223/93/$1.00+ .10

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During the past three decades, clear progress has been made in the outcome of treatment for bronchogenic carcinomas of the superior pulmonary sulcus situated in the narrow confines of the thoracic inlet. As reported by several authors.lf the combination of preoperative radiotherapy and radical resection has a better therapeutic index than does radiation alone, and it has become the standard treatment of these tumors. However, bronchogenic tumors with extensive involvement of adjacent structures above the thoracic inlet (such as the subclavian artery and vein and the brachial plexus) represent a contraindication to any surgical approach. 2, 4, 9 This is because the classic posterior thoracic approach, described by Paulson, '0 does not permit the complete exposure and radical resection of invaded, crucial structures of the thoracic inlet. By contrast, the supraclavicular approach offers several advantages in obtaining an adequate exposure for vessels and control of upper and lower branches of the brachial plexus in the operative treatment of a variety of thoracic inlet diseases." With this background, we created and describe an original anterior transcervical-thoracic approach for the surgical treatment of non-small-cell lung cancer (NSCLC) invading the thoracic inlet, and we present the therapeutic results that we have achieved during 10 years of experience.l?

Patients and methods Preoperative workup. The preoperative evaluation has been detailed in a previous study.':' It routinely included a record of medical history, a physical examination, a biochemical profile, a roentgenogram of the chest, bronchoscopy, computed tomography of the chest, abdominal ultrasonography, bone scan, and cardiopulmonary tests. Routinely, neurologic examination, electromyography, and fluoroscopy were done to delineate the extent of the tumor to the brachial plexus and phrenic nerve, and vascular invasion was studied with venous angiography, subclavian arteriography, and Doppler ultrasonography. Recently, magnetic resonance imaging was included in the diagnostic armamentarium. Indications. Any patient with an apical lung carcinoma of non-small-cell histologic structure invading the thoracic inlet can be considered for the present approach. Absolute contraindications for this type of surgical technique are the presence of extrathoracic sites of metastasis and histologically confirmed involvement of mediastinal lymph nodes. Extensive involvement of the brachial plexus is a relative contraindication, if a complete surgical resection is anticipated. Vertebral body involvement is an absolute contraindication, but tumors that abut the vertebral body should not be deemed inoperable unless invasion of the cortex is confirmed. Tumor classification. Tumors were classified according to the level of involvement of thefirst rib: (I) anterior type-the tumor invades the anterior part of the first rib, the subclavian vessels,the anterior scalenus muscle, and the phrenic nerve, and the symptoms may include phrenic nerve palsy, shoulder pain,

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and venous dilation; (2) middle type-the tumor involves the middle part of the first rib and frequently extends high into the middle scalenus muscle; (3) posterior type-the tumor is close to the vertebral body and invades the posterior part of the first rib and the lower roots of the brachial plexus. In addition, the posterior wall and the posterior branches of the subclavian artery may be invaded to the point of origin of the vertebral artery. This type of tumor generally causes, initially, all symptoms of the Pancoast and Tobias syndrome. 14. 15 More voluminous and extensive tumors may be classifiedas combined anterior and middle types. Surgical technique. The patient is placed in the supine position with the neck hyperextended and the head turned away from the involvedside. A cervicotomy with an L-shaped incision is made; the vertical and horizontal branches follow the anterior border of the sternocleidomastoid muscle and the inferior border of the internal half of the clavicle, respectively. Division of the sternal attachment of the sternocleidomastoid muscle allows good exposure of the superior border of the subclavian vessels. The scalene fat pad is dissected and examined for disease to screen for the presence of scalene lymph node micrometastasis; thereafter, the ipsilateral superior mediastinum is inspected. Extension of the tumor to the thoracic inlet is then carefully assessed, and, if the tumor is deemed resectable, the internal half of the clavicle is removed. Because of the anatomy of the thoracic inlet, the operative procedure is carried out in three steps: ( I ) primary dissection of the veins, (2) dissection of the arteries, and (3) exposure of the brachial plexus. First, jugular and subclavian veins are dissected so that branches to the subclavian vein can eventually be divided. On the left side, ligation of the thoracic duct is usually required. Division of the distal part of the jugular vein simplifies the approach of venous confluence at the origin of the innominate vein. If the subclavian vein is involved by the tumor, it can be resected easily after proximal and distal control has been achieved. Direct extension of the tumor to the innominate vein does not preclude resection. The subclavian artery is then dissected; its distal part can be exposed after division of the anterior scalenus muscle over the first rib in tumor-free margins (Fig. I). The phrenic nerve is identified and exposed on the anterior aspect of the scalenus muscle; it must be carefully preserved or resected according to the extent of tumor involvement. The eventual division of branches of the subclavian artery, if they have been invaded by tumor, is simplified after the proximal control of its origin is obtained. The internal mammary artery and the ascending cervical artery are often divided, and the vertebral artery, when involved,can also be resected. When the tumor rests against the wall of the subclavian artery, the artery can be freed along a subadventitial plane. Whenever the arterial wall is involved by tumor, resection of the artery to obtain tumor-free margins is necessary (Fig. 2); revascularization is done with either a polytetrafluoroethylene graft (No.6 or 8) or an end-to-end anastomosis at the end of the cervical step. In middle-type tumors, the middle scalenus muscle can be extensively invaded, which would require divisionat a high point in tumor-free margins. Both extension of the tumor and compression of the brachial nerves require an "out-in side" dissection. Secondary branches and then primary branches of the brachial plexus are freed. The lower trunk and C-8 and T-I nerve roots can be dissected up to

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Fig. 1. Exposure of subclavian artery after divisionof insertion of anterior scalenus muscle on first rib.

the spinal foramen. Although the spread of the tumor may be at a high position on the brachial plexus, neurolysis is usually achieved without the division of branches of the brachial plexus above Tl (Fig. 3). Thereafter, the exposure of the vertebral body, the sympathetic chain, and the stellate ganglion (Fig. 4) is easily obtained, and tumors that have spread to these structures can be resected in tumor-free margins. After structures above the thoracic inlet have been freed of tumor and eventually resected, the first and second ribs, if the latter is involved, are easily resected either through the same cervical approach or by extending the incision into the deltopectoral groove. The resection of the first two ribs allows the en bloc resection of the tumor and the involved underlying parenchyma. Becausethe majority of the tumors are peripheral lesions, wedge resection (done with TA-55 or T A-90 staplers; Auto Suture Company Division, United States Surgical Corporation, Norwalk, Conn.) or simple upper lobectomy is sufficient and easily done (Fig. 5). In posterior tumors, a complementary posterior thoracotomy allows further resection of the chest wall, control of pulmonary vessels if a pneumonectomy is planned, or both. I The cervical incision is closed in two layers after suture of the sternal insertion of the sternocleidomastoid muscle. Statistical analysis. Survival was calculated from the date

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Fig. 2. Subclavian artery can be freed from tumor by dividing all collateral branches (vertebral artery is generally preserved if not invaded), and, if involved, it can be divided proximally and distally.

of operation until death or the date oflast follow-up for patients who remained alive and disease free. We estimated survival with the product-limit method I6; differences on its distribution were evaluated with the log-rank test 17 for univariate analysis and the Cox proportional hazards stepwise model" for multivariate analysis. Standard errors associated with the Kaplan-Meier estimator and 95% confidence intervals (Cl) were evaluated.!" 20 The a priori level of significance was set at p < 0.05; all tests were two-sided.

Results Between January 1980 and June 1991, more than 3000 patients underwent operation for lung cancer at our institution. Among these, 29 (fewer than 1%; median, 56 years of age; range, 36 to 73 years of age) were treated with this technique for NSCLC invading the thoracic inlet. Their demographic profile is illustrated in Table I. As shown, the majority of them were men (83%) with right-sided (62%), nonsquamous histologic type (62%), and posterior-type (69%) tumors. There were no operative or hospital deaths. Other postoperative complications were easily

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Fig. 3. The spread of tumor to brachial plexus requires an "out-in side" neurolysis if upper nerve roots are involved or a resection of T -I if lower trunk or nerve roots are involved.

treated, and cases were uneventful. All patients underwent a radical resection of the tumor. The surgical outcomes are shown in Table II. En bloc removal of the inlet tumor, chest wall (ribs 1 to 2), and underlying lung was done with the anterior transcervical approach alone in 9 cases. An additional posterior thoracotomy was necessary, with and without simultaneous need for a lobectomy or pneumonectomy, in the remaining 20 patients because of chest wall involvement below the second rib. We performed 14 wedge resections, 14 lobectomies, and I pneumonectomy. The pneumonectomy was necessary because of metastatic lymph nodes in the aortopulmonary window and involvement of the intrathoracic vagus and the phrenic nerves. The remaining patients had normal mediastinal lymph nodes at the time of pathologic examination. In 15 patients (52%), the inferior root (T-I) of the brachial plexus was involved by the tumor and resected; among these, 4 required removal of the phrenic nerve as well. Two other patients underwent resection of the phrenic nerve alone. Twelve patients (41 %) had extensive pathologic vascular involvement, and their operative treatment included resection of the subclavian artery alone (n = 3); sub-

Fig. 4. Vertebral artery can be freed from tumor, prevertebral muscles detached from vertebral bodies,and both stellate ganglion and sympathetic chain isolated and eventually resected.

clavian artery and vein (n = 3); subclavian and vertebral arteries (n = I); subclavian artery and vein and vertebral artery (n = 2); subclavian vein alone (n = I); vertebral artery alone (n = I); and subclavian vein and vertebral artery, (n = I). The subclavian artery was revascularized with either a prosthetic replacement (n = 7) or an endto-end anastomosis (n = 2). The prosthetic revascularization was done with a PTFE tubular ringed graft in all but one patient. Early (3 month) and late (6 month) graft patency was studied in all patients by means of arteriography, computed tomographic scan, or magnetic resonance imaging. No early graft occlusion occurred. Only the patient whose revascularization was done with a nonringed PTFE graft had a late occlusion with concomitant thrombosis of the subclavian vein. The overall median graft patency was 18.5 months (range, 6 to more than 73 months). Postoperative radiotherapy (median dose, 56 Gy) was given to 25 (86%) patients, either alone (n = 14) or in combination with adjuvant chemotherapy (n = II). With

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Table I. Demographic profile of patients No.

Gender

Age (yr)

Tumor histologic structure

Tumor side

Tumor type

I

Male Male Male Male Male Male Male Male Female Male Male Male Male Male Male Male Female Male Male Male Male Male Female Male Male Male Male Female Male

59 65 52 60 46 71 48 36 63 48 59 54 48 45 57 73 62 50 58 67 37 68 40 68 52 64 60 45 51

Squamous cell Squamous cell Adenocarcinoma Large cell Mixed cell Squamous cell Squamous cell Mixed cell Squamous cell Adenocarcinoma Adenocarcinoma Squamous cell Squamous cell Adenocarcinoma Squamous cell Squamous cell Adenocarcinoma Large cell Squamous cell Large cell Large cell Large cell Large cell Adenocarcinoma Adenocarcinoma Adenocarcinoma Large cell Large cell Squamous cell

Right Right Right Right Left Right Right Right Right Right Right Right Right Left Right Right Left Right Left Left Left Left Left Left Left Right Right Right Left

Posterior Anterior Posterior Posterior Posterior Middle Anterior Posterior Posterior Posterior Anterior Anterior Posterior Posterior Posterior Posterior Anterior Posterior Posterior Posterior Posterior Posterior Posterior Anterior Posterior Posterior Posterior Posterior Anterior

2 3 4 5 6 7 8 9 10 II

12 13 14 15 16 17 18 19 20 21 22

23 24 25 26 27 28 29

a median follow-up of 2.5 years, overall 2- and 5-year survivals were 50% (95% CI, 37.2% to 67%) and 31% (95% cr, 27.1% to 35.8%), respectively (Fig. 6). Twelve patients were alive and free of carcinoma at 4 to more than 137 months; one patient died, free of carcinoma, of a myocardial infarction 15 months after operation, whereas the remaining 16 patients died of their primary tumor because of tumor recurrence, either locally (n = 2) or systemically (n = 14). As assessed by univariate and multivariate analysis, no clinical, pathologic, or surgical characteristics significantly influenced survival (Table III).

Discussion Bronchogenic tumors that involvethe thoracic inlet are different from and are of more pronounced extent and stage of involvement than superior sulcus tumors.l? Because of the peculiarity of their location and the proximity of subclavian vessels, brachial plexus, phrenic nerves,and other vital structures, the surgical resection of this tumor isgenerally considered hazardous.i! Almost all surgeons consider the involvement ofthis target area to be an absolute contraindication to any definitive surgical

approach. As a consequence, experience with the surgical treatment of these tumors has been sparse. It usually involved the posterolateral approach described by Paulson,'? and was obtained at the expense of serious morbidity and mortality rates 8, 10 and no remarkable survival benefit ( < 1 year ).10,22 Various experiences stimulated the idea for our approach. First, the classic posterolateral approach, as described by Paulson, 10 does not provide sufficient visualization or safe exposure of all cervical structures of the thoracic inlet. Second, previous experience using either a transcervical" or supraclavicular technique-' for surgical diagnosis of apical lung tumors and a supraclavicular approach for the surgical management of the thoracic outlet syndrome/" have stressed the cost-benefit ratio of these approaches. Third, the control of either subclavian artery and its related branches and reconstructive operations on major vessels of the thoracic inlet is best accomplished through a supraclavicular incision, with or without removal of the clavicle. I I. 25 On the basis of the results reported here, our technique offers several advantages. It provides excellent exposure of the entire thoracic inlet, which affords a safe dissection

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Table II. Surgical characteristics Patient No.

Surgical approach

I 2 3 4 5 6 7 8 9

Cervical + PT Cervical Cervical + PT Cervical + PT Cervico+ PT Cervical + PT Cervical + PT Cervical + PT Cervical + PT Cervical + PT Cervical + PT Cervical + PT Cervical + PT Cervical + PT Cervical + PT Cervical + PT Cervical Cervical + PT Cervical + PT Cervical Cervical + PT Cervical + PT Cervical + PT Cervical Cervical Cervical Cervical Cervical Cervical

10 II

12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29

Nerves resected

TI

PN

Tl PN+TI +T2 PN

Tl

TI C8-TI Tl TI Tl Tl PN+TI PN+TI Tl TI PN+T1

Ribs resected 1 I 1-3 1-3 1-2 1-2 1-2 1-3 1-4 1-2 1-3 I 1-4 1-3 1-5 1-4 1-2 1-4 1-3 1-2 1-2 1-3 1-2 I 1-2 1-2 I 1-3 1-2

Subclavian artery

Subclavian vein

Vertebral artery

Surgical procedure for the lung

WR WR WR UL PE

Involved

PTFE (6 mm)* PTFE (8 mm)*

Involved Involved

Involved PTFE (8 mm)

Involved Involved

Involved

EE PTFE (8 mm)* PTFE (8 mm)*

Involved

Involved Involved

PTFE (8 mm)*

Involved

Involved

EE PTFE (8 mm)*

UL UL UL UL UL WR UL UL UL UL WR UL WR UL WR WR WR WR UL WR WR WR UL WR

PT, Posterior thoracotomy; WR, wedge resection; C8, TJ, roots of the lower trunk of the brachial plexus; T2, second thoracic nerve; UL, upper lobectomy; PE, pneumonectomy; PN, phrenic nerve; C8, eighth cervical vertebra; EE, end-to-end reanastomosis with 6-0 polypropylenecontinuous suture. *Ringed graft (diameter)

and complete surgical clearance of involved segments of the subclavian vessels and related branches, phrenic nerve, and brachial plexus; (2) it provides uncomplicated visualization and safe treatment of the apex of the lung, the underlying involved parenchyma, the pulmonary pedicle, and the first two ribs (especially if the L-shaped incision is extended into the deltopectoral groove); (3) it does not preclude a complementary posterolateral thoracotomy if further resection of the chest wall or major pulmonary resections are necessary; (4) it results in negligible morbidity, no mortality, and minimal discomfort; and (5) it offers encouraging long-term survival. The major disadvantages include duration of operation, particularly if both cervical and thoracic incisions need to be performed, and development of minimal shoulder discomfort in those patients who require resection of both the clavicle and the external branch of the accessory nerve.

Although the few studies- 10 that have addressed lung tumors involving the subclavian artery and related branches have reported very dismal results with regard to complete resection and surgical morbidity and mortality rates, one plausible explanation is that these studies have included the posterolateral approach described by Shaw, Paulson, and Kee,l which provides an insufficient manipulation of the subclavian artery, By contrast, the anterior approach affords a superb and wide exposure of all the vascular inlet structures. In particular, the horizontal clavicular incision greatly increases the exposure of the subclavian vessels, and after the posterior periosteum of the clavicle and underlying subclavian muscle are divided, dissection of the subadjacent subclavian vein, the anterior scalenus muscle, the phrenic nerve, and the subclavian artery is easily performed. The approach exposes most of the right subclavian artery, both subclavian veins, the distal two thirds of the left subclavian artery, the

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Table III. Univariate survival analysis Five-year survival percentage Characteristics

(95% C/)

P Value

38.1 (26.2-55.1) 23.0 (16.1-32.1)

NS NS

30 (20.7-43.3) 30(21-43.1)

NS

40 (28.1-56.7) 30.3 (20.3-45. I)

NS

42.8 (27.2-65.9) 27 (19.2-37.9)

NS

41.4 (28.5-59.9) 18.1 (13.0-25.1)

NS

38.1 (24.7-58.5) 27 (19.4-37.5)

NS

41.3 (28.5-59.7) 17 (I 2.2-22.7)

NS

30.3 (20.7-44.3) 41.6 (28.7-60.2)

NS

36 (24.6-52.6) 23 (16.5-31.9)

NS

Age

.s 56 yr > 56 yr Tumor histology Squamous Nonsquamous Tumor side Right Left Tumor type Anterior Posterior No. of ribs resected ~2

>2 Surgical approach Cervical Cervical + PL T Nerve involvement Present Absent Vascular involvement Present Absent Extent of resection Wedge resection Lobectomy

*Nonsquamous histologic type includes tumor with adenocarcinoma and largecell histologic type; the variables that were not included in the statistical analysis because of their small cell samples ( < 5) were as follows; female, middle-type lesions. mixed tumor histologic, and pneumonectomy; nerve involvement was eitherphrenic or of the hrachial plexus;vascular invasion includes patients with at leastone invasionof the subclavian artery or vein or vertebral artery; differencesinsurvivaldistribution were calculated with the log-rank test. PLT, Posterolateral thoracotomy; NS. not statistically significant (p> 0.05).

Fig. 5. Operative view after en bloc resection of tumor. chest wall. subclavian artery. and underlying apex of upper lobe. which may be resected with a stapler instrument.

1.00

proximal portion of the carotid arteries, and the internal jugular veins. Moreover, after resection of the first rib, the proximal control of the left subclavian artery is easily obtained. In our experience, dissection and resection of either subclavian vessel have never represented a major operative problem. Because of their rich collateral circulations, the subclavian and internal jugular veins are generally ligated after proximal and distal control. Similarly, ligation of the vertebral artery is possible, if no cerebrovascular disease is present. Because of the high risk of significant ischemia of the upper limb after resection of the subclavian artery, our policy was to immediately revascularize this artery either by means of end-to-end anastomosis, whenever technically feasible, or with vascular grafts. This has allowed us to avoid fatal ischemic com-

0.75

0.25 PATIENTS AT RISK 0.00

(4)

(4)

(1)

(1)

(1)

(1)

+-~--"T....L.,~.--~---r~-r-~---r~-r-~--,

o

20

40

60

80

100

120

140

TIME (months)

Fig. 6. Survivalof all patients (n = 29). Vertical bars indicate standard errors. Overall median length of survival was 21 months.

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Dartevelle et al.

plications, as described by Paulson'? and Wright and associates.f We preferred to use a PTFE graft for this procedure because it has the tendency to remain patent despite the fibrotic changes that may occur as a result of postoperative radiotherapy. Follow-up arteriography failed to demonstrate reduction of the internal lumen of the PTFE graft; this is in accordance with experimental/? and clinical?" observations. In this study, only one patient had graft occlusion, and the overall median graft patency was 18.5 months (range, 6 to more than 73 months). In the patient who had late graft occlusion, revascularization of the subclavian artery was done with an unringed PTFE graft, and this may have been the cause of the late failure. Therefore, the two prerequisites that might guarantee the best long-term patency of the arterial graft are large size (usually 6 or 8 mm) and reinforcement by rings. It has been generally accepted" 10 that extensive local involvement of the brachial plexus constitutes a contraindication to surgical resection because of the poor survival'? and high incomplete resection rate (24% in the series of Wright and associatesj.f With the presented technique, involvement of secondary and primary branches of the brachial plexus are easily identified and dissected, up to the spinal foramen. In this study, 15 patients had involvement of the lower trunk of the brachial plexus, and, in all instances, resection was performed in tumor-free margins. As experience with this technique has increased, it has become evident that most NSCLCs of the thoracic inlet may be treated with the anterior transcervical approach without the need for the posterolateral thoracotomy described by Paulson. 10 In this series, the last six patients were treated in this fashion, and three of them had posterior-type tumors. The L-shaped incision can be easily extended either into the deltopectoral groove or according to the anatomic distribution of the tumor (for example, an anterior thoracotomy can be accomplished without affecting the hilar manipulation or oncologic radicality of the operation). From a theoretic point of view, the anterior approach has much less physiologic impact on patients with limited pulmonary reserve and allows the patient to remain stationary, unlike the combined anterior and posterior approach. According to the TNM classification.P NSCLCs invading the thoracic inlet are categorized as T4 lesions and, like other tumors of this stage, generally have a frustrating prognosis.i? However, the increasing improvement of surgical and anesthetic techniques has played a fundamental and expanding role in enhancing the local control of selected T4 tumors, for example, those invading the carina.'? superior vena cava,27 and vertebral column." Although these techniques have associated diffi-

The Journal of Thoracic and Cardiovascular Surgery June 1993

culties and hazards, which make their use rare, the complete resection of the lesions may be the sine qua non for long-term survival. Obviously, these approaches represent prime examples of the ultimate application of surgical science in the oncologic arena. The transcervical-thoracic technique might broaden the indications of operation for apical lung carcinomas, irrespective of their location. However, this technique is appropriate for a very small fraction of patients with lung carcinoma (less than I% in our series). Absolute contraindications for this operation are the presence of extrathoracic sites of metastasis, histologically confirmed mediastinal lymph node involvement, smallcell histologic type, and vertebral body involvement. In this regard, we do not recommend this operation for superior sulcus tumors, for which the posterior technique' remains preferable. The therapeutic index of the presented technique was impressive. The 2- and 5-year survival of 50% (95% CI, 37.2% to 67%) and 31% (95% CI, 27.1% to 35.8%) not only are very encouraging but justify and emphasize the need for the technique and its oncologic radicality. Because of the absence of reports dealing with similar, adequately diagnosed, and pathologically staged lesions, presented results may also provide an important benchmark for the estimation of the efficacy of future treatment modalities for these tumors. Although the number of patients included in the study is relatively small, the follow-up time is adequate (median, 2.5 years) for drawing conclusions from the results generated by univariate analysis. Patients who were younger than 56 years of age, who had right-sided and anterior-type tumors that extended to the first two ribs and involved the phrenic nerve or brachial plexus or both, showed a remarkable, albeit not significant, 5-year survival advantage over their respective counterparts. It is not surprising that patients without vessel involvement (41.6%) had a better outcome than those patients whose subclavian vessels were involved (30.3%). However, the survival of the latter group of patients is impressive considering that previous studies by Paulson.!" Wright and associates.f and Shields-? reported survival of less than 2 years for patients whose Pancoast tumor extensively involved the subclavian vessels. It is evident that the importance of careful preoperative staging cannot be overstressed. As suggested by Wright and associates.' computed tomographic scanning and magnetic resonance imaging are fundamental in the assessment of the extent of the lesion and vascular invasion, respectively, and, therefore, in the resectability of these tumors. We did not recommend, unlike Shaw, Paulson and Kee,1 preoperative radiation therapy because we believed

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that the debulking ofthe tumor was not necessary because of the radical nature of our technique and the radiationinducible local and systemic consequences. Conversely, we recommended postoperative radiation therapy because of the fear of late local relapse and because the volume of the entire tumor-bearing area is generally small. However, with longer follow-up, we noted that the majority of patients had a relapse and ultimately died as a result of systemic disease; this suggests that effective systemic rather than local adjuvant postoperative therapy is necessary. This transcervical-thoracic approach offers also a therapeutic option for benign and malignant tumors arising from the bone and soft tissues ofthe supraclavicular area, which have a particular tendency to invade adjacent structures.F The anterior transcervical-thoracic approach described here affords safe and complete exposure of the entire thoracic inlet and represents a new and effective treatment modality for selected cases of NSCLC that extensively involve this target area, which otherwise would be considered inoperable and would be associated with detrimental outcome. However, it must be done by experienced surgeons who are familiar with all aspects of vascular surgery and in major medical centers in which an appropriate number of operations for lung cancer are done.

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4. 5.

6.

7.

8.

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REFERENCES Shaw RR, Paulson DL, Kee JL Jr. Treatment of the superior sulcus tumor by irradiation followed by resection. Ann Surg 1961;154:29-40. Paulson DL. The "superior sulcus" lesion. In: Delarue N, Eschapasse H, eds. International trends in general thoracic surgery. Lung cancer. vol I. Philadelphia: WB Saunders, 1985:121-31. Miller JI, Mansour KA, Hatcher CR. Carcinoma of the superior pulmonary sulcus. Ann Thorac Surg 1979;28:447. Attar S, Miller JE, Satterfield J, et al. Pancoast's tumor: irradiation or surgery') Ann Thorac Surg 1979;28:578-86. Standford W, Barnes RP, Tucker AR. Influence of staging in superior sulcus (Pancoast) tumors of the lung. Ann Thorae Surg 1979;29:406-9. Devine JW, Mendenhall WM, Million RR, Carmichael MJ. Carcinoma of the superior pulmonary sulcus treated with surgery and/or radiation therapy. Cancer 1986;57: 941-3. Shahian OM, Wildford BN, Ellis FH Jr. Pancoast tumors: improved survival with preoperative and postoperative radiotherapy. Ann Thorac Surg 1987;43:32-8. Wright CD, Moncure AC, Shepard JOA, Wilkins EW, Mathisen OJ, Grillo He. Superior sulcus lung tumors. J THORAC CARDIOVASC SURG 1987;94:69-74. Anderson TM, Moy PM, Holmes Ee. Factors affecting

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28.

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survival in superior sulcus tumors. J C1in Oncol 1986;4: 1598-603. Paulson 0 L. Carcinomas in the superior pulmonary sulcus. J THoRAc CARDIOVASC SURG 1975;70:1095-104. Flint LM, Snyder WH, Perry MO, Shires GT. Management of major vascular injuries in the base of the neck. Arch Surg 1973;106:407-11. Dartevelle P, Levasseur P, Rojas-Miranda A, Merlier M, Le Brigand H. Exerese par voie combinee cervico-thoracique des tumeurs responsable de syndrome de PancoastTobias. Nouv Presse Med 1981;10:1051-4. Dartevelle P, Levasseur P, Rojas-Miranda A, George B, Le Brigand H, Merlier M. Interet de la cervicotomie elargie dans les syndromes de Pancoast-Tobias. Ann Chir 1984; 38:80-3. Pancoast HK. Importance of careful roentgen-ray investigations of apical chest tumors. JAMA 1924;83:1407-11. Tobias JW. Sindrome apico-costo-vertebral-doloroso per tumor apexiano: su valor diagnostico en Ie cancer primitivo del pulmon [Thesis). Buenos Aires: Impresora mercatali, 1932:193. Kaplan EL, Meier P. Nonparametric estimation from incomplete observations. J Am Stat Assoc 1958;53:457-81. Peto R, Pike MC, Armitage P, Breslow NE, Cox DR, Howard SY. Design and analysis of randomized clinical trials requiring prolonged observations of each patient. II. Analysis and examples. Br J Cancer 1977;35:1-39. Cox DR. Regression models in life tables. J R Stat Soc (B) 1972;34:187-220. Kalbfleish JD, Prentice RL. The statistical analysis of failure time data. New York: Wiley, 1980. Kahn HA, Sempos CT. Statistical methods in epidemiology. New York: Oxford University Press, 1989:45-71. McGoon De. Transcervical technique for removal of specimen from superior sulcus tumor for pathologic study. Ann Surg 1964;159:407-10. Shields TW. Carcinoma of the lung. In: Shields TW, ed. General thoracic surgery. 3rd ed. Philadelphia: Lea & Febiger, 1989:890-934. Dart CH, Braitman HE, Lalarb S. Supraclavicular thoracotomy for diagnosis of apical lung and superior mediastinal lesions. Ann Thorac Surg 1977;28:91-3. Roos DB. The place of scalenectomy and first rib resection in thoracic outlet syndrome. Surgery 1982;42:1077-85. Moore WS. Operative technique. In: Rutheford RB, ed. Vascular surgery. 2nd ed. Philadelphia: WB Saunders, 1984;1248-66. Masuda H, Ogata T, Kikuchi K, Tanaka S. Longevity of expanded polytetrafluoroethylene grafts for superior vena cava. Ann Thorac Surg 1989;48:376-80. Dartevelle P, Chapelier A, Pastorino U, et al. Long-term follow-up after prosthetic replacement of the superior vena cava combined with resection of mediastinal-pulmonary malignant tumors. J THORAc CARDIOVASC SURG 1991; 102:259-65. Mountain CF. A new international staging system for lung cancer. Chest 1986;89:225S-33S.

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29. Mountain CF. Prognostic implications of the international staging system for lung cancer. Semin Oncol 1988;15:23645. 30. Dartevelle PG, Khalife J, Chapelier A, et al. Tracheal sleeve pneumonectomy for bronchogenic carcinomas: report of 55 cases. Ann Thorac Surg 1988;46:68-72. 31. DeMeester TR, Albertucci M, Dawson r.r, Monter SM. Management of tumor adherent to the vertebral column. J THORAC CARDIOVASC SURG 1989;97:373-8. 32. Macchiarini P, Dartevelle P, Chapelier A, et al. Technique for resecting primary or metastatic non-bronchogenic tumors of the thoracic outlet. Ann Thorac Surg [In press].

Discussion Dr. G. Alexander Patterson (St. Louis. Mo.). I should point out that this is not the first time Dr. Dartevelle has made a significant contribution in the treatment of locally advanced bronchogenic carcinoma. You did not mention in your discussion the nodal status of patients in your series. What staging do these patients receive before the operation, and are you influenced by the presence of either N2 or N3 disease? Is routine supraclavicular node biopsy used in these patients and would the finding of a positive N3 node change the conduct of the operation? You had a small number of patients, but the results are excellent in your patients with T4 tumors; 30% of your patients had vascular involvement. Do you believe that the conduct of the operation with this anterior approach enables you to offer surgical resection to patients whose tumors would perhaps not be operable or completely resectable with the use of a classic posterior approach? Dr. Robert J. Ginsberg (New York, NiY']. You have introduced another approach to treatment of superior sulcus tumors in which these advanced tumors, although classified as T4, can be resected and occasionally eradicated. I commend you and your colleagues for this. You have shown us the occasional advantage of resecting superior vena cava and carinas.

The Journal of Thoracic and Cardiovascular Surgery June 1993

You did not mention your use of postoperative radiotherapy in all of your patients. I note that you do not use preoperative radiotherapy, which is very common in this country. I would like you to comment on the use of preopera tive radiotherapy as well. Although you did not use a combined approach in the last few patients that you treated in this manner, many of your patients did have both an anterior and posterior approach for treatment in the C-8 and T-l nerve root. I have found that when I use the anterior approach any tumor near the intervertebral foramen is difficult to address. Perhaps you have some advice regarding the proximity of the tumor to the intervertebral foramen and your decision on whether to use an anterior or a combined approach. Dr. Dartevelle No patient had clinical evidence of mediastinallymph node involvement at the time of operation. As for other locally advanced bronchogenic tumors (e.g., superior vena cava and carina), I strongly support the concept that extensive surgery is justifiable only when there is no evidence of clinical (preoperative) N2 disease, which I consider an absolute contraindication to any surgical approach. Radiation therapy was never administered in the preoperative setting; by contrast, the vast majority of patients received this treatment modality after the operation, with and without cancer chemotherapy. The question addressing which patients may benefit from the anterior and which from the posterior approach is appropriate. 1 believe that the anterior approach should be reserved for those apical lung tumors that originate from either upper lobe that have extensively invaded the thoracic inlet. For those apical tumors that have invaded the posterior path of the chest wall, the classic posterior approach, described by Dr. Paulson, remains the most appropriate one. Dr. Ginsberg, I realize that with the anterior approach it is difficult to remove the posterior path of the chest wall and, as a matter of fact, in two thirds of my patients, I had to use a combination of the anterior and posterior approach. However, in many of the cases, if the anterior approach had not been used, I am sure that some tumors would have been left in place behind the subclavian artery or the brachial plexus. For these reasons, I consider that the anterior approach was necessary.