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Surgical management of superior sulcus tumors

M. BLAIR MARSHALL MD

Chief, Division of Thoracic Surgery, Georgetown University Medical Center, Washington, District of Columbia, USA

LARRY R. KAISER, MD

The John Rhea Barton Professor and Chairman, Department of Surgery, University of Pennsylvania; Surgeon-in-Chief, University of Pennsylvania Health System, Philadelphia, PA, USA

HISTORY

In 1838 a patient with an apical lung tumor and involvement of the brachial plexus was described. This entity became more widely recognized when Pancoast reported a series of seven patients with apical lung tumors, Horner’s syndrome, rib destruction, atrophy of the intrinsic muscles of the hand, and pain. Because of their location, Pancoast tumors involve the neurovascular structures and historically were deemed inoperable.

The current “standard,” if one could actually call it a standard, came about serendipitously when a patient who was deemed inoperable underwent radiation therapy. This patient was restudied, found to be resectable, and went on to live for an additional 27 years. This case drove the management of these tumors toward preoperative radiation therapy followed by “curative” resection.

In 1961, Shaw reported results in 18 patients who received preoperative radiation therapy followed by resection. These results set the “standard of care” in these patients for years to follow. Currently, many surgeons continue to treat these patients with preoperative radiation followed by surgical resection, though the dose and schedule of preoperative radiation has not been standardized. Because several clinical trials have suggested a beneﬁt in survival in patients who received neoadjuvant chemoradiotherapy, some centers have added this treatment to their preoperative regimen for Pancoast tumors. Thoracic surgeons should be aware that no randomized prospective trials exist showing a beneﬁt of preoperative radiation and/or chemotherapy in patients with Pancoast tumors. This situation is due mainly to the fact that too few of these tumors are seen to allow for the conduct of a randomized trial that would be complete in our lifetime.

PRINCIPLES AND JUSTIFICATION

Not all apical lung tumors are classical Pancoast tumors. If this term is to be used, it should be reserved for those apical lung tumors involving the chest wall including the ﬁrst rib with secondary involvement of the brachial plexus and/or vascular structures. From both a therapeutic and prognostic standpoint, this distinction is important. True Pancoast tumors have a poor survival because of the locally advanced nature of these tumors with involvement of the brachial plexus and often the spine. Apical lung tumors that have not invaded the neurovascular structures can usually be completely resected and are associated with a better outcome, especially in the absence of lymph node involvement. These patients are not necessarily treated with preoperative radiotherapy.

PREOPERATIVE ASSESSMENT AND PREPARATION

Apical lung tumors, including those commonly referred to as Pancoast tumors, represent a signiﬁcant challenge to thoracic surgeons. Patients presenting with Pancoast’s syndrome should undergo a meticulous preoperative workup to determine the diagnosis, as other diseases and other tumors have been associated with this syndrome. Bronchoscopy with brushings may obtain a diagnosis in 40%, and needle biopsy results in a diagnosis in about 90% of these lesions.

A complete history and physical examination should be performed, paying close attention to any cardiac or respiratory disease. An extent of disease workup is carried out to determine stage and operability. A complete neurovascular

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examination is performed. If any question of vascular involvement exists, we perform magnetic resonance imaging (MRI) or angiography preoperatively.

The preoperative chest CT scan is helpful in determining which thoracic outlet structures are involved as well as the extent of chest wall and vertebral body involvement. Mediastinal nodal disease can be assessed. Because patients with mediastinal disease have the poorest survival, we perform a mediastinoscopy on all patients preoperatively. Those patients with a Pancoast tumor and mediastinal disease should be referred for either combined radio/chemotherapy or radiotherapy alone.

ANESTHESIA

In operations being performed through an anterior cervicothoracotomy, we have not found it necessary to place an epidural catheter for postoperative analgesia. This incision is associated with minimal pain when compared with a posterolateral thoracotomy. Epidural analgesia is deﬁnitely beneﬁcial for pain management following the posterolateral or combined approach. The patient is placed under general anesthesia, and a double-lumen endotracheal tube is placed. Appropriate electrocardiography (ECG) leads and an arterial line are placed for intraoperative monitoring. Bronchoscopy is performed in the operating room by the surgical team.

Brachial plexus

Tumor

Subclavian artery

Subclavian vein

OPERATION

These tumors classically have been approached

1,2

more recently, we have begun to approach the majority of these lesions through a cervicothoracic approach. This incision is similar to that described by Dartevelle and his colleagues. Although some discussion exists in the literature about which approach is best for speciﬁc locations, anterior versus posterior, we use the cervicothoracic approach for all apical lung tumors involving the thoracic outlet and/or ﬁrst rib.

through a posterolateral thoracotomy. However,

Vertebral bod

First rib

Tumor

Transverse process T1

Second rib

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Cervicothoracic approach (Dartevelle)

The patient is placed in the supine position, with the arms tucked and either a shoulder roll or inﬂatable bag beneath the

An “L” shaped incision is made along the medial border

of the sternocleidomastoid down to the sternal notch and then out along the inferior border of the clavicle to the deltopectoral groove. The subcutaneous tissues are divided and the clavicle is circumferentially dissected just above its insertion onto the manubrium.

scapulae. The patient is placed under general anesthesia, and a Foley catheter and an arterial line are placed. The arterial line should be on the contralateral side in case of subclavian artery involvement.

Line of division for oblique transection of clavicle

We divide the clavicle obliquely with a Gigli saw, or more

recently with an oscillating saw. This maneuver makes reapproximation of the clavicle possible at completion. We have not found it necessary to remove the medial third of the clavicle as described by Dartevelle and colleagues.

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End of clavicle being retracted with the skin flap and muscle

The sternal attachments of the sternocleidomastoid,

sternohyoid, and sternothyroid muscles are divided, and a Ruhltract retractor is used to elevate the clavicle. This maneuver exposes the brachiocephalic, subclavian, and internal jugular veins. The scalene fat pad is dissected and pathologically examined for disease. The veins are dissected, and at this point we usually divide the mammary vessels. The ascending cervical vein is divided. The resectability of the lesion is assessed.

Phrenic nerve

C7 C8

Brachial plexus

Transected head of clavicle

First rib

Middle scalenus muscle

Anterior scalenus muscle

Subclavian artery

Subclavian vein

Clavicle

The anterior scalene muscle is identiﬁed, and the phrenic

nerve can be observed coursing along its anterior border. Before the insertion of the anterior scalene onto the ﬁrst rib, the phrenic nerve turns medially. Thus, when dividing the anterior scalene, it is best to stay close to the rib if possible. The phrenic nerve should be carefully preserved or, if involved, deliberately resected. The subclavian vein may be divided if involved with tumor. If one anticipates involvement of the vessels, proximal and distal control should be obtained early in the dissection. This maneuver is facilitated by the anterior approach and is signiﬁcantly easier than when attempted from the posterolateral approach. The subclavian artery is dissected in the subadventitial plane. Branches from the subclavian artery may be sacriﬁced if necessary. The internal mammary, ascending cervical, and vertebral arteries may all be ligated. We divide the vertebral artery only if it is invaded by the tumor. The continuity of the circle of Willis should be established preoperatively if it is anticipated that the vertebral artery will need to be sacriﬁced. If necessary to obtain a complete resection, the subclavian artery is clamped and divided. The reconstruction may be performed with a direct end-to-end anastomosis or with a polytetraﬂuoroethylene (PTFE) interposition graft after the tumor has been resected.

The brachial plexus is evaluated. The middle and posterior scalene muscles are divided sharply as the brachial plexus is in close proximity. One should preserve the long thoracic nerve that courses along the posterior border of the middle scalene. If the brachial plexus is involved, most commonly it is the lower trunk that is encased. The upper trunks are rarely involved, but the occasional tumor may inﬁltrate widely thorough the plexus. The stellate ganglion usually must be divided to achieve a complete resection, recognizing that the patient will have a Horner’s syndrome postoperatively. Once the vessels and brachial plexus have been freed from the tumor, the chest wall can be resected. Initially, the ﬁrst rib is divided anteriorly at the junction of the manubrium.

Posteriorly, we incise the ligament between the neck of

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the ﬁrst rib and transverse process. An osteotome is placed into this space, and the rib is disarticulated from the transverse process and vertebral body. The C8 and T1 nerve roots can be identiﬁed straddling the head of the ﬁrst rib. The T1 nerve root may be sacriﬁced with minimal residua, but taking both the C8 and T1 roots results in a signiﬁcant disability of the hand. The nerve roots must be identiﬁed at the level of the neural foramina to assure that only the T1 root is taken as opposed to the entire lower trunk. The head of the second rib may be identiﬁed from within the chest and then dissected off the transverse process from an anterior approach. The pleura overlying the costovertebral junction is divided. This step gives access to then use the osteotome to disarticulate the rib from an anterior approach. Any additional posterior rib resections are done in this fashion. Partial vertebrectomy may be done, if necessary recognizing the negative prognostic implications of vertebral involvement.

C7 nerve root

C8 nerve root

First rib

Lower cord of brachial plexus

Operation 329

T1 nerve root

The pleura around the lesion and corresponding chest wall is incised, and the lesion with the attached chest wall is left with the underlying lung. The lobectomy is now completed. Usually we are able to complete this procedure through the cervicothoracic approach without an additional thoracotomy.

After the lobectomy and lymph node dissection, the chest is closed as described elsewhere. If the anterior chest wall has been removed, we reconstruct this with methylmethacrylate and polypropylene mesh. If the chest wall resection is limited to the posterior region, prosthetic reconstruction is not needed as the scapula covers the defect.

Latissimus dorsi muscle

Trapezius muscle

Posterolateral approach

This approach was popularized by Paulson. It is standard for apical lung lesions; however, exposure and control of the brachiocephalic vessels and the brachial plexus is more difﬁcult, especially with a larger tumor. The cervicothoracic approach, as described above, may be the more versatile approach to these lesions but does require a detailed knowledge of the anatomy of the thoracic inlet.

For the posterolateral approach, the patient is positioned

in the standard lateral decubitus position after placement of a double-lumen endotracheal tube as described in Chapter 23 on incisions. The chest is prepped from the C7 prominence to below the costal margin and from the spine to the nipple. A posterolateral thoracotomy is made as described elsewhere.

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The ﬁfth intercostal space is entered for exploration. If

the initial exploration indicates that the lesion is resectable, the incision is extended up to the C7 prominence, and the trapezius muscle and the rhomboids are divided. The Finochietto retractor is positioned with the inferior blade resting on the sixth rib and the superior blade under the tip of the scapula. The retractor is cranked open elevating the scapula off of the chest wall. This maneuver exposes the apex of the chest. The posterior scalene is divided with cautery.

Tip of scapula

Brachial

lexus

Subclavian artery

Divided serratus muscle

Subclavian vein

Tumor

The middle and anterior scalenes are dissected off the

the brachial plexus and subclavian vessels lie superior to the ﬁrst rib. Dividing the scalene muscles is made easier by placing the ﬁrst rib on downward traction. The anterior scalene muscle inserts on the ﬁrst rib between the subclavian vein and artery. Initially, the ﬁrst rib is dissected in the subperiosteal plane. This step frees the rib of the medial and anterior scalenes without risking injury to the brachial plexus or phrenic nerve. The exact location to begin the chest wall resection is determined by observing the extent of tumor from within the chest. Usually, a 4-cm margin is necessary. The dissection begins at the inferior margin and progresses superiorly. It is easiest to divide the rib to be taken at the anterior aspect ﬁrst and then divide posteriorly. The inferior ribs are taken working up toward the ﬁrst rib.

ﬁrst rib in the subperiosteal plane, recognizing that

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The sacrospinalis and thoracicus iliacus are dissected

away from the chest wall. The posterior margin is most commonly obtained by disarticulating the head and neck of the rib away from the transverse process and corresponding vertebral body. The ligament between the neck of the rib and transverse process is incised with electrocautery. A curved osteotome is inserted between these structures, and the rib is disarticulated. This maneuver exposes the nerve roots at the foraminal level where they may be ligated and divided in a controlled fashion. One must be careful to avoid avulsing these roots as the dural sheath may extend beyond the foramen for a variable extent and avulsion may result in a cerebrospinal ﬂuid leak. Sacriﬁcing the T1 nerve root may result in minimal motor weakness but often has no functional consequence, as mentioned above. Sacriﬁce of both C8 and T1 nerve roots results in a clawed hand with minimal function. Bleeding from the venous plexus at the neural foramen or intercostal vessels should be controlled with sutures or a bipolar cautery. Surgicel or other hemostatics should never be packed against the foramen in an attempt to control bleeding as migration of this material into the canal may result in compression of the spinal cord and paraplegia.

Transverse process

Costotransverse joint

Osteotome

Divided erector spinae muscle tendon

Head of rib

Transverse process

Chest wall block with attached lung and tumor

Once the chest wall has been divided and freed, it is

tomy with lymph node dissection is performed.

left in-continuity with the lung, and a formal lobec-

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If extensive involvement of the brachial plexus exists above these levels and a complete resection cannot be performed, all of the nerves are left intact, and the patient is referred for postoperative radiotherapy. Prior to dividing any of these structures, the resectability of the lesion should be thoroughly investigated. An incomplete resection is associated with poor long-term survival.

Following the lobectomy and lymph node dissection, a single thoracostomy tube is placed. Posterior defects involving the ﬁrst to third ribs do not need to be reconstructed. If the fourth rib is resected, we tend to reconstruct these with polypropylene mesh so that the tip of the scapula does not get trapped in the chest wall defect.

POSTOPERATIVE CARE

With the cervicothoracic approach, patients have less pain and limitation of motion in the immediate postoperative period. They are able to ambulate more readily. We put these patients in a sling for comfort. Physical rehabilitation plays an important role in their postoperative care. Patients with extensive apical dissections may have prolonged drainage; however, one must make sure that this situation does not represent a chyle or CSF leak.

Postoperative complications include those associated with lobectomy, bleeding, infection, bronchopleural ﬁstula, and chyle leak. These patients may also have neurological deﬁcits associated with resection of the lower roots of the brachial plexus.

OUTCOME

Treatment regimens include preoperative radiation therapy followed by complete resection, resection both complete and incomplete, followed by radiation therapy with or without chemotherapy, and curative radiation therapy alone. Negative prognostic indicators include mediastinal lymph node disease, subclavian artery involvement, and vertebral body involvement, although the latter two remain somewhat controversial. Some controversy exists over whether ipsilateral supraclavicular lymph node involvement (N3) represents “local” spread; and therefore, these patients have a better prognosis than those with supraclavicular lymph node disease in non-Pancoast non-small cell lung carcinoma (NSCLC).