80: Pancoast Syndrome: Extended Resection in Superior Pulmonary Sulcus and Anterior Approach

Approximately 5% of all non-small cell lung cancers (NSCLC) are located in the extreme apex of the lung, frequently with involvement of some combination of the first and second ribs, brachial plexus, subclavian vessels, and upper thoracic vertebral bodies. This phenomenon is referred to as a superior sulcus carcinoma, indicating tumor location in the uppermost portion of the costovertebral gutter within the chest. Pancoast syndrome refers to superior sulcus tumors along with the triad of (1) shoulder and arm pain, (2) wasting of the hand muscles, and (3) ipsilateral Horner syndrome (i.e., ptosis, miosis, and anhidrosis due invasion of the stellate ganglion). Henry Pancoast was a radiologist who described these findings in 1932 but failed to recognize the pulmonary origin of these tumors. Unaware of Pancoast report, Tobias, an Argentine physician, described similar clinical findings and ascribed them to the presence of peripheral lung tumors. Pancoast–Tobias syndrome is perhaps a more appropriate eponym for this entity. Anatomically, the superior pulmonary sulcus is the area on the superior surface of the lung traversed by the subclavian vessels and encircled by the first rib and spine (Fig. 80-1). It also may be described as the thoracic outlet or thoracic inlet.

For the next 25 years, these tumors were considered unresectable and uniformly fatal. In 1951, during irradiation therapy, a patient of Dr. Robert Shaw developed unbearable pain that precluded continuation of his irradiation therapy. With a threat of suicide, Dr. Shaw performed an en bloc resection of the cancer, with the chest wall, and lower trunk of the brachial plexus. Dr. Shaw did not expect him to live long; however, the patient survived over 40 years (outliving Dr. Shaw).

In 1961, Shaw et al.¹ described successful outcomes in 18 patients undergoing 30 Gy of radiation, followed by resection, and this became the standard of care for the next 20 to 30 years. In over 400 patients with N0 stage I, Urschel found that approximately 35% had a 5-year survival. The treatment of choice since these reports has been preoperative irradiation (3000 rads over 2–3 weeks) followed by surgical en bloc resection of the lung, chest wall, lower brachial plexus, and vertebrae at a 1- to 2-month interval. This effects approximately a 35% to 50% 5-year survival with N0 stage I patients. Recently, the Intergroup 0160 phase II trial demonstrated superior outcomes by using trimodality therapy for superior sulcus tumors, which now represents the standard of care.²

Dr. Shaw's initial successful outcome caused our group to treat several other patients in similar fashion with 3000 rads to the tumor and mediastinal lymph nodes over a period of 2 to 3 weeks, followed by a waiting period of 2 to 4 weeks. This delay allows time for the benefits of irradiation, which theoretically include shrinking of the tumor, blocking of the lymphatics, and weakening of the cells that might be left after surgery because the margins are extremely close in such tumor resections. In 1961, 14 patients were reported, with approximately 40% 5-year survival shown.¹ Chardack and MacCallum^3,4 presented a patient in 1953 and 1956 who had been resected and treated successfully with postoperative irradiation therapy. This approach, however, has not been as reproducible in other centers.

Factors that predict a favorable outcome after resection of superior sulcus tumors include R0 resection, absence of N2 or N3 metastases,⁵ lobectomy rather than limited pulmonary resection,⁶ and a complete pathologic response after induction chemoradiotherapy.^7,8 Surprisingly, tumor stage (T3 vs. T4 status) may be less important prognostically in this subset of patients; in the Intergroup 0160 study, this criterion was not a significant determinant of survival. The need for vertebral or subclavian vessel resection should not be considered an absolute contraindication to surgical treatment. Fadel et al.⁹ reported 5-year survival rates after resection of 36% in the presence of subclavian artery invasion.

Limited survival benefit occurs with surgical resection alone. Local recurrences are common and extremely debilitating in terms of pain and limb function. Even with induction radiotherapy, complete resection is achieved in only 60% of patients, and overall 5-year survival is no better than 30%. Resectability, local control, and long-term survival have been positively affected by the addition of concurrent chemotherapy, as demonstrated by the long-term results of the phase II multicenter Intergroup 0160 trial.² Two cycles of chemotherapy (i.e., cisplatin and etoposide) concurrent with 45 Gy of radiation to the primary tumor, followed by surgical resection 3 to 5 weeks later, with two adjuvant cycles of chemotherapy was well tolerated in 110 patients. This regimen resulted in R0 resection rates of 94% for T3 lesions, 96% for T4 lesions, an overall complete pathologic response rate of 56%, and 5-year survival of 44% (54% for R0 resection). Relapse occurred predominantly in the brain, with local failure in only 10 patients, a significant pattern shift in this disease. Ongoing questions exist about the optimal dose of radiation; our group⁸ has used higher radiation doses (median dose 56 Gy) with good tolerance and concomitant increased rates of complete pathologic response. Ideally, higher-dose regimens should be studied in a multicenter study protocol to make sure that these excellent results are generalizable.

Most superior sulcus tumors are approached posteriorly through a posterolateral thoracotomy extending up to the base of the neck, which is appropriate for posteriorly located tumors (Shaw–Paulson posterior approach). Exposure of tumors above the thoracic inlet is suboptimal with a posterior approach, however, and this may explain why there have been incomplete resections in the past. The anterior approach of Dartevelle is preferable for more anteriorly and superiorly located tumors because it provides better access to the subclavian vessels and other cervical structures. Many surgeons favor an anterior exposure when there is a palpable supraclavicular mass, clinical involvement of the C7 or C8 nerve root, Horner syndrome, proven or suspected vascular invasion, or any involvement of the thoracic inlet (or Sibson fascia) and structures superior to it.¹⁰ It is important to be familiar with both the anterior and posterior exposures to permit maximum flexibility while operating.

Given the magnitude of the surgical resections, especially following concurrent chemoradiation, it is important to select patients with satisfactory performance status, as well as adequate cardiac, pulmonary, and renal function (especially for platinum-based regimens). Smoking cessation is also critical. Marginal respiratory status in conjunction with pulmonary and chest wall resection increases perioperative risk. Careful neurologic assessment is critical to determine the extent of brachial plexus involvement. Any neurologic dysfunction higher than the lower trunk of the plexus is likely to lead to significant limb dysfunction after resection; in some rare cases, forequarter amputation may be considered a better palliative option.^11,12 In addition, long-track neurologic symptoms may indicate extensive spinal cord involvement owing to vertebral invasion.

Initial assessment is similar to that for any lung cancer resection. Tissue is almost always obtainable by transthoracic needle aspiration.¹³ Of note, tuberculosis and lymphoma have been reported to mimic Pancoast tumors. Tissue diagnosis therefore is critical before commencing multimodality therapy. In addition to chest and upper abdomen CT scanning and CT/PET, it is often helpful to include a neck CT scan to better image the thoracic inlet. To better delineate involvement of the brachial plexus, subclavian vessels, vertebral bodies, or neural foramina, MRI with contrast enhancement is the preferred imaging modality for this region. Involvement of the lower trunks of the brachial plexus may be considered a contraindication to resection because of limb dysfunction; however, resection of the T1 and C8 nerve roots can be easily accomplished. Brain imaging, using CT scanning or MRI, is also recommended as part of a thorough metastatic assessment. Extrathoracic metastases or persistent N2 or N3 disease after induction therapy is considered an absolute oncologic contraindication by most. It is critical to perform a thorough mediastinoscopic evaluation as part of the initial workup¹⁴ or after induction chemoradiation.⁸ If persistent postoperative N2 or N3 disease is documented, surgery should be attempted when it is the only satisfactory way to palliate pain because cure cannot be achieved.¹⁵

Extensive involvement of the subclavian and carotid arteries is not an absolute contraindication to resection (Table 80-1). Doppler ultrasound of the neck vessels and great vessels, including the vertebral artery, is helpful not only for assessment of tumor invasion but also to look for atherosclerotic changes that may affect clamp placement or critical stenosis.¹⁵ Careful neurologic examination and, in some cases, electromyography can help to define brachial plexus involvement, phrenic nerve involvement, and cord involvement. Preoperative neurosurgical consultation is highly recommended if there is any question of brachial plexus involvement or vertebral invasion; a team approach can be very useful intraoperatively (Table 80-2).

Clinical Presentation

Most patients present with shoulder and elbow pain because of involvement of the lower trunk of the brachial plexus. The discomfort often follows the distribution of the ulnar nerve because of malignant invasion of T1 and C8 nerve roots and extension into the parietal pleura and first rib.¹⁶ Weakness and atrophy of the intrinsic muscles in the hand, along with pain and paresthesias in the medial aspect of the arm and fourth and fifth digits (distribution of the ulnar nerve), sometimes associated with a loss of the triceps reflex, also are caused by C8 and T1 nerve root involvement. Pain may radiate into the neck and head and posteriorly into the scapular area or anteriorly into the chest (Fig. 80-2).

Classically, the patient presents holding the elbow with the opposite arm to support the shoulder and take the pressure off the brachial plexus for symptomatic relief (Fig. 80-3).^16,17 Frequently, the diagnosis is missed because of concentration on cervical osteoarthritis, discs, or other differential diagnoses, often delaying recognition of the true etiology. Horner syndrome classically presents as an ipsilateral ptosis, with narrowing of the palpebral fissure, miosis, and anhidrosis. It is produced by involvement of the sympathetic chain in the area of C7 and C8, the upper two-thirds of the stellate ganglion (Fig. 80-4).¹⁸ Vertebral involvement and spinal cord compression with paralysis (paraplegia) are observed occasionally. Phrenic or recurrent laryngeal nerve invasion is present infrequently, producing diaphragmatic paralysis or hoarseness. Superior vena cava syndrome may result if anterior tumors are present. This syndrome leads to swelling of the face and distention of the neck and upper chest wall veins. Primary pulmonary tumors also may produce the usual symptoms of cough, hemoptysis, dyspnea, wheeze, and weight loss.

Radiographic Findings

Chest roentgenographs (posteroanterior and lateral) are the simplest methods of discerning an apical mass (Fig. 80-5A). Apical lordotic chest views are valuable after the screening procedure. CT scan of the chest provides additional information, particularly about bone invasion (including the first rib) and vertebral involvement (Fig. 80-5B). It also may be used to delineate lung and liver metastases. MRI is particularly helpful in soft tissue areas, such as invasion of the brachial plexus, vascular structures, and chest wall, as well as lymph node metastases in the mediastinum (Fig. 80-5C).¹⁹

Diagnosis Tests

The definitive diagnosis is established by a transthoracic needle biopsy, usually through the supraclavicular space or the posterosuperior chest between the scapula and spine. These small needles are guided by fluoroscopy, ultrasound, or CT in most cases. The first description of transcervical biopsy via the supraclavicular approach was reported by McGoon ²⁰ in 1964. Biopsy may be performed under local or general anesthesia. The diagnostic yield for needle biopsy is greater than 90%. Diagnostic yield from sputum cytology is less than 20%, and for bronchoscopy (fiberoptic or rigid), it is less than 30%.²¹ The diagnostic yield of these tests is low because most of these tumors are peripheral.

Staging and Perioperative Assessment

Cervical mediastinal lymph node exploration is necessary before treatment in these patients to establish whether the lymph nodes are positive. The suggestion of enlarged nodes on either the CT scan or MRI may be helpful, but the staging of actual metastases is critical.²² False positive and false negatives occur frequently and often only supraclavicular lymph nodes are involved. If the mediastinal nodes are positive for a right upper lobe lesion, it is still treated as an operable case because the lymph nodes are assumed to be “regional.” Metastasis to the contralateral mediastinal lymph nodes is a poor prognosticator and surgical therapy is less likely to be successful. Mediastinal pathologic staging is mandatory in these patients and can be achieved using TBNA/EBUS/VATS or routine mediastinoscopy. The timing of staging can be either at the time of initiation of induction therapy or after completion of neoadjuvant chemoradiation in order to decide whether to proceed if residual positive lymph nodes are found. Our current approach is sample the lymph node by needle and then use surgical restaging prior to resection (where we will not resect if there are persistent positive mediastinal lymph nodes).

Although invasion of the vertebral body (T4) demonstrated by CT usually renders a patient inoperable (because “no reported cures” have resulted with vertebral involvement in our experience¹⁹); recent reports from the French groups have suggested possible cures even in these cases. Distant metastases are suspected by history and physical examination, as well as retroperitoneum, liver, and adrenal glands. These lesions should be biopsied and metastasis confirmed before a decision to proceed with aggressive therapy is made. Cell types encountered are predominantly squamous cell carcinoma, with large cell the second, and adenocarcinoma the third most commonly observed.²³ Many begin as so-called “scar” carcinomas or are secondary to other malignancies.^24–28 Metastatic carcinoma from other organs may produce similar symptoms in this area. Various other etiologies include benign tumors and infections such as actinomycosis, tuberculosis, Allescheria infection, cryptococcosis, and hydatid cyst.^29–36 Vascular aneurysms³⁷ and amyloidosis³⁸ also may produce the Pancoast syndrome.

Differential Diagnosis

Differential diagnosis includes thoracic outlet syndrome (TOS) that may mimic the symptoms of ulnar paresthesias and pain. First rib resection has been carried out mistakenly for TOS in patients with superior sulcus tumor of the lung.¹⁶ Vascular, esophageal, and cardiac disease also can mimic symptoms of superior pulmonary sulcus tumors, and these areas should be ruled out in the differential diagnosis.¹⁶

Indications for Surgery

If the patient has a tumor in the area of the superior pulmonary sulcus with or without rib involvement and with or without lower brachial plexus involvement, and it is staged as a T3N0 or N1, he or she is operable. N2 disease is operable if it is in the upper lobe and the mediastinal nodes are considered to be ipsilateral metastases. Involvement of the vena cava and subclavian artery or vein is not an absolute contraindication for surgery. These patients should undergo neoadjuvant chemoradiation followed by reassessment of the extent of disease prior to planned resection.

In addition to chest and upper abdomen CT scanning and CT/PET, it is often helpful to include a neck CT scan to better image the thoracic inlet. To better delineate involvement of the brachial plexus, subclavian vessels, vertebral bodies, or neural foramina, MRI with contrast enhancement is the preferred imaging modality for this region. Involvement of the lower trunks of the brachial plexus may be considered a contraindication to resection because of limb dysfunction; however, resection of the T1 and C8 nerve roots can be easily accomplished. Brain imaging, using CT scanning or MRI, is also recommended as part of a thorough metastatic assessment.

Extrathoracic metastases or persistent N2 or N3 disease after induction therapy is considered an absolute oncologic contraindication by most. It is critical to perform a thorough mediastinoscopic evaluation as part of the initial workup¹¹ or after induction chemoradiation.⁵ If persistent postoperative induction N2 or N3 disease is documented, surgery should be attempted when it is the only satisfactory way to palliate pain because cure cannot be achieved.¹²

Although vertebral involvement traditionally has been a contraindication for surgical resection of superior sulcus carcinoma, recent advances in spinal instrumentation have permitted a more complete resection of vertebral body tumor. Gandhi et al. ³⁹ (Garrett Walsh & Associates at MD Anderson) have published good results in 17 patients with vertebral resection of carcinoma extension. Contraindications include extensive involvement of the brachial plexus, mediastinal perinodal involvement, significant invasion of the soft tissues of the neck, and distant metastasis. Palliative resection is performed occasionally for intractable pain.¹⁹ Recent reports by Dartevelle et al.^40,41 and Grunenwald et al.⁴² suggest a role for extensive resection with good outcomes in selected patients.

Preoperative Radiotherapy Followed by Surgery

After preoperative radiotherapy (3000 rads delivered over 2–3 weeks) or chemoradiation followed by a 4-week waiting period, surgical extirpation with an en bloc resection of the pulmonary tumor, chest wall, lower brachial plexus, and vertebrae through the posterior thoracoplasty approach is performed. The en bloc resection of the pulmonary tumor and chest wall is accompanied by resection of the sympathetic chain, the lower trunk of the brachial plexus in most cases (T1 nerve root in most cases; C8 nerve root less frequently), and rarely, the subclavian artery with an interposed graft. A margin of vertebral body is removed with most tumors. A segmentectomy, subsegmental resection, lobectomy, or pneumonectomy is performed to complete the en bloc dissection, although sublobar resections have been reported by some to have a negative impact on local control and long-term survival. Chest wall replacement is required occasionally for anterior tumors but usually not for those lying under the scapula. If six or more ribs are taken, posterior reconstruction with Marlex or other synthetic material is important to keep the scapula from sticking inside the chest.⁴³

The anterior cervical approach championed by Dartevelle et al.⁴¹ involves a median sternotomy and cervical resection of the clavicle, as well as en bloc resection of the artery, often the vein, and the tumor.

Chemotherapy and/or Chemoradiation

Induction chemotherapy combined with radiation has markedly improved the treatment of superior sulcus tumors. Wright et al.⁴⁴ from Massachusetts General Hospital reported significant improvement in complete resection rate, pathologic response, 2- and 4-year survival, and reduction of local recurrence with CT/radiation induction therapy over induction radiation therapy alone in over 30 patients. Since then, they have treated 15 more patients (total 30), and there have been two distant recurrences. The 5-year survival approaches 50%.

The Southwest Oncology Group reported less good results with combination chemo/radiation induction therapy, but this was a multicenter study in contrast to the preceding study.⁴⁵ Recently, Kwong et al.⁸ have reported on excellent response rates and long-term survival in a single institution study of neoadjuvant chemoradiation including patients presenting with N2 disease.

Shaw-Posterior Surgical Technique

Routine measures for lung resection should be undertaken, such as use of preoperative antibiotics, deep vein thrombosis prophylaxis, and a double-lumen endotracheal tube. Central venous line placement is prudent for reliable IV access and central venous pressure monitoring and in most patients should be placed on the contralateral side to keep the line out of the surgical field. Radial arterial pressure monitoring is also recommended and also should be placed on the nonoperative side in case subclavian artery manipulation is required. It is also wise to coordinate surgical scheduling with a spine specialist (neurosurgeon of orthopedic) for backup in case of vertebral body or other neurologic involvement.

After induction of general anesthesia, the patient is intubated with a double-lumen endotracheal tube. The patient is placed in the lateral decubitus position with an axillary roll under the “down” side (Fig. 80-6). The incision begins above the angle of the scapula, halfway between it and the spinous processes (i.e., thoracoplasty technique), and extends inferiorly, angling anteriorly around the tip of the scapula. The subcutaneous tissue is divided, followed by trapezius and rhomboid muscles. Although we generally try to spare the posterior superior serratus muscle, occasionally, this too needs to be divided to allow adequate exposure.

The intercostal muscle overlying the fourth rib is incised. A Finochietto retractor is placed between the top of the fourth rib and the scapula superiorly. Since double-lumen intubation is used for the operation, the lung is already collapsed. The fourth interspace is opened. Alternatively, this can be done using the cautery. The surgeon places a hand in the patient's chest to palpate the tumor and determine its extent, the number of ribs involved, and the length of each rib to be resected (Fig. 80-7). If the tumor is large, a lower interspace may be used. If possible we generally try to preserve the intercostal muscle flap thus developed, to use for later reinforcement of the airway stump (especially after induction therapy). Anteriorly, the ribs are divided with the rib shears after ligating, dividing, or clipping the neurovascular bundle under each rib. The dissection is carried up to and through the first rib. Posteriorly, the ribs are sheared off with an osteotome, taking the rib at the level of the transverse processes, disarticulating the ribs or taking a small segment of vertebrae, if necessary. The intercostal bundles may be cauterized or clipped. This is carried through the third, second, and first ribs. Patients with CT evidence of tumor invading the vertebrae are generally considered inoperable. However, if at operation the tumor is found to lie adjacent to the vertebrae, a margin of vertebrae is taken with the osteotome. Preparation by involvement of a neurosurgical or orthopedic team may be prudent in this situation.

After the first rib is cut anteriorly and posteriorly, the surgeon inserts the index finger from one hand in the front and the index finger from the other hand from the back to palpate the tumor (Fig. 80-8) and identify its relationship to the T1 and C8 nerve roots, the lower trunk of the brachial plexus, and the axillary subclavian artery and vein (Fig. 80-9). The scalenus anticus and medius muscles are divided with the finger holding the en bloc section anteriorly and inferiorly. Caution is taken to avoid injury to the artery or vein. The T1 nerve root is divided posteriorly, and the segment is lifted up with the tumor. The C8 nerve root is visualized and may be divided if necessary. The anterior part of the T1 nerve root is divided. The subclavian artery is dissected from the tumor. If the artery is involved, an interposition graft, such as autogenous saphenous vein, is used. This is usually not the case because the adventitia protects the artery from tumor invasion.

A lobectomy optimally is performed after the en bloc chest wall resection. Segmental resection of the lung can considered if the patient is very high risk or no residual tumor is found. In general, these patients have had higher incidence of local recurrences. The chest wall is closed with Marlex if anterior in location. For posterior tumors, however, the scapula covers the posterior area, and usually no chest wall reconstruction is necessary (Fig. 80-10). If the fifth rib is removed, the scapula tip may get hooked under the sixth rib. If it appears that this may be a possibility, the tip of the scapula can be excised (Fig. 80-11). The wound is closed in layers with interrupted 0 Nurolon sutures in a figure-of-eight fashion (Tom Jones stitch), running 2-0 Vicryl in the subcutaneous tissues, and skin clips in the skin.

Dartevelle Transclavicular Technique

For the anterior approach as described by Dartevelle et al.,⁴¹ the patient is positioned supine with the neck hyperextended and turned away from the tumor. A rolled towel behind the shoulders helps with exposure of the operative site.⁴⁶ The arms can be tucked at the sides, but it may be wise to leave access to the anterolateral chest on the operative side in case an anterolateral thoracotomy is necessary. The patient should be sterilely prepared from the angle of the mandible to below the costal margin and from the midclavicular line of the contralateral chest to the midaxillary line on the side of the tumor and beyond the shoulder superiorly. An L-shaped incision is performed along the anterior border of the sternocleidomastoid muscle, extending horizontally a few centimeters below and parallel to the clavicle into the deltopectoral groove (Fig. 80-12). Depending on the planned area of entry into the thoracic cavity, this transverse incision can be placed over the second, third, or fourth intercostal space.

The sternal attachments of the sternocleidomastoid muscles are divided, as are the upper digitations of the pectoral muscle on the clavicle; a myocutaneous flap now can be pulled back to expose the thoracic inlet (Figs. 80-13 and 80-14). The medial half of the clavicle is removed (the sternal or Gigli saw works well for this). The omohyoid is divided, if necessary, and the scalene fat pad is removed and checked for metastases. The subclavian vein and its branches, as well as the distal internal jugular vein (depending on the cephalad extent of tumor), are dissected and controlled proximally and distally. On the left it is often necessary to ligate the thoracic duct as it enters the vein. In general, veins should be resected and not reconstructed, realizing that the patient may have edema in that extremity, which can be managed with arm elevation and compression garments. As collaterals develop, the end result is usually not significantly morbid. It can be helpful to divide the anterior, external, and even internal jugular vein to facilitate mobilization and resection of the subclavian vein.

The pleural cavity is entered one interspace below the tumor to assess its intrathoracic extent. Next, the anterior scalene muscle can be divided at the first rib, unless it is grossly invaded, in which case it is better to divide it as proximally as possible, taking care to preserve the phrenic nerve (Fig. 80-15). This is followed by dissection of the subclavian artery and its branches, which all can be divided to facilitate mobilization. The exception is that the vertebral artery should be preserved when possible, but if it is invaded by tumor and there is no significant extracranial carotid vascular disease by preoperative duplex study, it should be taken en bloc with the tumor. If it is not possible to free the tumor from the subclavian artery in a subadventitial plane, then preparations should be made to resect and reconstruct it (see below). Next, the middle scalene muscle is taken as high as necessary to better expose the brachial plexus. It may be helpful to have the neurosurgical team assist with neurolysis of the plexus. Nerve roots can be divided but should not be taken higher than C8 (see Fig. 80-15, inset). It is important to ligate the roots to avoid a cerebrospinal fluid leak. If necessary for an R0 resection, the prevertebral muscles along with the paravertebral sympathetic chain and stellate ganglion can be resected safely as well. Many of these patients will have preexisting Horner syndrome, but if not, this possibility should be mentioned when obtaining informed written consent for the operation.

At this point, the first rib can be divided at the transverse process posteriorly and a few centimeters anterior to the tumor or at the costosternal junction. The second and third ribs also can be resected en bloc with the tumor as needed. This provides an entry point into the pleural space through which the upper lobectomy can be performed. In the past, an accessory anterior or in some cases posterolateral thoracotomy (after repositioning and reprepping the patient) has been made, but with videothoracoscopy assistance, and use of long thoracoscopic instruments and staplers, the additional incisions are less often necessary.

Osteomuscular-Sparing Approach

This technique differs from the above-described operation in that the sternoclavicular joint is preserved. The same skin incision is made, and the sternocleidomastoid is mobilized, but the pectoral muscle is split along the fibers a few centimeters below the clavicle rather than separating it from the clavicle (Fig. 80-16). An L-shaped incision is made in the manubrium with the sternal saw to release the upper outer corner adjacent to the sternoclavicular joint. The proximal internal mammary artery is ligated, and the first costal cartilage is resected. Now the clavicle, with attached pectoral and sternocleidomastoid muscles, can be elevated as an “osteomuscular flap” (Fig. 80-17). The remainder of the resection is carried out as described earlier. For closure, the manubrium is reapproximated with two sternal wires. Aesthetic and functional results are reportedly superior to those of claviculectomy owing to preservation of the shoulder girdle architecture. The negative aspects of this technique are again the suboptimal exposure for lung resection and the fact that the vascular dissection deep to the scalene muscles can be more challenging than with the standard Dartevelle incision.⁴⁶

Hemiclamshell or Trapdoor Incision

The hemiclamshell or trapdoor incision (when extended above the clavicle or along the sternocleidomastoid) was proposed originally for trauma to the great vessels or for mediastinal tumors. It provides excellent exposure of the anterior mediastinum and chest apex and has been used with some success for superior sulcus tumors as well. The basic incision consists of a median sternotomy down to the fourth interspace with lateral extension through the intercostals (Fig. 80-18). A standard sternal retractor then may be used to elevate the sternum, or a mammary retractor can be helpful to elevate sternal and intercostal aspects of the incision. Several modifications have been suggested, including extension along the sternocleidomastoid or superior to the clavicle. In this case, the mammary artery should be ligated proximally. Some surgeons recommend resection of the medial clavicle, as in the Dartevelle approach.⁴⁶ Another alternative is to resect the first costal cartilage and costoclavicular ligament to preserve the architecture of the shoulder girdle while allowing improved mobility of the anterior chest wall and better exposure and control of the distal subclavian vessels.⁴⁷ The incision is closed by wiring the sternum, reapproximating the intercostal space, and then suturing the pectoral muscles if disturbed during the dissection. A major advantage to this incision is better exposure of the pulmonary hilum. However, the posterior aspect of the thoracic inlet is difficult to dissect with this technique; also, the incision maybe excessive for a smaller, anterior, truly apical tumor.

Vascular Resection

Before deciding on the need for vascular resection, the artery should be properly exposed. The vein should be mobilized as described earlier and divided proximal and distal to the tumor if invaded. Next, the artery should be prepared for proximal and distal control by dividing the anterior scalene muscle, preserving the phrenic nerve if not invaded by tumor. The internal mammary artery and ascending cervical artery are divided; the vertebral artery is sacrificed if involved or if the adjacent subclavian artery is involved. In many cases, the tumor can be dissected away from the subclavian artery in the subadventitial plane (Fig. 80-19A). If the media of the artery has been invaded by tumor, steps should be taken for resection (see Fig. 80-19B). Systemic heparinization should be performed, usually with 5000 units of IV heparin. Then the artery can be clamped proximally and distally to permit en bloc resection of the involved portion with the tumor. Reconstruction should be delayed until the rest of the tumor resection is performed. In some cases, it may be helpful to generously wedge the tumor-bearing portion of the upper lobe to be removed with attached ribs and vascular structures so that the vascular reconstruction can be completed immediately, and the heparin then can be reversed. In this way, the completion lobectomy can be performed off heparin. Another option is to give heparin, clamp the artery, complete all the resection en bloc, and then perform the vascular reconstruction, but the vessels will be clamped for a longer period of time.

Reconstruction often can be end-to-end because the distance to traverse is diminished after first rib resection. Otherwise, the material of choice for vascular reconstruction is ringed polytetrafluoroethylene (6 or 8 mm) with end-to-end anastomoses, followed by reversal of heparin with protamine. In the series reported by Fadel et al. ⁹, the graft length was 1.5 to 4 cm. Shunts were not used. There is no need to place a tissue flap between the vascular graft and the lung. Artery ligation is not an option; if all collaterals are divided during tumor resection and mobilization of the artery, limb ischemia will occur.

Postoperative Care

Postoperative care is similar to that of any lung resection. With extensive chest wall resection, atelectasis is more common.⁴⁵ Good postoperative analgesia, adequate pleural drainage, and aggressive pulmonary toilet cannot be overemphasized. Routine mechanical ventilatory support is not necessary. Special attention must be paid to the involved extremity when vascular resection is required, with hourly vascular checks initially. Some surgeons recommend IV heparinization within 4 to 6 hours postoperatively, and then aspirin, once the patient is ambulatory and continued for 6 months postoperatively.⁴⁶ When concomitant venous ligation is necessary, it can be challenging to assess the perfusion of the extremity, and frequent Doppler checks may be reassuring. Arm elevation and lymphatic massage may help to alleviate edema. Wound healing can be more of a problem when extensive collaterals are ligated along the subclavian artery; diligence for this is encouraged, with aggressive debridement if wound necrosis occurs. When the clavicle has been divided and rewired, an arm sling for stabilization for 4 to 6 weeks postoperatively is recommended.

After arterial resection, follow-up duplex studies should be carried out at 3 and 6 months and annually thereafter. In addition, the blood pressure should be measured in both upper extremities at each follow-up visit. If symptoms of arterial insufficiency occur or duplex study suggests significant stenosis (>80%), angiography is recommended.⁹ In case of graft occlusion (most often from radiation fibrosis), it may not require intervention in the absence of symptoms. Reported 5-year patency rates are 85%.⁷

Surgery

Surgical morbidity includes bleeding, atelectasis, infection, thromboembolism, persistent air leak, empyema, spinal fluid leak with pneumoencephalogram and meningitis, chylothorax, ulnar nerve paresis or paralysis, and Horner syndrome not present preoperatively.⁴⁸ Vascular issues mentioned earlier are unique to this subset of patients. Acute graft thrombosis is a possibility but occurs rarely.

Unusual neurologic sequelae deserve mention. Because of resection or dissection near nerve roots, several unusual problems may occur in the postoperative period, including meningitis, cerebrospinal fluid leaks, and even tension pneumocephalus.⁴⁹ This is usually related to nerve root division or dissection near the dural sac in cases of vertebral body invasion. Often the cerebrospinal fluid leak is visible in the operating room; careful closure of the leak with fine monofilament suture, buttressed with a soft tissue flap such as intercostal muscle, is usually effective. If the leak is detected postoperatively, a lumbar drain will be required, which confines the patient to bed in the supine position. This is less than ideal in a patient needing vigorous pulmonary toilet.⁵⁰ Subarachnoid-pleural fistula has been reported acutely or subacutely when a pulmonary parenchymal air leak communicates with the subarachnoid space.^49,50 Patients may present with altered mental status, seizures, or hyponatremia, and this may mimic the clinical presentation of cerebral metastases. In one patient, reoperation with tissue flap coverage of the leaks was required; in another, expectant management was satisfactory.

Other neurologic sequelae include weakness of intrinsic muscles of the hand after T1 nerve root division, but the hand is usually still functional. When C8 or the lower trunk of the brachial plexus must be divided, permanent paralysis of intrinsic muscles of the hand should be expected.³¹ Interestingly enough, taking T1 or even T2 does not seem to produce much of a clinical problem, and even C8 does not give the usual severe problems of ulnar plexus injuries. Possibly this is so because the slow growth of the tumor permits other nerve roots to assume function. Surgical morbidity is 38%, and mortality is between 5% and 10%.^51,52

Irradiation Therapy

Adverse effects of irradiation therapy include skin fibrosis, fatigue, esophagitis, radiation pneumonitis, pulmonary fibrosis, myelitis, and brachial neuritis, all of which may be extremely devastating to the patient.⁵³

Chemotherapy

Complications of chemotherapy include myelosuppression, increased risk of bleeding and infection, peripheral or central neuropathy, renal insufficiency, mucositis, nausea, vomiting, diarrhea, and hypersensitive reaction to secondary malignancies.⁵⁴

Recurrence

There is a significant risk of local or regional recurrence and distant metastases following treatment of superior sulcus tumors, just as there is for any bronchogenic carcinoma. Brain metastasis is one of the most common in younger patients with large cell and adenocarcinoma.⁵⁵

Pancoast syndrome is a collection of characteristic symptoms and signs that includes shoulder and arm pain in a specific dermatomal distribution, Horner syndrome, and weakness and atrophy of the muscles of the hand, most commonly caused by extension of an apical lung tumor located at the superior thoracic inlet. Although most cases are the result of bronchogenic carcinoma, other neoplastic and nonneoplastic causes exist, and a definitive histologic diagnosis should be sought before consideration of treatment options. Treatment should be attempted after careful evaluation of the extent of the disease and the underlying medical status.

The most effective treatment of Pancoast syndrome due to bronchogenic carcinoma is clearly preoperative irradiation (3000 rads) combined with extended en bloc surgical resection. Five-year survival for N0 stage I disease is 35%. The exact role of adjuvant and neoadjuvant systemic chemotherapy is not established at this time. Preliminary reports with preoperative chemoradiotherapy followed by surgical resection show that this approach is feasible and may be associated with similar survival. Whenever possible, patients with Pancoast tumors should be enrolled in prospective clinical trials so that we can add to our knowledge about this disease and determine the most effective and optimal therapy.

Understanding of the anatomy of the thoracic inlet has led to novel surgical approaches to superior sulcus tumors. Many technical challenges have been overcome, making R0 resection feasible in patients with tumors anterior and superior within the thoracic inlet that previously had been deemed unresectable. Several modifications to Dartevelle technique have either facilitated exposure or improved functional or cosmetic results. The latest data on trimodality therapy in patients with Pancoast–Tobias tumors have further extended the likelihood of prolonged survival. Further refinement of surgical technique, it is hoped, will continue to improve longevity and minimize the morbidity associated with resection.

A 55-year-old white woman with a history of smoking and a cough presented with left-sided shoulder pain. The patient developed numbness, tingling, and discoloration of the left fourth and fifth digits. Chest x-ray was positive for a lesion along the anterior apical superior sulcus with a shadow between the first and second ribs. A CT scan was positive for a tumor that appeared to be invading the first, second, and third ribs, and was questionably involving the subclavian artery and vein and the lower trunk of the brachial plexus. This was followed by MRI, which showed nerve root involvement at T1 with possible involvement of vertebral bodies C6–8. The edge of the subclavian artery was clear, and the edge of the subclavian vein was not.

The patient underwent a percutaneous needle biopsy that was positive for NSCLC. A PET scan was positive for a tumor in the lung and the chest wall with questionable mediastinal lymph nodes. The patient underwent a transbronchial needle aspiration of the paratracheal lymph nodes on the left side, and these were positive for metastatic NSCLC, and the patient was referred for neoadjuvant chemotherapy with carboplatin and taxol with radiation therapy concurrently at 61.2 Gy with a spinal cord dose at 45 Gy. Six weeks after treatment, the patient had repeat CT and PET scans. These both showed shrinkage of the tumor and no uptake in the mediastinum and decreased uptake in the tumor. An MRI of the brain at that time was negative, and the MRI of the chest still showed some questionable involvement of subclavian vessels and the lower trunk of the brachial plexus. The patient underwent a planned bronchoscopy and mediastinoscopy, which was negative for any evidence of persistent mediastinal nodal disease. The patient was explored starting with a left-sided anterior Dartevelle approach. Sparing the clavicle, the T1 nerve root was divided and the first rib was cut anteriorly. The subclavian artery was mobilized successfully without any tumor involvement. However, division of the subclavian vein was necessary. After this was done and full mobilization was achieved, the patient was repositioned in the lateral decubitus position, and the standard posterior Shaw approach was used for resection of the tumor and en bloc chest wall resection of ribs 1, 2, and 3. The chest then was entered from the fourth intercostal space, and a left upper lobectomy with mediastinal lymph dissection was performed. All lymph nodes were negative. The patient had a complete pathologic response on final pathology. An intercostal muscle flap, harvested at the time of posterior chest entry, was placed at the bronchial stump. Postoperatively, the patient developed upper extremity edema, as expected with vein ligation, and this was treated with Jobst stockings and arm elevation.

This chapter described with my coauthor, Hal Urschel, one of the world's experts in this field who, sadly, passed this year, provides an overview of superior sulcus tumors both from an oncological and technical perspective. Although generally treated with a combination of radiation and surgery, we currently routinely approach these lesions with neoadjuvant chemoradiation followed by surgical resection. After the standard posterior Shaw– Paulson approach is described, the anterior approach is noted. This is especially useful for patients with Pancoast tumors that involve the anterior chest wall and/or the anterior vessels. By using either a classic Dartevelle approach or a modified anterior “hemiclamshell,” one can gain excellent access to the upper lobes, sternum, ribs, and vena cava as necessary. We have found that by modifying the location of the incision one can either perform a separate thoracotomy posteriorly or remove the lobe from the same anterior incision.

Mrs. Rachel Montano is to be highly commended for her dedication and commitment to the completion of this chapter.