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Anterior Approach to Superior Sulcus Tumors

      The anatomy of the thoracic inlet is an important determinant of the radiographic appearance and clinical syndrome of superior sulcus tumors. The classic superior sulcus tumor is located sufficiently cephalad in the thorax that Henry Pancoast originally suspected a tumor of cervical origin.
      • Pancoast H.K.
      Importance of careful roentgen-ray investigations of apical chest tumours.
      As a radiologist, he noted the difficulty in detecting the tumor on a plain chest radiograph. Subsequently, both Pancoast
      • Pancoast H.K.
      Superior pulmonary sulcus tumor.
      and Tobias
      • Tobias J.W.
      Sindrome apico-costo-vertebral doloroso por tumour apexiano su valor diagnostico en el cancer primitivo pulmonar.
      recognized that the tumor was of pulmonary origin. In 1932, Pancoast elucidated his syndrome of arm pain, Horner’s syndrome, and a superior sulcus tumor.
      • Pancoast H.K.
      Superior pulmonary sulcus tumor.
      Before the development of contemporary scanning technology, the clinical syndrome was an important consideration in establishing a diagnosis of superior sulcus tumor. Patients with superior sulcus tumors commonly complain of pain and eventually weakness and numbness in the ipsilateral arm. The pain begins in the shoulder and scapular region before migrating down the ulnar aspect of the arm (T1 dermatome) and into the fourth and fifth digits of the hand (C8 dermatome). In a typical patient, prolonged involvement of the nerves results in atrophy of the muscles supplied by these dermatomes. In approximately 20% of patients, the tumor involves the sympathetic chain and the stellate ganglion resulting in Horner’s syndrome (pstosis, miosis, and hemianhydrosis).
      The radiographic appearance of superior sulcus tumors is often a subtle apical “cap” on frontal chest radiographs. Careful examination may reveal bony destruction of the first rib or vertebral body. Contemporary radiographic evaluation includes chest computed tomography and magnetic resonance imaging scanning. The preoperative evaluation, frequently involving PET scanning as well, establishes tumor presence and defines the extent of neural, bony, and vascular involvement. Although the cellular biology of superior sulcus tumors is likely similar to other non-small-cell carcinomas of the lung, the location of the tumor leads to advanced staging in most cases. Tumor involvement of the vertebral bodies (T4) or subclavian vessels (T4) is reflected in advanced stage (IIIB) and diminished survival.
      • Rusch V.W.
      • Parekh K.R.
      • Leon L.
      • et al.
      Factors determining outcome after surgical resection of T3 and T4 lung cancers of the superior sulcus.
      Several excellent reviews of superior sulcus tumor staging approaches and survival data have been published.
      • Dartevelle P.
      • Macchiarini P.
      Surgical management of superior sulcus tumors.
      • Detterbeck F.C.
      Pancoast (superior sulcus) tumors.
      • Pitz C.C.
      • de la Riviere A.B.
      • van Swieten H.A.
      • et al.
      Surgical treatment of Pancoast tumours.
      The anatomic relationships in the thoracic inlet determine the surgical approach to superior sulcus tumors. The companion article describes the posterior “Paulson–Shaw”
      • Paulson D.L.
      Carcinomas in the superior pulmonary sulcus.
      approach to superior sulcus tumors. This approach is effectively used in bulky posterior tumors without vascular involvement. The posterior approach, however, is limited in its exposure to the anterior portions of the thoracic inlet. In particular, there is limited exposure when the subclavian vessels are involved.

      Operative Technique

      Figure thumbnail grr1
      Figure 1Pancoast described the superior sulcus tumor syndrome as “characterized clinically by pain around the shoulder and down the arm, Horner’s syndrome, atrophy of the muscles of the hand and presented roentgenographic evidences of a small homogeneous shadow at the extreme apex, always more or less local rib destruction and often vertebral infiltration.”
      • Pancoast H.K.
      Superior pulmonary sulcus tumor.
      Figure thumbnail grr2
      Figure 2Case 3 in Pancoast’s original report on apical chest tumors.
      • Pancoast H.K.
      Importance of careful roentgen-ray investigations of apical chest tumours.
      The patient presented with shoulder pain that led to a shoulder radiograph (A). The apical shadow was initially overlooked. The patient’s later radiograph demonstrated a clear right apical tumor (B). A subsequent spine radiograph (C) demonstrated rib destruction. (Reprinted with permission from Pancoast HK: Importance of careful roentgen-ray investigations of apical chest tumours. J Am Med Assoc 83:1407-1411, 1924.)
      Figure thumbnail grr3
      Figure 3The surgical approach is influenced by the location of the tumor relative to the ribs, subclavian vessels, brachial plexus, and vertebral body.
      (1) Tumors near the anterior scalene muscle primarily invade the first rib and present with a pain syndrome reflecting chest wall, rather than upper extremity radicular pain. The tumor may involve the sternocleidomastoid muscule, the scalene fat pad, as well as the jugular (internal and external) and subclavian veins. The phrenic nerve is a useful anatomic reference, as well as a functional consideration. Tumor involvement of the phrenic nerve can be readily identified by ipsilateral hemidiaphragm elevation.
      (2) Tumors growing between the anterior and middle scalene muscles may invade the phrenic nerve, the subclavian artery (except the posterior scapular artery), the anterior and middle scalene muscles, and the trunks of the brachial plexus. Patients with tumors involving the phrenic nerve as well as the brachial plexus will present with an elevated hemidiaphragm as well as pain and parasthesias in the shoulder and upper arm.
      (3) Tumors located posterior to the middle scalene muscles typically lay in the costovertebral groove and involve the T1 nerve root, the posterior aspect of the subclavian and vertebral arteries, and the prevertebral muscles. Because tumors in this location commonly involve the intercostobrachial nerve as well as the superior portion of the sympathetic chain (including the stellate ganglion), patients present with a pain distribution that reflects involvement of the axilla and medial upper arm as well as Horner’s syndrome (ptosis, miosis, hemi-anhidrosis).
      Figure thumbnail grr4
      Figure 4The anterior surgical approach to Pancoast tumors is modified to optimize exposure. Depending on the location and size of the tumor, we employ variations of two basic incisions: (1) a transclavicular incision and (2) a hemi-clamshell incision with supraclavicular extension.
      The transclavicular incision is used with the patient in the supine position with the neck hyperextended and the head turned toward the uninvolved side. A bolster is placed behind the shoulder to facilitate hyperextension of the neck. The cervicotomy uses an L-shaped incision that follows the anterior border of the sternocleidomastoid muscle and the inferior border of the clavicle to the deltopectoral groove. The anterior chest-wall incision can be adjusted more caudad to accommodate the lower extent of the tumor. The skin is prepared from the mastoid process to the xyphoid process and from the midaxillary line to the contralateral midclavicular line. In early reports, the transclavicular approach included the resection of the clavicle.
      • Dartevelle P.G.
      • Chapelier A.R.
      • Macchiarini P.
      • et al.
      Anterior transcervical-thoracic approach for radical resection of lung tumors invading the thoracic inlet.
      • Macchiarini P.
      • Dartevelle P.
      • Chapelier A.
      • et al.
      Technique for resecting primary and metastatic nonbronchogenic tumors of the thoracic outlet.
      Resection of the clavicle, however, is associated with suboptimal cosmetic results and occasional functional disability. An alternative approach involves bisecting the manubrium to preserve the claviculomanubrial junction.
      • Grunenwald D.
      • Spaggiari L.
      Transmanubrial osteomuscular sparing approach for apical chest tumors.
      • Spaggiari L.
      • Calabrese L.
      • Gioacchino G.
      • et al.
      Cervico-thoracic tumors resection through transmanubrial osteomuscular sparing approach.
      Another clavicular-sparing approach is the hemi-clamshell incision.
      • Ohta M.
      • Hirabayasi H.
      • Shiono H.
      • et al.
      Hemi-clamshell approach for advanced primary lung cancer.
      The hemi-clamshell incision is used with the patient in the full lateral position with slight posterior rotation. The ipsilateral arm is abducted 90° and secured with an arm support on the posterior table rail. The patient is securely taped at the level of the iliac crest to allow ±30° axial rotation of the surgical table during the operation to approximate supine positioning during the partial sternotomy and lateral positioning during the hilar dissection. In patients requiring a supraclavicular extension, the ipsilateral arm is incorporated into the skin preparation. The arm can be variably positioned during the operation to facilitate exposure to the axilla and lateral chest wall, as well as the anterior chest and supraclavicular areas. The skin is prepared from the mastoid process to the xyphoid process and from the midback to the contralateral midclavicular line. Similar to the clavicular-sparing approach described above, involvement of the first rib requires disarticulation of the first costomanubrial junction before the lateral retraction of the sternum.
      The surgical principles of the neck dissection are similar for both the transclavicular incision and the supraclavicular extension of the hemi-clamshell incision. Because the supraclavicular extension is similar to the incision described by Mackinnon and coworkers,
      • Mackinnon S.
      • Patterson G.A.
      • Colbert S.H.
      Supraclavicular approach to first rib resection to thoracic outlet syndrome.
      this description will focus on the transcervical incision.
      Figure thumbnail grr5
      Figure 5The L-shaped incision is extended through the platysma using electrocautery. Both the sternal and the clavicular origins of the sternocleidomastoid muscle are detached from the periosteum. The muscle and soft-tissue flap is folded cephalad and secured with a traction suture. The omohyoid muscle is divided and the scalene fat pad is dissected to facilitate exposure and staging. The scalene lymph nodes, typically lying within the fad pad, can be examined for metastatic disease and a decision regarding resectability is made at this point. Alternatively, this node can be sampled at the time of staging cervical mediastinoscopy. Using the typical supraclavicular notch incision, finger dissection anterior to the jugular vein will commonly provide mediastinoscopy access to the scalene lymph node and pathologic staging before definitive surgery.
      The sequential steps of the operation involve the (1) dissection of the jugular veins, (2) dissection of the arteries, and (3) exposure of the brachial plexus.
      • Dartevelle P.G.
      • Chapelier A.R.
      • Macchiarini P.
      • et al.
      Anterior transcervical-thoracic approach for radical resection of lung tumors invading the thoracic inlet.
      The dissection of the jugular veins is necessary for adequate exposure. The branches of the subclavian vein, including the anterior, external, and internal jugular veins will commonly require ligation and division. Suture ligation of the internal jugular vein is well tolerated and should be performed to facilitate exposure to the confluence of the subclavian and innominate vein. On the left side the thoracic duct is typically ligated with care taken to avoid proximal injury to the ligated duct. Similarly, tumor involvement of the subclavian vein should be treated with resection of the vein.
      The right phrenic nerve passes inferiorly down the neck to the lateral border of anterior scalene, medially across the border of the muscle, and parallel to the internal jugular vein that lays inferomedially. At the anterior, inferomedial margin of the anterior scalene muscle, the nerve is superficial to the second part of the right subclavian artery. The phrenic nerve passes medially to cross the pleural cupola deep to the subclavian vein. More medially, it crosses the internal thoracic artery at approximately the level of the first costochondral junction. The phrenic nerve should be carefully mobilized, avoiding traction injury or thermal injury from electrocautery, and retracted away from the ongoing dissection (typically medially). Anesthetic techniques that avoid muscle relaxation will facilitate the intraoperative testing of nerve function.
      The anterior scalene muscle is divided either at its insertion on the scalene tubercle of the first rib or, if the first rib in involved with tumor, closer to its origin on the transverse processes of C3-C5. Of note, the anterior scalene muscle is poorly defined in as many as a third of patients. The anterior scalene muscle may be located behind the subclavian artery or split into two with the artery passing between the bundles. SCM = sternocleidomastoid muscle.
      Figure thumbnail grr6
      Figure 6Exposure to the subclavian artery is facilitated by the dissection of the jugular veins and divisions of the anterior scalene muscle. The subclavian artery is mobilized by dividing several branches. The vertebral artery, the first and usually the largest branch of the subclavian artery, ascends toward the transverse foramen of the C6 vertebral body. The vertebral artery is resected only with preexisting tumor-related occlusion or, rarely, after careful preoperative evaluation of potential extracranial vascular disease. Lateral to the vertebral artery is the short and thick thyrocervical trunk. The thyrocervical trunk is identifiable because it immediately branches into the inferior thyroid, suprascapular, and transverse cervical arteries. The thyrocervical trunk and its branches can be readily divided to facilitate exposure to the artery and tumor. Two additional branches of the subclavian artery can be similarly divided: the internal thoracic artery, which descends from the first portion of the subclavian artery, and the costocervical trunk, that arises from the posterior aspect of the subclavian artery. The artery is clamped and divided proximally and distally to the tumor. Subsequent to the resection of the tumor, revascularization is performed with either an end-to-end anastomosis or a polytetrafluoroethylene interposition graft.
      The middle scalene muscle originates from the transverse processes of C2-C7 and inserts broadly on the first rib between the subclavian groove and the posterior tubercle of the transverse process. The middle scalene muscle is divided above its insertion on the first rib. In tumors invading the middle compartment of the thoracic inlet, the scalene muscle may be extensively involved. In these cases, resection of the middle scalene muscle requires mobilization along its origin from the lower cervical vertebra.
      The cords of the brachial plexus are identified laterally. The cors are named the lateral, posterior, and medial cord according to their relationship to the axillary artery. The cords pass over the first rib close to the cupola of the lung and immediately posterior to the subclavian artery. The medial cord, arising from the C8 and T1 nerve root, is the cord most commonly involved by tumor. The consequence of medial cord involvement includes compromise of the ulnar nerve as well as medial cutaneous nerves to the arm and forearm. The T1 nerve roots are usually divided lateral to the vertebral foramen with care taken to spare the long thoracic nerve and minimize the risk of scapular winging. The long thoracic nerve arises from branches of the C5-C7 nerve roots.
      Figure thumbnail grr7
      Figure 7The chest-wall resection is performed with progressive resection of the first, second, and third ribs as necessary. The ribs may be resected from the costochondral junction anteriorly to the articulation with the transverse process. To facilitate mobility of the en bloc mass, resection of a short segment (1 to 2 cm) of rib may create a “floating” chest wall that facilitates mobilization of the mass before complete removal. The lung and chest wall is resected en bloc with a stapler. The hilar dissection, while possible with video-assistance, is challenging.

      Conclusions

      The feasibility of surgical resection of superior sulcus tumors depends on careful patient selection and staging. Knowledge of the anatomy of the thoracic inlet is essential in interpreting preoperative clinical and radiologic data. Similarly, the anatomic relationships in the thoracic inlet determine the surgical approach to superior sulcus tumors. For the treatment of anterior superior sulcus tumors, the transclavicular or clavicular-sparing (including hemi-clamshell) approaches provide a safe and effective exposure for resectable lung cancers.

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