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Anterior Approach to Superior Sulcus Tumors

Ben Dunne, Olaf Mercier, Marc dePerrot

Key Points

  • Thorough staging is imperative to identify patients with mediastinal nodal involvement (stage III) and systemic disease (stage IV).
  • A thorough understanding of the anatomy of the thoracic inlet is crucial. Dividing the thoracic inlet into 3 anterior zones and 2 posterior zones facilitate surgical planning and decision-making
  • There are a number of surgical approaches that can be utilized for pancoast tumors. It is essential to understand the strengths and weaknesses of each approach and tailor the approach chosen to the individual patient.
  • Complete en bloc R0 resection is the most critical factor for long-term survival.
  • Induction chemoradiation therapy can facilitate complete resection and potentially improve survival.

Historical Note

Pancoast coined the term of superior pulmonary sulcus tumors in 1924 to describe tumors invading the pulmonary sulcus at the level of T1 on chest x-ray.[1] The symptoms generated by these tumors are typical (Pancoast’s syndrome) with the combination of shoulder and arm pain in the distribution of the C8-T2 nerve roots, Horner’s syndrome, and weakness and atrophy of the hand muscles. The most common cause for this syndrome is local extension of an apical lung tumor in the posterior part of the thoracic inlet. Pancoast mistakenly believed that these tumors emanated from epithelial rests of the fifth branchial cleft. It was Tobias who correctly identified bronchopulmonary tissue as the origin of the Pancoast-Tobias syndrome.[2]

Nowadays, superior sulcus tumors define tumors that extend from the lung through the visceral pleura into the parietal pleura and the surrounding structures of the thoracic inlet and supraclavicular region. From the surgical perspective, Pancoast tumors are a specific subset of superior sulcus tumors that invade, and require resection of, the first rib and structures of the thoracic inlet.

These tumors were considered inoperable until Shaw and Paulson demonstrated that preoperative irradiation facilitated surgical resection and improved the survival rate at 5 years to 30%.[3],[4] The operation consisted in an extended posterolateral approach with en-bloc resection of the chest wall, including the first three ribs, the intercostal nerves, the lower trunk of the brachial plexus, and the involved lung.

Rusch reported the largest series of 225 patients operated on for superior sulcus tumors.[5] The 5-year survival rate was 46% for T3 N0 (stage IIB) disease and less than 15% for stage III. Survival was influenced by T and N status and completeness of resection. However, these results must be interpreted in light of the fact that 20% of these patients did not require chest wall resection and a complete resection was achieved for only two thirds of T3 tumors and 40% of T4 tumors. Importantly, locoregional disease was the most common form of relapse. This prompted the Southwest Oncology Group (SWOG) to perform a prospective, multi-institutional trial of induction chemoradiation therapy.[6] A total of 111 patients with mediastinoscopy-negative T3-4 N0-1 superior sulcus tumors received two cycles of cisplatin and etoposide concurrent with 45 Gy of radiation. Patients with stable or responding disease proceeded to thoracotomy 3 to 5 weeks later. One third of resections showed a complete pathologic response, and 92% had a complete resection. This preliminary report demonstrated that induction chemoradiation was feasible in a multi-institutional setting, improved resectability, and improved the 2-year survival rate to 70% for those with a complete resection (76 of 83 patients).

Increasingly complex resections have been reported with good peri-operative outcomes and long-term survival. The most dramatic change over the past 20 years have resulted from resection of tumors extending into the pulmonary sulcus and requiring spinal resection. These tumors typically lead to major morbidity due to the bony destruction and extension into the spinal canal. Radical resection with complete en bloc resection of the spine have changed the prognosis of these tumors. Excellent long-term outcome have been reported by multiple institutions if a complete R0 resection can be achieved.[7]

The presence of histologically confirmed N2 disease is still considered inoperable by most, although some data suggests that surgery may provide benefit in some very well selected patients, particularly if radical chemoradiation cannot be delivered due to the proximity of the brachial plexus or the spine.[8]

Surgical Anatomy

The anatomy of the superior sulcus is complex (Figure 1), and a thorough understanding of its contents and their spatial relationships is imperative for the thoracic surgeon. The thoracic inlet can be divided into 3 anterior zones and 2 posterior zones that facilitate surgical decision-making and planning the operative approach best suited to each individual patient (Table 1).

Figure 1
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Anatomy of the thoracic inlet[9]

Table 1: The 5 Anatomical Zones

Zone

Important Structures Involved

1

Anterolateral

Subclavian vein, anterior part of first rib, scalenus anterior, phrenic nerve

2

Anterocentral

Subclavian artery (1st and 2nd part), innominate vein, right recurrent laryngeal nerve

3

Posterosuperior

Superior border of first rib posteriorly, T1 vertebra/costo-vertebral junction, neural foramen, stellate ganglion, long thoracic nerve, spinal accessory nerve, scalenus medius, brachial plexus, vertebral artery

4

Posteroinferior

Inferior border of first rib posteriorly, lateral to transverse process

5

Inferolateral

Inferior border of first rib posterolaterally, 3rd part subclavian artery and axillary artery

A schematic representation of the 5 zones is presented in Figure 2. The 2 posterior zones (zone 4 and 5) described tumors extending to the first rib posteriorly and laterally. These tumors do not extend beyond the first rib and do not involve the first vertebra. They can be approached through an extended posterolateral thoracotomy as described by Shaw and Paulson. Posterior tumors located in zone 5 can extend into the subscapular space though the chest wall thus limiting the exposure to the subclavian vessels from the back. These tumors can be more adequately exposed through a “hook” approach described by some of the Japanese groups. This approach is characterized by extending the anterior part of the posterolateral thoracotomy upwards to the pectoralis muscles. This “C” incision allows anterior visualization of the subclavian vessels and facilitate exposure around bulky lateral tumors along the first rib behind the subclavian vessels.

Figure 2
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Posterior Approaches to the Thoracic Inlet.
Figure 3
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The 5 anatomical zones. Of note, Zones 4 and 5 do not necessarily invade the thoracic inlet but always require resection of the first rib.

Zone 1, 2 and 3 described tumors requiring an anterior approach.

The first zone (anterolateral zone) is located anteriorly and laterally to the subclavian vein between the lateral border of the sternum and the anterior scalene muscle. This zone includes the anterior part of the first rib and the subclavian vein. Access to this zone requires opening the costoclavicular space to expose the subclavian vein.

The second zone (anterocentral zone) is located medially to the subclavian vein and contains the subclavian artery up to the middle part of the first rib. The tumors included in this zone typically extend along the subclavian artery and/or brachiocephalic vein and can be accessed through a supraclavicular incision without opening the costoclavicular space.

The third zone (posterosuperior zone) extends from the top of the subclavian artery to the T1 vertebra and encompasses the posterior superior border of the first rib. The tumors located in this zone typically extend along the vertebral artery and/or involve the T1 vertebra at the level of the costovertebral articulation, neural foramen, and/or vertebral body. Because of the cephalad course of the first rib, structures located at the level of T1 and immediately anterior to T1 sit outside the chest and thus cannot be adequately accessed with a posterior approach alone.

For the purposes of this chapter we will focus on zones 1-3 and the surgical decision-making and techniques required for an optimal exposure for tumors involving these three zones.

Clinical Features

Pancoast tumors of non-small cell histology account for fewer than 5% of all bronchogenic carcinomas[10]. Most Pancoast tumors are peripherally located, and pulmonary symptoms such as cough, hemoptysis, and dyspnea are rare. The clinical features are influenced by tumor location and type of invasion of the thoracic inlet[11]. Tumors located in zone 1 usually manifest with chest wall pain due to invasion of parietal pleura, overlying ribs, and associated intercostal nerves. Many patients are incorrectly treated for cervical osteoarthritis or bursitis, delaying the correct diagnosis. Hand or arm swelling suggests subclavian vein invasion. Tumors located in zone 2 may present with arm swelling due to innominate vein involvement, rarely symptoms of arm ischaemia due to subclavian artery invasion. The phrenic nerve may be involved as it crosses the anterior scalene muscle behind the subclavian vein.

Tumors located in zone 3 frequently invade the brachial plexus at the level T1 and C8. They usually manifest with pain and parasthesias radiating to the shoulder and arm. These tumors tend to extend along the fibers of the middle scalene muscle. These tumors may manifest with the signs and symptoms of the Pancoast-Tobias syndrome. They are usually located in the costovertebral groove. They initially manifest with abnormal sensation and pain in the axilla due to T2 involvement and medial aspect of the upper arm along the territory of the intercostobrachial nerve if T1 nerve root is involved. They can also result in weakness and atrophy of the intrinsic muscles of the hand if the C8 nerve root is involved. Horner’s syndrome is also frequently present due to an extension into the stellate ganglion.

Diagnosis

Imaging

The radiologic findings can be subtle because these lesions are often hidden behind the 1st rib and clavicle. Posteroanterior and lateral chest radiographs have a low sensitivity for early lesions. Computed tomography (CT) provides precise localization of the tumor and its local extension. Magnetic resonance imaging (MRI) is more accurate than CT for the detection of tumor extension into the brachial plexus, vertebral body, vertebral foramina and spinal canal.[12] However, peri-tumoral inflammation can often be difficult to differentiate from vertebral body invasion on MRI.

Specific imaging must be performed if the vertebral artery is involved. This includes vascular dopplers to ensure that there is no stenosis of the carotid arteries and contralateral vertebral artery. CT angiography with 3D reconstruction is a useful alternative, although contrast should be injected from the arm on the side of the tumor to give better detail of the venous anatomy. An MRA of the circle of Willis is performed to ensure that the anatomy is normal with adequate collaterality. In the presence of a large vertebral artery or doubt about the safety of sacrificing the artery, an occlusion test of the selected vertebral artery can be performed to ensure that there is no neurological consequences.[13]

Histology

The majority of cases of Pancoast’s syndrome are caused by non–small cell lung cancer. However, the differential diagnosis for Pancoast’s syndrome and superior sulcus lesions is diverse[11] (Table 2). The most sensitive diagnostic procedure is a transthoracic needle biopsy under radiologic guidance. A diagnostic yield of greater than 95% has been reported.

Table 2: Etiology of Pancoast’s Syndrome and Superior Sulcus Lesions

Neoplasm

  • Primary bronchogenic carcinoma
  • Other primary thoracic neoplasms
  • Mesothelioma, adenoid cystic carcinoma, sarcomas
  • Metastatic neoplasms
  • Hematologic neoplasms
  • Plasmacytoma, lymphoma

Infectious Processes

  • Bacterial
  • Pneumonia, actinomycosis
  • Fungal
  • Aspergillosis, cryptococcosis, allescheriasis
  • Tuberculosis
  • Parasitic
  • Hydatid cyst

Miscellaneous Causes

  • Pulmonary amyloidoma

Staging and Preoperative Assessment

Operability of Patients

All patients being considered for surgery are thoroughly evaluated to ensure their fitness for major surgery. This includes a standard history, physical exam, and quantification of their exercise tolerance. All patients have full pulmonary function testing performed as well as a 6-minute walk test and echocardiogram.

Patients that may be borderline candidates for surgery are directed to further testing such as a Ventilation-Perfusion scan, Cardiopulmonary Exercise Test or further targeted cardiac investigations as required.

Staging

Initial staging is done with contrast-enhanced CT of the neck and chest. This gives excellent imaging of the tumor and its relation to the critical structures. MRI is used to further evaluate for invasion of the subclavian vessels, brachial plexus and spine, as this can yield additional information. Clinical evaluation is important to document the presence of a Horner’s syndrome as well as involvement of T1, C8 and other branches of the brachial plexus.

We routinely obtain a PET scan to further evaluate N and M stage. All patients have an MRI of the brain to complete staging imaging. Invasive staging of nodes is done with endobronchial ultrasound (EBUS) rather than mediastinoscopy and enlarged supraclaviclar nodes are biopsied with image guidance.

The aim is to ensure that the tumor will be completely resectable and there is no N2 nodal disease as these two elements are essential for good long-term outcomes. The results of concurrent chemoradiation therapy in N2 disease can provide an opportunity to add surgery in some well-selected patients, particularly if the mediastinum has been downstaged. Positive supraclavicular node in close proximity to the tumor with negative N2 nodes by EBUS is not a contraindication to surgery as it likely reflects local lymphatic extension rather than widespread lymphatic spread.

The extent of resection is determined according to the type of tumors. The subclavian, innominate, and internal jugular vein can be resected without major long-term consequence. The subclavian artery can also be resected but must be reconstructed and the vertebral artery can be considered for resection if there is normal anatomy up the level of the circle of Willis with adequate collaterals and no carotid or vertebral disease. The T1 nerve root of the brachial plexus can be resected without any motor deficit. C8 resection on the other can be resected but will leave motor dyfunctions at the level of the hand that can be partially overcome with physiotherapy. Detailed discussion with the patient about the morbidity associated with a functionally impaired hand must be performed before the surgery.

Induction Therapy

Tumors extending into the thoracic inlet can be treated with induction chemoradiation therapy, particularly if there is extension along the pulmonary sulcus. However, primary surgery with adjuvant therapy can lead to similar results if an R0 resection is achieved. Typically, 45 Gy of radiation concurrently with cisplatin/etoposide doublet chemotherapy is used for induction therapy. Patients are restaged after chemoradiation therapy with a CT scan and possibly PET scan. The operation is scheduled for 3-6 weeks post induction therapy although we will occasionally delay surgery to 8 weeks if they have had significant side effects from induction and require more time to recover. Wright et al. demonstrated improved pathological response, R0 resection rates, and 4-year survival with combined chemoradiation when compared to induction radiotherapy alone[14].

Operative Approach/Decision-Making

The choice of surgical approach taken will vary considerably from patient to patient. We believe that selecting the type of approach according to the location of the tumor and the level of potential difficulty is important.

Tumors involving zones 1-3 are best approached with one of the anterior techniques. Depending on the exact requirements of the individual patient, the most appropriate technique can be selected.

For tumors involving zone 1, the transclavicular[15] approach gives excellent access to the subclavian vessels, including the subclavian vein by resecting the head of the clavicle. There are concerns around impairment of arm function after clavicular resection but we have not found this to be a significant source of morbidity when the long thoracic nerve and spinal accessory nerve are preserved intra-operatively and the chest wall reection is limited.[16] The transmanubrial approach described by Grunenwald[17] allows access to the subclavian vein while preserving the clavicle and sternoclavicular joint. This exposure is excellent for tumors located anteriorly to the subclavian vessels, but can be more challenging than the transclavicular approach in the presence of a bulky tumor located posteriorly to the subclavian artery. The trapdoor approach initially described by Masaoka[18] with a supraclavicular incision provides excellent exposure to the subclavian artery. However, there is limited access to the costoclavicular space and the subclavian vein. The exposure to the subaclavian vein can be improved by sectioning the first rib anteriorly and the costoclavicular cartilage as described by Rusca.[19] This modified trapdoor allows the first rib to separate from the sternum and the clavicle as the trapdoor is opened and provides better exposure of the subclavian vein.

For zone 2 tumors, all of the anterior approaches provide adequate exposure and the clavicle/sternoclavicular joint can often be preserved, as access to the subclavian vein is not required.

For zone 3 tumors, we believe that the transclavicular approach provides optimal exposure for this zone at the back of the thoracic inlet. This exposure provides the ability to work from the lateral side of the thoracic inlet rather than from the medial side, which is necessary with the hemiclamshell approach or the transmanubrial approach. Therefore, the exposure to the brachial plexus, the spine, and the vascular structures are far superior. This approach also allows the spine surgeons to see the lateral part of the spine from C6 to T3, which is ideal if and anterior spinal reconstruction is required. The transmanubrial approach or hemiclamshell approach with cervical extension[20] are ideal for small benign tumor located in zone 3, but generally not optimal for large lung cancer extending into this zone.

For access to the pulmonary hilum, the trapdoor and hemiclamshell techniques are superior to the transclavicular, transmanubrial, and sternotomy approaches. However, the hilar dissection can be greatly facilitated with a VATS approach, which can be done in a second stage after the transmanubrial approach is required for the superior sulcus dissection.

Table 3: Common Techniques and Applicability to the 3 Anatomical Zones

Technique

Author

Z1

Z2

Z3

Hilum

Transclavicular

Dartevelle[15]

+++

+++

+++

+

Transmanubrial

Grunenwald[17]

++

++

+

-

Trapdoor/Hemiclamshell with supraclavicular incision

Masaoka[18]

+

++

-

++

Modified trapdoor hemiclamshell

Rusca[19]

++

++

++/-

++

Hemiclamshell with cervical incision

Korst[20]

-

++

++

++

Transclavicular Approach

The transclavicular approach provides the optimal exposure of the subclavian vein and the costoclavicular space (Figure 4). The patient is positioned supine with the head extended and turned away from the surgical side. A roll is placed behind the shoulder to elevate the surgical side. The arm located on the surgical side is placed along the body. The skin incision extends vertically along the sternocleidomastoid muscle (SCM) down to the manubrium and then is gently curved horizontally along the third rib toward the axilla. The incision should extend relatively high in the neck along the SCM to increase exposure in the thoracic inlet.

Figure 4
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Costoclavicular space[21]

The incision is deepened with cautery down to the chest wall. The SCM and pectoralis major muscles are dissected off the manubrium, clavicle, and chest wall. The sternal attachment of the SCM is divided sharply so it can be reattached on the manubrium at the end of the surgery. The muscle attachments are cauterized off the clavicle so the proximal one third of the clavicle is exposed. The muscle and the skin are folded laterally together as a myocutaneous flap. The preservation of a myocutaneous flap is important to obtain adequate healing of the wound as patients with lung cancer invading the thoracic inlet often undergo induction chemoradiation therapy before surgery. This provides exposure to the strap muscles, internal jugular vein, scalene fat pad, and anterolateral chest wall (Figure 4).

At this point, a thoracotomy is performed in the second intercostal space to palpate the tumor and ensure that there is no pleural seeding. The third rib is usually sectioned along the mid-axillary line in the chest (or anterior to the tumor if the third rib is involved by the tumor) to facilitate the exposure down to the pulmonary hilum. The omo-hyoid muscle is sectioned and the scalene fat pad dissected to expose the anterior scalene muscle. Once tracheal, esophageal and brachial plexus invasion higher than C8 have been ruled out and the tumor is deemed resectable, the proximal part of the clavicle is removed.

The proximal part of the clavicle is removed by disarticulating the sternoclavicular joint and dividing the proximal one third of the clavicle with the saw. The internal jugular vein and the subclavian vein are dissected off the clavicle and protected to prevent any vascular injury.

Resection of the proximal part of the clavicle provides excellent exposure of the first rib and subclavian vessels (Figure 5). The branches of the internal jugular and subclavian veins are ligated to facilitate exposure of the venous confluence. The cervical transverse vessels crossing over the anterior scalene muscle and the phrenic nerve can be visualized once the scalene fat pad is removed. On the left side, the thoracic duct must also be ligated. The transverse cervical vessels are ligated and sectioned, allowing exposure of the phrenic nerve along the anterior scalene muscle. The phrenic nerve must be carefully assessed to see whether it is involved by the tumor and needs to be resected. The phrenic nerve should be preserved whenever possible. The subclavian vein can also be assessed to determine whether it is involved by the tumor. If the subclavian and/or internal jugular veins are involved, they can be ligated and sectioned. The first and second ribs (and occasionally the third rib) are typically involved by the tumor and are sectioned anteriorly with adequate margin from the tumor.

Figure 5
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Reflection of the sternocleidomastoid muscle and pectoralis major muscle as a myocutaneous flap to expose and resect the proximal part of the clavicle.

The anterior scalene muscle is sectioned above the tumor, preserving the phrenic nerve if necessary (Figure 6). The subclavian artery can be exposed and controlled proximally and distally to the tumor. Its branches are ligated and sectioned to facilitate exposure. The vertebral artery can be resected if necessary so long as the preoperative assessment was adequate (see above). The subclavian artery can be clamped and sectioned on each side of the tumor if it is invaded. A bolus of heparin (50 units/kg) is given before clamping the subclavian artery. The subclavian artery can later be re-anastomosed primarily in most cases or using a 6-8mm ring-enforced PTFE graft once the resection of the tumor and the lobectomy has been completed. The vagus nerve should be localized and preserved when dissecting the internal jugular vein on the right or the left side. On the right side, the recurrent nerve should also be localized and preserved as it loops around the subclavian artery. Damage to the right recurrent nerve should be avoided when the proximal part of the subclavian artery is clamped. The first and second ribs remain attached to the specimen with the lower portion of the anterior scalene muscle and are resected en bloc with the tumor.

Figure 6
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After resection of the clavicle, the subclavian vein and anterior scalene muscle (underneath the scisors) are exposed. The phrenic nerve runs medially to the anterior scalene muscle in the lower part of the neck (located at the tip of the scisors).

Once the subclavian artery is dissected, the brachial plexus can be exposed. The dissection of the brachial plexus is performed from the lateral to the medial aspect, starting with the trunks and progressing toward the roots. The lower trunk of the brachial plexus can then be gently elevated to expose the insertion of the middle and posterior scalene muscles on the first rib. The middle and posterior scalene muscles are sectioned above the first rib away from the tumor. This allows exposure of the posterior part of the first rib as well as the nerve roots of C8 and T1. Branches of the fifth (C5), sixth (C6), and seventh (C7) cervical nerve roots passing through the body of the middle scalene muscle can occasionally be identified emerging on the lateral aspect of this muscle just above the brachial plexus.

These nerves are located above the brachial plexus and can be preserved by dividing the middle and posterior scalene muscles from the first rib after gently elevating the brachial plexus off the first rib and sectioning these muscles underneath the plexus. These small branches of C5, C6, and C7 will form the dorsal scapular (branches of C5) and long thoracic nerves (branches of C5, C6, and C7) innervating, respectively, the rhomboid and serratus anterior muscles.

T1 can then be identified and sectioned above the first rib if necessary. The T1 nerve root is often involved at the level of the first rib and should be resected with the tumor. The C8 nerve root should be preserved if possible because its section will result in loss of motor function in the forearm and the hand. The prevertebral muscles are then dissected off the anterior part of the T1 and T2 vertebra and removed with the sympathetic chain and the stellate ganglion.

The head of the first and second ribs can be disarticulated from the vertebra if the costotransverse foramen, the neural foramen, and the vertebral body are not involved. If the costotransverse foramen is involved, the anterior part of the vertebral body can be exposed and sectioned with a chisel to remove the lateral edge of the vertebral body and the transverse process at the level of T1, as shown on Figure 7. If the neural foramen and/or the vertebral body are involved, a hemivertebrectomy or a total vertebrectomy of T1 is required. In these cases, a posterior midline approach must be associated with the anterior approach to perform the laminectomy, ligation of nerve roots in the spinal canal, and posterior vertebral body osteotomy. If a hemivertebrectomy is performed, a posterior spinal stabilization is required. If a complete vertebrectomy is performed, a posterior and an anterior spinal stabilization are required. The posterior spinal stabilization can be performed from the posterior midline approach. The anterior transclavicular approach, however, does provide adequate exposure to instrument the anterior part of the spine if further stabilization is required (Figure 8). Careful hemostasis is required to prevent postoperative hemothorax, by securing small veins at the level of the intervertebral foramina.

Figure 7
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Section of anterior scalene muscle to expose the subclavian artery and the brachial plexus.
Figure 8
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Lateral access to spine.

The right upper lobectomy can be performed through the second intercostal space. The lobectomy is performed from an anterior to a posterior approach. The right upper lobe pulmonary vein and artery are ligated or stapled and the fissure is completed with staplers. The bronchus is then stapled. The right upper lobe can then be removed en bloc with the tumor. A lymph node dissection of stations 2R and 4R on the right side and stations 5 and 6 on the left side is then performed through the anterior approach as part of the oncologic procedure. Station 7 is also sampled or dissected according to the exposure. Thoracoscopic techniques can be used to facilitate the hilar dissection and nodal sampling and adds very little morbidity to the procedure in contrast to an additional posterolateral thoracotomy. We rarely use any prosthetic material to reconstruct the anterior chest wall. The SCM is reattached to the manubrium with 1 or 2 stitches and the incision is closed in 2 layers. Two chest tubes are placed in the pleural cavity.

Transmanubrial Approach

The transmanubrial approach[17] is a modification of the transclavicular technique that was developed to avoid the morbidity of clavicular resection and preserve continuity of the sternoclavicular joint. It employs a similar L-shaped incision along the anterior border of SCM to the manubrio-sternal angle and laterally 2 finger breadths below the clavicle. An L-shaped sternal incision is made dividing the manubrium in the midline then off to the side in the first intercostal space. The first costal cartilage is resected allowing elevation of this sterno-clavicular unit and permitting reasonable access to the costo-clavicular space and the structures of zone 1 (Figure 9).

Figure 9
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Spinal stabilization after total vertebrectomy of T1,2,3.
Figure 10
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Grunenwald Transmanubrial approach.

Once the necessary superior sulcus dissection has been completed the manubrium is reconstructed with sternal wires. Pulmonary resection is not possible with this approach and the original description described a posterolateral thoracotomy to complete the resection. However, this may be facilitated with VATS in the current era.

Trapdoor (Hemiclamshell) with Supraclavicular Extensionn

The trapdoor approach, or hemiclamshell with supraclavicular extension[18], was described originally by Masaoka. The patient is positioned supine with a shoulder roll to elevate the operative side. The head is turned away from the operative side. A 4th interspace anterior thoracotomy is made on the involved side and joined with a partial sternotomy. A supraclavicular incision is made from the top of the sternotomy incision laterally for approx. 8cm. Dividing part of the SCM and strap muscles from the clavicle and manubrium allows the ‘trapdoor’ segment of chest wall to be elevated (Figure 11). Very good access to the pulmonary hilum and zone 2 is obtained, particularly if lateral access to the subclavian vessels is required. Access to zone 3 is not as good as with a cervical incision along the SCM. Access to zone 1 is possible but limited.

Figure 11
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Trapdoor incision.

Hemiclamshell with Cervical Extension

This approach was described by Korst[20] and provides exposure of zone 3 as well as the pulmonary hilum. The incision is similar to the trapdoor approach, but the cervical extension is performed along the sternocleidomastoid muscle rather than along the clavicle. Hence, access to the subclavian artery, brachial plexus, and vertebral bodies is limited by the lack of a supraclavicular incision. The incision along the sternocleidomastoid muscle provides better access to the posterior part of the thoracic inlet (zone 3), but limit the exposure to zone 1 and 2 unless a counterincision is made along the clavicle (dotted line in Figure 12).

The patient is positioned supine with the ipsilateral arm tucked by the side and the contralateral arm abducted. The neck is extended, and the head is turned away from the operative side. An anterolateral thoracotomy is made from the sternum to the anterior axillary line in the fourth intercostal space. Medially, the incision is carried superiorly over the sternum and up the anterior border of the ipsilateral sternocleidomastoid muscle. A partial sternotomy is made from the suprasternal notch down to the fourth interspace. The internal thoracic vessels are ligated, and a sternal retractor is placed to elevate the chest wall and clavicle, exposing the mediastinum and ipsilateral hemithorax. The structures of zone 3 are accessible through this incision, albeit with limited access to the lateral portions of the subclavian artery, plexus, and vertebral bodies.

Figure 12
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Hemiclamshell with cervical extension and lateral supraclavicular counterincision.

Modified Trapdoor

In order to improve access to zone 1 through the hemiclamshell, Rusca[19] proposed a modification. After the hemiclamshell is performed, the first costal cartilage is resected and the costoclavicular ligament divided. This allows the chest wall to be retracted anteriorly while the first rib remains in its natural position and gives exposure to the subclavian vein (Figure 13). This can be combined with a supraclavicular incision as part of the trapdoor approach. This is a significant improvement in access to zone 1 but still provides less complete exposure of the subclavian vein, when compared to resecting the head of the clavicle.

Figure 13
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Modified trapdoor approach (Rusca).

Complications

Operative mortality in modern series ranges from 0% - 6.9%[22]. Patients undergoing resection of a superior sulcus tumor are at risk for the standard complications of pulmonary resections.

The most common complications are respiratory in nature. The combination of a pulmonary resection, chest wall resection (with the resultant ‘flail’ portion of chest wall), and potentially a phrenic nerve resection leaves these patients at high risk of atelectasis, respiratory insufficiency, and post-operative pneumonia. These patients are at significant risk for reintubation, prolonged mechanical ventilation, and may require tracheostomy to facilitate recovery.

The usual cardiovascular complications are seen in this patient population at rates comparable to standard lung resection.

Several specific complications after resection are discussed here.

A cerebrospinal fluid leak can be catastrophic. It can lead to meningitis or be the source for an air embolus to travel from the pleural space to the brain or spinal cord. If a leak is identified intraoperatively, it needs to be sealed. Postoperatively, a leak should be suspected if there is a change in level of consciousness, the occurrence of a new headache and new neurological symptoms. Reoperation is mandatory and repair may require neurosurgical consultation, foraminotomy, and direct dural repair.

The possibility of Horner’s syndrome and nerve deficits secondary to division of the nerve roots is discussed with the patient preoperatively. Resection of the lower trunk of the brachial plexus (C8 and T1) results in atrophic paralysis of the forearm and intrinsic muscles of the hand (Klumpke-Déjérine syndrome). This is very debilitating and is avoided whenever possible.

Chylothorax is more common after left-sided resections because the thoracic duct may be injured during the cervical portion of the resection. It can be avoided by ligation of the thoracic duct and its branches. If a chylothorax is identified and does not respond to conservative therapy, reoperation to identify the leak should be first conducted. In persistent leak, a thoracic duct ligation via a right thoracotomy may be required. If the subclavian vein has been resected, the ipsilateral forearm needs to be elevated to facilitate venous drainage and minimize edema. The edema will generally progressively resolved over 3-4 weeks. If a portion of the subclavian artery has been resected, the radial pulse must be monitored to assess the patency of the repair.

Adjuvant Therapy

Adjuvant therapy is given to patients who did not receive induction therapy. However, in the setting of induction chemoradiation, adjuvant therapy is used infrequently due to the lack of high-level evidence supporting its use in the setting of induction chemoradiation.

Long-Term Results and Prognostic Factors

Five-year survival in the landmark SWOG[6] and JCO[23] trials was 44 and 56% respectively. A number of factors have been shown to have a major impact on long-term outcome. Incomplete resection has been repeatedly shown to have a poor prognosis as has positive nodal status (N1, 2, or 3). T-stage (T4 vs T3), particularly with involvement of the subclavian artery or vertebral body, has been shown to impact survival irrespective of completeness of resection. Formal lobar resection, rather than sublobar resection, has shown better long-term results. Pathological complete response to induction therapy has also had a positive impact on 5-year survival when compared to those with viable tumor in the resected specimen. The best case scenario of a patient with a completely resected T3 tumor with negative nodes and complete or near complete pathological response could have a 5-year survival of up to 60-80%[24].

Summary

Resection of superior sulcus tumors is one of the most technically demanding procedures in thoracic surgery. Nonetheless, major technical advances have been made since Shaw and Paulson’s original description and multiple surgical series have shown that these operations can be performed with acceptable rates of morbidity and mortality and lead to excellent long-term outcome, particularly for tumors extending along the pulmonary sulcus and requiring spinal resection.

Each individual patient requires a tailored operative approach and a thorough knowledge of the anatomy. The various anterior approaches give ample flexibility to get good access to any tumor in zones 1-3, the advantages and disadvantages of each should be clearly understood. This will permit a safe and complete resection for patients with these challenging tumors.

Patients must be accurately staged pre-operatively to avoid an unnecessary operation. Similarly, the surgeon must be confident that an R0 resection can be achieved prior to embarking on tri-modality treatment. Recent advances have extended the limits of vascular and vertebral resection and reconstruction that can allow R0 resections in patients with locally advanced tumors.

Peri-operative care must be very attentive to the prevention of respiratory complications in these high-risk patients due to the nature of the operation required. Long-term outcomes depend heavily on the T and N stage, completeness of resection, and pathological response to induction therapy.

Comments and Controversies

The anterior approach to superior sulcus tumors encompasses a broad range of techniques. Any tumor in zones 1-3 can be accessed best with an anterior approach, the specific approach taken will depend on the individual tumor and the anatomic structures involved. Surgeons involved in these cases must be aware of the specific challenges presented by the involvement of each particular zone and understand the advantages and disadvantages of the available techniques in order to ensure the optimal outcome – a safe and thorough R0 resection.

References

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Last updated: February 1, 2021