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Pros and Cons of Anterior and Posterior Approaches to Pancoast Tumors: Posterolateral Superior Sulcus Tumor Resections

      The superior sulcus tumor, due to its location in the bony confines of the thoracic inlet and superior costovertebral gutter, provides the thoracic surgeon with a unique challenge. It is a peripheral T3 or T4 upper lobe tumor that invades the chest wall. It may also invade the vertebral bodies and structures of the thoracic inlet. Although earlier described as a squamous cell carcinoma, adenocarcinomas are more common in recent reports. They are relatively rare, accounting for less than 5% of all lung carcinomas.
      • Ginsberg R.J.
      • Martini N.
      • Zaman M.
      • et al.
      Influence of surgical resection and brachytherapy in the management of superior sulcus tumour.
      Historically, this process was described by Edwin Hare in the 1830s, and later, by Pancoast and Tobias.
      • Hare E.S.
      Tumor involving certain nerves.
      • Pancoast H.
      Importance of careful roentgen-ray investigations of apical chest tumors.
      • Pancoast H.K.
      Superior pulmonary sulcus tumor.
      • Tobias J.
      Síndrome apico-costo-vertebral doloroso por tumor apexiano su valor diagnostico en el cancer primitivo pulmonary.
      Pancoast, a radiologist, was a pioneer in radiation therapy for this lesion. In the last century, the management of the superior sulcus tumor has changed from inoperability and incurability to the current regimen of preoperative chemoradiation therapy, with an attempt at complete resection.
      • Rusch V.W.
      • Giroux D.J.
      • Kraut M.J.
      • et al.
      Induction chemoradiation and surgical resection for non-small cell lung carcinomas of the superior sulcus initial results of Southwest Oncology Group trial 9416 (Intergroup trial 0160).
      Surgical resection is most commonly accomplished with either a posterolateral or an anterior transcervical approach.
      • Shaw R.R.
      • Paulson D.L.
      • Kee Jr, J.L.
      Treatment of the superior sulcus tumor by irradiation followed by resection.
      • Dartevelle P.G.
      • Chapelier A.R.
      • Macchiarine P.
      • et al.
      Anterior transcervical-thoracic approach for radical resection of lung tumors invading the thoracic inlet.
      The posterolateral thoracotomy has certain advantages over the anterior approach. It is ideal for posterior tumors, particularly those that invade the vertebral bodies and the brachial plexus. If, on operative exploration, invasion of the subclavian artery is found, this approach can still be used. Proximal and distal control of the artery must be obtained and the position of the patient may even need to be changed. Once well exposed, the tumor may be freed through a subadventitial plane, or if necessary (for clear margins), the artery may be resected. Revascularization can be done with a polytetrafluoroethylene graft or end-to-end anastomosis. Despite the feasibility of dealing with unforeseen vascular invasion through the posterior approach, the anterior approach is better suited to that particular problem.
      There is probably no benefit to incomplete resection, even when combined with postoperative radiation.
      • Maggi G.
      • Casadio C.
      • Pischedda F.
      • et al.
      Combined radiosurgical treatment of Pancoast tumor.
      Therefore, to achieve complete resection, it is important that the surgeon be familiar with a combined approach. Contraindications to surgical resection are mediastinal lymph node metastases, extrathoracic metastases, pleural metastases, and spinal canal involvement. Invasion of the brachial plexus above the T1 nerve root (C8, C7, etc) is also a contraindication. Vertebral body involvement is not a contraindication if a complete resection can be achieved, but may require a neurosurgeon’s assistance. Similarly, invasion of the subclavian vessels is not a contraindication as long as a complete resection can be achieved.

      Preoperative Evaluation

      The presentation of these tumors often involves shoulder and/or arm pain. The “Pancoast–Tobias” syndrome includes a triad of shoulder pain, Horner’s syndrome, and atrophy of the hand.
      • Pancoast H.
      Importance of careful roentgen-ray investigations of apical chest tumors.
      • Pancoast H.K.
      Superior pulmonary sulcus tumor.
      • Tobias J.
      Síndrome apico-costo-vertebral doloroso por tumor apexiano su valor diagnostico en el cancer primitivo pulmonary.
      Tumors invading either the brachial plexus, the vertebral bodies, and the first and second ribs tend to produce a pain often following the distribution of the ulnar nerve. Invasion of the stellate ganglion causes a Horner’s syndrome (ipsilateral ptosis, miosis, and anhydrosis). More anterior tumors can cause unilateral upper extremity edema as a presenting symptom, or even hemorrhage. Performing a thorough neurological examination to assess for brachial plexus involvement is important. Pain or weakness on the ipsilateral hand may distinguish between C8 and T1 nerve root involvement. Weakness of the intrinsic hand muscles suggests C8 involvement, as opposed to T1 invasion, which is more consistent with ulnar forearm pain. Resecting the C8 nerve root for a clean margin would likely lead to a functionless hand.
      With regard to imaging, chest radiograph, computed tomography (CT), and a metastatic work-up are necessary. These tumors are often missed on routine radiograph, obscured by the clavicle and first rib. CT is ideal for identifying the lesion. Biopsy before definitive surgery is recommended. The differential diagnosis of these apical chest “tumors” includes infectious etiologies such as staphylococcal pneumonia, tuberculosis, as well as neoplasms such as lymphoma. Lymphoma and tuberculosis, in particular, can present with lesions that invade the chest wall or cause rib destruction. Magnetic resonance (MR) is a useful adjunct when suspicious of significant brachial plexus (C8 nerve root) involvement or vascular invasion.
      • Freundlich I.M.
      • Chasen M.H.
      • Varma D.G.
      Magnetic resonance imaging of pulmonary apical tumors.
      A brain MR, and possibly a positron emission tomography (PET) scan, should be performed to rule out metastatic disease. Because preoperative chemoradiation has become more prevalent, re-imaging before surgery is necessary. This is done not only to restage, but also to rule out disease progression. When there has been an unusual delay before surgery, the brain should be re-imaged as well. If there is any question involving the extent of tumor involvement (eg, pleural studding), the surgeon can always begin the procedure with thoracoscopy.
      Other preoperative issues include the role of mediastinoscopy. Mediastinoscopy is important for prognostic reasons. N2 involvement or greater is associated with a dismal prognosis. However, a controversial area is that of ipsilateral supraclavicular node involvement (N3), which may be better classified as N1 disease in these tumors.
      • Ginsberg R.J.
      • Martini N.
      • Zaman M.
      • et al.
      Influence of surgical resection and brachytherapy in the management of superior sulcus tumour.
      • Detterbeck F.C.
      Changes in the treatment of Pancoast tumors.
      Finally, the surgeon should engage the patient in a lengthy discussion addressing the potential morbidity of loss of hand function. This is a problem, if, intraoperatively, it is found that the tumor has invaded the brachial plexus significantly. Generally, involvement of C8 means the resection will be incomplete. Furthermore, the patient should quit smoking several weeks before the surgery and begin respiratory conditioning to better tolerate the distortion of the chest wall postoperatively.

      Operative Technique

      Figure thumbnail gr1
      Figure 1Chest radiograph and CT scan of right superior sulcus tumor. This chest radiograph shows a right-sided superior sulcus tumor (A). Unless large, they are often missed, obscured by the clavicle and first rib. The preoperative CT (B) demonstrates invasion of the chest wall and first rib, and it appears to involve the great vessels. This patient, like most patients with extensive Pancoast tumors, received neoadjuvant therapy. It is important to re-image these patients before surgery (C).
      Figure thumbnail gr2
      Figure 2Tumor invading brachial plexus. The ideal tumor for the posterolateral approach is situated posterior in the superior sulcus and does not invade the anterior structures of the thoracic inlet. It may, however, invade the vertebral bodies, or with regard to the thoracic inlet structures, the brachial plexus. The C8 and T1 nerve roots are most commonly invaded. It is important to assess the patient’s neurologic function preoperatively and to counsel the patient on the potential neurological postoperative morbidity.
      Figure thumbnail gr3
      Figure 3Incision. The patient is in the lateral decubitus position. A posterolateral thoracotomy incision is made extending from the anterior axillary line around the scapula to the base of the neck. Note the transected trapezius, latissimus dorsi, and rhomboids. The dorsal scapular nerve and scapular artery branches should be avoided when dividing the rhomboids at their insertion to the medial border of the scapula. These muscles will all be meticulously reapproximated at the end of the case. (Figure adapted from Nesbitt JC, Wind GG, Rusch VW (consulting ed.), Walsh GL (consulting ed.): Superior Sulcus Tumor Resection in Nesbitt JC, Wind GG (eds.): Thoracic surgical oncology: Exposures and techniques. Philadelphia, Lippincott Williams & Wilkins, 2003; p 162-193, with permission.

      Nesbitt JC, Wind GG, Rusch VW (consulting ed.), Walsh GL (consulting ed.): Superior Sulcus Tumor Resection in Nesbitt JC, Wind GG (eds): Thoracic surgical oncology: Exposures and techniques. Philadelphia, Lippincott Williams & Wilkins, 2003.

      )
      Figure thumbnail gr4
      Figure 4Thoracotomy. A thoracotomy is made in the fourth intercostal space. In the case of a smaller tumor, the thoracotomy can be made below the third rib. However, it is important to be at least one rib space below the tumor for adequate margins. The surgeon palpates the tumor before extending the thoracotomy. Next, the surgeon proceeds to divide the serratus anterior from the uppermost ribs. This permits the scapula’s elevation off of the chest wall. demonstrates the scapula being elevated with the superior retractor blade underneath the scapula and the inferior blade in the thoracotomy. (Figure adapted from Nesbitt JC, Wind GG, Rusch VW (consulting ed.), Walsh GL (consulting ed.): Superior Sulcus Tumor Resection in Nesbitt JC, Wind GG (eds.): Thoracic surgical oncology: Exposures and techniques. Philadelphia, Lippincott Williams & Wilkins, 2003; p 162-193, with permission.

      Nesbitt JC, Wind GG, Rusch VW (consulting ed.), Walsh GL (consulting ed.): Superior Sulcus Tumor Resection in Nesbitt JC, Wind GG (eds): Thoracic surgical oncology: Exposures and techniques. Philadelphia, Lippincott Williams & Wilkins, 2003.

      )
      Figure thumbnail gr5
      Figure 5Division of scalenes. After the scapula has been elevated, attention is directed toward the scalenes. Dividing the scalenes exposes the structures of the thoracic inlet. Note the insertions of the anterior and middle scalene on the first rib. Also of note is the phrenic nerve lying on the anterior surface of the anterior scalene. This, as well as the subclavian vein and artery, should be identified before dividing the anterior scalene. (Figure adapted from Nesbitt JC, Wind GG, Rusch VW (consulting ed.), Walsh GL (consulting ed.): Superior Sulcus Tumor Resection in Nesbitt JC, Wind GG (eds.): Thoracic surgical oncology: Exposures and techniques. Philadelphia, Lippincott Williams & Wilkins, 2003; p 162-193, with permission.

      Nesbitt JC, Wind GG, Rusch VW (consulting ed.), Walsh GL (consulting ed.): Superior Sulcus Tumor Resection in Nesbitt JC, Wind GG (eds): Thoracic surgical oncology: Exposures and techniques. Philadelphia, Lippincott Williams & Wilkins, 2003.

      )
      Figure thumbnail gr6
      Figure 6Anterior division of ribs. Once the first rib is adequately exposed, the lower trunk of the brachial plexus is apparent as well. At this point, we proceed to divide the ribs with shears anteriorly in this order: fourth rib, third rib, second rib. The neurovascular bundles are ligated and divided anteriorly, as well.
      Figure thumbnail gr7
      Figure 7Right upper lobectomy. Once the anterior division of the fourth through second ribs is accomplished, a standard right upper lobectomy is performed. A wedge resection is an option but is not recommended.
      • Ginsberg R.J.
      • Martini N.
      • Zaman M.
      • et al.
      Influence of surgical resection and brachytherapy in the management of superior sulcus tumour.
      A standard mediastinal lymph node dissection should be done at this point.
      Figure thumbnail gr8
      Figure 8Division of first rib. The anterior division of the first rib is accomplished using a Gigli saw after carefully dissecting around the rib with a right-angled clamp. The subclavian vessels may be gently retracted with a soft-tipped clamp before dividing the rib. Another option to protect the vessels is to lay a ribbon “retractor” on the vessels, placing the ribbon between the vessels and the Gigli saw. If the space around the artery is violated, it is easy to notice the saw grinding against the ribbon before any damage should occur.
      Figure thumbnail gr9
      Figure 9Assesment of C8 and T1 nerve roots. With all four ribs divided anteriorly, and the lobectomy done, attention is directed toward the tumor’s involvement with the brachial plexus. At this point, the tumor is still fixed posteriorly. The C8 and T1 nerve roots are apparent. Even if involved with tumor, every effort should be made to spare the C8 nerve root to avoid the morbidity of loss of function of the intrinsic muscles of the hand. When the T1 nerve root is divided, there is usually only a sensory deficit along the medial aspect of the hand.
      Figure thumbnail gr10
      Figure 10Posterior division of ribs. The ribs are divided posteriorly next. First, the paravertebral muscles are divided exposing the spine. The ribs are divided from inferior to superior with an osteotome at the costotransverse junction. When the osteotome pops into the costotransverse junction, this leverage exposes the neurovascular bundle for ligation. It is extremely important to ligate the neurovascular bundles. Potential complications include tension pneumocephalus, cerebrospinal fluid leak, or a progressive hematoma causing spinal compression. If there is bleeding, temporary packing can be placed but must be removed during the procedure to prevent embolism. (Figure adapted from Nesbitt JC, Wind GG, Rusch VW (consulting ed.), Walsh GL (consulting ed.): Superior Sulcus Tumor Resection in Nesbitt JC, Wind GG (eds.): Thoracic surgical oncology: Exposures and techniques. Philadelphia, Lippincott Williams & Wilkins, 2003; p 162-193, with permission.

      Nesbitt JC, Wind GG, Rusch VW (consulting ed.), Walsh GL (consulting ed.): Superior Sulcus Tumor Resection in Nesbitt JC, Wind GG (eds): Thoracic surgical oncology: Exposures and techniques. Philadelphia, Lippincott Williams & Wilkins, 2003.

      )
      Figure thumbnail gr11
      Figure 11Vertebral body articulation. If the transverse process is involved with tumor, rather than division at the costotransverse junction (A), the rib should be divided as in (B). (Figure adapted from Nesbitt JC, Wind GG, Rusch VW (consulting ed.), Walsh GL (consulting ed.): Superior Sulcus Tumor Resection in Nesbitt JC, Wind GG (eds.): Thoracic surgical oncology: Exposures and techniques. Philadelphia, Lippincott Williams & Wilkins, 2003; p 162-193, with permission.

      Nesbitt JC, Wind GG, Rusch VW (consulting ed.), Walsh GL (consulting ed.): Superior Sulcus Tumor Resection in Nesbitt JC, Wind GG (eds): Thoracic surgical oncology: Exposures and techniques. Philadelphia, Lippincott Williams & Wilkins, 2003.

      )
      Figure thumbnail gr12
      Figure 12Closure of defect. Once the ribs have been divided posteriorly, the tumor (still attached to the chest wall) is removed as one specimen. At this point, a routine evaluation of the margins is done, obtaining biopsies and placing clips to direct postoperative radiation. The divided muscles seen in must be reapproximated. Chest tubes are placed. A defect of three or more ribs, or a defect over the tip of the scapula, should be closed with synthetic mesh (eg, Gore-Tex®). Superiorly, the mesh is sewn to the scalenes and fascia surrounding the clavicle. Anteriorly, it is sewn to the intercostal fascia and muscle and around the cut rib ends. Posteriorly, it is sewn to the paraspinous muscles and fascia. Inferiorly it is sewn around (pericostal) the intact rib. Meticulous reapproximation and closure with mesh prevents major morbidity in respiratory chest wall motion.

      Postoperative Issues

      Because of the rarity of tumors that meet the specific “superior sulcus” definition, there is a lack of large prospective studies. In the North American intergroup trial 0160, a prospective multi-institutional study of non-small cell lung cancer of these tumors, the 5 year-survival rate was 41% (Table 1). Contributing factors to survival were pathologic response to chemoradiation and complete resection. The local recurrence rate was 12% but distant recurrence was significantly higher.
      • Rusch V.W.
      • Giroux D.J.
      • Kraut M.J.
      • et al.
      Induction chemoradiation and surgical resection for non-small cell lung carcinomas of the superior sulcus initial results of Southwest Oncology Group trial 9416 (Intergroup trial 0160).
      Table 1Selected 5-year Survival
      ReportNumber of patients5-year survival (%)
      Ginsberg et al
      • Ginsberg R.J.
      • Martini N.
      • Zaman M.
      • et al.
      Influence of surgical resection and brachytherapy in the management of superior sulcus tumour.
      12426
      Attar et al
      • Attar S.
      • Krasna M.J.
      • Sonnet J.R.
      • et al.
      Superior sulcus (Pancoast) tumor experience with 105 patients.
      10562
      Rusch et al
      • Rusch V.W.
      • Giroux D.J.
      • Kraut M.J.
      • et al.
      Induction chemoradiation and surgical resection for non-small cell lung carcinomas of the superior sulcus initial results of Southwest Oncology Group trial 9416 (Intergroup trial 0160).
      11041
      With regard to morbidity, there are several problems that can easily be avoided with careful intraoperative attention and postoperative care. Overall morbidity can be over 50% with most of these being minor complications. Common complications in the intergroup trial were atelectasis and pneumonia at 14.5 and 12%, respectively. There were also two (2.4%) postoperative deaths secondary to respiratory failure.
      • Rusch V.W.
      • Giroux D.J.
      • Kraut M.J.
      • et al.
      Induction chemoradiation and surgical resection for non-small cell lung carcinomas of the superior sulcus initial results of Southwest Oncology Group trial 9416 (Intergroup trial 0160).
      Other potential complications include frozen shoulder and chest wall motion issues that affect respiratory function and contribute to postoperative atelectasis. With meticulous muscle reapproximation, and coverage of both large defects and/or scapular tip defects with mesh, the risk of this occurring is decreased. Attention should be paid to preventing entrapment of the tip of the scapula in this reapproximation to protect shoulder girdle motion. Despite this, aggressive postoperative physical therapy most effectively prevents chest wall respiratory and frozen shoulder problems.
      The superior sulcus tumor is a rare tumor posing a unique challenge to thoracic surgeons. The current regimen of preoperative chemoradiation with complete surgical resection leads to reasonable long-term survival. However, it is important to put these patients in trials to further improve outcomes. The posterolateral approach, when compared with the anterior approach, gives the surgeon the most latitude in resecting these tumors.

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