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Posterolateral approaches to the superior sulcus

      Superior sulcus tumors are a complex subset of bronchogenic malignancies that pose significant technical challenges to the thoracic surgeon. A variety of approaches have been described in the literature, including a neoadjuvant treatment with radiation therapy followed by surgical resection. The dose of radiation therapy is often between 45 and 50 Gy. This approach often is associated with shrinkage of the tumor and perhaps facilitates resection. Unfortunately, if there are grossly positive or microscopic margins postoperatively, the dose of effective radiation therapy that can be given postoperatively is much reduced. We have enrolled patients with superior sulcus tumors on an institutional protocol in which the patients receive upfront resection followed by concurrent chemotherapy and radiation therapy postoperatively to a total of 69.6 Gy.
      • Gandi S
      • Walsh GL
      • Komaki R
      • et al.
      A multidisciplinary surgical approach to superior sulcus tumors with vertebral invasion.
      Because of a great deal of experience with our spinal surgical colleagues at our institution, even tumors with extensive vertebral body involvement can be safely approached surgically.
      • Komaki R
      • Putnam Jr, JB
      • Walsh G
      • et al.
      The management of superior sulcus tumors.
      • Komaki R
      • Roth JA
      • Walsh GL
      • et al.
      Outcome predictors for 143 patients with superior sulcus tumors treated by multidisciplinary approach at The University of Texas M. D. Anderson Cancer Center.
      • Komaki R
      • Roth JA
      • Walsh GL
      • et al.
      Multidisciplinary approach for 143 patients with superior sulcus tumors treated at The University of Texas M. D. Anderson Cancer Center.
      The preoperative assessment on all of these patients includes a physical examination with special attention to the evidence of a Horner's syndrome and a neurologic examination of the affected upper limb. Patients who present with significant functional motor loss associated with these tumors often demonstrate involvement of the brachial plexus to a point where clear margins could not be obtained. Sensory changes and some hand changes, however, are generally still amenable to en bloc complete surgical resection. Magnetic resonance imaging (MRI) of the brachial plexus and thoracic spine is routine and mandatory in these cases. All patients undergo a mediastinoscopy to rule out N2 or N3 disease before proceeding to resection. The position of the superior sulcus tumor must be assessed for involvement of the subclavian vessels. If this involvement is evident, then the initial approach will be through an anterior incision, either a supraclavicular incision or a Darteville incision with hemimanubriumotomy and elevation of the clavicle away from the thoracic inlet. If the blood vessels need to be grafted, then this can be accomplished from an anterior approach. This article will focus on the typical posteriorly situated superior sulcus tumor that does not involve the vessels but may involve the C8 or T1 nerve root.

      Surgical technique

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      1 The single-lumen endotracheal tube used to perform the mediastinoscopy is changed for a double-lumen tube and positioned under bronchoscopic guidance. The patient is positioned in a lateral decubitus position, taking care to pad all of the important sites that could result in nerve injury from prolonged positioning on the operating table. The axillary roll is placed to protect the brachial plexus. The head is stabilized with cervical tongs, and care is taken to align the cervical, thoracic, and lumbar spines. The patient is placed in a perfectly perpendicular orientation and is secured in this position with an inflated beanbag. Supplemental taping is used to further prevent any rotation of the torso. Care is taken to prep and drape the patient from the occiput, beyond the midline posteriorly, and to the sternum anteriorly. If it is anticipated that the patient will require posterior spinal instrumentation, then it is important for the extended posterolateral thoracotomy to meet the planned midline incision at a right angle to minimize any risk of acute angulation and skin flap ischemia, which can be an extremely important aspect of dealing with the complex superior sulcus tumors that invade the vertebral body. A breakdown of these skin flaps may subsequently result in exposed posterior hardware, which can be an extremely complicated surgical problem.
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      2 Initially, a limited posterolateral thoracotomy is performed by the division of the latissimus dorsi muscle and reflection of the serratus anterior muscle. According to the computed tomography scan, MRI, and clinical palpation of the upper rib interspaces, a decision is made to enter the chest cavity either in the fourth or fifth intercostal space. Care must be taken to enter at least 1 or 2 rib spaces below the tumor. The initial opening of the chest should be at least at the midpoint of the rib or more anteriorly for larger tumors. With a limited opening sufficient to palpate the inside of the chest cavity, a decision is made to either extend along the top of the fourth rib or the top of the fifth rib. Ideally, the interspace is chosen to minimize floating ribs at closure. If it is possible to maintain the fifth through 12th ribs intact as a unit, this procedure will improve the patient's postoperative chest wall mechanics.
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      3 Once the interspace has been divided, the initial rib retractor is placed to permit palpation of the lung in its entirety and the pleural and diaphragmatic surfaces to rule out intrathoracic metastatic spread. Once this area has been ascertained to be clear, then the initial limited posterolateral thoracotomy is extended to a fully extended posterolateral thoracotomy, with the incision continuing to the midline at the base of the neck at least to the level of the T1 spinous process. The extended posterolateral thoracotomy requires the division of the trapezius muscle and rhomboids to the base of the neck. A Burford retractor with a shallow and a deep blade is positioned with the crank on the assistant's side of the table. The large blade is positioned beneath the scapula, and the shallower blade is placed on the lower rib, which permits elevation of the scapula away from the thoracic inlet, freeing the assistant to help the surgeon with the dissection without any need for scapular retraction. Progressive elevation of the scapula provides an excellent view of the entire apex of the chest cavity.
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      4 The lung is now deflated. Care is taken to minimize the ventilatory pressure on the down lung and to reduce the FiO2 but to maintain the O2 saturations as monitored by a continuous O2-saturation monitor. With the lung deflated, a hand is inserted along the inside of the chest cavity to ascertain the extent of chest wall involvement by the tumor.
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      5 The initial chest wall division will include the anterior ribs. At least a 3- to 5-cm margin is taken anteriorly. The ribs are divided in sequence. The rib of the interspace that was entered is initially divided with clipping, ligation, or cautery of the intercostal vessels. The ribs are divided with rib shears, and small segments of the anterior rib edges are removed and sent as margins for permanent sectioning. This process also permits better visualization and mobility of the chest wall during the rest of the resection of the anterior portions of the ribs.
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      6 The scalenus posterior muscle is divided from its attachment with the second rib. For superior sulcus tumors that extend more anteriorly, a greater margin of the scalene posterior muscle is taken in case the tumor extends into this muscle.
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      7 The first rib is identified and the periosteum is gently scored with electrocautery. By using a cob elevator, a subperiosteal dissection of the first rib is performed. Again, depending on the anterior extent of this posteriorly situated tumor, it may be necessary to divide the insertion of the scalenus anterior muscle as it inserts into the tubercle of the first rib. The subclavian vessels are gently swept superiorly by blunt digital dissection. Care must be taken to completely clear all soft tissues away from the proposed site of division of the first rib.
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      8 The first rib is divided with a hooked first-rib shear or a Gigli saw. When using a Gigli saw, it is important to protect the soft tissue superiorly to avoid any inadvertent injury to the subclavian vessels or brachial plexus. Injury to the subclavian vessels at this point would be problematic because proximal control and repair may be difficult.
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      9 The paraspinal musculature is dissected away from the junction of the rib and transverse process. For tumors that are more extensive and by MRI imaging extend into the paraspinal musculature, then en bloc resection of the muscles with the tumor is performed. In the typical posterior superior sulcus tumor, which often involves the first and second ribs only, the paraspinal musculature usually can be preserved. The costotransverse ligaments are identified and divided with electrocautery. Sequentially, the rib heads are disarticulated from the transverse processes, from the more distal to proximal ribs. A cob elevator is used to “lift” the rib head and neck away from the transverse process and vertebral body. One should never lever on the transverse process. This maneuver is similar to the techniques of an anesthesiologist intubating a patient with a laryngoscope. The force is a lifting motion to elevate the larynx rather than lever the blade of the laryngoscope on the upper incisors. Force is always directed away from the neural foramina, therefore avoiding any risk of inadvertent entry into the neural foramina, with possible spinal cord injury. Tumor involvement can destroy the bone and weaken this area and cause a serious neurologic injury if these principles are not adhered to.
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      10 The assistant applies rotational pressure anteriorly to rotate the ribs away from the transverse process as the surgeon elevates the rib away from the vertebral body. This rotational pressure permits “opening” of the costotransverse joints. As these joints open up, the intercostal nerves and vessels can be identified and ligated or clipped.
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      11 As the ribs are disarticulated from inferior to superior, special attention must be placed in the region of the first and second ribs. The neck of the first rib courses immediately between the very large T1 nerve root and the C8 nerve root. The T1 nerve root can be identified as a very broad structure coursing anteriorly and superiorly from the surgeon's view at an angle of approximately 60°, at which point it joins the C8 root just below the neck of the first rib. The T1 root has both a motor and a sensory component.
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      12 The disarticulation of the first rib is technically the most difficult and carries with it the greatest risk of injury to the nerve roots. The first rib is almost a hook that must be gently rotated out of its joint through the use of a small cob that is gently placed in the joint with slight rotation to loosen the ligaments that are attached. A distinct sensation can be appreciated when the rib has been loosened. The neck of the first rib is grasped with a Kocher clamp, which facilitates the outward rotation of the first rib, again taking care to avoid injury to the C8 and T1 nerve roots. With the rib now rotated out of the joint, the soft tissues superiorly are cauterized to free the most posterior insertion of the scalene muscles.
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      13 Neurolysis occurs along the C8 root, and the junction between C8 and T1 is closely observed. The T1 root may be simply compressed by the superior sulcus tumor, in which case a neurolysis should be all that is required to free the T1 root. Often, however, the T1 root is involved with tumor and must be resected with the specimen. The T1 root can be sacrificed with very little change in hand function. The root is sharply divided at its junction with the C8 root. Care is taken to avoid sacrificing the C8 root if at all possible because this will significantly impair the intrinsic hand function of the patient.
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      14 After either neurolysis of the C8 and T1 roots or division of the T1 root, the sympathetic chain is next divided, along with some ligation of intercostal veins. Care must also be taken at this point because occasionally the vertebral artery, as it courses toward the cervical spine, can have a downward trajectory and can be injured. The dissection is extended with an apical pleurectomy and dissection of Sibson's fascia as it extends up into the neck. The pleural dissection is also extended onto the anterior portion of the vertebral body to include the prevertebral fascia. Once a clear margin is identified, then the pleura and prevertebral fascia are incised with electrocautery and extended up toward the neck. Often, the longus coli muscle may also be infiltrated and can be dissected high into the neck, as well as from the posterior approach. The lobe and chest wall have now been completely mobilized. At this point, for small apical tumors, the chest wall and tumor can be separated from the lobe with a series of linear (GIA) stapler firings. The specimen can be handed off and can be processed for frozen section analysis by the pathologist while a completion lobectomy and mediastinal lymphadenectomy is performed. Removal of the chest wall at this point minimizes some of the weight of the specimen that could result in a torsional injury to the delicate hilar vessels during the dissection of the hilum. Tumors that extend more centrally cannot be removed before the formal anatomic dissection. At this point, the vertebral bodies are closely examined. If there is any suggestion of involvement of the vertebral body or neural foramina, a spinal surgeon is consulted about performing either a foraminotomy or partial or complete vertebrectomy through this extended posterolateral thoracotomy exposure. Extended resections, including several level vertebral body resections with anterior and posterior stabilization, may be required for complex lesions. Provided no vertebral body work needs to be done, then the chest wall defect is closed by using a double layer of polypropylene mesh anchored to the transverse processes posteriorly and then pulled taut anteriorly and placed into the second, third, and fourth or fifth ribs anteriorly. The patient is positioned in a reverse flection to elevate the legs, and a very taut closure is then performed to the remaining ribs inferiorly. Large chest tubes are placed before the closure. Smaller resections do not require prosthetic closure of the chest wall because the overlying scapula and chest wall musculature are sufficient protection, despite the posteriorly resected ribs. For lesions that extend down to the fourth or fifth ribs, however, the mesh reconstruction is required to avoid scapula tip entrapment postoperatively. If a mesh reconstruction is not used, then a partial scapular tip resection needs to be performed. Patients postoperatively often require 24 to 48 hours of ventilatory support for the larger chest wall resections because the loss of the scalene musculature into these upper ribs accounts for a greater volume loss than would be expected after a routine lobectomy that would be performed without a concomitant chest wall resection. Reconstruction of the chest wall defect may improve some of the chest wall mechanics that can occur from these apical chest wall resections.

      Comments

      Superior sulcus tumors provide a unique challenge to the thoracic surgeon because of their anatomic location and often direct invasion into bone and neurovascular structures. An extended posterolateral thoracotomy and retraction of the scapula away from the apex of the chest facilitates the dissection of the brachial plexus and the subclavian vessels. Tumors with complex chest wall involvement, including the vertebral body, pedicles, and transverse processes, can be resected. Postoperatively, the patients often require vigorous pulmonary toilet and gentle range of motion exercises of the shoulder complex to minimize postoperative shoulder immobility. Specific complications that can arise from vertebral body resections include cerebrospinal fluid leaks that require primary repair and, often, autogenous tissue coverage. Special care must be taken in the wound closure and early ambulation of the patients to avoid any pressure necrosis of the skin and soft tissues overlying what may be an extensive posterior instrumentation and hardware. We have gained experience now in more than 30 extended posterior sulcus resections that have included the vertebral body on our institutional protocol. Two-year survival even in this patient subset of T4 vertebral body involvement has been more than 54%. Although aggressive surgical techniques have improved the local control of their potentially devastating tumors, distant metastatic disease still remains a biologic challenge in these patients.
      • Komaki R
      • Cox JD
      • Putnam Jr, JB
      • et al.
      The management of superior sulcus tumors.
      • Walsh GL
      • Gandhi S
      • Komaki R
      Management of superior sulcus tumors.
      • Walsh GL
      Invited commentary: superior sulcus tumor resection: posterior approach.

      Acknowledgements

      The author wishes to acknowledge the artists, Ian Suk and Gary Wind, for their contributions to the article.

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        • et al.
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        • Putnam Jr, JB
        • Walsh G
        • et al.
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        • Roth JA
        • Walsh GL
        • et al.
        Outcome predictors for 143 patients with superior sulcus tumors treated by multidisciplinary approach at The University of Texas M. D. Anderson Cancer Center.
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