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En Bloc Resection of Thoracic Tumors Involving the Spine

      Thoracic tumors involving the spine are challenging to manage. Successful treatment requires multidisciplinary surgical and oncological care. The most common subsets of such tumors encountered by thoracic surgeons are non-small-cell lung carcinomas (NSCLC) of the superior sulcus (Pancoast tumors) or posterolaterally located NSCLC involving the costovertebral junction or spine. Involvement of the spine and brachial plexus has traditionally portended a poor prognosis. Patients with tumors involving the spine are considered to have Stage IIIB disease, which until recently was considered unresectable for cure. However, newer techniques for resection, improvements in instrumentation for spine stabilization,
      • Komagata M.
      • Nishiyama M.
      • Imakiire A.
      • et al.
      Total spondylectomy for en bloc resection of lung cancer invading the chest wall and thoracic spine.
      • Mazel C.
      • Grunenwald D.
      • Laudrin P.
      • et al.
      Radical excision in the management of thoracic and cervicothoracic tumors involving the spine: results in a series of 36 cases.
      • York J.E.
      • Walsh G.L.
      • Lang F.F.
      • et al.
      Combined chest wall resection with vertebrectomy and spinal reconstruction for the treatment of Pancoast tumors.
      • Gandhi S.
      • Walsh G.L.
      • Komaki R.
      • et al.
      A multidisciplinary surgical approach to superior sulcus tumors with vertebral invasion.
      • Bilsky M.H.
      • Vitaz T.W.
      • Boland P.J.
      • et al.
      Surgical treatment of superior sulcus tumors with spinal and brachial plexus involvement.
      • Martin L.W.
      • Walsh G.L.
      Vertebral body resection.
      and advances in combined modality therapy, particularly preoperative chemoradiotherapy,
      • Rusch V.W.
      • Giroux D.J.
      • Kraut M.J.
      • et al.
      Induction chemoradiation and surgical resection for superior sulcus non-small cell lung carcinomas: long-term results of Southwest Oncology Group trial 9416 (Intergroup trial 0160).
      have made curative resection possible.
      Complete resection of superior sulcus tumors or other NSCLC involving the spine must take into account the degree of spinal and brachial plexus involvement. Radiographic spine assessment includes both computed tomography (CT) scan and magnetic resonance imaging (MRI). The MRI is critical for evaluating the extent of neuro foraminal and epidural tumor involvement. Although overtly lytic disease in the vertebral body will be obvious on CT, MRI is necessary to identify more subtle signs of infiltrative bone disease of the vertebral body or posterior elements, which may be seen as hypointensity on T1-weighted images or hyperintensity on T2 fat-suppressed short-tau inversion recovery sequences. Such infiltrative disease visualized on MRI may need to be addressed by both radiation therapy and resection. On this basis, a MRI classification was devised to facilitate decision-making regarding the extent of spinal elements requiring resection and the need to provide instrumented fusion.
      Class A tumors involve the periosteum of the vertebral body, whereas class B tumors extend to the proximal rib head and distal neural foramen. These tumors are both approached via a posterolateral thoracotomy with chest wall resection and multilevel rhizotomy. The transverse processes are sectioned at the articulation of the pars interarticularis lateral to the pedicle to achieve an en bloc resection at the level of the distal neural foramen. Class C tumors show extension of the tumor into the distal neural foramen and epidural space, whereas class D tumors extend to include the vertebral body and/or posterior elements (Figure 1, Figure 2). Both of these tumor types typically require instrumented fusion.
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      Figure 1Classification of thoracic tumors involving the spine. Class A tumors involve the periosteum of the vertebral body. Class B tumors extend to the proximal rib head and distal neural foramen. Class C tumors show extension of the tumor into the distal neural foramen and epidural space. Class D tumors extend to include the vertebral body and/or posterior elements.
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      Figure 2CT and MRI images demonstrating the radiologic findings of the classification of tumors involving the spine. As outlined in , these findings correspond to classes A, B, C, and D tumors, as labeled.
      Class A and B tumors are amenable to pulmonary resection with en bloc removal of the involved chest wall and transverse process. However, the traditional concept that a curative resection must use an en bloc technique to achieve wide or marginal margins is violated in class C and D tumors. En bloc resection in the presence of epidural or massive paraspinal tumors (ie, chest wall and lung involvement) is contraindicated according to the Weinstein, Boriani, Biagini classification used by spine surgeons to assess for the possibility of achieving negative margins using en bloc techniques.
      • Boriani S.
      • Weinstein J.N.
      • Biagini R.
      Primary bone tumors of the spine Terminology and surgical staging.
      The rationale for curettage resection of the epidural and vertebral body tumor component in class C and D tumors is twofold: (1) prevention of spinal cord injury; (2) the effectiveness of induction chemoradiotherapy and the evolution of image-guided intensity modulated radiotherapy (IGRT) in reducing the tumor to microscopic disease. Recent clinical trials have shown that in patients with superior sulcus NSCLC, induction chemoradiotherapy increases the rate of R0 resection and substantially improves 5-year overall survival relative to previous experience with preoperative radiation alone. The improved results with this combined modality approach were observed both in patients with T3 tumors and in those with T4 tumors involving the spine. IGRT has not generally been used for superior sulcus tumors but has been used extensively for spine tumors.
      In general, patients with paraspinal tumors with spinal involvement (ie, Class C and D tumors) need to be properly assessed for the most effective therapy to salvage neurologic function and spinal stability. The majority of patients who have high-grade spinal cord compression resulting from radioresistant tumor (eg, NSCLC) and/or who demonstrate gross spinal instability require surgery for decompression and stabilization followed by radiation for local tumor control.
      Conventional external beam radiation (ie, 30 Gy in 10 fractions) is effective therapy for patients with markedly radiosensitive tumors, such as multiple myeloma or lymphoma. Unfortunately, most spinal tumors, both primary and metastatic, are relatively radioresistant to doses that can be delivered below spinal cord tolerance. Using standard-fraction therapy (120 to 200 cGy/fraction), NSCLC in the lung is often treated to doses in excess of 60 Gy, whereas the TD5/5 of the spinal cord (toxic dose at which 5% of patients develop myelitis at 5 years) is 50 Gy. Recently, IGRT has been applied to spinal tumors. The advantage of IGRT is the ability to deliver cytotoxic doses of radiation while sparing spinal cord tolerance. With the exception of patients who have high-grade epidural spinal cord compression, IGRT can now be used to deliver doses in excess of 60 Gy to paraspinal NSCLC without causing spinal cord injury. Additionally, for metastatic and primary tumors, IGRT can be used to deliver single-fraction therapy (24 Gy). Single-fraction therapy markedly increases the biologic effective dose, particularly for radioresistant tumors. This translates into extraordinary local tumor control for radioresistant metastatic tumors without inducing spinal cord toxicity. At Memorial Sloan-Kettering Cancer Center, we are now exploring the use of IGRT as neoadjuvant therapy for primary tumors, such as superior sulcus tumors and chordoma tumors.

      Operative Technique

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      Figure 3Illustration of the thoracotomy incision for resection of class A and B tumors. The dotted line indicates the relationship of the posterolateral thoracotomy incision to the scapula and spine. A vertical incision is created midway between the spinous processes and the medial border of the scapula starting at the base of the neck and is extended around the inferior border of the scapula. In patients with superior sulcus NSCLC, the incision can then be carried anteriorly up to the axilla (so-called transcapular approach) to facilitate elevation of the scapula and exposure to the apex of the hemithorax.
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      Figure 4The scapula is mobilized from the chest wall by detaching the insertion of the serratus anterior muscle and dividing the rhomboids and levator scapulae muscles. The tip of the scapula can then be elevated by an internal mammary self-retaining retractor. The paraspinal muscles are elevated to expose the transverse processes, pars interarticularis, and laminae. Care is taken not to divide the interspinous ligaments because this would render the spine unstable and promote scoliosis in combination with extensive chest wall resection.
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      Figure 5This figure shows the plane of resection for class A and B tumors. Although simple disarticulation of the rib from the transverse process has sometimes been used for resection of class A tumors, the line of resection shown is most likely to achieve a complete (R0) resection whether the extent of the tumor is class A or class B. Careful attention must be paid to identifying the junction of the transverse processes, pars interarticularis, and laminae. Sectioning the spine at the base of the transverse process, but distal to the pars interarticularis, will allow one to preserve the facet joints and pedicle. This anatomic definition ensures that the spinal canal will not be breached.
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      Figure 6The anterior, superior, and inferior parts of the chest wall resection are performed first (not shown). A medium curved osteotome is then used to resect the base of the transverse process, as shown. The osteotome is used to cut tangential to the pars interarticularis through the transverse process.
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      Figure 7Forward traction is then applied to the anterior part of the resected chest wall to help gain exposure to the nerve roots. These are dissected free with tenotomy scissors and individually ligated with vascular clips. Failure to ligate the nerve roots can lead to a leak of cerebrospinal fluid and pneumocephalus.
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      Figure 8This figure shows the resected specimen. Once the chest wall resection is completed, en bloc resection of the underlying lung is performed. This may be either a wedge resection (as shown) or, more commonly, in patients with primary NSCLC, a lobectomy. In patients with superior sulcus NSCLC, the T1 nerve root may or may not be resected depending on the extent of tumor involvement. If there appears to be tumor involvement clinically, multiple biopsies are taken from the epineurium to establish whether tumor is present microscopically. This is particularly important in patients who have received induction chemoradiotherapy and have significant residual perineural fibrosis that makes it difficult to assess the extent of the tumor. Resection of the T1 nerve root can result in significant hand weakness. It should be recognized that the T1 nerve root exits the T1 to 2 neural foramen and traverses anterior to the first rib to join the lower trunk of the brachial plexus. Care must be taken to identify and preserve the C8 nerve root, which, if divided, leads to profound hand and arm weakness. After the chest wall and pulmonary resection are completed, the chest wall defect is reconstructed (not shown) and the thoracotomy incision is closed in the standard manner.
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      Figure 9Management of class C tumors that extend into the epidural space usually requires a posterolateral laminectomy performed with the patient in the prone position followed by a posterolateral thoracotomy. A posterolateral laminectomy includes resection of the lamina, pedicle, and facet joint to facilitate the resection of anterior, posterior, and lateral epidural disease. The extent of epidural tumor determines the number of laminae and whether unilateral or bilateral pedicles and joints need to be resected. Epidural tumor is resected and the transverse processes are sectioned from the epidural space with vascular clips. The transverse processes are also osteomized at this point.
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      Figure 10A posterolateral laminectomy renders patients unstable and should be addressed with a instrumented fusion. Cervicothoracic instrumentation is currently addressed with pedicle screws in the thoracic spine and lateral mass screws in the cervical spine. The rod that engages the screw heads tapers from a 6.25-mm rod to a 3.5-mm rod. This provides excellent stabilization over the cervicothoracic junction. Many superior sulcus tumor patients have significant osteoporosis based on a long smoking history and postmenopausal status. Bone cement augmentation of the screws will help prevent pullout until arthordesis potentially occurs. Autologous and allograft bone are placed along the lateral spine. Ao = aorta; Esoph = esophagus.
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      Figure 11Class D tumors involve the vertebral body and often the epidural space as well. Vertebrectomy can be accomplished as an extension of the posterolateral laminectomy or following the posterolateral thoracotomy. Following a posterolateral thoracotomy with en bloc chest wall resection, the involved vertebral body is identified. The disc spaces superior and inferior to the vertebral body are resected. Intralesional vertebral body resection is then accomplished. If epidural tumor is present, the posterior longitudinal ligament should be resected to provide a margin on the anterior dura. Anterior reconstruction can be accomplished by a number of methods including iliac crest or fibula autograft or allograft, polyetheretherketone carbon fiber or titanium cage, or polymethylmethacrylate and Steinman pins. For stand-alone reconstructions, an anterior plate or screw rod system will compress the graft into place. Currently, our preference for patients requiring vertebral body resection is to augment with posterior cervicothoracic fixation as well.

      Postoperative Care

      The postoperative care of patients after resection of thoracic tumors involving the spine is similar to that of all patients following major thoracotomy. Excellent respiratory care and pain management are critical to avoiding complications after these extensive operations. Epidural analgesia may or may not be possible depending on the extent of the spine resection and should be discussed preoperatively with the anesthesiology pain management team and with the spine surgeon. Mobilization of the patient out of bed is usually possible immediately postoperatively unless the spine surgeon has concerns about either spine stability or postoperative neurologic deficit. Frequent neurological monitoring of lower extremity function and bowel and bladder function is important during the first postoperative week especially in the patient undergoing resection of class C and D tumors. The use of corticosteroids may be necessary during the first week postoperatively depending on whether the spine surgeon considers this appropriate to reduce spinal cord edema and preserve neurological function. Any evolving neurological deficits during this period may require additional urgent imaging studies for evaluation, and rarely, additional surgical intervention by the spine surgeon if the clinical examination and imaging studies suggest spine instability and cord compression. Therefore, multidisciplinary postoperative care by the thoracic surgeon and the spine surgeon is key to a successful outcome.
      Physical therapy is important to helping the patient return to their preoperative functional level. For patients undergoing resection of superior sulcus NSCLC via a high posterolateral thoracotomy incision, range of motion and strengthening exercises starting during the first 2 weeks postoperatively and continuing for several months will prevent the development of a frozen shoulder and will maintain hand function. Patients with class C and D tumor resections who have neurological deficits in lower extremity, bowel, or bladder function may require several months of physical therapy directed to the correction of those deficits. The need for physical therapy should be evaluated and treatment initiated during the immediate postoperative period in the hospital and continued on an outpatient basis.
      Wound infection or breakdown can occur because of the extensive nature and duration of these operations, the use of instrumentation for spine stabilization and prostheses for chest wall reconstruction, and the use, in some cases, of preoperative radiation. Consideration should be given to this risk preoperatively as the thoracic and spine surgeons jointly plan the operation with respect to the incisions required and the availability of well-vascularized soft-tissue coverage.
      In summary, extensive primary thoracic tumors involving the spine that were formerly considered unresectable and incurable are now amenable to complete resection with an excellent chance for long-term survival and good quality of life. The success of such treatment depends on careful multidisciplinary surgical and oncological care and the use of newer surgical techniques and instrumentation.

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