Tumors of the thoracic apex, even when benign,

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1 Anterior Cervical Transsternal Approach for Resection of Benign Tumors at the Thoracic Inlet George Ladas, MD, Peter H. Rhys-Evans, FRCS, and Peter Goldstraw, FRCS Department of Thoracic Surgery, Royal Brompton Hospital, London, England Background. Neural tumors at the thoracic apex, even when benign, present technical problems for the surgeon because of their inaccessibility. The standard approach from below, using a posterolateral thoracotomy, offers suboptimal access to the vascular and neural structures of the thoracic inlet. Methods. We present a new technique for the resection of benign tumors of the thoracic inlet, combining an anterior cervical approach with a limited median sternotomy. We do not find it necessary to resect any part of the clavicle or to add a thoracotomy. We used this technique in 4 patients with apical tumors. In 3 patients the tumor arose from the sympathetic chain and in 1 patient from the T1 component of the brachial plexus. Results. The tumors ranged from 30 to 70 mm in diameter, and histologic findings were neurilemoma in 3 cases and ganglioneuroma in 1. There were no complications or deaths. All 4 patients were discharged 3 to 6 days postoperatively. Conclusions. In our experience this new technique provides improved exposure, good control of the neurovascular bundle, and less morbidity than that associated with thoracotomy. For malignant Pancoast s tumors we would still advocate the approach of Dartevelle or Grunenwald, supplemented by lateral thoracotomy to facilitate systematic intrathoracic evaluation. (Ann Thorac Surg 1999;67:785 9) 1999 by The Society of Thoracic Surgeons Tumors of the thoracic apex, even when benign, present technical problems for the surgeon because of their inaccessibility. The standard approach from below, using a posterolateral thoracotomy, offers limited exposure of the vascular and neural structures of the thoracic inlet that lie at the superior aspect of these tumors. Thus, the surgeon often has to perform the most critical part of the operation when reaching the limits of the available exposure. As a result of our experience with the approach by Dartevelle and colleagues [1] for Pancoast s tumors, we developed a technique for the resection of neural tumors of the thoracic inlet, using an anterior cervical approach together with a limited median sternotomy. We have not found it necessary to resect any part of the clavicle or to add a thoracotomy, but these procedures are an option if the tumor is found to be malignant and invading adjacent structures. Material and Methods Technique The patient is placed in a supine position, with the head hyperextended and turned away from the operating side. We use an anterior cervical incision from the level of the thyroid cartilage extending downward along the anterior border of the sternocleidomastoid muscle onto the upper sternum (Fig 1). A limited sternotomy is performed, splitting the manubrium at the midline initially and then Accepted for publication July 21, Address reprint requests to Mr Goldstraw, Department of Thoracic Surgery, Royal Brompton Hospital, Sydney St, London SW3 6NP, England. laterally toward the operated side to end at an intercostal space. We do not resect any part of the clavicle. After mobilization of the sternocleidomastoid, the muscle is reflected laterally. With very large tumors, when wider exposure is necessary, the muscle may be divided close to its lower insertions, leaving enough length for it to be reattached at the end of the operation. The omohyoid and sternohyoid muscles are divided. The inferior thyroid vessels are divided, and the thyroid is reflected medially (Fig 2). The recurrent laryngeal nerve is exposed and mobilized caudally. The sheath of the neurovascular bundle of the neck is opened, and the internal jugular vein, common carotid artery, and vagus nerve are identified and mobilized. Depending on the location of the tumor, these structures can then be reflected medially or laterally. The subclavian vein is reflected inferiorly. On the left the thoracic duct is identified and preserved or ligated. The scalene fat pad is excised and the phrenic nerve exposed on the scalenus anterior muscle. The transverse cervical vessels, passing superficial to the phrenic nerve, serve as a landmark and can then be divided (Fig 3). The phrenic nerve is mobilized and reflected medially, and the scalenus anterior muscle can then be divided, giving access to the subclavian artery and the brachial plexus. These structures are freed from the upper surface of the tumor by blunt dissection. The subclavian artery is mobilized and reflected inferiorly, giving excellent access to the posterior aspect of the thoracic inlet, the neck of the first rib, the T1 component of the brachial plexus, and the sympathetic trunk (Fig 4). The posterior scapular branch of the transverse cervical 1999 by The Society of Thoracic Surgeons /99/$20.00 Published by Elsevier Science Inc PII S (98)01323-X

2 786 LADAS ET AL Ann Thorac Surg CERVICAL APPROACH TO THORACIC INLET 1999;67:785 9 Fig 1. The skin incision is placed along the anterior border of the sternocleidomastoid extending from the level of the thyroid cartilage downward onto the upper sternum. artery is a useful landmark, running between the C6 and C7 roots of the brachial plexus. It is now possible to clearly identify the structure from which the tumor arises and to divide it with healthy Fig 3. The common carotid artery (1) and vagus nerve (2) are retracted medially, exposing the scalenus anterior muscle with the phrenic nerve (3) and brachial plexus. The forceps points at the transverse cervical vessels. The brachial plexus is accessible once the scalenus anterior muscle is divided. margins, after which, using blunt dissection above and below, the tumor is delivered from within the chest to the neck. Resection of the tumor is usually achieved without breaching the parietal pleura. The bed of the resected tumor is drained with a suction drain and the wound is closed. In the case of neurogenic tumors, in which the sacrifice of some components of the brachial plexus is necessary, we start intensive physiotherapy as soon as possible postoperatively. Patients Four patients with neural tumors of the thoracic inlet underwent operation using the present technique at the Royal Brompton Hospital between October 1994 and October They were all women, with a mean age of 56.5 years (range, 50 to 67 years). Their clinical data are summarized in Table 1. A thorough preoperative clinical assessment, including documentation of neurologic status was performed in all cases, and imaging investigations included chest radiography and computed tomography. In patient 4 we also performed a bone scan and a magnetic resonance imaging scan, to clarify the local extent, and to exclude an intraspinal extension; and Doppler ultrasound and digital subtraction angiography, to exclude arterial aneurysm or invasion of the subclavian artery. Fig 2. The manubrium has been divided, as well as the strap muscles. The sternocleidomastoid is retracted laterally and the thyroid gland medially. (1 sternum; 2 thyroid; 3 recurrent laryngeal nerve; 4 common carotid artery; 5 tumor.) Results Table 2 summarizes the operative data and final histologic results. The operation was uneventful in all cases.

3 Ann Thorac Surg LADAS ET AL 1999;67:785 9 CERVICAL APPROACH TO THORACIC INLET 787 Table 1. Clinical Data of Four Female Patients Pt No. Age (y) Sex Tumor Site Presentation 1 55 F Left apex Four-month history of painless mass at root of neck 2 54 F Right apex Granulomatous uveitis; apical opacity on CXR 3 50 F Left apex Apical opacity on CXR 4 67 F Right apex Six-year history of right arm and hand pain of ulnar distribution; painless mass at root of neck CXR chest radiograph; F female; Pt patient. Fig 4. The complete dissection after removal of the tumor mass. (1 common carotid artery; 2 innominate vein; 3 subclavian artery; 4 vertebral artery; 5 internal jugular vein; 6 vagus nerve; 7 recurrent laryngeal nerve.) There were no complications attributable to the technique and no deaths. Patient 4 had a bulky tumor arising from the T1 component of the brachial plexus (Fig 5), tightly wedged and completely filling the apex of the right chest. It was expanding within the arc of the first rib, scalloping the medial margin, and leaving a sharp edge. The tumor was bulging anteriorly, displacing and compressing the subclavian vessels. In this particular patient the thickened parietal pleura was opened in the course of tumor mobilization. At the end of the procedure, an intrapleural drain was used in addition to the standard neck drain, but a thoracotomy was not necessary. Postoperatively this patient developed a motor and sensory deficit consistent with the division of the T1 root of the brachial plexus. In all cases complete resection of the tumor was achieved, with optimal exposure and control of the vital structures. After the operation, patients 1, 2, and 3 developed Horner s syndrome, together with anhydrosis and vasodilatation of the arm and hand on the operated side, as expected. The postoperative hospital stay ranged from 3 to 6 days (mean, 4 days). Histopathologic results showed all tumors to be benign and of neural origin. Special immunocytochemical stains (S 100, SMA) were necessary to secure the diagnosis in patients 1 and 2. On follow-up, all patients remain well and free from recurrence. Patients 1, 2, and 3 reported early resumption of full activity shortly after their discharge. All our patients found the anterior cervical scar acceptable. Comment Benign tumors of the thoracic inlet are rare entities that may originate from any of the tissues in the area or may extend from adjacent structures. Tumors of neural origin (neurilemomas, ganglioneuromas, and paragangliomas) are the most common, arising from the sympathetic chain, the brachial plexus, or other nerves. Complete resection is justified to establish the diagnosis or to relieve or prevent compressive symptoms and because of the concern as to malignancy (2% to 3%) or the later development of malignant change [2]. When dealing with such neural tumors we do not find the use of fine-needle aspiration biopsy helpful in securing a preoperative diagnosis of malignancy. However, magnetic resonance imaging can demonstrate the presence or absence of invasion of adjacent structures and is helpful when assessing large symptomatic tumors of this area, as was the case with patient 4 in our series (Fig 5C). Tumors of the thoracic inlet have always presented particular technical problems for the surgeon because of Table 2. Operative Data for Four Female Patients Pt No. Final Histologic Results Tumor Origin Tumor Size (mm) Immunostaining Postop Stay (days) Resection 1 Benign schwannoma Sympathetic chain S 100, SMA 3 Complete 2 Benign schwannoma Sympathetic chain 23-mm diameter S Complete 3 Benign Sympathetic chain Complete ganglioneuroma 4 Benign schwannoma Brachial plexus (T1 root) Complete Postop postoperative; Pt patient.

4 788 LADAS ET AL Ann Thorac Surg CERVICAL APPROACH TO THORACIC INLET 1999;67:785 9 Fig 5. (A) Chest radiograph of a 67-year-old woman presenting with a 6-year history of right arm and hand pain of ulnar distribution and an ipsilateral painless mass at the root of the neck. A round opacity with smooth margins occupies the right apex. (B) Computed tomographic scan shows the soft tissue mass extruding through the thoracic apex, displacing the subclavian vessels anterolaterally. It proved to be a benign schwannoma arising from the T1 component of the brachial plexus. (C) Magnetic resonance imaging scan of the same patient showing a soft tissue mass wedged at the apex. Although there is a fat plane around the mass laterally and medially, its superior aspect is closely associated with the neurovascular bundle. their close association with the important vascular and neural structures of the root of the neck and their inaccessibility through the posterolateral thoracotomy. Various alternative approaches have been proposed in the past, but none has become popular [3, 4]. The anterior transcervical thoracic technique proposed by Macchiarini and colleagues [5], although providing a safe and effective approach, is technically demanding, and when dealing with benign disease, the functional and cosmetic results are probably not justified. An anterior cervical incision extending along the border of the sternocleidomastoid muscle has been traditionally used for carotid artery operation. This incision is well suited for dealing with trauma to the large vessels at the base of the neck and has been combined with partial sternotomy or removal of the clavicle for proximal control of the brachiocephalic vessels [6]. A hockey-stick oblique anterolateral cervical incision combined with a median sternotomy has been in use for the resection of large lymphangiomas (cystic hygromas) extending from the neck to the anterior mediastinum [7, 8]. The use of video assisted thoracic surgical intervention for resection of intrathoracic neural tumors not extending to the spinal canal has been reported [9]. We believe that a video assisted thoracic surgical approach can be useful when dealing with small, benign mediastinal tumors, but when there is involvement of the thoracic inlet, such an approach suffers from the same disadvantages as lateral thoracotomy. Our technique offers excellent exposure of the structures of the thoracic inlet and permits safe and controlled resection of benign neural tumors of this area, even when very large or wedged among the surrounding structures. Because these benign tumors are only loosely attached to the surrounding structures, mobilization from above is easily performed. The tumor can then be simply delivered into the neck. Compared with thoracotomy, the anterior cervical transsternal approach is quick and safe, allowing much better control of the neurovascular structures. The incision is less painful than a high posterolateral thoracotomy, resulting in much lower postoperative discomfort, reduced requirement for analgesics, speedy and complete mobilization, and a shorter postoperative stay. Our patients found the esthetic result to be satisfactory. When using this approach, one has the option of extending the exposure by utilizing the techniques of Dartevelle and colleagues [1] or Grunenwald and associates [10] if a tumor is found intraoperatively to be invading the surrounding structures.

5 Ann Thorac Surg LADAS ET AL 1999;67:785 9 CERVICAL APPROACH TO THORACIC INLET 789 Once familiar with the anatomy of this complex area, we have found the exposure excellent and the results satisfactory. We have since extended the indications for this approach to include metastatic tumors of the thoracic inlet. For malignant tumors of the thoracic inlet and Pancoast s cancers, we would still advocate an approach similar to that of Dartevelle and associates. References Fig 6. (A) Preoperative chest radiograph from patient 2, with a smooth, rounded opacity at the right apex. (B) Preoperative computed tomographic scan showing the tumor, which was a benign schwannoma arising from the sympathetic chain. 1. Dartevelle P, Chapellier AR, Macchiarini P, et al. Anterior transcervical-thoracic approach for radical resection of lung tumors invading the thoracic inlet. J Thorac Cardiovasc Surg 1993;105: Shields T. Primary lesions of the mediastinum and their investigation and treatment. In: Shields TW, ed. General thoracic surgery. Philadelphia: Williams & Wilkins, 1994: Masaoka A, Ito Y, Yasumitsu T. Anterior approach for tumor of the superior sulcus. J Thorac Cardiovasc Surg 1979;78: Roos DB. Transaxillary thoracic outlet decompression and sympathectomy. In: Bergan JJ, Yao JST, eds. Techniques in arterial surgery. Philadelphia: WB Saunders, 1990: Macchiarini P, Dartevelle P, Chapellier A, et al. Technique for resecting primary and metastatic nonbronchogenic tumors of the thoracic outlet. Ann Thorac Surg 1993;55: Flint LM, Snyder WH, Perry MO, et al. Management of major vascular injuries in the base of the neck. Arch Surg 1973;106: Kirschner PA. Cervicomediastinal cystic hygroma: one stage excision in an 8-week old infant. Surgery 1966;60: Grosfeld JS, Weber TR, Vane DW. One stage resection for massive cervicomediastinal hygroma. Surgery 1982;92: Landreneau RJ, Dowling RD, Ferson PF. Thoracoscopic resection of a posterior mediastinal mass. Chest 1992;102: Grunenwald D, Spaggiari L. Transmanubrial osteomuscular sparing approach for apical chest tumors. Ann Thorac Surg 1997;63:563 6.