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Eur J Cardiothorac Surg 1999;15:774-780
© 1999 Elsevier Science NL

Antero-superior approaches in the practice of thoracic surgery

Department of Thoracic Surgery, Royal Brompton Hospital, London, UK

Received 21 October 1998; received in revised form 23 February 1999; accepted 11 March 1999.

Corresponding author. Tel.: +44-171-351-8559; fax: +44-171-351-8560
e-mail: p.goldstraw{at}rbh.nthames.nhs.uk

	Abstract

Top Abstract 1. Introduction 2. Patients and methods... 3. Results 4. Discussion References

 
Objective: To review our experience using antero-superior approaches for resection of a heterogeneous group of tumors, both benign and malignant, involving the thoracic inlet and adjacent structures. These included Pancoast type bronchial carcinomas, primary neurogenic tumors, soft-tissue neoplasms, and metastases from a variety of primary sites. Methods: Between October 1993 and January 1998 we undertook 22 operations on 21 patients using a variety of antero-superior approaches. The anterior cervical-transsternal approach was used in 11 operations, the Dartevelle technique was used in five cases, the modification described by Nazari in one patient and that described by Grunenwald in five cases. Results: 21 of the 22 operations were considered to be complete resections with negative margins. There were no intraoperative or postoperative deaths. Major complications occurred in five patients; acute respiratory distress syndrome (n=4), and thrombosis of the arterial graft and acute respiratory distress syndrome (n=1). Chronic morbidity was observed in 12 patients; prolonged arm pain (n=1), arm edema (n=2), motor and sensory deficits (n=2), phrenic nerve paresis (n=1), disfigurement and instability of the pectoral girdle (n=4), and disturbances in shoulder girdle function (n=2). Conclusions: The anterior cervical-transsternal approach we previously described provides adequate exposure for the resection of neurogenic tumors originating in the brachial plexus and sympathetic chain, and for metastatic nodal disease at the base of the neck or in the superior mediastinum. We have found it to be associated with little morbidity, the postoperative stay has been short, and it has proven flexible enough to cope with the changed circumstances found at surgery. For Pancoast type bronchogenic carcinomas and other malignancies with extensive invasion of major structures at the thoracic inlet, we believe the best present option is the clavicle sparing antero-superior technique described by Grunenwald as a modification of the Dartevelle approach. When operating for lung cancer we presently feel that the antero-superior approach should be combined with a posterolateral thoracotomy, to accomplish complete intraoperative staging and undertake anatomical pulmonary resection under optimal conditions.

Key Words: Apical chest tumors • Antero-superior approaches • Thoracic surgery

	1. Introduction

Top Abstract 1. Introduction 2. Patients and methods... 3. Results 4. Discussion References

 
A heterogeneous group of tumors, both benign and malignant, involve the thoracic inlet and adjacent structures, including lung cancers originating at the lung apex, so called ’superior sulcus’ or Pancoast tumors, primary neurogenic tumors arising in autonomic and somatic nerves around the spine or brachial plexus, a wide variety of soft-tissue neoplasms, and metastases from a variety of primary sites involving lymph nodes from the base of the neck into the thorax. Although the incidence of these tumors is relatively low [1–4], they pose problems in surgical management due to the difficulty of access, the crowded anatomy of this region and the propensity of tumors in this area to involve important adjacent structures. Complete resection requires careful dissection, and may require the resection of major vascular, neural or skeletal structures. Limited access and poor visualization can result in inadvertent damage to these structures. The rib cage tapers inward acutely towards its apex restricting access by conventional thoracotomy. The downward slope of the upper ribs leaves the neurovascular bundle inaccessible to posterior approaches, and the overlapping pectoral girdle restricts access from the neck. These anatomical considerations also influence the pattern of local development of tumors. Those arising in the neurovascular structures of the thoracic inlet will exploit the greater capacity afforded by the chest cavity, expanding to fill the apex of the chest and becoming wedged in the thoracic inlet. The major neurovascular structures often lie above and medial to the tumor mass and access to such structures, which may be the site of origin or of local invasion, or merely be displaced by the tumor, is significantly limited using approaches from below such as the posterolateral-paravertebral thoracotomy proposed by Paulson [5] or minimally invasive approaches such as video-assisted thoracoscopy (VATS).

A range of antero-superior approaches [1,6,8,10–13] have been developed in recent years (Table 1), providing excellent exposure to undertake safe dissection of any involved structures. Such approaches have allowed improved radicality and allowed the surgeon to extend the indications for operation in this region, with low mortality and acceptable morbidity [1,6–9]. No single approach provides the best access to all of the heterogeneous tumors in this region, and the thoracic surgeon must be familiar with them all and choose the appropriate incision in each patient. This offers the thoracic surgeon a new and exciting challenge once the anatomy has been appreciated.

	2. Patients and methods

Top Abstract 1. Introduction 2. Patients and methods... 3. Results 4. Discussion References

 
At the Royal Brompton Hospital between October 1993 and January 1998 we undertook 22 operations on 21 patients using a variety of antero-superior approaches for tumors at the thoracic inlet (Table 2). There were 15 males and six females with a mean age of 45.6 years (range 20–67 years). Histologically the tumors consisted of bronchogenic carcinoma in nine cases, metastatic nodal disease in eight cases, and primary lesions of neurogenic origin in four cases (all were benign).

A variety of antero-superior approaches were employed in these patients. To avoid the confusing terms used to describe these different approaches we have employed those used by the original author.

Table 3 gives some details of the operations performed using these various approaches. The anterior cervical-transsternal approach [13] was used in 10 patients (11 operations); in four for benign neurogenic tumors and in six patients to resect metastatic tumors (seven operations). All these neoplasms involved the base of the neck and extended downward to involve the thoracic inlet (Fig. 1) or superior mediastinum (Fig. 2) . In one patient the internal jugular and subclavian veins were resected and simply ligated, whilst in another patient the innominate vein was divided and reanastomosed. One patient underwent resection of the lower root (T-1) of the brachial plexus.

View larger version (98K): [in this window] [in a new window]   Fig. 1. (A) Magnetic resonance imaging of patient no. 8, demonstrating a neurogenic tumor of the thoracic inlet, 6 cm in diameter, extending from the root of the neck into the chest posterior to the right clavicle. (B) Computed tomographic scan, showing that tumor is filling the apex of the right hemithorax becoming wedged in parietal pleura. A cervical-transsternal approach was employed for the resection of this tumor.

View larger version (109K): [in this window] [in a new window]   Fig. 2. Computed tomography scan of patient no. 7 showing a recurrent metastatic liposarcoma, involving the left lower cervical lymph nodes, extending posterior to the carotid artery and jugular vein to a further lobule of tumor and to the upper compartment of the superior mediastinum. The tumor was approached using a cervical-transsternal incision.

View larger version (115K): [in this window] [in a new window]   Fig. 3. Computed tomography scan of patient no. 10, demonstrating a superior sulcus tumor of bronchogenic origin, necessitating the resection of multiple vascular, neural and skeletal structures using, the cervical-transclavicular approach, as per Dartevelle [1], and an additional posterolateral thoracotomy.

Recently we have used the Grunenwald technique [6] in five patients: in four for bronchogenic carcinoma and in one for metastatic testicular teratoma. A posterolateral thoracotomy was added in four patients to facilitate pulmonary resection. In one patient with bronchogenic carcinoma, the incision was extended as an anterior thoracotomy into the first intercostal space, an apical wedge resection was performed and posterolateral thoracotomy was avoided. Four patients had tumor involvement of vascular structures requiring resection and in another patient the subclavian artery was temporarily clamped to allow safe dissection around the vessel. The innominate and internal jugular veins were resected and simply ligated in two patients. The venous confluence between the subclavian, internal jugular and innominate veins was reconstructed using an 8 mm reinforced Gortex graft in one patient. In another patient the subclavian artery was resected and replaced with a 6 mm Impra graft and the vertebral artery was implanted into the graft. The thoracic duct was ligated in four patients. The brachial plexus was involved in two patients, requiring the resection of the T-1 nerve root in one patient and C-8 and T-1 in one patient. The phrenic nerve was also resected in one patient and the diaphragm plicated at thoracotomy.

	3. Results

Top Abstract 1. Introduction 2. Patients and methods... 3. Results 4. Discussion References

 
Twenty-one of the 22 operations were considered to be complete resections with negative margins. One patient was found intraoperatively to require a pneumonectomy to achieve complete resection, but because of poor lung function had only a palliative, wedge resection. There were no intraoperative or postoperative deaths.

Major pulmonary and vascular complications, and neurological chronic morbidity were related to the extensive surgical resections [14], attempted for complete tumor clearance.

Pulmonary complications were related to acute respiratory distress syndrome (ARDS) in five patients which required intubation and mechanical ventilation in four patients, supplemented by tracheostomy in two patients and extracorporal membrane oxygenation (ECMO) in one patient. One patient was managed conservatively with intravenous antibiotics, physiotherapy, nebulizers and oxygen therapy. One patient had simultaneous vascular complication, related to thrombus in the arterial graft, which caused blockage of the vertebral artery and repeated embolization into the digital arteries. Unfortunately, after treatment with tissue-Plasminogen Activator, the graft blocked secondary to manipulation with a catheter which necessitated urgent carotico-subclavian bypass using the long saphenous vein. Upper extremity edema was present in two patients following resection of the innominate or subclavian vein. One of these patients also suffered from bilateral, non-malignant pleural effusions associated with cardiac failure 2 months after the operation.

Chronic morbidity due to neurological complications was as one would anticipate in the two patients who underwent resection of the T-1 and C-8 nerve roots of the brachial plexus. In addition, one patient had a temporary paresis of the left phrenic nerve, causing elevation of the left hemidiaphragm and collapse of the left lower lobe. Another patient experienced arm pain which lasted for 4 weeks following surgery.

Chronic morbidity was observed in all four patients who underwent resection of the medial half of the clavicle as per Dartevelle [1], with disfigurement and some instability of the pectoral girdle. There was some disturbance in shoulder girdle function resulting from the sternoclavicular arthrodesis in both patients following clavicular reconstruction.

The surgical approach was not the limiting factor for the delayed discharge from hospital in any of the cases. The postoperative stay was short in the group of patients operated upon for neurogenic benign tumors and metastatic nodal disease: 4 days (range 3–6 days) and 7.4 days (range 4–21), respectively. Of the nine patients undergoing more extensive procedures for bronchogenic carcinoma, five required prolonged hospitalization for recovery from ARDS or to regain satisfactory pain control. In this group the mean postoperative stay was 24.1 days (range: 6–63 days).

	4. Discussion

Top Abstract 1. Introduction 2. Patients and methods... 3. Results 4. Discussion References

 
Antero-superior approaches allow excellent exposure to deal with neurovascular or vertebral involvement in this complex anatomical area [15–22], but a flexible operative approach is essential as the degree of involvement is not always clear prior to operation [15,16,22].

The classic posterolateral thoracic approach for superior sulcus tumors, described by Shaw, Paulson and Kee [5], we feel, does not provide adequate access to the many important structures which may be involved by apical chest tumors of bronchogenic origin. This restricted access may be one of the reasons for the high rate of incomplete resections [23,24] and high surgical morbidity and mortality using this approach [25,26].

Following the encouraging report of Dartevelle and associates [1], we used the anterior transcervical-thoracic approach in two patients. This initial experience confirmed the excellent exposure possible through this approach and proved its safety in our hands. However, it became apparent that the resection of the medial half of the clavicle and detachment of the major muscles from the sternoclavicular insertions lead to significant cosmetic and functional defects of the pectoral girdle. It was also obvious that primary neurogenic tumors, originating from the brachial plexus, or sympathetic chain, and confined to the base of the neck could be approached with a less extensive incision. The modified antero-superior approach [13] we developed for resection of these neurogenic tumors, located at the root of the neck and apex of the superior mediastinum, avoids resection of the medial half of the clavicle. This cervical-transsternal approach has several advantages, chiefly that of avoiding disfigurement and loss of function of the pectoral girdle, whilst providing excellent exposure of the brachial plexus, sympathetic chain, and stellate ganglion. Such an approach results in a short postoperative stay (3–6 days), and yet allows extension as per Grunenwald [6], or by a high, anterior thoracotomy if necessary. We found this technique applicable not only for neurogenic tumors involving the lower cervical and thoracic inlet structures, but also for metastatic tumors, located in this area. The morbidity of this approach was associated only with the local extent of the tumor. The local recurrence in one case we believe was due to relapse in higher nodes and not by incomplete excision, as tumor-free margins were achieved. The cervical-transsternal approach can be repeated if necessary without additional morbidity. However, such an approach does not provide adequate access to the lung for primary cancer at the apex.

Increasing experience with the Dartevelle approach led us to wonder if in those patients requiring more extensive surgery it was possible to preserve the clavicle without compromising exposure. In two further patients we reconstructed the clavicle using bone plates and screws. This provided acceptable access with better functional and cosmetic results but required extra time and specialized equipment, and still disturbed shoulder girdle function. We therefore adopted the clavicle-sparing antero-superior approach devised by Grunenwald [6]. This has provided safe and excellent exposure of the entire thoracic inlet, including subclavian vessels, brachial plexus and the posterior part of the first two ribs. None of the five patients who underwent resection using the Grunenwald technique have experienced any significant cosmetic or functional disturbances of the pectoral girdle or shoulder, even when this approach has been combined with a lateral thoracotomy.

The addition of a standard posterolateral thoracotomy, performed after the tumor has been released from the neurovascular structures, and after resection the upper ribs by the antero-superior approach, is still controversial. The updated consensus report of the International Association for the Study of Lung Cancer recommends detailed intrathoracic staging in the assessment of resection options [27], and the recommendations of the Lung Cancer Study Group, that lobectomy gives better hope for cure than local resection [28], suggest that the addition of a lateral thoracotomy would be advantageous to evaluate the intrathoracic extent of disease and accomplish curative resection. An additional posterolateral thoracotomy with systematic nodal dissection was undertaken in nine patients in our series. Of these one was found to have N1 disease requiring pneumonectomy. The importance of accurate intraoperative staging [29] and the wide operative exposure for the safe dissection were distinct advantages, despite longer operation times and some early postoperative morbidity for pain and shoulder discomfort. One may argue that apical wedge resection for such bronchogenic carcinoma, causing the Pancoast syndrome [30], is adequate as these tumors are frequently low-grade non-small cell carcinomas, which grow slowly, are often limited locally and metastasize late [25]. Two patients in our series underwent wedge resection of the lung apex without posterolateral thoracotomy, but this was because we were dissatisfied with clearance of tumor at the thoracic inlet during the initial antero-superior operation.

In recent years antero-superior approaches have been developed which allow superior access to the varied pathology at the thoracic inlet and lung apex [1,6,7,10,12,20,31]. The excellent exposure of the cervicothoracic region allows one to be far more confident of complete resection in this difficult area. The anterior cervical-transsternal approach [13] provides adequate exposure for resection of neurogenic tumors originating in the brachial plexus and sympathetic chain, and for metastatic nodal disease in the root of the neck or the superior compartment of the mediastinum. This allows control of the structures invaded by the tumor and we have found it to be associated with little morbidity and a short postoperative stay. We emphasize the flexibility of this approach which allows the incision to be extended to the high ‘trap door’ access, similar to the Grunenwald modification of the Dartevelle procedure [6], when this is shown to be necessary during the operation. This cervical-transsternal approach can be repeated with excellent healing of the surgical wound and without any incision related morbidity. However when access is required to the lung apex and the neurovascular structures more laterally, as will be needed for all the Pancoast type bronchogenic carcinomas and other malignancies with extensive invasion of the thoracic inlet major structures, we believe the best option is the clavicle sparing antero-superior technique described by Grunenwald as a modification [6] of the Dartevelle approach. When operating for lung cancer we presently feel that an antero-superior approach should be combined with a posterolateral thoracotomy, to accomplish complete intraoperative staging and undertake adequate pulmonary resection under optimal conditions.

	References

Top Abstract 1. Introduction 2. Patients and methods... 3. Results 4. Discussion References

 

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Peter Goldstraw Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Vanakesa, T. Articles by Goldstraw, P. Search for Related Content PubMed PubMed Citation Articles by Vanakesa, T. Articles by Goldstraw, P.