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Ann Thorac Surg 1997;63:12-19
© 1997 The Society of Thoracic Surgeons

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Herbert Sloan Lecture

Extended Operations for the Treatment of Lung Cancer

Department of Thoracic and Vascular Surgery, Hôpital Marie Lannelongue, Le Plessis Robinson, France

Abstract

Ladies and Gentlemen: It is a distinct pleasure to introduce you to Philippe Dartevelle. Philippe was born in Paris in 1948. He earned his doctor of medicine degree from Lariboisière-Saint Louis University in Paris. His stellar rise in thoracic surgery began in 1978, when he became fellow in thoracic surgery at the Hôpital Marie Lannelongue.

My visit to the Hôpital Marie Lannelongue confirmed that this is a truly outstanding center devoted to thoracic surgery and that Professor Dartevelle is a master surgeon. Within 10 years of his arrival as a fellow at the Hôpital Marie Lannelongue, Philippe rose to his current position as Head of the Department of Thoracic and Vascular Surgery and Heart-Lung Transplantation. He also serves as Professor of Thoracic and Cardiovascular Surgery at Paris-Sud University.

Ladies and Gentlemen, it is with great pleasure that I give you Philippe Dartevelle, who will discuss extended operations for the treatment of lung cancer.

My odyssey began in 1979. I was completing my training in cardiothoracic and vascular surgery when I was asked by Drs Henri Le Brigand and Max Merlier (Fig 1) to join the Centre Chirurgical Marie Lannelongue, an already major referring national center exclusively devoted to general thoracic surgery and pediatric and adult cardiac surgery. Because no one refused the orders of these two giants, I enthusiastically went to the Centre Chirurgical Marie Lannelongue, located at the outer Parisian suburbs (Fig 2).

View larger version (121K): [in this window] [in a new window]   Fig 1. . (A) Doctor Max Merlier and (B) Dr Henri Le Brigand.

View larger version (133K): [in this window] [in a new window]   Fig 2. . Centre Chirurgical Marie Lannelongue.

Carinal Pneumonectomy

Carinal pneumonectomy consists of removing one lung and the tracheobronchial bifurcation followed by an end-to-end anastomosis of the contralateral main bronchus with the trachea. Traditionally considered a technically demanding procedure, the 5-year survival rates of which were less than or equal to the technical mortality and morbidity, carinal pneumonectomy was rarely indicated and experience was limited to a few institutions worldwide [1]. Based on our experience [2], and that acquired with the surgical management of tracheal diseases, I was stimulated to define better the indications and technical aspects of carinal pneumonectomy.

Undoubtedly, my task was enormously facilitated by developments in the allied disciplines of radiology and anesthesiology. The first lesson learned was the need to operate on highly selected patients, especially with regard to cardiopulmonary reserve and lymph node invasion. We now know that even the smallest postoperative complication may result in fatal repercussions such as prolonged mechanical ventilation that can lead to adverse consequences on the tracheobronchial anastomosis and the residual lung parenchyma. The second lesson was that the tracheobronchial anastomosis should not be under tension, and that tension is best avoided by considering the safe limit of resection to be approximately 4 cm between the lower end of the distal trachea and the contralateral main bronchus. In this sense, bronchogenic tumors involving the ispilateral proximal main bronchus within 1 cm from the carina, the distal trachea within 2 cm from the carina, and the first 1.5 cm of the contralateral main bronchus should be considered for carinal pneumonectomy, provided that there is no lymph node invasion above the subcarinal space. Patients who have carinal invasion only by diseased subcarinal nodes may benefit from resection because their cancers can be completely resected en bloc along with the tracheobronchial bifurcation.

Controlled unilateral ventilation was usually provided with a Carlens tube. More recently we have used a long, flexible, single-lumen endotracheal tube. Considering the risks of pulmonary edema in the remaining lung, excessive intravascular fluid overload should be avoided, especially when the lymphatic drainage has been impaired. During airway reconstruction, distal ventilation was afforded through cross-field intubation by a flexible endotracheal tube or high-frequency jet ventilation. All right-sided lesions were approached through a right posterolateral thoracotomy performed in the fifth intercostal space. For left-sided lesions, we used a left posterolateral thoracotomy three times and a median sternotomy once. We sought always to avoid any irrevocable step until resection could be guaranteed. The steps of the operation are as follows. After division and suture of the arch of the azygos vein, dissection and mobilization of the airways should be limited to the anterior surface of the trachea and proximal main bronchi. When the azygos vein drains the venous network below the liver, as it occasionally does, it needs to be reimplanted into the right atrium below the cavoatrial junction. Subsequently, the trachea first and contralateral main bronchus are divided next. Frozen sections aretaken to ensure clear margins at both tracheobronchial transection sites. The anastomotic technique reflects that of vascular surgery, ie, suturing is done within the lumen of the posterior aspect of the tracheobronchial anastomosis. An internal, cartilage-to-cartilage running polydiaxanone (PDS; Ethicon, Somerville, NJ) suture on the tracheal and bronchial stumps is placed. For example, in right carinal pneumonectomy, the left third of the anastomosis (the deepest aspect seen by the operator) is performed with a running suture up to the cartilaginous part of the airway. It is then tied and fixed with two independent PDS sutures, the knots of which are made outside the lumen. Thereafter, several interrupted stitches of PDS or polyglactin (Vicryl; Ethicon) are placed on the remaining part of the anastomosis; they are tied after all of the sutures have been placed to correct size discrepancies. One can safely resect about 2 cm of the distal trachea without creating anastomotic tension; in our experience, laryngeal release procedures have not been needed or worthwhile. The anastomosis is covered by available vascularized tissue flaps.

Since 1981, we have operated on 60 patients [3]. The majority of the tumors were of squamous cell histology (n = 46; 77%) and right-sided (n = 56; 93%); only a minority of patients (n = 12; 20%) received induction therapy before operation, usually because of N2 disease. Preoperatively, endoscopy showed invasion of the lower trachea in 5 patients, carina in 7, proximal main bronchus in 43, right upper lobe in 4, and intermediate bronchus in 1. Intraoperatively, extension to the lower trachea and contralateral main bronchus was observed in 11 patients and to other mediastinal structures in 24 (40%); they included the muscular wall of the esophagus in 6, SVC in 12, left atrium in 3, and retrocaval pulmonary artery in 3. All 60 patients had a complete resection. The disease stage was N0 in 11, N1 in 36, and N2 in 13 patients; among the 13 patients with N2 disease, 6 had inferior paratracheal node invasion and 7 had subcarinal node involvement. There were two early postoperative deaths (days 15 and 23) and two late postoperative deaths (days 53 and 58). Thus, the overall mortality rate was 6.6%. Early deaths occurred due to respiratory failure after noncardiogenic pulmonary edema, and late deaths were the result of bronchopleural fistula; two of the operative deaths were observed in patients who had received induction chemotherapy.

Our 5- and 10-year survival rates, including postoperative deaths, were 42.3% and 29%, respectively (Fig 3). With a median follow-up time of 4.3 years, the median survival was 2.9 years. There are 12 (20%) 5-year and 4 (6.7%) 10-year survivors. None of our patients experienced late anastomotic complications. Causes of death were systemic (n = 19) or regional (n = 2) relapse or acute respiratory distress syndrome (n = 2). The respiratory distress syndrome occurred only in the 2 patients who had induction therapy. Massive pulmonary embolism (n = 1) and death due to causes other than their bronchogenic carcinoma (n = 2) caused the remaining deaths. Long-term survival was significantly influenced by the nodal status (N0-1 versus N2; p = 0.02) and histology (squamous versus nonsquamous; p = 0.03) in univariate analysis; by multivariate analysis, the only independent and significant estimator of survival was the nodal status (p = 0.01). Among the 12 N2 patients, there are no survivors beyond 46 months.

View larger version (14K): [in this window] [in a new window]   Fig 3. . Survival of 60 patients who underwent carinal pneumonectomy for bronchogenic carcinoma. With a median follow-up of 4.3 years, the overall 5- and 10-year survival rates, including postoperative deaths, were 42.3% and 29%, respectively. Overall median survival was 2.9 years.

Although partial invasion of the SVC by NSCLC can be surgically managed by simple lateral partial resection of the vessel wall and primary suture, its circumferential invasion had almost always been considered a surgical contraindication. The reasons for this were the absence of suitable graft material for venous reconstruction, fear of the consequences of total SVC clamping, and skepticism about long-term survival. However, the lessons learned from 43 SVC prosthetic reconstructions for a variety of malignant and benign diseases are that polytetrafluoroethylene (PTFE) grafts usually remain definitively patent and their inner lumen becomes reendothelialized by a thin layer of neointima that persists 5 years or longer [4].

Operable NSCLC invading the SVC usually respects the patency of the SVC [5]. Under such circumstances, abrupt venous clamping could induce a hemodynamic cascade of events that might include first a decreased right ventricular preload, then decreased cardiac output, and eventually systemic hypotension. In parallel, increased venous pressure increases the risks of thrombosis in the head. The combination of these two phenomena decreases the arterial–venous cerebral gradient, which may result in irreversible brain damage. In fact, we have found that it is not difficult to reverse the hemodynamic effects of SVC clamping by using fluid supplementation and pharmacologic agents, reducing the venous clamping time, and giving adequate anticoagulation therapy (Fig 4).

View larger version (19K): [in this window] [in a new window]   Fig 4. . Hemodynamic repercussions during cross-clamping of a patent superior vena cava (SVC). Clampage of the SVC without any protection results in a low arterial–venous gradient in the cerebral vascular bed. The use of a shunt reestablishes a normal gradient but enhances the potential for a thrombosis and interferes with the operative field, making the performance of the vascular procedure difficult. It is easier to maintain a normal gradient in the cerebral vascular bed by increasing the intravascular fluid load to compensate for the clamping-induced hypovolemia and arterial systemic pressure by vascoconstrictive agents. (Reprinted with permission from Dartevelle P, Macchiarini P, Chapelier A. Technique of superior vena cava resection and reconstruction. Chest Surg Clin North Am 1995;5:345–58.)

View larger version (60K): [in this window] [in a new window]   Fig 5. . (A) Clamping and division of the superior vena cava beyond each side of the tumor. (B) This maneuver facilitates the exposure and stapling of the retrocaval pulmonary artery.

View larger version (95K): [in this window] [in a new window]   Fig 6. . (A) Computed tomographic scan of a 56-year-old man with a squamous tumor originating from the ventral segment of the right upper lobe and invading the tracheobronchial bifurcation and the posterior border of the superior vena cava (SVC). (B) Pulmonary angiography shows the amputation of the right mediastinal artery (arrow).

For a long time, operation on lung tumors invading the thoracic inlet was performed through a posterior approach, which makes it difficult to deal with the subclavian and vertebral vessels and nerve roots of the brachial plexus. Looking at the anatomy of the thoracic inlet, one realizes that the best approach by far to resect tumors invading this area is an anterior one that includes the resection of the internal part of the clavicle (Fig 7). Two types of thoracic inlet invasion can be described. The first (anterior) type invades the subclavian vessels but spares the brachial plexus (Fig 8). The second (posterior) type is the most common (Fig 9); it is located in the posterior costovertebral groove and invades the roots of T1, the posterior aspect of the subclavian and vertebral arteries, the sympathetic chain, and the prevertebral muscles. The malignancy of the posterior type of invasion is linked to the actual or potential spread of cancer along the neurolemma of the nerve roots up to the spinal canal through the intervertebral foramen.

View larger version (183K): [in this window] [in a new window]   Fig 7. . Anatomy of the thoracic inlet. The first encountered structure is the subclavian vein, which drains with the internal jugular vein into the brachiocephalic vein. The posterior jugular and vertebral veins with the thoracic duct drain into the posterior surface of this confluence. Behind, we find the plane of the subclavian artery, which is separated from the venous plane by the anterior scalene muscle and phrenic nerve. Several primary branches of the subclavian artery often vascularize the tumor. The last plane is made up of the brachial plexus. C8 is well above the first rib, whereas T1 arises between the first and second thoracic vertebrae and is usually included in the tumor. (Reprinted from Testut L, Jacob O. Anatomie topographique. Lyon: Renaux Valentin, 1909.)

View larger version (88K): [in this window] [in a new window]   Fig 8. . (A) Computed tomographic scan showing an apical bronchogenic tumor invading the anterior path of the left thoracic inlet. (B) On preoperative arteriography, the left subclavian artery is included by the tumor (arrow).beyond the origin of the left vertebral artery.

View larger version (122K): [in this window] [in a new window]   Fig 9. . Computed tomogram showing an apical bronchogenic tumor invading the posterior path of the left thoracic inlet. At operation, the subclavian artery was massively invaded. Note the absence of tumor at the level of the costotransverse foramen.

One of the limits of a radical resection is the spread of tumor along the sheath of the nerve roots into the intervertebral foramen, as observed in posteriorly located apical lesions. Unfortunately, I was faced with this circumstance several times and therefore realized that we might be able to perform a more radical procedure by resecting the intervertebral foramen and dividing the nerve roots inside the spinal canal. This does not mean, however, that one should resect tumors extending across the intervertebral foramen inside the spinal canal, but only those extending into the intervertebral foramen without intraspinal extension. A typical example of such a tumor invading the right costotransverse foramen and the intervertebral foramen is shown in Figure 10. To encompass the entire tumor, a combined transcervical anterior and median posterior approach was used and a hemivertebrectomy of T1, T2, and T3 was necessary (Fig 11), followed by spinal fixation with metal rods interposed between screws placed into the vertebral pedicles. The patient is placed in a ventral position and a median vertical incision is performed. After a unilateral laminectomy on three levels, the nerve roots are divided inside the spinal canal at the emergence of the external sheath covering the spinal cord. After the vertebral bodies on the middle part are cut, the specimen is resected en bloc with the lung, ribs, and vessels through this posterior incision (Fig 12). On the side of the tumor, the spinal fixation is made in the pedicle above and below the resection of hemivertebrae; on the contralateral side, there is a screw in each pedicle (Fig 13). Among the 7 patients who had this operation, 6 are still alive without recurrence with a median follow-up of 1 year. Before performing such an extended operation on the spine, one needs to be sure that there is no anterior spinal artery penetrating into the spinal canal through one of the invaded intervertebral foramina (Fig 14).

View larger version (169K): [in this window] [in a new window]   Fig 10. . Computed tomogram showing a left apical bronchogenic tumor invading the intervertebral foramen (arrow) between T1 and T2.

View larger version (38K): [in this window] [in a new window]   Fig 11. . (A) Right tumor invading the first thoracic intervertebral foramen. (B) The lesion is usually approached through transcervical (anterior) and middle (posterior) incisions for apical malignant tumors invading the first two thoracic intervertebral foramina. During the cervical step, the anterolateral aspects of the vertebral bodies of C7 throughout T2 are safely and perfectly exposed and a median slice (arrow) on the prevertebral planes can greatly facilitate the section of the invaded vertebral bodies during the posterior step of the operation. Usually, tumors invade two intervertebral foramina, necessitating resection of at least hemivertebrectomy (line of transection) above and below the invaded one. (C) The hemivertebrae need to be fixed thereafter.

View larger version (116K): [in this window] [in a new window]   Fig 12. . Chest roentgenogram of the postsurgical specimen shows the tumor resected en bloc with the first three ribs and hemivertebrae.

View larger version (148K): [in this window] [in a new window]   Fig 13. . Chest roentgenogram showing the bilateral spinal fixation with metal rods interposed.

View larger version (161K): [in this window] [in a new window]   Fig 14. . Preoperative arteriogram demonstrating a long, ascending and descending (arrow) spinal artery arising from the left fourth intercostal artery and entering the spinal canal between the second and third intervertebral foramina in a patient with left apical tumor invading the T2-T3 intervertebral foramen.

View larger version (14K): [in this window] [in a new window]   Fig 15. . Overall survival of 55 patients operated on for an apical tumor invading the thoracic inlet.

At the end of this review of extensive operations for special locally advanced NSCLC, let me conclude by saying that this type of extended operation requires a wide and in-depth training in the specialties of thoracic and vascular surgery and sometimes needs the collaboration of other surgical specialists like Doctor Gilles Missenard, who performed the spinal aspects of the seven operations when cancer extended to the spine. It is right that only highly selected patients are candidates for these extended and demanding operations. However, the thoracic surgical community should make all efforts to promote extended operations for T4 tumors because the presently available medical alternatives do not achieve the results achieved by operation.

Acknowledgments

I thank all my surgical (Alain Chapelier and Paolo Macchiarini) and medical (Jacques Cerrina and François Le Roy Ladurie) staff. Without them it would not have been possible to acquire this experience in extended operations for lung cancer.

Footnotes

Address reprint requests to Dr Dartevelle, Department of Thoracic and Vascular Surgery, Hôpital Marie Lannelongue, 133, Ave de le Resistance, Plessis-Robinson F-92350, France.

Presented at the Thirty-second Annual Meeting of The Society of Thoracic Surgeons, Orlando, FL, Jan 29–31, 1996.

References

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2. Dartevelle PG, Khalife J, Chapelier A, et al. Tracheal sleeve pneumonectomy for bronchogenic carcinoma: report of 55 cases. Ann Thorac Surg1988;46:68–72.[Abstract]
3. Dartevelle P, Macchiarini P. Carinal pneumonectomy for bronchogenic carcinoma. Semin Thorac Cardiovasc Surg1996;8:414–25.[Medline]
4. Dartevelle P, Chapelier A, Pastorino U, et al. Long-term follow-up after prosthetic replacement of the superior vena cava combined with resection of mediastinal-pulmonary malignant tumors. J Thorac Cardiovasc Surg1991;102:259–64.[Abstract]
5. Dartevelle P, Macchiarini P, Chapelier A. Technique of superior vena cava resection and recontruction. Chest Surg Clin North Am1995;5:345–58.[Medline]
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7. Dartevelle P, Chapelier A, Macchiarini P, et al. Anterior transcervical approach for radical resection of lung tumors invading the thoracic inlet. J Thorac Cardiovasc Surg1993;105:1025–34.[Abstract]
8. Dartevelle P, Macchiarini P. Cervical approach to apical lesions. In: Pearson FG, Deslauriers J, Ginsberg RJ, Hiebert CA, McKneally MFC, Urshel HC, eds. Thoracic surgery. New York: Churchill Livingstone, 1995:887–96.
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This Article Abstract 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): Philippe G. Dartevelle Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Dartevelle, P. G. Search for Related Content PubMed PubMed Citation Articles by Dartevelle, P. G.