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Ann Thorac Surg 2000;69:233-236
© 2000 The Society of Thoracic Surgeons


Original Articles

Extended resections for bronchogenic carcinoma invading the superior vena cava system

Lorenzo Spaggiari, MD, PhDa, Jean-François Regnard, MDa, Pierre Magdeleinat, MDa, Bertrand Jauffret, MDa, Philippe Puyo, MDa, Philippe Levasseur, MDa

a Department of Thoracic Surgery, Marie Lannelongue Hospital, Le Plessis Robinson, Paris, France

Address reprint requests to Dr Regnard, Department of Thoracic Surgery, Marie Lannelongue Hospital, 133 av de la Résistance, 92350, Le Plessis Robinson, Paris, France


    Abstract
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
Background. Extended resection of non-small-cell lung cancer (NSCLC) involving the superior vena cava (SVC) system is infrequently performed and oncologic benefits are still uncertain.

Methods. From 1983 to 1996, 25 patients underwent resection of the SVC system for T4, NSCLC.

Results. A total of 12 pneumonectomies (48%), ten lobectomies (40%), and three wedge resections (12%) were performed. Seven patients had complete resection of the SVC with graft interposition, 12 patients underwent tangential resection of the SVC, and 1 patient had a pericardial patch; 5 patients underwent resection of right innominate and subclavian veins without vessel reconstruction. The lymph node status was N0 in 8 patients (32%), N1 in 3 (12%) and N2 in 14 patients (56%). Five patients (20%) underwent incomplete resection. Nine patients (36%) developed postoperative complications (36%) that were fatal in 3 patients (12%). At the completion of the study, 10 patients were still alive. The median survival was 11.5 months and the 5-year actuarial survival rate was 29%, with 4 patients alive at 5 years.

Conclusions. The resection of the SVC system for direct involvement by T4, NSCLC can be performed in selected patients with an acceptable postoperative mortality. Even though no significant prognostic factors were observed, the patients who required a lobectomy with limited lymph node involvement seemed to benefit the most from surgery.


    Introduction
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 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
Surgery is considered the only reliable therapy to cure non-small-cell lung cancer (NSCLC), but locally advanced (T4) bronchogenic carcinoma is still regarded as unresectable disease [1]. Superior vena cava (SVC) system involvement by NSCLC has long been considered a technical and oncologic contraindication to surgical treatment. However, in recent years, several reports regarding SVC resection and replacement as well as advances in anesthesiology and surgical techniques have increased interest in these extended operations [2].

Burt and associates [3] reported no 5-year survivors in their series of 18 patients after pulmonary resection for lung cancer extended to SVC; by contrast, Thomas and colleagues [4] showed a 5-year survival rate of 24% with a median survival of 8.5 months in their series of 15 SVC resections for NSCLC, but with only 1 patient alive at 5 years. Tsuchiya and coworkers [5] reported the most important series of SVC resections for lung cancer with only 2 patients alive at 5 years. Even though few 5-year survivors have been described [6], these series suggest that this aggressive surgery is feasible in selected patients with acceptable postoperative mortality, hope of cure, and, at least, a good palliation.

The purpose of this retrospective study was to investigate the immediate and long-term results of a group of patients who underwent either pulmonary or SVC system resections for direct invasion (T4) by NSCLC.


    Material and methods
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
From January 1983 to June 1996, 25 consecutive patients with NSCLC invading the SVC system were operated on. Only patients with direct involvement of the SVC system by the tumor were considered for surgical resection, whereas patients with SVC involvement related to bulky N2 disease were not considered for resection.

There were 22 men and 3 women with a mean age of 59 years, ranging from 36 to 77 years.

Eligibility for SVC system resection included: (1) histologically proven invasion of the SVC system by NSCLC; (2) absence of mediastinal adenomegaly (more than 15 mm) on CT thoracic scan; and (3) absence of detectable extrathoracic disease on brain and abdominal CT scan and bone scanning.

Statistical methods
Overall survival was calculated by means of the actuarial method with the date of surgery as the starting date. Comparisons between the different curves were performed by the log-rank test.


    Results
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 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
The follow-up was complete for all but 1 patient, who was untraceable after 6 months of follow-up.

Five patients had neoadjuvant treatment (chemotherapy in 4 patients, radiotherapy in 1 patient) while the others were operated on before any medical treatment.

Operative procedures
The resections were done through a standard posterolateral thoracotomy in 17 patients, a cervico-sternotomy in 6 patients; 1 patient was approached by means of cervicotomy and posterolateral thoracotomy, whereas the remaining had a lateral muscle sparing thoracotomy. Twelve pneumonectomies (48%), 10 lobectomies (40%) and 3 wedge resections (12%) were performed. Seventeen patients required SVC resection, 3 patients a combined resection of the SVC and right brachiocephalic vein, and, finally, 5 patients (20%) had resection of the right innominate and subclavian veins without SVC resection. Six patients (24%) required an associated resection (carina, n = 3; carina and left atrium, n = 1; left atrium, n = 1; subclavian artery, n = 1). In the group of patients with SVC resection, 13 (65%) underwent tangential resection: 12 patients had a direct running suture, whereas the remaining patient underwent a pericardium patch.

Seven patients (35%) required SVC replacement with a PTFE graft after complete resection of the SVC. The sizes of the ringed PTFE grafts used were No. 12 (4 patients) No. 14 (2 patients), and No. 16 (1 patient). The proximal anastomosis was performed three times on the SVC and four times on the left brachiocephalic vein stump, while the distal anastomosis was performed five times on the distal part of the SVC and twice on the right atrium.

The patients who underwent resection of the right innominate and subclavian veins did not require any revascularization.

The median time of clamping of the SVC system was 53 minutes (range: 15 to 105 minutes), but no perioperative or postoperative complications due to the clamping were observed; the mean perioperative blood loss was 600 cc (range: 200 to 3,500 cc). The median hospital stay was 19 days (range: 9 to 39 days).

Postoperative pathologic features
Fifteen squamous cell carcinomas, eight adenocarcinomas, and two undifferentiated large cells carcinomas were resected.

The lymph node status was N0 in 8 patients (32%), N1 in 3 patients (12%), and N2 in 14 patients (56%); this last subgroup of patients had minimal N2 involvement discovered during the systematic mediastinal lymphadenectomy. A complete resection was achieved in 20 patients (80%) whereas in the remaining 5 patients a microscopic residual tumor was found on specimen analysis. The three wedge resections were performed in cases of incomplete resection.

Postoperative course
No perioperative death was observed. Nine patients (36%) developed postoperative complications that were fatal in 3 patients (12%) (one pulmonary embolism, one bronchopleural fistula, one postpneumonectomy edema). Six patients had major complications; 1 patient had a pulmonary embolism and 2 patients had pneumonias that were medically controlled. One patient developed a lung abscess despite the medical treatment of a pneumonia. This patient had a right, upper lobectomy with complete SVC resection and replacement with ringed PTFE graft, and a left brachiocephalic, vein-to-SVC, end-to-end anastomosis through a median sternotomy. The lung abscess was medically controlled and the patient was discharged from the hospital. Unfortunately, he was readmitted a week later for fever and evidence of empyema. As a result, he required a completion pneumonectomy through a lateral thoracotomy. The latissimus dorsi was harvested during the thoracotomy to cover the PTFE graft which was left in place after cleaning of the chest cavity. This patient had an uneventful postoperative course and he is still alive without recurrent infection and tumor, 5 years after the resection.

One patient suffered from early acute SVC syndrome after partial resection and tangential suture of the SVC, he was reoperated on, and required an enlargement of the SVC by a saphenous patch.

Finally, 1 other patient had a late SVC syndrome after a tangential resection of the SVC just before his discharge to the hospital. This patient did not require a reoperation and he had a good outcome with the medical treatment alone (ie, general heparinization).

In the group with complete SVC replacement, no early or late graft occlusion was observed.

Long-term results
Five patients had no postoperative treatment while 20 patients had adjuvant radiotherapy. At the completion of the study, 10 patients (40%) were still alive. The median survival was 11.5 months (ranging from 0 to 74 months). The overall estimate 5-year actuarial survival rate was 29% (confidence interval 95%: 7% to 51%) with 4 patients alive at 5 years (Fig 1). The median survival of patients with N0 involvement was 14 months (range 4 to 48 months) whereas the median survival of N2 patients was 5 months (range 0 to 70 months). Of the patients with N1 disease, 1 was lost at the follow-up, whereas the others died 31 and 74 months after the resection; finally, patients with associated carinal resection had a median survival of 8.5 months (range 4 to 72 months). Figures 2 and 3 show the actuarial survival according to the type of pulmonary resection (pneumonectomies versus other resections) and the N status (N0+N1 versus N2). Even though the comparison between these curves is not significant, there is a trend for a better survival in case of lobectomy and absence of N2 disease.



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Fig 1. Five-year probability of survival of 25 patients who underwent SVC system resection for T4 NSCLC. The survival was calculated by the actuarial method. The number along the curve show patients alive and still at risk.

 


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Fig 2. Survival curves (actuarial method) of patients who underwent lobectomy or wedge resections (dotted curve) or pneumonectomy (continuous curve) and SVC system resection for T4, NSCLC. The numbers along the curves indicate the patients alive and still at risk at the corresponding date. The 5-year probability of survival were respectively 55% and 11%. The comparison by log-rank test was not significant.

 


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Fig 3. Survival curves (actuarial method) of patients with N0–N1 lymph node involvement (continuous curve) or N2 involvement (dotted curve) and SVC system resection for T4, NSCLC. The numbers along the curves indicate the patients alive and still at risk at the corresponding date. The 5-year probabilities of survival were respectively 30% and 25%. The comparison by log-rank test was not significant.

 
No significant difference was noted in survival rates between cases of tangential versus complete SVC resections with PTFE graft replacement.

Similarly, no significant difference was observed between patients who required an associated mediastinal resection (carina and/or left atrium) and those who required a resection limited to the SVC.


    Comment
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
Tumor involvement of the SVC system can occur either by direct extension of the primary tumor (T4) or by invasion of bulky mediastinal adenomegaly (N2) [1, 2, 4]; moreover, often, bulky lung cancer involves other mediastinal structures such as carina, left atrium, or both. Thus, the unresectability of a lung cancer invading the SVC system may be technical (direct tumor invasion of other mediastinal structures) or/and oncologic due to the presence of bulky N2 disease. However, in some cases, SVC involvement is a direct involvement by the tumor and represents the only mediastinal structure involved, thus an en bloc resection may be attempted.

One of the major criticisms of the several series reported to date is the lack of differentiation between the tumor (T4) or lymph nodes (N2) SVC system involvement [4]. This distinction is important because the survival seems more influenced by the N status than by the T status. This study has retrospectively analyzed a homogeneous consecutive series of patients with direct involvement of the SVC system by NSCLC, excluding direct bulky N2 involvement.

The cervico-sternotomy approach was used for upper-localized tumors in which the origin of the SVC system was involved and complete SVC control was required; in fact, this approach provides optimal access to either the right atrium or both innominate veins and its confluences; moreover, it allows the proximal anastomosis to be performed distal to the site of the tumor resection (ie, left brachiocephalic vein). In the other cases, a posterolateral thoracotomy, as for standard lung resection, was preferred.

The SVC reconstruction can be performed in different ways. We try to perform tangential resection of the SVC followed by direct running suture or patch in all cases to avoid the risks of graft infection due to associated pulmonary resections. Nevertheless, when the resection of vascular wall is more than 50% of the original diameter of the SVC, a graft replacement is mandatory. The ringed PTFE graft safety permits SVC replacement with good early and long-term graft patency results. We usually prefer to revascularize only the left brachiocephalic vein, avoiding a Y-type graft that might create a reduction of venous pressure in the graft with early thrombosis. In our series no postoperative graft occlusion was observed. All replacements were performed under general heparinization and all patients were discharged with antivitamin K treatment. The conservative approach was responsible for the two postoperative SVC thromboses, necessitating a reoperation in one case. On the other hand, we only experienced one severe sepsis, which was successfully managed. The relatively long time of complete clamping (median 53 minutes) is due to the fact that SVC resection was often performed at the beginning of the surgical procedure, especially in cases of sternotomy approach, to facilitate the pulmonary resection. However, no perioperative or postoperative complications due to acute SVC syndrome were observed.

The hemodynamic variations occur mainly in patients with infiltrated but nonobstructed SVC during complete SVC system clamping. These alterations are characterized, first, by an increase of brain venous pressure with a reduction of the arterial-venous gradient, creating a serious risk of cerebral edema and second, by reduction of cardiac output. To avoid these hemodynamic effects, we administered vasoconstrictive agents and fluids during the clamping. However, in patients requiring pneumonectomy and extensive lymph nodes dissection, careful management of fluids administration is mandatory to prevent postpneumonectomy edema.

This extended surgery was associated with a risk of severe postoperative complications and we experienced three postoperative deaths. One of the deaths was directly related to the surgical procedure (bronchopleural fistula) but the two other represented the unpredictable postoperative complications observed in general thoracic surgery, especially following pneumonectomy (pulmonary embolism, postpneumonectomy edema).

Technical difficulties, extended local invasion, and poor outcome of N2 disease frequently associated with SVC involvement have limited the acceptance of this surgery; however, some considerations might be derived from the analysis of our data. In our experience, 4 patients are still alive at 5 years, an indication that in selected cases extended surgery can prolong survival and may cure the patient. However, considering the different types of pulmonary resections performed, patients who underwent lobectomy seemed to have a better survival than those who underwent pneumonectomy, even though the comparison was not significant.

Despite our criteria of selection, 56% of our patients had mediastinal lymph nodes metastases. This group of patients had a median survival lower than that of N0 patients (5 months versus 14 months), but comparing the curves of survival according to the N status (N0–N1 versus N2), no significant difference was observed. This last result is probably due to the low number of patients in each subgroup; nevertheless, analyzing the shapes of the curves, there was a trend for a better survival in cases of N0–N1 diseases in comparison with those of N2 diseases. Thus, patients with negative mediastinal lymph nodes may better benefit from the surgical resection and, as a result, mediastinoscopy should be advised in all patients with SVC involvement to exclude N2 patients.

Carefully selected patients might undergo associated carinal resection, but frequently in our experience, these patients had positive mediastinal lymph nodes. In our experience this subgroup of patients had a median survival of 8.5 months and we believe that these patients should be carefully selected preoperatively.

Our data concerning survival are consistent with the recent series of Thomas and colleagues [4] that report a 5-year probability of survival of 30% with a median survival of 8.5 months.

We think that the resection of superior vena cava system can be done in selected patients, especially those who present with direct invasion of the vessels by the tumor and with negative N status, and that the hope of long-term survival justifies the operative risk. Neoadjuvant chemotherapy is generally advised in patients with stage III NSCLC, but in these rare cases with SVC involvement, the place of such preoperative treatment remains unclear.


    References
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 

  1. Ginsberg R.J., Vokes E.E., Raben A. Non-small cell lung cancer. In: DeVita V.T., Hellman S., Rosenberg S.A., eds. Cancer. Principles and practice of oncology. Philadelphia: Lippincott-Raven, 1997:858-911.
  2. McCormack P.M. Extended pulmonary resections. In: Pearson F.G., Deslauriers J., Ginsberg R.J., Hiebert C.A., McKneally M.F., Urschel H.C., eds. Thoracic surgery. New York: Churchill Livingstone, 1995:897-908.
  3. Burt M.E., Pomerantz A.H., Bains M.S. Results of surgical treatment of stage III lung cancer invading the mediastinum. Surg Clin North Am 1987;67:987-1000.[Medline]
  4. Thomas P., Magnan P.E., Moulin G., Giudicelli R., Fuentes P.E. Extended operation for lung cancer invading the superior vena cava. Eur J Cardiothorac Surg 1994;8:177-182.[Abstract/Free Full Text]
  5. Tsuchiya R., Asamura H., Kondo H., Goya T., Naruke T. Extended resection of the left atrium, great vessels, or both for lung cancer. Ann Thorac Surg 1994;57:960-965.[Abstract/Free Full Text]
  6. Inoue H., Shohtsu A., Koide S., Ogawa J., Inoue H. Resection of the superior vena cava for primary lung cancer. Ann Thorac Surg 1990;50:661-662.[Abstract/Free Full Text]
Accepted for publication June 14, 1999.




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