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Ann Thorac Surg 2005;79:234-240
© 2005 The Society of Thoracic Surgeons

Original article: General thoracic

Extended Pneumonectomy With Partial Resection of the Left Atrium, Without Cardiopulmonary Bypass, for Lung Cancer

Lorenzo Spaggiari, MD, PhDa,*, Massimiliano D' Aiuto, MDa, Giulia Veronesi, MDa, Giuseppe Pelosi, MDb, Tommaso de Pas, MDc, Gianpiero Catalano, MDd, Filippo de Braud, MDc

a Department of Thoracic Surgery European Institute of Oncology, Milan, Italy
b Department of Pathology, European Institute of Oncology, Milan, Italy
c Department of Medical Oncology, European Institute of Oncology, Milan, Italy
d Department of Radiotherapy, European Institute of Oncology, Milan, Italy

Accepted for publication June 16, 2004.

* Address reprint requests to Dr Spaggiari, Department of Thoracic Surgery, European Institute of Oncology, Via Ripamonti 435, 20141Milan, Italy (E-mail: lorenzo.spaggiari{at}ieo.it).


   Abstract
Top
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 References
 
BACKGROUND: Extended pneumonectomy with partial resection of the left atrium for lung cancer is not frequently performed; therefore, its results remain controversial. The present study analyzed a single center's experience with this extended surgery, highlighting the surgery's technical aspects, postoperative outcomes, and oncologic results.

METHODS: From November 1996 to December 2003, 15 patients underwent extended pneumonectomy with partial resection of the left atrium for lung cancer, without cardiopulmonary bypass.

RESULTS: Of the 15 patients (median age of 63 years, range 35 to 74 years), 11 were men (73%) and 4 were women. Six patients (40%) underwent preoperative invasive mediastinal staging. Nine patients (60%) underwent induction chemotherapy. Nine patients (60%) underwent right pneumonectomy. Pathologic analysis of the specimens identified 8 patients (53%) with N2 disease, 5 patients (33%) with N1 disease, and 2 patients with N0 disease. The T status was T4 in 10 patients, pT3 in 3 patients, and T0 in the remaining 2 patients. The were 10 squamous cell carcinomas (60%), 2 adenocarcinomas, 1 adenosquamous carcinoma, 1 mucoepidermoid carcinoma, and 1 atypical carcinoid tumor. The median intensive care unit and hospital stay were 1 day and 6.4 days, respectively. There were only two (15.3%) minor postoperative complications (atrial arrhythmias), which were successfully treated medically. There was no postoperative mortality. At completion of the study, 9 patients (60%) were still alive, with 8 showing no evidence of disease. The remaining 6 patients died because of systemic recurrences. The 3-year probability of survival was 39%.

CONCLUSIONS: Extended pneumonectomy with partial resection of the left atrium for advanced lung cancer is a feasible procedure, with low postoperative morbidity and mortality. In fact, it can lead to excellent local control of the disease, if not to a permanent cure in select patients.


   Introduction
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 Abstract
 Introduction
Material and Methods
 Results
 Comment
 References
 
Lung malignancies with cardiac involvement are usually considered absolute contraindications to surgical resection; yet, lung tumors with left atrium involvement may occasionally be surgically removed. But since this extended resection has not been reported on to a large extent in the English-language literature, the lack of knowledge on this subject does not permit any conclusions regarding its technical aspects and oncologic advantages with respect to medical treatment alone [1]. In fact, from among the limited, international experiences described in the literature, it is not even possible to differentiate a resection of the left atrium for T3 lung cancer (ie, no cardiac involvement) performed to obtain free border margins from a resection for lung cancer that directly invaded the muscular wall of the left atrium (T4 disease). And in the latter situation, the resection is obviously more difficult because of the need for substantial clamping of the atrial wall.

First of all, a clarification of the term left atrium resection is mandatory. In our opinion, the true left atrium resection is an extended resection involving the heart, with part of the muscular wall of the left atrium included in the specimen. Resection at the origin of the pulmonary veins, which involves clamping of the left atrium, should not be considered an extended resection involving the heart.

Second, the key, open questions that deal with the technical aspects and their impact in terms of postoperative outcome as well as the oncologic benefits of such an extended surgery in curing this disease need to be addressed.

Without procedural distinctions and a suitable number of patients on which to perform statistical comparisons, no conclusive assessments regarding the real impact of such an extended surgery can be made. Therefore, this study has a threefold purpose: first, to describe the technique used in this extended resection; second, to evaluate morbidity and mortality of the series; and third, to present midterm survival data.


   Material and Methods
Top
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 References
 
A retrospective review of a computerized, single-surgeon (L.S.) database identified 15 patients who, between November 1996 and December 2003, underwent extended pneumonectomy with partial resection of the left atrium for non-small cell lung cancer (NSCLC), without cardiopulmonary bypass (CPB). We only considered the records of those patients who underwent left atrium resection (the presence of muscular atrial wall in the specimen) and pneumonectomy, and excluded the records of those patients in which the left atrium was clamped in order to permit the resection of the pulmonary veins at their origin.

Patients were studied preoperatively by total-body computed tomography (CT) scan, lung perfusion scan, echocardiography, and in the more recent patients, by positron emission tomography (PET) scan and intraoperative transesophageal echocardiography (TEE). Patients with mediastinal lymph nodes greater than 1 cm, or PET-positive in the paratracheal or subcarinal regions, or both, underwent cervical mediastinoscopy. If pleural effusion was suspected, preoperative thoracoscopy was performed to exclude carcinosis.

Our selection criteria for extended pneumonectomy with partial resection of the left atrium were: (1) patients younger than 75 years of age, (2) patients who were motivated and fully informed about the proposed surgery, and (3) a thorough, cardiorespiratory evaluation. Patients were excluded if they presented with cardiac diseases, chronic renal and hepatic insufficiencies, or a predicted postoperative forced expiratory volume in 1 second of less than 40%.

Our oncologic criteria were:

• Bulky N2 disease (ie, invasion of the mediastinal structures) was a definitive contraindication to surgical resection, even when there was a good response to preoperative chemotherapy.
• Metastases (diagnosed by mediastinoscopy) in R2 and L2 were absolute contraindications to surgical resection, even when there was a good response to preoperative chemotherapy, because of evidence of extensive metastatic disease.
• Intranodal metastases in R4 and 7 stations (diagnosed by mediastinoscopy) indicated induction chemotherapy, followed by surgery if there was a response.

Thus, patients with bulky or extensive lymph node involvement, or even contralateral node involvement, were considered not suitable for resection, even after induction chemotherapy.

The rationale for doing induction chemotherapy was (1) in the presence of positive (at mediastinoscopy) mediastinal lymph nodes in stations R4 and 7, induction chemotherapy improves survival among this group of patients, based on data derived from stage IIIA (ie, sterilized systemic micrometastases in patients with positive lymph nodes); and (2) induction chemotherapy decreases large disease from invading the left atrium, thus reducing the risk of incomplete resection or nonresectability at preoperative thoracic CT.

Preoperative pathologic confirmation of atrial infiltration is impossible with a minimally invasive approach, because it is necessary to perform a biopsy of the heart for the histologic confirmation that tumor is within the atrial wall (T4). Therefore, the criteria used for documenting direct invasion of the left atrium (T4) were clinical. Specifically, T4 status was clinically documented by using a spiral chest CT scan (Fig 1).



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  		Fig 1. Preoperative chest computed tomography scan after induction chemotherapy. The tumor has diffusely invaded the left atrium. Note the interatrial groove (arrow) which must be dissected in order to safely clamp the left atrium (LA) to perform the complete resection.

 
The radiologic criteria used for "suspicion" of infiltration were considerable contact with the atrial wall by the neoplasm, the loss of definition at the level of the atrial wall during fast-volume acquisitions, and alterations in the contact zone after intravenous contrast enhancement of the atrial wall. The presence of a voluminous polypoid mass in the atrial cavity also served as clear criterion, but became a contraindication to atrial resection without CPB. In the more recent patients, the use of TEE further increased clinical suspicion of left atrial infiltration.

Technique
All patients were resected without CPB. The operation was carefully planned, based on preoperative data from the chest CT scan, to better analyze the feasibility of resecting the atrial wall. For right side tumors in particular, it is important to take into consideration the length of the interatrial groove and the distance of the tumor from the origin of the contralateral pulmonary veins in order to maintain sufficient space and avoid occluding veins during clamping (Fig 1).

If the patient is a candidate for left atrium resection, the preferred approach is a full posterolateral thoracotomy. Before beginning the pneumonectomy, the pericardium is fully opened in order to identify the extent of atrial involvement. The origin of the contralateral veins is also identified, again in order to avoid their occlusion during clamping.

For anatomic reasons, right side tumors can invade the left atrium quickly and diffusely owing to the shortness of the right upper pulmonary vein. To increase the length of the right atrial cuff, the epicardium between the right and left atrium (the interatrial groove) is carefully dissected so that the left atrial cuff can be lengthened to about 2 cm. This procedure, the Sondergaard technique, [2] is more evident in the upper part of the left atrium, near the superior vena cava (Fig 2). It increases the margin of resection; thus, the risk of clamping the right atrium during the operation is avoided. A large Satinsky clamp is then put in place to evaluate the surgical feasibility of atrial resection and to observe the cardiocirculatory ef-fects of atrial volume reduction (Fig 3). During this preliminary clamping, the TEE permits cardiac alterations to be monitored.



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  		Fig 2. The Sondergaard technique, in which the dissection of the interatrial groove during right pneumonectomy permits elongation of the left atrial cuff to about 2 cm. The dashed line represents the incision on the LA. (LA = left atrium; RA = right atrium.)

 


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  		Fig 3. After dissection of the interatrial groove, and before resection, the left atrial wall is clamped with a large Satinsky clamp. This allows the identification of any cardiac alterations.

 
Pneumonectomy is then initiated, with resection of the pulmonary artery first, followed by resection of the main right bronchus (after complete dissection of the subcarinal nodes), leaving the resection of the atrial wall for last. A moderate traction of the lung towards the thoracotomy permits the lengthening of the atrial cuff so that the large clamp can be put in place safely. After detachment of the lung, two running 2-0 polypropylene sutures are generously placed on the left atrium (Fig 4).



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  		Fig 4. The resection and subsequent atrial reconstruction with double running sutures of 2-0 polypropylene are in progress.

 
The resection for left side tumors is easier, when feasible. The operative steps are virtually the same, except for the dissection of the interatrial groove. Also, the amount of the left atrium that can be removed is smaller because of the position of the heart and its relation to the other mediastinal organs. In fact, with left tumors, quick multiorgan infiltration (left atrium, aorta, esophagus, etc) is a common occurrence. Thus, the number of extended pneumonectomies with partial resection of the left atrium is lower than for those of the right (Fig 5).



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  		Fig 5. Operative picture shows extended left pneumonectomy with partial resection of the left atrium and thoracic aorta.

 

   Results
Top
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 References
 
Eleven of the 15 patients (median age of 63 years, range 35 to 74 years) were men (73%) and 4 were women. Six patients (40%) underwent preoperative invasive mediastinal staging by way of mediastinoscopy (n = 3), mediastinoscopy and thoracoscopy (n = 2), or thoracoscopy (n = 1) to evaluate the status of the mediastinal lymph nodes and to check for pleural effusion (to exclude carcinosis). Nine patients (60%) underwent preoperative chemotherapy (8 patients with a cisplatin-gemcitabine regimen). No preoperative radiotherapy was used. Right pneumonectomy with radical lymph node dissection was performed on 9 patients (60%), and left pneumonectomy with radical lymph node dissection was performed on the remaining 6 patients.

The pathologic nodal status was N2 in 8 patients (53%), N1 in 5 patients (33%), and N0 in the remaining 2 patients. The pathologic T status was T4 (histologic evidence of the tumor within the atrial wall) in 10 patients. The remaining 5 patients underwent chemotherapy before extended pneumonectomy. Three demonstrated T3 disease in which there was no histologic presence of the tumor within the atrial wall, but infiltration was noted at the origin of the pulmonary veins; thus, an atrial wall resection was required to achieve a complete resection. The remaining 2 patients demonstrated a complete response (T0) (no evidence of disease in the specimen). Before induction chemotherapy, all 5 of these patients were considered cT4, based on the criteria previously reported. According to our clinical criteria for defining T status, 70% of the cases thus had a pathologic confirmation of atrial involvement.

All patients underwent complete resection (no positive margin after resection). After pneumonectomy, there were 10 squamous cell carcinomas (60%), 2 adenocarcinomas, 1 adenosquamous carcinoma, 1 mucoepidermoid carcinoma, and 1 atypical carcinoid tumor. These last two patients had a preoperative diagnosis of NSCLC and were therefore included in the analysis of postoperative outcome (intent to treat). However, they were expected to demonstrate a different long-term outcome and thus were eliminated from the survival analysis.

The median intensive care unit stay and hospital stay of the overall series was 1 day and 6.4 days, respectively. There were only two (15.3%) minor postoperative complications (atrial arrhythmias), which were successfully treated medically. No postoperative deaths occurred. Adjuvant radiotherapy was performed on 5 patients.

All patients were followed-up within a median of 16.5 months, ranging from 2 to 45 months. At the completion of the study, 9 patients (60%) were still alive, of whom 8 had no evidence of disease. Local control was excellent (0% local recurrence), and those patients who died did so because of systemic recurrences.

Survival was calculated according to the Kaplan-Meier method (except for the 2 patients with mucoepidermoid carcinoma and atypical carcinoid tumor), with the 3-year probability of survival at 39% (Fig 6). The number of patients at risk at 1-, 2-, and 3-years were 12, 11, and 9, respectively.



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  		Fig 6. Survival curve (Kaplan-Meier method) of patients who underwent extended pneumonectomy with partial resection of the left atrium for lung cancer, without cardiopulmonary bypass. The 3-year probability of survival was 39%; the patients at risk at 12, 24, and 36 months were 12, 11, and 9 respectively.

 

   Comment
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
References
 
Extended resections for locally advanced NSCLC are not often performed, and the results in terms of survival are still unclear. Nevertheless, some T4 tumors can be safely resected—preferably after induction chemotherapy—and with interesting results in terms of local control and long-term survival [1, 3]. The resection of the left atrium because of invasion by NSCLC is also infrequently performed, with both technical data and oncologic results still unclear.

With regards to the technical aspects, one of the most viable ways to reach standardized results is through differentiation between the true atrial resection, characterized by the presence of a large piece of the atrial wall in the specimen that indicates a large infiltration by the tumor (T4 disease) (Fig 7), and the intrapericardial pneumonectomy that involves clamping the left atrium to allow resection for T3 disease at the origin of the pulmonary veins. We do not believe that the latter should be considered an extended resection involving the left atrium.



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  		Fig 7. Same patient as in Figure 1. Left atrial wall resection after right pneumonectomy. Note the large portion of the atrial wall resected without cardiopulmonary bypass. (LA = left atrium.)

 
This distinction is important because the intrapericardial resection at the origin of the pulmonary veins uses limited clamping of the left atrium and can be performed without particular difficulty. Resection of the atrial wall, on the other hand, is more complex. To obtain free border margins, the left atrium has to be substantially resected (Fig 7, Fig 8, Fig 9). This is possible either by using the technique reported here—resection after direct clamping of the left atrium—or by resection of the left atrium during cardiac arrest with CPB. With the latter technique, a large part of the atrial wall can be removed; in fact, it has been previously reported that with this technique, one third of the left atrial volume can be resected without reconstruction [4]. To reach this volume of resection without CPB (Fig 8, Fig 9), a careful, preoperative evaluation is mandatory.



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  		Fig 8. Same patient as in Figure 1. Operative view after extended right pneumonectomy with partial resection of the left atrium. Note the left-atrial volume reduction. Note the double 2-0 polypropylene suture (continuous arrow) with polytetrafluoroethylene reinforcements (dotted arrow) being used on the heart.

 


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  		Fig 9. Same patient as in Figure 1. Computed tomography thoracic scan taken at 1 month follow-up. Note the left atrium volume reduction (continuous arrow) and the origin of the (left) contralateral inferior pulmonary vein (dotted arrow). This resection was performed without cardiopulmonary bypass.

 
Apart from the radiologic exams used to exclude extrathoracic metastases, atrial resection should be planned based on data collected from high-resolution chest CT scans and TEE that are used to analyze the length of the interatrial groove (for right pneumonectomy) and to analyze the distance between the tumor and the origin of the contralateral veins. If the resection is not carefully planned, the risk is high of incomplete surgery that leaves microscopic residual tumor in the margin.

The atrial-clamping technique is not difficult to perform, but it could cause hemodynamic instability if the resection is not adequate (too large of an atrial volume reduction or occlusion of the contralateral vein). An alternative to this simple clamping technique could be the use of total CPB. However, this procedure is rarely used, and at present, reports on only a few patients have been published [5, 6].

Supporting CPB is that (1) it may facilitate resection with a subsequent reconstruction of the wall using a patch, thus reducing the risk of both hemodynamic instability and tumor fragmentation with subsequent embolization, and (2) during the operation, frozen-section analyses can done on the atrial margins to avoid incomplete resections.

However, cardiocirculatory arrest and its complications are associated with high risk in patients who require pneumonectomy. In fact, it has been suggested that CPB may reduce survival in patients with lung cancer [7] because its use may, theoretically, facilitate metastasization in that the need for blood transfusions and the activation of various cellular inflammatory systems decrease the patient's immune system. CPB may also increase the risk of acute respiratory distress syndrome in patients requiring pneumonectomy because of increased blood transfusions, heparinization, and the use of large volumes of saline solution, as well as increase the risk of postoperative hemothorax.

In our experience, no hemodynamic problems were recorded with the direct clamping technique, either during or after resection. An echocardiography performed on the more recent patients before their discharge did identify an increase in pulmonary artery pressure, but with no clinical significance. As long as preoperative selection is detailed and accurate, postoperative morbidity and mortality will be low, suggesting that this surgery can be safely performed. Right pneumonectomies are more frequently performed than left pneumonectomies. The reason for this is probably due to the anatomic characteristic of the left lung: the presence of the aortic arch and the position of the heart may contraindicate resection because the neoplasm could quickly infiltrate the multiorgans (aorta, heart, left atrium, etc.) (Fig 5).

With regards to the oncologic aspects, in our previous analysis (personal communication, Regnard JF, Spaggiari L, 8eme Journee de Pathologie Thoracique, Hopital Marie Lannelongue, Paris, 29 Mars 1996) that covered a 12-year period, the results from extended surgical resection with partial resection of the left atrium were disappointing (5-year survival, 19%; 11% in N2 patients). Most likely, these disappointing results were derived, in part, from an out-of-date patient selection; plus, only a small number of patients in that series underwent induction chemotherapy.

In the recent literature, Tsuchiya [8] reported on the largest study to date (in 1994) concerning this extended surgery. All 44 patients underwent left atrium resection, without CPB, with only a vascular clamp. The defect was then sutured directly. Only 7 patients (16%) survived for more than 3 years, and 3 of these had T3 disease. Fukuse and colleagues [9] later reported on 14 patients who underwent left atrium resection, with a median survival of 10 months.

Apart from these recent experiences and a few others with a very limited number of patients [10, 11], no other occurrences involving this surgery are available, leaving this surgery still anecdotal. However, these limited experiences do demonstrate that in select patients, extended pneumonectomy with partial resection of the left atrium may improve local control, with a permanent cure in some cases.

Sixty percent of the patients in our study underwent induction chemotherapy; however, 53% of patients still showed N2 disease even after induction chemotherapy, proving that in these patients, the percentage of mediastinal lymph node involvement was high. Induction chemoradiotherapy was never used in this series. The rationale for excluding radiotherapy was to limit the heart toxicity derived from high-dose radiotherapy before surgery. Yet, radiotherapy was indicated in those patients positive for highest mediastinal lymph nodes after resection. Even with the tumor's advanced stage, the results after complete surgery in terms of the rate of local recurrence were excellent. And the 3-year probability of survival of 39% confirmed the validity of this extended resection in treating such an extended disease. However, taking into account the small number of patients in the present series, no definitive conclusions can be made. In fact, questions concerning the role of induction chemotherapy and surgical resection for N2 disease are still open.

Based on our preliminary results, we suggest a preoperative mediastinoscopy be performed on all patients with left atrium involvement to exclude diffuse (R2) mediastinal lymph node involvement. All patients should then undergo preoperative chemotherapy. Intraoperative echocardiography should also be performed before resection to identify the risk of hemodynamic complications.

We conclude that if carefully evaluated, involvement of the left atrium need not be considered an absolute contraindication to surgical resection. In fact, in highly selected patients, extended pneumonectomy with partial resection of the left atrium can provide excellent local control of the disease, and even lead to a definitive cure in some patients.


   References
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 

  1. Patterson GA. Extended pulmonary resectionIn: Griffith Pearson F, Cooper JD, Deslauriers J, et al. editors. Thoracic Surgery. Philadelphia: Churchill Livingstone; 2002. pp. 1045-1061.
  2. Le Brigand H. Notions tactiques communesIn: Le Brigand H, editor. Nouveau traite de technique chirurgicale. Appareil respiratoire, mediastin, paroi thoracique. Paris: Masson; 1973. pp. 165-239.
  3. Grunenwald DH. Surgery for advanced stage lung cancer Semin Surg Oncol 2000;18:137-142.[Medline]
  4. Shirakusa T, Kimura M. Partial atrial resection in advanced lung carcinoma with and without cardiopulmonary bypass Thorax 1991;46:484-487.[Abstract/Free Full Text]
  5. Ferguson Jr ER, Reardon MJ. Atrial resection in advanced lung carcinoma under total cardiopulmonary bypass Tex Heart Inst J 2000;27:110-112.[Medline]
  6. Jouan J, Baron O, Sagan C, Despins P, Michaud JL. Exereses des cancers bronchopulmonaires envahissant l'oreillette gauche: apport de la circulation extracorporelle J Chir Thorac Cardiovasc 2003;7:23-26.
  7. Brutel de la Riviere A, Knaepen P, Van Swieten H, Vanderschueren R, Ernst J, Van den Bosch J. Concomitant open heart surgery and pulmonary resection for lung cancer Eur J Cardiothorac Surg 1995;9:310-313.[Abstract]
  8. 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]
  9. Fukuse T, Wada H, Hitomi S. Extended operation for non-small cell lung cancer invading great vessels and left atrium Eur J Cardiothorac Surg 1997;11:664-669.[Abstract]
  10. Bernard A, Bouchot O, Hagry O, Favre JP. Risk analysis and long-term survival in patients undergoing resection of T4 lung cancer Eur J Cardiothorac Surg 2001;20:344-349.[Abstract/Free Full Text]
  11. Doddoli C, Rollet G, Thomas P, et al. Is lung cancer surgery justified in patients with direct mediastinal invasion Eur J Cardiothorac Surg 2001;20:339-343.[Abstract/Free Full Text]



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