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Ann Thorac Surg 1996;62:342-346
© 1996 The Society of Thoracic Surgeons

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Original Articles: General Thoracic

Results of Combined Pulmonary Resection and Cardiac Operation

Divisions of Thoracic and Cardiovascular Surgery, The Toronto Hospital, University of Toronto, Toronto, Ontario, Canada

	Abstract

Top Footnotes Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
Background. Concomitant lesions of the heart and lung are uncommon, but when present they pose a therapeutic challenge for thoracic surgeons. A combined procedure avoids the need for a second major thoracic procedure and may improve outcomes and provide economic benefit. However, cardiopulmonary bypass may adversely affect the natural history of pulmonary malignancies.

Methods. The clinical records of 30 patients were reviewed who underwent simultaneous lung resection and cardiac operations between January 1982 and July 1995. Follow-up was obtained on all 30 patients (mean follow-up, 22 months; range, 1 to 100 months).

Results. Twenty-four patients underwent coronary artery bypass grafting in conjunction with pulmonary resection. Six patients underwent aortic (n = 4) or mitral (n = 2) valve replacement. The pulmonary resections consisted of pneumonectomy (n = 3), lobectomy (n = 14), wedge excision (n = 12), and tracheal resection (n = 1). Twenty-one patients had pathologic findings that confirmed adenocarcinoma (n = 10), squamous cell carcinoma (n = 5), small cell carcinoma (n = 2), or other malignancy (n = 4). Tumor stage of primary lung cancers was stage I, n = 12; stage II, n = 3; and stage IIIa, n = 2. Pathologic examination revealed benign disease in 9 patients. There were two operative deaths, one due to aspiration and one due to stroke. There were three late deaths, two cardiac and one of metastatic disease. Overall late survival was 85% ± 7% and 73% ± 16% at 1 and 5 years, respectively. Actuarial survival for patients with malignant disease was 64% at 5 years.

Conclusions. Simultaneous cardiac operation and lung resection was not associated with increased early or late morbidity or mortality. Cardiopulmonary bypass does not adversely affect survival in patients with malignant disease. Cardiac valve replacement can be performed safely in conjunction with pulmonary resection.

	Introduction

Top Footnotes Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
See also page 346.

Concomitant lesions of the heart and lungs are uncommon, but when present they pose a therapeutic dilemma to the cardiothoracic surgeon. Most patients present with coronary artery or other cardiac disease and are found to have an asymptomatic pulmonary lesion on their preoperative chest roentgenogram. Less frequently, patients with lung cancer are found to have substantial cardiac disease which, if untreated, greatly increases the perioperative morbidity and mortality of pulmonary resection [1, 2]. Surgeons may be reluctant to perform a one-stage simultaneous procedure because of concerns regarding systemic heparin administration or operative exposure through a median sternotomy [3, 4].

However, a one-stage combined procedure avoids the need for a second major thoracic procedure, may reduce overall hospital stay, and may result in economic benefit. The early results of combined cardiac operation and pulmonary resection have been encouraging [5–11]. Although a combined operation has proven to be a technical success, the relatively small number of patients who have both cardiac disease and lung cancer has made it difficult to study the long-term results of the combined procedure. In addition, the long interval required to accumulate enough experience with combined operation has resulted in a confounding of results because of changes in operative technique or perioperative management of lung cancer.

The long-term prognosis is particularly important in considering lung cancer, as the use of cardiopulmonary bypass (CPB) is known to have several systemic effects [1212–16]. The immunologic consequences of CPB and their effects on the long-term prognosis of patients with lung cancer are not well understood [17].

This study describes a 14-year experience with combined lung resection and cardiac operation at The Toronto Hospital. We compare the results of lung resection for malignant disease versus benign disease in an attempt to characterize the effect of CPB on the long-term prognosis of patients with lung cancer.

	Material and Methods

Top Footnotes Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
We reviewed the clinical records of all patients who underwent pulmonary resection and cardiac operation requiring extracorporeal circulation between January 1, 1982 and July 1, 1995. Patients who underwent single or double lung transplantation necessitating CPB (n = 69) were excluded.

Follow-up data were collected at the thoracic surgery postoperative clinics and were complete for all patients. Follow-up ranged from 1 to 101 months (mean, 29 months).

Operative Technique
Mediastinoscopy was performed at the beginning of the operative procedure in 16 of the 18 patients who presented preoperatively with abnormal chest roentgenograms or with a known diagnosis of malignancy. No N2 disease was found in any of these 16 patients. The pulmonary resection was performed before the institution of CPB in 4 patients, during CPB in 19 patients, and after reversal of heparin treatment in 7 patients. In 23 patients, the cardiac procedure was completed before the lung resection.

Postoperative care was uniform in all patients. Two patients received adjuvant chemotherapy after lung resection. Both of these patients had a diagnosis of small cell carcinoma.

Statistical Analysis
Statistical analysis was performed with the BMDP statistical program (BMDP Statistical Software, Los Angeles, CA). Categoric data were evaluated using ² analysis or Fisher's exact test as appropriate. Continuous variables were analyzed using analysis of variance. Actuarial survival was determined using the Kaplan-Meier method [18]. The generalized Wilcoxon test was used to compare survival between groups. Statistical significance was assumed at p less than 0.05.

	Results

Top Footnotes Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
Preoperative Data
The mean age of the 30 patients was 61 ± 13 years (range, 17 to 79 years). There were 26 men and 4 women. Left ventricular ejection fraction was greater than 0.60 in 9, 0.40 to 0.59 in 16, 0.20 to 0.39 in 5, and less than 0.20 in none. Tumor stage (primary lung cancer) was stage I in 12, stage II in 3, and stage IIIa in 2. Other malignancies were present in 4 patients.

Abnormal preoperative chest roentgenograms were detected in 18 patients who presented with cardiac complaints. Seven patients with known pulmonary neoplasms were discovered to have substantial underlying coronary artery disease on the basis of history and physical examination. These patients subsequently underwent exercise stress tests or thallium scanning before coronary angiography and consideration of simultaneous coronary revascularization. One patient presented with hemoptysis and was found to have a tracheal neoplasm and two-vessel coronary artery disease. Four patients underwent cardiac operation and had pulmonary lesions detected intraoperatively; the pulmonary lesion was found to be a benign granuloma or emphysematous bleb.

Operative Data
The average aortic cross-clamp time was 54 ± 21 minutes (range, 23 to 106 minutes), and CPB time was 109 ± 34 minutes (range, 38 to 158 minutes).

The pulmonary resection consisted of pneumonectomy in 3 patients (10%), lobectomy in 14 (47%), wedge resection in 12 (40%), and tracheal resection in 1 (3%). Twenty-four patients received one or more coronary artery bypass grafts (one in 1, two in 6, three in 10, four in 5, and more than four in 2). Six patients had either an aortic (n = 4) or mitral (n = 2) valve replacement. Right or left atrial resection was required in 2 patients. One patient required a right atrial resection and right upper lobe wedge resection for metastatic renal cell carcinoma, and the second patient required a left atrial resection for myxoma combined with a right lower lobectomy for a metastatic chondrosarcoma.

Pathologic examination revealed a malignant lesion in 21 patients: adenocarcinoma (n = 10), squamous cell carcinoma (n = 5), small cell carcinoma (n = 2), metastatic renal cell carcinoma (n = 3), and metastatic chondrosarcoma (n = 1). The majority of patients (n = 12, 57%) presented with stage I disease. Two patients were found to have N2 disease at thoracotomy despite negative mediastinoscopy results. These patients are both alive and disease free at 2 and 3 years, respectively. Benign lesions were excised in 9 patients (granulomata or emphysematous bleb) (Fig 1).

View larger version (19K): [in this window] [in a new window]   Fig 1. . Pathologic diagnosis in 30 patients undergoing combined lung resection and cardiac operation. (CA = carcinoma.)

Prolonged ventilation (>24 hours) was required for 4 additional patients, who were all discharged home in satisfactory condition. Only 1 patient required reopening for persistent chest tube drainage. This patient had undergone a tracheal resection and double coronary artery bypass. No source of bleeding was identified at reexploration. One patient suffered a pulmonary embolus on the third postoperative day. This patient experienced a second pulmonary embolus with resultant respiratory arrest. This patient received an inferior vena caval filter and was eventually discharged home on the 26th postoperative day. One patient who had received five coronary artery bypass grafts and underwent right upper lobectomy required a permanent pacemaker for third-degree heart block. There were no perioperative myocardial infarctions.

The postoperative length of stay for all patients was 12.1 ± 7.6 days (median, 10 days; range, 4 to 25 days). For those patients who were discharged from the hospital, the average length of stay was 12.5 ± 7.8 days (median, 10 days; range, 5 to 25 days).

Postoperative Data
There were three late deaths: Two patients died of fatal myocardial infarctions and the third patient died of recurrent malignant disease. Overall actuarial survival was 85% ± 7% at 1 year, 85% ± 7% at 5 years, and 61% ± 21% at 7 years (Fig 2).

View larger version (17K): [in this window] [in a new window]   Fig 2. . Actuarial survival in all 30 patients undergoing combined lung resection and cardiac operation.

View larger version (23K): [in this window] [in a new window]   Fig 3. . Comparison of actuarial survival in patients with benign disease (n = 9) versus malignant disease (n = 21) confirmed on pathologic examination. (NS = not significant.)

	Comment

Top Footnotes Abstract Introduction Material and Methods Results Comment Acknowledgments References

The Effect of Cardiopulmonary Bypass
Cardiopulmonary bypass has been shown to produce several systemic side effects [12–16]. The immunologic effects of CPB are of concern in patients with malignant disease. Cardiopulmonary bypass is known to affect neutrophils and platelets and to result in complement activation. This inflammatory stimulation may be of benefit in patients with malignancies. However, attempts to resect neoplasms during CPB may lead inadvertently to systemic seeding of malignant cells. Blood transfusion is associated with an increased risk of recurrence. In addition, there is a potent immunosuppressive effect of CPB, which may be detrimental to the long-term prognosis of patients with malignancies.

A report by Canver and associates [17] demonstrated that cardiac operation in patients with a previously resected cancer gave acceptable results, with a 96% 3-year survival. However, only 1 patient in this series of 46 had a diagnosis of lung cancer. In addition, all patients in this series had undergone a previous "curative" resection of their malignancy and thus, their tumor burden was minimal at the time of cardiac operation. A study by Ulicny and co-workers [9] examined the results of concomitant cardiac and pulmonary procedures. In this series of 19 patients, the authors found a 5-year survival of only 40% in patients with malignant disease, compared with 75% in patients found to have a benign pulmonary lesion. A similar result was obtained in a larger series reported by Brutel de la Riviere and colleagues [10]. In a group of 79 patients who underwent a combined procedure over a 15-year period, the overall survival at 5 years was 42%. The authors found that the 5-year survival was higher in patients who underwent lung resection before CPB (55%) versus those who underwent lung resection after CPB (20%). Unfortunately, this difference failed to achieve statistical significance because of the small number of patients available for analysis at 5 years. Nevertheless, these results do suggest a potential detrimental effect of CPB. A report by Naruke and associates [19] demonstrated that among stage I tumors, overall 5-year survival in non-small cell neoplasms was approximately 65%. Our results in patients with malignant disease appear to be similar to those obtained in patients with benign pulmonary lesions, with an overall 5-year survival of greater than 80%. Thus, it does not appear that CPB had a detrimental effect on 5-year survival in our series. In addition, the predominant cause of late death in our series was cardiac, not recurrence of malignancy. Therefore, patients who undergo a combined procedure may be at risk for recurrence, but they are just as likely to die of progression of their cardiac disease.

Timing of Lung Resection
The timing of the lung resection may be important for both early and late operative outcomes. In addition to the concern regarding systemic metastases during CPB, there is a danger of bleeding secondary to anticoagulation therapy. Ulicny and co-workers [9] examined the role of CPB in combined operations and concluded that lung resection during CPB was associated with excessive bleeding and pulmonary complications. These authors recommended resection after reversal of anticoagulation with protamine sulfate. In our series, 19 (63%) of the patients underwent resection during CPB, and only 1 patient suffered from a bleeding complication requiring reexploration.

Our preferred approach to the stable patient is to perform a preoperative staging mediastinoscopy. We then complete the cardiac procedure and remove the aortic cross-clamp. Resection of the pulmonary lesion is performed during CPB. Cardiopulmonary bypass facilitates resection of left lower lobe lesions through a median sternotomy. Four patients in our series underwent lung resection before the institution of CPB. All 4 of these patients underwent wedge resections of peripheral tumors. Three of the 4 were found to have benign disease; the fourth patient was found to have an adenocarcinoma and proceeded to formal right lower lobectomy after replacement of his aortic valve. Seven patients underwent pulmonary resection after discontinuation of CPB. If there is concern about the patient's ability to wean from CPB, we prefer to complete the cardiac procedure and decannulate. If the patient remains stable after discontinuation of CPB, we proceed with the pulmonary resection.

In patients undergoing valve operations, we prefer to resect the pulmonary lesion after closure of the pericardium to avoid contamination by respiratory pathogens. In our small series of 6 patients, we did not observe any complications related to infective endocarditis. We believe that our technique of pericardial closure partially protects against infection due to the presence of a transected airway.

Summary
The early outcomes of combined pulmonary resection and cardiac operation have demonstrated that this approach is both feasible and safe in carefully selected patients. The long-term results of concomitant operation are less well defined because of the lack of a large series of patients available for follow-up. In our series, late death was predominantly related to cardiac causes, which suggests that the adverse effects of CPB on pulmonary malignancies may not be an important factor when considering a patient for a simultaneous procedure.

When faced with a patient with concomitant pulmonary and cardiac disease, we favor a single-stage combined procedure. The pulmonary resection is facilitated by CPB, and we have not observed any increased morbidity from anticoagulation therapy. If the cardiac procedure is difficult or the patient is unstable, the lung resection can be delayed. We recommend closure of the pericardium in patients undergoing simultaneous valve operation and lung resection to protect against contamination from a transected airway.

In certain high-risk patients, separate staged procedures may be the most prudent course of action. However, in carefully selected patients with concomitant disease, a combined approach can be used with minimal perioperative morbidity and acceptable long-term results.

	Acknowledgments

Top Footnotes Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
This study was supported by the Heart and Stroke Foundation of Ontario (HSFO): Dr Rao is a Pharmaceutical Roundtable Fellow of the HSFO; Dr Weisel is a Career Investigator of the HSFO; Dr Cohen is a Surgical Scientist at the Department of Surgery, University of Toronto; and Dr Christakis is a Research Scholar of the HSFO.

We thank Ms Joan Ivanov, RN, MSc, for her statistical expertise and assistance with the preparation of the manuscript.

	Footnotes

Top Footnotes Abstract Introduction Material and Methods Results Comment Acknowledgments References

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

Address reprint requests to Dr Weisel, Division of Cardiovascular Surgery, EN 14-215, The Toronto Hospital, 200 Elizabeth St, Toronto, Ontario M5G 2C2, Canada.

	References

Top Footnotes Abstract Introduction Material and Methods Results Comment Acknowledgments References

 

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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): Vivek Rao Thomas R. J. Todd Richard D. Weisel Masashi Komeda Gideon Cohen John S. Ikonomidis George T. Christakis Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Rao, V. Articles by Christakis, G. T. Search for Related Content PubMed PubMed Citation Articles by Rao, V. Articles by Christakis, G. T. Related Collections Related Article