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Ann Thorac Surg 2004;77:1023-1027
© 2004 The Society of Thoracic Surgeons

Original article: general thoracic

Simultaneous lung resection for cancer and myocardial revascularization without cardiopulmonary bypass (off-pump coronary artery bypass grafting)

Wojciech Dyszkiewicz, MD, PhDa, Marek M. Jemielity, MD, PhDb, Cezary T. Piwkowski, MDa*, Bartlomiej Perek, MDb, Mariusz Kasprzyk, MDb

a Thoracic Surgery, Karol Marcinkowski University of Medical Sciences, Pozna, Poland
b Cardiac Surgery, Karol Marcinkowski University of Medical Sciences, Pozna, Poland

Accepted for publication July 21, 2003.

* Address reprint requests to Dr Piwkowski, Department of Thoracic Surgery, Karol Marcinkowski University of Medical Sciences, Szamarzewski st. 62, 60-569 Pozna, Poland
e-mail: cezary_p{at}hotmail.com


   Abstract
Top
 Abstract
Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 
BACKROUND: Patients with resectable lung cancer and unstable coronary heart disease are at high risk of postoperative death or severe cardiovascular complications. The aim of this study was to present the early results of radical lung resection for cancer with simultaneous myocardial revascularization on the beating heart (off-pump coronary artery bypass [OPCAB]).

METHODS: From 1999 to 2002, thirteen patients (9 men and 4 women, aged 54 to 71 years, mean age 64 yrs) with resectable lung cancer and unstable angina or a recent history of myocardial infarction, were operated on. All of them underwent coronary angiography and neither coronary angioplasty nor stenting were feasible. Eight lobectomies, three pneumonectomies, and two wedge resections were carried out together with aortocoronary graft implantation (mean number of grafts: 1.7 per patient). Myocardial revascularization without cardiopulmonary bypass (OPCAB) preceded the lung resections. The preferred approach to the heart and lung was by sternotomy.

RESULTS: There were no postoperative deaths in this group of patients. The most frequent postoperative complication was prolonged air leakage and one patient required respiratory support for two days. In one patient, significant blood loss was observed with a need for rethoracotomy. Transient supraventricular cardiac arrhythmias occurred in three patients. None of the patients showed evidence of myocardial ischemia after surgery. Patients were followed up for 7 to 36 months. None had acute myocardial infarction. In one patient, who underwent lobectomy, local recurrence was found. In another patient, who underwent pneumonectomy, distant metastases occurred in the third year of observation.

CONCLUSIONS: Lung resection carried out simultaneously with OPCAB is a safe and effective method for the treatment of lung cancer and myocardial ischemia.


   Introduction
Top
 Abstract
 Introduction
Material and methods
 Results
 Comment
 Acknowledgments
 References
 
Patients with lung cancer and concomitant unstable angina are at high operative risk if pulmonary resection is performed before myocardial revascularization [1–3]. This risk could be markedly reduced if both procedures were carried out during the same operative session and potentially dangerous delays would be avoided. Surprisingly, the number of patients referred for combined cardiothoracic procedures is very low and does not exceed 0.4% of all bypass operations reported by cardiac surgeons [4, 5]. It seems, however, that this number should be higher because approximately 10% of patients with operable lung cancer also have symptoms of ischemic heart disease [3]. There are three possible explanations for such an apparently low interest in combining cardiac and thoracic surgery. First, cardiac surgeons are not always involved in the preoperative assessment of patients with lung cancer. Second, less invasive methods such as coronary angioplasty and stenting are now replacing coronary surgery and these techniques are also applicable to oncology patients. Third, conventional coronary artery bypass grafting (CABG) involving the use of extracorporeal circulation, if done concomitantly with pulmonary resection, carries an increased risk of morbidity and mortality [5–7]. However, this opinion is now changing since coronary surgery carried out on the beating heart (off-pump CABG [OPCAB]) successfully competes with coronaroplasty and conventional coronary artery bypass (CCAB). The OPCAB method therefore appears to be very suitable for patients requiring simultaneous thoracic and cardiac operations.

In reviewing the literature to the year 2002, we found only a few publications on this topic and the majority of these were in the form of isolated case reports. We therefore decided to present the early results of treatment obtained in a group of 13 patients with lung cancer and unstable angina pectoris.


   Material and methods
Top
 Abstract
 Introduction
 Material and methods
Results
 Comment
 Acknowledgments
 References
 
This clinical study involved 13 patients who underwent simultaneous OPCAB and resection of lung cancer. The study documents the results of treatment carried out in the cardiac and thoracic departments of the University of Medical Sciences in Poznan, Poland, between 1999 and 2002. There were 9 men and 4 women with an age range of 54 to 71 years (mean 64). Their main symptoms were as follows: cough (30%), chest pain (64%), and hemoptysis (10%). Eight of them had had a myocardial infarction shortly before the established diagnosis of malignancy (20 days to 2 months). In the remaining 5 patients, symptoms of unstable angina pectoris were present in spite of pharmacological treatment. The preoperative diagnostic procedures included clinical histories, physical examination, complete blood cell count, liver and kidney function tests, chest roentgenogram, spirometry of the lung, ultrasonography of the abdomen, fiberoptic bronchoscopy with cytology and histology of the biopsy specimens, transthoracic or transbronchial needle biopsies, computed tomography of the chest, and mediastinoscopy whenever required (enlargement of mediastinal lymph nodes). The routine cardiologic examination consisted of a 12 lead electrocardiogram, echocardiography, catheterization of the heart, and blood sampling for the asessment of ischemic markers such as creatine kinase (CK-MB) and troponin I. Patients with marked deterioration of respiratory function (VC < 40%, FEV1/VC < 35%, FEV1 < 1.5 L) or cardiac function (New York Heart Association [NYHA] class III, Canadian Cardiovascular Society [CCS] III) were not referred to surgery.

Preoperative lung cancer staging, based on clinical, pathologic, and laboratory findings, was used in accordance with the New International System for Staging Lung Cancer. Five patients were assigned to stage II A, five to II B, one to I A, one to I B, and one to III A. Patients with N2 disease were not referred to surgery. Histopathologic examination revealed squamous cell carcinoma in 11 patients and adenocarcinoma in 2 patients. All preoperative clinical data are shown in Table 1.


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  		Table 1. Preoperative Clinical Data

 
Preoperative coronary angiography and hemodynamics revealed single vessel disease in 3 patients, two vessel disease in 8 patients, and three vessel disease in the 2 remaining patients. The left ventricular ejection fraction varied from 34% to 70%.

The following combined thoracic and cardiac procedures were carried out: two right pneumonectomies via sternotomy access and simultaneous coronary bypass to left anterior descending (LAD) and right coronary artery (RCA) in both cases, and one left pneumonectomy through a left thoracotomy and bypass to LAD. The sternotomy approach was also used to perform the lobectomies and wedge resections. There were eight lobectomies; six right superior, one right inferior, and one left superior combined with one or two coronary bypasses. Two wedge resections of the left upper lobe were also performed concomitantly with one or two coronary bypasses. All details of the surgical procedures are shown in Table 2. In each case, myocardial revascularization was carried out before pulmonary resection. After harvesting an arterial (internal mammary artery [IMA], radial artery [RA]) or venous graft, aortocoronary bypasses were implanted. (mean 1.7 per patient). A deep pericardial stitch was employed for the heart exposure except for the patient operated on via thoracotomy. An Octopus 3 stabilizer (Medtronic, Minneapolis, MN, USA) was then used to immobilize the site of the distal anastomosis. After myocardial revascularization was carried out, the position and size of the pulmonary tumor were assessed and a typical pulmonary resection (lobectomy or pneumonectomy) then completed the operation. The stumps of the main bronchii were hand sutured and the lobar bronchii and major pulmonary vessels were stapled. Finally, all the mediastinal lymph nodes on the side of the operation were dissected out and removed for pathologic examination. In patients who underwent right pneumonectomy or lobectomy with the sternotomy approach, the mediastinal lymphadenectomy included nodal stations 2, 4, and 7. This was carried out by exposing the trachea between the ascending aorta and superior vena cava. The paraesophageal lymph nodes (station 8) were only sampled. In the case of left upper lobectomy, mediastinal lymphadenectomy included nodal stations 6 and 7, while station 8 was only sampled. The aortopulmonary nodes were removed by dissection between aorta and left pulmonary artery. When the left thoracotomy approach was used, mediastinal lyphadenectomy was performed in the standard way. Drains were inserted into the chest and mediastinum for suction drainage in all except the pneumonectomy patients, in whom gravitational drainage was used.


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  		Table 2. Surgical Procedures

 
For statistical analysis of late results, patients with symptoms of angina or cancer relapse (n = 5) were combined into one group, and compared to those who were asymptomatic (n = 8). The Kaplan-Meier method was used to assess significant differences between these groups. The Kaplan-Meier curves, with added numbers of patients at risk, were then compared by the Wilcoxon-Gehan test. Differences between the groups were assumed as significant at p levels lower than 0.05.


   Results
Top
 Abstract
 Introduction
 Material and methods
 Results
Comment
 Acknowledgments
 References
 
All the patients survived the operation and the early postoperative period. One patient was reoperated on due to excessive blood loss. After bleeding from the intercostal artery was stopped, the subsequent postoperative course was uneventful and he was discharged from the hospital 7 days later in good condition. Total mean postoperative drainage in the remaining patients was 425 mL + 180 mL. In two patients, subcutaneous emphysema occurred and one of them had a prolonged air leak. Respiratory failure, requiring prolonged mechanical ventilation, developed in one patient. This patient was successfully extubated on the second postoperative day. Two patients, one after lobectomy and the other after pneumonectomy, required several bronchoscopic aspirations to prevent the development of atelectasis.

There were no perioperative or postoperative myocardial infarctions confirmed by electrocardiogram and elevation of CK-MB or troponin I. None of the patients required mechanical circulatory support. However, all were given infusions of dopamine and nitroglycerin in doses of 5 µg · kg-1 · min-1, and 4 µg · kg-1 · min-1, respectively, up to the third postoperative day if needed. Three patients developed cardiac arrhythmias, including atrial fibrillation in two and ventricular ectopic beats in one patient. All three were successfully treated with intravenous infusions of amiodarone in a dose of 8 µg · kg-1 · min-1. Mean stay in the intensive care unit was 42.3 ± 8 hours and stay in-hospital was 7.5 ± 1.5 days, respectively. Patients were followed up from 7 to 36 months, with a median value of 16 months. All are alive; none had myocardial infarction. Three patients developed symptoms of stable angina between the first and second year of observation. In the third year of follow-up in one patient who underwent lobectomy (II B, T2 N1), local recurrence was found. In another patient, who underwent pneumonectomy (III A, T3 N1), distant metastases occurred after two years of observation. Both latter patients were free from any cardiac symptoms.

The Kaplan-Meier curves for the groups of patients free of symptoms, and the patients with stable angina or lung cancer, relapse indicated nonsignificant differences between cumulative proportions of patients (Fig 1). The first cardiac symptoms occurred after 12 months after operation, while cancer relapse was observed at the thirtieth month of follow-up. The median time of follow-up was 22 months in symptomatic patients and 15 months in asymptomatic patients.



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  		Fig 1. Kaplan-Meier curves (p > 0.05) for cumulative proportion of patients after simultaneous lung resection and cardiac revascularization. (Dashed line = stable angina or cancer relapse; solid line = free of symptoms.)

 

   Comment
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
Acknowledgments
 References
 
Patients with lung cancer and severe ischemic heart disease pose a serious therapeutic dilemma for cardiothoracic surgeons. The question of how best to deal with these patients still remains open. Currently, many unstable coronary patients with one or two coronary vessel involvement can be successfully treated with the use of coronary angioplasty. Therefore, potential candidates for surgery are only those in whom this method has failed or is contraindicated. At present, there is no definite agreement on whether a combined cardiac (CABG) and thoracic (lung resection) procedure should be carried out as either a one-stage or two-stage operation [1, 5, 8]. There are several arguments for and against both treatment strategies. A two-stage procedure means two general anesthetic agents for the patient, two surgical incisions (sternotomy and thoracotomy), a longer overall stay in hospital, delay in the lung resection, double the preoperative stress and postoperative pain, and higher costs of treatment [2, 4], On the other hand, single-stage surgery increases the risk of postoperative bleeding related to heparinization and may result in technical difficulties in the exposure of both lungs (sternotomy approach) and in the dissection of mediastinal lymph nodes [5, 8, 9]. However, the main causes for concern in patients requiring concomitant cardiac and thoracic procedure were the side-effects of cardiopulmonary bypass (CPB), because the use of CPB may activate SIRS, impair the immune response, and increase the risk of edema in a residual lung [5, 8, 10]. An even greater cause for concern is that it can also cause the dissemination of neoplasmatic cells [10]. However, coronary artery surgery on the beating heart and withdrawal of CPB abolish all the disadvantages relating to CPB complications mentioned above. We started off-pump coronary surgery in 1999 and, since then, approximately 25% of all coronary surgery operations have been carried out using this technique. The good operative results obtained in our patients, as well as the first published results of OPCAB applied in patients with pulmonary malignancy, encouraged us to change our policy in the treatment of patients with both lung cancer and concomitant ischemic heart disease [11–15]. Initially, we considered using a combined cardiothoracic procedure in those oncologic patients who were at high operative risk due to a recent history (1 to 3 months) of myocardial infarction with the involvement of one or two coronary vessels. In two patients, the cardiologist was unable to restore blood inflow with the use of coronaroplasty or stenting and in three patients this technique had been used before, but without long lasting effect. In our opinion, coronaroplasty is not always a safe procedure in patients referred for lobectomy or pneumonectomy; it may increase the risk of postoperative bleeding related to the antithrombotic medication, which is required for at least 3 months following cardiologic intervention. This can be an argument for concomitant myocardial revascularization with lung resection in such patients.

Later, we also referred for one-stage surgery those patients who had symptoms of unstable coronary disease, which could not be sufficiently controlled by medication and where coronaroplasty had failed or was not feasible. These patients underwent simultaneous off-pump coronary bypass and lung resection. In addition, two of them subsequently required coronaroplasty of the RCA. The early results of treatment were good, thus confirming clinical reports published by Mariani and colleagues and others [16–20]. There were no perioperative deaths or myocardial infarctions. The type and number of postoperative complications were within the range commonly accepted for both surgical procedures. Morbidity was not affected by coexisting disease such as arterial hypertension and diabetes. The limited number of late observations (median value, 16 months) render it impossible to decide whether OPCAB, concomitant with lung resection, is a valuable method of treating both diseases at one operation, and therefore whether it should be recommended more extensively. We can only state that the combined procedure appears promising because within the period of follow-up there were no new acute coronary events and only 2 patients suffered from cancer relapse. However, while we are convinced that simultaneous myocardial revascularization and lung resection could be performed more frequently than at present, there are several matters which still need to be discussed, beginning with the indications for surgery. It seems that acceptable candidates for the double procedure are those patients with operable squamous cell lung carcinoma (stage IA to III A, N2 negative), with a history of recent myocardial infarction, or patients with unstable angina in whom coronaroplasty or stenting has failed or was not feasible. Care must be taken to avoid the operation in patients with N2 disease because of the generally poor late results of surgical treatment in this subgroup of patients. Therefore, if we are considering the combined surgical procedure, preoperative mediastinoscopy should be performed routinely, even if enlargement of mediastinal lymph nodes cannot be detected on computed tomographic (CT) scans, a fact which we soon learned from our experience in these patients. In one of them we postoperatively found metastatic N2 disease although CT of the chest had not revealed any mediastinal pathology. Because the main goal of a combined cardiac and thoracic operation is the prevention of myocardial ischemia, OPCAB should be carried out before lung resection [18]. Occasionally, this may cause technical problems with exposure of the lung, especially if both internal thoracic arteries are implanted or the circumflex artery is bypassed with the right mammary artery. In the latter situation we suggest the use of a free graft of the radial artery. Implantation of three grafts before lung resection also worsens the operative conditions and we do not refer such patients for combined procedures. In some patients, a possible solution is to perform two grafts to the vessels of greatest importance for myocardial perfusion and, if possible to complete postoperatively, myocardial revascularization with coronary angioplasty. Sternotomy, the preferred approach in cardiac operations, is also suitable for right lung resections and eventually left upper lobectomy [18]. In cases of right pneumonectomy, sternotomy even facilitates formation of a bronchial stump. Exposure of upper mediastinal lymph nodes, especially subcarinal, is good but requires a transpericardial approach. In turn, the dissection of paraesophageal lymph nodes on both sides after sternotomy is more demanding than from standard thoracotomy access. Left pneumonectomy and left lower lobectomy, to be performed safely in combination with a bypass procedure, require a standard left antero-lateral thoracotomy [17, 19] On the other hand, this approach precludes the surgeon creating a distal anastomosis on the diaphragmatic side of the heart. Therefore, left thoracotomy limits a bypass operation on a beating heart to the left coronary artery and its branches. Finally, the size and localization of the tumor plays a role in planning a combined cardiac and thoracic procedure. Patients with tumors adjacent to the descending aorta or esophagus, or invading the parietal pleura and diaphragm, or tumors requiring bronchoplastic procedures, are not suitable candidates for simultaneous operations. The feasibility of myocardial revascularization on a beating heart combined with lung resection, and its good results, are an argument for wider use of this method in the treatment of patients with lung cancer and severe ischemic heart disease. Further study is necessary to determine the long-term efficacy of this form of treatment.


   Acknowledgments
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
References
 
The author acknowledges Professor Geoffrey Shaw for his great contribution to the English version of this paper, and for his help in the preparation of the manuscript.


   References
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 

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