Ann Thorac Surg 2007;84:504-509
© 2007 The Society of Thoracic Surgeons
Original Articles: Cardiovascular
Comparison of On-Pump or Off-Pump Coronary Artery Revascularization With Lung Resection
Micha C.J. Schoenmakers,
Wim-Jan van Boven, MD,
Jules van den Bosch, MD, PhD,
Henry A. van Swieten, MD, PhD*
Department of Cardiothoracic Surgery and Lung Diseases, St. Antonius Hospital, Nieuwegein, the Netherlands
Accepted for publication April 2, 2007.
* Address correspondence to Dr van Swieten, Department of Cardiothoracic Surgery, UMC St. Radboud, Internal Postal Code 677, P.O. Box 9101, Nijmegen, 6500 HB, the Netherlands (Email: h.vanswieten{at}thorax.umcn.nl).
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Abstract
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Background: The simultaneous occurrence of coronary artery disease and lung cancer is rare. The best surgical treatment strategy remains controversial: performing a combined procedure with or without the use of extracorporeal circulation (ECC). The aim of this study was to compare the surgical procedure, postoperative complications, and survival of combined surgery with the use of ECC to combined surgery without ECC.
Methods: Forty-three patients underwent a combined procedure between 1994 and 2005. Twenty-eight patients (25 male and 3 female; mean age, 66 years; range, 54 to 76 years) underwent coronary artery (CA) revascularization with ECC after the lung resection was carried out (on-pump). Fifteen patients (14 male and 1 female; mean age, 71 years; range, 50 to 79 years) had first CA revascularization without ECC followed by lung resection (off-pump). Survival was estimated by the Kaplan-Meier method and analyzed using the log-rank test and the Cox proportional hazard regression model.
Results: Postoperative complications and hospital survival were not significantly different between groups. However, in the on-pump group late survival was significantly better. Late survival was significantly longer in patients without recurrent vessel disease and with stage I lung cancer.
Conclusions: These results show no significant difference in using an on-pump or off-pump technique to perform a combined cardiac and lung surgery in relation to postoperative complications and hospital survival. However, our data show a significantly longer late survival period in the on-pump group. Because the off-pump patients were older and had more advanced lung malignancy, the off-pump technique should be continued and evaluated.
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Introduction
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The simultaneous occurrence of coronary artery disease and lung cancer is rare. The majority of patients present with symptoms of cardiac disease and, during preoperative screening for coronary artery (CA) revascularization, an asymptomatic pulmonary nodule was discovered.
The best surgical treatment strategy for these patients remains controversial; the two-staged or the combined procedure [1–4]. The two-staged procedure means two surgical incisions (a sternotomy and a thoracotomy), a longer overall hospital stay, delay in the lung resection, and higher costs [3, 5]. The combined procedure increases the risk of bleeding due to heparinization and technical difficulties due to the exposure of the lungs by median sternotomy [6]. However, the side effects of extracorporeal circulation (ECC) are an important factor for concern in patients undergoing combined surgery. Extracorporeal circulation activates the systemic inflammatory response syndrome (SIRS) and impairs the immune response against the growth of tumor cells and infections. Extracorporeal circulation also increases the risk of edema in the residual lung tissue. An even greater concern is that it can also cause the dissemination of neoplastic cells; however, this has never actually been proved. Due to the side effects of ECC and limited exposure of the left lower lobe, surgeons were reluctant to perform the combined procedure in case of lower lobe tumor. With off-pump coronary bypass surgery the disadvantages related to the use of ECC are eliminated.
From 1979 to 2005, 122 patients underwent CA revascularization and pulmonary resection in our hospital. The results from 1979 to 1993 were summarized by Brutel de la Rivière and colleagues [2]. In a 15-year period 79 patients underwent a combined procedure. They concluded that the five-year survival was higher in patients who underwent lung resection before ECC (55%) versus those who underwent lung resection after ECC (20%). The aim of this study was to compare the surgical procedure, postoperative complications, hospital survival, and late survival of combined surgery with the use of ECC to combined surgery without ECC.
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Patients and Methods
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From January 1994 to December 2005, 43 patients underwent a concomitant procedure for lung cancer and CA revascularization, with or without the use of ECC. In 28 patients, CA revascularization was performed with ECC after the lung resection was carried out (on-pump). Fifteen patients had first CA revascularization without ECC and lung resection thereafter (off-pump). Comparisons between preoperative conditions were made using the Student t test and the Fisher exact test.
The primary and secondary outcome variables were hospital survival and late survival, respectively. For hospital survival the endpoint was death within the first 30 days after operation or during the same hospitalization. The endpoint for late survival was the date of death or last follow-up. Survival was calculated by the Kaplan-Meier method. The survival curves were analyzed using the log-rank test and the Cox proportional hazard model was used to test the influences of possible explanatory variables on survival. Differences between the groups were assumed as significant at p levels lower than 0.05. The Local Committee Testing Medical Experiments of the St. Antonius Hospital, Nieuwegein, The Netherlands, approved this retrospective study and waived the need for individual consent (registration number LTME/Z-07.01).
On-Pump Group
Twenty-eight patients (25 male and 3 female; mean age, 66 years; range, 54 to 76 years) underwent CA revascularization with the use of ECC after pulmonary resection for lung cancer was performed. Twenty-seven were elective procedures and one patient was operated on emergency because of unstable angina pectoris. Seventy-one percent of the patients presented with cardiac symptoms and during the initial evaluation were found to have a pulmonary tumor. The remaining patients presented with pulmonary symptoms. The standard preoperative evaluation of surgical patients includes lung function tests, chest X-ray, computed tomographic (CT) scan, and positron emission tomography (PET) scan. In addition, mediastinoscopy was performed in 29% of the patients preoperatively (Table 1). Because severe obstructive coronary artery disease is a contraindication for diagnostic operation, mediastinoscopy was only performed in patients with mediastinal lymph node enlargement on CT scan or a positive PET scan (since 2001) of the mediastinum or a central localized tumor.
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Table 1 Preoperative Baseline Characteristics of the Patients Undergoing Combined Surgery With or Without Extracorporeal Circulation
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The preoperative cardiac and pulmonary pathology is shown in Table 1. Fifty-three percent of the patients had a previous myocardial infarction. Almost 80% of the patients had three-vessel disease and the left ventricular function was normal in 43% of the patients. Four patients had concomitant aortic stenosis with a mean peak gradient of 80 mm Hg. The primary tumor was located in the right lung in 71% of the patients. One patient had a recurrent lung tumor 13 years after the resection of the primary lung tumor.
All patients were operated by median sternotomy for the cardiac and lung procedure. Due to hemodynamic instability two patients underwent their pulmonary resection after completion of the CA revascularization. The mean number of distal anastomoses was 3.6 (range, 1 to 6); the internal mammary artery was used in 18 patients (64%). The different pulmonary resections are shown in Table 2. The most frequently performed procedure was a lobectomy of the right upper lobe. Because left lower lobe resection is technically demanding and can result in hemodynamic problems no patients underwent a left lower lobe resection. During pulmonary resection routine lymph node resection was performed. Postoperative TNM staging is shown in Table 3. Postoperatively, 20 patients (71%) were in stage I, four in stage II (14%), and four in stage III (14%). The histology of the tumor was mostly squamous cell carcinoma and adenocarcinoma.
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Table 3 Postoperative Lung Pathology Staging After Combined Cardiac and Lung Surgery With or Without Extracorporeal Circulation
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Off-Pump Group
Fifteen patients (14 male and 1 female; mean age, 71 years; range, 50 to 79) underwent the combined procedure without ECC; all were elective procedures. Sixty percent of the patients presented with cardiac symptoms while their pulmonary neoplasm was discovered during preoperative screening. Mediastinoscopy was performed in 20% of the patients (Table 1).
The preoperative cardiac and pulmonary pathology is shown in Table 1. Sixty percent of the patients had three-vessel disease and a diminished left ventricular function. One patient had carotid stenosis with an indication for endarterectomy, which was simultaneously performed. The pulmonary tumor was located in the right lung in 67% of the patients. In six patients (40%) the tumor was located in the upper right lobe.
Since the introduction of off-pump coronary artery bypass grafting in 1998 in our hospital, the majority of combined procedures (77.7%) have been carried out off-pump. During this procedure the surgeon starts with the CA revascularization followed by the lung resection. In our series, 11 patients (73%) underwent their combined procedure in this order. Due to pleural adhesions, one patient underwent a sternotomy for the cardiac procedure followed by lateral thoracotomy for the lung resection. In one patient, a Starfish device (Starfish, Victoria, BC, Canada) was used to avoid hazardous manipulation of the heart to gain adequate access to the left lower pulmonary vein to perform a left pneumectomy [7].
The mean number of distal anastomoses was 3.1; the internal mammary artery was used in 14 patients (93%). The different pulmonary resections are shown in Table 2; the most frequently performed procedure was a lobectomy of the right upper lobe. Postoperative TNM staging is shown in Table 3. Postoperatively eight patients were in stage I (53%), five in stage II (33%), and one in stage III (7%).
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Results
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The patients in the off-pump group were significantly older (71 years vs 66 years; p = 0.03; Table 1). After surgery, seven patients (25%) of the on-pump group and three patients (20%) of the off-pump group had supraventricular extrasystoles and (or) temporary atrial fibrillation; all patients were converted to sinus rhythm with medical therapy or electrical cardioconversion (Table 4). Perioperative or postoperative myocardial infarctions were not detected.
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Table 4 Postoperative Hospital Mortality and Complications After a Combined Cardiac Surgery and Lung Resection With or Without Extracorporeal Circulation
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Postoperatively, 13 patients (46%) of the on-pump group suffered from pulmonary complications; six had upper airway infections or pneumonia, four a pneumothorax, and one patient a hematothorax. Respiratory failure, requiring prolonged mechanical ventilation, developed in two patients. In the off-pump group, one patient suffered from a pneumothorax and one had respiratory failure (Table 4). Pulmonary complications were significantly more frequent in the on-pump group (p = 0.04). Sepsis occurred in three patients (all died) and one patient in the on-pump group developed a sternal wound infection.
The mean hospital stay for the on-pump and the off-pump group was 14 days (SD, 4.6) and 12 days (SD, 6.8), respectively. In one patient in the off-pump group sternal refixation was performed two months after the procedure. One patient of the on-pump group had a late tamponade, which was drained through a subxiphoidal approach.
Hospital Survival
No patients died during the operation and early postoperative period. In the hospital, three patients died (7%); one due to sepsis (off-pump group) and two due to respiratory insufficiency resulting in sepsis (on-pump group). No significant difference in hospital survival was seen between the two surgical groups (p = 0.95) (Fig 1). Univariate analysis of hospital survival showed no significant relation with age, gender, cardiac or pulmonary pathology, or the use of ECC (data not shown).

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Fig 1. Hospital survival. Kaplan-Meier survival curve of hospital survival; patients operated with extracorporeal circulation (black line) and patients operated without extracorporeal circulation (gray line).
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Late Survival
The follow-up of the patients was complete. The overall survival of the operated patients was 4.8 years (SD 0.6) (Table 5). The long-term survival between the two groups was compared using the Kaplan-Meier survival curve (Fig 2). No significant difference in survival was seen between the two surgical groups (p = 0.09); however, the two-year survival rate and the five-year survival rate were significantly better for the on-pump group (Table 5). No significant difference in the cause of death was seen between both surgical groups (Table 6). Univariate analysis showed that late survival was significantly longer in patients without recurrent vessel disease and in patients with stage 1 lung cancer (Table 7).
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Table 5 The Mean Survival, and the Two-Year and Five-Year Survivals After a Combined Cardiac Surgery and Lung Resection With or Without Extracorporeal Circulation
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Fig 2. Late survival. Kaplan-Meier survival curve of late survival; all operated patients (gray line), patients operated with extracorporeal circulation (on-pump), and patients operated without extracorporeal circulation (off-pump).
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Table 6 Causes of Death After a Combined Cardiac Surgery and Lung Resection With or Without the Use of Extracorporeal Circulation
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Comment
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The simultaneous occurrence of coronary artery disease and lung cancer is rare. In the majority of patients in our series a pulmonary lesion was found during preoperative evaluation of patients planned for myocardial revascularization. Other authors have reported similar findings [1, 8].
When combined cardiac and pulmonary pathology is present the surgeon has three options: (1) percutaneous transluminal coronary angioplasty with or without coronary stenting followed by lung surgery; (2) a combined procedure with ECC; and (3) a combined procedure without ECC.
Recent reports of adverse outcomes of noncardiac surgery soon after coronary stenting is associated with a major risk of operative myocardial ischemia, even in case the recommended interval of six weeks is respected [9, 10]. Recently, a three-month delay between percutaneous transluminal coronary angioplasty with stenting and surgical intervention has been recommended to minimize the risk of in-stent thrombosis [11]. In the case of lung cancer, surgery should not be postponed for three months. In such cases, Marcucci and colleagues [10] recommend a preoperative revascularization limited to balloon angioplasty without stenting. Once the patient has recovered from the noncardiac operation, a definitive percutaneous transluminal coronary angioplasty with stenting could be performed [10].
Multiple disadvantages of ECC have been reported, such as the following: (1) increased risk of bleeding due to heparinization; (2) activation of the systemic inflammatory response syndrome (SIRS), impairing the immune response against the growth of tumor cells and infections; (3) the risk of edema in the residual lung tissue; and (4) the dissemination of neoplastic cells. With the use of off-pump coronary bypass surgery, all the disadvantages relating to ECC are eliminated.
Lower hospital mortality, postoperative complications, and longer survival in the group of patients who were operated without the use of ECC were expected. The incidence of bleeding complications, usually the main argument against the combined surgery with use of ECC, and cardiac complications were not significantly different in both groups. Thus, in our series the use of ECC did not result in a greater risk of bleeding complications. With special care for hemostasis the combined procedure can be safely performed.
Postoperatively, significantly more pulmonary complications were seen in the on-pump group. Others also have reported a greater risk of pulmonary complications after the use of ECC, which is supposed to be related to the edema of the remaining lung tissue caused by the ECC [5].
The hospital survival was not significantly different between both surgical groups, and the hospital mortality of 7% was quite acceptable. The expected relationship between ECC and hospital survival could not be confirmed.
Late survival in both groups was comparable, although the mean survival, two-year survival rate, and five-year survival rate were significantly longer for the patients in the on-pump group. As expected, late survival was significantly better in patients without recurrent vessel disease and stage 1 lung cancer. However, the small numbers of patients with recurrent vessel disease and a given tumor stage make comparison unreliable. In our series, late death was predominantly related to recurrence of the malignant process. Although a protective effect of the off-pump cardiac surgery was expected, this could not be demonstrated.
We conclude, so far, that there is no evidence that off-pump surgery is a better treatment strategy of patients with combined cardiac and lung pathology. The expected positive effect of not using ECC is reflected in lower complication rates. However, late survival was comparable in both groups. Taking into account the older age, the more advanced pulmonary malignancy, and the low number of patients in the off-pump group, the off-pump procedure in combined cardiac and pulmonary surgery should be continued and evaluated.
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References
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- Miller DL, Orszulak TA, Pairolero PC, Trastek VF, Schaff HV. Combined operation for lung cancer and cardiac disease Ann Thorac Surg 1994;58:989-994.[Abstract]
- Brutel de la Rivière 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;9:310-314.[Abstract]
- Rao V, Todd TRJ, Weisel RD, et al. Results of combined pulmonary resection and cardiac operation Ann Thorac Surg 1996;62:342-347.[Abstract/Free Full Text]
- Danton MHD, Anikin VA, McManus KG, McGuigan JA, Campalani G. Simultaneous cardiac surgery with pulmonary resection: presentation of series and review of literature Eur J Cardiothorac Surg 1998;13:667-672.[Medline]
- Ciriaco P, Carretta A, Calori G, Mazzone P, Zannini P. Lung resection for cancer in patients with coronary arterial disease: analysis of short-term results Eur J Cardiothorac Surg 2002;22:35-40.[Abstract/Free Full Text]
- Voets AJ, Joesoef KS, Van Teeffelen ME. Synchronously occurring lung cancer (stage I–II) and coronary artery disease: concomitant versus staged surgical approach Eur J Cardiothorac Surg 1997;12:713-717.[Abstract]
- Tan MESH, van Boven WJ, van Swieten HA. Combined off-pump coronary surgery and left lung resection through midline sternotomy with a Medtronic Starfish® 2 Heart Positioner Minerva Chir 2006;61:159-161.[Medline]
- Johnson JA, Landreneu RJ, Boley TM, et al. Should pulmonary lesions be resected at the time of open heart surgery? Am Surg 1996;62:300-303.[Medline]
- Kaluza GL, Joseph J, Lee JR, et al. Catastrophic outcomes of noncardiac surgery soon after coronary stenting J Am Coll Cardiol 2000;35:1288-1294.[Abstract/Free Full Text]
- Marcucci C, Chassot PG, Gardaz JP, et al. Fatal myocardial infarction after lung resection in a patient with prophylactic preoperative coronary stenting Br J Anaesth 2004;92:743-747.[Abstract/Free Full Text]
- Chassot PG, Delabays A, Spahn DR. Preoperative evaluation of patients with, or at risk of, coronary artery disease undergoing non-cardiac surgery Br J Anaeth 2002;89:747-759.[Abstract/Free Full Text]
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