Original papers. Concomitant Cardiac Surgery and Pulmonary Resection

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1 Original papers Acta Chir Belg, 2009, 109, Concomitant Cardiac Surgery and Pulmonary Resection K. Cathenis* ( 1 ), **, R. Hamerlijnck*, F. Vermassen**, G. Van Nooten***, F. Muysoms* *Department of General, Thoracic and Cardio-Vascular Surgery, AZ Maria Middelares, Gent, Belgium ; **Department of Thoracic and Vascular Surgery and ***Department of Cardiac Surgery, UZ Gent, Belgium. Key words. Cardiac surgery ; lung cancer surgery ; outcomes. Abstract. Background : Surgical management of concomitant pulmonary and cardiac disease remains controversial. There is no consensus on the use of a one- or two-staged procedure, the timing of heparinization and the utilisation of cardio-pulmonary bypass. Methods : We performed a retrospective review of 27 patients who underwent pulmonary and cardiac surgery, from 2000 to 2008, in two institutions. We focused on early postoperative morbidity and mortality. Results : 24 men and 3 women, with a mean age of 68 years, were treated. Cardiac procedures consisted of coronary artery bypass grafting (n = 22), heart valve surgery (n = 3) or a combination of both (n = 2). Pulmonary resection included segmental resection (n = 1), lobectomy (n = 21), bilobectomy (n = 2) and pneumonectomy (n = 3). Histology of the pulmonary lesion was squamous cell carcinoma in 14 patients (52%), adenocarcinoma in 10 (37%), large cell neuroendocrine tumour in 1 (3%) and typical carcinoid in 1 (3%). The stage of the pulmonary malignancy was IA in 8 patients (31%), stage IB in 11 (42%), stage IIB in 5 (19%) and stage IIIB in 2 (8%). A benign lesion was found in 1 patient (3%). There was no in-hospital mortality. Postoperative complications occurred in 16 patients (59%) consisting of supra - ventricular arrhythmias in 11 (41%), pneumonia in 8 (30%), atelectasis in 6 (22%), ventricular arrhythmias in 2 (7%), pneumothorax in 1 (3%), pleural effusion in 1 (3%), and renal insufficiency in 1 patient (3%). Revision for bleeding was necessary in 3 patients (11%). The mean follow-up was 30,7 months with a median survival for all patients of 46 months. Conclusions : Simultaneous procedures for cardiac disease and pulmonary lesions can be performed without lifethreatening morbidity and no in-hospital mortality. Introduction Although the first reports of simultaneous surgical procedures for cardiac disease and lesions of the lung are over 20 years old, the issue remains controversial. The largest series published until now, consists of 79 patients over a period of 14 years (1). Patients undergoing a combined procedure can be divided into two groups. The largest group are cardiac surgery patients in whom a lung tumour is discovered pre-operatively. The smaller group are patients with a pulmonary lesion, in whom an indication for cardiac surgery is found preoperatively (2). Although combined surgery has proven to be feasible, several questions remain unanswered. Because the occurrence of concomitant disease is rare, guidelines regarding a one- or two-staged surgical approach have not been established. The need for cardiopulmonary bypass, including systemic heparini - zation, during the cardiac procedure and its effect on oncological outcome and operative morbidity is still debated. The safety and adequacy ofoncological pulmonary resection through median sternotomy has been established (3). In this report we reviewed our experience with special emphasis on the early postoperative morbidity and mortality in a series of patients who underwent concomitant cardiac and pulmonary surgery. Material and methods We performed a retrospective study of all patients planned for concomitant cardiac surgery and pulmonary resection, at both institutions, between March 2000 and November The patient data were gathered from the medical records. These records were reviewed for age, sex, operative procedures, timing of cardiopulmonary bypass, final pathologic diagnosis, staging, morbidity, mortality, and follow-up. Follow-up data were obtained from the medical records, public registry in case of unknown date of death or loss to follow-up and telephonic contact with patients or relatives if needed. In all cases a cardiac surgeon performed the cardiac procedure and a general thoracic surgeon performed the pulmonary (1) Winner of the Young Investigators Award 2009 Prize of the Royal Belgian Society for Surgery.

2 Concomitant Cardio-Pulmonary Surgery 307 resection. A total of 28 patients were scheduled for a combined procedure. One patient was excluded from the review because, during the operation, the decision was made to do a two-staged procedure since the tumour unexpectedly invaded the thoracic wall. As a result, this patient underwent a Coronary Artery Bypass Grafting (CABG) first. Pulmonary resection, including thoracic wall resection, was performed through a lateral thoracotomy 6 weeks later. All patients had an extensive pre-operative cardio-pulmonary staging and evaluation. Evaluation was guided by medical history, physical examination, standard blood tests, and findings on chest radiography and thoracic computed tomography (CT) scans. Bronchoscopy and respiratory function tests were routinely executed. Echography of the abdomen, CT scan of the brain, bone scintigraphy or Fludeoxyglucose Positron Emission Tomography (FDG-PET) were usually performed to exclude extrathoracic metastasis. Transthoracic CT guided tumour biopsy, mediastinoscopy, transbronchial or transoesophageal endoscopic mediastinal lymph node biopsies were performed on indication for some patients. Cervical mediastinoscopy was performed in patients with (signs of) Non Small Cell Lung Carcinoma (NSCLC) in whom no extrathoracic metastases were found, and in whom CT and/or FDG-PET scans showed evidence of lymph node involvement. Preoperative investigations for cardiac surgery consisted of carotid Doppler or angiography if needed, a 12-lead ECG and a left heart catheterisation. All patients had a coronary angiography, aortography, left ventri - culography and manometry. In valvular disease a right heart catheterisation was performed with measurement of cardiac output, pulmonary artery and wedge pressure. Exercise (treadmill) testing was used as a screening test before coronary angiography. Transthoracic echocardiography (TTE) was frequently used to define cardiac anatomy and assess ventricular and valvular function. Additional investigations such as arterial blood gas analysis, creatinine clearance and evaluation of a permanent pacemakeror cardio-defibrillator were conducted as appropriate. A dental check-up was performed in every patient planned for valve repair. Postoperative morbidity was defined as the occurrence of complications within 30 days of operation or during hospitalisation. Likewise, operative mortality was defined as death within 30 days of operation or during the postoperative stay. Lung cancer stage grouping was carried out using standard TNM classification. Statistics Actuarial survival curves were plotted according to Kaplan and Meier, with the date of surgery as the starting point and the date of death or last follow-up as end point. The survival curves were analysed using the logrank test and the Cox proportional hazard model to test the influence of the different variables on the survival. Due to the small number of patients, a multi-variate analysis was not significant. Therefore, a bi-variate analysis was used. The p value was considered statistically significant if less than 0,05. This study was approved by the ethical committees of the Universitary Hospital of Gent and AZ Maria Middelares in Gent. Results Demographics 24 men (89%) and 3 women (11%) were treated with a mean age of 68 years (range, 48-81). Of these 27 patients, 15 (56%) were diagnosed with a pulmonary lesion in the pre-operative work-up for cardiac surgery and 12 (44%) were diagnosed with significant cardiac pathology in the work-up for a pulmonary lesion. Cardiac Surgery (Table I) Cardiac procedures consisted of CABG in 22 patients, Aortic Valve Replacement (AVR) in 2, Mitral Valve Replacement (MVR) in 1 (combined with a CABG), and Mitral Valve Plasty (MVP) in 2 (combined with a CABG in 1 patient). Median sternotomy (MS) was used in 26 patients (96%), and a lateral thoracotomy in 1 (3%). From the 22 patients who had a CABG without valvular repair, 16 patients (73%) had a procedure involving extracorporeal circulation (ECC) and 6 patients (27%) had an off-pump procedure (OPCAB). The mean number of distal anastomoses was 3.5 (range, 2-6). The combination of a left Internal Mammary Artery and saphenous vein graft was used in 20 patients (83%). 2 patients (8%) had a coronary revascularization with saphenous vein grafts only. The patient with the lateral thoracotomy had an OPCAB-procedure using a combination of a left Internal Mammary Artery and a free Arteria Radialis. The mean ejection fraction of the patients was 68% (range, 40-99). Pulmonary Surgery Pulmonary resection included segmental resection in 1 patient (3%), lobectomy in 21 (78%), bilobectomy in 2 (7%) and pneumonectomy in 3 (11%). Of the 21 procedures using ECC : 13 lung resections (62%) were performed before, 5 (24%) during and 3 (14%) after ECC. In the 6 OPCAB procedures, 2 lung resections were performed before heparinization, 1 during heparini - zation and 3 after protaminisation.

3 308 K. Cathenis et al. Table I Cardiac and Pulmonary Surgery Nr. Indication Cardiac Surgery Lung Resection Incision Lung vs ECC Construction APD Stage EF (%) 1 tumour OPCAB RUL MS / lima-d-lad, ao-mo, ao-rca SC IB 63 2 tumour AVR PN MS during ECC / SC IIIB 61 3 tumour CABG LUL MS before ECC ao-d-lad, ao-mo-rdp SC IB good 4 tumour OPCAB PN MS / ao-lad, ao-rca SC IA 81 5 tumour CABG RLL + RML MS before ECC lima-lad, ao-mo-rdp SC IB good 6 tumour CABG/MVR RUL MS after ECC lima-lad, ao-mo, ao-rca SC IB / 7 cardiac OPCAB RLL MS / lima-lad, ao-rca SC IB 75 8 cardiac CABG RLL MS before ECC lima-d, ao-mo-rdp AC IIB 63 9 tumour CABG LLL MS before ECC lima-lad, ao-al-mo-rdp AC IB cardiac CABG RML MS before ECC lima-d-lad, ao-al-mo-rdp AC IB good 11 tumour CABG PN MS before ECC lima-d-lad, ao-mo-rdp SC IB tumour CABG LUL MS before ECC lima-lad, ao-mo-plcx-rdp SC IB tumour CABG RML + RUL MS during ECC lima-lad, ao-al AC IB cardiac OPCAB LUL MS / lima-mo, rima-lad-d SC IA cardiac AVR RUL MS before ECC / SC IIB cardiac CABG RUL MS before ECC lima-d-lad, ao-mo1-mo2-rdp AC IIIB tumour MVP RLL MS after ECC / NE IA cardiac OPCAB LLL LLT / lima-lad, radialis-ramus AC IA cardiac CABG LUL MS before ECC lima-d-lad, ao-al-plr AC IIB cardiac CABG/MVP RLL MS before ECC lima-lad, ao-mo SC IA cardiac CABG RLL MS before ECC lima-d-lad, ao-mo-rdp AC IIB cardiac CABG RUL MS before ECC lima-lad, ao-mo, ao-rca SC IIB cardiac CABG WEDGE LLL MS during ECC lima-d-lad, ao-mo, ao-rca benign cardiac OPCAB RUL MS / lima-lad, ao-rca, ao-ang AC IA cardiac CABG LLL MS during ECC lima-d-lad, ao-mo SC IB tumour CABG RUL MS during ECC lima-lad, ao-mo, ao-rca carcinoid IA cardiac CABG RLL MS after ECC lima-d-lad, ao-mo, ao-rca AC IA 72 RUL : right upper lobe ; RLL : right lower lobe ; RML : right middle lobe ; LUL : left upper lobe ; LLL : left lower lobe ; PN : pneumonectomy ; MS : median sternotomy ; LLT : left lateral thoracotomy ; SC : squamous cell carcinoma ; AC : adenocarcinoma ; NE : neuro-endocrine carcinoma. Resections consisted of a left upper lobe resection in 4 patients, left lower lobe in 3, right upper lobe in 7, right middle lobe in 1, right middle and right upper lobe in 1, right lower lobe in 6, right lower and right middle lobe in 1, wedge resection in 1 and pneumonectomy in 3. Histology of the pulmonary lesion was squamous cell carcinoma in 14 patients (52%), adenocarcinoma in 10 (37%), large cell neuro-endocrine tumour in 1 (3%), typical carcinoid in 1 (3%) and a benign lesion was found in 1 patient (3%). The stage of the pulmonary malignancy was IA in 8 patients (31%), stage IB in 11 (42%), stage IIB in 5 (19%) and stage IIIB in 2 (8%). The large cell neuro-endocrine tumour and carcinoid tumour were staged IA. Morbidity and mortality (Table II) There was no in-hospital mortality. Postoperative complications occurred in 16 patients (59%) consisting of supraventricular arrhythmias in 11 (41%), pneumonia in 8 (30%), atelectasis in 6 (22%), ventricular arrhythmias in 2 (7%), pneumothorax in 1 (3%), pleural effusion in 1 (3%), and renal insufficiency in 1 patient (3%). Revision for bleeding was necessary in three patients (11%). The mean hospital stay was 13.4 days (range, 8-29). Because of the small number of patients, no post-operative complications such as pneumonia, atelectasis or arrhythmia had a significant impact on the survival rate. Long-term survival The follow-up was completed for all patients in November 2008 and ranged from 4 to 81 months. The mean follow-up was 30.7 months. The mean survival was 48.3 months. The median survival was 46 months (Fig. 1). There was no significant impact of the following factors on survival : age, gender, anatomopathology, indication for surgery, timing of the lung resection to the cardiac surgery, type of cardiac surgery, type of pulmonary surgery, number of anastomosed vessels and ejection fraction. Only the staging had a significant impact on survival (p = 0.013). Because of the low number of patients, no significant correlation between the different stages could be shown. Of the 24 patients diagnosed with squamous cell carcinoma or adenocarcinoma, 13 patients are currently alive. 10 patients had no evidence of disease at post - operative intervals ranging from 6 to 80 months (mean =

4 Concomitant Cardio-Pulmonary Surgery 309 Table II Morbidity and Mortality Nr. Revision Complication Pneumonia Arrythmia Atelectasis Other Stay (days) Deceased FU (months) 1 N Y N N Y 17 Y 74 2 N N N N N 10 Y 17 3 N N N N Y 12 Y 75 4 Y Y N AF N 11 Y 29 5 N Y N N Y pleural drainage 9 Y 26 6 N Y Y N N 12 N 81 7 N Y N VES N 20 Y 46 8 N N N N N 8 Y 19 9 N N N N N 8 N N N N N N 8 N N N N AF N 9 Y N Y Y AF Y pneumothorax 9 N N N N N N 8 Y N Y Y AF Y 20 N N Y N AF N 12 Y N Y N AF N 12 Y N Y N AF, VES N PM sick-sinus 28 Y 3 18 N Y Y AF Y 19 N N N N N N 8 N N Y N AF N 14 N N N N N N 8 N Y Y Y N N 17 N 7 23 N N N N N 11 N 7 24 N N N N N 14 N 7 25 N Y Y AF N 10 N 6 26 N Y Y AF N 19 N 5 27 Y Y Y N Y Renal insuff. 29 N 4 N : no ; Y : yes ; AF : atrial fibrillation ; VES : ventricular extrasystoles. 35.1). One patient had a brain metastasis 80 months post - operatively. The metastasis was resected and the patient was given pan-cranial radiotherapy. Two patients have had a relapse of tumour, respectively 8 and 9 months after surgery. In the 11 patients that died, there were five patients with non-cancer related or unknown cause of death. The patients with a carcinoid tumour (stage IA) and benign lesion are alive. The patient diagnosed with a large cell neuroendocrine tumour (stage IA) died after 3 months. This patient was readmitted to the hospital with an acute abdomen. Computed tomography showed diffuse metastases and a bowel perforation. The patient was regarded as inoperable, palliative treatment was started and the patient died four days after admission. Total resection of the neuro-endocrine tumour in the former surgery was obtained. As no biopsy was taken of the metastasis, no pathologic confirmation of their origin could be obtained. Discussion Lung malignancies are reported in about 0.4% of patients undergoing coronary surgery (4). When a patient with a resectable lung tumour and cardiac disease needs treatment, three options are available : percutaneous transluminal coronary angioplasty with or without coronary stenting followed by lung surgery, a combined procedure with or without ECC and a two-staged procedure. When the coronary anatomy is suitable for trans - catheter intervention, it can be dealt with in the catheteri - sation laboratory. However, the adjunctive pharmacotherapy, necessary after such an intervention might increase the risk for hemorrhagic complications and might delay the resection of the lung tumour (5). Three problems related to concomitant heart and lung procedures through median sternotomy are reported (6) : The limited exposure for lung resection, particularly for exposure of the lower left lobe hilum and the mediastinal lymph node dissection. The bleeding risk due to heparinization. The risk of mediastinal or sternal infection related to lung resection. The concomitant approach has the advantage that the patient is spared the expense and potential morbidity of a second operation. Furthermore, management in a staged fashion implies a delay in the treatment of the

5 310 K. Cathenis et al. Fig. 1 Kaplan-Meier survival for patients with concomitant cardiac and pulmonary operations. lung cancer potentially leading to unresectability or metastatic spreading (7). Median sternotomy has become accepted as an alternative to lateral thoracotomy for most lung resections (8) and is considered the best choice for the resection of bilateral pulmonary metastases, bilateral giant bullae (9) and, according to WATANABE (10), pneumonectomy. Moreover mediastinal lymphadenectomy can be performed through median sternotomy. Only nodes below the hilum are difficult to remove and on the left side they cannot be removed at all. Left lower lobectomy, which is usually troublesome through median sternotomy, can be performed under CPB which offers a unique situation in which forward luxation of the heart is not risky (6). A left lower lobectomy is mentioned as the only lung resection that should always be performed during CPB as it avoids hemodynamic instability related to extreme tilting of the heart. Moreover, lymph node sampling becomes possible in the lower left mediastinum ; however an almost complete fissure must be present. The risk of bleeding is very low in this setting. TERZI et al. stated that if a fused fissure would be present, exposure of the interlobar pulmonary artery under heparinization is very hazardous and a left lower lobectomy should be planned through a lateral thoracotomy after 4-6 weeks (6). We believe that an incomplete fissure is not an indication to abandon concomitant surgery. In our series, we performed one left lateral thoracotomy for a left lower lobe resection with an OPCAB procedure using a left Internal Mammary Artery and a free Radial Artery. We believe this is a valid option if adequate coronary revascularization can be acquired. A study by ULICNY et al. (11) 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 RIVEIRE et al. (1). In a group of 79 patients who underwent a combined procedure over a 15-year period, the overall survival was higher in patients who underwent lung resection before CPB (55%) compared to those who underwent lung resection after CPB (20%). This difference failed to achieve statistical significance because of the small number of patients available for analysis at 5 years (12). BRUTEL DE LA RIVIERE et al. stated that survival was shorter when the lung resection was performed during extracorporeal circulation. This finding underscores the statement that cardiopulmonary bypass may enhance malignant growth. However, the rather high number of cardiac deaths in this subgroup did not allow a definitive conclusion concerning the influence of bypass. In addition, the predominant cause of late death in the series of RAO et al. (12) was cardiac, not recurrence of malignancy. Therefore, patients undergoing a combined procedure may be at risk for recurrence, but they are just as likely to die of progression of their cardiac disease. Coronary surgery without CPB and systematic heparinization may reduce the risk of peri-operative complications (13, 14). DANTON M. H., et al. stated that off-pump coronary surgery combined with lung resection through midline sternotomy should be taken into consideration in patients with symptomatic coronary artery disease and malignancies involving the right lung (15). We also believe this is a valid option if adequate coronary revascularization and pulmonary resection can be assured. Although the left lower lobe remains a surgical challenge, resection with CPB or through lateral thoracotomy has been used in the literature and in our series. Although no significant results could be deducted from our series due to the small number of patients, some general instructions for concomitant surgery can be deducted. It is stated in the literature and we also believe that a one-staged procedure can be performed without lifethreatening morbidity or mortality and is the first choice in concomitant disease. If CPB is needed, it is probably advantageous to perform the lung resection before the CPB and heparinization. This is usually not possible for left lower lobe resections. If the coronary disease allows it, an OPCAB-procedure should be performed.

6 Concomitant Cardio-Pulmonary Surgery 311 In conclusion we found that concomitant cardiac surgery and resection of pulmonary lesions can be performed without life-threatening morbidity and no in-hospital mortality. References 1. BRUTEL DE LA RIVIERE A. et al. Concomitant open heart surgery and pulmonary resection for lung cancer. Eur J Cardiothorac Surg, 1995, 9 (6) : ; discussion CIRIACO P. et al. Lung resection for cancer in patients with coronary arterial disease : analysis of short-term results. Eur J Cardiothorac Surg, 2002, 22 (1) : ASAPH J. W. et al. Median sternotomy versus thoracotomy to resect primary lung cancer : analysis of 815 cases. Ann Thorac Surg, 2000, 70 (2) : MARIANI M. A. et al. Combined off-pump coronary surgery and right lung resections through midline sternotomy. Ann Thorac Surg, 2001, 71 (4) : ELAMI A., KORACH A., RUDIS E. Lung cancer resection or aortic graft replacement with simultaneous myocardial revascularization without cardiopulmonary bypass. Chest, 2001, 119 (6) : TERZI A. et al. Lung resections concomitant to coronary artery bypass grafting. Eur J Cardiothorac Surg, 1994, 8 (11) : THOMAS P. et al. Is lung cancer surgery justified in patients with coronary artery disease? Eur J Cardiothorac Surg, 1994, 8 (6) : ; discussion URSCHEL H. C. Jr., RAZZUK M. A. Median sternotomy as a standard approach for pulmonary resection. Ann Thorac Surg, 1986, 41 (2) : VOGT-MOYKOPF I. et al. Late results of surgical treatment of pulmonary metastases. Thorac Cardiovasc Surg, 1986, 34 Spec No 2 : WATANABE Y., ICHIHASHI T., IWA T. Median sternotomy as an approach for pulmonary surgery. Thorac Cardiovasc Surg, 1988, 36 (4) : ULICNY K. S. Jr. et al. Concomitant cardiac and pulmonary operation : the role of cardiopulmonary bypass. Ann Thorac Surg, 1992, 54 (2) : RAO V. et al. Results of combined pulmonary resection and cardiac operation. Ann Thorac Surg, 1996, 62 (2) : ; discussion GU Y. J. et al. Reduction of the inflammatory response in patients undergoing minimally invasive coronary artery bypass grafting. Ann Thorac Surg, 1998, 65 (2) : PARTRICK D. A. et al. Cardiopulmonary bypass renders patients at risk for multiple organ failure via early neutrophil priming and late neutrophil disability. J Surg Res, 1999, 86 (1) : DANTON M. H. et al. Simultaneous cardiac surgery with pulmonary resection : presentation of series and review of literature. Eur J Cardiothorac Surg, 1998, 13 (6) : K. K. J. Cathenis Kortrijkse Steenweg 1026 B-9000 Gent, Belgium Tel. : +32/ koen_cathenis@hotmail.com