Methods: Twenty-three patients (17 females, 6 males; mean age: 69.7±6.5 years; range, 59 to 83 years) who underwent concomitant off-pump coronary artery bypass grafting and thoracic surgery procedures for lung cancer or a thoracic mass between March 2018 and February 2024 were included in the retrospective study. The surgical approach was median sternotomy for off-pump coronary artery bypass grafting, and video-assisted thoracoscopic surgery was preferred for lung tumor resections. Mortality, major adverse cardiac events, cerebrovascular events, and duration of hospital stay were evaluated.
Results: There were no postoperative deaths or perioperative myocardial infarctions. None of the patients experienced pneumothorax or atelectasis. None of the patients sustained excessive blood loss requiring reoperation. Arterial grafts were the first choice during coronary artery bypass grafting. Wedge resections, lobectomies, segmentectomies were performed in the subsequent video-assisted thoracic surgery. All patients were followed for six to 86 months. Four patients died during the postoperative one-year period, and one patient died at postoperative 29 months due to cancer relapse. The overall one-year survival rate was 86.5%, and three- and five-year survival rates were 74% and 74%, respectively.
Conclusion: The video-assisted thoracoscopic surgery approach provides a more favorable perspective for pulmonary resection and mediastinal lymph node dissection, which has importance in patients" final diagnosis, than the sternal view due to more ample, wider workspace. Combined off-pump coronary artery bypass grafting and pulmonary resection in patients with lung cancer is safe and effective and reduces possible complications of a second major surgery.
Traditionally, surgeons have been reluctant to perform concomitant cardiac surgery and pulmonary resection for three reasons: (i) heparinization and cardiopulmonary bypass (CPB) can increase the patient"s risk of excessive bleeding; (ii) cardiac surgery requires a median sternotomy approach, which is believed to provide inadequate exposure for pulmonary resection for lung cancer; (iii) CPB may alter the immunologic response, increasing the patient"s risk of mediastinal and pleural infection.[3,4]
Coronary artery disease carries a significant risk factor on surgical morbidity of lung cancer patients. Although the percentage of patients affected by both diseases reported by surgeons is relatively small, with 0.5%.[5,6] On the other hand, from thoracic surgery standpoint, at least 5% of patients awaiting a major lung resection require preoperative cardiologic or surgical interventions. These interventions, particularly in patients with unstable coronary artery disease, or after a recent myocardial infarction, require a good standard of care in this high-risk group to reduce surgical morbidity and mortality.[6]
It is still unclear which therapeutic option is the most beneficial. The first option is coronary angioplasty or stent placement before lung resection, which postpones the timing of the lung surgery, and the use of antiplatelet and anticoagulation medication for a certain period. The second option is coronary artery bypass grafting (CABG), followed by lung resection, which is a two-stage procedure. The potential problems with this approach include the delay in the lung resection due to postoperative recovery phase, and the additional cost of two separate operations.[7]
However, the open approach has the risk of dissemination due to manipulation of the pulmonary lobe, mechanical stress on the cardiac chambers, more difficult radical lymph node dissection, and the risk of increasing the amount of blood loss due to heparinization.[8] A minimally invasive approach for resection of early-stage lung cancers is promoted, and there is increasing interest in robotic approach.
Video-assisted thoracoscopic surgery (VATS) with concurrent lower lobectomy in combined surgical approaches involving median sternotomy was reported to be more feasible compared to anterolateral thoracotomy for lower lobectomy and complete mediastinal lymph node dissection (mLND).[9]
In the present study, we aimed to evaluate the outcomes of concomitant off-pump CABG and pulmonary operations for lung cancer patients.
The records were reviewed for age, New York Heart Association (NYHA) classification, EuroSCORE, left ventricular ejection fraction (LVEF), comorbidities, smoking, previous operations, operative procedures, final pathological diagnosis, tumor, morbidity, mortality, and longterm follow-up.
All the patients underwent combined off-pump CABG and lung resection surgery in a single session. Patients had symptoms such as cough, chest pain, or chest discomfort after exercise. Clinical examination, blood serum analysis, and cardiac echocardiography were performed for all patients. Each patient underwent coronary angiography and preoperative evaluation by positron emission tomography or CT imaging or combined positron emission tomography/CT imaging, pulmonary function tests, or bronchoscopy. Patients with lung cancer were classified and staged postoperatively in accordance with the 2015-2021 World Health Organization classification of lung tumors and using the Tumor, Node, Metastasis (TNM) staging.[11]
Surgical procedure
The decision for combined surgery was approved at
a multidisciplinary meeting, including the departments
of cardiology, cardiac surgery, and thoracic surgery.
The best management option was separately evaluated
for each patient.
Surgery was performed under general anesthesia with double-lumen endotracheal tube intubation. The cardiac and lung surgical procedures were carried out simultaneously. Coronary anastomoses were performed first on the beating heart using off-pump CABG surgery, followed by VATS or thoracotomy. The off-pump CABG procedure included harvesting of an arterial or venous graft, followed by beating heart aortocoronary bypass implantation. All patients received complete coronary revascularization.
Surgical approaches included median sternotomy in 23 patients for off-pump CABG procedures. In two patients, median sternotomy was completed with thoracotomy for right upper lobectomy and left upper sleeve lobectomy. Fourteen patients had median sternotomy followed by VATS, and seven patients had their lung procedures through median sternotomy.
Video-assisted thoracoscopic surgery was performed through three incisions without rib spreading using a standardized three-port anterior approach. The first port for initial thoracoscopic exploration was placed at the seventh or eighth intercostal space (ICS) in the midaxillary line. A working window (utility incision) of about 4 cm in length was made at the fourth or fifth ICS in the midclavicular line. An additional 5-or 10-mm port was made at the fifth or sixth ICS below the scapular tip. This port location served as a prompt conversion to open thoracotomy in emergent situations by connecting the working window and the posterior port. All the lung lobes could be resected and mLND could be achieved by this three-port configuration without major modifications. Complete mLND was achieved in all cases by rotating the operating table to provide an improved visual operative field, which is crucial for achieving complete surgery.
Separate pleural and mediastinal drainage tubes were used in all patients at the end of the surgical procedure, and low-molecular-weight heparin was given to all patients until discharge. Patients received acetylsalicylic acid and clopidogrel for antiplatelet therapy.
Definitions and follow-up
Survival was estimated based on the date
of surgery as the starting point and the date
of the death or last follow-up as the end point.
Cancer-free survival was defined as cancer relapse and/or metastasis reoccurrence free survival at
postoperative follow-up period. Operative mortality
was defined as deaths occurring within 30 days of
operation or during hospitalization.
All patients were followed postoperatively at the first week, first month, and third month, with scheduled follow-ups at the outpatient clinic after hospital discharge. At follow-ups, all the patients underwent physical examination, chest X-ray, and echocardiography. After a six month duration close follow-up of the patients was managed by both outpatient clinics. These patients were also followed by their cardiology and pulmonology primary attending physicians. All the patients whose final diagnosis was lung cancer were followed by the oncology department for their ongoing medical treatment. The chest CT was performed at six months postoperatively. A follow-up bronchoscopy was performed in patients with suspicion of a local recurrence.
Statistical analysis
Statistical analysis was performed using the
SPSS version 27.0 software (IBM Corp., Armonk,
NY, USA). Descriptive data were expressed in mean
± standard deviation (SD), median (min-max) or
number and frequency, where applicable. Normality
of the variables was checked using the Levene's
test. Survival was estimated using the Kaplan-
Meier method. A p value of <0.05 was considered
statistically significant.
Twenty-one patients had both hypertension and hyperlipidemia. Six patients had diabetes mellitus type 2. Eight patients had chronic obstructive pulmonary disease, and three patients had previously underwent coronary stenting. One patient had previous history of CABG, and one patient had chronic atrial fibrillation preoperatively. Fifteen patients had a history of smoking (Table 1).
Table 1. Characteristics of patients
Three patients had single-vessel disease, three patients had two-vessel disease, and the rest of 17 patients had a triple-vessel coronary artery disease. Transthoracic echocardiography revealed that LVEF was 30 to 50% in five patients and >50% in 18 patients. Fifteen (65%) patients had a history of smoking.
The detailed histology/staging, cardiac procedure, lung procedure, and surgical approach are summarized in Table 2. The final pathological diagnosis of these patients was mostly squamous cell lung cancer or adenocarcinoma staging from 1A to 3B. Among the remaining four patients, two patients had thymoma, and the other two patient had final pathological diagnosis as interstitial fibrosis.
Table 2. Surgery details of patients underwent concomittant off-pump CABG and pulmonary resection
A no-touch aorta technique was performed in 19 (82.6%) patients. The mean number of anastomoses was 3.09±1.1 (range, 1 to 5). Sixteen (69.6%) patients had T-composite graft, one (4.3%) patient had Y-composite graft. Arterial revascularization was the first choice, and left internal mammary artery was used as a graft in 20 (87%) patients, right internal mammary artery in five (21.7%) patients, radial artery in 16 (69.6%) patients, and saphenous vein in one (4.3%) patient (Table 3).
All the patients had off-pump CABG with a median sternotomy approach, followed by lung operation for lung cancer or mass either via median sternotomy, thoracotomy, or VATS with mLND, including eight wedge resections, nine lobectomies, one mediastinal mass resection, two thymothymectomy, one chest wall reconstruction and forequarter amputation, and two segmentectomy was performed. Analyses of intraoperative frozen sections were used to verify the presence of tumor-free margins in all patients.
The postoperative period went uneventful for all patients. Ten patients were extubated in the operating room, and the rest of the patients were extubated in the cardiovascular intensive care unit (ICU) less than 10 h postoperatively, and one patient had CABGx4 and right pneumonectomy, who had inotropic support less than 8 h, transferred to the ward 24 h postoperatively, and discharged on the sixth postoperative day. None of the patients experienced pneumothorax or atelectasis. No patient sustained excessive blood loss requiring reoperation. The mean drainage from chest tubes was 623.3±249.4 mL during the first 24 h postoperatively. The chest and mediastinal tubes were removed if the drainage was less than 150 mL in a 24-h period.
The mean length of ICU stay was 30.8±18.7 h . One patient had postoperative atrial fibrillation, with a history of off-pump CABGx4, left lung lower lobe superior segmentectomy, and left upper lobe wedge resection with mLND. The patient"s rhythm reversed to sinus rhythm with beta-blockers, and the final pathological diagnosis was squamous cell lung cancer (Stage 1B).
None of our patients suffered from deep sternal wound infections due to strict blood glucose during the follow-up. Cerebrovascular events were not observed during follow-up. In our institution, patient blood management policy is based on the Enhanced Recovery After Cardiac Surgery (ERAS) Society Guidelines.[13] The mean blood product usage for erythrocyte suspension was 0.35±0.714 packs, and the mean fresh frozen plasma (FFP) was 0.43±0.843 packs as summarized in Table 4.
Table 4. Postoperative outcomes
No early postoperative patient mortality or myocardial ischemia occurred during follow-up. None of the patients had cardiovascular events, including myocardial infarction, sustained ventricular tachycardia, heart failure, or sudden cardiac death postoperatively. All the patients recovered and were discharged from the hospital. No case was lost to follow-up.
Five patients died of cancer metastasis or reoccurrence, with deaths occurring at postoperative two, three, six, 13 and 29 months. The remaining 18 patients who survived at the end of the study were followed for a mean of (31.87±21.1 months; range, 5 to 72 months).
The overall one-year survival rate was 86.5%, and three- and five-year survival rates were 74% and 74%. The one-, three-, and five-year cancer-free survival rates were 82.5%, 82.5%, and 82.5%, respectively (Figure 1).
Figure 1. Kaplan-Meier survival curves for (a) overall survival and (b) cancer-free survival.
Cardiovascular disease and lung cancer are both associated with cigarette smoking.[4] In our study group, 15 (65.2%) patients had a history of smoking. The treatment of coronary artery disease is required to minimize the perioperative risk of lung surgery for lung cancer.[14] The long-term o utcomes of patients with coronary artery disease following treatment with percutaneous coronary intervention or CABG were investigated in a propensity-matched study, which showed that although percutaneous coronary intervention was associated with lower rates of periprocedural stroke, major bleeding, and acute renal injury. Coronary artery bypass grafting was associated with decreased incidence of early and late recurrent ischemia and reduced repeat revascularization procedures.[15]
Stent placement should be avoided in patients who are being considered for soon after coronary intervention. Previously reported studies have shown preference for two-stage procedure, in which coronary intervention is performed first, followed by a lung resection with surgical treatment requiring interval of between six and twelve weeks after coronary stenting. This approach is preferred because surgeons are reluctant to perform concomitant cardiac surgery and pulmonary resection for heparinization, and CPB can increase the patient"s risk of excessive bleeding. The median sternotomy approach for cardiac surgery is believed to provide inadequate exposure for pulmonary resection and mLND.[12-14] Cardiopulmonary bypass may affect the immunologic response, which might increase the patient"s risk of mediastinal and pleural infection and complicate the postoperative outcome of the patient. On the other hand, if lung cancer is treated in a separate procedure, the condition that constitutes the most immediate risk to the patient (usually the cardiac disease) should be treated first, and the condition that constitutes a less immediate risk should be treated four to six weeks later.[3] Once the diagnosis of lung cancer is made, surgical resection should be performed as soon as possible. Patients also require intensive anticoagulation following coronary artery stenting, which is associated with high risk of hemorrhagic complications. In patients who have tumors with rapid doubling times, however, such a delay could affect survival. If CABG is performed, the postoperative recovery period may also postpone the lung resection, which may result in tumor progression. However, if lung tumor resection surgery is performed first, the perioperative risk of severe coronary artery impairment can reduce fatal complications. Additionally, a two-stage approach requires two rounds of general anesthesia, two separate incisions, and a longer hospital stay, whereas treating both diseases during the same procedure reduces risk, pain, and costs.[5]
In our study, a one-stage operation and concomitant off-pump CABG and pulmonary operations mainly for lung cancer were performed. None of our patients had required reoperation for excessive blood loss. All the analyses of intraoperative frozen sections were used to verify the presence of tumor-free margins in all patients. Based on the results of these analyses, pulmonary resection was complete in all our patients.
Five of our patients died between postoperative two to 29 months due metastasis or recurrence of cancer. Survival after surgical resection of lung cancer varies according to the cell type and stage of the cancer, both of which must be evaluated.[16]
In a series of 43 patients, the Mayo Clinic group reported only one death, which occurred in a patient who underwent pulmonary resection during CPB.[2] Only 11.6% of resections were performed during CPB. In their report, which compared staged and combined procedures, only three (10%) patients required reoperations for bleeding in combined cardiac and lung surgery procedure. The Texas Heart Institute reported one operative death among 21 patients who underwent cardiac and pulmonary surgery.[4] This death occurred in an 80-year-old male patient who had undergone triple-vessel CABG grafting with concomitant wedge resection of the right upper lobe for adenocarcinoma. After the operation, the patient developed an acute myocardial infarction and subsequent arrhythmias. Despite the pharmacological support and use of an intra-aortic balloon pump, the patient died on the second postoperative day. Their median follow-up duration was 4.1 years, ranging from 2 days to 7.4 years. The overall one-year survival rate was 90.5%, and the five-year survival was 52.4%.[4]
The advantage in combined CABG and lung operation was that none of our patients had extracorporeal circulation, which can increase the concentration of free oxygen radicals, leading to cell damage, inhibiting the immune system, enhancing tumor growth, and promoting tumor metastases. Off-pump full arterial revascularization CABG can reduce bleeding during tumor resection due to the decreased intraoperative heparin dose. Off-pump CABG is usually performed at first, and it can ensure that there is an adequate intraoperative coronary artery blood supply to avoid intraoperative myocardial ischemia and cardiac function.
In their study including 25 patients, Dyszkiewicz et al.[6] reported that simultaneous off-pump myocardial revascularization and lung resection was a safe and effective treatment modality, when unstable coronary artery disease and lung cancer coexisted. In their study, the median number of anastomosed coronary vessels was 1.9. Twenty of their patients had median sternotomy approach. In four patients, they preferred left lateral thoracotomy. In one patient, they used both sternotomy and a partial left thoracotomy. The three-year survival rate of their patients was 50%. The authors tended to perform combined procedure as their first-line treatment option.
In our study, simultaneous off-pump CABG and lung resection procedures require different surgical skills. The sternotomy approach, which is infrequently used by thoracic surgeons, is difficult when performing a left lower lobectomy and mLND. The combined surgery could have been reserved for patients who were clinically or surgically staged during the pre- and perioperative periods. An important aspect of this procedure is the sequence of the operative steps. It is crucial to perform the coronary anastomosis before lung resection.[17] In our patient group, mLND was performed in all patients. Pre- and perioperative judgement of the lesion was evaluated. We conclude that the sternotomy approach makes complete lymph node sampling of the posterior mediastinum difficult, and incomplete lymph node sampling could affect the long-term results of pulmonary resection for lung cancer. The survival after surgical resection of lung cancer varies according to the cell type and the stage of the cancer, both of which must be evaluated.
Fourteen of 23 our patients with concomitant cardiac and lung surgery were planned with VATS. Thoracoscopic equipment was used to minimize the incision size and minimize the postoperative pain. Thoracoscopic lobectomy has been shown to be superior in terms of length of stay, postoperative pain, pulmonary function, and postoperative complications compared to open lobectomy.[18] Lung cancer resection with a median sternotomy may be associated with technical problems, as left lower lobectomy is difficult to perform through a median sternotomy, and the use of two incision approach can lead to significant postoperative discomfort, pain, delayed mobilization, and increased incidence of early postoperative complications. Furthermore, VATS is safe in combined procedures, the operated heart and anastomosed new grafts would not be retracted, and there would be less incidence of arrhythmia and myocardial ischemia.
Liu et al.[14] reported their experience with combined off-pump CABG and lung resection in 23 patients over 50 years of age. Their mean length of hospital stay was 19.2±12.3 days, with a mean duration of stay in the ICU of 40.4±32.4 h. In our study of 23 patients, the mean length of hospital stay was 7.9±3.0 days, with a mean ICU stay of 30.8±18.7 h. Liu et al.[14] reported a five-year survival rate of 47.9% for the remaining 15 patients. The five-year survival rate of the remaining 18 patients was 74%.
Shaff et al.[2] showed that at the time of pulmonary resection, a thorough evaluation of paratracheal, subcarinal and inferior pulmonary ligament lymph nodes was mandatory. Limited sampling of these areas has the potential for underestimating the stage of disease and may be the reason of reduced longterm survival in previous studies with a combined technique.
Karagoz et al.[19] and Vural et al.[20] reported a total arterial revascularization experience on beating heart CABG in patients with low ejection fraction for more than 30 years. The patients with an ejection fraction between 30 and 50% tolerated the following lung surgery well. None of the patients had extracorporeal circulation during CABG and high doses of heparinization, whereas our patients did not require an extensive amount of blood products due to combined surgery. The mean postoperative blood drainage from chest and mediastinal tubes was 623.3±249.4 mL. In our study, we observed no atelectasis, pneumothorax, or any pleural infection due to combined surgery.
Kanzaki et al.[21] reported their combined and two-stage approach and concluded that the surgical risk related to the simultaneous lung cancer procedure and off-pump CABG was lower than that of cardiac surgery with extracorporeal circulation (on-pump).
Zhang et al.[22] reported that simultaneous procedure had advantages such as shorter hospital stay, lower perioperative morbidity, and the potential to avoid cancer growth and dissemination, particularly in on-pump cardiac surgery. They observed a much lower five-year survival rate of 43.6%. Older age was the major factor associated with worse outcomes in patients with malignant incidental solitary pulmonary nodules. Accurate surgical nodal staging is mandatory to identify patients who may need adjuvant therapy.
Al-Attar et al.[23] reported combined left pneumonectomy and off-pump CABG through left thoracotomy in early 2000s as a single-stage approach. Omeroglu et al.[24] summarized their three patients with combined off-pump CABG and lung surgery. They reported that myocardial revascularization on beating heart CABG, when feasible, was preferred over the use of CPB to avoid side effects, particularly hemorrhage, making the following lung surgery safer.
Furthermore, Zhang et al.[25] reported that during simultaneous off-pump revascularization and pulmonary operations, the pulmonary resection surgery should be performed after reversal of anticoagulation and recommended videoscopy to evaluate suspected bleeding. Tourmousoglou et al.[26] also showed that off-pump CABG and lung resection could be safe and effective treatment, when unstable coronary artery heart disease and lung cancer coexisted. In their systematic review, Cheng et al.[27] showed that off-pump CABG might reduce the complication rate compared to on-pump CABG. Considering median sternotomy approach compared to a lateral thoracotomy, mLND is technically more difficult and time-consuming, the subcarinal and posterior mediastinal lymph nodes are particularly difficult to sample.
In another study, Choong et al.[28] highlighted the importance of a skilled anesthetist in ensuring the proper placement of a double-lumen endotracheal tube and careful intraoperative management of the patient. Our patients had multi-arterial revascularization off-pump CABG following lung resection for lung cancer. All patients tolerated the perioperative period of lung surgery well. The utility of VATS assistance in performing lobectomy, lingulectomy, segmentectomy, and mediastinal lymph node resection in combined cardiac surgery is significant.
The limitations to this study include its retrospective design, the inclusion of patients from two centers, and the allocation of the patients to concomitant offpump CABG and pulmonary operations based on the surgeons' discretion regarding the surgical technique.
In conclusion, combined off-pump coronary artery bypass grafting and pulmonary resection for lung surgery can be safe and effective, preferably with video-assisted thoracoscopic surgery assistance. Complete mediastinal lymph node sampling is crucial for achieving long-term survival. Combined techniques should be performed at reference hospitals with skilled anesthesiologist teams.
Data Sharing Statement: The data that support the findings of this study are available from the corresponding author upon reasonable request.
Author Contributions: Idea/concept, design, control/ supervision, critical review: S.T., M.S.A.,S.E., Z.T.D.; Data collection and/or processing, analysis and/or interpretation: Z.T.D., S.E.; Literature review, writing the article: Z.T.D.; Materials: K.B.O., E.A., S.G, E.E.C.
Conflict of Interest: The authors declared no conflicts of interest with respect to the authorship and/or publication of this article.
Funding: The authors received no financial support for the research and/or authorship of this article.
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