Perioperative safety of simultaneous pulmonary resection and off-pump coronary artery bypass grafting: a retrospective analysis from a single institution

Introduction

Cigarette smoking is a major risk factor for lung cancer and coronary heart disease (CHD). Its effects on platelet aggregation and blood vessel constriction lead to CHD. Additionally, the relationship between cigarette smoking and the risk of lung cancer has been established for several decades (1,2). With the increasing incidence of lung cancer and coronary artery disease (CAD) in China, the number of lung cancer patients with CHD is also increasing. According to The Society of Thoracic Surgeons database, 20.9% of patients undergoing pulmonary resection for lung cancer have CAD; however, only 0.4–0.5% of these patients require coronary artery bypass grafting (CABG) (3-5). When dealing with such patients, it is not only necessary to complete the resection of tumor lesions but also to address coronary artery lesions. Treating patients with lung cancer and severe concurrent CHD is a challenge for thoracic surgeons because these patients face great cardiac risk if pulmonary resection is performed without myocardial revascularization. If lobectomy and cardiac bypass surgery are performed at different stages, there may be a risk of lung tumor progression due to prolonged antiplatelet after coronary artery bypass surgery, resulting in the patient losing the opportunity to undergo surgery. With the development of cardiac surgery and endoscopic technology, off-pump CABG and concurrent pulmonary resection can be performed successfully and safely (6,7). This report retrospectively analyzed the postoperative complications, perioperative safety (intraoperative blood loss, respirator usage time), and hospitalization status of patients who underwent both pulmonary resection (wedge resection or lobectomy) and off-pump CABG in Tianjin Chest Hospital. We present this article in accordance with the STROBE reporting checklist (available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-1369/rc).

Methods

Patient

This study reviewed the database of patients with pulmonary nodules and CHD who underwent simultaneous surgery at Tianjin Chest Hospital, China, between January 2020 and December 2023. This retrospective clinical study was divided into two groups based on different lung surgical methods: lobectomy combined with off-pump CABG (Group A) and wedge resection combined with off-pump CABG (Group B). Patients who underwent off-pump coronary CABG grafting alone were included in the control group. Group A consisted of 39 patients, Group B consisted of 46 patients, and control group consisted of 78 patients. Groups A and B were compared with control group in terms of hospitalization duration and expenses, perioperative safety, and surgical complications. Detailed baseline information is presented in Table 1.

Data collection

The patients selected for the study were symptomatic, with symptoms including 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 using positron emission tomography (PET), computed tomography (CT) imaging, or combined PET/CT imaging, as well as pulmonary function tests. Preoperative and postoperative echocardiography, as well as information related to surgery and perioperative period, are all obtained from patient examination reports, anesthesia records, or medical records.

Surgical intervention

Surgery was performed under general anesthesia with double-lumen endotracheal tube intubation. The lung and cardiac surgical procedures were performed simultaneously. Coronary anastomoses were first performed on the beating heart using off-pump, followed by wedge resection or lobectomy. All pulmonary nodules were subjected to intraoperative freezing to preliminarily determine their nature. Patients diagnosed with malignant tumors using frozen surgical specimens during surgery underwent systematic lymph node dissection. The nature of pulmonary nodules and lymph node is ultimately determined by hematoxylin-eosin staining and immunohistochemistry.

The surgical methods included: 73 patients who underwent median sternotomy and 5 patients who underwent left minimally invasive thoracotomy in the control group; 37 patients who underwent median sternotomy, and 2 patients who underwent left minimally invasive thoracotomy in Group A; 45 patients who underwent median sternotomy and 1 patient who underwent left minimally invasive thoracotomy in Group B. The off-pump CABG procedure included harvesting of an arterial or venous graft followed by aortocoronary bypass graft implantation. All patients underwent complete coronary revascularization. The average number of coronary artery bypass grafts in the control group was 2.5±0.8, in Group A was 2.5±0.8, and in Group B was 2.5±0.9. Among them, 74 patients in the control group received treatment with internal mammary artery bypass grafting, while 35 and 37 patients received treatment in Groups A and B, respectively. During the entire cardiac-related treatment process, 3 patients (3.8%) in the control group received intra-aortic balloon pump (IABP) treatment, with 1 case (2.6%) in Group A and 2 cases (4.3%) in Group B.

Pulmonary nodule resection was performed after the patient’s circulation stabilized and heparin was neutralized. Video-assisted thoracoscopy was performed in the lobectomy Group A. To achieve lymph node dissection, the operating table was rotated to provide a better surgical field of vision. Patients with median sternotomy can use an internal mammary artery distractor to expand the surgical field of view. Among them, 11 patients underwent lower lobectomy by reopening the surgical incision in the lateral chest wall, while the other patients still underwent the median incision of cardiac bypass for lobectomy. Wedge resection (Group B) was performed in the median incision of cardiac surgery without video-assisted thoracoscopy.

After surgery, when a patient achieved complete hemostasis, a water test was performed to dilate the lung and check for air leakage and bleeding. Separate thoracic and mediastinal drainage tubes were used in patients who underwent median sternotomy at the end of the surgical procedure, thoracic drainage tube was used in patients who underwent left minimally invasive thoracotomy. The patients were sent back to the intensive care unit (ICU) with endotracheal intubation retained. The general condition of the patients was evaluated and they were liberated from mechanical ventilation as early as possible to avoid postoperative pulmonary infection. The timing of the removal of the thoracic and mediastinal drainage tubes was determined according to the postoperative drainage volume and air leakage. The patients were asked to get out of bed as early as possible to avoid the formation of deep vein thrombosis and were given continuous atomization inhalation to promote coughing and expectoration to avoid complications of pulmonary atelectasis and pulmonary infection. After surgery, chest radiography was performed to check for pneumothorax or pleural effusion. Echocardiography was performed to evaluate cardiac function after surgery. All patients received subcutaneous injection of low molecular weight heparin (LMWH) until discharge. Treatment to prevent platelet aggregation and lower blood lipid level was maintained after discharge. Some postoperative patients with cough were treated with adjuvant cough suppressive/anti-asthma drugs.

Patients who experience arrhythmia or heart failure after surgery or transferred to the ICU because of unstable blood circulation are defined as having cardiovascular complications. Patients with iatrogenic pathogenic bacteria obtained through sputum culture, continuous fever accompanied by elevated white blood cells, or postoperative respiratory failure are defined as having respiratory complications. Prolonged hospitalization or increased treatment costs due to surgical factors are defined as surgical-related complications, such as postoperative bleeding leading to a second surgery, persistent air leakage for more than 7 days, chylothorax, symptoms caused by nerve damage, poor wound healing or sternum healing leading to a second surgery, and mediastinal infection and postoperative pulmonary embolism. Perioperative safety mainly includes surgical time, intraoperative blood loss, perioperative blood transfusion volume, respirator usage time and perioperative mortality.

The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). This study was approved by the Medical Ethics Committee of Tianjin Chest Hospital (approval No. 2024YS-031-01). The requirement for patient consent was waived due to the retrospective nature of the present study.

Statistical analysis

All statistical analyses were performed using IBM SPSS Statistics for Windows, version 23.0 (IBM Corp., Armonk, NY, USA). A propensity score-matched (PSM) analysis using Stata 11.2 was performed to balance any potential confounders between the groups. A total of 967 patients who underwent off-pump CABG at Tianjin Chest Hospital from 2020 to 2023 were subjected to propensity matching based on four factors (age, gender, smoking history, and number of coronary artery bypass grafts). Seventy-eight patients who underwent off-pump CABG were selected at a ratio of 1:2 and enrolled in the control group. All continuous variables were tested for normal distribution, and variables that conformed to normal distribution were expressed as mean ± standard deviation and were compared and analyzed using the t-test. The Kruskal-Wallis test was employed to assess differences between the three groups in terms of surgical and perioperative-related indicators and echocardiographic-related data. Postoperative complications were expressed as percentages, and comparisons and analyses were performed using the Chi-squared test.

Results

Surgical outcomes

The preoperative cardiac function assessment [left ventricle (LV)/pulmonary artery systolic pressure (PASP)/left ventricular ejection fraction (LVEF)] and New York Heart Association functional classification in three groups of patients were consistent. In terms of postoperative cardiac function evaluation, there was no statistically significant difference between the three groups. Regarding the nature of the nodules, there were 6 patients with benign diseases and 33 patients with malignant lung tumors in Group A; 17 patients with benign diseases and 29 patients with malignant lung tumors in Group B. From perspective of lung cancer staging, in Group A, 16 patients had stage IA, 8 patients had stage IB, 6 patients had stage II, and 3 patients had stage III disease. In Group B, there were 26 patients with stage IA, 2 with stage IB, and 1 with stage IV disease. Among them, stage IV patients were diagnosed with malignant pleural effusion during surgery and underwent pulmonary wedge resection for pathological diagnosis. Due to the intraoperative application of thoracoscopic technology, in Group A, 13 patients underwent right upper lobectomy, 1 patient underwent right middle lobectomy, 3 patients underwent right lower lobectomy, 13 patients underwent left upper lobectomy, and 9 patients underwent left lower lobectomy. The specific information is shown in Table 2.

Postoperative complications

There were no significant differences in postoperative pulmonary or cardiac-related complications in the three groups, which indicates that the combined surgery did not increase postoperative cardiovascular and pulmonary-related complications. For surgery-related complications, there is a statistical difference between Group A and control group. This was mainly because the risk of air leakage and chylothorax in patients after lobectomy combined with off-pump CABG was significantly higher than that in the off-pump CABG group alone. From the perspective of the rate of secondary surgery, there was no statistically significant difference between the three groups, which confirms that the combined surgery did not increase secondary surgery caused by postoperative bleeding or wound infection. The detailed information on postoperative complications is presented in Table 3.

Postoperative safety and hospitalization status

From the perspective of postoperative evaluation, there was a significant statistical difference between Group A and control group, Group B in terms of surgical time. From the perspective of intraoperative bleeding volume, there is a significant statistical difference between Group A and control group, while pulmonary wedge resection does not increase the risk of intraoperative bleeding. There was no significant statistical difference between the three groups in terms of duration of ventilator use. It can be inferred that loss of lung function after lobectomy dose not prolong the time for tracheal intubation. From the perspective of intraoperative and postoperative blood transfusion, there was no statistically significant difference between the Group A and control group. There were no perioperative deaths among the three groups of patients. In terms of hospitalization time, there was a statistically significant difference between Group A and B compared to the control group. From the perspective of total hospitalization expenses, there was a significant statistical difference between Groups A and B compared to control group, as there was a consumption of surgical consumables in lung surgery. Detailed information is presented in Figure 1.

Figure 1 Surgical and perioperative related indicators. (A) Surgical time; (B) intraoperative blood loss; (C) respirator usage time; (D) blood transfusion volume; (E) hospitalization time; (F) hospitalization expenses. ns, P>0.05; *, P<0.05. CABG, coronary artery bypass grafting; ns, not significant.

Discussion

Malignant tumors and cardiovascular diseases are the leading causes of death in men and women worldwide. Lung cancer is the most common malignant tumor and the main cause of cancer-related death in China (8). CAD, which accounts for almost one-third of deaths caused by cardiovascular disease worldwide, is the second leading cause of death in China (9). With the increase in the elderly population and the popularization of coronary artery CT scans, an increasing number of patients are being diagnosed with concurrent pulmonary nodules and CAD. However, there is a dilemma regarding surgical treatment strategies. Based on the different properties of pulmonary nodules and the severity of coronary artery stenosis, doctors will provide different treatment suggestions. A multidisciplinary approach is recommended to guide treatment decisions in this high-risk growing patient group (10). According to European guidelines (11), CABG is recommended as Class IA for patients with left main artery disease (regardless of the SYNTAX score), three-vessel disease (regardless of the presence of diabetes), and diabetes patients with multi-vessel disease including anterior descending artery disease. Based on the diagnosis and treatment guidelines for primary lung cancer (12), from the perspective of lung cancer alone, the absolute indication for lung cancer surgery is T_1–3N_0–1M₀ stage lesions, while the relative indications are T₄N_0–1M₀ and T_1–3N₂M₀ stage lesions. There is currently controversy over whether surgery should be performed for isolated T_1–3N_0–1M₁ stage lesions, and further evaluation of surgical indications is needed after neoadjuvant therapy. According to relevant literature (13), it is recommended that patients who meet the absolute indications for lung cancer surgery and off-pump CABG undergo coronary artery revascularization and lung cancer resection hybrid surgery. Our surgical center has summarized the contraindications for combined surgery as follows: it is not recommended to continue lung surgery for patients with hemodynamic instability after coronary revascularization. For patients with pulmonary groove tumors, positive N2 lymph nodes, or extensive thoracic adhesions, combined surgery is not recommended.

Conventional CABG surgery typically requires a midsternal incision that exposes the heart and major cardiovascular vessels, to complete coronary revascularization (14,15). For peripheral pulmonary nodules with a diameter ≤2 cm and a solid component less than 50%, wedge resection with a sternal midline incision does not pose technical difficulties due to exposure of the field of view. However, limited exposure during sternotomy may lead to technical difficulties in Lobectomy and mediastinal lymph node resection, especially if both internal thoracic arteries are implanted (7). Darling et al. (16) reported that compared to mediastinal lymph node sampling, mediastinal lymph node dissection did not improve the survival of patient with early non-small cell lung cancer (NSCLC). Therefore, lung cancer radical resection combined with lymph node dissection through a median sternal incision will not reduce the survival of early NSCLC patients. The contraindications for CABG combined with lobectomy from the sternal median incision are left lower lobe resection and upper sulcus tumor resection (17-19). Combined hybrid surgery is not recommended for patients with N2-positive lung cancer (7). The use of internal mammary artery distractors and thoracoscopic equipment improve the exposure of anatomical structures in the hilum and mediastinum of the lungs. In addition, combined surgery also involves other issues such as potential bleeding associated with heparinization. Ulicny et al. (20) reported that 15.8% of patients experienced bleeding problems. Therefore, it has been emphasized that in cases where both pulmonary surgery and off-pump coronary revascularization are performed simultaneously, pulmonary resection should be performed after anticoagulation reversal, and television endoscopy is recommended to examine suspected bleeding (6). Based on the clinical experience of the author and our center, with the application of minimally invasive techniques in cardiac surgery and thoracoscopic techniques, the left intercostal incision combined with thoracoscopic techniques can effectively reconstruct coronary artery blood flow and complete radical resection of lung cancer in the upper or lower left lobe.

There are several advantages of performing combined surgery in patients with CAD and surgically viable lung tumors. This approach avoids late thoracotomy, reduces surgical trauma, reduces anesthesia frequency, lowers treatment costs, and decreases the frequency of anesthesia (21-23). Early treatment of malignant tumors can prevent delays in lung cancer treatment, which may be more important in patients with highly invasive lung malignancies. The procedure is manageable from the perspective of perioperative safety and postoperative complications. In the present study, the combination of off-pump CABG and pulmonary resection did not increase the incidence of pulmonary or cardiac-related complications, or secondary thoracotomy. For patients with qualified preoperative lung function or blood gas analysis, lobectomy combined with off-pump CABG did not increase the risk of failed tracheal tube removal due to respiratory failure. Owing to the complications of pulmonary leakage or chyle fistula in radical lung cancer surgery, combined surgery is more prone to such complications than off-pump CABG alone. However, these postoperative complications are curable and manageable. Although off-pump CABG combined with lobectomy had a higher intraoperative blood loss than off-pump CABG alone due to limited surgical field, there were no intraoperative deaths or burden of blood transfusion. The second surgery rate remained consistent between the three groups owing to postoperative bleeding, indicating that combined surgery in terms of bleeding is also safe and manageable. Lobectomy combined with off-pump CABG involves two surgeries and requires a longer surgical time than off-pump CABG alone. However, wedge resection did not significantly increase the surgical time owing to its simplicity. Patients undergoing combined surgery have a longer hospitalization time than those undergoing CABG alone. This was mainly due to the increased hospitalization time caused by preoperative evaluation of pulmonary nodules and the surgical time determined by thoracic and cardiac surgeons. Although the expenses of pulmonary resection combined with off-pump CABG are significantly higher than those of individual off-pump CABG, cardiopulmonary surgery can reduce preoperative examination/anesthesia costs and postoperative support treatment-related costs, which reduces patient hospitalization expenses over the entire treatment process. Dyszkiewicz’s research (4) shows that simultaneous off-pump myocardial revascularization and lung resection is a safe and effective treatment when unstable CHD and lung cancer coexist, can be an alternative to the two-stage approach, surgical or non-surgical (cardiologic) interventions preceding the pulmonary resection. Ma’s article (7) indicates that combined off-pump CABG and pulmonary resection for early-stage lung cancer patients with concurrent severe CHD is a relatively safe and effective treatment with satisfactory long-term survival rates, especially for those patients with three-vessel disease. Yeginsu et al. (24) found that combination surgery is a safe and reliable option among 10 patients who underwent both off-pump GABG and pulmonary resection simultaneously. In summary, consistent with previous publications (4,7,24), off-pump CABG combined with pulmonary resection was safe and feasible. The author hereby declares that CABG combined with lobectomy is recommended to be carried out in experienced hospitals and requires multidisciplinary discussion.

There are several limitations in this study. First, its retrospective nature imposes inherent constraints, necessitating future large-scale randomized controlled trials to obtain more precise conclusions. Second, the relatively small sample size limited the statistical power of the study. Finally, as this was an observational study, there is a possibility of having unaccounted confounding factors related to baseline characteristics. Addressing these limitations in future studies could provide a more comprehensive understanding of the perioperative safety of CABG combined with lobectomy.

Conclusions

In conclusion, CABG in combination with pulmonary resection is safe during the perioperative period, and the incidence of postoperative complications is manageable, reducing patients’ overall hospitalization costs. However, combined surgery poses certain technical difficulties and should be performed at experienced institutions.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-1369/rc

Data Sharing Statement: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-1369/dss

Peer Review File: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-1369/prf

Funding: The present study was funded by the Tianjin Key Medical Discipline (Specialty) Construction Project (No. TJYXZDXK-018A) and the Tianjin Health Technology Project (No. TJWJ2024XK016).

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-1369/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). The research was evaluated and authorized by Medical Ethics Committee of Tianjin Chest Hospital (No. 2024YS-031-01). The requirement for patient consent was waived due to the retrospective nature of the present study.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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