Introduction

Despite the paucity of patients undergoing sleeve lobectomy compared to pneumonectomy, sleeve lobectomy surgery for non-small cell lung cancer (NSCLC) originating in the lobar bronchus is well established and is now the preferred and curative method to managing central airway tumors in surgical candidates [1, 2]. This conclusion has evolved over time and sleeve lobectomy was initially thought of as an alternative to pneumonectomy for managing central endobronchial tumors, in patients with impaired cardiopulmonary reserve. Sleeve lobectomy can now be safely performed from both open and minimally invasive approaches, and even following induction chemotherapy [3,4,5,6,7]. A very recent published series demonstrated the safety of robotic sleeve lobectomy for lung cancer in 21 patients with a mortality rate very similar to that reported of open series [8]. We continue to recognize, based on much experience, that sleeve lobectomy should be considered a primary intervention in lieu of pneumonectomy.

The first notable sleeve lobectomy was performed in 1947 by Price-Thomas, and several years later, Allison reported the first use of sleeve lobectomy in carcinoma treatment [9,10,11]. In 2008, Boffa et al. reviewed the Society of Thoracic Surgeons general thoracic surgery database and the surgical management of primary lung tumors. They reported that between 1999 and 2006, out of the 9033 pulmonary resections analyzed, there were 591 pneumonectomies and only 85 sleeve lobectomies completed for primary lung cancer (6.5 vs 0.9%). The reported operative mortality in the pneumonectomy group was 6.2% and the 30-day mortality 5.3%, compared to lobectomy and sleeve group with a reported 2 and 1.8%, respectively [1]. The increased operative risk observed in pneumonectomy compared with that of sleeve lobectomy and reported 11 years ago still stands today [1].

The benefits of sleeve lobectomy have been well established [12, 13]. In addition to being more cost effective and preserving pulmonary function, sleeve lobectomy when compared with pneumonectomy can be completed with a much lower risk of operative and overall mortality. It is also associated with improved local control and long-term survival and enhanced quality of life. Today, we expect the operative mortality for sleeve lobectomy to be less than 5%. [14]. The most recent large series by Pages et al. examining overall and disease-free survival rates associated with sleeve lobectomy in 942 patients showed a 71.9% overall 3-year survival after sleeve lobectomy compared to 60.8% after pneumonectomy. In addition, 3-year disease-free survival in the sleeve group was 46.4 and 31.6% in the pneumonectomy group. The pneumonectomy group also showed an increased risk of disease recurrence in comparison to the sleeve group [15]. The superior outcomes noted in this study of sleeve lobectomy patients with NSCLC should strongly encourage surgeons to embrace this surgical approach in similar patient populations.

In this paper, we review the patient selection factors and current indications for considering sleeve lobectomy. In addition, we describe our sleeve lobectomy surgical technique and review post-operative management strategies and potential associated complications. We also discuss the outcomes and survival rates associated with sleeve lobectomy in more recently available published series.

Considerations for patient selection

According to the Surveillance, Epidemiology, and End Results (SEER) database, the estimated number of new lung cancer cases in the USA is 222,500, with the disease most frequently being diagnosed in people aged 65–74 years old. Many of these patients will have tumors with involvement of the central airways at the time of diagnosis, in the form of endobronchial tumor extension, bulky disease, or compressive peribronchial lymphadenopathy. Often, partial or complete airway obstruction will limit functional status in these patients and cause dyspnea, hemoptysis, or cough. Many patients will go undiagnosed for some time and may only have vague symptoms on presentation. Tumor occurring in the lobar orifice or invading the main bronchus precludes standard surgical lobectomy, and in these cases, whenever R0 resection is feasible, sleeve lobectomy should be considered as the procedure of choice and considered equivalent to a pneumonectomy. Even in patients with N1 disease, sleeve lobectomy has been shown to have superior outcomes when compared to pneumonectomy [5, 6, 16, 17]. For every patient presenting with complex lung cancer, an assessment of operability should be expeditious and thorough, as surgical resection can often be curative in patients with central airway disease. In brief, the indications for sleeve lobectomy include the following: patients diagnosed with central lung cancer; a lobar resection margin positive for malignancy on frozen section; avoidance of pneumonectomy in patients where preservation of lung parenchyma is key, and those with compromised cardiopulmonary function.

Operability of patients with central airway tumors should be assessed by an interdisciplinary expert team involving thoracic surgeons, pulmonologists, cardiologists, radiologists, pathologists, oncologists, and radiation oncologists. This multidisciplinary team approach to lung cancer patients in general is also imperative to long-term follow-up and life-long surveillance. Detailed imaging and cardiopulmonary function testing is essential for determining candidacy for sleeve lobectomy or pneumonectomy and planning the operative strategy. It is reasonable to obtain an echocardiogram and cardiac stress test, in addition to pulmonary function testing on all patients being considered for this surgery. Patient selection for sleeve lobectomy thereafter will ultimately depend on tumor location, tumor type, and accurate preoperative nodal staging. The central airways should be assessed initially with non-invasive computed tomography (CT) imaging to evaluate for airway obstruction, narrowing, potential surgical margins, pulmonary artery involvement, associated nodal enlargement, and relationship of adjacent parenchymal lung masses. A CT angiogram can assist with planning for possible concomitant pulmonary artery resection if involvement is suspected. Three-dimensional reconstruction of images can help visualize disease with greater certainty and identify planes of potential dissection. Fiberoptic bronchoscopy is recommended to evaluate endobronchial extent of disease and can often be utilized for diagnostic purposes also. Tissue sampling for diagnosis is almost always possible with bronchoscopy for proximal endobronchial tumors and can be complimented with the use of navigational bronchoscopy and radial endobronchial ultrasound (EBUS) when needed. CT-guided lung biopsies of the primary lesion can be reliably used when diagnosis is called into question with these approaches. Once a diagnosis is firmly established, a positron emission tomography (PET)-CT scan should be obtained for complete staging purposes and to ensure no evidence of disease which would preclude resection. This can also be useful in determining the need of EBUS-transbronchial needle aspiration (TBNA) or mediastinoscopy for nodal sampling prior to lobectomy. Induction therapy when indicated is recommended in an effort to downstage locally advanced central tumors and encourage later resection. Either chemotherapy alone or concurrent chemoradiation, using a platinum-based combination therapy, is typically chosen. Although preoperative chemoradiotherapy can contribute to the complexity of the surgery, studies have shown improved long-term survival rates observed in patients who underwent sleeve lobectomy even after induction therapy when compared with pneumonectomy [18]. In a multicenter analysis by Cusumano et al. in 2014, the 5-year survival rates following sleeve lobectomy for NSCLC in 51 patients who received induction therapy was 53.8% [5]. Maurizi et al. reported on 82 patients in 2013 who had undergone sleeve lobectomy after induction therapy. There were no post-operative mortalities and no significant differences noted in post-operative complications when compared to those in the sleeve lobectomy patients without induction therapy [19]. Analysis of long-term survival rates according to stage and nodal status has shown that sleeve lobectomy typically results in higher survival rates for stages I and II [18]. There is no known survival benefit of performing a pneumonectomy in patients with N2 disease over a sleeve lobectomy [2].

Operative approach

Although sleeve lobectomy surgery is performed predominantly for right upper lobe lesions, the surgical principles can be applied for any lobar resection. Once it is decided by preoperative cardiopulmonary testing, clinical staging, and preoperative planning that a patient is a reasonable candidate for a sleeve lobectomy, the operative strategy should be carefully thought out. We will typically perform a thorough bronchoscopic evaluation of the airways, followed by an endobronchial ultrasound EBUS-TBNA or mediastinoscopy for N2 nodal assessment, within the same setting as the sleeve lobectomy procedure. Ipsilateral N2 disease may result in the patient being referred for neoadjuvant therapy with reassessment of operability after treatment. N2 disease does not absolutely contraindicate resection. We typically clinically restage after therapy with PET-CT. If there is no evidence of distant disease on subsequent PET-CT, we proceed with lung resection without restaging the mediastinum surgically. If multistation N2 disease is found, patients are given definitive chemoradiation and surgery is not offered. Since our sleeve resection rate in positive N2 disease is quite low, we have not compared outcomes of neoadjuvant vs adjuvant therapy in our institution. However, in 2013, Gonzalez et al. reported no significant differences noted in 90-day mortality and morbidity after sleeve resection for patients treated with and without induction therapy, including patients with N2 disease [20].

Once operability has been confirmed, it is typical to proceed with side-specific double-lumen endotracheal tube intubation for single lung ventilation. We recommend starting each case with a surveillance video-assisted thoracoscopic surgery (VATS) to ensure resectability and no evidence of metastatic disease. A single 5-mm incision made at the seventh or eighth posterior intercostal space facilitates placement of a single port and a 5-mm thoracoscopic camera to carry out an initial examination of the pleural space.

If a three-port VATS approach to sleeve lobectomy is planned thereafter, then the previous incision is extended to accomodate our 10-mm flexible-tip thoracoscope with high-definition picture quality. A second incision is made at the sixth intercostal space as anteriorly as possible, in line with the major fissure, in order to facilitate stapler placement during hilar structure division. Articulating and curved tip staplers can decrease vascular injury in our experience [21]. A 3–4-cm access incision at the midaxillary line is made at the fourth interspace for upper lobectomies and at the fifth interspace for lower lobectomies. A self-retaining wound-protector is typically placed to improve exposure and to decrease trauma to the adjacent tissues during thoracoscopic instrument placement. Mahtabifard et al. discussed the first series of VATS sleeve lobectomy procedures in 2008 in 13 patients. They showed that this procedure, though technically challenging, could be performed through a minimally invasive approach with results corresponding closely to open surgery. Since then, several authors have discussed outcomes of minimally invasive VATS sleeve lobectomy and current surgical approaches have now extended to include robotic sleeve lobectomies [3, 4, 7].

For open-sleeve lobectomies, a standard posterolateral serratus-sparing, at the fourth or fifth intercostal incision is made. The intercostal muscle is harvested as a pedicle and divided anteriorly and set aside for use in bronchial stump coverage later. The use of a vessel-sealing energy device or electrocautery is used to divide the inferior pulmonary ligament, anterior, and posterior mediastinal pleura. Once tumor resectability is confirmed, the hilum is exposed. We recommend careful dissection and control of the main pulmonary artery early on in preparation for pulmonary artery reconstruction as needed. Opening the pericardium can facilitate this dissection when a tumor is obstructing access. The pulmonary artery is encircled with a long vessel loop and an appropriately sized vascular clamp is set aside in anticipation of the need to obtain vascular control during dissection.

After sleeve lobectomy feasibility is determined, the venous and arterial branches are dissected and divided in a routine sequential manner. Frozen section bronchial margin analysis is paramount to sleeve lobectomy operation. In the event of a positive resection margin, additional tissue should be resected until a disease-free bronchial margin is assured. It is important to note that all bronchi should be divided perpendicular to the long axis of the airway. We use a red-rubber catheter to encircle the airways to allow easier passage of the stapling device. Devascularization of the bronchus is avoided in an attempt to minimize post-operative bronchial complications.

If pulmonary artery reconstruction is anticipated, we typically give 5000 U of intravenous heparin prior to clamping the main pulmonary artery. We will also place a vessel loop around the inferior pulmonary vein to minimize backflow during reconstruction. The bronchial anastomosis is completed first to avoid tension on the artery. Primary end-to-end arterial anastomosis can be completed when possible using a 5-0 prolene running suture or subsequent use of a bovine pericardial reconstructive patch. Side-biting vascular clamps can facilitate reconstruction nicely. We do not reverse the heparin and will continue patients on anticoagulation for 30 days if a pulmonary artery reconstruction is performed. As mentioned previously, although right upper lobe sleeve lobectomies are the most commonly performed, sleeve lobectomy with or without pulmonary artery involvement can be performed safely in all the lobes.

Important technical considerations include avoiding tension on the anastomosis and kinking of the pulmonary artery and vein. Lymph node stations should be cleared after completing the lobectomy in an effort to accurately stage the patient. A bronchoscopy is performed prior to chest closure to ensure adequacy of the anastomosis and patency of the reconstructed airway. Below, in (Tables 1, 2, 3, 4, and 5), we review the main operative steps taken for each sleeve lobectomy. With main stem tumors, a complete lung-sparing sleeve resection can be performed in select instances. The appended movie (video 1) demonstrates one such case.

Table 1 The main operative steps taken for right upper lobe sleeve resection
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Table 2 The main operative steps taken for right middle lobe sleeve resection
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Table 3 The main operative steps taken for right middle lobe sleeve resection
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Table 4 The main operative steps taken for left upper lobe sleeve resection
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Table 5 The main operative steps taken for left lower lobe sleeve resection
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(M4V 86048 kb)

Post-operative care

An intra-operative multilevel intercostal nerve block is performed for every thoracic surgery at our institution using liposomal bupivacaine. This has significantly decreased the amount of post-operative pain patients experience and the use of intravenous narcotics has been minimized. Epidural use is infrequent since the implementation of liposomal-based bupivacaine injection. Judicious use of intravenous fluids and diuretics are used in an effort to avoid post-operative pulmonary edema. Routine beta blockers are given in an attempt to minimize arrhythmias. A single chest tube is left in place and typically placed on water seal on the first post-operative day, with removal once any air leak has resolved. Patients are extubated immediately following the surgical procedure and pulmonary hygiene is emphasized. Inhaled mucolytic agents and nebulizers are prescribed routinely along with aggressive incentive spirometry and chest physiotherapy so as to mobilize secretions early in the post-operative course. Bronchoscopy is utilized on an as-needed basis for poor mucocilliary clearance and atelectasis. Patients are ambulatory immediately after surgery and daily physical therapy is standard. Length of stay has been evaluated in several studies. The average length of stay in our institution for an uncomplicated sleeve lobectomy patient is estimated at 5 days.

Potential complications

Potential complications reported after sleeve lobectomy in patients have been reported in many series with morbidities comparable to those noted after pneumonectomy. The most commonly reported complications are listed in Table 6 and include prolonged air leak, arrhythmias, pneumonia, and atelectasis. Sleeve lobectomy and pneumonectomy for patients with N2 and stage III disease was reported by Deslauriers et al. in 2004, indicating that pneumonectomy does not improve survival in patients with a more advanced disease [22]. Induction therapy can be considered in this group. As demonstrated in studies by Maurizi, Bagan, and Milman listed in Table 7, induction therapy has been shown to have no significant impact on procedure-related morbidity or mortality [19, 23, 24].

Table 6 Common morbidities observed with sleeve lobectomy
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Table 7 Morbidity and mortality reported with sleeve lobectomy (SL) following induction therapy
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Recurrence and survival

An important consideration for selecting sleeve resection over pneumonectomy is its safe completion with a potential of achieving at least equivalent oncological results. The studies comparing the locoregional recurrence and 5-year survival of sleeve lobectomy (SL) and pneumonectomy (PN) are shown in Table 8. With the exception of Maurizi et al., all other studies listed include patients with or without neoadjuvant therapy; the former including only the patients who had received neoadjuvant chemotherapy. Merritt et al., in a non-comparative study, reported a 44% overall 5-year survival rate in their NSCLC sleeve lobectomy patient population of 196 patients, and 39.3% in the patients with N1 disease [16]. With only few institutions performing VATS sleeve resections (with or without robot assistance), most of the literature available on this approach is relatively recent with reference to only short-term outcomes.

Table 8 Locoregional recurrence and 5-year survival of sleeve lobectomy (SL) and pneumonectomy (PN)
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Discussion

Despite continued encouraging results, sleeve lobectomy remains significantly underutilized worldwide. It is not always understood as the standard of care for anatomically suitable central airway cancers and pneumonectomy procedures continue to outnumber sleeve lobectomies. The studies comparing sleeve resections and pneumonectomies have shown an improved overall 5-year survival for the sleeves, comparable locoregional recurrence rates, and no increase in morbidity and mortality after induction therapy (Tables 7 and 8). This supports the oncologic validity of sleeve resections. The noted improved overall survival may be due to better cardiopulmonary status post-operatively in the sleeve groups. Owing to thoracic remodeling after pneumonectomy, we also expect lesser chronic pain issues after sleeve resection. With VATS pneumonectomy (with and without robot assistance), we have previously shown significantly more pain-free patients at 1 year compared to open approach [33]. As more literature for the VATS approach becomes available, it would be an interesting comparison of chronic pain between the VATS pneumonectomy vs VATS sleeve resections, in the absence of rib spreading.

With proven oncological equivalence to pneumonectomy and favorable rates of operative mortality, overall morbidity, and local recurrence rates, even after induction therapy and for advanced disease, sleeve lobectomy should be adopted as the preferred surgical option for all patients with central NSCLC [19, 20, 34]. A future prospective, randomized controlled trial comparing sleeve lobectomy to pneumonectomy in the management of the central airway tumors is needed. The results of a trial of this nature might be enough to encourage more surgeons to undertake this technically challenging operation in return for improved patient outcomes.