View of the RLL and RML bronchi after division of the inferior pulmonary vein.
Central Message.
A fissureless approach to right lower lobectomy allows for careful delineation of anatomy and helps avoid air leaks.
Video-assisted thoracoscopic surgery (VATS) is the predominant surgical approach for anatomic lung resection owing to its well-described perioperative benefits and potential long-term survival benefit over thoracotomy.1 However, as the number of incisions, choice of energy device, order of surgical steps, and many other variables are left to the discretion of individual surgeons, there is no standardized surgical technique for this procedure. Herein, we present our approach for VATS right lower lobectomy and mediastinal lymph node dissection.
The patient in Videos 1 through 9 presented with clinical T2b N2 M0 squamous cell carcinoma in 2020. Positron emission tomography (PET) showed a 5-cm hypermetabolic right lower lobe (RLL) mass with an additional PET-avid right paratracheal focus. Fine-needle aspiration using endobronchial ultrasound was nondiagnostic at the 4R station, but biopsy of the subcarinal lymph nodes was positive for metastatic squamous cell carcinoma. No distant metastases were seen on PET or magnetic resonance imaging of the brain. The patient therefore underwent induction chemotherapy with carboplatin and gemcitabine for 4 cycles, which was well tolerated. Restaging imaging showed a partial response to chemotherapy, and the patient underwent surgical resection as planned. As shown in Videos 1 through 9, this patient was found to have a substantial amount of inflammation and fibrosis surrounding the mediastinal lymph nodes, which is typical of resections after neoadjuvant therapy. The technique shown in these videos is designed to be reproducible and can be consistently applied to any RLL resection, regardless of completeness of fissure or prior induction therapy. The Memorial Sloan Kettering Cancer Center Institutional Review Board approved the submission because this does not constitute human subjects research and the project does not involve identifiable patient information (IRB #16-1631, October 27, 2020). The patient gave informed written consent for the publication of the study data.
Port Placement and Operative Steps
The initial camera port was placed in the eighth interspace in the posterior axillary line using a 5-mm trocar. Carbon dioxide insufflation to 8 mm Hg was used initially to induce atelectasis of the right lung. The hemithorax was inspected for adhesions, pleural implants, and other unexpected findings. A 3- to 4-cm access incision was then made in the fourth interspace overlying the anterior axillary line, and a small wound protector (Applied Medical) was placed to retract the soft tissues overlying the incision. Carbon dioxide insufflation was stopped at this point. A 1.5-cm assistant incision was made posteriorly just inferior to the scapular edge.
Step 1: Division of the Inferior Pulmonary Ligament and Level-9 Lymph Node Dissection
It is our practice to start all anatomic lung resections from a posterior approach. The lung was lifted cephalad and anterior using an atraumatic lung grasper from the anterior access incision, and an extended-tip Bovie cautery was used to open the inferior pulmonary ligament from the posterior port (Video 1, Figure 1). Any level-9 lymph nodes encountered were removed and sent for pathologic analysis.
Figure 1.
The right lower lobe (RLL) is retracted superiorly and the inferior pulmonary ligament is divided.
Step 2: Opening of the Posterior Pleura and Subcarinal Lymph Node Dissection
The lung was retracted anteriorly, and this line of prior dissection was extended cephalad up to the level of the carina (Video 2, Figure 2). After the pleura was opened, the bronchus intermedius (BI) was identified by visual inspection. A plane was then developed on the pericardium just cephalad to the superior border of the inferior pulmonary vein. This dissection was continued superiorly to elevate the level-7 lymph node packet. A plane was then developed between the en bloc lymph nodes and the BI, and finally the lymph node packet was separated from the carina and the esophagus. Bronchial vessels were clipped or controlled with electrocautery. This dissection can be challenging in patients with granulomatous disease, metastases to the lymph nodes, or prior induction therapy. In the case presented here, treatment effect from the involved level-7 lymph node made the dissection particularly tedious. Care was taken to use very limited energy around the carina and left mainstem bronchus to avoid inadvertent injury to the membranous airway. In difficult dissections, bipolar electrocautery, such as a Ligasure device (Medtronic), can be used to ensure that tributary lymphatics and remaining bronchial vessels are completely sealed. At the conclusion of this dissection, the left and right mainstem bronchi, carina, and pericardium were free of tissue.
Figure 2.
The subcarinal lymph node packet is excised; the borders of this dissection are the bronchus intermedius, carina, left mainstem bronchus (not shown) and pericaridium.
Step 3: Removal of the 11R “Sump” Lymph Node Between the Right Upper Lobe Bronchus and the BI
The pleura was then opened overlying the lateral edge of the BI to expose the 11R lymph node that lies between the right upper lobe (RUL) bronchus and the BI (Video 3, Figure 3). This lymph node is of oncologic significance in that it collects lymphatic drainage from each right-sided pulmonary lobe. Removal of this lymph node also creates a window from the posterior hilum into the fissure, which facilitates completion of the posterior fissure at a later point in the operation. The posterior ascending pulmonary artery branch (A2) to the RUL and the arterial branch to the superior segment of the lower lobe (A6) lie deep to these lymph nodes and were exposed upon completion of the dissection.
Figure 3.
After removal of the 11R “sump” lymph node, the A2 branch to the upper lobe can be seen. RUL, Right upper lobe; A2, posterior ascending pulmonary artery branch; A6, superior segment of the lower lobe.
Step 4: Identification and Division of the Inferior Pulmonary Vein
The lung was atraumatically retracted cephalad to expose the inferior pulmonary vein and anterior hilum of the lung (Video 4, Figure 4). With care taken to avoid the phrenic nerve, which runs just anterior to this plane of dissection, the remaining pleura overlying the vein was divided and a window around the vein was created to allow passage of a curved-tip vascular load stapler.
Figure 4.
The inferior pulmonary vein is encircled and divided. RLL, Right lower lobe.
Step 5: Identification of the Right Middle Lobe and RLL Bronchus and Removal of the Peribronchial Lymph Nodes
With lung retraction maintained superiorly, the lung parenchyma was swept up into the specimen to expose the RLL and right middle lobe (RML) bronchi (Video 5, Figure 5). This dissection is facilitated by keeping the RLL retracted superiorly and laterally toward the highest point of the chest wall so that the RLL bronchus can be easily identified in a vertical position and the RML bronchus can be seen inferiorly at an oblique angle. At the bifurcation of these structures, the 12R peribronchial lymph nodes were encountered and removed. If the dissection is difficult, as seen in these videos, the lymph nodes may be simply elevated from the bronchus at this point, to circumferentially dissect the bronchus, and then removed after transection of the bronchus. The basilar pulmonary artery lies immediately deep to this dissection but was not directly visualized at this point in the dissection.
Figure 5.
Peribronchial lymph nodes are elevated from the bifurcation of the right middle lobe (RML) and right lower lobe (RLL) bronchi.
Step 6: Isolation and Division of the RLL Bronchus
Retraction of the lung was shifted anteriorly to expose the superior aspect of the RLL bronchus (Video 6, Figure 6). The RLL pulmonary artery can clearly be seen in this video, directly deep to the RLL bronchus. The bronchus was elevated from the underlying pulmonary artery, and any 12R lymph nodes that were encountered were removed. Dissection proceeds in this manner until the RLL bronchus can be encircled and divided using a surgical stapler. If there is any doubt regarding the patency of the RML bronchus after clamping the presumed RLL bronchus, gentle inflation of the right lung can be performed by anesthesia to confirm that the RML is still easily ventilated after clamping of the RLL bronchus. This step is not shown in this video.
Figure 6.
The right lower lobe (RLL) bronchus is encircled after division of the inferior pulmonary vein, sparing the right middle lobe (RML) bronchus.
Step 7: Identification of the RML Pulmonary Artery and Division of the RLL Pulmonary Artery
Division of the RLL bronchus exposes the underlying pulmonary artery, which is now the only remaining hilar structure to the RLL (Video 7, Figure 7). An 11R lymph node is commonly encountered at the branch point of the RML pulmonary artery and ongoing basilar pulmonary artery, which is removed to facilitate this dissection and expose the underlying RML pulmonary artery branch(es). The RML bronchus comprises the deep or inferior border of this dissection. After removal of these lymph nodes, the RML artery should be clearly visible and protected throughout the remainder of the resection. The RLL pulmonary artery was then encircled and divided using a vascular staple load. Of note, the basilar pulmonary artery and A6 superior segmental pulmonary artery branch can be divided separately if needed (not shown). Care was taken to preserve the A2 and V2 posterior ascending branches to the upper lobe.
Figure 7.
After division of the right lower lobe (RLL) bronchus, the RLL pulmonary artery (PA) is exposed. A2, Posterior ascending pulmonary artery branch; RML, right middle lobe.
Step 8: Parenchymal Division
The lung was then rotated back into its native position and elevated off the divided hilar structures (Video 8, Figure 8). A line of parenchymal division was created along the oblique fissure, ensuring that all divided hilar structures of the RLL were taken as part of the specimen. Sequential fires of purple load staplers were used until the lobectomy was completed; the specimen was then removed using a specimen bag.
Figure 8.
The parenchymal fissure is divided. RLL, Right lower lobe; RML, right middle lobe.
Step 9: Paratracheal Lymph Node Dissection
The RUL was retracted inferiorly to expose the paratracheal space (Video 9, Figure 9). The pleura was incised along the inferior border of the azygos vein to expose the level 4R and 2R lymph nodes. These are elevated from the proximal right pulmonary artery and the underside of the azygos vein. The triangular space bounded by the trachea, the superior vena cava, the right main pulmonary artery, and the pericardium was cleared of all nodal tissue. We rarely divide the azygous vein to perform this dissection.
Figure 9.
The paratracheal lymph node packet is excised; the borders of this dissection are the superior vena cava (SVC), trachea, and pericardium.
Upon completion of these steps, the chest was inspected for hemostasis, and a leak test was performed. For postoperative analgesia, dilute (0.5%) bupivacaine was injected into the intercostal spaces using a mediastinal needle. A posteroapical chest tube was placed, and the lung was reinflated under direct visualization.
Discussion
Surgical pathology from the patient presented here showed completely resected ypT1c N2a squamous cell carcinoma with a small focus of adenocarcinoma. There was residual disease, with extranodal extension in the subcarinal lymph nodes, for which the patient underwent postoperative radiation therapy after an uncomplicated surgical course. The patient is disease-free at 2 years.
Advanced-stage lung cancer and prior induction therapy were previously considered contraindications to VATS resection. However, recent data have shown that, although VATS resections in this setting are associated with higher rates of conversion to thoracotomy, induction therapy is not associated with higher mortality and node-positive disease is not associated with higher morbidity or mortality.2,3 Furthermore, there is no difference in 5-year disease-free survival between patients with node-positive disease undergoing VATS resection after traditional cytotoxic induction therapy and those undergoing thoracotomy.4 Perioperative results are now available from a number of Phase 2 neoadjuvant immunotherapy trials, as well as the Phase 3 CheckMate 816 trial, showing the feasibility of a minimally invasive surgical approach after modern induction therapies (Table 1).5, 6, 7, 8 Thoracoscopic approaches have also been successfully used after neoadjuvant tyrosine kinase inhibitors.9
Table 1.
Selected Phase 2 and 3 neoadjuvant immunotherapy trials and relevant data showing the feasibility of thoracoscopic resection
| First author | No. of patients | Disease stage | Preoperative therapy | Thoracoscopic resection | Thoracoscopic resection converted to thoracotomy | R0 resection | Major pathologic response |
|---|---|---|---|---|---|---|---|
| Bott and colleagues5 | 22 | I-IIIA | 2 cycles of nivolumab | 6/20 (30) | 7/20 (35) | NR | 9/20 (45) |
| Lee and colleagues6 | 181 | IB-IIIB | 2 cycles of atezolizumab | 86/159 (54) | 15/159 (9) | 145/159 (91) | 30/147 (20)∗ |
| Tong and colleagues7 | 30 | IB-IIIA | 2 cycles of pembrolizumab | 18/25 (72) | 5/25 (20) | 22/25 (88) | 7/25 (24) |
| Forde and colleagues8 | 358 | IB-IIIA | 3 cycles of nivolumab + platinum doublet chemotherapy | 44/149 (30) | 17/149 (11%) | 124/149 (83) | 37% |
| 3 cycles of platinum doublet chemotherapy | 29/149 (22) | 21/149 (16) | 105/149 (78) | 9% |
Values are presented as n/N (%). NR, Not reported.
Patients without EGFR or ALK alterations.
Nonetheless, thoracoscopic lobectomy after induction therapy for advanced lung cancer is often technically difficult. This is secondary to frequent inflammatory adhesions formed as part of the treatment response, with resultant edema and fibrosis. In cases of node-positive tumors, this treatment effect can be significant during the nodal and hilar dissections, resulting in loss of tissue planes and difficulty in identifying structures. Care must be taken during lymphadenectomy to protect surrounding structures, such as the membranous airways and carina, which are in close proximity to the level-7 lymph node dissection. In all cases, we meticulously dissect and remove all encountered N1 lymph nodes, not only for thorough staging but also to better define anatomy, allow safe passage of staplers, and facilitate subsequent dissection. This step is particularly important in cases such as this in which the anatomy is difficult or obscured. Precise identification of anatomy, the use of bipolar dissection for effective control of lymphatic and small vascular tributaries, and a fissureless approach to increase reproducibility and minimize air leaks10 are all strategies shown here to facilitate these difficult dissections.
The technique for fissureless VATS right lower lobectomy we describe here can be applied routinely. By following the steps outlined in Videos 1 through 9, this technique can be safely applied even to patients with difficult anatomy, incomplete fissures, and loss of hilar definition due to tumor distortion or neoadjuvant therapy.
Footnotes
Supported by the National Institutes of Health/National Cancer Institute (grant No. P30 CA008748).
Disclosures: The authors reported no conflicts of interest.
The Journal policy requires editors and reviewers to disclose conflicts of interest and to decline handling or reviewing manuscripts for which they may have a conflict of interest. The editors and reviewers of this article have no conflicts of interest.
Supplementary Data
Division of the inferior pulmonary ligament and level 9 lymph node dissection. Video available at: https://www.jtcvs.org/article/S2666-2507(23)00045-7/fulltext.
Opening of the posterior pleura and subcarinal lymph node dissection. Video available at: https://www.jtcvs.org/article/S2666-2507(23)00045-7/fulltext.
Removal of the 11R “sump” lymph node between the right upper lobe bronchus and the bronchus intermedius. Video available at: https://www.jtcvs.org/article/S2666-2507(23)00045-7/fulltext.
Identification and division of the inferior pulmonary vein. Video available at: https://www.jtcvs.org/article/S2666-2507(23)00045-7/fulltext.
Identification of the right middle lobe and right lower lobe bronchus and removal of the peribronchial lymph nodes. Video available at: https://www.jtcvs.org/article/S2666-2507(23)00045-7/fulltext.
Isolation and division of the right lower lobe bronchus. Video available at: https://www.jtcvs.org/article/S2666-2507(23)00045-7/fulltext.
Identification of the right middle lobe pulmonary artery and division of the RLL pulmonary artery. Video available at: https://www.jtcvs.org/article/S2666-2507(23)00045-7/fulltext.
Parenchymal division. Video available at: https://www.jtcvs.org/article/S2666-2507(23)00045-7/fulltext.
Paratracheal lymph node dissection. Video available at: https://www.jtcvs.org/article/S2666-2507(23)00045-7/fulltext.
References
- 1.Taioli E., Lee D.-S., Lesser M., Flores R. Long-term survival in video-assisted thoracoscopic lobectomy vs open lobectomy in lung-cancer patients: a meta-analysis. Eur J Cardio Thorac Surg. 2013;44:591–597. doi: 10.1093/ejcts/ezt051. [DOI] [PubMed] [Google Scholar]
- 2.Yang C.-F.J., Meyerhoff R.R., Mayne N.R., Singhapricha T., Toomey C.B., Speicher P.J., et al. Long-term survival following open versus thoracoscopic lobectomy after preoperative chemotherapy for non-small cell lung cancer. Eur J Cardio Thorac Surg. 2016;49:1615–1623. doi: 10.1093/ejcts/ezv428. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.Villamizar N.R., Darrabie M., Hanna J., Onaitis M.W., Tong B.C., D'Amico T.A., et al. Impact of T status and N status on perioperative outcomes after thoracoscopic lobectomy for lung cancer. J Thorac Cardiovasc Surg. 2013;145:514–520. doi: 10.1016/j.jtcvs.2012.10.039. discussion 520. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Kamel M.K., Nasar A., Stiles B.M., Altorki N.K., Port J.L. Video-assisted thoracoscopic lobectomy is the preferred approach following induction chemotherapy. J Laparoendosc Adv Surg Tech. 2017;27:495–500. doi: 10.1089/lap.2016.0540. [DOI] [PubMed] [Google Scholar]
- 5.Bott M.J., Yang S.C., Park B.J., Adusumilli P.A., Rusch V.W., Isbell J.M., et al. Initial results of pulmonary resection after neoadjuvant nivolumab in patients with resectable non-small cell lung cancer. J Thorac Cardiovasc Surg. 2019;158:269–276. doi: 10.1016/j.jtcvs.2018.11.124. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6.Lee J., Chaft J., Nicholas A., Patterson A., Waqar S. PS01.05 Surgical and clinical outcomes with neoadjuvant atezolizumab in resectable stage IB–IIIB NSCLC: LCMC3 trial primary analysis. J Thorac Oncol. 2021;16:S59–S61. [Google Scholar]
- 7.Tong B.C., Gu L., Wang X., Wigle D.A., Philips J.D., Harpole D.H., Jr., et al. Perioperative outcomes of pulmonary resection after neoadjuvant pembrolizumab in patients with non-small cell lung cancer. J Thorac Cardiovasc Surg. 2022;163:427–436. doi: 10.1016/j.jtcvs.2021.02.099. [DOI] [PubMed] [Google Scholar]
- 8.Forde P.M., Spicer J., Lu S., Provencio M., Mitsudomi T., Awad M.M., et al. Neoadjuvant nivolumab plus chemotherapy in resectable lung cancer. N Engl J Med. 2022;386:1973–1985. doi: 10.1056/NEJMoa2202170. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.Chudgar N.P., Jones D.R. Thoracoscopic lobectomy following neoadjuvant tyrosine kinase inhibitor treatment. J Thorac Cardiovasc Surg Tech. 2021;7:294–297. doi: 10.1016/j.xjtc.2021.02.005. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Li S.-J., Zhou K., Li Y.-J., Li P.-F., Wu Y.-M., Liu L.-X., et al. Efficacy of the fissureless technique on decreasing the incidence of prolonged air leak after pulmonary lobectomy: a systematic review and meta-analysis. Int J Surg. 2017;42:1–10. doi: 10.1016/j.ijsu.2017.04.016. [DOI] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Supplementary Materials
Division of the inferior pulmonary ligament and level 9 lymph node dissection. Video available at: https://www.jtcvs.org/article/S2666-2507(23)00045-7/fulltext.
Opening of the posterior pleura and subcarinal lymph node dissection. Video available at: https://www.jtcvs.org/article/S2666-2507(23)00045-7/fulltext.
Removal of the 11R “sump” lymph node between the right upper lobe bronchus and the bronchus intermedius. Video available at: https://www.jtcvs.org/article/S2666-2507(23)00045-7/fulltext.
Identification and division of the inferior pulmonary vein. Video available at: https://www.jtcvs.org/article/S2666-2507(23)00045-7/fulltext.
Identification of the right middle lobe and right lower lobe bronchus and removal of the peribronchial lymph nodes. Video available at: https://www.jtcvs.org/article/S2666-2507(23)00045-7/fulltext.
Isolation and division of the right lower lobe bronchus. Video available at: https://www.jtcvs.org/article/S2666-2507(23)00045-7/fulltext.
Identification of the right middle lobe pulmonary artery and division of the RLL pulmonary artery. Video available at: https://www.jtcvs.org/article/S2666-2507(23)00045-7/fulltext.
Parenchymal division. Video available at: https://www.jtcvs.org/article/S2666-2507(23)00045-7/fulltext.
Paratracheal lymph node dissection. Video available at: https://www.jtcvs.org/article/S2666-2507(23)00045-7/fulltext.