Superiorities of robotic segmentectomy: a review

Lung cancer is the leading cause of cancer death in the United States (1,2). With the introduction of low-dose computed tomography (LDCT) for lung cancer screening, an expected two-thirds of all lung cancers in this screening population will be detected in their early-stage, hence will be surgically resectable (3). Pulmonary segmentectomy offers a lung preserving alternative for early-stage lung cancer resection especially for patients with emphysema.

Churchill and Belsey first introduced pulmonary segmental resection in 1939 for the surgical management of bronchiectasis (4). In 1973, Jensik and Faber endorsed segmentectomy to achieve parenchymal preservation for the management of recurrent lung cancer. Oncologic outcomes demonstrated a 56% 5-year survival rate with a rate of local recurrence of 10% following segmentectomy for T1 cancers (5). The North American Lung Cancer Group later found three times the local recurrence rate and 30% increased mortality compared to lobectomy (6). These findings firmly endorsed lobectomy as the continued standard of care and prevented acceptance of the sublobar approach to early NSCLC at that time.

Since then an increased number of reports have demonstrated equivalent outcomes. In 2002, Yoshikawa et al. showed improving survival rates for segmentectomy in smaller tumors, with 82% 5-year survival rate for tumors less than 2 cm (7). Additionally, in 2014 Okada et al. showed equivalent 5-year disease-free survival when comparing lobectomy and segmentectomy (8). Functional preservation was found to be superior with segmentectomy compared with lobectomy with the extent of parenchymal resection directly proportional to postoperative functional loss persisting up to 6 months postoperatively. Furthermore, in their prospective trial, the Cancer and Lymphoma Group B (CALGB 140503) demonstrated equal rates of survival and recurrence for patients with small peripheral NSCLC undergoing segmentectomy compared to lobectomy (9). Other studies additionally supported the feasibility and safety of segmentectomy (10-12). In 2010, Schuchert et al. showed equivalent recurrence rates and overall survival between techniques, specifically for stage 1 NSCLC (13). This would later be endorsed by multiple retrospective studies showing equivalent recurrence and survival in patients undergoing open segmentectomy vs. lobectomy who were 75 years or older, had large tumors and even patients with poor pulmonary reserve and associated comorbid conditions (14-17). Some studies have even demonstrated superior outcomes with segmentectomy (18-20). This data has allowed segmentectomy to become a reasonable alternative, with no compromise to oncologic survival while preserving lung parenchyma especially in older patients with small, stage I lung tumors who may not tolerate a lobectomy due to reduced pulmonary function (17,21).

The open thoracotomy approach to lung cancer resection has been challenged by the growing utility and enthusiasm for less invasive techniques first by video-assisted thoracoscopic (VATS) resection and, more recently, robotically assisted approaches (22,23). There is substantial evidence that minimally invasive techniques in the treatment of NSCLC results in superior perioperative results. Several reports have identified a reduction in pain, lower respiratory tract infections, arrhythmias, length of stay (LOS), and inflammatory markers (19-20). This has fueled the shift to a less invasive approach to resections and further studies have shown similar rates of locoregional recurrence, cancer-free survival, as well improved overall morbidity and mortality (22,24-26). A minimally invasive sublobar resection allows anatomic resection with acceptable margins while concurrently preserving lung function (22).

Comparing thoracoscopic segmentectomy to the open technique was first performed by Shiraishi et al. in 2004 with no significant difference in complications or perioperative deaths (27) and comparable rate of recurrence, survival, and operative time. Thoracoscopic segmentectomy resulted in reduction of hospital LOS, cost reduction and decreased rates of cardiopulmonary complications (21,28-30).

In the last two decades, the robotic approach has been introduced for a variety of thoracic procedures including lobectomy and segmentectomy. Review of national data have demonstrated increased robotic lung resections by 3.2% between the years 2008 and 2010 (17,31). The robotic approach affords superior visualization in the setting of three-dimensional optics and higher instrument precision with seven degrees of motion. The DaVinci system (Intuitive, Sunnyvale, CA, USA) results in improved dexterity, tremor filtration, and telesurgery (32). This is particularly useful during anatomical pulmonary segmentectomy which requires meticulous intraparenchymal dissection to expose the segmental bronchus and vessels. The robotic approach is also advantageous due to ability to perform dissection sharply using bipolar energy rather than blunt dissection carried out during the VATS approach.

Farivar et al. studied all robotic anatomic lung resections from two institutions between 2010 to 2012 (n=181) matched against the same variables for resections via thoracotomy (n=5,913) and VATS (n=4,612) from the STS National Database (33). Their results showed reduced 30-day mortality and perioperative rates of blood transfusion. Hospital LOS was also cut by 2 days vs. VATS and 4 days vs. thoracotomy (33). A review of the National Cancer Database between 2010 to 2015 found the robotic approach to be associated with significantly decreased conversion rates to open compared to VATS (9% vs. 14%) (34). These data further support the robotic approach in achieving comparable survival and reduction in length of hospital stay resulting in earlier return to work.

Many comparative studies have formally compared the two techniques particularly because of the increased resources necessary in the inception of a robotic surgery program and have demonstrated increased cost in establishing a robotic cancer surgery practice (33,35-37). One propensity matched analysis by Bao et al. in China noted increased cost and operative time with robotic pulmonary resection compared to thoracoscopic (38). Robotic approach was also noted to be more costly in a retrospective review of 2,868 patients undergoing VATS versus robotic lobectomy (39).

However, after these initial start-up costs, results by Musgrove et al. contradict the statement that robotic segmentectomy is more expensive than VATS approach. They compared their early robotic segmentectomy experience with VATS segmentectomy in their single institution retrospective analysis (40). The robotic group achieved a shorter length of hospital stay (2 vs. 4 days) and reduction in both air leaks (7% vs. 18%) and overall complications (14% vs. 36%) (40). Cost analysis was calculated by taking into account the cost of hospital stay per day and intraoperative instrument and resource allocation. This translated to cost savings in the robotic cohort compared to the VATS cohort (40). Although statistical significance was not reached (likely due to the small cohort size), these data suggest that robotic surgery for lung cancer would not certainly result in increased cost or result in poor outcomes. Similarly, Nelson et al. found similar cost between robotic and VATS lobectomy (41). Kneuertz et al. also found similar cost between robotic and VATS approach to lobectomy between 2012 and 2017 with increased procedural costs compared to open compensated by decreased LOS and improved post-operative outcomes (42).

Nasir et al. performed a retrospective review from 2010 to 2013 of 862 robotic lobectomies and segmentectomies and found that despite a median hospital charge of $32,000, the hospital profited $4,750 per patient. Most results were favorable including minimal morbidity and mortality, and reduced postoperative pain. Notably, the authors did find increased capital costs and number of robotic cases required to achieve expertise as downsides of robotic segmentectomy (43). Based on the variation in cost analysis within published literature, prospective studies are needed to accurately discern accurate cost and physician reimbursement associated with setting up and running a thoracic surgery robotic program.

In addition to cost, robotic approach to pulmonary resection does have an important learning curve that must be mastered which includes overcoming the lack of tactile feedback compared to VATS. Glenn et al. retrospectively reviewed 2,868 patients between 2010 to 2013 using the National Inpatient Sample (39). Whereas overall morbidity was similar, they noted an increased rate of accidental lung puncture or laceration as well as bleeding complications (39). Some studies also note increased operative time with robotic approach, however these limitations improve with surgeon experience and mastery of the learning curve (41,44).

Our experience in comparing 87 consecutive robotic lobectomies with 72 robotic segmentectomies demonstrated reduction in hospital LOS by 1-day (2 vs. 3 days) contradicting belief that segmentectomy is associated with increased air leak and longer LOS compared to lobectomy. Robotic surgery will likely continue to maintain superiority compared to VATS due to the greater precision of intraparenchymal dissection. This likely allows decreased air leak complications and LOS. Other studies have shown similar results. Dylewski et al. reported outcomes of 35 patients undergoing robotic thoracoscopic segmentectomy and reported mean operative time of 146 minutes, median lymph node harvest of 5, and zero 60-day mortality (45). Similarly, Pardolesi et al. reported outcomes of their initial experience on 17 patients demonstrating a mean operative time of 189 minutes, zero post-operative mortality, and no major intraoperative complications or conversions (46).

Liang et al., performed a meta-analysis analyzing outcomes of 7,438 patients undergoing robotic lobectomy and segmentectomy compared with video-assisted lobectomy and segmentectomy. The meta-analysis showed decreased mortality, decreased conversion to open, and increased completion of the planned segmentectomy in the robotic approach (47). There were similar postoperative complications, operative time, duration of hospitalization, and chest tube duration (47). Another meta-analysis by O’Sullivan et al. showed robotic lobectomy compared to VATS and open approaches had decreased 30-day mortality, overall complications, and duration of hospital stay (44).

Cerfolio and colleagues piloted the largest series to date evaluating outcomes after robotic segmentectomies. They reported no conversions to thoracotomy and zero mortality. Between 2010 and 2014, 100 patients underwent robotic segmentectomy with only 7 patients converting to lobectomy, median lymph node harvest of 19, median operative time 88 minutes, median LOS 3 days, and 3.4% recurrence rate with follow up of 2.5 years (48). Using the Society of Thoracic Surgeons General Thoracic Database (STS-GTS), Louie and colleagues demonstrated comparable morbidity and survival despite the fact that the majority of the patients undergoing robotic resection were older with poor functional status compared to patients undergoing VATS (49).

Robotic approach has also been shown in multiple studies to have similar to increased median number of lymph nodes harvested. A retrospective analysis in China of 1,075 patients undergoing robotic versus VATS lobectomies between 2013 to 2016 was performed. They noted increased retrieval of lymph nodes (9.7 vs. 8.4) and a decrease in duration of chest tube drainage (50). In 2017, Xie et al. compared 166 patients undergoing robotic versus VATS segmentectomy and found that in the robotic approach had statistically significant increased average of 13 vs. 10.8 lymph nodes removed (51). Kneuertz et al. retrospectively analyzed 1,053 patients between 2011 to 2018 undergoing robotic versus VATS or open lobectomy. They found similar number of lymph nodes removed however an increased number of stations for open and robotic approaches with similar rates of nodal upstaging in the robotic approach (42). Nelson et al. also noted robotic approach to lobectomy was associated with decreased blood loss, decreased LOS, and improved nodal harvest (41).

In summary, robotic segmentectomy allows superior precision during intraparenchymal dissection resulting in a decreased rate of air leaks and hospital LOS. The increased lymph node harvest, increased completion of the planned segmentectomy, decreased likelihood of conversion to open, and improved dexterity proffered by this technique are well documented advantages of robotic segmentectomy. Adoption of robotic segmentectomy within the thoracic surgery community will likely continue to grow given its demonstrated utility in older debilitated patients and its ability to achieve equivalent outcomes. These advantages will likely offset the greater resource allocation required for the inception of a robotic program. The authors acknowledge that further analysis and larger prospective studies are needed to validate these findings.

Acknowledgments

Funding: None.

Footnote

Provenance and Peer Review: This article was commissioned by the editorial office, Video-Assisted Thoracic Surgery for the series “Robotic Segmentectomies”. The article has undergone external peer review.

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at http://dx.doi.org/10.21037/vats-20-20). The series “Robotic Segmentectomies” was commissioned by the editorial office without any funding or sponsorship. AT served as the unpaid Guest Editor of the series and serves as an unpaid editorial board member of Video-Assisted Thoracic Surgery from Jun 2019 to May 2021. The authors have no other 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.

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/.

References

1. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2012. CA Cancer J Clin 2012;62:10-29. [Crossref] [PubMed]
2. National Cancer Institute. Cancer Stat Facts: Common Cancer Sites. 2018. Available online: https://seer.cancer.gov/statfacts/html//common.html
3. De Koning H, Van Der Aalst C, Ten Haaf K, et al. PL02.05 Effects of volume CT lung cancer screening: mortality results of the NELSON randomised-controlled population based trial. J Thorac Oncol 2018;13:S185. [Crossref]
4. Churchill ED, Belsey R. Segmental pneumonectomy in bronchiectasis: the lingula segment of the upper lobe. Ann Surg 1939;109:481-99. [Crossref] [PubMed]
5. Jensik RJ, Faber LP, Kittle CF, et al. Survival following resection for second primary bronchogenic carcinoma. J Thorac Cardiovasc Surg 1981;82:658-68. [Crossref] [PubMed]
6. Ginsberg RJ, Rubinstein LV. Randomized trial of lobectomy versus limited resection for T1 N0 non-small cell lung cancer. Lung Cancer Study Group. Ann Thorac Surg 1995;60:615-22; discussion 622-3. [Crossref] [PubMed]
7. Yoshikawa K, Tsubota N, Kodama K, et al. Prospective study of extended segmentectomy for small lung tumors: the final report. Ann Thorac Surg 2002;73:1055-8; discussion 1058-9. [Crossref] [PubMed]
8. Okada M, Mimae T, Tsutani Y, et al. Segmentectomy versus lobectomy for clinical stage IA lung adenocarcinoma. Ann Cardiothorac Surg 2014;3:153-9. [PubMed]
9. Mitchell KG, Antonoff MB. Encouraging early outcomes in cancer and leukemia group B (CALGB)/Alliance 140503: patient selection, not extent of resection, is the key to perioperative success. Ann Transl Med 2019;7:S50. [Crossref] [PubMed]
10. Cao C, Gupta S, Chandrakumar D, et al. Meta-analysis of intentional sublobar resections versus lobectomy for early stage non-small cell lung cancer. Ann Cardiothorac Surg 2014;3:134-41. [PubMed]
11. Cao C, Chandrakumar D, Gupta S, et al. Could less be more?-A systematic review and meta-analysis of sublobar resections versus lobectomy for non-small cell lung cancer according to patient selection. Lung Cancer 2015;89:121-32. [Crossref] [PubMed]
12. Yang F, Sui X, Chen X, et al. Sublobar resection versus lobectomy in surgical treatment of elderly patients with early-stage non-small cell lung cancer (STEPS): Study protocol for a randomized controlled trial. Trials 2016;17:191. [Crossref] [PubMed]
13. Schuchert MJ, Abbas G, Pennathur A, et al. Sublobar resection for early-stage lung cancer. Semin Thorac Cardiovasc Surg 2010;22:22-31. [Crossref] [PubMed]
14. Carr SR, Schuchert MJ, Pennathur A, et al. Impact of tumor size on outcomes after anatomic lung resection for stage 1A non-small cell lung cancer based on the current staging system. J Thorac Cardiovasc Surg 2012;143:390-7. [Crossref] [PubMed]
15. Kilic A, Schuchert MJ, Pettiford BL, et al. Anatomic segmentectomy for stage 1 non-small cell lung cancer in the elderly. Ann Thorac Surg 2009;87:1662-6. [Crossref] [PubMed]
16. Nomori H, Mori T, Ikeda K, et al. Segmentectomy for selected cT1N0M0 non-small cell lung cancer: a prospective study at a single institute. J Thorac Cardiovasc Surg 2012;144:87-93. [Crossref] [PubMed]
17. Yang CF, D'Amico TA. Open, thoracoscopic and robotic segmentectomy for lung cancer. Ann Cardiothorac Surg 2014;3:142-52. [PubMed]
18. Landreneau RJ, Normolle DP, Christie NA, et al. Recurrence and survival outcomes after anatomic segmentectomy versus lobectomy for clinical stage I non-small-cell lung cancer: a propensity-matched analysis. J Clin Oncol 2014;32:2449-55. [Crossref] [PubMed]
19. Pennathur A, Abbas G, Christie N, et al. Video assisted thoracoscopic surgery and lobectomy, sublobar resection, radiofrequency ablation, and stereotactic radiosurgery: Advances and controversies in the management of early stage non-small cell lung cancer. Curr Opin Pulm Med 2007;13:267-70. [Crossref] [PubMed]
20. Wei B, Eldaif SM, Cerfolio RJ. Robotic lung resection for non-small cell lung cancer. Surg Oncol Clin N Am 2016;25:515-31. [Crossref] [PubMed]
21. Yang CF, D’Amico TA. Thoracoscopic segmentectomy for lung cancer. Ann Thorac Surg 2012;94:668-81. [Crossref] [PubMed]
22. Cheng AM, Wood DE. Minimally invasive resection of early lung cancers. Oncology (Williston Park) 2015;29:160-6. [PubMed]
23. Park BJ, Heerdt PM. Minimally invasive surgical techniques in the treatment of lung cancer. Minerva Chir 2009;64:573-88. [PubMed]
24. Sullivan R, Alatise OI, Anderson BO, et al. Global cancer surgery: Delivering safe, affordable, and timely cancer surgery. Lancet Oncol 2015;16:1193-224. [Crossref] [PubMed]
25. Whitson BA, Groth SS, Duval SJ, et al. Surgery for early-stage non-small cell lung cancer: a systematic review of the video-assisted thoracoscopic surgery versus thoracotomy approaches to lobectomy. Ann Thorac Surg 2008;86:2008-16; discussion 2016-8.
26. Park BJ, Melfi F, Mussi A, et al. Robotic lobectomy for non-small cell lung cancer (NSCLC): Long-term oncologic results. J Thorac Cardiovasc Surg 2012;143:383-9. [Crossref] [PubMed]
27. Shiraishi T, Shirakusa T, Iwasaki A, et al. Video-assisted thoracoscopic surgery (VATS) segmentectomy for small peripheral lung cancer tumors: intermediate results. Surg Endosc 2004;18:1657-62. [PubMed]
28. Atkins BZ, Harpole DH Jr, Mangum JH, et al. Pulmonary segmentectomy by thoracotomy or thoracoscopy: reduced hospital length of stay with a minimally-invasive approach. Ann Thorac Surg 2007;84:1107-12. [Crossref] [PubMed]
29. Schuchert MJ, Pettiford BL, Pennathur A, et al. Anatomic segmentectomy for stage I non-small-cell lung cancer: comparison of video-assisted thoracic surgery versus open approach. J Thorac Cardiovasc Surg 2009;138:1318-25.e1. [Crossref] [PubMed]
30. Leshnower BG, Miller DL, Fernandez FG, et al. Video-assisted thoracoscopic surgery segmentectomy: a safe and effective procedure. Ann Thorac Surg 2010;89:1571-6. [Crossref] [PubMed]
31. Kent M, Wang T, Whyte R, et al. Open, video-assisted thoracic surger, and robotic lobectomy: review of a national database. Ann Thorac Surg. 2014;97:236-42. [Crossref] [PubMed]
32. Wei B, D'Amico TA. Thoracoscopic versus robotic approaches: advantages and disadvantages. Thorac Surg Clin 2014;24:177-88. [Crossref] [PubMed]
33. Farivar AS, Cerfolio RJ, Vallieres E, et al. Comparing robotic lung resection with thoracotomy and video-assisted thoracoscopic surgery cases entered into the society of thoracic surgeons database. Innovations (Phila) 2014;9:10-5. [Crossref] [PubMed]
34. Hendriksen BS, Hollenbeak CS, Taylor MD, et al. Minimally invasive lobectomy modality and other predictors of conversion to thoracotomy. Innovations (Phila) 2019;14:342-52. [Crossref] [PubMed]
35. Jang HJ, Lee HS, Park SY, et al. Comparison of the early robot-assisted lobectomy experience to video-assisted thoracic surgery lobectomy for lung cancer: a single-institution case series matching study. Innovations (Phila) 2011;6:305-10. [Crossref] [PubMed]
36. Deen SA, Wilson JL, Wilshire CL, et al. Defining the cost of care for lobectomy and segmentectomy: a comparison of open, video-assisted thoracoscopic, and robotic approaches. Ann Thorac Surg 2014;97:1000-7. [Crossref] [PubMed]
37. Swanson SJ, Miller DL, McKenna RJ Jr, et al. Comparing robot-assisted thoracic surgical lobectomy with conventional video-assisted thoracic surgical lobectomy and wedge resection: results from a multihospital database (premier). J Thorac Cardiovasc Surg 2014;147:929-37. [Crossref] [PubMed]
38. Bao F, Zhang C, Yang Y, et al. Comparison of robotic and video-assisted thoracic surgery for lung cancer: a propensity matched analysis. J Thorac Dis 2016;8:1798-803. [Crossref] [PubMed]
39. Glenn ZF, Zubair M, Hussain L, et al. Comparison of pulmonary lobectomies using robotic and video-assisted thoracoscopic approaches: results from 2010-2013 National Inpatient Sample. J Cardiovasc Surg (Torino) 2019;60:526-31. [Crossref] [PubMed]
40. Musgrove KA, Hayanga JA, Holmes SD, et al. Robotic versus video assisted thoracoscopic surgery pulmonary segmentectomy: a cost analysis. Innovations 2018;13:338-43. [Crossref] [PubMed]
41. Nelson DB, Mehran RJ, Mitchell KG, et al. Robotic-assisted lobectomy for non-small cell lung cancer: a comprehensive institutional experience. Ann Thorac Surg 2019;108:370-6. [Crossref] [PubMed]
42. Kneuertz PJ, Singer E, D'Souza DM, et al. Hospital cost and clinical effectiveness of robotic-assisted versus video-assisted thoracoscopic and open lobectomy: a propensity score-weighted comparison. J Thorac Cardiovasc Surg 2019;157:2018-26.e2. [Crossref] [PubMed]
43. Nasir BS, Bryant AS, Minnich DJ, et al. Performing robotic lobectomy and segmentectmy: cost, profitability, and outcomes. Ann Thorac Surg 2014;98:203-8. [Crossref] [PubMed]
44. O’Sullivan KE, Kreaden US, Hebert AE, et al. A systematic review and meta-analysis of robotic versus open and video-assisted thoracoscopic surgery approaches for lobectomy. Interact Cardiovasc Thorac Surg 2019;28:526-34. [Crossref] [PubMed]
45. Dylewski MR, Ohaeto AC, Pereira JF. Pulmonary resection using a total endoscopic robotic video-assisted approach. Semin Thorac Cardiovasc Surg 2011;23:36-42. [Crossref] [PubMed]
46. Pardolesi A, Bertolaccini L, Pastorino U. Is the video-assisted pulmonary segmentectomy the preferred approach to the early stage non-small cell lung cancer? Ann Transl Med 2019;7:24. [Crossref] [PubMed]
47. Liang H, Liang W, Zhao L, et al. Robotic versus video-assisted lobectomy/segmentectomy for lung cancer: a meta-analysis. Ann Surg 2018;268:254-9. [Crossref] [PubMed]
48. Cerfolio RJ, Watson C, Minnich DJ, et al. One hundred planned robotic segmentectomies: early results, technical details, and preferred port placement. Ann Thorac Surg 2016;101:1089-95. [Crossref] [PubMed]
49. Louie BE, Wilson JL, Kim S, et al. Comparison of video-assisted thoracoscopic surgery and robotic approaches for clinical stage I and stage II non-small cell lung cancer using the Society of Thoracic Surgeons Database. Ann Thorac Surg 2016;102:917-24. [Crossref] [PubMed]
50. Li JT, Liu PY, Huang J, et al. Perioperative outcomes of radical lobectomies using robotic-assisted thoracoscopic technique vs. video-assisted thoracoscopic technique: retrospective study of 1,075 consecutive p-stage 1 non-small cell lung cancer cases. J Thorac Dis 2019;11:882-91. [Crossref] [PubMed]
51. Xie B, Sui T, Qin Y, et al. Comparison of short-term outcomes of lung segmentectomy by robotic-assisted and video-assisted thoracoscopic surgery. Zhongguo Fei Ai Za Zhi 2019;22:767-71. [PubMed]