Abstract
Background
En bloc esophagectomy results in higher lymph node (LN) retrieval than standard esophagectomy. Minimally invasive esophagectomy (MIE) has gained traction due to improved short-term outcomes, but many large series report LN yields well below the international benchmark of 23. We sought to determine if an established approach to open en bloc resection can be safely transferred to MIE using LN yield as a quality benchmark.
Methods
An open approach to en bloc esophagectomy (OE) was established over 5 years (~ 300 cases) before en bloc MIE was introduced in 2010. Patients undergoing curative-intent en bloc Ivor-Lewis and McKeown esophagectomy for cancer from 2010 to 2019 by a single surgeon with formal minimally invasive surgery training were identified from a prospectively collected database. Mann–Whitney U and χ2 tests and cumulative sum analysis were used for statistical analysis. “Failure” was defined as LN yield less than AJCC’s 8th edition guidelines: 10 LNs for pT1 cancers, 20 for pT2 and 30 for pT3–4.
Results
A total of 269 esophageal resections met inclusion criteria [193(72%) OE; 76(28%) MIE]. Age, sex, BMI and comorbidities were comparable between groups. Tumors were larger and more often locally advanced in OE. Median LN retrieval was sufficient by international standards in both groups [OE:34(27–46); MIE:28(22–39); p = 0.01]. “Failures” occurred in 33(17%) of OE and 12(16%) MIE cases (p = 0.63). No learning effect was observed for LN yield. R0 resection rate was comparable [OE:191(99%); MIE:73(96%); p = 0.90]. Operative time was longer for MIE [275(246–300)] than OE [240(210–270) minutes], p < 0.0001, while estimated blood loss (OE:350(250–500)mL; MIE:300(200–400)mL; p = 0.02] and length of stay [OE:8(6–13); MIE7(6–9) days; p = 0.02] were higher for OE. Morbidity and mortality were comparable between groups and LN yield did not impact survival.
Conclusions
Under appropriate conditions, an established approach to open en bloc esophagectomy can be safely transferred to MIE without compromising surgical quality.
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References
van Rijswijk AS, Hagens ERC, van der Peet DL, van Berge Henegouwen MI, Gisbertz SS (2019) Differences in esophageal cancer surgery in terms of surgical approach and extent of lymphadenectomy: findings of an international survey. Ann Surg Oncol 26:2063–2072
Wang W, Liu F, Hu T, Wang C (2018) Matched-pair comparisons of minimally invasive esophagectomy versus open esophagectomy for resectable esophageal cancer: a systematic review and meta-analysis protocol. Medicine (Baltimore). https://doi.org/10.1097/MD.0000000000011447
Zhang X, Yang Y, Ye B, Sun Y, Guo X, Hua R, Mao T, Fang W, Li Z (2017) Minimally invasive esophagectomy is a safe surgical treatment for locally advanced pathologic T3 esophageal squamous cell carcinoma. J Thorac Dis 9:2982–2991
Yibulayin W, Abulizi S, Lv H, Sun W (2016) Minimally invasive oesophagectomy versus open esophagectomy for resectable esophageal cancer: a meta-analysis. World J Surg Oncol. https://doi.org/10.1186/s12957-016-1062-7
Bjelovic M, Babic T, Gunjic D, Veselinovic M, Spica B (2015) Minimally invasive esophagectomy for cancer: single center experience after 44 consecutive cases. Srp Arh Celok Lek 143:410–415
Yamamoto M, Weber JM, Karl RC, Meredith KL (2013) Minimally invasive surgery for esophageal cancer: review of the literature and institutional experience. Cancer Control 20:130–137
Altorki NK, Girardi L, Skinner DB (1997) En bloc esophagectomy improves survival for stage III esophageal cancer. J Thorac Cardiovasc Surg 114:948–955
Santillan AA, Farma JM, Meredith KL, Shah NR, Kelley ST (2008) Minimally invasive surgery for esophageal cancer. J Natl Compr Canc Netw 6:879–884
van der Werf LR, Dikken JL, van Berge Henegouwen MI, Lemmens V, Nieuwenhuijzen GAP, Wijnhoven BPL, Dutch Upper GICA (2018) A population-based study on lymph node retrieval in patients with esophageal cancer: results from the Dutch upper gastrointestinal cancer audit. Ann Surg Oncol 25:1211–1220
Wallner G, Zgodzinski W, Masiak-Segit W, Skoczylas T, Dabrowski A (2014) Minimally invasive surgery for esophageal cancer - benefits and controversies. Kardiochir Torakochirurgia Pol 11:151–155
Luketich JD, Pennathur A, Awais O, Levy RM, Keeley S, Shende M, Christie NA, Weksler B, Landreneau RJ, Abbas G, Schuchert MJ, Nason KS (2012) Outcomes after minimally invasive esophagectomy: review of over 1000 patients. Ann Surg 256:95–103
Peyre CG, Hagen JA, DeMeester SR, Altorki NK, Ancona E, Griffin SM, Holscher A, Lerut T, Law S, Rice TW, Ruol A, van Lanschot JJ, Wong J, DeMeester TR (2008) The number of lymph nodes removed predicts survival in esophageal cancer: an international study on the impact of extent of surgical resection. Ann Surg 248:549–556
Claassen L, van Workum F, Rosman C (2019) Learning curve and postoperative outcomes of minimally invasive esophagectomy. J Thorac Dis 11:S777–S785
Charlson ME, Pompei P, Ales KL, MacKenzie CR (1987) A new method of classifying prognostic comorbidity in longitudinal studies: development and validation. J Chronic Dis 40:373–383
Radovanovic D, Seifert B, Urban P, Eberli FR, Rickli H, Bertel O, Puhan MA, Erne P, Investigators AP (2014) Validity of Charlson Comorbidity Index in patients hospitalised with acute coronary syndrome. Insights from the nationwide AMIS Plus registry 2002–2012. Heart 100:288–294
Huang YQ, Gou R, Diao YS, Yin QH, Fan WX, Liang YP, Chen Y, Wu M, Zang L, Li L, Zang J, Cheng L, Fu P, Liu F (2014) Charlson comorbidity index helps predict the risk of mortality for patients with type 2 diabetic nephropathy. J Zhejiang Univ-Sc B 15:58–66
Moro-Sibilot D, Aubert A, Diab S, Lantunejoul S, Fourneret P, Brambilla E, Brambilla C, Brichon PY (2005) Comorbidities and Charlson score in resected stage I nonsmall cell lung cancer. Eur Respir J 26:480–486
Rice TW, Patil DT, Blackstone EH (2017) 8th edition AJCC/UICC staging of cancers of the esophagus and esophagogastric junction: application to clinical practice. Ann Cardiothorac Surg 6:119–130
Macdonald JS, Smalley SR, Benedetti J, Hundahl SA, Estes NC, Stemmermann GN, Haller DG, Ajani JA, Gunderson LL, Jessup JM, Martenson JA (2001) Chemoradiotherapy after surgery compared with surgery alone for adenocarcinoma of the stomach or gastroesophageal junction. N Engl J Med 345:725–730
Roses RE, Datta J, You N (2019) Defining the optimal treatment of locally advanced gastric cancer. https://bulletin.facs.org/2019/05/defining-the-optimal-treatment-of-locally-advanced-gastric-cancer/. May 2019; Accessed 11 Feb 2020
Berry MF (2014) Esophageal cancer: staging system and guidelines for staging and treatment. J Thorac Dis 6:S289–S297
Sudarshan M, Ferri L (2012) A critical review of minimally invasive esophagectomy. Surg Laparosc Endosc Tech 22:310–318
Visser E, van Rossum PSN, van Veer H, Al-Naimi K, Chaudry MA, Cuesta MA, Gisbertz SS, Gutschow CA, Holscher AH, Luyer MDP, Mariette C, Moorthy K, Nieuwenhuijzen GAP, Nilsson M, Rasanen JV, Schneider PM, Schroder W, Cheong E, van Hillegersberg R (2018) A structured training program for minimally invasive esophagectomy for esophageal cancer-a Delphi consensus study in Europe. Dis Esophagus. https://doi.org/10.1093/dote/dox124
Dhamija A, Rosen JE, Dhamija A, Gould Rothberg BE, Kim AW, Detterbeck FC, Boffa DJ (2014) Learning curve to lymph node resection in minimally invasive esophagectomy for cancer. Innovations (Phila) 9:286–291
Tapias LF, Morse CR (2014) Minimally invasive Ivor Lewis esophagectomy: description of a learning curve. J Am Coll Surg 218:1130–1140
van Workum F, Stenstra M, Berkelmans GHK, Slaman AE, van Berge Henegouwen MI, Gisbertz SS, van den Wildenberg FJH, Polat F, Irino T, Nilsson M, Nieuwenhuijzen GAP, Luyer MD, Adang EM, Hannink G, Rovers MM, Rosman C (2019) Learning curve and associated morbidity of minimally invasive esophagectomy: a retrospective multicenter study. Ann Surg 269:88–94
Oshikiri T, Yasuda T, Hasegawa H, Yamamoto M, Kanaji S, Yamashita K, Matsuda T, Sumi Y, Nakamura T, Fujino Y, Tominaga M, Suzuki S, Kakeji Y (2017) Short-term outcomes and one surgeon's learning curve for thoracoscopic esophagectomy performed with the patient in the prone position. Surg Today 47:313–319
Zhu ZY, Yong X, Luo RJ, Wang YZ (2018) Clinical analysis of minimally invasive McKeown esophagectomy in a single center by a single medical group. J Zhejiang Univ Sci B 19:718–725
Mu JW, Gao SG, Xue Q, Mao YS, Wang DL, Zhao J, Gao YS, Huang JF, He J (2015) Updated experiences with minimally invasive McKeown esophagectomy for esophageal cancer. World J Gastroenterol 21:12873–12881
Ding QQ, Zhou WY, Xue YB, Han X, Yin DD, Xue L, Luo JH (2019) Comparison of postoperative complications between different operation methods for esophageal cancer. Thorac Cancer 10:1669–1672
Cash JC, Zehetner J, Hedayati B, Bildzukewicz NA, Katkhouda N, Mason RJ, Lipham JC (2014) Outcomes following laparoscopic transhiatal esophagectomy for esophageal cancer. Surg Endosc Other Intervent Tech 28:492–499
Hagens ERC, Henegouwen MIV, Cuesta MA, Gisbertz SS (2017) The extent of lymphadenectomy in esophageal resection for cancer should be standardized. J Thorac Dis 9:S713–S723
Talsma K, van Hagen P, Grotenhuis BA, Steyerberg EW, Tilanus HW, van Lanschot JJB, Wijnhoven BPL (2012) Comparison of the 6th and 7th editions of the UICC-AJCC TNM classification for esophageal cancer. Ann Surg Oncol 19:2142–2148
Rizk NP, Ishwaran H, Rice TW, Chen LQ, Schipper PH, Kesler KA, Law S, Lerut TEMR, Reed CE, Salo JA, Scott WJ, Hofstetter WL, Watson TJ, Allen MS, Rusch VW, Blackstone EH (2010) Optimum lymphadenectomy for esophageal cancer. Ann Surg 251:46–50
Acknowledgements
We would like to thank Aya Siblini for assisting with securing research ethics review board approval and Samantha Lancione for obtaining mortality data.
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Drs. Carmen L. Mueller, Lorenzo E. Ferri, Liane S. Feldman, David Mulder, Jonathan Cools-Lartigue and Anitha Kammili have no conflicts of interest or financial ties to disclose.
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Kammili, A., Cools-Lartigue, J., Mulder, D. et al. Transition from open to minimally invasive en bloc esophagectomy can be achieved without compromising surgical quality. Surg Endosc 35, 3067–3076 (2021). https://doi.org/10.1007/s00464-020-07696-0
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DOI: https://doi.org/10.1007/s00464-020-07696-0