Abstract
Background
The use of minimally invasive esophagectomy (MIE) as a treatment for patients with esophageal cancer has recently become more common worldwide. However, differences in the pattern of recurrence between MIE and open esophagectomy (OE) using the transthoracic approach have not been fully investigated, particularly in patients treated with neoadjuvant chemotherapy.
Methods
We searched the prospective databases of two institutes for patients with esophageal cancer who underwent neoadjuvant chemotherapy followed by esophagectomy between 2011 and 2018. Propensity score–matched analysis was performed to reduce bias from confounding patient-related variables. Operative outcomes, regionally harvested lymph nodes (LNs), recurrence pattern, and prognosis were investigated in two groups.
Results
We identified 410 patients who underwent OE (n = 263) and MIE (n = 147). After propensity score matching, 131 pairs of patients were selected. There were no significant differences in baseline characteristics after matching. The total number of harvested LNs in both groups was similar (55.1 vs. 58.9, P = 0.132). The incidence of LN recurrence in the MIE group was significantly lower than that in the OE group (27% vs. 15%, P = 0.010). In particular, the incidence of mediastinal LN recurrence in the MIE group was significantly lower than that in the OE group (16% vs. 6%, P = 0.017). There were no significant differences between the two groups in hematogenous (19% vs.12%, P = 0.173), dissemination (5% vs. 4%, P = 0.769), local (4% vs. 1%. P = 0.213), and other recurrence (3% vs. 3%, P = 1.000). The 3-year disease-free and overall survival of MIE were significantly better than OE (71.4% vs. 50.5%, P = 0.004 and 80.3% vs. 61.2%, P = 0.002, respectively). Multivariate analysis showed that the thoracic approach (OE vs. MIE) (HR 1.93, P = 0.004) was an independent prognostic factor, along with the pathological N stage (HR 3.05, P < 0.001).
Conclusions
MIE has less intramediastinal LN recurrence than OE and may lead to a better long-term prognosis in patients with advanced esophageal cancer who underwent neoadjuvant chemotherapy.
Similar content being viewed by others
Abbreviations
- MIE:
-
Minimally invasive esophagectomy
- OE:
-
Open esophagectomy
- LN:
-
Lymph node
- HR:
-
Hazard ratio
- 5-FU:
-
5-Fluorouracil
- DCF:
-
5-Fluorouracil and cisplatin plus docetaxel
- CD:
-
Clavien-Dindo
- DFS:
-
Disease-free survival
- OS:
-
Overall survival
- PSM:
-
Propensity score–matched analysis
References
Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D (2011) Global cancer statistics. CA Cancer J Clin 61:69-90
Bronson NW, Luna RA, Hunter JG (2012) Tailoring esophageal cancer surgery. Semin Thorac Cardiovasc Surg 24:275-287
van Hagen P, Hulshof MC, van Lanschot JJ, Steyerberg EW, van Berge Henegouwen MI, Wijnhoven BP, Richel DJ, Nieuwenhuijzen GA, Hospers GA, Bonenkamp JJ, Cuesta MA, Blaisse RJ, Busch OR, ten Kate FJ, Creemers GJ, Punt CJ, Plukker JT, Verheul HM, Spillenaar Bilgen EJ, van Dekken H, van der Sangen MJ, Rozema T, Biermann K, Beukema JC, Piet AH, van Rij CM, Reinders JG, Tilanus HW, van der Gaast A, Group C (2012) Preoperative chemoradiotherapy for esophageal or junctional cancer. N Engl J Med 366:2074-2084
Shapiro J, van Lanschot JJB, Hulshof M, van Hagen P, van Berge Henegouwen MI, Wijnhoven BPL, van Laarhoven HWM, Nieuwenhuijzen GAP, Hospers GAP, Bonenkamp JJ, Cuesta MA, Blaisse RJB, Busch ORC, Ten Kate FJW, Creemers GM, Punt CJA, Plukker JTM, Verheul HMW, Bilgen EJS, van Dekken H, van der Sangen MJC, Rozema T, Biermann K, Beukema JC, Piet AHM, van Rij CM, Reinders JG, Tilanus HW, Steyerberg EW, van der Gaast A, group Cs (2015) Neoadjuvant chemoradiotherapy plus surgery versus surgery alone for oesophageal or junctional cancer (CROSS): long-term results of a randomised controlled trial. Lancet Oncol 16:1090-1098
Uttley L, Campbell F, Rhodes M, Cantrell A, Stegenga H, Lloyd-Jones M (2013) Minimally invasive esophagectomy versus open surgery: is there an advantage? Surg Endosc 27:4401-4402
Nagpal K, Ahmed K, Vats A, Yakoub D, James D, Ashrafian H, Darzi A, Moorthy K, Athanasiou T (2010) Is minimally invasive surgery beneficial in the management of esophageal cancer? A meta-analysis. Surg Endosc 24:1621-1629
Smithers BM, Gotley DC, Martin I, Thomas JM (2007) Comparison of the outcomes between open and minimally invasive esophagectomy. Ann Surg 245:232-240
Guo W, Ma X, Yang S, Zhu X, Qin W, Xiang J, Lerut T, Li H (2016) Combined thoracoscopic-laparoscopic esophagectomy versus open esophagectomy: a meta-analysis of outcomes. Surg Endosc 30:3873-3881
Biere SS, van Berge Henegouwen MI, Maas KW, Bonavina L, Rosman C, Garcia JR, Gisbertz SS, Klinkenbijl JH, Hollmann MW, de Lange ES, Bonjer HJ, van der Peet DL, Cuesta MA (2012) Minimally invasive versus open oesophagectomy for patients with oesophageal cancer: a multicentre, open-label, randomised controlled trial. Lancet 379:1887-1892
Mariette C, Markar SR, Dabakuyo-Yonli TS, Meunier B, Pezet D, Collet D, D'Journo XB, Brigand C, Perniceni T, Carrere N, Mabrut JY, Msika S, Peschaud F, Prudhomme M, Bonnetain F, Piessen G, Federation de Recherche en C, French Eso-Gastric Tumors Working G (2019) Hybrid Minimally Invasive Esophagectomy for Esophageal Cancer. N Engl J Med 380:152-162
Yamashita K, Watanabe M, Mine S, Toihata T, Fukudome I, Okamura A, Yuda M, Hayami M, Ishizuka N, Imamura Y (2018) Minimally invasive esophagectomy attenuates the postoperative inflammatory response and improves survival compared with open esophagectomy in patients with esophageal cancer: a propensity score matched analysis. Surg Endosc 32:4443-4450
Gottlieb-Vedi E, Kauppila JH, Malietzis G, Nilsson M, Markar SR, Lagergren J (2019) Long-term Survival in Esophageal Cancer After Minimally Invasive Compared to Open Esophagectomy: A Systematic Review and Meta-analysis. Ann Surg 270:1005-1017
Gottlieb-Vedi E, Kauppila JH, Mattsson F, Lindblad M, Nilsson M, Lagergren P, Rouvelas I, Lagergren J, group* F (2021) Long-term survival in esophageal cancer after minimally invasive esophagectomy compared to open esophagectomy. Ann Surg
Hayami M, Ndegwa N, Lindblad M, Linder G, Hedberg J, Edholm D, Johansson J, Lagergren J, Lundell L, Nilsson M, Rouvelas I (2022) Population-Based Cohort Study from a Prospective National Registry: Better Long-Term Survival in Esophageal Cancer After Minimally Invasive Compared with Open Transthoracic Esophagectomy. Ann Surg Oncol
Ando N, Kato H, Igaki H, Shinoda M, Ozawa S, Shimizu H, Nakamura T, Yabusaki H, Aoyama N, Kurita A, Ikeda K, Kanda T, Tsujinaka T, Nakamura K, Fukuda H (2011) A Randomized Trial Comparing Postoperative Adjuvant Chemotherapy with Cisplatin and 5-Fluorouracil Versus Preoperative Chemotherapy for Localized Advanced Squamous Cell Carcinoma of the Thoracic Esophagus (JCOG9907). Ann Surg Oncol
Nakamura K, Kato K, Igaki H, Ito Y, Mizusawa J, Ando N, Udagawa H, Tsubosa Y, Daiko H, Hironaka S, Fukuda H, Kitagawa Y, Japan Esophageal Oncology Group/Japan Clinical Oncology G (2013) Three-arm phase III trial comparing cisplatin plus 5-FU (CF) versus docetaxel, cisplatin plus 5-FU (DCF) versus radiotherapy with CF (CF-RT) as preoperative therapy for locally advanced esophageal cancer (JCOG1109, NExT study). Jpn J Clin Oncol 43:752-755
Yamasaki M, Yasuda T, Yano M, Hirao M, Kobayashi K, Fujitani K, Tamura S, Kimura Y, Miyata H, Motoori M, Shiraishi O, Makino T, Satoh T, Mori M, Doki Y (2017) Multicenter randomized phase II study of cisplatin and fluorouracil plus docetaxel (DCF) compared with cisplatin and fluorouracil plus Adriamycin (ACF) as preoperative chemotherapy for resectable esophageal squamous cell carcinoma (OGSG1003). Ann Oncol 28:116-120
Sugimura K, Yamasaki M, Yasuda T, Yano M, Hirao M, Fujitani K, Kimura Y, Miyata H, Motoori M, Takeno A, Shiraishi O, Makino T, Kii T, Tanaka K, Satoh T, Mori M, Doki Y (2021) Long-term results of a randomized controlled trial comparing neoadjuvant Adriamycin, cisplatin, and 5-fluorouracil vs docetaxel, cisplatin, and 5-fluorouracil followed by surgery for esophageal cancer (OGSG1003). Ann Gastroenterol Surg 5:75-82
Sugimura K MH, Tanaka K, Makino T, Takemo A, Shiraishi O, Motoori M, Yamasaki M, Kimura Y, Hirao M, Fujitani K, Yasuda T, Mori M, Eguchi H, Yano M, Doki Y (2021) Multicenter Randomized Phase 2 Trial Comparing Chemoradiotherapy and Docetaxel Plus 5-Fluorouracil and Cisplatin (DCF) Chemotherapy as Initial Induction Therapy for Subsequent Conversion Surgery in Patients with Clinical T4b Esophageal Cancer: Short-term Results. Ann Surg
Dindo D, Demartines N, Clavien PA (2004) Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 240:205-213
Japanese Classification of Esophageal Cancer, 11th Edition: part I Esophagus (2017): 14; 1–36
Japanese Classification of Esophageal Cancer, 11th Edition: part II and III Esophagus (2017): 14; 37–65
Thomson IG, Smithers BM, Gotley DC, Martin I, Thomas JM, O'Rourke P, Barbour AP (2010) Thoracoscopic-assisted esophagectomy for esophageal cancer: analysis of patterns and prognostic factors for recurrence. Ann Surg 252:281-291
Hsu PK, Huang CS, Wu YC, Chou TY, Hsu WH (2014) Open versus thoracoscopic esophagectomy in patients with esophageal squamous cell carcinoma. World J Surg 38:402-409
Watanabe M, Baba Y, Nagai Y, Baba H (2013) Minimally invasive esophagectomy for esophageal cancer: an updated review. Surg Today 43:237-244
Shanmugasundaram R, Hopkins R, Neeman T, Beenen E, Fergusson J, Gananadha S (2019) Minimally invasive McKeown's vs open oesophagectomy for cancer: A meta-analysis. Eur J Surg Oncol 45:941-949
Takeno S, Takahashi Y, Moroga T, Kawahara K, Yamashita Y, Ohtaki M (2013) Retrospective study using the propensity score to clarify the oncologic feasibility of thoracoscopic esophagectomy in patients with esophageal cancer. World J Surg 37:1673-1680
Kanekiyo S, Takeda S, Tsutsui M, Nishiyama M, Kitahara M, Shindo Y, Tokumitsu Y, Tomochika S, Tokuhisa Y, Iida M, Sakamoto K, Suzuki N, Yamamoto S, Yoshino S, Hazama S, Ueno T, Nagano H (2018) Low invasiveness of thoracoscopic esophagectomy in the prone position for esophageal cancer: a propensity score-matched comparison of operative approaches between thoracoscopic and open esophagectomy. Surg Endosc 32:1945-1953
Scarpa M, Cavallin F, Saadeh LM, Pinto E, Alfieri R, Cagol M, Da Roit A, Pizzolato E, Noaro G, Pozza G, Castoro C (2016) Hybrid minimally invasive esophagectomy for cancer: impact on postoperative inflammatory and nutritional status. Dis Esophagus 29:1064-1070
Worrell SG, Bachman KC, Sarode AL, Perry Y, Linden PA, Towe CW (2020) Minimally invasive esophagectomy is associated with superior survival, lymphadenectomy and surgical margins: propensity matched analysis of the National Cancer Database. Dis Esophagus 33
Straatman J, van der Wielen N, Cuesta MA, Daams F, Roig Garcia J, Bonavina L, Rosman C, van Berge Henegouwen MI, Gisbertz SS, van der Peet DL (2017) Minimally Invasive Versus Open Esophageal Resection: Three-year Follow-up of the Previously Reported Randomized Controlled Trial: the TIME Trial. Ann Surg 266:232-236
Nuytens F, Dabakuyo-Yonli TS, Meunier B, Gagniere J, Collet D, D'Journo XB, Brigand C, Perniceni T, Carrere N, Mabrut JY, Msika S, Peschaud F, Prudhomme M, Markar SR, Piessen G, Federation de Recherche en C, French Eso-Gastric Tumors Working G (2021) Five-Year Survival Outcomes of Hybrid Minimally Invasive Esophagectomy in Esophageal Cancer: Results of the MIRO Randomized Clinical Trial. JAMA Surg 156:323-332
Miyata H, Sugimura K, Motoori M, Omori T, Yamamoto K, Yanagimoto Y, Shinno N, Yasui M, Takahashi H, Wada H, Ohue M, Yano M (2019) Clinical features of metastasis from superficial squamous cell carcinoma of the thoracic esophagus. Surgery 166:1033-1040
Motoori M, Yano M, Ishihara R, Yamamoto S, Kawaguchi Y, Tanaka K, Kishi K, Miyashiro I, Fujiwara Y, Shingai T, Noura S, Ohue M, Ohigashi H, Nakamura S, Ishikawa O (2012) Comparison between radical esophagectomy and definitive chemoradiotherapy in patients with clinical T1bN0M0 esophageal cancer. Ann Surg Oncol 19:2135-2141
Miyata, H, Sugimura K, Motoori M, Omori T, Yamamoto K, Yanagimoto Y, Shinno N, Yasui M, Takahashi H, Wada H, Oue M, Yano M. (2019) Clinical Impact of the Location of Lymph Node Metastases After Neoadjuvant Chemotherapy for Middle and Lower Thoracic Esophageal Cancer. Ann Surg Oncol 26: 200-208.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Supplementary Fig. 1
Patient selection and propensity score matching. (PNG 1201 kb)
Supplementary Table
(DOCX 25 kb)
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Sugimura, K., Miyata, H., Kanemura, T. et al. Patterns of Recurrence and Long-Term Survival of Minimally Invasive Esophagectomy Versus Open Esophagectomy for Locally Advanced Esophageal Cancer Treated with Neoadjuvant Chemotherapy: a Propensity Score–Matched Analysis. J Gastrointest Surg 27, 1055–1065 (2023). https://doi.org/10.1007/s11605-023-05615-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11605-023-05615-x