Skip to main content

Advertisement

SpringerLink
Log in

Impact of minimally invasive total mesoesophageal excision and minimally invasive esophagectomy on failure patterns of locally advanced esophageal squamous cell carcinoma: a matched cohort study with long-term follow-up

  • Published:
Surgical Endoscopy Aims and scope Submit manuscript

Abstract

Background

The effects of minimally invasive total mesoesophageal excision (MITME) on the long-term prognosis of locally advanced esophageal squamous cell carcinoma (ESCC) remain unknown. The objective of this study was to compare the static and dynamic failure patterns of MITME and minimally invasive esophagectomy (MIE) for locally advanced ESCC.

Methods

We use propensity score matching (PSM) method to analyze the postoperative failure patterns of the two groups. Cumulative event curves were analyzed for cumulative incidence of failure between different groups, and independent prognostic factors were assessed using time-dependent multivariate analyses. The risk of dynamic failure calculated at 12-month intervals was compared between the two groups using the lifetime table.

Results

A total of 366 ESCC patients were studied by 1:1 PSM for T stage and TNM stage (MITME group, n = 183; MIE group, n = 183). In the matched cohort, there was significant differences between the MITME and MIE groups in the failure pattern of regional lymph node recurrence (0.5 vs 3.8%, P = 0.032) and non-tumor death (10.9 vs 31.7%, P < 0.001). The cumulative event curve found that the 5-year cumulative failure rate was lower in the MITME group than in the MIE group (3.3 vs 17.1%, P = 0.026) after 5 years of survival. In addition, multivariate Cox regression analysis showed that MIE was an independent poor prognostic factor for a high cumulative failure rate in locally advanced ESCC patients at 5 years after surgery (HR:4.110; 95% CI 1.047–16.135; P = 0.043). The dynamic risk curve showed that the MITME group had a lower risk of failure within 5 years after surgery than the MIE group.

Conclusion

Considering that MITME can significantly improve the postoperative failure pattern and the benefit lasts for at least 5 years, it is feasible to use MITME as a treatment for locally advanced ESCC.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data availability

The datasets used and/or analyzed during the current study are available from the corresponding author upon reasonable request.

References

  1. Arnold M, Soerjomataram I, Ferlay J, Forman D (2015) Global incidence of oesophageal cancer by histological subtype in 2012. Gut 64:381–387

    Article  PubMed  Google Scholar 

  2. Chen W, Zheng R, Baade PD, Zhang S, Zeng H, Bray F, Jemal A, Yu XQ, He J (2016) Cancer statistics in China, 2015. CA Cancer J Clin 66:115–132

    Article  PubMed  Google Scholar 

  3. Herskovic A, Russell W, Liptay M, Fidler MJ, Al-Sarraf M (2012) Esophageal carcinoma advances in treatment results for locally advanced disease: review. Ann Oncol 23:1095–1103

    Article  CAS  PubMed  Google Scholar 

  4. Cerfolio RJ, Laliberte AS, Blackmon S, Ruurda JP, Hillegersberg RV, Sarkaria I, Louie BE (2020) minimally invasive esophagectomy: a consensus statement. Ann Thorac Surg 110:1417–1426

    Article  PubMed  Google Scholar 

  5. Groth SS, Burt BM (2021) Minimally invasive esophagectomy: direction of the art. J Thorac Cardiovasc Surg 162:701–704

    Article  PubMed  Google Scholar 

  6. Gergen AK, Halpern AL, Helmkamp L, Torphy RJ, White AM, Mitchell JD, Meguid RA, Scott CD, Gleisner AL, McCarter MD, Weyant MJ (2021) Outcomes after converted minimally invasive to open esophagectomy in patients with esophageal cancer. Ann Thorac Surg 112:1593–1599

    Article  PubMed  Google Scholar 

  7. Matsubara T, Ueda M, Nagao N, Takahashi T, Nakajima T, Nishi M (1998) Cervicothoracic approach for total mesoesophageal dissection in cancer of the thoracic esophagus. J Am Coll Surg 187:238–245

    Article  CAS  PubMed  Google Scholar 

  8. Cuesta MA, Weijs TJ, Bleys RL, van Hillegersberg R, van Berge Henegouwen MI, Gisbertz SS, Ruurda JP, Straatman J, Osugi H, van der Peet DL (2015) A new concept of the anatomy of the thoracic oesophagus: the meso-oesophagus—observational study during thoracoscopic esophagectomy. Surg Endosc 29:2576–2582

    Article  PubMed  Google Scholar 

  9. Hwang SE, Kim JH, Bae SI, Rodríguez-Vázquez JF, Murakami G, Cho BH (2014) Mesoesophagus and other fascial structures of the abdominal and lower thoracic esophagus: a histological study using human embryos and fetuses. Anat Cell Biol 47:227–235

    Article  PubMed  PubMed Central  Google Scholar 

  10. Tsunoda S, Shinohara H, Kanaya S, Okabe H, Tanaka E, Obama K, Hosogi H, Hisamori S, Sakai Y (2020) Mesenteric excision of upper esophagus: a concept for rational anatomical lymphadenectomy of the recurrent laryngeal nodes in thoracoscopic esophagectomy. Surg Endosc 34:133–141

    Article  PubMed  Google Scholar 

  11. Lin J, He J, Chen S, Lin J, Han Z, Chen M, Yu S, Gao L, Peng K, Shen Z, Zhang P, Kang M (2022) Outcomes of minimally invasive total mesoesophageal excision: a propensity score-matched analysis. Surg Endosc 36:3234–3245

    Article  PubMed  Google Scholar 

  12. Peacock O, Waters PS, Bressel M, Lynch AC, Wakeman C, Eglinton T, Koh CE, Lee PJ, Austin KK, Warrier SK, Solomon MJ, Frizelle FA, Heriot AG (2019) Prognostic factors and patterns of failure after surgery for T4 rectal cancer in the beyond total mesorectal excision era. Br J Surg 106:1685–1696

    Article  CAS  PubMed  Google Scholar 

  13. Chen X, Yu X, Chen J, Zhang Z, Tuan J, Shao Z, Guo X, Feng Y (2013) Analysis in early stage triple-negative breast cancer treated with mastectomy without adjuvant radiotherapy: patterns of failure and prognostic factors. Cancer 119:2366–2374

    Article  PubMed  Google Scholar 

  14. Rajasooriyar C, Van Dyk S, Bernshaw D, Kondalsamy-Chennakesavan S, Barkati M, Narayan K (2011) Patterns of failure and treatment-related toxicity in advanced cervical cancer patients treated using extended field radiotherapy with curative intent. Int J Radiat Oncol Biol Phys 80:422–428

    Article  PubMed  Google Scholar 

  15. Huber PM, Afzal N, Arya M, Boxler S, Dudderidge T, Emberton M, Guillaumier S, Hindley RG, Hosking-Jervis F, Leemann L, Lewi H, McCartan N, Moore CM, Nigam R, Odgen C, Persad R, Thalmann GN, Virdi J, Winkler M, Ahmed HU (2020) Prostate specific antigen criteria to diagnose failure of cancer control following focal therapy of nonmetastatic prostate cancer using high intensity focused ultrasound. J Urol 203:734–742

    Article  PubMed  Google Scholar 

  16. Lu J, Wu D, Xu BB, Xue Z, Zheng HL, Xie JW, Wang JB, Lin JX, Li P, Zheng CH, Huang CM (2022) A matched cohort study of the failure pattern after laparoscopic and open gastrectomy for locally advanced gastric cancer: does the operative approach matter? Surg Endosc 36:689–700

    Article  PubMed  Google Scholar 

  17. Wei B, Zheng Z, Fang J, Xiao J, Han F, Huang M, Xu Q, Wang X, Hong C, Wang G, Ju Y, Su G, Deng H, Zhang J, Li J, Chen T, Huang Y, Huang J, Liu J, Yang X, Wei H (2021) Effect of denonvilliers’ fascia preservation versus resection during laparoscopic total mesorectal excision on postoperative urogenital function of male rectal cancer patients: initial results of Chinese PUF-01 randomized clinical trial. Ann Surg 274:e473–e480

    Article  PubMed  Google Scholar 

  18. Zhou H, Ruan C, Sun Y, Zhang J, Wang Z, Hu Z (2015) Nerve-guided laparoscopic total mesorectal excision for distal rectal cancer. Ann Surg Oncol 22:550–551

    Article  CAS  PubMed  Google Scholar 

  19. Emile SH, de Lacy FB, Keller DS, Martin-Perez B, Alrawi S, Lacy AM, Chand M (2018) Evolution of transanal total mesorectal excision for rectal cancer: from top to bottom. World J Gastrointest Surg 10:28–39

    Article  PubMed  PubMed Central  Google Scholar 

  20. Tachimori Y (2014) Total mesoesophageal esophagectomy. Chin Med J 127:574–579

    PubMed  Google Scholar 

  21. Liang L, Liu F, Yang W, Yang W, Chen L, He Y, Liu Z, Zhang L, Zhang F, Cai F, Xu H, Lin M, Liu M, Pan Y, Liu Y, Hu Z, Chen H, He Z, Ke Y (2022) Combined mean corpuscular hemoglobin, fibrinogen, and albumin (MF-A) is a novel prognostic marker in patients with resectable esophageal squamous cell carcinoma. Ann Surg Oncol 29:5626–5633

    Article  PubMed  Google Scholar 

  22. Xu SJ, Lin LQ, Chen C, Chen TY, You CX, Chen RQ, Deana C, Wakefield CJ, Shrager JB, Molena D, Yang CJ, Lin JH, Chen SC (2022) Textbook outcome after minimally invasive esophagectomy is an important prognostic indicator for predicting long-term oncological outcomes with locally advanced esophageal squamous cell carcinoma. Ann Transl Med 10:161

    Article  PubMed  PubMed Central  Google Scholar 

  23. Fu X, Li T, Dai Y, Li J (2019) Preoperative Systemic Inflammation Score (SIS) is superior to Neutrophil to Lymphocyte Ratio (NLR) as a predicting indicator in patients with esophageal squamous cell carcinoma. BMC Cancer 19:721

    Article  PubMed  PubMed Central  Google Scholar 

  24. Akiyama Y, Iwaya T, Endo F, Nikai H, Sato K, Baba S, Chiba T, Kimura T, Takahara T, Otsuka K, Nitta H, Mizuno M, Kimura Y, Koeda K, Sasaki A (2018) Thoracoscopic esophagectomy with total meso-esophageal excision reduces regional lymph node recurrence. Langenbecks Arch Surg 403:967–975

    Article  PubMed  Google Scholar 

  25. Xu SJ, Lin LQ, Chen TY, You CX, Chen C, Chen RQ, Chen SC (2022) Nomogram for prognosis of patients with esophageal squamous cell cancer after minimally invasive esophagectomy established based on non-textbook outcome. Surg Endosc 36:8326–8339

    Article  PubMed  Google Scholar 

  26. Yoo JE, Han K, Shin DW, Park SH, Cho IY, Yoon DW, Cho J, Jung KW (2021) Conditional relative survival and competing mortality in patients who underwent surgery for lung cancer: a nationwide cohort study. Int J Cancer 148:626–636

    Article  CAS  PubMed  Google Scholar 

  27. Xu SJ, Zhang SY, Dong LY, Lin GS, Zhou YJ (2021) Dynamic survival analysis of gastrointestinal stromal tumors (GISTs): a 10-year follow-up based on conditional survival. BMC Cancer 21:1170

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Hattori A, Suzuki K, Takamochi K, Wakabayashi M, Aokage K, Saji H, Watanabe SI (2021) Prognostic impact of a ground-glass opacity component in clinical stage IA non-small cell lung cancer. J Thorac Cardiovasc Surg 161:1469–1480

    Article  PubMed  Google Scholar 

  29. DeQuardo JR (1999) Landmark analysis of corpus callosum shape in schizophrenia. Biol Psychiatry 46:1712–1714

    Article  CAS  PubMed  Google Scholar 

  30. Yago A, Ohkura Y, Ueno M, Fujisawa K, Ogawa Y, Shimoyama H, Haruta S, Udagawa H (2022) Importance of long-term surveillance after curative esophagectomy for esophageal squamous cell carcinoma. Dis Esophagus. https://doi.org/10.1093/dote/doab098

    Article  PubMed  Google Scholar 

  31. Kelsey CR, Fornili M, Ambrogi F, Higgins K, Boyd JA, Biganzoli E, Demicheli R (2013) Metastasis dynamics for non-small-cell lung cancer: effect of patient and tumor-related factors. Clin Lung Cancer 14:425–432

    Article  PubMed  Google Scholar 

  32. Watanabe K, Sakamaki K, Ito H, Yokose T, Yamada K, Nakayama H, Masuda M (2020) Impact of the micropapillary component on the timing of recurrence in patients with resected lung adenocarcinoma. Eur J Cardiothorac Surg 58:1010–1018

    Article  PubMed  Google Scholar 

  33. Wang H, Tang H, Fang Y, Tan L, Yin J, Shen Y, Zeng Z, Zhu J, Hou Y, Du M, Jiao J, Jiang H, Gong L, Li Z, Liu J, Xie D, Li W, Lian C, Zhao Q, Chen C, Zheng B, Liao Y, Li K, Li H, Wu H, Dai L, Chen KN (2021) Morbidity and mortality of patients who underwent minimally invasive esophagectomy after neoadjuvant chemoradiotherapy vs neoadjuvant chemotherapy for locally advanced esophageal squamous cell carcinoma: a randomized clinical trial. JAMA Surg 156:444–451

    Article  PubMed  PubMed Central  Google Scholar 

  34. Tang H, Wang H, Fang Y, Zhu JY, Yin J, Shen YX, Zeng ZC, Jiang DX, Hou YY, Du M, Lian CH, Zhao Q, Jiang HJ, Gong L, Li ZG, Liu J, Xie DY, Li WF, Chen C, Zheng B, Chen KN, Dai L, Liao YD, Li K, Li HC, Zhao NQ, Tan LJ (2023) Neoadjuvant chemoradiotherapy versus neoadjuvant chemotherapy followed by minimally invasive esophagectomy for locally advanced esophageal squamous cell carcinoma: a prospective multicenter randomized clinical trial. Ann Oncol 34:163–172

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors thank all the medical staff who contributed to the maintenance of the medical record database.

Funding

This study was supported by grants from the Key Laboratory of Cardio-Thoracic Surgery (Fujian Medical University), Fujian Province University (No. 0713304); the Natural Science Foundation in Fujian Province (No. 2020J011004); the Fujian provincial health technology project (No. 2020CXA028); the cohort study of the School of Public Health, Fujian Medical University (No. 2021HX003); the Joint Funds for the innovation of science and Technology, Fujian province (No. 2020Y9076); and the National Nature Science Foundation of China (No. 82273415).

Author information

Author notes

  1. Ji-hong Lin and Shao-jun Xu have contributed equally to this work and should be considered co-first authors.

Authors and Affiliations

  1. Department of Thoracic Surgery, Fujian Medical University Union Hospital, No. 29 Xin Quan Road, Fuzhou, 350001, Fujian Province, China

    Ji-hong Lin, Shao-jun Xu, Chao Chen, Cheng-xiong You, Rui-qin Chen, Zhi-fan Zhang, Ming-qiang Kang & Shu-chen Chen

  2. Key Laboratory of Ministry of Education for Gastrointestinal Cancer, Fujian Medical University, Fuzhou, Fujian Province, China

    Ji-hong Lin, Shao-jun Xu, Chao Chen, Cheng-xiong You, Rui-qin Chen, Zhi-fan Zhang, Ming-qiang Kang & Shu-chen Chen

  3. Fujian Provincial Key Laboratory of Cardiothoracic Surgery, Fujian Medical University Union Hospital, Fuzhou, Fujian Province, China

    Ji-hong Lin, Shao-jun Xu, Chao Chen, Cheng-xiong You, Rui-qin Chen, Zhi-fan Zhang, Ming-qiang Kang & Shu-chen Chen

  4. Fujian Minimally Invasive Medical Center (Thoracic Surgery Department), Union Hospital of Fujian Medical University, Fuzhou, China

    Ji-hong Lin, Shao-jun Xu, Chao Chen, Cheng-xiong You, Rui-qin Chen, Zhi-fan Zhang, Ming-qiang Kang & Shu-chen Chen

Authors
  1. Ji-hong Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shao-jun Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Chao Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Cheng-xiong You
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Rui-qin Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Zhi-fan Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ming-qiang Kang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Shu-chen Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conception/Design: SCC, JHL and SJX. Collection and/or assembly of data: JHL, SJX, CC, CXY, RQC, ZFZ and SCC. Data analysis and interpretation: JHL, SJX, CXY, CC, ZFZ, RQC, and SCC. Manuscript writing: JHL, SJX, and SCC. All authors have read and approved the final manuscript.

Corresponding authors

Correspondence to Ming-qiang Kang or Shu-chen Chen.

Ethics declarations

Disclosures

Ji-hong Lin, Shao-jun Xu, Chao Chen, Cheng-xiong You, Rui-qin Chen, Zhi-fang Zhang, and Shu-chen Chen have no conflicts of interest or financial ties to disclose.

Informed consent

This article does not report individual participants’ data in any form.

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.

464_2023_10334_MOESM1_ESM.tif

Supplementary file1 (TIF 7340 KB) Fig. S1 Mesoesophagus of upper esophagus (A), mesoesophagus of middle esophagus (B), mesoesophagus of lower esophagus (C) in surgical field, esophagus from the total mesoesophageal excision (D)

Supplementary file2 (DOCX 16 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.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lin, Jh., Xu, Sj., Chen, C. et al. Impact of minimally invasive total mesoesophageal excision and minimally invasive esophagectomy on failure patterns of locally advanced esophageal squamous cell carcinoma: a matched cohort study with long-term follow-up. Surg Endosc 37, 7698–7708 (2023). https://doi.org/10.1007/s00464-023-10334-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00464-023-10334-0

Keywords

Search

Navigation