Associated risk factor analysis and the prognostic impact of positive resection margins after endoscopic resection in early esophageal squamous cell carcinoma

Feng,Yong; Wei,Wei; Guo,Shuo; Li,Bao-Qing

doi:10.3892/etm.2022.11384

Associated risk factor analysis and the prognostic impact of positive resection margins after endoscopic resection in early esophageal squamous cell carcinoma

Authors:
- Yong Feng
- Wei Wei
- Shuo Guo
- Bao-Qing Li
View Affiliations

Affiliations: Department of Thoracic Surgery, Fourth Hospital of Hebei Medical University, Shijiazhuang, Hebei 050011, P.R. China, Department of Outpatients, Fourth Hospital of Hebei Medical University, Shijiazhuang, Hebei 050011, P.R. China, Department of Gastroenterology, Fourth Hospital of Hebei Medical University, Shijiazhuang, Hebei 050011, P.R. China
Published online on: May 20, 2022 https://doi.org/10.3892/etm.2022.11384
Article Number: 457
Copyright: © Feng et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

Endoscopic resection for early esophageal cancer has a risk of residual margins. The risk these residual margins pose have not been fully evaluated. The present study aimed to investigate the associated risk factors and prognosis of residual margins following the endoscopic resection of early esophageal squamous cell carcinoma. In total, 369 patients (381 lesions) with early esophageal squamous cell carcinoma treated in the Fourth Hospital of Hebei Medical University (Shijiazhuang, China) with endoscopic resection were retrospectively analyzed. Sex, age, location, tumor diameter, depth of tumor invasion, endoscopic treatment, endoscopic ultrasonography (EUS) before resection, work experience of endoscopists and the degree of tumor differentiation were all evaluated as potential risk factors. In addition, the prognosis of patients with positive margins were analyzed. A total of 73 patients (73/381, 19.2%) had positive margins after endoscopic resection. Amongst the 65 patients who were successfully followed up, five patients succumbed to cardiovascular and cerebrovascular diseases, one patient received radiotherapy, two patients received radiotherapy and chemotherapy whilst one patient received chemotherapy. By contrast, 12 patients received surgery and 20 patients received additional endoscopic mucosal resection or endoscopic submucosal dissection. The other 29 patients were followed up regularly and no recurrence could be found. Univariate analysis revealed that tumor diameter, endoscopic treatment, depth of invasion, EUS before resection, degree of tumor differentiation and direction of invasion were all associated with the positive margin. Multivariate logistic regression analysis then found that EUS before resection, degree of tumor differentiation and depth of tumor invasion are independent risk factors for positive margins after endoscopic resection. These results suggest that poorly differentiated lesions and deeper invasion depth can increase the risk of positive margin after endoscopic resection. As a result, EUS evaluation before resection may reduce the risk of invasion depth. In addition, for poorly differentiated lesions, more aggressive treatment regimens may be recommended for preventing recurrence.

View Figures

View References

1	Zhang L, Zhou Y, Cheng C, Cui HY, Cheng L, Kong PZ, Wang JQ, Li Y, Chen WL, Song B, et al: Genomic analyses reveal mutational signatures and frequently altered genes in esophageal squamous cell carcinoma. Am J Hum Genet. 96:597–611. 2015.PubMed/NCBI View Article : Google Scholar
2	Njei B, McCarty TR and Birk JW: Trends in esophageal cancer survival in United States adults from 1973 to 2009: A SEER database analysis. J Gastroenterol Hepatol. 31:1141–1146. 2016.PubMed/NCBI View Article : Google Scholar
3	Naveed M and Kubiliun N: Endoscopic treatment of early-stage esophageal cancer. Curr Oncol Rep. 20(71)2018.PubMed/NCBI View Article : Google Scholar
4	Wani S, Early D, Edmundowicz S and Sharma P: Management of high-grade dysplasia and intramucosal adenocarcinoma in Barrett's esophagus. Clin Gastroenterol Hepatol. 10:704–711. 2012.PubMed/NCBI View Article : Google Scholar
5	Neuhaus H: Endoscopic submucosal dissection in the upper gastrointestinal tract: Present and future view of Europe. Dig Endosc. 21 (Suppl 1):S4–S6. 2009.PubMed/NCBI View Article : Google Scholar
6	Chennat J, Konda VJ, Ross AS, de Tejada AH, Noffsinger A, Hart J, Lin S, Ferguson MK, Posner MC and Waxman I: Complete Barrett's eradication endoscopic mucosal resection: an effective treatment modality for high-grade dysplasia and intramucosal carcinoma-an American single-center experience. Am J Gastroenterol. 104:2684–2692. 2009.PubMed/NCBI View Article : Google Scholar
7	Oyama T, Tomori A, Hotta K, Morita S, Kominato K, Tanaka M and Miyata Y: Endoscopic submucosal dissection of early esophageal cancer. Clin Gastroenterol Hepatol. 3 (Suppl 1):S67–S70. 2005.PubMed/NCBI View Article : Google Scholar
8	Mariette C, Fabre S, Balon JM, Finzi L and Triboulet JP: Factors predictive of complete resection of operable esophageal cancer: review of 746 patients. Gastroenterol Clin Biol. 26:454–462. 2002.PubMed/NCBI
9	Fujishiro M, Yahagi N, Kakushima N, Kodashima S, Muraki Y, Ono S, Yamamichi N, Tateishi A, Shimizu Y, Oka M, et al: Endoscopic submucosal dissection of esophageal squamous cell neoplasms. Clin Gastroenterol Hepatol. 4:688–694. 2006.PubMed/NCBI View Article : Google Scholar
10	Repici A, Hassan C, Carlino A, Pagano N, Zullo A, Rando G, Strangio G, Romeo F, Nicita R, Rosati R and Malesci A: Endoscopic submucosal dissection in patients with early esophageal squamous cell carcinoma: Results from a prospective Western series. Gastrointest Endosc. 71:715–721. 2010.PubMed/NCBI View Article : Google Scholar
11	Ono S, Fujishiro M, Niimi K, Goto O, Kodashima S, Yamamichi N and Omata M: Long-term outcomes of endoscopic submucosal dissection for superficial esophageal squamous cell neoplasms. Gastrointest Endosc. 70:860–886. 2009.PubMed/NCBI View Article : Google Scholar
12	Hamilton SR and Aaltonen LA: World Health Organization classification of tumours: Pathology and genetics of tumours of the digestive system. IARC Press, Lyon, pp11-36, 2000.
13	Birkmeyer JD, Siewers AE, Finlayson EV, Stukel TA, Lucas FL, Batista I, Welch HG and Wennberg DE: Hospital volume and surgical mortality in the United States. N Engl J Med. 346:1128–1137. 2002.PubMed/NCBI View Article : Google Scholar
14	Ell C, May A, Pech O, Gossner L, Guenter E, Behrens A, Nachbar L, Huijsmans J, Vieth M and Stolte M: Curative endoscopic resection of early esophageal adenocarcinomas (Barrett's cancer). Gastrointest Endosc. 65:3–10. 2007.PubMed/NCBI View Article : Google Scholar
15	Pech O, Behrens A, May A, Nachbar L, Gossner L, Rabenstein T, Manner H, Guenter E, Huijsmans J, Vieth M, et al: Long-term results and risk factor analysis for recurrence after curative endoscopic therapy in 349 patients with high-grade intraepithelial neoplasia and mucosal adenocarcinoma in Barrett's oesophagus. Gut. 57:1200–1206. 2008.PubMed/NCBI View Article : Google Scholar
16	Pech O, Gossner L, May A, Vieth M, Stolte M and Ell C: Endoscopic resection of superficial esophageal squamous-cell carcinomas: Western experience. Am J Gastroenterol. 99:1226–1232. 2004.PubMed/NCBI View Article : Google Scholar
17	Stahl M, Budach W, Meyer HJ and Cervantes A: Esophageal cancer: Clinical practice guidelines for diagnosis, treatment and follow-up. Ann Oncol. 21 (Suppl 5):v46–v49. 2010.PubMed/NCBI View Article : Google Scholar
18	Manner H, May A, Pech O, Gossner L, Rabenstein T, Günter E, Vieth M, Stolte M and Ell C: Early Barrett's carcinoma with ‘low-risk’ submucosal invasion: Long-term results of endoscopic resection with a curative intent. Am J Gastroenterol. 103:2589–2597. 2008.PubMed/NCBI View Article : Google Scholar
19	Hazama H, Tanaka M, Kakushima N, Yabuuchi Y, Yoshida M, Kawata N, Takizawa K, Ito S, Imai K, Hotta K, et al: Predictors of technical difficulty during endoscopic submucosal dissection of superficial esophageal cancer. Surg Endosc. 33:2909–2915. 2019.PubMed/NCBI View Article : Google Scholar
20	Plum PS, Hölscher AH, Pacheco Godoy K, Schmidt H, Berlth F, Chon SH, Alakus H and Bollschweiler E: Prognosis of patients with superficial T1 esophageal cancer who underwent endoscopic resection before esophagectomy-A propensity score-matched comparison. Surg Endosc. 32:3972–3980. 2018.PubMed/NCBI View Article : Google Scholar
21	Wang HY, Zeng X, Bai SY, Pu K, Zheng Y, Ji R, Guo QH, Guan QL, Wang YP and Zhou YN: The safety and efficacy of endoscopic submucosal dissection for treating early oesophageal carcinoma: A meta-analysis. Ann R Coll Surg Engl. 102:702–711. 2020.PubMed/NCBI View Article : Google Scholar
22	Sgourakis G, Gockel I and Lang H: Endoscopic and surgical resection of T1a/T1b esophageal neoplasms: A systematic review. World J Gastroenterol. 19:1424–1437. 2013.PubMed/NCBI View Article : Google Scholar
23	Qi ZP, Chen T, Li B, Ren Z, Yao LQ, Shi Q, Cai SL, Zhong YS and Zhou PH: Endoscopic submucosal dissection for early esophageal cancer in elderly patients with relative indications for endoscopic treatment. Endoscopy. 50:839–845. 2018.PubMed/NCBI View Article : Google Scholar
24	Wu Y, Zhang H, Zhou B, Han SY and Zhang YR: Clinical efficacy of endoscopic submucosal dissection in the treatment of early esophageal cancer and precancerous lesions. J Cancer Res Ther. 14:52–56. 2018.PubMed/NCBI View Article : Google Scholar
25	Yip HC and Chiu PW: Endoscopic diagnosis and management of early squamous cell carcinoma of esophagus. J Thorac Dis. 9 (Suppl 8):S689–S696. 2017.PubMed/NCBI View Article : Google Scholar
26	Isomoto H, Shikuwa S, Yamaguchi N, Fukuda E, Ikeda K, Nishiyama H, Ohnita K, Mizuta Y, Shiozawa J and Kohno S: Endoscopic submucosal dissection for early gastric cancer: A large-scale feasibility study. Gut. 58:331–336. 2009.PubMed/NCBI View Article : Google Scholar
27	Chung IK, Lee JH, Lee SH, Kim SJ, Cho JY, Cho WY, Hwangbo Y, Keum BR, Park JJ, Chun HJ, et al: Therapeutic outcomes in 1000 cases of endoscopic submucosal dissection for early gastric neoplasms: Korean ESD study group multicenter study. Gastrointest Endosc. 69:1228–1235. 2009.PubMed/NCBI View Article : Google Scholar
28	Thosani N, Singh H, Kapadia A, Ochi N, Lee JH, Ajani J, Swisher SG, Hofstetter WL, Guha S and Bhutani MS: Diagnostic accuracy of EUS in differentiating mucosal versus submucosal invasion of superficial esophageal cancers: A systematic review and meta-analysis. Gastrointest Endosc. 75:242–253. 2012.PubMed/NCBI View Article : Google Scholar
29	Yang J, Luo GY, Liang RB, Zeng TS, Long H, Fu LH, Xu GL, Yang MZ, Li S, Zhang LJ, et al: Efficacy of endoscopic ultrasonography for determining clinical T category for esophageal squamous cell carcinoma: Data from 1434 surgical cases. Ann Surg Oncol. 25:2075–2082. 2018.PubMed/NCBI View Article : Google Scholar
30	Ishii N, Horiki N, Itoh T, Maruyama M, Matsuda M, Setoyama T, Suzuki S, Uchida S, Uemura M, Iizuka Y, et al: Endoscopic submucosal dissection and preoperative assessment with endoscopic ultrasonogra-phy for the treatment of rectal carcinoid tumors. Surg Endosc. 24:1413–1419. 2010.PubMed/NCBI View Article : Google Scholar
31	Zhou FR, Huang LY and Wu CR: Endoscopic mucosal resection for rectal carcinoids under micro-probe ultrasound guidance. World J Gastroenterol. 19:2555–2559. 2013.PubMed/NCBI View Article : Google Scholar
32	Lee TH, Cho JY, Chang YW, Kim JO, Lee JS, Cho WY, Kim HG, Kim WJ, Park YS and Jin SY: Appropriate indications for endoscopic submucosal dissection of early gastric cancer according to tumor size and histologic type. Gastrointest Endosc. 71:920–926. 2010.PubMed/NCBI View Article : Google Scholar
33	Fujishiro M, Kodashima S, Goto O, Ono S, Niimi K, Yamamichi N, Oka M, Ichinose M and Omata M: Endoscopic submucosal dissection for esophageal squamous cell neoplasms. Dig Endosc. 21:109–115. 2009.PubMed/NCBI View Article : Google Scholar
34	Yoshida T, Inoue H, Usui S, Satodate H, Fukami N and Kudo SE: Narrow-band imaging system with magnifying endoscopy for superficial esophageal lesions. Gastrointest Endosc. 59:288–295. 2004.PubMed/NCBI View Article : Google Scholar
35	Kakushima N, Ono H, Tanaka M, Takizawa K, Yamaguchi Y and Matsubayashi H: Factors related to lateral margin positivity for cancer in gastric specimens of endoscopic submucosal dissection. Dig Endosc. 23:227–232. 2011.PubMed/NCBI View Article : Google Scholar
36	Wen J, Linghu EQ, Yang YS, Liu QS, Yang J and Lu ZS: Associated risk factor analysis for positive resection margins after endoscopic submucosal dissection in early-stage gastric cancer. J BUON. 20:421–427. 2015.PubMed/NCBI
37	Hwang JJ, Park KJ, Park YS, Lee HS, Yoon H, Shin CM, Kim N and Lee DH: A scoring system for patients with a tumor-positive lateral resection margin after endoscopic resection of early gastric cancer. Surg Endosc. 30:2751–2758. 2016.PubMed/NCBI View Article : Google Scholar
38	Oyama T, Inoue H, Arima M, Momma K, Omori T, Ishihara R, Hirasawa D, Takeuchi M, Tomori A and Goda K: Prediction of the invasion depth of superficial squamous cell carcinoma based on microvessel morphology: Magnifying endoscopic classification of the Japan esophageal society. Esophagus. 14:105–112. 2017.PubMed/NCBI View Article : Google Scholar
39	Hatta W, Gotoda T, Oyama T, Kawata N, Takahashi A, Yoshifuku Y, Hoteya S, Nakagawa M, Hirano M and Esaki M: , et al: Is the eCura system useful for selecting patients who require radical surgery after noncurative endoscopic submucosal dissection for early gastric cancer? A comparative study. Gastric Cancer. 21:481–489. 2018.PubMed/NCBI View Article : Google Scholar