Additional endoscopic treatments for patients with positive lateral margins after endoscopic resection of early esophageal squamous cell carcinoma
- Authors:
- Published online on: December 23, 2022 https://doi.org/10.3892/ol.2022.13653
- Article Number: 67
Abstract
Introduction
Esophageal cancer is the seventh most common malignant tumor, ranking sixth in global cancer-associated mortality (1,2). In terms of histological subtypes, adenocarcinoma is commonly observed in Europe and the United States, whereas squamous cell carcinoma is the primary subtype in China (2,3). Early esophageal cancer is defined as cancer confined to the mucosa (T1a) or submucosa (T1b), regardless of the presence of lymph node metastasis (LNM) (4–6). In previous years, endoscopic treatment, namely endoscopic mucosal resection or endoscopic submucosal dissection (ESD), has been increasingly regarded as a treatment option for early esophageal cancer (7,8).
The proportion of early (T1) stage detection has increased due to the improvement of endoscopic detection (9). Endoscopic resection (ER) of early tumors is the first step in patient management (9,10). ER is curative in most types of intramucosal (T1a) cancer and cancer that partially invades the submucosa (T1b) (11). Esophagectomy with lymph node dissection is not clearly indicated as the first choice in patients with ‘non-curative’ or ‘potentially curative’ ER (11). Based on previous studies, esophagectomy results in a 5–10% mortality rate (12,13). However, due to high morbidity and mortality as a result of complications with esophagectomy, certain patients do not receive surgical treatment (14–17).
According to the guidelines of the European Society of Gastrointestinal Endoscopy, if there are poorly differentiated lesions, lymphovascular invasion (LVI) or positive vertical margins, further treatment is recommended (11). By contrast, the Japanese Gastroenterology Endoscopy Society recommends additional treatment for patients with submucosal infiltration following ER of esophageal cancer, but there is still no consensus on what to do in these cases (18). To date, adjuvant management following non-curative or high-risk ER is not standardized. Therefore, the present study aimed to propose an additional treatment strategy for patients with non-curative resection (non-CR) and only positive lateral margin (LM+) following ER of early esophageal squamous cell carcinoma (ESCC).
Materials and methods
Patients
The present study retrospectively analyzed 511 patients (31–85 years) with early ESCC who underwent ER in the Fourth Hospital of Hebei Medical University (Shijiazhuang, China) from January 2000 to June 2022, of whom 84 had non-CR. The baseline characteristics, methods of endoscopic treatment and histological features in the medical records were reviewed.
The study included only patients with LM+ and non-CR (n=41). The exclusion criteria were as follows: i) Positive deep margin; ii) incomplete resection; iii) previous history of esophageal cancer; iv) additional history of chemotherapy or radiotherapy and v) clinical observation without additional treatment (Fig. 1). All patients provided written informed consent. The present study was approved by the Ethics Committee of the Fourth Hospital of Hebei Medical University (2020YB318).
Complete resection was defined as en bloc resection with margins macroscopically and microscopically free of tumor. Incomplete resection was defined as the presence of cancer cells in the lateral (anterior, posterior, proximal or distal) and deep margin. CR was achieved when a resected specimen met the requirements of complete resection without submucosal invasion or LVI. If the resection did not meet the criteria of CR, it was defined as non-CR (19–21). LM+ was defined as cancer cells histologically apparent in the LMs of the dissected specimens. Single LM+ referred to one direction (anterior, posterior, proximal or distal) of invasion and multiple LM+ to >2 directions. In addition, residual cancer was defined as the presence of cancer cells in pathological specimens following additional surgery or re-ER.
Endoscopic procedure and follow-up
Endoscopic treatment and follow-up were performed as previously described (22). For re-ER, Lugol's iodine staining was used to evaluate lesion size. Argon plasma coagulation (FiAPC® probes were used for the flexible endoscope; ERBE Elektromedizin GmbH) was used to mark ~5 mm outside the boundary of the lesion (22). This was the resection range of re-ER.
Histopathological evaluation
Endoscopically resected specimens were serially sectioned at 2 mm intervals. The protocol for detailed histopathological evaluation was as previously described (22).
Additional treatment following ER
Of the 41 patients who received ER, 13 (31.7%) underwent additional surgery and 28 (68.3%) underwent re-ER. The clinicians chose re-ER or additional surgery after evaluating the clinical and pathological factors of each patient (from inspecting the final pathology report and the patient condition), which included age, underlying disease and consent to additional surgery. Patients who refused additional treatment underwent close observation. Due to lack of consensus in the literature, the final choice of treatment was based on the doctor's evaluation (11,18). Re-ER and additional surgery were performed <3 months or 1 month following initial ER, respectively.
Statistical analysis
Categorical variables were analyzed using χ2 or the Fisher's exact test. Continuous variables are reported as median and range or mean ± standard deviation and were compared using Student's t or the Mann-Whitney U test. P<0.05 was considered to indicate a statistically significant difference. All analyses were performed using SPSS version 19.0 (IBM Corp.).
Results
Clinicopathological features of patients
The mean age of all patients was 64.5±8.5 years. Table I summarizes the baseline clinicopathological characteristics of patients with non-CR who were only LM+ following ER of early ESCC. There were 28 patients (68.3%) with single LM+ and 13 patients (31.7%) with multiple LM+. Following additional surgery or re-ER, 27 resected specimens (65.9%) showed residual cancer.
Comparison of additional treatment methods after ER
A comparison of the two additional treatment methods following non-CR is shown in Table II. The mean age of patients in the re-ER group was higher than that in the surgery group (69.5±9.5 vs. 62.5±7.8 years; P=0.023). Patients with multiple LM+ after ER were most often treated with surgery (re-ER (n=28), 21.4% vs. surgery (n=13), 53.8%; P=0.038). Patients with well-differentiated lesions were more likely to receive re-ER than additional surgery (P=0.003). Residual cancer was more common in the additional surgery group but there was not a statistically significant difference (re-ER (n=28), 60.7% vs. surgery (n=13), 76.9%; P=0.308). There were also no statistically significant differences between the two groups in terms of sex, tumor location, size, tumor shape or residual cancer at final pathology.
Table II.Comparison of additional treatment following ER for early esophageal squamous cell carcinoma. |
Pathological features of residual lesions following additional treatment after ER
Table III lists pathological features of residual lesions following non-CR (only LM+) with re-ER and additional surgery. In patients with poorly differentiated cancer, the proportion of residual cancer cells increased significantly (No residual cancer (n=14), 14.3% vs. Residual cancer (n=27), 29.6%; P=0.030). Residual cancer was also significantly higher in the multiple LM+ group than in the single LM+ group (single LM+, 7.1% vs. multiple LM+, 44.4%; P=0.015).
Table III.Pathological features of residual lesions following additional treatment post-endoscopic resection. |
Clinical results of additional treatments after ER
Themean follow-up time of all enrolled patients was 36.1±24.1 months. At the time of writing, there had been no recurrence, although in the additional surgery group, two patients had anastomotic leakage and one patient had respiratory failure.
Clinicopathological features of patients with additional surgery
The clinicopathological characteristics of 13 patients who underwent additional surgery are shown in Table IV. Among these 13 patients, LNM was present in three cases (23.1%). There was no significant difference between the LNM and non-LNM subgroups in terms of age, sex or tumor location, size, shape, circumference or differentiation.
Discussion
With the advancement of endoscopic equipment, ER has been widely used to treat early esophageal cancer (23,24). Moreover, ER has been shown to be effective for early esophageal cancer and can be used to histologically evaluate submucosal infiltration and LVI (7,8). This can help decide whether to recommend additional treatment following radical (R0) ER. ER is mostly curative in early esophageal cancer (11). However, the best adjuvant treatment methods following non-CR are still unclear (11,18), so subsequent curative treatment strategies need to be established. Xu et al (25) found that repeated esophageal ESD provides an alternative choice for recurrent superficial ESCC but did not assess early repeated ESD immediately following non-CR (confirmed pathologically). The focus of the present study was to propose treatment strategies for patients with only LM+ following non-CR.
Previous studies have shown that, when considering the age and complications (diabetes, cardiovascular and cerebrovascular diseases) of patients, additional ER is an option for patients with non-CR, as the overall survival rate and incidence of adverse events of these patients are not significantly different from those of patients undergoing surgery (26,27). Toya et al (28) recommended close follow-up as an alternative to surgery as there was no difference in the cancer-specific survival rate between the patients in these two groups (close follow-up or surgery) of their study. Additional surgical treatment after non-CR considering patient age and complications is controversial (27). Similarly, the present study found that older patients were more likely to choose re-ER as subsequent therapy. Due to perioperative risks and/or short life expectancy, old age is an important reason for forgoing additional surgery following non-CR (29–31). The aforementioned studies suggested that older patients choose conservative treatment over surgical treatment.
In the research of gastric cancer, certain scholars have found that the poorer the differentiation type, the more directions of invasion the tumor has and the total length of LM affected by the tumor is significantly associated with a non-CR of residual tumor caused by LM+ (32–35). Similarly, in the present study, in patients with non-CR of ESCC, residual cancer was more common when there was a poorly differentiated histology and multiple LM+.
Certain studies have shown that patients with ESCC and deep mucosal infiltration (pT1a-m3), submucosal involvement (pT1b-m1-3) or LVI are considered to be at high risk of LNM and esophagectomy and lymph node dissection are recommended (36,37). However, in other studies, the incidence of LNM in esophageal resection specimens is 0–30%, the perioperative mortality rate is 0–14% and the incidence of serious complications is 26–43% (13,38–43). These findings are consistent with the results of the present study. In the present study, three patients who underwent additional surgery (3/13, 23.1%) had serious complications. Therefore, the present results do not support recommendations for additional surgery.
In addition, three patients (3/13, 23.1%) had LNM. Searching for accurate risk factors for LNM will help to determine whether additional surgical treatment is needed. Previous studies have shown that surgery is not the best option for patients with early esophageal cancer whose ER is non-curative (44,45). Most notably, esophagectomy with lymphadenectomy cannot prevent tumor recurrence and the 5-year survival rate of T1N1 esophageal cancer following esophagectomy is <40% (46,47). Therefore, organ preservation strategy in the management of patients with early esophageal cancer has been implemented in daily clinical practice when patients refuse or are not suitable for surgery, but evaluation of whether other alternatives can bring greater benefits is needed. The positive margin may serve a role in patient prognosis (22) but a more detailed prognostic analysis needs to be confirmed by a multicenter study with long-term follow-up.
The present study investigated the optimal treatment strategy of only LM+ ESCC with non-curative ER. Younger patients with multiple LM+ and poorly differentiated histological lesions often chose additional surgical treatment. By contrast, older patients with single LM+ involvement and well-differentiated lesions were more likely to receive re-ER. There was no recurrence or metastasis in patients who received re-ER during the limited follow-up period (36.1±24.1 months) of the study. These results suggested that additional endoscopic treatment for patients with only LM+ following ER may be sufficient to remove residual tumors. Although some scholars have suggested that ER combined with radiotherapy and chemotherapy may be effective (48,49), the present study did not include patients who had received radiotherapy and chemotherapy so similar conclusions cannot be made.
The present study had certain limitations. Firstly, it was retrospective and single center, the number of cases was small and other endoscopic treatments (such as argon plasma coagulation and laser, photodynamic and microwave coagulation therapy) were not involved. Further studies on endoscopic treatment is required to conclude whether ER is useful. Secondly, the follow-up time was short, which may lead to bias in judging recurrence and metastasis of these patients. A multicenter long follow-up study is needed to verify the results of the present study. Thirdly, additional surgery was performed more often in patients with poor prognosis and/or multiple LM+, thereby potentially affecting the results.
In conclusion, re-ER may be adequate for patients with only LM+ and non-curative ER, especially older patients and those for whom surgical treatment is not recommended. This strategy is feasible, at least in the medium-term. Further studies, including large-scale, population-based, multicenter and prospective studies, should be conducted to evaluate additional endoscopic treatment strategies for patients with LM+ early ESCC after non-curative ER.
Acknowledgements
Not applicable.
Funding
The present study was supported by The Key Topics of Medical Science Research of Hebei Provincial Health Commission (grant no. 20190765).
Availability of data and materials
The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
Authors' contributions
YF and BQL designed the study. YF and SG confirm the authenticity of all the raw data. YF and WW collected clinical and pathological data of patients. SG and YF analyzed the data. BQL and WW contributed to the interpretation of results. All authors have read and approved the final manuscript.
Ethics approval and consent to participate
All patients agreed to participate in the present study and signed an informed consent form. The study was approved by the Ethics Committee of the Fourth Hospital of Hebei Medical University (2020YB318) (Shijiazhuang, China).
Patient consent for publication
Not applicable.
Competing interests
The authors declare that they have no competing interests.
References
Ferlay J, Colombet M, Soerjomataram I, Mathers C, Parkin DM, Piñeros M, Znaor A and Bray F: Estimating the global cancer incidence and mortality in 2018: GLOBOCAN sources and methods. Int J Cancer. 144:1941–1953. 2019. View Article : Google Scholar : PubMed/NCBI | |
Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A and Bray F: Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 71:209–249. 2021. View Article : Google Scholar : PubMed/NCBI | |
Chen W, Zheng R, Baade PD, Zhang S, Zeng H, Bray F, Jemal A, Yu XQ and He J: Cancer statistics in China, 2015. CA Cancer J Clin. 66:115–132. 2016. View Article : Google Scholar : PubMed/NCBI | |
Siegel RL, Miller KD and Jemal A: Cancer Statistics, 2017. CA Cancer J Clin. 67:7–30. 2017. View Article : Google Scholar : PubMed/NCBI | |
Bosetti C, Levi F, Ferlay J, Garavello W, Lucchini F, Bertuccio P, Negri E and La Vecchia C: Trends in oesophageal cancer incidence and mortality in Europe. Int J Cancer. 122:1118–1129. 2008. View Article : Google Scholar : PubMed/NCBI | |
Oyama T, Takahasi A, Takeuchi M, Ishihara R, Tanaka M, Odfa I and Abe S: Long-term prognosis of superficial esophageal cancers at least 50 mm in diameter treated by endoscopic submucosal dissection. United European Gastroenterol J. 2:A4222014. | |
Phoa KN, Pouw RE, Bisschops R, Pech O, Ragunath K, Weusten BL, Schumacher B, Rembacken B, Meining A, Messmann H, et al: Multimodality endoscopic eradication for neoplastic Barrett oesophagus: Results of an European multicentre study (EURO-II). Gut. 65:555–562. 2016. View Article : Google Scholar : PubMed/NCBI | |
Pech O, May A, Manner H, Behrens A, Pohl J, Weferling M, Hartmann U, Manner N, Huijsmans J, Gossner L, et al: Long-term efficacy and safety of endoscopic resection for patients with mucosal adenocarcinoma of the esophagus. Gastroenterology. 146:652–660.e1. 2014. View Article : Google Scholar : PubMed/NCBI | |
Guan CT, Song GH, Li BY, Gong YW, Hao CQ, Xue LY, Chen WQ and Chen W: Endoscopy screening effect on stage distributions of esophageal cancer: A cluster randomized cohort study in China. Cancer Sci. 109:1995–2002. 2018. View Article : Google Scholar : PubMed/NCBI | |
Merkow RP, Bilimoria KY, Keswani RN, Chung J, Sherman KL, Knab LM, Posner MC and Bentrem D: Treatment trends, risk of lymph node metastasis, and outcomes for localized esophageal cancer. J Natl Cancer Inst. 106:dju133. 2014. View Article : Google Scholar : PubMed/NCBI | |
Pimentel-Nunes P, Dinis-Ribeiro M, Ponchon T, Repici A, Vieth M, De Ceglie A, Amato A, Berr F, Bhandari P, Bialek A, et al: Endoscopic submucosal dissection: European society of gastrointestinal endoscopy (ESGE) guideline. Endoscopy. 47:829–854. 2015. View Article : Google Scholar : PubMed/NCBI | |
Degisors S, Pasquer A, Renaud F, Béhal H, Hec F, Gandon A, Vanderbeken M, Caranhac G, Duhamel A, Piessen G, et al: Are thoracotomy and/or intrathoracic anastomosis still predictors of postoperative mortality after esophageal cancer surgery?: A nationwide study. Ann Surg. 266:854–862. 2017. View Article : Google Scholar : PubMed/NCBI | |
Dermine S, Leconte M, Leblanc S, Dousset B, Terris B, Berger A, Berger A, Rahmi G, Lepilliez V, Plomteux O, et al: Outcomes of esophagectomy after noncurative endoscopic resection of early esophageal cancer. Ther Adv Gastroenterol. 12:17562848198925562019. View Article : Google Scholar : PubMed/NCBI | |
Wright CD, Kucharczuk JC, O'Brien SM, Grab JD and Allen MS; Society of Thoracic Surgeons General Thoracic Surgery Database, : Predictors of major morbidity and mortality after esophagectomy for esophageal cancer: A society of thoracic surgeons general thoracic surgery database risk adjustment model. J Thorac Cardiovasc Surg. 137:587–596. 2009. View Article : Google Scholar : PubMed/NCBI | |
Kohn GP, Galanko JA, Meyers MO, Feins RH and Farrell TM: National trends in esophageal surgery-are outcomes as good as we believe? J Gastrointest Surg. 13:1900–1910; discussion 1910-2. 2009. View Article : Google Scholar : PubMed/NCBI | |
Funk LM, Gawande AA, Semel ME, Lipsitz SR, Berry WR, Zinner MJ and Jha AK: Esophagectomy outcomes at low-volume hospitals: The association between systems characteristics and mortality. Ann Surg. 253:912–917. 2011. View Article : Google Scholar : PubMed/NCBI | |
Raymond DP, Seder CW, Wright CD, Magee MJ, Kosinski AS, Cassivi SD, Grogan EL, Blackmon SH, Allen MS, Park BJ, et al: Predictors of major morbidity or mortality after resection for esophageal cancer: A society of thoracic surgeons general thoracic surgery database risk adjustment model. Ann Thorac Surg. 102:207–214. 2016. View Article : Google Scholar : PubMed/NCBI | |
Ishihara R, Arima M, Iizuka T, Oyama T, Katada C, Kato M, Goda K, Goto O, Tanaka K, Yano T, et al: Endoscopic submucosal dissection/endoscopic mucosal resection guidelines for esophageal cancer. Dig Endosc. 32:452–493. 2020. View Article : Google Scholar : PubMed/NCBI | |
Park JS, Youn YH, Park JJ, Kim JH and Park H: Clinical outcomes of endoscopic submucosal dissection for superficial esophageal squamous neoplasms. Clin Endosc. 49:168–175. 2016. View Article : Google Scholar : PubMed/NCBI | |
Choi JY, Park YS, Jung HY, Ahn JY, Kim MY, Lee JH, Choi KS, Kim DH, Choi KD, Song HJ, et al: Feasibility of endoscopic resection in superficial esophageal squamous carcinoma. Gastrointest Endosc. 73:881–889, 889.e1-2. 2011. View Article : Google Scholar : PubMed/NCBI | |
Sano T and Aiko T: New Japanese classifications and treatment guidelines for gastric cancer: Revision concepts and major revised points. Gastric Cancer. 14:97–100. 2011. View Article : Google Scholar : PubMed/NCBI | |
Feng Y, Wei W, Guo S and Li BQ: Associated risk factor analysis and the prognostic impact of positive resection margins after endoscopic resection in early esophageal squamous cell carcinoma. Exp Ther Med. 24:4572022. View Article : Google Scholar : PubMed/NCBI | |
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. 70:860–866. 2009. View Article : Google Scholar : PubMed/NCBI | |
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. View Article : Google Scholar : PubMed/NCBI | |
Xu JQ, Zhang ZC, Chen WF, Xu MD, Chen SY, Zhong YS, Zhang YQ, Hu JW, Cai MY, Yao LQ, et al: Repeat endoscopic submucosal dissection as salvage treatment for local recurrence of esophageal squamous cell carcinoma after initial endoscopic submucosal dissection. Gastrointest Endosc. 96:18–27.e1. 2022. View Article : Google Scholar : PubMed/NCBI | |
Bae SY, Jang TH, Min BH, Lee JH, Rhee PL, Rhee JC and Kim JJ: Early additional endoscopic submucosal dissection in patients with positive lateral resection margins after initial endoscopic submucosal dissection for early gastric cancer. Gastrointest Endosc. 75:432–436. 2012. View Article : Google Scholar : PubMed/NCBI | |
Yamanouchi K, Ogata S, Sakata Y, Tsuruoka N, Shimoda R, Nakayama A, Akutagawa T, Shirai S, Takeshita E, Yamamoto K, et al: Effect of additional surgery after noncurative endoscopic submucosal dissection for early gastric cancer. Endosc Int Open. 4:E24–E29. 2016.PubMed/NCBI | |
Toya Y, Endo M, Nakamura S, Akasaka R, Kosaka T, Yanai S, Kawasaki K, Koeda K, Sugai T and Matsumoto T: Clinical outcomes of curative endoscopic submucosal dissection with negative resected margins for gastric cancer. Gastrointest Endosc. 6:1218–1224. 2017. View Article : Google Scholar : PubMed/NCBI | |
Oda I, Gotoda T, Sasako M, Sano T, Katai H, Fukagawa T, Shimoda T, Emura F and Saito D: Treatment strategy after non-curative endoscopic resection of early gastric cancer. Br J Surg. 95:1495–1500. 2008. View Article : Google Scholar : PubMed/NCBI | |
Kusano C, Iwasaki M, Kaltenbach T, Conlin A, Oda I and Gotoda T: Should elderly patients undergo additional surgery after noncurative endoscopic resection for early gastric cancer? Long-term comparative outcomes. Am J Gastroenterol. 106:1064–1069. 2011. View Article : Google Scholar : PubMed/NCBI | |
Pyo JH, Lee H, Min BH, Lee JH, Kim KM, Yoo H, Ahn S, An JY, Choi MG, Lee JH, et al: Comparison of long-term outcomes after non-curative endoscopic resection in older patients with early gastric cancer. Ann Surg Oncol. 24:2624–2631. 2017. View Article : Google Scholar : PubMed/NCBI | |
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. View Article : Google Scholar : PubMed/NCBI | |
Yoon H, Kim SG, Choi J, Im JP, Kim JS, Kim WH and Jung HC: Risk factors of residual or recurrent tumor in patients with a tumor-positive resection margin after endoscopic resection of early gastric cancer. Surg Endosc. 27:1561–1568. 2013. View Article : Google Scholar : PubMed/NCBI | |
Kim TK, Kim GH, Park DY, Lee BE, Jeon TY, Kim DH, Jo HJ and Song GA: Risk factors for local recurrence in patients with positive lateral resection margins after endoscopic submucosal dissection for early gastric cancer. Surg Endosc. 29:2891–2898. 2015. View Article : Google Scholar : PubMed/NCBI | |
Sekiguchi M, Suzuki H, Oda I, Abe S, Nonaka S, Yoshinaga S, Taniguchi H, Sekine S, Kushima R and Saito Y: Risk of recurrent gastric cancer after endoscopic resection with a positive lateral margin. Endoscopy. 46:273–278. 2014. View Article : Google Scholar : PubMed/NCBI | |
Yamashina T, Ishihara R, Nagai K, Matsuura N, Matsui F, Ito T, Fujii M, Yamamoto S, Hanaoka N, Takeuchi Y, et al: Long-term outcome and metastatic risk after endoscopic resection of superficial esophageal squamous cell carcinoma. Am J Gastroenterol. 108:544–551. 2013. View Article : Google Scholar : PubMed/NCBI | |
Takubo K, Aida J, Sawabe M, Kurosumi M, Arima M, Fujishiro M and Arai T: Early squamous cell carcinoma of the oesophagus: The Japanese viewpoint. Histopathology. 51:733–742. 2007. View Article : Google Scholar : PubMed/NCBI | |
Kitagawa Y, Uno T, Oyama T, Kato K, Kato H, Kawakubo H, Kawamura O, Kusano M, Kuwano H, Takeuchi H, et al: Esophageal cancer practice guidelines 2017 edited by the Japan esophageal society: Part 2. Esophagus. 16:25–43. 2019. View Article : Google Scholar : PubMed/NCBI | |
Wang S, Huang Y, Xie J, Zhuge L, Shao L, Xiang J, Zhang Y, Sun Y, Hu H, Chen S, et al: Does delayed esophagectomy after endoscopic resection affect outcomes in patients with stage T1 esophageal cancer? A propensity score-based analysis. Surg Endosc. 32:1441–1448. 2018. View Article : Google Scholar : PubMed/NCBI | |
Ikeda A, Hoshi N, Yoshizaki T, Fujishima Y, Ishida T, Morita Y, Ejima Y, Toyonaga T, Kakechi Y, Yokosaki H and Azuma T: Endoscopic submucosal dissection (ESD) with additional therapy for superficial esophageal cancer with submucosal invasion. Intern Med. 54:2803–2813. 2015. View Article : Google Scholar : PubMed/NCBI | |
Molena D, Schlottmann F, Boys JA, Blackmon SH, Dickinson KJ, Dunst CM, Hofstetter WL, Lada MJ, Louie BE, Mungo B, et al: Esophagectomy following endoscopic resection of submucosal esophageal cancer: A highly curative procedure even with nodal metastases. J Gastrointest Surg. 21:62–67. 2017. View Article : Google Scholar : PubMed/NCBI | |
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. View Article : Google Scholar : PubMed/NCBI | |
Suzuki G, Yamazaki H, Aibe N, Masui K, Sasaki N, Shimizu D, Kimoto T, Shiozaki A, Dohi O, Fujiwara H, et al: Endoscopic submucosal dissection followed by chemoradiotherapy for superficial esophageal cancer: Choice of new approach. Radiat Oncol. 13:2462018. View Article : Google Scholar : PubMed/NCBI | |
Hirasawa K, Kokawa A, Oka H, Yahara S, Sasaki T, Nozawa A and Tanaka K: Superficial adenocarcinoma of the esophagogastric junction: Long-term results of endoscopic submucosal dissection. Gastrointest Endosc. 72:960–966. 2010. View Article : Google Scholar : PubMed/NCBI | |
Motoyama S, Jin M, Matsuhashi T, Nanjo H, Ishiyama K, Sato Y, Yoshino K, Sasaki T, Wakita A, Saito H, et al: Outcomes of patients receiving additional esophagectomy after endoscopic resection for clinically mucosal, but pathologically submucosal, squamous cell carcinoma of the esophagus. Surg Today. 43:638–642. 2013. View Article : Google Scholar : PubMed/NCBI | |
Pennathur A, Farkas A, Krasinskas AM, Ferson PF, Gooding WE, Gibson MK, Schuchert MJ, Landreneau RJ and Luketich JD: Esophagectomy for T1 esophageal cancer: Outcomes in 100 patients and implications for endoscopic therapy. Ann Thorac Surg. 87:1048–1055. 2009. View Article : Google Scholar : PubMed/NCBI | |
Dubecz A, Kern M, Solymosi N, Schweigert M and Stein HJ: Predictors of lymph node metastasis in surgically resected T1 esophageal cancer. Ann Thorac Surg. 99:1879–1886. 2015. View Article : Google Scholar : PubMed/NCBI | |
Kawaguchi1 G, Sasamoto R, Abe A, Ohta A, Sato H, Tanaka K, Maruyama K, Kaizu M, Ayukawa F, Yamana N, et al: The effectiveness of endoscopic submucosal dissection followed by chemoradiotherapy for superficial esophageal cancer. Radiat Oncol. 10:312015. View Article : Google Scholar | |
Kam TY, Kountouri M, Roth A, Frossard JL, Huber O, Mönig S and Zilli T: Endoscopic resection with adjuvant chemo-radiotherapy for superficial esophageal squamous cell carcinoma: A critical review. Crit Rev Oncol Hemat. 124:61–65. 2018. View Article : Google Scholar : PubMed/NCBI |