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  • 1. Aims and Scope

    Gut and Liver is an international journal of gastroenterology, focusing on the gastrointestinal tract, liver, biliary tree, pancreas, motility, and neurogastroenterology. Gut atnd Liver delivers up-to-date, authoritative papers on both clinical and research-based topics in gastroenterology. The Journal publishes original articles, case reports, brief communications, letters to the editor and invited review articles in the field of gastroenterology. The Journal is operated by internationally renowned editorial boards and designed to provide a global opportunity to promote academic developments in the field of gastroenterology and hepatology. +MORE

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    Yong Chan Lee Professor of Medicine
    Director, Gastrointestinal Research Laboratory
    Veterans Affairs Medical Center, Univ. California San Francisco
    San Francisco, USA

    Deputy Editor

    Deputy Editor
    Jong Pil Im Seoul National University College of Medicine, Seoul, Korea
    Robert S. Bresalier University of Texas M. D. Anderson Cancer Center, Houston, USA
    Steven H. Itzkowitz Mount Sinai Medical Center, NY, USA
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    All papers submitted to Gut and Liver are reviewed by the editorial team before being sent out for an external peer review to rule out papers that have low priority, insufficient originality, scientific flaws, or the absence of a message of importance to the readers of the Journal. A decision about these papers will usually be made within two or three weeks.
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Pitfalls in Endoscopic Submucosal Dissection for Early Gastric Cancer with Papillary Adenocarcinoma

Gwang Ha Kim

Department of Internal Medicine, Pusan National University School of Medicine and Biomedical Research Institute, Pusan National University Hospital, Busan, Korea

Correspondence to: Gwang Ha Kim
ORCID https://orcid.org/0000-0001-9721-5734
E-mail doc0224@pusan.ac.kr

See “Clinical Outcome of Endoscopic Submucosal Dissection for Papillary Type Early Gastric Cancer: A Multicenter Study” by Hyun-Deok Shin, et al. on page 426, Vol. 18, No. 3, 2024

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Gut Liver 2024;18(3):368-369. https://doi.org/10.5009/gnl240139

Published online May 15, 2024, Published date May 15, 2024

Copyright © Gut and Liver.

Papillary adenocarcinoma is an uncommon histologic type of gastric cancer accounting for approximately 1% to 3% of early gastric cancers (EGC).1 Histopathologically, the Japanese classification categorizes it as a differentiated type, and the Lauren classification as an intestinal type.2 Therefore, endoscopic submucosal dissection (ESD) is suggested to be a safe therapeutic approach for EGC with papillary adenocarcinoma (EGC-P). However, patients with papillary adenocarcinoma have a poor prognosis compared with those with other differentiated-type histologies; patients with papillary adenocarcinoma have a higher rate of lymph node (LN) and liver metastases and a lower 5-year overall survival rate than those with non-papillary adenocarcinoma.3 In my previous study including 1,583 patients who underwent gastrectomy for EGC, the rate of submucosal invasion was significantly higher in EGC-P than in EGC with non-papillary adenocarcinoma (EGC-NP) having both differentiated-type and undifferentiated-type histologies (71.4% vs 50.8% and 37.6%, respectively). The rate of LN metastasis in EGC-P was higher than that in both EGC-NP histology types (17.9% vs 9.7% and 11.1%, respectively).1 In addition, of the 17 patients who met the current ESD indication, four (23.5%) had lymphovascular invasion (LVI) or LN metastasis. When patients with EGC-P who meet the ESD indication would undergo ESD, approximately one-fourth of them would require additional gastrectomy due to non-curative resection.1

In the current issue of Gut and Liver, Shin et al.4 reported post-ESD outcomes for 97 patients with EGC-P in a multicenter study. EGC-P showed a trend toward distal tumor location and elevated shape. Nine patients (9.3%) had positive resection margins with tumor, and submucosal invasion and LVI were observed in 18 (18.5%) and five (5.2%) patients, respectively; especially, LVI was observed in two patients with mucosal cancers. As the overall curative resection rate was 86.6% (84/97), the authors concluded that ESD was favorable for EGC-P. They also evaluated the risk factors for LN metastasis in 79 patients with EGC-P who underwent surgical resection. Submucosal invasion (odds ratio, 3.735) and LVI (odds ratio, 7.636) were significant risk factors for LN metastasis in multivariate analysis. The fact that the frequency of LVI was not low even in mucosal EGC-P should not be ignored. In another study including 4,140 patients who underwent ESD for differentiated-type EGC, the curative resection rate of EGC-P was 49.4%, which was significantly lower than that of other differentiated-type histologies (82.2%).5 A recent systemic review including 15 studies also showed that submucosal invasion and LVI were frequent in EGC-P, and the curative resection rate was only 67.0% (95% confidence interval, 43.0% to 84.5%).6 Accordingly, ESD should be more carefully applied for EGC-P than for EGC with other differentiated-type histologies.

How can papillary adenocarcinoma be accurately diagnosed before ESD? Although papillary adenocarcinoma is present within a tumor, it may not always be detected through pre-ESD biopsy owing to the limited amount of tissue obtained from endoscopic biopsy and tangential sectioning of specimens.1 Pre-ESD biopsy sometimes reveals a different histology than that observed in the post-ESD specimen, which can be attributed to inter- and intra-observer variability, as well as the histological heterogeneity of gastric cancer.7 Magnifying endoscopy with narrow-band imaging is reported to be effective in diagnosing papillary adenocarcinoma.8-10 The vessels within the epithelial circle pattern on magnifying endoscopy with narrow-band imaging exhibited a sensitivity and specificity of 84.6% and 96.9%, respectively, for diagnosing papillary adenocarcinoma. However, coexisting undifferentiated carcinomas were observed in 22.9% of vessels within the epithelial circle-positive cancers. Therefore, when endoscopic forceps biopsy reveals differentiated-type histology and vessels within the epithelial circle is observed on magnifying endoscopy with narrow-band imaging, papillary adenocarcinoma could be predicted before ESD, even in the absence of typical histopathological features of papillary adenocarcinoma, such as elongated finger-like epithelial projections, in the endoscopic biopsy specimens.

Although the curative resection rate of ESD for EGC-P is lower than that for EGC with other differentiated-type histologies, curative resection shows favorable long-term outcomes.5 The probability of LN metastasis is a very important factor influencing the success of ESD for EGC; LVI is an especially strong predictive factor of LN metastasis. Therefore, detailed histopathological examination of resected specimens is mandatory, especially to detect the presence of LVI after ESD for EGC-P.

G.H.K. is an editorial board member of the journal but was not involved in the peer reviewer selection, evaluation, or decision process of this article. No other potential conflicts of interest relevant to this article were reported.

  1. Lee HJ, Kim GH, Park DY, et al. Endoscopic submucosal dissection for papillary adenocarcinoma of the stomach: is it really safe?. Gastric Cancer 2017;20:978-986.
    Pubmed CrossRef
  2. Japanese Gastric Cancer Association. Japanese Gastric Cancer Treatment Guidelines 2021 (6th edition). Gastric Cancer 2023;26:1-25.
    Pubmed KoreaMed CrossRef
  3. Sekiguchi M, Kushima R, Oda I, et al. Clinical significance of a papillary adenocarcinoma component in early gastric cancer: a single-center retrospective analysis of 628 surgically resected early gastric cancers. J Gastroenterol 2015;50:424-434.
    Pubmed CrossRef
  4. Shin HD, Bang KB, Kang SH, et al. Clinical outcome of endoscopic submucosal dissection for papillary type early gastric cancer: a multicenter study. Gut Liver 2024;18:426-433.
    Pubmed CrossRef
  5. Kim TS, Min BH, Kim KM, Lee JH, Rhee PL, Kim JJ. Endoscopic submucosal dissection for papillary adenocarcinoma of the stomach: low curative resection rate but favorable long-term outcomes after curative resection. Gastric Cancer 2019;22:363-368.
    Pubmed CrossRef
  6. Bang CS, Lee JJ, Baik GH. Endoscopic submucosal dissection of papillary gastric adenocarcinoma; systematic review. J Clin Med 2020;9:1465.
    Pubmed KoreaMed CrossRef
  7. Kim JM, Sohn JH, Cho MY, et al. Pre- and post-ESD discrepancies in clinicopathologic criteria in early gastric cancer: the NECA-Korea ESD for Early Gastric Cancer Prospective Study (N-Keep). Gastric Cancer 2016;19:1104-1113.
    Pubmed KoreaMed CrossRef
  8. Kanemitsu T, Yao K, Nagahama T, et al. The vessels within epithelial circle (VEC) pattern as visualized by magnifying endoscopy with narrow-band imaging (ME-NBI) is a useful marker for the diagnosis of papillary adenocarcinoma: a case-controlled study. Gastric Cancer 2014;17:469-477.
    Pubmed CrossRef
  9. Yao K, Yao T, Uedo N, et al. E-learning system to improve the endoscopic diagnosis of early gastric cancer. Clin Endosc. Epub 2023 Aug 3. https://doi.org/10.5946/ce.2023.087
    CrossRef
  10. Horiuchi Y, Hirasawa T, Fujisaki J. Application of artificial intelligence for diagnosis of early gastric cancer based on magnifying endoscopy with narrow-band imaging. Clin Endosc 2024;57:11-17.
    Pubmed KoreaMed CrossRef

Article

Editorial

Gut and Liver 2024; 18(3): 368-369

Published online May 15, 2024 https://doi.org/10.5009/gnl240139

Copyright © Gut and Liver.

Pitfalls in Endoscopic Submucosal Dissection for Early Gastric Cancer with Papillary Adenocarcinoma

Gwang Ha Kim

Department of Internal Medicine, Pusan National University School of Medicine and Biomedical Research Institute, Pusan National University Hospital, Busan, Korea

Correspondence to:Gwang Ha Kim
ORCID https://orcid.org/0000-0001-9721-5734
E-mail doc0224@pusan.ac.kr

See “Clinical Outcome of Endoscopic Submucosal Dissection for Papillary Type Early Gastric Cancer: A Multicenter Study” by Hyun-Deok Shin, et al. on page 426, Vol. 18, No. 3, 2024

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Body

Papillary adenocarcinoma is an uncommon histologic type of gastric cancer accounting for approximately 1% to 3% of early gastric cancers (EGC).1 Histopathologically, the Japanese classification categorizes it as a differentiated type, and the Lauren classification as an intestinal type.2 Therefore, endoscopic submucosal dissection (ESD) is suggested to be a safe therapeutic approach for EGC with papillary adenocarcinoma (EGC-P). However, patients with papillary adenocarcinoma have a poor prognosis compared with those with other differentiated-type histologies; patients with papillary adenocarcinoma have a higher rate of lymph node (LN) and liver metastases and a lower 5-year overall survival rate than those with non-papillary adenocarcinoma.3 In my previous study including 1,583 patients who underwent gastrectomy for EGC, the rate of submucosal invasion was significantly higher in EGC-P than in EGC with non-papillary adenocarcinoma (EGC-NP) having both differentiated-type and undifferentiated-type histologies (71.4% vs 50.8% and 37.6%, respectively). The rate of LN metastasis in EGC-P was higher than that in both EGC-NP histology types (17.9% vs 9.7% and 11.1%, respectively).1 In addition, of the 17 patients who met the current ESD indication, four (23.5%) had lymphovascular invasion (LVI) or LN metastasis. When patients with EGC-P who meet the ESD indication would undergo ESD, approximately one-fourth of them would require additional gastrectomy due to non-curative resection.1

In the current issue of Gut and Liver, Shin et al.4 reported post-ESD outcomes for 97 patients with EGC-P in a multicenter study. EGC-P showed a trend toward distal tumor location and elevated shape. Nine patients (9.3%) had positive resection margins with tumor, and submucosal invasion and LVI were observed in 18 (18.5%) and five (5.2%) patients, respectively; especially, LVI was observed in two patients with mucosal cancers. As the overall curative resection rate was 86.6% (84/97), the authors concluded that ESD was favorable for EGC-P. They also evaluated the risk factors for LN metastasis in 79 patients with EGC-P who underwent surgical resection. Submucosal invasion (odds ratio, 3.735) and LVI (odds ratio, 7.636) were significant risk factors for LN metastasis in multivariate analysis. The fact that the frequency of LVI was not low even in mucosal EGC-P should not be ignored. In another study including 4,140 patients who underwent ESD for differentiated-type EGC, the curative resection rate of EGC-P was 49.4%, which was significantly lower than that of other differentiated-type histologies (82.2%).5 A recent systemic review including 15 studies also showed that submucosal invasion and LVI were frequent in EGC-P, and the curative resection rate was only 67.0% (95% confidence interval, 43.0% to 84.5%).6 Accordingly, ESD should be more carefully applied for EGC-P than for EGC with other differentiated-type histologies.

How can papillary adenocarcinoma be accurately diagnosed before ESD? Although papillary adenocarcinoma is present within a tumor, it may not always be detected through pre-ESD biopsy owing to the limited amount of tissue obtained from endoscopic biopsy and tangential sectioning of specimens.1 Pre-ESD biopsy sometimes reveals a different histology than that observed in the post-ESD specimen, which can be attributed to inter- and intra-observer variability, as well as the histological heterogeneity of gastric cancer.7 Magnifying endoscopy with narrow-band imaging is reported to be effective in diagnosing papillary adenocarcinoma.8-10 The vessels within the epithelial circle pattern on magnifying endoscopy with narrow-band imaging exhibited a sensitivity and specificity of 84.6% and 96.9%, respectively, for diagnosing papillary adenocarcinoma. However, coexisting undifferentiated carcinomas were observed in 22.9% of vessels within the epithelial circle-positive cancers. Therefore, when endoscopic forceps biopsy reveals differentiated-type histology and vessels within the epithelial circle is observed on magnifying endoscopy with narrow-band imaging, papillary adenocarcinoma could be predicted before ESD, even in the absence of typical histopathological features of papillary adenocarcinoma, such as elongated finger-like epithelial projections, in the endoscopic biopsy specimens.

Although the curative resection rate of ESD for EGC-P is lower than that for EGC with other differentiated-type histologies, curative resection shows favorable long-term outcomes.5 The probability of LN metastasis is a very important factor influencing the success of ESD for EGC; LVI is an especially strong predictive factor of LN metastasis. Therefore, detailed histopathological examination of resected specimens is mandatory, especially to detect the presence of LVI after ESD for EGC-P.

CONFLICTS OF INTEREST

G.H.K. is an editorial board member of the journal but was not involved in the peer reviewer selection, evaluation, or decision process of this article. No other potential conflicts of interest relevant to this article were reported.

References

  1. Lee HJ, Kim GH, Park DY, et al. Endoscopic submucosal dissection for papillary adenocarcinoma of the stomach: is it really safe?. Gastric Cancer 2017;20:978-986.
    Pubmed CrossRef
  2. Japanese Gastric Cancer Association. Japanese Gastric Cancer Treatment Guidelines 2021 (6th edition). Gastric Cancer 2023;26:1-25.
    Pubmed KoreaMed CrossRef
  3. Sekiguchi M, Kushima R, Oda I, et al. Clinical significance of a papillary adenocarcinoma component in early gastric cancer: a single-center retrospective analysis of 628 surgically resected early gastric cancers. J Gastroenterol 2015;50:424-434.
    Pubmed CrossRef
  4. Shin HD, Bang KB, Kang SH, et al. Clinical outcome of endoscopic submucosal dissection for papillary type early gastric cancer: a multicenter study. Gut Liver 2024;18:426-433.
    Pubmed CrossRef
  5. Kim TS, Min BH, Kim KM, Lee JH, Rhee PL, Kim JJ. Endoscopic submucosal dissection for papillary adenocarcinoma of the stomach: low curative resection rate but favorable long-term outcomes after curative resection. Gastric Cancer 2019;22:363-368.
    Pubmed CrossRef
  6. Bang CS, Lee JJ, Baik GH. Endoscopic submucosal dissection of papillary gastric adenocarcinoma; systematic review. J Clin Med 2020;9:1465.
    Pubmed KoreaMed CrossRef
  7. Kim JM, Sohn JH, Cho MY, et al. Pre- and post-ESD discrepancies in clinicopathologic criteria in early gastric cancer: the NECA-Korea ESD for Early Gastric Cancer Prospective Study (N-Keep). Gastric Cancer 2016;19:1104-1113.
    Pubmed KoreaMed CrossRef
  8. Kanemitsu T, Yao K, Nagahama T, et al. The vessels within epithelial circle (VEC) pattern as visualized by magnifying endoscopy with narrow-band imaging (ME-NBI) is a useful marker for the diagnosis of papillary adenocarcinoma: a case-controlled study. Gastric Cancer 2014;17:469-477.
    Pubmed CrossRef
  9. Yao K, Yao T, Uedo N, et al. E-learning system to improve the endoscopic diagnosis of early gastric cancer. Clin Endosc. Epub 2023 Aug 3. https://doi.org/10.5946/ce.2023.087
    CrossRef
  10. Horiuchi Y, Hirasawa T, Fujisaki J. Application of artificial intelligence for diagnosis of early gastric cancer based on magnifying endoscopy with narrow-band imaging. Clin Endosc 2024;57:11-17.
    Pubmed KoreaMed CrossRef
Gut and Liver

Vol.18 No.3
May, 2024

pISSN 1976-2283
eISSN 2005-1212

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