Skip to main content

Advertisement

SpringerLink
Log in

Morphologic pattern analysis of submucosal deformities identified by endoscopic ultrasonography for predicting the depth of invasion in early gastric cancer

  • Published:
Surgical Endoscopy Aims and scope Submit manuscript

Abstract

Background

The aims of this study are to evaluate the usefulness of submucosal deformity pattern analysis with endoscopic ultrasonography (EUS) for predicting the depth of invasion in early gastric cancer (EGC) and the treatment results of endoscopic submucosal dissection (ESD).

Methods

The endoscopic and EUS parameters of 345 patients with endoscopically suspected EGC who underwent endoscopic or surgical resection between July 2012 and May 2017 were retrospectively reviewed. All patients were classified into three categories as follows according to the morphologic type of submucosal deformity identified by EUS: (1) no submucosal deformity, (2) wedge-shaped deformity, and (3) arch-shaped deformity. The presence of an arch-shaped submucosal deformity on EUS and an active endoscopic ulcer or surrounding mucosal fold convergence/clubbing on conventional endoscopy were defined as suggestive of deep submucosal cancer invasion (SCI).

Results

Upper location (p = 0.034) and the presence of an arch-shaped submucosal deformity on EUS (p < 0.001) were significant predictors of deep submucosal invasion, with the presence of an arch-shaped submucosal deformity showing the highest predictive value (odds ratio of 26.27). The overall diagnostic accuracy of EUS for predicting deep SCI was 83.5%, with a sensitivity of 84.0% and a specificity of 83.3%, which were significantly higher than those of conventional endoscopy. A larger lesion size and the presence of an arch-shaped submucosal deformity were significant factors associated with noncurative resection after ESD.

Conclusions

Submucosal deformity pattern analysis with EUS can provide more accurate information than conventional endoscopy for predicting deep SCI. The presence of an arch-shaped submucosal deformity on EUS was an effective predictor of deep SCI and noncurative resection.

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

Similar content being viewed by others

References

  1. Kosaka T, Endo M, Toya Y, Abiko Y, Kudara N, Inomata M, Chiba T, Takikawa Y, Suzuki K, Sugai T (2014) Long-term outcomes of endoscopic submucosal dissection for early gastric cancer: a single-center retrospective study. Dig Endosc 26:183–191

    Article  PubMed  Google Scholar 

  2. Min BH, Kim KM, Park CK, Lee JH, Rhee PL, Rhee JC, Kim JJ (2015) Outcomes of endoscopic submucosal dissection for differentiated-type early gastric cancer with histological heterogeneity. Gastric Cancer 18:618–626

    Article  PubMed  Google Scholar 

  3. Suzuki H, Oda I, Abe S, Sekiguchi M, Mori G, Nonaka S, Yoshinaga S, Saito Y (2016) High rate of 5-year survival among patients with early gastric cancer undergoing curative endoscopic submucosal dissection. Gastric Cancer 19:198–205

    Article  PubMed  Google Scholar 

  4. Yano T, Ishido K, Tanabe S, Wada T, Azuma M, Kawanishi N, Yamane S, Watanabe A, Katada C, Koizumi W (2018) Long-term outcomes of patients with early gastric cancer found to have lesions for which endoscopic treatment is not indicated on histopathological evaluation after endoscopic submucosal dissection. Surg Endosc 32:1314–1323

    Article  PubMed  Google Scholar 

  5. Gotoda T, Yanagisawa A, Sasako M, Ono H, Nakanishi Y, Shimoda T, Kato Y (2000) Incidence of lymph node metastasis from early gastric cancer: estimation with a large number of cases at two large centers. Gastric Cancer 3:219–225

    Article  PubMed  Google Scholar 

  6. Lee HH, Yoo HM, Song KY, Jeon HM, Park CH (2013) Risk of limited lymph node dissection in patients with clinically early gastric cancer: indications of extended lymph node dissection for early gastric cancer. Ann Surg Oncol 20:3534–3540

    Article  PubMed  Google Scholar 

  7. Kwee RM, Kwee TC (2007) Imaging in local staging of gastric cancer: a systematic review. J Clin Oncol 25:2107–2116

    Article  PubMed  Google Scholar 

  8. Kim JH, Song KS, Youn YH, Lee YC, Cheon JH, Song SY, Chung JB (2007) Clinicopathologic factors influence accurate endosonographic assessment for early gastric cancer. Gastrointest Endosc 66:901–908

    Article  PubMed  Google Scholar 

  9. Kim GH, Park DY, Kida M, Kim DH, Jeon TY, Kang HJ, Kim DU, Choi CW, Lee BE, Heo J, Song GA (2010) Accuracy of high-frequency catheter-based endoscopic ultrasonography according to the indications for endoscopic treatment of early gastric cancer. J Gastroenterol Hepatol 25:506–511

    Article  PubMed  Google Scholar 

  10. Okada K, Fujisaki J, Kasuga A, Omae M, Yoshimoto K, Hirasawa T, Ishiyama A, Yamamoto Y, Tsuchida T, Hoshino E, Igarashi M, Takahashi H (2011) Endoscopic ultrasonography is valuable for identifying early gastric cancers meeting expanded-indication criteria for endoscopic submucosal dissection. Surg Endosc 25:841–848

    Article  PubMed  Google Scholar 

  11. Mandai K, Yasuda K (2012) Accuracy of endoscopic ultrasonography for determining the treatment method for early gastric cancer. Gastroenterol Res Pract 2012:245390

    Article  PubMed  PubMed Central  Google Scholar 

  12. Park JS, Kim H, Bang B, Kwon K, Shin Y (2016) Accuracy of endoscopic ultrasonography for diagnosing ulcerative early gastric cancers. Medicine (Baltimore) 95:e3955

  13. Ohashi S, Nakazawa S, Yoshino J (1989) Endoscopic ultrasonography in the assessment of invasive gastric cancer. Scand J Gastroenterol 24:1039–1048

    Article  CAS  PubMed  Google Scholar 

  14. Kida M, Tanabe S, Watanabe M, Kokutou M, Kondou I, Yamada Y, Sakaguchi T, Saigenji K (1998) Staging of gastric cancer with endoscopic ultrasonography and endoscopic mucosal resection. Endoscopy 30(Suppl 1):A64–A68

    PubMed  Google Scholar 

  15. Matsumoto Y, Yanai H, Tokiyama H, Nishiaki M, Higaki S, Okita K (2000) Endoscopic ultrasonography for diagnosis of submucosal invasion in early gastric cancer. J Gastroenterol 35:326–331

    Article  CAS  PubMed  Google Scholar 

  16. Sakita T, Oguro Y, Takasu S, Fukutomi H, Miwa T (1971) Observations on the healing of ulcerations in early gastric cancer. The life cycle of the malignant ulcer. Gastroenterology 60:835–839 passim

    Article  CAS  PubMed  Google Scholar 

  17. Minamoto T, Ooi A, Okada Y, Mai M, Nagai Y, Nakanishi I (1988) Desmoplastic reaction of gastric carcinoma: a light- and electron-microscopic immunohistochemical analysis using collagen type-specific antibodies. Hum Pathol 19:815–821

    Article  CAS  PubMed  Google Scholar 

  18. Matsui H, Kubochi K, Shimada A, Hasumi A (2000) Desmoplastic response in scirrhous gastric carcinoma: imbalance between collagen synthesis and degradation. Anticancer Res 20:4733–4738

    CAS  PubMed  Google Scholar 

  19. Im JP, Kim SG, Kim JS, Jung HC, Song IS (2009) Time-dependent morphologic change in depressed-type early gastric cancer. Surg Endosc 23:2509–2514

    Article  PubMed  Google Scholar 

  20. Lee JI, Kim JH, Kim JH, Choi BJ, Song YJ, Choi SB, Bae YS, Lee SH, Jee SR, Kang MS, Seol SY (2012) Indication for endoscopic treatment of ulcerative early gastric cancer according to depth of ulcer and morphological change. J Gastroenterol Hepatol 27:1718–1725

    Article  PubMed  Google Scholar 

  21. Sano T, Okuyama Y, Kobori O, Shimizu T, Morioka Y (1990) Early gastric cancer. Endoscopic diagnosis of depth of invasion. Dig Dis Sci 35:1340–1344

    Article  CAS  PubMed  Google Scholar 

  22. Yanai H, Noguchi T, Mizumachi S, Tokiyama H, Nakamura H, Tada M, Okita K (1999) A blind comparison of the effectiveness of endoscopic ultrasonography and endoscopy in staging early gastric cancer. Gut 44:361–365

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Choi J, Kim SG, Im JP, Kim JS, Jung HC, Song IS (2010) Comparison of endoscopic ultrasonography and conventional endoscopy for prediction of depth of tumor invasion in early gastric cancer. Endoscopy 42:705–713

    Article  CAS  PubMed  Google Scholar 

  24. Choi J, Kim SG, Im JP, Kim JS, Jung HC, Song IS (2011) Endoscopic prediction of tumor invasion depth in early gastric cancer. Gastrointest Endosc 73:917–927

    Article  PubMed  Google Scholar 

  25. Kang DH, Choi CW, Kim HW, Park SB, Kim SJ, Nam HS, Ryu DG (2017) Location characteristics of early gastric cancer treated with endoscopic submucosal dissection. Surg Endosc 31:4673–4679

    Article  PubMed  Google Scholar 

  26. Akashi Y, Noguchi T, Nagai K, Kawahara K, Shimada T (2011) Cytoarchitecture of the lamina muscularis mucosae and distribution of the lymphatic vessels in the human stomach. Med Mol Morphol 44:39–45

    Article  PubMed  Google Scholar 

  27. Park S, Chun HJ, Kwon YD, Keum B, Seo YS, Kim YS, Jeen YT, Um SH, Kim CD, Ryu HS, Lee JH, Chae YS (2008) Stretching causes extensive changes of gastric submucosa: is it acceptable to define 500 microm as the safe margin? Gut Liver 2:199–204

    Article  PubMed  PubMed Central  Google Scholar 

  28. Lee YJ, Kim JH, Park JJ, Youn YH, Park H, Kim JW, Choi SH, Noh SH (2016) The implications of endoscopic ulcer in early gastric cancer: can we predict clinical behaviors from endoscopy? PLoS ONE 11:e0164339

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Nagahama T, Yao K, Imamura K, Kojima T, Ohtsu K, Chuman K, Tanabe H, Yamaoka R, Iwashita A (2017) Diagnostic performance of conventional endoscopy in the identification of submucosal invasion by early gastric cancer: the “non-extension sign” as a simple diagnostic marker. Gastric Cancer 20:304–313

    Article  PubMed  Google Scholar 

  30. Higashimaya M, Oka S, Tanaka S, Sanomura Y, Yoshida S, Hiyama T, Arihiro K, Shimamoto F, Chayama K (2013) Outcome of endoscopic submucosal dissection for gastric neoplasm in relationship to endoscopic classification of submucosal fibrosis. Gastric Cancer 16:404–410

    Article  PubMed  Google Scholar 

  31. Myung YS, Hong SJ, Han JP, Park KW, Ko BM, Lee MS (2017) Effects of administration of a proton pump inhibitor before endoscopic submucosal dissection for differentiated early gastric cancer with ulcer. Gastric Cancer 20:200–206

    Article  CAS  PubMed  Google Scholar 

  32. Lee JY, Choi IJ, Kim CG, Cho SJ, Kook MC, Ryu KW, Kim YW (2016) Therapeutic decision-making using endoscopic ultrasonography in endoscopic treatment of early gastric cancer. Gut Liver 10:42–50

    Article  PubMed  PubMed Central  Google Scholar 

  33. Tsujii Y, Kato M, Inoue T, Yoshii S, Nagai K, Fujinaga T, Maekawa A, Hayashi Y, Akasaka T, Shinzaki S, Watabe K, Nishida T, Iijima H, Tsujii M, Takehara T (2015) Integrated diagnostic strategy for the invasion depth of early gastric cancer by conventional endoscopy and EUS. Gastrointest Endosc 82:452–459

    Article  PubMed  Google Scholar 

  34. Ohnita K, Isomoto H, Yamaguchi N, Fukuda E, Nakamura T, Nishiyama H, Mizuta Y, Akiyama M, Nakao K, Kohno S, Shikuwa S (2009) Factors related to the curability of early gastric cancer with endoscopic submucosal dissection. Surg Endosc 23:2713–2719

    Article  PubMed  Google Scholar 

  35. Jeong JY, Oh YH, Yu YH, Park HS, Lee HL, Eun CS, Han DS (2012) Does submucosal fibrosis affect the results of endoscopic submucosal dissection of early gastric tumors? Gastrointest Endosc 76:59–66

    Article  PubMed  Google Scholar 

  36. Fujiya K, Takizawa K, Tokunaga M, Kawata N, Hikage M, Makuuchi R, Tanizawa Y, Bando E, Kawamura T, Tanaka M, Kakushima N, Ono H, Terashima M (2018) The value of diagnostic endoscopic submucosal dissection for patients with clinical submucosal invasive early gastric cancer. Gastric Cancer 21:124–132

    Article  PubMed  Google Scholar 

  37. Kim SJ, Choi CW, Kang DH, Kim HW, Park SB, Nam HS, Shin DH (2017) Factors associated with the efficacy of miniprobe endoscopic ultrasonography after conventional endoscopy for the prediction of invasion depth of early gastric cancer. Scand J Gastroenterol 52:864–869

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by 2018 Inje University Busan Paik Hospital research grant.

Author information

Author notes

  1. Tae Young Kim and Nam Hee Yi share co-first authorships.

Authors and Affiliations

  1. Department of Gastroenterology, Busan Paik Hospital, Inje University College of Medicine, 75 Bokjiro, Busanjin-Gu, Busan, 47392, South Korea

    Tae Young Kim, Nam Hee Yi, Jin Won Hwang & Ji Hyun Kim

  2. Department of Internal Medicine, Pusan National University School of Medicine, Busan, South Korea

    Gwang Ha Kim

  3. Department of Pathology, Busan Paik Hospital, Inje University College of Medicine, Busan, South Korea

    Mi Seon Kang

Authors
  1. Tae Young Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nam Hee Yi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jin Won Hwang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ji Hyun Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Gwang Ha Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mi Seon Kang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ji Hyun Kim.

Ethics declarations

Disclosures

Drs. Tae Young Kim, Nam Hee Yi, Jin Won Hwang, Ji Hyun Kim, Gwang Ha Kim, and Mi Seon Kang have no conflicts of interest or financial ties to disclose.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kim, T.Y., Yi, N.H., Hwang, J.W. et al. Morphologic pattern analysis of submucosal deformities identified by endoscopic ultrasonography for predicting the depth of invasion in early gastric cancer. Surg Endosc 33, 2169–2180 (2019). https://doi.org/10.1007/s00464-018-6496-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00464-018-6496-2

Keywords

Search

Navigation