Surgical Endoscopy

, Volume 28, Issue 7, pp 2097–2105 | Cite as

Clinicopathologic factors and outcomes of histologic discrepancy between differentiated and undifferentiated types after endoscopic resection of early gastric cancer

  • Choong Nam Shim
  • Hyunki Kim
  • Dong Wook Kim
  • Hyun Soo Chung
  • Jun Chul Park
  • Hyuk Lee
  • Sung Kwan Shin
  • Sang Kil Lee
  • Yong Chan LeeEmail author



Histologic discrepancies among specimens obtained by forceps biopsy and endoscopic resection (ER) between the differentiated and undifferentiated types often occur in early gastric cancer (EGC). This study aimed to evaluate the predictive clinicopathologic characteristics and clinical implications of histologic discrepancies in EGC.


From August 2005 to March 2012, 596 lesions from 579 patients underwent ER for EGC. The lesions studied were diagnosed as the differentiated histologic type from forceps biopsy specimens. The lesions were grouped according to the occurrence of histologic discrepancy between the differentiated and undifferentiated types in specimens obtained by ER as concordant (n = 570) or discordant (n = 26). The main outcome measures were en bloc resection, complete resection, and curative resection rates.


The histologic discrepancy rate was 4.4 % among the studied lesions. Larger size, lesion location in the mid third of the stomach, easy friability, exudates, and submucosal invasion shown on endoscopic ultrasound were significantly related to histologic discrepancy in the univariate analysis. In the multivariate analysis, lesion location in the mid third of the stomach [odds ratio (OR) 5.34, 95 % confidence interval (CI) 1.59–19.13] and easy friability (OR 29.26, 95 % CI 2.30 to >999.9) were significant factors associated with histologic discrepancy. The complete resection and curative resection rates were significantly lower and the additional operation rates after ER were significantly higher in the discordant group.


The EGCs with histologic discrepancy between the differentiated and undifferentiated types changed the therapeutic outcomes of ER. Easily friable lesions located in the mid third of the stomach carry a significant risk for histologic discrepancy in undifferentiated histology when ER of EGCs is performed.


Early gastric cancer Endoscopic resection Histology Discrepancy 



Endoscopic resection


Early gastric cancer


Endoscopic ultrasound


Endoscopic mucosal resection


Endoscopic submucosal dissection



Choong Nam Shim, Hyunki Kim, Dong Wook Kim, Hyun Soo Chung, Jun Chul Park, Hyuk Lee, Sung Kwan Shin, Sang Kil Lee, and Yong Chan Lee have no conflicts of interest or financial ties to disclose.


  1. 1.
    Murakami T (1971) Pathomorphological diagnosis: definition and gross classification of early gastric cancer. Gann Monogr Cancer Res 11:53–55Google Scholar
  2. 2.
    Ahn YO, Park BJ, Yoo KY, Kim NK, Heo DS, Lee JK, Ahn HS, Kang DH, Kim H, Lee MS et al (1991) Incidence estimation of stomach cancer among Koreans. J Korean Med Sci 6:7–14PubMedCentralPubMedGoogle Scholar
  3. 3.
    Nakamura K, Ueyama T, Yao T, Xuan ZX, Ambe K, Adachi Y, Yakeishi Y, Matsukuma A, Enjoji M (1992) Pathology and prognosis of gastric carcinoma: findings in 10,000 patients who underwent primary gastrectomy. Cancer 70:1030–1037PubMedCrossRefGoogle Scholar
  4. 4.
    Tada M, Murakami A, Karita M, Yanai H, Okita K (1993) Endoscopic resection of early gastric cancer. Endoscopy 25:445–450PubMedCrossRefGoogle Scholar
  5. 5.
    Hirao M, Masuda K, Asanuma T, Naka H, Noda K, Matsuura K, Yamaguchi O, Ueda N (1988) Endoscopic resection of early gastric cancer and other tumors with local injection of hypertonic saline–epinephrine. Gastrointest Endosc 34:264–269PubMedCrossRefGoogle Scholar
  6. 6.
    Gotoda T, Kondo H, Ono H, Saito Y, Yamaguchi H, Saito D, Yokota T (1999) A new endoscopic mucosal resection procedure using an insulation-tipped electrosurgical knife for rectal flat lesions: report of two cases. Gastrointest Endosc 50:560–563PubMedCrossRefGoogle Scholar
  7. 7.
    Ohkuwa M, Hosokawa K, Boku N, Ohtu A, Tajiri H, Yoshida S (2001) New endoscopic treatment for intramucosal gastric tumors using an insulated-tip diathermic knife. Endoscopy 33:221–226PubMedCrossRefGoogle Scholar
  8. 8.
    Soetikno RM, Gotoda T, Nakanishi Y, Soehendra N (2003) Endoscopic mucosal resection. Gastrointest Endosc 57:567–579PubMedCrossRefGoogle Scholar
  9. 9.
    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 3:219–225PubMedCrossRefGoogle Scholar
  10. 10.
    Japanese Gastric Association (2011) Japanese gastric cancer treatment guidelines 2010 (version 3). Gastric Cancer 14:113–123CrossRefGoogle Scholar
  11. 11.
    Lee CK, Chung IK, Lee SH, Kim SP, Lee SH, Lee TH, Kim HS, Park SH, Kim SJ, Lee JH, Cho HD, Oh MH (2010) Is endoscopic forceps biopsy enough for a definitive diagnosis of gastric epithelial neoplasia? J Gastroenterol Hepatol 25:1507–1513PubMedCrossRefGoogle Scholar
  12. 12.
    Takao M, Kakushima N, Takizawa K, Tanaka M, Yamaguchi Y, Matsubayashi H, Kusafuka K, Ono H (2012) Discrepancies in histologic diagnoses of early gastric cancer between biopsy and endoscopic mucosal resection specimens. Gastric Cancer 15:91–96PubMedCrossRefGoogle Scholar
  13. 13.
    Japanese Gastric Cancer Association (2011) Japanese classification of gastric carcinoma, 3rd edn. Gastric Cancer 14:101–112CrossRefGoogle Scholar
  14. 14.
    Kim JH, Lee YC, Kim H, Song KH, Lee SK, Cheon JH, Kim H, Hyung WJ, Noh SH, Kim CB, Chung JB (2009) Endoscopic resection for undifferentiated early gastric cancer. Gastrointest Endosc 69:e1–e9PubMedCrossRefGoogle Scholar
  15. 15.
    Hamilton SR, Lauri L (eds) (2000) Pathology and genetics of tumours of the digestive system. World Health Organization Classification of Tumours. IARC, LyonGoogle Scholar
  16. 16.
    Kim WH, Park CK, Kim YB (2005) A standardized pathology report for gastric cancer. Korean J Pathol 39:106–113Google Scholar
  17. 17.
    Farhat S, Chaussade S, Ponchon T, Coumaros D, Charachon A, Barrioz T, Koch S, Houcke P, Cellier C, Heresbach D, Lepilliez V, Napoleon B, Bauret P, Coron E, Le Rhun M, Bichard P, Vaillant E, Calazel A, Bensoussan E, Bellon S, Mangialavori L, Robin F, Prat F (2011) Endoscopic submucosal dissection in a European setting: a multi-institutional report of a technique in development. Endoscopy 43:664–670PubMedCrossRefGoogle Scholar
  18. 18.
    Oka S, Tanaka S, Kaneko I, Mouri R, Hirata M, Kawamura T, Yoshihara M, Chayama K (2006) Advantage of endoscopic submucosal dissection compared with EMR for early gastric cancer. Gastrointest Endosc 64:877–883PubMedCrossRefGoogle Scholar
  19. 19.
    Yokoi C, Gotoda T, Hamanaka H, Oda I (2006) Endoscopic submucosal dissection allows curative resection of locally recurrent early gastric cancer after prior endoscopic mucosal resection. Gastrointest Endosc 64:212–218PubMedCrossRefGoogle Scholar
  20. 20.
    Yamamoto Y, Fujisaki J, Hirasawa T, Ishiyama A, Yoshimoto K, Ueki N, Chino A, Tsuchida T, Hoshino E, Hiki N, Fukunaga T, Sano T, Yamaguchi T, Takahashi H, Miyata S, Yamamoto N, Kato Y, Igarashi M (2010) Therapeutic outcomes of endoscopic submucosal dissection of undifferentiated-type intramucosal gastric cancer without ulceration and preoperatively diagnosed as 20 millimetres or less in diameter. Dig Endosc 22:112–118PubMedCrossRefGoogle Scholar
  21. 21.
    Kim YJ, Park JC, Kim JH, Shin SK, Lee SK, Lee YC, Chung JB (2010) Histologic diagnosis based on forceps biopsy is not adequate for determining endoscopic treatment of gastric adenomatous lesions. Endoscopy 42:620–626PubMedCrossRefGoogle Scholar
  22. 22.
    Jung MK, Jeon SW, Park SY, Cho CM, Tak WY, Kweon YO, Kim SK, Choi YH, Bae HI (2008) Endoscopic characteristics of gastric adenomas suggesting carcinomatous transformation. Surg Endosc 22:2705–2711PubMedCrossRefGoogle Scholar
  23. 23.
    Park DI, Rhee PL, Kim JE, Hyun JG, Kim YH, Son HJ, Kim JJ, Paik SW, Rhee JC, Choi KW, Oh YL (2001) Risk factors suggesting malignant transformation of gastric adenoma: univariate and multivariate analysis. Endoscopy 33:501–506PubMedCrossRefGoogle Scholar
  24. 24.
    Kang HY, Kim SG, Kim JS, Jung HC, Song IS (2010) Clinical outcomes of endoscopic submucosal dissection for undifferentiated early gastric cancer. Surg Endosc 24:509–516PubMedCrossRefGoogle Scholar
  25. 25.
    Namieno T, Koito K, Higashi T, Shimamura T, Yamashita K, Sato N, Kondo Y (1998) Assessing the suitability of gastric carcinoma for limited resection: histologic differentiation of endoscopic biopsy. World J Surg 22:865–868PubMedCrossRefGoogle Scholar
  26. 26.
    Tatsuta M, Iishi H, Okuda S, Oshima A, Taniguchi H (1989) Prospective evaluation of diagnostic accuracy of gastrofiberscopic biopsy in diagnosis of gastric cancer. Cancer 63:1415–1420PubMedCrossRefGoogle Scholar
  27. 27.
    Graham DY, Schwartz JT, Cain GD, Gyorkey F (1982) Prospective evaluation of biopsy number in the diagnosis of esophageal and gastric carcinoma. Gastroenterology 82:228–231PubMedGoogle Scholar
  28. 28.
    Ryu KW, Choi IJ, Doh YW, Kook MC, Kim CG, Park HJ, Lee JH, Lee JS, Lee JY, Kim YW, Bae JM (2007) Surgical indication for noncurative endoscopic resection in early gastric cancer. Ann Surg Oncol 14:3428–3434PubMedCrossRefGoogle Scholar
  29. 29.
    Nagahama T, Yao K, Maki S, Yasaka M, Takaki Y, Matsui T, Tanabe H, Iwashita A, Ota A (2011) Usefulness of magnifying endoscopy with narrow-band imaging for determining the horizontal extent of early gastric cancer when there is an unclear margin by chromoendoscopy (with video). Gastrointest Endosc 74:1259–1267PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Choong Nam Shim
    • 1
  • Hyunki Kim
    • 2
  • Dong Wook Kim
    • 3
  • Hyun Soo Chung
    • 1
  • Jun Chul Park
    • 1
  • Hyuk Lee
    • 1
  • Sung Kwan Shin
    • 1
  • Sang Kil Lee
    • 1
  • Yong Chan Lee
    • 1
    Email author
  1. 1.Department of Internal Medicine, Institute of GastroenterologyYonsei University College of MedicineSeoulKorea
  2. 2.Department of PathologyYonsei University College of MedicineSeoulKorea
  3. 3.Biostatistics Collaboration UnitYonsei University College of MedicineSeoulKorea

Personalised recommendations