Digestive Diseases and Sciences

, Volume 60, Issue 4, pp 936–943 | Cite as

Risk Factors of Developing Interval Early Gastric Cancer After Negative Endoscopy

  • Young Sin Cho
  • Il-Kwun Chung
  • Ji Hyun Kim
  • Yunho Jung
  • Tae Hoon Lee
  • Sang-Heum Park
  • Sun-Joo Kim
Original Article



New or missed gastric cancer rates after negative endoscopy are high. However, the clinicopathologic characteristics of missed or interval early gastric cancer (EGC) are not well known. The aim of this study was to evaluate clinicopathologic and endoscopic characteristics of missed or interval EGC after negative endoscopy.


We retrospectively analyzed 1,055 patients with EGC confirmed by endoscopic resection or surgery between June 2006 and July 2013. Referred patients with diagnosed or suspected gastric neoplasms were excluded (n = 771). Interval EGC was defined as gastric cancer diagnosed within 2 years of negative endoscopy. Clinicopathologic characteristics of patients with initially detected and interval EGC and risk factors for interval EGC were investigated.


Of 284 patients, 52 had interval EGC (18.3 %; mean age 65.4 years; average interval between diagnosis and previous endoscopy, 12.6 months). Tumors were significantly smaller (1.3 vs. 1.8 cm, P < 0.001), and the incidence of metaplasia was significantly higher (90.4 vs. 65.9 %, P < 0.001) for interval EGC than for initially detected EGC. And no symptoms (50 vs. 17.7 %, P < 0.001) were significantly associated with interval EGC. However, tumor location, differentiation, gross morphology, and Helicobacter pylori infection status did not differ significantly.


Subtle mucosal lesions with surrounding intestinal metaplasia were associated with interval EGC. Careful endoscopic screening for patients with intestinal metaplasia at short-term interval would be beneficial for decreasing interval EGC rates.


Early gastric cancer Interval gastric cancer Missed gastric cancer 



This work was supported by the Soonchunhyang University Research Fund.

Conflict of interest



  1. 1.
    Leung WK, Wu MS, Kakugawa Y, et al. Screening for gastric cancer in Asia: current evidence and practice. Lancet Oncol. 2008;9:279–287.CrossRefPubMedGoogle Scholar
  2. 2.
    Parkin DM, Bray F, Ferlay J, Pisani P. Global cancer statistics, 2002. CA Cancer J Clin. 2005;55:74–108.CrossRefPubMedGoogle Scholar
  3. 3.
    Crew KD, Neugut AI. Epidemiology of gastric cancer. World J Gastroenterol. 2006;12:354–362.PubMedCentralPubMedGoogle Scholar
  4. 4.
    Maruyama K, Kaminish M, Hayashi K, et al. Gastric cancer treated in 1991 in Japan: data analysis of nationwide registry. Gastric Cancer. 2006;9:51–66.CrossRefPubMedGoogle Scholar
  5. 5.
    Tsubono Y, Hisamich S. Screening for gastric cancer in Japan. Gastric Cancer. 2000;3:9–18.CrossRefPubMedGoogle Scholar
  6. 6.
    Yoo KY. Cancer control activities in the Republic of Korea. Jpn J Clin Oncol. 2008;38:327–333.CrossRefPubMedGoogle Scholar
  7. 7.
    Hisamich S, Sugawara N, Fukao A. Effectiveness of gastric mass screening in Japan. Cancer Detect Prev. 1988;11:323–329.Google Scholar
  8. 8.
    Hosokawa O, Miyanaga T, Kaizaki Y, et al. Decreased death from gastric cancer by endoscopic screening: association with a population-based cancer registry. Scand J Gastroenterol. 2008;43:1112–1115.CrossRefPubMedGoogle Scholar
  9. 9.
    Dan YY, So JB, Yeoh KG. Endoscopic screening for gastric cancer. Clin Gastroenterol Hepatol. 2006;4:709–716.CrossRefPubMedGoogle Scholar
  10. 10.
    Tashiro A, Sano M, Kinameri K, Fugita K, Takeuchi Y. Comparing mass screening techniques for gastric cancer in Japan. World J Gastroenterol. 2006;12:4873–4874.PubMedCentralPubMedGoogle Scholar
  11. 11.
    Choi KS, Jun JK, Lee HY, et al. Performance of gastric cancer screening by endoscopy testing through the National Cancer Screening Program of Korea. Cancer Sci. 2011;102:1559–1564.CrossRefPubMedGoogle Scholar
  12. 12.
    Isomoto H, Shikuwa S, Yamaguchi N, et al. Endoscopic submucosal dissection for early gastric cancer: a large-scale feasibility study. Gut. 2009;58:331–336.CrossRefPubMedGoogle Scholar
  13. 13.
    Gotoda T. Endoscopic resection of early gastric cancer. Gastric Cancer. 2007;10:1–11.CrossRefPubMedGoogle Scholar
  14. 14.
    Chung IK, Lee JH, Lee SH, et al. Therapeutic outcomes in 1000 cases of endoscopic submucosal dissection for early gastric neoplasms: Korean ESD Study Group multicenter study. Gastrointest Endosc. 2009;69:1228–1235.CrossRefPubMedGoogle Scholar
  15. 15.
    Hosokawa O, Hattori M, Douden K, et al. Difference in accuracy between gastroscopy and colonoscopy for detection of cancer. Hepatogastroenterology. 2007;54:442–444.PubMedGoogle Scholar
  16. 16.
    Aida K, Yoshikawa H, Mochizuki C, et al. Clinicopathological features of gastric cancer detected by endoscopy as part of annual health checkup. J Gastroenterol Hepatol. 2008;23:632–637.CrossRefPubMedGoogle Scholar
  17. 17.
    Kaminski MF, Regula J, Kraszewska E, et al. Quality indicators for colonoscopy and the risk of interval cancer. N Engl J Med. 2010;362:1795–1803.CrossRefPubMedGoogle Scholar
  18. 18.
    Bressler B, Paszat LF, Chen Z, et al. Rates of new or missed colorectal cancers after colonoscopy and their risk factors: a population-based analysis. Gastroenterology. 2007;132:96–102.CrossRefPubMedGoogle Scholar
  19. 19.
    Bressler B, Paszat LF, Chen Z, et al. Colonoscopic miss rates for right-sided colon cancer: a population-based analysis. Gastroenterology. 2004;127:452–456.CrossRefPubMedGoogle Scholar
  20. 20.
    Patel SG, Ahnen DJ. Prevention of interval colorectal cancers: what every clinician needs to know. Clin Gastroenterol Hepatol. 2014;12:7–15.CrossRefPubMedGoogle Scholar
  21. 21.
    Anonymous. National cancer control programs in Korea. J Korean Med Sci. 2007;22:S3–4.Google Scholar
  22. 22.
    Woodman CB, Threlfall AG, Boggis CR, Prior P. Is the three year breast screening interval to long? Occurrence of interval cancers in NHS breast screening programme’s north western region. BMJ. 1995;310:224–226.CrossRefPubMedCentralPubMedGoogle Scholar
  23. 23.
    Choi KS, Kwak MS, Lee HY, et al. Screening for gastric cancer in Korea: population-based preferences for endoscopy versus upper gastrointestinal series. Cancer Epidemiol Biomarkers Prev. 2009;18:1390–1398.CrossRefPubMedGoogle Scholar
  24. 24.
    Vakil N, Moayyedi P, Fennerty MB, Talley NJ. Limited value of alarm features in the diagnosis of upper gastrointestinal malignancy: systematic review and meta-analysis. Gastroenterology. 2006;131:390–401.CrossRefPubMedGoogle Scholar
  25. 25.
    Suzuki H, Gotoda T, Sasako M, Saito D. Detection of early gastric cancer: misunderstanding the role of mass screening. Gastric Cancer. 2006;9:315–319.CrossRefPubMedGoogle Scholar
  26. 26.
    Kong SH, Park DJ, Lee HJ, et al. Clinicopathologic features of asymptomatic gastric adenocarcinoma patients in Korea. Jpn J Clin Oncol. 2004;34:1–7.CrossRefPubMedGoogle Scholar
  27. 27.
    Gates TJ. Screening for cancer: evaluating the evidence. Am Fam Physician. 2001;63:513–522.PubMedGoogle Scholar
  28. 28.
    Adachi Y, Yasuda K, Inomata M, et al. Pathology and prognosis of gastric carcinoma: well versus poorly differentiated type. Cancer. 2000;89:1418–1424.CrossRefPubMedGoogle Scholar
  29. 29.
    Nam SY, Choi IJ, Park JW, et al. Effect of repeated endoscopic screening on the incidence and treatment of gastric cancer in health screenees. Eur J Gastroenterol Hepatol. 2009;21:855–860.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Young Sin Cho
    • 1
  • Il-Kwun Chung
    • 1
  • Ji Hyun Kim
    • 1
  • Yunho Jung
    • 1
  • Tae Hoon Lee
    • 1
  • Sang-Heum Park
    • 1
  • Sun-Joo Kim
    • 1
  1. 1.Division of Gastroenterology, Department of Internal Medicine, Soonchunhyang University College of MedicineCheonan HospitalCheonan, ChoongnamRepublic of Korea

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