Endoscopy 2022; 54(09): 848-858
DOI: 10.1055/a-1728-5673
Original article

Beneficial effects of endoscopic screening on gastric cancer and optimal screening interval: a population-based study

Wen-Qing Li*
1   Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education/Beijing), Department of Cancer Epidemiology, Peking University Cancer Hospital and Institute, Beijing, China
,
Xiang-Xiang Qin*
1   Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education/Beijing), Department of Cancer Epidemiology, Peking University Cancer Hospital and Institute, Beijing, China
,
Zhe-Xuan Li
1   Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education/Beijing), Department of Cancer Epidemiology, Peking University Cancer Hospital and Institute, Beijing, China
,
Le-Hua Wang
2   Linqu County People’s Hospital, Linqu, China
,
Zong-Chao Liu
1   Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education/Beijing), Department of Cancer Epidemiology, Peking University Cancer Hospital and Institute, Beijing, China
,
Xiao-Han Fan
1   Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education/Beijing), Department of Cancer Epidemiology, Peking University Cancer Hospital and Institute, Beijing, China
,
Li-Hui Zhang
3   Department of Disease Control, Linqu County Public Health Bureau, Linqu, China
,
Yi Li
2   Linqu County People’s Hospital, Linqu, China
,
Xiu-Zhen Wu
2   Linqu County People’s Hospital, Linqu, China
,
Jun-Ling Ma
1   Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education/Beijing), Department of Cancer Epidemiology, Peking University Cancer Hospital and Institute, Beijing, China
,
Yang Zhang
1   Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education/Beijing), Department of Cancer Epidemiology, Peking University Cancer Hospital and Institute, Beijing, China
,
Lan-Fu Zhang
2   Linqu County People’s Hospital, Linqu, China
,
Ming Li
3   Department of Disease Control, Linqu County Public Health Bureau, Linqu, China
,
Tong Zhou
1   Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education/Beijing), Department of Cancer Epidemiology, Peking University Cancer Hospital and Institute, Beijing, China
,
Jing-Ying Zhang
1   Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education/Beijing), Department of Cancer Epidemiology, Peking University Cancer Hospital and Institute, Beijing, China
,
Jian-Xi Wang
3   Department of Disease Control, Linqu County Public Health Bureau, Linqu, China
,
Wei-Dong Liu
4   Department of Epidemiology, Institute for Gastric Cancer Prevention, Linqu, China
,
Wei-Cheng You
1   Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education/Beijing), Department of Cancer Epidemiology, Peking University Cancer Hospital and Institute, Beijing, China
,
Kai-Feng Pan
1   Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education/Beijing), Department of Cancer Epidemiology, Peking University Cancer Hospital and Institute, Beijing, China
› Author Affiliations
Supported by: Natural Science Foundation of Beijing Municipality 7194245
Supported by: Beijing Municipal Administration of Hospitals’ Ascent Plan DFL20181102
Supported by: The National Key R&D Program of China 2018YFC1313105

Abstract

Background The effectiveness of endoscopic screening on gastric cancer has not been widely investigated in China and the screening interval of repeated screening has not been determined.

Methods In a population-based prospective study, we included 375,800 individuals, 14,670 of whom underwent endoscopic screening (2012–2018). We assessed the associations between endoscopic screening and risk of incident gastric cancer and gastric cancer-specific mortality, and examined changes in overall survival and disease-specific survival following screening. The optimal screening interval for repeated endoscopy for early detection of gastric cancer was explored.

Results Ever receiving endoscopic screening significantly decreased the risk of invasive gastric cancer (age- and sex-adjusted relative risk [RR] 0.69, 95 % confidence interval [CI] 0.52–0.92) and gastric cancer-specific mortality (RR 0.33, 95 %CI 0.20–0.56), particularly for noncardia gastric cancer. Repeated screening strengthened the beneficial effect on invasive gastric cancer-specific mortality of one-time screening. Among invasive gastric cancers, screening-detected individuals had significantly better overall survival (RR 0.18, 95 %CI 0.13–0.25) and disease-specific survival (RR 0.18, 95 %CI 0.13–0.25) than unscreened individuals, particularly for those receiving repeated endoscopy. For individuals with intestinal metaplasia or low grade intraepithelial neoplasia, repeated endoscopy at an interval of < 2 years, particularly within 1 year, significantly enhanced the detection of early gastric cancer, compared with repeated screening after 2 years (P-trend = 0.02).

Conclusion Endoscopic screening prevented gastric cancer occurrence and death, and improved its prognosis in a population-based study. Repeated endoscopy enhanced the effectiveness. Screening interval should be based on gastric lesion severity.

* These authors contributed equally to this work.


Tables 1 s–3 s, Figs. 1 s–3 s



Publication History

Received: 02 July 2021

Accepted: 28 December 2021

Accepted Manuscript online:
28 December 2021

Article published online:
15 March 2022

© 2021. Thieme. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 
  • References

  • 1 Sung H, Ferlay J, Siegel RL. et al. Global Cancer Statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2021; 71: 209-249
  • 2 Chen W, Zheng R, Baade PD. et al. Cancer statistics in China, 2015. CA Cancer J Clin 2016; 66: 115-132
  • 3 Zeng H, Chen W, Zheng R. et al. Changing cancer survival in China during 2003-15: a pooled analysis of 17 population-based cancer registries. Lancet Glob Health 2018; 6: e555-e567
  • 4 Jun JK, Choi KS, Lee HY. et al. Effectiveness of the Korean National Cancer Screening Program in reducing gastric cancer mortality. Gastroenterology 2017; 152: 1319-1328.e1317
  • 5 Hamashima C. Cancer screening guidelines and policy making: 15 years of experience in cancer screening guideline development in Japan. Jpn J Clin Oncol 2018; 48: 278-286
  • 6 Bureau of Disease Prevention and Control. Strategies of early detection and treatment in cancer project (2011 edn). Beijing: People’s Medical Publishing House; 2011
  • 7 Chen R, Liu Y, Song G. et al. Effectiveness of one-time endoscopic screening programme in prevention of upper gastrointestinal cancer in China: a multicentre population-based cohort study. Gut 2021; 70: 251-260
  • 8 Fan X, Qin X, Zhang Y. et al. Screening for gastric cancer in China: advances, challenges and visions. Chin J Cancer Res 2021; 33: 168-180
  • 9 You WC, Blot WJ, Chang YS. et al. Diet and high risk of stomach cancer in Shandong, China. Cancer Res 1988; 48: 3518-3523
  • 10 Li WQ, Zhang JY, Ma JL. et al. Effects of Helicobacter pylori treatment and vitamin and garlic supplementation on gastric cancer incidence and mortality: follow-up of a randomized intervention trial. BMJ 2019; 366: 5016
  • 11 Pan KF, Zhang L, Gerhard M. et al. A large randomised controlled intervention trial to prevent gastric cancer by eradication of Helicobacter pylori in Linqu County, China: baseline results and factors affecting the eradication. Gut 2016; 65: 9-18
  • 12 You WC, Blot WJ, Li JY. et al. Precancerous gastric lesions in a population at high risk of stomach cancer. Cancer Res 1993; 53: 1317-1321
  • 13 Dixon MF, Genta RM, Yardley JH. et al. Classification and grading of gastritis. The updated Sydney System. International Workshop on the Histopathology of Gastritis, Houston 1994. Am J Surg Pathol 1996; 20: 1161-1181
  • 14 Song H, Ekheden IG, Zheng Z. et al. Incidence of gastric cancer among patients with gastric precancerous lesions: observational cohort study in a low risk Western population. BMJ 2015; 351: h3867
  • 15 Chen Q, Yu L, Hao CQ. et al. Effectiveness of endoscopic gastric cancer screening in a rural area of Linzhou, China: results from a case–control study. Cancer Med 2016; 5: 2615-2622
  • 16 Kim H, Hwang Y, Sung H. et al. Effectiveness of gastric cancer screening on gastric cancer incidence and mortality in a community-based prospective cohort. Cancer Res Treat 2018; 50: 582-589
  • 17 Kunisaki C, Ishino J, Nakajima S. et al. Outcomes of mass screening for gastric carcinoma. Ann Surg Oncol 2006; 13: 221-228
  • 18 Suh YS, Lee J, Woo H. et al. National cancer screening program for gastric cancer in Korea: nationwide treatment benefit and cost. Cancer 2020; 126: 1929-1939
  • 19 Correa P. A human model of gastric carcinogenesis. Cancer Res 1988; 48: 3554-3560
  • 20 de Vries AC, van Grieken NC, Looman CW. et al. Gastric cancer risk in patients with premalignant gastric lesions: a nationwide cohort study in the Netherlands. Gastroenterology 2008; 134: 945-952
  • 21 Hosokawa O, Watanabe K, Hatorri M. et al. Detection of gastric cancer by repeat endoscopy within a short time after negative examination. Endoscopy 2001; 33: 301-305
  • 22 Jin S, Jeon SW, Kwon Y. et al. Optimal endoscopic screening interval for early detection of gastric cancer: a single-center study. J Korean Med Sci 2018; 33: e166
  • 23 Hamashima C, Narisawa R, Ogoshi K. et al. Optimal interval of endoscopic screening based on stage distributions of detected gastric cancers. BMC Cancer 2017; 17: 740
  • 24 Park CH, Kim EH, Chung H. et al. The optimal endoscopic screening interval for detecting early gastric neoplasms. Gastrointest Endosc 2014; 80: 253-259
  • 25 Choi SI, Park B, Joo J. et al. Three-year interval for endoscopic screening may reduce the mortality in patients with gastric cancer. Surg Endosc 2019; 33: 861-869
  • 26 Lee H, Min BH, Lee JH. et al. Survival outcome associated with the screening interval for gastric cancer in Korea. Digestion 2011; 84: 142-148
  • 27 Yoon H, Kim N, Lee HS. et al. Effect of endoscopic screening at 1-year intervals on the clinicopathologic characteristics and treatment of gastric cancer in South Korea. J Gastroenterol Hepatol 2012; 27: 928-934
  • 28 Banks M, Graham D, Jansen M. et al. British Society of Gastroenterology guidelines on the diagnosis and management of patients at risk of gastric adenocarcinoma. Gut 2019; 68: 1545-1575
  • 29 Pimentel-Nunes P, Libanio D, Marcos-Pinto R. et al. Management of epithelial precancerous conditions and lesions in the stomach (MAPS II): European Society of Gastrointestinal Endoscopy (ESGE), European Helicobacter and Microbiota Study Group (EHMSG), European Society of Pathology (ESP), and Sociedade Portuguesa de Endoscopia Digestiva (SPED) guideline update 2019. Endoscopy 2019; 51: 365-388