J Korean Med Assoc.  2015 May;58(5):373-384. 10.5124/jkma.2015.58.5.373.

The Korean guideline for gastric cancer screening

• Park HA
• Nam SY
• Lee SK
• Kim SG
• Shim KN
• Park SM
• Lee SY
• Han HS
• Shin YM
• Kim KM
• Lee KJ
• Lee TY
• Choi IJ
• Hong SS
• Kim JW
• Lee YJ
• Kim SY
• Kim Y
• Lee WC
• Chung IK

• KMID: 2195034
• DOI: http://doi.org/10.5124/jkma.2015.58.5.373

Abstract

Despite improvements in treatment modalities, gastric cancer is the second cause of mortality among Korean men and third among females in Korea. Korea implemented a gastric cancer screening program for the general population in 1999. However, the effectiveness and harms of gastric cancer screening using gastric endoscopy and upper gastrointestinal (UGI) series have not been fully evaluated. In an effort to evaluate the screening program, the Korean multidisciplinary expert committee for developing a gastric cancer screening guideline systematically reviewed the evidence regarding the benefits and harms of gastric cancer screening, and developed an evidence-based clinical guideline. There is 'low' level evidence that gastric cancer screening using gastric endoscopy or UGI series can reduce gastric cancer mortality for asymptomatic adults aged between 40 to 74 years. The benefits of gastric cancer screening using gastric endoscopy are substantially higher than its harms, while the benefits of screening with UGI series are moderately higher. We recommend that asymptomatic adults from 40 to 75 years of age undergo biannual gastric cancer screening using gastric endoscopy (recommendation B). Gastric cancer screening using UGI series in asymptomatic adults aged between 40 to 74 years may be recommended based on clinicians' judgment regarding the patient's risk and the patient's preference (recommendation C). There is insufficient evidence to assess the benefits and harms of gastric cancer screening for adults aged between 75 to 84 years (recommendation I). We recommend against gastric cancer screening for adults older than 85 years (recommendation D).

Keyword

Early detection of cancer; Gastric neoplasms; Guideline; Gastric endoscopy; Upper gastrointestinal series

MeSH Terms

Adult
Early Detection of Cancer
Endoscopy
Female
Humans
Judgment
Korea
Male
Mass Screening*
Mortality
Stomach Neoplasms*

Figure

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  Figure 1 Framework of developing a guideline for stomach cancer screening. Key question 1, benefit of stomach cancer screening to decrease mortality or shift to earlier stage; Key question 2, harms of stomach cancer screening; Key question 3, accuracy of gastric endoscopy and upper gastrointestinal (UGI) series; Key question 4, initiation and termination age of stomach cancer screening; Key question 5, interval and duration of stomach cancer screening.

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  Figure 2 Flowchart of literature selection. NDSL, National Digital Science Library; KISS, Koreanstudies Information Service System; KISTI, Korea Institute of Science and Technology Information; KMBase, Korean Medical Database; KQ, key question.

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  Figure 3 Meta-analysis on the Accuracy of upper gastrointestinal series. TP, true positive; FP, false positive; FN, false negative; TN, true negative CI, confidence interval.

Reference

1. National Cancer Information Center. Cancer registry statistics 2012 [Internet]. Goyang: National Cancer Information Center;2013. cited 2015 Mar 13. Available from: http://www.cancer.go.kr/mbs/cancer/index.jsp.

2. Jung KW, Won YJ, Kong HJ, Oh CM, Shin A, Lee JS. Survival of Korean adult cancer patients by stage at diagnosis, 2006-2010: national cancer registry study. Cancer Res Treat. 2013; 45:162–171.

3. Hamashima C, Ogoshi K, Okamoto M, Shabana M, Kishi-moto T, Fukao A. A community-based, case-control study evaluating mortality reduction from gastric cancer by endoscopic screening in Japan. PLoS One. 2013; 8:e79088.

4. Cho BR. Evaluation of the validity of current national health screening program and plan to improve the system. Cheongju: Korea Centers for Disease Control and Prevention;2013.

5. Matsumoto S. Effectiveness of gastric endoscopic screening in reducing the mortality of gastric cancer, in comparison with barium X-ray examination and non-examination. J Gastroenterol Cancer Scree. 2010; 48:436–441.

6. Hosokawa O, Miyanaga T, Kaizaki Y, Hattori M, Dohden K, Ohta K, Itou Y, Aoyagi H. Decreased death from gastric cancer by endoscopic screening: association with a population-based cancer registry. Scand J Gastroenterol. 2008; 43:1112–1115.

7. Oshima A, Hirata N, Ubukata T, Umeda K, Fujimoto I. Evaluation of a mass screening program for stomach cancer with a case-control study design. Int J Cancer. 1986; 38:829–833.

8. Pisani P, Oliver WE, Parkin DM, Alvarez N, Vivas J. Case-control study of gastric cancer screening in Venezuela. Br J Cancer. 1994; 69:1102–1105.

9. Fukao A, Tsubono Y, Tsuji I, HIsamichi S, Sugahara N, Takano A. The evaluation of screening for gastric cancer in Miyagi Prefecture, Japan: a population-based case-control study. Int J Cancer. 1995; 60:45–48.

10. Tsubono Y, Hisamichi S. Case-control studies of screening for gastric cancer in Japan. J Gastroenterol Mass Surv. 1999; 37:182–185.

11. Inaba S, Hirayama H, Nagata C, Kurisu Y, Takatsuka N, Kawakami N, Shimizu H. Evaluation of a screening program on reduction of gastric cancer mortality in Japan: preliminary results from a cohort study. Prev Med. 1999; 29:102–106.

12. Mizoue T, Yoshimura T, Tokui N, Hoshiyama Y, Yatsuya H, Sakata K, Kondo T, Kikuchi S, Toyoshima H, Hayakawa N, Tamakoshi A, Ohno Y, Fujino Y, Kaneko S. Japan Collaborative Cohort Study Group. Prospective study of screening for stomach cancer in Japan. Int J Cancer. 2003; 106:103–107.

13. Lee KJ, Inoue M, Otani T, Iwasaki M, Sasazuki S, Tsugane S. JPHC Study Group. Gastric cancer screening and subsequent risk of gastric cancer: a large-scale population-based cohort study, with a 13-year follow-up in Japan. Int J Cancer. 2006; 118:2315–2321.

14. Miyamoto A, Kuriyama S, Nishino Y, Tsubono Y, Nakaya N, Ohmori K, Kurashima K, Shibuya D, Tsuji I. Lower risk of death from gastric cancer among participants of gastric cancer screening in Japan: a population-based cohort study. Prev Med. 2007; 44:12–19.

15. Rosero-Bixby L, Sierra R. X-ray screening seems to reduce gastric cancer mortality by half in a community-controlled trial in Costa Rica. Br J Cancer. 2007; 97:837–843.

16. Kubota H, Kotoh T, Masunaga R, Dhar DK, Shibakita M, Tachibana M, Kohno H, Nagasue N. Impact of screening survey of gastric cancer on clinicopathological features and survival: retrospective study at a single institution. Surgery. 2000; 128:41–47.

17. Kunisaki C, Ishino J, Nakajima S, Motohashi H, Akiyama H, Nomura M, Matsuda G, Otsuka Y, Ono HA, Shimada H. Outcomes of mass screening for gastric carcinoma. Ann Surg Oncol. 2006; 13:221–228.

18. Nam SY, Choi IJ, Park KW, Kim CG, Lee JY, Kook MC, Lee JS, Park SR, Lee JH, Ryu KW, Kim YW. Effect of repeated endoscopic screening on the incidence and treatment of gastric cancer in health screenees. Eur J Gastroenterol Hepatol. 2009; 21:855–860.

19. Chung SJ, Park MJ, Kang SJ, Kang HY, Chung GE, Kim SG, Jung HC. Effect of annual endoscopic screening on clinicopathologic characteristics and treatment modality of gastric cancer in a high-incidence region of Korea. Int J Cancer. 2012; 131:2376–2384.

20. Lee HJ, Chung JM, Seo EH, Jeon SW. Clinicopathologic characteristics of gastric cancer diagnosed at health screening. Korean J Med. 2008; 75:665–672.

21. Akifuji Y, Yoshinaka M, Okamoto K, Miura K. Ten-year evaluation of mass screening for gastric cancer using endoscopy in Tottori prefecture. J Gastroenterol Cancer Screen. 2013; 51:36–44.

22. Yoon H, Kim N, Lee HS, Shin CM, Park YS, Lee DH, Park DJ, Kim HH, Jung HC. 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.

23. Nam JH, Choi IJ, Cho SJ, Kim CG, Jun JK, Choi KS, Nam BH, Lee JH, Ryu KW, Kim YW. Association of the interval between endoscopies with gastric cancer stage at diagnosis in a region of high prevalence. Cancer. 2012; 118:4953–4960.

24. Kim YS, Park HA, Kim BS, Yook JH, Lee MS. Efficacy of screening for gastric cancer in a Korean adult population: a case-control study. J Korean Med Sci. 2000; 15:510–515.

25. Koo JW, Lee WC, Park CH, Han JY, Chung IS, Paik NS, Kim HK. The effect of screening of stomach cancer on stage shift. Korean J Prev Med. 2000; 33:25–30.

26. Shibuya D, Konno Y, Aida S, Kato K, Shimada T. Complications of gastric mass screening by indirect fluororadiography. J Gastroenterol Cancer Screen. 2006; 44:251–258.

27. Shibuya D, Ishikawa Tsutomu, Ichinose M, Entrance Y, Kitagawa S, Toffoli F, Nagahama T, Kenichi I, Hosokawa O, Masuda H, Mizuguchi M, Yamazaki H. 2010 Fiscal gastric cancer screening accidental disease survey report. J Gastroenterol Cancer Screen. 2013; 51:250–255.

28. National Cancer Center. Korea Institute for Accreditation of Medical Imaging. Quality assurance radiologic evaluation: 2013 National Health Promotion Fund Subsidy projects final report. Goyang: National Cancer Center;2014.

29. International Commission on Radiological Protection. Radiation and your patient: a guide for medical practitioners [Internet]. Ottawa: International Commission on Radiological Protection;cited 2015 Apr 27. Available from: http://www.icrp.org/page.asp?id=32.

30. Hamashima C, Shibuya D, Yamazaki H, Inoue K, Fukao A, Saito H, Sobue T. The Japanese guidelines for gastric cancer screening. Jpn J Clin Oncol. 2008; 38:259–267.

31. Kimmery MB, Burnett DA, Carr-Locke DL, DiMarino AJ, Jensen DM, Katon R, MacFadyen BV, Scobey MW, Stein TN, Steinberg AM. Transmission of infection by gastrointestinal endoscopy. Gastrointest Endosc. 1993; 39:885–888.

32. Choi KS, Jun JK, Park EC, Park S, Jung KW, Han MA, Choi IJ, Lee HY. Performance of different gastric cancer screening methods in Korea: a population-based study. PLoS One. 2012; 7:e50041.

33. Hamashima C, Okamoto M, Shabana M, Osaki Y, Kishimoto T. Sensitivity of endoscopic screening for gastric cancer by the incidence method. Int J Cancer. 2013; 133:653–659.

34. Fukao A, Hisamichi S, Takano A, Sugawara N. Accuracies of mass screening for gastric cancer: test sensitivity and program sensitivity. J Gastroenterol Mass Surv. 1992; 97:59–63.

35. Abe S, Shibuya D, Noguchi T, Shimada T. An estimate of the false-negative rate of mass-screening for gastric carcinoma. J Gastroenterol Mass Surv. 2000; 38:475–482.

36. Ishida T, Suematsu T, Oobayashi K, Takada Y, Kimura S, Suematsu C. Measurement of accuracy of stomach mass screening by population-based cancer registration. J Gastroenterol Mass Sur. 1994; 32:9–16.

37. Yamamoto K, Yamazaki H, Kuroda C, Kubo T, Oshima A, Katsuda T, Kuwano T, Takeda Y. Diagnostic validity of high-density barium sulfate in gastric cancer screening: follow-up of screenees by record linkage with the Osaka Cancer Registry. J Epidemiol. 2010; 20:287–294.

38. Higashiyama K, Yamazaki H. Diagnostic validity of mass screening programs for gastric cancer and colorectal cancer. J Gastroenterol Cancer Screen. 2010; 48:429–435.

39. Cho E, Kang MH, Choi KS, Suh M, Jun JK, Park EC. Cost-effectiveness outcomes of the national gastric cancer screening program in South Korea. Asian Pac J Cancer Prev. 2013; 14:2533–2540.

40. Kobayashi D, Takahashi O, Arioka H, Fukui T. The optimal screening interval for gastric cancer using esophago-gastro-duodenoscopy in Japan. BMC Gastroenterol. 2012; 12:144.

41. Chang HS, Park EC, Chung W, Nam CM, Choi KS, Cho E, Cho WH. Comparing endoscopy and upper gastrointestinal X-ray for gastric cancer screening in South Korea: a cost-utility analysis. Asian Pac J Cancer Prev. 2012; 13:2721–2728.

42. Bae JM. An optimal interval of gastroendoscopy for stomach cancer screening: a retrospective cohort study. Sejong: Ministry of Health and Welfare;2014.

43. Kohrogi N. A study on the efficiency of gastric cancer screening, with special reference to the appropriate frequency of screening. Fukuoka Igaku Zasshi. 1987; 78:67–81.

44. Mitsushima T, Wada R, Nagatani K. Screening endoscopy for gastric cancer: optimal starting age and interval for screening. Gastroenterology. 2011; 53:130–137.

45. Abe Y, Mitsushima T, Nagatani K, Ikuma H, Minamihara Y. Epidemiological evaluation of the protective effect for dying of stomach cancer by screening programme for stomach cancer with applying a method of case-control study: a study of a efficient screening programme for stomach cancer. Nihon Shokakibyo Gakkai Zasshi. 1995; 92:836–845.

46. Suzuki SI, Tamura S. Evaluation of gastric cancer screening program in NTT company workers: analysis of the results in recent 16 years. Teishin Igaku. 2001; 53:153–157.

47. Triantafillidis JK, Merikas E, Nikolakis D, Papalois AE. Sedation in gastrointestinal endoscopy: current issues. World J Gastroenterol. 2013; 19:463–481.

48. Petersen BT, Chennat J, Cohen J, Cotton PB, Greenwald DA, Kowalski TE, Krinsky ML, Park WG, Pike IM, Romagnuolo J, Rutala WA. ASGE Quality Assurance In Endoscopy Committee. Society for Healthcare Epidemiology of America. Multisociety guideline on reprocessing flexible gastrointestinal endoscopes 2011. Gastrointest Endosc. 2011; 73:1075–1084.

49. Suh M, Choi KS, Lee YY, Park B, Jun JK. Cancer screening in Korea, 2012: results from the Korean National Cancer Screening Survey. Asian Pac J Cancer Prev. 2013; 14:6459–6463.

50. Hosokawa O, Hattori M, Takeda T, Watanabe K, Fujita M. Accuracy of endoscopy in detecting gastric cancer. J Gastroenterol Mass Sur. 2004; 42:33–39.

51. Park CH, Kim EH, Chung H, Lee H, Park JC, Shin SK, Lee YC, An JY, Kim HI, Cheong JH, Hyung WJ, Noh SH, Kim CB, Lee SK. The optimal endoscopic screening interval for detecting early gastric neoplasms. Gastrointest Endosc. 2014; 80:253–259.

52. Jung KW, Won YJ, Kong HJ, Oh CM, Lee DH, Lee JS. Cancer statistics in Korea: incidence, mortality, survival, and prevalence in 2011. Cancer Res Treat. 2014; 46:109–123.

53. Correa P. Human gastric carcinogenesis: a multistep and multifactorial process. First American Cancer Society Award lecture on cancer epidemiology and prevention. Cancer Res. 1992; 52:6735–6740.

54. Zanghieri G, Di Gregorio C, Sacchetti C, Fante R, Sassatelli R, Cannizzo G, Carriero A, Ponz de Leon M. Familial occurrence of gastric cancer in the 2-year experience of a population-based registry. Cancer. 1990; 66:2047–2051.

55. Shin CM, Kim N, Yang HJ, Cho SI, Lee HS, Kim JS, Jung HC, Song IS. Stomach cancer risk in gastric cancer relatives: interaction between Helicobacter pylori infection and family history of gastric cancer for the risk of stomach cancer. J Clin Gastroenterol. 2010; 44:e34–e39.

56. Research Center for Cancer Prevention and Screening. National Cancer Center. 2014 Japanese guideline for stomach cancer screening based on effectiveness evaluation [Internet]. Tokyo: National Cancer Center;2015. cited 2015 Apr 25. Available from: http://www.ncc.go.jp/jp/information/press_release_20150420.html.