Cancer Causes & Control

, Volume 20, Issue 10, pp 2021–2029

Effects of Helicobacter pylori infection and smoking on gastric cancer incidence in China: a population-level analysis of trends and projections

  • Jennifer M. Yeh
  • Sue J. Goldie
  • Karen M. Kuntz
  • Majid Ezzati
Original paper



Although gastric cancer incidence is declining in China, trends may differ from historical patterns in developed countries. Our aim was to (1) retrospectively estimate the effects of Helicobacter pylori (H. pylori) and smoking on past gastric cancer incidence and (2) project how interventions on these two risk factors can reduce future incidence.


We used a population-based model of intestinal-type gastric cancer to estimate gastric cancer incidence between 1985 and 2050. Disease and risk factor data in the model were from community-based epidemiological studies and national prevalence surveys.


Between 1985 and 2005, age-standardized gastric cancer incidence among Chinese men declined from 30.8 to 27.2 per 100,000 (12%); trends in H. pylori and smoking prevalences accounted for >30% of overall decline. If past risk factor trends continue, gastric cancer incidence will decline an additional 30% by 2050. Yet, annual cases will increase from 116,000 to 201,000 due to population growth and aging. Assuming that H. pylori prevention/treatment and tobacco control are implemented in 2010, the decline in gastric cancer incidence is projected to increase to 33% with universal H. pylori treatment for 20-year-olds, 42% for a hypothetical childhood H. pylori vaccine, and 34% for aggressive tobacco control.


The decline in gastric cancer incidence has been slower than in developed countries and will be offset by population growth and aging. Public health interventions should be implemented to reduce the total number of cases.


Gastric cancer Helicobacter pylori Smoking Cancer prevention China 

Supplementary material

10552_2009_9397_MOESM1_ESM.doc (274 kb)
(DOC 275 kb)


  1. 1.
    Ferlay J, Bray F, Pisani P, Parkin DM (2004) GLOBOCAN 2002. Cancer incidence, mortality and prevalence worldwide. IARC cancer base no. 5 Version 2.0. IARC Press, LyonGoogle Scholar
  2. 2.
    Howson CP, Hiyama T, Wynder EL (1986) The decline in gastric cancer: epidemiology of an unplanned triumph. Epidemiol Rev 8:1–27PubMedGoogle Scholar
  3. 3.
    Parkin DM (2006) The global health burden of infection-associated cancers in the year 2002. Int J Cancer 118:3030–3044CrossRefPubMedGoogle Scholar
  4. 4.
    Haruma K (2000) Trend toward a reduced prevalence of Helicobacter pylori infection, chronic gastritis, and gastric cancer in Japan. Gastroenterol Clin North Am 29:623–631CrossRefPubMedGoogle Scholar
  5. 5.
    Banatvala N, Mayo K, Megraud F, Jennings R, Deeks JJ, Feldman RA (1993) The cohort effect and Helicobacter pylori. J Infect Dis 168:219–221PubMedGoogle Scholar
  6. 6.
    The EUROGAST Study Group (1993) Epidemiology of, and risk factors for, Helicobacter pylori infection among 3194 asymptomatic subjects in 17 populations. Gut 34:1672–1676CrossRefGoogle Scholar
  7. 7.
    Correa P (1992) Human gastric carcinogenesis: a multistep and multifactorial process—first American Cancer Society award lecture on cancer epidemiology and prevention. Cancer Res 52:6735–6740PubMedGoogle Scholar
  8. 8.
    Fuchs CS, Mayer RJ (1995) Gastric carcinoma. N Engl J Med 333:32–41CrossRefPubMedGoogle Scholar
  9. 9.
    Chao A, Thun MJ, Henley SJ, Jacobs EJ, McCullough ML, Calle EE (2002) Cigarette smoking, use of other tobacco products and stomach cancer mortality in US adults: the cancer prevention study II. Int J Cancer 101:380–389CrossRefPubMedGoogle Scholar
  10. 10.
    Ezzati M, Henley SJ, Lopez AD, Thun MJ (2005) Role of smoking in global and regional cancer epidemiology: current patterns and data needs. Int J Cancer 116:963–971CrossRefPubMedGoogle Scholar
  11. 11.
    Liu BQ, Peto R, Chen ZM, Boreham J, Wu YP, Li JY et al (1998) Emerging tobacco hazards in China: 1. Retrospective proportional mortality study of one million deaths. BMJ 317:1411–1422PubMedGoogle Scholar
  12. 12.
    Forman D (2003) Results of intervention trials in Helicobacter pylori-infected populations. In: Hunt R, Tytgat G (eds) Helicobacter pylori: basic mechanisms to clinical cure 2002. Kluwer, Dordrecht, pp 225–230Google Scholar
  13. 13.
    Wong BC, Lam SK, Wong WM, Chen JS, Zheng TT, Feng RE et al (2004) Helicobacter pylori eradication to prevent gastric cancer in a high-risk region of China: a randomized controlled trial. JAMA 291:187–194CrossRefPubMedGoogle Scholar
  14. 14.
    Malfertheiner P, Megraud F, O’Morain C, Bazzoli F, El-Omar E, Graham D et al (2007) Current concepts in the management of Helicobacter pylori infection: the Maastricht III Consensus Report. Gut 56:772–781CrossRefPubMedGoogle Scholar
  15. 15.
    Correa P, Fontham ET, Bravo JC, Bravo LE, Ruiz B, Zarama G et al (2000) Chemoprevention of gastric dysplasia: randomized trial of antioxidant supplements and anti-Helicobacter pylori therapy. J Natl Cancer Inst 92:1881–1888CrossRefPubMedGoogle Scholar
  16. 16.
    You WC, Brown LM, Zhang L, Li JY, Jin ML, Chang YS et al (2006) Randomized double-blind factorial trial of three treatments to reduce the prevalence of precancerous gastric lesions. J Natl Cancer Inst 98:974–983PubMedCrossRefGoogle Scholar
  17. 17.
    Mackay J, Eriksen M, Shafey O (2006) The tobacco atlas. American Cancer Society, AtlantaGoogle Scholar
  18. 18.
    Lopez A, Collishaw NE, Piha T (1994) A descriptive model of the cigarette epidemic in developed countries. Tob Control 3:242–247CrossRefGoogle Scholar
  19. 19.
    Yang G, Fan L, Tan J, Qi G, Zhang Y, Samet JM et al (1999) Smoking in China: findings of the 1996 National Prevalence Survey. JAMA 282:1247–1253CrossRefPubMedGoogle Scholar
  20. 20.
    Yeh JM, Kuntz KM, Ezzati M, Hur C, Kong CY, Goldie SJ (2008) Development of an empirically calibrated model of gastric cancer in two high-risk countries. Cancer Epidemiol Biomarkers Prev 17:1179–1187CrossRefPubMedGoogle Scholar
  21. 21.
    Population Division of the Department of Economic and Social Affairs of the United Nations Secretariat (2004) World population prospects: the 2004 revision and world urbanization prospects: the 2003 revision. 2004 last update [cited 22 Jan 2007]. Available from:
  22. 22.
    Forman D, Sitas F, Newell DG, Stacey AR, Boreham J, Peto R et al (1990) Geographic association of Helicobacter pylori antibody prevalence and gastric cancer mortality in rural China. Int J Cancer 46:608–611CrossRefPubMedGoogle Scholar
  23. 23.
    Zhou D, Yang H (1995) Epidemiology of Helicobacter pylori infection in the People’s Republic of China. Chin Med J (Engl) 108:304–313Google Scholar
  24. 24.
    Segi M (1960) Cancer mortality for selected sites in 24 countries (1950–57). Tohoku University of Medicine, SendaiGoogle Scholar
  25. 25.
    Ministry of Health (MOH), People’s Republic of China (1994) Reports on the 1993 National Health Services Survey results. The Ministry of Health, BeijingGoogle Scholar
  26. 26.
    Ministry of Health (MOH), People’s Republic of China (1999) Reports on the 1998 National Health Services Survey results. The Ministry of Health, BeijingGoogle Scholar
  27. 27.
    Ministry of Health (MOH), People’s Republic of China (2004) Reports on the 2003 National Health Services Survey results. The Ministry of Health, BeijingGoogle Scholar
  28. 28.
    Yang GH, Ma JM, Liu N, Zhou LN (2005) Smoking and passive smoking in Chinese, 2002. Chin J Epidemiol 26:77–83Google Scholar
  29. 29.
    Xia HH, Talley NJ (1997) Natural acquisition and spontaneous elimination of Helicobacter pylori infection: clinical implications. Am J Gastroenterol 92:1780–1787PubMedGoogle Scholar
  30. 30.
    Yang G, Ma J, Chen A, Zhang Y, Samet JM, Taylor CE et al (2001) Smoking cessation in China: findings from the 1996 national prevalence survey. Tob Control 10:170–174CrossRefPubMedGoogle Scholar
  31. 31.
    Mendall MA, Goggin PM, Molineaux N, Levy J, Toosy T, Strachan D et al (1992) Childhood living conditions and Helicobacter pylori seropositivity in adult life. Lancet 339:896–897CrossRefPubMedGoogle Scholar
  32. 32.
    McCallion WA, Murray LJ, Bailie AG, Dalzell AM, O’Reilly DP, Bamford KB (1996) Helicobacter pylori infection in children: relation with current household living conditions. Gut 39:18–21CrossRefPubMedGoogle Scholar
  33. 33.
    Moayyedi P, Axon AT, Feltbower R, Duffett S, Crocombe W, Braunholtz D et al (2002) Relation of adult lifestyle and socioeconomic factors to the prevalence of Helicobacter pylori infection. Int J Epidemiol 31:624–631CrossRefPubMedGoogle Scholar
  34. 34.
    Kneller RW, You WC, Chang YS, Liu WD, Zhang L, Zhao L et al (1992) Cigarette smoking and other risk factors for progression of precancerous stomach lesions. J Natl Cancer Inst 84:1261–1266CrossRefPubMedGoogle Scholar
  35. 35.
    Kato I, Vivas J, Plummer M, Lopez G, Peraza S, Castro D et al (2004) Environmental factors in Helicobacter pylori-related gastric precancerous lesions in Venezuela. Cancer Epidemiol Biomarkers Prev 13:468–476PubMedGoogle Scholar
  36. 36.
    Helicobacter and Cancer Collaborative Group (2001) Gastric cancer and Helicobacter pylori: a combined analysis of 12 case–control studies nested within prospective cohorts. Gut 49:347–353CrossRefGoogle Scholar
  37. 37.
    Banister J, Hill K (2004) Mortality in China 1964–2000. Popul Stud (Camb) 58:55–75CrossRefGoogle Scholar
  38. 38.
    Coale AJ (1984) Rapid population change in China, 1952–1982. National Academy Press, Washington, DCGoogle Scholar
  39. 39.
    Mathers CD, Murray CJL, Lopez A, Salomon JA, Sadana R, Tandon A et al (2000) Estimates of healthy life expectancy for 191 countries in the year 2000: methods and results. GPE discussion paper no. 38. World Health Organization, GenevaGoogle Scholar
  40. 40.
    Mathers CD, Loncar D (2006) Projections of global mortality and burden of disease from 2002 to 2030. PLoS Med 3:e442CrossRefPubMedGoogle Scholar
  41. 41.
    Oeppen J, Vaupel JW (2002) Demography. Broken limits to life expectancy. Science 296:1029–1031CrossRefPubMedGoogle Scholar
  42. 42.
    Mitchell HM, Hu P, Chi Y, Chen MH, Li YY, Hazell SL (1998) A low rate of reinfection following effective therapy against Helicobacter pylori in a developing nation (China). Gastroenterology 114:256–261CrossRefPubMedGoogle Scholar
  43. 43.
    Parsonnet J (2003) What is the Helicobacter pylori global reinfection rate? Can J Gastroenterol 17(Suppl B):46B–48BPubMedGoogle Scholar
  44. 44.
    Everhart JE, Kruszon-Moran D, Perez-Perez GI, Tralka TS, McQuillan G (2000) Seroprevalence and ethnic differences in Helicobacter pylori infection among adults in the United States. J Infect Dis 181:1359–1363CrossRefPubMedGoogle Scholar
  45. 45.
    Centers for Disease Control, Prevention (2005) Cigarette smoking among adults—United States, 2003. Morb Mortal Wkly Rep 54:509–513Google Scholar
  46. 46.
    Yang L, Parkin DM, Li LD, Chen YD, Bray F (2004) Estimation and projection of the national profile of cancer mortality in China: 1991–2005. Br J Cancer 90:2157–2166PubMedGoogle Scholar
  47. 47.
    Epplein M, Nomura AM, Hankin JH, Blaser MJ, Perez-Perez G, Stemmermann GN et al (2008) Association of Helicobacter pylori infection and diet on the risk of gastric cancer: a case–control study in Hawaii. Cancer Causes Control 19:869–877CrossRefPubMedGoogle Scholar
  48. 48.
    You WC, Blot WJ, Li JY, Chang YS, Jin ML, Kneller R et al (1993) Precancerous gastric lesions in a population at high risk of stomach cancer. Cancer Res 53:1317–1321PubMedGoogle Scholar
  49. 49.
    Bray F, Moller B (2006) Predicting the future burden of cancer. Nat Rev Cancer 6:63–74CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Jennifer M. Yeh
    • 1
  • Sue J. Goldie
    • 1
    • 2
  • Karen M. Kuntz
    • 3
  • Majid Ezzati
    • 4
    • 5
  1. 1.Center for Health Decision ScienceHarvard School of Public HealthBostonUSA
  2. 2.Department of Health Policy and ManagementHarvard School of Public HealthBostonUSA
  3. 3.Division of Health Policy and Management, School of Public HealthUniversity of MinnesotaMinneapolisUSA
  4. 4.Department of Global Health and PopulationHarvard School of Public HealthBostonUSA
  5. 5.Department of Environmental HealthHarvard School of Public HealthBostonUSA

Personalised recommendations