Gastric Cancer

, Volume 21, Issue 4, pp 588–597 | Cite as

Higher risk of gastric cancer among immigrants to Ontario: a population-based matched cohort study with over 2 million individuals

  • Rinku Sutradhar
  • Nnenna Asidianya
  • Faith Lee
  • Natalie Coburn
  • Linda Rabeneck
  • Lawrence Paszat
Original Article



The risk of gastric carcinoma (GC) varies around the world and between females and males. We aimed to compare the risk of GC among immigrants to Ontario, Canada, to the risk of GC in its general population.


This was a retrospective population-based matched cohort study from 1991 to 2014. We identified immigrants who were first eligible for the Ontario Health Insurance Plan at age 40 years or older, and matched 5 controls by year of birth and sex. We calculated crude rates and relative rates of GC stratified by sex. We modeled GC hazard using multivariable Cox proportional hazards regression, where a time-varying coefficient was incorporated to examine changes in the association of immigrant status with GC hazard over time.


Among females, 415 GC cases were identified among 209,843 immigrants and 1872 among 1,049,215 controls. Among males, 596 GC cases were identified among 191,792 immigrants and 2998 among 958,960 controls. Comparing immigrants from East Asia and Pacific with the controls, the crude relative rate of GC was 1.54 for females and 1.32 for males. The adjusted hazard ratio (HR) for GC among female immigrants was 1.29 [95% confidence interval (CI) 1.12, 1.48] within 10 years and 1.19 (1.01, 1.40) beyond 10 years; for males, the HR was 1.17 (1.04, 1.31) within 10 years and 1.00 (0.87, 1.15) beyond 10 years.


The risk of GC among immigrants is elevated. Although high-risk immigrant populations in Ontario have been identified, further knowledge is required before a program of GC prevention that is targeted to them can be planned.


Immigrants Matched cohort study Gastric cancer Cox regression model with time-varying coefficient Relative rate 



This study was conducted with the support of Cancer Care Ontario through funding provided by the Government of Ontario. It was supported by the Institute for Clinical Evaluative Sciences (ICES), which is funded by an annual grant from the Ontario Ministry of Health and Long-Term Care (MOHLTC). The opinions, results, and conclusions reported in this paper are those of the authors and are independent from the funding sources. Parts of this material are based on data and information provided by Cancer Care Ontario (CCO). The opinions, results, views, and conclusions reported in this paper are those of the authors and do not necessarily reflect those of CCO. No endorsement by ICES or the MOHLTC or CCO is intended or should be inferred.

Author contribution statement

All of the authors had roles in the design and conduct of the study. RS, NA, and FL planned and executed the statistical analyses. All of the authors had roles in the interpretation of the results, as well as the preparation and approval of the article.

Compliance with ethical standards

Conflict of interest

We declare that we have no conflict of interest.

Ethical standards

This study was approved by the Sunnybrook Health Sciences Centre Research Ethics Board.


  1. 1.
    Freedman ND, Derakhshan MH, Abnet CC, Schatzkin A, Hollenbeck AR, McColl KEL. Male predominance of upper gastrointestinal adenocarcinoma cannot be explained by differences in tobacco smoking in men versus women. Eur J Cancer. 2010;46:2473–8.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Camargo MC, Goto Y, Zabaleta J, Morgan DR, Correa P, Rabkin CS. Sex hormones, hormonal interventions, and gastric cancer risk: a meta-analysis. Cancer Epidemiol Biomark Prev. 2012;21:20–38.CrossRefGoogle Scholar
  3. 3.
    Ang TL, Fock KM. Clinical epidemiology of gastric cancer. Singap Med J. 2014;55:621–8.CrossRefGoogle Scholar
  4. 4.
    Luo G, Zhang Y, Guo P, Wang L, Huang Y, Li K. Global patterns and trends in stomach cancer incidence: age, period and birth cohort analysis. Int J Cancer. 2017;141:1333–44.
  5. 5.
    Plummer M, Franceschi S, Vignat J, Forman D, de Martel C. Global burden of gastric cancer attributable to Helicobacter pylori. Int J Cancer. 2015;136:487–90.CrossRefPubMedGoogle Scholar
  6. 6.
    Hooi JK, Lai WY, Ng WK, Suen MM, Underwood FE, Tanyingoh D, et al. Global prevalence of Helicobacter pylori infection: systematic review and meta-analysis. Gastroenterology. 2017;153:420–9.
  7. 7.
    Moss SF. The clinical evidence linking Helicobacter pylori to gastric cancer. Cell Mol Gastroenterol Hepatol. 2017;3:183–91.CrossRefPubMedGoogle Scholar
  8. 8.
    Freedman ND, Abnet CC, Leitzmann MF, Mouw T, Subar AF, Hollenbeck AR, et al. A prospective study of tobacco, alcohol, and the risk of esophageal and gastric cancer subtypes. Am J Epidemiol. 2007;165:1424–33.CrossRefPubMedGoogle Scholar
  9. 9.
    Ladeiras-Lopes R, Pereira AK, Nogueira A, Pinheiro-Torres T, Pinto I, Santos-Pereira R, et al. Smoking and gastric cancer: systematic review and meta-analysis of cohort studies. Cancer Causes Control. 2008;19:689–701.CrossRefPubMedGoogle Scholar
  10. 10.
    Chen I, Mathews-Greiner L, Li D, Abisoye-Ogunniyan A, Ray S, Bian Y, et al. Transcriptomic profiling and quantitative high-throughput (qHTS) drug screening of CDH1 deficient hereditary diffuse gastric cancer (HDGC) cells identify treatment leads for familial gastric cancer. J Transl Med. 2017;15:92.CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Yaghoobi M, Nabb-Baltar J, Bijarchi R, Hunt RH. What is the quantitative risk of gastric cancer in the first-degree relatives of patients? A meta-analysis. World J Gastroenterol. 2017;23:2435.CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Howson CP, Hiyama T, Wynder EL. The decline in gastric cancer: epidemiology of an unplanned triumph. Epidemiol Rev. 1986;8:1–27.CrossRefPubMedGoogle Scholar
  13. 13.
    Canadian Cancer Society Advisory Committee on Cancer Statistics. Canadian cancer statistics 2017. Toronto: Canadian Cancer Society. Accessed 21 Jun 2017.
  14. 14.
    International Agency for Research on Cancer. Global Cancer Observatory. Lyon: IARC. Accessed 21 Jun 2017.
  15. 15.
    Morais S, Costa AR, Ferro A, Lunet N, Peleteiro B. Contemporary migration patterns in the prevalence of Helicobacter pylori infection: a systematic review. Helicobacter. 2017. (Epub ahead of print).PubMedCrossRefGoogle Scholar
  16. 16.
    Haenszel W, Kurihara M. Studies of Japanese migrants. I. Mortality from cancer and other diseases among Japanese in the United States. J Natl Cancer Inst. 1968;40:43–68.PubMedGoogle Scholar
  17. 17.
    Shimizu H, Mack TM, Ross RK, Henderson BE. Cancer of the gastrointestinal tract among japanese and white immigrants in Los Angeles County 2. J Natl Cancer Inst. 1987;78:223–8.Google Scholar
  18. 18.
    Loffeld RJ, Van Der Putten AB. Changes in prevalence of Helicobacter pylori infection in two groups of patients undergoing endoscopy and living in the same region in the Netherlands. Scand J Gastroenterol. 2003;38:938–41.CrossRefPubMedGoogle Scholar
  19. 19.
    Karimi P, Islami F, Anandasabapathy S, Freedman ND, Kamangar F. Gastric cancer: descriptive epidemiology, risk factors, screening, and prevention. Cancer Epidemiol Biomark Prev. 2014;23:700–13.CrossRefGoogle Scholar
  20. 20.
    Rugge M, Genta RM, Di Mario F, El-Omar EM, El-Serag HB, Fassan M, et al. Gastric cancer as preventable disease. Clin Gastroenterol Hepatol. 2017;15:1833–43.
  21. 21.
    Malfertheiner P, Megraud F, O’Morain CA, Gisbert JP, Kuipers EJ, Axon AT, et al. Management of Helicobacter pylori infection: The Maastricht V/Florence Consensus Report. Gut. 2017;66:6–30.Google Scholar
  22. 22.
    Ford AC, Forman D, Hunt R, Yuan Y, Moayyedi P. Helicobacter pylori eradication for the prevention of gastric neoplasia. Cochrane Database Syst Rev. 2015. Scholar
  23. 23.
    Lee YC, Chiang TH, Chou CK, Tu YK, Liao WC, Wu MS, et al. Association between Helicobacter pylori eradication and gastric cancer incidence: a systematic review and meta-analysis. Gastroenterology. 2016;150:1113–24.CrossRefPubMedGoogle Scholar
  24. 24.
    Hamashima C, Ogoshi K, Okamoto M, Shabana M, Kishimoto 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.CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Sutradhar R, Gu S, Paszat L. Multistate transitional models for measuring adherence to breast cancer screening: a population-based longitudinal cohort study with over 2 million women. J Med Screen. 2017;24(2):75–82 (PMID 27440758).CrossRefPubMedGoogle Scholar
  26. 26.
    Lofters AK, Hwang SW, Moineddin R, Glazier RH. Cervical cancer screening among urban immigrants by region of origin: a population-based cohort study. Prev Med. 2010;51:509–16.CrossRefPubMedGoogle Scholar
  27. 27.
    Creatore MI, Booth GL, Manuel DG, Moineddin R, Glazier RH. Diabetes screening among immigrants. Diabetes Care. 2012;35:754–61.CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Lofters AK, Moineddin R, Hwang SW, Glazier RH. Predictors of low cervical cancer screening among immigrant women in Ontario, Canada. BMC Womens Health. 2011;11:20.CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Rosner B. Fundamentals of biostatistics. 6th ed. Belmont: Duxbury Press; 2006.Google Scholar
  30. 30.
    Therneau TM, Grambsch PM. Modeling survival data: extending the Cox model. New York: Springer; 2000.CrossRefGoogle Scholar
  31. 31.
    Allison PD. Survival analysis using SAS: a practical guide. 2nd ed. Cary: SAS Institute; 1995.Google Scholar
  32. 32.
    R Development Core Team. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing; 2009. Accessed 28 July 2014.
  33. 33.
    McDermott S, Desmeules M, Lewis R, Gold J, Payne J, Lafrance B, Vissandjée B, Kliewer E, Mao Y. Cancer incidence among Canadian immigrants, 1980–1998: results from a national cohort study. J Immigr Minor Health. 2011;13(1):15–26.CrossRefPubMedGoogle Scholar
  34. 34.
    Park JY, Forman D, Greenberg ER, Herrero R. Helicobacter pylori eradication in the prevention of gastric cancer: are more trials needed? Curr Oncol Rep. 2013;15:517–25.CrossRefPubMedGoogle Scholar
  35. 35.
    Cheng HC, Wang JD, Chen WY, Chen CW, Chang SC, Sheu BS. Helicobacter pylori test-and-treat program can be cost-effective to prevent gastric cancer in Taiwanese adults: referred to the Nationwide Reimbursement Database. Helicobacter. 2015;20:114–24.Google Scholar
  36. 36.
    Areia M, Carvalho R, Cadime AT, Rocha Goncalves F, Dinis-Ribeiro M. Screening for gastric cancer and surveillance of premalignant lesions: a systematic review of cost-effectiveness studies. Helicobacter. 2013;18:325–37.CrossRefPubMedGoogle Scholar
  37. 37.
    Lansdorp-Vogelaar I, Sharp L. Cost-effectiveness of screening and treating Helicobacter pylori for gastric cancer prevention. Best Prac Res Clin Gastroenterol. 2013;27:933–47.CrossRefGoogle Scholar
  38. 38.
    Schulz TR, McBryde ES, Leder K, Biggs BA. Using stool antigen to screen for Helicobacter pylori in immigrants and refugees from high prevalence countries is relatively cost effective in reducing the burden of gastric cancer and peptic ulceration. PLoS One. 2014;9:e108610.CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Marshall JK, Armstrong D, O’Brien BJ. Test-and-treat strategies for Helicobacter pylori in uninvestigated dyspepsia: a Canadian economic analysis. Can J Gastroenterol. 2000;14:379–88.CrossRefPubMedGoogle Scholar
  40. 40.
    Chiba N, Veldhuyzen Van Zanten SJ, Escobedo S, Grace E, Lee J, Sinclair P, et al. Economic evaluation of Helicobacter pylori eradication in the CADET-Hp randomized controlled trial of H. pylori-positive primary care patients with uninvestigated dyspepsia. Aliment Pharmacol Ther. 2004;19:349–58.CrossRefPubMedGoogle Scholar
  41. 41.
    Masucci L, Blackhouse G, Goeree R. Cost-effectiveness of the carbon-13 urea breath test for the detection of Helicobacter pylori: an economic analysis. Ont Health Technol Assess Ser. 2013;13:1–28.PubMedPubMedCentralGoogle Scholar
  42. 42.
    Xie F, O’Reilly D, Ferrusi IL, Blackhouse G, Bowen JM, Tarride JE, et al. Illustrating economic evaluation of diagnostic technologies: comparing Helicobacter pylori screening strategies in prevention of gastric cancer in Canada. J Am Coll Radiol. 2009;6:317–23.CrossRefPubMedGoogle Scholar

Copyright information

© The International Gastric Cancer Association and The Japanese Gastric Cancer Association 2017

Authors and Affiliations

  • Rinku Sutradhar
    • 1
    • 2
    • 3
  • Nnenna Asidianya
    • 1
  • Faith Lee
    • 2
    • 4
  • Natalie Coburn
    • 3
    • 5
  • Linda Rabeneck
    • 3
    • 5
    • 6
    • 7
  • Lawrence Paszat
    • 2
    • 3
    • 5
  1. 1.Department of Biostatistics, Dalla Lana School of Public HealthUniversity of TorontoTorontoCanada
  2. 2.Institute for Clinical Evaluative SciencesTorontoCanada
  3. 3.Institute of Health Policy, Management and EvaluationUniversity of TorontoTorontoCanada
  4. 4.Department of StatisticsUniversity of WaterlooWaterlooCanada
  5. 5.Sunnybrook Research InstituteTorontoCanada
  6. 6.Prevention and Cancer ControlCancer Care OntarioTorontoCanada
  7. 7.Department of MedicineUniversity of TorontoTorontoCanada

Personalised recommendations