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Association of Helicobacter pylori infection and diet on the risk of gastric cancer: a case–control study in Hawaii

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Abstract

Objective

The risk factors most strongly associated with gastric cancer are the gastric bacteria Helicobacter pylori and diet. Utilizing data from a case–control study among residents in Hawaii, we examined the association of diet, presence of H. pylori, and non-cardia gastric cancer risk.

Methods

Serum taken at diagnosis for cases (n = 212) and at interview for controls (n = 336) was assayed for IgG antibodies to H. pylori group antigens and to a recombinant fragment of the cytotoxin-associated antigen A (CagA) protein, and subjects completed food frequency questionnaires. Risk measures were calculated using logistic regression. The likelihood ratio test was used to assess interactions.

Results

Inverse associations were found between gastric cancer risk and increasing intake of several micronutrients and vegetables among all individuals. For H. pylori/CagA-positive subjects, significant trends were present for total, green, and yellow vegetables, while a significant trend was present only for yellow vegetables among H. pylori/CagA-negative individuals. For intestinal gastric cancer, there was a suggestion that intake of vegetables, especially cruciferous vegetables, had a stronger protective effect for the H. pylori/CagA-positive group.

Conclusions

Diet may play a greater role in the etiology of non-cardia gastric cancer among individuals with evidence of H. pylori infection than among those without.

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References

  1. Ferlay J, Bray F, Pisani P, Parkin DM (2004) GLOBOCAN 2002. Cancer incidence, mortality and prevalence worldwide. IARC CancerBase No.5, Version 2.0. IARC Press, Lyon

  2. Surveillance, Epidemiology, and End Results (SEER) Program (www.seer.cancer.gov) SEER*Stat Database: Incidence—SEER 9 Regs Public-Use, November 2003 Sub (1973–2001). National Cancer Institute, DCCPS, Surveillance Research Program, Cancer Statistics Branch (released April 2004, based on the November 2003 submission)

  3. Stewart BW, Kleihues P (eds) (2003) Stomach cancer. In: World cancer report. World Health Organization, International Agency for Research on Cancer, IARC Press, Lyon, pp 194–197

  4. Kamineni A, Williams MA, Schwartz SM, Cook LS, Weiss NS (1999) The incidence of gastric carcinoma in Asian migrants to the United States and their descendents. Cancer Causes Control 10:77–83

    Article  PubMed  CAS  Google Scholar 

  5. Nyren O, Adami H-O (2002) Stomach cancer. In: Adami H-O, Hunter D, Trichopoulos D (eds) Textbook of cancer epidemiology. Oxford University Press, New York, pp 162–187

    Google Scholar 

  6. Helicobacter and Cancer Collaborative Group (2001) Gastric cancer and Helicobacter pylori: a combined analysis of 12 case control studies nested within prospective cohorts. Gut 49:347–353

    Article  Google Scholar 

  7. Kamangar F, Dawsey SM, Blaser MJ et al (2006) Opposing risks of gastric cardia and noncardia gastric adenocarcinomas associated with Helicobacter pylori seropositivity. J Natl Cancer Inst 98:1445–1452

    PubMed  Google Scholar 

  8. Uemura N, Okamoto S, Yamamoto S et al (2001) Helicobacter pylori infection and the development of gastric cancer. N Engl J Med 345:784–789

    Article  PubMed  CAS  Google Scholar 

  9. World Health Organization, International Agency for Research on Cancer (1994) IARC monographs on the evaluation of carcinogenic risks to humans: schistosomes, liver flukes, and Helicobacter pylori, vol 61. IARC, Lyon, pp 1–241

    Google Scholar 

  10. Rocco A, Nardone G (2007) Diet, H pylori infection and gastric cancer: evidence and controversies. World J Gastroenterol 13:2901–2912

    PubMed  CAS  Google Scholar 

  11. Tsugane S, Sasazuki S (2007) Diet and the risk of gastric cancer: review of epidemiological evidence. Gastric Cancer 10:75–83

    Article  PubMed  Google Scholar 

  12. Mirvish S (1983) The etiology of gastric cancer: intragastric nitrosamide formation and other theories. J Natl Cancer Inst 71:629–647

    PubMed  CAS  Google Scholar 

  13. Ramon JM, Serra L, Cerdo C, Oromi J (1993) Dietary factors and gastric cancer risk: a case-control study in Spain. Cancer 71:1731–1735

    Article  PubMed  CAS  Google Scholar 

  14. Steinmetz KA, Potter JD (1991) Vegetables, fruit, and cancer. II Mechanisms. Cancer Causes Control 2:427–442

    Article  PubMed  CAS  Google Scholar 

  15. Bartsch H, Ohshima H, Pignatelli B (1988) Inhibitors of endogenous nitrosation: mecahnisms and implications in human cancer prevention. Mutat Res 202:307–324

    PubMed  CAS  Google Scholar 

  16. International Agency for Research on Cancer (1994) Schistosomes, liver flukes, and Helicobacter pylori. IARC monographs on the evaluation of carcinogenic risks to humans, vol 61. International Agency for Research on Cancer, Lyon

    Google Scholar 

  17. Ward MH, Lopez-Carillo L (1999) Dietary factors and the risk of gastric cancer in Mexico City. Am J Epidemiol 149:925–932

    PubMed  CAS  Google Scholar 

  18. Fox JG, Dangler CA, Taylor NS, King A, Koh TJ, Wang TC (1999) High-salt diet induces gastric epithelial hyperplasia and parietal cell loss, and enhances Helicobacter pylori colonization in C57BL/6 mice. Cancer Res 59:4823–4828

    PubMed  CAS  Google Scholar 

  19. Ekstrom AM, Serafini M, Nyren O, Hansson L-E, Ye W, Wolk A (2000) Dietary antioxident intake and the risk of cardia cancer and noncardia cancer of the intestinal and diffuse types: a population-based case-control study in Sweden. Int J Cancer 87:133–140

    Article  PubMed  CAS  Google Scholar 

  20. Kim HJ, Kim MK, Chang WK, Choi HS, Choi BY, Lee SS (2005) Effect of nutrient intake and Helicobacter pylori infection on gastric cancer in Korea: a case-control study. Nutr Cancer 52:138–146

    Article  PubMed  CAS  Google Scholar 

  21. Lee SA, Kang D, Shim KN, Choe JW, Hong WS, Choi H (2003) Effect of diet and Helicobacter pylori infection to the risk of early gastric cancer. J Epidemiol 13:162–168

    PubMed  Google Scholar 

  22. Lopez-Carrillo L, Lopez-Cervantes M, Robles-Diaz G et al (2003) Capsaicin consumption, Helicobacter pylori positivity and gastric cancer in Mexico. Int J Cancer 106:277–282

    Article  PubMed  CAS  Google Scholar 

  23. Lunet N, Valbuena C, Carneiro F, Lopes C, Barros H (2006) Antioxidant vitamins and risk of gastric cancer: a case-control study in Portugal. Nutr Cancer 55:71–77

    Article  PubMed  CAS  Google Scholar 

  24. Machida-Montani A, Sasazuki S, Inoue M et al. (2004) Association of Helicobacter pylori infection and environmental factors in non-cardia gastric cancer in Japan. Gastric Cancer 7:46–53

    Article  PubMed  Google Scholar 

  25. Serafini M, Bellocco R, Wolk A, Ekstrom AM (2002) Total antioxidant potential of fruit and vegetables and risk of gastric cancer. Gastroenterology 123:985–991

    Article  PubMed  CAS  Google Scholar 

  26. Phukan RK, Narain K, Zomawia E, Hazarika NC, Mahanta J (2006) Dietary habits and stomach cancer in Mizoram, India. J Gastroenterol 41:418–424

    Article  PubMed  Google Scholar 

  27. Gonzalez CA, Jakszyn P, Pera G et al (2006) Meat intake and risk of stomach and esophageal adenocarcinoma within the European Prospective Investigation Into Cancer and Nutrition (EPIC). J Natl Cancer Inst 98:345–354

    Article  PubMed  Google Scholar 

  28. Gonzalez CA, Pera G, Agudo A et al (2006) Fruit and vegetable intake and the risk of stomach and oesophagus adenocarcinoma in the European Prospective Investigation into Cancer and Nutrition (EPIC-EURGAST). Int J Cancer 118:2559–2566

    Article  PubMed  CAS  Google Scholar 

  29. Shikata K, Kiyohara Y, Kubo M et al (2006) A prospective study of dietary salt intake and gastric cancer incidence in a defined Japanese population: the Hisayama study. Int J Cancer 119:196–201

    Article  PubMed  CAS  Google Scholar 

  30. Nomura AM, Hankin JH, Kolonel LN, Wilkens LR, Goodman MT, Stemmermann GN (2003) Case-control study of diet and other risk factors for gastric cancer in Hawaii (United States). Cancer Causes Control 14:547–558

    Article  PubMed  Google Scholar 

  31. Nomura AM, Kolonel LN, Miki K et al (2005) Helicobacter pylori, pepsinogen, and gastric adenocarcinoma in Hawaii. J Infect Dis 191:2075–2081

    Article  PubMed  CAS  Google Scholar 

  32. Young JLJ, Percy CL, Asire AJ et al (1981) Surveillance, epidemiology, end results: incidence and mortality data 1973–1977. National Institutes of Health publication 81-2330. Government Printing Office, Washington, DC

    Google Scholar 

  33. Oyama N, Johnson DB (1996) Hawaii Health Surveillance Program survey methods and procedures. Research and statistics report 54. Hawaii State Department of Health, Research and Statistics Office, Honolulu

    Google Scholar 

  34. Hatten J (1980) Medicare's common denominator: the covered population. Health Care Financ Rev 2:53–64

    PubMed  CAS  Google Scholar 

  35. Hankin JH, Wilkens LR, Kolonel LN, Yoshizawa CN (1991) Validation of a quantitative diet history method in Hawaii. Am J Epidemiol 133:616–628

    PubMed  CAS  Google Scholar 

  36. US Department of Agriculture (1976–1986) Composition of foods: raw, procesed, prepared. In: USDA handbooks. USDA, Hyattsville, MD, pp 1–16

  37. Japan Dietetic Association (1964) Standard tables of food composition. Daiichi, Shuppan, Tokyo

    Google Scholar 

  38. Paul AA, Southgate DAT (1978) McCance and Widdowson’s The composition of foods, 4th edn. Elsevier/North Holland, New York, pp 1–417

    Google Scholar 

  39. Pennington JAT, Church HN (1985) Bowes and Church's food values of portions commonly used, 14th edn. Harper & Row, New York, pp 1–257

    Google Scholar 

  40. WuLeung WT, Butrum RR, Chang FH (1972) Food composition table for use in East Asia. FAO, Rome, pp 1–334

    Google Scholar 

  41. Englyst HN, Bingham SA, Runswick SA, Collinson E, Cummings JH (1988) Distary fiber (non-starch polysaccharides) in fruit, vegetables and nuts. J Human Nutr Diet 1:247–286

    Article  Google Scholar 

  42. Lauren P (1965) The two histological types of gastric carcinoma: diffuse and so-called intestinal type carcinoma: an attempt at a histoclinical classification. Acta Pathol Microbiol Scand 64:31–49

    PubMed  CAS  Google Scholar 

  43. Blaser MJ, Perez-Perez GI, Kleanthous H et al (1995) Infection with Helicobacter pylori strains possessing cagA is associated with an increased risk of developing adenocarcinoma of the stomach. Cancer Res 55:2111–2115

    PubMed  CAS  Google Scholar 

  44. Nomura A, Stemmermann GN, Chyou PH, Kato I, Perez-Perez GI, Blaser MJ (1991) Helicobacter pylori infection and gastric carcinoma among Japanese Americans in Hawaii. N Engl J Med 325:1132–1136

    Article  PubMed  CAS  Google Scholar 

  45. Pinto-Santini D, Salama NR (2005) The biology of Helicobacter pylori infection, a major risk factor for gastric adenocarcinoma. Cancer Epidemiol Biomarkers Prev 14:1853–1858

    Article  PubMed  CAS  Google Scholar 

  46. Peek RM Jr, Blaser MJ (2002) Helicobacter pylori and gastrointestinal tract adenocarcinomas. Nat Rev Cancer 2:28–37

    Article  PubMed  CAS  Google Scholar 

  47. Romero-Gallo J, Perez-Perez GI, Novick RP, Kamath K, Norbu T, Blaser MJ (2002) Responses of endoscopy patients in Ladakh, India, to Helicobacter pylori whole-cell and CagA antigens. Clin Diagn Lab Immunol 9:1313–1317

    Article  PubMed  CAS  Google Scholar 

  48. Yamaguchi N, Kakizoe T (2001) Synergistic interaction between Helicobacter pylori gastritis and diet in gastric cancer. Lancet Oncol 2:88–94

    Article  PubMed  CAS  Google Scholar 

  49. Talalay P, Fahey JW (2001) Phytochemicals from cruciferous plants protect against cancer by modulating carcinogen metabolism. J Nutr 131:3027S–3033S

    PubMed  CAS  Google Scholar 

  50. Karnes WE Jr, Samloff IM, Siurala M et al (1991) Positive serum antibody and negative tissue staining for Helicobacter pylori in subjects with atrophic body gastritis. Gastroenterology 101:167–174

    PubMed  Google Scholar 

  51. Muñoz N, Kato I, Peraza S et al (1996) Prevalence of precancerous lesions of the stomach in Venezuela. Cancer Epidemiol Biomarkers Prev 5:41–46

    PubMed  Google Scholar 

  52. Shibata A, Parsonnet J (2006) Stomach cancer. In: Schottenfeld D, Fraumeni JF, (eds) Cancer epidemiology and prevention, 3rd edn. Oxford University Press, New York, pp 707–720

    Google Scholar 

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Author information

Authors and Affiliations

  1. Epidemiology Program, Cancer Research Center of Hawaii, 1236 Lauhala Street, Honolulu, HI, 96813, USA

    Meira Epplein, Abraham M. Y. Nomura, Jean H. Hankin, Lynne R. Wilkens & Laurence N. Kolonel

  2. Department of Medicine, New York University School of Medicine, New York, NY, USA

    Martin J. Blaser & Guillermo Perez-Perez

  3. Department of Pathology, University of Cincinnati Medical Center, Cincinnati, OH, USA

    Grant N. Stemmermann

Authors
  1. Meira Epplein
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  2. Abraham M. Y. Nomura
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  3. Jean H. Hankin
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  4. Martin J. Blaser
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  5. Guillermo Perez-Perez
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  6. Grant N. Stemmermann
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  7. Lynne R. Wilkens
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  8. Laurence N. Kolonel
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Corresponding author

Correspondence to Meira Epplein.

Additional information

G. N. Stemmermann is now deceased.

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Epplein, M., Nomura, A.M.Y., Hankin, J.H. et al. Association of Helicobacter pylori infection and diet on the risk of gastric cancer: a case–control study in Hawaii. Cancer Causes Control 19, 869–877 (2008). https://doi.org/10.1007/s10552-008-9149-2

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  • DOI: https://doi.org/10.1007/s10552-008-9149-2

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