Skip to main content

Advertisement

SpringerLink
Log in

Macronutrient intake and stomach cancer

  • Original paper
  • Published:
Cancer Causes & Control Aims and scope Submit manuscript

Abstract

Purpose

This study examines the association between intake of selected macronutrients and the risk of stomach cancer in a Northern American population.

Methods

Mailed questionnaires were completed between 1994 and 1997 in eight Canadian provinces by 1,181 incident, histologically confirmed cases of stomach cancer and 5,039 population controls. Information on nutrient intake was obtained using a food frequency questionnaire. Odds ratios (ORs) and the corresponding 95 % confidence intervals (CIs) were derived through unconditional logistic regression to adjust for potential confounders, including an estimate of total energy intake.

Results

Intakes of total fat, saturated fat, and cholesterol were significantly associated with the risk of stomach cancer: The ORs for the highest versus the lowest quartile were 1.58 (95 % CI 1.13–2.20), 1.86 (95 % CI 1.37–2.52), and 1.75 (95 % CI 1.36–2.25), respectively. Total fiber was inversely associated with stomach cancer (p = 0.03). The positive associations with intake of total fat and saturated fat were apparently stronger in women, overweight or obese subjects, and ever smokers. Saturated fat was specifically associated with increased risk of gastric cardia cancer, with an OR of 3.31 (95 % CI 1.48–7.43).

Conclusions

A diet high in saturated fat appears to increase the risk of stomach cancer, particularly among obese subjects and for gastric cardia cancer.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

BMI:

Body mass index

CI:

Confidence interval

FFQ:

Food frequency questionnaire

ICD-O-2:

International Classification of Diseases for Oncology, 2nd edition

OR:

Odds ratio

References

  1. Ferlay J, Soerjomataram II, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin DM, Forman DD, Bray F (2014) Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. doi:10.1002/ijc.29210

    PubMed  Google Scholar 

  2. Canadian Cancer Society (2011) Canadian cancer statistics 2011, Toronto

  3. Piazuelo MB, Correa P (2013) Gastric cancer: overview. Colomb Med 44:192–201

    PubMed  Google Scholar 

  4. González CA, Sala N, Rokkas T (2013) Gastric cancer: epidemiologic aspects. Helicobacter 18(Suppl 1):34–38

    Article  PubMed  Google Scholar 

  5. Peleteiro B, La Vecchia C, Lunet N (2012) The role of Helicobacter pylori infection in the web of gastric cancer causation. Eur J Cancer Prev 21:118–125

    Article  PubMed  Google Scholar 

  6. IARC (2004) IARC monographs on the evaluation of carcinogenic risk to humans, vol 83, Tobacco smoke and involuntary smoking. IARC Press, Lyon

  7. Duell EJ, Travier N, Lujan-Barroso L, Clavel-Chapelon F, Boutron-Ruault MC, Morois S et al (2011) Alcohol consumption and gastric cancer risk in the European Prospective Investigation into Cancer and Nutrition (EPIC) cohort. Am J Clin Nutr 94:1266–1275

    Article  CAS  PubMed  Google Scholar 

  8. Tramacere I, Negri E, Pelucchi C, Bagnardi V, Rota M, Scotti L et al (2012) A meta-analysis on alcohol drinking and gastric cancer risk. Ann Oncol 23:28–36

    Article  CAS  PubMed  Google Scholar 

  9. Yang P, Zhou Y, Chen B, Wan HW, Jia GQ, Bai HL et al (2009) Overweight, obesity and gastric cancer risk: results from a meta-analysis of cohort studies. Eur J Cancer 45:2867–2873

    Article  PubMed  Google Scholar 

  10. D’Elia L, Rossi G, Ippolito R, Cappuccio FP, Strazzullo P (2012) Habitual salt intake and risk of gastric cancer: a meta-analysis of prospective studies. Clin Nutr 31:489–498

    Article  PubMed  Google Scholar 

  11. Liu C, Russell RM (2008) Nutrition and gastric cancer risk: an update. Nutr Rev 66:237–249

    Article  PubMed  Google Scholar 

  12. Zhang Z, Xu G, Ma M, Yang J, Liu X (2013) Dietary fiber intake reduces risk for gastric cancer: a meta-analysis. Gastroenterology 145:113–120

    Article  PubMed  Google Scholar 

  13. de Martel C, Forman D, Plummer M (2013) Gastric cancer: epidemiology and risk factors. Gastroenterol Clin N Am 42:219–240

    Article  Google Scholar 

  14. Berretta M, Cappellani A, Lleshi A, Di Vita M, Lo Menzo E, Bearz A et al (2012) The role of diet in gastric cancer: still an open question. Front Biosci (Landmark Ed) 17:1640–1647

    Article  CAS  Google Scholar 

  15. World Cancer Research Fund/American Institute for Cancer Research (2007) Food, nutrition, physical activity, and the prevention of cancer: a global perspective. AICR, Washington

  16. Buiatti E, Palli D, Decarli A, Amadori D, Avellini C, Bianchi S et al (1990) A case–control study of gastric cancer and diet in Italy: II. Association with nutrients. Int J Cancer 45:896–901

    Article  CAS  PubMed  Google Scholar 

  17. López-Carrillo L, López-Cervantes M, Ward MH, Bravo-Alvarado J, Ramírez-Espitia A (1999) Nutrient intake and gastric cancer in Mexico. Int J Cancer 83:601–605

    Article  PubMed  Google Scholar 

  18. Palli D, Russo A, Decarli A (2001) Dietary patterns, nutrient intake and gastric cancer in a high-risk area of Italy. Cancer Causes Control 12:163–172

    Article  CAS  PubMed  Google Scholar 

  19. Mayne ST, Risch HA, Dubrow R, Chow WH, Gammon MD, Vaughan TL et al (2001) Nutrient intake and risk of subtypes of esophageal and gastric cancer. Cancer Epidemiol Biomark Prev 10:1055–1062

    CAS  Google Scholar 

  20. Qiu JL, Chen K, Zheng JN, Wang JY, Zhang LJ, Sui LM (2005) Nutritional factors and gastric cancer in Zhoushan Islands, China. World J Gastroenterol 11:4311–4316

    CAS  PubMed  Google Scholar 

  21. González CA, Riboli E, Badosa J, Batiste E, Cardona T, Pita S et al (1994) Nutritional factors and gastric cancer in Spain. Am J Epidemiol 139:466–473

    PubMed  Google Scholar 

  22. Hansson LE, Nyrén O, Bergström R, Wolk A, Lindgren A, Baron J et al (1994) Nutrients and gastric cancer risk. A population-based case–control study in Sweden. Int J Cancer 57:638–644

    Article  CAS  PubMed  Google Scholar 

  23. Pakseresht M, Forman D, Malekzadeh R, Yazdanbod A, West RM, Greenwood DC et al (2011) Dietary habits and gastric cancer risk in north-west Iran. Cancer Causes Control 22:725–736

    Article  PubMed  Google Scholar 

  24. Cornée J, Pobel D, Riboli E, Guyader M, Hémon B (1995) A case–control study of gastric cancer and nutritional factors in Marseille, France. Eur J Epidemiol 11:55–65

    Article  PubMed  Google Scholar 

  25. Chen H, Tucker KL, Graubard BI, Heineman EF, Markin RS, Potischman NA et al (2002) Nutrient intakes and adenocarcinoma of the esophagus and distal stomach. Nutr Cancer 42:33–40

    Article  PubMed  Google Scholar 

  26. Kaaks R, Tuyns AJ, Haelterman M, Riboli E (1998) Nutrient intake patterns and gastric cancer risk: a case–control study in Belgium. Int J Cancer 78:415–420

    Article  CAS  PubMed  Google Scholar 

  27. Harrison LE, Zhang ZF, Karpeh MS, Sun M, Kurtz RC (1997) The role of dietary factors in the intestinal and diffuse histologic subtypes of gastric adenocarcinoma: a case–control study in the U.S. Cancer 80:1021–1028

    Article  CAS  PubMed  Google Scholar 

  28. Lissowska J, Gail MH, Pee D, Groves FD, Sobin LH, Nasierowska-Guttmejer A et al (2004) Diet and stomach cancer risk in Warsaw, Poland. Nutr Cancer 48:149–159

    Article  CAS  PubMed  Google Scholar 

  29. 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  CAS  PubMed  Google Scholar 

  30. Lucenteforte E, Bosetti C, Gallus S, Bertuccio P, Pelucchi C, Tavani A et al (2009) Macronutrients, fatty acids and cholesterol intake and stomach cancer risk. Ann Oncol 20:1434–1438

    Article  CAS  PubMed  Google Scholar 

  31. Ji BT, Chow WH, Yang G, McLaughlin JK, Zheng W, Shu XO et al (1998) Dietary habits and stomach cancer in Shanghai, China. Int J Cancer 76:659–664

    Article  CAS  PubMed  Google Scholar 

  32. O’Doherty MG, Freedman ND, Hollenbeck AR, Schatzkin A, Murray LJ, Cantwell MM et al (2012) Association of dietary fat intakes with risk of esophageal and gastric cancer in the NIH-AARP diet and health study. Int J Cancer 131:1376–1387

    Article  PubMed Central  PubMed  Google Scholar 

  33. Wu AH, Tseng CC, Hankin J, Bernstein L (2007) Fiber intake and risk of adenocarcinomas of the esophagus and stomach. Cancer Causes Control 18:713–722

    Article  PubMed  Google Scholar 

  34. Jedrychowski W, Popiela T, Steindorf K, Tobiasz-Adamczyk B, Kulig J, Penar A et al (2001) Nutrient intake patterns in gastric and colorectal cancers. Int J Occup Med Environ Health 14:391–395

    CAS  PubMed  Google Scholar 

  35. Lazarević K, Nagorni A, Jeremić M (2009) Carbohydrate intake, glycemic index, glycemic load and risk of gastric cancer. Cent Eur J Public Health 17:75–78

    PubMed  Google Scholar 

  36. Larsson SC, Bergkvist L, Wolk A (2006) Glycemic load, glycemic index and carbohydrate intake in relation to risk of stomach cancer: a prospective study. Int J Cancer 118:3167–3169

    Article  CAS  PubMed  Google Scholar 

  37. Terry P, Lagergren J, Ye W, Wolk A, Nyrén O (2001) Inverse association between intake of cereal fiber and risk of gastric cardia cancer. Gastroenterology 120:387–391

    Article  CAS  PubMed  Google Scholar 

  38. Bravi F, Scotti L, Bosetti C, Bertuccio P, Negri E, La Vecchia C (2009) Dietary fiber and stomach cancer risk: a case–control study from Italy. Cancer Causes Control 20:847–853

    Article  PubMed  Google Scholar 

  39. Mendez AM, Pera G, Agudo A, Bueno-de-Mesquita HB, Palli D, Boeing H et al (2007) Cereal fiber intake may reduce risk of gastric adenocarcinomas: the EPIC-EURGAST study. Int J Cancer 121:1618–1623

    Article  CAS  Google Scholar 

  40. Botterweck AA, van den Brandt PA, Goldbohm RA (2000) Vitamins, carotenoids, dietary fiber, and the risk of gastric carcinoma: results from a prospective study after 6.3 years of follow-up. Cancer 88:737–748

    Article  CAS  PubMed  Google Scholar 

  41. Percy C, Holten VV, Muir C (1990) International classification of diseases for oncology, 2nd edn. World Health Organization, Geneva

    Google Scholar 

  42. World Health Organization (2000) Obesity: preventing and managing the global epidemic. World Health Organization technical report series, no. 894. Report of a WHO consultation. World Health Organization, Geneva

  43. Block G, Hartman AM, Naughton D (1990) A reduced dietary questionnaire: development and validation. Epidemiology 1:58–64

    Article  CAS  PubMed  Google Scholar 

  44. Willett WC (1998) Nutritional epidemiology, 2nd edn. Oxford University Press, New York

    Book  Google Scholar 

  45. Health Canada (2005) Canadian nutrient file compilation of Canadian food composition data. Users’ guide. Nutrition Research Division and Office of Information Management Technology. Health Products and Food Branch, Health Canada

  46. SAS Institute Inc. (2002) The SAS system for Windows Release 9.01. SAS Institute Inc., Carey

  47. Weisburger JH (1997) Dietary fat and risk of chronic disease: mechanistic insights from experimental studies. J Am Diet Assoc 97(7 Suppl):S16–S23

    Article  CAS  PubMed  Google Scholar 

  48. Tsubura A, Yuri T, Yoshizawa K, Uehara N, Takada H (2009) Role of fatty acids in malignancy and visual impairment: epidemiological evidence and experimental studies. Histol Histopathol 24:223–234

    CAS  PubMed  Google Scholar 

  49. Hu J, La Vecchia C, Desmeules M, Negri E, Mery L (2008) Meat and fish consumption and cancer in Canada. Nutr Cancer 60:313–324

    Article  PubMed  Google Scholar 

  50. Haslam D, Sattar N, Lean M (2006) ABC of obesity. Obesity time to wake up. BMJ 333:640–642

    Article  PubMed Central  PubMed  Google Scholar 

  51. Stein CJ, Colditz GA (2004) The epidemic of obesity. J Clin Endocrinol Metab 89:2522–2525

    Article  CAS  PubMed  Google Scholar 

  52. Li Q, Zhang J, Zhou Y, Qiao L (2012) Obesity and gastric cancer. Front Biosci (Landmark Ed) 17:2383–2390

    Article  Google Scholar 

  53. Calle EE, Rodriguez C, Walker-Thurmond K, Thun MJ (2003) Overweight, obesity, and mortality from cancer in a prospectively studied cohort of U.S. adults. N Engl J Med 348:1625–3849

    Article  PubMed  Google Scholar 

  54. Oh SW, Yoon YS, Shin SA (2005) Effects of excess weight on cancer incidences depending on cancer sites and histologic findings among men: Korea National Health Insurance Corporation Study. J Clin Oncol 23:4742–4754

    Article  PubMed  Google Scholar 

  55. Lukanova A, Björ O, Kaaks R, Lenner P, Lindahl B, Hallmans G et al (2006) Body mass index and cancer: results from the Northern Sweden Health and Disease Cohort. Int J Cancer 118:458–466

    Article  CAS  PubMed  Google Scholar 

  56. Reeves GK, Pirie K, Beral V, Green J, Spencer E, Bull D, for the Million Women Study Collaborators (2007) Cancer incidence and mortality in relation to body mass index in the Million Women Study: cohort study. BMJ 335:1134–1144

  57. Jee SH, Yun JE, Park EJ, Cho ER, Park IS, Sull JW et al (2008) Body mass index and cancer risk in Korean men and women. Int J Cancer 123:1892–1896

    Article  CAS  PubMed  Google Scholar 

  58. Merry AH, Schouten LJ, Goldbohm RA, van den Brandt PA (2007) Body mass index, height and risk of adenocarcinoma of the oesophagus and gastric cardia: a prospective cohort study. Gut 56:1503–1511

    Article  PubMed Central  PubMed  Google Scholar 

  59. Abnet CC, Freedman ND, Hollenbeck AR, Fraumeni JF Jr, Leitzmann M, Schatzkin A (2008) A prospective study of BMI and risk of oesophageal and gastric adenocarcinoma. Eur J Cancer 44:465–471

    Article  PubMed Central  PubMed  Google Scholar 

  60. Turati F, Tramacere I, La Vecchia C, Negri E (2013) A meta-analysis of body mass index and esophageal and gastric cardia adenocarcinoma. Ann Oncol 24:609–617

    Article  CAS  PubMed  Google Scholar 

  61. Zhang J, Su XQ, Wu XJ, Liu YH, Wang H, Zong XN et al (2003) Effect of body mass index on adenocarcinoma of gastric cardia. World J Gastroenterol 9:2658–2661

    PubMed  Google Scholar 

  62. Lindblad M, Rodríguez LA, Lagergren J (2005) Body mass, tobacco and alcohol and risk of esophageal, gastric cardia, and gastric non-cardia adenocarcinoma among men and women in a nested case–control study. Cancer Causes Control 16:285–294

    Article  PubMed  Google Scholar 

  63. Ryan AM, Rowley SP, Fitzgerald AP, Ravi N, Reynolds JV (2006) Adenocarcinoma of the oesophagus and gastric cardia: male preponderance in association with obesity. Eur J Cancer 42:1151–1158

    Article  PubMed  Google Scholar 

  64. Trinchieri G (2012) Cancer and inflammation: an old intuition with rapidly evolving new concepts. Annu Rev Immunol 30:677–706

    Article  CAS  PubMed  Google Scholar 

  65. Miwa K, Kinami S, Miyazaki I, Hattori T (1996) Positive association between dietary fat intake and risk of gastric stump carcinoma in rats. Carcinogenesis 17:1885–1889

    Article  CAS  PubMed  Google Scholar 

  66. Ferretti G, Bacchetti T, Rabini RA, Vignini A, Nanetti L, Moroni C et al (2006) Homocysteinylation of low-density lipoproteins (LDL) from subjects with type 1 diabetes: effect on oxidative damage of human endothelial cells. Diabet Med 23:808–813

    Article  CAS  PubMed  Google Scholar 

  67. Bradbury KE, Appleby PN, Key TJ (2014) Fruit, vegetable, and fiber intake in relation to cancer risk: findings from the European Prospective Investigation into Cancer and Nutrition (EPIC). Am J Clin Nutr 100(Supplement 1):394S–398S

    Article  CAS  PubMed  Google Scholar 

  68. Lupton JR, Turner ND (1999) Potential protective mechanisms of wheat bran fiber. Am J Med 106(1A):24S–27S

    Article  CAS  PubMed  Google Scholar 

  69. Marlett JA, McBurney MI, Slavin JL, American Dietetic Association (2002) Position of the American Dietetic Association: health implications of dietary fiber. J Am Diet Assoc 102:993–1000

    Article  PubMed  Google Scholar 

  70. Copeland KT, Checkoway H, McMichale AJ, Holbrook RH (1977) Bias due to misclassification in the estimate of relative risk. Am J Epidemiol 105:488–495

    CAS  PubMed  Google Scholar 

  71. D’Avanzo B, La Vecchia C, Katsouyanni K, Negri E, Trichopoulos D (1997) An assessment and reproducibility of food frequency data provided by hospital controls. Eur J Cancer Prev 6:288–293

    Article  PubMed  Google Scholar 

  72. Cavaleiro-Pinto M, Peleteiro B, Lunet N, Barros H (2011) Helicobacter pylori infection and gastric cardia cancer: systematic review and meta-analysis. Cancer Causes Control 22:375–387

    Article  PubMed  Google Scholar 

  73. González CA, Megraud F, Buissonniere A, Lujan Barroso L, Agudo A, Duell EJ et al (2012) Helicobacter pylori infection assessed by ELISA and by immunoblot and noncardia gastric cancer risk in a prospective study: the Eurgast-EPIC project. Ann Oncol 23:1320–1324

    Article  PubMed  Google Scholar 

  74. Yoshida T, Kato J, Inoue I, Yoshimura N, Deguchi H, Mukoubayashi C et al (2013) Cancer development based on chronic active gastritis and resulting gastric atrophy as assessed by serum levels of pepsinogen and Helicobacter pylori antibody titer. Int J Cancer. doi:10.1002/ijc.28470

    Google Scholar 

  75. Boccia S, Hung R, Ricciardi G, Gianfagna F, Ebert MP, Fang JY et al (2008) Meta- and pooled analyses of the methylenetetrahydrofolate reductase C677T and A1298C polymorphisms and gastric cancer risk: a huge-GSEC review. Am J Epidemiol 167:505–516

    Article  PubMed  Google Scholar 

  76. Boccia S, La Vecchia C (2013) Dissecting causal components in gastric carcinogenesis. Eur J Cancer Prev 22:489–491

    Article  PubMed  Google Scholar 

  77. 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 19:869–877

    Article  PubMed Central  PubMed  Google Scholar 

  78. González CA, López-Carrillo L (2010) Helicobacter pylori, nutrition and smoking interactions: their impact in gastric carcinogenesis. Scand J Gastroenterol 45:6–14

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

Carlo La Vecchia and Eva Negri are supported by the Italian Foundation for Cancer Research (FIRC). The authors thank Ms I. Garimoldi for her help in preparing this manuscript.

Author information

Authors and Affiliations

  1. Science Integration Division, Social Determinants and Science Integration Directorate, Public Health Agency of Canada, 785 Carling Avenue, AL: 6807B, Ottawa, ON, K1A 0K9, Canada

    Jinfu Hu, Margaret de Groh, Howard Morrison & Les Mery

  2. Department of Clinical Medicine and Community Health, Università degli Studi di Milano, Milan, Italy

    Carlo La Vecchia

  3. IRCCS-Istituto di Ricerche Farmacologiche “Mario Negri”, Milan, Italy

    Eva Negri

Authors
  1. Jinfu Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Carlo La Vecchia
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Eva Negri
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Margaret de Groh
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Howard Morrison
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Les Mery
    View author publications

    You can also search for this author in PubMed Google Scholar

Consortia

The Canadian Cancer Registries Epidemiology Research Group

Corresponding author

Correspondence to Jinfu Hu.

Additional information

The members of the Canadian Cancer Registries Epidemiology Research Group are listed in the “Appendix” section.

Appendix

Appendix

The Canadian Cancer Registries Epidemiology Research Group comprises a principal investigator from each of the provincial cancer registries involved in the National Enhanced Cancer Surveillance System: Bertha Paulse, MSc, BN, Newfoundland Cancer Foundation; Ron Dewar, MA, Nova Scotia Cancer Registry; Dagny Dryer, MD, Prince Edward Island Cancer Registry; Nancy Kreiger, PhD, Cancer Care Ontario; Heather Whittaker, Manitoba Cancer Treatment and Research Foundation; Diane Robson, BA, Saskatchewan Cancer Foundation; Shirley Fincham, PhD, Alberta Cancer Board; and Nhu Le, PhD, British Columbia Cancer Agency.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hu, J., La Vecchia, C., Negri, E. et al. Macronutrient intake and stomach cancer. Cancer Causes Control 26, 839–847 (2015). https://doi.org/10.1007/s10552-015-0557-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10552-015-0557-9

Keywords

Search

Navigation