European Journal of Nutrition

, Volume 56, Issue 3, pp 1169–1177 | Cite as

Association between dietary carbohydrate intake, glycemic index and glycemic load, and risk of gastric cancer

Original Contribution

Abstract

Purpose

The association between dietary carbohydrate intake, glycemic index (GI) and glycemic load (GL), and risk of gastric cancer (GC) has been investigated by many studies. However, the results of these studies were controversial. The aim of our study was to systematically assess this issue.

Methods

PUBMED and EMBASE were searched up to March 2015, and either a fixed- or a random-effects model was adopted to estimate overall relative risks (RRs). Dose–response, meta-regression, subgroup, and publication bias analyses were applied.

Results

Twenty-six studies with approximately 540,000 participants were finally included in this meta-analysis. High level of dietary carbohydrate intake (pooled RR 1.17, 95 % CI 0.91–1.50), GI (pooled RR 1.17, 95 % CI 0.80–1.69), and GL (pooled RR 1.06, 95 % CI 0.90–1.26) were all nonsignificantly associated with incidence of GC. In addition, no significant dose–response relationship was observed between carbohydrate intake, GI and GL, and the risk of GC. However, further subgroup analyses based on gender and geographic region suggested a significant association between higher carbohydrate intake (pooled RR 1.52, 95 % CI 1.10–2.08), GL (pooled RR 1.41, 95 % CI 1.04–1.92), and GC risk in males subgroup, and between higher carbohydrate intake (pooled RR 1.69, 95 % CI 1.36–2.09) and GC risk in Asian studies.

Conclusions

No significant association was found between dietary carbohydrate intake, GI and GL, and risk of GC. However, significantly positive association was observed in the males subgroup and Asian studies.

Keywords

Carbohydrate intake Glycemic index Glycemic load Gastric cancer 

Supplementary material

394_2016_1166_MOESM1_ESM.docx (26 kb)
Supplementary material 1 (DOCX 26 kb)
394_2016_1166_MOESM2_ESM.tif (6.8 mb)
Supplementary material 2 (TIFF 6947 kb)

References

  1. 1.
    IARC (2014) Glonocan 2012: estimated cancer incidence, mortality and prevalence worldwide in 2012Google Scholar
  2. 2.
    Lissowska J, Gail MH, Pee D, Groves FD, Sobin LH, Nasierowska-Guttmejer A, Sygnowska E, Zatonski W, Blot WJ, Chow WH (2004) Diet and stomach cancer risk in Warsaw, Poland. Nutr Cancer 48:149–159CrossRefGoogle Scholar
  3. 3.
    Palli D, Russo A, Decarli A (2001) Dietary patterns, nutrient intake and gastric cancer in a high-risk area of Italy. Cancer Causes Control 12:163–172CrossRefGoogle Scholar
  4. 4.
    Ji BT, Chow WH, Yang G, McLaughlin JK, Zheng W, Shu XO, Jin F, Gao RN, Gao YT, Fraumeni JF Jr (1998) Dietary habits and stomach cancer in Shanghai, China. Int J Cancer 76:659–664CrossRefGoogle Scholar
  5. 5.
    Risch HA, Jain M, Choi NW, Fodor JG, Pfeiffer CJ, Howe GR, Harrison LW, Craib KJ, Miller AB (1985) Dietary factors and the incidence of cancer of the stomach. Am J Epidemiol 122:947–959CrossRefGoogle Scholar
  6. 6.
    Hidaka A, Sasazuki S, Goto A, Sawada N, Shimazu T, Yamaji T, Iwasaki M, Inoue M, Noda M, Tajiri H, Tsugane S (2014) Plasma insulin, C-peptide and blood glucose and the risk of gastric cancer: the Japan Public Health Center-based prospective study. Int J Cancer 136:1402–1410CrossRefGoogle Scholar
  7. 7.
    Stocks T, Rapp K, Bjorge T, Manjer J, Ulmer H, Selmer R, Lukanova A, Johansen D, Concin H, Tretli S, Hallmans G, Jonsson H, Stattin P (2009) Blood glucose and risk of incident and fatal cancer in the metabolic syndrome and cancer project (me-can): analysis of six prospective cohorts. PLoS Med 6:e1000201CrossRefGoogle Scholar
  8. 8.
    Nakajima TE, Yamada Y, Hamano T, Furuta K, Gotoda T, Katai H, Kato K, Hamaguchi T, Shimada Y (2009) Adipocytokine levels in gastric cancer patients: resistin and visfatin as biomarkers of gastric cancer. J Gastroenterol 44:685–690CrossRefGoogle Scholar
  9. 9.
    Ikeda F, Doi Y, Yonemoto K, Ninomiya T, Kubo M, Shikata K, Hata J, Tanizaki Y, Matsumoto T, Iida M, Kiyohara Y (2009) Hyperglycemia increases risk of gastric cancer posed by Helicobacter pylori infection: a population-based cohort study. Gastroenterology 136:1234–1241CrossRefGoogle Scholar
  10. 10.
    Stattin P, Bjor O, Ferrari P, Lukanova A, Lenner P, Lindahl B, Hallmans G, Kaaks R (2007) Prospective study of hyperglycemia and cancer risk. Diabetes Care 30:561–567CrossRefGoogle Scholar
  11. 11.
    Rapp K, Schroeder J, Klenk J, Ulmer H, Concin H, Diem G, Oberaigner W, Weiland SK (2006) Fasting blood glucose and cancer risk in a cohort of more than 140,000 adults in Austria. Diabetologia 49:945–952CrossRefGoogle Scholar
  12. 12.
    Wolever TM, Mehling C (2003) Long-term effect of varying the source or amount of dietary carbohydrate on postprandial plasma glucose, insulin, triacylglycerol, and free fatty acid concentrations in subjects with impaired glucose tolerance. Am J Clin Nutr 77:612–621Google Scholar
  13. 13.
    Crapo PA, Reaven G, Olefsky J (1977) Postprandial plasma-glucose and -insulin responses to different complex carbohydrates. Diabetes 26:1178–1183CrossRefGoogle Scholar
  14. 14.
    Onitilo AA, Engel JM, Glurich I, Stankowski RV, Williams GM, Doi SA (2012) Diabetes and cancer II: role of diabetes medications and influence of shared risk factors. Cancer Causes Control 23:991–1008CrossRefGoogle Scholar
  15. 15.
    Wolever TM, Bolognesi C (1996) Source and amount of carbohydrate affect postprandial glucose and insulin in normal subjects. J Nutr 126:2798–2806Google Scholar
  16. 16.
    Jenkins DJ, Wolever TM, Taylor RH, Barker H, Fielden H, Baldwin JM, Bowling AC, Newman HC, Jenkins AL, Goff DV (1981) Glycemic index of foods: a physiological basis for carbohydrate exchange. Am J Clin Nutr 34:362–366Google Scholar
  17. 17.
    Foster-Powell K, Holt SH, Brand-Miller JC (2002) International table of glycemic index and glycemic load values: 2002. Am J Clin Nutr 76:5–56Google Scholar
  18. 18.
    Atkinson FS, Foster-Powell K, Brand-Miller JC (2008) International tables of glycemic index and glycemic load values: 2008. Diabetes Care 31:2281–2283CrossRefGoogle Scholar
  19. 19.
    Hu J, La Vecchia C, Augustin LS, Negri E, de Groh M, Morrison H, Mery L (2013) Glycemic index, glycemic load and cancer risk. Ann Oncol 24:245–251CrossRefGoogle Scholar
  20. 20.
    Lazarevic K, Nagorni A, Jeremic M (2009) Carbohydrate intake, glycemic index, glycemic load and risk of gastric cancer. Cent Eur J Public Health 17:75–78Google Scholar
  21. 21.
    George SM, Mayne ST, Leitzmann MF, Park Y, Schatzkin A, Flood A, Hollenbeck A, Subar AF (2009) Dietary glycemic index, glycemic load, and risk of cancer: a prospective cohort study. Am J Epidemiol 169:462–472CrossRefGoogle Scholar
  22. 22.
    Bertuccio P, Praud D, Chatenoud L, Lucenteforte E, Bosetti C, Pelucchi C, Rossi M, Negri E, La Vecchia C (2009) Dietary glycemic load and gastric cancer risk in Italy. Br J Cancer 100:558–561CrossRefGoogle Scholar
  23. 23.
    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 118:3167–3169CrossRefGoogle Scholar
  24. 24.
    Augustin LSA, Gallus S, Negri E, La Vecchia C (2004) Glycemic index, glycemic load and risk of gastric cancer. Ann Oncol 15:581–584CrossRefGoogle Scholar
  25. 25.
    Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D, Moher D, Becker BJ, Sipe TA, Thacker SB (2000) Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group. JAMA 283:2008–2012CrossRefGoogle Scholar
  26. 26.
    Moher D, Liberati A, Tetzlaff J, Altman DG (2010) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Int J Surg 8:336–341CrossRefGoogle Scholar
  27. 27.
    Stang A (2010) Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol 25:603–605CrossRefGoogle Scholar
  28. 28.
    Higgins JP, Thompson SG (2002) Quantifying heterogeneity in a meta-analysis. Stat Med 21:1539–1558CrossRefGoogle Scholar
  29. 29.
    Greenland S (1995) Dose-response and trend analysis in epidemiology: alternatives to categorical analysis. Epidemiology 6:356–365CrossRefGoogle Scholar
  30. 30.
    Laroiya I, Pankaja S, Mittal S, Kate V (2012) A study of Helicobacter pylori infection, dietary pattern and habits in patients with gastric cancer in South India. Asian Pac J Trop Dis 2:24–26CrossRefGoogle Scholar
  31. 31.
    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 11:4311–4316CrossRefGoogle Scholar
  32. 32.
    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 52:138–146CrossRefGoogle Scholar
  33. 33.
    Chen H, Tucker KL, Graubard BI, Heineman EF, Markin RS, Potischman NA, Russell RM, Weisenburger DD, Ward MH (2002) Nutrient intakes and adenocarcinoma of the esophagus and distal stomach. Nutr Cancer 42:33–40CrossRefGoogle Scholar
  34. 34.
    Munoz N, Plummer M, Vivas J, Moreno V, De Sanjose S, Lopez G, Oliver W (2001) A case–control study of gastric cancer in Venezuela. Int J Cancer 93:417–423CrossRefGoogle Scholar
  35. 35.
    Mayne ST, Risch HA, Dubrow R, Chow WH, Gammon MD, Vaughan TL, Farrow DC, Schoenberg JB, Stanford JL, Ahsan H, West AB, Rotterdam H, Blot WJ, Fraumeni JF Jr (2001) Nutrient intake and risk of subtypes of esophageal and gastric cancer. Cancer Epidemiol Biomark Prev 10:1055–1062Google Scholar
  36. 36.
    Jedrychowski W, Popiela T, Steindorf K, Tobiasz-Adamczyk B, Kulig J, Penar A, Wahrendorf J (2001) Nutrient intake patterns in gastric and colorectal cancers. Int J Occup Med Environ Health 14:391–395Google Scholar
  37. 37.
    Lopez-Carrillo L, Lopez-Cervantes M, Ward MH, Bravo-Alvarado J, Ramirez-Espitia A (1999) Nutrient intake and gastric cancer in Mexico. Int J Cancer 83:601–605CrossRefGoogle Scholar
  38. 38.
    De Stefani E, Boffetta P, Deneo-Pellegrini H, Mendilaharsu M, Carzoglio JC, Ronco A (1999) Carbohydrates and risk of stomach cancer in Uruguay. Int J Cancer 82:618–621CrossRefGoogle Scholar
  39. 39.
    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 80:1021–1028CrossRefGoogle Scholar
  40. 40.
    Li D, Gao X, Xing W (1995) Use of nutrient density in etiologic studies on stomach cancer. Zhonghua Yu Fang Yi Xue Za Zhi 29:339–341Google Scholar
  41. 41.
    Cornee J, Pobel D, Riboli E, Guyader M, Hemon B (1995) A case–control study of gastric cancer and nutritional factors in Marseille, France. Eur J Epidemiol 11:55–65CrossRefGoogle Scholar
  42. 42.
    Hansson LE, Nyren O, Bergstrom R, Wolk A, Lindgren A, Baron J, Adami HO (1994) Nutrients and gastric cancer risk. A population-based case–control study in Sweden. Int J Cancer 57:638–644CrossRefGoogle Scholar
  43. 43.
    Ramon JM, Serra-Majem L, Cerdo C, Oromi J (1993) Nutrient intake and gastric cancer risk: a case–control study in Spain. Int J Epidemiol 22:983–988CrossRefGoogle Scholar
  44. 44.
    Buiatti E, Palli D, Bianchi S, Decarli A, Amadori D, Avellini C, Cipriani F, Cocco P, Giacosa A, Lorenzini L et al (1991) A case–control study of gastric cancer and diet in Italy. III. Risk patterns by histologic type. Int J Cancer 48:369–374CrossRefGoogle Scholar
  45. 45.
    Nomura A, Grove JS, Stemmermann GN, Severson RK (1990) A prospective study of stomach cancer and its relation to diet, cigarettes, and alcohol consumption. Cancer Res 50:627–631Google Scholar
  46. 46.
    Correa P, Fontham E, Pickle LW, Chen V, Lin YP, Haenszel W (1985) Dietary determinants of gastric cancer in south Louisiana inhabitants. J Natl Cancer Inst 75:645–654Google Scholar
  47. 47.
    Tseng CH, Tseng FH (2014) Diabetes and gastric cancer: the potential links. World J Gastroenterol 20:1701–1711CrossRefGoogle Scholar
  48. 48.
    Szablewski L (2014) Diabetes mellitus: influences on cancer risk. Diabetes Metab Res Rev 30:543–553CrossRefGoogle Scholar
  49. 49.
    Hunt RH, Xiao SD, Megraud F, Leon-Barua R, Bazzoli F, van der Merwe S, Vaz Coelho LG, Fock M, Fedail S, Cohen H, Malfertheiner P, Vakil N, Hamid S, Goh KL, Wong BC, Krabshuis J, Le Mair A (2011) Helicobacter pylori in developing countries. World Gastroenterology Organisation global guideline. J Gastrointest Liver Dis 20:299–304Google Scholar
  50. 50.
    Marimuthu SP, Vijayaragavan P, Moysich KB, Jayaprakash V (2011) Diabetes mellitus and gastric carcinoma: is there an association? J Carcinog 10:30CrossRefGoogle Scholar
  51. 51.
    Tian T, Zhang LQ, Ma XH, Zhou JN, Shen J (2012) Diabetes mellitus and incidence and mortality of gastric cancer: a meta-analysis. Exp Clin Endocrinol Diabetes 120:217–223CrossRefGoogle Scholar
  52. 52.
    Jenkins D, Axelsen M, Kendall C, Augustin L, Vuksan V, Smith U (2000) Dietary fibre, lente carbohydrates and the insulin-resistant diseases. Br J Nutr 83(Suppl 1):S157–S163Google Scholar
  53. 53.
    Lorenzi M, Montisano DF, Toledo S, Barrieux A (1986) High glucose induces DNA damage in cultured human endothelial cells. J Clin Invest 77:322–325CrossRefGoogle Scholar
  54. 54.
    Mahdy RA, Nada WM (2011) Evaluation of the role of vascular endothelial growth factor in diabetic retinopathy. Ophthalmic Res 45:87–91CrossRefGoogle Scholar
  55. 55.
    Kasuga M, Ueki K, Tajima N, Noda M, Ohashi K, Noto H, Goto A, Ogawa W, Sakai R, Tsugane S, Hamajima N, Nakagama H, Tajima K, Miyazono K, Imai K (2013) Report of the Japan Diabetes Society/Japanese Cancer Association Joint Committee on diabetes and cancer. Cancer Sci 104:965–976CrossRefGoogle Scholar
  56. 56.
    Giovannucci E (2001) Insulin, insulin-like growth factors and colon cancer: a review of the evidence. J Nutr 131:3109s–3120sGoogle Scholar
  57. 57.
    Biddinger SB, Ludwig DS (2005) The insulin-like growth factor axis: a potential link between glycemic index and cancer. Am J Clin Nutr 82:277–278Google Scholar
  58. 58.
    Aune D, Chan DS, Lau R, Vieira R, Greenwood DC, Kampman E, Norat T (2012) Carbohydrates, glycemic index, glycemic load, and colorectal cancer risk: a systematic review and meta-analysis of cohort studies. Cancer Causes Control 23:521–535CrossRefGoogle Scholar
  59. 59.
    Mulholland HG, Murray LJ, Cardwell CR, Cantwell MM (2009) Glycemic index, glycemic load, and risk of digestive tract neoplasms: a systematic review and meta-analysis. Am J Clin Nutr 89:568–576CrossRefGoogle Scholar
  60. 60.
    Pi-Sunyer FX (2002) Glycemic index and disease. Am J Clin Nutr 76:290s–298sGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Department of ToxicologyZhejiang University School of Public HealthHangzhouChina
  2. 2.Department of Oncology, Second Affiliated HospitalZhejiang University College of MedicineHangzhouChina
  3. 3.Department of Epidemiology and Health StatisticsZhejiang University School of Public HealthHangzhouChina
  4. 4.Jinhua Central HospitalJinhua Hospital of Zhejiang UniversityJinhuaChina
  5. 5.Zhejiang University School of Public HealthHangzhouChina

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