Skip to main content
Log in

Rye bread consumption in early life and reduced risk of advanced prostate cancer

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

Abstract

Objective

To determine whether consumption of whole-grain rye bread, oatmeal, and whole-wheat bread, during different periods of life, is associated with risk of prostate cancer (PCa).

Methods

From 2002 to 2006, 2,268 men, aged 67–96 years, reported their dietary habits in the AGES-Reykjavik cohort study. Dietary habits were assessed for early life, midlife, and current life using a validated food frequency questionnaire. Through linkage to cancer and mortality registers, we retrieved information on PCa diagnosis and mortality through 2009. We used regression models to estimate odds ratios (ORs) and hazard ratios (HRs) for PCa according to whole-grain consumption, adjusted for possible confounding factors including fish, fish liver oil, meat, and milk intake.

Results

Of the 2,268 men, 347 had or were diagnosed with PCa during follow-up, 63 with advanced disease (stage 3+ or died of PCa). Daily rye bread consumption in adolescence (vs. less than daily) was associated with a decreased risk of PCa diagnosis (OR = 0.76, 95 % confidence interval (CI): 0.59–0.98) and of advanced PCa (OR = 0.47, 95 % CI: 0.27–0.84). High intake of oatmeal in adolescence (≥5 vs. ≤4 times/week) was not significantly associated with risk of PCa diagnosis (OR = 0.99, 95 % CI: 0.77–1.27) nor advanced PCa (OR = 0.67, 95 % CI: 0.37–1.20). Midlife and late life consumption of rye bread, oatmeal, or whole-wheat bread was not associated with PCa risk.

Conclusion

Our results suggest that rye bread consumption in adolescence may be associated with reduced risk of PCa, particularly advanced disease.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

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

    Google Scholar 

  2. Rastogi T, Devesa S, Mangtani P, Mathew A, Cooper N, Kao R, Sinha R (2008) Cancer incidence rates among South Asians in four geographic regions: India, Singapore, UK and US. Int J Epidemiol 37(1):147–160. doi:10.1093/ije/dym219

    Article  PubMed  Google Scholar 

  3. Slavin JL (2000) Mechanisms for the impact of whole grain foods on cancer risk. J Am Coll Nutr 19(3 suppl):300S–307S

    PubMed  CAS  Google Scholar 

  4. Adlercreutz H (2007) Lignans and human health. Crit Rev Clin Lab Sci 44(5–6):483–525. doi:10.1080/10408360701612942

    Article  PubMed  CAS  Google Scholar 

  5. Tsubaki J, Hwa V, Twigg SM, Rosenfeld RG (2002) Differential activation of the IGF binding protein-3 promoter by butyrate in prostate cancer cells. Endocrinology 143(5):1778–1788

    Article  PubMed  CAS  Google Scholar 

  6. Laaksonen DE, Toppinen LK, Juntunen KS, Autio K, Liukkonen KH, Poutanen KS, Niskanen L, Mykkanen HM (2005) Dietary carbohydrate modification enhances insulin secretion in persons with the metabolic syndrome. Am J Clin Nutr 82(6):1218–1227

    PubMed  CAS  Google Scholar 

  7. Leinonen K, Liukkonen K, Poutanen K, Uusitupa M, Mykkanen H (1999) Rye bread decreases postprandial insulin response but does not alter glucose response in healthy Finnish subjects. Euro J Clin Nutr 53(4):262–267

    Article  CAS  Google Scholar 

  8. Coughlin SS, Calle EE, Teras LR, Petrelli J, Thun MJ (2004) Diabetes mellitus as a predictor of cancer mortality in a large cohort of US adults. Am J Epidemiol 159(12):1160–1167. doi:10.1093/aje/kwh161159/12/1160

    Article  PubMed  Google Scholar 

  9. Giovannucci E, Michaud D (2007) The role of obesity and related metabolic disturbances in cancers of the colon, prostate, and pancreas. Gastroenterology 132(6):2208–2225. doi:10.1053/j.gastro.2007.03.050

    Article  PubMed  CAS  Google Scholar 

  10. Hsu IR, Kim SP, Kabir M, Bergman RN (2007) Metabolic syndrome, hyperinsulinemia, and cancer. Am J Clin Nutr 86(3):s867–s871

    PubMed  Google Scholar 

  11. Lewis JE, Soler-Vila H, Clark PE, Kresty LA, Allen GO, Hu JJ (2009) Intake of plant foods and associated nutrients in prostate cancer risk. Nutr Cancer 61(2):216–224. doi:10.1080/01635580802419756

    Article  PubMed  CAS  Google Scholar 

  12. Jain MG, Hislop GT, Howe GR, Ghadirian P (1999) Plant foods, antioxidants, and prostate cancer risk: findings from case-control studies in Canada. Nutr Cancer 34(2):173–184. doi:10.1207/S15327914NC3402_8

    Article  PubMed  CAS  Google Scholar 

  13. La Vecchia C, Chatenoud L, Negri E, Franceschi S (2003) Session: whole cereal grains, fibre and human cancer wholegrain cereals and cancer in Italy. Proc Nutr Soc 62(1):45–49. doi:10.1079/PNS2002235

    Article  PubMed  Google Scholar 

  14. Chatenoud L, Tavani A, La Vecchia C, Jacobs DR Jr, Negri E, Levi F, Franceschi S (1998) Whole grain food intake and cancer risk. Int J Cancer 77(1):24–28

    Article  PubMed  CAS  Google Scholar 

  15. Nimptsch K, Kenfield S, Jensen MK, Stampfer MJ, Franz M, Sampson L, Brand-Miller JC, Willett WC, Giovannucci E (2011) Dietary glycemic index, glycemic load, insulin index, fiber and whole-grain intake in relation to risk of prostate cancer. Cancer Causes Control 22(1):51–61. doi:10.1007/s10552-010-9671-x

    Article  PubMed  CAS  Google Scholar 

  16. Egeberg R, Olsen A, Christensen J, Johnsen NF, Loft S, Overvad K, Tjonneland A (2011) Intake of whole-grain products and risk of prostate cancer among men in the Danish diet, cancer and health cohort study. Cancer Causes Control 22(8):1133–1139. doi:10.1007/s10552-011-9789-5

    Article  PubMed  Google Scholar 

  17. Adlercreutz H, Mazur W (1997) Phyto-oestrogens and Western diseases. Ann Med 29(2):95–120

    PubMed  CAS  Google Scholar 

  18. Bylund A, Zhang JX, Bergh A, Damber JE, Widmark A, Johansson A, Adlercreutz H, Aman P, Shepherd MJ, Hallmans G (2000) Rye bran and soy protein delay growth and increase apoptosis of human LNCaP prostate adenocarcinoma in nude mice. Prostate 42(4):304–314. doi:10.1002/(SICI)1097-0045(20000301)42:4<304:AID-PROS8>3.0.CO;2-Z

    Article  PubMed  CAS  Google Scholar 

  19. Landstrom M, Zhang JX, Hallmans G, Aman P, Bergh A, Damber JE, Mazur W, Wahala K, Adlercreutz H (1998) Inhibitory effects of soy and rye diets on the development of dunning R3327 prostate adenocarcinoma in rats. Prostate 36(3):151–161. doi:10.1002/(SICI)1097-0045(19980801)36:3<151:AID-PROS2>3.0.CO;2-K

    Article  PubMed  CAS  Google Scholar 

  20. Landberg R, Andersson SO, Zhang JX, Johansson JE, Stenman UH, Adlercreutz H, Kamal-Eldin A, Aman P, Hallmans G (2010) Rye whole grain and bran intake compared with refined wheat decreases urinary C-peptide, plasma insulin, and prostate specific antigen in men with prostate cancer. J Nutr 140(12):2180–2186. doi:10.3945/jn.110.127688

    Article  PubMed  CAS  Google Scholar 

  21. Bylund A, Lundin E, Zhang JX, Nordin A, Kaaks R, Stenman UH, Aman P, Adlercreutz H, Nilsson TK, Hallmans G, Bergh A, Stattin P (2003) Randomised controlled short-term intervention pilot study on rye bran bread in prostate cancer. Euro J Cancer Prev 12(5):407–415. doi:10.1097/01.cej.0000090180.08740.05

    Article  CAS  Google Scholar 

  22. Torfadottir JE, Steingrimsdottir L, Mucci L, Aspelund T, Kasperzyk JL, Olafsson O, Fall K, Tryggvadottir L, Harris TB, Launer L, Jonsson E, Tulinius H, Stampfer M, Adami HO, Gudnason V, Valdimarsdottir UA (2012) Milk intake in early life and risk of advanced prostate cancer. Am J Epidemiol 175(2):144–153. doi:10.1093/aje/kwr289

    Article  PubMed  Google Scholar 

  23. Jónsson G (1998) Changes in food consumption in Iceland, 1770–1940. Scand Econ Hist Rev XLVI 1:24–41

    Article  Google Scholar 

  24. Sigurjonsson J (1943) Survey on diet and health in Iceland (1939–1940). Icelandic Nutrition Council, Reykjavik

  25. Harris TB, Launer LJ, Eiriksdottir G, Kjartansson O, Jonsson PV, Sigurdsson G, Thorgeirsson G, Aspelund T, Garcia ME, Cotch MF, Hoffman HJ, Gudnason V (2007) Age, gene/environment susceptibility-Reykjavik Study: multidisciplinary applied phenomics. Am J Epidemiol 165(9):1076–1087. doi:10.1093/aje/kwk115

    Article  PubMed  Google Scholar 

  26. Eysteinsdottir T, Gunnarsdottir I, Thorsdottir I, Harris T, Launer LJ, Gudnason V, Steingrimsdottir L (2011) Validity of retrospective diet history: assessing recall of midlife diet using food frequency questionnaire in later life. J Nutr Health Aging 15(10):809–814

    Article  PubMed  CAS  Google Scholar 

  27. Eysteinsdottir T, Gunnarsdottir I, Thorsdottir I, Harris T, Launer LJ, Gudnason V, Steingrimsdottir L (2010) Validity of retrospective diet history: assessing recall of midlife diet using food frequency questionnaire in later life. JNHA (in press)

  28. Vilbergsson S, Sigurdsson G, Sigvaldason H, Hreidarsson AB, Sigfusson N (1997) Prevalence and incidence of NIDDM in Iceland: evidence for stable incidence among males and females 1967–1991–the Reykjavik Study. Diabet Med 14(6):491–498. doi:10.1002/(SICI)1096-9136(199706)14:6<491:AID-DIA365>3.0.CO;2-1

    Article  PubMed  CAS  Google Scholar 

  29. Møller B, Fekjaer H, Hakulinen T, Tryggvadottir L, Storm HH, Talback M, Haldorsen T (2002) Prediction of cancer incidence in the Nordic countries up to the year 2020. Euro J Cancer Prev 11(Suppl 1):S1–S96

    Google Scholar 

  30. Jonasson JG, Tryggvadottir L (2007) Iceland. In: Curado MP, Edwards B, Shin HR, Storm H, Ferlay J, Heanue M, Boyle P (eds) Cancer incidence in five continents. International agency for research on cancer (IARC Scientific Publications No. 160). Lyon, p 312

  31. Icelandic Cancer Registry Homepage of the Icelandic Cancer Registry (2006) http://www.cancerregistry.is. Accessed July 2010

  32. Bray F, Klint A, Gislum M, Hakulinen T, Engholm G, Tryggvadottir L, Storm HH (2010) Trends in survival of patients diagnosed with male genital cancers in the Nordic countries 1964–2003 followed up until the end of 2006. Acta Oncol 49(5):644–654

    Article  PubMed  Google Scholar 

  33. Andresdottir MB, Sigfusson N, Sigvaldason H, Gudnason V (2003) Erythrocyte sedimentation rate, an independent predictor of coronary heart disease in men and women: the Reykjavik Study. Am J Epidemiol 158(9):844–851

    Article  PubMed  Google Scholar 

  34. Chen PC, Tseng TC, Hsieh JY, Lin HW (2011) Association between stroke and patients with pelvic inflammatory disease: a nationwide population-based study in Taiwan. Stroke J Cerebr Circul 42(7):2074–2076. doi:10.1161/STROKEAHA.110.612655

    Article  Google Scholar 

  35. Shimizu H, Ross RK, Bernstein L, Yatani R, Henderson BE, Mack TM (1991) Cancers of the prostate and breast among Japanese and white immigrants in Los Angeles County. Br J Cancer 63(6):963–966

    Article  PubMed  CAS  Google Scholar 

  36. Hemminki K, Li X (2002) Cancer risks in second-generation immigrants to Sweden. Int J Cancer 99(2):229–237. doi:10.1002/ijc.10323

    Article  PubMed  CAS  Google Scholar 

  37. Dwyer JT, Coleman KA (1997) Insights into dietary recall from a longitudinal study: accuracy over four decades. Am J Clin Nutr 65(4 suppl):1153S–1158S

    PubMed  CAS  Google Scholar 

  38. Strom SS, Yamamura Y, Duphorne CM, Spitz MR, Babaian RJ, Pillow PC, Hursting SD (1999) Phytoestrogen intake and prostate cancer: a case-control study using a new database. Nutr Cancer 33(1):20–25. doi:10.1080/01635589909514743

    Article  PubMed  CAS  Google Scholar 

  39. McCann SE, Ambrosone CB, Moysich KB, Brasure J, Marshall JR, Freudenheim JL, Wilkinson GS, Graham S (2005) Intakes of selected nutrients, foods, and phytochemicals and prostate cancer risk in western New York. Nutr Cancer 53(1):33–41. doi:10.1207/s15327914nc5301_4

    Article  PubMed  CAS  Google Scholar 

  40. Hedelin M, Klint A, Chang ET, Bellocco R, Johansson JE, Andersson SO, Heinonen SM, Adlercreutz H, Adami HO, Gronberg H, Balter KA (2006) Dietary phytoestrogen, serum enterolactone and risk of prostate cancer: the cancer prostate Sweden study (Sweden). Cancer Causes Control 17(2):169–180. doi:10.1007/s10552-005-0342-2

    Article  PubMed  Google Scholar 

  41. Stattin P, Bylund A, Biessy C, Kaaks R, Hallmans G, Adlercreutz H (2004) Prospective study of plasma enterolactone and prostate cancer risk (Sweden). Cancer Causes Control 15(10):1095–1102

    Article  PubMed  Google Scholar 

  42. Stattin P, Adlercreutz H, Tenkanen L, Jellum E, Lumme S, Hallmans G, Harvei S, Teppo L, Stumpf K, Luostarinen T, Lehtinen M, Dillner J, Hakama M (2002) Circulating enterolactone and prostate cancer risk: a Nordic nested case-control study. Int J Cancer 99(1):124–129. doi:10.1002/ijc.10313

    Article  PubMed  CAS  Google Scholar 

  43. Kilkkinen A, Virtamo J, Virtanen MJ, Adlercreutz H, Albanes D, Pietinen P (2003) Serum enterolactone concentration is not associated with prostate cancer risk in a nested case-control study. Cancer Epidemiol Biomarkers Prev 12(11 Pt 1):1209–1212

    PubMed  CAS  Google Scholar 

  44. Pettersson K, Gustafsson JA (2001) Role of estrogen receptor beta in estrogen action. Annu Rev Physiol 63:165–192. doi:10.1146/annurev.physiol.63.1.16563/1/165

    Article  PubMed  CAS  Google Scholar 

  45. Hall JM, Couse JF, Korach KS (2001) The multifaceted mechanisms of estradiol and estrogen receptor signaling. J Biol Chem 276(40):36869–36872. doi:10.1074/jbc.R100029200R100029200

    Article  PubMed  CAS  Google Scholar 

  46. Mueller SO, Simon S, Chae K, Metzler M, Korach KS (2004) Phytoestrogens and their human metabolites show distinct agonistic and antagonistic properties on estrogen receptor alpha (ERalpha) and ERbeta in human cells. Toxicol Sci 80(1):14–25. doi:10.1093/toxsci/kfh147kfh147

    Article  PubMed  CAS  Google Scholar 

  47. Cummings JH, Pomare EW, Branch WJ, Naylor CP, Macfarlane GT (1987) Short chain fatty acids in human large intestine, portal, hepatic and venous blood. Gut 28(10):1221–1227

    Article  PubMed  CAS  Google Scholar 

  48. Arts CJ, Govers CA, van den Berg H, Wolters MG, van Leeuwen P, Thijssen JH (1991) In vitro binding of estrogens by dietary fiber and the in vivo apparent digestibility tested in pigs. J Steroid Biochem Mol Biol 38(5):621–628

    Article  PubMed  CAS  Google Scholar 

  49. Collier A, Ghosh S, McGlynn B, Hollins G (2011) Prostate cancer, androgen deprivation therapy, obesity, the metabolic syndrome, type 2 diabetes, and cardiovascular disease: a review. Am J Clin Oncol. doi:10.1097/COC.0b013e318201a406

  50. Renehan AG, Zwahlen M, Minder C, O’Dwyer ST, Shalet SM, Egger M (2004) Insulin-like growth factor (IGF)-I, IGF binding protein-3, and cancer risk: systematic review and meta-regression analysis. Lancet 363(9418):1346–1353. doi:10.1016/S0140-6736(04)16044-3S0140-6736(04)16044-3

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We wish to thank Oddur Benediktsson (1937–2010) and the organization Framför for their support and interest in the study. JET is supported by Framför (Progress), an Icelandic organization that aims to fund research and education initiatives related to prostate cancer, the Icelandic Cancer Society and NordForsk, Nordic Centre of Excellence programme: HELGA: Nordic Health Whole Grain Food. JLK is supported by HELGA, in part by training grant NIH 5 T32 CA09001-36 and by the American Institute for Cancer Research. This study was also funded in part by the National Institute on Aging contract N01-AG-1-2100, in part by the Intramural Research Program of the National Institute on Aging, the Icelandic Heart Association, and the Althingi (the Icelandic Parliament).

Conflict of interest

None declared.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Johanna E. Torfadottir.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Torfadottir, J.E., Valdimarsdottir, U.A., Mucci, L. et al. Rye bread consumption in early life and reduced risk of advanced prostate cancer. Cancer Causes Control 23, 941–950 (2012). https://doi.org/10.1007/s10552-012-9965-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10552-012-9965-2

Keywords

Navigation