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Epidemiology

Adolescent animal product intake in relation to later prostate cancer risk and mortality in the NIH-AARP Diet and Health Study

British Journal of Cancer volume 125, pages 1158–1167 (2021)Cite this article

Subjects

Abstract

Background

Adolescent intake of animal products has been proposed to contribute to prostate cancer (PCa) development because of its potentially carcinogenic constituents and influence on hormone levels during adolescence.

Methods

We used data from 159,482 participants in the NIH-AARP Diet and Health Study to investigate associations for recalled adolescent intake of red meat (unprocessed beef and processed red meat), poultry, egg, canned tuna, animal fat and animal protein at ages 12–13 years with subsequent PCa risk and mortality over 14 years of follow-up. Cox proportional hazard regression was used to calculate hazard ratios (HRs) and 95% confidence intervals (CIs) of total (n = 17,349), advanced (n = 2,297) and fatal (n = 804) PCa.

Results

Suggestive inverse trends were observed for adolescent unprocessed beef intake with risks of total, advanced and fatal PCa (multivariable-adjusted P-trends = 0.01, 0.02 and 0.04, respectively). No consistent patterns of association were observed for other animal products by PCa outcome.

Conclusion

We found evidence to suggest that adolescent unprocessed beef intake, or possibly a correlate of beef intake, such as early-life socioeconomic status, may be associated with reduced risk and mortality from PCa. Additional studies with further early-life exposure information are warranted to better understand this association.

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Data availability

AARP Study data are available through the National Cancer Institute.

References

  1. Siegel RL, Miller KD, Jemal A. Cancer statistics, 2020. CA: Cancer J Clin. 2020;70:7–30.

    Google Scholar 

  2. Armstrong B, Doll R. Environmental factors and cancer incidence and mortality in different countries, with special reference to dietary practices. Int J Cancer. 1975;15:617–631.

    Article  CAS  PubMed  Google Scholar 

  3. Gronberg H. Prostate cancer epidemiology. Lancet. 2003;361:859–64.

    Article  PubMed  Google Scholar 

  4. Parkin DM, Steinitz R, Khlat M, Kaldor J, Katz L, Young J. Cancer in Jewish migrants to Israel. Int J Cancer. 1990;45:614–21.

    Article  CAS  PubMed  Google Scholar 

  5. Tyczynski J, Tarkowski W, Parkin DM, Zatonski, W. Cancer mortality among Polish migrants to Australia. Eur J Cancer. 1994;30A:478–84.

  6. Whittemore AS, Kolonel LN, Wu AH, John EM, Gallagher RP, Howe GR, et al. Prostate cancer in relation to diet, physical activity, and body size in blacks, whites, and Asians in the United States and Canada. J Natl Cancer Inst. 1995;87:652–61.

    Article  CAS  PubMed  Google Scholar 

  7. McCredie M, Williams S, Coates M. Cancer mortality in East and Southeast Asian migrants to New South Wales, Australia, 1975-95. Br J Cancer. 1999;79:1277–82.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Beiki O, Ekbom A, Allebeck P, Moradi T. Risk of prostate cancer among Swedish-born and foreign-born men in Sweden, 1961-2004. Int J Cancer. 2009;124:1941–53.

    Article  CAS  PubMed  Google Scholar 

  9. Andersson SO, Baron J, Wolk A, Lindgren C, Bergstrom R, Adami HO. Early life risk factors for prostate cancer: a population-based case-control study in Sweden. Cancer Epidemiol Biomark Prev. 1995;4:187–92.

    CAS  Google Scholar 

  10. Torfadottir JE, Steingrimsdottir L, Mucci L, Aspelund T, Kasperzyk JL, Olafsson O, et al. Milk intake in early life and risk of advanced prostate cancer. Am J Epidemiol. 2012;175:144–53.

    Article  PubMed  Google Scholar 

  11. Mills PK, Beeson WL, Phillips RL, Fraser GE. Cohort study of diet, lifestyle, and prostate cancer in Adventist men. Cancer. 1989;64:598–604.

    Article  CAS  PubMed  Google Scholar 

  12. Slattery ML, Schumacher MC, West DW, Robison LM, French TK. Food-consumption trends between adolescent and adult years and subsequent risk of prostate cancer. Am J Clin Nutr. 1990;52:752–7.

    Article  CAS  PubMed  Google Scholar 

  13. Torfadottir JE, Valdimarsdottir UA, Mucci LA, Kasperzyk JL, Fall K, Tryggvadottir L, et al. Consumption of fish products across the lifespan and prostate cancer risk. PLoS ONE. 2013;8:e59799.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Whittemore AS, Paffenbarger RS Jr., Anderson K, Lee JE. Early precursors of site-specific cancers in college men and women. J Natl Cancer Inst. 1985;74:43–51.

    CAS  PubMed  Google Scholar 

  15. Dirx MJ, van den Brandt PA, Goldbohm RA, Lumey, LJAJOE. Energy restriction in childhood and adolescence and risk of prostate cancer: results from the Netherlands Cohort Study. Am J Epidemiol. 2001;154:530–7.

  16. Sutcliffe S, Colditz GA. Prostate cancer: is it time to expand the research focus to early-life exposures? Nat Rev Cancer. 2013;13:208–518.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Suttie AW, Dinse GE, Nyska A, Moser GJ, Goldsworthy TL, Maronpot RR. An investigation of the effects of late-onset dietary restriction on prostate cancer development in the TRAMP mouse. Toxicol Pathol. 2005;33:386–97.

    Article  CAS  PubMed  Google Scholar 

  18. Cai LQ, Imperato-McGinley J, Zhu YS. Regulation of prostate 5alpha-reductase-2 gene expression and prostate weight by dietary fat and caloric intake in the rat. Prostate. 2006;66:738–48.

    Article  CAS  PubMed  Google Scholar 

  19. Diamandis EP, Yu H. Does prostate cancer start at puberty? J Clin Lab Anal. 1996;10:468–9.

    Article  CAS  PubMed  Google Scholar 

  20. Van Egeren D, Escabi J, Nguyen M, Liu S, Reilly CR, Patel S, et al. Reconstructing the lineage histories and differentiation trajectories of individual cancer cells in myeloproliferative neoplasms. Cell Stem Cell. 2021;28:514–23. e519

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. Mitchell TJ, Turajlic S, Rowan A, Nicol D, Farmery J, O’brien T, et al. Timing the landmark events in the evolution of clear cell renal cell cancer: TRACERx renal. Cell. 2018;173:611–23. e617

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Sakr WA, Grignon DJ, Crissman JD, Heilbrun LK, Cassin BJ, Pontes JJ, et al. High grade prostatic intraepithelial neoplasia (HGPIN) and prostatic adenocarcinoma between the ages of 20-69: an autopsy study of 249 cases. In Vivo. 1994;8:439–43.

    CAS  PubMed  Google Scholar 

  23. Gu FL, Xia TL, Kong XT. Preliminary study of the frequency of benign prostatic hyperplasia and prostatic cancer in China. Urology. 1994;44:688–91.

    Article  CAS  PubMed  Google Scholar 

  24. Jackson MA, Kovi J, Heshmat MY, Jones GW, Rao MS, Ahluwalia BS. Factors involved in the high incidence of prostatic cancer among American blacks. Prog Clin Biol Res. 1981;53:111–32.

    CAS  PubMed  Google Scholar 

  25. Sakr WA, Haas GP, Cassin BF, Pontes JE, Crissman JD. The frequency of carcinoma and intraepithelial neoplasia of the prostate in young male patients. J Urol. 1993;150:379–85.

    Article  CAS  PubMed  Google Scholar 

  26. Sanchez-Chapado M, Olmedilla G, Cabeza M, Donat E, Ruiz A. Prevalence of prostate cancer and prostatic intraepithelial neoplasia in Caucasian Mediterranean males: an autopsy study. Prostate. 2003;54:238–47.

    Article  PubMed  Google Scholar 

  27. Yin M, Bastacky S, Chandran U, Becich MJ, Dhir R. Prevalence of incidental prostate cancer in the general population: a study of healthy organ donors. J Urol. 2008;179:892–5.

    Article  PubMed  Google Scholar 

  28. Jahn JL, Giovannucci EL, Stampfer MJ. The high prevalence of undiagnosed prostate cancer at autopsy: implications for epidemiology and treatment of prostate cancer in the prostate-specific antigen-era. Int J Cancer. 2015;137:2795–802.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Howlader N, Noone A, Krapcho M, Noone A, Neyman N, Aminou R et al. SEER cancer statistics review. 1975–2009 (vintage 2009 populations). Bethesda, MD: National Cancer Institute. 2012. https://seer.cancer.gov/archive/csr/1975_2009_pops09/. Accessed 11 June 2021.

  30. Alimujiang A, Colditz GA, Gardner JD, Park Y, Berkey CS, Sutcliffe S. Childhood diet and growth in boys in relation to timing of puberty and adult height: the Longitudinal Studies of Child Health and Development. Cancer Causes Control. 2018;29:915–26.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Gunnell D, Okasha M, Smith GD, Oliver SE, Sandhu J, Holly JM. Height, leg length, and cancer risk: a systematic review. Epidemiol. Rev. 2001;23:313–42.

    Article  CAS  PubMed  Google Scholar 

  32. Cook MB, Gamborg M, Aarestrup J, Sorensen TI, Baker JL. Childhood height and birth weight in relation to future prostate cancer risk: a cohort study based on the copenhagen school health records register. Cancer Epidemiol Biomark Prev. 2013;22:2232–40.

    Article  Google Scholar 

  33. Aarestrup J, Gamborg M, Cook MB, Baker JL. Childhood height increases the risk of prostate cancer mortality. Eur J Cancer. 2015;51:1340–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Bonilla C, Lewis SJ, Martin RM, Donovan JL, Hamdy FC, Neal DE, et al. Pubertal development and prostate cancer risk: Mendelian randomization study in a population-based cohort. BMC Med. 2016;14:66.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  35. Zuccolo L, Harris R, Gunnell D, Oliver S, Lane JA, Davis M, et al. Height and prostate cancer risk: a large nested case-control study (ProtecT) and meta-analysis. Cancer Epidemiol Biomark Prev. 2008;17:2325–36.

    Article  CAS  Google Scholar 

  36. Emerging Risk Factors, C. Adult height and the risk of cause-specific death and vascular morbidity in 1 million people: individual participant meta-analysis. Int J Epidemiol. 2012;41:1419–33.

    Article  Google Scholar 

  37. Lan T, Park Y, Colditz GA, Liu J, Wang M, Wu K, et al. Adolescent dairy product and calcium intake in relation to later prostate cancer risk and mortality in the NIH-AARP Diet and Health Study. Cancer Causes Control. 2020;31:891–904.

    Article  PubMed  PubMed Central  Google Scholar 

  38. McCullough ML, Giovannucci EL. Diet and cancer prevention. Oncogene. 2004;23:6349–64.

    Article  CAS  PubMed  Google Scholar 

  39. Bylsma LC, Alexander DD. A review and meta-analysis of prospective studies of red and processed meat, meat cooking methods, heme iron, heterocyclic amines and prostate cancer. Nutr J. 2015;14:125.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  40. Wu K, Spiegelman D, Hou T, Albanes D, Allen NE, Berndt SI, et al. Associations between unprocessed red and processed meat, poultry, seafood and egg intake and the risk of prostate cancer: a pooled analysis of 15 prospective cohort studies. Int J Cancer. 2016;138:2368–82.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Ruder EH, Thiébaut AC, Thompson FE, Potischman N, Subar AF, Park Y, et al. Adolescent and mid-life diet: risk of colorectal cancer in the NIH-AARP Diet and Health Study. Am J Clin Nutr. 2011;94:1607–19.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Gordon-Dseagu V, Thompson FE, Subar AF, Ruder EH, Thiébaut A, Potischman N, et al. A cohort study of adolescent and midlife diet and pancreatic cancer risk in the NIH-AARP Diet and Health Study. Am J Epidemiol. 2017;186:305–17.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Linos E, Willett WC, Cho E, Frazier L. Adolescent diet in relation to breast cancer risk among premenopausal women. Cancer Epidemiol Biomark Prev. 2010;19:689–96.

    Article  CAS  Google Scholar 

  44. Linos E, Willett WC, Cho E, Colditz G, Frazier LA. Red meat consumption during adolescence among premenopausal women and risk of breast cancer. Cancer Epidemiol Biomark Prev. 2008;17:2146–51.

    Article  Google Scholar 

  45. Chan JM, Gann PH, Giovannucci EL. Role of diet in prostate cancer development and progression. J Clin Oncol. 2005;23:8152–60.

    Article  CAS  PubMed  Google Scholar 

  46. Allen NE, Appleby PN, Davey GK, Key TJ. Hormones and diet: low insulin-like growth factor-I but normal bioavailable androgens in vegan men. Br J Cancer. 2000;83:95–97.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Barnard RJ, Ngo TH, Leung PS, Aronson WJ, Golding LA. A low-fat diet and/or strenuous exercise alters the IGF axis in vivo and reduces prostate tumor cell growth in vitro. Prostate. 2003;56:201–6.

    Article  PubMed  Google Scholar 

  48. Ngo TH, Barnard RJ, Cohen P, Freedland S, Tran C, deGregorio F, et al. Effect of isocaloric low-fat diet on human LAPC-4 prostate cancer xenografts in severe combined immunodeficient mice and the insulin-like growth factor axis. Clin Cancer Res. 2003;9:2734–43.

    CAS  PubMed  Google Scholar 

  49. Chen C, Chen Y, Zhang Y, Sun W, Jiang Y, Song Y, et al. Association between dietary patterns and precocious puberty in children: a population-based study. Int J Endocrinol. 2018;2018:4528704.

    PubMed  PubMed Central  Google Scholar 

  50. Gunther AL, Karaolis-Danckert N, Kroke A, Remer T, Buyken AE. Dietary protein intake throughout childhood is associated with the timing of puberty. J Nutr. 2010;140:565–71.

    Article  PubMed  CAS  Google Scholar 

  51. Hur J, Giovannucci E. Racial differences in prostate cancer: does timing of puberty play a role? Br J Cancer. 2020;123:349–54.

    Article  PubMed  PubMed Central  Google Scholar 

  52. Szymanski KM, Wheeler DC, Mucci LA. Fish consumption and prostate cancer risk: a review and meta-analysis. Am J Clin Nutr. 2010;92:1223–33.

    Article  CAS  PubMed  Google Scholar 

  53. Reese AC, Fradet V, Witte JS. Omega-3 fatty acids, genetic variants in COX-2 and prostate cancer. J Nutrigenetics Nutrigenomics. 2009;2:149–58.

    CAS  Google Scholar 

  54. Schatzkin A, Subar AF, Thompson FE, Harlan LC, Tangrea J, Hollenbeck AR, et al. Design and serendipity in establishing a large cohort with wide dietary intake distributions: the National Institutes of Health-American Association of Retired Persons Diet and Health Study. Am J Epidemiol. 2001;154:1119–25.

    Article  CAS  PubMed  Google Scholar 

  55. USDA. Food and nutrient intake of individuals in the US, Spring 1965. Washington, DC: US Dept of Agriculture; 1972.

  56. Michaud D, Midthune D, Hermansen S, Leitzmann M, Harlan L, Kipnis V, et al. Comparison of cancer registry case ascertainment with SEER estimates and self-reporting in a subset of the NIH-AARP Diet and Health Study. J Registry Manag. 2005;32:70–5.

  57. Rosenblatt KA, Wicklund KG, Stanford JL. Sexual factors and the risk of prostate cancer. Am J Epidemiol . 2001;153:1152–8.

    Article  CAS  PubMed  Google Scholar 

  58. Xu Y, Huang D, Wu Y, Ye D, Zhang N, Gao Y, et al. Family history is significantly associated with prostate cancer and its early onset in Chinese population. Prostate. 2019;79:1762–6.

    Article  CAS  PubMed  Google Scholar 

  59. Potosky AL, Miller BA, Albertsen PC, Kramer BS. The role of increasing detection in the rising incidence of prostate cancer. J Am Med Assoc. 1995;273:548–52.

    Article  CAS  Google Scholar 

  60. Maruti SS, Feskanich D, Colditz GA, Frazier AL, Sampson LA, Michels KB, et al. Adult recall of adolescent diet: reproducibility and comparison with maternal reporting. Am J Epidemiol. 2005;161:89–97.

    Article  PubMed  Google Scholar 

  61. Maruti SS, Feskanich D, Rockett HR, Colditz GA, Sampson LA, Willett WC. Validation of adolescent diet recalled by adults. Epidemiology. 2006;17:226–9.

    Article  PubMed  Google Scholar 

  62. Potischman N, Weiss HA, Swanson CA, Coates RJ, Gammon MD, Malone KE, et al. Diet during adolescence and risk of breast cancer among young women. J Natl Cancer Inst. 1998;90:226–33.

    Article  CAS  PubMed  Google Scholar 

  63. Dwyer JT, Gardner J, Halvorsen K, Krall EA, Cohen A, Valadian I. Memory of food intake in the distant past. Am J Epidemiol. 1989;130:1033–46.

    Article  CAS  PubMed  Google Scholar 

  64. Chavarro JE, Rosner BA, Sampson L, Willey C, Tocco P, Willett WC, et al. Validity of adolescent diet recall 48 years later. Am J Epidemiol. 2009;170:1563–70.

    Article  PubMed  PubMed Central  Google Scholar 

  65. Wolk A, Bergstrom R, Hansson LE, Nyren O. Reliability of retrospective information on diet 20 years ago and consistency of independent measurements of remote adolescent diet. Nutr Cancer. 1997;29:234–41.

    Article  CAS  PubMed  Google Scholar 

  66. Stiebeling H. Are we well fed?: a report on the diets of families in the United States. U.S. Department of Agriculture. Miscellaneous Publication Number 430. 1941;41–278.

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Acknowledgements

We thank Dr. Linda Liao for assistance with acquiring AARP Study data, and Dr. Stephanie Smith-Warner, Sherry Yaun and Tao Hou for assistance defining prostate cancer outcomes.

Author information

Authors and Affiliations

  1. Department of Occupational and Environmental Health, College of Public Health, The University of Iowa, Iowa City, IA, USA

    Tuo Lan

  2. Division of Public Health Sciences, Department of Surgery; and the Alvin J. Siteman Cancer Center, Washington University School of Medicine, St. Louis, MO, USA

    Yikyung Park, Graham A. Colditz, Jingxia Liu & Siobhan Sutcliffe

  3. Metabolic Epidemiology Branch, Division of Cancer Epidemiology and Genetics, National Cancer Institute, Department of Health and Human Services, Bethesda, MD, USA

    Rashmi Sinha

  4. Department of Biostatistics, Harvard T. H. Chan School of Public Health, Boston, MA, USA

    Molin Wang

  5. Department of Epidemiology, Harvard T. H. Chan School of Public Health, Boston, MA, USA

    Molin Wang & Edward Giovannucci

  6. Channing Division of Network Medicine, Department of Medicine, Harvard Medical School and Brigham and Women’s Hospital, Boston, MA, USA

    Molin Wang & Edward Giovannucci

  7. Department of Nutrition, Harvard T. H. Chan School of Public Health, Boston, MA, USA

    Kana Wu & Edward Giovannucci

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Contributions

YP and RS participated in the design of the parent study. TL, YP, GAC, MW, KW, EG and SS conceived the present study. TL, YP and SS participated in the analysis of the study. TL and SS drafted the paper, and take responsibility for the integrity of the data and the accuracy of the data analysis. All authors of this paper have critically reviewed the paper.

Corresponding author

Correspondence to Siobhan Sutcliffe.

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Funding information

This analysis was funded by the Barnes-Jewish Hospital Foundation, the Alvin J. Siteman Cancer Center and the Institute for Clinical and Translational Sciences.

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The authors declare no competing interests.

Ethics approval and consent to participate

This study was approved by the Special Studies Institutional Review Board of the National Cancer Institute. Consent from participants was obtained from investigators for the NIH-AARP Diet and Health Study at enrolment.

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Lan, T., Park, Y., Colditz, G.A. et al. Adolescent animal product intake in relation to later prostate cancer risk and mortality in the NIH-AARP Diet and Health Study. Br J Cancer 125, 1158–1167 (2021). https://doi.org/10.1038/s41416-021-01463-1

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