Article | Published:

Higher baseline dietary fat and fatty acid intake is associated with increased risk of incident prostate cancer in the SABOR study

Prostate Cancer and Prostatic Diseases (2018) | Download Citation

Abstract

Background

To study the association of nutrient intake measured by baseline food frequency questionnaire and risk of subsequent prostate cancer (PCa) in the SABOR (San Antonio Biomarkers of Risk) cohort study.

Methods

After IRB approval, more than 1903 men enrolled in a prospective cohort from 2000 to 2010 as part of the SABOR clinical validation site for the National Cancer Institute Early Detection Research Network. Food and nutrient intakes were calculated using a Food Frequency Questionnaire. Cox proportional hazards modeling and covariate-balanced propensity scores were used to assess the associations between all nutrients and PCa.

Results

A total of 229 men were diagnosed with PCa by prostate biopsy. Among all nutrients, increased risk of PCa was associated with intake of dietary fat scaled by the total caloric intake, particularly saturated fatty acid (SFA) [HR 1.19; 95% CI, 1.07–1.32), P value < 0.001, False discovery rate (FDR) 0.047] and trans fatty acid (TFA) [HR per quintile 1.21; (95% CI) (1.08–1.35), P < 0.001, FDR 0.039]. There was an increased risk of PCa with increasing intake of monounsaturated fatty acid (MUFA) (HR per quintile 1.14; 95% CI 1.03–1.27, P = 0.01, FDR 0.15) and cholesterol [HR per quintile 1.13; 95% confidence interval (95% CI) (1.02–1.26), P-value 0.02, FDR 0.19].

Conclusion

After examining a large, population-based cohort for PCa diagnosis, we identified dietary total fat and certain fatty acids as associated with increased risk of PCa. We found no factors that were protective from PCa. Dietary modification of fatty acid intake may reduce risk of PCa.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

References

  1. 1.

    Bray F, Jemal A, Grey N, Ferlay J, Forman D. Global cancer transitions according to the Human Development Index (2008–2030): a population-based study. Lancet Oncol. 2012;13:790–801.

  2. 2.

    Center MM, Jemal A, Lortet-Tieulent J, Ward E, Ferlay J, Brawley O, et al. International variation in prostate cancer incidence and mortality rates. Eur Urol. 2012;61:1079–92.

  3. 3.

    Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 2015;136:E359–386.

  4. 4.

    Lichtenstein P, Holm NV, Verkasalo PK, Iliadou A, Kaprio J, Koskenvuo M, et al. Environmental and heritable factors in the causation of cancer—analyses of cohorts of twins from Sweden, Denmark, and Finland. N Engl J Med. 2000;343:78–85.

  5. 5.

    Rose DP, Boyar AP, Wynder EL. International comparisons of mortality rates for cancer of the breast, ovary, prostate, and colon, and per capita food consumption. Cancer. 1986;58:2363–71.

  6. 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.

  7. 7.

    Lopez Fontana CM, Recalde Rincon GM, Messina Lombino D, Uvilla Recupero AL, Perez Elizalde RF, Lopez Laur JD. Body mass index and diet affect prostate cancer development. Actas Urol Esp. 2009;33:741–6.

  8. 8.

    Wu K, Hu FB, Willett WC, Giovannucci E. Dietary patterns and risk of prostate cancer in U.S. men. Cancer Epidemiol Biomark Prev. 2006;15:167–71.

  9. 9.

    Kristal AR, Arnold KB, Neuhouser ML, Goodman P, Platz EA, Albanes D, et al. Diet, supplement use, and prostate cancer risk: results from the prostate cancer prevention trial. Am J Epidemiol. 2010;172:566–77.

  10. 10.

    Priolo C, Pyne S, Rose J, Regan ER, Zadra G, Photopoulos C, et al. AKT1 and MYC induce distinctive metabolic fingerprints in human prostate cancer. Cancer Res. 2014;74:7198–204.

  11. 11.

    Ankerst DP, Hoefler J, Bock S, Goodman PJ, Vickers A, Hernandez J, et al. Prostate cancer prevention trial risk calculator 2.0 for the prediction of low-vs high-grade prostate cancer. Urology. 2014;83:1362–8.

  12. 12.

    Cui X, Churchill GA. Statistical tests for differential expression in cDNA microarray experiments. Genome Biol. 2003;4:210.

  13. 13.

    Imai K, Ratkovic M. Covariate balancing propensity score. J R Stat Soc Ser B. 2014;76:243–63.

  14. 14.

    Ohwaki K, Endo F, Kachi Y, Hattori K, Muraishi O, Nishikitani M, et al. Relationship between dietary factors and prostate-specific antigen in healthy men. Urol Int. 2012;89:270–4.

  15. 15.

    Eckel RH, Jakicic JM, Ard JD, de Jesus JM, Houston Miller N, Hubbard VS, et al. 2013 AHA/ACC guideline on lifestyle management to reduce cardiovascular risk: a report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines. J Am Coll Cardiol. 2014;63(25 Pt B):2960–84.

  16. 16.

    Bassett JK, Severi G, Hodge AM, MacInnis RJ, Gibson RA, Hopper JL, et al. Plasma phospholipid fatty acids, dietary fatty acids and prostate cancer risk. Int J Cancer. 2013;133:1882–91.

  17. 17.

    Strom SS, Yamamura Y, Forman MR, Pettaway CA, Barrera SL, DiGiovanni J. Saturated fat intake predicts biochemical failure after prostatectomy. Int J Cancer. 2008;122:2581–5.

  18. 18.

    Kurahashi N, Inoue M, Iwasaki M, Sasazuki S, Tsugane AS, Japan Public Health Center-Based Prospective Study G. Dairy product, saturated fatty acid, and calcium intake and prostate cancer in a prospective cohort of Japanese men. Cancer Epidemiol Biomark Prev. 2008;17:930–7.

  19. 19.

    Klein EA, Thompson IM Jr., Tangen CM, Crowley JJ, Lucia MS, Goodman PJ, et al. Vitamin E and the risk of prostate cancer: the Selenium and Vitamin E Cancer Prevention Trial (SELECT). JAMA. 2011;306:1549–56.

  20. 20.

    Di Sebastiano KM, Mourtzakis M. The role of dietary fat throughout the prostate cancer trajectory. Nutrients. 2014;6:6095–109.

  21. 21.

    Pelser C, Mondul AM, Hollenbeck AR, Park Y. Dietary fat, fatty acids, and risk of prostate cancer in the NIH-AARP diet and health study. Cancer Epidemiol Biomark Prev. 2013;22:697–707.

  22. 22.

    Nishida C1, Uauy R, Kumanyika S, Shetty P., The joint WHO/FAO expert consultation on diet, nutrition and the prevention of chronic diseases: process, product and policy implications. Public Health Nutr. 2004 Feb;7(1A):245-50.

  23. 23.

    Zhang J, Dhakal IB, Zhao Z, Li L. Trends in mortality from cancers of the breast, colon, prostate, esophagus, and stomach in East Asia: role of nutrition transition. Eur J Cancer Prev. 2012;21:480–9.

  24. 24.

    Crowe FL, Allen NE, Appleby PN, Overvad K, Aardestrup IV, Johnsen NF, et al. Fatty acid composition of plasma phospholipids and risk of prostate cancer in a case-control analysis nested within the European Prospective Investigation into Cancer and Nutrition. Am J Clin Nutr. 2008;88:1353–63.

  25. 25.

    Ma RW, Chapman K. A systematic review of the effect of diet in prostate cancer prevention and treatment. J Hum Nutr Diet. 2009;22:187–99. quiz200-182

  26. 26.

    Michaud DS, Augustsson K, Rimm EB, Stampfer MJ, Willet WC, Giovannucci E. A prospective study on intake of animal products and risk of prostate cancer. Cancer Causes Control. 2001;12:557–67.

  27. 27.

    Crowe FL, Key TJ, Appleby PN, Travis RC, Overvad K, Jakobsen MU, et al. Dietary fat intake and risk of prostate cancer in the European Prospective Investigation into Cancer and Nutrition. Am J Clin Nutr. 2008;87:1405–13.

  28. 28.

    Dennis LK, Snetselaar LG, Smith BJ, Stewart RE, Robbins ME. Problems with the assessment of dietary fat in prostate cancer studies. Am J Epidemiol. 2004;160:436–44.

  29. 29.

    Neuhouser ML, Barnett MJ, Kristal AR, Ambrosone CB, King I, Thornquist M, et al. n-6) PUFA increase and dairy foods decrease prostate cancer risk in heavy smokers. J Nutr. 2007;137:1821–7.

  30. 30.

    Smith BK, Robinson LE, Nam R, Ma DW. Trans-fatty acids and cancer: a mini-review. Br J Nutr. 2009;102:1254–66.

  31. 31.

    Kishino S, Takeuchi M, Park SB, Hirata A, Kitamura N, Kunisawa J, et al. Polyunsaturated fatty acid saturation by gut lactic acid bacteria affecting host lipid composition. Proc Natl Acad Sci USA. 2013;110:17808–13.

  32. 32.

    Wang DD, Li Y, Chiuve SE, Stampfer MJ, Manson JE, Rimm EB, et al. Association of specific dietary fats with total and cause-specific mortality. JAMA Intern Med. 2016;176:1134–45.

  33. 33.

    Haytowitz DB, Pehrsson PR. USDA's National Food and Nutrient Analysis Program (NFNAP) produces high-quality data for USDA food composition databases: Two decades of collaboration. Food Chem. 2018 Jan 1;238:134-138. https://doi.org/10.1016/j.foodchem.2016.11.082. Epub 2016 Nov 19.

  34. 34.

    Gao X, LaValley MP, Tucker KL. Prospective studies of dairy product and calcium intakes and prostate cancer risk: a meta-analysis. J Natl Cancer Inst. 2005;97:1768–77.

  35. 35.

    Yang M, Kenfield SA, Van Blarigan EL, Wilson KM, Batista JL, Sesso HD, et al. Dairy intake after prostate cancer diagnosis in relation to disease-specific and total mortality. Int J Cancer. 2015;137:2462–9.

  36. 36.

    Bidoli E, Talamini R, Bosetti C, Negri E, Maruzzi D, Montella M, et al. Macronutrients, fatty acids, cholesterol and prostate cancer risk. Ann Oncol. 2005;16:152–7.

  37. 37.

    Lopez-Miranda J, Perez-Jimenez F, Ros E, De Caterina R, Badimon L, Covas MI, et al. Olive oil and health: summary of the II international conference on olive oil and health consensus report, Jaen and Cordoba (Spain) 2008. Nutr Metab Cardiovasc Dis. 2010;20:284–94.

  38. 38.

    Park SY, Wilkens LR, Henning SM, Le Marchand L, Gao K, Goodman MT, et al. Circulating fatty acids and prostate cancer risk in a nested case-control study: the Multiethnic Cohort. Cancer Causes Control. 2009;20:211–23.

  39. 39.

    Chavarro JE, Kenfield SA, Stampfer MJ, Loda M, Campos H, Sesso HD, et al. Blood levels of saturated and monounsaturated fatty acids as markers of de novo lipogenesis and risk of prostate cancer. Am J Epidemiol. 2013;178:1246–55.

  40. 40.

    Agalliu I, Kirsh VA, Kreiger N, Soskolne CL, Rohan TE. Oxidative balance score and risk of prostate cancer: results from a case-cohort study. Cancer Epidemiol. 2011;35:353–61.

  41. 41.

    Khandrika L, Kumar B, Koul S, Maroni P, Koul HK. Oxidative stress in prostate cancer. Cancer Lett. 2009;282:125–36.

  42. 42.

    Heymach JV, Shackleford TJ, Tran HT, Yoo SY, Do KA, Wergin M, et al. Effect of low-fat diets on plasma levels of NF-kappaB-regulated inflammatory cytokines and angiogenic factors in men with prostate cancer. Cancer Prev Res. 2011;4:1590–8.

  43. 43.

    Shankar E, Vykhovanets EV, Vykhovanets OV, Maclennan GT, Singh R, Bhaskaran N, et al. High-fat diet activates pro-inflammatory response in the prostate through association of Stat-3 and NF-kappaB. Prostate. 2012;72:233–43.

  44. 44.

    Bishop GA, McMillan MS, Haughton G, Frelinger JA. Signaling to a B-cell clone by Ek, but not Ak, does not reflect alteration of Ak genes. Immunogenetics. 1988;28:184–92.

  45. 45.

    Ho PJ, Baxter RC. Insulin-like growth factor-binding protein-2 in patients with prostate carcinoma and benign prostatic hyperplasia. Clin Endocrinol. 1997;46:333–42.

  46. 46.

    Ngo TH, Barnard RJ, Leung PS, Cohen P, Aronson WJ. Insulin-like growth factor I (IGF-I) and IGF binding protein-1 modulate prostate cancer cell growth and apoptosis: possible mediators for the effects of diet and exercise on cancer cell survival. Endocrinology. 2003;144:2319–24.

  47. 47.

    Huang M, Koizumi A, Narita S, Inoue T, Tsuchiya N, Nakanishi H, et al. Diet-induced alteration of fatty acid synthase in prostate cancer progression. Oncogenesis. 2016;5:e195.

  48. 48.

    Benesh EC, Humphrey PA, Wang Q, Moley KH. Maternal high-fat diet induces hyperproliferation and alters Pten/Akt signaling in prostates of offspring. Sci Rep. 2013;3:3466.

  49. 49.

    Furriel A, Campos-Silva P, Silva PC, Costa WS, Sampaio FJ, Gregorio BM. Diets rich in saturated and polyunsaturated fatty acids induce morphological alterations in the rat ventral prostate. PLoS ONE. 2014;9:e102876.

  50. 50.

    Bancroft EK, Page EC, Castro E, Lilja H, Vickers A, Sjoberg D, et al. Targeted prostate cancer screening in BRCA1 and BRCA2 mutation carriers: results from the initial screening round of the IMPACT study. Eur Urol. 2014;66:489–99.

  51. 51.

    Parsons JK, Pierce JP, Mohler J, Paskett E, Jung SH, Morris MJ, et al. Men’s Eating and Living (MEAL) study (CALGB 70807 [Alliance]): recruitment feasibility and baseline demographics of a randomized trial of diet in men on active surveillance for prostate cancer. BJU Int. 2018;121:534–9.

  52. 52.

    Freedman LS, Schatzkin A, Midthune D, Kipnis V. Dealing with dietary measurement error in nutritional cohort studies. J Natl Cancer Inst. 2011;103:1086–92.

  53. 53.

    Subar AF, Freedman LS, Tooze JA, Kirkpatrick SI, Boushey C, Neuhouser ML, et al. Addressing current criticism regarding the value of self-report dietary data. J Nutr. 2015;145:2639–45.

Download references

Acknowledgements

This work was sponsored in part by grants from the National Institute of Health: U01 CA86402, and P30 CA0541474. JG was also supported by NIH grant GM07033. This work was also supported by the Office of the Assistant Secretary of Defense for Health Affairs through the Prostate Cancer Research Program under Award No. W81XWH-15-1-0441. Opinions, interpretations, conclusions and recommendations are those of the author and are not necessarily endorsed by the Department of Defense. Nutrition assessment shared resource at Fred Hutch utilized funds from NIH/NCI award number P30 CA015704.

Author information

Affiliations

  1. Department of Urology, University of Texas Health San Antonio, San Antonio, TX, USA

    • Michael A. Liss
    • , Osamah Al-Bayati
    • , Denise O’Keefe
    • , Dean Bacich
    • , Brandi Weaver
    •  & Robin Leach
  2. Division of Pharmacology and Toxicology, College of Pharmacy, The University of Texas, Austin, TX, USA

    • Michael A. Liss
    •  & John DiGiovanni
  3. Department of Epidemiology and Biostatistics, University of Texas Health San Antonio, San Antonio, TX, USA

    • Jonathan Gelfond
    •  & Martin Goros
  4. Department of Kinesiology, Health, and Nutrition, University of Texas Health San Antonio, San Antonio, TX, USA

    • Sarah Ullevig
  5. Department of Urology, University of Kansas, Kansas City, KS, USA

    • Jill Hamilton-Reeves
  6. Cell and Structural biology, University of Texas Health San Antonio, San Antonio, TX, USA

    • Robin Leach
  7. CHRISTUS Health, CHRISTUS Santa Rosa Medical Center, San Antonio, TX, USA

    • Ian M. Thompson

Authors

  1. Search for Michael A. Liss in:

  2. Search for Osamah Al-Bayati in:

  3. Search for Jonathan Gelfond in:

  4. Search for Martin Goros in:

  5. Search for Sarah Ullevig in:

  6. Search for John DiGiovanni in:

  7. Search for Jill Hamilton-Reeves in:

  8. Search for Denise O’Keefe in:

  9. Search for Dean Bacich in:

  10. Search for Brandi Weaver in:

  11. Search for Robin Leach in:

  12. Search for Ian M. Thompson in:

Conflict of interest

The authors declare that they have no conflict of interest.

Corresponding author

Correspondence to Michael A. Liss.

Electronic supplementary material

About this article

Publication history

Received

Revised

Accepted

Published

DOI

https://doi.org/10.1038/s41391-018-0105-2