Diet and BMI Correlate with Metabolite Patterns Associated with Aggressive Prostate Cancer

Three metabolite patterns have previously shown prospective inverse associations with the risk of aggressive prostate cancer within the European Prospective Investigation into Cancer and Nutrition (EPIC). Here, we investigated dietary and lifestyle correlates of these three prostate cancer-related metabolite patterns, which included: 64 phosphatidylcholines and three hydroxysphingomyelins (Pattern 1), acylcarnitines C18:1 and C18:2, glutamate, ornithine, and taurine (Pattern 2), and 8 lysophosphatidylcholines (Pattern 3). In a two-stage cross-sectional discovery (n = 2524) and validation (n = 518) design containing 3042 men free of cancer in EPIC, we estimated the associations of 24 dietary and lifestyle variables with each pattern and the contributing individual metabolites. Associations statistically significant after both correction for multiple testing (False Discovery Rate = 0.05) in the discovery set and at p < 0.05 in the validation set were considered robust. Intakes of alcohol, total fish products, and its subsets total fish and lean fish were positively associated with Pattern 1. Body mass index (BMI) was positively associated with Pattern 2, which appeared to be driven by a strong positive BMI-glutamate association. Finally, both BMI and fatty fish were inversely associated with Pattern 3. In conclusion, these results indicate associations of fish and its subtypes, alcohol, and BMI with metabolite patterns that are inversely associated with risk of aggressive prostate cancer.

[1]  J. Boer,et al.  Lifestyle correlates of eight breast cancer-related metabolites: a cross-sectional study within the EPIC cohort , 2021, BMC Medicine.

[2]  M. Waldenberger,et al.  The blood metabolome of incident kidney cancer: A case–control study nested within the MetKid consortium , 2021, PLoS medicine.

[3]  M. Schulze,et al.  A New Pipeline for the Normalization and Pooling of Metabolomics Data , 2021, bioRxiv.

[4]  M. Schulze,et al.  Metabolic signatures of greater body size and their associations with risk of colorectal and endometrial cancers in the European Prospective Investigation into Cancer and Nutrition , 2021, BMC Medicine.

[5]  E. Weiderpass,et al.  Comparing Calculated Nutrient Intakes Using Different Food Composition Databases: Results from the European Prospective Investigation into Cancer and Nutrition (EPIC) Cohort , 2020, Nutrients.

[6]  G. Hallmans,et al.  Identification of metabolites associated with prostate cancer risk: a nested case-control study with long follow-up in the Northern Sweden Health and Disease Study , 2020, BMC Medicine.

[7]  E. Riboli,et al.  Patterns in metabolite profile are associated with risk of more aggressive prostate cancer: A prospective study of 3,057 matched case–control sets from EPIC , 2019, International journal of cancer.

[8]  N. Nonomura,et al.  Obesity, Inflammation, and Prostate Cancer , 2019, Journal of clinical medicine.

[9]  G. Giles,et al.  Metabolomics and risk of kidney cancer , 2018 .

[10]  L. Hodson,et al.  Effect of supplementation with flaxseed oil and different doses of fish oil for 2 weeks on plasma phosphatidylcholine fatty acids in young women , 2018, European Journal of Clinical Nutrition.

[11]  E. Riboli,et al.  Consumption of fruits, vegetables and fruit juices and differentiated thyroid carcinoma risk in the European Prospective Investigation into Cancer and Nutrition (EPIC) study , 2018, International journal of cancer.

[12]  P. Vineis,et al.  Blood Metabolic Signatures of Body Mass Index: A Targeted Metabolomics Study in the EPIC Cohort. , 2017, Journal of proteome research.

[13]  E. Riboli,et al.  Consumption of Fish Is Not Associated with Risk of Differentiated Thyroid Carcinoma in the European Prospective Investigation into Cancer and Nutrition (EPIC) Study. , 2017, The Journal of nutrition.

[14]  D. Albanes,et al.  Prospective serum metabolomic profile of prostate cancer by size and extent of primary tumor , 2017, Oncotarget.

[15]  Jerzy Adamski,et al.  Interlaboratory Reproducibility of a Targeted Metabolomics Platform for Analysis of Human Serum and Plasma. , 2017, Analytical chemistry.

[16]  Treelet transform with Stata , 2017 .

[17]  D. Rujescu,et al.  Cardiovascular Risk Factors Associated With Blood Metabolite Concentrations and Their Alterations During a 4-Year Period in a Population-Based Cohort , 2016, Circulation. Cardiovascular genetics.

[18]  T. Spector,et al.  Characterizing Blood Metabolomics Profiles Associated with Self-Reported Food Intakes in Female Twins , 2016, PloS one.

[19]  E. Giovannucci,et al.  Body size across the life course and prostate cancer in the Health Professionals Follow‐up Study , 2016, International journal of cancer.

[20]  P. Vineis,et al.  Alteration of amino acid and biogenic amine metabolism in hepatobiliary cancers: Findings from a prospective cohort study , 2016, International journal of cancer.

[21]  F. Clavel-Chapelon,et al.  Metabolomic profiles of hepatocellular carcinoma in a European prospective cohort , 2015, BMC Medicine.

[22]  D. Wishart,et al.  The food metabolome: a window over dietary exposure. , 2014, The American journal of clinical nutrition.

[23]  S. Mousa,et al.  The effects of aspirin and fish oil consumption on lysophosphatidylcholines and lysophosphatidic acids and their correlates with platelet aggregation in adults with diabetes mellitus. , 2014, Prostaglandins, leukotrienes, and essential fatty acids.

[24]  M. Schulze,et al.  Variation of serum metabolites related to habitual diet: a targeted metabolomic approach in EPIC-Potsdam , 2013, European Journal of Clinical Nutrition.

[25]  F. Clavel-Chapelon,et al.  Consumption of Dairy Products and Colorectal Cancer in the European Prospective Investigation into Cancer and Nutrition (EPIC) , 2013, PloS one.

[26]  T. Spector,et al.  Alcohol-induced metabolomic differences in humans , 2013, Translational Psychiatry.

[27]  Susan Cheng,et al.  Metabolite Profiling Identifies Pathways Associated With Metabolic Risk in Humans , 2012, Circulation.

[28]  Anders Gorst-Rasmussen,et al.  tt: Treelet Transform with Stata , 2012 .

[29]  Xue Chuan Alcohol and prostate cancer in the NHANES I:An epidemiologic follow-up study , 2012 .

[30]  Claus Dethlefsen,et al.  Exploring dietary patterns by using the treelet transform. , 2011, American journal of epidemiology.

[31]  Yin Cao,et al.  Body Mass Index, Prostate Cancer–Specific Mortality, and Biochemical Recurrence: a Systematic Review and Meta-analysis , 2011, Cancer Prevention Research.

[32]  F. Clavel-Chapelon,et al.  Meat, eggs, dairy products, and risk of breast cancer in the European Prospective Investigation into Cancer and Nutrition (EPIC) cohort. , 2009, The American journal of clinical nutrition.

[33]  Oliver Fiehn,et al.  Mass-spectrometry-based metabolomics: limitations and recommendations for future progress with particular focus on nutrition research , 2009, Metabolomics.

[34]  E. Riboli,et al.  Alcohol consumption and the risk for prostate cancer in the European Prospective Investigation into Cancer and Nutrition. , 2008, Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology.

[35]  A. Kristal,et al.  Anthropometrics and prostate cancer risk. , 2007, American journal of epidemiology.

[36]  Carmen Rodriguez,et al.  Body Mass Index, Weight Change, and Risk of Prostate Cancer in the Cancer Prevention Study II Nutrition Cohort , 2007, Cancer Epidemiology Biomarkers & Prevention.

[37]  D. Albanes,et al.  Dietary factors of one-carbon metabolism and prostate cancer risk. , 2006, The American journal of clinical nutrition.

[38]  D. English,et al.  Alcohol consumption and prostate cancer risk: Results from the Melbourne collaborative cohort study , 2006, International journal of cancer.

[39]  A. Kristal,et al.  Alcohol Use and the Risk of Prostate Cancer: Results From the VITAL Cohort Study , 2006, Nutrition and cancer.

[40]  A. Roddam,et al.  A prospective study of diet and prostate cancer in Japanese men , 2004, Cancer Causes & Control.

[41]  Edward Giovannucci,et al.  Alcohol intake, drinking patterns, and risk of prostate cancer in a large prospective cohort study. , 2004, American journal of epidemiology.

[42]  L. Vatten,et al.  Anthropometry and prostate cancer risk: a prospective study of 22,248 Norwegian men , 1999, Cancer Causes & Control.

[43]  R. Goldbohm,et al.  A prospective cohort study on consumption of alcoholic beverages in relation to prostate cancer incidence (The Netherlands) , 2004, Cancer Causes & Control.

[44]  Jo Mitchell,et al.  Validity and repeatability of a simple index derived from the short physical activity questionnaire used in the European Prospective Investigation into Cancer and Nutrition (EPIC) study , 2003, Public Health Nutrition.

[45]  E. Rimm,et al.  A prospective study of intake of fish and marine fatty acids and prostate cancer. , 2003, Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology.

[46]  N E Day,et al.  European Prospective Investigation into Cancer and Nutrition (EPIC): study populations and data collection , 2002, Public Health Nutrition.

[47]  A. Miller,et al.  Consumption of added fats and oils in the European Prospective Investigation into Cancer and Nutrition (EPIC) centres across 10 European countries as assessed by 24-hour dietary recalls , 2002, Public Health Nutrition.

[48]  R. Paffenbarger,et al.  Alcohol consumption and risk of prostate cancer: The Harvard Alumni Health Study. , 2001, International journal of epidemiology.

[49]  A. Wolk,et al.  Fatty fish consumption and risk of prostate cancer , 2001, The Lancet.

[50]  R. Goldbohm,et al.  Animal products, calcium and protein and prostate cancer risk in the Netherlands Cohort Study , 1999, British Journal of Cancer.

[51]  P. Pietinen,et al.  European Prospective Investigation into Cancer and Nutrition: validity studies on dietary assessment methods. , 1997, International journal of epidemiology.

[52]  H. Grönberg,et al.  Total food consumption and body mass index in relation to prostate cancer risk: a case-control study in Sweden with prospectively collected exposure data. , 1996, The Journal of urology.

[53]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[54]  L. Kolonel,et al.  Animal Fat Consumption and Prostate Cancer: A Prospective Study in Hawaii , 1994, Epidemiology.

[55]  S. Wacholder,et al.  Diet, tobacco use, and fatal prostate cancer: results from the Lutheran Brotherhood Cohort Study. , 1990, Cancer research.

[56]  W. L. Beeson,et al.  Cohort study of diet, lifestyle, and prostate cancer in adventist men , 1989, Cancer.

[57]  R. Severson,et al.  A prospective study of demographics, diet, and prostate cancer among men of Japanese ancestry in Hawaii. , 1989, Cancer research.