NOTICE: We are experiencing technical issues with Academy members trying to log into the JAND site using Academy member login credentials. We are working to resolve the issue as soon as possible. Alternatively, if you are an Academy member, you can access the JAND site by registering for an Elsevier account and claiming access using the links at the top of the JAND site. Email us at [email protected] for assistance. Thanks for your patience!

Association between Dietary Energy Density and Obesity-Associated Cancer: Results from the Women’s Health Initiative

Published:August 17, 2017DOI:https://doi.org/10.1016/j.jand.2017.06.010

      Abstract

      Background

      Dietary energy density (DED) is the ratio of energy (kilocalories or kilojoules) intake to food weight (grams) and is a measure of diet quality. Consumption of foods high in DED has been associated with weight gain in adults.

      Objective

      To investigate the association between baseline DED and incident obesity-associated cancers in the Women’s Health Initiative.

      Design

      Prospective cohort study of clinical trial and observational study participants.

      Participants/setting

      Postmenopausal women aged 50 to 79 years (N=92,295) enrolled in the observational study or the calcium and vitamin D trial and hormone replacement therapy trials of the Women’s Health Initiative.

      Main outcome measures

      Incident, medical record-adjudicated, obesity-related cancers during follow-up. Exposure variable was DED (kilocalories per gram for the total diet) from self-reported dietary intake at baseline using a food frequency questionnaire.

      Statistical analyses

      The associations between DED and each incident cancer, or any obesity-related cancer, were examined using competing-risks regression models, with death as a competing risk. Body mass index-stratified models were generated to investigate body mass index as a potential modifying factor.

      Results

      DED was associated with higher body mass index (28.9±6.0 vs 26.3±4.9) and waist circumference (89.3±14.2 vs 82.4±12.4 cm) for DED quintiles 5 vs 1, respectively. DED was associated with a 10% increased risk of any obesity-related cancer (subhazard ratioQ5 vs Q1: 1.1, 95% CI 1.03 to 1.2; P=0.004). This increased risk appeared limited to women who were normal weight at enrollment.

      Conclusions

      Higher DED may be a contributing factor for obesity-related cancers, especially among normal-weight postmenopausal women and, as such, could serve as a modifiable behavior for dietary interventions to reduce obesity-associated cancer risk.

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Journal of the Academy of Nutrition and Dietetics
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Beliveau R.
        • Gingras D.
        Role of nutrition in preventing cancer.
        Can Fam Physician. 2007; 53: 1905-1911
        • Key T.J.
        • Schatzkin A.
        • Willett W.C.
        • Allen N.E.
        • Spencer E.A.
        • Travis R.C.
        Diet, nutrition and the prevention of cancer.
        Public Health Nutr. 2004; 7: 187-200
        • Chan D.S.
        • Lau R.
        • Aune D.
        • et al.
        Red and processed meat and colorectal cancer incidence: Meta-analysis of prospective studies.
        PLoS One. 2011; 6: e20456
        • Rodriguez C.
        • McCullough M.L.
        • Mondul A.M.
        • et al.
        Meat consumption among Black and White men and risk of prostate cancer in the Cancer Prevention Study II Nutrition Cohort.
        Cancer Epidemiol Biomarkers Prev. 2006; 15: 211-216
        • Cross A.J.
        • Sinha R.
        Meat-related mutagens/carcinogens in the etiology of colorectal cancer.
        Environ Mol Mutagen. 2004; 44: 44-55
        • Anand P.
        • Kunnumakkara A.B.
        • Sundaram C.
        • et al.
        Cancer is a preventable disease that requires major lifestyle changes.
        Pharm Res. 2008; 25: 2097-2116
        • Ceschi M.
        • Gutzwiller F.
        • Moch H.
        • Eichholzer M.
        • Probst-Hensch N.M.
        Epidemiology and pathophysiology of obesity as cause of cancer.
        Swiss Med Wkly. 2007; 137: 50-56
        • Iyengar N.M.
        • Hudis C.A.
        • Dannenberg A.J.
        Obesity and cancer: Local and systemic mechanisms.
        Annu Rev Med. 2015; 66: 297-309
        • Carmichael A.R.
        Obesity as a risk factor for development and poor prognosis of breast cancer.
        BJOG. 2006; 113: 1160-1166
        • Schulze M.B.
        • Fung T.T.
        • Manson J.E.
        • Willett W.C.
        • Hu F.B.
        Dietary patterns and changes in body weight in women.
        Obesity (Silver Spring). 2006; 14: 1444-1453
        • Bes-Rastrollo M.
        • van Dam R.M.
        • Martinez-Gonzalez M.A.
        • Li T.Y.
        • Sampson L.L.
        • Hu F.B.
        Prospective study of dietary energy density and weight gain in women.
        Am J Clin Nutr. 2008; 88: 769-777
        • Romaguera D.
        • Angquist L.
        • Du H.
        • et al.
        Dietary determinants of changes in waist circumference adjusted for body mass index—A proxy measure of visceral adiposity.
        PLoS ONE. 2010; 5: e11588
        • Vergnaud A.C.
        • Estaquio C.
        • Czernichow S.
        • et al.
        Energy density and 6-year anthropometric changes in a middle-aged adult cohort.
        Br J Nutr. 2009; 102: 302-309
        • Ello-Martin J.A.
        • Roe L.S.
        • Ledikwe J.H.
        • Beach A.M.
        • Rolls B.J.
        Dietary energy density in the treatment of obesity: A year-long trial comparing 2 weight-loss diets.
        Am J Clin Nutr. 2007; 85: 1465-1477
        • Ledikwe J.H.
        • Blanck H.M.
        • Khan L.K.
        • et al.
        Dietary energy density determined by eight calculation methods in a nationally representative United States population.
        J Nutr. 2005; 135: 273-278
        • Savage J.S.
        • Marini M.
        • Birch L.L.
        Dietary energy density predicts women's weight change over 6 y.
        Am J Clin Nutr. 2008; 88: 677-684
        • Du H.
        • van der A.D.
        • Ginder V.
        • et al.
        Dietary energy density in relation to subsequent changes of weight and waist circumference in European men and women.
        PLoS One. 2009; 4: e5339
        • McCrory M.A.
        • Saltzman E.
        • Rolls B.J.
        • Roberts S.B.
        A twin study of the effects of energy density and palatability on energy intake of individual foods.
        Physiol Behav. 2006; 87: 451-459
        • Rolls B.J.
        • Drewnowski A.
        • Ledikwe J.H.
        Changing the energy density of the diet as a strategy for weight management.
        J Am Diet Assoc. 2005; 105: S98-S103
        • Neuhouser M.L.
        • Tinker L.
        • Shaw P.A.
        • et al.
        Use of recovery biomarkers to calibrate nutrient consumption self-reports in the Women's Health Initiative.
        Am J Epidemiol. 2008; 167: 1247-1259
        • Prentice R.L.
        • Shaw P.A.
        • Bingham S.A.
        • et al.
        Biomarker-calibrated energy and protein consumption and increased cancer risk among postmenopausal women.
        Am J Epidemiol. 2009; 169: 977-989
        • Devaraj S.
        • Wang-Polagruto J.
        • Polagruto J.
        • Keen C.L.
        • Jialal I.
        High-fat, energy-dense, fast-food-style breakfast results in an increase in oxidative stress in metabolic syndrome.
        Metabolism. 2008; 57: 867-870
        • Pereira M.A.
        • Kartashov A.I.
        • Ebbeling C.B.
        • et al.
        Fast-food habits, weight gain, and insulin resistance (the CARDIA study): 15-year prospective analysis.
        Lancet. 2005; 365: 36-42
        • Mendoza J.A.
        • Drewnowski A.
        • Christakis D.A.
        Dietary energy density is associated with obesity and the metabolic syndrome in U.S. adults.
        Diabetes Care. 2007; 30: 974-979
        • Wang J.
        • Zhang W.
        • Sun L.
        • et al.
        Dietary energy density is positively associated with risk of pancreatic cancer in urban Shanghai Chinese.
        J Nutr. 2013; 143: 1626-1629
      1. Design of the Women's Health Initiative clinical trial and observational study. The Women's Health Initiative Study Group.
        Control Clin Trials. 1998; 19: 61-109
      2. World Cancer Research Fund/American Institute for Cancer Research. Food, nutrition, physical activity, and the prevention of cancer: A global perspective. 2007. http://www.aicr.org/assets/docs/pdf/reports/Second_Expert_Report.pdf. Accessed June 6, 2017.

        • Patterson R.E.
        • Kristal A.R.
        • Tinker L.F.
        • Carter R.A.
        • Bolton M.P.
        • Agurs-Collins T.
        Measurement characteristics of the Women's Health Initiative food frequency questionnaire.
        Ann Epidemiol. 1999; 9: 178-187
        • Qi L.
        • Nassir R.
        • Kosoy R.
        • et al.
        Relationship between diabetes risk and admixture in postmenopausal African-American and Hispanic-American women.
        Diabetologia. 2012; 55: 1329-1337
        • Goris A.H.
        • Westerterp-Plantenga M.S.
        • Westerterp K.R.
        Undereating and underrecording of habitual food intake in obese men: Selective underreporting of fat intake.
        Am J Clin Nutr. 2000; 71: 130-134
        • Subar A.F.
        • Kipnis V.
        • Troiano R.P.
        • et al.
        Using intake biomarkers to evaluate the extent of dietary misreporting in a large sample of adults: The OPEN study.
        Am J Epidemiol. 2003; 158: 1-13
      3. StataCorp. 2015. Stata Statistical Software: Release 14. College Station, TX: StataCorp LP.

        • Tahergorabi Z.
        • Khazaei M.
        • Moodi M.
        • Chamani E.
        From obesity to cancer: A review on proposed mechanisms.
        Cell Biochem Funct. 2016; 34: 533-545
        • Donohoe C.L.
        • Lysaght J.
        • O'Sullivan J.
        • Reynolds J.V.
        Emerging concepts linking obesity with the hallmarks of cancer.
        Trends Endocrinol Metab. 2017; 28: 46-62
        • Perez-Escamilla R.
        • Obbagy J.E.
        • Altman J.M.
        • et al.
        Dietary energy density and body weight in adults and children: A systematic review.
        J Acad Nutr Diet. 2012; 112: 671-684
        • Harvie M.
        • Hooper L.
        • Howell A.H.
        Central obesity and breast cancer risk: A systematic review.
        Obes Rev. 2003; 4: 157-173
        • Kaaks R.
        • Lukanova A.
        • Kurzer M.S.
        Obesity, endogenous hormones, and endometrial cancer risk: A synthetic review.
        Cancer Epidemiol Biomarkers Prev. 2002; 11: 1531-1543
        • Rouhani M.H.
        • Haghighatdoost F.
        • Surkan P.J.
        • Azadbakht L.
        Associations between dietary energy density and obesity: A systematic review and meta-analysis of observational studies.
        Nutrition. 2016; 32: 1037-1047
        • Howarth N.C.
        • Murphy S.P.
        • Wilkens L.R.
        • Hankin J.H.
        • Kolonel L.N.
        Dietary energy density is associated with overweight status among 5 ethnic groups in the multiethnic cohort study.
        J Nutr. 2006; 136: 2243-2248
        • Wang J.
        • Luben R.
        • Khaw K.T.
        • Bingham S.
        • Wareham N.J.
        • Forouhi N.G.
        Dietary energy density predicts the risk of incident type 2 diabetes: The European Prospective Investigation of Cancer (EPIC)-Norfolk Study.
        Diabetes Care. 2008; 31: 2120-2125
        • Hingle M.D.
        • Wertheim B.C.
        • Neuhouser M.L.
        • et al.
        Association between dietary energy density and incident type 2 diabetes in the Women's Health Initiative.
        J Acad Nutr Diet. 2017; 117: 778-785.e771
        • Prentice R.L.
        • Pettinger M.
        • Tinker L.F.
        • et al.
        Regression calibration in nutritional epidemiology: Example of fat density and total energy in relationship to postmenopausal breast cancer.
        Am J Epidemiol. 2013; 178: 1663-1672
        • Jones J.A.
        • Hartman T.J.
        • Klifa C.S.
        • et al.
        Dietary energy density is positively associated with breast density among young women.
        J Acad Nutr Diet. 2015; 115: 353-359
        • Liang X.
        • Margolis K.L.
        • Hendryx M.
        • et al.
        Metabolic phenotype and risk of colorectal cancer in normal-weight postmenopausal women.
        Cancer Epidemiol Biomarkers Prev. 2017; 26: 155-161
        • Lim H.S.
        • Shin E.J.
        • Yeom J.W.
        • Park Y.H.
        • Kim S.K.
        Association between nutrient intake and metabolic syndrome in patients with colorectal cancer.
        Clin Nutr Res. 2017; 6: 38-46
        • Sun W.
        • Lu J.
        • Wu S.
        • et al.
        Association of insulin resistance with breast, ovarian, endometrial and cervical cancers in non-diabetic women.
        Am J Cancer Res. 2016; 6: 2334-2344
        • Nead K.T.
        • Sharp S.J.
        • Thompson D.J.
        • et al.
        Evidence of a causal association between insulinemia and endometrial cancer: A Mendelian randomization analysis [published online ahead of print July 1, 2015].
        J Natl Cancer Inst. 2015; 107https://doi.org/10.1093/jnci/djv178
        • Gadducci A.
        • Biglia N.
        • Tana R.
        • Cosio S.
        • Gallo M.
        Metformin use and gynecological cancers: A novel treatment option emerging from drug repositioning.
        Crit Rev Oncol Hematol. 2016; 105: 73-83
        • Heckman-Stoddard B.M.
        • Gandini S.
        • Puntoni M.
        • Dunn B.K.
        • DeCensi A.
        • Szabo E.
        Repurposing old drugs to chemoprevention: the case of metformin.
        Semin Oncol. 2016; 43: 123-133
        • Caan B.J.
        • Kroenke C.H.
        Next steps in understanding the obesity paradox in cancer.
        Cancer Epidemiol Biomarkers Prev. 2017; 26: 12
        • Strulov Shachar S.
        • Williams G.R.
        The obesity paradox in cancer—Moving beyond BMI.
        Cancer Epidemiol Biomarkers Prev. 2017; 26: 13-16
        • Basen-Engquist K.
        • Chang M.
        Obesity and cancer risk: Recent review and evidence.
        Curr Oncol Rep. 2011; 13: 71-76
        • Johnson L.
        • Wilks D.C.
        • Lindroos A.K.
        • Jebb S.A.
        Reflections from a systematic review of dietary energy density and weight gain: Is the inclusion of drinks valid?.
        Obes Rev. 2009; 10: 681-692
        • Horner N.K.
        • Patterson R.E.
        • Neuhouser M.L.
        • Lampe J.W.
        • Beresford S.A.
        • Prentice R.L.
        Participant characteristics associated with errors in self-reported energy intake from the Women's Health Initiative food-frequency questionnaire.
        Am J Clin Nutr. 2002; 76: 766-773

      Biography

      C. A. Thomson is a professor, Mel and Enid Zuckerman College of Public Health, The University of Arizona, Tucson.

      Biography

      T. E. Crane is an assistant professor, College of Nursing, The University of Arizona, Tucson.

      Biography

      D. O. Garcia is an assistant professor, Mel and Enid Zuckerman College of Public Health, The University of Arizona, Tucson.

      Biography

      B. C. Wertheim is a data analyst/statistician, University of Arizona Cancer Center, The University of Arizona, Tucson.

      Biography

      M. Hingle is an assistant professor, Department of Nutritional Sciences, College of Agriculture & Life Sciences, The University of Arizona, Tucson.

      Biography

      L. Snetselaar is a professor and associate provost, College of Public Health, The University of Iowa, Iowa City.

      Biography

      M. Datta is an assistant professor and director, Coordinated Program in Dietetics, Department of Nutrition Science, Purdue University, West Lafayette, IN.

      Biography

      T. Rohan is a professor, Department of Epidemiology and Population Health, Albert Einstein College of Medicine, Bronx, NY.

      Biography

      E. LeBlanc is an endocrinologist, Kaiser Permanente Center for Health Research, Portland, OR.

      Biography

      R. T. Chlebowski is chief and professor in residence, Medical Oncology/Hematology, Los Angeles Biomedical Research Institute at Harbor-UCLA Medical Center, Torrance, CA.

      Biography

      L. Qi is an associate professor, Department of Public Health Sciences, The University of California, Davis.