Nutr Res Pract.  2018 Oct;12(5):396-405. 10.4162/nrp.2018.12.5.396.

Egg consumption is associated with a lower risk of type 2 diabetes in middle-aged and older men

• Lee J
• Kim J

• KMID: 2446999
• DOI: http://doi.org/10.4162/nrp.2018.12.5.396

Abstract

BACKGROUND/OBJECTIVES
This prospective study examined gender-specific associations between egg intake and the risk of developing type 2 diabetes using data from a large-scale cohort study.
SUBJECTS/METHODS
A total of 7,002 Korean adults (40-69 years) without type 2 diabetes at baseline were analyzed. Dietary intake was evaluated by a food frequency questionnaire administered at baseline (2001-2002) and the second follow-up examination (2005-2006). Type 2 diabetes was diagnosed as a fasting glucose concentration ≥ 126 mg/dL or current use of glucose-lowering medications or insulin injection. Multivariate Cox proportional hazard models were used to calculate hazard ratios (HRs) with 95% confidence intervals (CIs) for incident type 2 diabetes according to egg consumption or cholesterol intake.
RESULTS
During a 14-year follow up period, 857 subjects developed type 2 diabetes. In men, frequent egg intake (2- < 4 servings/week) was associated with a 40% lower risk of developing type 2 diabetes than infrequent egg intake (0- < 1 serving/week) (HR = 0.60, 95% CI: 0.37-0.97), whereas no association between egg intake and incidence of type 2 diabetes was observed in women (HR = 0.61, 95% CI: 0.27-1.37). There was no association between cholesterol intake and risk of incident type 2 diabetes in either men or women.
CONCLUSIONS
Egg consumption was inversely related to the risk of incident type 2 diabetes in men, but not in women, suggesting gender differences in the relationship between diet and disease risk.

Keyword

Eggs; diabetes mellitus; cholesterol; gender

MeSH Terms

Adult
Cholesterol
Cohort Studies
Diabetes Mellitus
Diet
Eggs
Fasting
Female
Follow-Up Studies
Glucose
Humans
Incidence
Insulin
Male
Ovum*
Proportional Hazards Models
Prospective Studies
Cholesterol
Glucose
Insulin

Reference

1. Kretowski A, Ruperez FJ, Ciborowski M. Genomics and metabolomics in obesity and type 2 diabetes. J Diabetes Res. 2016; 2016:9415645.

2. Guariguata L, Whiting DR, Hambleton I, Beagley J, Linnenkamp U, Shaw JE. Global estimates of diabetes prevalence for 2013 and projections for 2035. Diabetes Res Clin Pract. 2014; 103:137–149.

3. Ha KH, Kim DJ. Trends in the diabetes epidemic in Korea. Endocrinol Metab. 2015; 30:142–146.

4. Djoussé L, Driver JA, Gaziano JM, Buring JE, Lee IM. Association between modifiable lifestyle factors and residual lifetime risk of diabetes. Nutr Metab Cardiovasc Dis. 2013; 23:17–22.

5. Adamopoulos PN, Papamichael CM, Zampelas A, Moulopoulos SD. Cholesterol and unsaturated fat diets influence lipid and glucose concentrations in rats. Comp Biochem Physiol B Biochem Mol Biol. 1996; 113:659–663.

6. Herron KL, McGrane MM, Waters D, Lofgren IE, Clark RM, Ordovas JM, Fernandez ML. The ABCG5 polymorphism contributes to individual responses to dietary cholesterol and carotenoids in eggs. J Nutr. 2006; 136:1161–1165.

7. Song WO, Kerver JM. Nutritional contribution of eggs to American diets. J Am Coll Nutr. 2000; 19:556S–562S.

8. Salmerón J, Hu FB, Manson JE, Stampfer MJ, Colditz GA, Rimm EB, Willett WC. Dietary fat intake and risk of type 2 diabetes in women. Am J Clin Nutr. 2001; 73:1019–1026.

9. Song Y, Manson JE, Buring JE, Liu S. A prospective study of red meat consumption and type 2 diabetes in middle-aged and elderly women: the women's health study. Diabetes Care. 2004; 27:2108–2115.

10. Virtanen JK, Mursu J, Tuomainen TP, Virtanen HE, Voutilainen S. Egg consumption and risk of incident type 2 diabetes in men: the Kuopio Ischaemic Heart Disease Risk Factor Study. Am J Clin Nutr. 2015; 101:1088–1096.

11. Djoussé L, Gaziano JM, Buring JE, Lee IM. Egg consumption and risk of type 2 diabetes in men and women. Diabetes Care. 2009; 32:295–300.

12. Montonen J, Järvinen R, Heliövaara M, Reunanen A, Aromaa A, Knekt P. Food consumption and the incidence of type II diabetes mellitus. Eur J Clin Nutr. 2005; 59:441–448.

13. Vang A, Singh PN, Lee JW, Haddad EH, Brinegar CH. Meats, processed meats, obesity, weight gain and occurrence of diabetes among adults: findings from Adventist Health Studies. Ann Nutr Metab. 2008; 52:96–104.

14. Djoussé L, Kamineni A, Nelson TL, Carnethon M, Mozaffarian D, Siscovick D, Mukamal KJ. Egg consumption and risk of type 2 diabetes in older adults. Am J Clin Nutr. 2010; 92:422–427.

15. Kurotani K, Nanri A, Goto A, Mizoue T, Noda M, Oba S, Sawada N, Tsugane S. Japan Public Health Center-based Prospective Study Group. Cholesterol and egg intakes and the risk of type 2 diabetes: the Japan Public Health Center-based Prospective Study. Br J Nutr. 2014; 112:1636–1643.

16. Wallin A, Forouhi NG, Wolk A, Larsson SC. Egg consumption and risk of type 2 diabetes: a prospective study and dose-response meta-analysis. Diabetologia. 2016; 59:1204–1213.

17. Kong A, Odoms-Young AM, Schiffer LA, Berbaum ML, Porter SJ, Blumstein L, Fitzgibbon ML. Racial/ethnic differences in dietary intake among WIC families prior to food package revisions. J Nutr Educ Behav. 2013; 45:39–46.

18. Torréns JI, Skurnick J, Davidow AL, Korenman SG, Santoro N, Soto-Greene M, Lasser N, Weiss G. Study of Women's Health Across the Nation (SWAN). Ethnic differences in insulin sensitivity and beta-cell function in premenopausal or early perimenopausal women without diabetes: the Study of Women's Health Across the Nation (SWAN). Diabetes Care. 2004; 27:354–361.

19. Finucane MM, Stevens GA, Cowan MJ, Danaei G, Lin JK, Paciorek CJ, Singh GM, Gutierrez HR, Lu Y, Bahalim AN, Farzadfar F, Riley LM, Ezzati M. Global Burden of Metabolic Risk Factors of Chronic Diseases Collaborating Group (Body Mass Index). National, regional, and global trends in body-mass index since 1980: systematic analysis of health examination surveys and epidemiological studies with 960 country-years and 9·1 million participants. Lancet. 2011; 377:557–567.

20. Tian X, Xu X, Zhang K, Wang H. Gender difference of metabolic syndrome and its association with dietary diversity at different ages. Oncotarget. 2017; 8:73568–73578.

21. Song S, Kim J, Kim J. Gender differences in the association between dietary pattern and the incidence of hypertension in middle-aged and older adults. Nutrients. 2018; 10:pii: E252.

22. Ahn Y, Kwon E, Shim JE, Park MK, Joo Y, Kimm K, Park C, Kim DH. Validation and reproducibility of food frequency questionnaire for Korean genome epidemiologic study. Eur J Clin Nutr. 2007; 61:1435–1441.

23. Kim D, Kim J. Dairy consumption is associated with a lower incidence of the metabolic syndrome in middle-aged and older Korean adults: the Korean Genome and Epidemiology Study (KoGES). Br J Nutr. 2017; 117:148–160.

24. The Korean Nutrition Society. Food composition table. Recommended Dietary Allowances for Koreans. 7th ed. Seoul: The Korean Nutrition Society;2000.

25. Alberti KG, Zimmet PZ. Definition, diagnosis and classification of diabetes mellitus and its complications. Part 1: diagnosis and classification of diabetes mellitus provisional report of a WHO consultation. Diabet Med. 1998; 15:539–553.

26. Ainsworth BE, Haskell WL, Whitt MC, Irwin ML, Swartz AM, Strath SJ, O'Brien WL, Bassett DR Jr, Schmitz KH, Emplaincourt PO, Jacobs DR Jr, Leon AS. Compendium of physical activities: an update of activity codes and MET intensities. Med Sci Sports Exerc. 2000; 32:Suppl. S498–S504.

27. Hu FB, Stampfer MJ, Rimm E, Ascherio A, Rosner BA, Spiegelman D, Willett WC. Dietary fat and coronary heart disease: a comparison of approaches for adjusting for total energy intake and modeling repeated dietary measurements. Am J Epidemiol. 1999; 149:531–540.

28. Hess KR. Graphical methods for assessing violations of the proportional hazards assumption in Cox regression. Stat Med. 1995; 14:1707–1723.

29. Schoenfeld D. Partial residuals for the proportional hazards regression model. Biometrika. 1982; 69:239–241.

30. Hernán MA, Hernández-Díaz S, Werler MM, Mitchell AA. Causal knowledge as a prerequisite for confounding evaluation: an application to birth defects epidemiology. Am J Epidemiol. 2002; 155:176–184.

31. Zazpe I, Beunza JJ, Bes-Rastrollo M, Basterra-Gortari FJ, Mari-Sanchis A, Martínez-González MA. SUN Project Investigators. Egg consumption and risk of type 2 diabetes in a Mediterranean cohort; the sun project. Nutr Hosp. 2013; 28:105–111.

32. Pan A, Sun Q, Bernstein AM, Schulze MB, Manson JE, Willett WC, Hu FB. Red meat consumption and risk of type 2 diabetes: 3 cohorts of US adults and an updated meta-analysis. Am J Clin Nutr. 2011; 94:1088–1096.

33. Kovacs-Nolan J, Phillips M, Mine Y. Advances in the value of eggs and egg components for human health. J Agric Food Chem. 2005; 53:8421–8431.

34. Kim JE, Leite JO, DeOgburn R, Smyth JA, Clark RM, Fernandez ML. A lutein-enriched diet prevents cholesterol accumulation and decreases oxidized LDL and inflammatory cytokines in the aorta of guinea pigs. J Nutr. 2011; 141:1458–1463.

35. Chung HY, Rasmussen HM, Johnson EJ. Lutein bioavailability is higher from lutein-enriched eggs than from supplements and spinach in men. J Nutr. 2004; 134:1887–1893.

36. Detopoulou P, Panagiotakos DB, Antonopoulou S, Pitsavos C, Stefanadis C. Dietary choline and betaine intakes in relation to concentrations of inflammatory markers in healthy adults: the ATTICA study. Am J Clin Nutr. 2008; 87:424–430.

37. Pearce KL, Clifton PM, Noakes M. Egg consumption as part of an energy-restricted high-protein diet improves blood lipid and blood glucose profiles in individuals with type 2 diabetes. Br J Nutr. 2011; 105:584–592.

38. Joyce KE, Biggs ML, Djoussé L, Ix JH, Kizer JR, Siscovick DS, Shores MM, Matsumoto AM, Mukamal KJ. Testosterone, dihydrotestosterone, sex hormone-binding globulin, and incident diabetes among older men: the cardiovascular health study. J Clin Endocrinol Metab. 2017; 102:33–39.

39. Stellato RK, Feldman HA, Hamdy O, Horton ES, McKinlay JB. Testosterone, sex hormone-binding globulin, and the development of type 2 diabetes in middle-aged men: prospective results from the Massachusetts male aging study. Diabetes Care. 2000; 23:490–494.

40. Vandenput L, Mellström D, Lorentzon M, Swanson C, Karlsson MK, Brandberg J, Lönn L, Orwoll E, Smith U, Labrie F, Ljunggren O, Tivesten A, Ohlsson C. Androgens and glucuronidated androgen metabolites are associated with metabolic risk factors in men. J Clin Endocrinol Metab. 2007; 92:4130–4137.

41. Fan W, Yanase T, Nomura M, Okabe T, Goto K, Sato T, Kawano H, Kato S, Nawata H. Androgen receptor null male mice develop late-onset obesity caused by decreased energy expenditure and lipolytic activity but show normal insulin sensitivity with high adiponectin secretion. Diabetes. 2005; 54:1000–1008.

42. Selvin E, Feinleib M, Zhang L, Rohrmann S, Rifai N, Nelson WG, Dobs A, Basaria S, Golden SH, Platz EA. Androgens and diabetes in men: results from the Third National Health and Nutrition Examination Survey (NHANES III). Diabetes Care. 2007; 30:234–238.

43. Hiza HA, Casavale KO, Guenther PM, Davis CA. Diet quality of Americans differs by age, sex, race/ethnicity, income, and education level. J Acad Nutr Diet. 2013; 113:297–306.

44. Vitale M, Masulli M, Cocozza S, Anichini R, Babini AC, Boemi M, Bonora E, Buzzetti R, Carpinteri R, Caselli C, Ceccarelli E, Cignarelli M, Citro G, Clemente G, Consoli A, Corsi L, De Gregorio A, Di Bartolo P, Di Cianni G, Fontana L, Garofolo M, Giorda CB, Giordano C, Grioni S, Iovine C, Longhitano S, Mancastroppa G, Mazzucchelli C, Montani V, Mori M, Perriello G, Rinaldi ME, Ruffo MC, Salvi L, Sartore G, Scaranna C, Tonutti L, Zamboni C, Zogheri A, Krogh V, Cappellini F, Signorini S, Riccardi G, Vaccaro O. TOSCA.IT Study Group. Sex differences in food choices, adherence to dietary recommendations and plasma lipid profile in type 2 diabetes-The TOSCA.IT study. Nutr Metab Cardiovasc Dis. 2016; 26:879–885.