Age at natural menopause and risk of type 2 diabetes: a prospective cohort study

Diabetologia

Volumn 60, Issue 10, 2017, Pages 1951-1960

  Muka, Taulant ^a   Asllanaj, Eralda ^a   Avazverdi, Naim ^a   Jaspers, Loes ^a   Stringa, Najada ^a   Milic, Jelena ^a   Ligthart, Symen ^a   Ikram, M Arfan ^a   Laven, Joop S E ^a   Kavousi, Maryam ^a   Dehghan, Abbas ^a   Franco, Oscar H ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

Diabetes; Early menopause; Menopause; Type 2 diabetes; Women

Indexed keywords

ANDROSTENEDIONE; C REACTIVE PROTEIN; ESTRADIOL; GLUCOSE; INSULIN; PRASTERONE; PRASTERONE SULFATE; SEX HORMONE BINDING GLOBULIN; TESTOSTERONE; THYROTROPIN;

ADULT; AGE; AGED; ARTICLE; COHORT ANALYSIS; EARLY MENOPAUSE; FEMALE; HEREDITY; HUMAN; MAJOR CLINICAL STUDY; MEDICAL RECORD; MENOPAUSE; MIDDLE AGED; NON INSULIN DEPENDENT DIABETES MELLITUS; OBESITY; POPULATION; POSTMENOPAUSE; PRIORITY JOURNAL; PROSPECTIVE STUDY; RETROSPECTIVE STUDY; RISK FACTOR; INCIDENCE; RISK;

ADULT; AGE FACTORS; DIABETES MELLITUS, TYPE 2; FEMALE; HUMANS; INCIDENCE; MENOPAUSE; MIDDLE AGED; POSTMENOPAUSE; PROSPECTIVE STUDIES; RISK;

EID: 85024484779     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-017-4346-8     Document Type: Article

References (48)

1. Jaspers L, Daan NM, van Dijk GM et al (2015) Health in middle-aged and elderly women: a conceptual framework for healthy menopause. Maturitas 81:93–98
2. Gold EB (2011) The timing of the age at which natural menopause occurs. Obstet Gynecol Clin N Am 38:425–440
3. Ihara K, Fukano C, Ayabe T et al (2017) FUT2 non-secretor status is associated with type 1 diabetes susceptibility in Japanese children. Diabet Med 34:586–589
4. Canto JG, Iskandrian AE (2003) Major risk factors for cardiovascular disease: debunking the “only 50%” myth. JAMA 290:947–949
5. Malacara JM, Huerta R, Rivera B, Esparza S, Fajardo ME (1997) Menopause in normal and uncomplicated NIDDM women: physical and emotional symptoms and hormone profile. Maturitas 28:35–45
6. Di Donato P, Giulini NA, Bacchi Modena A et al (2005) Risk factors for type 2 diabetes in women attending menopause clinics in Italy: a cross-sectional study. Climacteric 8:287–293
7. Luborsky JL, Meyer P, Sowers MF, Gold EB, Santoro N (2003) Premature menopause in a multi-ethnic population study of the menopause transition. Hum Reprod 18:199–206
8. Brand JS, van der Schouw YT, Onland-Moret NC et al (2013) Age at menopause, reproductive life span, and type 2 diabetes risk: results from the EPIC-InterAct study. Diabetes Care 36:1012–1019
9. Gambacciani M, Ciaponi M, Cappagli B, De Simone L, Orlandi R, Genazzani AR (2001) Prospective evaluation of body weight and body fat distribution in early postmenopausal women with and without hormonal replacement therapy. Maturitas 39:125–132
10. Wu SI, Chou P, Tsai ST (2001) The impact of years since menopause on the development of impaired glucose tolerance. J Clin Epidemiol 54:117–120
11. Laven JS, Visser JA, Uitterlinden AG, Vermeij WP, Hoeijmakers JH (2016) Menopause: genome stability as new paradigm. Maturitas 92:15–23
12. Muka T, Nano J, Jaspers L et al (2017) Associations of steroid sex hormones and sex hormone-binding globulin with the risk of type 2 diabetes in women: a population-based cohort study and meta-analysis. Diabetes 66:577–586
13. Brahimaj A, Muka T, Kavousi M, Laven JS, Dehghan A, Franco OH (2017) Serum dehydroepiandrosterone levels are associated with lower risk of type 2 diabetes: the Rotterdam Study. Diabetologia 60:98–106
14. Chubak J, Tworoger SS, Yasui Y, Ulrich CM, Stanczyk FZ, McTiernan A (2004) Associations between reproductive and menstrual factors and postmenopausal sex hormone concentrations. Cancer Epidemiol Biomark Prev 13:1296–1301
15. Madigan MP, Troisi R, Potischman N, Dorgan JF, Brinton LA, Hoover RN (1998) Serum hormone levels in relation to reproductive and lifestyle factors in postmenopausal women (United States). Cancer Causes Control 9:199–207
16. Ness RB, Buhari A, Gutai J, Kuller LH (2000) Reproductive history in relation to plasma hormone levels in healthy post-menopausal women. Maturitas 35:149–157
17. Trichopoulos D, Brown J, Macmahon B (1987) Urine estrogens and breast-cancer risk-factors among postmenopausal women. Int J Cancer 40:721–725
18. Hofman A, Brusselle GG, Darwish Murad S et al (2015) The Rotterdam study: 2016 objectives and design update. Eur J Epidemiol 30:661–708
19. Leening MJ, Kavousi M, Heeringa J et al (2012) Methods of data collection and definitions of cardiac outcomes in the Rotterdam Study. Eur J Epidemiol 27:173–185
20. World Health Organization (2006) Definition and diagnosis of diabetes mellitus and intermediate hyperglycemia: report of a WHO/IDF consultation. World Health Organization, Geneva
21. Friedewald WT, Levy RI, Fredrickson DS (1972) Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem 18:499–502
22. Stel VS, Smit JH, Pluijm SM, Visser M, Deeg DJ, Lips P (2004) Comparison of the LASA physical activity questionnaire with a 7-day diary and pedometer. J Clin Epidemiol 57:252–258
23. Day FR, Ruth KS, Thompson DJ et al (2015) Large-scale genomic analyses link reproductive aging to hypothalamic signaling, breast cancer susceptibility and BRCA1-mediated DNA repair. Nat Genet 47:1294–1303
24. Sun L, Tan L, Yang F et al (2012) Meta-analysis suggests that smoking is associated with an increased risk of early natural menopause. Menopause 19:126–132
25. Gold EB, Bromberger J, Crawford S et al (2001) Factors associated with age at natural menopause in a multiethnic sample of midlife women. Am J Epidemiol 153:865–874
26. Rubin BD (1987) Multiple imputation for nonresponse in surveys. Wiley, New York
27. Godsland IF (2005) Oestrogens and insulin secretion. Diabetologia 48:2213–2220
28. Stubbins RE, Najjar K, Holcomb VB, Hong J, Nunez NP (2012) Oestrogen alters adipocyte biology and protects female mice from adipocyte inflammation and insulin resistance. Diabetes Obes Metab 14:58–66
29. Kanaya AM, Herrington D, Vittinghoff E et al (2003) Glycemic effects of postmenopausal hormone therapy: the Heart and Estrogen/progestin Replacement Study. A randomized, double-blind, placebo-controlled trial. Ann Intern Med 138:1–9
30. Margolis KL, Bonds DE, Rodabough RJ et al (2004) Effect of oestrogen plus progestin on the incidence of diabetes in postmenopausal women: results from the Women’s Health Initiative Hormone Trial. Diabetologia 47:1175–1187
31. Bonds DE, Lasser N, Qi L et al (2006) The effect of conjugated equine oestrogen on diabetes incidence: the Women’s Health Initiative randomised trial. Diabetologia 49:459–468
32. Ding EL, Song Y, Manson JE, Rifai N, Buring JE, Liu S (2007) Plasma sex steroid hormones and risk of developing type 2 diabetes in women: a prospective study. Diabetologia 50:2076–2084
33. Kalyani RR, Franco M, Dobs AS et al (2009) The association of endogenous sex hormones, adiposity, and insulin resistance with incident diabetes in postmenopausal women. J Clin Endocrinol Metab 94:4127–4135
34. Golden SH, Dobs AS, Vaidya D et al (2007) Endogenous sex hormones and glucose tolerance status in postmenopausal women. J Clin Endocrinol Metab 92:1289–1295
35. Goodman-Gruen D, Barrett-Connor E (2000) Sex differences in the association of endogenous sex hormone levels and glucose tolerance status in older men and women. Diabetes Care 23:912–918
36. Livingstone C, Collison M (2002) Sex steroids and insulin resistance. Clin Sci (Lond) 102:151–166
37. Lakshman R, Forouhi N, Luben R et al (2008) Association between age at menarche and risk of diabetes in adults: results from the EPIC-Norfolk cohort study. Diabetologia 51:781–786
38. He C, Zhang C, Hunter DJ et al (2010) Age at menarche and risk of type 2 diabetes: results from 2 large prospective cohort studies. Am J Epidemiol 171:334–344
39. Wang N, Kuang L, Han B et al (2016) Follicle-stimulating hormone associates with prediabetes and diabetes in postmenopausal women. Acta Diabetol 53:227–236
40. Rocca WA, Shuster LT, Grossardt BR et al (2009) Long-term effects of bilateral oophorectomy on brain aging: unanswered questions from the Mayo Clinic Cohort Study of Oophorectomy and Aging. Womens Health (Lond) 5:39–48
41. Taneri PE, Kiefte-de Jong JC, Bramer WM, Daan NM, Franco OH, Muka T (2016) Association of alcohol consumption with the onset of natural menopause: a systematic review and meta-analysis. Hum Reprod Update 22:516–528
42. Jackson SP, Bartek J (2009) The DNA-damage response in human biology and disease. Nature 461:1071–1078
43. Shimizu I, Yoshida Y, Suda M, Minamino T (2014) DNA damage response and metabolic disease. Cell Metab 20:967–977
44. Muka T, Nano J, Voortman T et al (2016) The role of global and regional DNA methylation and histone modifications in glycemic traits and type 2 diabetes: a systematic review. Nutr Metab Cardiovasc Dis 26:553–566
45. den Tonkelaar I (1997) Validity and reproducibility of self-reported age at menopause in women participating in the DOM-project. Maturitas 27:117–123
46. Braem MG, Voorhuis M, van der Schouw YT et al (2013) Interactions between genetic variants in AMH and AMHR2 may modify age at natural menopause. PLoS One 8:e59819
47. Hu FB, Grodstein F, Hennekens CH et al (1999) Age at natural menopause and risk of cardiovascular disease. Arch Intern Med 159:1061–1066
48. Brand JS, Onland-Moret NC, Eijkemans MJ et al (2015) Diabetes and onset of natural menopause: results from the European Prospective Investigation into Cancer and Nutrition. Hum Reprod 30:1491–1498