Diabetes and Menopause

Current Diabetes Reports

Volumn 16, Issue 4, 2016, Pages 1-8

  Karvonen Gutierrez, Carrie A ^a   Park, Sung Kyun ^a   Kim, Catherine ^b  

^a UNIVERSITY OF MICHIGAN SCHOOL OF PUBLIC HEALTH   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Diabetes; Estrogen therapy; Menarche; Menopause; Women

Indexed keywords

CONJUGATED ESTROGEN PLUS MEDROXYPROGESTERONE ACETATE; ESTRADIOL; ESTROGEN; GLUCOSE; PLACEBO; SEX HORMONE;

BODY COMPOSITION; CLIMACTERIUM; DIABETES MELLITUS; DISEASE ASSOCIATION; DISEASE PREDISPOSITION; DRUG EFFICACY; DRUG SAFETY; ESTROGEN THERAPY; GLUCOSE METABOLISM; HIGH RISK POPULATION; HUMAN; INSULIN DEPENDENT DIABETES MELLITUS; LIVER METABOLISM; MATERNAL AGE; MENARCHE; MENOPAUSAL SYNDROME; MENOPAUSE; META ANALYSIS (TOPIC); METABOLIC PARAMETERS; NON INSULIN DEPENDENT DIABETES MELLITUS; OVARIECTOMY; OVARY INSUFFICIENCY; PATHOPHYSIOLOGY; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; RISK BENEFIT ANALYSIS; ANIMAL; FEMALE; HORMONE SUBSTITUTION; RISK FACTOR;

ANIMALS; DIABETES MELLITUS, TYPE 1; DIABETES MELLITUS, TYPE 2; FEMALE; HORMONE REPLACEMENT THERAPY; HUMANS; MENOPAUSE; RISK FACTORS;

EID: 84958258489     PISSN: 15344827     EISSN: 15390829     Source Type: Journal    
DOI: 10.1007/s11892-016-0714-x     Document Type: Review

References (85)

1. Narayan KM, Boyle JP, Thompson TJ, et al. Lifetime risk for diabetes mellitus in the United States. JAMA. 2003;290(14):1884–90.
2. Harlow SD, Gass M, Hall JE, et al. Executive summary of the Stages of Reproductive Aging Workshop + 10: addressing the unfinished agenda of staging reproductive aging. J Clin Endocrinol Metab. 2012;97(4):1159–68. This paper provides the contemporary methodology for defining the stages of reproductive aging and makes recommendations on the future directions for staging the menopausal transition.
3. Kim C. Does menopause increase diabetes risk? Strategies for diabetes prevention in midlife women. Womens Health. 2012;8(2):155–67.
4. Sowers MR, Zheng H, McConnell D, et al. Follicle stimulating hormone and its rate of change in defining menopause transition stages. J Clin Endocrinol Metab. 2008;93(10):3958–64.
5. Sowers MR, Zheng H, McConnell D, et al. Estradiol rates of change in relation to the final menstrual period in a population-based cohort of women. J Clin Endocrinol Metab. 2008;93(10):3847–52.
6. Randolph Jr JF, Zheng H, Sowers MR, et al. Change in follicle-stimulating hormone and estradiol across the menopausal transition: effect of age at the final menstrual period. J Clin Endocrinol Metab. 2011;96(3):746–54.
7. Sowers MR, Eyvazzadeh AD, McConnell D, et al. Anti-mullerian hormone and inhibin B in the definition of ovarian aging and the menopause transition. J Clin Endocrinol Metab. 2008;93(9):3478–83.
8. Rosen MP, Johnstone E, McCulloch CE, et al. A characterization of the relationship of ovarian reserve markers with age. Fertil Steril. 2012;97(1):238–43.
9. van Rooij IA, Broekmans FJ, Scheffer GJ, et al. Serum antimullerian hormone levels best reflect the reproductive decline with age in normal women with proven fertility: a longitudinal study. Fertil Steril. 2005;83(4):979–87.
10. de Vet A, Laven JS, de Jong FH, et al. Antimüllerian hormone serum levels: a putative marker for ovarian aging. Fertil Steril. 2002;77(2):357–62.
11. Ledger WL. Clinical utility of measurement of anti-mullerian hormone in reproductive endocrinology. J Clin Endocrinol Metab. 2010;95(12):5144–54.
12. Lauritsen M, Bentzen J, Pinborg A, et al. The prevalence of polycystic ovary syndrome in a normal population according to the Rotterdam criteria versus revised criteria including anti-mullerian hormone. Hum Reprod. 2014;29(4):791–801.
13. Heianza Y, Arase Y, Kodama S, et al. Effect of postmenopausal status and age at menopause on type 2 diabetes and prediabetes in Japanese individuals: Toranomon Hospital Health Management Center Study 17 (TOPICS 17). Diabetes Care. 2013;36(12):4007–14.
14. Di Donato P, Giulini NA, Bacchi Modena A, et al. Risk factors for type 2 diabetes in women attending menopause clinics in Italy: a cross-sectional study. Climacteric. 2005;8(3):287–93.
15. Muscelli E, Kozakova M, Flyvbjerg A, et al. The effect of menopause on carotid artery remodeling, insulin sensitivity, and plasma adiponectin in healthy women. Am J Hypertens. 2009;4:364–70.
16. Monterrosa-Castro A, Blumel JE, Portela-Buelvas K, et al. Type II diabetes mellitus and menopause: a multinational study. Climacteric. 2013;16:663–72.
17. Lee JS, Hayashi K, Mishra G, et al. Independent association between age at natural menopause and hypercholesterolemia, hypertension, and diabetes mellitus: Japan nurses’ health study. J Atheroscler Thromb. 2013;20(2):161–9.
18. Soriguer F, Morcillo S, Hernando V, et al. Type 2 diabetes mellitus and other cardiovascular risk factors are no more common during menopause: longitudinal study. Menopause. 2009;16(4):817–21.
19. Mishra GD, Carrigan G, Brown WJ, et al. Short-term weight change and the incidence of diabetes in midlife: results from the Australian Longitudinal Study on Women’s Health. Diabetes Care. 2007;30(6):1418–24.
20. Kim C, Edelstein SL, Crandall JP, et al. Menopause and risk of diabetes in the Diabetes Prevention Program. Menopause. 2011;18(8):857–68.
21. Malacara JM, Huerta R, Rivera B, et al. Menopause in normal and uncomplicated NIDDM women: physical and emotional symptoms and hormone profile. Maturitas. 1997;28(1):35–45.
22. Appiah D, Winters SJ, Hornung CA. Bilateral oophorectomy and the risk of incident diabetes in postmenopausal women. Diabetes Care. 2014;37(3):725–33.
23. Brand JS, van der Schouw YT, Onland-Moret NC, et al. Age at menopause, reproductive life span, and type 2 diabetes risk: results from the EPIC-InterAct study. Diabetes Care. 2013;36(4):1012–9. This is a subcohort analysis of the larger EPIC study, reference 25.
24. Luborsky JL, Meyer P, Sowers MF, et al. Premature menopause in a multi-ethnic population study of the menopause transition. Hum Reprod. 2003;18(1):199–206.
25. Brand JS, Onland-Moret NC, Eijkemans MJ, et al. Diabetes and onset of natural menopause: results from the European Prospective Investigation into Cancer and Nutrition. Hum Reprod. 2015;30(6):1491–8. This is the largest prospective study examining the association between diabetes and age at natural menopause.
26. Qiu C, Chen H, Wen J, et al. Associations between age at menarche and menopause with cardiovascular disease, diabetes, and osteoporosis in Chinese women. J Clin Endocrinol Metab. 2013;98(4):1612–21.
27. He L, Tang X, Li N, et al. Menopause with cardiovascular disease and its risk factors among rural Chinese women in Beijing: a population-based study. Maturitas. 2012;72(2):132–8.
28. Lopez-Lopez R, Huerta R, Malacara JM. Age at menopause in women with type 2 diabetes mellitus. Menopause. 1999;6(2):174–8.
29. Lejskova M, Pit’ha J, Adamkova S, et al. Bilateral oophorectomy may have an unfavorable effect on glucose metabolism compared with natural menopause. Physiol Res. 2014;63 Suppl 3:S395–402.
30. Riant E, Waget A, Cogo H, et al. Estrogens protect against high-fat diet-induced insulin resistance and glucose intolerance in mice. Endocrinology. 2009;150(5):2109–17.
31. Zhu L, Martinez MN, Emfinger CH, et al. Estrogen signaling prevents diet-induced hepatic insulin resistance in male mice with obesity. Am J Physiol Endocrinol Metab. 2014;306(10):E1188–97.
32. Baek TH, Lim NK, Kim MJ, et al. Age at menarche and its association with dysglycemia in Korean middle-aged women. Menopause. 2015;22(5):542–8.
33. Chen L, Zhang C, Yeung E, et al. Age at menarche and metabolic markers for type 2 diabetes in premenopausal women: the Biocycle Study. J Clin Endocrinol Metab. 2011;96(6):E1007–12.
34. Day FR, Elks CE, Murray A, et al. Puberty timing associated with diabetes, cardiovascular disease and also diverse health outcomes in men and women: the UK Biobank study. Sci Rep. 2015;18(5):11208.
35. He C, Zhang C, Hunter DJ, et al. Age at menarche and risk of type 2 diabetes: results from 2 large prospective cohort studies. Am J Epidemiol. 2010;171(3):334–44.
36. Lakshman R, Forouhi N, Luben R, et al. Association between age at menarche and risk of diabetes in adults: results from the EPIC-Norfolk cohort study. Diabetologia. 2008;51(5):781–6.
37. Sternfeld B, Wang H, Quesenberry Jr CP, et al. Physical activity and changes in weight and waist circumference in midlife women: findings from the Study of Women’s Health Across the Nation. Am J Epidemiol. 2004;160(9):912–22.
38. Davies KM, Heaney RP, Recker RR, et al. Hormones, weight change and menopause. Int J Obes Relat Metab Disord. 2001;25(6):874–9.
39. Davis SR, Castelo-Branco C, Chedraui P, et al. Understanding weight gain at menopause. Climacteric. 2012;15(5):419–29.
40. Toth MJ, Tchernof A, Sites CK, et al. Menopause-related changes in body fat distribution. Ann N Y Acad Sci. 2000;904:502–6.
41. Sowers M, Zheng H, Tomey K, et al. Changes in body composition in women over six years at midlife: ovarian and chronological aging. J Clin Endocrinol Metab. 2007;92(3):895–901.
42. De Pergola G, Maldera S, Tartagni M, et al. Inhibitory effect of obesity on gonadotropin, estradiol, and inhibin B levels in fertile women. Obesity. 2006;14(11):1954–60.
43. Freeman EW, Sammel MD, Lin H, et al. Obesity and reproductive hormone levels in the transition to menopause. Menopause. 2010;17:718–26.
44. Nelson LR, Bulun SE. Estrogen production and action. J Am Acad Dermatol. 2001;45(3 Suppl):S116–124.
45. Szymczak J, Milewicz A, Thijssen JH, et al. Concentration of sex steroids in adipose tissue after menopause. Steroids. 1998;63(5-6):319–21.
46. Pfeilschifter J, Koditz R, Pfohl M, et al. Changes in proinflammatory cytokine activity after menopause. Endocr Rev. 2002;23(1):90–119.
47. Malutan AM, Dan M, Nicolae C, et al. Proinflammatory and anti-inflammatory cytokine changes related to menopause. Prz Menopauzalny. 2014;13(3):162–8.
48. Vryonidou A, Paschou SA, Muscogiuri G, et al. Mechanisms in endocrinology: metabolic syndrome through the female life cycle. Eur J Endocrinol. 2015;173(5):R153–163.
49. Sites CK, Calles-Escandon J, Brochu M, et al. Relation of regional fat distribution to insulin sensitivity in postmenopausal women. Fertil Steril. 2000;73(1):61–5.
50. Barrett-Connor E, Schrott HG, Greendale G, et al. Factors associated with glucose and insulin levels in healthy postmenopausal women. Diabetes Care. 1996;19:333–40.
51. Campbell AJ, Busby WJ, Horwath CC, et al. Relation of age, exercise, anthropometric measurements, and diet with glucose and insulin levels in a population aged 70 years and over. Am J Epidemiol. 1993;138:688–96.
52. Kim C, Halter JB. Endogenous sex hormones, metabolic syndrome, and diabetes in men and women. Curr Cardiol Rep. 2014;16(4):467.
53. Sowers MF, Zheng H, McConnell D, et al. Testosterone, sex hormone-binding globulin and free androgen index among adult women: chronological and ovarian aging. Hum Reprod. 2009;24(9):2276–85.
54. Oh JY, Barrett-Connor E, Wedick NM, et al. Endogenous sex hormones and the development of type 2 diabetes in older men and women: the Rancho Bernardo study. Diabetes Care. 2002;25(1):55–60.
55. Goodman-Gruen D, Barrett-Connor E. Sex hormone-binding globulin and glucose tolerance in postmenopausal women. The Rancho Bernardo study. Diabetes Care. 1997;20(4):645–9.
56. Golden SH, Dobs AS, Vaidya D, et al. Endogenous sex hormones and glucose tolerance status in postmenopausal women. J Clin Endocrinol Metab. 2007;92(4):1289–95.
57. Kalyani RR, Franco M, Dobs AS, et al. The association of endogenous sex hormones, adiposity, and insulin resistance with incident diabetes in postmenopausal women. J Clin Endocrinol Metab. 2009;94(11):4127–35.
58. Ding EL, Song Y, Manson JE, et al. Plasma sex steroid hormones and risk of developing type 2 diabetes in women: a prospective study. Diabetologia. 2007;50(10):2076–84.
59. Ding EL, Song Y, Manson JE, et al. Sex hormone-binding globulin and risk of type 2 diabetes in women and men. N Engl J Med. 2009;361(12):1152–63.
60. Janssen I, Powell LH, Crawford S, et al. Menopause and the metabolic syndrome: the Study of Women’s Health Across the Nation. Arch Intern Med. 2008;168(14):1568–75.
61. Cignarella A, Kratz M, Bolego C. Emerging role of estrogen in control of cardiometabolic disease. Trends Pharmacol Sci. 2010;31(4):183–9.
62. Mather KM, Kim C, Christophi CA, et al. Steroid sex hormones, sex hormone binding globulin and diabetes incidence in the Diabetes Prevention Program. J Clin Endocrinol Metab. 2015;100(10):3778–86.
63. Buschur E, Sarma A, Pietropaolo M, et al. Self-reported autoimmune disease by sex in the Diabetes Control and Complications Trial/Epidemiology of Diabetes Interventions and Complications (DCCT/EDIC) Study. Diabetes Care. 2014;37(2):E28–29.
64. Dorman JS, Steenkiste AR, Foley TP, et al. Menopause in type 1 diabetic women: is it premature? Diabetes. 2001;50(8):1857–62.
65. Strotmeyer ES, Steenkiste AR, Foley Jr TP, et al. Menstrual cycle differences between women with type 1 diabetes and women without diabetes. Diabetes Care. 2003;26(4):1016–21.
66. Snell-Bergeon JK, Dabelea D, Ogden LG, et al. Reproductive history and hormonal birth control use are associated with coronary calcium progression in women with type 1 diabetes mellitus. J Clin Endocrinol Metab. 2008;93(6):2142–8.
67. SEARCH for Diabetes in Youth Study Group. The burden of diabetes mellitus among U.S. youth: prevalence estimates from the SEARCH for Diabetes in Youth Study. Pediatrics. 2006;118:1510–8.
68. Sjoberg L, Pitkaniemi J, Harjutsalo V, et al. Menopause in women with type 1 diabetes. Menopause. 2011;18(2):158–63.
69. Kim C, Cleary PA, Cowie CC, et al. Effect of glycemic treatment and microvascular complications on menopause in women with type 1 diabetes in the Diabetes Control and Complications Trial/Epidemiology of Diabetes Interventions and Complications (DCCT/EDIC) cohort. Diabetes Care. 2014;37(3):701–8.
70. Yarde F, van der Schouw YT, de Valk HW, et al. Age at menopause in women with type 1 diabetes mellitus: the OVADIA study. Hum Reprod. 2015;30(2):441–6.
71. Khalil N, Sutton-Tyrrell K, Strotmeyer ES, et al. Menopausal bone changes and incident fractures in diabetic women: a cohort study. Osteoporos Int. 2011;22(5):1367–76.
72. Kanaya AM, Herrington D, Vittinghoff E, et al. Glycemic effects of postmenopausal hormone therapy: the Heart and Estrogen/Progestin Replacement Study. A randomized, double-blind, placebo-controlled trial. Ann Intern Med. 2003;138(1):1–9.
73. Margolis KL, Bonds DE, Rodabough RJ, et al. Effect of oestrogen plus progestin on the incidence of diabetes in postmenopausal women: results from the Women’s Health Initiative Hormone Trial. Diabetologia. 2004;47(7):1175–87.
74. Bonds DE, Lasser N, Qui L, et al. The effect of conjugated equine estrogen on diabetes incidence: the Women’s Health Initiative randomized trial. Diabetologia. 2006;49(3):459–68.
75. Rossi R, Origliani G, Modena MG. Transdermal 17-beta-estradiol and risk of developing type 2 diabetes in a population of healthy, nonobese postmenopausal women. Diabetes Care. 2004;27(3):645–9.
76. Manson JE, Rimm EB, Colditz GA, et al. A prospective study of postmenopausal estrogen therapy and subsequent incidence of non-insulin-dependent diabetes mellitus. Ann Epidemiol. 1992;2(5):665–73.
77. Pentti K, Tuppurainen MT, Honkanen R, et al. Hormone therapy protects from diabetes: the Kuopio Osteoporosis Risk Factor and Prevention Study. Eur J Endocrinol. 2009;160(6):979–83.
78. de Lauzon-Guillain B, Fournier A, Fabre A, et al. Menopausal hormone therapy and new-onset diabetes in the French Etude Epidemiologique de Femmes de la Mutuelle Generale de l’Education Nationale (E3N) cohort. Diabetologia. 2009;52(10):2092–100.
79. Salpeter SR, Walsh JM, Ormiston TM, et al. Meta-analysis: effect of hormone-replacement therapy on components of the metabolic syndrome in postmenopausal women. Diabetes Obes Metab. 2006;8(5):538–54.
80. Xu Y, Lin J, Wang S, et al. Combined estrogen replacement therapy on metabolic control in postmenopausal women with diabetes mellitus. Kaohsiung J Med Soc. 2014;30(7):350–61. This is a meta-analysis of studies published between 2001 and 2011 which evaluated the association of hormone therapy and diabetes risk.
81. Espeland MA, Hogan PE, Fineberg SE, et al. Effect of postmenopausal hormone therapy on glucose and insulin concentrations. Postmenopausal Estrogen/Progestin Interventions. Diabetes Care. 1998;21(10):1589–95.
82. Moyer VA, U.S. Preventative Services Task Force. Menopausal hormone therapy for the primary prevention of chronic conditions: U.S. Preventative Services Task Force recommendation statement. Ann Intern Med. 2013;158(1):47–54.
83. Cignarella A, Bolego C. Mechanisms of estrogen protection in diabetes and metabolic disease. Horm Mol Biol Clin Investig. 2010;4(2):575–80.
84. Hodis HN, Mack WJ. Hormone replacement therapy and the association with coronary heart disease and overall mortality: clinical application of the timing hypothesis. J Steroid Biochem Mol Biol. 2014;142:68–75.
85. Pereira RI, Casey BA, Swibas TA, et al. Timing of estradiol treatment after menopause may determine benefit or harm to insulin action. J Clin Endocrinol Metab. 2015. [Epub ahead of print]. This study evaluated the hypothesized ‘timing hypothesis’ with regard to estrogen therapy and diabetes. Findings from this study may explain some of the discordant findings regarding menopause and diabetes.