nach oben

Hormones

Erschienen in:

01.09.2020 | Review Article

Reproductive health in women with type 2 diabetes mellitus

verfasst von: Doina Creţu, Simona Cernea, Corina Roxana Onea, Raluca-Monica Pop

Erschienen in: Hormones | Ausgabe 3/2020

Einloggen, um Zugang zu erhalten

Abstract

As type 2 diabetes mellitus (T2DM) reaches epidemic proportions in the developed world and the age at diagnosis decreases, more women of reproductive age are being affected. In this article, we provide a synoptic view on potential mechanisms and relevant factors underlying menstrual cycle disorders and fertility issues in women with T2DM. The article discusses the function of the hypothalamic-pituitary-ovarian (HPO) axis, the central role of the hypothalamus in the homeostasis of this system, the central modulators of the axis, and the peripheral metabolic signals involved in neuroendocrine control of reproduction. The available literature on the relationship between T2DM and the female reproductive lifespan, menstrual cycle disorders, fertility issues, and gestational health in women with T2DM are also discussed. The data so far indicate that there is a “U-shaped” relationship between menarche, menopause, and T2DM, both early and late menarche/menopause being risk factors for T2DM. Hyperglycemia and its consequences may be responsible for the effects of T2DM on reproductive health in women, but the exact mechanisms are not as yet fully understood; thus, more studies are needed in order to identify factors causing disruption of the HPO axis.

Cho NH, Shaw JE, Karuranga S, Huang Y, da Rocha Fernandes JD, Ohlrogge AW, Malanda B (2018) IDF diabetes atlas: global estimates of diabetes prevalence for 2017 and projections for 2045. Diabetes Res Clin Pract 138:271–281. https://doi.org/10.1016/j.diabres.2018.02.023CrossRefPubMed

Kelsey MM, Braffett BH, Geffner ME, Levitsky LL, Caprio S, McKay SV, Shah R, Sprague JE, Arslanian SA, Group TS (2018) Menstrual dysfunction in girls from the treatment options for type 2 diabetes in adolescents and youth (TODAY) study. J Clin Endocrinol Metab 103(6):2309–2318. https://doi.org/10.1210/jc.2018-00132CrossRefPubMedPubMedCentral

Pinilla L, Aguilar E, Dieguez C, Millar RP, Tena-Sempere M (2012) Kisspeptins and reproduction: physiological roles and regulatory mechanisms. Physiol Rev 92(3):1235–1316. https://doi.org/10.1152/physrev.00037.2010CrossRefPubMed

Manfredi-Lozano M, Roa J, Tena-Sempere M (2018) Connecting metabolism and gonadal function: novel central neuropeptide pathways involved in the metabolic control of puberty and fertility. Front Neuroendocrinol 48:37–49. https://doi.org/10.1016/j.yfrne.2017.07.008CrossRefPubMed

Di Giorgio NP, Bizzozzero M, Libertun C, Lux-Lantos V (2019) Unraveling the connection between GABA and Kisspeptin in the control of reproduction. Reproduction 157(6):R225–R233. https://doi.org/10.1530/rep-18-0527CrossRefPubMed

Tsutsui K, Ubuka T (2018) How to contribute to the progress of neuroendocrinology: discovery of GnIH and progress of GnIH research. Front Endocrinol (Lausanne) 9:662. https://doi.org/10.3389/fendo.2018.00662CrossRef

Asimakopoulos B (2012) Hypothalamus-pituitary-gonadal axis: it is time for revision. Hum Genet Embryol 02(01):e106. https://doi.org/10.4172/2161-0436.1000e106CrossRef

Simonneaux V (2020) A kiss to drive rhythms in reproduction. Eur J Neurosci 51(1):509–530. https://doi.org/10.1111/ejn.14287CrossRefPubMed

Elias CF (2012) Leptin action in pubertal development: recent advances and unanswered questions. Trends Endocrinol Metab 23(1):9–15. https://doi.org/10.1016/j.tem.2011.09.002CrossRefPubMed

10.

Seminara SB, Messager S, Chatzidaki EE, Thresher RR, Acierno JS Jr, Shagoury JK, Bo-Abbas Y, Kuohung W, Schwinof KM, Hendrick AG, Zahn D, Dixon J, Kaiser UB, Slaugenhaupt SA, Gusella JF, O'Rahilly S, Carlton MB, Crowley WF Jr, Aparicio SA, Colledge WH (2003) The GPR54 gene as a regulator of puberty. N Engl J Med 349(17):1614–1627. https://doi.org/10.1056/NEJMoa035322CrossRefPubMed

11.

Cortes ME, Carrera B, Rioseco H, Pablo del Rio J, Vigil P (2015) The role of kisspeptin in the onset of puberty and in the ovulatory mechanism: a mini-review. J Pediatr Adolesc Gynecol 28(5):286–291. https://doi.org/10.1016/j.jpag.2014.09.017CrossRefPubMed

12.

Lunenfeld B, Buhler K (2018) The neuro control of the ovarain cycle - a hypothesis. Gynecol Endocrinol 34(4):278–282. https://doi.org/10.1080/09513590.2017.1405933CrossRefPubMed

13.

Goldsammler M, Merhi Z, Buyuk E (2018) Role of hormonal and inflammatory alterations in obesity-related reproductive dysfunction at the level of the hypothalamic-pituitary-ovarian axis. Reprod Biol Endocrinol 16(1):45. https://doi.org/10.1186/s12958-018-0366-6CrossRefPubMedPubMedCentral

14.

Vazquez MJ, Romero-Ruiz A, Tena-Sempere M (2015) Roles of leptin in reproduction, pregnancy and polycystic ovary syndrome: consensus knowledge and recent developments. Metabolism 64(1):79–91. https://doi.org/10.1016/j.metabol.2014.10.013CrossRefPubMed

15.

Ramos-Lobo AM, Donato J Jr (2017) The role of leptin in health and disease. Temperature (Austin) 4(3):258–291. https://doi.org/10.1080/23328940.2017.1327003CrossRef

16.

Sliwowska JH, Fergani C, Gawalek M, Skowronska B, Fichna P, Lehman MN (2014) Insulin: its role in the central control of reproduction. Physiol Behav 133:197–206. https://doi.org/10.1016/j.physbeh.2014.05.021CrossRefPubMed

17.

Dupont J, Scaramuzzi RJ (2016) Insulin signalling and glucose transport in the ovary and ovarian function during the ovarian cycle. Biochem J 473(11):1483–1501. https://doi.org/10.1042/BCJ20160124CrossRefPubMedPubMedCentral

18.

Psilopanagioti A, Papadaki H, Kranioti EF, Alexandrides TK, Varakis JN (2009) Expression of adiponectin and adiponectin receptors in human pituitary gland and brain. Neuroendocrinology 89(1):38–47. https://doi.org/10.1159/000151396CrossRefPubMed

19.

Dos Santos E, Serazin V, Morvan C, Torre A, Wainer R, de Mazancourt P, Dieudonne MN (2012) Adiponectin and leptin systems in human endometrium during window of implantation. Fertil Steril 97(3):771–778 e771. https://doi.org/10.1016/j.fertnstert.2011.12.042CrossRefPubMed

20.

Wen JP, Liu C, Bi WK, Hu YT, Chen Q, Huang H, Liang JX, Li LT, Lin LX, Chen G (2012) Adiponectin inhibits KISS1 gene transcription through AMPK and specificity protein-1 in the hypothalamic GT1-7 neurons. J Endocrinol 214(2):177–189. https://doi.org/10.1530/JOE-12-0054CrossRefPubMed

21.

Dobrzyn K, Smolinska N, Kiezun M, Szeszko K, Rytelewska E, Kisielewska K, Gudelska M, Kaminski T (2018) Adiponectin: a new regulator of female reproductive system. Int J Endocrinol 2018:7965071. https://doi.org/10.1155/2018/7965071CrossRefPubMedPubMedCentral

22.

Takei Y, Takahashi A (2016) Appetite-regulating peptides. In: Takei Y, Ando H, Tsutsui K (eds) Handbook of Hormones. Elsevier, Amsterdam, pp 78–79. https://doi.org/10.1016/b978-0-12-801028-0.00010-6CrossRef

23.

Lanfranco F, Bonelli L, Baldi M, Me E, Broglio F, Ghigo E (2008) Acylated ghrelin inhibits spontaneous luteinizing hormone pulsatility and responsiveness to naloxone but not that to gonadotropin-releasing hormone in young men: evidence for a central inhibitory action of ghrelin on the gonadal axis. J Clin Endocrinol Metab 93(9):3633–3639. https://doi.org/10.1210/jc.2008-0049CrossRefPubMed

24.

Lanfranco F, Motta G, Baldi M, Gasco V, Grottoli S, Benso A, Broglio F, Ghigo E (2010) Ghrelin and anterior pituitary function. Front Horm Res 38:206–211. https://doi.org/10.1159/000318512CrossRefPubMed

25.

Tena-Sempere M (2013) Ghrelin, the gonadal axis and the onset of puberty. Endocr Dev 25:69–82. https://doi.org/10.1159/000346055CrossRefPubMed

26.

Klenke U, Constantin S, Wray S (2010) Neuropeptide Y directly inhibits neuronal activity in a subpopulation of gonadotropin-releasing hormone-1 neurons via Y1 receptors. Endocrinology 151(6):2736–2746. https://doi.org/10.1210/en.2009-1198CrossRefPubMedPubMedCentral

27.

Wang Y, Meng RW, Kunutsor SK, Chowdhury R, Yuan JM, Koh WP, Pan A (2018) Plasma adiponectin levels and type 2 diabetes risk: a nested case-control study in a Chinese population and an updated meta-analysis. Sci Rep 8(1):406. https://doi.org/10.1038/s41598-017-18709-9CrossRefPubMedPubMedCentral

28.

Gotlieb N, Moeller J, Kriegsfeld LJ (2018) Circadian control of neuroendocrine function: implications for health and disease. Curr Opin Physiol 5:133–140. https://doi.org/10.1016/j.cophys.2018.11.001CrossRefPubMedPubMedCentral

29.

Zimmet P, Alberti K, Stern N, Bilu C, El-Osta A, Einat H, Kronfeld-Schor N (2019) The circadian syndrome: is the metabolic syndrome and much more! J Intern Med 286(2):181–191. https://doi.org/10.1111/joim.12924CrossRefPubMedPubMedCentral

30.

Stenvers DJ, Jongejan A, Atiqi S, Vreijling JP, Limonard EJ, Endert E, Baas F, Moerland PD, Fliers E, Kalsbeek A, Bisschop PH (2019) Diurnal rhythms in the white adipose tissue transcriptome are disturbed in obese individuals with type 2 diabetes compared with lean control individuals. Diabetologia 62(4):704–716. https://doi.org/10.1007/s00125-019-4813-5CrossRefPubMed

31.

Parent AS, Teilmann G, Juul A, Skakkebaek NE, Toppari J, Bourguignon JP (2003) The timing of normal puberty and the age limits of sexual precocity: variations around the world, secular trends, and changes after migration. Endocr Rev 24(5):668–693. https://doi.org/10.1210/er.2002-0019CrossRefPubMed

32.

Brix N, Ernst A, Lauridsen LLB, Parner E, Stovring H, Olsen J, Henriksen TB, Ramlau-Hansen CH (2019) Timing of puberty in boys and girls: a population-based study. Paediatr Perinat Epidemiol 33(1):70–78. https://doi.org/10.1111/ppe.12507CrossRefPubMed

33.

Harris HR, Cramer DW, Vitonis AF, DePari M, Terry KL (2012) Folate, vitamin B(6) , vitamin B(12) , methionine and alcohol intake in relation to ovarian cancer risk. Int J Cancer 131(4):E518–E529. https://doi.org/10.1002/ijc.26455CrossRefPubMed

34.

Petersohn I, Zarate-Ortiz AG, Cepeda-Lopez AC, Melse-Boonstra A (2019) Time trends in age at menarche and related non-communicable disease risk during the 20th century in Mexico. Nutrients 11(2). https://doi.org/10.3390/nu11020394

35.

Wilson DA, Derraik JG, Rowe DL, Hofman PL, Cutfield WS (2015) Earlier menarche is associated with lower insulin sensitivity and increased adiposity in young adult women. PLoS One 10(6):e0128427. https://doi.org/10.1371/journal.pone.0128427CrossRefPubMedPubMedCentral

36.

Jansen EC, Stern D, Peterson KE, Lajous M, Lopez-Ridaura R (2019) Early menstrual factors are associated with adulthood cardio-metabolic health in a survey of Mexican teachers. Matern Child Health J 23(3):356–368. https://doi.org/10.1007/s10995-018-2650-7CrossRefPubMedPubMedCentral

37.

Comninos AN, Jayasena CN, Dhillo WS (2014) The relationship between gut and adipose hormones, and reproduction. Hum Reprod Update 20(2):153–174. https://doi.org/10.1093/humupd/dmt033CrossRefPubMed

38.

Lebenthal Y, Gat-Yablonski G, Shtaif B, Padoa A, Phillip M, Lazar L (2006) Effect of sex hormone administration on circulating ghrelin levels in peripubertal children. J Clin Endocrinol Metab 91(1):328–331. https://doi.org/10.1210/jc.2005-0204CrossRefPubMed

39.

Janghorbani M, Mansourian M, Hosseini E (2014) Systematic review and meta-analysis of age at menarche and risk of type 2 diabetes. Acta Diabetol 51(4):519–528. https://doi.org/10.1007/s00592-014-0579-xCrossRefPubMed

40.

Dreyfus JG, Lutsey PL, Huxley R, Pankow JS, Selvin E, Fernandez-Rhodes L, Franceschini N, Demerath EW (2012) Age at menarche and risk of type 2 diabetes among African-American and white women in the atherosclerosis risk in communities (ARIC) study. Diabetologia 55(9):2371–2380. https://doi.org/10.1007/s00125-012-2616-zCrossRefPubMedPubMedCentral

41.

Stockl D, Doring A, Peters A, Thorand B, Heier M, Huth C, Stockl H, Rathmann W, Kowall B, Meisinger C (2012) Age at menarche is associated with prediabetes and diabetes in women (aged 32-81 years) from the general population: the KORA F4 study. Diabetologia 55(3):681–688. https://doi.org/10.1007/s00125-011-2410-3CrossRefPubMed

42.

Shen C, Wen J, Pan X, Su J, Du W, Pan E, Zhang Q, Zhang N, Sheng H, Liu C, Wang H, Wu M, Qin Y (2018) Age at menarche and age at natural menopause as predictors of glycemic control in type 2 diabetic patients. J Diabetes Complicat 32(7):623–629. https://doi.org/10.1016/j.jdiacomp.2018.04.012CrossRefPubMed

43.

Sumi A, Iwase M, Nakamura U, Fujii H, Ohkuma T, Ide H, Jodai-Kitamura T, Komorita Y, Yoshinari M, Kitazono T (2018) Impact of age at menarche on obesity and glycemic control in Japanese patients with type 2 diabetes: Fukuoka diabetes registry. J Diabetes Investig 9(5):1216–1223. https://doi.org/10.1111/jdi.12839CrossRefPubMedPubMedCentral

44.

Shim U, Oh JY, Lee HJ, Hong YS, Sung YA (2011) Long menstrual cycle is associated with type 2 diabetes mellitus in korean women. Diabetes Metab J 35(4):384–389. https://doi.org/10.4093/dmj.2011.35.4.384CrossRefPubMedPubMedCentral

45.

Zargar AH, Gupta VK, Wani AI, Masoodi SR, Bashir MI, Laway BA, Ganie MA, Salahuddin M (2005) Prevalence of ultrasonography proved polycystic ovaries in north Indian women with type 2 diabetes mellitus. Reprod Biol Endocrinol 3:35. https://doi.org/10.1186/1477-7827-3-35CrossRefPubMedPubMedCentral

46.

Conn JJ, Jacobs HS, Conway GS (2000) The prevalence of polycystic ovaries in women with type 2 diabetes mellitus. Clin Endocrinol 52(1):81–86. https://doi.org/10.1046/j.1365-2265.2000.00884.xCrossRef

47.

Isik S, Ozcan HN, Ozuguz U, Tutuncu YA, Berker D, Alimli AG, Akbaba G, Karademir MA, Guler S (2012) Evaluation of ovarian reserve based on hormonal parameters, ovarian volume, and antral follicle count in women with type 2 diabetes mellitus. J Clin Endocrinol Metab 97(1):261–269. https://doi.org/10.1210/jc.2011-1923CrossRefPubMed

48.

Rostami Dovom M, Ramezani Tehrani F, Djalalinia S, Cheraghi L, Behboudi Gandavani S, Azizi F (2016) Menstrual cycle irregularity and metabolic disorders: a population-based prospective study. PLoS One 11(12):e0168402. https://doi.org/10.1371/journal.pone.0168402CrossRefPubMedPubMedCentral

49.

Solomon CG, Hu FB, Dunaif A, Rich-Edwards J, Willett WC, Hunter DJ, Colditz GA, Speizer FE, Manson JE (2001) Long or highly irregular menstrual cycles as a marker for risk of type 2 diabetes mellitus. JAMA 286(19):2421–2426. https://doi.org/10.1001/jama.286.19.2421CrossRefPubMed

50.

Roumain J, Charles MA, de Courten MP, Hanson RL, Brodie TD, Pettitt DJ, Knowler WC (1998) The relationship of menstrual irregularity to type 2 diabetes in Pima Indian women. Diabetes Care 21(3):346–349. https://doi.org/10.2337/diacare.21.3.346CrossRefPubMed

51.

Glueck CJ, Woo JG, Khoury PR, Morrison JA, Daniels SR, Wang P (2015) Adolescent oligomenorrhea (age 14-19) tracks into the third decade of life (age 20-28) and predicts increased cardiovascular risk factors and metabolic syndrome. Metabolism 64(4):539–553. https://doi.org/10.1016/j.metabol.2015.01.005CrossRefPubMed

52.

Wu Y, Li Y, Liao X, Wang Z, Li R, Zou S, Jiang T, Zheng B, Duan P, Xiao J (2017) Diabetes induces abnormal ovarian function via triggering apoptosis of granulosa cells and suppressing ovarian angiogenesis. Int J Biol Sci 13(10):1297–1308. https://doi.org/10.7150/ijbs.21172CrossRefPubMedPubMedCentral

53.

Livshits A, Seidman DS (2009) Fertility issues in women with diabetes. Womens Health (Lond) 5(6):701–707. https://doi.org/10.2217/whe.09.47CrossRef

54.

Tobias DK, Gaskins AJ, Missmer SA, Hu FB, Manson JE, Buck Louis GM, Zhang C, Chavarro JE (2015) History of infertility and risk of type 2 diabetes mellitus: a prospective cohort study. Diabetologia 58(4):707–715. https://doi.org/10.1007/s00125-015-3493-zCrossRefPubMedPubMedCentral

55.

Amaral S, Oliveira PJ, Ramalho-Santos J (2008) Diabetes and the impairment of reproductive function: possible role of mitochondria and reactive oxygen species. Curr Diabetes Rev 4(1):46–54. https://doi.org/10.2174/157339908783502398CrossRefPubMed

56.

Agarwal A, Gupta S, Sharma R (2005) Oxidative stress and its implications in female infertility - a clinician’s perspective. Reprod BioMed Online 11(5):641–650. https://doi.org/10.1016/s1472-6483(10)61174-1CrossRefPubMed

57.

Maresch CC, Stute DC, Alves MG, Oliveira PF, de Kretser DM, Linn T (2018) Diabetes-induced hyperglycemia impairs male reproductive function: a systematic review. Hum Reprod Update 24(1):86–105. https://doi.org/10.1093/humupd/dmx033CrossRefPubMed

58.

Coton SJ, Nazareth I, Petersen I (2016) A cohort study of trends in the prevalence of pregestational diabetes in pregnancy recorded in UK general practice between 1995 and 2012. BMJ Open 6(1):e009494. https://doi.org/10.1136/bmjopen-2015-009494CrossRefPubMedPubMedCentral

59.

Dunne F, Brydon P, Smith K, Gee H (2003) Pregnancy in women with type 2 diabetes: 12 years outcome data 1990-2002. Diabet Med 20(9):734–738. https://doi.org/10.1046/j.1464-5491.2003.01017.xCrossRefPubMed

60.

Cundy T, Gamble G, Neale L, Elder R, McPherson P, Henley P, Rowan J (2007) Differing causes of pregnancy loss in type 1 and type 2 diabetes. Diabetes Care 30(10):2603–2607. https://doi.org/10.2337/dc07-0555CrossRefPubMed

61.

Clausen TD, Mathiesen E, Ekbom P, Hellmuth E, Mandrup-Poulsen T, Damm P (2005) Poor pregnancy outcome in women with type 2 diabetes. Diabetes Care 28(2):323–328. https://doi.org/10.2337/diacare.28.2.323CrossRefPubMed

62.

de Valk HW, van Nieuwaal NH, Visser GH (2006) Pregnancy outcome in type 2 diabetes mellitus: a retrospective analysis from the Netherlands. Rev Diabet Stud 3(3):134–142. https://doi.org/10.1900/RDS.2006.3.134CrossRefPubMedPubMedCentral

63.

Bashir M, Dabbous Z, Baagar K, Elkhatib F, Ibrahim A, Brich SA, Abdel-Rahman ME, Konje JC, Abou-Samra AB (2019) Type 2 diabetes mellitus in pregnancy: the impact of maternal weight and early glycaemic control on outcomes. Eur J Obstet Gynecol Reprod Biol 233:53–57. https://doi.org/10.1016/j.ejogrb.2018.12.008CrossRefPubMed

64.

Verheijen EC, Critchley JA, Whitelaw DC, Tuffnell DJ (2005) Outcomes of pregnancies in women with pre-existing type 1 or type 2 diabetes, in an ethnically mixed population. BJOG 112(11):1500–1503. https://doi.org/10.1111/j.1471-0528.2005.00747.xCrossRefPubMed

65.

Wahabi HA, Esmaeil SA, Fayed A, Al-Shaikh G, Alzeidan RA (2012) Pre-existing diabetes mellitus and adverse pregnancy outcomes. BMC Res Notes 5:496. https://doi.org/10.1186/1756-0500-5-496CrossRefPubMedPubMedCentral

66.

Parellada CB, Asbjornsdottir B, Ringholm L, Damm P, Mathiesen ER (2014) Fetal growth in relation to gestational weight gain in women with type 2 diabetes: an observational study. Diabet Med 31(12):1681–1689. https://doi.org/10.1111/dme.12558CrossRefPubMedPubMedCentral

67.

Rodstrom K, Bengtsson C, Milsom I, Lissner L, Sundh V, Bjourkelund C (2003) Evidence for a secular trend in menopausal age: a population study of women in Gothenburg. Menopause 10(6):538–543. https://doi.org/10.1097/01.GME.0000094395.59028.0FCrossRefPubMed

68.

Thomas F, Renaud F, Benefice E, Td M, Guegan J-F (2001) International variability of ages at menarche and menopause: patterns and main determinants. Hum Biol 73(2):271–290. https://doi.org/10.1353/hub.2001.0029CrossRefPubMed

69.

Kok HS, van Asselt KM, van der Schouw YT, van der Tweel I, Peeters PH, Wilson PW, Pearson PL, Grobbee DE (2006) Heart disease risk determines menopausal age rather than the reverse. J Am Coll Cardiol 47(10):1976–1983. https://doi.org/10.1016/j.jacc.2005.12.066CrossRefPubMed

70.

Lopez-Lopez R, Huerta R, Malacara JM (1999) Age at menopause in women with type 2 diabetes mellitus. Menopause 6(2):174–178PubMed

71.

Gold EB, Bromberger J, Crawford S, Samuels S, Greendale GA, Harlow SD, Skurnick J (2001) Factors associated with age at natural menopause in a multiethnic sample of midlife women. Am J Epidemiol 153(9):865–874. https://doi.org/10.1093/aje/153.9.865CrossRefPubMed

72.

LeBlanc ES, Kapphahn K, Hedlin H, Desai M, Parikh NI, Liu S, Parker DR, Anderson M, Aroda V, Sullivan S, Woods NF, Waring ME, Lewis CE, Stefanick M (2017) Reproductive history and risk of type 2 diabetes mellitus in postmenopausal women: findings from the Women’s Health Initiative. Menopause 24(1):64–72. https://doi.org/10.1097/GME.0000000000000714CrossRefPubMedPubMedCentral

73.

Pandeya N, Huxley RR, Chung HF, Dobson AJ, Kuh D, Hardy R, Cade JE, Greenwood DC, Giles GG, Bruinsma F, Demakakos P, Simonsen MK, Adami HO, Weiderpass E, Mishra GD (2018) Female reproductive history and risk of type 2 diabetes: a prospective analysis of 126 721 women. Diabetes Obes Metab 20(9):2103–2112. https://doi.org/10.1111/dom.13336CrossRefPubMedPubMedCentral

74.

Brand JS, Onland-Moret NC, Eijkemans MJ, Tjonneland A, Roswall N, Overvad K, Fagherazzi G, Clavel-Chapelon F, Dossus L, Lukanova A, Grote V, Bergmann MM, Boeing H, Trichopoulou A, Tzivoglou M, Trichopoulos D, Grioni S, Mattiello A, Masala G, Tumino R, Vineis P, Bueno-de-Mesquita HB, Weiderpass E, Redondo ML, Sanchez MJ, Castano JM, Arriola L, Ardanaz E, Duell EJ, Rolandsson O, Franks PW, Butt S, Nilsson P, Khaw KT, Wareham N, Travis R, Romieu I, Gunter MJ, Riboli E, van der Schouw YT (2015) Diabetes and onset of natural menopause: results from the European prospective investigation into cancer and nutrition. Hum Reprod 30(6):1491–1498. https://doi.org/10.1093/humrep/dev054CrossRefPubMedPubMedCentral

75.

Lee JS, Hayashi K, Mishra G, Yasui T, Kubota T, Mizunuma H (2013) Independent association between age at natural menopause and hypercholesterolemia, hypertension, and diabetes mellitus: Japan nurses’ health study. J Atheroscler Thromb 20(2):161–169. https://doi.org/10.5551/jat.14746CrossRefPubMed

76.

Muka T, Oliver-Williams C, Kunutsor S, Laven JS, Fauser BC, Chowdhury R, Kavousi M, Franco OH (2016) Association of age at onset of menopause and time since onset of menopause with cardiovascular outcomes, intermediate vascular traits, and all-cause mortality: a systematic review and meta-analysis. JAMA Cardiol 1(7):767–776. https://doi.org/10.1001/jamacardio.2016.2415CrossRefPubMed

77.

Shen L, Song L, Li H, Liu B, Zheng X, Zhang L, Yuan J, Liang Y, Wang Y (2017) Association between earlier age at natural menopause and risk of diabetes in middle-aged and older Chinese women: the Dongfeng-Tongji cohort study. Diabetes Metab 43(4):345–350. https://doi.org/10.1016/j.diabet.2016.12.011CrossRefPubMed

78.

Wang M, Hu RY, Wang H, Gong WW, Wang CM, Xie KX, Chen ZM, Guo Y, Yu M, Li LM (2018) Age at natural menopause and risk of diabetes in adult women: findings from the China Kadoorie Biobank study in the Zhejiang area. J Diabetes Investig 9(4):762–768. https://doi.org/10.1111/jdi.12775CrossRefPubMed

79.

Golden SH, Dobs AS, Vaidya D, Szklo M, Gapstur S, Kopp P, Liu K, Ouyang P (2007) Endogenous sex hormones and glucose tolerance status in postmenopausal women. J Clin Endocrinol Metab 92(4):1289–1295. https://doi.org/10.1210/jc.2006-1895CrossRefPubMed

Titel: Reproductive health in women with type 2 diabetes mellitus
verfasst von: Doina Creţu
Simona Cernea
Corina Roxana Onea
Raluca-Monica Pop
Publikationsdatum: 01.09.2020
Verlag: Springer International Publishing
Erschienen in: Hormones / Ausgabe 3/2020
Print ISSN: 1109-3099
Elektronische ISSN: 2520-8721
DOI: https://doi.org/10.1007/s42000-020-00225-7

Leitlinien kompakt für die Innere Medizin

Mit medbee Pocketcards sicher entscheiden.

^{Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag}

Kostenlos registrieren

Neu im Fachgebiet Innere Medizin

„Jeder Fall von plötzlichem Tod muss obduziert werden!“

17.05.2024 Plötzlicher Herztod Nachrichten

Ein signifikanter Anteil der Fälle von plötzlichem Herztod ist genetisch bedingt. Um ihre Verwandten vor diesem Schicksal zu bewahren, sollten jüngere Personen, die plötzlich unerwartet versterben, ausnahmslos einer Autopsie unterzogen werden.

Hirnblutung unter DOAK und VKA ähnlich bedrohlich

17.05.2024 Direkte orale Antikoagulanzien Nachrichten

Kommt es zu einer nichttraumatischen Hirnblutung, spielt es keine große Rolle, ob die Betroffenen zuvor direkt wirksame orale Antikoagulanzien oder Marcumar bekommen haben: Die Prognose ist ähnlich schlecht.

Schlechtere Vorhofflimmern-Prognose bei kleinem linken Ventrikel

17.05.2024 Vorhofflimmern Nachrichten

Nicht nur ein vergrößerter, sondern auch ein kleiner linker Ventrikel ist bei Vorhofflimmern mit einer erhöhten Komplikationsrate assoziiert. Der Zusammenhang besteht nach Daten aus China unabhängig von anderen Risikofaktoren.

Semaglutid bei Herzinsuffizienz: Wie erklärt sich die Wirksamkeit?

17.05.2024 Herzinsuffizienz Nachrichten

Bei adipösen Patienten mit Herzinsuffizienz des HFpEF-Phänotyps ist Semaglutid von symptomatischem Nutzen. Resultiert dieser Benefit allein aus der Gewichtsreduktion oder auch aus spezifischen Effekten auf die Herzinsuffizienz-Pathogenese? Eine neue Analyse gibt Aufschluss.

Update Innere Medizin

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.

Newsletter bestellen

Die Highlights vom Kongress des American College of Cardiology 2024

Springer Medizin

Abstract

Bitte loggen Sie sich ein, um Zugang zu diesem Inhalt zu erhalten

Weitere Artikel der Ausgabe 3/2020

Thyroid hormones and the mechanisms of adaptation to cold

A closer look at NIFTP

Minding the gap between cortisol levels measured with second-generation assays and current diagnostic thresholds for the diagnosis of adrenal insufficiency: a single-center experience

Premature ovarian insufficiency in adolescence: a chance for early diagnosis?

Correction to: Effect of selenium supplementation on antioxidant markers: a systematic review and meta-analysis of randomized controlled trials