Age at menarche and the risk of diabetic microvascular complications in patients with type 1 diabetes

Diabetologia

Volumn 59, Issue 3, 2016, Pages 472-480

  Harjutsalo, Valma ^a,b,c   Maric Bilkan, Christine ^d   Forsblom, Carol ^a,b   Groop, Per Henrik ^a,b,e  

^a UNIVERSITY OF HELSINKI   (Finland)

^b HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

^c NATIONAL PUBLIC HEALTH INSTITUTE   (Finland)

^d NATIONAL INSTITUTES OF HEALTH   (United States)

^e BAKER IDI HEART AND DIABETES INSTITUTE   (Australia)

Author keywords

Age at menarche; Age at onset of diabetes; Delayed menarche; Diabetic nephropathy; Diabetic retinopathy; Puberty; Type 1 diabetes

Indexed keywords

GLYCOSYLATED HEMOGLOBIN; HEMOGLOBIN A1C PROTEIN, HUMAN;

ADOLESCENT; ADULT; AGE; AGED; BLOOD; COMPLICATION; DIABETIC NEPHROPATHIES; DIABETIC RETINOPATHY; FEMALE; HUMAN; INSULIN DEPENDENT DIABETES MELLITUS; MALE; MENARCHE; METABOLISM; MIDDLE AGED; ONSET AGE; PHYSIOLOGY; RISK FACTOR; VERY ELDERLY; YOUNG ADULT;

ADOLESCENT; ADULT; AGE FACTORS; AGE OF ONSET; AGED; AGED, 80 AND OVER; DIABETES MELLITUS, TYPE 1; DIABETIC NEPHROPATHIES; DIABETIC RETINOPATHY; FEMALE; HEMOGLOBIN A, GLYCOSYLATED; HUMANS; MALE; MENARCHE; MIDDLE AGED; RISK FACTORS; YOUNG ADULT;

EID: 84957431305     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-015-3816-0     Document Type: Article

References (47)

1. Harjutsalo V, Maric C, Forsblom C et al (2011) Sex-related differences in the long-term risk of microvascular complications by age at onset of type 1 diabetes. Diabetologia 54:1992–1999
2. Finne P, Reunanen A, Stenman S, Groop PH, Gronhagen-Riska C (2005) Incidence of end-stage renal disease in patients with type 1 diabetes. JAMA 294:1782–1787
3. Hietala K, Harjutsalo V, Forsblom C, Summanen P, Groop PH (2010) Age at onset and the risk of proliferative retinopathy in type 1 diabetes. Diabetes Care 33:1315–1319
4. Krolewski AS, Warram JH, Christlieb AR, Busick EJ, Kahn CR (1985) The changing natural history of nephropathy in type I diabetes. Am J Med 78:785–794
5. Andersen AR, Christiansen JS, Andersen JK, Kreiner S, Deckert T (1983) Diabetic nephropathy in type 1 (insulin-dependent) diabetes: an epidemiological study. Diabetologia 25:496–501
6. Kostraba JN, Dorman JS, Orchard TJ et al (1989) Contribution of diabetes duration before puberty to development of microvascular complications in IDDM subjects. Diabetes Care 12:686–693
7. Lawson ML, Sochett EB, Chait PG, Balfe JW, Daneman D (1996) Effect of puberty on markers of glomerular hypertrophy and hypertension in IDDM. Diabetes 45:51–55
8. Svensson M, Nystrom L, Schon S, Dahlquist G (2006) Age at onset of childhood-onset type 1 diabetes and the development of end-stage renal disease: a nationwide population-based study. Diabetes Care 29:538–542
9. Schultz CJ, Konopelska-Bahu T, Dalton RN et al (1999) Microalbuminuria prevalence varies with age, sex, and puberty in children with type 1 diabetes followed from diagnosis in a longitudinal study. Oxford Regional Prospective Study Group. Diabetes Care 22:495–502
10. Schweiger BM, Snell-Bergeon JK, Roman R, McFann K, Klingensmith GJ (2011) Menarche delay and menstrual irregularities persist in adolescents with type 1 diabetes. Reprod Biol Endocrinol: 9:61
11. Rudberg S, Ullman E, Dahlquist G (1993) Relationship between early metabolic control and the development of microalbuminuria–a longitudinal study in children with type 1 (insulin-dependent) diabetes mellitus. Diabetologia 36:1309–1314
12. Codner E, Cassorla F (2009) Puberty and ovarian function in girls with type 1 diabetes mellitus. Horm Res 71:12–21
13. Mauer M, Drummond K (2002) The early natural history of nephropathy in type 1 diabetes: I. Study design and baseline characteristics of the study participants. Diabetes 51:1572–1579
14. Drummond KN, Kramer MS, Suissa S et al (2003) Effects of duration and age at onset of type 1 diabetes on preclinical manifestations of nephropathy. Diabetes 52:1818–1824
15. Janner M, Knill SE, Diem P, Zuppinger KA, Mullis PE (1994) Persistent microalbuminuria in adolescents with type I (insulin-dependent) diabetes mellitus is associated to early rather than late puberty. Results of a prospective longitudinal study. Eur J Pediatr 153:403–408
16. Codner E (2008) Estrogen and type 1 diabetes mellitus. Pediatr Endocrinol Rev 6:228–234
17. Deltsidou A (2010) Age at menarche and menstrual irregularities of adolescents with type 1 diabetes. J Pediatr Adolesc Gynecol 23:162–167
18. Lombardo F, Salzano G, Crisafulli G et al (2009) Menarcheal timing in intensively treated girls with type 1 diabetes mellitus. Nutr Metab Cardiovasc Dis: NMCD 19:35–38
19. Kjaer K, Hagen C, Sando SH, Eshoj O (1992) Epidemiology of menarche and menstrual disturbances in an unselected group of women with insulin-dependent diabetes mellitus compared to controls. J Clin Endocrinol Metab 75:524–529
20. Zhang H, Xia W, Yu Q et al (2008) Increasing incidence of type 1 diabetes in children aged 0-14 years in Harbin, China (1990-2000). Prim Care Diabetes 2:121–126
21. Soltesz G, Patterson CC, Dahlquist G (2007) Worldwide childhood type 1 diabetes incidence—what can we learn from epidemiology? Pediatr Diabetes 8(Suppl 6):6–14
22. Lammi N, Taskinen O, Moltchanova E et al (2007) A high incidence of type 1 diabetes and an alarming increase in the incidence of type 2 diabetes among young adults in Finland between 1992 and 1996. Diabetologia 50:1393–1400
23. Ostman J, Lonnberg G, Arnqvist HJ et al (2008) Gender differences and temporal variation in the incidence of type 1 diabetes: results of 8012 cases in the nationwide Diabetes Incidence Study in Sweden 1983-2002. J Intern Med 263:386–394
24. Thorn LM, Forsblom C, Fagerudd J et al (2005) Metabolic syndrome in type 1 diabetes: association with diabetic nephropathy and glycemic control (the FinnDiane study). Diabetes Care 28:2019–2024
25. Codner E, Soto N, Merino PM (2012) Contraception and pregnancy in adolescents with type 1 diabetes: a review. Pediatr Diabetes 13:108–123
26. Hastie TJ, Tibshirani RJ (1990) Generalized additive models. Chapman & Hall/CRC, London
27. Wood SN (2006) Generalized additive models: an introduction with R. Chapman & Hall/CRC, London
28. Wood S (2015) Mixed GAM computation vehicle with GCV/AIC/REML smoothness estimation. Available from https://cran.r-project.org/web/packages/mgcv/mgcv.pdf. Accessed 9 Nov 2015
29. Yeshaya A, Orvieto R, Dicker D, Karp M, Ben-Rafael Z (1995) Menstrual characteristics of women suffering from insulin-dependent diabetes mellitus. Int J Fertil Menopausal Stud 40:269–273
30. Picardi A, Cipponeri E, Bizzarri C, Fallucca S, Guglielmi C, Pozzilli P (2008) Menarche in type 1 diabetes is still delayed despite good metabolic control. Fertil Steril 90:1875–1877
31. Koponen P, Luoto R (2004) Reproductive health in Finland. Health 2000 Survey. Publications of National Public Health Institute, Helsinki [article in Finnish]
32. Abetew DF, Enquobahrie DA, Dishi M, Rudra CB, Miller RS, Williams MA (2011) Age at menarche, menstrual characteristics, and risk of preeclampsia. ISRN Obstet Gynecol 2011:472083
33. Janghorbani M, Mansourian M, Hosseini E (2014) Systematic review and meta-analysis of age at menarche and risk of type 2 diabetes. Acta Diabetol 51:519–528
34. Prentice P, Viner RM (2013) Pubertal timing and adult obesity and cardiometabolic risk in women and men: a systematic review and meta-analysis. Int J Obes 37:1036–1043
35. Codner E, Merino PM, Tena-Sempere M (2012) Female reproduction and type 1 diabetes: from mechanisms to clinical findings. Hum Reprod Update 18:568–585
36. Lane PH (2002) Diabetic kidney disease: impact of puberty. Am J Physiol Renal Physiol 283:F589–F600
37. Sjoberg L, Pitkaniemi J, Harjutsalo V et al (2011) Menopause in women with type 1 diabetes. Menopause 18:158–163
38. Mankhey RW, Bhatti F, Maric C (2005) 17β-Estradiol replacement improves renal function and pathology associated with diabetic nephropathy. Am J Physiol Renal Physiol 288:F399–F405
39. Keck M, Romero-Aleshire MJ, Cai Q, Hoyer PB, Brooks HL (2007) Hormonal status affects the progression of STZ-induced diabetes and diabetic renal damage in the VCD mouse model of menopause. Am J Physiol Renal Physiol 293:F193–F199
40. Kaja S, Yang SH, Wei J et al (2003) Estrogen protects the inner retina from apoptosis and ischemia-induced loss of Vesl-1L/Homer 1c immunoreactive synaptic connections. Invest Ophthalmol Vis Sci 44:3155–3162
41. Chabrolle C, Jeanpierre E, Tosca L, Rame C, Dupont J (2008) Effects of high levels of glucose on the steroidogenesis and the expression of adiponectin receptors in rat ovarian cells. Reprod Biol Endocrinol 6:11
42. Bestetti GE, Junker U, Locatelli V, Rossi GL (1987) Continuous subtherapeutic insulin counteracts hypothalamopituitary-gonadal alterations in diabetic rats. Diabetes 36:1315–1319
43. Wells CC, Riazi S, Mankhey RW, Bhatti F, Ecelbarger C, Maric C (2005) Diabetic nephropathy is associated with decreased circulating estradiol levels and imbalance in the expression of renal estrogen receptors. Gend Med 2:227–237
44. Towne B, Czerwinski SA, Demerath EW, Blangero J, Roche AF, Siervogel RM (2005) Heritability of age at menarche in girls from the Fels Longitudinal Study. Am J Phys Anthropol 128:210–219
45. Perry JR, Day F, Elks CE et al (2014) Parent-of-origin-specific allelic associations among 106 genomic loci for age at menarche. Nature 514:92–97
46. Sandholm N, McKnight AJ, Salem RM et al (2013) Chromosome 2q31.1 associates with ESRD in women with type 1 diabetes. J Am Soc Nephrol 24:1537–1543
47. Levey AS, Stevens LA, Schmid CH et al (2009) CKD-EPI (Chronic Kidney Disease Epidemiology Collaboration). A new equation to estimate glomerular filtration rate. Ann Intern Med 150:604–612