Sex-related differences in the long-term risk of microvascular complications by age at onset of type 1 diabetes

Diabetologia

Volumn 54, Issue 8, 2011, Pages 1992-1999

  Harjutsalo, V ^a,b,c   Maric, C ^d,e   Forsblom, C ^a,b   Thorn, L ^a,b   Waden J ^a,b   Groop, P H ^a,b,f  

^a UNIVERSITY OF HELSINKI   (Finland)

^b HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

^c NATIONAL PUBLIC HEALTH INSTITUTE   (Finland)

^d UNIVERSITY OF MISSISSIPPI SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF MISSISSIPPI MEDICAL CENTER   (United States)

^f BAKER IDI HEART AND DIABETES INSTITUTE   (Australia)

Author keywords

Age at onset; Diabetic nephropathy; End stage renal disease (ESRD); Hormonal changes; Proliferative retinopathy; Sex; Type 1 diabetes

Indexed keywords

SEX HORMONE BINDING GLOBULIN;

ADOLESCENT; ARTICLE; CHILD; CONTROLLED STUDY; DIABETIC NEPHROPATHY; DIABETIC RETINOPATHY; DISEASE DURATION; FEMALE; HUMAN; INCIDENCE; INFANT; INSULIN DEPENDENT DIABETES MELLITUS; KIDNEY FAILURE; MAJOR CLINICAL STUDY; MALE; MICROANGIOPATHY; ONSET AGE; PRESCHOOL CHILD; PRIORITY JOURNAL; RISK ASSESSMENT; RISK FACTOR; SCHOOL CHILD; SEX DIFFERENCE;

EID: 85028119143     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-011-2144-2     Document Type: Article

References (40)

1. 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 (Pubitemid 14200886)
2. Jacobsen P, Rossing K, Tarnow L et al (1999) Progression of diabetic nephropathy in normotensive type 1 diabetic patients. Kidney Int (Suppl) 71:S101-S105 (Pubitemid 29304825)
3. 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 (Pubitemid 29106911)
4. Svensson M, Nyström 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 (Pubitemid 44115350)
5. Raile K, Galler A, Hofer S et al (2007) Diabetic nephropathy in 27,805 children, adolescents, and adults with type 1 diabetes: effect of diabetes duration, A1C, hypertension, dyslipidemia, diabetes onset, and sex. Diabetes Care 30:2523-2528 (Pubitemid 47547787)
6. Harjutsalo V, Katoh S, Sarti C, Tajima N, Tuomilehto J (2004) Population-based assessment of familial clustering of diabetic nephropathy in type 1 diabetes. Diabetes 53:2449-2454 (Pubitemid 39145602)
7. Klein R, Knudtson MD, Lee KE, Gangnon R, Klein BE (2008) The Wisconsin Epidemiologic Study of Diabetic Retinopathy: XXII. The twenty-five-year progression of retinopathy in persons with type 1 diabetes. Ophthalmology 115:1859-1868
8. Donaghue KC, Fairchild JM, Craig ME et al (2003) Do all prepubertal years of diabetes duration contribute equally to diabetes complications? Diabetes Care 26:1224-1229 (Pubitemid 36929276)
9. 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
10. 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 (Pubitemid 23353032)
11. 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 (Pubitemid 34826627)
12. 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 (Pubitemid 36792475)
13. 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 (Pubitemid 24183775)
14. Klein R, Klein BE, Moss SE, Cruickshanks KJ (1998) The Wisconsin epidemiologic study of diabetic retinopathy: XVII. The 14-year incidence and progression of diabetic retinopathy and associated risk factors in type 1 diabetes. Ophthalmology 105:1801-1815 (Pubitemid 28509717)
15. 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 (Pubitemid 19284091)
16. 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 (Pubitemid 26010422)
17. The Epidemiology of Diabetes Intervention and Complications (EDIC) Study (2003) Sustained effect of intensive treatment of type 1 diabetes mellitus on development and progression ofdiabetic nephropathy: the Epidemiology of Diabetes Interventions and Complications (EDIC) Study. JAMA 290:2159-2167
18. Kauffman AS (2010) Coming of age in the kisspeptin era: sex differences, development, and puberty. Mol Cell Endocrinol 324:51-63
19. Harjutsalo V, Sjoberg L, Tuomilehto J (2008) Time trends in the incidence of type 1 diabetes in Finnish children: a cohort study. Lancet 371:1777-1782 (Pubitemid 351697953)
20. 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 (Pubitemid 47323762)
21. 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
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 (Pubitemid 46879019)
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 (Pubitemid 351342676)
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 (Pubitemid 41060978)
25. Monti MC, Lonsdale JT, Montomoli C, Montross R, Schlag E, Greenberg DA (2007) Familial risk factors for microvascular complications and differential male-female risk in a large cohort of American families with type 1 diabetes. J Clin Endocrinol Metab 92:4650-4655 (Pubitemid 350223440)
26. Harvey JN, Allagoa B (2004) The long-term renal and retinal outcome of childhood-onset type 1 diabetes. Diabet Med 21:26-31 (Pubitemid 38168025)
27. Mollsten A, Svensson M, Waernbaum I et al (2010) Cumulative risk, age at onset, and sex-specific differences for developing end-stage renal disease in young patients with type 1 diabetes: a nationwide population-based cohort study. Diabetes 59:1803-1808
28. El-Osta A, Brasacchio D, Yao D et al (2008) Transient high glucose causes persistent epigenetic changes and altered gene expression during subsequent normoglycemia. J Exp Med 205:2409-2417
29. Kaminsky Z, Wang SC, Petronis A (2006) Complex disease, gender and epigenetics. Ann Med 38:530-544 (Pubitemid 46292018)
30. Cummings EA, Sochett EB, Dekker MG, Lawson ML, Daneman D (1998) Contribution of growth hormone and IGF-I to early diabetic nephropathy in type 1 diabetes. Diabetes 47:1341-1346 (Pubitemid 28357014)
31. Amin R, Schultz C, Ong K et al (2003) Low IGF-I and elevated testosterone during puberty in subjects with type 1 diabetes developing microalbuminuria in comparison to normoalbuminuric control subjects: the Oxford Regional Prospective Study. Diabetes Care 26:1456-1461 (Pubitemid 36929178)
32. Maric C, Forsblom C, Thorn L, Waden J, Groop PH (2010) Association between testosterone, estradiol and sex hormone binding globulin levels in men with type 1 diabetes with nephropathy. Steroids 75:772-778
33. Haffner SM, Klein R, Moss SE, Klein BE (1993) Sex hormones and the incidence of severe retinopathy in male subjects with type I diabetes. Ophthalmology 100:1782-1786 (Pubitemid 24004598)
34. Haffner SM, Klein R, Dunn JF, Moss SE, Klein BE (1990) Increased testosterone in type I diabetic subjects with severe retinopathy. Ophthalmology 97:1270-1274 (Pubitemid 20353970)
35. Chaurasia RK, Singh R, Agrawal JK, Maurya OP (1993) Sex hormones and diabetic retinopathy. Ann Ophthalmol 25:227-230
36. Mankhey RW, Bhatti F, Maric C (2005) 17beta-Estradiol replacement improves renal function and pathology associated with diabetic nephropathy. Am J Physiol Renal Physiol 288:F399-F405 (Pubitemid 40105399)
37. 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 (Pubitemid 47345018)
38. 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 (Pubitemid 36759787)
39. Maric C, Sullivan S (2008) Estrogens and the diabetic kidney. Gend Med 5(Suppl A):S103-S113 (Pubitemid 351455235)
40. Xu Q, Wells CC, Garman JH, Asico L, Escano CS, Maric C (2008) Imbalance in sex hormone levels exacerbates diabetic renal disease. Hypertension 51:1218-1224 (Pubitemid 351398951)