Diabetic nephropathy in children and adolescents

Pediatric Nephrology volume 23, pages507–525(2008)Cite this article

Abstract

Type 1 diabetes mellitus (T1DM) commonly occurs in childhood or adolescence, although the rising prevalence of type 2 diabetes mellitus (T2DM) in these age groups is now being seen worldwide. Diabetic nephropathy (DN) develops in 15–20% of subjects with T1DM and in similar or higher percentage of T2DM patients, causing increased morbidity and premature mortality. Although overt DN or kidney failure caused by either type of diabetes are very uncommon during childhood or adolescence, diabetic kidney disease in susceptible patients almost certainly begins soon after disease onset and may accelerate during adolescence, leading to microalbuminuria or incipient DN. Therefore, all diabetics warrant ongoing assessment of kidney function and screening for the earliest manifestations of renal injury. Pediatric health care professionals ought to understand about risk factors, strategy for prevention, method for screening, and treatment of early DN. This review considers each form of diabetes separately, including natural history, risk factors for development, screening for early manifestations, and strategy recommended for prevention and treatment of DN in children and adolescents.

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References

  1. 1.

    Daneman D (2006) Type 1 diabetes. Lancet 367:847–858

    CAS  PubMed  Google Scholar 

  2. 2.

    DIAMOND Project Group (2006) Incidence and trends of childhood type 1 diabetes worldwide 1990–1999. Diabet Med 23:857–866

    Google Scholar 

  3. 3.

    Gungor N, Hannon T, Libman I, Bacha F, Arslanian S (2005) Type 2 diabetes mellitus in youth: The complete picture to date. Pediatr Clin North Am 52:1579–1609

    PubMed  Google Scholar 

  4. 4.

    Singh R, Shaw J, Zimmet P (2004) Epidemiology of childhood type 2 diabetes in the developing world. Pediatr Diabetes 5:154–168

    CAS  PubMed  Google Scholar 

  5. 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

    CAS  PubMed  Google Scholar 

  6. 6.

    Ballard DJ, Humphrey LL, Melton LJ 3rd, Frohnert PP, Chu PC, O’Fallon WM, Palumbo PJ (1988) Epidemiology of persistent proteinuria in type II diabetes mellitus. Population-based study in Rochester, Minnesota. Diabetes 37:405–412

    CAS  PubMed  Google Scholar 

  7. 7.

    Rossing P, Hougaard P, Borch-Johnsen K, Parving HH (1996) Predictors of mortality in insulin dependent diabetes: 10 years observational follow up study. BMJ 313:779–784

    CAS  PubMed  PubMed Central  Google Scholar 

  8. 8.

    Harvey JN, Allagoa B (2004) The long-term renal and retinal outcome of childhood-onset type 1 diabetes. Diabet Med 21:26–31

    CAS  PubMed  Google Scholar 

  9. 9.

    Narayan KMV, Boyle JP, Thompson TJ, Sorensen SW, Williamson DF (2003) Lifetime risk for diabetes mellitus in the United States. JAMA 290:1884–1890

    CAS  PubMed  Google Scholar 

  10. 10.

    Bojestig M, Arnqvist HJ, Hermansson G, Karlberg B, Ludvigsson J (1994) Declining incidence of nephropathy in insulin-dependent diabetes mellitus. N Engl J Med 330:15–18

    CAS  PubMed  Google Scholar 

  11. 11.

    Harvey JN, Rizvi K, Craney L, Messenger J, Shah R, Meadows PA (2001) Population-based survey and analysis of trends in the prevalence of diabetic nephropathy in type 1 diabetes. Diabet Med 18:998–1002

    CAS  PubMed  Google Scholar 

  12. 12.

    Hovind P, Tarnow L, Rossing K, Eising S, Larsen N, Binder C, Parving HH (2003) Decreasing incidence of severe diabetic microangiopathy in type 1 diabetes. Diabetes Care 26:1258–1264

    PubMed  Google Scholar 

  13. 13.

    Skrivarhaug T, Bangstad HJ, Stene LC, Sandvik L, Hanssen KF, Joner G (2006) Low risk of overt nephropathy after 24 yr of childhood-onset type 1 diabetes mellitus (T1DM) in Norway. Pediatr Diabetes 7:239–246

    PubMed  Google Scholar 

  14. 14.

    Osterby R (1972) Morphometric studies of the peripheral glomerular basement membrane in early juvenile diabetes. I. Development of initial basement membrane thickening. Diabetologia 8:84–92

    CAS  PubMed  Google Scholar 

  15. 15.

    Schultz CJ, Neil HA, Dalton RN, Dunger DB; Oxford Regional Prospective Study Group (2000) Risk of nephropathy can be detected before the onset of microalbuminuria during the early years after diagnosis of type 1 diabetes. Diabetes Care 23:1811–1815

    CAS  PubMed  Google Scholar 

  16. 16.

    Schultz CJ, Konopelska-Bahu T, Dalton RN, Carroll TA, Stratton I, Gale EA, Neil A, Dunger DB (1999) Microalbuminuria prevalence varies with age, sex, and puberty in children with type 1 diabetes followed from diagnosis in a longitudinal study. Oxford Regional Study Group. Diabetes Care 22:495–502

    CAS  PubMed  Google Scholar 

  17. 17.

    Jones CA, Leese GP, Kerr S, Bestwick K, Isherwood DI, Vora JP, Hughes DA, Smith C (1998) Development and progression of microalbuminuria in a clinic sample of patients with insulin dependent diabetes mellitus. Arch Dis Child 78:518–523

    CAS  PubMed  PubMed Central  Google Scholar 

  18. 18.

    Barkai L, Vamosi I, Lukacs K (1998) Enchanced progression of urinary albumin excretion in IDDM during puberty. Diabetes Care 21:1019–1023

    CAS  PubMed  Google Scholar 

  19. 19.

    Drummond K, Mauer M; International Diabetic Nephropathy Study Group (2002) The early natural history of nephropathy in type 1 diabetes. II. Early renal structural changes in type 1 diabetes. Diabetes 51:1580–1587

    CAS  PubMed  Google Scholar 

  20. 20.

    Mortensen HB, Marinelli K, Norgaard K, Main K, Kastrup KW, Ibsen KK, Villumsen J, Parving HH (1990) A nation-wide cross-sectional study of urinary albumin excretion rate, arterial blood pressure and blood glucose control in Danish children with type 1 diabetes mellitus. Danish Study Group on Diabetes in Childhood. Diabet Med 7:887–897

    CAS  Google Scholar 

  21. 21.

    Daneman D (2005) Early diabetes-related complications in adolescents. Horm Res 63:75–85

    CAS  PubMed  Google Scholar 

  22. 22.

    Lane P, Steffes M, Mauer M (1991) The role of the pediatric nephrologist in the care of children with diabetes mellitus. Pediatr Nephrol 5:359–363

    CAS  PubMed  Google Scholar 

  23. 23.

    Mathiesen ER, Ronn B, Storm B, Foght V, Deckert T (1995) The natural course of microalbuminuria in insulin-dependent diabetes mellitus. A 10 year prospective study. Diabet Med 12:482–487

    CAS  PubMed  Google Scholar 

  24. 24.

    Mogensen CE (1997) How to protect the kidney in diabetic patients with special references to IDDM. Diabetes 46(Suppl 2):104–111

    Google Scholar 

  25. 25.

    Chiarelli F, Verrotti A, Morgese G (1995) Glomerular hyperfiltration increases the risk of developing microalbuminuria in diabetic children. Pediatr Nephrol 9:154–158

    CAS  PubMed  Google Scholar 

  26. 26.

    Dahlquist G, Stattin EL, Rudberg S (2001) Urinary albumin excretion rate in the prediction of diabetic nephropathy; a long-term follow-up study of childhood onset type-1 diabetic patients. Nephrol Dial Transplant 16:1382–1386

    CAS  PubMed  Google Scholar 

  27. 27.

    Amin R, Turner C, van Aken S, Konopelska-Bahu T, Watts A, Lindsell DR, Dalton RN, Dunger DB (2005) The relationship between microalbuminuria and glomerular filtration rate in young type 1 diabetic subjects: The oxford regional prospective study. Kidney Int 68:1740–1749

    PubMed  Google Scholar 

  28. 28.

    Zerbini G, Bonfanti R, Meschi F, Bognetti E, Paesano PL, Gianolli L, Querques M, Maestroni A, Calori G, DelMaschio A, Fazio F, Luzi L, Chiumello G (2006) Persistent renal hypertrophy and faster decline of glomerular filtratio rate precede the development of microalbuminuria in type 1 diabetes. Diabetes 55:2620–2625

    CAS  PubMed  Google Scholar 

  29. 29.

    Gorman D, Sochett E, Daneman D (1999) The natural history of microalbuminuria in adolescents with type I diabetes. J Pediatr 134:333–337

    CAS  Google Scholar 

  30. 30.

    Twyman S, Rowe D, Mansell P, Schapira D, Betts P, Leatherdale B (2001) Longitudinal study of urinary albumin excretion in young diabetic patients—Wessex diabetic nephropathy project. Diabet Med 18:402–408

    CAS  PubMed  Google Scholar 

  31. 31.

    Lurbe E, Redon J, Kesani A, Pascual JM, Tacons J, Alvarez V, Batlle D (2002) Increase in nocturnal BP and progression to microalbuminuria in type 1 diabetes. N Engl J Med 347:797–805

    CAS  Google Scholar 

  32. 32.

    Caramori ML, Fioretto P, Mauer M (2003) Low glomerular filtration rate in normoalbuminuric type 1 diabetic patients. An indicator of more advanced glomerular lesions. Diabetes 52:1036–1040

    CAS  PubMed  Google Scholar 

  33. 33.

    Chobanian MC, Chevalier RF, Sturgill BC, Bolton WK (1984) Early onset of clinical diabetic nephropathy in children-a new subgroup? Int J Pediatr Nephrol 5:23–29

    CAS  PubMed  Google Scholar 

  34. 34.

    Ellis EN, Pysher TJ (1993) Renal disease in adolescents with type I diabetes mellitus: a report of the southwest pediatric nephrology study group. Am J Kidney Dis 22:783–790

    CAS  PubMed  Google Scholar 

  35. 35.

    Francis J, Rose SJ, Rafaat F, Milford DV (1997) Early onset of diabetic nephropathy. Arch Dis Child 77:524–525

    CAS  PubMed  PubMed Central  Google Scholar 

  36. 36.

    Steffes MW, Osterby R, Chavers B, Mauer SM (1989) Mesangial expansion as a central mechanism for loss of kidney function in diabetic patients. Diabetes 38:1077–1081

    CAS  PubMed  Google Scholar 

  37. 37.

    Osterby R (1992) Glomerular structural changes in type 1 (insulin-dependent) diabetes mellitus: causes, consequences and prevention. Diabetologia 35:803–812

    CAS  PubMed  Google Scholar 

  38. 38.

    Mauer SM, Steffes MW, Ellis EN, Sutherland DER, Brown DM, Goetz PC (1984) Structural-functional relationships in diabetic nephropathy. J Clin Invest 74:1143–1155

    CAS  PubMed  PubMed Central  Google Scholar 

  39. 39.

    Ellis EN, Warady BA, Wood EG, Hassanein R, Richardson WP, Lane PH, Howard C, Kemp SF, Aceto T, Garibaldi L, Wiegmann TB, Savin VJ (1997) Renal structural-functional relationships in early diabetes mellitus. Pediatr Nephrol 11:584–591

    CAS  PubMed  Google Scholar 

  40. 40.

    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

    CAS  PubMed  Google Scholar 

  41. 41.

    Perrin NE, Torbjornsdotter TB, Jaremko GA, Berg UB (2004) Follow up of kidney biopsies in normoalbuinuric patients with type 1 diabetes. Pediatr Nephrol 19:1004–1013

    Google Scholar 

  42. 42.

    Schena FP, Gesualdo L (2005) Pathogenetic mechanisms of diabetic nephropathy. J Am Soc Nephrol 16:S30–S33

    CAS  PubMed  Google Scholar 

  43. 43.

    Rich SS (2006) Genetics of diabetes and its complications. J Am Soc Nephrol 17:353–360

    CAS  PubMed  Google Scholar 

  44. 44.

    Bangstad HJ, Osterby R, Dahl-Jorgensen K, Berg KJ, Hartmann A, Hanssen KF (1994) Improvement of blood glucose control in IDDM patients retards the progression of morphological changes in early diabetic nephropathy. Diabetologia 37:483–490

    CAS  PubMed  Google Scholar 

  45. 45.

    Caramori ML, Mauer M (2003) Diabetes and nephropathy. Curr Opin Nephrol Hypertens 12:273–282

    CAS  PubMed  Google Scholar 

  46. 46.

    Brownlee M (2001) Biochemistry and molecular cell biology of diabetic complications. Nature 414:813–820

    CAS  PubMed  Google Scholar 

  47. 47.

    DCCT Research Group (1993) The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. N Engl J Med 329:977–986

    Google Scholar 

  48. 48.

    DCCT Research Group (1994) Effect of intensive diabetes treatment on the development and pregression of long-term complications in adolescents with insulin-dependent diabetes mellitus. Diabetes Control and Complications Trial. J Pediatr 125:177–188

    Google Scholar 

  49. 49.

    DCCT Research Group (1995) The effect of intensive therapy on the development and progression of diabetic nephropathy in the diabetes control and complications trial. Kidney Int 47:1703–1720

    Google Scholar 

  50. 50.

    DCCT/EDIC Research Group (2000) Retinopathy and nephropathy in patients with type 1 diabetes four years after a trial of intensive therapy. N Engl J Med 342:381–389

    Google Scholar 

  51. 51.

    DCCT/EDIC Research Group (2002) Effect of intensive therapy on the microvascular complications of type 1 diabetes mellitus. JAMA 287:2563–2569

    Google Scholar 

  52. 52.

    DCCT/EDIC Research Group (2003) Sustained effect of intensive treatment of type 1 diabetes mellitus on development and progression of diabetic nephropathy. JAMA 290:2159–2167

    Google Scholar 

  53. 53.

    DCCT/EDIC Research Group (2001) Beneficial effects of intensive therapy of diabetes during adolescence: Outcomes after the conclusion of the Diabetes Control and Complications Trial (DCCT). J Pediatr 139:804–812

    Google Scholar 

  54. 54.

    DCCT Research Group (1996) The absence of a glycemic threshold for the development of long-term complications: the perspective of the diabetes control and complications trial. Diabetes 45:1289–1298

    Google Scholar 

  55. 55.

    Krolewski AS, Laffel LM, Krolewski M, Quinn M, Warram JH (1995) Glycosylated hemoglobin and the risk of microalbuminuria in patients with insulin-dependent diabetes mellitus. N Engl J Med 332:1251–1255

    CAS  PubMed  Google Scholar 

  56. 56.

    Orchard TJ, Dorman JS, Maser RE, Becker DJ, Drash AL, Ellis D, LaPorte RE, Kuller LH (1990) Prevalence of complications in IDDM by sex and duration: Pittsburgh epidemiology of diabetes complications study II. Diabetes 39:1116–1124

    CAS  PubMed  Google Scholar 

  57. 57.

    Zhang L, Krzentowski G, Albert A, Lefebvre J (2003) Factors predictive of nephropathy in DCCT type 1 diabetic patients with good or poor metabolic control. Diabet Med 20:580–585

    CAS  PubMed  Google Scholar 

  58. 58.

    Davies AG, Price DA, Postlethwaite RJ, Addison GM, Burn JL, Fielding BA (1985) Renal function in diabetes mellitus. Arch Dis Child 60:299–304

    CAS  PubMed  PubMed Central  Google Scholar 

  59. 59.

    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

    CAS  PubMed  Google Scholar 

  60. 60.

    Olsen BS, Sjolie AK, Hougaard P, Johannesen J, Marinelli K, Jacobsen BB, Mortensen HB; Danish Study Group of Diabetes in Childhood (2004) The significance of the prepubertal diabetes duration for the development of retinopathy and nephropathy in patients with type 1 diabetes. J Diabetes Compl 18:160–164

    Google Scholar 

  61. 61.

    Svensson M, Eriksson JW, Dahlquist G (2004) Early glycemic control, age at onset, and development of microvascular complications in childhood-onset type diabetes. Diabetes Care 27:955–962

    PubMed  Google Scholar 

  62. 62.

    Sochett E, Daneman D (1999) Early diabetes-related complications in children and adolescents with type 1 diabetes. Endocrinol Metab Clin North Am 128:865–882

    Google Scholar 

  63. 63.

    Kostraba JN, Dorman JS, Orchard TJ, Becker DJ, Ohki Y, Ellis D, Doft BH, Lobes LA, LaPorte RE, Drash AL (1989) Contribution of diabetes duration before puberty to development of microvascular complications in IDDM subjects. Diabetes Care 12:686–693

    CAS  PubMed  Google Scholar 

  64. 64.

    Donaghue KC, Fung AT, Hung S, Fairchild J, King J, Chan A, Howard NJ, Silink M (1997) The effect of prepubertal diabetes duration on diabetes microvascular complications in early and late adolescence. Diabetes Care 20:77–80

    CAS  PubMed  Google Scholar 

  65. 65.

    Holl W, Grabert M, Thon A, Heinze E (1999) Urinary excretion of albumin in adolescents with type 1 diabetes. Diabetes Care 22:1555–1560

    CAS  PubMed  Google Scholar 

  66. 66.

    Donaghue KC, Fairchild JM, Craig ME, Chan AK, Hing S, Cutler LR, Howard LR, Silink M (2003) Do all prepubertal years of diabetes duration contribute equally to diabetes complications? Diabetes Care 26:1224–1229

    PubMed  Google Scholar 

  67. 67.

    Gallego PH, Bulsara MK, Frazer F, Lafferty AR, Davis EA, Jones TW (2006) Prevalence and risk factors for microalbuminuria in a population-based sample of children and adolescents with T1DM in Western Australia. Pediatr Diabetes 7:165–172

    PubMed  Google Scholar 

  68. 68.

    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. Diabetes Care 29:538–542

    PubMed  Google Scholar 

  69. 69.

    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

    CAS  PubMed  Google Scholar 

  70. 70.

    Lane PH (2002) Diabetic kidney disease: impact of puberty. Am J Physiol 283:589–600

    Google Scholar 

  71. 71.

    Amin R, Schultz C, Ong K, Frystyk J, Dalton RN, Perry L, Orskov H, Dunger DB (2003) Low IGF-I and elevated testosterone during puberty in subjects with type 1 diabetes developing microalbuminuria in comparison to normoalbuminuric control subjects. Diabetes Care 26:1456–1461

    CAS  PubMed  Google Scholar 

  72. 72.

    Amin R, Williams RM, Frystyk J, Ummpleby M, Matthewst D, Orskov H, Dalton RN, Dunger DB (2005) Increasing urine albumin excretion is associated with growth hormone hypersecretion and reduced clearance of insulin in adolescents and young adults with type 1 diabetes: The Oxford Regional Prospective Study. Clin Endocrinol 62:137–144

    CAS  Google Scholar 

  73. 73.

    Stone ML, Craig ME, Chan AK, Lee JW, Verge CF, Donaghue KC (2006) Natural history and risk factors for microalbuminuria in adolescents with type 1 diabetes. Diabetes Care 29:2072–2077

    CAS  PubMed  Google Scholar 

  74. 74.

    Moran A, Jacobs D, Steinberger J, Hong C, Prineas R, Luepker S, Sinaiko A (1999) Insulin resistance during puberty. Diabetes 48:2039–2044

    CAS  PubMed  Google Scholar 

  75. 75.

    Yip J, Mattock MB, Morocutti A, Sethi M, Trevisan R, Viberty GC (1993) Insulin resistance in insulin-dependent diabetic patients with microalbuminuria. Lancet 342:883–887

    CAS  PubMed  Google Scholar 

  76. 76.

    Orchard TJ, Chang YF, Ferrel RE, Petro N, Ellis DE (2002) Nephropathy in type 1 diabetes. A manifestation of insulin resistance and multiple genetic susceptibilities? Kidney Int 62:963–970

    CAS  PubMed  Google Scholar 

  77. 77.

    Janner M, Eberhard KS, Diem P, Zuppinger KA, Mullis PE (1994) Persisting microalbuminuria in adolescents with type 1 (insulin-dependent) diabetes mellitus is associated to early rather than late puberty. Eur J Pediatr 153:403–408

    CAS  PubMed  Google Scholar 

  78. 78.

    Hovind P, Tarnow L, Rossing P, Jensen BR, Graae M, Torp I, Binder C, Parving HH (2004) Predictors for the development of microalbuminuria and macroalbuminuria in patients with type 1 diabetes: inception cohort study. BMJ 328:1105–1109

    PubMed  PubMed Central  Google Scholar 

  79. 79.

    Caramori ML, Fioretto P, Mauer M (2000) The Need for Early Predictors of Diabetic Nephropathy Risk. Diabetes 49:1399–1408

    CAS  PubMed  Google Scholar 

  80. 80.

    Drummond KM, Kramer MS, Suissa S, Levy-Marchal C, Dell Aniello S, Mauer M (2003) Effects of duration and age at onset of type 1 diabetes on preclinical manifestations of nephropathy. Diabetes 52:1818–1824

    CAS  PubMed  Google Scholar 

  81. 81.

    Microalbuminuria Collaborative Study Group (1999) Predictors of the development of microalbuminuria in patients with type 1 diabetes mellitus: a seven-year prospective study. Diabet Med 16:918–925

    Google Scholar 

  82. 82.

    Barzilay J, Warram JH, Laffel LM, Canessa M, Krolewski AS (1992) Predisposition to hypertension: Risk factor for nephropathy and hypertension in IDDM. Kidney Int 41:723–730

    CAS  PubMed  Google Scholar 

  83. 83.

    Microalbuminuria Collaborative Study Group, UK (1993) Risk factors for the development of microalbuminuria in insulin-dependent diabetic patients: a cohort study. BMJ 306:1235–1239

    Google Scholar 

  84. 84.

    Norgaard K, Feldt-Rasmussen BF, Borch-Johnsen K, Saelan H, Deckert T (1990) Prevalence of hypertension in type 1 (insulin-dependent) diabetes mellitus. Diabetologia 33:407–410

    CAS  PubMed  Google Scholar 

  85. 85.

    Mathiesen ER, Saurbrey N, Hommel E, Parving HH (1986) Prevalence of microalbuminuria in children with type 1 (insulin-dependent) diabetes mellitus. Diabetologia 29:640–643

    CAS  PubMed  Google Scholar 

  86. 86.

    Virdis R, Vanelli M, Street M, Zampolli M, De Fanti A, Cantoni S, Vittorangeli R, Pezzarossa A, Giovannelli G, Terzi C (1994) Blood pressure tracking in adolescents with insulin-dependent diabetes mellitus. J Hum Hypertens 8:313–317

    CAS  PubMed  Google Scholar 

  87. 87.

    Schultz CJ, Neil HA, Dalton RN, Konopelska BT, Dunger DB (2001) Blood pressure does not rise before the onset of microalbuminuria in children followed from diagnosis of type 1 diabetes. Oxford Regional Prospective Study Group. Diabetes Care 24:555–560

    CAS  PubMed  Google Scholar 

  88. 88.

    Moore WV, Donaldson DL, Chonko AM, Ideus P, Wiegmann TB (1992) Ambulatory blood pressure in type 1 diabetes mellitus. Comparison to presence of incipient nephropathy in adolescents and young adults. Diabetes 41:1035–1041

    CAS  PubMed  Google Scholar 

  89. 89.

    Sochett EB, Poon I, Balfe W, Daneman D (1998) Ambulatory blood pressure monitoring in insulin-dependent diabetes mellitus adolescents with and without microalbuminuria. J Diabetes Complications 12:18–23

    CAS  PubMed  Google Scholar 

  90. 90.

    Holl W, Pavlovic M, Heinze E, Thon A (1999) Circadian blood pressure during the early course of type 1 diabetes. Diabetes Care 22:1151–1157

    CAS  PubMed  Google Scholar 

  91. 91.

    Lopes CA, Lerario AC, Mion D Jr, Koch V, Wajchenberg BL, Rosenbloom AL (2002) Ambulatory blood pressure monitoring (ABPMA) in normotensive adolescents with type 1 diabetes. Pediatr Diabetes 3:31–36

    PubMed  Google Scholar 

  92. 92.

    Lafferty AR, Werther GA, Clarke CF (2000) Ambulatory blood pressure, microalbuminuria, and autonomic neuropathy in adolescents with type 1 diabetes. Diabetes Care 23:533–538

    CAS  PubMed  Google Scholar 

  93. 93.

    Garg SK, Chase HP, Rothman RL, Osberg I, Carmain JA (1997) 24-hour ambulatory blood pressure and renal disease in young subjects with type 1 diabetes. J Diabetes Complications 11:263–267

    CAS  PubMed  Google Scholar 

  94. 94.

    Gallego PH, Gilbey AJ, Grant MT, Bulsara MK, Byme GC, Jones TW, Frazer FL (2005) Early changes in 24-hour ambulatory blood pressure are associated with high normal albumin excretion rate in children with type 1 diabetes mellitus. J Pediatr Endocrinol Metab 18:879–885

    CAS  PubMed  Google Scholar 

  95. 95.

    Lurbe E, Sorof JM, Daniels SR (2004) Clinical and research aspects of ambulatory blood pressure monitoring in children. J Pediatr 144:7–16

    Google Scholar 

  96. 96.

    Torbjornsdotter TB, Jaremko GA, Berg UB (2001) Ambulatory blood pressure and heart rate in relation to kidney structure and metabolic control in adolescents with type I diabetes. Diabetologia 44:865–873

    CAS  PubMed  Google Scholar 

  97. 97.

    Torbjornadotter TB, Jaremko GA, Berg UB (2004) Nondipping and its relation to glomerulopathy and hyperfiltration in adolescents with type 1 diabetes. Diabetes Care 27:510–516

    Google Scholar 

  98. 98.

    Darcan S, Goksen D, Mir S, Serdaroglu E, Buyukinan M, Coker M, Berdeli A, Kose T, Cura A (2006) Alterations of blood pressure in type 1 diabetic children and adolescents. Pediatr Nephrol 21:672–676

    PubMed  Google Scholar 

  99. 99.

    Chiareli F, Santilli F (2005) Diabetic nephropathy in children and adolescents. In: Chiarelli F, Dahl-Jorgensen K, Kiess W (eds): Diabetes in childhood and adolescence. Pediatr Adolesc Med Basel, Karger, vol 10, pp 225–258

  100. 100.

    Hargrave DR, Mc Master C, O'Hare MM, Carson DJ (1999) Tobacco smoke exposure in children and adolescents with diabetes mellitus. Diabet Med 16:31–34

    CAS  PubMed  Google Scholar 

  101. 101.

    Holl RW, Grabert M, Heinze E, Debatin KM (1998) Objective assessment of smoking habits by urinary cotinine measurement in adolescents and young adults with type I diabetes: Reliability of cigarette consumption and relationship to urinary albumin excretion. Diabetes Care 21:787–791

    CAS  PubMed  Google Scholar 

  102. 102.

    Chase HP, Marshall G, Garg SK, Harris S, Osberg I (1991) Borderline increases in albumin excretion rate and the relation to glycaemic control in subjects with type 1 diabetes. Clin Chem 37:2048–2052

    CAS  PubMed  Google Scholar 

  103. 103.

    Chaturvedi N, Stephenson JM, Fuller JH (1995) The relationship between smoking and microvascular complications in the EURODIAB Complications Study. Diabetes Care 18:785–792

    CAS  PubMed  Google Scholar 

  104. 104.

    Orth SR (2002) Smoking and the kidney. J Am Soc Nephrol 13:1663–1672

    CAS  PubMed  Google Scholar 

  105. 105.

    Sawicki PT, Didjurgeit U, Muhlhauser I, Bender R, Heinemann L, Berger M (1994) Smoking is associated with progression of diabetic nephropathy. Diabetes Care 17:1216–1231

    Google Scholar 

  106. 106.

    Scott LJ, Warram JH, Hanna LS, Laffel LM, Ryan L, Krolewski AS (2001) A nonlinear effect of hyperglycemia and current cigarette smoking as major determinants of the onset of microalbuminuria in type 1 diabetes. Diabetes 50:2842–2849

    CAS  PubMed  Google Scholar 

  107. 107.

    Orth SR, Schroeder T, Ritz E, Ferrari P (2005) Effects of smoking on renal function in patients with type 1 and type 2 diabetes mellitus. Nephrol Dial Transplant 20:2414–2419

    PubMed  Google Scholar 

  108. 108.

    Couper JJ, Staples AJ, Cocciolone R, Nairn J, Badcock N, Henning P (1994) Relationship of smoking and albuminuria in children with insulin-dependent diabetes. Diabet Med 11:666–669

    CAS  PubMed  Google Scholar 

  109. 109.

    Bangstad HJ, Osterby R, Rundberg S, Hartmann A, Brabrand K, Hanssen KF (2002). Kidney function and glomerulopathy over 8 years in young patients with type I (insulin-dependent) diabetes mellitus and microalbuminuria. Diabetologia 45:253–261

    CAS  PubMed  Google Scholar 

  110. 110.

    Rippin JD, Patel A, Bain SC (2001) Genetics of diabetic nephropathy. Best Pract Res Clin Endocrinol Metab 15:345–358

    CAS  PubMed  Google Scholar 

  111. 111.

    Seaquist ER, Goetz FC, Rich S, Barbosa J (1989) Familial clustering of diabetic kidney disease. Evidence for genetic susceptibility to diabetic nephropathy. N Engl J Med 320:1161–1165

    CAS  PubMed  Google Scholar 

  112. 112.

    Quinn M, Angelico MC, Warram JH, Krolewski AS (1996) Familial factors determine the development of diabetic nephropathy in patients with IDDM. Diabetologia 39:940–945

    CAS  PubMed  Google Scholar 

  113. 113.

    DCCT Research Group (1997) Clustering of long-term complications in families with diabetes in the diabetes control and complications trial. Diabetes 46:1829–1839

    Google Scholar 

  114. 114.

    Fioretto P, Steffes MW, Barbosa J, Rich SS, Miller ME, Mauer M (1999) Is diabetic nephropathy inherited? Studies of glomerular structure in type 1 diabetic sibling pairs. Diabetes 48:865–869

    CAS  PubMed  Google Scholar 

  115. 115.

    Roglic G, Colhoun HM, Stevens LK, Lemkes HH, Manes C, Fuller JH (1998) Parental history of hypertension and parental history of diabetes and microvascular complications in insulin-dependent diabetes mellitus: the EURODIAB IDDM complications study. Diabet Med 15:418–426

    CAS  PubMed  Google Scholar 

  116. 116.

    Rudberg S, Stattin EL, Dahlquist G (1998) Familial and perinatal risk factors for micro- and macroalbuminuria in young IDDM patients. Diabetes 47:1121–1126

    CAS  PubMed  Google Scholar 

  117. 117.

    Fagerudd JA, Pettersson-Fernholm KJ, Gronhagen-Riska C, Groop PH (1999) The impact of a family history of type II (non-insulin-dependent) diabetes mellitus on the risk of diabetic nephropathy in patients with type I (insulin-dependent) diabetes mellitus. Diabetologia 42:519–526

    CAS  PubMed  Google Scholar 

  118. 118.

    Mangili R, Bending JJ, Scott G, Li LK, Gupta A, Viberti GC (1988) Increased sodium-lithium countertransport activity in red cells of patients with insulin-dependent diabetes and nephropathy. N Engl J Med 318:146–150

    CAS  PubMed  Google Scholar 

  119. 119.

    Lurbe A, Fioretto P, Barbosa J, Mauer M, LaPointe MS, Battle D (1996) Growth phenotype of cultured skin fibroblasts from IDDM patients with and without nephropathy and overactivity of the Na/H antiporter. Kidney Int 50:1684–1693

    CAS  PubMed  Google Scholar 

  120. 120.

    Fujisawa T, Ikegami H, Kawaguchi Y, Hamada Y, Vesta H, Shintani M, Fukuda M, Ogihara T (1998) Meta-analysis of association of insertion/deletion polymorphism of angiotensin I-converting enzyme gene with diabetic nephropathy and retinopathy. Diabetologia 41:47–53

    CAS  PubMed  Google Scholar 

  121. 121.

    Hadjadj S, Belloum R, Bouhanick B Gallois Y, Guilloteau G, Chatellier G, Alhenc-Gelas F, Marre M (2001) Prognostic value of angiotensin-I converting enzyme I/D polymorphism for nephropathy in type I diabetes mellitus: a prospective study. J Am Soc Nephrol 12:541–549

    CAS  PubMed  Google Scholar 

  122. 122.

    Penno G, Chaturvedi N, Talmud PJ, Cotroneo P, Manto A, Nannigieri M, Luong LA, Fuller JH (1998) Effect of angiotensin-converting enzyme (ACE) gene polymorphism on progression of renal disease and the influence of ACE inhibition in IDDM patients. Diabetes 47:1507–1511

    CAS  PubMed  Google Scholar 

  123. 123.

    Jacobsen P, Andersen S, Jensen BR, Parving HH (2003) Additive effect of ACE-inhibition and angiotensin II receptor blockade in type 1 diabetic patients with diabetic nephropathy. J Am Soc Nephrol 14:992–999

    CAS  PubMed  Google Scholar 

  124. 124.

    Boright A, Patterson AD, Mirea L, Bull S, Mowjoodi A, Scherer SW, Zinman B; DCC/EDIC Research Group (2005) Genetic variation at the ACE gene is associated with persistent microalbuminuria and severe nephropathy in type 1 diabetes. Diabetes 54:1238–1244

    CAS  PubMed  PubMed Central  Google Scholar 

  125. 125.

    Moczulski DK, Rogus JJ, Antonellis A, Warram JH, Krolewski AS (1998) Major susceptibility locus for nephropathy in type 1 diabetes on chromosome 3q: Results of a novel discordant sib pairs analysis. Diabetes 147:1164–1169

    Google Scholar 

  126. 126.

    Osterholm AM, He B, Pitkaniemi J, Albinsson L, Berg T, Sarti C, Tuomilehto J, Tryggvason K (2007) Genome-wide scan for type 1 diabetic nephropathy in the Finnish population reveals suggestive linkage to a single locus on chromosome 3q. Kidney Int 71:140–145

    CAS  PubMed  Google Scholar 

  127. 127.

    Caramori ML, Fioretto P, Mauer M (2006) Enhancing the predictive value of urinary albumin for diabetic nephropathy. J Am Soc Nephrol 17:339–352

    CAS  PubMed  Google Scholar 

  128. 128.

    Jenkins AJ, Lyons TJ, Zheng D, Otvos JD, Lackland DT, McGee D, Garvey WT, Klein RL; DCCT/EDIC Research Group (2003) Lipoproteins in the DCCT/EDIC cohort: association with diabetic nephropathy. Kidney Int 64:817–828

    CAS  PubMed  Google Scholar 

  129. 129.

    Hovind P, Rossing P, Tarnow L, Smidt VM, Parving H-H (2001) Progression of diabetic nephropathy. Kidney Int 59:702–709

    CAS  PubMed  Google Scholar 

  130. 130.

    Danne T, Kordonouri O, Hovener G, Weber B (1997) Diabetic angiopathy in children. Diabet Med 14:1012–1025

    CAS  PubMed  Google Scholar 

  131. 131.

    Perkins BA, Ficociello LH, Silva KH, Finkelstein DM, Warram JH, Krolewski AS (2003) Regression of microalbuminuria in type 1 diabetes. N Engl J Med 348:2285–2293

    CAS  PubMed  Google Scholar 

  132. 132.

    Lervang HH, Jensen S, Brochner-Mortensen J, Ditzel J (1988) Early glomerular hyperfiltration and the development of late nephropathy in type 1 (insulin-dependent) diabetes mellitus. Diabetologia 31:723–729

    CAS  PubMed  Google Scholar 

  133. 133.

    Steinke JM, Sinaikko AR, Kramer MS, Suissa S, Chavers BM, Mauer M; International Diabetic Nephropathy Study Group (2005) The early natural history of nephropathy in type 1 diabetes. Diabetes 54:2164–2171

    CAS  PubMed  Google Scholar 

  134. 134.

    Brenner BM, Chertow GM (1994) Congenital oligonephropathy and the etiology of adult hypertension and progressive renal injury. Am J Kidney Dis 23:171–175

    CAS  Google Scholar 

  135. 135.

    Rossing P, Tarnow L, Nielsen FS, Boelskifte S, Brenner BM, Parving HH (1995) Short stature and diabetic nephropathy. BMJ 310:296–297

    CAS  PubMed  PubMed Central  Google Scholar 

  136. 136.

    Silverstein J, Klingensmith G, Copeland K, Plotnick L, Kaufman F, Laffel L, Deeb L, Grey M, Anderson B, Holzmeister LA, Clark N (2005) Care of children and adolescents with type 1 diabetes. Diabetes Care 28:186–212

    PubMed  Google Scholar 

  137. 137.

    Gross JL, de Azevedo MJ, Silveiro SP, Canani LH, Caramori ML, Zelmanovitz T (2005) Diabetic nephropathy: Diagnosis, prevention, and treatment. Diabetes Care 28:176–188

    Google Scholar 

  138. 138.

    Donaghue KC, Chiarelli F, Trotta D, Allgrove J, Dahl-Jorgensen K (2007) Microvascular and macrovascular complications. Pediatr Diabetes 8:163–170

    PubMed  Google Scholar 

  139. 139.

    KDOQI (2007) Clinical Practice Guidelines and Clinical Practice Recommendations for Diabetes and Chronic Kidney Disease. Am J Kidney Dis 49(2 Suppl 2):S12–S154

    Google Scholar 

  140. 140.

    Mogensen CE, Chachati A, Christensen CK, Close CF, Deckert T, Hommel E, Kastrup J, Lefebvre P, Mathiesen EF, Feldt-Rasmussen B, Schmity A, Viberti GC (1985) Microalbuminuria: an early marker of renal involvement in diabetes. Uremia Invest 9:85–95

    PubMed  Google Scholar 

  141. 141.

    Mogensen CE, Keane WF, Bennett PH, Jerums G, Parving HH, Passa P, Steffes MW, Striker GE, Viberti GC (1995) Prevention of diabetic renal disease with special reference to microalbuminuria. Lancet 346:1080–1084

    CAS  PubMed  Google Scholar 

  142. 142.

    Couper JJ, Clarke CF, Byrne GC, Jones TW, Donaghue KC, Nairn J, Boyce D, Russel M, Stephens M, Raymond J, Bates DJ, McCaul K (1997) Progression of borderline increase in albuminuria in adolescents with insulin-dependent diabetes. Diabet Med 14:766–771

    CAS  PubMed  Google Scholar 

  143. 143.

    Bangstaad HJ, Dahl-Jorgensen K, Kjaersgaard P, Mevold K, Hanssen KF (1993) Urinary albumin excretion rate and puberty in non-diabetic children and adolescents. Acta Paediatr 82:857–862

    Google Scholar 

  144. 144.

    Gatling W, Knight C, Hill RD (1985) Screening for early diabetic nephropathy: which sample to detect microalbuminuria? Diabet Med 2:451–455

    CAS  PubMed  Google Scholar 

  145. 145.

    Chiarelli F, Verrotti A, Mohn A, Morgese G (1997) The importance of microalbuminuria as an indicator of incipient diabetic nephropathy: therapeutic implications. Ann Med 29:439–445

    CAS  PubMed  Google Scholar 

  146. 146.

    Shield JP, Hunt LP, Karachliou F, Karavanaki K, Baum JD (1995) Is microalbuminuria progressive? Arch Dis Child 73:512–514

    CAS  PubMed  PubMed Central  Google Scholar 

  147. 147.

    Brink SJ (2001) Complications of pediatric and adolescent type 1 diabetes mellitus. Curr Diabetes Rep 1:47–55

    CAS  Google Scholar 

  148. 148.

    Schultz CJ, Amin R, Dunger DB (2002) Markers of microvascular complications in insulin dependent diabetes. Arch Dis Child 87:10–12

    CAS  PubMed  PubMed Central  Google Scholar 

  149. 149.

    Campbell F (1995) Microalbuminuria and nephropathy in insulin dependent diabetes mellitus. Arch Dis Child 73:4–7

    CAS  PubMed  PubMed Central  Google Scholar 

  150. 150.

    Joner G, Brinchmann-Hansen O, Torres CG, Hanssen KF (1992) A nationwide cross-sectional study of retinopathy and microalbuminuria in young Norwegian type 1 (insulin-dependent) diabetic patients. Diabetologia 35:1049–1054

    CAS  PubMed  Google Scholar 

  151. 151.

    Moore TH, Shield JP; Microalbuminuria in Diabetic Adolescents and Children (MIDAC) Research Group (2000) Prevalence of abnormal urinary albumin excretion in adolescents and children with insulin dependent diabetes: The MIDAC study. Arch Dis Child 83:239–243

    CAS  PubMed  PubMed Central  Google Scholar 

  152. 152.

    Norgaard K, Storm B, Graae M, Feldt-Rasmussen B (1989) Elevated albumin excretion and retinal changes in children with type 1 diabetes are related to long-term poor blood glucose control. Diabet Med 6:325–328

    CAS  PubMed  Google Scholar 

  153. 153.

    Karavanaki K, Baum JD (1999) Prevalence of microvascular and neurologic abnormalities in a population of diabetic children. J Pediatr Endocrinol Metab 12:411–422

    CAS  PubMed  Google Scholar 

  154. 154.

    Mullis P, Kochli HP, Zuppinger K, Schwarz HP (1988) Intermittent microalbuminuria in children with type 1 diabetes mellitus without clinical evidence of nephropathy. Eur J Pediatr 147:385–388

    CAS  PubMed  Google Scholar 

  155. 155.

    Berg UB, Torbjornsdotter TB, Jaremko G, Thalme B (1998) Kidney morphological changes in relation to long-term renal function and metabolic control in adolescents with IDDM. Diabetologia 41:1047–1056

    CAS  Google Scholar 

  156. 156.

    Chaturvedi N, Bandinelli S, Mangili R, Penno G, Rottiers RE, Fuller JH (2001) Microalbuminuria in type 1 diabetes: rates,risk factors and glycemic threshold. Kidney Int 60:219–227

    CAS  PubMed  Google Scholar 

  157. 157.

    Royal College of Physicians of Edinburgh Diabetes Register Group (2002) Near-normal urinary albumin concentrations predict progression to diabetic nephropathy in type 1 diabetes mellitus. Diabet Med 17:782–791

    Google Scholar 

  158. 158.

    Parving HH, Oxenboll B, Svendsen PA, Christiansen JS, Andersen AR (1982) Early detection of patients at risk of developing diabetic nephropathy. Acta Endocrinol (Copenh) 100:550–555

    CAS  Google Scholar 

  159. 159.

    Viberti GC, Hill RD, Jarrett RJ, Argyropoulos A, Mahmud U, Keen H (1982) Microalbuminuria as a predictor of clinical nephropathy in insulin-dependent diabetes mellitus. Lancet i:1430–1432

    Google Scholar 

  160. 160.

    Mogensen C, Christensen C, Vittinghus E (1983) The stages in diabetic renal disease with emphasis on the stage of incipient diabetic nephropathy. Diabetes 32(Suppl 2):64–78

    Google Scholar 

  161. 161.

    Rossing P, Hougaard P, Parving HH (2005) Progression of microalbuminuria in type 1 diabetes: ten year prospective observational study. Kidney Int 68:1446–1450

    PubMed  Google Scholar 

  162. 162.

    Tabaei BP, Al-Kassab AS, Ilag LL, Zawacki CM, Herman WH (2001) Does microalbuminuria predict diabetic nephropathy? Diabetes Care 24:1560–1566

    CAS  PubMed  Google Scholar 

  163. 163.

    Giorgino F, Laviola L, Cavallo Perin P, Solnica B, Fuller J, Chaturvedi N (2004) Factors associated with progression to macroalbuminuria in microalbuminuric type 1 diabetic patients: the EURODIAB Prospective Complications Study. Diabetologia 47:1020–1028

    CAS  PubMed  Google Scholar 

  164. 164.

    Bojestig M, Arnqvist HJ, Karlberg BE, Ludvigsson J (1996) Glycemic control and prognosis in type 1 diabetic patients with microalbuminuria. Diabetes Care 19:313–317

    CAS  PubMed  Google Scholar 

  165. 165.

    Rudberg S, Dahlquist G (1996) Determinants of progression of microalbuminuria in adolescents with IDDM. Diabetes Care 369–371

    CAS  PubMed  Google Scholar 

  166. 166.

    Nordwall M, Bojestig M, Arnqvist HJ, Ludvigsson J (2004) Declining incidence of severe retinopathy and persisting decrease of nephropathy in an unselected population of type 1 diabetes-the Linkoping diabetes complications study. Diabetologia 47:1266–1272

    CAS  PubMed  Google Scholar 

  167. 167.

    Walsh MG, Zgibor J, Borch-Johnsen K, Orchard TJ; DiComp Investigators (2004) A multinational comparison of complications assessment in type 1 diabetes. Diabetes Care 27:1610–1617

    PubMed  Google Scholar 

  168. 168.

    Schwarze CP, Dunger DB (2005) Management of early diabetic nephropathy in adolescents with type 1 diabetes mellitus. Pract Diabetes Int 22:65–69

    Google Scholar 

  169. 169.

    Chiarelli F, Trotta D, Verrotti A, Mohn A (2002) Treatment of hypertension and microalbuminuria in children and adolescents with type 1 diabetes mellitus. Pediatr Diabetes 3:113–124

    PubMed  Google Scholar 

  170. 170.

    Mortensen HB, Hougard P (1997) Comparison of metabolic control in a cross sectional study of 2873 children and adolescents with insulin-dependent diabetes from 18 countries. Diabetes Care 20:714–720

    CAS  PubMed  Google Scholar 

  171. 171.

    Parving HH (2001) Diabetic nephropathy: Prevention and treatment. Kidney Int 60:2041–2055

    CAS  PubMed  Google Scholar 

  172. 172.

    Giannini C, Mohn A, Chiarelli F (2006) Physical exercise and diabetes during childhood. Acta Biomed Ateneo Parmense 1:18–25

    Google Scholar 

  173. 173.

    National High Blood Pressure Education Program Working Group on High Blood Pressure in Children and Adolescents (2004) The fourth report on the diagnosis, evaluation, and treatment of high blood pressure in children and adolescents. Pediatrics 114:555–576

    Google Scholar 

  174. 174.

    Pedrini MT, Levey AS, Lau J, Chalmers TC, Wang PH (1996) The effect of dietary protein restriction on the progression of diabetic and nondiabetic renal diseases: A meta-analysis. Ann Intern Med 124:627–632

    CAS  PubMed  Google Scholar 

  175. 175.

    Hansen HP, Tauber-Lassen E, Jensen BR, Parving HH (2002) Effect of dietary protein restriction on prognosis in patients with diabetic nephropathy. Kidney Int 62:220–228

    PubMed  Google Scholar 

  176. 176.

    The ACE Inhibitors in Diabetic Nephropathy Trialist Group (2001) Should all type 1 diabetic microalbuminuric patients receive ACE inhibitors? A meta-regression analysis. Ann Intern Med 134:370–379

    Google Scholar 

  177. 177.

    Mathiesen ER, Hommel E, Hansen HP, Smidt UM, Parving HH (1999) Randomized controlled trial of long term efficacy of captopril on preservation of kidney function in normotensive patients with insulin dependent diabetes and microalbuminuria. BMJ 319:24–25

    CAS  PubMed  PubMed Central  Google Scholar 

  178. 178.

    Ahmad J, Shafique S, Abidi SM, Parwez I (2003) Effect of 5-year enalapril therapy on progression of microalbuminuria and glomerular structural changes in type 1 diabetic subjects. Diabetes Res Clin Pract 60:131–138

    CAS  PubMed  Google Scholar 

  179. 179.

    Cook J, Daneman D, Spino MA (1990) Angiotensin converting enzyme inhibitor therapy to decrease microalbuminuria in normotensive children with diabetes mellitus. J Pediatr 117:39–45

    CAS  PubMed  PubMed Central  Google Scholar 

  180. 180.

    Rudberg S, Aperia A, Freyschuss U, Persson B (1990) Enalapril reduces microalbuminuria in young normotensive type 1 (insulin-dependent) diabetic patients irrespective of its hypotensive effect. Diabetologia 33:470–476

    CAS  PubMed  PubMed Central  Google Scholar 

  181. 181.

    Rudberg S, Osterby R, Bangstad HJ, Dahlquist, Persson B (1999) Effect of angiotensin converting enzyme inhibitor or beta blocker on glomerular structural changes in young microalbuminuric patients with type I (insulin-dependent) diabetes mellitus. Diabetologia 42:589–595

    CAS  Google Scholar 

  182. 182.

    Yuksel H, Dancan S, Kabasakal C, Cura A, Mir S, Mavi E (1998) Effect of enalapril on proteinuria, phosphaturia, and calciuria in insulin-dependent diabetes. Pediatr Nephrol 12:648–650

    CAS  PubMed  Google Scholar 

  183. 183.

    Strippoli GF, Craig M, Deeks JJ, Schena FP, Craig JC (2004) Effects of angiotensin converting enzyme inhibitors and angiotensin II receptor antagonists on mortality and renal outcomes in diabetic nephropathy: systemic review. BMJ 329:828–831

    CAS  PubMed  PubMed Central  Google Scholar 

  184. 184.

    MacKinnon M, Shurraw S, Akbari A, Knoll GA, Jaffey J, Clark HD (2006) Combination therapy with an angiotensin receptor blocker and an ACE inhibitor in proteinuric renal disease: a systematic review of the efficacy and safety data. Am J Kidney Dis 48:8–20

    CAS  PubMed  Google Scholar 

  185. 185.

    White CT, Macpherson CF, Hurley RM, Matsell DG (2003) Antiproteinuric effects of enalapril and losartan: a pilot study. Pediatr Nephrol 18:1038–1043

    Google Scholar 

  186. 186.

    Lubrano R, Soscia F, Elli M, Ventriglia F, Raggi C, Travasso E, Scateni S, Di Maio V, Versacci P, Masciangelo R, Romero S (2006) Renal and cardiovascular effects of angiotensin-converting enzyme inhibitor plus angiotensin II receptor antagonist therapy in children with proteinuria. Pediatrics 118:833–838

    Google Scholar 

  187. 187.

    Andersen S, Brochner-Mortensen J, Parving HH; Irbesartan in Patients With Type 2 Diabetes and Microalbuminuria Study Group (2003) Kidney function during and after withdrawal of long-term irbesartan treatment in patients with type 2 diabetes and microalbuminuria. Diabetes Care 26:3296–3302

    PubMed  Google Scholar 

  188. 188.

    Klein R, Zinman B, Gardiner R, Suissa S, Donnelly SM, Sinaiko AR, Kramer MS, Goodyer P, Moss SE, Strand T, Mauer M (2005) The relationship of diabetic retinopathy to preclinical diabetic glomerulopathy lesions in type 1 diabetic patients. Diabetes 54:527–533

    CAS  PubMed  Google Scholar 

  189. 189.

    Mathiesen ER, Oxenboll B, Johansen K, Svendsen PA, Deckert T (1984) Incipient nephropathy in type 1 (insulin-dependent) diabetes. Diabetologia 26:406–410

    CAS  PubMed  Google Scholar 

  190. 190.

    Hansen HP, Lund SS, Rossing P, Tarnow L, Nielsen FS, Jensen T, Parving HH (2001) Preventing diabetic nephropathy: An audit. Scand J Clin Lab Invest 61:471–477

    CAS  PubMed  Google Scholar 

  191. 191.

    Rosenbloom AL, Joe JR, Young RS, Winter WE (1999) Emerging epidemic of type 2 diabetes in youth. Diabetes Care 22:345–354

    CAS  PubMed  Google Scholar 

  192. 192.

    Hannon TS, Rao G, Arslanian S (2005) Childhood obesity and type 2 diabetes mellitus. Pediatrics 116:473–480

    PubMed  Google Scholar 

  193. 193.

    Alberti G, Zimmet P, Shaw J, Bloomgarden Z, Kaufman F, Silink M; Consensus Workshop Group (2004) Type 2 diabetes in the young: the evolving epidemic. Diabetes Care 27:1798–1811

    PubMed  Google Scholar 

  194. 194.

    Kiess W, Bottner A, Blufer S, Raile K, Galler A, Kapellen TM (2004) Type 2 diabetes mellitus in children and adolescents-the beginning of a renal catastrophe? Nephrol Dial Transplant 19:2693–2696

    PubMed  Google Scholar 

  195. 195.

    Pinhas-Hamiel P, Zeitler P (2007) Acute and chronic complications of type 2 diabetes mellitus in children and adolescents. Lancet 369:1823–1831

    PubMed  Google Scholar 

  196. 196.

    Ibrahim HAA, Vora JP (1999) Diabetic nephropathy. Best Pract Res Clin Endocrinol Metab 13:239–264

    CAS  Google Scholar 

  197. 197.

    Vora JP, Dolben J, Dean JD, Thomas D, Williams JD, Owens DR, Peters JR (1992) Renal hemodynamics in newly presenting non-insulin dependent diabetes mellitus. Kidney Int 41:829–835

    CAS  PubMed  Google Scholar 

  198. 198.

    Adler AI, Stevens RJ, Manley SE, Bilous RW, Cull CA, Holman RR; UKPDS Group (2003) Development and progression of nephropathy in type 2 diabetes: The United Kingdom Prospective Diabetes Study (UKPDS 64). Kidney Int 63:225–232

    PubMed  Google Scholar 

  199. 199.

    Fagot-Campagna A, Knowler WC, Pettitt DJ (1998) Type 2 diabetes in Pima Indian children: cardiovascular risk factors at diagnosis and 10 years later. Diabetes 47 (Suppl 1):A155 (abstract)

    Google Scholar 

  200. 200.

    Pavkov ME, Bennett PH, Knowler WC, Krakoff J, Sievers ML, Nelson RG (2006) Effect of youth-onset type 2 diabetes mellitus on incidence of end-stage renal disease and mortality in young and middle-aged Pima Indians. JAMA 296:421–426

    CAS  Google Scholar 

  201. 201.

    Dean H, Flett B (2002) Natural history of type 2 diabetes diagnosed in childhood: Long term follow-up in young adult years. Diabetes 51(Suppl 2):A25–A26

    Google Scholar 

  202. 202.

    Yokoyama H, Okudaira M, Otani T, Takaike H, Miura J, Saeki A, Uchigata Y, Omori Y (1997) Existence of early-onset NIDDM Japanese demonstrating severe diabetic complications. Diabetes Care 20:844–847

    CAS  PubMed  Google Scholar 

  203. 203.

    Gambara V, Mecca G, Remuzzi G, Bertani T (1993) Heterogeneous nature of renal lesions in type II diabetes. J Am Soc Nephrol 3:1458–1466

    CAS  PubMed  PubMed Central  Google Scholar 

  204. 204.

    Fioretto P, Mauer M, Brocco E, Velussi M, Frigato F, Muollo B, Sambataro M, Abaterusso C, Baggio B, Crepaldi G, Nosadini R (1996) Patterns of renal injury in NIDDM patients with microalbuminuria. Diabetologia 39:1569–1576

    CAS  PubMed  Google Scholar 

  205. 205.

    Gall MA, Hougaard P, Borch-Johnsen K, Parving HH (1997) Risk factors for development of incipient and overt diabetic nephropathy in patients with non-insulin dependent diabetes mellitus: prospective, observational study. BMJ 314:783–788

    CAS  PubMed  PubMed Central  Google Scholar 

  206. 206.

    Bruno G, Cavallo PP, Bargero G, Borra M, Calvi V, Derrico N, Deambrogio P, Pagano G (1996) Prevalence and risk factors for micro-and macroalbuminuria in an Italian population-based cohort of NIDDM subjects. Diabetes Care 19:43–47

    CAS  PubMed  Google Scholar 

  207. 207.

    Yokoyama H, Okudaira M, Otani T, Watanabe C, Takaike H, Miuira J, Yamada H, Mutou K, Satou A, Uchigata Y, Iwamoto Y (1998) High incidence of diabetic nephropathy in early-onset Japanese NIDDM patients. Diabetes Care 21:1080–1085

    CAS  PubMed  Google Scholar 

  208. 208.

    Krakoff J, Lindsay R, Looker HC, Nelson RG, Hanson RL, Knowler WC (2003) Incidence of retinopathy and nephropathy in youth-onset compared with adult-onset type 2 diabetes. Diabetes Care 26:76–81

    PubMed  Google Scholar 

  209. 209.

    Ettinger LM, Freeman K, DiMartino-Nardi J, Flynn J (2005) Microalbuminuria and abnormal ambulatory blood pressure in adolescents with type 2 diabetes mellitus. J Pediatr 147:67–73

    CAS  Google Scholar 

  210. 210.

    Eppens MC, Craig ME, Cusumano J, Hing S, Chan AK, Howard NJ, Silink M, Donaghue KC (2006) Prevalence of diabetes complications in adolescents with type 2 compared with type 1 diabetes. Diabetes Care 29:1300–1306

    PubMed  PubMed Central  Google Scholar 

  211. 211.

    Svensson M, Sundkvist G, Arnqvist H, Bjork E, Blohme G, Bolinder J, Henricsson M, Nystrom L, Torffvit O, Waernbaum I, Ostman J, Eriksson JW (2003) Signs of nephropathy may occur early in young adults with diabetes despite modern diabetes management. Diabetes Care 26:2903–2909

    PubMed  Google Scholar 

  212. 212.

    Yokoyama H, Okudaira M, Otani T, Sato A, Miura J, Takaike H, Yamada H, Muto K, Uchigata Y, Ohashi Y, Iwamoto Y (2000) Higher incidence of diabetic nephropathy in type 2 than in type 1 diabetes in early-onset diabetes in Japan. Kidney Int 58:302–311

    CAS  PubMed  Google Scholar 

  213. 213.

    Keller CK, Bergis KH, Fliser D, Ritz E (1996) Renal findings in patients with short-term type 2 diabetes. J Am Soc Nephrol 7:2627–2635

    CAS  PubMed  Google Scholar 

  214. 214.

    Mather HM, Chaturvedi N, Kehely AM (1998) Comparison of prevalence and risk factors for microalbuminuria in South Asian and Europeans with type 2 diabetes mellitus. Diabet Med 15:672–677

    CAS  PubMed  Google Scholar 

  215. 215.

    American Diabetes Association (2000) Type 2 diabetes in children and adolescents. Diabetes Care 23:381–389

    Google Scholar 

  216. 216.

    Fava S, Azzopardi J, Hattersley AT, Watkins PJ (2000) Increased prevalence of proteinuria in diabetic sibs of proteinuric type 2 diabetic subjects. Am J Kidney Dis 35:708–712

    CAS  PubMed  Google Scholar 

  217. 217.

    McCance DR, Hanson RL, Pettitt DJ, Jacobsson LTH, Bennett PH, Bishop DT, Knowier WC (2004) Diabetic nephropathy: a risk factor for diabetes mellitus in offspring. Diabetologia 38:221–226

    Google Scholar 

  218. 218.

    Nelson RG, Pettitt DJ, de Courten MP, Hanson RI, Knowler WC, Bennett PH (1996) Parental hypertension and proteinuria in Pima Indians with NIDDM. Diabetologia 39:433–438

    CAS  PubMed  Google Scholar 

  219. 219.

    Fogarty DG, Rich SS, Hanna L, Warram JH, Krolewski AS (2000) Urinary albumin excretion in families with type 2 diabetes is heritable and genetically correlated to blood pressure. Kidney Int 57:250–257

    CAS  PubMed  Google Scholar 

  220. 220.

    Agius E, Attard G, Shakespeare L, Clark P, Vidya MA, Hattersley AT, Fava S (2006) Familial factors in diabetic nephropathy: an offspring study. Diabet Med 23:331–334

    CAS  PubMed  Google Scholar 

  221. 221.

    Solini A, Dalla Vestra M, Saller A, Nosadini R, Crepaldi G, Fiorretto P (2002) The angiotensin-converting enzyme DD genotype is associated with glomerulopathy lesions in type 2 diabetes. Diabetes 51:251–255

    CAS  PubMed  Google Scholar 

  222. 222.

    Fradin S, Goulet-Salmon B, Chantepie M, Grandhomme F, Morrello R, Jauzac P, Reznik Y (2002) Relationship between polymorphisms in the renin-angiotensin system and nephropathy in type 2 diabetic patients. Diabetes Metab 28:27–32

    CAS  PubMed  Google Scholar 

  223. 223.

    Hermann SM, Ringel J, Wang JG, Staessen JA, Brand E; Berlin Diabetes Mellitus (BeDiaM) Study (2002) Peroxisome proliferator-activated receptor-gamma2 polymorphism Pro12Ala is associated with nephropathy in type 2 diabetes: The Berlin Diabetes Mellitus (BeDiaM) Study. Diabetes 51:2653–2657

    Google Scholar 

  224. 224.

    Bowden DW, Colicigno CJ, Langefeld CD, Sale MM, Williams A, Anderson PJ, Rich SS, Freedman BI (2004) A genome scan for diabetic nephropathy in African Americans. Kidney Int 66:1517–1526

    CAS  PubMed  Google Scholar 

  225. 225.

    Csernus K, Lanyi E, Erhardt E, Molnar D (2005) Effect of childhood obesity and obesity-related cardiovascular risk factors on glomerular and tubular protein excretion. Eur J Pediatr 164:44–49

    CAS  PubMed  Google Scholar 

  226. 226.

    Mykkanen L, Zaccaro DJ, Wagenknecht LE, Robbins DC, Gabriel M, Haffner SM (1998) Microalbuminuria is associated with insulin resistance in nondiabetic subjects: the insulin resistance atherosclerosis study. Diabetes 47:793–800

    CAS  PubMed  Google Scholar 

  227. 227.

    Farah SE, Wals KT, Friedman IB, Pisacano MA, DiMartino-Nardi J (2006) Prevalence of retinopathy and microalbuminuria in pediatric type 2 diabetes mellitus. Pediatr Endocrinol Metab 19:937–942

    Google Scholar 

  228. 228.

    Lane PH (2004) Microalbuminuria as a marker of cardiovascular and renal risk in type 2 diabetes mellitus: a temporal perspective. Am J Physiol Renal Physiol 286:F442–F450

    CAS  PubMed  Google Scholar 

  229. 229.

    Lane PH (2005) Pediatric aspects of diabetic kidney disease. Adv Chr Kidney Dis 12:230–235

    Google Scholar 

  230. 230.

    American Diabetes Association (2006) Standards of medical care in diabetes—2006. Diabetes Care 29(Suppl l):S4–S42

    Google Scholar 

  231. 231.

    Robinson TN (1999) Reducing children´s television viewing to prevent obesity: a randomized controlled trial. JAMA 282:1561–1567

    CAS  PubMed  Google Scholar 

  232. 232.

    Hernandez B, Gortmaker SL, Colditz GA, Peterson KE, Laird NM, Parra-Cabrera S (1999) Association of obesity with physical activity, television programs and other forms of video viewing among children in Mexico city. Int J Obes Metab Disord 23:845–854

    CAS  Google Scholar 

  233. 233.

    American Diabetes Association (2003) Management of dyslipidemia in children and adolescents with diabetes. Diabetes Care 26:2194–2197

    Google Scholar 

  234. 234.

    Ferrari P (2007) Prescribing angiotensin-converting enzyme inhibitors and angiotensin receptor blockers in chronic kidney disease. Nephrology 12:81–89

    CAS  PubMed  Google Scholar 

  235. 235.

    Lewis EJ, Hunsicker LG, Clarke WR, Berl T, Pohl MA, Lewis JB, Ritz E, Atkins RC, Rhonde R, Raz I; Collaborative Study Group (2001) Renoprotective effect of the angiotensin-receptor antagonist irbesartan in patients with nephropathy due to type 2 diabetes. N Engl J Med 345:851–860

    CAS  PubMed  Google Scholar 

  236. 236.

    Brenner BM, Cooper ME, deZeeuw D, Keane WF, Mitch WE, Parving HH, Remuzzi G, Snapinn SM, Zhang Z, Shahinfar S; RENAAL Study Investigators (2001) Effects of losartan on renal and cardiovascular outcomes in patients with type 2 diabetes and nephropathy. N Engl J Med 345:861–869

    CAS  PubMed  Google Scholar 

  237. 237.

    Parving HH, Lehnert H, Brochner-Mortensen J, Gomis R, Andersen S, Arner P (2001) The effect of irbesartan on the development of diabetic nephropathy in patients with type 2 diabetes. N Engl J Med 345:870–878

    CAS  PubMed  Google Scholar 

  238. 238.

    Remuzzi G, Macia M, Ruggenenti P (2006) Prevention and treatment of diabetic renal disease in type 2 diabetes: The BENEDICT Study. J Am Soc Nephrol 17:90–97

    Google Scholar 

  239. 239.

    Gaede P, Vedel P, Parving HH, Pedersen O (1999) Intensified multifactorial intervention in patients with type 2 diabetes mellitus and microalbuminuria. The Steno type 2 randomised study. Lancet 353:617–622

    CAS  PubMed  Google Scholar 

  240. 240.

    Gaede P, Vedel P, Larsen N, Jensen GVH, Parving HH, Pedersen O (2003) Multifactorial intervention and cardiovascular disease in patients with type 2 diabetes. N Engl J Med 348:383–393

    PubMed  Google Scholar 

  241. 241.

    Fioretto P, Solini A (2005) Antihypertensive treatment and multifactorial approach for renal protection in diabetes. J Am Soc Nephrol 16:18–21

    Google Scholar 

  242. 242.

    Gahagan S, Silverstein J; Committee on Native American Child Health and Section on Endocrinology (2003) Prevention and treatment of type 2 diabetes mellitus in children, with special emphasis on American Indian and alaska native children. Pediatrics 112:e328–e347

    PubMed  Google Scholar 

  243. 243.

    Brinkman JW, Bakker SJL, Gansevoort RT, Hillege HL, Kema IP, Gans ROB, de Jong PE, de Zeeuw D (2004) Which method for quantifying urinary albumin excretion gives what outcome? A comparison of immunonephelometry with HPLC. Kidney Int 66(Suppl 92):S69–S75

    Google Scholar 

  244. 244.

    Comper WD, Osicka TM (2004) Albumin-like material in urine. Kidney Int 66(Suppl 92):S67–S68

    Google Scholar 

  245. 245.

    Chan OT, Herold DA (2006) Chip electrophoresis as a method for quantifying total microalbuminuria. Clin Chem 52:2141–2146

    CAS  PubMed  Google Scholar 

  246. 246.

    Meier M, Kaiser T, Herrmann A, Knueppel S, Hillmann M, Koester P, Danne T, Haller H, Fliser D, Mischak H (2005) Identification of urinary protein pattern in type 1 diabetic adolescents with early diabetic nephropathy by a novel combined proteome analysis. J Diabetes Compl 19:223–232

    Google Scholar 

  247. 247.

    Otu HH, Can H, Spentzos D, Nelson RG, Hanson RL, Looker HC, Knowler WC, Monroy M, Libermann TA, Karumanchi SA, Thadhani R (2007) Prediction of diabetic nephropathy using urine proteomic profiling 10 years prior to development of nephropathy. Diabetes Care 30:638–643

    CAS  PubMed  Google Scholar 

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Acknowledgments

This review is based on the lectures presented at the 2nd Meeting of the Southeastern Europe Pediatric Nephrology Working Group (SEPNWG), 7–9 April 2006, Belgrade, and at the 18th Danube Symposium of Nephrology, 26–28 September 2006, Novi Sad (Serbia). The review appeared in abstract form (Kidney Blood Press Res 2006; 29:195). The work is supported by the Ministry of Science and Environmental Protection, Government of Serbia, Grant No 145046D. The author is indebted to Professor O. Mehls for critical reading and to Mrs. B. Krsmanovic for invaluable help in preparing the manuscript.

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    Radovan Bogdanović

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  1. Radovan Bogdanović
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Correspondence to Radovan Bogdanović.

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Bogdanović, R. Diabetic nephropathy in children and adolescents. Pediatr Nephrol 23, 507–525 (2008). https://doi.org/10.1007/s00467-007-0583-2

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Keywords

  • Diabetic nephropathy
  • Children
  • Adolescents
  • Risk factors
  • Microalbuminuria
  • Screening
  • Prevention
  • Treatment