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Microalbuminuria: causes and implications

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Abstract

Management strategies are increasingly focused on tackling the increasing burden of cardiovascular disease worldwide. Microalbuminuria is a powerful predictor of cardiovascular disease and mortality in adults. This holds true in the general adult population but is particularly recognized in those with diabetes, where it identifies those likely to develop progressive atherosclerotic vascular disease and renal impairment. The atherosclerotic process begins in childhood with likely consequences in later life. In-depth understanding of the mechanisms through which microalbuminuria occurs holds promise for designing therapies to arrest its development in the future. Microalbuminuria arises from increased leakage of albumin through the complex glomerular sieve known as the glomerular filtration barrier. This requires changes in the physio-chemical properties of components of this barrier. However, the increased glomerular permeability confirmed in disease does not necessarily correlate with recognized histological changes in the glomerulus, suggesting that perhaps more subtle ultrastructural changes may be relevant. The epidemiology of microalbuminuria reveals a close association between systemic endothelial dysfunction and vascular disease, also implicating glomerular endothelial dysfunction in microalbuminuria. This review discusses the mechanisms of microalbuminuria in disease, particularly the emerging role of the glomerular endothelium and its glycocalyx, and examines its implications for cardiovascular disease in the pediatric population.

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References

  1. 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 1:1430–1432

    CAS  PubMed  Google Scholar 

  2. Dinneen SF, Gerstein HC (1997) The association of microalbuminuria and mortality in non-insulin-dependent diabetes mellitus. A systematic overview of the literature. Arch Intern Med 157:1413–1418

    CAS  PubMed  Google Scholar 

  3. Gerstein HC, Mann JF, Yi Q, Zinman B, Dinneen SF, Hoogwerf B, Halle JP, Young J, Rashkow A, Joyce C, Nawaz S, Yusuf S (2001) Albuminuria and risk of cardiovascular events, death, and heart failure in diabetic and nondiabetic individuals. JAMA 286:421–426

    CAS  PubMed  Google Scholar 

  4. Allen KV, Walker JD (2003) Microalbuminuria and mortality in long-duration type 1 diabetes. Diab Care 26:2389–2391

    Google Scholar 

  5. Wachtell K, Ibsen H, Olsen MH, Borch-Johnsen K, Lindholm LH, Mogensen CE, Dahlof B, Devereux RB, Beevers G, de Faire U, Fyhrquist F, Julius S, Kjeldsen SE, Kristianson K, Lederballe-Pedersen O, Nieminen MS, Okin PM, Omvik P, Oparil S, Wedel H, Snapinn SM, Aurup P (2003) Albuminuria and cardiovascular risk in hypertensive patients with left ventricular hypertrophy: the LIFE study. Ann Intern Med 139:901–906

    PubMed  Google Scholar 

  6. 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: systematic review. BMJ 329:828

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Hillege HL, Fidler V, Diercks GF, van Gilst WH, de Zeeuw D, van Veldhuisen DJ, Gans RO, Janssen WM, Grobbee DE, de Jong PE (2002) Urinary albumin excretion predicts cardiovascular and noncardiovascular mortality in general population. Circulation 106:1777–1782

    CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  9. Weiss R, Dziura J, Burgert TS, Tamborlane WV, Taksali SE, Yeckel CW, Allen K, Lopes M, Savoye M, Morrison J, Sherwin RS, Caprio S (2004) Obesity and the metabolic syndrome in children and adolescents. N Engl J Med 350:2362–2374

    CAS  PubMed  Google Scholar 

  10. Haraldsson B, Nystrom J, Deen WM (2008) Properties of the glomerular barrier and mechanisms of proteinuria. Physiol Rev 88:451–487

    CAS  PubMed  Google Scholar 

  11. Dyer AR, Greenland P, Elliott P, Daviglus ML, Claeys G, Kesteloot H, Ueshima H, Stamler J (2004) Evaluation of measures of urinary albumin excretion in epidemiologic studies. Am J Epidemiol 160:1122–1131

    PubMed  Google Scholar 

  12. Bakker AJ (1999) Detection of microalbuminuria. Receiver operating characteristic curve analysis favors albumin-to-creatinine ratio over albumin concentration. Diab Care 22:307–313

    CAS  Google Scholar 

  13. Jafar TH, Chaturvedi N, Hatcher J, Levey AS (2007) Use of albumin creatinine ratio and urine albumin concentration as a screening test for albuminuria in an Indo-Asian population. Nephrol Dial Transplant 22:2194–2200

    CAS  PubMed  Google Scholar 

  14. Gansevoort RT, Brinkman J, Bakker SJ, De Jong PE, de Zeeuw D (2006) Evaluation of measures of urinary albumin excretion. Am J Epidemiol 164:725–727

    PubMed  Google Scholar 

  15. Brantsma AH, Atthobari J, Bakker SJ, de Zeeuw D, de Jong PE, Gansevoort RT (2007) What predicts progression and regression of urinary albumin excretion in the nondiabetic population? J Am Soc Nephrol 18:637–645

    CAS  PubMed  Google Scholar 

  16. Sanchez-Bayle M, Rodriguez-Cimadevilla C, Asensio C, Ruiz-Jarabo C, Baena J, Arnaiz P, Villa S, Cocho P (1995) Urinary albumin excretion in Spanish children. Nino Jesus Group. Pediatr Nephrol 9:428–430

    CAS  PubMed  Google Scholar 

  17. Gibb DM, Shah V, Preece M, Barratt TM (1989) Variability of urine albumin excretion in normal and diabetic children. Pediatr Nephrol 3:414–419

    CAS  PubMed  Google Scholar 

  18. Rademacher ER, Sinaiko AR (2009) Albuminuria in children. Curr Opin Nephrol Hypertens 18:246–251

    CAS  PubMed  Google Scholar 

  19. Jefferson IG, Greene SA, Smith MA, Smith RF, Griffin NK, Baum JD (1985) Urine albumin to creatinine ratio-response to exercise in diabetes. Arch Dis Child 60:305–310

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Marshall SM (1991) Screening for microalbuminuria: which measurement? Diabet Med 8:706–711

    CAS  PubMed  Google Scholar 

  21. Davies AG, Postlethwaite RJ, Price DA, Burn JL, Houlton CA, Fielding BA (1984) Urinary albumin excretion in school children. Arch Dis Child 59:625–630

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Skinner AM, Addison GM, Price DA (1996) Changes in the urinary excretion of creatinine, albumin and N-acetyl-beta-D-glucosaminidase with increasing age and maturity in healthy schoolchildren. Eur J Pediatr 155:596–602

    CAS  PubMed  Google Scholar 

  23. Hanevold CD, Pollock JS, Harshfield GA (2008) Racial differences in microalbumin excretion in healthy adolescents. Hypertension 51:334–338

    CAS  PubMed  Google Scholar 

  24. Jones CA, Francis ME, Eberhardt MS, Chavers B, Coresh J, Engelgau M, Kusek JW, Byrd-Holt D, Narayan KM, Herman WH, Jones CP, Salive M, Agodoa LY (2002) Microalbuminuria in the US population: third National Health and Nutrition Examination Survey. Am J Kidney Dis 39:445–459

    PubMed  Google Scholar 

  25. Nguyen S, McCulloch C, Brakeman P, Portale A, Hsu CY (2008) Being overweight modifies the association between cardiovascular risk factors and microalbuminuria in adolescents. Pediatrics 121:37–45

    PubMed  Google Scholar 

  26. Janssen I, Katzmarzyk PT, Boyce WF, Vereecken C, Mulvihill C, Roberts C, Currie C, Pickett W (2005) Comparison of overweight and obesity prevalence in school-aged youth from 34 countries and their relationships with physical activity and dietary patterns. Obes Rev 6:123–132

    CAS  PubMed  Google Scholar 

  27. Bahrami H, Bluemke DA, Kronmal R, Bertoni AG, Lloyd-Jones DM, Shahar E, Szklo M, Lima JA (2008) Novel metabolic risk factors for incident heart failure and their relationship with obesity: the MESA (Multi-Ethnic Study of Atherosclerosis) study. J Am Coll Cardiol 51:1775–1783

    CAS  PubMed  Google Scholar 

  28. Sharma K (2009) The link between obesity and albuminuria: adiponectin and podocyte dysfunction. Kidney Int 76:145–148

    CAS  PubMed  Google Scholar 

  29. Brandt JR, Jacobs A, Raissy HH, Kelly FM, Staples AO, Kaufman E, Wong CS (2010) Orthostatic proteinuria and the spectrum of diurnal variability of urinary protein excretion in healthy children. Pediatr Nephrol 25:1131–1137

    PubMed  PubMed Central  Google Scholar 

  30. Springberg PD, Garrett LE Jr, Thompson AL Jr, Collins NF, Lordon RE, Robinson RR (1982) Fixed and reproducible orthostatic proteinuria: results of a 20-year follow-up study. Ann Intern Med 97:516–519

    CAS  PubMed  Google Scholar 

  31. Robinson RR (1980) Isolated proteinuria in asymptomatic patients. Kidney Int 18:395–406

    CAS  PubMed  Google Scholar 

  32. Rytand DA, Spreiter S (1981) Prognosis in postural (orthostatic) proteinuria: forty to fifty-year follow-up of six patients after diagnosis by Thomas Addis. N Engl J Med 305:618–621

    CAS  PubMed  Google Scholar 

  33. Berns JS, McDonald B, Gaudio KM, Siegel NJ (1986) Progression of orthostatic proteinuria to focal and segmental glomerulosclerosis. Clin Pediatr Phila 25:165–166

    CAS  PubMed  Google Scholar 

  34. Ragazzi M, Milani G, Edefonti A, Burdick L, Bianchetti MG, Fossali EF (2008) Left renal vein entrapment: a frequent feature in children with postural proteinuria. Pediatr Nephrol 23:1837–1839

    PubMed  Google Scholar 

  35. Milani GP, Mazzoni MB, Burdick L, Bianchetti MG, Fossali EF (2010) Postural proteinuria associated with left renal vein entrapment: a follow-up evaluation. Am J Kidney Dis 55:e29–e31

    PubMed  Google Scholar 

  36. Yoshioka T, Mitarai T, Kon V, Deen WM, Rennke HG, Ichikawa I (1986) Role for angiotensin II in an overt functional proteinuria. Kidney Int 30:538–545

    CAS  PubMed  Google Scholar 

  37. Ritz E (2006) Heart and kidney: fatal twins? Am J Med 119:S31–S39

    PubMed  Google Scholar 

  38. Klausen K, Borch-Johnsen K, Feldt-Rasmussen B, Jensen G, Clausen P, Scharling H, Appleyard M, Jensen JS (2004) Very low levels of microalbuminuria are associated with increased risk of coronary heart disease and death independently of renal function, hypertension, and diabetes. Circulation 110:32–35

    CAS  PubMed  Google Scholar 

  39. Matsushita K, van der Velde M, Astor BC, Woodward M, Levey AS, de Jong PE, Coresh J, Gansevoort RT (2010) Association of estimated glomerular filtration rate and albuminuria with all-cause and cardiovascular mortality in general population cohorts: a collaborative meta-analysis. Lancet 375:2073–2081

    PubMed  PubMed Central  Google Scholar 

  40. Berenson GS, Srinivasan SR, Bao W, Newman WP 3rd, Tracy RE, Wattigney WA (1998) Association between multiple cardiovascular risk factors and atherosclerosis in children and young adults. The Bogalusa Heart Study. N Engl J Med 338:1650–1656

    CAS  PubMed  Google Scholar 

  41. Charakida M, Deanfield JE, Halcox JP (2007) Childhood origins of arterial disease. Curr Opin Pediatr 19:538–545

    PubMed  Google Scholar 

  42. Burgert TS, Dziura J, Yeckel C, Taksali SE, Weiss R, Tamborlane W, Caprio S (2006) Microalbuminuria in pediatric obesity: prevalence and relation to other cardiovascular risk factors. Int J Obes Lond 30:273–280

    CAS  PubMed  Google Scholar 

  43. Invitti C, Maffeis C, Gilardini L, Pontiggia B, Mazzilli G, Girola A, Sartorio A, Morabito F, Viberti GC (2006) Metabolic syndrome in obese Caucasian children: prevalence using WHO-derived criteria and association with nontraditional cardiovascular risk factors. Int J Obes Lond 30:627–633

    CAS  PubMed  Google Scholar 

  44. Amin R, Widmer B, Prevost AT, Schwarze P, Cooper J, Edge J, Marcovecchio L, Neil A, Dalton RN, Dunger DB (2008) Risk of microalbuminuria and progression to macroalbuminuria in a cohort with childhood onset type 1 diabetes: prospective observational study. BMJ 336:697–701

    PubMed  PubMed Central  Google Scholar 

  45. Rademacher E, Mauer M, Jacobs DR Jr, Chavers B, Steinke J, Sinaiko A (2008) Albumin excretion rate in normal adolescents: relation to insulin resistance and cardiovascular risk factors and comparisons to type 1 diabetes mellitus patients. Clin J Am Soc Nephrol 3:998–1005

    PubMed  PubMed Central  Google Scholar 

  46. Ladeia AM, Ladeia-Frota C, Pinho L, Stefanelli E, Adan L (2005) Endothelial dysfunction is correlated with microalbuminuria in children with short-duration type 1 diabetes. Diab Care 28:2048–2050

    Google Scholar 

  47. Haffner SM, Gonzales C, Valdez RA, Mykkanen L, Hazuda HP, Mitchell BD, Monterrosa A, Stern MP (1993) Is microalbuminuria part of the prediabetic state? The Mexico City Diabetes Study. Diabetologia 36:1002–1006

    CAS  PubMed  Google Scholar 

  48. 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. Diab Care 29:1300–1306

    Google Scholar 

  49. Marcovecchio ML, Tossavainen PH, Acerini CL, Barrett TG, Edge J, Neil A, Shield J, Widmer B, Dalton RN, Dunger DB (2010) Maternal but not paternal association of ambulatory blood pressure with albumin excretion in young offspring with type 1 diabetes. Diab Care 33:366–371

    CAS  Google Scholar 

  50. 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  PubMed  Google Scholar 

  51. Assadi F (2008) Relation of left ventricular hypertrophy to microalbuminuria and C-reactive protein in children and adolescents with essential hypertension. Pediatr Cardiol 29:580–584

    PubMed  Google Scholar 

  52. Franks PW, Hanson RL, Knowler WC, Sievers ML, Bennett PH, Looker HC (2010) Childhood obesity, other cardiovascular risk factors, and premature death. N Engl J Med 362:485–493

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Schiffrin EL (2001) A critical review of the role of endothelial factors in the pathogenesis of hypertension. J Cardiovasc Pharmacol 38(Suppl 2):S3–S6

    CAS  PubMed  Google Scholar 

  54. Endemann DH, Schiffrin EL (2004) Endothelial dysfunction. J Am Soc Nephrol 15:1983–1992

    CAS  PubMed  Google Scholar 

  55. Sutton TA, Fisher CJ, Molitoris BA (2002) Microvascular endothelial injury and dysfunction during ischemic acute renal failure. Kidney Int 62:1539–1549

    CAS  PubMed  Google Scholar 

  56. Davison JM, Homuth V, Jeyabalan A, Conrad KP, Karumanchi SA, Quaggin S, Dechend R, Luft FC (2004) New aspects in the pathophysiology of preeclampsia. J Am Soc Nephrol 15:2440–2448

    CAS  PubMed  Google Scholar 

  57. van Setten PA, van Hinsbergh VW, van der Velden TJ, van de Kar NC, Vermeer M, Mahan JD, Assmann KJ, van den Heuvel LP, Monnens LA (1997) Effects of TNF alpha on verocytotoxin cytotoxicity in purified human glomerular microvascular endothelial cells. Kidney Int 51:1245–1256

    PubMed  Google Scholar 

  58. Deanfield JE, Halcox JP, Rabelink TJ (2007) Endothelial function and dysfunction: testing and clinical relevance. Circulation 115:1285–1295

    PubMed  Google Scholar 

  59. Celermajer DS, Sorensen KE, Spiegelhalter DJ, Georgakopoulos D, Robinson J, Deanfield JE (1994) Aging is associated with endothelial dysfunction in healthy men years before the age-related decline in women. J Am Coll Cardiol 24:471–476

    CAS  PubMed  Google Scholar 

  60. Halcox JP, Deanfield JE (2005) Childhood origins of endothelial dysfunction. Heart 91:1272–1274

    CAS  PubMed  PubMed Central  Google Scholar 

  61. Schalkwijk CG, Poland DC, van Dijk W, Kok A, Emeis JJ, Drager AM, Doni A, van Hinsbergh VW, Stehouwer CD (1999) Plasma concentration of C-reactive protein is increased in type I diabetic patients without clinical macroangiopathy and correlates with markers of endothelial dysfunction: evidence for chronic inflammation. Diabetologia 42:351–357

    CAS  PubMed  Google Scholar 

  62. Stehouwer CD, Fischer HR, van Kuijk AW, Polak BC, Donker AJ (1995) Endothelial dysfunction precedes development of microalbuminuria in IDDM. Diabetes 44:561–564

    CAS  PubMed  Google Scholar 

  63. Stehouwer CD, Gall MA, Twisk JW, Knudsen E, Emeis JJ, Parving HH (2002) Increased urinary albumin excretion, endothelial dysfunction, and chronic low-grade inflammation in type 2 diabetes: progressive, interrelated, and independently associated with risk of death. Diabetes 51:1157–1165

    CAS  PubMed  Google Scholar 

  64. Deen WM, Lazzara MJ (2004) Glomerular filtration of albumin: how small is the sieving coefficient? Kidney Int Suppl:S63-64.

  65. Deen WM, Lazzara MJ, Myers BD (2001) Structural determinants of glomerular permeability. Am J Physiol Ren Physiol 281:F579–F596

    CAS  Google Scholar 

  66. Endlich K, Kriz W, Witzgall R (2001) Update in podocyte biology. Curr Opin Nephrol Hypertens 10:331–340

    CAS  PubMed  Google Scholar 

  67. Pavenstadt H, Kriz W, Kretzler M (2003) Cell biology of the glomerular podocyte. Physiol Rev 83:253–307

    CAS  PubMed  Google Scholar 

  68. Sharma SG, Spencer T, Gokden N (2010) The significance of foot process effacement in immunoglobulin a nephropathy: clinicopathologic study of 161 cases with light, immunofluorescence and electron microscopic studies. Ultrastruct Pathol 34:279–272

    Google Scholar 

  69. Deegens JK, Dijkman HB, Borm GF, Steenbergen EJ, van den Berg JG, Weening JJ, Wetzels JF (2008) Podocyte foot process effacement as a diagnostic tool in focal segmental glomerulosclerosis. Kidney Int 74:1568–1576

    PubMed  Google Scholar 

  70. Pagtalunan ME, Miller PL, Jumping-Eagle S, Nelson RG, Myers BD, Rennke HG, Coplon NS, Sun L, Meyer TW (1997) Podocyte loss and progressive glomerular injury in type II diabetes. J Clin Invest 99:342–348

    CAS  PubMed  PubMed Central  Google Scholar 

  71. Ballermann BJ (2007) Contribution of the endothelium to the glomerular permselectivity barrier in health and disease. Nephron Physiol 106:p19–p25

    PubMed  Google Scholar 

  72. Satchell SC, Braet F (2009) Glomerular endothelial cell fenestrations: an integral component of the glomerular filtration barrier. Am J Physiol Ren Physiol 296:F947–F956

    CAS  Google Scholar 

  73. Hjalmarsson C, Johansson BR, Haraldsson B (2004) Electron microscopic evaluation of the endothelial surface layer of glomerular capillaries. Microvasc Res 67:9–17

    PubMed  Google Scholar 

  74. Rostgaard J, Qvortrup K (2002) Sieve plugs in fenestrae of glomerular capillaries–site of the filtration barrier? Cells Tissues Organs 170:132–138

    PubMed  Google Scholar 

  75. Huxley VH, Williams DA (2000) Role of a glycocalyx on coronary arteriole permeability to proteins: evidence from enzyme treatments. Am J Physiol Heart Circ Physiol 278:H1177–H1185

    CAS  PubMed  Google Scholar 

  76. Ballermann BJ, Stan RV (2007) Resolved: capillary endothelium is a major contributor to the glomerular filtration barrier. J Am Soc Nephrol 18:2432–2438

    PubMed  Google Scholar 

  77. Singh A, Satchell SC, Neal CR, McKenzie EA, Tooke JE, Mathieson PW (2007) Glomerular endothelial glycocalyx constitutes a barrier to protein permeability. J Am Soc Nephrol 18:2885–2893

    CAS  PubMed  Google Scholar 

  78. Jeansson M, Haraldsson B (2006) Morphological and functional evidence for an important role of the endothelial cell glycocalyx in the glomerular barrier. Am J Physiol Ren Physiol 290:F111–F116

    CAS  Google Scholar 

  79. Ryan GB, Karnovsky MJ (1976) Distribution of endogenous albumin in the rat glomerulus: role of hemodynamic factors in glomerular barrier function. Kidney Int 9:36–45

    CAS  PubMed  Google Scholar 

  80. Henry CB, Duling BR (2000) TNF-alpha increases entry of macromolecules into luminal endothelial cell glycocalyx. Am J Physiol Heart Circ Physiol 279:H2815–H2823

    CAS  PubMed  Google Scholar 

  81. Yoshioka T, Ichikawa I, Fogo A (1991) Reactive oxygen metabolites cause massive, reversible proteinuria and glomerular sieving defect without apparent ultrastructural abnormality. J Am Soc Nephrol 2:902–912

    CAS  PubMed  Google Scholar 

  82. Kuwabara A, Satoh M, Tomita N, Sasaki T, Kashihara N (2010) Deterioration of glomerular endothelial surface layer induced by oxidative stress is implicated in altered permeability of macromolecules in Zucker fatty rats. Diabetologia 53:2056–2065

    CAS  PubMed  PubMed Central  Google Scholar 

  83. Dalla Vestra M, Saller A, Bortoloso E, Mauer M, Fioretto P (2000) Structural involvement in type 1 and type 2 diabetic nephropathy. Diab Metab 26(Suppl 4):8–14

    CAS  Google Scholar 

  84. Fioretto P, Stehouwer CD, Mauer M, Chiesura-Corona M, Brocco E, Carraro A, Bortoloso E, van Hinsbergh VW, Crepaldi G, Nosadini R (1998) Heterogeneous nature of microalbuminuria in NIDDM: studies of endothelial function and renal structure. Diabetologia 41:233–236

    CAS  PubMed  Google Scholar 

  85. Karumanchi SA, Epstein FH, Stillman IE (2005) Is loss of podocyte foot processes necessary for the induction of proteinuria? Am J Kidney Dis 45:436

    PubMed  Google Scholar 

  86. Lemley KV, Blouch K, Abdullah I, Boothroyd DB, Bennett PH, Myers BD, Nelson RG (2000) Glomerular permselectivity at the onset of nephropathy in type 2 diabetes mellitus. J Am Soc Nephrol 11:2095–2105

    CAS  PubMed  Google Scholar 

  87. Nieuwdorp M, van Haeften TW, Gouverneur MC, Mooij HL, van Lieshout MH, Levi M, Meijers JC, Holleman F, Hoekstra JB, Vink H, Kastelein JJ, Stroes ES (2006) Loss of endothelial glycocalyx during acute hyperglycemia coincides with endothelial dysfunction and coagulation activation in vivo. Diabetes 55:480–486

    CAS  PubMed  Google Scholar 

  88. Nieuwdorp M, Mooij HL, Kroon J, Atasever B, Spaan JA, Ince C, Holleman F, Diamant M, Heine RJ, Hoekstra JB, Kastelein JJ, Stroes ES, Vink H (2006) Endothelial glycocalyx damage coincides with microalbuminuria in type 1 diabetes. Diabetes 55:1127–1132

    CAS  PubMed  Google Scholar 

  89. Jeansson M, Granqvist AB, Nystrom JS, Haraldsson B (2006) Functional and molecular alterations of the glomerular barrier in long-term diabetes in mice. Diabetologia 49:2200–2209

    CAS  PubMed  Google Scholar 

  90. Jensen JS, Borch-Johnsen K, Deckert T, Deckert M, Jensen G, Feldt-Rasmussen B (1995) Reduced glomerular size- and charge-selectivity in clinically healthy individuals with microalbuminuria. Eur J Clin Invest 25:608–614

    CAS  PubMed  Google Scholar 

  91. Deckert T, Kofoed-Enevoldsen A, Vidal P, Norgaard K, Andreasen HB, Feldt-Rasmussen B (1993) Size- and charge selectivity of glomerular filtration in Type 1 (insulin-dependent) diabetic patients with and without albuminuria. Diabetologia 36:244–251

    CAS  PubMed  Google Scholar 

  92. Noble MI, Drake-Holland AJ, Vink H (2008) Hypothesis: arterial glycocalyx dysfunction is the first step in the atherothrombotic process. QJM 101:513–518

    CAS  PubMed  Google Scholar 

  93. Cook J, Daneman D, Spino M, Sochett E, Perlman K, Balfe JW (1990) Angiotensin converting enzyme inhibitor therapy to decrease microalbuminuria in normotensive children with insulin-dependent diabetes mellitus. J Pediatr 117:39–45

    CAS  PubMed  Google Scholar 

  94. 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  Google Scholar 

  95. (2009) Adolescent type 1 Diabetes Cardio-renal Intervention Trial (AdDIT). BMC Pediatr 9:79.

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Correspondence to Anurag Singh.

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1. a

2. d

3. c

4. b

5. d

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Singh, A., Satchell, S. Microalbuminuria: causes and implications. Pediatr Nephrol 26, 1957–1965 (2011). https://doi.org/10.1007/s00467-011-1777-1

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