Capillary rarefaction associates with albuminuria: The Maastricht study

Journal of the American Society of Nephrology

Volumn 27, Issue 12, 2016, Pages 3748-3757

  Martens, Remy J H ^a,b   Henry, Ronald M A ^c,d   Houben, Alfons J H M ^c,d   Van Der Kallen, Carla J H ^c,d   Kroon, Abraham A ^c,d   Schalkwijk, Casper G ^c,d   Schram, Miranda T ^c,d   Sep, Simone J S ^c,d   Schaper, Nicolaas C ^c,d,e   Dagnelie, Pieter C ^d,e,f   Muris, Dennis M J ^c,d   Gronenschild, Ed H B M ^c,e   Van Der Sande, Frank M ^a   Leunissen, Karel M L ^a,b   Kooman, Jeroen P ^a,b   Stehouwer, Coen D A ^c,d  

^a Division of Nephrology   (United States)

^b School of Nutrition and Translational Research in Metabolism   (United States)

^c MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

^d MAASTRICHT UNIVERSITY   (Netherlands)

^e MAASTRICHT UNIVERSITY   (Netherlands)

^f Department of Epidemiology ^*  (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; AGED; ALBUMINURIA; ARTERY OCCLUSION; ARTICLE; BLOOD VESSEL PARAMETERS; CAPILLAROSCOPY; CAPILLARY DENSITY; CAPILLARY RAREFACTION; COHORT ANALYSIS; CROSS-SECTIONAL STUDY; DISEASE ASSOCIATION; FEMALE; HUMAN; HYPEREMIA; KIDNEY FUNCTION; MAJOR CLINICAL STUDY; MALE; MICROCIRCULATION; OBSERVATIONAL STUDY; PRIORITY JOURNAL; PROSPECTIVE STUDY; SKIN CAPILLARY; VEIN OCCLUSION; VENOUS CONGESTION; CAPILLARY; COMPLICATION; MIDDLE AGED; PATHOLOGY; SKIN; VASCULARIZATION;

ALBUMINURIA; CAPILLARIES; COHORT STUDIES; CROSS-SECTIONAL STUDIES; FEMALE; HUMANS; HYPEREMIA; MALE; MICROCIRCULATION; MIDDLE AGED; PROSPECTIVE STUDIES; SKIN;

EID: 85016935630     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2015111219     Document Type: Article

References (57)

1. Matsushita K, van der Velde M, Astor BC, Woodward M, Levey AS, de Jong PE, Coresh J, Gansevoort RT; Chronic Kidney Disease Prognosis Consortium: 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, 2010
2. Deckert T, Feldt-Rasmussen B, Borch-Johnsen K, Jensen T, Kofoed-Enevoldsen A: Albuminuria reflects widespread vascular damage. The Steno hypothesis. Diabetologia 32: 219-226, 1989
3. Stehouwer CD, Smulders YM: Microalbuminuria and risk for cardiovascular disease: Analysis of potential mechanisms. J Am Soc Nephrol 17: 2106-2111, 2006
4. Brenner BM, Meyer TW, Hostetter TH: Dietary protein intake and the progressive nature of kidney disease: The role of hemodynamically mediated glomerular injury in the pathogenesis of progressive glomerular sclerosis in aging, renal ablation, and intrinsic renal disease. N Engl J Med 307: 652-659, 1982
5. Stehouwer CD, Henry RM, Dekker JM, Nijpels G, Heine RJ, Bouter LM: Microalbuminuria is associated with impaired brachial artery, flowmediated vasodilation in elderly individuals without and with diabetes: Further evidence for a link between microalbuminuria and endothelial dysfunction-The Hoorn Study. Kidney Int Suppl 92: S42-S44, 2004
6. Dogra G, Rich L, Stanton K, Watts GF: Endothelium-dependent and independent vasodilation studies at normoglycaemia in type I diabetes mellitus with andwithout microalbuminuria. Diabetologia 44: 593-601, 2001
7. Poredos P, Kek A: Relation of blunted dilation of the brachial artery in insulin-dependent diabetesmellitus to microalbuminuria. AmJ Cardiol 86: 364-367, 2000
8. Clausen P, Jensen JS, Jensen G, Borch-Johnsen K, Feldt-Rasmussen B: Elevated urinary albumin excretion is associated with impaired arterial dilatory capacity in clinically healthy subjects. Circulation 103: 1869-1874, 2001
9. Papaioannou GI, Seip RL, Grey NJ, Katten D, Taylor A, Inzucchi SE, Young LH, Chyun DA, Davey JA,Wackers FJ, Iskandrian AE, Ratner RE, Robinson EC, Carolan S, Engel S, Heller GV: Brachial artery reactivity in asymptomatic patients with type 2 diabetes mellitus and microalbuminuria (from the Detection of Ischemia in Asymptomatic Diabetics-brachial artery reactivity study). Am J Cardiol 94: 294-299, 2004
10. ZenereBM,ArcaroG, SaggianiF, Rossi L,MuggeoM, LechiA:Noninvasive detection of functional alterations of the arterial wall in IDDM patients with and without microalbuminuria. Diabetes Care 18: 975-982, 1995
11. Cosson E, Pham I, Valensi P, Pariès J, Attali JR, Nitenberg A: Impaired coronary endothelium-dependent vasodilation is associated with microalbuminuria in patients with type 2 diabetes and angiographically normal coronary arteries. Diabetes Care 29: 107-112, 2006
12. StehouwerCD,Nauta JJ, ZeldenrustGC,HackengWH, Donker AJ, den Ottolander GJ: Urinary albumin excretion, cardiovascular disease, and endothelial dysfunction in non-insulin-dependent diabetes mellitus. Lancet 340: 319-323, 1992
13. Stehouwer CD, Gall MA, Twisk JW, Knudsen E, Emeis JJ, Parving HH: 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, 2002
14. Stehouwer CD, Fischer HR, van Kuijk AW, Polak BC, Donker AJ: Endothelial dysfunction precedes development of microalbuminuria in IDDM. Diabetes 44: 561-564, 1995
15. Jager A, van Hinsbergh VW, Kostense PJ, Emeis JJ, Nijpels G, Dekker JM, Heine RJ, Bouter LM, Stehouwer CD: C-reactive protein and soluble vascular cell adhesion molecule-1 are associated with elevated urinary albumin excretion but do not explain its link with cardiovascular risk. Arterioscler Thromb Vasc Biol 22: 593-598, 2002
16. Clausen P, Feldt-Rasmussen B, Jensen G, Jensen JS: Endothelial haemostatic factors are associated with progression of urinary albumin excretion in clinically healthy subjects: A4-year prospective study. Clin Sci (Lond) 97: 37-43, 1999
17. Persson F, Rossing P, Hovind P, Stehouwer CD, Schalkwijk CG, Tarnow L, Parving HH: Endothelial dysfunction and inflammation predict development of diabetic nephropathy in the Irbesartan in Patients with Type 2Diabetes and Microalbuminuria (IRMA 2) study. Scand J Clin Lab Invest 68: 731-738, 2008
18. Feldt-Rasmussen B: Increased transcapillary escape rate of albumin in type 1 (insulin-dependent) diabetic patients with microalbuminuria. Diabetologia 29: 282-286, 1986
19. Nannipieri M, Rizzo L, Rapuano A, Pilo A, Penno G, Navalesi R: Increased transcapillary escape rate of albumin in microalbuminuric type II diabetic patients. Diabetes Care 18: 1-9, 1995
20. Nannipieri M, Penno G, Rizzo L, Pucci L, Bandinelli S, Mattei P, Taddei S, Salvetti A, Navalesi R: Transcapillary escape rate of albumin in type II diabetic patients. The relationship with microalbuminuria and hypertension. Diabetes Care 20: 1019-1026, 1997
21. Jensen EW, Espersen K, Knudsen JH, Nielsen SL: Increased transcapillary escape rate of albumin in elderly subjects due to long-term smoking habits. Clin Physiol 15: 159-167, 1995
22. Guglielmi MD, Pierdomenico SD, Salvatore L, Romano F, Tascione E, Pupillo M, Porreca E, Imbastaro T, Cuccurullo F, Mezzetti A: Impaired left ventricular diastolic function and vascular postischemic vasodilation associated with microalbuminuria in IDDMpatients. Diabetes Care 18: 353-360, 1995
23. Schmiedel O, Schroeter ML, Harvey JN: Microalbuminuria in Type 2 diabetes indicates impaired microvascular vasomotion and perfusion. Am J Physiol Heart Circ Physiol 293: H3424-H3431, 2007
24. Houben AJ, Schaper NC, Slaaf DW, Tangelder GJ, Nieuwenhuijzen Kruseman AC: Skin blood cell flux in insulin-dependent diabetic subjects in relation to retinopathy or incipient nephropathy. Eur J Clin Invest 22: 67-72, 1992
25. Triantafyllou A, Anyfanti P, Zabulis X, Gavriilaki E, Karamaounas P, Gkaliagkousi E, Petidis K, Pyrpasopoulou A, Girasis C, Aslanidis S, Douma S: Accumulation of microvascular target organ damage in newly diagnosed hypertensive patients. J AmSoc Hypertens 8: 542-549, 2014
26. Serné EH, Gans RO, ter Maaten JC, Tangelder GJ, Donker AJ, Stehouwer CD: Impaired skin capillary recruitment in essential hypertension is caused by both functional and structural capillary rarefaction. Hypertension 38: 238-242, 2001
27. Imanishi M, Yoshioka K, Konishi Y, Okumura M, Okada N, Sato T, Tanaka S, Fujii S, Kimura G: Glomerular hypertension as one cause of albuminuria in type II diabetic patients. Diabetologia 42: 999-1005, 1999
28. Novick AC, Gephardt G, Guz B, Steinmuller D, Tubbs RR: Long-term follow-up after partial removal of a solitary kidney. N Engl J Med 325: 1058-1062, 1991
29. Holowatz LA, Thompson-Torgerson CS, Kenney WL: The human cutaneous circulation as a model of generalized microvascular function. J Appl Physiol (1985) 105: 370-372, 2008
30. de Jongh RT, Serné EH, IJzerman RG, Stehouwer CD: Microvascular function: A potential link between salt sensitivity, insulin resistance and hypertension. J Hypertens 25: 1887-1893, 2007
31. Serné EH, Stehouwer CD, ter Maaten JC, terWee PM, Donker AJ,Gans RO: Birth weight relates to blood pressure and microvascular function in normal subjects. J Hypertens 18: 1421-1427, 2000
32. IJzerman RG, van Weissenbruch MM, Voordouw JJ, Yudkin JS, Serne EH, Delemarre-van de Waal HA, Stehouwer CD: The association between birth weight and capillary recruitment is independent of blood pressure and insulin sensitivity: A study in prepubertal children. J Hypertens 20: 1957-1963, 2002
33. Mañalich R, Reyes L, Herrera M, Melendi C, Fundora I: Relationship between weight at birth and the number and size of renal glomeruli in humans: A histomorphometric study. Kidney Int 58: 770-773, 2000
34. Hughson M, Farris AB 3rd, Douglas-Denton R, Hoy WE, Bertram JF: Glomerular number and size in autopsy kidneys: The relationship to birth weight. Kidney Int 63: 2113-2122, 2003
35. Jonk AM, Houben AJ, Schaper NC, de Leeuw PW, Serné EH, Smulders YM, Stehouwer CD: Angiotensin II enhances insulin-stimulated wholebody glucose disposal but impairs insulin-induced capillary recruitment in healthy volunteers. J Clin Endocrinol Metab 95: 3901-3908, 2010
36. Antonios TF, Rattray FE, Singer DR, Markandu ND, Mortimer PS, MacGregor GA:Maximization of skin capillaries during intravital videomicroscopy in essential hypertension: Comparison between venous congestion, reactive hyperaemia and core heat load tests. Clin Sci (Lond) 97: 523-528, 1999
37. Anderson S, Rennke HG, Garcia DL, Brenner BM: Short and long term effects of antihypertensive therapy in the diabetic rat. Kidney Int 36: 526-536, 1989
38. Pelayo JC, Quan AH, Shanley PF: Angiotensin II control of the renal microcirculation in rats with reduced renal mass. Am J Physiol 258: F414-F422, 1990
39. Morales E, Caro J, Gutierrez E, Sevillano A, Auñón P, Fernandez C, Praga M: Diverse diuretics regimens differentially enhance the antialbuminuric effect of renin-angiotensin blockers in patientswith chronic kidney disease. Kidney Int 88: 1434-1441, 2015
40. Kidney Disease: Improving Global Outcomes (KDIGO) Blood Pressure Work Group: KDIGO clinical practice guideline for the management of blood pressure in chronic kidney disease. Kidney Int Suppl 2: 337-414, 2012
41. Birn H, Christensen EI: Renal albumin absorption in physiology and pathology. Kidney Int 69: 440-449, 2006
42. Schisterman EF, Cole SR, Platt RW: Overadjustment bias and unnecessary adjustment in epidemiologic studies. Epidemiology 20: 488-495, 2009
43. Levy BI,Ambrosio G, Pries AR, Struijker-BoudierHA:Microcirculation in hypertension: A new target for treatment? Circulation 104: 735-740, 2001
44. Remuzzi A, Sangalli F, Macconi D, Tomasoni S, Cattaneo I, Rizzo P, Bonandrini B, Bresciani E, Longaretti L, Gagliardini E, Conti S, Benigni A, Remuzzi G: Regression of renal disease by angiotensin II antagonism is caused by regeneration of kidney vasculature. J AmSocNephrol 27: 699-705, 2016
45. Jonk AM, Houben AJ, Schaper NC, de Leeuw PW, Serné EH, Smulders YM, Stehouwer CD: Meal-related increases in microvascular vasomotion are impaired in obese individuals: A potential mechanismin the pathogenesis of obesity-related insulin resistance. Diabetes Care 34 [Suppl 2]: S342-S348, 2011
46. Keske MA, Clerk LH, Price WJ, Jahn LA, Barrett EJ: Obesity blunts microvascular recruitment in human forearmmuscle after amixed meal. Diabetes Care 32: 1672-1677, 2009
47. Clerk LH, Vincent MA, Jahn LA, Liu Z, Lindner JR, Barrett EJ: Obesity blunts insulin-mediated microvascular recruitment in human forearm muscle. Diabetes 55: 1436-1442, 2006
48. SchramMT, Sep SJ, van der Kallen CJ, Dagnelie PC, Koster A, Schaper N, Henry RM, Stehouwer CD: The Maastricht Study: An extensive phenotyping study on determinants of type 2 diabetes, its complications and its comorbidities. Eur J Epidemiol 29: 439-451, 2014
49. Gronenschild EH, Muris DM, Schram MT, Karaca U, Stehouwer CD, Houben AJ: Semi-automatic assessment of skin capillary density: Proof of principle and validation. Microvasc Res 90: 192-198, 2013
50. Inker LA, Schmid CH, Tighiouart H, Eckfeldt JH, Feldman HI, Greene T, Kusek JW, Manzi J, Van Lente F, Zhang YL, Coresh J, Levey AS; CKDEPI Investigators: Estimating glomerular filtration rate from serum creatinine and cystatin C. N Engl J Med 367: 20-29, 2012
51. National Kidney Foundation: K/DOQI clinical practice guidelines for chronic kidney disease: Evaluation, classification, and stratification. Am J Kidney Dis 39[Suppl 1]: S1-S266, 2002
52. Ward KM: Renal function (microalbuminuria). Anal Chem 67: 383R-391R, 1995
53. Spauwen PJ, van Boxtel MP, Verhey FR, Köhler S, Sep SJ, Koster A, Dagnelie PC, Henry RM, Schaper NC, van der Kallen CJ, SchramMT, Kroon AA, Stehouwer CD: Both low and high 24-hour diastolic blood pressure are associated with worse cognitive performance in type 2 diabetes: The Maastricht Study. Diabetes Care 38: 1473-1480, 2015
54. van Dooren FE, Verhey FR, Pouwer F, Schalkwijk CG, Sep SJ, Stehouwer CD, Henry RM, Dagnelie PC, Schaper NC, van der Kallen CJ, Koster A, SchramMT, Denollet J: Association of Type D personality with increased vulnerability to depression: Is there a role for inflammation or endothelial dysfunction?-TheMaastricht Study. J Affect Disord 189: 118-125, 2016
55. Muller CJ, MacLehose RF: Estimating predicted probabilities from logistic regression: Different methods correspond to different target populations. Int J Epidemiol 43: 962-970, 2014
56. Ix JH, Wassel CL, Stevens LA, Beck GJ, Froissart M, Navis G, Rodby R, Torres VE, Zhang YL, Greene T, Levey AS: Equations to estimate creatinine excretion rate: The CKD epidemiology collaboration. Clin J Am Soc Nephrol 6: 184-191, 2011
57. Altman DG: Practical Statistics for Medical Research, London, Chapman and Hall/CRC, 1990, pp 143-145