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Published in: BMC Cardiovascular Disorders 1/2020

Open Access 01-12-2020 | Arterial Occlusive Disease | Research article

Patterns of urinary albumin and IgM associate with markers of vascular ageing in young to middle-aged individuals in the Malmö offspring study

Authors: Per Swärd, Rafid Tofik, Omran Bakoush, Ole Torffvit, Peter M. Nilsson, Anders Christensson

Published in: BMC Cardiovascular Disorders | Issue 1/2020

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Abstract

Background

Increased urinary excretion of IgM and low-grade albuminuria are associated with increased risk of cardiovascular morbidity and mortality. The objective of this study was to investigate the association between urinary IgM, albuminuria, and vascular parameters reflecting arterial structure and function.

Methods

Subjects of the present study were from the Malmö Offspring study (MOS) cohort, and included 1531 offspring (children and grand-children) to first-generation subjects that participated in the Malmö Diet Cancer-Cardiovascular Arm study cohort. At baseline, technical measurements of arterial stiffness (carotid-femoral pulse wave velocity; c-f PWV), carotid arterial morphology, 24-h ambulatory blood pressure recordings, ankle-brachial-index (ABI), and evaluation of endothelial function (reactive hyperemia index, RHI) were performed. Urinary (U) IgM, U-albumin, and U-creatinine were measured. Multivariate adjusted logistic regression was used to test whether U-IgM excretion and increasing urinary albumin excretion were related to vascular parameters.

Results

Detectable U-IgM was independently associated with higher systolic blood pressure, odds ratio (OR) 1.021, 95% confidence interval (CI, 1.003–1.039), p = 0.025 and lower ABI; ABI dx: OR 0.026, 95% CI (0.002–0.381), p = 0.008, ABI sin: OR 0.040, 95% CI (0.003–0.496), p = 0.012. Low-grade albuminuria was independently associated with systolic and diastolic blood pressure, aortic blood pressure, the c-f PWV and the number of carotid intima plaques (p < 0.05).

Conclusions

In young to middle-aged, mostly healthy individuals, increased U-IgM excretion and low-grade albuminuria are associated with adverse vascular parameters. Increased U-IgM excretion may reflect subclinical peripheral atherosclerosis, whereas increased U-albumin excretion is associated with a wide range of cardiovascular abnormalities. This may reflect different pathophysiological mechanisms.
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Literature
1.
go back to reference Go AS, Chertow GM, Fan D, McCulloch CE, Hsu CY. Chronic kidney disease and the risks of death, cardiovascular events, and hospitalization. N Engl J Med. 2004;351(13):1296–305.PubMed Go AS, Chertow GM, Fan D, McCulloch CE, Hsu CY. Chronic kidney disease and the risks of death, cardiovascular events, and hospitalization. N Engl J Med. 2004;351(13):1296–305.PubMed
2.
go back to reference Weiner DE, Tighiouart H, Amin MG, Stark PC, MacLeod B, Griffith JL, et al. Chronic kidney disease as a risk factor for cardiovascular disease and all-cause mortality: a pooled analysis of community-based studies. J Am Soc Nephrol. 2004;15(5):1307–15.PubMed Weiner DE, Tighiouart H, Amin MG, Stark PC, MacLeod B, Griffith JL, et al. Chronic kidney disease as a risk factor for cardiovascular disease and all-cause mortality: a pooled analysis of community-based studies. J Am Soc Nephrol. 2004;15(5):1307–15.PubMed
3.
go back to reference Bonarjee VVS. Arterial stiffness: a prognostic marker in coronary heart disease. Available Methods and Clinical Application. Front Cardiovasc Med. 2018;5:64.PubMedPubMedCentral Bonarjee VVS. Arterial stiffness: a prognostic marker in coronary heart disease. Available Methods and Clinical Application. Front Cardiovasc Med. 2018;5:64.PubMedPubMedCentral
4.
go back to reference Laurent S, Boutouyrie P, Asmar R, Gautier I, Laloux B, Guize L, et al. Aortic stiffness is an independent predictor of all-cause and cardiovascular mortality in hypertensive patients. Hypertension. 2001;37(5):1236–41.PubMed Laurent S, Boutouyrie P, Asmar R, Gautier I, Laloux B, Guize L, et al. Aortic stiffness is an independent predictor of all-cause and cardiovascular mortality in hypertensive patients. Hypertension. 2001;37(5):1236–41.PubMed
5.
go back to reference Verbeke F, Van Biesen W, Honkanen E, Wikstrom B, Jensen PB, Krzesinski JM, et al. Prognostic value of aortic stiffness and calcification for cardiovascular events and mortality in dialysis patients: outcome of the calcification outcome in renal disease (CORD) study. Clin J Am Soc Nephrol. 2011;6(1):153–9.PubMedPubMedCentral Verbeke F, Van Biesen W, Honkanen E, Wikstrom B, Jensen PB, Krzesinski JM, et al. Prognostic value of aortic stiffness and calcification for cardiovascular events and mortality in dialysis patients: outcome of the calcification outcome in renal disease (CORD) study. Clin J Am Soc Nephrol. 2011;6(1):153–9.PubMedPubMedCentral
6.
go back to reference Ankle Brachial Index C, Fowkes FG, Murray GD, Butcher I, Heald CL, Lee RJ, et al. Ankle brachial index combined with Framingham Risk Score to predict cardiovascular events and mortality: a meta-analysis. JAMA. 2008;300(2):197–208. Ankle Brachial Index C, Fowkes FG, Murray GD, Butcher I, Heald CL, Lee RJ, et al. Ankle brachial index combined with Framingham Risk Score to predict cardiovascular events and mortality: a meta-analysis. JAMA. 2008;300(2):197–208.
7.
go back to reference Fowkes FG, Murray GD, Butcher I, Folsom AR, Hirsch AT, Couper DJ, et al. Development and validation of an ankle brachial index risk model for the prediction of cardiovascular events. Eur J Prev Cardiol. 2014;21(3):310–20.PubMed Fowkes FG, Murray GD, Butcher I, Folsom AR, Hirsch AT, Couper DJ, et al. Development and validation of an ankle brachial index risk model for the prediction of cardiovascular events. Eur J Prev Cardiol. 2014;21(3):310–20.PubMed
8.
go back to reference American College of Cardiology F, American Heart Association task F, Society for Cardiovascular a, interventions, Society of Interventional R, Society for Vascular M, Society for Vascular S, et al. 2011 ACCF/AHA focused update of the guideline for the management of patients with peripheral artery disease (updating the 2005 guideline). Vasc Med. 2011;16(6):452–76. American College of Cardiology F, American Heart Association task F, Society for Cardiovascular a, interventions, Society of Interventional R, Society for Vascular M, Society for Vascular S, et al. 2011 ACCF/AHA focused update of the guideline for the management of patients with peripheral artery disease (updating the 2005 guideline). Vasc Med. 2011;16(6):452–76.
9.
go back to reference Tofik R, Sward P, Ekelund U, Struglics A, Torffvit O, Rippe B, et al. Plasma pro-inflammatory cytokines, IgM-uria and cardiovascular events in patients with chest pain: a comparative study. Scand J Clin Lab Invest. 2015;75(8):638–45.PubMed Tofik R, Sward P, Ekelund U, Struglics A, Torffvit O, Rippe B, et al. Plasma pro-inflammatory cytokines, IgM-uria and cardiovascular events in patients with chest pain: a comparative study. Scand J Clin Lab Invest. 2015;75(8):638–45.PubMed
10.
go back to reference Tofik R, Torffvit O, Rippe B, Bakoush O. Increased urine IgM excretion predicts cardiovascular events in patients with type 1 diabetes nephropathy. BMC Med. 2009;7:39.PubMedPubMedCentral Tofik R, Torffvit O, Rippe B, Bakoush O. Increased urine IgM excretion predicts cardiovascular events in patients with type 1 diabetes nephropathy. BMC Med. 2009;7:39.PubMedPubMedCentral
11.
go back to reference Arnlov J, Evans JC, Meigs JB, Wang TJ, Fox CS, Levy D, et al. Low-grade albuminuria and incidence of cardiovascular disease events in nonhypertensive and nondiabetic individuals: the Framingham heart study. Circulation. 2005;112(7):969–75.PubMed Arnlov J, Evans JC, Meigs JB, Wang TJ, Fox CS, Levy D, et al. Low-grade albuminuria and incidence of cardiovascular disease events in nonhypertensive and nondiabetic individuals: the Framingham heart study. Circulation. 2005;112(7):969–75.PubMed
12.
go back to reference Gerstein HC, Mann JF, Yi Q, Zinman B, Dinneen SF, Hoogwerf B, et al. Albuminuria and risk of cardiovascular events, death, and heart failure in diabetic and nondiabetic individuals. JAMA. 2001;286(4):421–6.PubMed Gerstein HC, Mann JF, Yi Q, Zinman B, Dinneen SF, Hoogwerf B, et al. Albuminuria and risk of cardiovascular events, death, and heart failure in diabetic and nondiabetic individuals. JAMA. 2001;286(4):421–6.PubMed
13.
go back to reference Klausen K, Borch-Johnsen K, Feldt-Rasmussen B, Jensen G, Clausen P, Scharling H, et al. Very low levels of microalbuminuria are associated with increased risk of coronary heart disease and death independently of renal function, hypertension, and diabetes. Circulation. 2004;110(1):32–5.PubMed Klausen K, Borch-Johnsen K, Feldt-Rasmussen B, Jensen G, Clausen P, Scharling H, et al. Very low levels of microalbuminuria are associated with increased risk of coronary heart disease and death independently of renal function, hypertension, and diabetes. Circulation. 2004;110(1):32–5.PubMed
14.
go back to reference Reinhard H, Wiinberg N, Hansen PR, Kjaer A, Petersen CL, Winther K, et al. NT-proBNP levels, atherosclerosis and vascular function in asymptomatic type 2 diabetic patients with microalbuminuria: peripheral reactive hyperaemia index but not NT-proBNP is an independent predictor of coronary atherosclerosis. Cardiovasc Diabetol. 2011;10:71.PubMedPubMedCentral Reinhard H, Wiinberg N, Hansen PR, Kjaer A, Petersen CL, Winther K, et al. NT-proBNP levels, atherosclerosis and vascular function in asymptomatic type 2 diabetic patients with microalbuminuria: peripheral reactive hyperaemia index but not NT-proBNP is an independent predictor of coronary atherosclerosis. Cardiovasc Diabetol. 2011;10:71.PubMedPubMedCentral
15.
go back to reference Lee YH, Kweon SS, Choi JS, Rhee JA, Nam HS, Jeong SK, et al. Determining the optimal cut-off value of the urinary albumin-to-creatinine ratio to detect atherosclerotic vascular diseases. Kidney Blood Press Res. 2012;36(1):290–300.PubMed Lee YH, Kweon SS, Choi JS, Rhee JA, Nam HS, Jeong SK, et al. Determining the optimal cut-off value of the urinary albumin-to-creatinine ratio to detect atherosclerotic vascular diseases. Kidney Blood Press Res. 2012;36(1):290–300.PubMed
16.
go back to reference Tofik R, Torffvit O, Rippe B, Bakoush O. Urine IgM-excretion as a prognostic marker for progression of type 2 diabetic nephropathy. Diabetes Res Clin Pract. 2012;95(1):139–44.PubMed Tofik R, Torffvit O, Rippe B, Bakoush O. Urine IgM-excretion as a prognostic marker for progression of type 2 diabetic nephropathy. Diabetes Res Clin Pract. 2012;95(1):139–44.PubMed
17.
go back to reference Tofik R, Ekelund U, Torffvit O, Sward P, Rippe B, Bakoush O. Increased urinary IgM excretion in patients with chest pain due to coronary artery disease. BMC Cardiovasc Disord. 2013;13:72.PubMedPubMedCentral Tofik R, Ekelund U, Torffvit O, Sward P, Rippe B, Bakoush O. Increased urinary IgM excretion in patients with chest pain due to coronary artery disease. BMC Cardiovasc Disord. 2013;13:72.PubMedPubMedCentral
18.
go back to reference Tencer J, Frick IM, Oquist BW, Alm P, Rippe B. Size-selectivity of the glomerular barrier to high molecular weight proteins: upper size limitations of shunt pathways. Kidney Int. 1998;53(3):709–15.PubMed Tencer J, Frick IM, Oquist BW, Alm P, Rippe B. Size-selectivity of the glomerular barrier to high molecular weight proteins: upper size limitations of shunt pathways. Kidney Int. 1998;53(3):709–15.PubMed
19.
go back to reference Bakoush O, Segelmark M, Torffvit O, Ohlsson S, Tencer J. Urine IgM excretion predicts outcome in ANCA-associated renal vasculitis. Nephrol Dial Transplant. 2006;21(5):1263–9.PubMed Bakoush O, Segelmark M, Torffvit O, Ohlsson S, Tencer J. Urine IgM excretion predicts outcome in ANCA-associated renal vasculitis. Nephrol Dial Transplant. 2006;21(5):1263–9.PubMed
20.
go back to reference Haraldsson B, Nystrom J, Deen WM. Properties of the glomerular barrier and mechanisms of proteinuria. Physiol Rev. 2008;88(2):451–87.PubMed Haraldsson B, Nystrom J, Deen WM. Properties of the glomerular barrier and mechanisms of proteinuria. Physiol Rev. 2008;88(2):451–87.PubMed
21.
go back to reference Nilsson PM, Boutouyrie P, Cunha P, Kotsis V, Narkiewicz K, Parati G, et al. Early vascular ageing in translation: from laboratory investigations to clinical applications in cardiovascular prevention. J Hypertens. 2013;31(8):1517–26.PubMed Nilsson PM, Boutouyrie P, Cunha P, Kotsis V, Narkiewicz K, Parati G, et al. Early vascular ageing in translation: from laboratory investigations to clinical applications in cardiovascular prevention. J Hypertens. 2013;31(8):1517–26.PubMed
22.
go back to reference Hedblad B, Nilsson P, Janzon L, Berglund G. Relation between insulin resistance and carotid intima-media thickness and stenosis in non-diabetic subjects. Results from a cross-sectional study in Malmo, Sweden. Diabet Med. 2000;17(4):299–307.PubMed Hedblad B, Nilsson P, Janzon L, Berglund G. Relation between insulin resistance and carotid intima-media thickness and stenosis in non-diabetic subjects. Results from a cross-sectional study in Malmo, Sweden. Diabet Med. 2000;17(4):299–307.PubMed
23.
go back to reference Ottosson F, Brunkwall L, Ericson U, Nilsson PM, Almgren P, Fernandez C, et al. Connection between BMI-related plasma metabolite profile and gut microbiota. J Clin Endocrinol Metab. 2018;103(4):1491–501.PubMed Ottosson F, Brunkwall L, Ericson U, Nilsson PM, Almgren P, Fernandez C, et al. Connection between BMI-related plasma metabolite profile and gut microbiota. J Clin Endocrinol Metab. 2018;103(4):1491–501.PubMed
24.
go back to reference Jonsson D, Orho-Melander M, Demmer RT, Engstrom G, Melander O, Klinge B, et al. Periodontal disease is associated with carotid plaque area: the Malmo offspring dental study (MODS). J Intern Med 2020;287(3):301-9. Jonsson D, Orho-Melander M, Demmer RT, Engstrom G, Melander O, Klinge B, et al. Periodontal disease is associated with carotid plaque area: the Malmo offspring dental study (MODS). J Intern Med 2020;287(3):301-9.
25.
go back to reference Chahal S, Vohra K, Syngle A. Association of sudomotor function with peripheral artery disease in type 2 diabetes. Neurol Sci. 2017;38(1):151–6.PubMed Chahal S, Vohra K, Syngle A. Association of sudomotor function with peripheral artery disease in type 2 diabetes. Neurol Sci. 2017;38(1):151–6.PubMed
26.
go back to reference Fatehali AA, Gottsater M, Nilsson PM. Family history of cardiometabolic diseases and its association with arterial stiffness in the Malmo diet Cancer cohort. J Hypertens. 2017;35(11):2262–7.PubMed Fatehali AA, Gottsater M, Nilsson PM. Family history of cardiometabolic diseases and its association with arterial stiffness in the Malmo diet Cancer cohort. J Hypertens. 2017;35(11):2262–7.PubMed
27.
go back to reference Gottsater M, Hindy G, Orho-Melander M, Nilsson PM, Melander O. A genetic risk score for fasting plasma glucose is independently associated with arterial stiffness: a Mendelian randomization study. J Hypertens. 2018;36(4):809–14.PubMed Gottsater M, Hindy G, Orho-Melander M, Nilsson PM, Melander O. A genetic risk score for fasting plasma glucose is independently associated with arterial stiffness: a Mendelian randomization study. J Hypertens. 2018;36(4):809–14.PubMed
28.
go back to reference Muhammad IF, Borne Y, Ostling G, Kennback C, Gottsater M, Persson M, et al. Arterial stiffness and incidence of diabetes: a population-based cohort study. Diabetes Care. 2017;40(12):1739–45.PubMed Muhammad IF, Borne Y, Ostling G, Kennback C, Gottsater M, Persson M, et al. Arterial stiffness and incidence of diabetes: a population-based cohort study. Diabetes Care. 2017;40(12):1739–45.PubMed
29.
go back to reference Rosvall M, Janzon L, Berglund G, Engstrom G, Hedblad B. Incident coronary events and case fatality in relation to common carotid intima-media thickness. J Intern Med. 2005;257(5):430–7.PubMed Rosvall M, Janzon L, Berglund G, Engstrom G, Hedblad B. Incident coronary events and case fatality in relation to common carotid intima-media thickness. J Intern Med. 2005;257(5):430–7.PubMed
30.
go back to reference Bassareo PP, Fanos V, Puddu M, Demuru P, Cadeddu F, Balzarini M, et al. Reduced brachial flow-mediated vasodilation in young adult ex extremely low birth weight preterm: a condition predictive of increased cardiovascular risk? J Matern Fetal Neonatal Med. 2010;23(Suppl 3):121–4.PubMed Bassareo PP, Fanos V, Puddu M, Demuru P, Cadeddu F, Balzarini M, et al. Reduced brachial flow-mediated vasodilation in young adult ex extremely low birth weight preterm: a condition predictive of increased cardiovascular risk? J Matern Fetal Neonatal Med. 2010;23(Suppl 3):121–4.PubMed
31.
go back to reference Bjork J, Grubb A, Larsson A, Hansson LO, Flodin M, Sterner G, et al. Accuracy of GFR estimating equations combining standardized cystatin C and creatinine assays: a cross-sectional study in Sweden. Clin Chem Lab Med. 2015;53(3):403–14.PubMed Bjork J, Grubb A, Larsson A, Hansson LO, Flodin M, Sterner G, et al. Accuracy of GFR estimating equations combining standardized cystatin C and creatinine assays: a cross-sectional study in Sweden. Clin Chem Lab Med. 2015;53(3):403–14.PubMed
32.
go back to reference Grubb A, Horio M, Hansson LO, Bjork J, Nyman U, Flodin M, et al. Generation of a new cystatin C-based estimating equation for glomerular filtration rate by use of 7 assays standardized to the international calibrator. Clin Chem. 2014;60(7):974–86.PubMed Grubb A, Horio M, Hansson LO, Bjork J, Nyman U, Flodin M, et al. Generation of a new cystatin C-based estimating equation for glomerular filtration rate by use of 7 assays standardized to the international calibrator. Clin Chem. 2014;60(7):974–86.PubMed
33.
go back to reference Kyhse-Andersen J, Schmidt C, Nordin G, Andersson B, Nilsson-Ehle P, Lindstrom V, et al. Serum cystatin C, determined by a rapid, automated particle-enhanced turbidimetric method, is a better marker than serum creatinine for glomerular filtration rate. Clin Chem. 1994;40(10):1921–6.PubMed Kyhse-Andersen J, Schmidt C, Nordin G, Andersson B, Nilsson-Ehle P, Lindstrom V, et al. Serum cystatin C, determined by a rapid, automated particle-enhanced turbidimetric method, is a better marker than serum creatinine for glomerular filtration rate. Clin Chem. 1994;40(10):1921–6.PubMed
34.
go back to reference Friedewald WT, Levy RI, Fredrickson DS. Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem. 1972;18(6):499–502. Friedewald WT, Levy RI, Fredrickson DS. Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem. 1972;18(6):499–502.
35.
go back to reference Bjork J, Grubb A, Sterner G, Nyman U. Revised equations for estimating glomerular filtration rate based on the Lund-Malmo study cohort. Scand J Clin Lab Invest. 2011;71(3):232–9.PubMed Bjork J, Grubb A, Sterner G, Nyman U. Revised equations for estimating glomerular filtration rate based on the Lund-Malmo study cohort. Scand J Clin Lab Invest. 2011;71(3):232–9.PubMed
36.
go back to reference Tencer J, Torffvit O, Thysell H, Rippe B, Grubb A. Proteinuria selectivity index based upon alpha 2-macroglobulin or IgM is superior to the IgG based index in differentiating glomerular diseases. Technical note. Kidney Int. 1998;54(6):2098–105.PubMed Tencer J, Torffvit O, Thysell H, Rippe B, Grubb A. Proteinuria selectivity index based upon alpha 2-macroglobulin or IgM is superior to the IgG based index in differentiating glomerular diseases. Technical note. Kidney Int. 1998;54(6):2098–105.PubMed
37.
go back to reference Linton MRF, Yancey PG, Davies SS, Jerome WG, Linton EF, Song WL, et al. The Role of Lipids and Lipoproteins in Atherosclerosis. In: Feingold KR, Anawalt B, Boyce A, Chrousos G, Dungan K, Grossman A, Hershman JM, Kaltsas G, Koch C, Kopp P, editors. et al Endotext. South Dartmouth (MA); 2000. Linton MRF, Yancey PG, Davies SS, Jerome WG, Linton EF, Song WL, et al. The Role of Lipids and Lipoproteins in Atherosclerosis. In: Feingold KR, Anawalt B, Boyce A, Chrousos G, Dungan K, Grossman A, Hershman JM, Kaltsas G, Koch C, Kopp P, editors. et al Endotext. South Dartmouth (MA); 2000.
38.
go back to reference Tofik R, Ohlsson S, Bakoush O. Urinary concentration of monocyte chemoattractant protein-1 in idiopathic glomerulonephritis: a long-term follow-up study. PLoS One. 2014;9(1):e87857.PubMedPubMedCentral Tofik R, Ohlsson S, Bakoush O. Urinary concentration of monocyte chemoattractant protein-1 in idiopathic glomerulonephritis: a long-term follow-up study. PLoS One. 2014;9(1):e87857.PubMedPubMedCentral
39.
go back to reference Bakoush O, Tencer J, Torffvit O, Tenstad O, Skogvall I, Rippe B. Increased glomerular albumin permeability in old spontaneously hypertensive rats. Nephrol Dial Transplant. 2004;19(7):1724–31.PubMed Bakoush O, Tencer J, Torffvit O, Tenstad O, Skogvall I, Rippe B. Increased glomerular albumin permeability in old spontaneously hypertensive rats. Nephrol Dial Transplant. 2004;19(7):1724–31.PubMed
40.
go back to reference Diamond JR. Analogous pathobiologic mechanisms in glomerulosclerosis and atherosclerosis. Kidney Int Suppl. 1991;31:S29–34.PubMed Diamond JR. Analogous pathobiologic mechanisms in glomerulosclerosis and atherosclerosis. Kidney Int Suppl. 1991;31:S29–34.PubMed
41.
go back to reference Rippe C, Rippe A, Larsson A, Asgeirsson D, Rippe B. Nature of glomerular capillary permeability changes following acute renal ischemia-reperfusion injury in rats. Am J Physiol Ren Physiol. 2006;291(6):F1362–8. Rippe C, Rippe A, Larsson A, Asgeirsson D, Rippe B. Nature of glomerular capillary permeability changes following acute renal ischemia-reperfusion injury in rats. Am J Physiol Ren Physiol. 2006;291(6):F1362–8.
42.
go back to reference Marshall SM. Natural history and clinical characteristics of CKD in type 1 and type 2 diabetes mellitus. Adv Chronic Kidney Dis. 2014;21(3):267–72.PubMed Marshall SM. Natural history and clinical characteristics of CKD in type 1 and type 2 diabetes mellitus. Adv Chronic Kidney Dis. 2014;21(3):267–72.PubMed
43.
go back to reference Toyama T, Furuichi K, Ninomiya T, Shimizu M, Hara A, Iwata Y, et al. The impacts of albuminuria and low eGFR on the risk of cardiovascular death, all-cause mortality, and renal events in diabetic patients: meta-analysis. PLoS One. 2013;8(8):e71810.PubMedPubMedCentral Toyama T, Furuichi K, Ninomiya T, Shimizu M, Hara A, Iwata Y, et al. The impacts of albuminuria and low eGFR on the risk of cardiovascular death, all-cause mortality, and renal events in diabetic patients: meta-analysis. PLoS One. 2013;8(8):e71810.PubMedPubMedCentral
44.
go back to reference Ratto E, Leoncini G, Viazzi F, Vaccaro V, Parodi A, Falqui V, et al. Microalbuminuria and cardiovascular risk assessment in primary hypertension: should threshold levels be revised? Am J Hypertens. 2006;19(7):728–34 discussion 735-726.PubMed Ratto E, Leoncini G, Viazzi F, Vaccaro V, Parodi A, Falqui V, et al. Microalbuminuria and cardiovascular risk assessment in primary hypertension: should threshold levels be revised? Am J Hypertens. 2006;19(7):728–34 discussion 735-726.PubMed
45.
go back to reference Yu Y, Suo L, Yu H, Wang C, Tang H. Insulin resistance and endothelial dysfunction in type 2 diabetes patients with or without microalbuminuria. Diabetes Res Clin Pract. 2004;65(2):95–104.PubMed Yu Y, Suo L, Yu H, Wang C, Tang H. Insulin resistance and endothelial dysfunction in type 2 diabetes patients with or without microalbuminuria. Diabetes Res Clin Pract. 2004;65(2):95–104.PubMed
46.
go back to reference Sward P, Rippe B. Acute and sustained actions of hyperglycaemia on endothelial and glomerular barrier permeability. Acta Physiol (Oxford). 2012;204(3):294–307. Sward P, Rippe B. Acute and sustained actions of hyperglycaemia on endothelial and glomerular barrier permeability. Acta Physiol (Oxford). 2012;204(3):294–307.
47.
go back to reference Axelsson J, Rippe A, Sverrisson K, Rippe B. Scavengers of reactive oxygen species, paracalcitol, RhoA, and Rac-1 inhibitors and tacrolimus inhibit angiotensin II-induced actions on glomerular permeability. Am J Physiol Ren Physiol. 2013;305(3):F237–43. Axelsson J, Rippe A, Sverrisson K, Rippe B. Scavengers of reactive oxygen species, paracalcitol, RhoA, and Rac-1 inhibitors and tacrolimus inhibit angiotensin II-induced actions on glomerular permeability. Am J Physiol Ren Physiol. 2013;305(3):F237–43.
48.
go back to reference Axelsson J, Rippe A, Oberg CM, Rippe B. Rapid, dynamic changes in glomerular permeability to macromolecules during systemic angiotensin II (ANG II) infusion in rats. Am J Physiol Ren Physiol. 2012;303(6):F790–9. Axelsson J, Rippe A, Oberg CM, Rippe B. Rapid, dynamic changes in glomerular permeability to macromolecules during systemic angiotensin II (ANG II) infusion in rats. Am J Physiol Ren Physiol. 2012;303(6):F790–9.
49.
go back to reference Enhorning S, Wang TJ, Nilsson PM, Almgren P, Hedblad B, Berglund G, et al. Plasma copeptin and the risk of diabetes mellitus. Circulation. 2010;121(19):2102–8.PubMedPubMedCentral Enhorning S, Wang TJ, Nilsson PM, Almgren P, Hedblad B, Berglund G, et al. Plasma copeptin and the risk of diabetes mellitus. Circulation. 2010;121(19):2102–8.PubMedPubMedCentral
Metadata
Title
Patterns of urinary albumin and IgM associate with markers of vascular ageing in young to middle-aged individuals in the Malmö offspring study
Authors
Per Swärd
Rafid Tofik
Omran Bakoush
Ole Torffvit
Peter M. Nilsson
Anders Christensson
Publication date
01-12-2020
Publisher
BioMed Central
Published in
BMC Cardiovascular Disorders / Issue 1/2020
Electronic ISSN: 1471-2261
DOI
https://doi.org/10.1186/s12872-020-01638-3

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