Skip to main content
Top
Published in: International Urology and Nephrology 12/2015

01-12-2015 | Nephrology - Original Paper

Serum neutrophil gelatinase-associated lipocalin is associated with cardiovascular events in patients with chronic kidney disease

Authors: Yalcin Solak, Mahmut Ilker Yilmaz, Dimitrie Siriopol, Mutlu Saglam, Hilmi Umut Unal, Halil Yaman, Mahmut Gok, Hakki Cetinkaya, Abduzhappar Gaipov, Tayfun Eyileten, Sebahattin Sari, Ali Osman Yildirim, Halil Zeki Tonbul, Suleyman Turk, Adrian Covic, Mehmet Kanbay

Published in: International Urology and Nephrology | Issue 12/2015

Login to get access

Abstract

Background

Neutrophil gelatinase-associated lipocalin (NGAL) is a member of the lipocalin family best known as a novel and early marker of acute kidney injury (AKI). Recent data suggest that NGQueryAL is not only a marker of AKI, but also an important player in the vascular remodeling, atherosclerotic plaque stability and thrombus formation. We conducted this study to investigate the association of serum NGAL levels with fatal and composite (fatal and non-fatal) cardiovascular events (CVE) in a cohort of patients with stage 1–5 CKD.

Methods

This was an observational cohort study in which serum NGAL was obtained from 298 CKD (stages 1–5) patients. Fatal and composite CVE were recorded for a median 41 months. We examined alteration of serum NGAL through CKD groups as well as association with inflammatory markers. We also performed a Cox regression analysis to determine the association of NGAL with predefined clinical outcomes.

Results

The median value of NGAL was 50.5 ng/mL (IR 47.6–54.9 ng/mL), and higher NGAL values were recorded in diabetic patients. In a multiple linear regression model, including all univariate associates of NGAL, only log eGFR, log hs-CRP and log HDL cholesterol maintained an independent association with log NGAL. During the observational period, 30 patients died due to cardiovascular causes and 69 non-fatal CVE were registered. In the fully adjusted model, we observed a 2.08-fold increase in the risk of fatal CVE and a 1.50-fold increase in the risk of fatal and non-fatal CVE for each increment of 1 SD in log NGAL values.

Conclusions

This is the first study that shows that serum NGAL is associated with cardiovascular events (fatal and non-fatal) in patients with CKD, independently of traditional risk factors, renal function and inflammation.
Appendix
Available only for authorised users
Literature
1.
go back to reference Makris K, Rizos D, Kafkas N, Haliassos A (2012) Neutrophil gelatinase-associated lipocalin as a new biomarker in laboratory medicine. Clin Chem Lab Med 50(9):1519–1532CrossRefPubMed Makris K, Rizos D, Kafkas N, Haliassos A (2012) Neutrophil gelatinase-associated lipocalin as a new biomarker in laboratory medicine. Clin Chem Lab Med 50(9):1519–1532CrossRefPubMed
2.
go back to reference Hirsch R, Dent C, Pfriem H, Allen J, Beekman RH 3rd, Ma Q et al (2007) NGAL is an early predictive biomarker of contrast-induced nephropathy in children. Pediatr Nephrol 22(12):2089–2095CrossRefPubMed Hirsch R, Dent C, Pfriem H, Allen J, Beekman RH 3rd, Ma Q et al (2007) NGAL is an early predictive biomarker of contrast-induced nephropathy in children. Pediatr Nephrol 22(12):2089–2095CrossRefPubMed
3.
go back to reference Schilcher G, Ribitsch W, Otto R, Portugaller RH, Quehenberger F, Truschnig-Wilders M et al (2011) Early detection and intervention using neutrophil gelatinase-associated lipocalin (NGAL) may improve renal outcome of acute contrast media induced nephropathy: a randomized controlled trial in patients undergoing intra-arterial angiography (ANTI-CIN Study). BMC Nephrol 12:39PubMedCentralCrossRefPubMed Schilcher G, Ribitsch W, Otto R, Portugaller RH, Quehenberger F, Truschnig-Wilders M et al (2011) Early detection and intervention using neutrophil gelatinase-associated lipocalin (NGAL) may improve renal outcome of acute contrast media induced nephropathy: a randomized controlled trial in patients undergoing intra-arterial angiography (ANTI-CIN Study). BMC Nephrol 12:39PubMedCentralCrossRefPubMed
4.
go back to reference Valette X, Savary B, Nowoczyn M, Daubin C, Pottier V, Terzi N et al (2013) Accuracy of plasma neutrophil gelatinase-associated lipocalin in the early diagnosis of contrast-induced acute kidney injury in critical illness. Intensive Care Med 39(5):857–865CrossRefPubMed Valette X, Savary B, Nowoczyn M, Daubin C, Pottier V, Terzi N et al (2013) Accuracy of plasma neutrophil gelatinase-associated lipocalin in the early diagnosis of contrast-induced acute kidney injury in critical illness. Intensive Care Med 39(5):857–865CrossRefPubMed
5.
go back to reference Alharazy SM, Kong N, Saidin R, Gafor AH, Maskon O, Mohd M et al (2014) Neutrophil gelatinase-associated lipocalin as an early marker of contrast-induced nephropathy after coronary angiography. Angiology 65(3):216–223CrossRefPubMed Alharazy SM, Kong N, Saidin R, Gafor AH, Maskon O, Mohd M et al (2014) Neutrophil gelatinase-associated lipocalin as an early marker of contrast-induced nephropathy after coronary angiography. Angiology 65(3):216–223CrossRefPubMed
6.
go back to reference Filiopoulos V, Biblaki D, Vlassopoulos D (2014) Neutrophil gelatinase-associated lipocalin (NGAL): a promising biomarker of contrast-induced nephropathy after computed tomography. Ren Fail 36(6):976–986CrossRef Filiopoulos V, Biblaki D, Vlassopoulos D (2014) Neutrophil gelatinase-associated lipocalin (NGAL): a promising biomarker of contrast-induced nephropathy after computed tomography. Ren Fail 36(6):976–986CrossRef
7.
go back to reference Mishra J, Dent C, Tarabishi R, Mitsnefes MM, Ma Q, Kelly C et al (2005) Neutrophil gelatinase-associated lipocalin (NGAL) as a biomarker for acute renal injury after cardiac surgery. Lancet 365(9466):1231–1238CrossRefPubMed Mishra J, Dent C, Tarabishi R, Mitsnefes MM, Ma Q, Kelly C et al (2005) Neutrophil gelatinase-associated lipocalin (NGAL) as a biomarker for acute renal injury after cardiac surgery. Lancet 365(9466):1231–1238CrossRefPubMed
8.
go back to reference Dent CL, Ma Q, Dastrala S, Bennett M, Mitsnefes MM, Barasch J et al (2007) Plasma neutrophil gelatinase-associated lipocalin predicts acute kidney injury, morbidity and mortality after pediatric cardiac surgery: a prospective uncontrolled cohort study. Crit Care 11(6):R127PubMedCentralCrossRefPubMed Dent CL, Ma Q, Dastrala S, Bennett M, Mitsnefes MM, Barasch J et al (2007) Plasma neutrophil gelatinase-associated lipocalin predicts acute kidney injury, morbidity and mortality after pediatric cardiac surgery: a prospective uncontrolled cohort study. Crit Care 11(6):R127PubMedCentralCrossRefPubMed
9.
go back to reference Prabhu A, Sujatha DI, Ninan B, Vijayalakshmi MA (2010) Neutrophil gelatinase associated lipocalin as a biomarker for acute kidney injury in patients undergoing coronary artery bypass grafting with cardiopulmonary bypass. Ann Vasc Surg 24(4):525–531CrossRefPubMed Prabhu A, Sujatha DI, Ninan B, Vijayalakshmi MA (2010) Neutrophil gelatinase associated lipocalin as a biomarker for acute kidney injury in patients undergoing coronary artery bypass grafting with cardiopulmonary bypass. Ann Vasc Surg 24(4):525–531CrossRefPubMed
10.
go back to reference Parikh CR, Coca SG, Thiessen-Philbrook H, Shlipak MG, Koyner JL, Wang Z et al (2011) Postoperative biomarkers predict acute kidney injury and poor outcomes after adult cardiac surgery. J Am Soc Nephrol 22(9):1748–1757PubMedCentralCrossRefPubMed Parikh CR, Coca SG, Thiessen-Philbrook H, Shlipak MG, Koyner JL, Wang Z et al (2011) Postoperative biomarkers predict acute kidney injury and poor outcomes after adult cardiac surgery. J Am Soc Nephrol 22(9):1748–1757PubMedCentralCrossRefPubMed
11.
go back to reference Bagshaw SM, Haase M, Haase-Fielitz A, Bennett M, Devarajan P, Bellomo R (2012) A prospective evaluation of urine microscopy in septic and non-septic acute kidney injury. Nephrol Dial Transplant 27(2):582–588CrossRefPubMed Bagshaw SM, Haase M, Haase-Fielitz A, Bennett M, Devarajan P, Bellomo R (2012) A prospective evaluation of urine microscopy in septic and non-septic acute kidney injury. Nephrol Dial Transplant 27(2):582–588CrossRefPubMed
12.
go back to reference Lentini P, de Cal M, Clementi A, D’Angelo A, Ronco C (2012) Sepsis and AKI in ICU patients: the role of plasma biomarkers. Crit Care Res Pract 2012:856401PubMedCentralPubMed Lentini P, de Cal M, Clementi A, D’Angelo A, Ronco C (2012) Sepsis and AKI in ICU patients: the role of plasma biomarkers. Crit Care Res Pract 2012:856401PubMedCentralPubMed
13.
go back to reference Camou F, Oger S, Paroissin C, Guilhon E, Guisset O, Mourissoux G et al (2013) Plasma neutrophil gelatinase-associated lipocalin (NGAL) predicts acute kidney injury in septic shock at ICU admission. Ann Fr Anesth Reanim 32(3):157–164CrossRefPubMed Camou F, Oger S, Paroissin C, Guilhon E, Guisset O, Mourissoux G et al (2013) Plasma neutrophil gelatinase-associated lipocalin (NGAL) predicts acute kidney injury in septic shock at ICU admission. Ann Fr Anesth Reanim 32(3):157–164CrossRefPubMed
14.
go back to reference Xu S, Venge P (2000) Lipocalins as biochemical markers of disease. Biochim Biophys Acta 1482(1–2):298–307CrossRefPubMed Xu S, Venge P (2000) Lipocalins as biochemical markers of disease. Biochim Biophys Acta 1482(1–2):298–307CrossRefPubMed
15.
go back to reference van der Wal AC, Becker AE, van der Loos CM, Das PK (1994) Site of intimal rupture or erosion of thrombosed coronary atherosclerotic plaques is characterized by an inflammatory process irrespective of the dominant plaque morphology. Circulation 89(1):36–44CrossRefPubMed van der Wal AC, Becker AE, van der Loos CM, Das PK (1994) Site of intimal rupture or erosion of thrombosed coronary atherosclerotic plaques is characterized by an inflammatory process irrespective of the dominant plaque morphology. Circulation 89(1):36–44CrossRefPubMed
16.
go back to reference Galis ZS, Muszynski M, Sukhova GK, Simon-Morrissey E, Unemori EN, Lark MW et al (1994) Cytokine-stimulated human vascular smooth muscle cells synthesize a complement of enzymes required for extracellular matrix digestion. Circ Res 75(1):181–189CrossRefPubMed Galis ZS, Muszynski M, Sukhova GK, Simon-Morrissey E, Unemori EN, Lark MW et al (1994) Cytokine-stimulated human vascular smooth muscle cells synthesize a complement of enzymes required for extracellular matrix digestion. Circ Res 75(1):181–189CrossRefPubMed
17.
go back to reference Kai H, Ikeda H, Yasukawa H, Kai M, Seki Y, Kuwahara F et al (1998) Peripheral blood levels of matrix metalloproteases-2 and -9 are elevated in patients with acute coronary syndromes. J Am Coll Cardiol 32(2):368–372CrossRefPubMed Kai H, Ikeda H, Yasukawa H, Kai M, Seki Y, Kuwahara F et al (1998) Peripheral blood levels of matrix metalloproteases-2 and -9 are elevated in patients with acute coronary syndromes. J Am Coll Cardiol 32(2):368–372CrossRefPubMed
18.
go back to reference Cruz DN, Gaiao S, Maisel A, Ronco C, Devarajan P (2012) Neutrophil gelatinase-associated lipocalin as a biomarker of cardiovascular disease: a systematic review. Clin Chem Lab Med 50(9):1533–1545PubMedCentralCrossRefPubMed Cruz DN, Gaiao S, Maisel A, Ronco C, Devarajan P (2012) Neutrophil gelatinase-associated lipocalin as a biomarker of cardiovascular disease: a systematic review. Clin Chem Lab Med 50(9):1533–1545PubMedCentralCrossRefPubMed
19.
go back to reference Alvelos M, Lourenço P, Dias C, Amorim M, Rema J, Leite AB et al (2013) Prognostic value of neutrophil gelatinase-associated lipocalin in acute heart failure. Int J Cardiol 165(1):51–55CrossRefPubMed Alvelos M, Lourenço P, Dias C, Amorim M, Rema J, Leite AB et al (2013) Prognostic value of neutrophil gelatinase-associated lipocalin in acute heart failure. Int J Cardiol 165(1):51–55CrossRefPubMed
20.
go back to reference Yndestad A, Landrø L, Ueland T, Dahl CP, Flo TH, Vinge LE et al (2009) Increased systemic and myocardial expression of neutrophil gelatinase-associated lipocalin in clinical and experimental heart failure. Eur Heart J 30(10):1229–1236CrossRefPubMed Yndestad A, Landrø L, Ueland T, Dahl CP, Flo TH, Vinge LE et al (2009) Increased systemic and myocardial expression of neutrophil gelatinase-associated lipocalin in clinical and experimental heart failure. Eur Heart J 30(10):1229–1236CrossRefPubMed
21.
go back to reference Maisel AS, Mueller C, Fitzgerald R, Brikhan R, Hiestand BC, Iqbal N et al (2011) Prognostic utility of plasma neutrophil gelatinase-associated lipocalin in patients with acute heart failure: the NGAL EvaLuation Along with B-type NaTriuretic Peptide in acutely decompensated heart failure (GALLANT) trial. Eur J Heart Fail 13(8):846–851PubMedCentralCrossRefPubMed Maisel AS, Mueller C, Fitzgerald R, Brikhan R, Hiestand BC, Iqbal N et al (2011) Prognostic utility of plasma neutrophil gelatinase-associated lipocalin in patients with acute heart failure: the NGAL EvaLuation Along with B-type NaTriuretic Peptide in acutely decompensated heart failure (GALLANT) trial. Eur J Heart Fail 13(8):846–851PubMedCentralCrossRefPubMed
22.
go back to reference Falke P, Elneihoum AM, Ohlsson K (2000) Leukocyte activation: relation to cardiovascular mortality after cerebrovascular ischemia. Cerebrovasc Dis 10(2):97–101CrossRefPubMed Falke P, Elneihoum AM, Ohlsson K (2000) Leukocyte activation: relation to cardiovascular mortality after cerebrovascular ischemia. Cerebrovasc Dis 10(2):97–101CrossRefPubMed
23.
go back to reference Bolignano D, Basile G, Parisi P, Coppolino G, Nicocia G, Buemi M (2009) Increased plasma neutrophil gelatinase-associated lipocalin levels predict mortality in elderly patients with chronic heart failure. Rejuvenation Res 12(1):7–14CrossRefPubMed Bolignano D, Basile G, Parisi P, Coppolino G, Nicocia G, Buemi M (2009) Increased plasma neutrophil gelatinase-associated lipocalin levels predict mortality in elderly patients with chronic heart failure. Rejuvenation Res 12(1):7–14CrossRefPubMed
24.
go back to reference Shrestha K, Borowski AG, Troughton RW, Thomas JD, Klein AL, Tang WH (2011) Renal dysfunction is a stronger determinant of systemic neutrophil gelatinase-associated lipocalin levels than myocardial dysfunction in systolic heart failure. J Card Fail 17(6):472–478PubMedCentralCrossRefPubMed Shrestha K, Borowski AG, Troughton RW, Thomas JD, Klein AL, Tang WH (2011) Renal dysfunction is a stronger determinant of systemic neutrophil gelatinase-associated lipocalin levels than myocardial dysfunction in systolic heart failure. J Card Fail 17(6):472–478PubMedCentralCrossRefPubMed
25.
go back to reference Whitman IR, Feldman HI, Deo R (2012) CKD and sudden cardiac death: epidemiology, mechanisms, and therapeutic approaches. J Am Soc Nephrol 23(12):1929–1939PubMedCentralCrossRefPubMed Whitman IR, Feldman HI, Deo R (2012) CKD and sudden cardiac death: epidemiology, mechanisms, and therapeutic approaches. J Am Soc Nephrol 23(12):1929–1939PubMedCentralCrossRefPubMed
26.
go back to reference Bolignano D, Donato V, Coppolino G, Campo S, Buemi A, Lacquaniti A et al (2008) Neutrophil gelatinase-associated lipocalin (NGAL) as a marker of kidney damage. Am J Kidney Dis 52(3):595–605CrossRefPubMed Bolignano D, Donato V, Coppolino G, Campo S, Buemi A, Lacquaniti A et al (2008) Neutrophil gelatinase-associated lipocalin (NGAL) as a marker of kidney damage. Am J Kidney Dis 52(3):595–605CrossRefPubMed
27.
go back to reference Bolignano D, Coppolino G, Campo S, Aloisi C, Nicocia G, Frisina N et al (2008) Urinary neutrophil gelatinase-associated lipocalin (NGAL) is associated with severity of renal disease in proteinuric patients. Nephrol Dial Transplant 23(1):414–416CrossRefPubMed Bolignano D, Coppolino G, Campo S, Aloisi C, Nicocia G, Frisina N et al (2008) Urinary neutrophil gelatinase-associated lipocalin (NGAL) is associated with severity of renal disease in proteinuric patients. Nephrol Dial Transplant 23(1):414–416CrossRefPubMed
28.
go back to reference Bolignano D, Coppolino G, Lacquaniti A, Nicocia G, Buemi M (2008) Pathological and prognostic value of urinary neutrophil gelatinase-associated lipocalin in macroproteinuric patients with worsening renal function. Kidney Blood Press Res 31(4):274–279CrossRefPubMed Bolignano D, Coppolino G, Lacquaniti A, Nicocia G, Buemi M (2008) Pathological and prognostic value of urinary neutrophil gelatinase-associated lipocalin in macroproteinuric patients with worsening renal function. Kidney Blood Press Res 31(4):274–279CrossRefPubMed
29.
go back to reference Bolignano D, Lacquaniti A, Coppolino G, Donato V, Campo S, Fazio MR et al (2009) Neutrophil gelatinase-associated lipocalin (NGAL) and progression of chronic kidney disease. Clin J Am Soc Nephrol 4(2):337–344PubMedCentralCrossRefPubMed Bolignano D, Lacquaniti A, Coppolino G, Donato V, Campo S, Fazio MR et al (2009) Neutrophil gelatinase-associated lipocalin (NGAL) and progression of chronic kidney disease. Clin J Am Soc Nephrol 4(2):337–344PubMedCentralCrossRefPubMed
30.
go back to reference Smith ER, Lee D, Cai MM, Tomlinson LA, Ford ML, McMahon LP et al (2013) Urinary neutrophil gelatinase-associated lipocalin may aid prediction of renal decline in patients with non-proteinuric Stages 3 and 4 chronic kidney disease (CKD). Nephrol Dial Transplant 28(6):1569–1579CrossRefPubMed Smith ER, Lee D, Cai MM, Tomlinson LA, Ford ML, McMahon LP et al (2013) Urinary neutrophil gelatinase-associated lipocalin may aid prediction of renal decline in patients with non-proteinuric Stages 3 and 4 chronic kidney disease (CKD). Nephrol Dial Transplant 28(6):1569–1579CrossRefPubMed
31.
go back to reference Furuya F, Shimura H, Yokomichi H, Takahashi K, Akiyama D, Asakawa C et al. (2013) Neutrophil gelatinase-associated lipocalin levels associated with cardiovascular disease in chronic kidney disease patients. Clin Exp Nephrol 18(5):778–783CrossRefPubMed Furuya F, Shimura H, Yokomichi H, Takahashi K, Akiyama D, Asakawa C et al. (2013) Neutrophil gelatinase-associated lipocalin levels associated with cardiovascular disease in chronic kidney disease patients. Clin Exp Nephrol 18(5):778–783CrossRefPubMed
32.
go back to reference Levey AS, Stevens LA, Schmid CH, Zhang YL, Castro AF 3rd, Feldman HI et al (2009) A new equation to estimate glomerular filtration rate. Ann Intern Med 150:604–612PubMedCentralCrossRefPubMed Levey AS, Stevens LA, Schmid CH, Zhang YL, Castro AF 3rd, Feldman HI et al (2009) A new equation to estimate glomerular filtration rate. Ann Intern Med 150:604–612PubMedCentralCrossRefPubMed
33.
go back to reference Kidney Disease: Improving Global Outcomes (KDIGO) CKD Work Group (2013) KDIGO 2012 Clinical Practice Guideline for the Evaluation and Management of Chronic Kidney Disease. Kidney Int Suppl 3:1–150CrossRef Kidney Disease: Improving Global Outcomes (KDIGO) CKD Work Group (2013) KDIGO 2012 Clinical Practice Guideline for the Evaluation and Management of Chronic Kidney Disease. Kidney Int Suppl 3:1–150CrossRef
34.
go back to reference Stejskal D, Karpísek M, Humenanska V, Hanulova Z, Stejskal P, Kusnierova P et al (2008) Lipocalin-2: development, analytical characterization, and clinical testing of a new ELISA. Horm Metab Res 40(6):381–385CrossRefPubMed Stejskal D, Karpísek M, Humenanska V, Hanulova Z, Stejskal P, Kusnierova P et al (2008) Lipocalin-2: development, analytical characterization, and clinical testing of a new ELISA. Horm Metab Res 40(6):381–385CrossRefPubMed
35.
go back to reference Hanley JA, McNeil BJ (1983) A method of comparing the areas under receiver operating characteristic curves derived from the same cases. Radiology 148(3):839–843CrossRefPubMed Hanley JA, McNeil BJ (1983) A method of comparing the areas under receiver operating characteristic curves derived from the same cases. Radiology 148(3):839–843CrossRefPubMed
36.
go back to reference Pencina MJ, D’Agostino RB Sr, D’Agostino RB Jr, Vasan RS (2008) Evaluating the added predictive ability of a new marker: from area under the ROC curve to reclassification and beyond. Stat Med 27(2):157–172CrossRefPubMed Pencina MJ, D’Agostino RB Sr, D’Agostino RB Jr, Vasan RS (2008) Evaluating the added predictive ability of a new marker: from area under the ROC curve to reclassification and beyond. Stat Med 27(2):157–172CrossRefPubMed
37.
go back to reference Devarajan P (2008) NGAL in acute kidney injury: from serendipity to utility. Am J Kidney Dis 52:395–399CrossRefPubMed Devarajan P (2008) NGAL in acute kidney injury: from serendipity to utility. Am J Kidney Dis 52:395–399CrossRefPubMed
38.
39.
go back to reference Daniels LB, Barrett-Connor E, Clopton P, Laughlin GA, Ix JH, Maisel AS (2012) Plasma neutrophil gelatinase-associated lipocalin is independently associated with cardiovascular disease and mortality in community-dwelling older adults: the Rancho Bernardo Study. J Am Coll Cardiol 59(12):1101–1109PubMedCentralCrossRefPubMed Daniels LB, Barrett-Connor E, Clopton P, Laughlin GA, Ix JH, Maisel AS (2012) Plasma neutrophil gelatinase-associated lipocalin is independently associated with cardiovascular disease and mortality in community-dwelling older adults: the Rancho Bernardo Study. J Am Coll Cardiol 59(12):1101–1109PubMedCentralCrossRefPubMed
40.
go back to reference Helmersson-Karlqvist J, Larsson A, Carlsson AC, Venge P, Sundström J, Ingelsson E et al (2013) Urinary neutrophil gelatinase-associated lipocalin (NGAL) is associated with mortality in a community-based cohort of older Swedish men. Atherosclerosis 227(2):408–413CrossRefPubMed Helmersson-Karlqvist J, Larsson A, Carlsson AC, Venge P, Sundström J, Ingelsson E et al (2013) Urinary neutrophil gelatinase-associated lipocalin (NGAL) is associated with mortality in a community-based cohort of older Swedish men. Atherosclerosis 227(2):408–413CrossRefPubMed
41.
go back to reference Damman K, van Veldhuisen DJ, Navis G, Voors AA, Hillege HL (2008) Urinary neutrophil gelatinase associated lipocalin (NGAL), a marker of tubular damage, is increased in patients with chronic heart failure. Eur J Heart Fail 10:997–1000CrossRefPubMed Damman K, van Veldhuisen DJ, Navis G, Voors AA, Hillege HL (2008) Urinary neutrophil gelatinase associated lipocalin (NGAL), a marker of tubular damage, is increased in patients with chronic heart failure. Eur J Heart Fail 10:997–1000CrossRefPubMed
42.
go back to reference Damman K, Masson S, Hillege HL, Maggioni AP, Voors AA, Opasich C et al (2011) Clinical outcome of renal tubular damage in chronic heart failure. Eur Heart J 32(21):2705–2712CrossRefPubMed Damman K, Masson S, Hillege HL, Maggioni AP, Voors AA, Opasich C et al (2011) Clinical outcome of renal tubular damage in chronic heart failure. Eur Heart J 32(21):2705–2712CrossRefPubMed
43.
go back to reference van Deursen VM, Damman K, Voors AA, van der Wal MH, Jaarsma T, van Veldhuisen DJ et al (2014) Prognostic value of plasma neutrophil gelatinase-associated lipocalin for mortality in patients with heart failure. Circ Heart Fail 7(1):35–42CrossRefPubMed van Deursen VM, Damman K, Voors AA, van der Wal MH, Jaarsma T, van Veldhuisen DJ et al (2014) Prognostic value of plasma neutrophil gelatinase-associated lipocalin for mortality in patients with heart failure. Circ Heart Fail 7(1):35–42CrossRefPubMed
44.
go back to reference Nymo SH, Ueland T, Askevold ET, Flo TH, Kjekshus J, Hulthe J et al (2012) The association between neutrophil gelatinase-associated lipocalin and clinical outcome in chronic heart failure: results from CORONA*. J Intern Med 271(5):436–443CrossRefPubMed Nymo SH, Ueland T, Askevold ET, Flo TH, Kjekshus J, Hulthe J et al (2012) The association between neutrophil gelatinase-associated lipocalin and clinical outcome in chronic heart failure: results from CORONA*. J Intern Med 271(5):436–443CrossRefPubMed
45.
go back to reference Hasegawa M, Ishii J, Kitagawa F, Takahashi K, Hayashi H, Koide S et al. (2013) Urinary neutrophil gelatinase-associated lipocalin as a predictor of cardiovascular events in patients with chronic kidney disease. Heart Vessels 30(1):81–88CrossRefPubMed Hasegawa M, Ishii J, Kitagawa F, Takahashi K, Hayashi H, Koide S et al. (2013) Urinary neutrophil gelatinase-associated lipocalin as a predictor of cardiovascular events in patients with chronic kidney disease. Heart Vessels 30(1):81–88CrossRefPubMed
Metadata
Title
Serum neutrophil gelatinase-associated lipocalin is associated with cardiovascular events in patients with chronic kidney disease
Authors
Yalcin Solak
Mahmut Ilker Yilmaz
Dimitrie Siriopol
Mutlu Saglam
Hilmi Umut Unal
Halil Yaman
Mahmut Gok
Hakki Cetinkaya
Abduzhappar Gaipov
Tayfun Eyileten
Sebahattin Sari
Ali Osman Yildirim
Halil Zeki Tonbul
Suleyman Turk
Adrian Covic
Mehmet Kanbay
Publication date
01-12-2015
Publisher
Springer Netherlands
Published in
International Urology and Nephrology / Issue 12/2015
Print ISSN: 0301-1623
Electronic ISSN: 1573-2584
DOI
https://doi.org/10.1007/s11255-015-1136-4

Other articles of this Issue 12/2015

International Urology and Nephrology 12/2015 Go to the issue