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Published in: International Urology and Nephrology 1/2017

01-01-2017 | Nephrology - Original Paper

Do HDL and LDL subfractions play a role in atherosclerosis in end-stage renal disease (ESRD) patients?

Authors: Anna Gluba-Brzózka, Beata Franczyk, Maciej Banach, Magdalena Rysz-Górzyńska

Published in: International Urology and Nephrology | Issue 1/2017

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Abstract

Background

Significantly increased cardiovascular mortality in patients with chronic kidney (CKD) disease cannot be explained by traditional risk factors. Recent studies revealed that the quality of HDL and LDL cholesterol may be more important than their serum levels. The aim of this study was to assess which LDL and HDL subfractions were more abundant in end-stage renal disease (ESRD) patients and to analyse whether subfraction distribution could be associated with accelerated atherosclerotic processes.

Methods

This study included 50 ESRD patients undergoing dialysis and 20 healthy volunteers. LDL and HDL subfractions were analysed in serum with the use of Lipoprint system. All patients had intima-media thickness (IMT) measured.

Results

Statistically significant differences in subfractions between control and study group were observed in case of: HDL1 (p < 0.0001), HDL2 (p = 0.009), HDL3 (p < 0.0001), HDL4 (p = 0.003), HDL5 (p = 0.01), HDL7 (p < 0.0001), HDL8 (p < 0.0001), HDL9 (p < 0.0001), HDL10 (p < 0.0001), large HDL (p < 0.0001), HDL Small (p < 0.0001) as well as IDL-B (p = 0.014), IDLA (p = 0.011), LDL2 (p = 0.007). Significant differences were also observed in HDL and LDL subfraction distribution between haemodialysis patients with normal and increased IMT: HDL6 (p = 0.020), HDL Large (HDL1-3) (p = 0.017), HDL Intermediate (HDL4-7) (p = 0.017).

Conclusions

This study revealed that ESRD influenced HDL subfractions. In HD patients, large HDL subfractions are more abundant while small HDL fraction is more frequent in healthy persons. It failed to show the influence of end-stage disease on LDL subfraction levels. Shift in HDL subfractions might be responsible for the increased risk of atherosclerosis in CKD patients.
Literature
1.
go back to reference Navab KD, Elboudwarej O, Gharif M, Yu J, Hama SY, Safarpour S et al (2011) Chronic inflammatory disorders and accelerated atherosclerosis: chronic kidney disease. Curr Pharm Des 17(1):17–20CrossRefPubMed Navab KD, Elboudwarej O, Gharif M, Yu J, Hama SY, Safarpour S et al (2011) Chronic inflammatory disorders and accelerated atherosclerosis: chronic kidney disease. Curr Pharm Des 17(1):17–20CrossRefPubMed
2.
3.
go back to reference McCullough PA, Li S, Jurkovitz CT et al (2008) Chronic kidney disease, prevalence of premature cardiovascular disease, and relationship to short-term mortality. Am Heart J 156:277–283CrossRefPubMed McCullough PA, Li S, Jurkovitz CT et al (2008) Chronic kidney disease, prevalence of premature cardiovascular disease, and relationship to short-term mortality. Am Heart J 156:277–283CrossRefPubMed
4.
go back to reference Suganuma E, Zuo Y, Ayabe N et al (2006) Antiatherogenic effects of angiotensin receptor antagonism in mild renal dysfunction. J Am Soc Nephrol 17:433–441CrossRefPubMed Suganuma E, Zuo Y, Ayabe N et al (2006) Antiatherogenic effects of angiotensin receptor antagonism in mild renal dysfunction. J Am Soc Nephrol 17:433–441CrossRefPubMed
5.
6.
go back to reference Matsushita K, van der Velde M, Chronic Kidney Disease Prognosis Consortium et al (2010) Association of estimated glomerular filtration rate and albuminuria with all-cause and cardiovascular mortality in general population cohorts: a collaborative meta-analysis. Lancet 375:2073–2081CrossRefPubMedPubMedCentral Matsushita K, van der Velde M, Chronic Kidney Disease Prognosis Consortium et al (2010) Association of estimated glomerular filtration rate and albuminuria with all-cause and cardiovascular mortality in general population cohorts: a collaborative meta-analysis. Lancet 375:2073–2081CrossRefPubMedPubMedCentral
7.
go back to reference Wanner C, Krane V, Marz W et al (2005) Atorvastatin in patients with type 2 diabetes mellitus undergoing hemodialysis. N Engl J Med 353:238–248CrossRefPubMed Wanner C, Krane V, Marz W et al (2005) Atorvastatin in patients with type 2 diabetes mellitus undergoing hemodialysis. N Engl J Med 353:238–248CrossRefPubMed
8.
go back to reference Kones R (2013) Molecular sources of residual cardiovascular risk, clinical signals, and innovative solutions: relationship with subclinical disease, undertreatment, and poor adherence: implications of new evidence upon optimizing cardiovascular patient outcomes. Vasc Health Risk Manag 9:617–670CrossRefPubMedPubMedCentral Kones R (2013) Molecular sources of residual cardiovascular risk, clinical signals, and innovative solutions: relationship with subclinical disease, undertreatment, and poor adherence: implications of new evidence upon optimizing cardiovascular patient outcomes. Vasc Health Risk Manag 9:617–670CrossRefPubMedPubMedCentral
9.
go back to reference Palmer SC, Navaneethan SD, Craig JC et al (2014) HMG CoA reductase inhibitors (statins) for people with chronic kidney disease not requiring dialysis. Cochrane Database Syst Rev 5:CD007784 Palmer SC, Navaneethan SD, Craig JC et al (2014) HMG CoA reductase inhibitors (statins) for people with chronic kidney disease not requiring dialysis. Cochrane Database Syst Rev 5:CD007784
10.
go back to reference Homma K, Homma Y, Shiina Y, Wakino S, Suzuki M, Fujishima S et al (2013) Skew of plasma low- and high-density lipoprotein distributions to less dense subfractions in normotriglyceridemic chronic kidney disease patients on maintenance hemodialysis treatment. Nephron Clin Pract 123(1–2):41–45CrossRefPubMed Homma K, Homma Y, Shiina Y, Wakino S, Suzuki M, Fujishima S et al (2013) Skew of plasma low- and high-density lipoprotein distributions to less dense subfractions in normotriglyceridemic chronic kidney disease patients on maintenance hemodialysis treatment. Nephron Clin Pract 123(1–2):41–45CrossRefPubMed
11.
go back to reference Griffin BA, Freeman DJ, Tait GW, Thompson J, Caslake MJ, Packard C et al (1994) Role of plasma triglyceride in the regulation of plasma low-density lipoprotein (LDL) subfractions: relative contribution of small, dense LDL to coronary heart disease risk. Atherosclerosis 106:241–253CrossRefPubMed Griffin BA, Freeman DJ, Tait GW, Thompson J, Caslake MJ, Packard C et al (1994) Role of plasma triglyceride in the regulation of plasma low-density lipoprotein (LDL) subfractions: relative contribution of small, dense LDL to coronary heart disease risk. Atherosclerosis 106:241–253CrossRefPubMed
12.
go back to reference Hirano T, Ito Y, Koba S, Toyoda M, Ikejiri A, Saegusa H et al (2004) Clinical significance of small dense low-density lipoprotein cholesterol levels determined by the simple precipitation method. Arterioscler Thromb Vasc Biol 24:558–563CrossRefPubMed Hirano T, Ito Y, Koba S, Toyoda M, Ikejiri A, Saegusa H et al (2004) Clinical significance of small dense low-density lipoprotein cholesterol levels determined by the simple precipitation method. Arterioscler Thromb Vasc Biol 24:558–563CrossRefPubMed
13.
go back to reference Homma Y, Michishita I, Hayashi H, Shigematsu H, Kanagawa Lipid Research Group (2010) Effects of low-dose simvastatin on the distribution of plasma cholesterol and oxidized low-density lipoprotein in three ultracentrifugally separated low-density lipoprotein subfractions: 12-month, open-label trial. J Atheroscler Thromb 17:1049–1053CrossRefPubMed Homma Y, Michishita I, Hayashi H, Shigematsu H, Kanagawa Lipid Research Group (2010) Effects of low-dose simvastatin on the distribution of plasma cholesterol and oxidized low-density lipoprotein in three ultracentrifugally separated low-density lipoprotein subfractions: 12-month, open-label trial. J Atheroscler Thromb 17:1049–1053CrossRefPubMed
14.
go back to reference Kaseda R, Jabs K, Hunley TE, Jones D, Bian A, Allen RM et al (2015) Dysfunctional high-density lipoproteins in children with chronic kidney disease. Metabolism 64(2):263–273CrossRefPubMed Kaseda R, Jabs K, Hunley TE, Jones D, Bian A, Allen RM et al (2015) Dysfunctional high-density lipoproteins in children with chronic kidney disease. Metabolism 64(2):263–273CrossRefPubMed
15.
go back to reference Holzer M, Birner-Gruenberger R, Stojakovic T, El-Gamal D, Binder V, Wadsack C et al (2011) Uremia alters HDL composition and function. J Am Soc Nephrol 22(9):1631–1641CrossRefPubMedPubMedCentral Holzer M, Birner-Gruenberger R, Stojakovic T, El-Gamal D, Binder V, Wadsack C et al (2011) Uremia alters HDL composition and function. J Am Soc Nephrol 22(9):1631–1641CrossRefPubMedPubMedCentral
16.
go back to reference Tölle M, Huang T, Schuchardt M, Jankowski V, Prüfer N, Jankowski J et al (2012) High-density lipoprotein loses its anti-inflammatory capacity by accumulation of pro-inflammatory-serum amyloid A. Cardiovasc Res 94(1):154–162CrossRefPubMed Tölle M, Huang T, Schuchardt M, Jankowski V, Prüfer N, Jankowski J et al (2012) High-density lipoprotein loses its anti-inflammatory capacity by accumulation of pro-inflammatory-serum amyloid A. Cardiovasc Res 94(1):154–162CrossRefPubMed
17.
go back to reference Yamamoto S, Yancey PG, Ikizler TA, Jerome WG, Kaseda R, Cox B et al (2012) Dysfunctional high-density lipoprotein in patients on chronic hemodialysis. J Am Coll Cardiol 60(23):2372–2379CrossRefPubMed Yamamoto S, Yancey PG, Ikizler TA, Jerome WG, Kaseda R, Cox B et al (2012) Dysfunctional high-density lipoprotein in patients on chronic hemodialysis. J Am Coll Cardiol 60(23):2372–2379CrossRefPubMed
18.
go back to reference Maugeais C, Perez A, von der Mark E, Magg C, Pflieger P, Niesor EJ (2013) Evidence for a role of CETP in HDL remodeling and cholesterol efflux: role of cysteine 13 of CETP. Biochim Biophys Acta 1831(11):1644–1650CrossRefPubMed Maugeais C, Perez A, von der Mark E, Magg C, Pflieger P, Niesor EJ (2013) Evidence for a role of CETP in HDL remodeling and cholesterol efflux: role of cysteine 13 of CETP. Biochim Biophys Acta 1831(11):1644–1650CrossRefPubMed
19.
go back to reference Rysz J, Gluba A, Fliser D, Speer T, Wiecek A (2014) Chronic kidney disease—different role for HDL? Curr Med Chem 21(25):2910–2916CrossRef Rysz J, Gluba A, Fliser D, Speer T, Wiecek A (2014) Chronic kidney disease—different role for HDL? Curr Med Chem 21(25):2910–2916CrossRef
20.
go back to reference Lorenz MW, Markus HS, Bots ML, Rosvall M, Sitzer M (2007) Prediction of clinical cardiovascular events with carotid intima-media thickness: a systematic review and meta-analysis. Circulation 115:459–467CrossRefPubMed Lorenz MW, Markus HS, Bots ML, Rosvall M, Sitzer M (2007) Prediction of clinical cardiovascular events with carotid intima-media thickness: a systematic review and meta-analysis. Circulation 115:459–467CrossRefPubMed
21.
go back to reference Shimizu M, Furusyo N, Mitsumoto F, Takayama K, Ura K, Hiramine S et al (2015) Subclinical carotid atherosclerosis and triglycerides predict the incidence of chronic kidney disease in the Japanese general population: results from the Kyushu and Okinawa Population Study (KOPS). Atherosclerosis 238(2):207–212CrossRefPubMed Shimizu M, Furusyo N, Mitsumoto F, Takayama K, Ura K, Hiramine S et al (2015) Subclinical carotid atherosclerosis and triglycerides predict the incidence of chronic kidney disease in the Japanese general population: results from the Kyushu and Okinawa Population Study (KOPS). Atherosclerosis 238(2):207–212CrossRefPubMed
22.
go back to reference Chonchol M, Gnahn H, Sander D (2008) Impact of subclinical carotid atherosclerosis on incident chronic kidney disease in the elderly. Nephrol Dial Transpl 23:2593–2598CrossRef Chonchol M, Gnahn H, Sander D (2008) Impact of subclinical carotid atherosclerosis on incident chronic kidney disease in the elderly. Nephrol Dial Transpl 23:2593–2598CrossRef
23.
go back to reference Dukát A, Oravec S, Wawruch M, Gavorník P, Sabaka P (2011) The incidence of dyslipidemia in a sample of asymptomatic probands established by the means of Lipoprint system]. Vnitr Lek 57(3):258–260PubMed Dukát A, Oravec S, Wawruch M, Gavorník P, Sabaka P (2011) The incidence of dyslipidemia in a sample of asymptomatic probands established by the means of Lipoprint system]. Vnitr Lek 57(3):258–260PubMed
25.
go back to reference Moradi H, Vaziri ND, Said HM, Kalantar-Zadeh K (2013) Role of HDL dysfunction in end-stage renal disease: a double-edged sword. J Ren Nutr. 23(3):203–206CrossRefPubMedPubMedCentral Moradi H, Vaziri ND, Said HM, Kalantar-Zadeh K (2013) Role of HDL dysfunction in end-stage renal disease: a double-edged sword. J Ren Nutr. 23(3):203–206CrossRefPubMedPubMedCentral
26.
go back to reference Vaziri ND, Navab K, Gollapudi P, Moradi H, Pahl MV, Barton CH, Fogelman AM, Navab M (2011) Salutary effects of hemodialysis on low-density lipoprotein proinflammatory and high-density lipoprotein anti-inflammatory properties in patient with end-stage renal disease. J Natl Med Assoc 103(6):524–533CrossRefPubMedPubMedCentral Vaziri ND, Navab K, Gollapudi P, Moradi H, Pahl MV, Barton CH, Fogelman AM, Navab M (2011) Salutary effects of hemodialysis on low-density lipoprotein proinflammatory and high-density lipoprotein anti-inflammatory properties in patient with end-stage renal disease. J Natl Med Assoc 103(6):524–533CrossRefPubMedPubMedCentral
27.
go back to reference Stack AG, Bloembergen WE (2001) Prevalence and clinical correlates of coronary artery disease among new dialysis patients in the United States: a cross-sectional study. J Am Soc Nephrol 12(7):1516–1523PubMed Stack AG, Bloembergen WE (2001) Prevalence and clinical correlates of coronary artery disease among new dialysis patients in the United States: a cross-sectional study. J Am Soc Nephrol 12(7):1516–1523PubMed
28.
go back to reference Rysz J, Stolarek RA, Pedzik A, Nowicki M, Nowak D (2010) Serum antioxidant capacity is preserved in peritoneal dialysis contrary to its robust depletion after hemodialysis and hemodiafiltration sessions. Ther Apher Dial 14(2):209–217CrossRefPubMed Rysz J, Stolarek RA, Pedzik A, Nowicki M, Nowak D (2010) Serum antioxidant capacity is preserved in peritoneal dialysis contrary to its robust depletion after hemodialysis and hemodiafiltration sessions. Ther Apher Dial 14(2):209–217CrossRefPubMed
29.
go back to reference Rysz J, Potargowicz E, Banach M, Luczyńska M, Stolarek R, Białasiewicz P et al (2006) Increased whole blood chemiluminescence in patients with chronic renal failure independent of hemodialysis treatment. Arch Immunol Ther Exp (Warsz) 54(5):347–355CrossRef Rysz J, Potargowicz E, Banach M, Luczyńska M, Stolarek R, Białasiewicz P et al (2006) Increased whole blood chemiluminescence in patients with chronic renal failure independent of hemodialysis treatment. Arch Immunol Ther Exp (Warsz) 54(5):347–355CrossRef
30.
go back to reference Maeda S, Nakanishi S, Yoneda M, Awaya T, Yamane K, Hirano T et al (2012) Associations between small dense LDL, HDL subfractions (HDL2, HDL3) and risk of atherosclerosis in Japanese-Americans. J Atheroscler Thromb 19(5):444–452CrossRefPubMed Maeda S, Nakanishi S, Yoneda M, Awaya T, Yamane K, Hirano T et al (2012) Associations between small dense LDL, HDL subfractions (HDL2, HDL3) and risk of atherosclerosis in Japanese-Americans. J Atheroscler Thromb 19(5):444–452CrossRefPubMed
31.
go back to reference Bjornheded T, Babyi A, Bodjers G, Wiklund O (1996) Accumulation of lipoprotein fractions and subfractions in the arterial wall, determined in an in vitro perfusion system. Atherosclerosis 123:43–56CrossRef Bjornheded T, Babyi A, Bodjers G, Wiklund O (1996) Accumulation of lipoprotein fractions and subfractions in the arterial wall, determined in an in vitro perfusion system. Atherosclerosis 123:43–56CrossRef
32.
go back to reference Berneis KK, Krauss RM (2002) Metabolic origins and clinical significance of LDL heterogeneity. J Lipid Res 43:1363–1379CrossRefPubMed Berneis KK, Krauss RM (2002) Metabolic origins and clinical significance of LDL heterogeneity. J Lipid Res 43:1363–1379CrossRefPubMed
33.
go back to reference Salonen JT, Salonen R, Seppanen K, Rauramaa R, Tuomilehto J (1991) HDL, HDL2, and HDL3 subfractions, and the risk of acute myocardial infarction: a prospective study in eastern Finnish men. Circulation 84:129–139CrossRefPubMed Salonen JT, Salonen R, Seppanen K, Rauramaa R, Tuomilehto J (1991) HDL, HDL2, and HDL3 subfractions, and the risk of acute myocardial infarction: a prospective study in eastern Finnish men. Circulation 84:129–139CrossRefPubMed
34.
go back to reference Smuts CM, Weich HF, Weight MJ, Faber M, Kruger M, Lombard CJ et al (1994) Free cholesterol concentrations in the high-density lipoprotein subfraction-3 as a risk indicator in patients with angiographically documented coronary artery disease. Coron Artery Dis 5:331–338CrossRefPubMed Smuts CM, Weich HF, Weight MJ, Faber M, Kruger M, Lombard CJ et al (1994) Free cholesterol concentrations in the high-density lipoprotein subfraction-3 as a risk indicator in patients with angiographically documented coronary artery disease. Coron Artery Dis 5:331–338CrossRefPubMed
35.
go back to reference Iwanejko J, Kwasniak M, Wybranska I, Hartwich J, Guevara I, Zdzienicka A et al (1996) Heterogeneity of high-density lipoprotein particles and insulin output during oral glucose tolerance test in men with coronary artery disease. Acta Diabetol 33:58–61CrossRefPubMed Iwanejko J, Kwasniak M, Wybranska I, Hartwich J, Guevara I, Zdzienicka A et al (1996) Heterogeneity of high-density lipoprotein particles and insulin output during oral glucose tolerance test in men with coronary artery disease. Acta Diabetol 33:58–61CrossRefPubMed
36.
go back to reference Tsuzaki K, Kotani K, Sano Y, Fujiwara S, Gazi IF, Elisaf M et al (2012) The relationship between adiponectin, an adiponectin gene polymorphism, and high-density lipoprotein particle size: from the Mima study. Metabolism 61(1):17–21CrossRefPubMed Tsuzaki K, Kotani K, Sano Y, Fujiwara S, Gazi IF, Elisaf M et al (2012) The relationship between adiponectin, an adiponectin gene polymorphism, and high-density lipoprotein particle size: from the Mima study. Metabolism 61(1):17–21CrossRefPubMed
37.
go back to reference Eisenberg S (1984) High density lipoprotein metabolism. J Lipid Res 25(10):1017–1058PubMed Eisenberg S (1984) High density lipoprotein metabolism. J Lipid Res 25(10):1017–1058PubMed
38.
go back to reference Yamashita S, Ishigami M, Arai T, Sakai N, Hirano K, Kameda-Takemura K et al (1995) Very high density lipoproteins induced by plasma cholesteryl ester transfer protein CETP have a potent antiatherogenic function. Ann NY Acad Sci 748:606–608CrossRefPubMed Yamashita S, Ishigami M, Arai T, Sakai N, Hirano K, Kameda-Takemura K et al (1995) Very high density lipoproteins induced by plasma cholesteryl ester transfer protein CETP have a potent antiatherogenic function. Ann NY Acad Sci 748:606–608CrossRefPubMed
39.
go back to reference Kontush A, Chantepie S, Chapman MJ (2003) Small, dense HDL particles exert potent protection of atherogenic LDL against oxidative stress. Arterioscler Thromb Vasc Biol 23:1881–1888CrossRefPubMed Kontush A, Chantepie S, Chapman MJ (2003) Small, dense HDL particles exert potent protection of atherogenic LDL against oxidative stress. Arterioscler Thromb Vasc Biol 23:1881–1888CrossRefPubMed
40.
go back to reference Favari E, Calabresi L, Adorni MP, Jessup W, Simonelli S, Franceschini G, Bernini F (2009) Small discoidal pre-beta1 HDL particles are efficient acceptors of cell cholesterol via ABCA1 and ABCG1. Biochemistry 48:11067–11074CrossRefPubMed Favari E, Calabresi L, Adorni MP, Jessup W, Simonelli S, Franceschini G, Bernini F (2009) Small discoidal pre-beta1 HDL particles are efficient acceptors of cell cholesterol via ABCA1 and ABCG1. Biochemistry 48:11067–11074CrossRefPubMed
41.
go back to reference de Souza JA, Vindis C, Nègre-Salvayre A, Rye KA, Couturier M, Therond P, Chantepie S, Salvayre R, Chapman MJ, Kontush A (2010) Small, dense HDL 3 particles attenuate apoptosis in endothelial cells: pivotal role of apolipo-protein A-I. J Cell Mol Med 14:608–620PubMed de Souza JA, Vindis C, Nègre-Salvayre A, Rye KA, Couturier M, Therond P, Chantepie S, Salvayre R, Chapman MJ, Kontush A (2010) Small, dense HDL 3 particles attenuate apoptosis in endothelial cells: pivotal role of apolipo-protein A-I. J Cell Mol Med 14:608–620PubMed
42.
go back to reference Camont L, Lhomme M, Rached F, Le Goff W, Nègre-Salvayre A, Salvayre R, Calzada C, Lagarde M, Chapman MJ, Kontush A (2013) Small, dense high-density lipoprotein-3 particles are enriched in negatively charged phospholipids relevance to cellular cholesterol efflux, antioxidative, antithrombotic, anti-inflammatory, and antiapoptotic functionalities. Arterioscler Thromb Vasc Biol 33:2715–2723CrossRefPubMed Camont L, Lhomme M, Rached F, Le Goff W, Nègre-Salvayre A, Salvayre R, Calzada C, Lagarde M, Chapman MJ, Kontush A (2013) Small, dense high-density lipoprotein-3 particles are enriched in negatively charged phospholipids relevance to cellular cholesterol efflux, antioxidative, antithrombotic, anti-inflammatory, and antiapoptotic functionalities. Arterioscler Thromb Vasc Biol 33:2715–2723CrossRefPubMed
43.
go back to reference Bjornheden T, Babyi A, Bondjers G, Wiklund O (1996) Accumulation of lipoprotein fractions and subfractions in the arterial wall, determined in an in vitro perfusion system. Atherosclerosis 123:43–56CrossRefPubMed Bjornheden T, Babyi A, Bondjers G, Wiklund O (1996) Accumulation of lipoprotein fractions and subfractions in the arterial wall, determined in an in vitro perfusion system. Atherosclerosis 123:43–56CrossRefPubMed
44.
go back to reference Galeano NF, Al-Haideri M, Keyserman F, Rumsey SC, Deckelbaum RJ (1998) Small dense low density lipoprotein has increased affinity for LDL receptor-independent cell surface binding sites: a potential mechanism for increased atherogenicity. J Lipid Res 39:1263–1273PubMed Galeano NF, Al-Haideri M, Keyserman F, Rumsey SC, Deckelbaum RJ (1998) Small dense low density lipoprotein has increased affinity for LDL receptor-independent cell surface binding sites: a potential mechanism for increased atherogenicity. J Lipid Res 39:1263–1273PubMed
45.
go back to reference Tribble DL, Rizzo M, Chait A, Lewis DM, Blanche PJ, Krauss RM (2001) Enhanced oxidative susceptibility and reduced antioxidant content of metabolic precursors of small, dense low-density lipoproteins. Am J Med 110:103–110CrossRefPubMed Tribble DL, Rizzo M, Chait A, Lewis DM, Blanche PJ, Krauss RM (2001) Enhanced oxidative susceptibility and reduced antioxidant content of metabolic precursors of small, dense low-density lipoproteins. Am J Med 110:103–110CrossRefPubMed
46.
go back to reference Touboul PJ, Labreuche J, Bruckert E, Schargrodsky H, Prati P, Tosetto A et al (2014) HDL-C, triglycerides and carotid IMT: a meta-analysis of 21,000 patients with automated edge detection IMT measurement. Atherosclerosis 232(1):65–71CrossRefPubMed Touboul PJ, Labreuche J, Bruckert E, Schargrodsky H, Prati P, Tosetto A et al (2014) HDL-C, triglycerides and carotid IMT: a meta-analysis of 21,000 patients with automated edge detection IMT measurement. Atherosclerosis 232(1):65–71CrossRefPubMed
47.
go back to reference Kaseda R, Jabs K, Hunley TE, Jones D, Bian A, Allen RM et al (2015) Dysfunctional high-density lipoproteins in children with chronic kidney disease. Metabolism 64(2):263–273CrossRefPubMed Kaseda R, Jabs K, Hunley TE, Jones D, Bian A, Allen RM et al (2015) Dysfunctional high-density lipoproteins in children with chronic kidney disease. Metabolism 64(2):263–273CrossRefPubMed
48.
go back to reference Moradi H, Streja E, Kashyap ML, Vaziri ND, Fonarow GC, Kalantar-Zadeh K (2014) Elevated high-density lipoprotein cholesterol and cardiovascular mortality in maintenance hemodialysis patients. Nephrol Dial Transplant 29(8):1554–1562CrossRefPubMedPubMedCentral Moradi H, Streja E, Kashyap ML, Vaziri ND, Fonarow GC, Kalantar-Zadeh K (2014) Elevated high-density lipoprotein cholesterol and cardiovascular mortality in maintenance hemodialysis patients. Nephrol Dial Transplant 29(8):1554–1562CrossRefPubMedPubMedCentral
49.
go back to reference Vaziri ND, Navab M, Fogelman AM (2010) HDL metabolism and activity in chronic kidney disease. Nat Rev Nephrol 6(5):287–296CrossRefPubMed Vaziri ND, Navab M, Fogelman AM (2010) HDL metabolism and activity in chronic kidney disease. Nat Rev Nephrol 6(5):287–296CrossRefPubMed
50.
go back to reference Rysz J, Majewska E, Stolarek RA, Banach M, Ciałkowska-Rysz A, Baj Z (2006) Increased levels of soluble TNF-alpha receptors and cellular adhesion molecules in patients undergoing bioincompatible hemodialysis. Am J Nephrol 26(5):437–444CrossRefPubMed Rysz J, Majewska E, Stolarek RA, Banach M, Ciałkowska-Rysz A, Baj Z (2006) Increased levels of soluble TNF-alpha receptors and cellular adhesion molecules in patients undergoing bioincompatible hemodialysis. Am J Nephrol 26(5):437–444CrossRefPubMed
Metadata
Title
Do HDL and LDL subfractions play a role in atherosclerosis in end-stage renal disease (ESRD) patients?
Authors
Anna Gluba-Brzózka
Beata Franczyk
Maciej Banach
Magdalena Rysz-Górzyńska
Publication date
01-01-2017
Publisher
Springer Netherlands
Published in
International Urology and Nephrology / Issue 1/2017
Print ISSN: 0301-1623
Electronic ISSN: 1573-2584
DOI
https://doi.org/10.1007/s11255-016-1466-x

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