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A comprehensive review on apolipoproteins as nontraditional cardiovascular risk factors in end-stage renal disease: current evidence and perspectives

  • Nephrology - Review
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Abstract

Purpose

Nontraditional cardiovascular risk factors such as lipoprotein(a) (Lp(a)), the genetic polymorphisms of apolipoprotein(a), apolipoprotein E (ApoE), and apolipoprotein B (ApoB) increase the prevalence of atherosclerosis in end-stage renal disease (ESRD) through quantitative and qualitative alterations. Given the high burden of cardiovascular fatal events in ESRD, this review aims to gather studies depicting apolipoproteins’ changes in ESRD, to describe current evidence and to explore potential lipid-lowering therapies.

Methods

We searched the electronic database of PubMed, SCOPUS, EBSCO, and Cochrane CENTRAL for studies evaluating apolipoproteins in ESRD. Randomized controlled trials, observational studies (including case–control, prospective, or retrospective cohort), and reviews/meta-analysis were included if reference was made to apolipoproteins and cardiovascular consequences in ESRD.

Results

21 studies met the inclusion criteria. We found a significant correlation between Lp(a) plasma concentrations and atherosclerosis. Lp(a) levels were independent risk factors for atherothrombosis and cardiovascular mortality. LMW apo(a) phenotype proved to be the best predictor for coronary events in ESRD. Single nucleotide polymorphisms in ApoE gene affected the expression and function of the protein, increasing the risk of cardiovascular events. ApoB had a significant correlation with the value of carotid intima–media thickness and vascular stiffness.

Conclusions

The picture of “lipid milieu” in ESRD has not been clearly described. Novel studies show that specific apolipoproteins suffer modifications in uremic patients, being correlated with cardiovascular events. Probably in the next years, the treatment of dyslipidemia in ESRD will not merely target LDL or total cholesterol, but specific isoforms of apolipoproteins which seem to become the central part of the problem.

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References

  1. Parsons DS, Reaveley DA, Pavitt DV, Misra M, Brown EA (2003) Lipoprotein(a) levels in those with high molecular weight apo(a) isoforms may remain low in a significant proportion of patients with end-stage renal disease. Nephrol Dial Transpl 18(9):1848–1853

    Article  CAS  Google Scholar 

  2. Park KA, Jo HM, Han JS, Kim MJ, do Kwun H, Park MY, Choi SJ, Kim JK, Hwang SD (2013) Features of atherosclerosis in hemodialysis patients. Kidney Res Clin Pract 32(4):177–182. https://doi.org/10.1016/j.krcp.2013.10.002

    Article  PubMed  PubMed Central  Google Scholar 

  3. Nusair MB, Rajpurohit N, Alpert MA (2012) Chronic inflammation and coronary atherosclerosis in patients with end-stage renal disease. Cardioren Med 2(2):117–124

    Article  CAS  Google Scholar 

  4. Mathew RO, Bangalore S, Lavelle MP, Pellikka PA, Sidhu MS, Boden WE, Asif A (2017) Diagnosis and management of atherosclerotic cardiovascular disease in chronic kidney disease: a review. Kidney Int 91(4):797–807. https://doi.org/10.1016/j.kint.2016.09.049

    Article  PubMed  Google Scholar 

  5. Shroff GR, Frederick PD, Herzog CA (2012) Renal failure and acute myocardial infarction: clinical characteristics in patients with advanced chronic kidney disease, on dialysis, and without chronic kidney disease. A collaborative project of the United States Renal Data System/National Institutes of Health and the National Registry of Myocardial Infarction. Am Heart J 163(3):399–406. https://doi.org/10.1016/j.ahj.2011.12.002

    Article  PubMed  PubMed Central  Google Scholar 

  6. Olechnowicz-Tietz S, Gluba A, Paradowska A, Banach M, Rysz J (2013) The risk of atherosclerosis in patients with chronic kidney disease. Int Urol Nephrol 45(6):1605–1612. https://doi.org/10.1007/s11255-013-0407-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Drueke TB, Massy ZA (2010) Atherosclerosis in CKD: differences from the general population. Nat Rev Nephrol 6(12):723–735. https://doi.org/10.1038/nrneph.2010.143

    Article  PubMed  Google Scholar 

  8. Mikolasevic I, Zutelija M, Mavrinac V, Orlic L (2017) Dyslipidemia in patients with chronic kidney disease: etiology and management. Int J Nephrol Renovasc Dis 10:35–45. https://doi.org/10.2147/IJNRD.S101808

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Kon V, Linton MF, Fazio S (2011) Atherosclerosis in chronic kidney disease: the role of macrophages. Nat Rev Nephrol 7(1):45–54. https://doi.org/10.1038/nrneph.2010.157

    Article  CAS  PubMed  Google Scholar 

  10. Shrestha P, van de Sluis B, Dullaart RPF, van den Born J (2019) Novel aspects of PCSK9 and lipoprotein receptors in renal disease-related dyslipidemia. Cell Signal 55:53–64. https://doi.org/10.1016/j.cellsig.2018.12.001

    Article  CAS  PubMed  Google Scholar 

  11. Emanuele E, Lusignani LS, Peros E, Montagna G, D’Angelo A, Montagna L, Geroldi D (2004) Lipoprotein(a)-associated atherothrombotic risk in hemodialysis patients. Am J Nephrol 24(2):221–229. https://doi.org/10.1159/000077293

    Article  CAS  PubMed  Google Scholar 

  12. Vaziri ND (2016) Disorders of lipid metabolism in nephrotic syndrome: mechanisms and consequences. Kidney Int 90(1):41–52. https://doi.org/10.1016/j.kint.2016.02.026

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Kronenberg F, Utermann G, Dieplinger H (1996) Lipoprotein(a) in renal disease. Am J Kidney Dis 27(1):1–25

    Article  CAS  Google Scholar 

  14. Longenecker JC, Coresh J, Marcovina SM, Powe NR, Levey AS, Giaculli F, Fink NE, Klag MJ (2003) Lipoprotein(a) and prevalent cardiovascular disease in a dialysis population: the choices for healthy outcomes in caring for ESRD (CHOICE) study. Am J Kidney Dis 42(1):108–116

    Article  CAS  Google Scholar 

  15. Kollerits B, Drechsler C, Krane V, Lamina C, Marz W, Dieplinger H, Ritz E, Wanner C, Kronenberg F, German D, Dialysis Study I (2016) Lipoprotein(a) concentrations, apolipoprotein(a) isoforms and clinical endpoints in haemodialysis patients with type 2 diabetes mellitus: results from the 4D Study. Nephrol Dial Transpl 31(11):1901–1908. https://doi.org/10.1093/ndt/gfv428

    Article  CAS  Google Scholar 

  16. Kronenberg F (2014) Causes and consequences of lipoprotein(a) abnormalities in kidney disease. Clin Exp Nephrol 18(2):234–237. https://doi.org/10.1007/s10157-013-0875-8

    Article  CAS  PubMed  Google Scholar 

  17. Kronenberg F, Neyer U, Lhotta K, Trenkwalder E, Auinger M, Pribasnig A, Meisl T, Konig P, Dieplinger H (1999) The low molecular weight apo(a) phenotype is an independent predictor for coronary artery disease in hemodialysis patients: a prospective follow-up. J Am Soc Nephrol JASN 10(5):1027–1036

    CAS  PubMed  Google Scholar 

  18. Kaysen GA (2007) Hyperlipidemia in chronic kidney disease. Int J Artif Organs 30(11):987–992

    Article  CAS  Google Scholar 

  19. Longenecker JC, Klag MJ, Marcovina SM, Liu YM, Jaar BG, Powe NR, Fink NE, Levey AS, Coresh J (2005) High lipoprotein(a) levels and small apolipoprotein(a) size prospectively predict cardiovascular events in dialysis patients. J Am Soc Nephrol JASN 16(6):1794–1802. https://doi.org/10.1681/ASN.2004110922

    Article  CAS  PubMed  Google Scholar 

  20. Catapano AL, Graham I, De Backer G, Wiklund O, Chapman MJ, Drexel H, Hoes AW, Jennings CS, Landmesser U, Pedersen TR, Reiner Z, Riccardi G, Taskinen MR, Tokgozoglu L, Verschuren WMM, Vlachopoulos C, Wood DA, Zamorano JL, Cooney MT, Group ESCSD (2016) 2016 ESC/EAS guidelines for the management of dyslipidaemias. Eur Heart J 37(39):2999–3058. https://doi.org/10.1093/eurheartj/ehw272

    Article  PubMed  Google Scholar 

  21. Kamstrup PR, Tybjaerg-Hansen A, Steffensen R, Nordestgaard BG (2009) Genetically elevated lipoprotein(a) and increased risk of myocardial infarction. JAMA 301(22):2331–2339. https://doi.org/10.1001/jama.2009.801

    Article  CAS  PubMed  Google Scholar 

  22. Ohashi H, Oda H, Ohno M, Watanabe S, Sakata S (1999) Lipoprotein(a) as a risk factor for coronary artery disease in hemodialysis patients. Kidney Int Suppl 71:S242–S244

    Article  CAS  Google Scholar 

  23. Willeit P, Kiechl S, Kronenberg F, Witztum JL, Santer P, Mayr M, Xu Q, Mayr A, Willeit J, Tsimikas S (2014) Discrimination and net reclassification of cardiovascular risk with lipoprotein(a): prospective 15-year outcomes in the Bruneck Study. J Am Coll Cardiol 64(9):851–860. https://doi.org/10.1016/j.jacc.2014.03.061

    Article  PubMed  Google Scholar 

  24. Koda Y, Nishi S, Suzuki M, Hirasawa Y (1999) Lipoprotein(a) is a predictor for cardiovascular mortality of hemodialysis patients. Kidney Int Suppl 71:S251–S253

    Article  CAS  Google Scholar 

  25. Longenecker JC, Coresh J, Klag MJ, Powe NR, Fink NE, Marcovina SM (2008) Lipoprotein(a) level as a predictor of cardiovascular disease and small apolipoprotein(a) isoforms in dialysis patients: assay-related differences are important. Clin Chim Acta 397(1–2):36–41. https://doi.org/10.1016/j.cca.2008.07.012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Kollerits B, Krane V, Drechsler C, Lamina C, Marz W, Ritz E, Wanner C, Kronenberg F, German D, Dialysis Study I (2012) Apolipoprotein A-IV concentrations and clinical outcomes in haemodialysis patients with type 2 diabetes mellitus—a post hoc analysis of the 4D Study. J Intern Med 272(6):592–600. https://doi.org/10.1111/j.1365-2796.2012.02585.x

    Article  CAS  PubMed  Google Scholar 

  27. Zimmermann J, Herrlinger S, Pruy A, Metzger T, Wanner C (1999) Inflammation enhances cardiovascular risk and mortality in hemodialysis patients. Kidney Int 55(2):648–658. https://doi.org/10.1046/j.1523-1755.1999.00273.x

    Article  CAS  PubMed  Google Scholar 

  28. Kronenberg F, Trenkwalder E, Sturm W, Kathrein H, Konig P, Neyer U, Grochenig E, Utermann G, Dieplinger H (1997) LDL-unbound apolipoprotein(a) and carotid atherosclerosis in hemodialysis patients. Clin Genet 52(5):377–386

    Article  CAS  Google Scholar 

  29. Stenvinkel P, Heimburger O, Paultre F, Diczfalusy U, Wang T, Berglund L, Jogestrand T (1999) Strong association between malnutrition, inflammation, and atherosclerosis in chronic renal failure. Kidney Int 55(5):1899–1911. https://doi.org/10.1046/j.1523-1755.1999.00422.x

    Article  CAS  PubMed  Google Scholar 

  30. Koch M, Kutkuhn B, Trenkwalder E, Bach D, Grabensee B, Dieplinger H, Kronenberg F (1997) Apolipoprotein B, fibrinogen, HDL cholesterol, and apolipoprotein(a) phenotypes predict coronary artery disease in hemodialysis patients. J Am Soc Nephrol JASN 8(12):1889–1898

    CAS  PubMed  Google Scholar 

  31. Wanner C, Krane V, Marz W, Olschewski M, Mann JF, Ruf G, Ritz E, German D, Dialysis Study I (2005) Atorvastatin in patients with type 2 diabetes mellitus undergoing hemodialysis. N Engl J Med 353(3):238–248. https://doi.org/10.1056/nejmoa043545

    Article  CAS  PubMed  Google Scholar 

  32. Fellstrom BC, Jardine AG, Schmieder RE, Holdaas H, Bannister K, Beutler J, Chae DW, Chevaile A, Cobbe SM, Gronhagen-Riska C, De Lima JJ, Lins R, Mayer G, McMahon AW, Parving HH, Remuzzi G, Samuelsson O, Sonkodi S, Sci D, Suleymanlar G, Tsakiris D, Tesar V, Todorov V, Wiecek A, Wuthrich RP, Gottlow M, Johnsson E, Zannad F (2009) Rosuvastatin and cardiovascular events in patients undergoing hemodialysis. N Engl J Med 360(14):1395–1407. https://doi.org/10.1056/nejmoa0810177

    Article  CAS  PubMed  Google Scholar 

  33. Verdoodt A, Honore PM, Jacobs R, De Waele E, Van Gorp V, De Regt J, Spapen HD (2018) Do statins induce or protect from acute kidney injury and chronic kidney disease: an update review in 2018. J Transl Intern Med 6(1):21–25. https://doi.org/10.2478/jtim-2018-0005

    Article  Google Scholar 

  34. Kotani K, Banach M (2017) Lipoprotein(a) and inhibitors of proprotein convertase subtilisin/kexin type 9. J Thorac Dis 9(1):E78–E82

    Article  Google Scholar 

  35. Castro Cabezas M, Burggraaf B, Klop B (2018) Dyslipidemias in clinical practice. Clin Chim Acta 487:117–125. https://doi.org/10.1016/j.cca.2018.09.010

    Article  CAS  PubMed  Google Scholar 

  36. Viney NJ, van Capelleveen JC, Geary RS, Xia S, Tami JA, Yu RZ, Marcovina SM, Hughes SG, Graham MJ, Crooke RM, Crooke ST, Witztum JL, Stroes ES, Tsimikas S (2016) Antisense oligonucleotides targeting apolipoprotein(a) in people with raised lipoprotein(a): two randomised, double-blind, placebo-controlled, dose-ranging trials. Lancet 388(10057):2239–2253. https://doi.org/10.1016/S0140-6736(16)31009-1

    Article  CAS  PubMed  Google Scholar 

  37. Corsetti JP, Gansevoort RT, Bakker SJL, Dullaart RPF (2016) Apolipoprotein E levels and apolipoprotein E genotypes in incident cardiovascular disease risk in subjects of the prevention of renal and vascular end-stage disease study. J Clin Lipidol 10(4):842–850. https://doi.org/10.1016/j.jacl.2016.03.003

    Article  PubMed  Google Scholar 

  38. Guz G, Nurhan Ozdemir F, Sezer S, Isiklar I, Arat Z, Turan M, Haberal M (2000) Effect of apolipoprotein E polymorphism on serum lipid, lipoproteins, and atherosclerosis in hemodialysis patients. Am J Kidney Dis 36(4):826–836. https://doi.org/10.1053/ajkd.2000.17682

    Article  CAS  PubMed  Google Scholar 

  39. Liberopoulos E, Siamopoulos K, Elisaf M (2004) Apolipoprotein E and renal disease. Am J Kidney Dis 43(2):223–233

    Article  CAS  Google Scholar 

  40. Liu J, Rosner MH (2006) Lipid abnormalities associated with end-stage renal disease. Semin Dial 19(1):32–40. https://doi.org/10.1111/j.1525-139X.2006.00117.x

    Article  PubMed  Google Scholar 

  41. Ilveskoski E, Perola M, Lehtimaki T, Laippala P, Savolainen V, Pajarinen J, Penttila A, Lalu KH, Mannikko A, Liesto KK, Koivula T, Karhunen PJ (1999) Age-dependent association of apolipoprotein E genotype with coronary and aortic atherosclerosis in middle-aged men: an autopsy study. Circulation 100(6):608–613

    Article  CAS  Google Scholar 

  42. Imura T, Kimura H, Gejyo F (1999) Apolipoprotein E phenotypes in hemodialysis patients. Kidney Int Suppl 71:S245–S247

    Article  CAS  Google Scholar 

  43. Freedman BI, Bostrom M, Daeihagh P, Bowden DW (2007) Genetic factors in diabetic nephropathy. Clin J Am Soc Nephrol CJASN 2(6):1306–1316. https://doi.org/10.2215/CJN.02560607

    Article  CAS  PubMed  Google Scholar 

  44. Wang Y, Wang N, Lu Y, Yu Q, Zhou L, Xu Q (2017) Detection of apolipoprotein E gene polymorphism and blood lipid level in hemodialysis patients. J Clin Med Res 9(8):695–700. https://doi.org/10.14740/jocmr3046e

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Winkler K, Hoffmann MM, Krane V, Marz W, Drechsler C, Wanner C (2010) Apolipoprotein E genotype predicts cardiovascular endpoints in dialysis patients with type 2 diabetes mellitus. Atherosclerosis 208(1):197–202. https://doi.org/10.1016/j.atherosclerosis.2009.06.036

    Article  CAS  PubMed  Google Scholar 

  46. Olmer M, Renucci JE, Planells R, Bouchouareb D, Purgus R (1997) Preliminary evidence for a role of apolipoprotein E alleles in identifying haemodialysis patients at high vascular risk. Nephrol Dial Transpl 12(4):691–693

    Article  CAS  Google Scholar 

  47. Choi KH, Song HY, Shin SK, Noh H, Kang SW, Kim JH, Lee HY, Han DS (1999) Influence of apolipoprotein E genotype on lipid and lipoprotein levels in continuous ambulatory peritoneal dialysis patients. Adv Perit Dial Conf Perit Dial 15:243–246

    CAS  Google Scholar 

  48. Kwan BC, Kronenberg F, Beddhu S, Cheung AK (2007) Lipoprotein metabolism and lipid management in chronic kidney disease. J Am Soc Nephrol JASN 18(4):1246–1261. https://doi.org/10.1681/ASN.2006091006

    Article  CAS  PubMed  Google Scholar 

  49. Zhang Y, Zhang L, Cao B (2015) The association between serum ApoE genetic polymorphism and serum lipid level in hemodialysis patients. Genet Test Mol Biomark 19(2):93–97. https://doi.org/10.1089/gtmb.2014.0267

    Article  CAS  Google Scholar 

  50. Wang K, Wang P, Qiao Y, Lu X, Wang X, Liu Z (2015) The effects of serum apolipoprotein E genetic variants and concentration on serum lipid parameters in haemodialysis patients. J Pharm Pharmacol 67(5):696–702. https://doi.org/10.1111/jphp.12356

    Article  CAS  PubMed  Google Scholar 

  51. Zheng CZ, Qi XM, Shu YB, Bai YW, Wu YG (2018) Associations between apolipoprotein E gene polymorphisms and cardiovascular complications of uremic patients on maintenance hemodialysis. Blood Purif 46(1):48–55. https://doi.org/10.1159/000486846

    Article  CAS  PubMed  Google Scholar 

  52. Lim PS, Liu CS, Hong CJ, Wei YH (1997) Prevalence of apolipoprotein E genotypes in ischaemic cerebrovascular disease in end-stage renal disease patients. Nephrol Dial Transpl 12(9):1916–1920

    Article  CAS  Google Scholar 

  53. Dergunov AD (2011) Apolipoprotein E genotype as a most significant predictor of lipid response at lipid-lowering therapy: mechanistic and clinical studies. Biomed Pharmacother 65(8):597–603. https://doi.org/10.1016/j.biopha.2011.04.003

    Article  CAS  PubMed  Google Scholar 

  54. Conejero-Goldberg C, Gomar JJ, Bobes-Bascaran T, Hyde TM, Kleinman JE, Herman MM, Chen S, Davies P, Goldberg TE (2014) APOE2 enhances neuroprotection against Alzheimer’s disease through multiple molecular mechanisms. Mol Psychiatry 19(11):1243–1250. https://doi.org/10.1038/mp.2013.194

    Article  CAS  PubMed  Google Scholar 

  55. Singhrao SK, Harding A, Chukkapalli S, Olsen I, Kesavalu L, Crean S (2016) Apolipoprotein E related co-morbidities and Alzheimer’s disease. J Alzheimer’s Dis JAD 51(4):935–948. https://doi.org/10.3233/JAD150690

    Article  CAS  Google Scholar 

  56. Safieh M, Korczyn AD, Michaelson DM (2019) ApoE4: an emerging therapeutic target for Alzheimer’s disease. BMC Med 17(1):64. https://doi.org/10.1186/s12916-019-1299-4

    Article  PubMed  PubMed Central  Google Scholar 

  57. Kirmizis D, Koutoupa E, Tsiandoulas A, Valtopoulou A, Niavis G, Markou P, Barboutis K (2007) Serum lipid profile constituents as markers of cardiovascular morbidity in patients on chronic hemodialysis. Biomark Insights 1:185–192

    PubMed  PubMed Central  Google Scholar 

  58. Zhan X, Chen Y, Yan C, Liu S, Deng L, Yang Y, Qiu P, Pan D, Zeng B, Chen Q (2018) Apolipoprotein B/apolipoprotein A1 ratio and mortality among incident peritoneal dialysis patients. Lipids Health Dis 17(1):117. https://doi.org/10.1186/s12944-018-0771-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Ramasamy I (2016) Update on the molecular biology of dyslipidemias. Clin Chim Acta 454:143–185. https://doi.org/10.1016/j.cca.2015.10.033

    Article  CAS  PubMed  Google Scholar 

  60. Ferro CJ, Mark PB, Kanbay M, Sarafidis P, Heine GH, Rossignol P, Massy ZA, Mallamaci F, Valdivielso JM, Malyszko J, Verhaar MC, Ekart R, Vanholder R, London G, Ortiz A, Zoccali C (2018) Lipid management in patients with chronic kidney disease. Nat Rev Nephrol 14(12):727–749. https://doi.org/10.1038/s41581-018-0072-9

    Article  CAS  PubMed  Google Scholar 

  61. Prinsen BH, de Sain-van der Velden MG, de Koning EJ, Koomans HA, Berger R, Rabelink TJ (2003) Hypertriglyceridemia in patients with chronic renal failure: possible mechanisms. Kidney Int Suppl 84:S121–S124. https://doi.org/10.1046/j.1523-1755.63.s84.34.x

    Article  CAS  Google Scholar 

  62. Prichard SS (2006) Management of hyperlipidemia in patients on peritoneal dialysis: current approaches. Kidney Int Suppl 103:S115–S117. https://doi.org/10.1038/sj.ki.5001926

    Article  Google Scholar 

  63. Bevc S, Hojs R, Ekart R, Hojs-Fabjan T (2006) Atherosclerosis in hemodialysis patients: traditional and nontraditional risk factors. Acta dermatovenerologica Alpina, Pannonica, et Adriatica 15(4):151–157

    PubMed  Google Scholar 

  64. Ye M, Liu Y, Wang H, Tian N, Li W, He W, Lin H, Fan R, Li C, Liu D, Yao F (2018) Serum apolipoprotein B is inversely associated with eccentric left ventricular hypertrophy in peritoneal dialysis patients. Int Urol Nephrol 50(1):155–165. https://doi.org/10.1007/s11255-017-1737-1

    Article  CAS  PubMed  Google Scholar 

  65. Cicero AFG, Kuwabara M, Johnson R, Bove M, Fogacci F, Rosticci M, Giovannini M, D’Addato S, Borghi C, Brisighella Heart Study g (2018) LDL-oxidation, serum uric acid, kidney function and pulse-wave velocity: data from the Brisighella Heart Study cohort. Int J Cardiol 261:204–208. https://doi.org/10.1016/j.ijcard.2018.03.077

    Article  PubMed  Google Scholar 

  66. Sato Y, Fujimoto S, Toida T, Nakagawa H, Yamashita Y, Iwakiri T, Fukuda A, Iwatsubo S (2016) Apoprotein B/apoprotein A-1 ratio and mortality among prevalent dialysis patients. Clin J Am Soc Nephrol CJASN 11(5):840–846. https://doi.org/10.2215/CJN.09830915

    Article  CAS  PubMed  Google Scholar 

  67. Vaziri ND, Liang K (2002) Up-regulation of acyl-coenzyme A:cholesterol acyltransferase (ACAT) in nephrotic syndrome. Kidney Int 61(5):1769–1775. https://doi.org/10.1046/j.1523-1755.2002.00319.x

    Article  CAS  PubMed  Google Scholar 

  68. Zodda D, Giammona R, Schifilliti S (2018) Treatment strategy for dyslipidemia in cardiovascular disease prevention: focus on old and new drugs. Pharmacy 6(1):1. https://doi.org/10.3390/pharmacy6010010

    Article  Google Scholar 

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Funding

AB: was supported by the Romanian Academy of Medical Sciences and European Regional Development Fund, MySMIS 107124: Funding Contract 2/Axa 1/31.07.2017/107124 SMIS. AC: was supported by a grant of Ministry of Research and Innovation, CNCS—UEFISCDI, project number PN-III-P4-ID-PCE-2016-0908, contract number 167/2017, within PNCDI III.

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Vlad, C., Burlacu, A., Florea, L. et al. A comprehensive review on apolipoproteins as nontraditional cardiovascular risk factors in end-stage renal disease: current evidence and perspectives. Int Urol Nephrol 51, 1173–1189 (2019). https://doi.org/10.1007/s11255-019-02170-w

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