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ISSN 2522-9028 (Print)
ISSN 2522-9036 (Online)
DOI: https://doi.org/10.15407/fz

Fiziologichnyi Zhurnal

is a scientific journal issued by the

Bogomoletz Institute of Physiology
National Academy of Sciences of Ukraine

Editor-in-chief: V.F. Sagach

The journal was founded in 1955 as
1955 – 1977 "Fiziolohichnyi zhurnal" (ISSN 0015 – 3311)
1978 – 1993 "Fiziologicheskii zhurnal" (ISSN 0201 – 8489)
1994 – 2016 "Fiziolohichnyi zhurnal" (ISSN 0201 – 8489)
2017 – "Fiziolohichnyi zhurnal" (ISSN 2522-9028)

Fiziol. Zh. 2017; 63(5): 80-93


CALCIFICATION OF HEART AND VESSELS IN CHRONIC KIDNEY DISEASE: PROBLEMS OF ETIOLOGY AND PATHOGENESIS

О.B. Susla1, А.I. Gozhenko2, J. Bergier3, І.R. Мysula1, М.I. Shved1, O.M. Lykhodid2

  1. I.Horbachevsky Ternopil State Medical University, Ukraine
  2. Ukrainian Scientific Research Institute of Transport Medicine, Odesa, Ukraine
  3. Pope John Paul II State Higher School in Biala Podlaska,Poland
DOI: https://doi.org/10.15407/fz63.05.080


Abstract

Literature data and our research results have been summarized, regarding the reasons and development mechanisms of cardiovascular system calcification in chronic kidney disease. The role of the disordered mineral metabolism, inflammation, uremic intoxication and endothelial damage with development of nitric oxide deficiency has been underlined in formation and progression of ectopic calcifications. Significant effect of hemodialysis treatment upon accelerated mechanisms of athero- and arteriosclerosis has been shown in patients with end-stage renal disease. There is a need of further studies on etiology and pathogenesis of cardiovascular calcifications in chronic renal dysfunction in order to optimize the early diagnosis, implementation of new effective preventive and treatment strategies, stratification of cardiovascular risk.

Keywords: Chronic kidney disease; cardiovascular system; calcification; risk factors; pathogenesis; endothelial damage/ dysfunction.

References

  1. Vervloet M, Cozzolino M. Vascular calcification in chronic kidney disease: different bricks in the wall. Kidney Int. 2017 Apr; 91(4):808-17. CrossRef PubMed
  2.  
  3. Kolesnyk MO, Lapchyns'ka II, Tashchuk VK, Dyadyk OI, Kulyz'kyy MV. 2010. Cardiovascular complications in patients with chronic kidney disease. Kyiv: Polihraf Plyus, 224 p. [Ukrainian].
  4.  
  5. Rattazzi M, Bertacco E, Del Vecchio A, Puato M, Faggin E, Pauletto P. Aortic valve calcification in chronic kidney disease. Nephrol Dial Transplant. 2013 Dec;28(12):2968-76. CrossRef PubMed
  6.  
  7. Bover J, Evenepoel P, Ure-a-Torres P, Vervloet MG, Brandenburg V, Mazzaferro S et al. Pro: Cardiovascular calcification are clinically relevant. Nephrol Dial Transplant. 2015 Mar;30(3):345-51. CrossRef PubMed
  8.  
  9. London GM. Arterial calcification: cardiovascular function and clinical outcome. Nefrologia. 2011;31(6):644-7. PubMed
  10.  
  11. Peeters MJ, van den Brand JA, van Zuilen AD, Koster Y, Bots ML, Vervloet MG et al. Abdominal aortic calcification in patients with CKD. J Nephrol. 2017 Feb;30(1):109-18. CrossRef PubMed PubMedCentral
  12.  
  13. Kidney Disease: Improving Global Outcomes (KDIGO) CKD-MBD Work Group. KDIGO clinical practice guideline for the diagnosis, evaluation, prevention, and treatment of chronic kidney disease-mineral and bone disorder (CKD-MBD). Kidney Int Suppl. 2009 Aug;(113):S1-130.
  14.  
  15. Schlieper G, Schurgers L, Brandenburg V, Reutelingsperger C, Floege J. Vascular calcification in chronic kidney disease: an update. Nephrol Dial Transplant. 2016 Jan;31(1):31-9. CrossRef PubMed
  16.  
  17. Safder O, Al sharif S, Kari JA. Pediatric CKD and cardiovascular disease. Cardiovasc Hematol Disord Drug Targets. 2014;14(3):177-84. CrossRef PubMed
  18.  
  19. Valdivielso JM. Vascular calcification: types and mechanisms Nefrologia. 2011;31(2):142-7. PubMed
  20.  
  21. Zoccali C, London G. Con: Vascular calcification is a surrogate marker, but not the cause of ongoing vascular disease, and it is not a treatment target in chronic kidney disease. Nephrol Dial Transplant. 2015 Mar;30(3):352-7. CrossRef PubMed
  22.  
  23. Hruska K, Mathew S, Lund R, Fang Y, Sugatani T. Cardiovascular risk factors in chronic kidney disease: does phosphate qualify. Kidney Int. 2011 Apr;79 Suppl 121:S9-S13. CrossRef PubMedCentral
  24.  
  25. Kovalenko VN, Nesukay YeG, Titov YeYu. Acquired aortic stenosis: issues of etiology and pathogenesis. Ukrayins'kyy kardiolohichnyy zhurnal. 2010;1:96-103. [Russian].
  26.  
  27. Aronov DM. Diffuse calcinosis of the arteries: its relation to atherosclerosis and focal arterial calcinosis. Ter Arkh. 1963 Apr;35:54-8. PubMed
  28.  
  29. Bazarnaya N. 1976. Arterial calcification in atherosclerosis. Stavropol': kn. izd-vo, 212 p. [Russian].
  30.  
  31. Block GA, Hulbert-Shearon TE, Levin NW, Port FK. Association of serum phosphorus and calcium x phosphate product with mortality risk in chronic hemodialysis patients: a national study. Am J Kidney Dis. 1998 Apr;31(4):607-17. CrossRef PubMed
  32.  
  33. Giachelli CM. The emergency role of phosphate in vascular calcification. Kidney Int. 2009 May;75(9):890-7. CrossRef PubMed PubMedCentral
  34.  
  35. Korotkiy DV, Gerasimchuk RP, Makeeva YI, Zaparitskaya OP, Zemchenkov AYu. Secondary hyperparathyroidism and cardiac valve calcification in patients with predialysis CKD stages and on the renal replacement therapy. Nefrologiya i dializ. 2011;13(2):89-95. [Russian].
  36.  
  37. Kendrick J, Chonchol M. The role of phosphorus in the development and progression of vascular calcification. Am J Kidney Dis. 2011 Nov;58(5):826-34. CrossRef PubMed PubMedCentral
  38.  
  39. Coen G, Mantella D, Sardella D, Beraldi MP, Ferrari I, Pierantozzi A et al. Asymmetric dimethylarginine, vascular calcification and parathyroid hormone serum levels in hemodialysis patients. J Nephrol. 2009 SepOct;22(5):616-22.
  40.  
  41. Zemchenkov AYu, Gerasimchuk RP. Recommendations on CKD-MBD: succession, update and future (as a preface). Nefrologiya i dializ. 2011;13(1):20-30. [Russian].
  42.  
  43. Volkov MM. 2009. Significance of phosphorus-calcium metabolism disorders in the development of bone and cardiovascular pathology in patients with chronic kidney disease. Dr. med. sci. author's thesis. St. Petersburg, 44 p. [Russian].
  44.  
  45. Leskinen Y, Paana T, Saha H, Groundstroem K, Lehtimäki T, Kilpinen S et al. Valvular calcification and its relationship to atherosclerosis in chronic kidney disease J Heart Valve Dis. 2009 Jul;18(4):429-38. PubMed
  46.  
  47. Moe SM, Chen NX. Mechanisms of vascular calcification in chronic kidney disease. J Am Soc Nephrol. 2008 Feb;19(2):213-6. CrossRef PubMed
  48.  
  49. Komaba H, Fukagawa M. Phosphate – a poison for humans? Kidney Int. 2016 Oct;90(4):753-63. CrossRef PubMed
  50.  
  51. Susla OB. 2016. Clinical and pathogenetic substantiation of optimizing diagnosis, treatment and prevention of cardiovascular calcification in patients with chronic kidney disease. Dr. med. sci. author's thesis. Ternopil, 44 p. [Ukrainian].
  52.  
  53. Martynyuk LP. 2004. Clinical and pathogenetic variants of bone tissue's disturbances in chronic renal insufficiency: diagnosis, different programs of prophylaxis and treatment (clinical and experimental investigation). Dr. med. sci. author's thesis. Kyiv, 41 p. [Ukrainian].
  54.  
  55. Cannata-Andia JB, Roman-Garcia P, Hruska K. The connections between vascular calcification and bone health. Nephrol Dial Transplant. 2011 Nov;26(11):3429-36. CrossRef PubMed PubMedCentral
  56.  
  57. Shanahan CM, Crouthamel MH, Kapustin A, Giachelli CM. Arterial calcification in chronic kidney disease: key roles for calcium and phosphate. Circ Res. 2011 Sep 2;109(6):697-711. CrossRef PubMed PubMedCentral
  58.  
  59. Torun D, Sezer S, Baltali M, Adam FU, Erdem A, Ozdemir FN et al. Association of cardiac valve calcification and inflammation in patients on hemodialysis. Ren Fail. 2005;27(2):221-6. CrossRef PubMed
  60.  
  61. Simic-Ogrizovic S, Bogavac-Stanojevic N, Vuckovic M, Dopsaj V, Giga V, Kravljaca M et al. Risk factors associated with coronary artery calcification should be examined before kidney transplantation. Tohoku J Exp Med. 2012;226(2):137-44. CrossRef PubMed
  62.  
  63. Schlieper G. Vascular calcification in chronic kidney disease: not all arteries are created equal. Kidney Int. 2014 Mar;85(3):501-3. CrossRef PubMed
  64.  
  65. Dai XY, Zhao MM, Cai Y, Guan QC, Zhao Y, Guan Y, et al. Phosphate-induced autophagy counteracts vascular calcification by reducing matrix vesicle release. Kidney Int. 2013 Jun;83(6):1042-51. CrossRef PubMed
  66.  
  67. Rong S, Zhao X, Jin X, Zhang Z, Chen L, Zhu Y et al. Vascular calcification in chronic kidney disease is induced by bone morphogenetic protein-2 via a mechanism involving the Wnt/ß-catenin pathway. Cell Physiol Biochem. 2014;34(6):2049-60. CrossRef PubMed
  68.  
  69. Jean G, Chazot C. Sclerostin in CKD-MBD: one more paradoxical bone protein? Nephrol Dial Transplant. 2013 Dec;28(12):2932-5. CrossRef PubMed
  70.  
  71. Ketteler M, Elder GJ, Evenepoel P, Ix JH, Jamal SA, Lafage-Proust MH et al. Revisting KDIGO clinical practice guideline on chronic kidney disease – mineral and bone disorders: a commentary from a Kidney Disease: Improving Global Outcomes controversies conference. Kidney Int. 2015 Mar;87(3):502-28. CrossRef PubMed
  72.  
  73. Cozzolino M, Ure-a-Torres P, Vervloet MG, Brandenburg V, Bover J, Goldsmith D et al. Is chronic kidney diseasemineral bone disorders (CKD-MBD) really a syndrome? Nephrol Dial Transplant. 2014 Oct;29(10):1815-20. CrossRef PubMed
  74.  
  75. Mehrotra R, Peralta CA, Chen SC, Li S, Sachs M, Shah A et al. No independent association of serum phosphorus with risk for death or progression to end-stage renal disease in a large screen for chronic kidney disease. Kidney Int. 2013 Nov;84(5):989-97. CrossRef PubMed PubMedCentral
  76.  
  77. Scialla JJ, Lau WL, Reilly MP, Isakova T, Yang HY, Crouthamel MH et al. Fibroblast grows factor 23 is not associated with and does not induce arterial calcification. Kidney Int. 2013 Jun;83(6):1159-68. CrossRef PubMed PubMedCentral
  78.  
  79. Pelisek J, Hahntow IN, Eckstein HH, Ockert S, Reeps C, Heider P et al. Impact of chronic kidney disease on carotid plaque vulnerability. J Vasc Surg. 2011 Dec;54(6):1643-9. CrossRef PubMed
  80.  
  81. Ikee R, Honda K, Ishioka K, Oka M, Maesato K, Moriya H et al. Differences in associated factors between aortic and mitral valve calcification in hemodialysis. Hypertens Res. 2010 Jun;33(6):622-6. CrossRef PubMed
  82.  
  83. Bellasi A, Ferramosca E, Ratti C, Block G, Raggi P. Cardiac valve calcification is a marker of vascular disease in prevalent hemodialysis patients. J Nephrol. 2012 Mar-Apr;25(2):211-8. CrossRef PubMed
  84.  
  85. Susla O. Oxidative stress and systemic inflammation as important components of cardiac valve calcification in predialysis patients. Nephrol Dial Transplant. 2012 May; 27 Suppl 2:ii405.
  86.  
  87. Massy ZA, de Zeeuw D. LDL cholesterol in CKD – to treat or not to treat? Kidney Int. 2013 Sep;84(3):451-6. CrossRef PubMed
  88.  
  89. Krasniak A, Drozdz M, Pasowicz M, Chmiel G, Kowalczyk-Michalek M, Szumilak D et al. Influence of microinflammation and oxidative stress on atherosclerosis progression and calcification in cardiovascular system of hemodialyzed patients during two years follow-up. Przegl Lek. 2007;64(3):140-7. PubMed
  90.  
  91. Taki K, Takayama F, Tsuruta Y, Niwa T. Oxidative stress, advanced glycation end product, and coronary artery calcification in hemodialysis patients Kidney Int. 2006 Jul;70(1):218-24. CrossRef PubMed
  92.  
  93. Irtiuga OB, Zhiduleva EV, Dubrovskaia OB, Moiseeva OM. Concentration of osteoprotegerin and RANKL in blood serum of patients with aortic stenosis. Kardiologiia. 2014;54(6):44-8. CrossRef PubMed
  94.  
  95. Sverdlov AL, Ngo DT, Chapman MJ, Ali OA, Chirkov YY, Horowitz JD. Pathogenesis of aortic stenosis: not just a matter of wear and tear. Am J Cardiovasc Dis. 2011;1(2):185-99. PubMed PubMedCentral
  96.  
  97. Lanzer P, Boehm M, Sorribas V, Thiriet M, Janzen J, Zeller T et al. Medial vascular calcification revisited: review and perspectives. Eur Heart J. 2014 Jun 14;35(23):1515-25. CrossRef PubMed PubMedCentral
  98.  
  99. Zhao MM, Xu MJ, Cai Y, Zhao G, Guan Y, Kong W et al. Mitochondrial reactive oxygen species promote p65 nuclear translocation mediating high-phosphate-induced vascular calcification in vitro and in vivo. Kidney Int. 2011 May;79(10):1071-9. CrossRef PubMed
  100.  
  101. Miller JD, Chu Y, Brooks RM, Richenbacher WE, Pe-a-Silva R, Heistad DD. Dysregulation of antioxidant mechanisms contributes to increased oxidative stress in calcific aortic valvular stenosis in humans. J Am Coll Cardiol. 2008 Sep 2;52(10):843-50. CrossRef PubMed PubMedCentral
  102.  
  103. Byon CH, Javed A, Dai Q, Kappes JC, Clemens TL, Darley-Usmar VM et al. Oxidative stress induces vascular calcification through modulation of the osteogenic transcription factor Runx2 by AKT signaling. J Biol Chem. 2008 May 30;283(22):15319-27. CrossRef PubMed PubMedCentral
  104.  
  105. Olszowska M. Pathogenesis and pathophysiology of aortic valve stenosis in adults. Pol Arch Med Wewn. 2011 Nov;121(11):409-13. PubMed
  106.  
  107. Moradi H, Sica DA, Kalantar-Zadeh K. Cardiovascular burden associated with uremic toxins in patients with chronic kidney disease. Am J Nephrol. 2013;38(2):136-48. CrossRef PubMed
  108.  
  109. Bellien J, Fréguin-Bouilland C, Joannidès R, Hanoy M, Rémy-Jouet I, Monteil C et al. High-efficiency on-line haemodiafiltration improves conduit artery endothelial function compared with high-flux haemodialysis in endstage renal disease patients. Nephrol Dial Transplant. 2014 Feb;29(2):414-22. CrossRef PubMed
  110.  
  111. Susla OB. Activity of chronic inflammation and endothelial damage in patients with cardiac valve calcification in dialysis-dependent chronic kidney disease Ukrayins'kyy zhurnal nefrolohiyi ta dializu. 2014;4:59-64. [Ukrainian].
  112.  
  113. Drüeke TB, Olgaard K. Report on 2012 ISN Nexus Symposium: 'Bone and the Kidney'. Kidney Int. 2013 Apr;83(4):557-62. CrossRef PubMed
  114.  
  115. Shroff R. 2012. Mechanism of vascular calcification in CKD. Proceeding of the ISN Nexus Symposium 2012 «Bone and the Kidney». Copenhagen, P. 24.
  116.  
  117. Di Marco GS, König M, Stock C, Wiesinger A, Hillebrand U, Reiermann S et al. High phosphate directly affects endothelial function by downregulating annexin II. Kidney Int. 2013 Feb;83(2):213-22. CrossRef PubMed
  118.  
  119. Buendía P, Montes de Oca A, Madue-o JA, Merino A, Martín-Malo A, Aljama P et al. Endothelial microparticles mediate inflammation-induced vascular calcification. FASEB J. 2015 Jan;29(1):173-81. CrossRef PubMed
  120.  
  121. Susla O, Gozhenko A, Mysula I, Shved M. Remodeling of carotid arteries and endothelial dysfunction in patients with end-stage renal disease. NDT Plus. 2010 Jun;3(Suppl 3):iii179.
  122.  
  123. Gozhenko AI, Susla AB. The functional state of endothelium in patients with carotid artery calcification on chronic hemodialysis. Nefrologiya. 2011;15(1):37-42. [Russian].
  124.  
  125. Susla AB. Endothelial dysfunction and carotid artery calcification in patients with predialysis chronic kidney disease. Meditsina i obrazovaniye v Sibiri: elektronnyy nauchnyy zhurnal. 2013;4. Available from: http:.www.ngmu.ru/ cozo/mos/article/text_full.php?id=1103 [Russian].
  126.  
  127. Gozhenko AI, Susla AB. The functional state of endothelium in patients with carotid artery calcification on chronic hemodialysis. Nefrologiya. 2011;15(1):37-42. [Russian].
  128.  
  129. Susla AB. Endothelial dysfunction and carotid artery calcification in patients with predialysis chronic kidney disease. Meditsina i obrazovaniye v Sibiri: elektronnyy nauchnyy zhurnal. 2013;4. Available from: http:.www.ngmu.ru/ cozo/mos/article/text_full.php?id=1103 [Russian].
  130.  
  131. Rashid G, Bernheim J, Green J, Benchetrit S. Parathyroid hormone stimulates endothelial expression of atherosclerotic parameters through protein kinase pathways. Am J Physiol Renal Physiol. 2007 Apr;292(4):F1215-8. CrossRef PubMed
  132.  
  133. Wu M, Tang RN, Liu H, Pan MM, Liu BC. Parathyroid hormone-mediated chondrocyte transition of endothelial cells promotes mediate calcification in experimental secondary hyperparathyroidism. Nephrol Dial Transplant. 2013 May;28 Suppl 1:i34.
  134.  
  135. Munoz Mendoza J, Isakova T, Cai X, Bayes LY, Faul C, Scialla JJ et al. Inflammation and elevated levels of fibroblast growth factor 23 are independent risk factors for death in chronic kidney disease. Kidney Int. 2017 Mar;91(3):711-19. CrossRef PubMed PubMedCentral
  136.  
  137. Galperin TA, Cronin AJ, Leslie KS. Cutaneous manifestation of ESRD. Clin J Am Soc Nephrol. 2014 Jan;9(1):201-18. CrossRef PubMed PubMedCentral
  138.  
  139. Kramann R, Brandenburg VM, Schurgers LJ, Ketteler M, Westphal S, Leisten I et al. Novel insight into osteogenesis and matrix remodeling associated with calcific uremic arteriolopathy. Nephrol Dial Transplant. 2013 Apr;28(4):856-68. CrossRef PubMed
  140.  
  141. Zawada AM, Rogacev KS, Heine GH. Clinical relevance of epigenetic dysregulation in chronic kidney diseaseassociated cardiovascular disease. Nephrol Dial Transplant. 2013 Jul;28(7):1663-71. CrossRef PubMed
  142.  
  143. Lang F, Ritz E, Voelkl J, Alesutan I. Vascular calcification – is aldosterone a culprit? Nephrol Dial Transplant. 2013 May;28(5):1080-4. CrossRef PubMed
  144.  
  145. Majer JA. Endothelial cells and magnesium: implications in atherosclerosis. Clin Sci (Lond). 2012 May;122(9):397-407. CrossRef PubMed
  146.  
  147. Kanno Y, Into T, Lowenstein CJ, Matsushita K. Nitric oxide regulates vascular calcification by interfering with TGF-ß signaling. Cardiovasc Res. 2008 Jan;77(1):221-30. CrossRef PubMed
  148.  
  149. Bubnova MG. Pleiotropic effects of the super selective ß1- blocker nebivolol in the treatment of arterial hypertension and its complications. Consilium Medicum. 2007; 9 (9):52-60. [Russian].
  150.  
  151. Grekas D, Economou H, Makedou A, Destanis E, Theodoridou A, Avdelidou A et al. Association between hyperhomocysteinemia and ultrasonographic atherosclerotic indices of carotid arteries in chronic hemodialysis patients. Nephron Clin Pract. 2005;101(4):c180-6. CrossRef PubMed
  152.  
  153. Aggarwal HK, Jain D, Lathar M, Yadav RK, Sawhney A. Lipoproteine-A and carotid intima media thickness as cardiovascular risk factors in patients of chronic kidney disease. Ren Fail. 2010 Jul;32(6):647-52. CrossRef PubMed
  154.  
  155. Loboda OM, Krasyuk IV, Alyeksyeyeva VV, Korol' LV, Driyans'ka VYe, Dudar IO. Relationship of lipid peroxidation processes and chronic inflammation with atherosclerotic vascular changes and indicators of endothelial dysfunction in patients with CKD stages II-IV. Ukrayins'kyy zhurnal nefrolohiyi ta dializu. 2015;1:13-20. [Ukrainian].
  156.  
  157. Janda K, Krzanowski M, Gajda M, Dumnicka P, Fedak D, Grzegorz L et al. Asymmetric dimethylarginin as a risk factor for radial artery calcification in chronic kidney disease patients. Nephrol Dial Transplant. 2014 May;29 Suppl 3:iii237.
  158.  
  159. Virmani R, Joner M, Sakakura K. Recent Highlights of ATVB: calcification. Arterioscler Thromb Vasc Biol. 2014 Jul;34(7):1329-32. CrossRef PubMed
  160.  
  161. Cheng SL, Shao JS, Behrmann A, Krchma K, Towler DA. Dkk1 and MSX2-Wnt7b signaling reciprocally regulate the endothelial-mesenchimal transition in aortic endothelial cells. Arterioscler Thromb Vasc Biol. 2013 Jul;33(7):1679-89. CrossRef PubMed PubMedCentral
  162.  
  163. Nakano T, Ninomiya T, Sumiyoshi S, Onimaru M, Fujii H, Itabe H et al. Shronic kidney disease is associated with neovascularization and intraplaque hemorrhage in coronary atherosclerosis in elders: results from the Hisayama Study. Kidney Int. 2013 Aug;84(2):373-80. CrossRef PubMed
  164.  
  165. Bertacco E, Millioni R, Arrigoni G, Faggin E, Iop L, Puato M et al. Proteomic analysis of clonal interstitial aortic valve cells acquiring a pro-calcific profile. J Proteome Res. 2010 Nov 5;9(11):5913-21. CrossRef PubMed
  166.  
  167. Kennedy JA, Hua X, Mishra K, Murphy GA, Rosenkranz AC, Horowitz JD. Inhibition of calcifying nodule formation in cultured porcine aortic valve cells by nitric oxide donors. Eur J Pharmacol. 2009 Jan 5;602(1):28-35. CrossRef PubMed
  168.   Mokas S, Larivière R, Lamalice L, Gobeil S, Cornfield DN, Agharazii M et al. Hypoxia-inducible factor-1 plays a role in phosphate-induced vascular smooth muscle cell calcification. Kidney Int. 2016 Sep;90(3):598-609. Balachandran K, Sucosky P, Yoganathan AP. Hemodynamics and mechanobiology of aortic valve inflammation and calcification. Int J Inflam. 2011;2011:263870. doi:10.4061/2011/263870 CrossRef  
  169. Engelberger RP, Teta D, Henry H, De Senarclens O, Dischl B, Liaudet L, et al. Hemodialysis acutely reduces the plasma levels of ADMA without reversing impaired NO-dependent vasodilatation. Clin Sci (Lond). 2009 Aug 24;117(8):293-303. CrossRef PubMed
  170.  
  171. Khaira A, Mahajan S, Kumar A, Saraya A, Tiwari SC, Prakash S et al. Endothelial function and oxidative stress in chronic kidney disease of varying severity and effect of acute hemodialysis. Ren Fail. 2011;33(4):411-7. CrossRef PubMed
  172.  
  173. Varan HI, Dursun B, Dursun E, Ozben T, Suleymanlar G. Acute effects of hemodialysis on oxidative stress parameters in chronic uremic patients: comparison of two dialysis membranes. Int J Nephrol Renovasc Dis. 2010;3:39-45. PubMed PubMedCentral
  174.  
  175. Errakonda PR, Paladugu R, Bitla AR, Musturu SM, Lakshman J, Pemmaraju SR et al. Effect of a single hemodialysis session on endothelial dysfunction. J Nephrol. 2011 Jan-Feb;24(1):83-90. CrossRef PubMed
  176.  
  177. Migliacci R, Falcinelli F, Imperiali P, Floridi A, Nenci GG, Gresele P. Endothelial dysfunction in patients with kidney failure and vascular risk factors: acute effects of hemodialysis. Ital Heart J. 2004 May;5(5):371-7. PubMed
  178.  
  179. Koç M, Bihorac A, Segal MS. Circulating endothelial cells as potential markers of the state of the endothelium in hemodialysis patients. Am J Kidney Dis. 2003 Oct;42(4):704-12. CrossRef  
  180. Ivanochko RB, Sklyarov OYa. Status of synthase/arginase system and oxidative processes in lymphocytes lysate in blood of patients with chronic renal insufficiency after the session of hemodialysis. Medychna khimiya. 2014;16(2):26-30. [Ukrainian].
  181.  
  182. Di Marco GS, Pavenstädt H, Brand M. Soluble Flt-1 release response to heparin use: implications for dialysis patients? Nephrol Dial Transplant. 2014 Jun;29(6):1112-5. CrossRef PubMed
  183.  
  184. Gozhenko AI, Susla OB, Klym AA, Yaremchuk OZ. Effect of a hemodialysis session on structural and functional state of endothelium in patients with end-stage renal disease. Ukrayins'kyy zhurnal nefrolohiyi ta dializu. 2013;1 Suppl 1:102-7. [Ukrainian].

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