Korean Circ J.  2021 Dec;51(12):961-982. 10.4070/kcj.2021.0995.

Vascular Calcification in Chronic Kidney Disease: Distinct Features of Pathogenesis and Clinical Implication

Affiliations
  • 1Division of Nephrology, Department of Internal Medicine, Kyung Hee University, Seoul, Korea

Abstract

Chronic kidney disease (CKD) is associated with a higher prevalence of vascular calcification (VC) and cardiovascular disease. VC in CKD patients showed different pathophysiological features from those of the general population. The pathogenesis of VC in CKD is a highly organized process, and prior studies have suggested that patients with CKD have their own specific contributors to the phenotypic change of vascular smooth muscle cells (VSMCs), including uremic toxins, CKD-mineral and bone disease (CKD-MBD), inflammation, and oxidative stress. For the diagnosis and monitoring of VC in CKD, several imaging modalities, including plain radiography, ultrasound, and computed tomography have been utilized. VC in CKD patients has distinct clinical features and implications. CKD patients revealed a more intense and more prevalent calcification on the intimal and medial layers, whereas intimal calcification is predominantly observed in the general population. While a higher VC score is clearly associated with a higher risk of all-cause mortality and cardiovascular events, a greater VC score in CKD patients does not fully reflect the burden of atherosclerosis, because they have more calcification at equal volumes of atheromatous plaques. The primary goal of VC treatment in CKD is the prevention of VC progression, and the main management is to control the biochemical components of CKD-MBD. Cinacalcet and non-calcium-containing phosphate binders are the mainstay of VC prevention in CKD-MBD management. VC in patients with CKD is an ongoing area of research and is expected to advance soon.

Keyword

Vascular calcification; Chronic kidney disease; Pathogenesis; Clinical implication

Figure

  • Figure 1 Immunohistochemistry of von Kossa, fetuin-A, and CRP in the iliac artery of kidney transplant recipients. Scale bar 100 μm. Original magnification×100.39) CRP = C-reactive protein.

  • Figure 2 (A) In patients without renal dysfunction, calcification is deposited in the intimal layer; (B) CKD patients obtain the medial calcification in the absence of the atherosclerotic factor, because mineral bone disorder accelerates the calcific process; (C) In clinical practice, intimal and medial calcification frequently co-exists in CKD patients, because they already had several traditional risk factors. Notably, the intimal or medial calcific burden is greater in CKD patients than in non-CKD patients.CKD = chronic kidney disease.

  • Figure 3 The prevalence of coronary artery calcification in different CKD stages. KSN News Factsheet Vol. 15 (Sep. 2019).CKD = chronic kidney disease; KSN = Korean Society of Nephrology.

  • Figure 4 Clinical connection of vascular calcification to cardiovascular or non-cardiovascular organs in CKD.CKD = chronic kidney disease; LVH = left ventricular hypertrophy.

  • Figure 5 Target achievement of the CKD-MBD parameters and mortality risk in dialysis patients. KSN News Factsheet Vol. 18 (May 2020).Ca = calcium; CKD-MBD = chronic kidney disease-mineral and bone disease; HR = hazard ratio; KSN = Korean Society of Nephrology; P = phosphate; iPTH = intact parathyroid hormone.


Reference

1. Leopold JA. Vascular calcification: an age-old problem of old age. Circulation. 2013; 127:2380–2382. PMID: 23690467.
2. Demer LL, Tintut Y. Vascular calcification: pathobiology of a multifaceted disease. Circulation. 2008; 117:2938–2948. PMID: 18519861.
3. Braun J, Oldendorf M, Moshage W, Heidler R, Zeitler E, Luft FC. Electron beam computed tomography in the evaluation of cardiac calcification in chronic dialysis patients. Am J Kidney Dis. 1996; 27:394–401. PMID: 8604709.
4. Goodman WG, Goldin J, Kuizon BD, et al. Coronary-artery calcification in young adults with end-stage renal disease who are undergoing dialysis. N Engl J Med. 2000; 342:1478–1483. PMID: 10816185.
Article
5. Fang Y, Ginsberg C, Sugatani T, Monier-Faugere MC, Malluche H, Hruska KA. Early chronic kidney disease-mineral bone disorder stimulates vascular calcification. Kidney Int. 2014; 85:142–150. PMID: 23884339.
Article
6. Mizobuchi M, Towler D, Slatopolsky E. Vascular calcification: the killer of patients with chronic kidney disease. J Am Soc Nephrol. 2009; 20:1453–1464. PMID: 19478096.
Article
7. Rennenberg RJ, Kessels AG, Schurgers LJ, van Engelshoven JM, de Leeuw PW, Kroon AA. Vascular calcifications as a marker of increased cardiovascular risk: a meta-analysis. Vasc Health Risk Manag. 2009; 5:185–197. PMID: 19436645.
Article
8. Fang Y, Ginsberg C, Seifert M, et al. CKD-induced wingless/integration1 inhibitors and phosphorus cause the CKD-mineral and bone disorder. J Am Soc Nephrol. 2014; 25:1760–1773. PMID: 24578135.
Article
9. Zhan JK, Wang YJ, Wang Y, et al. The protective effect of GLP-1 analogue in arterial calcification through attenuating osteoblastic differentiation of human VSMCs. Int J Cardiol. 2015; 189:188–193. PMID: 25897902.
Article
10. Hénaut L, Chillon JM, Kamel S, Massy ZA. Updates on the mechanisms and the care of cardiovascular calcification in chronic kidney disease. Semin Nephrol. 2018; 38:233–250. PMID: 29753400.
Article
11. Metz RP, Patterson JL, Wilson E. Vascular smooth muscle cells: isolation, culture, and characterization. Methods Mol Biol. 2012; 843:169–176. PMID: 22222531.
Article
12. Durham AL, Speer MY, Scatena M, Giachelli CM, Shanahan CM. Role of smooth muscle cells in vascular calcification: implications in atherosclerosis and arterial stiffness. Cardiovasc Res. 2018; 114:590–600. PMID: 29514202.
Article
13. Monroy MA, Fang J, Li S, et al. Chronic kidney disease alters vascular smooth muscle cell phenotype. Front Biosci (Landmark Ed). 2015; 20:784–795. PMID: 25553479.
Article
14. Madsen M, Aarup A, Albinsson S, et al. Uremia modulates the phenotype of aortic smooth muscle cells. Atherosclerosis. 2017; 257:64–70. PMID: 28107707.
Article
15. Patidar A, Singh DK, Thakur S, Farrington K, Baydoun AR. Uremic serum-induced calcification of human aortic smooth muscle cells is a regulated process involving Klotho and RUNX2. Biosci Rep. 2019; 39:BSR20190599. PMID: 31519772.
Article
16. Cazaña-Pérez V, Cidad P, Donate-Correa J, et al. Phenotypic modulation of cultured primary human aortic vascular smooth muscle cells by uremic serum. Front Physiol. 2018; 9:89. PMID: 29483881.
Article
17. Patidar A, Singh DK, Winocour P, Farrington K, Baydoun AR. Human uraemic serum displays calcific potential in vitro that increases with advancing chronic kidney disease. Clin Sci (Lond). 2013; 125:237–245. PMID: 23464884.
Article
18. Moradi H, Sica DA, Kalantar-Zadeh K. Cardiovascular burden associated with uremic toxins in patients with chronic kidney disease. Am J Nephrol. 2013; 38:136–148. PMID: 23941724.
Article
19. Cottone S, Lorito MC, Riccobene R, et al. Oxidative stress, inflammation and cardiovascular disease in chronic renal failure. J Nephrol. 2008; 21:175–179. PMID: 18446711.
20. Kelly D, Rothwell PM. Disentangling the multiple links between renal dysfunction and cerebrovascular disease. J Neurol Neurosurg Psychiatry. 2020; 91:88–97. PMID: 31511306.
Article
21. Johnson-Davis KL, Fernelius C, Eliason NB, Wilson A, Beddhu S, Roberts WL. Blood enzymes and oxidative stress in chronic kidney disease: a cross sectional study. Ann Clin Lab Sci. 2011; 41:331–339. PMID: 22166502.
22. Yamada S, Taniguchi M, Tokumoto M, et al. The antioxidant tempol ameliorates arterial medial calcification in uremic rats: important role of oxidative stress in the pathogenesis of vascular calcification in chronic kidney disease. J Bone Miner Res. 2012; 27:474–485. PMID: 21987400.
Article
23. Huang M, Zheng L, Xu H, et al. Oxidative stress contributes to vascular calcification in patients with chronic kidney disease. J Mol Cell Cardiol. 2020; 138:256–268. PMID: 31866376.
Article
24. Podkowińska A, Formanowicz D. Chronic kidney disease as oxidative stress- and inflammatory-mediated cardiovascular disease. Antioxidants. 2020; 9:752.
Article
25. Bover J, Evenepoel P, Ureña-Torres P, et al. Pro: cardiovascular calcifications are clinically relevant. Nephrol Dial Transplant. 2015; 30:345–351. PMID: 25712934.
Article
26. Kiu Weber CI, Duchateau-Nguyen G, Solier C, et al. Cardiovascular risk markers associated with arterial calcification in patients with chronic kidney disease Stages 3 and 4. Clin Kidney J. 2014; 7:167–173. PMID: 24683472.
Article
27. Benz K, Hilgers KF, Daniel C, Amann K. Vascular calcification in chronic kidney disease: the role of inflammation. Int J Nephrol. 2018; 2018:4310379. PMID: 30186632.
Article
28. Choi SR, Lee YK, Cho AJ, et al. Malnutrition, inflammation, progression of vascular calcification and survival: Inter-relationships in hemodialysis patients. PLoS One. 2019; 14:e0216415. PMID: 31048884.
Article
29. Hénaut L, Massy ZA. New insights into the key role of interleukin 6 in vascular calcification of chronic kidney disease. Nephrol Dial Transplant. 2018; 33:543–548. PMID: 29420799.
Article
30. Benz K, Varga I, Neureiter D, et al. Vascular inflammation and media calcification are already present in early stages of chronic kidney disease. Cardiovasc Pathol. 2017; 27:57–67. PMID: 28171827.
Article
31. Gross ML, Meyer HP, Ziebart H, et al. Calcification of coronary intima and media: immunohistochemistry, backscatter imaging, and x-ray analysis in renal and nonrenal patients. Clin J Am Soc Nephrol. 2007; 2:121–134. PMID: 17699396.
Article
32. Masuda M, Miyazaki-Anzai S, Levi M, Ting TC, Miyazaki M. PERK-eIF2α-ATF4-CHOP signaling contributes to TNFα-induced vascular calcification. J Am Heart Assoc. 2013; 2:e000238. PMID: 24008080.
Article
33. Moe SM, Drüeke T, Lameire N, Eknoyan G. Chronic kidney disease-mineral-bone disorder: a new paradigm. Adv Chronic Kidney Dis. 2007; 14:3–12. PMID: 17200038.
Article
34. Block GA, Klassen PS, Lazarus JM, Ofsthun N, Lowrie EG, Chertow GM. Mineral metabolism, mortality, and morbidity in maintenance hemodialysis. J Am Soc Nephrol. 2004; 15:2208–2218. PMID: 15284307.
Article
35. Yang H, Curinga G, Giachelli CM. Elevated extracellular calcium levels induce smooth muscle cell matrix mineralization in vitro. Kidney Int. 2004; 66:2293–2299. PMID: 15569318.
36. Giachelli CM. The emerging role of phosphate in vascular calcification. Kidney Int. 2009; 75:890–897. PMID: 19145240.
Article
37. Jono S, McKee MD, Murry CE, et al. Phosphate regulation of vascular smooth muscle cell calcification. Circ Res. 2000; 87:E10–E17. PMID: 11009570.
Article
38. Jono S, Shioi A, Ikari Y, Nishizawa Y. Vascular calcification in chronic kidney disease. J Bone Miner Metab. 2006; 24:176–181. PMID: 16502129.
Article
39. Hwang HS, Lim SW, Sun IO, et al. Clinical significance of preexisting microcalcification in the iliac artery in renal transplant recipients. Transplantation. 2015; 99:811–817. PMID: 25211516.
Article
40. Quarles LD. Role of FGF23 in vitamin D and phosphate metabolism: implications in chronic kidney disease. Exp Cell Res. 2012; 318:1040–1048. PMID: 22421513.
Article
41. Scialla JJ, Xie H, Rahman M, et al. Fibroblast growth factor-23 and cardiovascular events in CKD. J Am Soc Nephrol. 2014; 25:349–360. PMID: 24158986.
Article
42. Hu MC, Shi M, Zhang J, et al. Klotho deficiency causes vascular calcification in chronic kidney disease. J Am Soc Nephrol. 2011; 22:124–136. PMID: 21115613.
Article
43. Krishnasamy R, Tan SJ, Hawley CM, et al. Progression of arterial stiffness is associated with changes in bone mineral markers in advanced CKD. BMC Nephrol. 2017; 18:281. PMID: 28870151.
Article
44. Baralić M, Brković V, Stojanov V, et al. Dual roles of the mineral metabolism disorders biomarkers in prevalent hemodilysis patients: in renal bone disease and in vascular calcification. J Med Biochem. 2019; 38:134–144. PMID: 30867641.
Article
45. Desjardins L, Liabeuf S, Renard C, et al. FGF23 is independently associated with vascular calcification but not bone mineral density in patients at various CKD stages. Osteoporos Int. 2012; 23:2017–2025. PMID: 22109743.
Article
46. Morena M, Jaussent I, Halkovich A, et al. Bone biomarkers help grading severity of coronary calcifications in non dialysis chronic kidney disease patients. PLoS One. 2012; 7:e36175. PMID: 22567137.
Article
47. Zhu D, Mackenzie NC, Millan JL, Farquharson C, MacRae VE. A protective role for FGF-23 in local defence against disrupted arterial wall integrity? Mol Cell Endocrinol. 2013; 372:1–11. PMID: 23523568.
Article
48. Boyce BF, Xing L. Functions of RANKL/RANK/OPG in bone modeling and remodeling. Arch Biochem Biophys. 2008; 473:139–146. PMID: 18395508.
Article
49. Bucay N, Sarosi I, Dunstan CR, et al. Osteoprotegerin-deficient mice develop early onset osteoporosis and arterial calcification. Genes Dev. 1998; 12:1260–1268. PMID: 9573043.
50. Kiechl S, Werner P, Knoflach M, Furtner M, Willeit J, Schett G. The osteoprotegerin/RANK/RANKL system: a bone key to vascular disease. Expert Rev Cardiovasc Ther. 2006; 4:801–811. PMID: 17173497.
Article
51. Kaden JJ, Bickelhaupt S, Grobholz R, et al. Receptor activator of nuclear factor kappaB ligand and osteoprotegerin regulate aortic valve calcification. J Mol Cell Cardiol. 2004; 36:57–66. PMID: 14734048.
52. Van Campenhout A, Golledge J. Osteoprotegerin, vascular calcification and atherosclerosis. Atherosclerosis. 2009; 204:321–329. PMID: 19007931.
Article
53. Morena M, Jaussent I, Dupuy AM, et al. Osteoprotegerin and sclerostin in chronic kidney disease prior to dialysis: potential partners in vascular calcifications. Nephrol Dial Transplant. 2015; 30:1345–1356. PMID: 25854266.
Article
54. Mesquita M, Demulder A, Damry N, et al. Plasma osteoprotegerin is an independent risk factor for mortality and an early biomarker of coronary vascular calcification in chronic kidney disease. Clin Chem Lab Med. 2009; 47:339–346. PMID: 19676147.
Article
55. Mikami S, Hamano T, Fujii N, et al. Serum osteoprotegerin as a screening tool for coronary artery calcification score in diabetic pre-dialysis patients. Hypertens Res. 2008; 31:1163–1170. PMID: 18716364.
Article
56. Heiss A, DuChesne A, Denecke B, et al. Structural basis of calcification inhibition by alpha 2-HS glycoprotein/fetuin-A. Formation of colloidal calciprotein particles. J Biol Chem. 2003; 278:13333–13341. PMID: 12556469.
57. Cai MM, Smith ER, Holt SG. The role of fetuin-A in mineral trafficking and deposition. Bonekey Rep. 2015; 4:672. PMID: 25987986.
Article
58. Schäfer C, Heiss A, Schwarz A, et al. The serum protein alpha 2-Heremans-Schmid glycoprotein/fetuin-A is a systemically acting inhibitor of ectopic calcification. J Clin Invest. 2003; 112:357–366. PMID: 12897203.
59. Ketteler M, Bongartz P, Westenfeld R, et al. Association of low fetuin-A (AHSG) concentrations in serum with cardiovascular mortality in patients on dialysis: a cross-sectional study. Lancet. 2003; 361:827–833. PMID: 12642050.
Article
60. Reynolds JL, Skepper JN, McNair R, et al. Multifunctional roles for serum protein fetuin-a in inhibition of human vascular smooth muscle cell calcification. J Am Soc Nephrol. 2005; 16:2920–2930. PMID: 16093453.
Article
61. Matsui I, Hamano T, Mikami S, et al. Fully phosphorylated fetuin-A forms a mineral complex in the serum of rats with adenine-induced renal failure. Kidney Int. 2009; 75:915–928. PMID: 19190677.
Article
62. Hamano T, Matsui I, Mikami S, et al. Fetuin-mineral complex reflects extraosseous calcification stress in CKD. J Am Soc Nephrol. 2010; 21:1998–2007. PMID: 20947626.
Article
63. Disthabanchong S, Boongird S. Role of different imaging modalities of vascular calcification in predicting outcomes in chronic kidney disease. World J Nephrol. 2017; 6:100–110. PMID: 28540199.
Article
64. Kauppila LI, Polak JF, Cupples LA, Hannan MT, Kiel DP, Wilson PW. New indices to classify location, severity and progression of calcific lesions in the abdominal aorta: a 25-year follow-up study. Atherosclerosis. 1997; 132:245–250. PMID: 9242971.
Article
65. Raggi P, Bellasi A, Ferramosca E, Islam T, Muntner P, Block GA. Association of pulse wave velocity with vascular and valvular calcification in hemodialysis patients. Kidney Int. 2007; 71:802–807. PMID: 17311068.
Article
66. Bellasi A, Ferramosca E, Muntner P, et al. Correlation of simple imaging tests and coronary artery calcium measured by computed tomography in hemodialysis patients. Kidney Int. 2006; 70:1623–1628. PMID: 16955104.
Article
67. Okuno S, Ishimura E, Kitatani K, et al. Presence of abdominal aortic calcification is significantly associated with all-cause and cardiovascular mortality in maintenance hemodialysis patients. Am J Kidney Dis. 2007; 49:417–425. PMID: 17336703.
Article
68. Verbeke F, Van Biesen W, Honkanen E, et al. CORD Study Investigators. Prognostic value of aortic stiffness and calcification for cardiovascular events and mortality in dialysis patients: outcome of the calcification outcome in renal disease (CORD) study. Clin J Am Soc Nephrol. 2011; 6:153–159. PMID: 20829424.
Article
69. Bellasi A, Raggi P. Techniques and technologies to assess vascular calcification. Semin Dial. 2007; 20:129–133. PMID: 17374086.
70. Guérin AP, London GM, Marchais SJ, Metivier F. Arterial stiffening and vascular calcifications in end-stage renal disease. Nephrol Dial Transplant. 2000; 15:1014–1021. PMID: 10862640.
Article
71. Oh DJ. Continuous ambulatory peritoneal dialysis patients show high prevalence of carotid artery calcification which is associated with a higher left ventricular mass index. J Korean Med Sci. 2005; 20:848–852. PMID: 16224161.
Article
72. Sumida Y, Nakayama M, Nagata M, et al. Carotid artery calcification and atherosclerosis at the initiation of hemodialysis in patients with end-stage renal disease. Clin Nephrol. 2010; 73:360–369. PMID: 20420796.
Article
73. Nakayama M, Ura Y, Nagata M, et al. Carotid artery calcification at the initiation of hemodialysis is a risk factor for cardiovascular events in patients with end-stage renal disease: a cohort study. BMC Nephrol. 2011; 12:56. PMID: 21999942.
Article
74. Disthabanchong S. Vascular calcification in chronic kidney disease: Pathogenesis and clinical implication. World J Nephrol. 2012; 1:43–53. PMID: 24175241.
Article
75. Lima A, Carrilho P, Germano A. Clinical and ultrasound evaluation for hemodialysis access creation. Nefrologia (Engl Ed). 2021.
Article
76. Shenoy S, Darcy M. Ultrasound as a tool for preoperative planning, monitoring, and interventions in dialysis arteriovenous access. AJR Am J Roentgenol. 2013; 201:W539–W543. PMID: 24059390.
Article
77. Dube P, DeRiso A, Patel M, et al. Vascular calcification in chronic kidney disease: diversity in the vessel wall. Biomedicines. 2021; 9:404. PMID: 33917965.
Article
78. Agatston AS, Janowitz WR, Hildner FJ, Zusmer NR, Viamonte M Jr, Detrano R. Quantification of coronary artery calcium using ultrafast computed tomography. J Am Coll Cardiol. 1990; 15:827–832. PMID: 2407762.
Article
79. Karohl C, D'Marco Gascón L, Raggi P. Noninvasive imaging for assessment of calcification in chronic kidney disease. Nat Rev Nephrol. 2011; 7:567–577. PMID: 21862991.
Article
80. De Mauri A, Brambilla M, Chiarinotti D, Matheoud R, Carriero A, De Leo M. Estimated radiation exposure from medical imaging in hemodialysis patients. J Am Soc Nephrol. 2011; 22:571–578. PMID: 21355057.
Article
81. Marinelli A, Pistolesi V, Pasquale L, et al. Diagnosis of arterial media calcification in chronic kidney disease. Cardiorenal Med. 2013; 3:89–95. PMID: 23922548.
Article
82. Mehrotra R, Budoff M, Hokanson JE, Ipp E, Takasu J, Adler S. Progression of coronary artery calcification in diabetics with and without chronic kidney disease. Kidney Int. 2005; 68:1258–1266. PMID: 16105059.
Article
83. Poli FE, Gulsin GS, McCann GP, Burton JO, Graham-Brown MP. The assessment of coronary artery disease in patients with end-stage renal disease. Clin Kidney J. 2019; 12:721–734. PMID: 31583096.
Article
84. Kidney Disease: Improving Global Outcomes (KDIGO) CKD-MBD Update Work Group. KDIGO 2017 clinical practice guideline update for the diagnosis, evaluation, prevention, and treatment of chronic kidney disease-mineral and bone disorder (CKD-MBD). Kidney Int Suppl (2011). 2017; 7:1–59. PMID: 30675420.
85. Reiss AB, Miyawaki N, Moon J, et al. CKD, arterial calcification, atherosclerosis and bone health: inter-relationships and controversies. Atherosclerosis. 2018; 278:49–59. PMID: 30253289.
Article
86. Zoccali C. Traditional and emerging cardiovascular and renal risk factors: an epidemiologic perspective. Kidney Int. 2006; 70:26–33. PMID: 16723985.
Article
87. Kim Y, Cho JS, Cho WK, et al. Retinopathy and left ventricular hypertrophy in patients with chronic kidney disease: Interrelationship and impact on clinical outcomes. Int J Cardiol. 2017; 249:372–376. PMID: 29121742.
Article
88. Hwang HS, Choi YA, Kim SY, et al. Diabetes retinopathy is a poor predictor for renal and cardiovascular outcomes in comparison with hypertensive retinopathy in patients with chronic kidney disease. Diabetes Res Clin Pract. 2015; 109:312–318. PMID: 26008724.
Article
89. Drüeke TB, Massy ZA. Atherosclerosis in CKD: differences from the general population. Nat Rev Nephrol. 2010; 6:723–735. PMID: 20978469.
Article
90. Nakano T, Ninomiya T, Sumiyoshi S, et al. Association of kidney function with coronary atherosclerosis and calcification in autopsy samples from Japanese elders: the Hisayama study. Am J Kidney Dis. 2010; 55:21–30. PMID: 19765871.
Article
91. Nakamura S, Ishibashi-Ueda H, Niizuma S, Yoshihara F, Horio T, Kawano Y. Coronary calcification in patients with chronic kidney disease and coronary artery disease. Clin J Am Soc Nephrol. 2009; 4:1892–1900. PMID: 19833908.
Article
92. Oh KH, Kang M, Kang E, et al. The KNOW-CKD Study: What we have learned about chronic kidney diseases. Kidney Res Clin Pract. 2020; 39:121–135. PMID: 32550711.
Article
93. Goodman WG, London G, Amann K, et al. Vascular calcification in chronic kidney disease. Am J Kidney Dis. 2004; 43:572–579. PMID: 14981617.
Article
94. Moe SM, O'Neill KD, Duan D, et al. Medial artery calcification in ESRD patients is associated with deposition of bone matrix proteins. Kidney Int. 2002; 61:638–647. PMID: 11849407.
Article
95. Milliner DS, Zinsmeister AR, Lieberman E, Landing B. Soft tissue calcification in pediatric patients with end-stage renal disease. Kidney Int. 1990; 38:931–936. PMID: 2266678.
Article
96. Hwang HS, Cho JS, Hong YA, et al. Vascular calcification and left ventricular hypertrophy in hemodialysis patients: interrelationship and clinical impacts. Int J Med Sci. 2018; 15:557–563. PMID: 29725245.
Article
97. London GM, Marchais SJ, Guérin AP, Métivier F. Arteriosclerosis, vascular calcifications and cardiovascular disease in uremia. Curr Opin Nephrol Hypertens. 2005; 14:525–531. PMID: 16205470.
Article
98. Lee HY, Lim S, Park S. Role of inflammation in arterial calcification. Korean Circ J. 2021; 51:114–125. PMID: 33525066.
Article
99. Mori D, Matsui I, Shimomura A, et al. Protein carbamylation exacerbates vascular calcification. Kidney Int. 2018; 94:72–90. PMID: 29716796.
Article
100. Voelkl J, Cejka D, Alesutan I. An overview of the mechanisms in vascular calcification during chronic kidney disease. Curr Opin Nephrol Hypertens. 2019; 28:289–296. PMID: 30985336.
Article
101. Merjanian R, Budoff M, Adler S, Berman N, Mehrotra R. Coronary artery, aortic wall, and valvular calcification in nondialyzed individuals with type 2 diabetes and renal disease. Kidney Int. 2003; 64:263–271. PMID: 12787418.
Article
102. Kramer H, Toto R, Peshock R, Cooper R, Victor R. Association between chronic kidney disease and coronary artery calcification: the Dallas Heart Study. J Am Soc Nephrol. 2005; 16:507–513. PMID: 15601745.
Article
103. Lee W, Yoon YE, Kwon O, et al. Evaluation of coronary artery calcium progression in asymptomatic individuals with an initial score of zero. Korean Circ J. 2019; 49:448–457. PMID: 30808082.
Article
104. Bover J, Aguilar A, Arana C, et al. Clinical approach to vascular calcification in patients with non-dialysis dependent chronic kidney disease: mineral-bone disorder-related aspects. Front Med (Lausanne). 2021; 8:642718. PMID: 34095165.
Article
105. Budoff MJ, Rader DJ, Reilly MP, et al. CRIC Study Investigators. Relationship of estimated GFR and coronary artery calcification in the CRIC (Chronic Renal Insufficiency Cohort) Study. Am J Kidney Dis. 2011; 58:519–526. PMID: 21783289.
Article
106. Górriz JL, Molina P, Cerverón MJ, et al. Vascular calcification in patients with nondialysis CKD over 3 years. Clin J Am Soc Nephrol. 2015; 10:654–666. PMID: 25770175.
Article
107. Kestenbaum BR, Adeney KL, de Boer IH, Ix JH, Shlipak MG, Siscovick DS. Incidence and progression of coronary calcification in chronic kidney disease: the Multi-Ethnic Study of Atherosclerosis. Kidney Int. 2009; 76:991–998. PMID: 19692998.
Article
108. Kronmal RA, McClelland RL, Detrano R, et al. Risk factors for the progression of coronary artery calcification in asymptomatic subjects: results from the Multi-Ethnic Study of Atherosclerosis (MESA). Circulation. 2007; 115:2722–2730. PMID: 17502571.
109. Reynolds JL, Joannides AJ, Skepper JN, et al. Human vascular smooth muscle cells undergo vesicle-mediated calcification in response to changes in extracellular calcium and phosphate concentrations: a potential mechanism for accelerated vascular calcification in ESRD. J Am Soc Nephrol. 2004; 15:2857–2867. PMID: 15504939.
Article
110. Daniel WT, Weber C, Bailey JA, Raggi P, Sharma J. Prospective analysis of coronary calcium in patients on dialysis undergoing a near-total parathyroidectomy. Surgery. 2013; 154:1315–1321. PMID: 24238050.
Article
111. Savage T, Clarke AL, Giles M, Tomson CR, Raine AE. Calcified plaque is common in the carotid and femoral arteries of dialysis patients without clinical vascular disease. Nephrol Dial Transplant. 1998; 13:2004–2012. PMID: 9719155.
Article
112. Schlieper G, Aretz A, Verberckmoes SC, et al. Ultrastructural analysis of vascular calcifications in uremia. J Am Soc Nephrol. 2010; 21:689–696. PMID: 20203159.
Article
113. Kim SY, Hong YA, Yoon HE, et al. Vascular calcification and intradialytic hypotension in hemodialysis patients: Clinical relevance and impact on morbidity and mortality. Int J Cardiol. 2016; 217:156–160. PMID: 27183451.
Article
114. Alappan HR, Vasanth P, Manzoor S, O'Neill WC. Vascular calcification slows but does not regress after kidney transplantation. Kidney Int Rep. 2020; 5:2212–2217. PMID: 33305114.
Article
115. Schankel K, Robinson J, Bloom RD, et al. Determinants of coronary artery calcification progression in renal transplant recipients. Am J Transplant. 2007; 7:2158–2164. PMID: 17640315.
Article
116. Bargnoux AS, Dupuy AM, Garrigue V, et al. Evolution of coronary artery calcifications following kidney transplantation: relationship with osteoprotegerin levels. Am J Transplant. 2009; 9:2571–2579. PMID: 19775319.
Article
117. Mazzaferro S, Pasquali M, Taggi F, et al. Progression of coronary artery calcification in renal transplantation and the role of secondary hyperparathyroidism and inflammation. Clin J Am Soc Nephrol. 2009; 4:685–690. PMID: 19211668.
Article
118. Messa P, Sindici C, Cannella G, et al. Persistent secondary hyperparathyroidism after renal transplantation. Kidney Int. 1998; 54:1704–1713. PMID: 9844148.
Article
119. Lou I, Foley D, Odorico SK, et al. How well does renal transplantation cure hyperparathyroidism? Ann Surg. 2015; 262:653–659. PMID: 26366545.
Article
120. Mathur A, Sutton W, Ahn JB, et al. Association between treatment of secondary hyperparathyroidism and posttransplant outcomes. Transplantation. 2021.
Article
121. Hwang HS, Kim JS, Kim YG, et al. Circulating PCSK9 level and risk of cardiovascular events and death in hemodialysis patients. J Clin Med. 2020; 9:9.
Article
122. Hwang HS, Kim JS, Kim YG, et al. Circulating neprilysin level predicts the risk of cardiovascular events in hemodialysis patients. Front Cardiovasc Med. 2021; 8:684297. PMID: 34212014.
Article
123. Cho IJ, Chang HJ, Lee SE, Shim CY, Hong GR, Chung N. Prognostic application of thoracic aortic calcium scoring for adverse clinical outcome risk in elderly patients with left ventricular hypertrophy. Korean Circ J. 2017; 47:918–928. PMID: 29035431.
Article
124. Chen J, Budoff MJ, Reilly MP, et al. Coronary artery calcification and risk of cardiovascular disease and death among patients with chronic kidney disease. JAMA Cardiol. 2017; 2:635–643. PMID: 28329057.
Article
125. Nelson AJ, Raggi P, Wolf M, Gold AM, Chertow GM, Roe MT. Targeting vascular calcification in chronic kidney disease. JACC Basic Transl Sci. 2020; 5:398–412. PMID: 32368697.
Article
126. 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; S1–S130.
127. Dilsizian V, Gewirtz H, Marwick TH, et al. Cardiac imaging for coronary heart disease risk stratification in chronic kidney disease. JACC Cardiovasc Imaging. 2021; 14:669–682. PMID: 32828780.
128. Herzog CA, Natwick T, Li S, Charytan DM. Comparative utilization and temporal trends in cardiac stress testing in U.S. Medicare beneficiaries with and without chronic kidney disease. JACC Cardiovasc Imaging. 2019; 12:1420–1426. PMID: 29909107.
129. Mathew RO, Bangalore S, Lavelle MP, et al. Diagnosis and management of atherosclerotic cardiovascular disease in chronic kidney disease: a review. Kidney Int. 2017; 91:797–807. PMID: 28040264.
130. Schwarz U, Buzello M, Ritz E, et al. Morphology of coronary atherosclerotic lesions in patients with end-stage renal failure. Nephrol Dial Transplant. 2000; 15:218–223. PMID: 10648668.
Article
131. Sharples EJ, Pereira D, Summers S, et al. Coronary artery calcification measured with electron-beam computerized tomography correlates poorly with coronary artery angiography in dialysis patients. Am J Kidney Dis. 2004; 43:313–319. PMID: 14750097.
Article
132. Haydar AA, Hujairi NM, Covic AA, Pereira D, Rubens M, Goldsmith DJ. Coronary artery calcification is related to coronary atherosclerosis in chronic renal disease patients: a study comparing EBCT-generated coronary artery calcium scores and coronary angiography. Nephrol Dial Transplant. 2004; 19:2307–2312. PMID: 15213315.
Article
133. Yiu KH, de Graaf FR, van Velzen JE, et al. Different value of coronary calcium score to predict obstructive coronary artery disease in patients with and without moderate chronic kidney disease. Neth Heart J. 2013; 21:347–353. PMID: 23579986.
Article
134. Hwang HS, Kim SY, Hong YA, et al. Clinical impact of coexisting retinopathy and vascular calcification on chronic kidney disease progression and cardiovascular events. Nutr Metab Cardiovasc Dis. 2016; 26:590–596. PMID: 27089976.
Article
135. Hwang HS, Park MW, Yoon HE, et al. Clinical significance of chronic kidney disease and atrial fibrillation on morbidity and mortality in patients with acute myocardial infarction. Am J Nephrol. 2014; 40:345–352. PMID: 25358406.
Article
136. Naves M, Rodríguez-García M, Díaz-López JB, Gómez-Alonso C, Cannata-Andía JB. Progression of vascular calcifications is associated with greater bone loss and increased bone fractures. Osteoporos Int. 2008; 19:1161–1166. PMID: 18180973.
Article
137. London GM, Marty C, Marchais SJ, Guerin AP, Metivier F, de Vernejoul MC. Arterial calcifications and bone histomorphometry in end-stage renal disease. J Am Soc Nephrol. 2004; 15:1943–1951. PMID: 15213285.
Article
138. Lee SM, Kim SE, Lee JY, Jeong HJ, Son YK, An WS. Serum myostatin levels are associated with abdominal aortic calcification in dialysis patients. Kidney Res Clin Pract. 2019; 38:481–489. PMID: 31537054.
Article
139. Osako MK, Nakagami H, Koibuchi N, et al. Estrogen inhibits vascular calcification via vascular RANKL system: common mechanism of osteoporosis and vascular calcification. Circ Res. 2010; 107:466–475. PMID: 20595654.
140. Viegas C, Araújo N, Marreiros C, Simes D. The interplay between mineral metabolism, vascular calcification and inflammation in Chronic Kidney Disease (CKD): challenging old concepts with new facts. Aging (Albany NY). 2019; 11:4274–4299. PMID: 31241466.
Article
141. Nam YJ, Hwang SY, Kim DW, Kim D, Shin SJ, Yoon HE. Sex-specific relationship between vascular calcification and incident fracture in patients with end-stage renal disease. Kidney Res Clin Pract. 2020; 39:344–355. PMID: 32522894.
Article
142. An WS. Sex hormones impact vascular calcification and fracture in dialysis patients. Kidney Res Clin Pract. 2020; 39:236–238. PMID: 32958722.
Article
143. Jensky NE, Criqui MH, Wright CM, Wassel CL, Alcaraz JE, Allison MA. The association between abdominal body composition and vascular calcification. Obesity (Silver Spring). 2011; 19:2418–2424. PMID: 21475146.
Article
144. Ko BJ, Chang Y, Jung HS, et al. Relationship between low relative muscle mass and coronary artery calcification in healthy adults. Arterioscler Thromb Vasc Biol. 2016; 36:1016–1021. PMID: 27034471.
Article
145. Lee MJ, Park JT, Park KS, et al. Normal body mass index with central obesity has increased risk of coronary artery calcification in Korean patients with chronic kidney disease. Kidney Int. 2016; 90:1368–1376. PMID: 27884313.
Article
146. Paoli S, Mitsnefes MM. Coronary artery calcification and cardiovascular disease in children with chronic kidney disease. Curr Opin Pediatr. 2014; 26:193–197. PMID: 24632542.
Article
147. Cordeiro AC, Qureshi AR, Lindholm B, et al. Visceral fat and coronary artery calcification in patients with chronic kidney disease. Nephrol Dial Transplant. 2013; 28(Suppl 4):iv152–iv159. PMID: 23832273.
Article
148. Moreno-Gonzalez R, Corbella X, Mattace-Raso F, et al. Prevalence of sarcopenia in community-dwelling older adults using the updated EWGSOP2 definition according to kidney function and albuminuria: the Screening for CKD among Older People across Europe (SCOPE) study. BMC Geriatr. 2020; 20(Suppl 1):327. PMID: 33008317.
Article
149. Kim SH, Choi G, Song Y, et al. Low muscle mass in patients receiving hemodialysis: correlations with vascular calcification and vascular access failure. J Clin Med. 2021; 10:10.
Article
150. Pérez-Ricart A, Galicia-Basart M, Comas-Sugrañes D, Cruzado-Garrit JM, Segarra-Medrano A, Montoro-Ronsano JB. Long-term effectiveness of cinacalcet in non-dialysis patients with chronic kidney disease and secondary hyperparathyroidism. Kidney Res Clin Pract. 2019; 38:229–238. PMID: 31022778.
Article
151. Park EJ, Jung SW, Kim DR, et al. Conversion from acetate dialysate to citrate dialysate in a central delivery system for maintenance hemodialysis patients. Kidney Res Clin Pract. 2019; 38:100–107. PMID: 30754934.
Article
152. Shroff R, Egerton M, Bridel M, et al. A bimodal association of vitamin D levels and vascular disease in children on dialysis. J Am Soc Nephrol. 2008; 19:1239–1246. PMID: 18337484.
Article
153. Mathew S, Lund RJ, Chaudhary LR, Geurs T, Hruska KA. Vitamin D receptor activators can protect against vascular calcification. J Am Soc Nephrol. 2008; 19:1509–1519. PMID: 18448587.
Article
154. Ketteler M, Martin KJ, Wolf M, et al. Paricalcitol versus cinacalcet plus low-dose vitamin D therapy for the treatment of secondary hyperparathyroidism in patients receiving haemodialysis: results of the IMPACT SHPT study. Nephrol Dial Transplant. 2012; 27:3270–3278. PMID: 22387567.
Article
155. Teng M, Wolf M, Lowrie E, Ofsthun N, Lazarus JM, Thadhani R. Survival of patients undergoing hemodialysis with paricalcitol or calcitriol therapy. N Engl J Med. 2003; 349:446–456. PMID: 12890843.
Article
156. Anis KH, Pober D, Rosas SE. Vitamin D analogues and coronary calcification in CKD Stages 3 and 4: a randomized controlled trial of calcitriol versus paricalcitol. Kidney Med. 2020; 2:450–458. PMID: 32775985.
Article
157. Raggi P, Chertow GM, Torres PU, et al. The ADVANCE study: a randomized study to evaluate the effects of cinacalcet plus low-dose vitamin D on vascular calcification in patients on hemodialysis. Nephrol Dial Transplant. 2011; 26:1327–1339. PMID: 21148030.
Article
158. Moe SM, Abdalla S, Chertow GM, et al. Effects of cinacalcet on fracture events in patients receiving hemodialysis: the EVOLVE trial. J Am Soc Nephrol. 2015; 26:1466–1475. PMID: 25505257.
Article
159. Chertow GM, Block GA, Correa-Rotter R, et al. Effect of cinacalcet on cardiovascular disease in patients undergoing dialysis. N Engl J Med. 2012; 367:2482–2494. PMID: 23121374.
Article
160. Komaba H, Wang M, Taniguchi M, et al. Initiation of sevelamer and mortality among hemodialysis patients treated with calcium-based phosphate binders. Clin J Am Soc Nephrol. 2017; 12:1489–1497. PMID: 28724618.
Article
161. Kakuta T, Tanaka R, Hyodo T, et al. Effect of sevelamer and calcium-based phosphate binders on coronary artery calcification and accumulation of circulating advanced glycation end products in hemodialysis patients. Am J Kidney Dis. 2011; 57:422–431. PMID: 21239096.
Article
162. Patel L, Bernard LM, Elder GJ. Sevelamer versus calcium-based binders for treatment of hyperphosphatemia in CKD: a meta-analysis of randomized controlled trials. Clin J Am Soc Nephrol. 2016; 11:232–244. PMID: 26668024.
Article
163. Block GA, Raggi P, Bellasi A, Kooienga L, Spiegel DM. Mortality effect of coronary calcification and phosphate binder choice in incident hemodialysis patients. Kidney Int. 2007; 71:438–441. PMID: 17200680.
Article
164. Krueger T, Schlieper G, Schurgers L, et al. Vitamin K1 to slow vascular calcification in haemodialysis patients (VitaVasK trial): a rationale and study protocol. Nephrol Dial Transplant. 2014; 29:1633–1638. PMID: 24285427.
Article
165. Caluwé R, Pyfferoen L, De Boeck K, De Vriese AS. The effects of vitamin K supplementation and vitamin K antagonists on progression of vascular calcification: ongoing randomized controlled trials. Clin Kidney J. 2016; 9:273–279. PMID: 26985380.
Article
166. Caluwé R, Verbeke F, De Vriese AS. Evaluation of vitamin K status and rationale for vitamin K supplementation in dialysis patients. Nephrol Dial Transplant. 2020; 35:23–33. PMID: 30590803.
Article
167. Chan KE, Lazarus JM, Thadhani R, Hakim RM. Warfarin use associates with increased risk for stroke in hemodialysis patients with atrial fibrillation. J Am Soc Nephrol. 2009; 20:2223–2233. PMID: 19713308.
Article
168. Olesen JB, Lip GY, Kamper AL, et al. Stroke and bleeding in atrial fibrillation with chronic kidney disease. N Engl J Med. 2012; 367:625–635. PMID: 22894575.
Article
169. Rattazzi M, Faggin E, Bertacco E, et al. Warfarin, but not rivaroxaban, promotes the calcification of the aortic valve in ApoE-/- mice. Cardiovasc Ther. 2018; 36:e12438. PMID: 29847020.
Article
170. Hasific S, Øvrehus KA, Gerke O, et al. Extent of arterial calcification by conventional vitamin K antagonist treatment. PLoS One. 2020; 15:e0241450. PMID: 33119722.
Article
171. Plank F, Beyer C, Friedrich G, et al. Influence of vitamin K antagonists and direct oral anticoagulation on coronary artery disease: a CTA analysis. Int J Cardiol. 2018; 260:11–15. PMID: 29530620.
Article
172. Lee J, Nakanishi R, Li D, et al. Randomized trial of rivaroxaban versus warfarin in the evaluation of progression of coronary atherosclerosis. Am Heart J. 2018; 206:127–130. PMID: 30227941.
Article
173. Win TT, Nakanishi R, Osawa K, et al. Apixaban versus warfarin in evaluation of progression of atherosclerotic and calcified plaques (prospective randomized trial). Am Heart J. 2019; 212:129–133. PMID: 31002997.
Article
174. De Vriese AS, Caluwé R, Pyfferoen L, et al. Multicenter randomized controlled trial of vitamin K antagonist replacement by rivaroxaban with or without vitamin K2 in hemodialysis patients with atrial fibrillation: the Valkyrie study. J Am Soc Nephrol. 2020; 31:186–196. PMID: 31704740.
Article
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