Vascular calcification in chronic kidney disease: different bricks in the wall?

Kidney International

Volumn 91, Issue 4, 2017, Pages 808-817

  Vervloet, Marc ^a   Cozzolino, Mario ^b  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UNIVERSITY OF MILAN   (Italy)

Author keywords

arteriosclerosis; cardiovascular disease; chronic kidney disease; coronary calcification; mineral metabolism; vascular calcification

Indexed keywords

HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; PHOSPHATE BINDING AGENT; BIOLOGICAL MARKER;

ARTERY CALCIFICATION; BLOOD VESSEL CALCIFICATION; CARDIOVASCULAR RISK; CAUSALITY; CHRONIC KIDNEY FAILURE; DISEASE ASSOCIATION; HUMAN; INCIDENCE; NONHUMAN; PATHOGENESIS; PATHOPHYSIOLOGY; PREVALENCE; REVIEW; TUNICA INTIMA CALCIFICATION; ANIMAL; ARTERY; BLOOD; COMORBIDITY; METABOLISM; PATHOLOGY; PROGNOSIS; RENAL INSUFFICIENCY, CHRONIC; RISK ASSESSMENT; RISK FACTOR; SIGNAL TRANSDUCTION; VASCULAR CALCIFICATION;

ANIMALS; ARTERIES; BIOMARKERS; COMORBIDITY; HUMANS; INCIDENCE; PREVALENCE; PROGNOSIS; RENAL INSUFFICIENCY, CHRONIC; RISK ASSESSMENT; RISK FACTORS; SIGNAL TRANSDUCTION; VASCULAR CALCIFICATION;

EID: 85007418095     PISSN: 00852538     EISSN: 15231755     Source Type: Journal    
DOI: 10.1016/j.kint.2016.09.024     Document Type: Review

References (96)

1. 1 Detrano, R., Guerci, A.D., Carr, J.J., et al. Coronary calcium as a predictor of coronary events in four racial or ethnic groups. N Engl J Med 358 (2008), 1336–1345.
2. 2 London, G.M., Guerin, A.P., Marchais, S.J., et al. Arterial media calcification in end-stage renal disease: impact on all-cause and cardiovascular mortality. Nephrol Dial Transplant 18 (2003), 1731–1740.
3. 3 Peeters MJ, van den Brand JA, van Zuilen AD, et al. Abdominal aortic calcification in patients with CKD [e-pub ahead of print]. J Nephrol. doi:10.1007/s40620-015-0260-7.
4. 4 Block, G.A., Raggi, P., Bellasi, A., et al. Mortality effect of coronary calcification and phosphate binder choice in incident hemodialysis patients. Kidney Int 71 (2007), 438–441.
5. 5 Bover, J., Evenepoel, P., Urena-Torres, P., et al. Pro: cardiovascular calcifications are clinically relevant. Nephrol Dial Transplant 30 (2015), 345–351.
6. 6 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 30 (2015), 352–357.
7. 7 Koleganova, N., Piecha, G., Ritz, E., et al. Arterial calcification in patients with chronic kidney disease. Nephrol Dial Transplant 24 (2009), 2488–2496.
8. 8 Usman, A., Ribatti, D., Sadat, U., Gillard, J.H., From lipid retention to immune-mediate inflammation and associated angiogenesis in the pathogenesis of atherosclerosis. J Atheroscler Thromb 22 (2015), 739–749.
9. 9 Amann, K., Media calcification and intima calcification are distinct entities in chronic kidney disease. Clin J Am Soc Nephrol 3 (2008), 1599–1605.
10. 10 Drueke, T.B., Arterial intima and media calcification: distinct entities with different pathogenesis or all the same?. Clin J Am Soc Nephrol 3 (2008), 1583–1584.
11. 11 Paloian, N.J., Giachelli, C.M., A current understanding of vascular calcification in CKD. Am J Physiol Renal Physiol 307 (2014), F891–F900.
12. 12 Lanzer, P., Boehm, M., Sorribas, V., et al. Medial vascular calcification revisited: review and perspectives. Eur Heart J 35 (2014), 1515–1525.
13. 13 Abdelbaky, A., Corsini, E., Figueroa, A.L., et al. Focal arterial inflammation precedes subsequent calcification in the same location: a longitudinal FDG-PET/CT study. Circ Cardiovasc Imaging 6 (2013), 747–754.
14. 14 Ewence, A.E., Bootman, M., Roderick, H.L., et al. Calcium phosphate crystals induce cell death in human vascular smooth muscle cells: a potential mechanism in atherosclerotic plaque destabilization. Circ Res 103 (2008), e28–e34.
15. 15 Toutouzas, K., Benetos, G., Karanasos, A., et al. Vulnerable plaque imaging: updates on new pathobiological mechanisms. Eur Heart J 36 (2015), 3147–3154.
16. 16 Kataoka, Y., Puri, R., Hammadah, M., et al. Spotty calcification and plaque vulnerability in vivo: frequency-domain optical coherence tomography analysis. Cardiovasc Diagn Ther 4 (2014), 460–469.
17. 17 Bellasi, A., Ferramosca, E., Ratti, C., et al. The density of calcified plaques and the volume of calcium predict mortality in hemodialysis patients. Atherosclerosis 250 (2016), 166–171.
18. 18 Agatston, A.S., Janowitz, W.R., Hildner, F.J., et al. Quantification of coronary artery calcium using ultrafast computed tomography. J Am Coll Cardiol 15 (1990), 827–832.
19. 19 Kauppila, L.I., Polak, J.F., Cupples, L.A., et al. New indices to classify location, severity and progression of calcific lesions in the abdominal aorta: a 25-year follow-up study. Atherosclerosis 132 (1997), 245–250.
20. 20 Adragao, T., Pires, A., Lucas, C., et al. A simple vascular calcification score predicts cardiovascular risk in haemodialysis patients. Nephrol Dial Transplant 19 (2004), 1480–1488.
21. 21 Bolland, M.J., Wang, T.K., van Pelt, N.C., et al. Abdominal aortic calcification on vertebral morphometry images predicts incident myocardial infarction. J Bone Miner Res 25 (2010), 505–512.
22. 22 Watanabe, R., Lemos, M.M., Manfredi, S.R., et al. Impact of cardiovascular calcification in nondialyzed patients after 24 months of follow-up. Clin J Am Soc Nephrol 5 (2010), 189–194.
23. 23 Barraclough, K.A., Stevens, L.A., Er, L., et al. Coronary artery calcification scores in patients with chronic kidney disease prior to dialysis: reliability as a trial outcome measure. Nephrol Dial Transplant 23 (2008), 3199–3205.
24. 24 Beckman, J.A., Ganz, J., Creager, M.A., et al. Relationship of clinical presentation and calcification of culprit coronary artery stenoses. Arterioscler Thromb Vasc Biol 21 (2001), 1618–1622.
25. 25 Puri, R., Nicholls, S.J., Shao, M., et al. Impact of statins on serial coronary calcification during atheroma progression and regression. J Am Coll Cardiol 65 (2015), 1273–1282.
26. 26 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 4 (2009), 1892–1900.
27. 27 Wallin, R., Wajih, N., Greenwood, G.T., Sane, D.C., Arterial calcification: a review of mechanisms, animal models, and the prospects for therapy. Med Res Rev 21 (2001), 274–301.
28. 28 Adeseun, G.A., Xie, D., Wang, X., et al. Carotid plaque, carotid intima-media thickness, and coronary calcification equally discriminate prevalent cardiovascular disease in kidney disease. Am J Nephrol 36 (2012), 342–347.
29. 29 Kalsch, H., Lehmann, N., Mahabadi, A.A., et al. Beyond Framingham risk factors and coronary calcification: does aortic valve calcification improve risk prediction? The Heinz Nixdorf Recall Study. Heart 100 (2014), 930–937.
30. 30 Hoffmann, U., Massaro, J.M., D'Agostino, R.B. Sr., Kathiresan, S., Fox, C.S., O'Donnell, C.J., Cardiovascular event prediction and risk reclassification by coronary, aortic, and valvular calcification in the Framingham Heart Study. J Am Heart Assoc, 5, 2016 pii:e003144.
31. 31 London, G., Covic, A., Goldsmith, D., et al. Arterial aging and arterial disease: interplay between central hemodynamics, cardiac work, and organ flow-implications for CKD and cardiovascular disease. Kidney Int Suppl 1 (2011), 10–12.
32. 32 Cozzolino, M., Brancaccio, D., Gallieni, M., Slatopolsky, E., Pathogenesis of vascular calcification in chronic kidney disease. Kidney Int 68 (2005), 429–436.
33. 33 Cozzolino, M., Mazzaferro, S., Pugliese, F., Brancaccio, D., Vascular calcification and uremia: what do we know?. Am J Nephrol 28 (2008), 339–346.
34. 34 Shroff, R.C., McNair, R., Figg, N., et al. Dialysis accelerates medial vascular calcification in part by triggering smooth muscle cell apoptosis. Circulation 118 (2008), 1748–1757.
35. 35 Foley, R.N., Parfrey, P.S., Sarnak, M.J., Clinical epidemiology of cardiovascular disease in chronic renal disease. Am J Kidney Dis 32 (1998), S112–S119.
36. 36 Russo, D., Palmiero, G., De Blasio, A.P., et al. Coronary artery calcification in patients with CRF not undergoing dialysis. Am J Kidney Dis 44 (2004), 1024–1030.
37. 37 Sigrist, M.K., Taal, M.W., Bungay, P., McIntyre, C.W., Progressive vascular calcification over 2 years is associated with arterial stiffening and increased mortality in patients with stages 4 and 5 chronic kidney disease. Clin J Am Soc Nephrol 2 (2007), 1241–1248.
38. 38 Wilson, A.C., Mitsnefes, M.M., Cardiovascular disease in CKD in children: update on risk factors, risk assessment, and management. Am J Kidney Dis 54 (2009), 345–360.
39. 39 Pai, A., Leaf, E.M., El-Abbadi, M., Giachelli, C.M., Elastin degradation and vascular smooth muscle cell phenotype change precede cell loss and arterial medial calcification in a uremic mouse model of chronic kidney disease. Am J Pathol 178 (2011), 764–773.
40. 40 Shanahan, C.M., Crouthamel, M.H., Kapustin, A., Giachelli, C.M., Arterial calcification in chronic kidney disease: key roles for calcium and phosphate. Circ Res 109 (2011), 697–711.
41. 41 Ciceri, P., Volpi, E., Brenna, I., et al. Combined effects of ascorbic acid and phosphate on rat VSMC osteoblastic differentiation. Nephrol Dial Transplant 27 (2012), 122–127.
42. 42 Hu, M.C., Shi, M., Zhang, J., et al. Klotho deficiency causes vascular calcification in chronic kidney disease. J Am Soc Nephrol 22 (2011), 124–136.
43. 43 Giachelli, C.M., Vascular calcification: in vitro evidence for the role of inorganic phosphate. J Am Soc Nephrol 14 (2003), S300–S304.
44. 44 Yang, H., Curinga, G., Giachelli, C.M., Elevated extracellular calcium levels induce smooth muscle cell matrix mineralization in vitro. Kidney Int 66 (2004), 2293–2299.
45. 45 Moe, S.M., Reslerova, M., Ketteler, M., et al. Role of calcification inhibitors in the pathogenesis of vascular calcification in chronic kidney disease (CKD). Kidney Int 67 (2005), 2295–2304.
46. 46 Jono, S., McKee, M.D., Murry, C.E., et al. Phosphate regulation of vascular smooth muscle cell calcification. Circ Res 87 (2000), E10–E17.
47. 47 Takx RA, MacNabb MH, Emami H, et al. Increased arterial inflammation in individuals with stage 3 chronic kidney disease [e-pub ahead of print]. Eur J Nucl Med Mol Imaging. doi:10.1007/s00259-015-3203-6.
48. 48 Joshi, F.R., Rajani, N.K., Abt, M., et al. Does Vascular Calcification Accelerate Inflammation?: A Substudy of the dal-PLAQUE Trial. J Am Coll Cardiol 67 (2016), 69–78.
49. 49 Terkeltaub, R.A., Santoro, D.A., Mandel, G., Mandel, N., Serum and plasma inhibit neutrophil stimulation by hydroxyapatite crystals. Evidence that serum alpha 2-HS glycoprotein is a potent and specific crystal-bound inhibitor. Arthritis Rheum 31 (1988), 1081–1089.
50. 50 Reynolds, J.L., Skepper, J.N., McNair, R., et al. Multifunctional roles for serum protein fetuin-a in inhibition of human vascular smooth muscle cell calcification. J Am Soc Nephrol 16 (2005), 2920–2930.
51. 51 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 361 (2003), 827–833.
52. 52 Cozzolino, M., Galassi, A., Biondi, M.L., et al. Serum fetuin-A levels link inflammation and cardiovascular calcification in hemodialysis patients. Am J Nephrol 26 (2006), 423–429.
53. 53 Shearer, M.J., Role of vitamin K and Gla proteins in the pathophysiology of osteoporosis and vascular calcification. Curr Opin Clin Nutr Metab Care 3 (2000), 433–438.
54. 54 Luo, G., Ducy, P., McKee, M.D., et al. Spontaneous calcification of arteries and cartilage in mice lacking matrix GLA protein. Nature 386 (1997), 78–81.
55. 55 Schurgers, L.J., Cranenburg, E.C., Vermeer, C., Matrix Gla-protein: the calcification inhibitor in need of vitamin K. Thromb Haemost 100 (2008), 593–603.
56. 56 Cranenburg, E.C., Vermeer, C., Koos, R., et al. The circulating inactive form of matrix Gla Protein (ucMGP) as a biomarker for cardiovascular calcification. J Vasc Res 45 (2008), 427–436.
57. 57 Cranenburg, E.C., Brandenburg, V.M., Vermeer, C., et al. Uncarboxylated matrix Gla protein (ucMGP) is associated with coronary artery calcification in haemodialysis patients. Thromb Haemost 101 (2009), 359–366.
58. 58 Shea, M.K., O'Donnell, C.J., Hoffmann, U., et al. Vitamin K supplementation and progression of coronary artery calcium in older men and women. Am J Clin Nutr 89 (2009), 1799–1807.
59. 59 Liabeuf, S., Okazaki, H., Desjardins, L., et al. Vascular calcification in chronic kidney disease: are biomarkers useful for probing the pathobiology and the health risks of this process in the clinical scenario?. Nephrol Dial Transplant 29 (2014), 1275–1284.
60. 60 Pasch, A., Farese, S., Graber, S., et al. Nanoparticle-based test measures overall propensity for calcification in serum. J Am Soc Nephrol 23 (2012), 1744–1752.
61. 61 Keyzer, C.A., de Borst, M.H., van den Berg, E., et al. Calcification Propensity and Survival among Renal Transplant Recipients. J Am Soc Nephrol 27 (2016), 239–248.
62. 62 Smith, E.R., Ford, M.L., Tomlinson, L.A., et al. Serum calcification propensity predicts all-cause mortality in predialysis CKD. J Am Soc Nephrol 25 (2014), 339–348.
63. 63 Thompson, R.C., Allam, A.H., Lombardi, G.P., et al. Atherosclerosis across 4000 years of human history: the Horus study of four ancient populations. Lancet 381 (2013), 1211–1222.
64. 64 Murphy, W.A. Jr., Nedden Dz, D., Gostner, P., Knapp, R., Recheis, W., Seidler, H., The iceman: discovery and imaging. Radiology 226 (2003), 614–629.
65. 65 Otsuka, F., Sakakura, K., Yahagi, K., et al. Has our understanding of calcification in human coronary atherosclerosis progressed?. Arterioscler Thromb Vasc Biol 34 (2014), 724–736.
66. 66 Ikeda, K., Souma, Y., Akakabe, Y., et al. Macrophages play a unique role in the plaque calcification by enhancing the osteogenic signals exerted by vascular smooth muscle cells. Biochem Biophys Res Commun 425 (2012), 39–44.
67. 67 Chatrou, M.L., Cleutjens, J.P., van der Vusse, G.J., Roijers, R.B., Mutsaers, P.H., Schurgers, L.J., Intra-section analysis of human coronary arteries reveals a potential role for micro-calcifications in macrophage recruitment in the early stage of atherosclerosis. PLoS One, 10, 2015, e0142335.
68. 68 Chen, Q., Bei, J.J., Liu, C., et al. HMGB1 induces secretion of matrix vesicles by macrophages to enhance ectopic mineralization. PLoS One, 11, 2016, e0156686.
69. 69 Brown, A.J., Teng, Z., Evans, P.C., Gillard, J.H., Samady, H., Bennett, M.R., Role of biomechanical forces in the natural history of coronary atherosclerosis. Nat Rev Cardiol 13 (2016), 210–220.
70. 70 Watabe, H., Sato, A., Akiyama, D., et al. Impact of coronary plaque composition on cardiac troponin elevation after percutaneous coronary intervention in stable angina pectoris: a computed tomography analysis. J Am Coll Cardiol 59 (2012), 1881–1888.
71. 71 Shmilovich, H., Cheng, V.Y., Tamarappoo, B.K., et al. Vulnerable plaque features on coronary CT angiography as markers of inducible regional myocardial hypoperfusion from severe coronary artery stenoses. Atherosclerosis 219 (2011), 588–595.
72. 72 Motoyama, S., Kondo, T., Sarai, M., et al. Multislice computed tomographic characteristics of coronary lesions in acute coronary syndromes. J Am Coll Cardiol 50 (2007), 319–326.
73. 73 Pundziute, G., Schuijf, J.D., Jukema, J.W., et al. Evaluation of plaque characteristics in acute coronary syndromes: non-invasive assessment with multi-slice computed tomography and invasive evaluation with intravascular ultrasound radiofrequency data analysis. Eur Heart J 29 (2008), 2373–2381.
74. 74 Shoji, T., Abe, T., Matsuo, H., et al. Chronic kidney disease, dyslipidemia, and atherosclerosis. J Atheroscler Thromb 19 (2012), 299–315.
75. 75 Adeney, K.L., Siscovick, D.S., Ix, J.H., et al. Association of serum phosphate with vascular and valvular calcification in moderate CKD. J Am Soc Nephrol 20 (2009), 381–387.
76. 76 Kestenbaum, B., Sampson, J.N., Rudser, K.D., et al. Serum phosphate levels and mortality risk among people with chronic kidney disease. J Am Soc Nephrol 16 (2005), 520–528.
77. 77 Dhingra, R., Sullivan, L.M., Fox, C.S., et al. Relations of serum phosphorus and calcium levels to the incidence of cardiovascular disease in the community. Arch Intern Med 167 (2007), 879–885.
78. 78 Cancela, A.L., Santos, R.D., Titan, S.M., et al. Phosphorus is associated with coronary artery disease in patients with preserved renal function. PLoS One, 7, 2012, e36883.
79. 79 Giachelli, C.M., Speer, M.Y., Li, X., et al. Regulation of vascular calcification: roles of phosphate and osteopontin. Circ Res 96 (2005), 717–722.
80. 80 Ciceri, P., Elli, F., Cappelletti, L., et al. A new in vitro model to delay high phosphate-induced vascular calcification progression. Mol Cell Biochem 410 (2015), 197–206.
81. 81 Mozar, A., Haren, N., Chasseraud, M., et al. High extracellular inorganic phosphate concentration inhibits RANK-RANKL signaling in osteoclast-like cells. J Cell Physiol 215 (2008), 47–54.
82. 82 Palmer SC, Gardner S, Tonelli M, et al. Phosphate-binding agents in adults with CKD: a network meta-analysis of randomized trials [e-pub ahead of print]. Am J Kidney Dis. doi:10.1053/j.ajkd.2016.05.015.
83. 83 Mizobuchi, M., Ogata, H., Koiwa, F., et al. Vitamin D and vascular calcification in chronic kidney disease. Bone 45 Suppl 1 (2009), S26–S29.
84. 84 Lim, K., Lu, T.S., Molostvov, G., et al. Vascular Klotho deficiency potentiates the development of human artery calcification and mediates resistance to fibroblast growth factor 23. Circulation 125 (2012), 2243–2255.
85. 85 Barreto, D.V., Barreto, F.C., Liabeuf, S., et al. Vitamin D affects survival independently of vascular calcification in chronic kidney disease. Clin J Am Soc Nephrol 4 (2009), 1128–1135.
86. 86 Cozzolino, M., Brandenburg, V., Paricalcitol and outcome: a manual on how a vitamin D receptor activator (VDRA) can help us to get down the “U”. Clin Nephrol 71 (2009), 593–601.
87. 87 Levin, A., Li, Y.C., Vitamin D and its analogues: do they protect against cardiovascular disease in patients with kidney disease?. Kidney Int 68 (2005), 1973–1981.
88. 88 Ciceri, P., Elli, F., Brenna, I., et al. The calcimimetic calindol prevents high phosphate-induced vascular calcification by upregulating matrix GLA protein. Nephron Exp Nephrol 122 (2012), 75–82.
89. 89 Raggi, P., Chertow, G.M., Torres, P.U., 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 26 (2011), 1327–1339.
90. 90 Leonard, O., Spaak, J., Goldsmith, D., Regression of vascular calcification in chronic kidney disease - feasible or fantasy? a review of the clinical evidence. Br J Clin Pharmacol 76 (2013), 560–572.
91. 91 Yazbek, D.C., Carvalho, A.B., Barros, C.S., et al. Effect of statins on the progression of coronary calcification in kidney transplant recipients. PLoS One, 11, 2016, e0151797.
92. 92 Henein, M., Granasen, G., Wiklund, U., et al. High dose and long-term statin therapy accelerate coronary artery calcification. Int J Cardiol 184 (2015), 581–586.
93. 93 Rodriguez-Granillo, G.A., Carrascosa, P., Bruining, N., Progression of coronary artery calcification at the crossroads: sign of progression or stabilization of coronary atherosclerosis?. Cardiovasc Diagn Ther 6 (2016), 250–258.
94. 94 Lei, Y., Grover, A., Sinha, A., Vyavahare, N., Efficacy of reversal of aortic calcification by chelating agents. Calcif Tissue Int 93 (2013), 426–435.
95. 95 Adirekkiat, S., Sumethkul, V., Ingsathit, A., et al. Sodium thiosulfate delays the progression of coronary artery calcification in haemodialysis patients. Nephrol Dial Transplant 25 (2010), 1923–1929.
96. 96 Mathews, S.J., de Las Fuentes, L., Podaralla, P., et al. Effects of sodium thiosulfate on vascular calcification in end-stage renal disease: a pilot study of feasibility, safety and efficacy. Am J Nephrol 33 (2011), 131–138.