Abstract
The prevalence of cardiovascular morbidity and mortality is higher in patients with chronic kidney disease (CKD)—especially those with end-stage renal disease—than in the general population. The contribution of atherosclerosis to cardiovascular disease in patients with CKD remains unclear. Researchers in the 1970s proposed that atherosclerosis was the main cause of cardiovascular disease in patients with CKD and that its progression, based on observations of patients on long-term dialysis, was accelerated by the uremic state. Subsequent reports, however, favor the involvement of other mechanisms, such as arteriosclerosis (characterized by vascular stiffening), vascular calcification, 'myocyte/capillary mismatch', congestive cardiomyopathy, and sudden cardiac death. Imaging and morphological studies have contributed to our understanding of the pathogenesis and progression of cardiovascular disease associated with CKD. Based on clinical and experimental findings, we hypothesize the following: the initial cardiovascular abnormalities in the CKD setting include arteriosclerosis, left ventricular diastolic dysfunction, and left ventricular hypertrophy, abnormalities which, in adult patients, are often accompanied by atherosclerosis. The prevalence of atherosclerosis increases with age and is aggravated, but not specifically induced, by CKD. The cardiovascular events associated with atherosclerosis are more often fatal in patients with CKD than in individuals without CKD.
Key Points
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The first cardiovascular changes observed in patients with chronic kidney disease (CKD) are arteriosclerosis (characterized by arterial stiffening and loss of cushioning function), altered left ventricular diastolic function and left ventricular hypertrophy
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Atherosclerosis (characterized by intimal thickening and loss of conduit function) often occurs in parallel with initial cardiovascular changes (especially in elderly patients with CKD) and is probably not induced, but is aggravated by CKD
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The severity of atherosclerosis in patients with CKD could be affected by changes in plaque composition (that is, by qualitative differences) rather than by atheromatous plaque number or volume
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Intimal calcification is high in patients with CKD; although medial calcification is associated with arteriosclerosis, it is probably a secondary event in the late stages of CKD
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The role of uremia-specific factors in cardiovascular disease, as opposed to the classical risk factors (age, hypertension, diabetes, and smoking) requires further investigation
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Atherosclerosis clearly contributes to the high cardiovascular mortality rate of patients with CKD but is probably not one of the main causes of death
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References
Chronic Kidney Disease Prognosis Consortium. Association of estimated glomerular filtration rate and albuminuria with all-cause and cardiovascular mortality in general population cohorts: a collaborative meta-analysis. Lancet 375, 2073–2081 (2010).
Foley, R. N., Parfrey, P. S. & Sarnak, M. J. Clinical epidemiology of cardiovascular disease in chronic renal disease. Am. J. Kidney Dis. 32, S112–S119 (1998).
Go, A. S., Chertow, G. M., Fan, D., McCulloch, C. E. & Hsu, C. Y. Chronic kidney disease and the risks of death, cardiovascular events, and hospitalization. N. Engl. J. Med. 351, 1296–1305 (2004).
Shlipak, M. G., Fried, L. F., Stehman-Breen, C., Siscovick, D. & Newman, A. B. Chronic renal insufficiency and cardiovascular events in the elderly: findings from the Cardiovascular Health Study. Am. J. Geriatr. Cardiol. 13, 81–90 (2004).
Vanholder, R. et al. Chronic kidney disease as cause of cardiovascular morbidity and mortality. Nephrol. Dial. Transplant. 20, 1048–1056 (2005).
Muntner, P., He, J., Astor, B. C., Folsom, A. R. & Coresh, J. Traditional and nontraditional risk factors predict coronary heart disease in chronic kidney disease: results from the atherosclerosis risk in communities study. J. Am. Soc. Nephrol. 16, 529–538 (2005).
Weiner, D. E. et al. Cardiovascular outcomes and all-cause mortality: exploring the interaction between CKD and cardiovascular disease. Am. J. Kidney Dis. 48, 392–401 (2006).
London, G. M. & Drüeke, T. B. Atherosclerosis and arteriosclerosis in chronic renal failure. Kidney Int. 51, 1678–1695 (1997).
Fishbein, G. A. & Fishbein, M. C. Arteriosclerosis: rethinking the current classification. Arch. Pathol. Lab. Med. 133, 1309–1316 (2009).
Guérin, A. P., Pannier, B., Métivier, F., Marchais, S. J. & London, G. M. Assessment and significance of arterial stiffness in patients with chronic kidney disease. Curr. Opin. Nephrol. Hypertens. 17, 635–641 (2008).
García-Cardeña, G. & Gimbrone, M. A. Jr. Biomechanical modulation of endothelial phenotype: implications for health and disease. Handb. Exp. Pharmacol. 176, 79–95 (2006).
Chung, A. W. et al. Upregulation of matrix metalloproteinase-2 in the arterial vasculature contributes to stiffening and vasomotor dysfunction in patients with chronic kidney disease. Circulation 120, 792–801 (2009).
Van Herck, J. L. et al. Impaired fibrillin-1 function promotes features of plaque instability in apolipoprotein E-deficient mice. Circulation 120, 2478–2487 (2009).
Guérin, A. P., London, G. M., Marchais, S. J. & Metivier, F. Arterial stiffening and vascular calcifications in end-stage renal disease. Nephrol. Dial. Transplant. 15, 1014–1021 (2000).
McEniery, C. M. et al. Aortic calcification is associated with aortic stiffness and isolated systolic hypertension in healthy individuals. Hypertension 53, 524–531 (2009).
Toussaint, N. D., Lau, K. K., Strauss, B. J., Polkinghorne, K. R. & Kerr, P. G. Relationship between vascular calcification, arterial stiffness and bone mineral density in a cross-sectional study of prevalent Australian haemodialysis patients. Nephrology (Carlton) 14, 105–112 (2009).
Lindner, A., Charra, B., Sherrard, D. J. & Scribner, B. H. Accelerated atherosclerosis in prolonged maintenance hemodialysis. N. Engl. J. Med. 290, 697–701 (1974).
Burke, J. F. Jr, Francos, G. C., Moore, L. L., Cho, S. Y. & Lasker, N. Accelerated atherosclerosis in chronic-dialysis patients—another look. Nephron 21, 181–185 (1978).
Degoulet, P. et al. Mortality risk factors in patients treated by chronic hemodialysis. Report of the Diaphane collaborative study. Nephron 31, 103–110 (1982).
Coll, B. et al. Cardiovascular risk factors underestimate atherosclerotic burden in chronic kidney disease: usefulness of non-invasive tests in cardiovascular assessment. Nephrol. Dial. Transplant. 25, 3017–3025 (2010).
Menon, V. & Sarnak, M. J. The epidemiology of chronic kidney disease stages 1 to 4 and cardiovascular disease: a high-risk combination. Am. J. Kidney Dis. 45, 223–232 (2005).
Meier, P., Golshayan, D., Blanc, E., Pascual, M. & Burnier, M. Oxidized LDL modulates apoptosis of regulatory T cells in patients with ESRD. J. Am. Soc. Nephrol. 20, 1368–1384 (2009).
Ok, E., Basnakian, A. G., Apostolov, E. O., Barri, Y. M. & Shah, S. V. Carbamylated low-density lipoprotein induces death of endothelial cells: a link to atherosclerosis in patients with kidney disease. Kidney Int. 68, 173–178 (2005).
Wang, Z. et al. Protein carbamylation links inflammation, smoking, uremia and atherogenesis. Nat. Med. 13, 1176–1184 (2007).
Amabile, N. et al. Circulating endothelial microparticles are associated with vascular dysfunction in patients with end-stage renal failure. J. Am. Soc. Nephrol. 16, 3381–3388 (2005).
Dursun, I. et al. The relationship between circulating endothelial microparticles and arterial stiffness and atherosclerosis in children with chronic kidney disease. Nephrol. Dial. Transplant. 24, 2511–2518 (2009).
Faure, V. et al. Elevation of circulating endothelial microparticles in patients with chronic renal failure. J. Thromb. Haemost. 4, 566–573 (2006).
Basta, G. et al. Circulating soluble receptor of advanced glycation end product inversely correlates with atherosclerosis in patients with chronic kidney disease. Kidney Int. 77, 225–231 (2010).
Abramson, J. L., Jurkovitz, C. T., Vaccarino, V., Weintraub, W. S. & McClellan, W. Chronic kidney disease, anemia, and incident stroke in a middle-aged, community-based population: the ARIC Study. Kidney Int. 64, 610–615 (2003).
Shlipak, M. G. et al. Cardiovascular mortality risk in chronic kidney disease: comparison of traditional and novel risk factors. JAMA 293, 1737–1745 (2005).
Liu, Y. et al. Association between cholesterol level and mortality in dialysis patients: role of inflammation and malnutrition. JAMA 291, 451–459 (2004).
Kalantar-Zadeh, K. What is so bad about reverse epidemiology anyway? Semin. Dial. 20, 593–601 (2007).
Shoji, T. et al. Additive impacts of diabetes and renal failure on carotid atherosclerosis. Atherosclerosis 153, 257–258 (2000).
Wanner, C. et al. Atorvastatin in patients with type 2 diabetes mellitus undergoing hemodialysis. N. Engl. J. Med. 353, 238–248 (2005).
Fellström, B. C. et al. Rosuvastatin and cardiovascular events in patients undergoing hemodialysis. N. Engl. J. Med. 360, 1395–1407 (2009).
Navaneethan, S. D. et al. HMG CoA reductase inhibitors (statins) for people with chronic kidney disease not requiring dialysis. Cochrane Database of Systematic Reviews, Issue 2. Art. No.: CD007784. doi: 10.1002/14651858.CD007784 (2009).
Baigent, C. & Landry, M. Study of Heart and Renal Protection (SHARP). Kidney Int. Suppl. 84, S207–S210 (2003).
Lowrie, E. G., Lazarus, J. M., Hampers, C. L. & Merrill, J. P. Cardiovascular disease in dialysis patients. N. Engl. J. Med. 290, 737–738 (1974).
Lazarus, J. M., Lowrie, E. G., Hampers, C. L. & Merrill, J. P. Cardiovascular disease in uremic patients on hemodialysis. Kidney Int. Suppl. 167–175 (1975).
Wing, A. J. et al. Combined report on regular dialysis and transplantation in Europe, VIII, 1977. Proc. Eur. Dial. Transplant. Assoc. 15, 2–76 (1978).
Weinrauch, L. A. et al. Asymptomatic coronary artery disease: angiography in diabetic patients before renal transplantation. Relation of findings to postoperative survival. Ann. Intern. Med. 88, 346–348 (1978).
Raine, A. E. et al. Report on management of renal failure in Europe, XXII. Nephrol. Dial. Transplant. 7 (Suppl. 2), 7–35 (1991).
Rostand, S. G., Gretes, J. C., Kirk, K. A., Rutsky, E. A. & Andreoli, T. E. Ischemic heart disease in patients with uremia undergoing maintenance hemodialysis. Kidney Int. 16, 600–611 (1979).
Parfrey, P. S. et al. Outcome and risk factors of ischemic heart disease in chronic uremia. Kidney Int. 49, 1428–1434 (1996).
Rostand, S. G., Kirk, K. A. & Rutsky, E. A. Dialysis-associated ischemic heart disease: insights from coronary angiography. Kidney Int. 25, 653–659 (1984).
Nicholls, A. J., Catto, G. R., Edward, N., Engeset, J. & Macleod, M. Accelerated atherosclerosis in long-term dialysis and renal-transplant patients: fact or fiction? Lancet 1, 276–278 (1980).
Ritz, E., Strumpf, C., Katz, F., Wing, A. J. & Quellhorst, E. Hypertension and cardiovascular risk factors in hemodialyzed diabetic patients. Hypertension 7, II118–II124 (1985).
Drüeke, T. et al. Congestive cardiomyopathy in uraemic patients on long term haemodialysis. Br. Med. J. 1, 350–353 (1977).
Silberberg, J. S., Barre, P. E., Prichard, S. S. & Sniderman, A. D. Impact of left ventricular hypertrophy on survival in end-stage renal disease. Kidney Int. 36, 286–290 (1989).
Foley, R. N. et al. Clinical and echocardiographic disease in patients starting end-stage renal disease therapy. Kidney Int. 47, 186–192 (1995).
Harnett, J. D. et al. Congestive heart failure in dialysis patients: prevalence, incidence, prognosis and risk factors. Kidney Int. 47, 884–890 (1995).
Parfrey, P. S. Cardiac disease in dialysis patients: diagnosis, burden of disease, prognosis, risk factors and management. Nephrol. Dial. Transplant. 15 (Suppl. 5), 58–68 (2000).
Collins, A. J. et al. Excerpts from the United States Renal Data System 2007 annual data report. Am. J. Kidney Dis. 51 (Suppl. 1), S1–S320 (2008).
Baigent, C., Burbury, K. & Wheeler, D. Premature cardiovascular disease in chronic renal failure. Lancet 356, 147–152 (2000).
Iseki, K. & Fukiyama, K. Long-term prognosis and incidence of acute myocardial infarction in patients on chronic hemodialysis. The Okinawa Dialysis Study Group. Am. J. Kidney Dis. 36, 820–825 (2000).
Iseki, K., Fukiyama, K. & The Okinawa Dialysis Study Group. Clinical demographics and long-term prognosis after stroke in patients on chronic haemodialysis. The Okinawa Dialysis Study (OKIDS) Group. Nephrol. Dial. Transplant. 15, 1808–1813 (2000).
Wright, R. S. et al. Acute myocardial infarction and renal dysfunction: a high-risk combination. Ann. Intern. Med. 137, 563–570 (2002).
Al Suwaidi, J. et al. Prognostic implications of abnormalities in renal function in patients with acute coronary syndromes. Circulation 106, 974–980 (2002).
Anavekar, N. S. et al. Relation between renal dysfunction and cardiovascular outcomes after myocardial infarction. N. Engl. J. Med. 351, 1285–1295 (2004).
Meisinger, C., Doring, A. & Lowel, H. Chronic kidney disease and risk of incident myocardial infarction and all-cause and cardiovascular disease mortality in middle-aged men and women from the general population. Eur. Heart J. 27, 1245–1250 (2006).
Levin, A. et al. Cardiovascular disease in patients with chronic kidney disease: getting to the heart of the matter. Am. J. Kidney Dis. 38, 1398–1407 (2001).
Mathew, A. et al. Carotid endarterectomy benefits patients with CKD and symptomatic high-grade stenosis. J. Am. Soc. Nephrol. 21, 145–152 (2010).
Shoji, T., Tsubakihara, Y., Nakai, S. & Nishizawa, Y. Reverse epidemiology in hemodialysis patients. Lessons from Japanese registries. Nephrol. Ther. 4, 223–227 (2008).
Chmielewski, M., Carrero, J. J., Stenvinkel, P. & Lindholm, B. Metabolic abnormalities in chronic kidney disease that contribute to cardiovascular disease, and nutritional initiatives that may diminish the risk. Curr. Opin. Lipidol. 20, 3–9 (2009).
Covic, A. et al. Systematic review of the evidence underlying the association between mineral metabolism disturbances and risk of all-cause mortality, cardiovascular mortality and cardiovascular events in chronic kidney disease. Nephrol. Dial. Transplant. 24, 1506–1523 (2009).
Barreto, F. C., Barreto, D. V., Liabeuf, S., Drüeke, T. B. & Massy, Z. A. Effects of uremic toxins on vascular and bone remodeling. Semin. Dial. 22, 433–437 (2009).
Jourde-Chiche, N. et al. Levels of circulating endothelial progenitor cells are related to uremic toxins and vascular injury in hemodialysis patients. J. Thromb. Haemost. 7, 1576–1584 (2009).
Drechsler, C., Krane, V., Ritz, E., März, W. & Wanner, C. Glycemic control and cardiovascular events in diabetic hemodialysis patients. Circulation 120, 2421–2428 (2009).
Leskinen, Y. et al. Carotid atherosclerosis in chronic renal failure-the central role of increased plaque burden. Atherosclerosis 171, 295–302 (2003).
Cho, I. et al. Coronary atherosclerosis detected by coronary CT angiography in asymptomatic subjects with early chronic kidney disease. Atherosclerosis 208, 406–411 (2010).
Chonchol, M. et al. Chronic kidney disease is associated with angiographic coronary artery disease. Am. J. Nephrol. 28, 354–360 (2008).
Ohtake, T. et al. High prevalence of occult coronary artery stenosis in patients with chronic kidney disease at the initiation of renal replacement therapy: an angiographic examination. J. Am. Soc. Nephrol. 16, 1141–1148 (2005).
Krasniak, A. et al. Factors involved in vascular calcification and atherosclerosis in maintenance haemodialysis patients. Nephrol. Dial. Transplant. 22, 515–521 (2007).
Leonardi, G. et al. Assessment of cardiovascular risk in waiting-listed renal transplant patients: a single center experience in 558 cases. Clin. Transplant. 23, 653–659 (2009).
Atkinson, P. et al. Predictive value of myocardial and coronary imaging in the long-term outcome of potential renal transplant recipients. Int. J. Cardiol. doi: 10.1016/j.ijcard.2009.06.050.
Joki, N. et al. Optimum second screening point for detection of coronary artery disease in hemodialysis patients without advanced coronary artery disease. Am. J. Nephrol. 29, 420–425 (2009).
Wu, I. W. et al. Ventricular function and all-cause mortality in chronic kidney disease patients with angiographic coronary artery disease. J. Nephrol. 23, 181–188 (2010).
Hage, F. G. et al. The scope of coronary heart disease in patients with chronic kidney disease. J. Am. Coll. Cardiol. 53, 2129–2140 (2009).
Hage, F. G. et al. Predictors of survival in patients with end-stage renal disease evaluated for kidney transplantation. Am. J. Cardiol. 100, 1020–1025 (2007).
Venkataraman, R. et al. Role of myocardial perfusion imaging in patients with end-stage renal disease undergoing coronary angiography. Am. J. Cardiol. 102, 1451–1456 (2008).
Patel, A. D. et al. Prognostic value of myocardial perfusion imaging in predicting outcome after renal transplantation. Am. J. Cardiol. 92, 146–151 (2003).
Yilmaz, M. I. et al. Predictors of carotid artery intima-media thickness in chronic kidney disease and kidney transplant patients without overt cardiovascular disease. Am. J. Nephrol. 31, 214–221 (2010).
Alexopoulos, N. & Raggi, P. Calcification in atherosclerosis. Nat. Rev. Cardiol. 6, 681–688 (2009).
McCullough, P. A., Agarwal, M. & Agrawal, V. Risks of coronary artery calcification in chronic kidney disease: do the same rules apply? Nephrology (Carlton) 14, 428–436 (2009).
Hemmelgarn, B. R. et al. Relation between kidney function, proteinuria, and adverse outcomes. JAMA 303, 423–429 (2010).
Pun, P. H. et al. Chronic kidney disease is associated with increased risk of sudden cardiac death among patients with coronary artery disease. Kidney Int. 76, 652–658 (2009).
Charytan, D. M., Setoguchi, S., Solomon, D. H., Avorn, J. & Winkelmayer, W. C. Clinical presentation of myocardial infarction contributes to lower use of coronary angiography in patients with chronic kidney disease. Kidney Int. 71, 938–945 (2007).
Temmar, M. et al. Pulse wave velocity and vascular calcification at different stages of chronic kidney disease. J. Hypertens. 28, 163–169 (2010).
Sengstock, D. et al. Dominance of traditional cardiovascular risk factors over renal function in predicting arterial stiffness in subjects with chronic kidney disease. Nephrol. Dial. Transplant. 25, 853–861 (2010).
McCullough, P. A., Agrawal, V., Danielewicz, E. & Abela, G. S. Accelerated atherosclerotic calcification and Monckeberg's sclerosis: a continuum of advanced vascular pathology in chronic kidney disease. Clin. J. Am. Soc. Nephrol. 3, 1585–1598 (2008).
Curry, R. C. Jr & Roberts, W. C. Status of the coronary arteries in the nephrotic syndrome. Analysis of 20 necropsy patients aged 15 to 35 years to determine if coronary atherosclerosis is accelerated. Am. J. Med. 63, 183–192 (1977).
Ibels, L. S. et al. Arterial calcification and pathology in uremic patients undergoing dialysis. Am. J. Med. 66, 790–796 (1979).
Moe, S. M. et al. Medial artery calcification in ESRD patients is associated with deposition of bone matrix proteins. Kidney Int. 61, 638–647 (2002).
Schwarz, U. et al. Morphology of coronary atherosclerotic lesions in patients with end-stage renal failure. Nephrol. Dial. Transplant. 15, 218–223 (2000).
Stary, H. C. et al. A definition of advanced types of atherosclerotic lesions and a histological classification of atherosclerosis. A report from the Committee on Vascular Lesions of the Council on Arteriosclerosis, American Heart Association. Circulation 92, 1355–1374 (1995).
Gross, M. L. 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. 2, 121–134 (2007).
Nakamura, S. et al. Coronary calcification in patients with chronic kidney disease and coronary artery disease. Clin. J. Am. Soc. Nephrol. 4, 1892–1900 (2009).
Nakano, T. et al. Association of kidney function with coronary atherosclerosis and calcification in autopsy samples from Japanese elders: the Hisayama study. Am. J. Kidney Dis. 55, 21–30 (2010).
Ansari, A., Kaupke, C. J., Vaziri, N. D., Miller, R. & Barbari, A. Cardiac pathology in patients with end-stage renal disease maintained on hemodialysis. Int. J. Artif. Organs 16, 31–36 (1993).
Clyne, N., Lins, L. E. & Pehrsson, S. K. Occurrence and significance of heart disease in uraemia. An autopsy study. Scand. J. Urol. Nephrol. 20, 307–311 (1986).
Amann, K., Breitbach, M., Ritz, E. & Mall, G. Myocyte/capillary mismatch in the heart of uremic patients. J. Am. Soc. Nephrol. 9, 1018–1022 (1998).
Massy, Z. A. et al. Uremia accelerates both atherosclerosis and arterial calcification in apolipoprotein E knockout mice. J. Am. Soc. Nephrol. 16, 109–116 (2005).
Buzello, M. et al. The apolipoprotein E knockout mouse: a model documenting accelerated atherogenesis in uremia. J. Am. Soc. Nephrol. 14, 311–316 (2003).
Bro, S. et al. Chronic renal failure accelerates atherogenesis in apolipoprotein E-deficient mice. J. Am. Soc. Nephrol. 14, 2466–2474 (2003).
Westenfeld, R. et al. Fetuin-A protects against atherosclerotic calcification in CKD. J. Am. Soc. Nephrol. 20, 1264–1274 (2009).
Phan, O. et al. Sevelamer prevents uremia-enhanced atherosclerosis progression in apolipoprotein E-deficient mice. Circulation 112, 2875–2882 (2005).
Ivanovski, O. et al. The calcimimetic R-568 retards uremia-enhanced vascular calcification and atherosclerosis in apolipoprotein E deficient (ApoE−/−) mice. Atherosclerosis 205, 55–62 (2009).
Mathew, S. et al. Reversal of the adynamic bone disorder and decreased vascular calcification in chronic kidney disease by sevelamer carbonate therapy. J. Am. Soc. Nephrol. 18, 122–130 (2007).
Davies, M. R., Lund, R. J., Mathew, S. & Hruska, K. A. Low turnover osteodystrophy and vascular calcification are amenable to skeletal anabolism in an animal model of chronic kidney disease and the metabolic syndrome. J. Am. Soc. Nephrol. 16, 917–928 (2005).
Maizel, J. et al. Mechanisms of aortic and cardiac dysfunction in uremic mice with aortic calcification. Circulation 119, 306–313 (2009).
Otsuka, T., Suzuki, M., Yoshikawa, H. & Sugi, K. Left ventricular diastolic dysfunction in the early stage of chronic kidney disease. J. Cardiol. 54, 199–204 (2009).
Civilibal, M. et al. Left ventricular function by 'conventional' and 'tissue Doppler' echocardiography in paediatric dialysis patients. Nephrology (Carlton) 14, 636–642 (2009).
Shurraw, S. & Tonelli, M. AURORA: is there a role for statin therapy in dialysis patients? Am. J. Kidney Dis. 55, 237–240 (2010).
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The authors wish to thank S. Rostand, from the University of Alabama at Birmingham, AL, USA, for helpful discussion and suggestions for this manuscript.
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T. B. Drüeke and Z. A. Massy contributed equally to researching data for the article, substantial discussion of the content of the article and reviewing/editing the manuscript before submission. T. B. Drüeke wrote the initial draft of the article.
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Drüeke, T., Massy, Z. Atherosclerosis in CKD: differences from the general population. Nat Rev Nephrol 6, 723–735 (2010). https://doi.org/10.1038/nrneph.2010.143
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