The elephant in uremia: Oxidant stress as a unifying concept of cardiovascular disease in uremia

Himmelfarb, Jonathan; Stenvinkel, Peter; Ikizler, T. Alp; Hakim, Raymond M.

doi:10.1046/j.1523-1755.2002.00600.x

Cited by 1,179Dialysis and Renal Disease ManagementAntioxidant Activity and Oxidative StressNitric Oxide and Endothelin Effects

The elephant in uremia: Oxidant stress as a unifying concept of cardiovascular disease in uremia

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Himmelfarb, Jonathan, Stenvinkel, Peter, Ikizler, T. Alp, Hakim, Raymond M.·2002·Kidney International

DOI 10.1046/j.1523-1755.2002.00600.x

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Abstract

Cardiovascular disease is the leading cause of mortality in uremic patients. In large cross-sectional studies of dialysis patients, traditional cardiovascular risk factors such as hypertension and hypercholesterolemia have been found to have low predictive power, while markers of inflammation and malnutrition are highly correlated with cardiovascular mortality. However, the pathophysiology of the disease process that links uremia, inflammation, and malnutrition with increased cardiovascular complications is not well understood. We hereby propose the hypothesis that increased oxidative stress and its sequalae is a major contributor to increased atherosclerosis and cardiovascular morbidity and mortality found in uremia. This hypothesis is based on studies that conclusively demonstrate an increased oxidative burden in uremic patients, before and particularly after renal replacement therapies, as evidenced by higher concentrations of multiple biomarkers of oxidative stress. This hypothesis also provides a framework to explain the link that activated phagocytes provide between oxidative stress and inflammation (from infectious and non-infections causes) and the synergistic role that malnutrition (as reflected by low concentrations of albumin and/or antioxidants) contributes to the increased burden of cardiovascular disease in uremia. We further propose that retained uremic solutes such as beta-2 microglobulin, advanced glycosylated end products (AGE), cysteine, and homocysteine, which are substrates for oxidative injury, further contribute to the pro-atherogenic milieu of uremia. Dialytic therapy, which acts to reduce the concentration of oxidized substrates, improves the redox balance. However, processes related to dialytic therapy, such as the prolonged use of catheters for vascular access and the use of bioincompatible dialysis membranes, can contribute to a pro-inflammatory and pro-oxidative state and thus to a pro-atherogenic state. Anti-oxidative therapeutic strategies for patients with uremia are in their very early stages; nonetheless, early studies demonstrate the potential for significant efficacy in reducing cardiovascular complications.

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Uncoupling of endothelial nitric oxide synthase (eNOS) oxidative stress mechanism is involved in uremia.
“The uncoupling of endothelial nitric oxide synthase (eNOS), oxidative stress mechanism is involved in uremia, a condition when the kidney does not work properly and waste products instead of urine are excreted into the bloodstream (Himmelfarb et al. 2002).”
From Reactive Oxygen Species, Toxicity, Oxidative Stress, and Antioxidants: Chronic Diseases and Aging (2023) · cites this paper as Himmelfarb et al. 2002

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Tonsillar Distribution of IgA and IgG Immunocytes and Production of IgA Subclasses and J Chain in Tonsillitis Vary with the Presence or Absence of IgA Nephropathy
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Microalbuminuria in Patients With Essential Hypertension
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Hormonal and metabolic effects of calcium channel antagonists in man
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Amlodipine increases cyclosporine levels in hypertensive renal transplant patients
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KCl and angiotensin responses in isolated rat renal arterioles: effects of diltiazem and low-calcium medium
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Long-Term Effects of Enalapril and Nicardipine on Urinary Albumin Excretion in Patients with Chronic Renal Insufficiency: A 1-Year Follow-Up
Bianchi, S., Bigazzi, R., Baldari, G., & Campese, V. M. (1991) · American Journal of Nephrology · doi:10.1159/000168289 · Cited by 43 · see citing works
Effects of Large Dose Vitamin E Supplementation on Anemia in Hemodialysis Patients
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Comparative Trial of Lisinopril and Nifedipine in Mild to Severe Essential Hypertension
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Combination treatment of enalapril with nitrendipine in rats with renovascular hypertension.
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Angiotensin converting enzyme inhibition and calcium channel blockade in incipient diabetic nephropathy
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Oxidant stress in nephrotic syndrome: comparison of F2‐isoprostanes and plasma antioxidant potential
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Increase in tonsillar germinal centre B-1 cell numbers in IgA nephropathy (IgAN) patients and reduced susceptibility to Fas-mediated apoptosis
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Pharmacologic and Therapeutic Differences Among Calcium Channel Antagonists: Profile of Mibefradil, a New Calcium Antagonist
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Influence of nifedipine on interstitial fibrosis in renal transplant allografts treated with cyclosporin A.
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Lone-Term Effects of a Converting Enzyme Inhibitor and a Calcium Channel Blocker on Urinary Albumin Excretion in Patients With Essential Hypertension
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Comparative effects of captopril versus nifedipine on proteinuria and renal function of type 2 diabetic patients
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Longitudinal Analysis of Human Salivary Immunoglobulins, Nonimmune Antimicrobial Agents, and Microflora after Tonsillectomy
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Effect of and Indication for Tonsillectomy in IgA Nephropathy
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The composite nodule. A structural and functional unit of the reactive human lymph node.
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Treating hypertension in black compared with white non-insulin dependent diabetics: a double blind trial of verapamil and metoprolol.
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Effect of biocompatibility of hemodialysis membranes on serum albumin levels
Tayeb, J. S., Provenzano, R., El-Ghoroury, M., Bellovich, K. A., Khairullah, Q. T., Pieper, D. R., Morrison, L., & Calleja, Y. (2000) · American Journal of Kidney Diseases · doi:10.1016/s0272-6386(00)70005-9 · Cited by 33 · see citing works
Effect of diltiazem on glomerular heparan sulfate and albuminuria in diabetic rats.
Jyothirmayi, G. N., & Reddi, A. S. (1993) · Hypertension · doi:10.1161/01.hyp.21.6.795 · Cited by 33 · see citing works
Dissociation between antiproteinuric and antihypertensive effect of angiotensin converting enzyme inhibitors in rats
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Adipose Tissue as an Endocrine Organ
Kershaw, E. E., & Flier, J. S. (2004) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2004-0395 · Cited by 5,522 · see citing works
Kidney Disease as a Risk Factor for Development of Cardiovascular Disease: A Statement From the American Heart Association Councils on Kidney in Cardiovascular Disease, High Blood Pressure Research, Clinical Cardiology, and Epidemiology and Prevention
Sarnak, M. J., Levey, A. S., Schoolwerth, A. C., Coresh, J., Culleton, B., Hamm, L. L., McCullough, P. A., Kasiske, B. L., Kelepouris, E., Klag, M. J., et al. (2003) · Circulation · doi:10.1161/01.cir.0000095676.90936.80 · Cited by 3,768 · see citing works
Reactive Oxygen Species, Toxicity, Oxidative Stress, and Antioxidants: Chronic Diseases and Aging
Jomova, K., Raptova, R., Alomar, S. Y., Alwasel, S. H., Nepovimova, E., Kuca, K., & Valko, M. (2023) · Archives of Toxicology · doi:10.1007/s00204-023-03562-9 · Cited by 2,638 · see citing works
Atorvastatin in patients with type 2 diabetes mellitus undergoing hemodialysis
Wanner, C., Krane, V., März, W., Olschewski, M., Mann, J. F. E., Ruf, G., & Ritz, E. (2005) · New England Journal of Medicine · doi:10.1056/nejmoa043545 · Cited by 2,614 · see citing works
A proposed nomenclature and diagnostic criteria for protein–energy wasting in acute and chronic kidney disease
Fouque, D. P., Kalantar‐Zadeh, K., Kopple, J. D., Cano, N., Chauveau, P., Cuppari, L., Franch, H. A., Guarnieri, G., Ikizler, T. A., Kaysen, G. A., et al. (2007) · Kidney International · doi:10.1038/sj.ki.5002585 · Cited by 2,004 · see citing works
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Chronic Kidney Disease: Effects on the Cardiovascular System
Schiffrin, E. L., Lipman, M. L., & Mann, J. F. E. (2007) · Circulation · doi:10.1161/circulationaha.106.678342 · Cited by 1,448 · see citing works
K/DOQI Clinical Practice Guidelines for Cardiovascular Disease in Dialysis Patients
(2005) · American Journal of Kidney Diseases · doi:10.1053/j.ajkd.2005.01.019 · Cited by 1,433 · see citing works
Chronic kidney disease alters intestinal microbial flora
Vaziri, N. D., Wong, J., Pahl, M., Piceno, Y. M., Yuan, J., DeSantis, T. Z., Ni, Z., Nguyen, T.-H., & Andersen, G. L. (2013) · Kidney International · doi:10.1038/ki.2012.345 · Cited by 1,164 · see citing works
Kidney Disease as a Risk Factor for Development of Cardiovascular Disease: A Statement From the American Heart Association Councils on Kidney in Cardiovascular Disease, High Blood Pressure Research, Clinical Cardiology, and Epidemiology and Prevention
Sarnak, M. J., Levey, A. S., Schoolwerth, A. C., Coresh, J., Culleton, B., Hamm, L. L., McCullough, P. A., Kasiske, B. L., Kelepouris, E., Klag, M. J., et al. (2003) · Hypertension · doi:10.1161/01.hyp.0000102971.85504.7c · Cited by 1,144 · see citing works
Oxidative stress in chronic kidney disease
Daenen, K., Andries, A., Mekahli, D., Schepdael, A. V., Jouret, F., & Bammens, B. (2018) · Pediatric Nephrology · doi:10.1007/s00467-018-4005-4 · Cited by 888 · see citing works
Increased prevalence of oxidant stress and inflammation in patients with moderate to severe chronic kidney disease
Oberg, B. P., McMenamin, E., Lucas, F. L., McMonagle, E., Morrow, J. D., Ikizler, T. A., & Himmelfarb, J. (2004) · Kidney International · doi:10.1111/j.1523-1755.2004.00465.x · Cited by 780 · see citing works
Self-citation
Targeting the transcription factor Nrf2 to ameliorate oxidative stress and inflammation in chronic kidney disease
Ruiz, S., Pérgola, P. E., Zager, R. A., & Vaziri, N. D. (2013) · Kidney International · doi:10.1038/ki.2012.439 · Cited by 722 · see citing works
Curcumin, Inflammation, and Chronic Diseases: How Are They Linked?
He, Y., Yue, Y., Zheng, X., Zhang, K., Chen, S., & Du, Z. (2015) · Molecules · doi:10.3390/molecules20059183 · Cited by 611 · see citing works
Emerging Biomarkers for Evaluating Cardiovascular Risk in the Chronic Kidney Disease Patient
Stenvinkel, P., Carrero, J. J., Axelsson, J., Lindholm, B., Heimbürger, O., & Massy, Z. A. (2008) · Clinical Journal of the American Society of Nephrology · doi:10.2215/cjn.03670807 · Cited by 567 · see citing works
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Iron behaving badly: inappropriate iron chelation as a major contributor to the aetiology of vascular and other progressive inflammatory and degenerative diseases
Kell, D. B. (2009) · BMC Medical Genomics · doi:10.1186/1755-8794-2-2 · Cited by 554 · see citing works
Dyslipidemia of chronic renal failure: the nature, mechanisms, and potential consequences
Vaziri, N. D. (2006) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.00099.2005 · Cited by 542 · see citing works
Iron management in chronic kidney disease: conclusions from a “Kidney Disease: Improving Global Outcomes” (KDIGO) Controversies Conference
Macdougall, I. C., Bircher, A. J., Eckardt, K., Obrador, G. T., Pollock, C. A., Stenvinkel, P., Swinkels, D. W., Wanner, C., Weiß, G., Chertow, G. M., et al. (2016) · Kidney International · doi:10.1016/j.kint.2015.10.002 · Cited by 488 · see citing works
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Contribution of impaired Nrf2-Keap1 pathway to oxidative stress and inflammation in chronic renal failure
Kim, H. J., & Vaziri, N. D. (2009) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.00421.2009 · Cited by 474 · see citing works
Trained immunity — basic concepts and contributions to immunopathology
Ochando, J., Mulder, W. J. M., Madsen, J. C., Netea, M. G., & Duivenvoorden, R. (2022) · Nature Reviews Nephrology · doi:10.1038/s41581-022-00633-5 · Cited by 474 · see citing works
The severe cardiorenal syndrome: ‘Guyton revisited’
Bongartz, L. G., Cramer, M. J., Doevendans, P. A., Joles, J. A., & Braam, B. G. (2004) · European Heart Journal · doi:10.1093/eurheartj/ehi020 · Cited by 459 · see citing works
Uremia
Meyer, T. W., & Hostetter, T. H. (2007) · New England Journal of Medicine · doi:10.1056/nejmra071313 · Cited by 458 · see citing works
Insulin resistance in chronic kidney disease: a systematic review
Spoto, B., Pisano, A., & Zoccali, C. (2016) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.00340.2016 · Cited by 453 · see citing works
NAFLD as a driver of chronic kidney disease
Byrne, C. D., & Targher, G. (2020) · Journal of Hepatology · doi:10.1016/j.jhep.2020.01.013 · Cited by 449 · see citing works
Associations between circulating inflammatory markers and residual renal function in CRF patients
Pecoits‐Filho, R., Heimbürger, O., Barany, P. F., Suliman, M., Fehrman‐Ekholm, I., Lindholm, B., & Stenvinkel, P. (2003) · American Journal of Kidney Diseases · doi:10.1016/s0272-6386(03)00353-6 · Cited by 449 · see citing works
Self-citation
The uremic solute indoxyl sulfate induces oxidative stress in endothelial cells
Dou, L., Jourde‐Chiche, N., Faure, V., Cérini, C., Berland, Y., Dignat‐George, F., & Brunet, P. (2007) · Journal of Thrombosis and Haemostasis · doi:10.1111/j.1538-7836.2007.02540.x · Cited by 432 · see citing works
Oxidative Stress Is Progressively Enhanced With Advancing Stages of CKD
Dounousi, E. C., Papavasiliou, E. C., Makedou, A., Ioannou, K. I., Katopodis, K. P., Tselepis, A. D., Siamopoulos, K. C., & Tsakiris, D. (2006) · American Journal of Kidney Diseases · doi:10.1053/j.ajkd.2006.08.015 · Cited by 412 · see citing works
Impact of inflammation on epigenetic DNA methylation – a novel risk factor for cardiovascular disease?
Stenvinkel, P., Karimi, M., Johansson, S., Axelsson, J., Suliman, M., Lindholm, B., Heimbürger, O., Barany, P. F., Alvestrand, A., Nordfors, L., et al. (2007) · Journal of Internal Medicine · doi:10.1111/j.1365-2796.2007.01777.x · Cited by 396 · see citing works
Self-citation
Altered intestinal microbial flora and impaired epithelial barrier structure and function in CKD: the nature, mechanisms, consequences and potential treatment
Vaziri, N. D., Zhao, Y., & Pahl, M. V. (2015) · Nephrology Dialysis Transplantation · doi:10.1093/ndt/gfv095 · Cited by 394 · see citing works
Oxidative Stress in the Pathogenesis and Evolution of Chronic Kidney Disease: Untangling Ariadne’s Thread
Duni, Α., Liakopoulos, V., Roumeliotis, S. K., Peschos, D., & Dounousi, E. C. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20153711 · Cited by 388 · see citing works
Hemodialysis
Himmelfarb, J., & Ikizler, T. A. (2010) · New England Journal of Medicine · doi:10.1056/nejmra0902710 · Cited by 397 · see citing works
Self-citation
Role of Urea in Intestinal Barrier Dysfunction and Disruption of Epithelial Tight Junction in Chronic Kidney Disease
Vaziri, N. D., Yuan, J. J., & Norris, K. C. (2012) · American Journal of Nephrology · doi:10.1159/000345969 · Cited by 385 · see citing works
Chronic kidney disease and premature ageing
Kooman, J. P., Kotanko, P., Schols, A. M. W. J., Shiels, P. G., & Stenvinkel, P. (2014) · Nature Reviews Nephrology · doi:10.1038/nrneph.2014.185 · Cited by 383 · see citing works
Self-citation
Chemistry and Antihypertensive Effects of Tempol and Other Nitroxides
Wilcox, C. S., & Pearlman, A. (2008) · Pharmacological Reviews · doi:10.1124/pr.108.000240 · Cited by 377 · see citing works
Concentrated red grape juice exerts antioxidant, hypolipidemic, and antiinflammatory effects in both hemodialysis patients and healthy subjects
Castilla, P., Echarri, R., Dávalos, A., Cerrato, F., Ortega, H., Teruel, J. L., Lucas, M. F., Gómez‐Coronado, D., Ortuño, J. Á., & Lasunción, M. A. (2006) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/84.1.252 · Cited by 368 · see citing works
Towards a unifying, systems biology understanding of large-scale cellular death and destruction caused by poorly liganded iron: Parkinson’s, Huntington’s, Alzheimer’s, prions, bactericides, chemical toxicology and others as examples
Kell, D. B. (2010) · Archives of Toxicology · doi:10.1007/s00204-010-0577-x · Cited by 361 · see citing works
Biomarkers of inflammation and progression of chronickidney disease
Tonelli, M. A., Sacks, F. M., Pfeffer, M. A., Jhangri, G. S., & Curhan, G. C. (2005) · Kidney International · doi:10.1111/j.1523-1755.2005.00398.x · Cited by 358 · see citing works
Oxidative stress in uremia: Nature, mechanisms, and potential consequences
Vaziri, N. D. (2004) · Seminars in Nephrology · doi:10.1016/j.semnephrol.2004.06.026 · Cited by 357 · see citing works
Metabolomics for clinical use and research in chronic kidney disease
Hocher, B., & Adamski, J. (2017) · Nature Reviews Nephrology · doi:10.1038/nrneph.2017.30 · Cited by 335 · see citing works
Coronary Microvascular Dysfunction
Vancheri, F., Longo, G., Vancheri, S., & Henein, M. Y. (2020) · Journal of Clinical Medicine · doi:10.3390/jcm9092880 · Cited by 344 · see citing works
Chronic kidney disease, anemia, and incident stroke in a middle-aged, community-based population: The ARIC Study
Abramson, J. L., Jurkovitz, C. T., Vaccarino, V., Weintraub, W., & McClellan, W. (2003) · Kidney International · doi:10.1046/j.1523-1755.2003.00109.x · Cited by 334 · see citing works
Gamma-Glutamyltransferase: A Predictive Biomarker of Cellular Antioxidant Inadequacy and Disease Risk
Koenig, G., & Seneff, S. (2015) · Disease Markers · doi:10.1155/2015/818570 · Cited by 332 · see citing works
Chronic kidney disease: a public health priority and harbinger of premature cardiovascular disease
Stenvinkel, P. (2010) · Journal of Internal Medicine · doi:10.1111/j.1365-2796.2010.02269.x · Cited by 331 · see citing works
Self-citation
Disintegration of colonic epithelial tight junction in uremia: a likely cause of CKD-associated inflammation
Vaziri, N. D., Yuan, J. J., Rahimi, A., Ni, Z., Said, H., & Subramanian, V. S. (2011) · Nephrology Dialysis Transplantation · doi:10.1093/ndt/gfr624 · Cited by 306 · see citing works
Effect of malnutrition-inflammation complex syndrome on EPO hyporesponsiveness in maintenance hemodialysis patients
Kalantar‐Zadeh, K., McAllister, C. J., Lehn, R. S., Lee, G. H., Nissenson, A. R., & Kopple, J. D. (2003) · American Journal of Kidney Diseases · doi:10.1016/s0272-6386(03)00915-6 · Cited by 303 · see citing works
Chronic Inflammation in Chronic Kidney Disease Progression: Role of Nrf2
Stenvinkel, P., Chertow, G. M., Devarajan, P., Levin, A., Andreoli, S. P., Bangalore, S., & Warady, B. A. (2021) · Kidney International Reports · doi:10.1016/j.ekir.2021.04.023 · Cited by 301 · see citing works
Self-citation
Oxidative Stress in Hemodialysis Patients: A Review of the Literature
Liakopoulos, V., Roumeliotis, S. K., Gorny, X., Dounousi, E. C., & Mertens, P. R. (2017) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2017/3081856 · Cited by 298 · see citing works
Chronic Kidney Disease: A Clinical Model of Premature Aging
Stenvinkel, P., & Larsson, T. E. (2013) · American Journal of Kidney Diseases · doi:10.1053/j.ajkd.2012.11.051 · Cited by 298 · see citing works
Self-citation
Protective Role for Antioxidants in Acute Kidney Disease
Dennis, J. M., & Witting, P. K. (2017) · Nutrients · doi:10.3390/nu9070718 · Cited by 298 · see citing works
Exercise in Individuals With CKD
Johansen, K. L., & Painter, P. (2011) · American Journal of Kidney Diseases · doi:10.1053/j.ajkd.2011.10.008 · Cited by 291 · see citing works
Advances and New Frontiers in the Pathophysiology of Venous Neointimal Hyperplasia and Dialysis Access Stenosis
Lee, T. C., & Roy‐Chaudhury, P. (2009) · Advances in Chronic Kidney Disease · doi:10.1053/j.ackd.2009.06.009 · Cited by 290 · see citing works
Endothelial Dysfunction in Chronic Kidney Disease, from Biology to Clinical Outcomes: A 2020 Update
Roumeliotis, S. K., Mallamaci, F., & Zoccali, C. (2020) · Journal of Clinical Medicine · doi:10.3390/jcm9082359 · Cited by 295 · see citing works
Nitric oxide, oxidative stress, and progression of chronic renal failure
Modlinger, P., Wilcox, C. S., & Aslam, S. (2004) · Seminars in Nephrology · doi:10.1016/j.semnephrol.2004.04.007 · Cited by 283 · see citing works
Rokumi-jio-gan-Containing Prescriptions Attenuate Oxidative Stress, Inflammation, and Apoptosis in the Remnant Kidney
Park, C. H., Lee, S. L., Okamoto, T., Tanaka, T., & Yokozawa, T. (2012) · Evidence-based Complementary and Alternative Medicine · doi:10.1155/2012/587902 · Cited by 282 · see citing works
Oxidants in Chronic Kidney Disease
Shah, S. V., Baliga, R., Rajapurkar, M. M., & Fonseca, V. A. (2006) · Journal of the American Society of Nephrology · doi:10.1681/asn.2006050500 · Cited by 277 · see citing works
Uremia Alters HDL Composition and Function
Holzer, M., Birner‐Gruenberger, R., Stojaković, T., El‐Gamal, D., Binder, V., Wadsack, C., Heinemann, Á., & Marsche, G. (2011) · Journal of the American Society of Nephrology · doi:10.1681/asn.2010111144 · Cited by 269 · see citing works
The molecular mechanisms of hemodialysis vascular access failure
Brahmbhatt, A. N., Remuzzi, A., Franzoni, M., & Misra, S. (2016) · Kidney International · doi:10.1016/j.kint.2015.12.019 · Cited by 263 · see citing works
Oxidative stress and reactive oxygen species.
Galli, F., Piroddi, M., Annetti, C., Aisa, C., Floridi, E., & Floridi, A. (2005) · Contributions to Nephrology · doi:10.1159/000085686 · Cited by 242 · see citing works
Roles of oxidative stress and antioxidant therapy in chronic kidney disease and hypertension
Vaziri, N. D. (2003) · Current Opinion in Nephrology & Hypertension · doi:10.1097/00041552-200401000-00013 · Cited by 253 · see citing works
Endothelial Cell Dysfunction and Increased Cardiovascular Risk in Patients With Chronic Kidney Disease
Baaten, C. C. F. M. J., Vondenhoff, S., & Noels, H. (2023) · Circulation Research · doi:10.1161/circresaha.123.321752 · Cited by 250 · see citing works
Mitochondrial dysregulation and oxidative stress in patients with chronic kidney disease
Granata, S., Zaza, G., Simone, S., Villani, G., Latorre, D., Pontrelli, P., Carella, M., Schena, F. P., Grandaliano, G., & Pertosa, G. B. (2009) · BMC Genomics · doi:10.1186/1471-2164-10-388 · Cited by 242 · see citing works
Inflammation and premature aging in advanced chronic kidney disease
Kooman, J. P., Dekker, M. J. E., Usvyat, L. A., Kotanko, P., SANDE, F. M. V. D., Schalkwijk, C. G., Shiels, P. G., & Stenvinkel, P. (2017) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.00256.2017 · Cited by 242 · see citing works
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Authors: Himmelfarb, J., Stenvinkel, P., Ikizler, T. A., & Hakim, R. M.
Affiliations: Maine Medical Center (US)
Corresponding author: Himmelfarb, Jonathan
ORCID: Himmelfarb, Jonathan
Stenvinkel, Peter
Ikizler, T. Alp
Hakim, Raymond M.
Venue: Kidney International
Publisher: Elsevier BV
Published: 2002-11
Volume: 62
Issue: 5
Pages: 1524-1538
ISSN: 0085-2538 (ISSN-L)
DOI: 10.1046/j.1523-1755.2002.00600.x
OpenAlex: W1996978408
Cited by: 1,179
References: 294
Citations by year: 2026: 15 · 2025: 16 · 2024: 29 · 2023: 31 · 2022: 36 · 2021: 51 · 2020: 40 · 2019: 30 · 2018: 43 · 2017: 57 · 2016: 49 · 2015: 57 · 2014: 58 · 2013: 71 · 2012: 68
FWCI: 10.70
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 4784 d)
Locations: Kidney International (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Nephrology › Dialysis and Renal Disease Management
Health Sciences › Medicine › Biochemistry › Antioxidant Activity and Oxidative Stress
Health Sciences › Medicine › Physiology › Nitric Oxide and Endothelin Effects
Keywords: uremia, oxidative stress, cardiovascular disease, atherosclerosis, inflammation, malnutrition, dialysis, uremic solutes, beta2-microglobulin, homocysteine, cysteine, antioxidant therapy, vascular access catheters, cardiovascular mortality
MeSH terms: Cardiovascular Diseases, Humans, Uremia, Oxidative Stress

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The elephant in uremia: Oxidant stress as a unifying concept of cardiovascular disease in uremia

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