Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Sudden cardiac death in chronic kidney disease: epidemiology and prevention

Nature Reviews Nephrology volume 7, pages 145–154 (2011)Cite this article

Subjects

Abstract

Annual cardiovascular mortality in patients with chronic kidney disease (CKD) is much higher than in the general population. The rate of sudden cardiac death increases as the stage of CKD increases and could be responsible for 60% of cardiac deaths in patients undergoing dialysis. In hemodialysis units treating patients with CKD, cardiac arrest occurs at a rate of seven arrests per 100,000 hemodialysis sessions. Important risk factors for sudden cardiac death in patients with CKD include hospitalization within the past 30 days, a drop of 30 mmHg in systolic blood pressure during hemodialysis, duration of life on hemodialysis, time since the previous dialysis session, and the presence of concomitant diabetes mellitus. As a result of the adverse cardiomyopathic and vasculopathic milieu in CKD, the occurrence of arrhythmias, conduction abnormalities, and sudden cardiac death could be exacerbated by electrolyte shifts, divalent ion abnormalities, diabetes, sympathetic overactivity, in addition to inflammation and perhaps iron deposition. Impaired baroreflex effectiveness and sensitivity, as well as obstructive sleep apnea, might also contribute to the risk of sudden death in CKD. The likelihood of survival following cardiac arrest is very low in dialysis patients. Primary and secondary prevention of cardiac arrest could reduce cardiovascular mortality in patients with CKD. Cardioverter-defibrillator implantation decreases the risk of sudden death in patients with CKD. The decision to implant a cardioverter-defibrillator should be influenced by the patient's age and stage of CKD.

Key Points

  • Chronic kidney disease (CKD) is a risk factor for sudden cardiac death; the rate of sudden cardiac death increases as the stage of CKD increases

  • In hemodialysis units, cardiac arrest occurs at a rate of seven per 100,000 hemodialysis sessions

  • Survival following cardiac arrest is very poor

  • Adverse cardiomyopathic and vasculopathic milieu in CKD predispose to conduction abnormalities and arrhythmic events

  • Multiple risk factors and mechanisms can contribute to the risk of sudden death in CKD; primary and secondary prevention could reduce cardiovascular mortality in patients with CKD

  • Patients with CKD at risk of sudden cardiac death can be identified and the decision to implant a cardioverter-defibrillator should be influenced by age and stage of CKD

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Learn more

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Sudden cardiac death rate according to stage of chronic kidney disease.
Figure 2: Ratio of actual to expected number of occurrences of sudden death for each 12 h interval from the start of hemodialysis.
Figure 3: The pathophysiology of diseases that predispose patients with chronic kidney disease to cardiac arrest.
Figure 4: The pathophysiology of sudden cardiac death in patients with chronic kidney disease.
Figure 5: Pathophysiology of inflammation and cardiac death.

References

  1. Parfrey, P. S. & Foley, R. N. The clinical epidemiology of cardiac disease in chronic renal failure. J. Am. Soc. Nephrol. 10, 1606–1615 (1999).

    CAS  PubMed  Google Scholar 

  2. Foley, R. N. et al. Chronic kidney disease and the risk for cardiovascular disease, renal replacement, and death in the United State Medicare population, 1998 to 1999. J. Am. Soc. Nephrol. 16, 489–495 (2005).

    Article  PubMed  Google Scholar 

  3. Schiffrin, E. L., Lipman, M. L. & Mann, J. F. Chronic kidney disease: effects on the cardiovascular system. Circulation 116, 85–97 (2007).

    Article  PubMed  Google Scholar 

  4. Herzog, C. A. Cardiac arrest in dialysis patients: approaches to alter an abysmal outcome. Kidney Int. 63 (Suppl. 84), 197–200 (2003).

    Article  Google Scholar 

  5. Mann, J. F. E. et al. Renal insufficiency as a predictor of cardiovascular outcomes and the impact of ramipril: the HOPE randomized trial. Ann. Intern. Med. 134, 629–636 (2001).

    Article  CAS  PubMed  Google Scholar 

  6. Mann, J. F. E., Gerstein, H. C., Dulau-Florea, I. & Lonn, E. Cardiovascular risk in patients with mild renal insufficiency. Kidney Int. 63 (Suppl. 84), S192–S196 (2003).

    Article  Google Scholar 

  7. Ruilope, L. M. et al. Renal function and intensive lowering of blood pressure in hypertensive participants of the hypertension optimal treatment (HOT) study. J. Am. Soc. Nephrol. 12, 218–225 (2001).

    CAS  PubMed  Google Scholar 

  8. Thomas, A. C., Knapman, P. A., Krikler, D. M. & Davis, M. J. Community study of the causes of “natural' sudden death. BMI 297, 1453–1456 (1988).

    CAS  Google Scholar 

  9. Ritz, E. & Warnner, C. The challege of sudden death in dialysis patients. Clin. J. Am. Soc. Nephrol. 3, 920–929 (2008).

    Article  PubMed  Google Scholar 

  10. Ganesh, S. K., Stack, A. G., Levin, N. W., Hulbert-Shearon, T. & Port, F. K. Association of elevated serum PO4, Ca × PO4 product, and parathyroid hormone with cardiac mortality risk in chronic hemodialysis patients. J. Am. Soc. Nephrol. 12, 2131–2138 (2001).

    CAS  PubMed  Google Scholar 

  11. Herzog, C. A., Strief, J. W., Collins, A. J. & Gilbertson, D. T. Cause-specific mortality of dialysis patients after coronary revascularization: why don't dialysis patients have better survival after coronary intervention? Nephrol. Dial. Transplant. 23, 2629–2633 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  12. 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).

    Article  PubMed  PubMed Central  Google Scholar 

  13. Karnik, J. A. et al. Cardiac arrest and sudden death in dialysis units. Kidney Int. 60, 350–357 (2001).

    Article  CAS  PubMed  Google Scholar 

  14. Bleyer, A. J. et al. Characteristics of sudden death in hemodialysis patients. Kidney Int. 69, 2268–2273 (2006).

    Article  CAS  PubMed  Google Scholar 

  15. US Renal Data System. USRDS 2008 Annual Data Report. National Institutes of Health, National Institute of Diabetes and Digestive and Kidney Diseases. [online] (2008).

  16. 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).

    Article  CAS  PubMed  Google Scholar 

  17. Foley, R. N. et al. Long-term evolution of cardiomyopathy in dialysis patients. Kidney Int. 54, 1720–1725 (1998).

    Article  CAS  PubMed  Google Scholar 

  18. Parfrey, P. S. et al. Double-blind comparison of full and partial anemia correction in incident hemodialysis patients without symptomatic heart disease. J. Am. Soc. Nephrol. 16, 2180–2189 (2005).

    Article  PubMed  Google Scholar 

  19. Foley, R. N. et al. The prognostic importance of left ventricular geometry in uremic cardiomyopathy. J. Am. Soc. Nephrol. 5, 2024–2031 (1995).

    CAS  PubMed  Google Scholar 

  20. Foley, R. N. et al. Left ventricular hypertrophy in new hemodialysis patients without symptomatic cardiac disease. Clin. J. Am. Soc. Nephrol. 5, 805–813 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Stewart, G. A. et al. Electrocardiographic abnormalities and uremic cardiomyopathy. Kidney Int. 67, 217–226 (2005).

    Article  PubMed  Google Scholar 

  22. Sforzini, S. et al. Ventricular arrhythmias and four-year mortality in hemodialysis patients. Lancet 339, 212–213 (1992).

    Article  CAS  PubMed  Google Scholar 

  23. Kitano, Y. et al. Severe coronary stenosis is an important factor for induction and lengthy persistence of ventricular arrhythmias during and after hemodialysis. Am. J. Kidney Dis. 44, 328–336 (2004).

    Article  PubMed  Google Scholar 

  24. Parekh, R. S. et al. Severe coronary stenosis is an important factor for induction and lengthy persistence of ventricular arrhythmias during and after hemodialysis. Kidney Int. 74, 1335–1342 (2008).

    Article  CAS  PubMed  Google Scholar 

  25. Sinha, M. K., Gaze, D. C., Tippins, J. R., Collinson, P. O. & Kaski, J. C. Ischemia modified albumin is a sensitive marker of myocardial ischemia after percutaneous coronary intervention. Circulation 107, 2403–2405 (2003).

    Article  CAS  PubMed  Google Scholar 

  26. Pollack, C. et al. Ischemia modified albumin is useful in risk stratification of emergency department chest pain patients. Acad. Emerg. Med. 10, 555–556 (2003).

    Article  Google Scholar 

  27. Sharma, R. et al. Ischemia-modified albumin predicts mortality in ESRD. Am. J. Kidney Dis. 47, 493–502 (2006).

    Article  CAS  PubMed  Google Scholar 

  28. Nishimura, M. et al. Prediction of cardiac death in hemodialysis patients by myocardial fatty acid imaging. J. Am. Coll. Cardiol. 51, 139–145 (2008).

    Article  CAS  PubMed  Google Scholar 

  29. Patanè, S. et al. QT interval prolongation, torsade de pointes and renal disease. Int. J. Cardiol. 130, e71–e73 (2008).

    Article  PubMed  Google Scholar 

  30. Amann, K. et al. Cardiac remodeling in experimental renal failure—an immunohistochemical study. Nephrol. Dial. Transplant. 13, 1958–1966 (1998).

    Article  CAS  PubMed  Google Scholar 

  31. Covic, A. et al. Hemodialysis increases QTc interval but not QTc dispersion in ESRD patients without manifest cardiac disease. Nephrol. Dial. Transplant. 17, 2170–2177 (2002).

    Article  CAS  PubMed  Google Scholar 

  32. De Bruyne, M. C. et al. QTc dispersion predicts cardiac mortality in the elderly: the Rotterdam Study. Circulation 97, 467–472 (1998).

    Article  CAS  PubMed  Google Scholar 

  33. Kantarci, G., Ozener, C., Tokay, S., Bihorac, A. & Akoglu, E. QT dispersion in hemodialysis and CAPD patients. Nephron 91, 739–741 (2002).

    Article  CAS  PubMed  Google Scholar 

  34. Beaubien, E. R., Pylypchuk, G. B., Akhtar, J. & Biem, H. J. Value of corrected QT interval dispersion in identifying patients initiating dialysis at increased risk of total and cardiovascular mortality. Am. J. Kidney Dis. 39, 834–842 (2002).

    Article  PubMed  Google Scholar 

  35. Johnsson, M. et al. Elevated temporal QT variability index in patients with chronic renal failure. Clin. Sci. 107, 583–588 (2004).

    Article  Google Scholar 

  36. Atiga, W. L. et al. Beat-to-beat repolarization lability identifies patients at risk for sudden cardiac death. J. Cardiovasc. Electrophysiol. 9, 899–908 (1998).

    Article  CAS  PubMed  Google Scholar 

  37. Agarwal, A., Anand, I. S., Sakhuja, V. & Chugh, K. S. Effect of dialysis and renal transplantation on autonomic dysfunction in chronic renal failure. Kidney Int. 40, 489–495 (1991).

    Article  CAS  PubMed  Google Scholar 

  38. Tisdale, J. E. & Miller, D. A. Drug-Induced Disease: Prevention, Detection, and Management 2nd edn, Ch. 26 (American Society of Health-System Pharmacists, Bethesda, MD, 2005).

    Google Scholar 

  39. Parekh, R. S. et al. The association of sudden cardiac death with inflammation and other traditional risk factors. Kidney Int. 74, 1335–1342 (2008).

    Article  CAS  PubMed  Google Scholar 

  40. Ravani, P. et al. Asymmetrical dimethylarginine predicts progression to dialysis and death in patients with chronic kidney disease: a competing risks modeling approach. J. Am. Soc. Nephrol. 16, 2449–2455 (2005).

    Article  CAS  PubMed  Google Scholar 

  41. Shamseddin, M. K. & Parfrey, P. S. Mechanisms of the cardiorenal syndromes. Nat. Rev. Nephrol. 5, 641–649 (2009).

    Article  PubMed  Google Scholar 

  42. Mallamaci, F. et al. CREED Investigators: Hyperhomocysteinemia predicts cardiovascular outcomes in hemodialysis patients. Kidney Int. 61, 609–614 (2002).

    Article  PubMed  Google Scholar 

  43. Hoffman, B. F., Feinmark, S. J. & Guo, S. D. Electrophysiologic effects of interactions between activated canine neutrophils and cardiac myocytes. J. Cardiovasc. Electrophysiol. 8, 679–687 (1997).

    Article  CAS  PubMed  Google Scholar 

  44. Hoffman, B. F., Guo, S. D. & Feinmark, S. J. Arrhythmias caused by platelet activating factor. J. Cardiovasc. Electrophysiol. 7, 120–133 (1996).

    Article  CAS  PubMed  Google Scholar 

  45. Naghavi, M. et al. From vulnerable plaque to vulnerable patient: a call for new definitions and risk assessment strategies: part II. Circulation 108, 1772–1778 (2003).

    Article  PubMed  Google Scholar 

  46. Myerburg, R. J. Sudden cardiac death: exploring the limits of our knowledge. J. Cardiovasc. Electrophysiol. 12, 369–381 (2001).

    Article  CAS  PubMed  Google Scholar 

  47. Bleyer, A. J., Russell, G. B. & Satko, S. G. Sudden and cardiac death rates in hemodialysis patients. Kidney Int. 55, 1553–1559 (1999).

    Article  CAS  PubMed  Google Scholar 

  48. Santoro, A. et al. Patients with complex arrhythmias during and after hemodialysis suffer from different regimens of potassium removal. Nephrol. Dial. Transplant. 23, 1415–1421 (2008).

    Article  PubMed  Google Scholar 

  49. Howse, M., Sastry, S. & Bell, G. M. Changes in the corrected QT interval and corrected QT dispersion during hemodialysis. Postgrad. Med. J. 78, 273–275 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Block, G. A., Hulbert-Shearon, T. E., Levin, N. W. & Port, F. K. Association of serum phosphorous and calcium × phosphate product with mortality risk in chronic hemodialysis patients: a national study. Am. J. Kidney Dis. 31, 607–617 (1998).

    Article  CAS  PubMed  Google Scholar 

  51. Schwarz, U. et al. Morphology of coronary atherosclerotic lesions in patients with end-stage renal failure. Nephrol. Dial. Transplant. 15, 218–233 (2000).

    Article  CAS  PubMed  Google Scholar 

  52. Amann, K. & Ritz, E. Microvascular disease—the Cinderella of uremic heart disease. Nephrol. Dial. Transplant. 15, 1493–1503 (2000).

    Article  CAS  PubMed  Google Scholar 

  53. Sharma, R. et al. Mitral annular calcification predicts mortality and coronary artery disease in end stage renal disease. Atherosclerosis 191, 348–354 (2007).

    Article  CAS  PubMed  Google Scholar 

  54. Besarab, A. Iron and cardiac disease in the end-stage renal disease setting. Am. J. Kidney Dis. 34, S18–S24 (1999).

    Article  CAS  PubMed  Google Scholar 

  55. Wardman, P. & Candeias, L. P. Fenton chemistry: an introduction. Radiat. Res. 145, 523–531 (1996).

    Article  CAS  PubMed  Google Scholar 

  56. Wu, V. C. et al. The effect of iron stores on corrected QT dispersion in patients undergoing peritoneal dialysis. Am. J. Kidney Dis. 44, 720–728 (2004).

    Article  CAS  PubMed  Google Scholar 

  57. Rump, L. C., Amann, K., Orth, S. & Ritz, E. Sympathetic overactivity in renal disease: a window to understand progression and cardiovascular complications of uremia? Nephrol. Dial. Transplant. 15, 1735–1738 (2000).

    Article  CAS  PubMed  Google Scholar 

  58. Converse, R. L. Jr et al. Sympathetic overactivity in patients with chronic renal failure. N. Engl. J. Med. 327, 1912–1918 (1992).

    Article  PubMed  Google Scholar 

  59. Amann, K. et al. Effects of low dose sympathetic inhibition on glomerulosclerosis and albuminuria in subtotally nephrectomized rats. J. Am. Soc. Nephrol. 11, 1469–1478 (2000).

    CAS  PubMed  Google Scholar 

  60. Xu, J. et al. Renalase is a novel, soluble monoamine oxidase that regulates cardiac function and blood pressure. J. Clin. Invest. 115, 1275–1280 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Pressman, M. R., Benz, R. L., Schleifer, C. R. & Peterson, D. D. Sleep disordered breathing in ESRD: acute beneficial effects of treatment with nasal continuous positive airway pressure. Kidney Int. 43, 1134–1139 (1993).

    Article  CAS  PubMed  Google Scholar 

  62. Johansson, M. et al. Reduced baroreflex effectiveness index in hypertensive patients with chronic renal failure. Am. J. Hypertens. 18, 995–1000 (2005).

    Article  PubMed  Google Scholar 

  63. Di Rienzo, M. et al. Baroreflex effectiveness index: an additional measure of baroreflex control of heart rate in daily life. Am. J. Physiol. Regul. Integr. Comp. Physiol. 280, 744–751 (2001).

    Article  Google Scholar 

  64. La Rovere, M. T., Bigger, J. T. Jr, Marcus, F. I., Mortara, A. & Schwartz, P. J. Baroreflex sensitivity and heart-rate variability in prediction of total cardiac mortality after myocardial infarction ATRAMI (Autonomic Tone and Reflexes After Myocardial Infarction) Investigators. Lancet 351, 478–484 (1998).

    Article  CAS  PubMed  Google Scholar 

  65. Johansson, M. et al. Baroreflex effectiveness index and baroreflex sensitivity predict all-cause mortality and sudden death in hypertensive patients with chronic renal failure. J. Hypertens. 25, 163–168 (2007).

    Article  CAS  PubMed  Google Scholar 

  66. Cice, G. et al. Carvedilol increases two-year survival in dialysis patients with dilated cardiomyopathy: a prospective, placebo-controlled trial. J. Am. Coll. Cardiol. 41, 1438–1444 (2003).

    Article  CAS  PubMed  Google Scholar 

  67. Pun, P. H., Lehrich, R. W., Smith, S. R. & Middleton, J. P. Predictors of survival after cardiac arrest in outpatient hemodialysis clinics. Clin. J. Am. Soc. Nephrol. 2, 491–500 (2007).

    Article  PubMed  Google Scholar 

  68. Takahashi, A. et al. Candesartan, an angiotensin II type-1 receptor blocker, reduces cardiovascular events in patients on chronic hemodialysis-—a randomized study. Nephrol. Dial. Transplant. 21, 2507–2512 (2006).

    Article  CAS  PubMed  Google Scholar 

  69. Brenner, B. M. et al. Effects of losartan on renal and cardiovascular outcomes in patients with type 2 diabetes and nephropathy. N. Engl. J. Med. 345, 861–869 (2001).

    Article  CAS  PubMed  Google Scholar 

  70. Zannad, F. et al. Prevention of cardiovascular events in end-stage renal disease: results of a randomized trial of fosinopril and implications for future studies. Kidney Int. 70, 1318–1324 (2006).

    Article  CAS  PubMed  Google Scholar 

  71. Foley, R. N., Herzog, C. A. & Collins, A. J. Blood pressure and long-term mortality in United States hemodialysis patients: USRDS Waves 3 and 4 Study1. Kidney Int. 62, 1784–1790 (2002).

    Article  PubMed  Google Scholar 

  72. Ishani, A., Herzog, C. A., Collins, A. L. & Foley, R. N. Cardiac medications and their association with cardiovascular events in incident dialysis patients: cause or effect? Kidney Int. 65, 1017–1025 (2004).

    Article  PubMed  Google Scholar 

  73. Todd, F. et al. Characteristics of treated hypertension in incident hemodialysis and peritoneal dialysis patients. Am. J. Kidney Dis. 42, 1260–1269 (2003).

    Article  Google Scholar 

  74. Van der Sman-de Beer, F. et al. NECOSAD Study Group: ACE I/D polymorphism is associated with mortality in a cohort study of patients starting with dialysis. Kidney Int. 68, 2237–2243 (2005).

    Article  CAS  PubMed  Google Scholar 

  75. Rocco, M. V., Cheung, A. K., Greene, T. & Eknoyan, G. The HEMO Study: applicability and generalizability. Nephrol. Dial. Transplant. 20, 278–284 (2005).

    Article  PubMed  Google Scholar 

  76. Culleton, B. F. et al. Effect of frequent nocturnal hemodialysis vs conventional hemodialysis on left ventricular mass and quality of life: a randomized controlled trial. JAMA 298, 1291–1299 (2007).

    Article  CAS  PubMed  Google Scholar 

  77. Davis, T. R. et al. Outcome of cardiac arrests attended by emergency medical services staff at community outpatient dialysis centers. Kidney Int. 73, 933–939 (2008).

    Article  CAS  PubMed  Google Scholar 

  78. Bloom, H. et al. Renal insufficiency and the risk of infection from pacemaker or defibrillator surgery. Pacing Clin. Electrophysiol. 29, 142–145 (2006).

    Article  PubMed  Google Scholar 

  79. Eckart, R. E., Gula, L. J., Reynolds, M. R., Shry, E. A. & Maisel, W. H. Mortality following defibrillator implantation in patients with renal insufficiency. J. Cardiovasc. Electrophysiol. 17, 940–943 (2006).

    Article  PubMed  PubMed Central  Google Scholar 

  80. Dasgupta, A. et al. Increased complication rates of cardiac rhythm management devices in ESRD patients. Am. J. Kidney Dis. 49, 656–663 (2007).

    Article  PubMed  Google Scholar 

  81. Hreybe, H. et al. Renal insufficiency predicts the time to first appropriate defibrillator shock. Am. Heart J. 151, 852–856 (2006).

    Article  PubMed  Google Scholar 

  82. Cuculic, P. et al. Poor prognosis for patients with chronic kidney disease despite ICD therapy for the primary prevention of sudden death. Pacing Clin. Electrophysiol. 30, 207–213 (2007).

    Article  Google Scholar 

  83. Amin, M. S. et al. Benefit of primary prevention implantable cardioverter-defibrillators in the setting of chronic kidney disease: a decision model analysis. J. Cardiovasc. Electrophysiol. 19, 1275–1280 (2008).

    Article  PubMed  Google Scholar 

  84. Sanders, G. D., Hlatky, M. A. & Owens, D. K. Cost-effectiveness of implantable cardioverter-defibrillators. N. Engl. J. Med. 353, 1471–1480 (2005).

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

C. P. Vega, University of California, Irvine, CA, is the author of and is solely responsible for the content of the learning objectives, questions and answers of the MedscapeCME-accredited continuing medical education activity associated with this article.

Author information

Authors and Affiliations

  1. Division of Nephrology, Memorial University of Newfoundland, Patient Research Centre, Health Science Centre, 300 Prince Phillip Drive, St John's, A1B 3V6, NL, Canada

    M. Khaled Shamseddin

  2. Patient Research Centre, Health Science Centre, 300 Prince Phillip Drive, St John's, A1B 3V6, NL, Canada

    Patrick S. Parfrey

Authors
  1. M. Khaled Shamseddin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Patrick S. Parfrey
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

M. K. Shamseddin and P. S. Parfrey contributed equally to all aspects of this manuscript.

Corresponding author

Correspondence to Patrick S. Parfrey.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Shamseddin, M., Parfrey, P. Sudden cardiac death in chronic kidney disease: epidemiology and prevention. Nat Rev Nephrol 7, 145–154 (2011). https://doi.org/10.1038/nrneph.2010.191

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrneph.2010.191

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing