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BioMed Research International
Volume 2013 (2013), Article ID 123589, 8 pages
http://dx.doi.org/10.1155/2013/123589
Review Article

Why Is Diabetes Mellitus a Risk Factor for Contrast-Induced Nephropathy?

1Department of Medicine, Hadassah Hospital, Mt. Scopus and the Hebrew University Medical School, P.O. Box 24035, Jerusalem 91240, Israel
2Department of Nephrology, Charité Campus Mitte, Berlin 10115, Germany
3Department of Pathology, Beth Israel Deaconess Medical Center and Harvard Medical School, Boston, MA 02215, USA
4Joslin Diabetes Center, Harvard Medical School, Boston, MA 02215, USA

Received 5 September 2013; Accepted 24 October 2013

Academic Editor: Michele Andreucci

Copyright © 2013 Samuel N. Heyman et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. S. N. Heyman, S. Rosen, M. Khamaisi, J. M. Idee, and C. Rosenberger, “Hypoxia, oxidative stress and the pathophysiology of contrast-media-induced nephropathy,” in Oxidative Stress in Basic Research and Clinical Practice: Studies on Renal Disorders, T. Miyata, K. W. Eckardt, and M. Nangaku, Eds., pp. 229–256, Humana Press/Springer Science, 2011.
  2. S. N. Heyman, S. Rosen, and C. Rosenberger, “Renal parenchymal hypoxia, hypoxia adaptation, and the pathogenesis of radiocontrast nephropathy,” Clinical Journal of the American Society of Nephrology, vol. 3, no. 1, pp. 288–296, 2008. View at Publisher · View at Google Scholar · View at Scopus
  3. S. N. Heyman, S. Rosen, M. Khamaisi, J. M. Idée, and C. Rosenberger, “Reactive oxygen species and the pathogenesis of radiocontrast-induced nephropathy,” Investigative Radiology, vol. 45, no. 4, pp. 188–195, 2010. View at Publisher · View at Google Scholar · View at Scopus
  4. R. Mehran, E. D. Aymong, E. Nikolsky et al., “A simple risk score for prediction of contrast-induced nephropathy after percutaneous coronary intervention: development and initial validation,” Journal of the American College of Cardiology, vol. 44, no. 7, pp. 1393–1399, 2004. View at Publisher · View at Google Scholar · View at Scopus
  5. P. A. McCullough, R. Wolyn, L. L. Rocher, R. N. Levin, and W. W. O'Neill, “Acute renal failure after coronary intervention: incidence, risk factors, and relationship to mortality,” American Journal of Medicine, vol. 103, no. 5, pp. 368–375, 1997. View at Publisher · View at Google Scholar · View at Scopus
  6. O. Toprak, M. Cirit, M. Yesil et al., “Impact of diabetic and pre-diabetic state on development of contrast-induced nephropathy in patients with chronic kidney disease,” Nephrology Dialysis Transplantation, vol. 22, no. 3, pp. 819–826, 2007. View at Publisher · View at Google Scholar · View at Scopus
  7. M. Brezis and S. Rosen, “Mechanisms of disease: hypoxia of the renal medulla—its implications for disease,” New England Journal of Medicine, vol. 332, no. 10, pp. 647–655, 1995. View at Publisher · View at Google Scholar · View at Scopus
  8. R. G. Evans, C. Ince, J. A. Joles et al., “Haemodynamic influences on kidney oxygenation: clinical implications of integrative physiology,” Clinical and Experimental Pharmacology and Physiology, vol. 40, no. 2, pp. 106–122, 2013. View at Publisher · View at Google Scholar
  9. M. Nangaku, C. Rosenberger, S. N. Heyman, and K. U. Eckardt, “HIF regulation in kidney disease,” Clinical and Experimental Pharmacology and Physiology, vol. 40, pp. 148–157, 2013. View at Publisher · View at Google Scholar
  10. C. Rosenberger, S. N. Heyman, S. Rosen et al., “Up-regulation of HIF in experimental acute renal failure: evidence for a protective transcriptional response to hypoxia,” Kidney International, vol. 67, no. 2, pp. 531–542, 2005. View at Publisher · View at Google Scholar · View at Scopus
  11. S. N. Heyman, R. Evans, S. Rosen, and C. Rosenberger, “Cellular adaptive changes in AKI: mitigating renal hypoxic injury,” Nephrology Dialysis Transplantation, vol. 27, no. 5, pp. 1721–1728, 2012. View at Publisher · View at Google Scholar
  12. S. N. Heyman, C. Rosenberger, and S. Rosen, “Acute kidney injury: lessons from experimental models,” Contributions to Nephrology, vol. 169, pp. 286–296, 2011. View at Publisher · View at Google Scholar · View at Scopus
  13. Y. Agmon, H. Peleg, Z. Greenfeld, S. Rosen, and M. Brezis, “Nitric oxide and prostanoids protect the renal outer medulla from radiocontrast toxicity in the rat,” Journal of Clinical Investigation, vol. 94, no. 3, pp. 1069–1075, 1994. View at Scopus
  14. G. Schley, N. Cordasic, B. Klanke, et al., “Evidence for primary endothelial cell injury and subsequent scarring in a mouse model of radiocontrast nephropathy,” in Proceedings of the American Society of Nephrology Annual Meeting, Atlanta, GA, USA, 2013.
  15. M. M. Sendeski, A. B. Persson, Z. Z. Liu et al., “Iodinated contrast media cause endothelial damage leading to vasoconstriction of human and rat vasa recta,” American Journal of Physiology—Renal Physiology, vol. 303, no. 12, pp. F1592–F1598, 2012. View at Publisher · View at Google Scholar
  16. M. Sendeski, A. Patzak, T. L. Pallone, C. Cao, A. E. Persson, and P. B. Persson, “Iodixanol, constriction of medullary descending vasa recta, and risk for contrast medium-induced nephropathy,” Radiology, vol. 251, no. 3, pp. 697–704, 2009. View at Publisher · View at Google Scholar · View at Scopus
  17. F. Palm, L. Nordquist, C. S. Wilcox, and P. Hansell, “Oxidative stress and hypoxia in the pathogenesis of diabetic nephropathy,” in Oxidative Stress in Basic Research and Clinical Practice: Studies on Renal Disorders, T. Miyata, K. W. Eckardt, and M. Nangaku, Eds., pp. 559–586, Humana Press/Springer Science, 2011.
  18. F. Palm, J. Cederberg, P. Hansell, P. Liss, and P. O. Carlsson, “Reactive oxygen species cause diabetes-induced decrease in renal oxygen tension,” Diabetologia, vol. 46, no. 8, pp. 1153–1160, 2003. View at Publisher · View at Google Scholar · View at Scopus
  19. M. Ries, F. Basseau, B. Tyndal et al., “Renal diffusion and BOLD MRI in experimental diabetic nephropathy,” Journal of Magnetic Resonance Imaging, vol. 17, no. 1, pp. 104–113, 2003. View at Publisher · View at Google Scholar · View at Scopus
  20. Y. Zhang, J. Wang, X. Yang et al., “The serial effect of iodinated contrast media on renal hemodynamics and oxygenation as evaluated by ASL and BOLD MRI,” Contrast Media & Molecular Imaging, vol. 7, no. 4, pp. 418–425, 2012. View at Publisher · View at Google Scholar
  21. C. Rosenberger, M. Khamaisi, Z. Abassi et al., “Adaptation to hypoxia in the diabetic rat kidney,” Kidney International, vol. 73, no. 1, pp. 34–42, 2008. View at Publisher · View at Google Scholar · View at Scopus
  22. V. Vallon, “The proximal tubule in the pathophysiology of the diabetic kidney,” American Journal of Physiology—Regulatory Integrative and Comparative Physiology, vol. 300, no. 5, pp. R1009–R1022, 2011. View at Publisher · View at Google Scholar · View at Scopus
  23. Y. Nechemia-Arbeli, M. Khamaisi, C. Rosenberger et al., “In vivo evidence suggesting reciprocal renal HIF-1 up-regulation and STAT3 activation in response to hypoxic and non-hypoxic stimuli,” Clinical and Experimental Pharmacology and Physiology, vol. 40, no. 2, pp. 262–272, 2013. View at Publisher · View at Google Scholar
  24. P. Hansell, W. J. Welch, R. C. Blantz, and F. Palm, “Determinants of kidney oxygen consumption and their relationship to tissue oxygen tension in diabetes and hypertension,” Clinical and Experimental Pharmacology and Physiology, vol. 40, no. 2, pp. 123–137, 2013. View at Publisher · View at Google Scholar
  25. M. Bak, K. Thomsen, T. Christiansen, and A. Flyvbjerg, “Renal enlargement precedes renal hyperfiltration in early experimental diabetes in rats,” Journal of the American Society of Nephrology, vol. 11, no. 7, pp. 1287–1292, 2000. View at Scopus
  26. F. H. Epstein, P. Silva, K. Spokes, M. Brezis, and S. Rosen, “Renal medullary Na-K-ATPase and hypoxic injury in perfused rat kidneys,” Kidney International, vol. 36, no. 5, pp. 768–772, 1989. View at Scopus
  27. S. N. Heyman, M. Brezis, C. A. Reubinoff et al., “Acute renal failure with selective medullary injury in the rat,” Journal of Clinical Investigation, vol. 82, no. 2, pp. 401–412, 1988. View at Scopus
  28. S. N. Heyman, M. Brezis, F. H. Epstein, K. Spokes, and S. Rosen, “Effect of glycine and hypertrophy on renal outer medullary hypoxic injury in ischemia reflow and contrast nephropathy,” American Journal of Kidney Diseases, vol. 19, no. 6, pp. 578–586, 1992. View at Scopus
  29. R. Juncos and J. L. Garvin, “Superoxide enhances Na-K-2Cl cotransporter activity in the thick ascending limb,” American Journal of Physiology—Renal Physiology, vol. 288, no. 5, pp. F982–F987, 2005. View at Publisher · View at Google Scholar · View at Scopus
  30. F. Palm, P. Hansell, G. Ronquist, A. Waldenström, P. Liss, and P. O. Carlsson, “Polyol-pathway-dependent disturbances in renal medullary metabolism in experimental insulin-deficient diabetes mellitus in rats,” Diabetologia, vol. 47, no. 7, pp. 1223–1231, 2004. View at Scopus
  31. R. G. Evans and S. M. Fitzgerald, “Nitric oxide and superoxide in the renal medulla: a delicate balancing act,” Current Opinion in Nephrology and Hypertension, vol. 14, no. 1, pp. 9–15, 2005. View at Publisher · View at Google Scholar · View at Scopus
  32. F. Palm, M. Friederich, P. O. Carlsson, P. Hansell, T. Teerlink, and P. Liss, “Reduced nitric oxide in diabetic kidneys due to increased hepatic arginine metabolism: implications for renomedullary oxygen availability,” American Journal of Physiology—Renal Physiology, vol. 294, no. 1, pp. F30–F37, 2008. View at Publisher · View at Google Scholar · View at Scopus
  33. S. N. Heyman, M. Goldfarb, F. Carmeli et al., “Effect of radiocontrast agents on intrarenal nitric oxide (NO) and NO synthase activity,” Experimental Nephrology, vol. 6, no. 6, pp. 557–562, 1998. View at Scopus
  34. S. N. Heyman, B. A. Clark, N. Kaiser et al., “Radiocontrast agents induce endothelin Release in vivo and in vitro,” Journal of the American Society of Nephrology, vol. 3, no. 1, pp. 58–65, 1992. View at Scopus
  35. B. A. Clark, D. Kim, and F. H. Epstein, “Endothelin and atrial natriuretic peptide levels following radiocontrast exposure in humans,” American Journal of Kidney Diseases, vol. 30, no. 1, pp. 82–86, 1997. View at Scopus
  36. M. Khamaisi, I. Raz, V. Shilo et al., “Diabetes and radiocontrast media increase endothelin converting enzyme-1 in the kidney,” Kidney International, vol. 74, no. 1, pp. 91–100, 2008. View at Publisher · View at Google Scholar · View at Scopus
  37. H. Ishii, D. Koya, and G. L. King, “Protein kinase C activation and its role in the development of vascular complications in diabetes mellitus,” Journal of Molecular Medicine, vol. 76, no. 1, pp. 21–31, 1998. View at Scopus
  38. M. Khamaisi, R. Dahan, S. Hamed, Z. Abassi, S. N. Heyman, and I. Raz, “Role of protein kinase C in the expression of endothelin converting enzyme-1,” Endocrinology, vol. 150, no. 3, pp. 1440–1449, 2009. View at Publisher · View at Google Scholar · View at Scopus
  39. M. Khamaisi, I. Mimura, H. Toukan, et al., “Endothelin converting enzyme (ECE)-1: a plausible target gene for hypoxia inducible factor (HIF),” in Proceedings of the American Society of Nephrology Annual Meeting, San Diego, CA, USA, 2012.
  40. V. Vallon, B. Mühlbauer, and H. Osswald, “Adenosine and kidney function,” Physiological Reviews, vol. 86, no. 3, pp. 901–940, 2006. View at Publisher · View at Google Scholar · View at Scopus
  41. D. Dinour and M. Brezis, “Effects of adenosine on intrarenal oxygenation,” American Journal of Physiology—Renal Fluid and Electrolyte Physiology, vol. 261, no. 5, pp. F787–F791, 1991. View at Scopus
  42. L. J. Arend, G. L. Bakris, J. C. Burnett Jr., C. Megerian, and W. S. Spielman, “Role for intrarenal adenosine in the renal hemodynamic response to contrast media,” Journal of Laboratory and Clinical Medicine, vol. 110, no. 4, pp. 406–411, 1987. View at Scopus
  43. R. E. Katholi, G. J. Taylor, W. P. McCann et al., “Nephrotoxicity from contrast media: attenuation with theophylline,” Radiology, vol. 195, no. 1, pp. 17–22, 1995. View at Scopus
  44. C. M. Erley, S. H. Duda, S. Schlepckow et al., “Adenosine antagonist theophylline prevents the reduction of glomerular filtration rate after contrast media application,” Kidney International, vol. 45, no. 5, pp. 1425–1431, 1994. View at Scopus
  45. C. M. Erley, N. Heyne, K. Burgert, J. Langanke, T. Risler, and H. Osswald, “Prevention of radiocontrast-induced nephropathy by adenosine antagonists in rats with chronic nitric oxide deficiency,” Journal of the American Society of Nephrology, vol. 8, no. 7, pp. 1125–1132, 1997. View at Scopus
  46. K. Yao, N. Heyne, C. M. Erley, T. Risler, and H. Osswald, “The selective adenosine A1 receptor antagonist KW-3902 prevents radiocontrast media-induced nephropathy in rats with chronic nitric oxide deficiency,” European Journal of Pharmacology, vol. 414, no. 1, pp. 99–104, 2001. View at Publisher · View at Google Scholar · View at Scopus
  47. A. Kapoor, S. Kumar, S. Gulati, S. Gambhir, R. S. Sethi, and N. Sinha, “The role of theophylline in contrast-induced nephropathy: a case-control study,” Nephrology Dialysis Transplantation, vol. 17, no. 11, pp. 1936–1941, 2002. View at Scopus
  48. W. Huber, C. Schipek, K. Ilgmann et al., “Effectiveness of theophylline prophylaxis of renal impairment after coronary angiography in patients with chronic renal insufficiency,” American Journal of Cardiology, vol. 91, no. 10, pp. 1157–1162, 2003. View at Publisher · View at Google Scholar · View at Scopus
  49. H. T. Lee, M. Jan, C. B. Soo et al., “A1 adenosine receptor knockout mice are protected against acute radiocontrast nephropathy in vivo,” American Journal of Physiology—Renal Physiology, vol. 290, no. 6, pp. F1367–F1375, 2006. View at Publisher · View at Google Scholar · View at Scopus
  50. L. Pihl, P. Persson, A. Fasching, P. Hansell, G. F. DiBona, and F. Palm, “Insulin induces the correlation between renal blood flow and glomerular filtration rate in diabetes: implications for mechanisms causing hyperfiltration,” American Journal of Physiology—Regulatory, Integrative and Comparative Physiology, vol. 303, no. 1, pp. R39–R47, 2012.
  51. T. Takenaka, T. Inoue, Y. Ohno et al., “Elucidating mechanisms underlying altered renal autoregulation in diabetes,” American Journal of Physiology—Regulatory Integrative and Comparative Physiology, vol. 303, no. 5, pp. R495–R504, 2012. View at Publisher · View at Google Scholar
  52. P. Persson, P. Hansell, and F. Palm, “Adenosine A2 receptor-mediated regulation of renal hemodynamics and glomerular filtration rate is abolished in diabetes,” Advances in Experimental Medicine and Biology, vol. 765, pp. 225–230, 2013. View at Publisher · View at Google Scholar
  53. A. C. Pflueger, F. Schenk, and H. Osswald, “Increased sensitivity of the renal vasculature to adenosine in streptozotocin-induced diabetes mellitus rats,” American Journal of Physiology—Renal Fluid and Electrolyte Physiology, vol. 269, no. 4, part 2, pp. F529–F535, 1995. View at Scopus
  54. A. C. Pflueger, J. M. Gross, and F. G. Knox, “Adenosine-induced renal vasoconstriction in diabetes mellitus rats: role of prostaglandins,” American Journal of Physiology—Regulatory Integrative and Comparative Physiology, vol. 277, no. 5, pp. R1410–R1417, 1999. View at Scopus
  55. A. C. Pflueger, H. Osswald, and F. G. Knox, “Adenosine-induced renal vasoconstriction in diabetes mellitus rats: role of nitric oxide,” American Journal of Physiology—Renal Physiology, vol. 276, no. 3, pp. F340–F346, 1999. View at Scopus
  56. F. Palm, P. O. Carlsson, P. Hansell, O. Hellberg, A. Nygren, and P. Liss, “Altered response in renal blood flow and oxygen tension to contrast media in diabetic rats,” Acta Radiologica, vol. 44, no. 3, pp. 347–353, 2003. View at Publisher · View at Google Scholar · View at Scopus
  57. L. S. Weisberg, P. B. Kurnik, and B. R. C. Kurnik, “Risk of radiocontrast nephropathy in patients with and without diabetes mellitus,” Kidney International, vol. 45, no. 1, pp. 259–265, 1994. View at Scopus
  58. C. Rosenberger, M. Khamaisi, M. Goldfarb et al., “Acute kidney injury in the diabetic rat: studies in the isolated perfused and intact kidney,” American Journal of Nephrology, vol. 28, no. 5, pp. 831–839, 2008. View at Publisher · View at Google Scholar · View at Scopus
  59. M. Goldfarb, C. Rosenberger, Z. Abassi et al., “Acute-on-chronic renal failure in the rat: functional compensation and hypoxia tolerance,” American Journal of Nephrology, vol. 26, no. 1, pp. 22–33, 2006. View at Publisher · View at Google Scholar · View at Scopus
  60. R. Hirsch, C. Dent, H. Pfriem et al., “NGAL is an early predictive biomarker of contrast-induced nephropathy in children,” Pediatric Nephrology, vol. 22, no. 12, pp. 2089–2095, 2007. View at Publisher · View at Google Scholar · View at Scopus
  61. B. R. C. Kurnik, R. L. Allgren, F. C. Center, R. J. Solomon, E. R. Bates, and L. S. Weisberg, “Prospective study of atrial natriuretic peptide for the prevention of radiocontrast-induced nephropathy,” American Journal of Kidney Diseases, vol. 31, no. 4, pp. 674–680, 1998. View at Scopus
  62. C. Briguori, G. Visconti, A. Focaccio et al., “Renal insufficiency after contrast media administration trial II (REMEDIAL II): renalguard system in high-risk patients for contrast-induced acute kidney injury,” Circulation, vol. 124, no. 11, pp. 1260–1269, 2011. View at Publisher · View at Google Scholar · View at Scopus
  63. P. Liss, P. O. Carlsson, F. Palm, and P. Hansell, “Adenosine A1 receptors in contrast media-induced renal dysfunction in the normal rat,” European Radiology, vol. 14, no. 7, pp. 1297–1302, 2004. View at Scopus
  64. P. Liss, P. O. Carlsson, A. Nygren, F. Palm, and P. Hansell, “ET-A receptor antagonist BQ123 prevents radiocontrast media-induced renal medullary hypoxia,” Acta Radiologica, vol. 44, no. 1, pp. 111–117, 2003. View at Publisher · View at Google Scholar · View at Scopus
  65. D. Andress, B. Coll, Y. Pritchett, J. Brennan, M. Molitch, and D. Kohan, “Clinical efficacy of the selective endothelin A receptor antagonist, atrasentan, in patients with diabetes and chronic kidney disease (CKD),” Life Sciences, vol. 91, no. 13-14, pp. 739–742, 2012. View at Publisher · View at Google Scholar · View at Scopus
  66. S. N. Heyman, M. Brezis, F. H. Epstein, K. Spokes, P. Silva, and S. Rosen, “Early renal medullary hypoxic injury from radiocontrast and indomethacin,” Kidney International, vol. 40, no. 4, pp. 632–642, 1991. View at Scopus
  67. S. N. Heyman, M. Brezis, Z. Greenfeld, and S. Rosen, “Protective role of furosemide and saline in radiocontrast-induced acute renal failure in the rat,” American Journal of Kidney Diseases, vol. 14, no. 5, pp. 377–385, 1989. View at Scopus
  68. D. Yang, S. Lin, D. Yang, L. Wei, and W. Shang, “Effects of short- and long-term hypercholesterolemia on contrast-induced acute kidney injury,” American Journal of Nephrology, vol. 35, no. 1, pp. 80–89, 2012. View at Publisher · View at Google Scholar · View at Scopus
  69. C. Quintavalle, D. Fiore, F. De Micco et al., “Impact of a high loading dose of atorvastatin on contrast-induced acute kidney injury,” Circulation, vol. 126, no. 25, pp. 3008–3016, 2012. View at Publisher · View at Google Scholar