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Cardiology Research and Practice
Volume 2012 (2012), Article ID 319432, 8 pages
http://dx.doi.org/10.1155/2012/319432
Review Article

Cardiovascular Risk in Chronic Kidney Disease: Role of the Sympathetic Nervous System

1Renal Division, Department of Medicine, Emory University School of Medicine, 1639 Pierce Drive, WMB 338, Atlanta, GA 30322, USA
2Research Service, Department of Veterans Affairs Medical Center, Decatur, GA 30033, USA

Received 19 May 2012; Accepted 24 June 2012

Academic Editor: Kazuko Masuo

Copyright © 2012 Jeanie Park. 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. A. S. Go, G. M. Chertow, D. Fan, C. E. McCulloch, and C. Y. Hsu, “Chronic kidney disease and the risks of death, cardiovascular events, and hospitalization,” New England Journal of Medicine, vol. 351, no. 13, pp. 1296–1305, 2004. View at Publisher · View at Google Scholar · View at Scopus
  2. K. Matsushita, M. van der Velde, B. C. Astor, M. Woodward, A. S. Levey, P. E. de Jong et al., “Association of estimated glomerular filtration rate and albuminuria with all-cause and cardiovascular mortality in general population cohorts: a collaborative meta-analysis,” The Lancet, vol. 375, no. 9731, pp. 2073–2081, 2010. View at Publisher · View at Google Scholar
  3. D. Rucker and M. Tonelli, “Cardiovascular risk and management in chronic kidney disease,” Nature Reviews Nephrology, vol. 5, no. 5, pp. 287–296, 2009. View at Publisher · View at Google Scholar · View at Scopus
  4. M. J. Sarnak, A. S. Levey, A. C. Schoolwerth et al., “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,” Hypertension, vol. 42, no. 5, pp. 1050–1065, 2003. View at Publisher · View at Google Scholar · View at Scopus
  5. C. P. Wen, T. Y. D. Cheng, M. K. Tsai et al., “All-cause mortality attributable to chronic kidney disease: a prospective cohort study based on 462 293 adults in Taiwan,” The Lancet, vol. 371, no. 9631, pp. 2173–2182, 2008. View at Publisher · View at Google Scholar · View at Scopus
  6. C. A. Herzog, R. W. Asinger, A. K. Berger et al., “Cardiovascular disease in chronic kidney disease. A clinical update from Kidney Disease: improving Global Outcomes (KDIGO),” Kidney International, vol. 80, no. 6, pp. 572–586, 2011. View at Publisher · View at Google Scholar · View at Scopus
  7. D. Green, P. R. Roberts, D. I. New, and P. A. Kalra, “Sudden cardiac death in hemodialysis patients: an in-depth review,” American Journal of Kidney Diseases, vol. 57, no. 6, pp. 921–929, 2011. View at Publisher · View at Google Scholar · View at Scopus
  8. J. Sosnov, D. Lessard, R. J. Goldberg, J. Yarzebski, and J. M. Gore, “Differential symptoms of acute myocardial infarction in patients with kidney disease: a community-wide perspective,” American Journal of Kidney Diseases, vol. 47, no. 3, pp. 378–384, 2006. View at Publisher · View at Google Scholar · View at Scopus
  9. P. Stenvinkel, J. J. Carrero, J. Axelsson, B. Lindholm, O. Heimbürger, and Z. Massy, “Emerging biomarkers for evaluating cardiovascular risk in the chronic kidney disease patient: how do new pieces fit into the uremic puzzle?” Clinical Journal of the American Society of Nephrology, vol. 3, no. 2, pp. 505–521, 2008. View at Publisher · View at Google Scholar · View at Scopus
  10. G. Grassi, F. Quarti-Trevano, G. Seravalle et al., “Early sympathetic activation in the initial clinical stages of chronic renal failure,” Hypertension, vol. 57, no. 4, pp. 846–851, 2011. View at Publisher · View at Google Scholar · View at Scopus
  11. I. H. H. T. Klein, G. Ligtenberg, J. Neumann, P. L. Oey, H. A. Koomans, and P. J. Blankestijn, “Sympathetic nerve activity is inappropriately increased in chronic renal disease,” Journal of the American Society of Nephrology, vol. 14, no. 12, pp. 3239–3244, 2003. View at Publisher · View at Google Scholar · View at Scopus
  12. J. A. Joles and H. A. Koomans, “Causes and consequences of increased sympathetic activity inrenal disease,” Hypertension, vol. 43, no. 4, pp. 699–706, 2004. View at Publisher · View at Google Scholar · View at Scopus
  13. R. L. Converse Jr., T. N. Jacobsen, R. D. Toto et al., “Sympathetic overactivity in patients with chronic renal failure,” New England Journal of Medicine, vol. 327, no. 27, pp. 1912–1918, 1992. View at Google Scholar · View at Scopus
  14. J. P. Fisher, C. N. Young, and P. J. Fadel, “Central sympathetic overactivity: maladies and mechanisms,” Autonomic Neuroscience, vol. 148, no. 1-2, pp. 5–15, 2009. View at Publisher · View at Google Scholar · View at Scopus
  15. P. G. A. Volders, “Novel insights into the role of the sympathetic nervous system in cardiac arrhythmogenesis,” Heart Rhythm, vol. 7, no. 12, pp. 1900–1906, 2010. View at Publisher · View at Google Scholar · View at Scopus
  16. C. Zoccali, F. Mallamaci, S. Parlongo et al., “Plasma norepinephrine predicts survival and incident cardiovascular events in patients with end-stage renal disease,” Circulation, vol. 105, no. 11, pp. 1354–1359, 2002. View at Publisher · View at Google Scholar · View at Scopus
  17. C. Zoccali, F. Mallamaci, G. Tripepi et al., “Norepinephrine and concentric hypertrophy in patients with end-stage renal disease,” Hypertension, vol. 40, no. 1, pp. 41–46, 2002. View at Publisher · View at Google Scholar · View at Scopus
  18. D. R. Seals and F. A. Dinenno, “Collateral damage: cardiovascular consequences of chronic sympathetic activation with human aging,” American Journal of Physiology, vol. 287, no. 5, pp. H1895–H1905, 2004. View at Publisher · View at Google Scholar · View at Scopus
  19. G. Grassi, G. Seravalle, R. Dell'Oro, and G. Mancia, “Sympathetic mechanisms, organ damage, and antihypertensive treatment,” Current Hypertension Reports, vol. 13, no. 4, pp. 303–308, 2011. View at Publisher · View at Google Scholar · View at Scopus
  20. K. Amann, L. C. Rump, A. Simonaviciene et al., “Effects of low dose sympathetic inhibition on glomerulosclerosis and albuminuria in subtotally nephrectomized rats,” Journal of the American Society of Nephrology, vol. 11, no. 8, pp. 1469–1478, 2000. View at Google Scholar · View at Scopus
  21. A. H. Nguyen, A. Garfinkel, D. O. Walter et al., “Dynamics of muscle sympathetic nerve activity in advanced heart failure patients,” American Journal of Physiology, vol. 271, no. 5, pp. H1962–H1969, 1996. View at Google Scholar · View at Scopus
  22. W. N. Leimbach, B. G. Wallin, and R. G. Victor, “Direct evidence from intraneural recordings for increased central sympathetic outflow in patients with heart failure,” Circulation, vol. 73, no. 5, pp. 913–919, 1986. View at Google Scholar · View at Scopus
  23. R. Fraga, F. G. Franco, F. Roveda et al., “Exercise training reduces sympathetic nerve activity in heart failure patients treated with carvedilol,” European Journal of Heart Failure, vol. 9, no. 6-7, pp. 630–636, 2007. View at Publisher · View at Google Scholar · View at Scopus
  24. M. B. Patel, J. M. Stewart, A. V. Loud et al., “Altered function and structure of the heart in dogs with chronic elevation in plasma norepinephrine,” Circulation, vol. 84, no. 5, pp. 2091–2100, 1991. View at Google Scholar · View at Scopus
  25. S. Perlini, G. Palladini, I. Ferrero et al., “Sympathectomy or doxazosin, but not propranolol, blunt myocardial interstitial fibrosis in pressure-overload hypertrophy,” Hypertension, vol. 46, no. 5, pp. 1213–1218, 2005. View at Publisher · View at Google Scholar · View at Scopus
  26. S. P. Levick, D. B. Murray, J. S. Janicki, and G. L. Brower, “Sympathetic nervous system modulation of inflammation and remodeling in the hypertensive heart,” Hypertension, vol. 55, no. 2, pp. 270–276, 2010. View at Publisher · View at Google Scholar · View at Scopus
  27. R. D. Bevan, “Trophic effects of peripheral adrenergic nerves on vascular structure,” Hypertension, vol. 6, no. 6, pp. I-19–I-26, 1984. View at Google Scholar · View at Scopus
  28. M. Failla, A. Grappiolo, G. Emanuelli et al., “Sympathetic tone restrains arterial distensibility of healthy and atherosclerotic subjects,” Journal of Hypertension, vol. 17, no. 8, pp. 1117–1123, 1999. View at Publisher · View at Google Scholar · View at Scopus
  29. T. Bleeke, H. Zhang, N. Madamanchi, C. Patterson, and J. E. Faber, “Catecholamine-induced vascular wall growth is dependent on generation of reactive oxygen species,” Circulation Research, vol. 94, no. 1, pp. 37–45, 2004. View at Publisher · View at Google Scholar · View at Scopus
  30. K. A. Jamerson, S. Julius, T. Gudbrandsson, O. Andersson, and D. O. Brant, “Reflex sympathetic activation induces acute insulin resistance in the human forearm,” Hypertension, vol. 21, no. 5, pp. 618–623, 1993. View at Google Scholar · View at Scopus
  31. P. G. Krespi, T. K. Makris, A. N. Hatzizacharias et al., “Moxonidine effect on microalbuminuria, thrombomodulin, and plasminogen activator inhibitor-1 levels in patients with essential hypertension,” Cardiovascular Drugs and Therapy, vol. 12, no. 5, pp. 463–467, 1998. View at Publisher · View at Google Scholar · View at Scopus
  32. K. Strojek, W. Grzeszczak, J. Górska, M. I. Leschinger, and E. Ritz, “Lowering of microalbuminuria in diabetic patients by a sympathicoplegic agent: novel approach to prevent progression of diabetic nephropathy?” Journal of the American Society of Nephrology, vol. 12, no. 3, pp. 602–605, 2001. View at Google Scholar · View at Scopus
  33. J. L. Cuche, J. Prinseau, and F. Selz, “Plasma free, sulfo- and glucuro-conjugated catecholamines in uremic patients,” Kidney International, vol. 30, no. 4, pp. 566–572, 1986. View at Google Scholar · View at Scopus
  34. A. N. Elias, N. D. Vaziri, and M. Maksy, “Plasma norepinephrine, epinephrine, and dopamine levels in end-stage renal disease. Effect of hemodialysis,” Archives of Internal Medicine, vol. 145, no. 6, pp. 1013–1015, 1985. View at Publisher · View at Google Scholar · View at Scopus
  35. G. Ligtenberg, P. J. Blankestijn, P. L. Oey et al., “Reduction of sympathetic hyperactivity by enalapril in patients with chronic renal failure,” New England Journal of Medicine, vol. 340, no. 17, pp. 1321–1328, 1999. View at Publisher · View at Google Scholar · View at Scopus
  36. J. Park, V. M. Campese, and H. R. Middlekauff, “Exercise pressor reflex in humans with end-stage renal disease,” American Journal of Physiology, vol. 295, no. 4, pp. R1188–R1194, 2008. View at Publisher · View at Google Scholar · View at Scopus
  37. J. Park, V. M. Campese, N. Nobakht, and H. R. Middlekauff, “Differential distribution of muscle and skin sympathetic nerve activity in patients with end-stage renal disease,” Journal of Applied Physiology, vol. 105, no. 6, pp. 1873–1876, 2008. View at Publisher · View at Google Scholar · View at Scopus
  38. I. H. H. T. Klein, G. Ligtenberg, P. L. Oey, H. A. Koomans, and P. J. Blankestijn, “Enalapril and losartan reduce sympathetic hyperactivity in patients with chronic renal failure,” Journal of the American Society of Nephrology, vol. 14, no. 2, pp. 425–430, 2003. View at Publisher · View at Google Scholar · View at Scopus
  39. V. M. Campese and E. Kogosov, “Renal afferent denervation prevents hypertension in rats with chronic renal failure,” Hypertension, vol. 25, no. 4, pp. 878–882, 1995. View at Google Scholar · View at Scopus
  40. V. M. Campese, E. Kogosov, and M. Koss, “Renal afferent denervation prevents the progression of renal disease in the renal ablation model of chronic renal failure in the rat,” American Journal of Kidney Diseases, vol. 26, no. 5, pp. 861–865, 1995. View at Google Scholar · View at Scopus
  41. S. Ye, B. Ozgur, and V. M. Campese, “Renal afferent impulses, the posterior hypothalamus, and hypertension in rats with chronic renal failure,” Kidney International, vol. 51, no. 3, pp. 722–727, 1997. View at Google Scholar · View at Scopus
  42. S. Ye, H. Zhong, and V. M. Campese, “Oxidative stress mediates the stimulation of sympathetic nerve activity in the phenol renal injury model of hypertension,” Hypertension, vol. 48, no. 2, pp. 309–315, 2006. View at Publisher · View at Google Scholar · View at Scopus
  43. S. Ye, H. Zhong, V. Yanamadala, and V. M. Campese, “Renal injury caused by intrarenal injection of phenol increases afferent and efferent renal sympathetic nerve activity,” American Journal of Hypertension, vol. 15, no. 8, pp. 717–724, 2002. View at Publisher · View at Google Scholar · View at Scopus
  44. I. H. H. T. Klein, G. Ligtenberg, P. L. Oey, H. A. Koomans, and P. J. Blankestijn, “Sympathetic activity is increased in polycystic kidney disease and is associated with hypertension,” Journal of the American Society of Nephrology, vol. 12, no. 11, pp. 2427–2433, 2001. View at Google Scholar · View at Scopus
  45. V. M. Campese, E. Ku, and J. Park, “Sympathetic renal innervation and resistant hypertension,” International Journal of Hypertension, vol. 2011, Article ID 814354, 2011. View at Google Scholar
  46. M. Hausberg, M. Kosch, P. Harmelink et al., “Sympathetic nerve activity in end-stage renal disease,” Circulation, vol. 106, no. 15, pp. 1974–1979, 2002. View at Publisher · View at Google Scholar · View at Scopus
  47. R. E. Katholi, P. L. Whitlow, G. R. Hageman, and W. T. Woods, “Intrarenal adenosine produces hypertension by activating the sympathetic nervous system via the renal nerves in the dog,” Journal of Hypertension, vol. 2, no. 4, pp. 349–359, 1984. View at Google Scholar · View at Scopus
  48. C. T. Bergamaschi, R. R. Campos, and O. U. Lopes, “Rostral ventrolateral medulla: a source of sympathetic activation in rats subjected to long-term treatment with L-NAME,” Hypertension, vol. 34, no. 4, pp. 744–747, 1999. View at Google Scholar · View at Scopus
  49. M. Sander, B. Chavoshan, and R. G. Victor, “A large blood pressure-raising effect of nitric oxide synthase inhibition in humans,” Hypertension, vol. 33, no. 4, pp. 937–942, 1999. View at Google Scholar · View at Scopus
  50. M. Sander and R. G. Victor, “Neural mechanisms in nitric-oxide-deficient hypertension,” Current Opinion in Nephrology and Hypertension, vol. 8, no. 1, pp. 61–73, 1999. View at Publisher · View at Google Scholar
  51. G. Grassi, G. Seravalle, L. Ghiadoni, G. Tripepi, R. M. Bruno, G. Mancia et al., “. Sympathetic nerve traffic and asymmetric dimethylarginine in chronic kidney disease,” Clinical Journal of the American Society of Nephrology, vol. 6, no. 11, pp. 2620–2627, 2011. View at Publisher · View at Google Scholar
  52. S. Ueda, S. I. Yamagishi, Y. Matsumoto, K. Fukami, and S. Okuda, “Asymmetric dimethylarginine (ADMA) is a novel emerging risk factor for cardiovascular disease and the development of renal injury in chronic kidney disease,” Clinical and Experimental Nephrology, vol. 11, no. 2, pp. 115–121, 2007. View at Publisher · View at Google Scholar · View at Scopus
  53. P. Vallance, A. Leone, A. Calver, J. Collier, and S. Moncada, “Accumulation of an endogenous inhibitor of nitric oxide synthesis in chronic renal failure,” The Lancet, vol. 339, no. 8793, pp. 572–575, 1992. View at Publisher · View at Google Scholar · View at Scopus
  54. C. Zoccali, “Asymmetric dimethylarginine in end-stage renal disease patients: a biomarker modifiable by calcium blockade and angiotensin II antagonism?” Kidney International, vol. 70, no. 12, pp. 2053–2055, 2006. View at Publisher · View at Google Scholar · View at Scopus
  55. C. Zoccali, “Asymmetric dimethylarginine (ADMA): a cardiovascular and renal risk factor on the move,” Journal of Hypertension, vol. 24, no. 4, pp. 611–619, 2006. View at Publisher · View at Google Scholar · View at Scopus
  56. F. Mallamaci, G. Tripepi, R. Maas, L. Malatino, R. Böger, and C. Zoccali, “Analysis of the Relationship between Norepinephrine and Asymmetric Dimethyl Arginine Levels among Patients with End-Stage Renal Disease,” Journal of the American Society of Nephrology, vol. 15, no. 2, pp. 435–441, 2004. View at Publisher · View at Google Scholar · View at Scopus
  57. R. H. Böger and C. Zoccali, “ADMA: a novel risk factor that explains excess cardiovascular event rate in patients with end-stage renal disease,” Atherosclerosis Supplements, vol. 4, no. 4, pp. 23–28, 2003. View at Publisher · View at Google Scholar · View at Scopus
  58. R. A. Augustyniak, R. G. Victor, D. A. Morgan, and W. Zhang, “L-NAME- and ADMA-induced sympathetic neural activation in conscious rats,” American Journal of Physiology, vol. 290, no. 3, pp. R726–R732, 2006. View at Publisher · View at Google Scholar · View at Scopus
  59. C. Zoccali, F. Mallamaci, R. Maas et al., “Left ventricular hypertrophy, cardiac remodeling and asymmetric dimethylarginine (ADMA) in hemodialysis patients,” Kidney International, vol. 62, no. 1, pp. 339–345, 2002. View at Publisher · View at Google Scholar · View at Scopus
  60. C. Zoccali, F. A. Benedetto, R. Maas et al., “Asymmetric dimethylarginine, C-reactive protein, and carotid intima-media thickness in end-stage renal disease,” Journal of the American Society of Nephrology, vol. 13, no. 2, pp. 490–496, 2002. View at Google Scholar · View at Scopus
  61. C. Zoccali, S. M. Bode-Böger, F. Mallamaci et al., “Plasma concentration of asymmetrical dimethylarginine and mortality in patients with end-stage renal disease: a prospective study,” The Lancet, vol. 358, no. 9299, pp. 2113–2117, 2001. View at Publisher · View at Google Scholar · View at Scopus
  62. S. Cottone, M. C. Lorito, R. Riccobene et al., “Oxidative stress, inflammation and cardiovascular disease in chronic renal failure,” Journal of Nephrology, vol. 21, no. 2, pp. 175–179, 2008. View at Google Scholar · View at Scopus
  63. S. V. Shah, R. Baliga, M. Rajapurkar, and V. A. Fonseca, “Oxidants in chronic kidney disease,” Journal of the American Society of Nephrology, vol. 18, no. 1, pp. 16–28, 2007. View at Publisher · View at Google Scholar · View at Scopus
  64. E. L. Schiffrin, M. L. Lipman, and J. F. E. Mann, “Chronic kidney disease: effects on the cardiovascular system,” Circulation, vol. 116, no. 1, pp. 85–97, 2007. View at Publisher · View at Google Scholar · View at Scopus
  65. V. M. Campese, S. Ye, H. Zhong, V. Yanamadala, Z. Ye, and J. Chiu, “Reactive oxygen species stimulate central and peripheral sympathetic nervous system activity,” American Journal of Physiology, vol. 287, no. 2, pp. H695–H703, 2004. View at Publisher · View at Google Scholar · View at Scopus
  66. Y. Hirooka, “Oxidative stress in the cardiovascular center has a pivotal role in the sympathetic activation in hypertension,” Hypertension Research, vol. 34, no. 4, pp. 407–412, 2011. View at Publisher · View at Google Scholar · View at Scopus
  67. M. Fujita, K. Ando, A. Nagae, and T. Fujita, “Sympathoexcitation by oxidative stress in the brain mediates arterial pressure elevation in salt-sensitive hypertension,” Hypertension, vol. 50, no. 2, pp. 360–367, 2007. View at Publisher · View at Google Scholar · View at Scopus
  68. E. B. Oliveira-Sales, A. P. Dugaich, B. A. Carillo et al., “Oxidative stress contributes to renovascular hypertension,” American Journal of Hypertension, vol. 21, no. 1, pp. 98–104, 2008. View at Publisher · View at Google Scholar · View at Scopus
  69. M. Fujita, K. Ando, H. Kawarazaki, C. Kawarasaki, K. Muraoka, H. Ohtsu et al., “Sympathoexcitation by brain oxidative stress mediates arterial pressure elevation in salt-induced chronic kidney disease,” Hypertension, vol. 59, no. 1, pp. 105–112, 2012. View at Publisher · View at Google Scholar
  70. H. Macarthur, T. C. Westfall, and G. H. Wilken, “Oxidative stress attenuates NO-induced modulation of sympathetic neurotransmission in the mesenteric arterial bed of spontaneously hypertensive rats,” American Journal of Physiology, vol. 294, no. 1, pp. H183–H189, 2008. View at Publisher · View at Google Scholar · View at Scopus
  71. I. A. Reid, “Interactions between ANG II, sympathetic nervous system, and baroreceptor reflexes in regulation of blood pressure,” American Journal of Physiology, vol. 262, no. 6, pp. E763–E778, 1992. View at Google Scholar · View at Scopus
  72. T. Matsukawa, E. Gotoh, K. Minamisawa et al., “Effects of intravenous infusions of angiotensin II on muscle sympathetic nerve activity in humans,” American Journal of Physiology, vol. 261, no. 3, pp. R690–R696, 1991. View at Google Scholar · View at Scopus
  73. L. Siddiqi, P. L. Oey, and P. J. Blankestijn, “Aliskiren reduces sympathetic nerve activity and blood pressure in chronic kidney disease patients,” Nephrology Dialysis Transplantation, vol. 26, no. 9, pp. 2930–2934, 2011. View at Publisher · View at Google Scholar
  74. N. Tangri, S. Shastri, H. Tighiouart, G. J. Beck, A. K. Cheung, G. Eknoyan et al., “beta-Blockers for prevention of sudden cardiac death in patients on hemodialysis: a propensity score analysis of the HEMO Study,” American Journal of Kidney Diseases, vol. 58, no. 6, pp. 939–945, 2011. View at Publisher · View at Google Scholar
  75. G. L. Bakris, P. Hart, and E. Ritz, “Beta blockers in the management of chronic kidney disease,” Kidney International, vol. 70, no. 11, pp. 1905–1913, 2006. View at Publisher · View at Google Scholar · View at Scopus
  76. L. Siddiqi, J. A. Joles, P. L. Oey, and P. J. Blankestijn, “Atorvastatin reduces sympathetic activity in patients with chronic kidney disease,” Journal of Hypertension, vol. 29, no. 11, pp. 2176–2180, 2011. View at Publisher · View at Google Scholar
  77. O. Zilch, P. F. Vos, P. L. Oey et al., “Sympathetic hyperactivity in haemodialysis patients is reduced by short daily haemodialysis,” Journal of Hypertension, vol. 25, no. 6, pp. 1285–1289, 2007. View at Publisher · View at Google Scholar · View at Scopus
  78. O. Friedman, T. D. Bradley, C. T. Chan, R. Parkes, and A. G. Logan, “Relationship between overnight rostral fluid shift and obstructive sleep apnea in drug-resistant hypertension,” Hypertension, vol. 56, no. 6, pp. 1077–1082, 2010. View at Publisher · View at Google Scholar · View at Scopus
  79. T. Dudenbostel and D. A. Calhoun, “Resistant hypertension, obstructive sleep apnoea and aldosterone,” Journal of Human Hypertension, vol. 26, no. 5, pp. 281–287, 2012. View at Publisher · View at Google Scholar · View at Scopus
  80. G. Grassi, A. Facchini, F. Q. Trevano et al., “Obstructive sleep apnea-dependent and -independent adrenergic activation in obesity,” Hypertension, vol. 46, no. 2, pp. 321–325, 2005. View at Publisher · View at Google Scholar · View at Scopus
  81. K. Narkiewicz, P. J. H. Van De Borne, R. L. Cooley, M. E. Dyken, and V. K. Somers, “Sympathetic activity in obese subjects with and without obstructive sleep apnea,” Circulation, vol. 98, no. 8, pp. 772–776, 1998. View at Google Scholar · View at Scopus
  82. K. Narkiewicz, P. J. H. Van De Borne, N. Montano, M. E. Dyken, B. G. Phillips, and V. K. Somers, “Contribution of tonic chemoreflex activation to sympathetic activity and blood pressure in patients with obstructive sleep apnea,” Circulation, vol. 97, no. 10, pp. 943–945, 1998. View at Google Scholar · View at Scopus
  83. K. Abdel-Kader, S. Dohar, N. Shah, M. Jhamb, S. E. Reis, P. Strollo et al., “Resistant hypertension and obstructive sleep apnea in the setting of kidney disease,” Journal of Hypertension, vol. 30, no. 5, pp. 960–966, 2012. View at Publisher · View at Google Scholar
  84. M. D. Esler, H. Krum, P. A. Sobotka et al., “Renal sympathetic denervation in patients with treatment-resistant hypertension (The Symplicity HTN-2 Trial): a randomised controlled trial,” The Lancet, vol. 376, no. 9756, pp. 1903–1909, 2010. View at Publisher · View at Google Scholar · View at Scopus
  85. M. P. Schlaich, D. Hering, P. Sobotka, H. Krum, G. W. Lambert, E. Lambert et al., “Effects of renal denervation on sympathetic activation, blood pressure, and glucose metabolism in patients with resistant hypertension,” Frontiers in Physiology, vol. 3, artilce 10, 2012. View at Google Scholar
  86. M. P. Schlaich, P. A. Sobotka, H. Krum, E. Lambert, and M. D. Esler, “Renal sympathetic-nerve ablation for uncontrolled hypertension,” New England Journal of Medicine, vol. 361, no. 9, pp. 932–934, 2009. View at Publisher · View at Google Scholar · View at Scopus
  87. G. Grassi, R. Dell'Oro, G. Seravalle, G. Foglia, F. Q. Trevano, and G. Mancia, “Short- and long-term neuroadrenergic effects of moderate dietary sodium restriction in essential hypertension,” Circulation, vol. 106, no. 15, pp. 1957–1961, 2002. View at Publisher · View at Google Scholar · View at Scopus
  88. F. Roveda, H. R. Middlekauff, M. U. P. B. Rondon et al., “The effects of exercise training on sympathetic neural activation in advanced heart failure: a randomized controlled trial,” Journal of the American College of Cardiology, vol. 42, no. 5, pp. 854–860, 2003. View at Publisher · View at Google Scholar · View at Scopus
  89. P. E. Pergola, P. Raskin, R. D. Toto et al., “Bardoxolone methyl and kidney function in CKD with type 2 diabetes,” New England Journal of Medicine, vol. 365, no. 4, pp. 327–336, 2011. View at Publisher · View at Google Scholar · View at Scopus