Novel targets for sepsis-induced kidney injury: The glomerular arterioles and the sympathetic nervous system

Experimental Physiology

Volumn 97, Issue 11, 2012, Pages 1168-1177

  May, Clive N ^a   Calzavacca, Paolo ^a   Ishikawa, Ken ^a   Langenberg, Christoph ^a   Wan, Li ^a   Ramchandra, Rohit ^a   Bellomo, Rinaldo ^b  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b AUSTIN HEALTH   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84868142108     PISSN: 09580670     EISSN: 1469445X     Source Type: Journal    
DOI: 10.1113/expphysiol.2011.061804     Document Type: Review

References (84)

1. Abboud FM, Harwani SC & Chapleau MW (2012). Autonomic neural regulation of the immune system: implications for hypertension and cardiovascular disease. Hypertension 59, 755-762.
2. 1-adrenoceptor blockade in severe sepsis in rats. Crit Care Med 38, 388-394.
3. Angus DC, Linde-Zwirble WT, Lidicker J, Clermont G, Carcillo J & Pinsky MR (2001). Epidemiology of severe sepsis in the United States: analysis of incidence, outcome, and associated costs of care. Crit Care Med 29, 1303-1310.
4. Aninat C, Seguin P, Descheemaeker PN, Morel F, Malledant Y & Guillouzo A (2008). Catecholamines induce an inflammatory response in human hepatocytes. Crit Care Med 36, 848-854.
5. Annane D, Sanquer S, Sebille V, Faye A, Djuranovic D, Raphael JC, Gajdos P & Bellissant E (2000). Compartmentalised inducible nitric-oxide synthase activity in septic shock. Lancet 355, 1143-1148.
6. Bagshaw SM, George C & Bellomo R (2008). Early acute kidney injury and sepsis: a multicentre evaluation. Crit Care 12, R47.
7. Bellomo R, Chapman M, Finfer S, Hickling K & Myburgh J (2000). Low-dose dopamine in patients with early renal dysfunction: a placebo-controlled randomised trial. Australian and New Zealand Intensive Care Society (ANZICS) Clinical Trials Group. Lancet 356, 2139-2143.
8. Benes J, Chvojka J, Sykora R, Radej J, Krouzecky A, Novak I & Matejovic M (2011). Searching for mechanisms that matter in early septic acute kidney injury: an experimental study. Crit Care 15, R256.
9. Berk JL, Hagen JF, Maly G & Koo R (1972). The treatment of shock with beta adrenergic blockade. Arch Surg 104, 46-51.
10. Borovikova LV, Ivanova S, Zhang M, Yang H, Botchkina GI, Watkins LR, Wang H, Abumrad N, Eaton JW & Tracey KJ (2000). Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin. Nature 405, 458-462.
11. Brenner M, Schaer GL, Mallory DL, Suffredini AF & Parrillo JE (1990). Detection of renal blood flow abnormalities in septic and critically ill patients using a newly designed indwelling thermodilution renal vein catheter. Chest 98, 170-179.
12. Breuhaus BA, Demarest KT & Chimoskey JE (1989). Comparison of intracerebroventricular and intracarotid infusions of PGE2 in conscious sheep. Am J Physiol 256, R685-R693.
13. Briest W, Hölzl A, Rassler B, Deten A, Leicht M, Baba HA & Zimmer HG (2001). Cardiac remodeling after long term norepinephrine treatment in rats. Cardiovasc Res 52, 265-273.
14. Cauwels A (2007). Nitric oxide in shock. Kidney Int 72, 557-565.
15. Cheyuo C, Jacob A & Wang P (2012). Ghrelin-mediated sympathoinhibition and suppression of inflammation in sepsis. Am J Physiol Endocrinol Metab 302, E265-E272.
16. Chvojka J, Sykora R, Krouzecky A, Radej J, Varnerova V, Karvunidis T, Hes O, Novak I, Radermacher P & Matejovic M (2008). Renal haemodynamic, microcirculatory, metabolic and histopathological responses to peritonitis-induced septic shock in pigs. Crit Care 12, R164.
17. Denton KM, Anderson WP & Sinniah R (2000). Effects of angiotensin II on regional afferent and efferent arteriole dimensions and the glomerular pole. Am J Physiol Regul Integr Comp Physiol 279, R629-R638.
18. Denton KM, Fennessy PA, Alcorn D & Anderson WP (1992). Morphometric analysis of the actions of angiotensin II on renal arterioles and glomeruli. Am J Physiol 262, F367-F372.
19. Denton KM, Shweta A, Flower RL & Anderson WP (2004). Predominant postglomerular vascular resistance response to reflex renal sympathetic nerve activation during ANG II clamp in rabbits. Am J Physiol Regul Integr Comp Physiol 287, R780-R786.
20. Di Giantomasso D, May CN & Bellomo R (2003a). Norepinephrine and vital organ blood flow during experimental hyperdynamic sepsis. Intensive Care Med 29, 1774-1781.
21. Di Giantomasso D, May CN & Bellomo R (2003b). Vital organ blood flow during hyperdynamic sepsis. Chest 124, 1053-1059.
22. Di Giantomasso D, Morimatsu H, Bellomo R & May CN (2006). Effect of low-dose vasopressin infusion on vital organ blood flow in the conscious normal and septic sheep. Anaesth Intensive Care 34, 427-433.
23. Dunser MW & Hasibeder WR (2009). Sympathetic overstimulation during critical illness: adverse effects of adrenergic stress. J Intensive Care Med 24, 293-316.
24. Elmquist JK, Scammell TE & Saper CB (1997). Mechanisms of CNS response to systemic immune challenge: the febrile response. Trends Neurosci 20, 565-570.
25. Esmon CT (2004). Why do animal models (sometimes) fail to mimic human sepsis? Crit Care Med 32, S219-S222.
26. Fenhammar J, Rundgren M, Forestier J, Kalman S, Eriksson S & Frithiof R (2011). Toll-like receptor 4 inhibitor TAK-242 attenuates acute kidney injury in endotoxemic sheep. Anesthesiology 114, 1130-1137.
27. Francis J, Weiss RM, Wei SG, Johnson AK, Beltz TG, Zimmerman K & Felder RB (2001). Central mineralocorticoid receptor blockade improves volume regulation and reduces sympathetic drive in heart failure. Am J Physiol Heart Circ Physiol 281, H2241-H2251.
28. Gaillard PJ, de Boer AB & Breimer DD (2003). Pharmacological investigations on lipopolysaccharide-induced permeability changes in the blood-brain barrier in vitro. Microvasc Res 65, 24-31.
29. Groeneveld AB & Sipkema P (2000). Interaction of oxyradicals, antioxidants, and nitric oxide during sepsis. Crit Care Med 28, 2161-2162.
30. Groves AC, Griffiths J, Leung F & Meek RN (1973). Plasma catecholamines in patients with serious postoperative infection. Ann Surg 178, 102-107.
31. Herndon DN, Hart DW, Wolf SE, Chinkes DL & Wolfe RR (2001). Reversal of catabolism by beta-blockade after severe burns. N Engl J Med 345, 1223-1229.
32. Hofer S, Steppan J, Wagner T, Funke B, Lichtenstern C, Martin E, Graf BM, Bierhaus A & Weigand MA (2009). Central sympatholytics prolong survival in experimental sepsis. Crit Care 13, R11.
33. Hotchkiss RS, Coopersmith CM, McDunn JE & Ferguson TA (2009). The sepsis seesaw: tilting toward immunosuppression. Nat Med 15, 496-497.
34. Ishikawa K, Bellomo R & May CN (2011). The impact of intrarenal nitric oxide synthase inhibition on renal blood flow and function in mild and severe hyperdynamic sepsis. Crit Care Med 39, 770-776.
35. Ishikawa K, Calzavacca P, Bellomo R, Bailey M & May CN (2012a). Effect of selective inhibition of renal inducible nitric oxide synthase on renal blood flow and function in experimental hyperdynamic sepsis. Crit Care Med (In Press).
36. Ishikawa K, Wan L, Calzavacca P, Bellomo R, Bailey M & May CN (2012b). The effects of terlipressin on regional hemodynamics and kidney function in experimental hyperdynamic sepsis. PLoS One 7, e29693.
37. Kanoore Edul VS, Dubin A & Ince C (2011). The microcirculation as a therapeutic target in the treatment of sepsis and shock. Semin Respir Crit Care Med 32, 558-568.
38. Kaye DM, Lefkovits J, Jennings GL, Bergin P, Broughton A & Esler MD (1995). Adverse consequences of high sympathetic nervous activity in the failing human heart. J Am Coll Cardiol 26, 1257-1263.
39. Kim MH & Hahn TH (2000). The effect of clonidine pretreatment on the perioperative proinflammatory cytokines, cortisol, and ACTH responses in patients undergoing total abdominal hysterectomy. Anesth Analg 90, 1441-1444.
40. Koo DJ, Chaudry IH & Wang P (1999). Kupffer cells are responsible for producing inflammatory cytokines and hepatocellular dysfunction during early sepsis. J Surg Res 83, 151-157.
41. Landmann R (1992). Beta-adrenergic receptors in human leukocyte subpopulations. Eur J Clin Invest 22(Suppl 1), 30-36.
42. Langenberg C, Bagshaw SM, May CN & Bellomo R (2008). The histopathology of septic acute kidney injury: a systematic review. Crit Care 12, R38.
43. Langenberg C, Bellomo R, May C, Wan L, Egi M & Morgera S (2005). Renal blood flow in sepsis. Crit Care 9, R363-R374.
44. Langenberg C, Bellomo R, May CN, Egi M, Wan L & Morgera S (2006a). Renal vascular resistance in sepsis. Nephron Physiol 104, p1-p11.
45. Langenberg C, Wan L, Egi M, May CN & Bellomo R (2006b). Renal blood flow in experimental septic acute renal failure. Kidney Int 69, 1996-2002.
46. Langenberg C, Wan L, Egi M, May CN & Bellomo R (2007). Renal blood flow and function during recovery from experimental septic acute kidney injury. Intensive Care Med 33, 1614-1618.
47. Levy MM, Fink MP, Marshall JC, Abraham E, Angus D, Cook D, Cohen J, Opal SM, Vincent JL & Ramsay G (2003). 2001 SCCM/ESICM/ACCP/ATS/SIS International Sepsis Definitions Conference. Crit Care Med 31, 1250-1256.
48. Liang C, Rounds NK, Dong E, Stevens SY, Shite J & Qin F (2000). Alterations by norepinephrine of cardiac sympathetic nerve terminal function and myocardial β-adrenergic receptor sensitivity in the ferret: normalization by antioxidant vitamins. Circulation 102, 96-103.
49. López A, Lorente JA, Steingrub J, Bakker J, McLuckie A, Willatts S, Brockway M, Anzueto A, Holzapfel L, Breen D, Silverman MS, Takala J, Donaldson J, Arneson C, Grove G, Grossman S & Grover R (2004). Multiple-center, randomized, placebo-controlled, double-blind study of the nitric oxide synthase inhibitor 546C88: effect on survival in patients with septic shock. Crit Care Med 32, 21-30.
50. Lucas CE, Rector FE, Werner M & Rosenberg IK (1973). Altered renal homeostasis with acute sepsis. Clinical significance. Arch Surg 106, 444-449.
51. MacNeil BJ, Jansen AH, Janz LJ, Greenberg AH & Nance DM (1997). Peripheral endotoxin increases splenic sympathetic nerve activity via central prostaglandin synthesis. Am J Physiol 273, R609-R614.
52. May CN, Ishikawa K, Wan L, Williams J, Wellard RM, Pell GS, Jackson GD & Bellomo R (2012). Renal bioenergetics during early gram-negative mammalian sepsis and angiotensin II infusion. Intensive Care Med 38, 886-893.
53. Miksa M, Wu R, Zhou M & Wang P (2005). Sympathetic excitotoxicity in sepsis: pro-inflammatory priming of macrophages by norepinephrine. Front Biosci 10, 2217-2229.
54. Morelli A, Rocco M, Conti G, Orecchioni A, De Gaetano A, Cortese G, Coluzzi F, Vernaglione E, Pelaia P & Pietropaoli P (2004). Effects of terlipressin on systemic and regional haemodynamics in catecholamine-treated hyperkinetic septic shock. Intensive Care Med 30, 597-604.
55. Mori T, Shimizu T & Tani T (2010). Septic acute renal failure. Contrib Nephrol 166, 40-46.
56. Nance DM & Sanders VM (2007). Autonomic innervation and regulation of the immune system (1987-2007). Brain Behav Immun 21, 736-745.
57. 2 is mediated by the brain but does not require afferent vagal signaling. Am J Physiol Regul Integr Comp Physiol 294, R1294-R1303.
58. Palsson J, Ricksten SE, Delle M & Lundin S (1988). Changes in renal sympathetic nerve activity during experimental septic and endotoxin shock in conscious rats. Circ Shock 24, 133-141.
59. Pandharipande PP, Sanders RD, Girard TD, McGrane S, Thompson JL, Shintani AK, Herr DL, Maze M & Ely EW (2010). Effect of dexmedetomidine versus lorazepam on outcome in patients with sepsis: an a priori-designed analysis of the MENDS randomized controlled trial. Crit Care 14, R38.
60. Patel BM, Chittock DR, Russell JA & Walley KR (2002). Beneficial effects of short-term vasopressin infusion during severe septic shock. Anesthesiology 96, 576-582.
61. Pichot C, Géloën A, Ghignone M & Quintin L (2010a). Alpha-2 agonists to reduce vasopressor requirements in septic shock? Med Hypotheses 75, 652-656.
62. Pichot C, Mathern P, Khettab F, Ghignone M, Geloen A & Quintin L (2010b). Increased pressor response to noradrenaline during septic shock following clonidine? Anaesth Intensive Care 38, 784-785.
63. Poli-de-Figueiredo LF, Garrido AG, Nakagawa N & Sannomiya P (2008). Experimental models of sepsis and their clinical relevance. Shock 30(Suppl 1), 53-59.
64. Ramchandra R, Wan L, Hood SG, Frithiof R, Bellomo R & May CN (2009). Septic shock induces distinct changes in sympathetic nerve activity to the heart and kidney in conscious sheep. Am J Physiol Regul Integr Comp Physiol 297, R1247-R1253.
65. Rector F, Goyal S, Rosenberg IK & Lucas CE (1973). Sepsis: a mechanism for vasodilatation in the kidney. Ann Surg 178, 222-226.
66. Riedel W, Kozawa E & Iriki M (1982). Renal and cutaneous vasomotor and respiratory rate adjustments to peripheral cold and warm stimuli and to bacterial endotoxin in conscious rabbits. J Auton Nerv Syst 5, 177-194.
67. Rittirsch D, Hoesel LM & Ward PA (2007). The disconnect between animal models of sepsis and human sepsis. J Leukoc Biol 81, 137-143.
68. 2 Adrenoreceptor blockade attenuates the hyperinflammatory response induced by traumatic injury. Surgery 145, 235-242.
69. Sakr Y, Reinhart K, Vincent JL, Sprung CL, Moreno R, Ranieri VM, De Backer D & Payen D (2006). Does dopamine administration in shock influence outcome? Results of the Sepsis Occurrence in Acutely Ill Patients (SOAP) Study. Crit Care Med 34, 589-597.
70. 1-adrenergic receptors and circulatory failure during CLP-induced sepsis. Shock 32, 239-246.
71. Schmittinger CA, Wurzinger B, Deutinger M, Wohlmuth C, Knotzer H, Torgersen C, Dünser MW & Hasibeder WR (2009). How to protect the heart in septic shock: a hypothesis on the pathophysiology and treatment of septic heart failure. Med Hypotheses 74, 460.
72. Schmitz D, Wilsenack K, Lendemanns S, Schedlowski M & Oberbeck R (2007). β-Adrenergic blockade during systemic inflammation: impact on cellular immune functions and survival in a murine model of sepsis. Resuscitation 72, 286-294.
73. Schrier RW & Wang W (2004). Acute renal failure and sepsis. N Engl J Med 351, 159-169.
74. Shimizu S, Akiyama T, Kawada T, Sonobe T, Kamiya A, Shishido T, Tokudome T, Hosoda H, Shirai M, Kangawa K & Sugimachi M (2011). Centrally administered ghrelin activates cardiac vagal nerve in anesthetized rabbits. Auton Neurosci 162, 60-65.
75. Strand OA, Leone A, Giercksky KE & Kirkeboen KA (2000). Nitric oxide indices in human septic shock. Crit Care Med 28, 2779-2785.
76. Suzuki T, Morisaki H, Serita R, Yamamoto M, Kotake Y, Ishizaka A & Takeda J (2005). Infusion of the β-adrenergic blocker esmolol attenuates myocardial dysfunction in septic rats. Crit Care Med 33, 2294-2301.
77. Taniguchi T, Kidani Y, Kanakura H, Takemoto Y & Yamamoto K (2004). Effects of dexmedetomidine on mortality rate and inflammatory responses to endotoxin-induced shock in rats. Crit Care Med 32, 1322-1326.
78. Vayssettes-Courchay C, Bouysset F & Verbeuren TJ (2005). Sympathetic activation and tachycardia in lipopolysaccharide treated rats are temporally correlated and unrelated to the baroreflex. Auton Neurosci 120, 35-45.
79. Wan L, Langenberg C, Bellomo R & May CN (2009). Angiotensin II in experimental hyperdynamic sepsis. Crit Care 13, R190.
80. Wang JF, Meissner A, Malek S, Chen Y, Ke Q, Zhang J, Chu V, Hampton TG, Crumpacker CS, Abelmann WH, Amende I & Morgan JP (2005). Propranolol ameliorates and epinephrine exacerbates progression of acute and chronic viral myocarditis. Am J Physiol Heart Circ Physiol 289, H1577-H1583.
81. Warren HS, Fitting C, Hoff E, Adib-Conquy M, Beasley-Topliffe L, Tesini B, Liang X, Valentine C, Hellman J, Hayden D & Cavaillon JM (2010). Resilience to bacterial infection: difference between species could be due to proteins in serum. J Infect Dis 201, 223-232.
82. Wu R, Dong W, Zhou M, Zhang F, Marini CP, Ravikumar TS & Wang P (2007a). Ghrelin attenuates sepsis-induced acute lung injury and mortality in rats. Am J Respir Crit Care Med 176, 805-813.
83. Wu R, Zhou M, Das P, Dong W, Ji Y, Yang D, Miksa M, Zhang F, Ravikumar TS & Wang P (2007b). Ghrelin inhibits sympathetic nervous activity in sepsis. Am J Physiol Endocrinol Metab 293, E1697-E1702.
84. Zhang H, Wang HY, Bassel-Duby R, Maass DL, Johnston WE, Horton JW & Tao W (2007). Role of interleukin-6 in cardiac inflammation and dysfunction after burn complicated by sepsis. Am J Physiol Heart Circ Physiol 292, H2408-H2416.