Sepsis-Associated Acute Kidney Injury: Macrohemodynamic and Microhemodynamic Alterations in the Renal Circulation

Seminars in Nephrology

Volumn 35, Issue 1, 2015, Pages 64-74

  Prowle, John R ^a,b   Bellomo, Rinaldo ^c,d  

^a ROYAL LONDON HOSPITAL   (United Kingdom)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^c AUSTIN HOSPITAL   (Australia)

^d MONASH UNIVERSITY   (Australia)

Author keywords

Acute kidney injury; Critical care; Hemodynamic management; Microcirculation; Renal blood flow; Sepsis

Indexed keywords

HYPERTENSIVE FACTOR;

ACUTE KIDNEY FAILURE; DRUG RESPONSE; FLUID THERAPY; GLOMERULUS CAPILLARY; GLOMERULUS FILTRATION RATE; HUMAN; HYDROSTATIC PRESSURE; HYPOTENSION; KIDNEY BLOOD FLOW; KIDNEY CIRCULATION; KIDNEY CLEARANCE; KIDNEY ISCHEMIA; MANAGED CARE; NEPHRITIS; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REVIEW; SEPSIS; SEPSIS ASSOCIATED ACUTE KIDNEY INJURY; TREATMENT OUTCOME; VASODILATATION; ACUTE KIDNEY INJURY; COMPLICATION; HEMODYNAMICS; KIDNEY; MICROCIRCULATION; VASCULARIZATION;

ACUTE KIDNEY INJURY; HEMODYNAMICS; HUMANS; KIDNEY; MICROCIRCULATION; RENAL CIRCULATION; SEPSIS;

EID: 84925243332     PISSN: 02709295     EISSN: 15584488     Source Type: Journal    
DOI: 10.1016/j.semnephrol.2015.01.007     Document Type: Review

References (78)

1. Uchino S., Kellum J.A., Bellomo R., Doig G.S., Morimatsu H., Morgera S., et al. Acute renal failure in critically ill patients: a multinational, multicenter study. JAMA 2005, 294:813-818.
2. Bagshaw S.M., Uchino S., Bellomo R., Morimatsu H., Morgera S., Schetz M., et al. Septic acute kidney injury in critically ill patients: clinical characteristics and outcomes. Clin J Am Soc Nephrol 2007, 2:431-439.
3. Palevsky P.M., Zhang J.H., Oconnor T.Z., Chertow G.M., Crowley S.T., Choudhury D., et al. Intensity of renal support in critically ill patients with acute kidney injury. N Engl J Med 2008, 359:7-20.
4. Bellomo R., Cass A., Cole L., Finfer S., Gallagher M., et al. Intensity of continuous renal-replacement therapy in critically ill patients. N Engl J Med 2009, 361:1627-1638. RENAL Study Investigators.
5. Coca S.G., Yusuf B., Shlipak M.G., Garg A.X., Parikh C.R. Long-term risk of mortality and other adverse outcomes after acute kidney injury: a systematic review and meta-analysis. Am J Kidney Dis 2009, 53:961-973.
6. Kidney Disease: Improving Global Outcomes (KDIGO). KDIGO Clinical Practice Guideline for acute kidney injury. Section 2: AKI definition. Kidney Int Suppl. 2012;2:19-36.
7. Heyman S.N., Lieberthal W., Rogiers P., Bonventre J.V. Animal models of acute tubular necrosis. Curr Opin Crit Care 2002, 8:526-534.
8. Badenoch A.W., Darmady E.M. The effects of temporary occlusion of the renal artery in rabbits and its relationship to traumatic uraemia. J Pathol Bacteriol 1947, 59:79-94.
9. Oliver J., Mac D.M., Tracy A. The pathogenesis of acute renal failure associated with traumatic and toxic injury; renal ischemia, nephrotoxic damage and the ischemic episode. J Clin Invest 1951, 30:1307-1439.
10. Sharfuddin A.A., Molitoris B.A. Pathophysiology of ischemic acute kidney injury. Nat Rev Nephrol 2011, 7:189-200.
11. Kwon O., Nelson W.J., Sibley R., Huie P., Scandling J.D., Dafoe D., et al. Backleak, tight junctions, and cell-cell adhesion in postischemic injury to the renal allograft. J Clin Invest 1998, 101:2054-2064.
12. Kwon O., Corrigan G., Myers B.D., Sibley R., Scandling J.D., Dafoe D., et al. Sodium reabsorption and distribution of Na+/K+-ATPase during postischemic injury to the renal allograft. Kidney Int 1999, 55:963-975.
13. Lerolle N., Nochy D., Guerot E., Bruneval P., Fagon J.Y., Diehl J.L., et al. Histopathology of septic shock induced acute kidney injury: apoptosis and leukocytic infiltration. Intensive Care Med 2010, 36:471-478.
14. Kashani K., Al-Khafaji A., Ardiles T., Artigas A., Bagshaw S.M., Bell M., et al. Discovery and validation of cell cycle arrest biomarkers in human acute kidney injury. Crit Care 2013, 17:R25.
15. Cinel I., Opal S.M. Molecular biology of inflammation and sepsis: a primer. Crit Care Med 2009, 37:291-304.
16. Schrier R.W., Wang W. Acute renal failure and sepsis. N Engl J Med 2004, 351:159-169.
17. Saotome T., Ishikawa K., May C.N., Birchall I.E., Bellomo R. The impact of experimental hypoperfusion on subsequent kidney function. Intensive Care Med 2010, 36:533-540.
18. Chua H.R., Glassford N., Bellomo R. Acute kidney injury after cardiac arrest. Resuscitation 2012, 83:721-727.
19. Phillips R.A., Dole V.P., et al. Effects of acute hemorrhagic and traumatic shock on renal function of dogs. Am J Physiol 1946, 145:314-336.
20. Ravikant T., Lucas C.E. Renal blood flow distribution in septic hyperdynamic pigs. J Surg Res 1977, 22:294-298.
21. Brenner M., Schaer G.L., Mallory D.L., Suffredini A.F., Parrillo J.E. Detection of renal blood flow abnormalities in septic and critically ill patients using a newly designed indwelling thermodilution renal vein catheter. Chest 1990, 98:170-179.
22. Langenberg C., Wan L., Egi M., May C.N., Bellomo R. Renal blood flow in experimental septic acute renal failure. Kidney Int 2006, 69:1996-2002.
23. Langenberg C., Bellomo R., May C., Wan L., Egi M., Morgera S. Renal blood flow in sepsis. Crit Care 2005, 9:R363-R374.
24. Jacob L.P., Chazalet J.J., Payen D.M., Villiers S.M., Boudaoud S., Teillac P., et al. Renal hemodynamic and functional effect of PEEP ventilation in human renal transplantations. Am J Respir Crit Care Med 1995, 152:103-107.
25. Prowle J.R., Molan M.P., Hornsey E., Bellomo R. Measurement of renal blood flow by phase-contrast magnetic resonance imaging during septic acute kidney injury: a pilot investigation. Crit Care Med 2012, 40:1768-1776.
26. Langenberg C., Wan L., Egi M., May C.N., Bellomo R. Renal blood flow and function during recovery from experimental septic acute kidney injury. Intensive Care Med 2007, 33:1614-1618.
27. Ishikawa K., Calzavacca P., Bellomo R., Bailey M., May C.N. Effect of selective inhibition of renal inducible nitric oxide synthase on renal blood flow and function in experimental hyperdynamic sepsis. Crit Care Med 2012, 40:2368-2375.
28. Ishikawa K., Bellomo R., May C.N. The impact of intrarenal nitric oxide synthase inhibition on renal blood flow and function in mild and severe hyperdynamic sepsis. Crit Care Med 2011, 39:770-776.
29. Di Giantomasso D., Morimatsu H., May C.N., Bellomo R. Intrarenal blood flow distribution in hyperdynamic septic shock: effect of norepinephrine. Crit Care Med 2003, 31:2509-2513.
30. Kikeri D., Pennell J.P., Hwang K.H., Jacob A.I., Richman A.V., Bourgoignie J.J. Endotoxemic acute renal failure in awake rats. Am J Physiol 1986, 250:F1098-F1106.
31. Legrand M., Bezemer R., Kandil A., Demirci C., Payen D., Ince C. The role of renal hypoperfusion in development of renal microcirculatory dysfunction in endotoxemic rats. Intensive Care Med 2011, 37:1534-1542.
32. Wang Z., Holthoff J.H., Seely K.A., Pathak E., Spencer H.J., Gokden N., et al. Development of oxidative stress in the peritubular capillary microenvironment mediates sepsis-induced renal microcirculatory failure and acute kidney injury. Am J Pathol 2012, 180:505-516.
33. Seely K.A., Holthoff J.H., Burns S.T., Wang Z., Thakali K.M., Gokden N., et al. Hemodynamic changes in the kidney in a pediatric rat model of sepsis-induced acute kidney injury. Am J Physiol Renal Physiol 2011, 301:F209-F217.
34. Regueira T., Djafarzadeh S., Brandt S., Gorrasi J., Borotto E., Porta F., et al. Oxygen transport and mitochondrial function in porcine septic shock, cardiogenic shock, and hypoxaemia. Acta Anaesthesiol Scand 2012, 56:846-859.
35. Dyson A., Bezemer R., Legrand M., Balestra G., Singer M., Ince C. Microvascular and interstitial oxygen tension in the renal cortex and medulla studied in a 4-h rat model of LPS-induced endotoxemia. Shock 2011, 36:83-89.
36. May C.N., Ishikawa K., Wan L., Williams J., Wellard R.M., Pell G.S., et al. Renal bioenergetics during early gram-negative mammalian sepsis and angiotensin II infusion. Intensive Care Med 2012, 38:886-893.
37. Siegemund M., van Bommel J., Stegenga M.E., Studer W., van Iterson M., Annaheim S., et al. Aortic cross-clamping and reperfusion in pigs reduces microvascular oxygenation by altered systemic and regional blood flow distribution. Anesth Analg 2010, 111:345-353.
38. Bonventre J.V., Yang L. Cellular pathophysiology of ischemic acute kidney injury. J Clin Invest 2011, 121:4210-4221.
39. Fenhammar J., Rundgren M., Forestier J., Kalman S., Eriksson S., Frithiof R. Toll-like receptor 4 inhibitor TAK-242 attenuates acute kidney injury in endotoxemic sheep. Anesthesiology 2011, 114:1130-1137.
40. Holthoff J.H., Wang Z., Seely K.A., Gokden N., Mayeux P.R. Resveratrol improves renal microcirculation, protects the tubular epithelium, and prolongs survival in a mouse model of sepsis-induced acute kidney injury. Kidney Int 2012, 81:370-378.
41. Ko G.J., Jang H.R., Huang Y., Womer K.L., Liu M., Higbee E., et al. Blocking Fas ligand on leukocytes attenuates kidney ischemia-reperfusion injury. J Am Soc Nephrol 2011, 22:732-742.
42. Prowle J.R., Ishikawa K., May C.N., Bellomo R. Renal blood flow during acute renal failure in man. Blood Purif 2009, 28:216-225.
43. Prowle J.R., Ishikawa K., May C.N., Bellomo R. Renal plasma flow and glomerular filtration rate during acute kidney injury in man. Ren Fail 2010, 32:349-355.
44. Benes J., Chvojka J., Sykora R., Radej J., Krouzecky A., Novak I., et al. Searching for mechanisms that matter in early septic acute kidney injury: an experimental study. Crit Care 2011, 15:R256.
45. Singh P., Okusa M.D. The role of tubuloglomerular feedback in the pathogenesis of acute kidney injury. Contrib Nephrol 2011, 174:12-21.
46. Wilson D.R. Pathophysiology of obstructive nephropathy. Kidney Int 1980, 18:281-292.
47. Alejandro V., Scandling J.D., Sibley R.K., Dafoe D., Alfrey E., Deen W., et al. Mechanisms of filtration failure during postischemic injury of the human kidney. A study of the reperfused renal allograft. J Clin Invest 1995, 95:820-831.
48. Reubi F.C., Vorburger C., Tuckman J. Renal distribution volumes of indocyanine green, (51 Cr)EDTA, and 24 Na in man during acute renal failure after shock. Implications for the pathogenesis of anuria. J Clin Invest 1973, 52:223-235.
49. Thomson S.C., Blantz R.C. Glomerulotubular balance, tubuloglomerular feedback, and salt homeostasis. J Am Soc Nephrol 2008, 19:2272-2275.
50. Herrler T., Tischer A., Meyer A., Feiler S., Guba M., Nowak S., et al. The intrinsic renal compartment syndrome: new perspectives in kidney transplantation. Transplantation 2010, 89:40-46.
51. Williams R.H., Thomas C.E., Navar L.G., Evan A.P. Hemodynamic and single nephron function during the maintenance phase of ischemic acute renal failure in the dog. Kidney Int 1981, 19:503-515.
52. Xu C., Chang A., Hack B.K., Eadon M.T., Alper S.L., Cunningham P.N. TNF-mediated damage to glomerular endothelium is an important determinant of acute kidney injury in sepsis. Kidney Int 2014, 85:72-81.
53. Adembri C., Sgambati E., Vitali L., Selmi V., Margheri M., Tani A., et al. Sepsis induces albuminuria and alterations in the glomerular filtration barrier: a morphofunctional study in the rat. Crit Care 2011, 15:R277.
54. Wan L., Bellomo R., May C.N. A comparison of 4% succinylated gelatin solution versus normal saline in stable normovolaemic sheep: global haemodynamic, regional blood flow and oxygen delivery effects. Anaesth Intensive Care 2007, 35:924-931.
55. Legrand M., Mik E.G., Balestra G.M., Lutter R., Pirracchio R., Payen D., et al. Fluid resuscitation does not improve renal oxygenation during hemorrhagic shock in rats. Anesthesiology 2010, 112:119-127.
56. Prowle J.R., Kirwan C.J., Bellomo R. Fluid management for the prevention and attenuation of acute kidney injury. Nat Rev Nephrol 2014, 10:37-47.
57. Mullens W., Abrahams Z., Francis G.S., Sokos G., Taylor D.O., Starling R.C., et al. Importance of venous congestion for worsening of renal function in advanced decompensated heart failure. J Am Coll Cardiol 2009, 53:589-596.
58. Legrand M., Dupuis C., Simon C., Gayat E., Mateo J., Lukaszewicz A.C., et al. Association between systemic hemodynamics and septic acute kidney injury in critically ill patients: a retrospective observational study. Crit Care 2013, 17:R278.
59. Winton F.R. The influence of venous pressure on the isolated mammalian kidney. J Physiol 1931, 72:49-61.
60. Li X., Liu M., Bedja D., Thoburn C., Gabrielson K., Racusen L., et al. Acute renal venous obstruction is more detrimental to the kidney than arterial occlusion: implication for murine models of acute kidney injury. Am J Physiol Renal Physiol 2012, 302:F519-F525.
61. Gottschalk C.W., Mylle M. Micropuncture study of pressures in proximal tubules and peritubular capillaries of the rat kidney and their relation to ureteral and renal venous pressures. Am J Physiol 1956, 185:430-439.
62. Haase N., Perner A., Hennings L.I., Siegemund M., Lauridsen B., Wetterslev M., et al. Hydroxyethyl starch 130/0.38-0.45 versus crystalloid or albumin in patients with sepsis: systematic review with meta-analysis and trial sequential analysis. BMJ 2013, 346:f839.
63. Myburgh J.A., Finfer S., Bellomo R., Billot L., Cass A., Gattas D., et al. Hydroxyethyl starch or saline for fluid resuscitation in intensive care. N Engl J Med 2012, 367:1901-1911.
64. Perner A., Haase N., Guttormsen A.B., Tenhunen J., Klemenzson G., Aneman A., et al. Hydroxyethyl starch 130/0.42 versus Ringer[U+05F3]s acetate in severe sepsis. N Engl J Med 2012, 367:124-134.
65. Zarychanski R., Abou-Setta A.M., Turgeon A.F., Houston B.L., McIntyre L., Marshall J.C., et al. Association of hydroxyethyl starch administration with mortality and acute kidney injury in critically ill patients requiring volume resuscitation: a systematic review and meta-analysis. JAMA 2013, 309:678-688.
66. Chowdhury A.H., Cox E.F., Francis S.T., Lobo D.N. A randomized, controlled, double-blind crossover study on the effects of 2-L infusions of 0.9% saline and Plasma-Lyte 148 on renal blood flow velocity and renal cortical tissue perfusion in healthy volunteers. Ann Surg 2012, 256:18-24.
67. Shaw A.D., Bagshaw S.M., Goldstein S.L., Scherer L.A., Duan M., Schermer C.R., et al. Major complications, mortality, and resource utilization after open abdominal surgery: 0.9% saline compared to Plasma-Lyte. Ann Surg 2012, 255:821-829.
68. Yunos N.M., Bellomo R., Bailey M. Chloride-restrictive fluid administration and incidence of acute kidney injury--reply. JAMA 2013, 309:543-544.
69. Anderson W.P., Korner P.I., Selig S.E. Mechanisms involved in the renal responses to intravenous and renal artery infusions of noradrenaline in conscious dogs. J Physiol 1981, 321:21-30.
70. Bellomo R., Kellum J.A., Wisniewski S.R., Pinsky M.R. Effects of norepinephrine on the renal vasculature in normal and endotoxemic dogs. Am J Respir Crit Care Med 1999, 159:1186-1192.
71. Morimatsu H., Ishikawa K., May C.N., Bailey M., Bellomo R. The systemic and regional hemodynamic effects of phenylephrine in sheep under normal conditions and during early hyperdynamic sepsis. Anesth Analg 2012, 115:330-342.
72. Redfors B., Bragadottir G., Sellgren J., Sward K., Ricksten S.E. Effects of norepinephrine on renal perfusion, filtration and oxygenation in vasodilatory shock and acute kidney injury. Intensive Care Med 2011, 37:60-67.
73. Wan L., Langenberg C., Bellomo R., May C.N. Angiotensin II in experimental hyperdynamic sepsis. Crit Care 2009, 13:R190.
74. Fallet R.W., Ikenaga H., Bast J.P., Carmines P.K. Relative contributions of Ca2+ mobilization and influx in renal arteriolar contractile responses to arginine vasopressin. Am J Physiol Renal Physiol 2005, 288:F545-F551.
75. Di Giantomasso D., Morimatsu H., Bellomo R., May C.N. Effect of low-dose vasopressin infusion on vital organ blood flow in the conscious normal and septic sheep. Anaesth Intensive Care 2006, 34:427-433.
76. Russell J.A., Walley K.R., Singer J., Gordon A.C., Hebert P.C., Cooper D.J., et al. Vasopressin versus norepinephrine infusion in patients with septic shock. N Engl J Med 2008, 358:877-887.
77. Gordon A.C., Russell J.A., Walley K.R., Singer J., Ayers D., Storms M.M., et al. The effects of vasopressin on acute kidney injury in septic shock. Intensive Care Med 2010, 36:83-91.
78. Ishikawa K., Wan L., Calzavacca P., Bellomo R., Bailey M., May C.N. The effects of terlipressin on regional hemodynamics and kidney function in experimental hyperdynamic sepsis. PLoS One 2012, 7:e29693.