Haemodynamic influences on kidney oxygenation: Clinical implications of integrative physiology

Clinical and Experimental Pharmacology and Physiology

Volumn 40, Issue 2, 2013, Pages 106-122

  Evans, Roger G ^a   Ince, Can ^b   Joles, Jaap A ^c   Smith, David W ^d   May, Clive N ^e   O'Connor, Paul M ^f   Gardiner, Bruce S ^d  

^a MONASH UNIVERSITY   (Australia)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^d UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^e UNIVERSITY OF MELBOURNE   (Australia)

^f MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

Acute kidney injury; Kidney circulation; Mathematical model; Oxygen consumption; Oxygen delivery; Tissue oxygenation

Indexed keywords

NITRIC OXIDE; OXYGEN; SODIUM;

ACUTE KIDNEY FAILURE; BLOOD VESSEL TONE; CARDIOPULMONARY BYPASS; CONTRAST INDUCED NEPHROPATHY; HEMATOCRIT; HUMAN; KIDNEY BLOOD FLOW; KIDNEY FUNCTION; KIDNEY OXYGENATION; MATHEMATICAL MODEL; MEAN ARTERIAL PRESSURE; NONHUMAN; OXIDATIVE STRESS; OXYGEN BLOOD LEVEL; OXYGEN CONSUMPTION; OXYGEN TRANSPORT; PATHOPHYSIOLOGY; RENAL REPLACEMENT THERAPY; REVIEW; SEPSIS; SODIUM ABSORPTION; TISSUE OXYGENATION;

ACUTE KIDNEY INJURY; ANIMALS; HEMODYNAMICS; HUMANS; KIDNEY; OXYGEN CONSUMPTION; RENAL CIRCULATION;

EID: 84873192308     PISSN: 03051870     EISSN: 14401681     Source Type: Journal    
DOI: 10.1111/1440-1681.12031     Document Type: Review

References (165)

1. Ranucci M, Romitti F, Isgro G et al. Oxygen delivery during cardiopulmonary bypass and acute renal failure after coronary operations. Ann. Thorac. Surg. 2005; 80: 2213-20.
2. Ranucci M. Perioperative renal failure: Hypoperfusion during cardiopulmonary bypass? Semin. Cardiothorac. Vasc. Anesth. 2007; 11: 265-8.
3. Hattori R, Ono Y, Kato M, Komatsu T, Matsukawa Y, Yamamoto T. Direct visualization of cortical peritubular capillary of transplanted human kidney with reperfusion injury using a magnifying endoscopy. Transplantation 2005; 79: 1190-4.
4. Kwon O, Hong SM, Sutton TA, Temm CJ. Preservation of peritubular capillary endothelial integrity and increasing pericytes may be critical to recovery from postischemic acute kidney injury. Am. J. Physiol. Renal Physiol. 2008; 295: F351-9.
5. Legrand M, Mik EG, Johannes T, Payen D, Ince C. Renal hypoxia and dysoxia after reperfusion of the ischemic kidney. Mol. Med. 2008; 14: 502-16.
6. Oostendorp M, de Vries EE, Slenter JM et al. MRI of renal oxygenation and function after normothermic ischemia-reperfusion injury. NMR Biomed. 2010; 24: 194-200.
7. Wang JJ, Hendrich KS, Jackson EK, Ildstad ST, Williams DS, Ho C. Perfusion quantitation in transplanted rat kidney by MRI with arterial spin labeling. Kidney Int. 1998; 53: 1783-91.
8. Heyman SN, Evans RG, Rosen S, Rosenberger C. Cellular adaptive changes in AKI. Mitigating renal hypoxic injury. Nephrol. Dial. Transplant. 2012; 27: 1721-8.
9. Heyman SN, Rosen S, Rosenberger C. Renal parenchymal hypoxia, hypoxia adaptation, and the pathogenesis of radiocontrast nephropathy. Clin. J. Am. Soc. Nephrol. 2008; 3: 288-96.
10. Brezis M, Heyman SN, Sugar AM. Reduced amphotericin toxicity in an albumin vehicle. J. Drug Target. 1993; 1: 185-9.
11. Zhong Z, Arteel GE, Connor HD et al. Cyclosporin A increases hypoxia and free radical production in rat kidneys: Prevention by dietary glycine. Am. J. Physiol. 1998; 275: F595-604.
12. Heyman SN, Brezis M, Epstein FH, Spokes K, Silva P, Rosen S. Early renal medullary hypoxic injury from radiocontrast and indomethacin. Kidney Int. 1991; 40: 632-42.
13. Heyman SN, Rosen S, Fuchs S, Epstein FH, Brezis M. Myoglobinuric acute renal failure in the rat: A role for medullary hypoperfusion, hypoxia, and tubular obstruction. J. Am. Soc. Nephrol. 1996; 7: 1066-74.
14. Fine LG, Norman JT. Chronic hypoxia as a mechanism of progression of chronic kidney diseases: From hypothesis to novel therapeutics. Kidney Int. 2008; 74: 867-72.
15. Heyman SN, Khamaisi M, Rosen S, Rosenberger C. Renal parenchymal hypoxia, hypoxia response and the progression of chronic kidney disease. Am. J. Nephrol. 2008; 28: 998-1006.
16. Van Slyke DD, Rhoads CP, Hiller A, Alving AS. Relationships between urea excretion, renal blood flow, renal oxygen consumption, and diuresis. The mechanism of urea excretion. Am. J. Physiol. 1934; 109: 336-74.
17. Dole VP, Emerson KJ, Phillips RA, Hamilton P, Van Slyke DD. The renal extraction of oxygen in experimental shock. Am. J. Physiol. 1946; 145: 261-9.
18. Kramer K, Winton FR. The influence of urea and of change in arterial pressure on the oxygen consumption of the isolated kidney of the dog. J. Physiol. 1939; 96: 87-103.
19. Levy SE, Blalock A. The effects of unilateral nephrectomy on the renal blood flow and oxygen consumption of unanesthetized dogs. Am. J. Physiol. 1938; 122: 609-13.
20. Levy SE, Light RA, Blalock A. The blood flow and oxygen consumption of the kidney in experimental hypertension. Am. J. Physiol. 1938; 122: 38-42.
21. Levy MN. Oxygen consumption and blood flow in the hypothermic, perfused kidney. Am. J. Physiol. 1959; 197: 1111-14.
22. Levy MN. Effect of variations of blood flow on renal oxygen extraction. Am. J. Physiol. 1960; 199: 13-18.
23. Levy MN, Imperial ES. Oxygen shunting in renal cortical and medullary capillaries. Am. J. Physiol. 1961; 200: 159-62.
24. 2. Acta Physiol. Scand. 1969; 75: 353-9.
25. Aukland K, Krog J. Renal oxygen tension. Nature 1960; 188: 671.
26. Lassen NA, Munck O, Thaysen JH. Oxygen consumption and sodium reabsorption in the kidney. Acta Physiol. Scand. 1961; 51: 371-84.
27. Blantz RC, Weir MR. Are the oxygen costs of kidney function highly regulated? Curr. Opin. Nephrol. Hypertens. 2004; 13: 67-71.
28. Evans RG, Gardiner BS, Smith DW, O'Connor PM. Intrarenal oxygenation: Unique challenges and the biophysical basis of homeostasis. Am. J. Physiol. Renal Physiol. 2008; 295: F1259-70.
29. Brezis M, Rosen S. Hypoxia of the renal medulla: Its implications for disease. N. Engl. J. Med. 1995; 332: 647-55.
30. Pallone TL, Robertson CR, Jamison RL. Renal medullary microcirculation. Physiol. Rev. 1990; 70: 885-920.
31. 2 on limb, renal, and coronary vascular resistances. Am. J. Physiol. 1967; 213: 1102-10.
32. Marshall JM. The Joan Mott Prize Lecture. The integrated response to hypoxia: From circulation to cells. Exp. Physiol. 1999; 84: 449-70.
33. Wong DH, Weir PD, Wesley RC et al. Changes in renal vein, renal surface, and urine oxygen tension during hypoxia in pigs. J. Clin. Monit. 1993; 9: 1-4.
34. Evans RG, Goddard D, Eppel GA, O'Connor PM. Factors that render the kidney susceptible to tissue hypoxia in hypoxemia. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2011; 300: R931-40.
35. Leong CL, Anderson WP, O'Connor PM, Evans RG. Evidence that renal arterial-venous oxygen shunting contributes to dynamic regulation of renal oxygenation. Am. J. Physiol. Renal Physiol. 2007; 292: F1726-33.
36. Korner PI. The role of the arterial chemoreceptors and baroreceptors in the circulatory response to hypoxia of the rabbit. J. Physiol. 1965; 180: 279-303.
37. 2 uptake during hypoxia in the anesthetized rabbit. Pflügers Arch. 1976; 365: 213-20.
38. Malpas SC, Evans RG. Do different levels and patterns of sympathetic activation all provoke renal vasoconstriction? J. Auton. Nerv. Syst. 1998; 69: 72-82.
39. Leonard BL, Malpas SC, Denton KM, Madden AC, Evans RG. Differential control of intrarenal blood flow during reflex increases in sympathetic nerve activity. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2001; 280: R62-8.
40. Sharkey RA, Mulloy EM, O'Neill SJ. Acute effects of hypoxaemia, hyperoxaemia and hypercapnia on renal blood flow in normal and renal transplant subjects. Eur. Respir. J. 1998; 12: 653-7.
41. Flemming B, Seeliger E, Wronski T, Steer K, Arenz N, Persson PB. Oxygen and renal hemodynamics in the conscious rat. J. Am. Soc. Nephrol. 2000; 11: 18-24.
42. Neylon M, Marshall JM, Johns EJ. The effects of systemic hypoxia on renal function in the anaesthetized rat. J. Physiol. 1995; 487: 497-511.
43. Halperin ML, Cheema-Dhadli S, Lin SH, Kamel KS. Properties permitting the renal cortex to be the oxygen sensor for the release of erythropoietin: Clinical implications. Clin. J. Am. Soc. Nephrol. 2006; 1: 1049-53.
44. Eppel GA, Denton KM, Malpas SC, Evans RG. Nitric oxide in responses of regional kidney perfusion to renal nerve stimulation and renal ischaemia. Pflügers Arch. 2003; 447: 205-13.
45. Saotome T, Ishikawa K, May CN, Birchall IE, Bellomo R. The impact of experimental hypoperfusion on subsequent kidney function. Intensive Care Med. 2010; 36: 533-40.
46. Zhang W, Edwards A. Oxygen transport across vasa recta in the renal medulla. Am. J. Physiol. Heart Circ. Physiol. 2002; 283: H1042-55.
47. Gardiner BS, Smith DW, O'Connor PM, Evans RG. A mathematical model of diffusional shunting of oxygen from arteries to veins in the kidney. Am. J. Physiol. Renal Physiol. 2011; 300: F1339-52.
48. Just A. Mechanisms of renal blood flow autoregulation: Dynamics and contributions. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2007; 292: R1-17.
49. Hall JE, Guyton AC, Cowley AW Jr. Dissociation of renal blood flow and filtration rate autoregulation by renin depletion. Am. J. Physiol. 1977; 232: F215-21.
50. Evans RG, Eppel GA, Michaels S et al. Multiple mechanisms act to maintain kidney oxygenation during renal ischemia in anesthetized rabbits. Am. J. Physiol. Renal Physiol. 2010; 298: F1235-43.
51. Warner L, Gomez SI, Bolterman R et al. Regional decreases in renal oxygenation during graded acute renal arterial stenosis: A case for renal ischemia. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2009; 296: R67-71.
52. Brezis M, Heyman SN, Epstein FH. Determinants of intrarenal oxygenation II. Hemodynamic effects. Am. J. Physiol. 1994; 267: F1063-8.
53. Evans RG, Majid DS, Eppel GA. Mechanisms mediating pressure natriuresis: What we know and what we need to find out. Clin. Exp. Pharmacol. Physiol. 2005; 32: 400-9.
54. Gloviczki ML, Glockner JF, Lerman LO et al. Preserved oxygenation despite reduced blood flow in poststenotic kidneys in human atherosclerotic renal artery stenosis. Hypertension 2010; 55: 961-6.
55. Carey RM. Are kidneys not ischemic in human renal vascular disease? Hypertension 2010; 55: 838-9.
56. Gardiner BS, Thompson SL, Ngo JP et al. Diffusive shunting between vessels in the pre-glomerular vasculature: Anatomical observations and computational modeling. Am. J. Physiol. Renal Physiol. 2012; 303: F605-18.
57. 2 transport in the rat outer medulla. I. Model formulation and baseline results. Am. J. Physiol. Renal Physiol. 2009; 297: F517-36.
58. 2 transport in the rat outer medulla. II. Impact of outer medullary architecture. Am. J. Physiol. Renal Physiol. 2009; 297: F537-48.
59. Chen J, Edwards A, Layton AT. Effects of pH and medullary blood flow on oxygen transport and sodium reabsorption in the rat outer medulla. Am. J. Physiol. Renal Physiol. 2010; 298: F1369-83.
60. 2 shunting is a structural anti-oxidant defence mechanism of the renal cortex. Clin. Exp. Pharmacol. Physiol. 2006; 33: 637-41.
61. O'Connor PM, Evans RG. Structural antioxidant defense mechanisms in the mammalian and nonmammalian kidney: Different solutions to the same problem? Am. J. Physiol. Regul. Integr. Comp. Physiol. 2010; 299: R723-7.
62. Edwards A, Layton AT. Impact of nitric oxide-mediated vasodilation on outer medullary NaCl transport and oxygenation. Am. J. Physiol. Renal Physiol. 2012; 303: F907-17.
63. O'Connor PM. Renal oxygen delivery: Matching delivery to metabolic demand. Clin. Exp. Pharmacol. Physiol. 2006; 33: 961-7.
64. 2 in the face of altered perfusion: A phenomenon specific to the renal cortex and independent of resting renal oxygen consumption. Clin. Exp. Pharmacol. Physiol. 2011; 38: 247-54.
65. Palm F, Teerlink T, Hansell P. Nitric oxide and kidney oxygenation. Curr. Opin. Nephrol. Hypertens. 2009; 18: 68-73.
66. Gullans SR, Hebert SC. Metabolic basis of ion transport. In: Brenner BM (ed). Brenner and Rector's The Kidney, 5th edn. Philadelphia, WB Saunders, 1996; 211-46.
67. 2 during acute normovolemic hemodilution. Am. J. Physiol. Renal Physiol. 2007; 292: F796-803.
68. Donnelly S. Why is erythropoietin made in the kidney? The kidney functions as a 'critmeter' to regulate the hematocrit. Adv. Exp. Med. Biol. 2003; 543: 73-87.
69. van Bommel J, Siegemund M, Henny ChP, Ince C. Heart, kidney, and intestine have different tolerances for anemia. Transl. Res. 2008; 151: 110-17.
70. Franchini KG. Influence of hemodilution on the renal blood flow autoregulation during acute expansion in rats. Am. J. Physiol. 1999; 277: R1662-74.
71. Sinagowitz E, Baker R, Strauss J, Kessler M. Renal tissue oxygenation during hypoxic hypoxia. Adv. Exp. Med. Biol. 1975; 75: 441-7.
72. Mehta RL, Chertow GM. Acute renal failure definitions and classification: Time for change? J. Am. Soc. Nephrol. 2003; 14: 2178-87.
73. Rosenberger C, Rosen S, Heyman SN. Renal parenchymal oxygenation and hypoxia adaptation in acute kidney injury. Clin. Exp. Pharmacol. Physiol. 2006; 33: 980-8.
74. Evans RG, May CN. Tissue hypoxia as a therapeutic target in acute kidney injury. Clin. Exp. Pharmacol. Physiol. 2009; 36: 867-9.
75. Legrand M, Almac E, Mik EG et al. l-NIL prevents renal microvascular hypoxia and increase of renal oxygen consumption after ischemia-reperfusion in rats. Am. J. Physiol. Renal Physiol. 2009; 296: F1109-17.
76. Siegemund M, van Bommel J, Stegenga ME et al. Aortic cross-clamping and reperfusion in pigs reduces microvascular oxygenation by altered systemic and regional blood flow distribution. Anesth. Analg. 2010; 111: 345-53.
77. 2 in a normotensive rat model of endotoxemia. Crit. Care 2006; 10: R88.
78. Evans RG, Gardiner BS, Smith DW, O'Connor PM. Methods for studying the physiology of kidney oxygenation. Clin. Exp. Pharmacol. Physiol. 2008; 35: 1405-12.
79. Liss P, Cox EF, Eckerbom P, Francis ST. Imaging of intrarenal haemodynamics and oxygen metabolism. Clin. Exp. Pharmacol. Physiol. 2013; 40: 158-167.
80. Evans RG, Leong CL, Anderson WP, O'Connor PM. Don't be so BOLD. Potential limitations in the use of BOLD MRI for studies of renal oxygenation. Kidney Int. 2007; 71: 1327-8.
81. Tran M, Tam D, Bardia A et al. PGC-1alpha promotes recovery after acute kidney injury during systemic inflammation in mice. J. Clin. Invest. 2011; 121: 4003-14.
82. Bezemer R, Faber DJ, Almac E et al. Evaluation of multi-exponential curve fitting analysis of oxygen-quenched phosphorescence decay traces for recovering microvascular oxygen tension histograms. Med. Biol. Eng. Comput. 2010; 48: 1233-42.
83. Chade AR. Renovascular disease, microcirculation, and the progression of renal injury: Role of angiogenesis. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2011; 300: R783-90.
84. Siddiqi L, Joles JA, Grassi G, Blankestijn PJ. Is kidney ischemia the central mechanism in parallel activation of the renin and sympathetic system? J. Hypertens. 2009; 27: 1341-9.
85. Siddiqi L, Prakken NH, Velthuis BK et al. Sympathetic activity in chronic kidney disease patients is related to left ventricular mass despite antihypertensive treatment. Nephrol. Dial. Transplant. 2010; 25: 3272-7.
86. Faber JE, Brody MJ. Afferent renal nerve-dependent hypertension following acute renal artery stenosis in the conscious rat. Circ. Res. 1985; 57: 676-88.
87. Miyajima E, Yamada Y, Yoshida Y et al. Muscle sympathetic nerve activity in renovascular hypertension and primary aldosteronism. Hypertension 1991; 17: 1057-62.
88. Klein IH, Ligtenberg G, Oey PL, Koomans HA, Blankestijn PJ. Sympathetic activity is increased in polycystic kidney disease and is associated with hypertension. J. Am. Soc. Nephrol. 2001; 12: 2427-33.
89. Bernhardt WM, Wiesener MS, Weidemann A et al. Involvement of hypoxia-inducible transcription factors in polycystic kidney disease. Am. J. Pathol. 2007; 170: 830-42.
90. Ding A, Kalaignanasundaram P, Ricardo SD et al. Chronic treatment with tempol does not significantly ameliorate renal tissue hypoxia or disease progression in a rodent model of polycystic kidney disease. Clin. Exp. Pharmacol. Physiol. 2012; 39: 917-29.
91. Hering D, Zdrojewski Z, Krol E et al. Tonic chemoreflex activation contributes to the elevated muscle sympathetic nerve activity in patients with chronic renal failure. J. Hypertens. 2007; 25: 157-61.
92. Singh P, Ricksten S-E, Bragadottir G, Redfors B, Nordquist L. Renal oxygenation and hemodynamics in acute kidney injury and chronic kidney disease. Clin. Exp. Pharmacol. Physiol. 2013; 40: 138-147.
93. Devarajan P. Update on mechanisms of ischemic acute kidney injury. J. Am. Soc. Nephrol. 2006; 17: 1503-20.
94. Le Dorze M, Legrand M, Payen D, Ince C. The role of the microcirculation in acute kidney injury. Curr. Opin. Crit. Care 2009; 15: 503-8.
95. Redfors B, Bragadottir G, Sellgren J, Sward K, Ricksten SE. Acute renal failure is NOT an 'acute renal success': A clinical study on the renal oxygen supply/demand relationship in acute kidney injury. Crit. Care Med. 2010; 38: 1695-701.
96. Basile DP, Donohoe D, Roethe K, Osborn JL. Renal ischemic injury results in permanent damage to peritubular capillaries and influences long-term function. Am. J. Physiol. Renal Physiol. 2001; 281: F887-99.
97. Basile DP. The endothelial cell in ischemic acute kidney injury: Implications for acute and chronic function. Kidney Int. 2007; 72: 151-6.
98. Rosenberger C, Pratschke J, Rudolph B et al. Immunohistochemical detection of hypoxia-inducible factor-1alpha in human renal allograft biopsies. J. Am. Soc. Nephrol. 2007; 18: 343-51.
99. Sadowski EA, Djamali A, Wentland AL et al. Blood oxygen level-dependent and perfusion magnetic resonance imaging: Detecting differences in oxygen bioavailability and blood flow in transplanted kidneys. Magn. Reson. Imaging 2010; 28: 56-64.
100. McCullough PA. Radiocontrast-induced acute kidney injury. Nephron Physiol. 2008; 109: 61-72.
101. Tumlin J, Stacul F, Adam A et al. Pathophysiology of contrast-induced nephropathy. Am. J. Cardiol. 2006; 98(Suppl. 1): K14-20.
102. Harmon RC, Duffy SP, Terneus MV, Ball JG, Valentovic MA. Characterization of a novel model for investigation of radiocontrast nephrotoxicity. Nephrol. Dial. Transplant. 2009; 24: 763-8.
103. Liss P, Nygren A, Erikson U, Ulfendahl HR. Injection of low and iso-osmolar contrast medium decreases oxygen tension in the renal medulla. Kidney Int. 1998; 53: 698-702.
104. Prasad PV, Priatna A, Spokes K, Epstein FH. Changes in intrarenal oxygenation as evaluated by BOLD MRI in a rat kidney model for radiocontrast nephropathy. J. Magn. Reson. Imaging 2001; 13: 744-7.
105. Hofmann L, Simon-Zoula S, Nowak A et al. BOLD-MRI for the assessment of renal oxygenation in humans: Acute effect of nephrotoxic xenobiotics. Kidney Int. 2006; 70: 144-50.
106. Hsu SP, Tsai TJ, Chien CT. Ioxitalamate induces renal tubular apoptosis via activation of renal efferent nerve-mediated adrenergic signaling, renin activity, and reactive oxygen species production in rats. Toxicol. Sci. 2010; 114: 149-58.
107. Seeliger E, Flemming B, Wronski T et al. Viscosity of contrast media perturbs renal hemodynamics. J. Am. Soc. Nephrol. 2007; 18: 2912-20.
108. Brezis M, Agmon Y, Epstein FH. Determinants of intrarenal oxygenation. I. Effects of diuretics. Am. J. Physiol. 1994; 267: F1059-62.
109. Epstein FH, Prasad P. Effects of furosemide on medullary oxygenation in younger and older subjects. Kidney Int. 2000; 57: 2080-3.
110. Fenoy FJ, Roman RJ. Effect of volume expansion on papillary blood flow and sodium excretion. Am. J. Physiol. 1991; 260: F813-22.
111. Damkjaer M, Vafaee M, Braad PE, Petersen H, Hoilund-Carlsen PF, Bie P. Renal cortical and medullary blood flow during modest saline loading in humans. Acta Physiol. 2012; 205: 472-83.
112. Wan L, Bellomo R, May CN. The effects of normal and hypertonic saline on regional blood flow and oxygen delivery. Anesth. Analg. 2007; 105: 141-7.
113. 2 during water diuresis as evaluated by blood oxygenation level-dependent magnetic resonance imaging: Effects of aging and cyclooxygenase inhibition. Kidney Int. 1999; 55: 294-8.
114. Talati S, Kirtane AJ, Hassanin A et al. Direct infusion of fenoldopam into the renal arteries to protect from contrast-induced nephropathy in patients at increased risk. Clin. Exp. Pharmacol. Physiol. 2012; 39: 506-9.
115. Caixeta A, Dogan O, Weisz G. Contrast-induced nephropathy. Protective role of fenoldopam. Clin. Exp. Pharmacol. Physiol. 2012; 39: 497-505.
116. Karkouti K, Wijeysundera DN, Yau TM et al. Acute kidney injury after cardiac surgery: Focus on modifiable risk factors. Circulation 2009; 119: 495-502.
117. Mangano CM, Diamondstone LS, Ramsay JG, Aggarwal A, Herskowitz A, Mangano DT. Renal dysfunction after myocardial revascularization: Risk factors, adverse outcomes, and hospital resource utilization. The Multicenter Study of Perioperative Ischemia Research Group. Ann. Intern. Med. 1998; 128: 194-203.
118. Huen SC, Parikh CR. Predicting acute kidney injury after cardiac surgery: A systematic review. Ann. Thorac. Surg. 2012; 93: 337-47.
119. Parolari A, Pesce LL, Pacini D et al. Risk factors for perioperative acute kidney injury after adult cardiac surgery: Role of perioperative management. Ann. Thorac. Surg. 2012; 93: 584-91.
120. Katagiri D, Doi K, Honda K et al. Combination of two urinary biomarkers predicts acute kidney injury after adult cardiac surgery. Ann. Thorac. Surg. 2012; 93: 577-83.
121. Wan L, Yang N, Hiew CY et al. An assessment of the accuracy of renal blood flow estimation by Doppler ultrasound. Intensive Care Med. 2008; 34: 1503-10.
122. Rosner MH, Portilla D, Okusa MD. Cardiac surgery as a cause of acute kidney injury: Pathogenesis and potential therapies. J. Intensive Care Med. 2008; 23: 3-18.
123. Karkouti K, Beattie WS, Wijeysundera DN et al. Hemodilution during cardiopulmonary bypass is an independent risk factor for acute renal failure in adult cardiac surgery. J. Thorac. Cardiovasc. Surg. 2005; 129: 391-400.
124. 2 production during cardiopulmonary bypass as determinants of acute kidney injury: Time for a goal-directed perfusion management? Crit. Care 2011; 15: R192.
125. Ihle BU. Acute renal dysfunction after cardiac surgery: Still a big problem!. Heart Lung Circ. 2007; 16(Suppl. 3): S39-44.
126. Rosner MH, Okusa MD. Acute kidney injury associated with cardiac surgery. Clin. J. Am. Soc. Nephrol. 2006; 1: 19-32.
127. O'Connor PM, Kett MM, Anderson WP, Evans RG. Renal medullary tissue oxygenation is dependent on both cortical and medullary blood flow. Am. J. Physiol. Renal Physiol. 2006; 290: F688-94.
128. Dasta JF, Kane-Gill SL, Durtschi AJ, Pathak DS, Kellum JA. Costs and outcomes of acute kidney injury (AKI) following cardiac surgery. Nephrol. Dial. Transplant. 2008; 23: 1970-4.
129. Lassnigg A, Schmidlin D, Mouhieddine M et al. Minimal changes of serum creatinine predict prognosis in patients after cardiothoracic surgery: A prospective cohort study. J. Am. Soc. Nephrol. 2004; 15: 1597-605.
130. Doenst T, Wijeysundera D, Karkouti K et al. Hyperglycemia during cardiopulmonary bypass is an independent risk factor for mortality in patients undergoing cardiac surgery. J. Thorac. Cardiovasc. Surg. 2005; 130: 1144. e1-8.
131. Redfors B, Bragadottir G, Sellgren J, Sward K, Ricksten SE. Dopamine increases renal oxygenation: A clinical study in post-cardiac surgery patients. Acta Anaesthesiol. Scand. 2010; 54: 183-90.
132. Redfors B, Bragadottir G, Sellgren J, Sward K, Ricksten SE. Effects of norepinephrine on renal perfusion, filtration and oxygenation in vasodilatory shock and acute kidney injury. Intensive Care Med. 2011; 37: 60-7.
133. Bragadottir G, Redfors B, Nygren A, Sellgren J, Ricksten SE. Low-dose vasopressin increases glomerular filtration rate, but impairs renal oxygenation in post-cardiac surgery patients. Acta Anaesthesiol. Scand. 2009; 53: 1052-9.
134. Redfors B, Sward K, Sellgren J, Ricksten SE. Effects of mannitol alone and mannitol plus furosemide on renal oxygen consumption, blood flow and glomerular filtration after cardiac surgery. Intensive Care Med. 2009; 35: 115-22.
135. Bagshaw SM, George C, Bellomo R. Early acute kidney injury and sepsis: A multicentre evaluation. Crit. Care 2008; 12: R47.
136. Parmar A, Langenberg C, Wan L, May CN, Bellomo R, Bagshaw SM. Epidemiology of septic acute kidney injury. Curr. Drug Targets 2009; 10: 1169-78.
137. Mori T, Shimizu T, Tani T. Septic acute renal failure. Contrib. Nephrol. 2010; 166: 40-6.
138. Pelte CH, Chawla LS. Novel therapeutic targets for prevention and therapy of sepsis associated acute kidney injury. Curr. Drug Targets 2009; 10: 1205-11.
139. Aksu U, Demirci C, Ince C. The pathogenesis of acute kidney injury and the toxic triangle of oxygen, reactive oxygen species and nitric oxide. Contrib. Nephrol. 2011; 174: 119-28.
140. 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: 83-9.
141. 2, measured by in vivo electron paramagnetic resonance oximetry and magnetic resonance imaging. Free Radic. Biol. Med. 1996; 21: 25-34.
142. Johannes T, Mik EG, Klingel K et al. Effects of 1400W and/or nitroglycerin on renal oxygenation and kidney function during endotoxaemia in anaesthetised rats. Clin. Exp. Pharmacol. Physiol. 2009; 36: 870-9.
143. Langenberg C, Wan L, Egi M, May CN, Bellomo R. Renal blood flow in experimental septic acute renal failure. Kidney Int. 2006; 69: 1996-2002.
144. Ishikawa K, Bellomo R, May CN. 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: 770-6.
145. Langenberg C, Bagshaw SM, May CN, Bellomo R. The histopathology of septic acute kidney injury: A systematic review. Crit. Care 2008; 12: R38.
146. Ishikawa K, May CN, Gobe G, Langenberg C, Bellomo R. Pathophysiology of septic acute kidney injury: A different view of tubular injury. Contrib. Nephrol. 2010; 165: 18-27.
147. Bellomo R, Wan L, Langenberg C, Ishikawa K, May CN. Septic acute kidney injury: The glomerular arterioles. Contrib. Nephrol. 2011; 174: 98-107.
148. Johannes T, Mik EG, Ince C. Nonresuscitated endotoxemia induces microcirculatory hypoxic areas in the renal cortex in the rat. Shock 2009; 31: 97-103.
149. Legrand M, Bezemer R, Ince C. The role of renal hypoperfusion in development of renal microcirculatory dysfunction in endotoxemic rats. Intensive Care Med. 2011; 37: 1534-42.
150. Humer MF, Phang PT, Friesen BP, Allard MF, Goddard CM, Walley KR. Heterogeneity of gut capillary transit times and impaired gut oxygen extraction in endotoxemic pigs. J. Appl. Physiol. 1996; 81: 895-904.
151. Walley KR. Heterogeneity of oxygen delivery impairs oxygen extraction by peripheral tissues: Theory. J. Appl. Physiol. 1996; 81: 885-94.
152. Kanoore Edul VS, Dubin A, Ince C. The microcirculation as a therapeutic target in the treatment of sepsis and shock. Semin. Respir. Crit. Care Med. 2011; 32: 558-68.
153. Gullichsen E, Nelimarkka O, Halkola L, Niinikoski J. Renal oxygenation in endotoxin shock in dogs. Crit. Care Med. 1989; 17: 547-50.
154. Seely KA, Holthoff JH, Burns ST 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: F209-17.
155. Melican K, Boekel J, Mansson LE et al. Bacterial infection-mediated mucosal signalling induces local renal ischaemia as a defence against sepsis. Cell. Microbiol. 2008; 10: 1987-98.
156. Melican K, Sandoval RM, Kader A et al. Uropathogenic Escherichia coli P and Type 1 fimbriae act in synergy in a living host to facilitate renal colonization leading to nephron obstruction. PLoS Pathog. 2011; 7: e1001298.
157. Hansell P, Welch WJ, Blantz RC, Palm F. Determinants of kidney oxygen consumption and the relation to tissue oxygen tension in diabetes and hypertension. Clin. Exp. Pharmacol. Physiol. 2013; 40: 123-137.
158. Balestra GM, Legrand M, Ince C. Microcirculation and mitochondria in sepsis. Getting out of breath. Curr. Opin. Anaesthesiol. 2009; 22: 184-90.
159. Legrand M, Mik EG, Balestra GM et al. Fluid resuscitation does not improve renal oxygenation during hemorrhagic shock in rats. Anesthesiology 2010; 112: 119-27.
160. Maerz L, Kaplan LJ. Abdominal compartment syndrome. Crit. Care Med. 2008; 36(Suppl.): S212-15.
161. Johannes T, Mik EG, Klingel K, Dieterich HJ, Unertl KE, Ince C. Low-dose dexamethasone-supplemented fluid resuscitation reverses endotoxin-induced acute renal failure and prevents cortical microvascular hypoxia. Shock 2009; 31: 521-8.
162. Calzia E, Asfar P, Hauser B et al. Hyperoxia may be beneficial. Crit. Care Med. 2010; 38(Suppl.): S559-68.
163. Efrati S, Berman S. Ben Aharon G, Siman-Tov Y, Averbukh Z, Weissgarten J. Application of normobaric hyperoxia therapy for amelioration of haemorrhagic shock-induced acute renal failure. Nephrol. Dial. Transplant. 2008; 23: 2213-22.
164. Nangaku M, Rosenberger C, Heyman SN, Eckardt K-U. HIF regulation in kidney disease. Clin. Exp. Pharmacol. Physiol. 2013; 40: 148-157.
165. Eppel GA, Malpas SC, Denton KM, Evans RG. Neural control of renal medullary perfusion. Clin. Exp. Pharmacol. Physiol. 2004; 31: 387-96.