Hyperoxia Increases Kidney Injury During Renal Ischemia and Reperfusion in Mice

Anesth Analg. 2023 Nov 1;137(5):996-1006. doi: 10.1213/ANE.0000000000006600. Epub 2023 Oct 20.

Abstract

Background: Renal ischemia and reperfusion (IR) contribute to perioperative acute kidney injury, and oxygen is a key regulator of this process. We hypothesized that oxygen administration during surgery and renal IR would impact postoperative kidney function and injury in mice.

Methods: Mice were anesthetized, intubated, and mechanically ventilated with a fraction of inspired oxygen (F io2 ) 0.10 (hypoxia), 0.21 (normoxia), 0.60 (moderate hyperoxia), or 1.00 (severe hyperoxia) during 67 minutes of renal IR or sham IR surgery. Additional mice were treated before IR or sham IR surgery with 50 mg/kg tempol, a superoxide scavenger. At 24 hours, mice were sacrificed, and blood and kidney collected. We assessed and compared kidney function and injury across groups by measuring blood urea nitrogen (BUN, primary end point), renal histological injury, renal expression of neutrophil gelatinase-associated lipocalin (NGAL), and renal heme oxygenase 1 ( Ho-1 ), peroxisome proliferator-activated receptor gamma coactivator 1-α ( Pgc1-α ), and glutathione peroxidase 4 ( Gpx-4 ) transcripts, to explore potential mechanisms of any effect of oxygen.

Results: Hyperoxia and hypoxia during renal IR surgery decreased renal function and increased kidney injury compared to normoxia. Baseline median (interquartile range) BUN was 22.2 mg/dL (18.4-26.0), and 24 hours after IR surgery, BUN was 17.5 mg/dL (95% confidence interval [CI], 1.3-38.4; P = .034) higher in moderate hyperoxia-treated animals, 51.8 mg/dL (95% CI, 24.9-74.8; P < .001) higher in severe hyperoxia-treated animals, and 64.9 mg/dL (95% CI, 41.2-80.3; P < .001) higher in hypoxia-treated animals compared to animals treated with normoxia ( P < .001, overall effect of hyperoxia). Hyperoxia-induced injury, but not hypoxia-induced injury, was attenuated by pretreatment with tempol. Histological injury scores, renal NGAL staining, and renal transcription of Ho-1 and suppression of Pgc1- α followed the same pattern as BUN, in relation to the effects of oxygen treatment.

Conclusions: In this controlled preclinical study of oxygen treatment during renal IR surgery, hyperoxia and hypoxia impaired renal function, increased renal injury, and impacted expression of genes that affect mitochondrial biogenesis and antioxidant response. These results might have implications for patients during surgery when high concentrations of oxygen are frequently administered, especially in cases involving renal IR.

MeSH terms

  • Acute Kidney Injury* / etiology
  • Acute Kidney Injury* / metabolism
  • Acute Kidney Injury* / pathology
  • Acute Kidney Injury* / physiopathology
  • Acute-Phase Proteins / genetics
  • Acute-Phase Proteins / metabolism
  • Animals
  • Blood Urea Nitrogen
  • Cyclic N-Oxides / pharmacology
  • Disease Models, Animal
  • Heme Oxygenase-1 / genetics
  • Heme Oxygenase-1 / metabolism
  • Hyperoxia* / complications
  • Hyperoxia* / metabolism
  • Kidney* / metabolism
  • Kidney* / pathology
  • Lipocalin-2 / genetics
  • Lipocalin-2 / metabolism
  • Male
  • Membrane Proteins
  • Mice
  • Mice, Inbred C57BL*
  • Oxygen / metabolism
  • Oxygen Inhalation Therapy
  • Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha / genetics
  • Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha / metabolism
  • Proto-Oncogene Proteins / genetics
  • Proto-Oncogene Proteins / metabolism
  • Reperfusion Injury* / metabolism
  • Reperfusion Injury* / pathology
  • Spin Labels
  • Transcription Factors / genetics
  • Transcription Factors / metabolism

Substances

  • Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha
  • Lcn2 protein, mouse
  • Lipocalin-2
  • Ppargc1a protein, mouse
  • Hmox1 protein, mouse
  • Acute-Phase Proteins
  • Proto-Oncogene Proteins
  • Spin Labels
  • Transcription Factors
  • Oxygen
  • tempol
  • Cyclic N-Oxides
  • Heme Oxygenase-1
  • Membrane Proteins