Mitochondrial dysfunction in a long-term rodent model of sepsis and organ failure.

Although sepsis is the major cause of mortality and morbidity in the critically ill, precise mechanism(s) causing multiorgan dysfunction remain unclear. Findings of impaired oxygen utilization in septic patients and animals implicate nitric oxide-mediated inhibition of the mitochondrial respiratory chain. We recently reported a relationship between skeletal muscle mitochondrial dysfunction, clinical severity, and poor outcome in patients with septic shock. We thus developed a long-term, fluid-resuscitated, fecal peritonitis model utilizing male Wistar rats that closely replicates human physiological, biochemical, and histological findings with a 40% mortality. As with humans, the severity of organ dysfunction and eventual poor outcome were associated with nitric oxide overproduction and increasing mitochondrial dysfunction (complex I inhibition and ATP depletion). This was seen in both vital (liver) and nonvital (skeletal muscle) organs. Likewise, histological evidence of cell death was lacking, suggesting the possibility of an adaptive programmed shutdown of cellular function. This study thus supports the hypothesis that multiorgan dysfunction induced by severe sepsis has a bioenergetic etiology. Despite the well-recognized limitations of laboratory models, we found clear parallels between this long-term model and human disease characteristics that will facilitate future translational research.

[1]  P. Boekstegers,et al.  Peripheral oxygen availability within skeletal muscle in sepsis and septic shock: Comparison to limited infection and cardiogenic shock , 1991, Infection.

[2]  Guy C. Brown Nitric oxide inhibition of cytochrome oxidase and mitochondrial respiration: Implications for inflammatory, neurodegenerative and ischaemic pathologies , 1997, Molecular and Cellular Biochemistry.

[3]  L. Carbonell,et al.  Oxidative stress in critically ill patients with systemic inflammatory response syndrome , 2002, Critical care medicine.

[4]  John Land,et al.  Association between mitochondrial dysfunction and severity and outcome of septic shock , 2002, The Lancet.

[5]  E. Clementi,et al.  Nitric oxide inhibits mitochondrial NADH:ubiquinone reductase activity through peroxynitrite formation. , 2001, The Biochemical journal.

[6]  D. Hoyert,et al.  Age-adjusted death rates: trend data based on the year 2000 standard population. , 2001, National vital statistics reports : from the Centers for Disease Control and Prevention, National Center for Health Statistics, National Vital Statistics System.

[7]  K D Kochanek,et al.  Deaths: final data for 1999. , 2001, National vital statistics reports : from the Centers for Disease Control and Prevention, National Center for Health Statistics, National Vital Statistics System.

[8]  G. Clermont,et al.  Epidemiology of severe sepsis in the United States: Analysis of incidence, outcome, and associated costs of care , 2001, Critical care medicine.

[9]  I. Németh,et al.  Xanthine oxidase activity and blood glutathione redox ratio in infants and children with septic shock syndrome , 2001, Intensive Care Medicine.

[10]  C. Cooper,et al.  Effects of nitric oxide and peroxynitrite on the cytochrome oxidase K(m) for oxygen: implications for mitochondrial pathology. , 2000, Biochimica et biophysica acta.

[11]  G. Brown,et al.  Reversal of nitric oxide-, peroxynitrite- and S-nitrosothiol-induced inhibition of mitochondrial respiration or complex I activity by light and thiols. , 2000, Biochimica et biophysica acta.

[12]  S. Heales,et al.  Astrocyte‐Derived Nitric Oxide Causes Both Reversible and Irreversible Damage to the Neuronal Mitochondrial Respiratory Chain , 2000, Journal of neurochemistry.

[13]  D. Bredt,et al.  Nitric oxide mediated induction of cytochrome c oxidase mRNA and protein in a mouse macrophage cell line , 2000, Neuroscience Letters.

[14]  E. Clementi,et al.  Oxidative stress and S‐nitrosylation of proteins in cells , 2000, British journal of pharmacology.

[15]  M. Singer,et al.  Mitochondrial dysfunction in sepsis , 2003, Current infectious disease reports.

[16]  R. Hotchkiss,et al.  Apoptotic cell death in patients with sepsis, shock, and multiple organ dysfunction. , 1999, Critical care medicine.

[17]  C. Ince,et al.  Microcirculatory oxygenation and shunting in sepsis and shock. , 1999, Critical care medicine.

[18]  M. Titheradge Nitric oxide in septic shock. , 1999, Biochimica et biophysica acta.

[19]  J. Bolaños,et al.  The assumption that nitric oxide inhibits mitochondrial ATP synthesis is correct , 1999, FEBS letters.

[20]  A. Schapira,et al.  Mitochondrial involvement in Parkinson's disease, Huntington's disease, hereditary spastic paraplegia and Friedreich's ataxia. , 1999, Biochimica et biophysica acta.

[21]  S. Heales The biochemical investigation of mitochondrial respiratory chain disorders , 1999 .

[22]  S. Moncada,et al.  Nitric oxide and the haemodynamic profile of endotoxin shock in the conscious mouse , 1998, British journal of pharmacology.

[23]  G. Giovannoni,et al.  Adaptation of the Nitrate Reductase and Griess Reaction Methods for the Measurement of Serum Nitrate plus Nitrite Levels , 1997, Annals of clinical biochemistry.

[24]  K. Andersson,et al.  Skeletal muscle glutathione is depleted in critically ill patients. , 1997, Critical care medicine.

[25]  D. Hearse Myocardial hibernation. A form of endogenous protection? , 1997, European heart journal.

[26]  D. Menon,et al.  Plasma antioxidant potential in severe sepsis: a comparison of survivors and nonsurvivors. , 1996, Critical care medicine.

[27]  J. Bolaños,et al.  Nitric oxide-mediated mitochondrial damage: a potential neuroprotective role for glutathione. , 1996, Free radical biology & medicine.

[28]  M. Singer,et al.  Oxygen tension in the bladder epithelium rises in both high and low cardiac output endotoxemic sepsis. , 1995, Journal of applied physiology.

[29]  C. Cooper,et al.  Nanomolar concentrations of nitric oxide reversibly inhibit synaptosomal respiration by competing with oxygen at cytochrome oxidase , 1994, FEBS letters.

[30]  S. Matthaei,et al.  Oxygen consumption and resting metabolic rate in sepsis, sepsis syndrome, and septic shock , 1993, Critical care medicine.

[31]  A. Nakao,et al.  Changes in the glutathione redox system during ischemia and reperfusion in rat liver. , 1992, Scandinavian journal of gastroenterology.

[32]  E. Deitch,et al.  Multiple organ failure. Pathophysiology and potential future therapy. , 1992, Annals of surgery.

[33]  R. Smolenski,et al.  Determination of sixteen nucleotides, nucleosides and bases using high-performance liquid chromatography and its application to the study of purine metabolism in hearts for transplantation. , 1990, Journal of chromatography.

[34]  Peter Riederer,et al.  Transition Metals, Ferritin, Glutathione, and Ascorbic Acid in Parkinsonian Brains , 1989, Journal of neurochemistry.

[35]  B Eiseman,et al.  Multiple organ failure. , 1977, Surgery, gynecology & obstetrics.

[36]  O. H. Lowry,et al.  Protein measurement with the Folin phenol reagent. , 1951, The Journal of biological chemistry.