Impact of Metabolism on Surviving Sepsis:
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1 Impact of Metabolism on Surviving Sepsis: Implications for Sepsis-Induced AKI Sarah Huen M.D., Ph.D. UT Southwestern Medical Center Internal Medicine-Nephrology, Pharmacology AKI & CRRT 2019
2 Overview Defining Sepsis 3 Metabolic Examples of Uncertainty Glycemia, Nutrition, Venous O2 saturation Role of Anorexia in Acute Illness Metabolism as Disease Tolerance in Host Defense Implications of Metabolism as Disease Tolerance in Septic Acute Kidney Injury
3 Sepsis Life-threatening organ dysfunction owing to dysregulated host response to infection Incidence rising 13% / year Kidney, Lung, Heart, Liver/GI, CNS Dysfunction 10% hospitalizations 50% in-hospital mortality #1 most expensive hospital diagnosis Singer et al JAMA 2016 Martin et al NEJM 2003 Gaieski et al Crit Care Med 2013 Agency for Healthcare Research and Quality (AHRQ) 2013
4 Sepsis: Dysglycemia in Critically Ill Mortality Risk Blood Glucose (mg/dl) Adapted from Mesotten & Van den Berghe 2009 Van Wyngene, Vandewalle, Libert EMBO 2018
5 Sepsis: Role in Normalizing Glycemia Probability of Survival P=0.03 Conventional Glucose Control Intensive Glucose Control More insulin exposure More glucose exposure More hypoglycemic events Not stratified by type of critical illness Days after Randomization NICE SUGAR Trial NEJM 2009
6 Optimal ICU Nutrition Unclear 835 kcal vs 1300 kcal Control protein, volume* No Stratification by Type of critical illness Type of infection Arabi et al NEJM 2015
7 Optimal ICU Nutrition Unclear 1.0 kcal/ml (1262) vs 1.5 kcal/ml (1863) Control protein, volume No Stratification by Type of critical illness Type of infection TARGET/ANZICS Trial NEJM 2018
8 Meaning of Central Venous O2? Early Goal Directed Therapy (EGDT) Inotropes & RBC transfusion To Increase O2 Delivery 3 Large Multi-Center Trials No benefit to EGDT O2 Delivery vs. O2 Consumption/Extraction (EGDT) Rivers et al NEJM 2001 (ProCESS) Yealy et al NEJM 2014 (ARISE) Peake et al NEJM 2014 (ProMISE) Mouncey et al NEGM 2015
9 O2 Consumption: Protective, Maladaptive, or Sign of Failure of Recovery? 90 Max ScvO2 (%) Non-Survivors Survivors Small Retrospective Cohort n=152, septic shock, at least 2 ScvO2 samples within 72 hours of shock Textoris et al Crit Care 2011
10 Energy Expenditure in Sepsis Sepsis: Clinical evidence of infection or positive blood culture Rectal Temp > 38.3 C or <35.5 C Heart rate > 90 Resp rate > 20 Sepsis syndrome: + at least 1 of the following: Altered mental status Hypoxemia Decreased urine production Septic shock: + Volume repletion unsuccessful to stabilized MAP > 65 mmhg Kreymann et al 1993 Crit Care Clin Sepsis Sepsis Syndrome Septic Shock Recovery
11 Phases of Sepsis: Inflammatory State Secondary Infection Hotchkiss et al Nat Med 2009
12 Phases of Sepsis: Metabolic State Change from baseline + - Time Death Acute phase Chronic phase Recovery Conserved Sickness Behavior: Anorexia Lethargy/Malaise Conservation / Reorganization of Energy Expenditure? OR Maladaptive in face of hypercatabolic state? Mongardon & Singer Crit Care Clin 2010
13 Sickness Behavior: Purpose of Anorexia in Acute Illness Mouse Models of Infection Food Consumption after Listeria Infection 4 Food Consumption after Influenza Infection 4 Grams food/mouse Grams food/mouse Days post infection Uninfected Listeria Days post infection Uninfected Flu Wang, Huen, Luan Medzhitov Cell 2016
14 Glucose is Lethal in Listeria Infection Inhibition of Glucose Utilization is Lethal in Influenza Infection Listeria Survival Influenza Survival Percent survival 50 Percent survival PBS Food (Abbott Promote) Days post infection Glucose 2DG (glucose analog) PBS Food (Abbott Promote) Days post infection Glucose 2DG (glucose analog) Abbott Promote 25% Protein 52% Carbs 23% Fat Normal Chow 24% Protein 58% Carbs 18% Fat Wang, Huen, Luan Medzhitov Cell 2016
15 Glucose is Lethal in Listeria Infection Inhibition of Glucose Utilization is Lethal in Influenza Infection Listeria Survival Influenza Survival Percent survival 50 Percent survival PBS Food (Abbott Promote) Days post infection Glucose 2DG (glucose analog) PBS Food (Abbott Promote) Days post infection Glucose 2DG (glucose analog) Independent of pathogen load, inflammation Effect phenocopied with LPS and Poly(I:C) Wang, Huen, Luan Medzhitov Cell 2016
16 Host Defense Against Infection Pathogen Immune System Other Tissues Pathogen Clearance Resistance Limit Tissue Damage Cellular Adaptation Physiologic/Metabolic Adaptation Tolerance
17 Host Defense Against Infection Pathogen Immune System Pathogen Clearance LPS+glucose seizures Poly(I:C)+2DG HR RR Resistance Tolerance
18 Brain Glucose Distribution Differs with Type of Inflammation ROI T2 CT Baseline LPS PolyIC Hypothalamus Wang, Huen, Luan Medzhitov Cell 2016
19 Brain Glucose Distribution Differs with Type of Inflammation ROI T2 CT Baseline LPS PolyIC Brainstem Wang, Huen, Luan Medzhitov Cell 2016
20 Mechanism for 2DG-mediated Death in Viral Inflammation?
21 Viral Infection and ER Stress ER Stress Unfolded Protein Response (UPR) UPR target genes CHOP (Ddit3) Resolution of ER Stress Apoptosis
22 Inhibition of glucose utilization dysregulates unfolded protein response CHOP β-actin WT Poly(I:C) Poly(I:C) +2DG 100 Ifnar -/- Percent survival Poly(I:C) Poly(I:C) +2DG 50 Poly(I:C)+2DG Survival Hours post injection Whole Hindbrain Lysate WB 24 hours after Poly(I:C) ± 2DG WT: Poly(I:C) WT: Poly(I:C) + 2DG CHOP KO: Poly(I:C) CHOP KO: Poly(I:C) + 2DG Wang, Huen, Luan Medzhitov Cell 2016
23 Mechanism for Glucose-mediated Death in Bacterial Inflammation? Fasting Metabolism Adipose Lipolysis FFA Liver Ketogenesis Ketones (BHOB) Brain PPARα FGF21 Enhances Ketogenesis Stimulates Gluconeogenesis Growth hormone resistance Disruption of hypothalamic-pituitary-ovarian axis LPS+Glucose Seizures (no difference in blood glucose)
24 Mechanism Glucose Supplementation for Glucose-mediated Suppresses Death LPS-induced Bacterial Fasting Inflammation? Metabolism Fasting Metabolism Adipose Lipolysis Free Fatty Acids (FFA) Liver Ketogenesis PPARa Ketones (BHB) FGF21 Brain LPS-induced Fasting Metabolism Plasma Free Fatty Acids (FFA) mm 2.0 *** PBS Glucose Hours post injection mm Plasma Ketones (BHB) **** Hours post LPS injection ng/ml Plasma FGF21 **** *** Hours post LPS injection
25 Glucose Supplementation Increases Mechanism for Glucose-mediated Death Oxidative Stress in the Brain in Bacterial Inflammation? During LPS Sepsis Fasting Metabolism Adipose Lipolysis Liver Ketogenesis Free Fatty Acids (FFA) LPS PBS Brain PPARa Ketones (BHB) FGF21 LPS Glucose Dihydroethidium Staining of Brain (Reactive Oxygen Species)
26 Fasting Metabolic Programs Protect Against LPS Sepsis Mortality Fasting Metabolism Adipose Lipolysis Free Fatty Acids (FFA) Liver Ketogenesis PPARa Ketones (BHB) FGF21 Brain ng/ml Plasma FGF Hours post injection WT Fgf21 -/- Ppara -/- mm BHB WT Fgf21 -/ Hours post injection mm BHB **** WT Ppara -/ Hours post injection Percent survival LPS Survival WT Fgf21 -/- Ppara -/ Hours post LPS injection Wang, Huen, Luan Medzhitov Cell 2016
27 Fasting Metabolic Programs Protect Against Mechanism for Glucose-mediated Death LPS Sepsis Mortality in Bacterial Inflammation? Fasting Metabolism Adipose Lipolysis Free Fatty Acids (FFA) Liver Ketogenesis PPARa Ketones (BHB) FGF21 Brain Percent survival LPS Survival WT Fgf21 -/- Ppara -/ Hours post LPS injection Percent survival LPS Survival Duration of therapy Hours post injection Fgf21 -/- VEH Fgf21 -/- rmfgf21 Percent survival LPS Survival Duration of therapy Hours post injection Ppara -/- VEH Ppara -/- rmfgf21
28 Fasting Metabolism in Bacterial Inflammation Fasting metabolism is associated with improved survival in bacterial inflammation FGF21 and PPARa/ketogenesis promote survival in bacterial sepsis via different mechanisms Open questions: How does FGF21 promote survival in sepsis? Is ketogenesis per se required for survival or merely a byproduct of fasting metabolism?
29 Context Specific Metabolic Adaptation During Inflammation Bacterial Inflammation Viral Inflammation Reactive Oxygen Species Glucose Unfolded Protein Response Ketones Ketones Glucose Glucose Adaptation Dysfunction Adaptation Dysfunction Wang, Huen, Luan Medzhitov Cell 2016
30 Implications for the Management of Septic Patients Changes in metabolism as part of immune defense Metabolic changes differ depending on type of infection Optimal nutritional management will differ depending on type of infection (or, cause of inflammation) Purpose and regulation of metabolic changes during sepsis not completely understood Dismal outcomes in patients with septic kidney injury requiring dialysis despite normalizing electrolytes, acid-base, volume Missing some other metabolic component? Could nutritional/energy sources affect renal outcomes depending on type of inflammation?
31 Septic AKI: Pathophysiology: Differences from Acute Tubular Necrosis Normal ATN Sepsis AKI Sepsis AKI Takasu et al AJP Resp Crit Care Med 2013
32 Septic AKI: Pathophysiology Pathogen associated Molecular Patterns Direct toxicity Indirect toxicity (cytokines) Hemodynamic? Hypoperfusion Ischemia-reperfusion Endogenous Microthrombosis Heme proteins Exogenous Antibiotics Contrast Vasopressors Hypoxia Oxidative Stress Endothelial dysfunction *Mitochondrial dysfunction **Protein Translational Shutdown Energy Homeostasis Substrate Preference? Temporal Dynamics? Renal Cell Injury Adapted from Ronco C et al CJASN 2008 *Parikh, S. Curr Opin Crit Care 2013 *Gómez, Kellum, Ronco Nat Rev Nephrol 2017 **Hato et al JCI 2019
33 Phases of Sepsis: Metabolism Change from baseline + - Nutrient / Metabolic Interventions? Time Death Modifiers: Time Dependence? Organ Specificity? Type of Infection? Potential for macronutrient / caloric mismatch / mis-timing disrupting protective adaptive metabolic programs? Acute phase Glycolysis Autophagy Chronic phase Recovery Fatty acid Oxidation Mitochondrial Biogenesis Septic Renal Metabolism Protective vs Maladaptive? Regulation? Local vs Distant effects? Figure adapted from Mongardon & Singer Crit Care Clin 2010 Gómez & Kellum Curr Opin Crit Care 2016
34 Acknowledgements Huen Lab Kyle Feola Richard Hogg Andrea Venable UTSW-Pharmacology David Mangelsdorf Steven Kliewer FGF21 Yale Ruslan Medzhitov Andrew Wang Harding Luan The George M. O Brien Kidney Center (Yale & UTSW) Kidney Cancer Program (UTSW) UTSW DOCS Award
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