Harm by hyperglycemia, early (parenteral) nutrition or both? from bed to bench and back
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1 Harm by hyperglycemia, early (parenteral) nutrition or both? from bed to bench and back G. Van den Berghe MD, PhD Department of Intensive Care Medicine University of Leuven (KU Leuven) Leuven, Belgium
2 Conflict of interest statement Funding Institute for Science and Technology (IWT), Flanders, Belgium Methusalem program, Flemish Government Research Foundation, Flanders, Belgium (FWO) EU 7th FP, ERC Advanced Grant
3 Cause of hyperglycemia in ICU patients Increased glycogenolysis/gluconeogenesis Resistant to exogenous nutrition Driven by counter-regulatory stress hormones (cortisol, glucagon, catecholamines, growth hormone, )? Not many good studies Reduced peripheral glucose uptake Due to insulin resistance Which tissues? Not many good studies
4 Cause of hyperglycemia in ICU patients Increased glycogenolysis/gluconeogenesis Resistant to exogenous nutrition Driven by counter-regulatory stress hormones (cortisol, glucagon, catecholamines, growth hormone, )? Not many good studies Reduced peripheral glucose uptake Due to insulin resistance Which tissues? Not many good studies
5 MORTALITY Association hyperglycemia and death Don t touch hypo normal for age renal threshold BLOOD GLUCOSE
6 MORTALITY Association hyperglycemia and death: causal? Don t touch hypo normal for age renal threshold BLOOD GLUCOSE
7 MORTALITY Association hyperglycemia and death: causal? Don t touch hypo normal for age renal threshold BLOOD GLUCOSE
8 Controversy is ongoing until today
9 Association hyperglycemia and death: causal?
10 MORTALITY Association hyperglycemia and death: causal? The Leuven comparison Don t touch hypo normal for age renal threshold BLOOD GLUCOSE
11 How did we do this? Arterial blood for blood glucose monitoring ABL blood gas analyzer Frequent blood glucose sampling (0.5h-4h) Continuous IV insulin (regular) infusion Syringe pump for insulin infusion Central venous line for insulin infusion (connection of infusion as close as possible to patient; dedicated lumen) Nurse driven guideline; most patients included While providing early EN+PN
12 Blood glucose control Conventional Intensive S-ICU M-ICU Medians Boxes = IQR Whiskers = P10-P90 60 admission peak day 1 60 >1- to last day admission peak day 1 >1- to last day N Engl G.V.d.B., J Med. K.U.Leuven 2001 & 2006
13 Mixed M-ICU / S-ICU population (N=2748) Van den Berghe G et al. NEJM 2001; NEJM 2009; DIABETES 2006 Cumulative risk for in-hospital mortality Intention-to-treat (N = 2748) In ICU at least 3 days (N = 1389) %.2.1-8% p = p = Hosp mort 24% -> 20% Hosp mort 38% -> 30% Conventional Intensive
14 Mixed M-ICU / S-ICU population (N=2748) Van den Berghe G et al. NEJM 2001; NEJM 2009; DIABETES 2006 % new kidney injury p < first EMG positive for CIPNP Cumulative hazard Conventional Intensive conventional intensive p < days after inclusion
15 Post-hoc comparison in M-ICU / S-ICU population (N=2748) Cumulative risk in-hospital mortality % new kidney injury NS * first EMG positive for CIPNP Cum hazard ** * p = p = mean BG > 150 mg/dl mean BG mg/dl mean BG <110 mg/dl Van den Berghe G et al. NEJM 2001; NEJM 2009; DIABETES 2006
16 Survival effect: glucose control! ICU 1 0,9 0,8 0,7 0,6 0,5 0, NI/NG n=8 HI/NG n=8 NI/HG n=9 HI/HG n=8 Normal insulin NORMOGLYCEMIC GROUPS High insulin Normal insulin HYPERGLYCEMIC GROUPS High insulin Ellger B, Debaveye Y et al. DIABETES 2006; 55:
17 Kidney damage by hyperglycemia Vanhorebeek I et al. Kidney International, 2009 ICU tubules with flattening and/or loss of tubular epithelium and filled with debris tubules with flattening and/or loss of tubular epithelium and with calcifications in the lumen Normal Mild Moderate Severe Healthy NI/NG HI/NG NI/HG HI/HG
18 Liver (mitochondrial) damage by hyperglycemia ICU Normal Moderate Severe Vanhorebeek I et al. Crit Care Med 2008 Control NI/NG HI/NG NI/HG HI/HG Control HI/HG HI/HG
19 Human data : hyperglycemia is toxic for mitochondria during CI Conventional : 78% abnormal <P=0.002> Intensive : 11% abnormal Vanhorebeek I, et al. Lancet 2005; 365: 53-59
20 Improved leukocyte function Reduced inflammation (Ellger Diabetes 2006) Strict blood glucose control with IIT Improved liver, kidney mitochondrial ultrastructure and function (Vanhorebeek The Lancet 2005, Kidney Int 2009) (Schetz, JASN 2008) Reduced endothelial activation (Langouche JCI 2005) Improved cardiac contractility (Ellger Diabetes 2006) Prevented dyslipidemia (Mesotten JCEM 2004) Protection of central & peripheral nervous system (Van den Berghe, Vanhorebeek, )
21 Intensive insulin therapy for patients in pediatric intensive care: A prospective randomized controlled study Vlasselaers D, Milants I, Desmet L, Wouters PJ, Vanhorebeek I, van den Heuvel I, Mesotten D, Casaer MP, Meyfroidt G, Ingels C, Muller J, Van Cromphaut S, Schetz M, Van den Berghe G Lancet 2009; 373:
22 Blood glucose (mmol/l) Age-adjusted glucose control in PICU study 11.0 Infants (aged < 1 y) Children (aged >= 1 y) TGC Usual care mg/dl mg/dl 2.2 Vlasselaers et al. Lancet LD LD Days after ICU admission
23 Blood glucose (mmol/l) Age-adjusted glucose control in PICU study 11.0 Infants (aged < 1 y) Children (aged >= 1 y) TGC Usual care mmol/l 4.8 mmol/l 115 mg/dl 86 mg/dl 8.2 mmol/l 5.3 mmol/l 148 mg/dl 95 mg/dl Boxes : Med & IQR Vlasselaers et al. Lancet LD LD Days after ICU admission
24 Age-adjusted glucose control in PICU : reduced mortality Cumulative incidence of PICU death (%) p = % 5.7% Usual care TGC N = 700 Vlasselaers et al. Lancet days after admission
25 Hypoglycemia increased substantially Hypoglycemia (safety endpoint) Number of patients with hypoglycemia (<40 mg/dl, <2.2 mmol/l) Usual care TGC p-value 5 (1.4%) 87 (24.9%) <0.0001
26 Frontal Cortex Hippocampus Hyperglycemia?? Hypoglycemia?
27
28 Poor outcomes at follow-up (4 y after inclusion) Usual Care TGC P Death at FU (%) 11 % 9 % 0.4 risk adjusted OR death at FU (95% CI) 0.45 ( ) 0.03
29 With IIT: better executive function after 4 years! Healthy Tested post ICU P (TGC vs. UC) UC TGC Tested Imputed (N=216) (N=234) (N=222) Alertness RT Dominant hand (msec) 488 ( ) 679 ( ) 641 ( ) RT Non-dominant hand (msec) 501 ( ) 647 ( ) 612 ( ) Motor coordination N unimanual taps Dominant hand 35 (25-46) 28 (21-37) 30 (23-42) Non-dominant hand 29 (21-43) 23 (17-31) 25 (19-36) N valid synchronous taps 21 (12-31) 15 (8-23) 18 (10-27) Inhibition & flexibility RT (inhibition) (msec) 209 (80-487) 340 ( ) 259 ( ) RT (flexibility) (msec) 550 ( ) 679 ( ) 548 ( )
30 Hyperglycemia neuronal damage in rabbit CI ICU CONTROL HYPERGLYCEMIA NORMOGLYCEMIA R. Sonneville, J Clin Endocrinol Metab 2012
31 Hyperglycemia microglial activation in rabbit CI ICU CONTROL HYPERGLYCEMIA NORMOGLYCEMIA R. Sonneville, J Clin Endocrinol Metab 2012
32 Hypoglycemia in Leuven: no harm on the developing brain Neuron (NSE ng/ml) Astrocyte (S100b pg/ml) No hypo hypo No effect of hypoglycemia before 24h after before 24h after Means +/- 95% CI Vanhorebeek I, Gielen M et al. JCEM 2010
33 In NICE-SUGAR : Hypoglycemia explained harm Finfer S et al. NEJM 2012; 367:1108
34 Outcome of NICE-SUGAR (N=6100) no difference in organ function more cardiovascular deaths hypoglycemia x 13 The NICE-SUGAR investigators. N Engl J Med 2009; 360:
35 Why these different results in NICE-SUGAR?
36 Why these different results in NICE-SUGAR? As compared with the Leuven studies: 1) Lower target range for blood glucose in the control group 2) Poor accuracy of the meters used for blood glucose 3) Poor algorithm
37 MORTALITY Lower Target in Control Group of NICE-SUGAR The Leuven comparison The NICE-SUGAR comparison Don t touch hypo normal for age renal threshold BLOOD GLUCOSE
38 NICE-SUGAR: inaccurate blood glucose meters... the NICE-SUGAR study should be repeated with more attention paid to the accuracy of the glucose measuring device (reported by a Nice-Sugar participating center, Alberta Canada) Cembrowski G et al. Clin Chem 2010; 56: 7
39 Different algorithm performances Nurses in Leuven Vs. NICE-SUGAR If-then algorithm
40 The Leuven algorithm computerized version : LOGIC-Insulin Van Herpe T et al. Diabetes Care 2012
41 Blood glucose (mg/dl) LOGIC Insulin RCT - II unpublished results AMC JESSA LEUVEN Target range BG (mg/dl)
42 Why these different results in NICE-SUGAR? As compared with the Leuven studies: 1) Lower target range for blood glucose in the control group 2) Poor accuracy of the meters used for blood glucose 3) Poor algorithm 4) No early PN
43 Is all this about blood glucose concentration or about infusion of glucose via parenteral nutrition? Van den Berghe et al. NEJM 2001, NEJM 2006, Lancet 2009, NEJM 2011, JAMA 2012, NEJM 2013, NEJM 2016
44 Accumulated macronutrient deficit: associated with adverse outcome Villet et al. Clinical Nutrition 2005
45 EPaNIC RCT & PEPaNIC RCT 2 multicenter randomized controlled trials : Different strategies
46 2011; 365:
47 Nutrition administered Adult multi-center RCT EPaNIC Pediatric multi-center RCT PEPaNIC EN PN TOTAL Casaer M et al. N Engl J Med 2011; 365: Fivez T et al. N Engl J Med 2016; 374:
48 EPaNIC : In both groups Enteral nutrition initiated on day 2 Vitamins, trace elements, minerals administered early Overfeeding and hyperglycemia avoided Late PN Early PN Insulin dose 31 (19 48) IU 58 (40 85) IU P < Blood glucose levels 102 ± 14 mg/dl 107 ± 18 mg/dl P < Casaer M et al. N Engl J Med 2011; 365:
49 Not giving PN: higher likelihood for earlier live discharge! Adult multi-center RCT EPaNIC Pediatric multi-center RCT PEPaNIC Casaer M et al. N Engl J Med 2011; 365: Fivez T et al. N Engl J Med 2016; 374:
50 Due to fewer infections and faster recovery of organ damage Fivez T et al. N Engl J Med 2016; 374:
51 Not glucose, but amino acids appeared deleterious Casaer M et al. AJRCCM 2012
52 Not glucose, but amino acids appeared deleterious Casaer M et al. AJRCCM 2012
53 Not glucose, but amino acids appeared deleterious Casaer M et al. AJRCCM 2012
54 Different from other studies? How much is given early?
55 Let s compare EPANIC with other studies EDEN (N=1000) Early PN (N=1372) EPaNIC (N=4640) SPN (N=305) TICACOS (N=130) Casaer MP, Van den Berghe G. NEJM 2014; 370:
56 Let s compare EPANIC with other studies EDEN (N=1000) Early PN (N=1372) EPaNIC (N=4640) SPN (N=305) TICACOS (N=130) Casaer MP, Van den Berghe G. NEJM 2014; 370:
57 Let s compare EPANIC with other studies EDEN (N=1000) Early PN (N=1372) EPaNIC (N=4640) SPN (N=305) TICACOS (N=130) Benefit of early feeding in ITT analysis? NO NO (tertiary endpoint : fewer ventilator-free days) Outcome worse with early PN Fewer infections between day 9 and 28 (no effect between day 4 and 28) NO (morbidity worse with more PN) Casaer MP, Van den Berghe G. NEJM 2014; 370:
58 Maybe it has to do with how?
59 Role of the route of feeding: enteral or parenteral?
60 Role of the route of feeding: enteral or parenteral? N=2400 Harvey SE et al. N Engl J Med 2014; 371:
61 Role of the route of feeding: enteral or parenteral? Harvey SE et al. N Engl J Med 2014; 371:
62 Why?
63 Why? What do we know about recovery from CI.
64 Recovery from CI = cell damage removal
65 Autophagy
66 Autophagy Christian De Duve (BELGIUM) Nobel prize Medicine 1974 Yoshinori Ohsumi (JAPAN) Nobel prize Medicine 2016
67 Phenotype of autophagy-deficiency in muscle (KO mice) Masiero E, et al. Cell Metabolism 2009
68 Fasting & feeding : physiological regulators of autophagy Nutrients (AA) Insulin Growth factors
69 Nutrients and autophagy in critical illness Derde S, et al. Endocrinology 2012
70 Phenotype of impaired autophagy with PN Derde S, et al. Endocrinology 2012
71 Phenotype of impaired autophagy with PN Derde S, et al. Endocrinology 2012
72 Autophagy during (fed) critical illness
73 The difference in protein intake was large in EPaNIC Hermans G et al. Lancet Resp Med 2013, 1:
74 Effect of early PN on muscle function in human patients? Hypothesis : Early PN may reduce muscle breakdown, but via suppression of autophagy may also impair clearance of damaged organelles and protein aggregates, whereby threatening muscle function and aggravating ICU-acquired weakness Hermans G et al. Lancet Resp Med 2013, 1:
75 Effect of early PN on muscle function in human patients? Clinically : effect on ICU-acquired weakness (based on MRC score) in 600 patients Mechanistically : effect on atrophy and autophagy in 122 skeletal muscle biopsies Focus on patients with an ICU stay 8 days Hermans G et al. Lancet Resp Med 2013, 1:
76 Patients Hermans G et al. Lancet Resp Med 2013, 1: Early PN Late PN randomisation D8 time
77 Patients Hermans G et al. Lancet Resp Med 2013, 1: Early PN Late PN randomisation Alive discharged D8 time
78 Patients Hermans G et al. Lancet Resp Med 2013, 1: Early PN Late PN randomisation Alive discharged D8 Died time
79 Patients Hermans G et al. Lancet Resp Med 2013, 1: Early PN Late PN randomisation Alive discharged D8 Died time
80 Patients Hermans G et al. Lancet Resp Med 2013, 1: N=600 ICU stay 8 days random sample of short-stay ICU patients computer-generated stratified for admission category 1/10
81 Evaluations: MRC-sum score Hermans G et al. Lancet Resp Med 2013, 1: Evaluated 3 times weekly Adequately awake and cooperative First evaluation on day 8 of ICU stay (±1 day) Physiotherapists trained and blinded ICUAW : MRC sum score<48
82 Baseline characteristics Hermans G et al. Lancet Resp Med 2013, 1: MRC sum clinical study Biopsy study Late PN Early PN Late PN Early PN N = 305 N = 295 N = 61 N = 61 Age (years) Median (IQR) 65 (53-74) 62 (52-73) 62 (45-73) 63 (54-71) BMI (kg/m²) Median (IQR) 24.9 ( ) 25.0 ( ) 26.1 ( ) 25.7 ( ) NRS score 5 n (%) 88 (28.9) 89 (30.2) 20 (32.8) 18 (29.5) Sepsis n (%) 127 (41.6) 137 (46.4) 37 (60.7) 35 (57.4) Emergency n (%) 206 (67.5) 207 (70.2) 58 (95.1) 55 (90.2) APACHE II score Median (IQR) 30 (20-36) 32 (21-37) 34 (27-40) 36 (28-42)
83 Clinical effect on muscle weakness
84 Clinical effect on muscle weakness Hermans G et al. Lancet Resp Med 2013, 1: Late PN Early PN First MRC sum score < % 43 % P = 0.03 Worst MRC sum score < % 46 % P = 0.02 Last MRC sum score < % 31 % P = 0.15
85 Time to recovery of ICU - acquired weakness P=0.02 Late PN Hermans G et al. Lancet Resp Med 2013, 1: Early PN
86 Biopsy results : effect on atrophy & autophagy Hermans G et al. Lancet Resp Med 2013, 1:
87 myofiber area per total muscle area (%) Atrophy: myofiber density Hermans G et al. Lancet Resp Med 2013, 1: p=0 02 p=0 19 Control Critically ill Control Early PN Late PN
88 % of myofybers Atrophy: myofiber size (cross-sectional area) Hermans G et al. Lancet Resp Med 2013, 1: Myofiber cross-sectional area (x1000 mm 2 ) 10 8 Total myofibers 10 Type I 10 Type II Control Early PN Late PN
89 relative mrna level Atrophy: gene expression of myofibrillary proteins Hermans G et al. Lancet Resp Med 2013, 1: MyHC-I MyHC-IIa Actin p= p= p= p= p< p=0.03 Control Early PN Late PN
90 relative mrna level Atrophy: ubiquitin-proteasome pathway: E3 ligases Hermans G et al. Lancet Resp Med 2013, 1: MuRF-1 Atrogin p= p= p< p=0.78 Control Early PN Late PN
91 Atrophy: loss of muscle mass unaltered but fat in muscle increased with PN Paired CT scans in ICU patients Casaer MP, et al. Critical Care Medicine 2013 ICU day 2 ICU day 9 7% = = 10%
92 Autophagy Hermans G et al. Lancet Resp Med 2013, 1: LC3-II/LC3-I p= p= Actin Control LC3-I LC3-II Early PN Late PN
93 % of muscle stained for ubiqutin relative intensity Autophagy Hermans G et al. Lancet Resp Med 2013, 1: LC3-II/LC3-I Ubiquitin staining p= p=0.02 p= p= p< p= Actin Control LC3-I LC3-II Early PN Late PN Control Early PN Late PN
94 Blood glucose control or avoiding parenteral nutrition? Early PN Early PN Late PN No BG control BG <110 mg/dl BG <110 mg/dl Reduced mortality Mortality = Reduced organ failure Enhanced recovery Van den Berghe et al. NEJM 2001, NEJM 2006, Lancet 2009, NEJM 2011, JAMA 2012, NEJM 2013, NEJM 2016
95 What are the underlying mechanisms?
96 What are the underlying mechanisms? HYPERGLYCEMIA MACRONUTRIENTS (AA)
97 Where do we go from here?
98 Where do we go from here? We should redo the RCT on blood glucose control In the context of no parenteral nutrition during week 1 With an effective algorithm (LOGIC-insulin)
99 Clinical Department and Laboratory of Intensive Care Medicine Thank You
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