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01-04-2015 | Original

Acute brain failure in severe sepsis: a prospective study in the medical intensive care unit utilizing continuous EEG monitoring

Authors: Emily J. Gilmore, Nicolas Gaspard, Huimahn A. Choi, Emily Cohen, Kristin M. Burkart, David H. Chong, Jan Claassen, Lawrence J. Hirsch

Published in: Intensive Care Medicine | Issue 4/2015

Abstract

Purpose

Investigate the prevalence, risk factors and impact of continuous EEG (cEEG) abnormalities on mortality through the 1-year follow-up period in patients with severe sepsis.

Methods

Prospective, single-center, observational study of consecutive patients admitted with severe sepsis to the Medical ICU at an academic medical center.

Results

A total of 98 patients with 100 episodes of severe sepsis were included; 49 patients (50%) were female, median age was 60 (IQR 52–74), the median non-neuro APACHE II score was 23.5 (IQR 18–28) and median non-neuro SOFA score was 8 (IQR 6–11). Twenty-five episodes had periodic discharges (PD), of which 11 had nonconvulsive seizures (NCS). No patient had NCS without PD. Prior neurological history was associated with a higher risk of PD or NCS (45 vs. 17%; CI 1.53–10.43), while the non-neuro APACHE II, non-neuro SOFA, severity of cardiovascular shock and presence of sedation during cEEG were associated with a lower risk of PD or NCS. Clinical seizures before cEEG were associated with a higher risk of nonconvulsive status epilepticus (24 vs. 6%; CI 1.42–19.94) while the non-neuro APACHE II and non-neuro SOFA scores were associated with a lower risk. Lack of EEG reactivity was present in 28% of episodes. In the survival analysis, a lack of EEG reactivity was associated with higher 1-year mortality [mean survival time 3.3 (95% CI 1.8–4.9) vs. 7.5 (6.4–8.7) months; p = 0.002] but the presence of PD or NCS was not [mean survival time 3.3 (95% CI 1.8–4.9) vs. 7.5 (6.4–8.7) months; p = 0.592]. Lack of reactivity was more frequent in patients on continuous sedation during cEEG. In patients with available 1-year data (34% of the episodes), 82% had good functional outcome (mRS ≤ 3, n = 27). There were no significant predictors of functional outcome, late cognition, and no patient with complete follow-up data developed late seizure or new epilepsy.

Conclusions

NCS and PD are common in patients with severe sepsis and altered mental status. They were less frequent among the most severely sick patients and were not associated with outcome in this study. Lack of EEG reactivity was more frequent in patients on continuous sedation and was associated with mortality up to 1 year after discharge. Larger studies are needed to confirm these findings in a broader population and to further evaluate long-term cognitive outcome, risk of late seizure and epilepsy.

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Angus DC, van der Poll T (2013) Severe sepsis and septic shock. N Engl J Med 369:840–851CrossRefPubMed

Pandharipande PP, Girard TD, Jackson JC, Morandi A, Thompson JL, Pun BT, Brummel NE, Hughes CG, Vasilevskis EE, Shintani AK, Moons KG, Geevarghese SK, Canonico A, Hopkins RO, Bernard GR, Dittus RS, Ely EW, Investigators B-IS (2013) Long-term cognitive impairment after critical illness. N Engl J Med 369:1306–1316CrossRefPubMedCentralPubMed

Chong DJ, Hirsch LJ (2005) Which EEG patterns warrant treatment in the critically ill? Reviewing the evidence for treatment of periodic epileptiform discharges and related patterns. J Clin Neurophysiol 22:79–91CrossRefPubMed

Hirsch LJ, Claassen J, Mayer SA, Emerson RG (2004) Stimulus-induced rhythmic, periodic, or ictal discharges (SIRPIDs): a common EEG phenomenon in the critically ill. Epilepsia 45:109–123CrossRefPubMed

Kamel H, Betjemann JP, Navi BB, Hegde M, Meisel K, Douglas VC, Josephson SA (2012) Diagnostic yield of electroencephalography in the medical and surgical intensive care unit. Neurocrit Care 19(3):336–341CrossRef

Kurtz P, Gaspard N, Wahl AS, Bauer RM, Hirsch LJ, Wunsch H, Claassen J (2014) Continuous electroencephalography in a surgical intensive care unit. Int Care Med 40:228–234CrossRef

Oddo M, Carrera E, Claassen J, Mayer SA, Hirsch LJ (2009) Continuous electroencephalography in the medical intensive care unit. Crit Care Med 37:2051–2056CrossRefPubMed

Young GB, Jordan KG, Doig GS (1996) An assessment of nonconvulsive seizures in the intensive care unit using continuous EEG monitoring: an investigation of variables associated with mortality. Neurology 47:83–89CrossRefPubMed

Claassen J, Jette N, Chum F, Green R, Schmidt M, Choi H, Jirsch J, Frontera JA, Connolly ES, Emerson RG, Mayer SA, Hirsch LJ (2007) Electrographic seizures and periodic discharges after intracerebral hemorrhage. Neurology 69:1356–1365CrossRefPubMed

10.

Claassen J, Mayer SA, Kowalski RG, Emerson RG, Hirsch LJ (2004) Detection of electrographic seizures with continuous EEG monitoring in critically ill patients. Neurology 62:1743–1748CrossRefPubMed

11.

Vespa PM, Miller C, McArthur D, Eliseo M, Etchepare M, Hirt D, Glenn TC, Martin N, Hovda D (2007) Nonconvulsive electrographic seizures after traumatic brain injury result in a delayed, prolonged increase in intracranial pressure and metabolic crisis. Crit Care Med 35:2830–2836CrossRefPubMedCentralPubMed

12.

Vespa PM, O’Phelan K, Shah M, Mirabelli J, Starkman S, Kidwell C, Saver J, Nuwer MR, Frazee JG, McArthur DA, Martin NA (2003) Acute seizures after intracerebral hemorrhage: a factor in progressive midline shift and outcome. Neurology 60:1441–1446CrossRefPubMed

13.

Claassen J, Mayer SA, Hirsch LJ (2005) Continuous EEG monitoring in patients with subarachnoid hemorrhage. J Clin Neurophysiol 22:92–98CrossRefPubMed

14.

Young GB, Bolton CF, Archibald YM, Austin TW, Wells GA (1992) The electroencephalogram in sepsis-associated encephalopathy. J Clin Neurophysiol 9:145–152CrossRefPubMed

15.

Gutling E, Gonser A, Imhof HG, Landis T (1995) EEG reactivity in the prognosis of severe head injury. Neurology 45:915–918CrossRefPubMed

16.

Rossetti AO, Urbano LA, Delodder F, Kaplan PW, Oddo M (2010) Prognostic value of continuous EEG monitoring during therapeutic hypothermia after cardiac arrest. Crit Care 14:R173CrossRefPubMedCentralPubMed

17.

Sutter R, Kaplan PW (2013) Clinical and electroencephalographic correlates of acute encephalopathy. J Clin Neurophysiol 30:443–453CrossRefPubMed

18.

Dellinger RP, Levy MM, Carlet JM, Bion J, Parker MM, Jaeschke R, Reinhart K, Angus DC, Brun-Buisson C, Beale R, Calandra T, Dhainaut JF, Gerlach H, Harvey M, Marini JJ, Marshall J, Ranieri M, Ramsay G, Sevransky J, Thompson BT, Townsend S, Vender JS, Zimmerman JL, Vincent JL, International Surviving Sepsis Campaign Guidelines C, American Association of Critical-Care N, American College of Chest P, American College of Emergency P, Canadian Critical Care S, European Society of Clinical M, Infectious D, European Society of Intensive Care M, European Respiratory S, International Sepsis F, Japanese Association for Acute M, Japanese Society of Intensive Care M, Society of Critical Care M, Society of Hospital M, Surgical Infection S, World Federation of Societies of I, Critical Care M (2008) Surviving sepsis campaign: international guidelines for management of severe sepsis and septic shock. Crit Care Med 36:296–327CrossRefPubMed

19.

Claassen J, Hirsch LJ, Emerson RG, Bates JE, Thompson TB, Mayer SA (2001) Continuous EEG monitoring and midazolam infusion for refractory nonconvulsive status epilepticus. Neurology 57:1036–1042CrossRefPubMed

20.

Hirsch LJ, LaRoche SM, Gaspard N, Gerard E, Svoronos A, Herman ST, Mani R, Arif H, Jette N, Minazad Y, Kerrigan JF, Vespa P, Hantus S, Claassen J, Young GB, So E, Kaplan PW, Nuwer MR, Fountain NB, Drislane FW (2013) American Clinical Neurophysiology Society’s standardized critical care EEG terminology: 2012 version. J Clin Neurophysiol 30:1–27CrossRefPubMed

21.

Beniczky S, Hirsch LJ, Kaplan PW, Pressler R, Bauer G, Aurlien H, Brogger JC, Trinka E (2013) Unified EEG terminology and criteria for nonconvulsive status epilepticus. Epilepsia 54(Suppl 6):28–29CrossRefPubMed

22.

Bonita R, Beaglehole R (1988) Recovery of motor function after stroke. Stroke J Cereb Circ 19:1497–1500CrossRef

23.

Mayer SA, Kreiter KT, Copeland D, Bernardini GL, Bates JE, Peery S, Claassen J, Du YE, Connolly ES Jr (2002) Global and domain-specific cognitive impairment and outcome after subarachnoid hemorrhage. Neurology 59:1750–1758CrossRefPubMed

24.

Knopman DS, Roberts RO, Geda YE, Pankratz VS, Christianson TJ, Petersen RC, Rocca WA (2010) Validation of the telephone interview for cognitive status-modified in subjects with normal cognition, mild cognitive impairment, or dementia. Neuroepidemiology 34:34–42CrossRefPubMedCentralPubMed

25.

Polito A, Eischwald F, Maho AL, Polito A, Azabou E, Annane D, Chretien F, Stevens RD, Carlier R, Sharshar T (2013) Pattern of brain injury in the acute setting of human septic shock. Crit Care 17:R204CrossRefPubMedCentralPubMed

26.

Taccone FS, Su F, De Deyne C, Abdellhai A, Pierrakos C, He X, Donadello K, Dewitte O, Vincent JL, De Backer D (2014) Sepsis is associated with altered cerebral microcirculation and tissue hypoxia in experimental peritonitis. Crit Care Med 42:e114–e122CrossRefPubMed

27.

Amano S, Obata T, Hazama F, Kashiro N, Shimada M (1990) Hypoxia prevents seizures and neuronal damages of the hippocampus induced by kainic acid in rats. Brain Res 523:121–126CrossRefPubMed

28.

Mitchell WG, Grubbs RC (1956) Inhibition of audiogenic seizures by carbon dioxide. Science 123:223–224CrossRefPubMed

29.

Waziri A, Claassen J, Stuart RM, Arif H, Schmidt JM, Mayer SA, Badjatia N, Kull LL, Connolly ES, Emerson RG, Hirsch LJ (2009) Intracortical electroencephalography in acute brain injury. Ann Neurol 66:366–377CrossRefPubMed

30.

Vespa PM, Boscardin WJ, Hovda DA, McArthur DL, Nuwer MR, Martin NA, Nenov V, Glenn TC, Bergsneider M, Kelly DF, Becker DP (2002) Early and persistent impaired percent alpha variability on continuous electroencephalography monitoring as predictive of poor outcome after traumatic brain injury. J Neurosurg 97:84–92CrossRefPubMed

31.

Rossetti AO, Oddo M, Logroscino G, Kaplan PW (2010) Prognostication after cardiac arrest and hypothermia: a prospective study. Ann Neurol 67:301–307PubMed

32.

Moruzzi G, Magoun HW (1949) Brain stem reticular formation and activation of the EEG. Electroencephalogr Clin Neurophysiol 1:455–473CrossRefPubMed

33.

Lindsley DB, Bowden JW, Magoun HW (1949) Effect upon the EEG of acute injury to the brain stem activating system. Electroencephalogr Clin Neurophysiol 1:475–486CrossRefPubMed

34.

Sharshar T, Porcher R, Siami S, Rohaut B, Bailly-Salin J, Hopkinson NS, Clair B, Guidoux C, Iacobone E, Sonneville R, Polito A, Aboab J, Gaudry S, Morla O, Amouyal G, Azuar J, Allary J, Vieillard-Baron A, Wolff M, Cariou A, Annane D, Paris-Ouest Study Group on Neurological Effect of S (2011) Brainstem responses can predict death and delirium in sedated patients in intensive care unit. Crit Care Med 39:1960–1967CrossRefPubMed

35.

Watson PL, Shintani AK, Tyson R, Pandharipande PP, Pun BT, Ely EW (2008) Presence of electroencephalogram burst suppression in sedated, critically ill patients is associated with increased mortality. Crit Care Med 36:3171–3177CrossRefPubMedCentralPubMed

36.

Shehabi Y, Riker RR, Bokesch PM, Wisemandle W, Shintani A, Ely EW, Group SS (2010) Delirium duration and mortality in lightly sedated, mechanically ventilated intensive care patients. Crit Care Med 38:2311–2318CrossRef

37.

Knaus WA, Zimmerman JE, Wagner DP, Draper EA, Lawrence DE (1981) APACHE-acute physiology and chronic health evaluation: a physiologically based classification system. Crit Care Med 9:591–597CrossRefPubMed

38.

Payne ET, Zhao XY, Frndova H, McBain K, Sharma R, Hutchison JS, Hahn CD (2014) Seizure burden is independently associated with short term outcome in critically ill children. Brain J Neurol 137:1429–1438CrossRef

39.

Wagenman KL, Blake TP, Sanchez SM, Schultheis MT, Radcliffe J, Berg RA, Dlugos DJ, Topjian AA, Abend NS (2014) Electrographic status epilepticus and long-term outcome in critically ill children. Neurology 82:396–404CrossRefPubMedCentralPubMed

Title: Acute brain failure in severe sepsis: a prospective study in the medical intensive care unit utilizing continuous EEG monitoring
Authors: Emily J. Gilmore
Nicolas Gaspard
Huimahn A. Choi
Emily Cohen
Kristin M. Burkart
David H. Chong
Jan Claassen
Lawrence J. Hirsch
Publication date: 01-04-2015
Publisher: Springer Berlin Heidelberg
Published in: Intensive Care Medicine / Issue 4/2015
Print ISSN: 0342-4642
Electronic ISSN: 1432-1238
DOI: https://doi.org/10.1007/s00134-015-3709-1

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Acute brain failure in severe sepsis: a prospective study in the medical intensive care unit utilizing continuous EEG monitoring

Abstract

Purpose

Methods

Results

Conclusions

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Purpose

Methods

Results

Conclusions

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