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01-01-2020 | Magnetic Resonance Imaging | Review Article

Diagnosing acute brain dysfunction due to sepsis

Authors: Figen Esen, Günseli Orhun, Perihan Ergin Özcan, Andres R. Brenes Bastos, Erdem Tüzün

Published in: Neurological Sciences | Issue 1/2020

Abstract

Developments in the management of critically ill patients suffering organ dysfunctions have demonstrated that brain is the prominent organ to be effected during critical illness. Acute brain dysfunction due to pathologic neuroinflammatory processes associated with sepsis is commonly seen and related to morbidity and mortality in the ICU treatment. Studies reported that survivors of sepsis may suffer long-term cognitive dysfunction that affects quality of life. However, there are no specific approaches to diagnose acute brain dysfunction in the early phase to target protective measures. In recent years, imaging methods and biomarkers are the most important issues of studies. This review will address the current diagnostic approaches to acute brain dysfunction related to sepsis.

Sharshar T, Hopkinson NS, Orlikowski D, Annane D (2005) Science review: the brain in sepsis--culprit and victim. Crit Care 9:37–44CrossRef

Dantzer R (2004) Cytokine-induced sickness behaviour: a neuroimmune response to activation of innate immunity. Eur J Pharmacol 500:399–411CrossRef

Sharshar T, Annane D, de la Grandmaison GL, Brouland JP, Hopkinson NS, Francoise G (2004) The neuropathology of septic shock. Brain Pathol 14:21–33CrossRef

Iacobone E, Bailly-Salin J, Polito A, Friedman D, Stevens RD, Sharshar T (2009) Sepsis-associated encephalopathy and its differential diagnosis. Crit Care Med 37:S331–S336CrossRef

Eidelman LA, Putterman D, Putterman C, Sprung CL (1996) The spectrum of septic encephalopathy. Definitions, etiologies, and mortalities. JAMA 275:470–473CrossRef

Ely EW, Shintani A, Truman B, Speroff T, Gordon SM, Harrell FE Jr, Inouye SK, Bernard GR, Dittus RS (2004) Delirium as a predictor of mortality in mechanically ventilated patients in the intensive care unit. JAMA 291:1753–1762CrossRef

Hopkins RO, Weaver LK, Collingridge D, Parkinson RB, Chan KJ, Orme JF (2005) Two-year cognitive, emotional, and quality-of-life outcomes in acute respiratory distress syndrome. Am J Respir Crit Care Med 171:340–347CrossRef

American Psychiatric Association (2013) Diagnostic and statistical manual of mental disorders: DSM-5, 5th edn. American Psychiatric Association, Arlington, VACrossRef

Young GB, Bolton CF, Austin TW, Archibald YM, Gonder J, Wells GA (1990) The encephalopathy associated with septic illness. Clin Invest Med 13:297–304PubMed

10.

Zhang LN, Wang XT, Ai YH, Guo QL, Huang L, Liu ZY, Yao B (2012) Epidemiological features and risk factors of sepsis-associated encephalopathy in intensive care unit patients: 2008-2011. Chin Med J 125:828–831PubMed

11.

Gofton TE, Young GB (2012) Sepsis-associated encephalopathy. Nat Rev Neurol 8:557–566. https://doi.org/10.1038/nrneurol.2012.183 CrossRefPubMed

12.

Bleck TP, Smith MC, Pierre-Louis SJ, Jares JJ, Murray J, Hansen CA (1993) Neurologic complications of critical medical illnesses. Crit Care Med 21:98–103CrossRef

13.

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

14.

Salluh JI, Soares M, Teles JM, Ceraso D, Raimondi N, Nava VS, Blasquez P, Ugarte S, Ibanez-Guzman C, Centeno JV, Laca M, Grecco G, Jimenez E, Árias-Rivera S, Duenas C, Rocha MG (2010) Delirium Epidemiology in Critical Care Study Group. Delirium epidemiology in critical care (DECCA): an international study. Crit Care 14:R210. https://doi.org/10.1186/cc9333 CrossRefPubMedPubMedCentral

15.

Sharshar T, Citerio G, Andrews PJ, Chieregato A, Latronico N, Menon DK, Puybasset L, Sandroni C, Stevens RD (2014) Neurological examination of critically ill patients: a pragmatic approach. Report of an ESICM expert panel. Intensive Care Med 40:484–495. https://doi.org/10.1007/s00134-014-3214-y CrossRefPubMed

16.

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 Sedation (POSGNES) (2011) Brainstem responses can predict death and delirium in sedated patients in intensive care unit. Crit Care Med 39:1960–1967CrossRef

17.

Singer BH, Dickson RP, Denstaedt SJ, Newstead MW, Kim K, Falkowski NR, Erb-Downward JR, Schmidt TM, Huffnagle GB, Standiford TJ (2018) Bacterial dissemination to the brain in sepsis. Am J Respir Crit Care Med 197:747–756CrossRef

18.

Ely EW, Inouye SK, Bernard GR, Gordon S, Francis J, May L, Truman B, Speroff T, Gautam S, Margolin R, Hart RP, Dittus R (2001) Delirium in mechanically ventilated patients: validity and reliability of the confusion assessment method forthe intensive care unit (CAM-ICU). JAMA 286:2703–2710CrossRef

19.

Bergeron N, Dubois MJ, Dumont M, Dial S, Skrobik Y (2001) Intensive care delirium screening checklist: evaluation of a new screening tool. Intensive Care Med 27:859–864CrossRef

20.

Haenggi M, Blum S, Brechbuehl R, Brunello A, Jakob SM, Takala J (2013) Effect of sedation level on the prevalence of delirium when assessed with CAM-ICU and ICDSC. Intensive Care Med 39:2171–2179. https://doi.org/10.1007/s00134-013-3034-5 CrossRefPubMed

21.

Francis J, Martin D, Kapoor WN (1990) A prospective study of delirium in hospitalized elderly. JAMA 263:1097–1101CrossRef

22.

Jackson AC, Gilbert JJ, Young GB, Bolton CF (1985) The encephalopathy of sepsis. Can J Neurol Sci 12:303–307CrossRef

23.

Young GB (1995) Neurologic complications of systemic critical illness. Neurol Clin 13:645–658 Review CrossRef

24.

Bartynski WS, Boardman JF, Zeigler ZR, Shadduck RK, Lister J (2006) Posterior reversible encephalopathy syndrome in infection, sepsis, and shock. AJNR Am J Neuroradiol 27:2179–2190PubMed

25.

Sharshar T, Carlier R, Bernard F, Guidoux C, Brouland JP, Nardi O, de la Grandmaison GL, Aboab J, Gray F, Menon D, Annane D (2007) Brain lesions in septic shock: a magnetic resonance imaging study. Intensive Care Med 33:798–806CrossRef

26.

Morandi A, Gunther ML, Vasilevskis EE, Girard TD, Hopkins RO, Jackson JC, Pandharipande P, Ely EW (2010) Neuroimaging in delirious intensive care unit patients: a preliminary case series report. Psychiatry (Edgmont) 7(9):28–33

27.

Fugate JE, Claassen DO, Cloft HJ, Kallmes DF, Kozak OS, Rabinstein AA (2010) Posterior reversible encephalopathy syndrome: associated clinical and radiologic findings. Mayo Clin Proc 85(5):427–432. https://doi.org/10.4065/mcp.2009.0590 CrossRefPubMedPubMedCentral

28.

Suchyta MR, Jephson A, Hopkins RO (2010) Neurologic changes during critical illness: brain imaging findings and neurobehavioral outcomes. Brain Imaging Behav 4:22–34. https://doi.org/10.1007/s11682-009-9082-3 CrossRefPubMed

29.

Gunther ML, Morandi A, Krauskopf E, Pandharipande P, Girard TD, Jackson JC, Thompson J, Shintani AK, Geevarghese S, Miller RR 3rd, Canonico A, Merkle K, Cannistraci CJ, Rogers BP, Gatenby JC, Heckers S, Gore JC, Hopkins RO, Ely EW, VISIONS Investigation, VISualizing Icu SurvivOrs Neuroradiological Sequelae (2012) The association between brain volumes, delirium duration, and cognitive outcomes in intensive care unit survivors: the VISIONS cohort magnetic resonance imaging study*. Crit Care Med 40:2022–2032CrossRef

30.

Morandi A, Rogers BP, Gunther ML, Merkle K, Pandharipande P, Girard TD, Jackson JC, Thompson J, Shintani AK, Geevarghese S, Miller RR 3rd, Canonico A, Cannistraci CJ, Gore JC, Ely EW, Hopkins RO, VISIONS Investigation, VISualizing Icu SurvivOrs Neuroradiological Sequelae (2012) The relationship between delirium duration, white matter integrity, and cognitive impairment in intensive care unit survivors as determined by diffusion tensor imaging: the VISIONS prospective cohort magnetic resonance imaging study*. Crit Care Med 40(7):2182–2189. https://doi.org/10.1097/CCM.0b013e318250acdc CrossRefPubMedPubMedCentral

31.

Polito A, Eischwald F, Maho AL, Polito A, Azabou E, Annane D, Chrétien F, Stevens RD, Carlier R, Sharshar T (2013) Pattern of brain injury in the acute setting of human septic shock. Crit Care 17:R204. https://doi.org/10.1186/cc12899 CrossRefPubMedPubMedCentral

32.

Semmler A, Widmann CN, Okulla T, Urbach H, Kaiser M, Widman G, Mormann F, Weide J, Fliessbach K, Hoeft A, Jessen F, Putensen C, Heneka MT (2013) Persistent cognitive impairment, hippocampal atrophy and EEG changes in sepsis survivors. J Neurol Neurosurg Psychiatry 84(1):62–69. https://doi.org/10.1136/jnnp-2012-302883 CrossRefPubMed

33.

Sutter R, Chalela JA, Leigh R, Kaplan PW, Yenokyan G, Sharshar T, Stevens RD (2015) Significance of parenchymal brain damage in patients with critical illness. Neurocrit Care 23(2):243–252. https://doi.org/10.1007/s12028-015-0110-4 CrossRefPubMed

34.

Ehler J, Barrett LK, Taylor V, Groves M, Scaravilli F, Wittstock M, Kolbaske S, Grossmann A, Henschel J, Gloger M, Sharshar T, Chretien F, Gray F, Nöldge-Schomburg G, Singer M, Sauer M, Petzold A (2017) Translational evidence for two distinct patterns of neuroaxonal injury in sepsis: a longitudinal, prospective translational study. Crit Care 23;21(1):262. https://doi.org/10.1186/s13054-017-1850-7 CrossRef

35.

Orhun G, Esen F, Ozcan PE, Sencer S, Bilgic B, Ulusoy C, Noyan H, Kucukerden M, Ali A, Barburoglu M, Tuzun E (2019) Neuroimaging findings in Sepsis-induced brain dysfunction: association with clinical and laboratory findings. Neurocrit Care 30:106–117CrossRef

36.

Ehler J, Petzold A, Wittstock M, Kolbaske S, Gloger M, Henschel J, Heslegrave A, Zetterberg H, Lunn MP, Rommer PS, Grossmann A, Sharshar T, Richter G, Nöldge-Schomburg G, Sauer M (2019) The prognostic value of neurofilament levels in patients with sepsis-associated encephalopathy - a prospective, pilot observational study. PLoS One 24;14(1):e0211184. https://doi.org/10.1371/journal.pone.0211184 CrossRef

37.

Orhun G, Tüzün E, Bilgiç B, Ergin Özcan P, Sencer S, Barburoğlu M, Esen F Brain volume changes in patients with acute brain dysfunction due to sepsis. Neurocrit Care 11. https://doi.org/10.1007/s12028-019-00759-8

38.

Hosokawa K, Gaspard N, Su F, Oddo M, Vincent JL, Taccone FS (2014) Clinical neurophysiological assessment of sepsis-associated brain dysfunction: a systematic review. Crit Care 18:674. https://doi.org/10.1186/s13054-014-0674-y CrossRefPubMedPubMedCentral

39.

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

40.

Ely EW, Truman B, Manzi DJ, Sigl JC, Shintani A, Bernard GR (2004) Consciousness monitoring in ventilated patients: bispectral EEG monitors arousal not delirium. Intensive Care Med 30:1537–1543CrossRef

41.

Azabou E, Fischer C, Guerit JM, Annane D, Mauguiere F, Lofaso F, Sharshar T (2017) Neurophysiological assessment of brain dysfunction in critically ill patients: an update. Neurol Sci 38:715–726. https://doi.org/10.1007/s10072-017-2824-x CrossRefPubMed

42.

Foreman B, Claassen J, Abou Khaled K, Jirsch J, Alschuler DM, Wittman J, Emerson RG, Hirsch LJ (2012) Generalized periodic discharges in the critically ill: a case-control study of 200 patients. Neurology 79:1951–1956CrossRef

43.

Gilmore EJ, Gaspard N, Choi HA, Cohen E, Burkart KM, Chong DH, Claassen J, Hirsch LJ (2015) Acute brain failure in severe sepsis: a prospective study in the medical intensive care unit utilizing continuous EEG monitoring. Intensive Care Med 41:686–694. https://doi.org/10.1007/s00134-015-3709-1 CrossRefPubMed

44.

Yao B, Zhang LN, Ai YH, Liu ZY, Huang L (2014) Serum S100β is a better biomarker than neuron-specific enolase for sepsis-associated encephalopathy and determining its prognosis: a prospective and observational study. Neurochem Res 39:1263–1269. https://doi.org/10.1007/s11064-014-1308-0 CrossRefPubMed

45.

Nguyen DN, Spapen H, Su F, Schiettecatte J, Shi L, Hachimi-Idrissi S, Huyghens L (2006) Elevated serum levels of S-100beta protein and neuron-specific enolase are associated with brain injury in patients with severe sepsis and septic shock. Crit Care Med 34:1967–1974CrossRef

46.

Hughes CG, Pandharipande PP, Thompson JL, Chandrasekhar R, Ware LB, Ely EW, Girard TD (2016) Endothelial activation and blood-brain barrier injury as risk factors for delirium in critically ill patients. Crit Care Med 44:e809–e817. https://doi.org/10.1097/CCM.0000000000001739 CrossRefPubMedPubMedCentral

47.

van den Boogaard M, Kox M, Quinn KL, van Achterberg T, van der Hoeven JG, Schoonhoven L, Pickkers P (2011) Biomarkers associated with delirium in critically ill patients and their relation with long-term subjective cognitive dysfunction; indications for different pathways governing delirium in inflamed and noninflamed patients. Crit Care 15:R297CrossRef

48.

Orhun G, Tüzün E, Ozcan PE, Ulusoy C, Yıldırım E, Küçükerden M, Gürvit H, Ali A, Esen F (2019) Association between inflammatory markers and cognitive outcome in patients with acute brain dysfunction due to Sepsis. Arch Neuropsychiatry 56:63–70. https://doi.org/10.29399/npa.23212 CrossRef

49.

Esen F, Orhun G, Ozcan PE, Senturk E, Kucukerden M, Giris M, Akcan U, Yilmaz CU, Orhan N, Arican N, Kaya M, Gazioglu SB, Tuzun E (2017) Neuroprotective effects of intravenous immunoglobulin are mediated through inhibition of complement activation and apoptosis in a rat model of sepsis. Intensive Care Med Exp 5:1. https://doi.org/10.1186/s40635-016-0114-1 CrossRefPubMedPubMedCentral

50.

Puvenna V, Engeler M, Banjara M, Brennan C, Schreiber P, Dadas A, Bahrami A, Solanki J, Bandyopadhyay A, Morris JK, Bernick C, Ghosh C, Rapp E, Bazarian JJ, Janigro D (2016) Is phosphorylated tau unique to chronic traumatic encephalopathy? Phosphorylated tau in epileptic brain and chronic traumatic encephalopathy. Brain Res 1630:225–240. https://doi.org/10.1016/j.brainres.2015.11.007 CrossRefPubMed

51.

Kovacs GG, Rahimi J, Ströbel T, Lutz MI, Regelsberger G, Streichenberger N, Perret-Liaudet A, Höftberger R, Liberski PP, Budka H, Sikorska B (2017) Tau pathology in Creutzfeldt-Jakob disease revisited. Brain Pathol 27:332–344. https://doi.org/10.1111/bpa.12411 CrossRefPubMed

52.

Esen F, Erdem T, Aktan D, Orhan M, Kaya M, Eraksoy H, Cakar N, Telci L (2005) Effect of magnesium sulfate administration on blood-brain barrier in a rat model of intraperitoneal sepsis: a randomized controlled experimental study. Crit Care 9:R18–R23. https://doi.org/10.1186/cc3004 CrossRefPubMed

53.

Toklu HZ, Uysal MK, Kabasakal L, Sirvanci S, Ercan F, Kaya M (2009) The effects of riluzole on neurological, brain biochemical, and histological changes in early and late term of sepsis in rats. J Surg Res 152:238–248. https://doi.org/10.1016/j.jss.2008.03.013 CrossRefPubMed

54.

Flierl MA, Stahel PF, Rittirsch D, Huber-Lang M, Niederbichler AD, Hoesel LM, Touban BM, Morgan SJ, Smith WR, Ward PA, Ipaktchi K (2009) Inhibition of complement C5a prevents breakdown of the blood-brain barrier and pituitary dysfunction in experimental sepsis. Crit Care 13:R12. https://doi.org/10.1186/cc7710 CrossRefPubMedPubMedCentral

55.

Ozcan PE, Senturk E, Orhun G, Gumru S, Arican N, Orhan N, Yılmaz CU, Kaya M, Aricioglu F, Esen F (2015) Effects of intravenous immunoglobulin therapy on behavior deficits and functions in sepsis model. Ann Intensive Care 5:62. https://doi.org/10.1186/s13613-015-0062-z CrossRefPubMed

Title: Diagnosing acute brain dysfunction due to sepsis
Authors: Figen Esen
Günseli Orhun
Perihan Ergin Özcan
Andres R. Brenes Bastos
Erdem Tüzün
Publication date: 01-01-2020
Publisher: Springer International Publishing
Keywords: Magnetic Resonance Imaging
Magnetic Resonance Imaging
Septicemia
Septicemia
Electroencephalography
Encephalopathy
Published in: Neurological Sciences / Issue 1/2020
Print ISSN: 1590-1874
Electronic ISSN: 1590-3478
DOI: https://doi.org/10.1007/s10072-019-04069-x

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Diagnosing acute brain dysfunction due to sepsis

Abstract

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Abstract

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