Intensive Care Medicine

, Volume 33, Issue 5, pp 798–806

Brain lesions in septic shock: a magnetic resonance imaging study

  • Tarek Sharshar
  • Robert Carlier
  • Francis Bernard
  • Céline Guidoux
  • Jean-Philippe Brouland
  • Olivier Nardi
  • Geoffroy Lorin de la Grandmaison
  • Jérôme Aboab
  • Françoise Gray
  • David Menon
  • Djillali Annane
Original

Abstract

Background

Understanding of sepsis-induced brain dysfunction remains poor, and relies mainly on data from animals or post-mortem studies in patients. The current study provided findings from magnetic resonance imaging of the brain in septic shock.

Methods

Nine patients with septic shock and brain dysfunction [7 women, median age 63 years (interquartile range 61–79 years), SAPS II: 48 (44–56), SOFA: 8 (6–10)] underwent brain magnetic resonance imaging including gradient echo T1-weighted, fluid-attenuated inversion recovery (FLAIR), T2-weighted and diffusion isotropic images, and mapping of apparent diffusion coefficient.

Results

Brain imaging was normal in two patients, showed multiple ischaemic strokes in two patients, and in the remaining patients showed white matter lesions at the level of the centrum semiovale, predominating around Virchow–Robin spaces, ranging from small multiple areas to diffuse lesions, and characterised by hyperintensity on FLAIR images. The main lesions were also characterised by reduced signal on diffusion isotropic images and increased apparent diffusion coefficient. The lesions of the white matter worsened with increasing duration of shock and were correlated with Glasgow Outcome Score.

Conclusion

This preliminary study showed that sepsis-induced brain lesions can be documented by magnetic resonance imaging. These lesions predominated in the white matter, suggesting increasedblood–brain barrier permeability, and were associated with poor outcome.

Keywords

Septic shock Brain Inflammation Blood–brain barrier 

References

  1. 1.
    Annane D, Bellissant E, Cavaillon J-M (2005) Septic shock. Lancet 365:63–77PubMedCrossRefGoogle Scholar
  2. 2.
    Nguyen DN, Spapen H, Su F, Schiettecatte J, Shi L, Hachimi-Idrissi S, Huyghens L (2006) Elevated serum levels of S-100β protein and neuron-specific enolase are associated with brain injury in patients with severe sepsis and septic shock. Crit Care Medicine 34:1967–1974CrossRefGoogle Scholar
  3. 3.
    Sprung CL, Peduzzi PN, Shatney CH, Schein RMH, Wilson MF, Sheagren JN, Hinshaw LB, The Veterans Administration Systemic Sepsis Cooperative Study Group (1990) Impact of encephalopathy on mortality of sepsis. Crit Care Med 18:801–806PubMedCrossRefGoogle Scholar
  4. 4.
    Eidelman LA, Putterman D, Putterman C, Sprung CL (1996) The spectrum of septic encephalopathy. Definitions, etiologies, and mortalities. JAMA 275:470–473PubMedCrossRefGoogle Scholar
  5. 5.
    Sharshar T, Annane D, de la Grandmaison G, Brouland JP, Hopkinson NS, Gray F (2004) The neuropathology of septic shock. Brain Pathol 14:21–33PubMedCrossRefGoogle Scholar
  6. 6.
    Sharshar T, Gray F, Poron F, Raphael JC, Gajdos P, Annane D (2002) Multifocal necrotizing leukoencephalopathy in septic shock. Crit Care Med 30:2371–2375PubMedCrossRefGoogle Scholar
  7. 7.
    Papadopoulos MC, Lamb FJ, Moss RF, Davies DC, Tighe D, Bennett ED (1999) Faecal peritonitis causes oedema and neuronal injury in pig cerebral cortex. Clin Sci (Lond) 96:461–466CrossRefGoogle Scholar
  8. 8.
    Sharshar T, Hopkinson NS, Orlikowski D, Annane D (2005) The brain in sepsis – culprit and victim. Crit Care 9:37–44PubMedCrossRefGoogle Scholar
  9. 9.
    Sprung CL, Cerra FB, Freund HR, Schein RM, Konstantinides FN, Marcial EH, Pena M (1991) Amino acid alterations and encephalopathy in the sepsis syndrome. Crit Care Med 19:753–757PubMedCrossRefGoogle Scholar
  10. 10.
    Sharshar T, Gray F, Lorin de la Grandmaison G, Hopkinson NS, Ross E, Dorandeu A, Orlikowski D, Raphael J-C, Gajdos P, Annane D (2003) Apoptosis of neurons in cardiovascular autonomic centres triggered by inducible nitric oxide synthase after death from septic shock. Lancet 362:1799–1805PubMedCrossRefGoogle Scholar
  11. 11.
    Bone RC, Balk RA, Cerra FB, Dellinger RP, Fein AM, Knaus WA, Schein RM, Sibbald WJ (1992) Definitions for sepsis and organ failure and guidelines for use of innovative therapies in sepsis. The ACCP/SCCM Consensus Conference. American College of Chest Physician/Society of Critical Care Medicine. Chest 101:1644–1655.PubMedGoogle Scholar
  12. 12.
    LeGall JR, Lemeshow S, Saulnier F (1993) A new simplified acute physiology score (SAPSII) based on a European/North American multicenter study. JAMA 270:2957–2963CrossRefGoogle Scholar
  13. 13.
    Vincent JL, Moreno R, Takala J, Willatts S, De Mendonca A, Bruining H, Reinhardt CK, Suter PM, Thijs LG (1996) The SOFA (Sepsis-related Organ Failure Assessment) score to describe organ dysfunction/failure. On behalf of the Working Group on Sepsis-Related Problems of the European Society of Intensive Care Medicine. Intensive Care Med 22:707–710PubMedGoogle Scholar
  14. 14.
    de Jonghe B, Cook D, Griffith L, Appere-de-Vecchi C, Guyatt G, Theron V, Vagnerre A, Outin H (2003) Adaptation to the Intensive Care Environment (ATICE): development and validation of a new sedation assessment instrument. Crit Care Med 31:2344–2354PubMedCrossRefGoogle Scholar
  15. 15.
    Wijdicks EF (2002) Coma and other states of altered awareness. In: Wijdicks EF (ed). Neurologic complications of critical illness. Oxford University Press, pp 3–27Google Scholar
  16. 16.
    Schmidt R, Fazekas F, Kleinert G, Offenbacher H, Gindl K, Payer F, Freidl W, Niederkon K, Lechner H (1992) Magnetic resonance imaging signal hyperintensities in the deep and sucortical white matter: a comparative study between stroke patients and normal volunteers. Arch Neurol 49:825–827PubMedGoogle Scholar
  17. 17.
    Jennet B, Snoek J, Bond M, Brooks N (1981) Disability after severe head injury: observations on the use of the Glasgow outcome scale. J Neurol Neurosurg Psychiatry 44:285–293Google Scholar
  18. 18.
    Bakhtiari K, Meijers JC, de Jonge E, Levi M (2004) Prospective validation of the International Society of Thrombosis and Haemostasis scoring system for disseminated intravascular coagulation. Crit Care Med 32:2416–2421PubMedCrossRefGoogle Scholar
  19. 19.
    Nagaratnam N, Brakoudias V, Ng K (2002) Multiple cerebral infarcts following septic shock. J Clin Neurosci 9:473–476PubMedCrossRefGoogle Scholar
  20. 20.
    Black DA, Maws DSJ (1984) Toxic shock syndrome presenting as cerebral infarct (letter). J Neurol Neurosurg Psychiatry 47:568PubMedCrossRefGoogle Scholar
  21. 21.
    Hollinger P, Zurcher R, Schroth G, Mattle HP (2000) Diffusion magnetic resonance imaging findings in cerebritis and brain abscesses in a patient with septic encephalopathy. J Neurol 247:232–234PubMedCrossRefGoogle Scholar
  22. 22.
    Heier LA, Bauer CJ, Schwartz L, Zimmerman RD, Morgello S, Deck MD (1989) Large Virchow–Robin spaces: MR–clinical coorelation. Am J Neuroradiol 10:929–936PubMedGoogle Scholar
  23. 23.
    Finelli PF, Uphoff DF (2004) Magnetic resonance imaging abnormalities with septic encephalopathy. J Neurol Neurosurg Psychiatry 75:1189–1191PubMedCrossRefGoogle Scholar
  24. 24.
    Mirfakhraee M, Crofford MJ, Guinto FC Jr, Nauta HJ, Weedn VW (1986) Virchow–Robin space: a path of spread in neurosarcoidosis. Radiology 158:715–720PubMedGoogle Scholar
  25. 25.
    Campi A, Benndorf G, Filippi M, Reganati P, Martinelli V, Terreni MR (2001) Primary angeitis of the central nervous system: serial MRI of brain and spinal cord. Neuroradiology 43:599–607PubMedCrossRefGoogle Scholar
  26. 26.
    Holmin S, Soderlund J, Biberfeld P, Mathiesen T (1998) Intracerebral inflammation after human brain contusion. Neurosurgery 42:291–298PubMedCrossRefGoogle Scholar
  27. 27.
    Inglese M, Bromsztyk E, Gonen O, Mannon LJ, Grossman RI, Rusinek H (2005) Dilated perivascular spaces: hallmarks of mild traumatic brain injury. Am J Neuroradiol 26:719–724PubMedGoogle Scholar
  28. 28.
    Fayed N, Modrego PJ, Morales H (2006) Evidence of brain damage after high-altitude climbing by means of magnetic resonance imaging. Am J Med 19:161–166Google Scholar
  29. 29.
    Mueller CA, Schluesener HJ, Conrad S, Meyermann R, Schwab JM (2003) Lesional expression of a proinflammatory and antiangionic cytokine EMAP II confined to endothelium and microglia/macrophages during secondary damage following experimental traumatic brain injury. J Neuroimmunol 135:1–9PubMedCrossRefGoogle Scholar
  30. 30.
    Schwab JM, Beschorner R, Meyermann R, Gozalan F, Schluesener HJ (2002) Persistent accumulation of cyclooxygenase-1-expressing microglial cells and macrophages and transient upregulation by endothelium in human brain injury. J Neurosurg 96:892–899PubMedCrossRefGoogle Scholar
  31. 31.
    Ely EW, Truman B, Shintani A, Thomason JWW, Wheeler AP, Gordon S, Francis J, Speroff T, Gautam S, Margolin R, Sessler CN, Dittus RS, Bernard GR (2003) Monitoring sedation status over time in ICU patients. Reliability and validity of the Richmond Agitation–Sedation Scale (RASS). JAMA 289:2983–2991PubMedCrossRefGoogle Scholar
  32. 32.
    Young GB, Bolton CF, Archibald YM, Austin TW, Wells GA (1992) The electroencephalogram in sepsis-associated encephalopathy. J Clin Neurophysiol 9:145–152PubMedCrossRefGoogle Scholar
  33. 33.
    Zauner C, Gendo A, Kramer L, Funk GC, Bauer E, Schenk P, Ratheipser K, Madl C (2002) Impaired subcortical and cortical sensory evoked potential pathways in septic patients. Crit Care Med 30:1136–1139PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Tarek Sharshar
    • 1
  • Robert Carlier
    • 2
  • Francis Bernard
    • 3
  • Céline Guidoux
    • 1
  • Jean-Philippe Brouland
    • 4
  • Olivier Nardi
    • 1
  • Geoffroy Lorin de la Grandmaison
    • 5
  • Jérôme Aboab
    • 1
  • Françoise Gray
    • 4
  • David Menon
    • 3
  • Djillali Annane
    • 1
  1. 1.Service de Réanimation Médicale, Hôpital Raymond Poincaré (APHP)Faculté de Médecine Paris Ile de France Ouest (UVSQ)GarchesFrance
  2. 2.Service de Radiologie, Hôpital Raymond Poincaré (APHP)Faculté de Médecine Paris Ile de France Ouest (UVSQ)GarchesFrance
  3. 3.University of Cambridge, Box 93Addenbrooke’s HospitalCambridgeUK
  4. 4.Service d’Anatomo-PathologieHôpital LariboisièreParisFrance
  5. 5.Service d’Anatomo-Pathologie et de Médecine LégaleUniversité de Versailles SQY, Hôpital Raymond Poincaré (AP-HP)GarchesFrance

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