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Hepatic encephalopathy on magnetic resonance imaging and its uncertain differential diagnoses: a narrative review

  • Chun Geun Lim (Department of Radiology, Kyungpook National University Hospital, School of Medicine, Kyungpook National University) ;
  • Myong Hun Hahm (Department of Radiology, Kyungpook National University Hospital, School of Medicine, Kyungpook National University) ;
  • Hui Joong Lee (Department of Radiology, Kyungpook National University Hospital, School of Medicine, Kyungpook National University)
  • Received : 2022.09.29
  • Accepted : 2022.11.11
  • Published : 2023.04.30

Abstract

Hepatic encephalopathy (HE) is a severe neuropsychiatric abnormality in patients with either acute or chronic liver failure. Typical brain magnetic resonance imaging findings of HE are bilateral basal ganglia high signal intensities due to manganese deposition in chronic liver disease and hyperintensity in T2, fluid-attenuated inversion recovery, or diffusion-weighted imaging (DWI) with hemispheric white matter changes including the corticospinal tract. Low values on apparent diffusion coefficient mapping of the affected area on DWI, indicating cytotoxic edema, can be observed in acute HE. However, neuropsychological impairment in HE ranges from mild deficits in psychomotor abilities affecting quality of life to stupor or coma with higher grades of hepatic dysfunction. In particular, the long-lasting compensatory mechanisms for the altered metabolism in chronic liver disease make HE imaging results variable. Therefore, the clinical relevance of imaging findings is uncertain and differentiating HE from other metabolic diseases can be difficult. The recent introduction of concepts such as "acute-on-chronic liver failure (ACLF)," a new clinical entity, has led to a change in the clinical view of HE. Accordingly, there is a need to establish a corresponding concept in the field of neuroimaging diagnosis. Herein, we review HE from a historical and etiological perspective to increase understanding of brain imaging and help establish an imaging approach for advanced new concepts such as ACLF. The purpose of this manuscript is to provide an understanding of HE by reviewing neuroimaging findings based on pathological and clinical concepts of HE, thereby assisting in neuroimaging interpretation.

Keywords

References

  1. Hazell AS, Butterworth RF. Hepatic encephalopathy: an update of pathophysiologic mechanisms. Proc Soc Exp Biol Med 1999;222:99-112. https://doi.org/10.1046/j.1525-1373.1999.d01-120.x
  2. Sherlock S. Hepatic encephalopathy. Br J Hosp Med 1977;17: 144-6, 151-4, 159. 
  3. Inoue E, Hori S, Narumi Y, Fujita M, Kuriyama K, Kadota T, et al. Portal-systemic encephalopathy: presence of basal ganglia lesions with high signal intensity on MR images. Radiology 1991;179:551-5. https://doi.org/10.1148/radiology.179.2.2014310
  4. Syh HW, Chu WK, Mar N, McConnell JR. An image analysis on MR imaging of the brain for hepatic encephalopathy. Biomed Sci Instrum 1991;27:29-33.
  5. Zeneroli ML, Cioni G, Crisi G, Vezzelli C, Ventura E. Globus pallidus alterations and brain atrophy in liver cirrhosis patients with encephalopathy: an MR imaging study. Magn Reson Imaging 1991;9:295-302. https://doi.org/10.1016/0730-725X(91)90414-H
  6. Zeron HM, Rodriguez MR, Montes S, Castaneda CR. Blood manganese levels in patients with hepatic encephalopathy. J Trace Elem Med Biol 2011;25:225-9. https://doi.org/10.1016/j.jtemb.2011.07.003
  7. Pujol A, Pujol J, Graus F, Rimola A, Peri J, Mercader JM, et al. Hyperintense globus pallidus on T1-weighted MRI in cirrhotic patients is associated with severity of liver failure. Neurology 1993;43:65-9. 
  8. Krieger D, Krieger S, Jansen O, Gass P, Theilmann L, Lichtnecker H. Manganese and chronic hepatic encephalopathy. Lancet 1995;346:270-4. 
  9. Lee DH, Lee HJ, Hahm MH. The pallidal index in patients with acute-on-chronic liver disease: is it a predictor of severe hepatic encephalopathy? Investig Magn Reson Imaging 2017;21:125-30. https://doi.org/10.13104/imri.2017.21.3.125
  10. Rovira A, Cordoba J, Sanpedro F, Grive E, Rovira-Gols A, Alonso J. Normalization of T2 signal abnormalities in hemispheric white matter with liver transplant. Neurology 2002;59:335-41. https://doi.org/10.1212/WNL.59.3.335
  11. Gabriel S, Grossmann A, Hoppner J, Benecke R, Rolfs A. Marchiafava-Bignami syndrome: extrapontine myelinolysis in chronic alcoholism. Nervenarzt 1999;70:349-56. https://doi.org/10.1007/s001150050447
  12. Alvarez-Leal M, Contreras-Hernandez D, Chavez A, Diaz-Contreras JA, Careaga-Olivares J, Zuniga-Charles MA, et al. Leukocyte arylsulfatase A activity in patients with alcohol-related cirrhosis. Am J Hum Biol 2001;13:297-300. https://doi.org/10.1002/ajhb.1052
  13. Rovira A, Alonso J, Cordoba J. MR imaging findings in hepatic encephalopathy. AJNR Am J Neuroradiol 2008;29:1612-21. https://doi.org/10.3174/ajnr.A1139
  14. Arnold SM, Els T, Spreer J, Schumacher M. Acute hepatic encephalopathy with diffuse cortical lesions. Neuroradiology 2001;43:551-4. https://doi.org/10.1007/s002340000461
  15. Matsusue E, Kinoshita T, Ohama E, Ogawa T. Cerebral cortical and white matter lesions in chronic hepatic encephalopathy: MR-pathologic correlations. AJNR Am J Neuroradiol 2005; 26:347-51.
  16. Kreis R, Ross BD, Farrow NA, Ackerman Z. Metabolic disorders of the brain in chronic hepatic encephalopathy detected with H-1 MR spectroscopy. Radiology 1992;182:19-27. https://doi.org/10.1148/radiology.182.1.1345760
  17. Binesh N, Huda A, Thomas MA, Wyckoff N, Bugbee M, Han S, et al. Hepatic encephalopathy: a neurochemical, neuroanatomical, and neuropsychological study. J Appl Clin Med Phys 2006; 7:86-96. https://doi.org/10.1120/jacmp.2027.25374
  18. Binesh N, Huda A, Bugbee M, Gupta R, Rasgon N, Kumar A, et al. Adding another spectral dimension to 1H magnetic resonance spectroscopy of hepatic encephalopathy. J Magn Reson Imaging 2005;21:398-405. https://doi.org/10.1002/jmri.20291
  19. Taylor-Robinson SD, Sargentoni J, Oatridge A, Bryant DJ, Hajnal JV, Marcus CD, et al. MR imaging and spectroscopy of the basal ganglia in chronic liver disease: correlation of T1-weighted contrast measurements with abnormalities in proton and phosphorus-31 MR spectra. Metab Brain Dis 1996;11:249-68. https://doi.org/10.1007/BF02237962
  20. Butterworth R. Neuronal cell death in hepatic encephalopathy. Metab Brain Dis 2007;22:309-20. https://doi.org/10.1007/s11011-007-9072-3
  21. Norenberg MD, Bender AS. Astrocyte swelling in liver failure: role of glutamine and benzodiazepines. Acta Neurochir Suppl (Wien) 1994;60:24-7.
  22. Kril JJ, Butterworth RF. Diencephalic and cerebellar pathology in alcoholic and nonalcoholic patients with end-stage liver disease. Hepatology 1997;26:837-41. https://doi.org/10.1002/hep.510260405
  23. Kreis R, Farrow N, Ross BD. Localized 1H NMR spectroscopy in patients with chronic hepatic encephalopathy: analysis of changes in cerebral glutamine, choline and inositols. NMR Biomed 1991;4:109-16. https://doi.org/10.1002/nbm.1940040214
  24. Romero-Gomez M, Montagnese S, Jalan R. Hepatic encephalopathy in patients with acute decompensation of cirrhosis and acute-on-chronic liver failure. J Hepatol 2015;62:437-47. https://doi.org/10.1016/j.jhep.2014.09.005
  25. Victor M, Adams RD, Cole M. The acquired (non-Wilsonian) type of chronic hepatocerebral degeneration. Medicine (Baltimore) 1965;44:345-96. https://doi.org/10.1097/00005792-196509000-00001
  26. Sobel RA, DeArmond SJ, Forno LS, Eng LF. Glial fibrillary acidic protein in hepatic encephalopathy: an immunohistochemical study. J Neuropathol Exp Neurol 1981;40:625-32. https://doi.org/10.1097/00005072-198111000-00004
  27. Butterworth RF, Giguere JF, Michaud J, Lavoie J, Layrargues GP. Ammonia: key factor in the pathogenesis of hepatic encephalopathy. Neurochem Pathol 1987;6:1-12. https://doi.org/10.1007/BF02833598
  28. Kato M, Hughes RD, Keays RT, Williams R. Electron microscopic study of brain capillaries in cerebral edema from fulminant hepatic failure. Hepatology 1992;15:1060-6. https://doi.org/10.1002/hep.1840150615
  29. Desjardins P, Belanger M, Butterworth RF. Alterations in expression of genes coding for key astrocytic proteins in acute liver failure. J Neurosci Res 2001;66:967-71. https://doi.org/10.1002/jnr.10045
  30. Rama Rao KV, Chen M, Simard JM, Norenberg MD. Suppression of ammonia-induced astrocyte swelling by cyclosporin A. J Neurosci Res 2003;74:891-7. https://doi.org/10.1002/jnr.10755
  31. Ferenci P, Lockwood A, Mullen K, Tarter R, Weissenborn K, Blei AT. Hepatic encephalopathy--definition, nomenclature, diagnosis, and quantification: final report of the working party at the 11th World Congresses of Gastroenterology, Vienna, 1998. Hepatology 2002;35:716-21. https://doi.org/10.1053/jhep.2002.31250
  32. Ridola L, Faccioli J, Nardelli S, Gioia S, Riggio O. Hepatic encephalopathy: diagnosis and management. J Transl Int Med 2020;8:210-9. https://doi.org/10.2478/jtim-2020-0034
  33. Haussinger D, Schliess F, Kircheis G. Pathogenesis of hepatic encephalopathy. J Gastroenterol Hepatol 2002;17(Suppl 3):S256-9. https://doi.org/10.1046/j.1440-1746.17.s3.10.x
  34. Jalan R, Williams R. Acute-on-chronic liver failure: pathophysiological basis of therapeutic options. Blood Purif 2002;20:252-61. https://doi.org/10.1159/000047017
  35. Moreau R, Jalan R, Gines P, Pavesi M, Angeli P, Cordoba J, et al. Acute-on-chronic liver failure is a distinct syndrome that develops in patients with acute decompensation of cirrhosis. Gastroenterology 2013;144:1426-37. https://doi.org/10.1053/j.gastro.2013.02.042
  36. Arroyo V, Moreau R, Jalan R. Acute-on-chronic liver failure. N Engl J Med 2020;382:2137-45. https://doi.org/10.1056/NEJMra1914900
  37. Kleinschmidt-DeMasters BK, Filley CM, Rojiani AM. Overlapping features of extrapontine myelinolysis and acquired chronic (non-Wilsonian) hepatocerebral degeneration. Acta Neuropathol 2006;112:605-16. https://doi.org/10.1007/s00401-006-0112-6
  38. Adams RD, Victor M, Mancall EL. Central pontine myelinolysis: a hitherto undescribed disease occurring in alcoholic and malnourished patients. AMA Arch Neurol Psychiatry 1959;81:154-72. https://doi.org/10.1001/archneurpsyc.1959.02340140020004
  39. Ho VB, Fitz CR, Yoder CC, Geyer CA. Resolving MR features in osmotic myelinolysis (central pontine and extrapontine myelinolysis). AJNR Am J Neuroradiol 1993;14:163-7.
  40. Gocht A, Colmant HJ. Central pontine and extrapontine myelinolysis: a report of 58 cases. Clin Neuropathol 1987;6:262-70.
  41. Kim E, Na DG, Kim EY, Kim JH, Son KR, Chang KH. MR imaging of metronidazole-induced encephalopathy: lesion distribution and diffusion-weighted imaging findings. AJNR Am J Neuroradiol 2007;28:1652-8. https://doi.org/10.3174/ajnr.A0655
  42. Behzadi F, Fiester PJ, Rao D. Bilateral hypertrophic olivary degeneration following brainstem insult: a retrospective review and examination of causative pathology. Neurosci Insights 2021;16:26331055211007445.
  43. Jang S, Suh SI, Ha SM, Byeon JH, Eun BL, Lee YH, et al. Enterovirus 71-related encephalomyelitis: usual and unusual magnetic resonance imaging findings. Neuroradiology 2012;54:239-45. https://doi.org/10.1007/s00234-011-0921-8
  44. Di Rocco M, Biancheri R, Rossi A, Allegri AE, Vecchi V, Tortori-Donati P. MRI in acute intermittent maple syrup urine disease. Neurology 2004;63:1078.
  45. Geyer HL, Schaumburg HH, Herskovitz S. Methyl bromide intoxication causes reversible symmetric brainstem and cerebellar MRI lesions. Neurology 2005;64:1279-81. https://doi.org/10.1212/01.WNL.0000156835.12492.30