Korean Journal of Radiology

The Korean Society of Radiology (대한영상의학회)
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Acute Acquired Metabolic Encephalopathy Based on Diffusion MRI

  • Se Jeong Jeon (Department of Radiology, Wonkwang University Hospital) ;
  • See Sung Choi (Department of Radiology, Wonkwang University Hospital) ;
  • Ha Yon Kim (Department of Radiology, Eulji University Hospital) ;
  • In Kyu Yu (Department of Radiology, Eulji University Hospital)
  • Received : 2019.05.15
  • Accepted : 2020.11.20
  • Published : 2021.12.01
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Abstract

Metabolic encephalopathy is a critical condition that can be challenging to diagnose. Imaging provides early clues to confirm clinical suspicions and plays an important role in the diagnosis, assessment of the response to therapy, and prognosis prediction. Diffusion-weighted imaging is a sensitive technique used to evaluate metabolic encephalopathy at an early stage. Metabolic encephalopathies often involve the deep regions of the gray matter because they have high energy requirements and are susceptible to metabolic disturbances. Understanding the imaging patterns of various metabolic encephalopathies can help narrow the differential diagnosis and improve the prognosis of patients by initiating proper treatment regimen early.

Keywords

References

  1. Bathla G, Policeni B, Agarwal A. Neuroimaging in patients with abnormal blood glucose levels. AJNR Am J Neuroradiol 2014;35:833-840  https://doi.org/10.3174/ajnr.A3486
  2. Sharma P, Eesa M, Scott JN. Toxic and acquired metabolic encephalopathies: MRI appearance. AJR Am J Roentgenol 2009;193:879-886  https://doi.org/10.2214/AJR.08.2257
  3. Sutter R, Kaplan PW. Neuroimaging correlates of acute encephalopathy. J Clin Neurophysiol 2013;30:517-525  https://doi.org/10.1097/WNP.0b013e3182a73be3
  4. Karaarslan E, Arslan A. Diffusion weighted MR imaging in non-infarct lesions of the brain. Eur J Radiol 2008;65:402-416  https://doi.org/10.1016/j.ejrad.2007.04.023
  5. Sutter R, Kaplan PW. What to see when you are looking at confusion: a review of the neuroimaging of acute encephalopathy. J Neurol Neurosurg Psychiatry 2015;86:446-459  https://doi.org/10.1136/jnnp-2014-308216
  6. Koh E, Tsai LK, Hong CT. Serum calcium concentration affects signal changes on diffusion-weighted imaging in hypoglycemic encephalopathy. AJNR Am J Neuroradiol 2012;33:297-300  https://doi.org/10.3174/ajnr.A2766
  7. Kang EG, Jeon SJ, Choi SS, Song CJ, Yu IK. Diffusion MR imaging of hypoglycemic encephalopathy. AJNR Am J Neuroradiol 2010;31:559-564  https://doi.org/10.3174/ajnr.A1856
  8. Witsch J, Neugebauer H, Flechsenhar J, Juttler E. Hypoglycemic encephalopathy: a case series and literature review on outcome determination. J Neurol 2012;259:2172-2181  https://doi.org/10.1007/s00415-012-6480-z
  9. Ikeda T, Takahashi T, Sato A, Tanaka H, Igarashi S, Fujita N, et al. Predictors of outcome in hypoglycemic encephalopathy. Diabetes Res Clin Pract 2013;101:159-163  https://doi.org/10.1016/j.diabres.2013.05.007
  10. Berkovic SF, Bladin PF, Darby DG. Metabolic disorders presenting as stroke. Med J Aust 1984;140:421-424  https://doi.org/10.5694/j.1326-5377.1984.tb108105.x
  11. Cordonnier C, Oppenheim C, Lamy C, Meder JF, Mas JL. Serial diffusion and perfusion-weighted MR in transient hypoglycemia. Neurology 2005;65:175 
  12. Auer RN. Hypoglycemic brain damage. Forensic Sci Int 2004;146:105-110  https://doi.org/10.1016/j.forsciint.2004.08.001
  13. Johkura K, Nakae Y, Kudo Y, Yoshida TN, Kuroiwa Y. Early diffusion MR imaging findings and short-term outcome in comatose patients with hypoglycemia. AJNR Am J Neuroradiol 2012;33:904-909  https://doi.org/10.3174/ajnr.A2903
  14. Ma JH, Kim YJ, Yoo WJ, Ihn YK, Kim JY, Song HH, et al. MR imaging of hypoglycemic encephalopathy: lesion distribution and prognosis prediction by diffusion-weighted imaging. Neuroradiology 2009;51:641-649  https://doi.org/10.1007/s00234-009-0544-5
  15. Bathla G, Hegde AN. MRI and CT appearances in metabolic encephalopathies due to systemic diseases in adults. Clin Radiol 2013;68:545-554  https://doi.org/10.1016/j.crad.2012.05.021
  16. Schmidt P, Bottcher J, Ragoschke-Schumm A, Mentzel HJ, Wolf G, Muller UA, et al. Diffusion-weighted imaging of hyperacute cerebral hypoglycemia. AJNR Am J Neuroradiol 2011;32:1321-1327  https://doi.org/10.3174/ajnr.A2464
  17. Chan R, Erbay S, Oljeski S, Thaler D, Bhadelia R. Case report: hypoglycemia and diffusion-weighted imaging. J Comput Assist Tomogr 2003;27:420-423  https://doi.org/10.1097/00004728-200305000-00020
  18. Kitabchi AE, Umpierrez GE, Murphy MB, Kreisberg RA. Hyperglycemic crises in adult patients with diabetes: a consensus statement from the American Diabetes Association. Diabetes Care 2006;29:2739-2748  https://doi.org/10.2337/dc06-9916
  19. Kitabchi AE, Umpierrez GE, Miles JM, Fisher JN. Hyperglycemic crises in adult patients with diabetes. Diabetes Care 2009;32:1335-1343  https://doi.org/10.2337/dc09-9032
  20. Cherian A, Thomas B, Baheti NN, Chemmanam T, Kesavadas C. Concepts and controversies in nonketotic hyperglycemia-induced hemichorea: further evidence from susceptibility-weighted MR imaging. J Magn Reson Imaging 2009;29:699-703  https://doi.org/10.1002/jmri.21672
  21. Lee EJ, Choi JY, Lee SH, Song SY, Lee YS. Hemichorea-hemiballism in primary diabetic patients: MR correlation. J Comput Assist Tomogr 2002;26:905-911  https://doi.org/10.1097/00004728-200211000-00009
  22. Atay M, Yetis H, Kurtcan S, Aralasmak A, Alkan A. Susceptibility weighted imaging features of nonketotic hyperglycemia: unusual cause of hemichorea-hemiballismus. J Neuroimaging 2015;25:319-324  https://doi.org/10.1111/jon.12084
  23. Bizet J, Cooper CJ, Quansah R, Rodriguez E, Teleb M, Hernandez GT. Chorea, Hyperglycemia, Basal Ganglia Syndrome (C-H-BG) in an uncontrolled diabetic patient with normal glucose levels on presentation. Am J Case Rep 2014;15:143-146  https://doi.org/10.12659/AJCR.890179
  24. Lee BC, Hwang SH, Chang GY. Hemiballismus-hemichorea in older diabetic women: a clinical syndrome with MRI correlation. Neurology 1999;52:646-648  https://doi.org/10.1212/WNL.52.3.646
  25. Nagai C, Kato T, Katagiri T, Sasaki H. Hyperintense putamen on T1-weighted MR images in a case of chorea with hyperglycemia. AJNR Am J Neuroradiol 1995;16:1243-1246 
  26. Kandiah N, Tan K, Lim CC, Venketasubramanian N. Hyperglycemic choreoathetosis: role of the putamen in pathogenesis. Mov Disord 2009;24:915-919  https://doi.org/10.1002/mds.22277
  27. Dewey RB Jr, Jankovic J. Hemiballism-hemichorea. Clinical and pharmacologic findings in 21 patients. Arch Neurol 1989;46:862-867  https://doi.org/10.1001/archneur.1989.00520440044020
  28. Wintermark M, Fischbein NJ, Mukherjee P, Yuh EL, Dillon WP. Unilateral putaminal CT, MR, and diffusion abnormalities secondary to nonketotic hyperglycemia in the setting of acute neurologic symptoms mimicking stroke. AJNR Am J Neuroradiol 2004;25:975-976 
  29. Chu K, Kang DW, Kim DE, Park SH, Roh JK. Diffusion-weighted and gradient echo magnetic resonance findings of hemichorea-hemiballismus associated with diabetic hyperglycemia: a hyperviscosity syndrome? Arch Neurol 2002;59:448-452  https://doi.org/10.1001/archneur.59.3.448
  30. Chua CB, Sun CK, Hsu CW, Tai YC, Liang CY, Tsai IT. "Diabetic striatopathy": clinical presentations, controversy, pathogenesis, treatments, and outcomes. Sci Rep 2020;10:1594 
  31. Kumar S, Berl T. Sodium. Lancet 1998;352:220-228  https://doi.org/10.1016/S0140-6736(97)12169-9
  32. Cordoba J, Garcia-Martinez R, Simon-Talero M. Hyponatremic and hepatic encephalopathies: similarities, differences and coexistence. Metab Brain Dis 2010;25:73-80  https://doi.org/10.1007/s11011-010-9172-3
  33. Fraser CL, Arieff AI. Epidemiology, pathophysiology, and management of hyponatremic encephalopathy. Am J Med 1997;102:67-77  https://doi.org/10.1016/S0002-9343(96)00274-4
  34. Reynolds RM, Padfield PL, Seckl JR. Disorders of sodium balance. BMJ 2006;332:702-705  https://doi.org/10.1136/bmj.332.7543.702
  35. Forster A, Nolte I, Wenz H, Al-Zghloul M, Kerl HU, Brockmann C, et al. Value of diffusion-weighted imaging in central pontine and extrapontine myelinolysis. Neuroradiology 2013;55:49-56  https://doi.org/10.1007/s00234-012-1083-z
  36. Chu K, Kang DW, Ko SB, Kim M. Diffusion-weighted MR findings of central pontine and extrapontine myelinolysis. Acta Neurol Scand 2001;104:385-388  https://doi.org/10.1034/j.1600-0404.2001.00096.x
  37. Menger H, Jorg J. Outcome of central pontine and extrapontine myelinolysis (n = 44). J Neurol 1999;246:700-705  https://doi.org/10.1007/s004150050435
  38. Graff-Radford J, Fugate JE, Kaufmann TJ, Mandrekar JN, Rabinstein AA. Clinical and radiologic correlations of central pontine myelinolysis syndrome. Mayo Clin Proc 2011;86:1063-1067  https://doi.org/10.4065/mcp.2011.0239
  39. Chen JJ, Chang HF, Chen DL. Recurrent episodic vertigo secondary to hyponatremic encephalopathy from water intoxication. Neurosciences (Riyadh) 2014;19:328-330 
  40. Yalcin-Cakmakli G, Karli Oguz K, Shorbagi A, Funda Bas D, Ergan-Arsava B, Kunt M, et al. Hyponatremic encephalopathy after excessive water ingestion prior to pelvic ultrasound: neuroimaging findings. Intern Med 2010;49:1807-1811  https://doi.org/10.2169/internalmedicine.49.3395
  41. Adrogue HJ, Madias NE. Hypernatremia. N Engl J Med 2000;342:1493-1499  https://doi.org/10.1056/NEJM200005183422006
  42. Bhatia S, Kapoor AK, Sharma A, Gupta R, Kataria S. Cerebral encephalopathy with extrapontine myelinolysis in a case of postpartum hypernatremia. Indian J Radiol Imaging 2014;24:57-60  https://doi.org/10.4103/0971-3026.130697
  43. Ismail FY, Szollics A, Szolics M, Nagelkerke N, Ljubisavljevic M. Clinical semiology and neuroradiologic correlates of acute hypernatremic osmotic challenge in adults: a literature review. AJNR Am J Neuroradiol 2013;34:2225-2232  https://doi.org/10.3174/ajnr.A3392
  44. Saroja AO, Naik KR, Mali RV, Kunam SR. 'Wine Glass' sign in recurrent postpartum hypernatremic osmotic cerebral demyelination. Ann Indian Acad Neurol 2013;16:106-110  https://doi.org/10.4103/0972-2327.107719
  45. Brouns R, De Deyn PP. Neurological complications in renal failure: a review. Clin Neurol Neurosurg 2004;107:1-16  https://doi.org/10.1016/j.clineuro.2004.07.012
  46. Kang E, Jeon SJ, Choi SS. Uremic encephalopathy with atypical magnetic resonance features on diffusion-weighted images. Korean J Radiol 2012;13:808-811  https://doi.org/10.3348/kjr.2012.13.6.808
  47. Wang HC, Cheng SJ. The syndrome of acute bilateral basal ganglia lesions in diabetic uremic patients. J Neurol 2003;250:948-955  https://doi.org/10.1007/s00415-003-1122-0
  48. Wang HC, Brown P, Lees AJ. Acute movement disorders with bilateral basal ganglia lesions in uremia. Mov Disord 1998;13:952-957  https://doi.org/10.1002/mds.870130615
  49. Kim TK, Seo SI, Kim JH, Lee NJ, Seol HY. Diffusion-weighted magnetic resonance imaging in the syndrome of acute bilateral basal ganglia lesions in diabetic uremia. Mov Disord 2006;21:1267-1270  https://doi.org/10.1002/mds.20932
  50. Moe SM, Sprague SM. Uremic encephalopathy. Clin Nephrol 1994;42:251-256 
  51. Okada J, Yoshikawa K, Matsuo H, Kanno K, Oouchi M. Reversible MRI and CT findings in uremic encephalopathy. Neuroradiology 1991;33:524-526  https://doi.org/10.1007/BF00588046
  52. Biasioli S, D'Andrea G, Feriani M, Chiaramonte S, Fabris A, Ronco C, et al. Uremic encephalopathy: an updating. Clin Nephrol 1986;25:57-63 
  53. Pruss H, Siebert E, Masuhr F. Reversible cytotoxic brain edema and facial weakness in uremic encephalopathy. J Neurol 2009;256:1372-1373  https://doi.org/10.1007/s00415-009-5125-3
  54. U-King-Im JM, Yu E, Bartlett E, Soobrah R, Kucharczyk W. Acute hyperammonemic encephalopathy in adults: imaging findings. AJNR Am J Neuroradiol 2011;32:413-418  https://doi.org/10.3174/ajnr.A2290
  55. Kim JY, Yu IK. Acute hyperammonemic encephalopathy with features on diffusion-weighted images: report of two cases. J Korean Soc Radiol 2015;72:131-135  https://doi.org/10.3348/jksr.2015.72.2.131
  56. Rosario M, McMahon K, Finelli PF. Diffusion-weighted imaging in acute hyperammonemic encephalopathy. Neurohospitalist 2013;3:125-130  https://doi.org/10.1177/1941874412467806
  57. McKinney AM, Sarikaya B, Spanbauer J, Lohman BD, Uhlmann E. Acute hepatic (or hyperammonemic) encephalopathy: diffuse cortical injury and the significance of ammonia. AJNR Am J Neuroradiol 2011;32:E142; author reply E143 
  58. Scott TR, Kronsten VT, Hughes RD, Shawcross DL. Pathophysiology of cerebral oedema in acute liver failure. World J Gastroenterol 2013;19:9240-9255  https://doi.org/10.3748/wjg.v19.i48.9240
  59. Rodrigo R, Cauli O, Boix J, ElMlili N, Agusti A, Felipo V. Role of NMDA receptors in acute liver failure and ammonia toxicity: therapeutical implications. Neurochem Int 2009;55:113-118  https://doi.org/10.1016/j.neuint.2009.01.007
  60. Lichter-Konecki U, Mangin JM, Gordish-Dressman H, Hoffman EP, Gallo V. Gene expression profiling of astrocytes from hyperammonemic mice reveals altered pathways for water and potassium homeostasis in vivo. Glia 2008;56:365-377  https://doi.org/10.1002/glia.20624
  61. Bindu PS, Sinha S, Taly AB, Christopher R, Kovoor JM. Cranial MRI in acute hyperammonemic encephalopathy. Pediatr Neurol 2009;41:139-142  https://doi.org/10.1016/j.pediatrneurol.2009.02.012
  62. Takanashi J, Barkovich AJ, Cheng SF, Kostiner D, Baker JC, Packman S. Brain MR imaging in acute hyperammonemic encephalopathy arising from late-onset ornithine transcarbamylase deficiency. AJNR Am J Neuroradiol 2003;24:390-393 
  63. Capizzano AA, Sanchez A, Moritani T, Yager J. Hyperammonemic encephalopathy: time course of MRI diffusion changes. Neurology 2012;78:600-601  https://doi.org/10.1212/WNL.0b013e318247ccd1
  64. Atluri DK, Prakash R, Mullen KD. Pathogenesis, diagnosis, and treatment of hepatic encephalopathy. J Clin Exp Hepatol 2011;1:77-86  https://doi.org/10.1016/S0973-6883(11)60126-6
  65. Rovira A, Alonso J, Cordoba J. MR imaging findings in hepatic encephalopathy. AJNR Am J Neuroradiol 2008;29:1612-1621  https://doi.org/10.3174/ajnr.A1139
  66. Poordad FF. Review article: the burden of hepatic encephalopathy. Aliment Pharmacol Ther 2007;25 Suppl 1:3-9  https://doi.org/10.1111/j.1746-6342.2006.03215.x
  67. Thumburu KK, Taneja S, Vasishta RK, Dhiman RK. Neuropathology of acute liver failure. Neurochem Int 2012;60:672-675  https://doi.org/10.1016/j.neuint.2011.10.013
  68. Desjardins P, Du T, Jiang W, Peng L, Butterworth RF. Pathogenesis of hepatic encephalopathy and brain edema in acute liver failure: role of glutamine redefined. Neurochem Int 2012;60:690-696  https://doi.org/10.1016/j.neuint.2012.02.001
  69. McKinney AM, Lohman BD, Sarikaya B, Uhlmann E, Spanbauer J, Singewald T, et al. Acute hepatic encephalopathy: diffusion-weighted and fluid-attenuated inversion recovery findings, and correlation with plasma ammonia level and clinical outcome. AJNR Am J Neuroradiol 2010;31:1471-1479  https://doi.org/10.3174/ajnr.A2112
  70. Zhang LJ, Zhong J, Lu GM. Multimodality MR imaging findings of low-grade brain edema in hepatic encephalopathy. AJNR Am J Neuroradiol 2013;34:707-715  https://doi.org/10.3174/ajnr.A2968
  71. Bleibel W, Al-Osaimi AM. Hepatic encephalopathy. Saudi J Gastroenterol 2012;18:301-309  https://doi.org/10.4103/1319-3767.101123
  72. Wernicke C. Die akute hamorrhagische Polioencephalitis superior. In: Wernicke C, ed. Lehrbuch der Gehirnkrankheiten fur Arzte und Studierende, Vol. 1-3. Kassel: Fisher Verlag, 1881:229-242 
  73. Manzo G, De Gennaro A, Cozzolino A, Serino A, Fenza G, Manto A. MR imaging findings in alcoholic and nonalcoholic acute Wernicke's encephalopathy: a review. Biomed Res Int 2014;2014:503596 
  74. Cerase A, Rubenni E, Rufa A, Vallone I, Galluzzi P, Coratti G, et al. CT and MRI of Wernicke's encephalopathy. Radiol Med 2011;116:319-333  https://doi.org/10.1007/s11547-011-0618-x
  75. Halavaara J, Brander A, Lyytinen J, Setala K, Kallela M. Wernicke's encephalopathy: is diffusion-weighted MRI useful? Neuroradiology 2003;45:519-523  https://doi.org/10.1007/s00234-003-1043-8
  76. Fattal-Valevski A, Kesler A, Sela BA, Nitzan-Kaluski D, Rotstein M, Mesterman R, et al. Outbreak of life-threatening thiamine deficiency in infants in Israel caused by a defective soy-based formula. Pediatrics 2005;115:e233-e238  https://doi.org/10.1542/peds.2004-1255
  77. Harper C. The incidence of Wernicke's encephalopathy in Australia--a neuropathological study of 131 cases. J Neurol Neurosurg Psychiatry 1983;46:593-598  https://doi.org/10.1136/jnnp.46.7.593
  78. Hazell AS, Todd KG, Butterworth RF. Mechanisms of neuronal cell death in Wernicke's encephalopathy. Metab Brain Dis 1998;13:97-122  https://doi.org/10.1023/A:1020657129593
  79. Moritani T, Smoker WR, Sato Y, Numaguchi Y, Westesson PL. Diffusion-weighted imaging of acute excitotoxic brain injury. AJNR Am J Neuroradiol 2005;26:216-228 
  80. Weidauer S, Rosler A, Zanella FE, Lanfermann H. Diffusion-weighted imaging in Wernicke encephalopathy associated with stomach cancer: case report and review of the literature. Eur Neurol 2004;51:55-57  https://doi.org/10.1159/000075093
  81. Chu K, Kang DW, Kim HJ, Lee YS, Park SH. Diffusion-weighted imaging abnormalities in wernicke encephalopathy: reversible cytotoxic edema? Arch Neurol 2002;59:123-127  https://doi.org/10.1001/archneur.59.1.123