Neuroimaging of Toxic and Metabolic Disorders

ABSTRACT

Imaging of the brain, magnetic resonance imaging (MRI) in particular, is a key adjunctive tool in the diagnosis and management of toxic-metabolic disorders such as alcoholism, mitochondrial encephalopathies, disorders of iron or copper metabolism, exposure to carbon monoxide, radiotherapy, immunosuppressive agents, toluene, and recreational drugs. In this article, we review the neuroimaging findings of common toxic and metabolic disorders focusing on the role of conventional MRI. We also consider advanced imaging methods, such as magnetic resonance spectroscopy, diffusion MRI, and positron emission tomography. We hope this article will prove useful to trainees and practitioners in the clinical and imaging fields of the neurosciences.

KEYWORDS

Toxin exposure - metabolic disorders - MRI - brain - neurotoxicity

REFERENCES

• 1 Crépat G, Fritsch R. Carbon monoxide: the unnoticed poison of the 21st century. Proceedings of the Satellite Meeting IUTOX VIIIth International Congress of Toxicology July 3–4, 1998 Université de Bourgogne, Dijon, France;
• 2 Ernst A, Zibrak J. Carbon monoxide poisoning.  N Engl J Med. 1998;  339 1603-1608
• 3 Bour H, Tutin M, Pasquier P. The central nervous system and carbon monoxide poisoning: clinical data with reference to 20 fatal cases.  Prog Brain Res. 1967;  24 1-30
• 4 Okazaki H. Fundamentals of Neuropathology. Tokyo; Agaku-Shoin 1989
• 5 Schils F, Cabay J E, Flandroy P, Dondelinger R F. Unusual CT and MRI appearance of carbon monoxide poisoning.  JBR-BTR. 1999;  82 13-15
• 6 Prockop L D. Carbon monoxide brain toxicity: clinical, magnetic resonance imaging, magnetic resonance spectroscopy, and neuropsychological effects in 9 people.  J Neuroimaging. 2005;  15 144-149
• 7 Murata T, Kimura H, Kado H et al.. Neuronal damage in the interval form of CO poisoning determined by serial diffusion weighted magnetic resonance imaging plus 1H-magnetic resonance spectroscopy.  J Neurol Neurosurg Psychiatry. 2001;  71 250-253
• 8 Sener R N. Acute carbon monoxide poisoning: diffusion MR imaging findings.  AJNR Am J Neuroradiol. 2003;  24 1475-1477
• 9 Lo C P, Chen S Y, Chou M C et al.. Diffusion-tensor MR imaging for evaluation of the efficacy of hyperbaric oxygen therapy in patients with delayed neuropsychiatric syndrome caused by carbon monoxide inhalation.  Eur J Neurol. 2007;  14 777-782
• 10 Prockop L D, Chichkova R I. Carbon monoxide intoxication: an updated review.  J Neurol Sci. 2007;  262 122-130
• 11 Scroop R, Sage M R, Voyvodic F, Kat E. Radiographic imaging procedures in the diagnosis of the major central neuropathological consequences of alcohol abuse.  Australas Radiol. 2002;  46 146-153
• 12 Heinrich A, Runge U, Khaw A V. Clinicoradiologic subtypes of Marchiafava-Bignami disease.  J Neurol. 2004;  251 1050-1059
• 13 Kohler C G, Ances B M, Coleman A R, Ragland J D, Lazarev M, Gur R C. Marchiafava-Bignami disease: literature review and case report.  Neuropsychiatry Neuropsychol Behav Neurol. 2000;  13 67-76
• 14 Lavin P J, Smith D, Kori S H, Ellenberger Jr C. Wernicke's encephalopathy: a predictable complication of hyperemesis gravidarum.  Obstet Gynecol. 1983;  62 13s-15s
• 15 Nightingale S, Bates D, Heath P D, Barron S L. Wernicke's encephalopathy in hyperemesis gravidarum.  Postgrad Med J. 1982;  58 558-559
• 16 Wood P, Murray A, Sinha B, Godley M, Goldsmith H J. Wernicke's encephalopathy induced by hyperemesis gravidarum. Case reports.  Br J Obstet Gynaecol. 1983;  90 583-586
• 17 Drenick E J, Joven C B, Swendseid M E. Occurrence of acute Wernicke's encephalopathy during prolonged starvation for the treatment of obesity.  N Engl J Med. 1966;  274 937-939
• 18 Lopez R I, Collins G H. Wernicke's encephalopathy. A complication of chronic hemodialysis.  Arch Neurol. 1968;  18 248-259
• 19 Faris A A. Wernicke's encephalopathy in uremia.  Neurology. 1972;  22 1293-1297
• 20 Park S H, Kim M, Na D L, Jeon B S. Magnetic resonance reflects the pathological evolution of Wernicke encephalopathy.  J Neuroimaging. 2001;  11 406-411
• 21 D'Aprile P, Gentile M A, Carella A. Enhanced MR in the acute phase of Wernicke encephalopathy.  AJNR Am J Neuroradiol. 1994;  15 591-593
• 22 Chu K, Kang D W, Kim H J, Lee Y S, Park S H. Diffusion-weighted imaging abnormalities in Wernicke encephalopathy: reversible cytotoxic edema?.  Arch Neurol. 2002;  59 123-127
• 23 Omer S M, al Kawi M Z, al Watban J, Bohlega S, McLean D R, Miller G. Acute Wernicke's encephalopathy associated with hyperemesis gravidarum: magnetic resonance imaging findings.  J Neuroimaging. 1995;  5 251-253
• 24 Doss A, Mahad D, Romanowski C A. Wernicke encephalopathy: unusual findings in nonalcoholic patients.  J Comput Assist Tomogr. 2003;  27 235-240
• 25 Jauhar P, Montaldi D. Wernicke-Korsakoff syndrome and the use of brain imaging.  Alcohol Alcohol Suppl. 2000;  35 21-23
• 26 Lee S-T, Jung Y-M, Na D L, Park S H, Kim M. Corpus callosum atrophy in Wernicke's encephalopathy.  J Neuroimaging. 2005;  15 367-372
• 27 Liu Y T, Fuh J L, Lirng J F, Li A F, Ho D M, Wang S J. Correlation of magnetic resonance images with neuropathology in acute Wernicke's encephalopathy.  Clin Neurol Neurosurg. 2006;  108 682-687
• 28 Halavaara J, Brander A, Lyytinen J, Setala K, Kallela M. Wernicke's encephalopathy: is diffusion-weighted MRI useful?.  Neuroradiology. 2003;  45 519-523
• 29 Gaul H P, Wallace C J, Auer R N, Fong T C. MR findings in methanol intoxication.  AJNR Am J Neuroradiol. 1995;  16 1783-1786
• 30 Server A, Hovda K E, Nakstad P H, Jacobsen D, Dullerud R, Haakonsen M. Conventional and diffusion-weighted MRI in the evaluation of methanol poisoning. A case report.  Acta Radiol. 2003;  44 691-695
• 31 Keles G T, Orgüç S, Toprak B, Ozaslan S, Sakarya M. Methanol poisoning with necrosis corpus callosum.  Clin Toxicol (Phila). 2007;  45 307-308
• 32 Kuteifan K, Oesterle H, Tajahmady T, Gutbub A M, Laplatte G. Necrosis and haemorrhage of the putamen in methanol poisoning shown on MRI.  Neuroradiology. 1998;  40 158-160
• 33 Halavaara J, Valanne L, Setala K. Neuroimaging supports the clinical diagnosis of methanol poisoning.  Neuroradiology. 2002;  44 924-928
• 34 Peters A S, Schwarze B, Tomandl B, Probst-Cousin S, Lang C J, Hilz M J. Bilateral striatal hyperintensities on diffusion weighted MRI in acute methanol poisoning.  Eur J Neurol. 2007;  14 e1-e2
• 35 Watson J M. Solvent abuse: presentation and clinical diagnosis.  Hum Toxicol. 1982;  1 249-256
• 36 Ashton C H. Solvent abuse.  BMJ. 1990;  300 135-136
• 37 Gospe S M, Calaban M J. Central nervous system distribution of inhaled toluene.  Fundam Appl Toxicol. 1988;  11 540-545
• 38 Aydin K, Sencer S, Demir T, Ogel K, Tunaci A, Minareci O. Cranial MR findings in chronic toluene abuse by inhalation.  AJNR Am J Neuroradiol. 2002;  23 1173-1179
• 39 Kamran S, Bakshi R. MRI in chronic toluene abuse: low signal in the cerebral cortex on T2-weighted images.  Neuroradiology. 1998;  40 519-521
• 40 Caldemeyer K S, Armstrong S W, George K K, Moran C C, Pascuzzi R M. The spectrum of neuroimaging abnormalities in solvent abuse and their clinical correlation.  J Neuroimaging. 1996;  6 167-173
• 41 Aydin K, Sencer S, Ogel K, Genchellac H, Demir T, Minareci O. Single-voxel proton MR spectroscopy in toluene abuse.  Magn Reson Imaging. 2003;  21 777-785
• 42 Caldemeyer K S, Pascuzzi R M, Moran C C, Smith R R. Toluene abuse causing reduced MR signal intensity in the brain.  AJR Am J Roentgenol. 1993;  161 1259-1261
• 43 Unger E, Alexander A, Fritz T, Rosenberg N, Dreisbach J. Toluene abuse: physical basis for hypointensity of the basal ganglia on T2-weighted MR images.  Radiology. 1994;  193 473-476
• 44 Kumar A J, Leeds N E, Fuller G N et al.. Malignant gliomas: MR imaging spectrum of radiation therapy- and chemotherapy-induced necrosis of the brain after treatment.  Radiology. 2000;  217 377-384
• 45 Marks J E, Baglan R J, Prassad S C, Blank W F. Cerebral radionecrosis: incidence and risk in relation to dose, time, fractionation and volume.  Int J Radiat Oncol Biol Phys. 1981;  7 243-252
• 46 Corn B W, Yousem D M, Scott C B et al.. White matter changes are correlated significantly with radiation dose. Observations from a randomized dose-escalation trial for malignant glioma (Radiation Therapy Oncology Group 83–02).  Cancer. 1994;  74 2828-2835
• 47 Valk P E, Dillon W P. Radiation injury of the brain.  AJNR Am J Neuroradiol. 1991;  12 45-62
• 48 Rowley H A, Dillon W P. Iatrogenic white matter diseases.  Neuroimag Clin N Am. 1993;  3 379-404
• 49 Dooms G C, Hecht S, Brant-Zawadzki M, Berthiaume Y, Norman D, Newton T H. Brain radiation lesions: MR imaging.  Radiology. 1986;  158 149-155
• 50 Hein P A, Eskey C J, Dunn J F, Hug E B. Diffusion-weighted imaging in the follow-up of treated high-grade gliomas: tumor recurrence versus radiation injury.  AJNR Am J Neuroradiol. 2004;  25 201-209
• 51 Asao C, Korogi Y, Kitajima M et al.. Diffusion-weighted imaging of radiation-induced brain injury for differentiation from tumor recurrence.  AJNR Am J Neuroradiol. 2005;  26 1455-1460
• 52 Sundgren P C, Fan X, Weybright P et al.. Differentiation of recurrent brain tumor versus radiation injury using diffusion tensor imaging in patients with new contrast-enhancing lesions.  Magn Reson Imaging. 2006;  24 1131-1142
• 53 Langleben D D, Segall G M. PET in differentiation of recurrent brain tumor from radiation injury.  J Nucl Med. 2000;  41 1861-1867
• 54 Wang S X, Boethius J, Ericson K. FDG-PET on irradiated brain tumor: ten years' summary.  Acta Radiol. 2006;  47 85-90
• 55 Tsuyuguchi N, Sunada I, Iwai Y et al.. Methionine positron emission tomography of recurrent metastatic brain tumor and radiation necrosis after stereotactic radiosurgery: is a differential diagnosis possible?.  J Neurosurg. 2003;  98 1056-1064
• 56 Weybright P, Sundgren P C, Maly P et al.. Differentiation between brain tumor recurrence and radiation injury using MR spectroscopy.  AJR Am J Roentgenol. 2005;  185 1471-1476
• 57 Zeng Q S, Li C F, Zhang K, Liu H, Kang X S, Zhen J H. Multivoxel 3D proton MR spectroscopy in the distinction of recurrent glioma from radiation injury.  J Neurooncol. 2007;  84 63-69
• 58 Zeng Q S, Li C F, Liu H, Zhen J H, Feng D C. Distinction between recurrent glioma and radiation injury using magnetic resonance spectroscopy in combination with diffusion-weighted imaging.  Int J Radiat Oncol Biol Physiol. 2007;  68 151-158
• 59 Bakshi R, Ketonen L. MRI of the brain in clinical neurology. In: Joynt RJ, Griggs RC Baker and Joynt's Clinical Neurology [book on CD-ROM]. Philadelphia, PA; Lippincott Williams & Wilkins 2004
• 60 Bakshi R, Shaikh Z A, Bates V E, Kinkel P R. Thrombotic thrombocytopenic purpura: brain CT and MRI findings in 12 cases.  Neurology. 1999;  52 1285-1288
• 61 Watanabe Y, Mitomo M, Tokuda Y et al.. Eclamptic encephalopathy: MRI, including diffusion-weighted images.  Neuroradiology. 2002;  44 981-985
• 62 Hinchey J, Chaves C, Appignani B et al.. A reversible posterior leukoencephalopathy syndrome.  N Engl J Med. 1996;  334 494-500
• 63 Schwartz R B, Bravo S M, Klufas R A et al.. Cyclosporin neurotoxicity and its relationship to hypertensive encephalopathy: CT and MR findings in 16 cases.  AJR Am J Roentgenol. 1995;  165 627-631
• 64 Galassi G, Tassone G, Sintini M, Spagnoli M, Bertolani L, Mavilla L. 5-Fluorouracil- and levamisole-associated multifocal leukoencephalopathy.  Eur Neurol. 1996;  36 244-246
• 65 Savarese D M, Gordon J, Smith T W et al.. Cerebral demyelination syndrome in a patient treated with 5-fluorouracil and levamisole. The use of thallium SPECT imaging to assist in noninvasive diagnosis—a case report.  Cancer. 1996;  77 387-394
• 66 Honkaniemi J, Kähärä V, Dastidar P et al.. Reversible posterior leukoencephalopathy after combination chemotherapy.  Neuroradiology. 2000;  42 895-899
• 67 Furukawa M, Terae S, Chu B C et al.. MRI in seven cases of tacrolimus (FK-506) encephalopathy: utility of FLAIR and diffusion-weighted imaging.  Neuroradiology. 2001;  43 615-621
• 68 Yamamoto A, Hayakawa K, Houjyou M. CT and MRI findings of cyclosporine-related encephalopathy and hypertensive encephalopathy.  Pediatr Radiol. 2002;  32 340-343
• 69 Jarosz J M, Howlett D C, Cox T C, Bingham J B. Cyclosporine-related reversible posterior leukoencephalopathy: MRI.  Neuroradiology. 1997;  39 711-715
• 70 Pace M T, Slovis T L, Kelly J K, Abella S D. Cyclosporin A toxicity: MRI appearance of the brain.  Pediatr Radiol. 1995;  25 180-183
• 71 Goodman J M, Kuzma B. Encephalopathy following heart-lung transplantation.  Surg Neurol. 1996;  46 157
• 72 Fisher N C, Ruban E, Carey M, Heafield M T, West R J, Adams D H. Late-onset fatal acute leucoencephalopathy in liver transplant recipient.  Lancet. 1997;  349 1884-1885
• 73 Kanekiyo T, Hara J, Matsuda-Hashii Y et al.. Tacrolimus-related encephalopathy following allogeneic stem cell transplantation in children.  Int J Hematol. 2005;  81 264-268
• 74 Israel Z H, Lossos A, Barak V, Soffer D, Siegal T. Multifocal demyelinative leukoencephalopathy associated with 5-fluorouracil and levamisole.  Acta Oncol. 2000;  39 117-120
• 75 Franco D A, Greenberg H S. 5-FU multifocal inflammatory leukoencephalopathy and dihydropyrimidine dehydrogenase deficiency.  Neurology. 2001;  56 110-112
• 76 Hook C C, Kimmell D W, Kvols L K et al.. Multifocal inflammatory leukoencephalopathy with 5-fluorouracil and levamisole.  Ann Neurol. 1992;  31 262-267
• 77 Ishibashi S, Nishimura H, Mizusawa H. 5-FU-induced acute leukoencephalopathy.  Intern Med. 2004;  43 1009-1010
• 78 Lazarus H M, Herzig R H, Herzig G P, Phillips G L, Roessmann U, Fishman D J. Central nervous system toxicity of high-dose systemic cytosine arabinoside.  Cancer. 1981;  48 2577-2582
• 79 Zawacki T, Friedman J H, Grace J, Shetty N. Cerebellar toxicity of cytosine arabinoside: clinical and neuropsychological signs.  Neurology. 2000;  55 1234
• 80 Friedman J H, Shetty N. Permanent cerebellar toxicity of cytosine arabinoside (Ara C) in a young woman.  Mov Disord. 2001;  16 575-577
• 81 Yeshurun M, Marsot Dupuch K. Acute cerebellar syndrome following intermediate-dose cytarabine.  Br J Haematol. 2001;  113 846
• 82 Henderson R D, Rajah T, Nicol A J, Read S J. Posterior leukoencephalopathy following intrathecal chemotherapy with MRA-documented vasospasm.  Neurology. 2003;  60 326-328
• 83 Counsel P, Khangure M. Myelopathy due to intrathecal chemotherapy: magnetic resonance imaging findings.  Clin Radiol. 2007;  62 172-176
• 84 Ziereisen F, Dan B, Azzi N, Ferster A, Damry N, Christophe C. Reversible acute methotrexate leukoencephalopathy: atypical brain MR imaging features.  Pediatr Radiol. 2006;  36 205-212
• 85 Ebner F, Ranner G, Slavc I et al.. MR findings in methotrexate-induced CNS abnormalities.  AJR Am J Roentgenol. 1989;  153 1283-1288
• 86 Lien H H, Blomlie V, Saeter G, Solheim O, Fossa S D. Osteogenic sarcoma: MR signal abnormalities of the brain in asymptomatic patients treated with high-dose methotrexate.  Radiology. 1991;  179 547-550
• 87 Chu W C, Chik K W, Chan Y L et al.. White matter and cerebral metabolite changes in children undergoing treatment for acute lymphoblastic leukemia: longitudinal study with MR imaging and 1H MR spectroscopy.  Radiology. 2003;  229 659-669
• 88 Bartzokis G, Beckson M, Hance D B et al.. Magnetic resonance imaging evidence of “silent” cerebrovascular toxicity in cocaine dependence.  Biol Psychiatry. 1999;  45 1203-1211
• 89 Lyoo I K, Streeter C C, Ahn K H et al.. White matter hyperintensities in subjects with cocaine and opiate dependence and healthy comparison subjects.  Psychiatry Res. 2004;  131 135-145
• 90 He G Q, Zhang A, Altura B T, Altura B M. Cocaine-induced cerebrovasospasm and its possible mechanism of action.  J Pharmacol Exp Ther. 1994;  268 1532-1539
• 91 Madden J A, Konkol R J, Keller P A, Alvarez T A. Cocaine and benzoylecgonine constrict cerebral arteries by different mechanisms.  Life Sci. 1995;  56 679-686
• 92 Andrews P. Cocaethylene toxicity.  J Addict Dis. 1997;  16 75-84
• 93 Bartzokis G, Beckson M, Lu P H et al.. Age-related brain volume reductions in amphetamine and cocaine addicts and normal controls: implications for addiction research.  Psychiatry Res. 2000;  98 93-102
• 94 Moeller F G, Hasan K M, Steinberg J L et al.. Reduced anterior corpus callosum white matter integrity is related to increased impulsivity and reduced discriminability in cocaine-dependent subjects: diffusion tensor imaging.  Neuropsychopharmacology. 2005;  30 610-617
• 95 Aron J L, Paulus M P. Location, location: using functional magnetic resonance imaging to pinpoint brain differences relevant to stimulant use.  Addiction. 2007;  102(S1) 33-43
• 96 Bae S C, Lyoo I K, Sung Y H et al.. Increased white matter hyperintensities in male methamphetamine abusers.  Drug Alcohol Depend. 2006;  81 83-88
• 97 Myers R E, Anderson L I, Dluzen D E. Estrogen, but not testosterone, attenuates methamphetamine-evoked dopamine output from superfused striatal tissue of female and male mice.  Neuropharmacology. 2003;  44 624-632
• 98 Jernigan T L, Gamst A C, Archibald S L et al.. Effects of methamphetamine dependence and HIV infection on cerebral morphology.  Am J Psychiatry. 2005;  162 1461-1472
• 99 Chang L, Cloak C, Patterson K, Grob C, Miller E N, Ernst T. Enlarged striatum in abstinent methamphetamine abusers: a possible compensatory response.  Biol Psychiatry. 2005;  57 967-974
• 100 Oh J S, Lyoo I K, Sung Y H et al.. Shape changes of the corpus callosum in abstinent methamphetamine users.  Neurosci Lett. 2005;  384 76-81
• 101 Sung Y H, Cho S C, Hwang J et al.. Relationship between N-acetyl-aspartate in gray and white matter of abstinent methamphetamine abusers and their history of drug abuse: a proton magnetic resonance spectroscopy study.  Drug Alcohol Depend. 2007;  88 28-35
• 102 Hagel J, Andrews G, Vertinsky T, Heran M K, Keogh C. “Chasing the dragon”–imaging of heroin inhalation leukoencephalopathy.  Can Assoc Radiol J. 2005;  56 199-203
• 103 Wolters E C, van Wijngaarden G K, Stam F C et al.. Leukoencephalopathy after inhaling “heroin” pyrolysate.  Lancet. 1982;  2 1233-1237
• 104 Kriegstein A R, Shungu D C, Millar W S, Armitage B A, Brust J C, Chillrud S. Leukoencephalopathy and raised brain lactate from heroin vapor inhalation (“chasing the dragon”).  Neurology. 1999;  53 1765-1773
• 105 Au-Yeung K, Lai C. Toxic leucoencephalopathy after heroin inhalation.  Australas Radiol. 2002;  46 306-308
• 106 Keogh C F, Andrews G T, Spacey S D, Forkheim K E, Graeb D A. Neuroimaging features of heroin inhalation toxicity: “chasing the dragon.”  AJR Am J Roentgenol. 2003;  180 847-850
• 107 Weber W, Henkes H, Moller P, Bade K, Kuhne D. Toxic spongiform leucoencephalopathy after inhaling heroin vapour.  Eur Radiol. 1998;  8 749-755
• 108 Tan T P, Algra P R, Valk J, Wolters E C. Toxic leukoencephalopathy after inhalation of poisoned heroin: MR findings.  AJNR Am J Neuroradiol. 1994;  15 175-178
• 109 Fitsanakis V A, Zhang N, Avison M, Gore J C, Ashner J L, Ashner M. The use of MRI in the study of manganese neurotoxicity.  Neurotoxicology. 2006;  27 798-806
• 110 Jiang Y, Zheng W, Long L et al.. Brain magnetic resonance imaging and manganese concentrations in red blood cells of smelting workers: search for biomarkers of manganese exposure.  Neurotoxicology. 2007;  28 126-135
• 111 Pujol A, Graus F, Peri J, Mercader J M, Rimola A. Hyperintensity in the globus pallidus on T1-weighted and inversion-recovery MRI: a possible marker of advanced liver disease.  Neurology. 1991;  41 1526-1527
• 112 Kulisevsky J, Pujol J, Balanzo J et al.. Pallidal hyperintensity on magnetic resonance imaging in cirrhotic patients: clinical correlations.  Hepatology. 1992;  16 1382-1388
• 113 Pujol A, Pujol J, Graus F et al.. Hyperintense globus pallidus on T1-weighted MRI in cirrhotic patients is associated with severity of liver failure.  Neurology. 1993;  43 65-69
• 114 Krieger D, Krieger S, Jansen O, Gass P, Theilmann L, Lichtnecker H. Manganese and chronic hepatic encephalopathy.  Lancet. 1995;  346 270-274
• 115 Ross B D, Jacobson S, Villamil F et al.. Subclinical hepatic encephalopathy: proton MR spectroscopic abnormalities.  Radiology. 1994;  193 457-463
• 116 Laubenberger J, Haussinger D, Bayer S, Gufler H, Hennig J, Langer M. Proton magnetic resonance spectroscopy of the brain in symptomatic and asymptomatic patients with liver cirrhosis.  Gastroenterology. 1997;  112 1610-1616
• 117 Rovira A, Grive E, Pedraza S, Rovira A, Alonso J. Magnetization transfer ratio values and proton MR spectroscopy of normal-appearing cerebral white matter in patients with liver cirrhosis.  AJNR Am J Neuroradiol. 2001;  22 1137-1142
• 118 Miese F, Kircheis G, Wittsack H J et al.. 1H-MR spectroscopy, magnetization transfer, and diffusion-weighted imaging in alcoholic and nonalcoholic patients with cirrhosis with hepatic encephalopathy.  AJNR Am J Neuroradiol. 2006;  27 1019-1026
• 119 Binesh N, Huda A, Thomas M A et al.. Hepatic encephalopathy: a neurochemical, neuroanatomical, and neuropsychological study.  J Appl Clin Med Phys. 2006;  7 86-96
• 120 Pavlakis S G, Phillips P C, DiMauro S, De Vivo D C, Rowland L P. Mitochondrial myopathy, encephalopathy, lactic acidosis, and stroke-like episodes: a distinctive clinical syndrome.  Ann Neurol. 1984;  16 481-488
• 121 Bianchi M C, Sgandurra G, Tosetti M, Battini R, Cioni G. Brain magnetic resonance in the diagnostic evaluation of mitochondrial encephalopathies.  Biosci Rep. 2007;  27 69-85
• 122 Scaglia F, Northrop J L. The mitochondrial myopathy encephalopathy, lactic acidosis with stroke-like episodes (MELAS) syndrome: a review of treatment options.  CNS Drugs. 2006;  20 443-464
• 123 Abe K, Yoshimura H, Tanaka H, Fujita N, Hikita T, Sakoda S. Comparison of conventional and diffusion-weighted MRI and proton MR spectroscopy in patients with mitochondrial encephalomyopathy, lactic acidosis, and stroke-like events.  Neuroradiology. 2004;  46 113-117
• 124 Möller H E, Kurlemann G, Pützler M, Wiedermann D, Hilbich T, Fiedler B. Magnetic resonance spectroscopy in patients with MELAS.  J Neurol Sci. 2005;  229–230 131-139
• 125 Oppenheim C, Galanaud D, Samson Y et al.. Can diffusion weighted magnetic resonance imaging help differentiate stroke from stroke-like events in MELAS?.  J Neurol Neurosurg Psychiatry. 2000;  69 248-250
• 126 Barragan-Campos H M, Vallee J N, Lo D et al.. Brain magnetic resonance imaging findings in patients with mitochondrial cytopathies.  Arch Neurol. 2005;  62 737-742
• 127 Valanne L, Ketonen L, Majander A, Suomalainen A, Pihko H. Neuroradiologic findings in children with mitochondrial disorders.  AJNR Am J Neuroradiol. 1998;  19 369-377
• 128 Chu B C, Terae S, Takahashi C et al.. MRI of the brain in the Kearns-Sayre syndrome: report of four cases and a review.  Neuroradiology. 1999;  41 759-764
• 129 Harding A E, Sweeney M G, Miller D H et al.. Occurrence of a multiple sclerosis-like illness in women who have a Leber's hereditary optic neuropathy mitochondrial DNA mutation.  Brain. 1992;  115 979-989
• 130 Küker W, Weir A, Quaghebeur G, Palace J. White matter changes in Leber's hereditary optic neuropathy: MRI findings.  Eur J Neurol. 2007;  14 591-593
• 131 Inglese M, Rovaris M, Bianchi S et al.. Magnetic resonance imaging, magnetisation transfer imaging, and diffusion weighted imaging correlates of optic nerve, brain, and cervical cord damage in Leber's hereditary optic neuropathy.  J Neurol Neurosurg Psychiatry. 2001;  70 444-449
• 132 Arii J, Tanabe Y. Leigh syndrome: serial MR imaging and clinical follow-up.  AJNR Am J Neuroradiol. 2000;  21 1502-1509
• 133 Finsterer J. Central nervous system manifestations of mitochondrial disorders.  Acta Neurol Scand. 2006;  114 217-238
• 134 Medina L, Chi T L, DeVivo D C, Hilal S K. MR findings in patients with subacute necrotizing encephalomyelopathy (Leigh disease): correlation with biochemical defect.  AJNR Am J Neuroradiol. 1990;  11 379-384
• 135 Cooper M A, Fox R. Anesthesia for corrective spinal surgery in a patient with Leigh's disease.  Anesth Analg. 2003;  97 1539-1541
• 136 Detre J A, Wang Z Y, Bogdan A R et al.. Regional variation in brain lactate in Leigh syndrome by localized 1H magnetic resonance spectroscopy.  Ann Neurol. 1991;  29 218-221
• 137 Takahashi S, Oki J, Miyamoto A, Okuno A. Proton magnetic resonance spectroscopy to study the metabolic changes in the brain of a patient with Leigh syndrome.  Brain Dev. 1999;  21 200-204
• 138 Sakai Y, Kira R, Torisu H, Ihara K, Yoshiura T, Hara T. Persistent diffusion abnormalities in the brain stem of three children with mitochondrial diseases.  AJNR Am J Neuroradiol. 2006;  27 1924-1926
• 139 Leutner C, Layer G, Zierz S, Solymosi L, Dewes W, Reiser M. Cerebral MR in ophthalmoplegia plus.  AJNR Am J Neuroradiol. 1994;  15 681-687
• 140 Wray S H, Provenzale J M, Johns D R, Thulborn K R. MR of the brain in mitochondrial myopathy.  AJNR Am J Neuroradiol. 1995;  16 1167-1173
• 141 Zhou B, Westaway S K, Levinson B, Johnson M A, Gitschier J, Hayflick S J. A novel pantothenate kinase gene (PANK2) is defective in Hallervorden-Spatz syndrome.  Nat Genet. 2001;  28 345-349
• 142 Hayflick S J, Westaway S K, Levinson B et al.. Genetic, clinical, and radiographic delineation of Hallervorden-Spatz syndrome.  N Engl J Med. 2003;  348 33-40
• 143 Hayflick S J. Unraveling the Hallervorden-Spatz syndrome: pantothenate kinase-associated neurodegeneration is the name.  Curr Opin Pediatr. 2003;  15 572-577
• 144 Sethi K D, Adams R J, Loring D W, el Gammal T. Hallervorden-Spatz syndrome: clinical and magnetic resonance imaging correlations.  Ann Neurol. 1988;  24 692-694
• 145 Schaffert D A, Johnsen S D, Johnson P C, Drayer B P. Magnetic resonance imaging in pathologically proven Hallervorden-Spatz disease.  Neurology. 1989;  39 440-442
• 146 Hayflick S J, Penzien J M, Michl W et al.. Cranial MRI changes may precede symptoms in Hallervorden-Spatz syndrome.  Pediatr Neurol. 2001;  25 166-169
• 147 Hayflick S J, Hartman M, Coryell J, Gitschier J, Rowley H. Brain MRI in neurodegeneration with brain iron accumulation with and without PANK2 mutations.  AJNR Am J Neuroradiol. 2006;  27 1230-1233
• 148 Curtis A R, Fey C, Morris C M et al.. Mutation in the gene encoding ferritin light polypeptide causes dominant adult-onset basal ganglia disease.  Nat Genet. 2001;  28 350-354
• 149 Chinnery P F, Crompton D E, Birchall D et al.. Clinical features and natural history of neuroferritinopathy caused by the FTL1 460InsA mutation.  Brain. 2007;  130 110-119
• 150 Morita H, Ikeda S, Yamamoto K et al.. Hereditary ceruloplasmin deficiency with hemosiderosis: a clinicopathological study of a Japanese family.  Ann Neurol. 1995;  37 646-656
• 151 Grisoli M, Piperno A, Chiapparini L, Mariani R, Savoiardo M. MR imaging of cerebral cortical involvement in aceruloplasminemia.  AJNR Am J Neuroradiol. 2005;  26 657-661
• 152 Kumar N, Cohen-Gadol A A, Wright R A, Miller G M, Piepgras D G, Ahlskog J E. Superficial siderosis.  Neurology. 2006;  66 1144-1152
• 153 Offenbacher H, Fazekas F, Schmidt R, Kapeller P, Fazekas G. Superficial siderosis of the central nervous system: MRI findings and clinical significance.  Neuroradiology. 1996;  38 S51-S56
• 154 Adams R D, Victor M, Mancall E L. Central pontine myelinolysis: a hitherto undescribed disease occurring in alcoholic and malnourished patients.  AMA Arch Neurol Psychiatry. 1959;  81 154-172
• 155 Tomlinson B E, Pierides A M, Bradley W G. Central pontine myelinolysis: two cases with associated electrolyte disturbance.  Q J Med. 1976;  45 373-386
• 156 Newell K L, Kleinschmidt-Demasters B K. Central pontine myelinolysis at autopsy: a twelve-year retrospective analysis.  J Neurol Sci. 1996;  142 134-139
• 157 Uchino A, Yuzuriha T, Murakami M et al.. Magnetic resonance imaging of sequelae of central pontine myelinolysis in chronic alcohol abusers.  Neuroradiology. 2003;  45 877-880
• 158 Cramer S C, Stegbauer K C, Schneider A, Mukai J, Maravilla K R. Decreased diffusion in central pontine myelinolysis.  AJNR Am J Neuroradiol. 2001;  22 1476-1479
• 159 Ruzek K A, Campeau N G, Miller G M. Early diagnosis of central pontine myelinolysis with diffusion-weighted imaging.  AJNR Am J Neuroradiol. 2004;  25 210-213
• 160 Sinha S, Taly A B, Ravishankar S et al.. Wilson's disease: cranial MRI observations and clinical correlation.  Neuroradiology. 2006;  48 613-621
• 161 Sener R N. Wilson's disease: MRI demonstration of cavitations in basal ganglia and thalami.  Pediatr Radiol. 1993;  23 157
• 162 Singcharoen T, Chakkaphak K, Udompanich O. Unusual magnetic resonance findings in Wilson's disease.  Br J Radiol. 1991;  64 752-754
• 163 van Wassenaer-van Hall H N, van den Heuvel A G, Algra A, Hoogenraad T U, Mali W P. Wilson disease: findings at MR imaging and CT of the brain with clinical correlation.  Radiology. 1996;  198 531-536
• 164 Bakshi R, Ketonen L. MRI of the brain in clinical neurology. In: Joynt RJ, Griggs RC Baker and Joynt's Clinical Neurology [book on CD-ROM]. Philadelphia, PA; Lippincott Williams & Wilkins 2001
• 165 Guillerman R P. The eye-of-the-tiger sign.  Radiology. 2000;  217 895-896
• 166 Koyama M, Yagishita A. Pantothenate kinase-associated neurodegeneration with increased lentiform nuclei cerebral blood flow.  AJNR Am J Neuroradiol. 2006;  27 212-213
• 167 Hedera P, Brewer G J, Fink J K. White matter changes in Wilson disease.  Arch Neurol. 2002;  59 866-867