High-field magnetic resonance imaging of brain iron in Alzheimer disease

Topics in Magnetic Resonance Imaging

Volumn 17, Issue 1, 2006, Pages 41-50

  Schenck, John F ^a,b,c   Zimmerman, Earl A ^c   Li, Zhu ^a,b,d   Adak, Sudeshna ^a,b   Saha, Angshuman ^a,b   Tandon, Reeti ^a,b   Fish, Kenneth M ^a,b   Belden, Clifford ^c   Gillen, Robert W ^e   Barba, Anne ^c   Henderson, David L ^a,b   Neil, William ^c   O'Keefe, Timothy ^c  

^a GE GLOBAL RESEARCH   (United States)

^b GE GLOBAL RESEARCH   (India)

^c ALBANY MEDICAL COLLEGE   (United States)

^d GE HEALTHCARE   (United States)

^e Sunnyview Rehabilitation Hospital   (United States)

Author keywords

Alzheimer disease; Brain iron; High field MRI; Histograms; T2 relaxation

Indexed keywords

IRON; BIOLOGICAL MARKER;

AGED; ALZHEIMER DISEASE; ARTICLE; BRAIN CORTEX; BRAIN MAPPING; BRAIN REGION; CADAVER; CLINICAL ARTICLE; CONTRAST ENHANCEMENT; CONTROLLED STUDY; FEMALE; HIPPOCAMPUS; HISTOGRAM; HUMAN; HUMAN TISSUE; IMAGE ANALYSIS; IMAGE DISPLAY; IMAGE QUALITY; IRON BLOOD LEVEL; MALE; NEUROANATOMY; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; THREE DIMENSIONAL IMAGING; TISSUE WATER; WHITE MATTER; BRAIN; COMPUTER ASSISTED DIAGNOSIS; IRON METABOLISM DISORDER; METABOLISM; METHODOLOGY; PATHOLOGY;

AGED; ALZHEIMER DISEASE; BIOLOGICAL MARKERS; BRAIN; FEMALE; HUMANS; IMAGE INTERPRETATION, COMPUTER-ASSISTED; IRON; IRON METABOLISM DISORDERS; MAGNETIC RESONANCE IMAGING; MALE;

EID: 34247562371     PISSN: 08993459     EISSN: None     Source Type: Journal    
DOI: 10.1097/01.rmr.0000245455.59912.40     Document Type: Article

References (105)

1. Killiany RJ, Gomez-Isla T, Moss M, et al. Use of structural magnetic resonance imaging to predict who will get Alzheimer's disease. Ann Neurol. 2000;47:430-439.
2. Jack CR Jr, Shiung MM, Gunter JL, et al. Comparison of different MRI brain atrophy rate measures with clinical disease progression in AD. Neurology. 2004;62:591-600.
3. Jack CR Jr, Petersen RC, Xu YC, et al. Medial temporal atrophy on MRI in normal aging and very mild Alzheimer's disease. Neurology. 1997;49:786-794.
4. Fox NC, Schott JM. Imaging cerebral atrophy: normal ageing to Alzheimer's disease. Lancet. 2004;363:392-394.
5. Hancu I, Zimmerman EA, Sailasuta N, et al. 1H MR spectroscopy using TE averaged PRESS: a more sensitive technique to detect neurodegeneration associated with Alzheimer's disease. Magn Reson Med. 2005;53:777-782.
6. Klunk WE, Engler H, Nordberg A, et al. Imaging brain amyloid in Alzheimer's disease with Pittsburgh Compound-B. Ann Neurol. 2004;55:306-319.
7. Schenck JF, Zimmerman EA. High-field magnetic resonance imaging of brain iron: birth of a biomarker? NMR Biomed. 2004;17:433-445.
8. Haacke EM, Cheng NY, House MJ, et al. Imaging iron stores in the brain using magnetic resonance imaging. Magn Reson Imaging. 2005;23:1-25.
9. Jensen JH, Chandra R. Strong field behavior of the NMR signal from magnetically heterogeneous tissues. Magn Reson Med. 2000;43:226-236.
10. Schenck JF. Imaging of brain iron by magnetic resonance: T2 relaxation at different field strengths. J Neurol Sci. 1995;134(suppl):10-18.
11. McKhann G, Drachman D, Folstein M, et al. Clinical diagnosis of Alzheimer's disease: report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer's Disease. Neurology. 1984;34:939-944.
12. Morris CM, Candy JM, Oakley AE, et al. Histochemical distribution of non-haem iron in the human brain. Acta Anat (Basel). 1992;144:235-257.
13. Mesulam M, Shaw P, Mash D, et al. Cholinergic nucleus basalis tauopathy emerges early in the aging-MCI-AD continuum. Ann Neurol. 2004;55:815-828.
14. Gilissen EP, Ghosh P, Jacobs RE, et al. Topographical localization of iron in brains of the aged fat-tailed dwarf lemur (Cheirogaleus medius) and gray lesser mouse lemur (Microcebus murinus). Am J Primatol. 1998;45:291-299.
15. Sasaki M, Ehara S, Tamakawa Y, et al. MR anatomy of the substantia innominata and findings in Alzheimer disease: a preliminary report. AJNR Am J Neuroradiol. 1995;16:2001-2007.
16. Huckman MS. Where's the chicken? AJNR Am J Neuroradiol. 1995;16:2008-2009.
17. Alheid GF, Heimer L, Switzer RC III. Basal ganglia. In: Paxinos G, ed. The Human Nervous System. San Diego, CA: Academic Press; 1990:483-582.
18. Sakamoto M, Pearson J, Shinoda K, et al. The human basal forebrain. Part I. An overview. In: Bloom FE, Björkland A, Hökfelt T, eds. The Primate Nervous System. Part III. Handbook of Chemical Neuroanatomy, Vol. 15. Amsterdam: Elsevier; 1999:1-55.
19. Heimer L, DeOlmos JS, Alheid GF, et al. The human basal forebrain. Part II. In: Bloom FE, Björkland A, Hökfelt T, eds. The Primate Nervous System. Part III. Handbook of Chemical Neuroanatomy, Vol 15. Amsterdam: Elsevier; 1999:57-226.
20. Watson C, Andermann F, Gloor P, et al. Anatomic basis of amygdaloid and hippocampal volume measurement by magnetic resonance imaging. Neurology. 1992;42:1743-1750.
21. Pruessner JC, Li LM, Serles W, et al. Volumetry of hippocampus and amygdala with high-resolution MRI and three-dimensional analysis software: minimizing the discrepancies between laboratories. Cereb Cortex. 2000;10:433-442.
22. Westmoreland P, Cretsinger K. Caudate Tracing Guidelines. Iowa City, IA: University of Iowa Mental Health Clinical Research Center. Available at: http://www.psychiatry.uiowa.edu/mhcrc/IPLpages/manual_tracing.htm. Accessed October 3, 2006.
23. Westmoreland P, Cretsinger K. Putamen Tracing Guidelines. Iowa City, IA: University of Iowa Mental Health Clinical Research Center. Available at: http://www.psychiatry.uiowa.edu/mhcrc/IPLpages/manual_tracing.htm. Accessed October 3, 2006.
24. Cox RW. AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput Biomed Res. 1996;29:162-173.
25. Freedman D, Pisani R, Purves R. Statistics. 3rd ed. New York: WW Norton; 1998.
26. Cornell RM, Schwertmann U. The Iron Oxides: Structure, Properties, Reactions, Occurrences, and Uses. 2nd ed. Weinheim: Wiley-VCH; 2003.
27. D'Agostino RB, Stephens MA. Goodness-of-Fit Techniques. New York: Marcel Dekker; 1986.
28. Eisen MB, Spellman PT, Brown PO, et al. Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad USA Sci. 1998;95:14863-14868.
29. Chiang DY, Brown PO, Eisen MB. Visualizing associations between genome sequences and gene expression data using genome-mean expression profiles. Bioinformatics. 2001;17(suppl 1):S49-S55.
30. LeVine SM, Macklin WB. Iron-enriched oligodendrocytes: a reexamination of their spatial distribution. J Neurosci Res. 1990;26:508-512.
31. Morris CM, Kerwin JM, Edwardson JA. Non-haem iron histochemistry of the normal and Alzheimer's disease hippocampus. Neurodegeneration. 1994;3:267-275.
32. Morris CM, Candy JM, Kerwin JM, et al. Transferrin receptors in the normal human hippocampus and in Alzheimer's disease. Neuropathol Appl Neurobiol. 1994;20:473-477.
33. Koeppen AH. The history of iron in the brain. J Neurol Sci. 1995;134(suppl):1-9.
34. Gelman BB. Iron in CNS disease. J Neuropathol Exp Neurol. 1995;54:477-486.
35. Connor JR. Metals and Oxidative Damage in Neurological Disorders. New York: Plenum Press; 1997.
36. Qian ZM, Shen X. Brain iron transport and neurodegeneration. Trends Mol Med. 2001;7:103-108.
37. Rouault TA. Iron on the brain. Nat Genet. 2001;28:299-300.
38. Zatta P. Metal Ions and Neurodegenerative Disorders. London: World Scientific; 2003.
39. LeVine SM, Connor JR, Schipper HM. Redox-active Metals in Neurological Disorders. New York: New York Academy of Sciences; 2004.
40. Crichton RR, Ward RJ. Metal-based Neurodegeneration: From Molecular Mechanisms to Therapeutic Strategies. Chichester: Wiley; 2006.
41. Goodman L. Alzheimer's disease; a clinico-pathologic analysis of twenty-three cases with a theory on pathogenesis. J Nerv Ment Dis. 1953;118:97-130.
42. Bishop GM, Robinson SR, Liu Q, et al. Iron: a pathological mediator of Alzheimer disease? Dev Neurosci. 2002;24:184-187.
43. Collingwood JF, Mikhaylova A, Davidson M, et al. In situ characterization and mapping of iron compounds in Alzheimer's disease tissue. J Alzheimers Dis. 2005;7:267-272.
44. Jellinger K, Paulus W, Grundke-Iqbal I, et al. Brain iron and ferritin in Parkinson's and Alzheimer's diseases. J Neural Transm Park Dis Dement Sect. 1990;2:327-340.
45. Zecca L, Youdim MB, Riederer P, et al. Iron, brain ageing and neurodegenerative disorders. Nat Rev Neurosci. 2004;5:863-873.
46. Bermel RA, Puli SR, Rudick RA, et al. Prediction of longitudinal brain atrophy in multiple sclerosis by gray matter magnetic resonance imaging T2 hypointensity. Arch Neurol. 2005;62:1371-1376.
47. Grabill C, Silva AC, Smith SS, et al. MRI detection of ferritin iron overload and associated neuronal pathology in iron regulatory protein-2 knockout mice. Brain Res. 2003;971:95-106.
48. Smith SR, Cooperman S, Lavaute T, et al. Severity of neurodegeneration correlates with compromise of iron metabolism in mice with iron regulatory protein deficiencies. Ann N Y Acad Sci. 2004;1012:65-83.
49. Su JH, Kesslak JP, Head E, et al. Caspase-cleaved amyloid precursor protein and activated caspase-3 are co-localized in the granules of granulovacuolar degeneration in Alzheimer's disease and Down's syndrome brain. Acta Neuropathol (Berl). 2002;104:1-6.
50. Smith MA, Wehr K, Harris PL, et al. Abnormal localization of iron regulatory protein in Alzheimer's disease. Brain Res. 1998;788:232-236.
51. Grundke-Iqbal I, Fleming J, Tung YC, et al. Ferritin is a component of the neuritic (senile) plaque in Alzheimer dementia. Acta Neuropathol (Berl). 1990;81:105-110.
52. Schubert D, Chevion M. The role of iron in beta amyloid toxicity. Biochem Biophys Res Commun. 1995;216:702-707.
53. Robinson S, Noone D, Kril J, et al. Most amyloid plaques contain ferritin-rich cells. Alzheimer's Res. 1995;1:191-196.
54. Lovell MA, Robertson JD, Teesdale WJ, et al. Copper, iron and zinc in Alzheimer's disease senile plaques. J Neurol Sci. 1998;158 47-52.
55. Bishop GM, Robinson SR. Human Abeta1-42 reduces iron-induced toxicity in rat cerebral cortex. J Neurosci Res. 2003;73:316-323.
56. Dobson J, Batich C. A potential iron-based mechanism for enhanced deposition of amyloid plaques due to cognitive stimulation in Alzheimer disease. J Neuropathol Exp Neurol. 2004;63:674-675.
57. Good PF, Perl DP, Bierer LM, et al. Selective accumulation of aluminum and iron in the neurofibrillary tangles of Alzheimer's disease: a laser microprobe (LAMMA) study. Ann Neurol. 1992;31:286-292.
58. Bouras C, Giannakopoulos P, Good PF, et al. A laser microprobe mass analysis of brain aluminum and iron in dementia pugilistica: comparison with Alzheimer's disease. Eur Neurol. 1997;38:53-58.
59. Bush AI. The metallobiology of Alzheimer's disease. Trends Neurosci. 2003;26:207-214.
60. Rogers JT, Randall JD, Cahill CM, et al. An iron-responsive element type II in the 5-untranslated region of the Alzheimer's amyloid precursor protein transcript. J Biol Chem. 2002;277:45518-45528.
61. Benveniste H, Einstein G, Kim KR, et al. Detection of neuritic plaques in Alzheimer's disease by magnetic resonance microscopy. Proc Natl Acad Sci U S A. 1999;96:14079-14084.
62. Helpern JA, Lee SP, Falangola MF, et al. MRI assessment of neuropathology in a transgenic mouse model of Alzheimer's disease. Magn Reson Med. 2004;51:794-798.
63. Lee SP, Falangola MF, Nixon RA, et al. Visualization of β-amyloid plaques in a transgenic mouse model of Alzheimer's disease using MR microscopy without contrast reagents. Magn Reson Med. 2004;52:538-544.
64. Zhang J, Yarowsky P, Gordon MN, et al. Detection of amyloid plaques in mouse models of Alzheimer's disease by magnetic resonance imaging. Magn Reson Med. 2004;51:452-457.
65. Jack CR Jr, Garwood M, Wengenack TM, et al. In vivo visualization of Alzheimer's amyloid plaques by magnetic resonance imaging in transgenic mice without a contrast agent. Magn Reson Med. 2004;52:1263-1271.
66. Vanhoutte G, Dewachter I, Borghgraef P, et al. Noninvasive in vivo MRI detection of neuritic plaques associated with iron in APP[V717I] transgenic mice, a model for Alzheimer's disease. Magn Reson Med. 2005;53:607-613.
67. Zimmerman EA, Li Z, Keefe O'T, et al. High field strength (3T) magnetic resonance imaging in Alzheimer's disease. Ann Neurol. 2003;54(suppl 7):S68.
68. Adak S, Saha A, Paul S, et al. Classification of Alzheimer's disease using T2 distribution parameters from 3T MRI International Society for Magnetic Resonance in Medicine (ISMRM) 12th Annual Meeting; May 15-21, 2004; Kyoto, Japan.
69. Press DZ, Casement MD, Schenck JF, et al. High field MRI demonstrates brain iron in Alzheimer's disease. Neurobiol Aging. 2004;25:378.
70. Braak H, Del Tredici K, Schultz C, et al. Vulnerability of select neuronal types to Alzheimer's disease. Ann N Y Acad Sci. 2000;924:53-61.
71. Deibel MA, Ehmann WD, Markesbery WR. Copper, iron, and zinc imbalances in severely degenerated brain regions in Alzheimer's disease: possible relation to oxidative stress. J Neurol Sci. 1996;143:137-142.
72. Smith MA, Harris PL, Sayre LM, et al. Iron accumulation in Alzheimer disease is a source of redox-generated free radicals. Proc Natl Acad Sci U S A. 1997;94:9866-9868.
73. Markesbery WR, Carney JM. Oxidative alterations in Alzheimer's disease. Brain Pathol. 1999;9:133-146.
74. Rottkamp CA, Raina AK, Zhu X, et al. Redox-active iron mediates amyloid-beta toxicity. Free Radic Biol Med. 2001;30:447-450.
75. Halliwell B. Role of free radicals in the neurodegenerative diseases: therapeutic implications for antioxidant treatment. Drugs Aging. 2001;18:685-716.
76. Perry G, Cash AD, Smith MA. Alzheimer disease and oxidative stress. J Biomed Biotechnol. 2002;2:120-123.
77. Egana JT, Zambrano C, Nunez MT, et al. Iron-induced oxidative stress modify tau phosphorylation patterns in hippocampal cell cultures. Biometals. 2003;16:215-223.
78. Honda K, Casadesus G, Petersen RB, et al. Oxidative stress and redox-active iron in Alzheimer's disease. Ann N Y Acad Sci. 2004;1012:179-182.
79. Huang X, Moir RD, Tanzi RE, et al. Redox-active metals, oxidative stress, and Alzheimer's disease pathology. Ann N Y Acad Sci. 2004;1012:153-163.
80. Berg D, Youdim MB, Riederer P. Redox imbalance. Cell Tissue Res. 2004;318:201-213.
81. Levenson CW, Tassabehji NM. Iron and ageing: an introduction to iron regulatory mechanisms. Ageing Res Rev. 2004;3:251-263.
82. Schipper HM. Brain iron deposition and the free radical-mitochondrial theory of ageing. Ageing Res Rev. 2004;3:265-301.
83. Atamna H. Heme, iron, and the mitochondrial decay of ageing. Ageing Res Rev. 2004;3:303-318.
84. Allkemper T, Schwindt W, Maintz D, et al. Sensitivity of T2-weighted FSE sequences towards physiological iron depositions in normal brains at 1.5 and 3.0 T. Eur Radiol. 2004;14:1000-1004.
85. Ye FQ, Martin W, Allen PS. Estimation of the iron concentration in excised gray matter by means of proton relaxation measurements. Magn Reson Med. 1996;35:285-289.
86. Bartzokis G, Sultzer D, Cummings J, et al. In vivo evaluation of brain iron in Alzheimer disease using magnetic resonance imaging. Arch Gen Psychiatry. 2000;57:47-53.
87. Bartzokis G, Tishler TA, Lu PH, et al. Brain ferritin iron may influence age- and gender-related risks of neurodegeneration. Neurobiol Aging. March 22, 2006. [Epub ahead of print].
88. Haacke EM, Xu Y, Cheng YC, et al. Susceptibility weighted imaging (SWI). Magn Reson Med. 2004;52:612-618.
89. Jensen JH, Chandra R, Ramani A, et al. Magnetic field correlation imaging. Magn Reson Med. 2006;55(6):1350-1361.
90. Gaeta A, Hider RC. The crucial role of metal ions in neurodegeneration: the basis for a promising therapeutic strategy. Br J Pharmacol. 2005;146(8):1041-1059.
91. Ritchie CW, Bush AI, Mackinnon A, et al. Metal-protein attenuation with iodochlorhydroxyquin (clioquinol) targeting Abeta amyloid deposition and toxicity in Alzheimer disease: a pilot phase 2 clinical trial. Arch Neurol. 2003;60:1685-1691.
92. Raman B, Ban T, Yamaguchi KI, et al. Metal ion-dependent effects of clioquinol on the fibril growth of an amyloid beta peptide. J Biol Chem. 2005;280:16157-16162.
93. Richardson DR. Novel chelators for central nervous system disorders that involve alterations in the metabolism of iron and other metal ions. Ann N Y Acad Sci. 2004;1012:326-341.
94. Shachar DB, Kahana N, Kampel V, et al. Neuroprotection by a novel brain permeable iron chelator, VK-28, against 6-hydroxydopamine lesion in rats. Neuropharmacology. 2004;46:254-263.
95. Hallgren B, Sourander P. The effect of age on the non-haemin iron in the human brain. J Neurochem. 1958;3:41-51.
96. Drayer B, Burger P, Darwin R, et al. Magnetic resonance imaging of brain iron. AJR Am J Roentgenol. 1986;147:103-110.
97. Gelman N, Gorell JM, Barker PB, et al. MR imaging of human brain at 3.0 T: preliminary report on transverse relaxation rates and relation to estimated iron content. Radiology. 1999;210:759-767.
98. Hardy PA, Gash D, Yokel R, et al. Correlation of R2 with total iron concentration in the brains of rhesus monkeys. J Magn Reson Imaging. 2005;21:118-127.
99. Grisoli M, Piperno A, Chiapparini L, et al. MR imaging of cerebral cortical involvement in aceruloplasminemia. AJNR Am J Neuroradiol. 2005;26:657-661.
100. Hayflick SJ, Westaway SK, Levinson B, et al. Genetic, clinical, and radiographic delineation of Hallervorden-Spatz syndrome. N Engl J Med. 2003;348:33-40.
101. Atlas SW, Thulborn KR. Intracranial hemorrhage. In: Atlas SW, ed. Magnetic Resonance Imaging of the Brain and Spine. 3rd ed. Philadelphia, PA: Lippincott Williams & Wilkins; 2002:773-832.
102. Small SA, Nava AS, Perera GM, et al. Evaluating the function of hippocampal subregions with high-resolution MRI in Alzheimer's disease and aging. Microsc Res Tech. 2000;51:101-108.
103. Yamada N, Imakita S, Sakuma T, et al. Intracranial calcification on gradient-echo phase image: depiction of diamagnetic susceptibility. Radiology. 1996;198:171-178.
104. Curnes JT, Burger PC, Djang WT, et al. MR imaging of compact white matter pathways. AJNR Am J Neuroradiol. 1988;9:1061-1068.
105. Zhou J, Golay X, van Zijl PC, et al. Inverse T(2) contrast at 1.5 Tesla between gray matter and white matter in the occipital lobe of normal adult human brain. Magn Reson Med. 2001;46:401-406.