Diabetic Encephalopathy Studied by Magnetic Resonance Imaging and Spectroscopy

Abstract

Abstract:

Diabetes mellitus (DM) is a chronic metabolic disease characterized by either insulin deficiency or insulin resistance. It is known that longstanding DM causes damages to the central nervous system. The manifestations include brain atrophy and white matter lesions. Magnetic resonance imaging (MRI) and spectroscopy (MRS) are noninvasive and can provide information on the anatomical, functional and metabolic aspects of the brain. MRI and MRS have been used as diagnostic tools for many brain diseases, including diabetic encephalopathy. In this review, clinical manifestations of diabetic encephalopathy were reviewed, with emphasis on the findings detected by MRI/MRS techniques.

Key words: MRI, MRS, diabetic encephalopathy, diabetic striatopathy

CLC Number:

O482.53

HUANG Ming-Ming, LIN Fu-Chun, GAO Li-Feng, LEI Hao. Diabetic Encephalopathy Studied by Magnetic Resonance Imaging and Spectroscopy[J]. Chinese Journal of Magnetic Resonance, 2012, 29(3): 446-456.

References

[1] Brownlee M. Biochemistry and molecular cell biology of diabetic complications[J]. Nature, 2001, 414(6 865): 813-820.

[2] Reske-Nielsen E, Lundbaek K. Pathological changes in the central and peripheral nervous system of young long-term diabetics. II. The spinal cord and peripheral nerves[J]. Diabetologia, 1968, 4(1): 34-43.

[3] Wessels a M, Simsek S, Remijnse P L, et al. Voxel-based morphometry demonstrates reduced grey matter density on brain MRI in patients with diabetic retinopathy[J]. Diabetologia, 2006, 49(10): 2 474-2 480.

[4] Wong T Y, Mosley T H, Jr., Klein R, et al. Retinal microvascular changes and MRI signs of cerebral atrophy in healthy, middle-aged people
[J]. Neurology, 2003, 61(6): 806-811.

[5] Patton N, Aslam T, Macgillivray T, et al. Retinal vascular image analysis as a potential screening tool for cerebrovascular disease: a rationale based on homology between cerebral and retinal microvasculatures[J]. J Anat, 2005, 206(4): 319-348.

[6] Ferguson S C, Blane A, Perros P, et al. Cognitive ability and brain structure in type 1 diabetes: relation to microangiopathy and preceding severe hypoglycemia[J]. Diabetes, 2003, 52(1): 149-156.

[7] Gaudieri P A, Chen R, Greer T F, et al. Cognitive function in children with type 1 diabetes: a meta-analysis[J]. Diabetes Care, 2008, 31(9): 1 892-1 897.

[8] Shan D E, Ho D M, Chang C, et al. Hemichorea-hemiballism: an explanation for MR signal changes[J]. Am J Neuroradiol, 1998, 19(5): 863-870.

[9] Van Elderen S G C, Brandts A, Westenberg J J M, et al. Aortic stiffness is associated with cardiac function and cerebral small vessel disease in patients with type 1 diabetes mellitus: assessment by magnetic resonance imaging[J]. Eur Radiol, 2010, 20(5): 1 132-1 138.

[10] Van Elderen S G, De Roos A, De Craen a J, et al. Progression of brain atrophy and cognitive decline in diabetes mellitus: a 3-year follow-up[J]. Neurology, 2010, 75(11): 997-1 002.

[11] Van Harten B, De Leeuw F E, Weinstein H C, et al. Brain imaging in patients with diabetes: a systematic review[J]. Diabetes Care, 2006, 29(11): 2 539-2 548.

[12] Ryan C M, Geckle M O, Orchard T J. Cognitive efficiency declines over time in adults with Type 1 diabetes: effects of micro- and macrovascular complications[J]. Diabetologia, 2003, 46(7): 940-948.

[13] Wessels A M, Rombouts S A, Remijnse P L, et al. Cognitive performance in type 1 diabetes patients is associated with cerebral white matter volume[J]. Diabetologia, 2007, 50(8): 1 763-1 769.

[14] Brands A M, Kessels R P, Hoogma R P, et al. Cognitive performance, psychological well-being, and brain magnetic resonance imaging in older patients with type 1 diabetes[J]. Diabetes, 2006, 55(6): 1 800-1 806.

[15] Beaulieu C. The basis of anisotropic water diffusion in the nervous system——a technical review[J]. NMR Biomed, 2002, 15(7-8): 435-455.

[16] Pierpaoli C, Jezzard P, Basser P J, et al. Diffusion tensor MR imaging of the human brain[J]. Radiology, 1996, 201(3): 637-648.

[17] Alexander a L, Lee J E, Lazar M, et al. Diffusion tensor imaging of the brain[J]. Neurotherapeutics, 2007, 4(3): 316-329.

[18] Ramin S L, Tognola W A, Spotti A R. Proton magnetic resonance spectroscopy: clinical applications in patients with brain lesions[J]. Sao Paulo Med J, 2003, 121(6): 254-259.

[19] Bjartmar C, Battistuta J, Terada N, et al. N-acetylaspartate is an axon-specific marker of mature white matter in vivo: a biochemical and immunohistochemical study on the rat optic nerve[J]. Ann Neurol, 2002, 51(1): 51-58.

[20] De Stefano N, Filippi M. MR spectroscopy in multiple sclerosis[J]. J Neuroimaging, 2007, 17(Suppl 1): 31S-35S.

[21] Birken D L, Oldendorf W H. N-acetyl-L-aspartic acid——a literaturereview of a compound prominent in H-1-nmr spectroscopic studies of brain[J]. Neurosci Biobehav Rev, 1989, 13(1): 23-31.

[22] Musen G, Lyoo I K, Sparks C R, et al. Effects of type 1 diabetes on gray matter density as measured by voxel-based morphometry[J]. Diabetes, 2006, 55(2): 326-333.

[23] Weinger K, Jacobson A M, Musen G, et al. The effects of type 1 diabetes on cerebral white matter[J]. Diabetologia, 2008, 51(3): 417-425.
[24] Duker A P, Espay A J. Images in clinical medicine. Hemichorea-hemiballism after diabetic ketoacidosis[J]. N Engl J Med, 2010, 363(17): e27.

[25] Schmidt R, Fazekas F, Kleinert G, et al. Magnetic-resonance-imaging signal hyperintensities in the deep and subcortical white matter-a -comparative-study between stroke patients and normal volunteers[J]. Arch Neurol, 1992, 49(8): 825-827.

[26] Kario K, Ishikawa J, Hoshide S, et al. Diabetic brain damage in hypertension: role of renin-angiotensin system[J]. Hypertension, 2005, 45(5): 887-893.

[27] Launer L J, Korf E S C, White L R, et al. Brain aging in very old men with type 2 diabetes - the honolulu-asia aging study[J]. Diabetes Care, 2006, 29(10): 2 268-2 274.

[28] Lazarus R, Prettyman R, Cherryman G. White matter lesions on magnetic resonance imaging and their relationship with vascular risk factors in memory clinic attenders[J]. Int J Geriatr Psych, 2005, 20(3): 274-279.

[29] Northam E A, Rankins D, Lin A, et al. Central nervous system function in youth with type 1 diabetes 12 years after disease onset[J]. Diabetes Care, 2009, 32(3): 445-450.

[30] Kodl C T, Franc D T, Rao J P, et al. Diffusion tensor imaging identifies deficits in white matter microstructure in subjects with type 1 diabetes that correlate with reduced neurocognitive function[J]. Diabetes, 2008, 57(11): 3 083-3 089.

[31] Franc D T, Kodl C T, Mueller B A, et al. High connectivity between reduced cortical thickness and disrupted white matter tracts in longstanding type 1 diabetes[J]. Diabetes, 2011, 60(1): 315-319.

[32] Yau P L, Javier D, Tsui W, et al. Emotional and neutral declarative memory impairments and associated white matter microstructural abnormalities in adults with type 2 diabetes[J]. Psychiat Res, 2009, 174(3): 223-230.

[33] Francis G J, Martinez J A, Liu W Q, et al. Intranasal insulin prevents cognitive decline, cerebral atrophy and white matter changes in murine type I diabetic encephalopathy[J]. Brain, 2008, 131(Pt 12): 3 311-3 334.

[34] Mooradian A D. Central nervous system complications of diabetes mellitus——a perspective from the blood-brain barrier[J]. Brain Res Brain Res Rev, 1997, 23(3): 210-218.

[35] Ho M S, Weller N J, Ives F J, et al. Prevalence of structural central nervous system abnormalities in early-onset type 1 diabetes mellitus[J]. J Pediatr, 2008, 153(3): 385-390.

[36] Ferguson S C, Blane A, Wardlaw J, et al. Influence of an early-onset age of type 1 diabetes on cerebral structure and cognitive function[J]. Diabetes Care, 2005, 28(6): 1 431-1 437.

[37] Lobnig B M, Kromeke O, Optenhostert-Porst C, et al. Hippocampal volume and cognitive performance in long-standing Type 1 diabetic patients without macrovascular complications[J]. Diabet Med, 2006, 23(1): 32-39.

[38] Wrighten S A, Piroli G G, Grillo C A, et al. A look inside the diabetic brain: Contributors to diabetes-induced brain aging[J]. Biochim Biophys Acta, 2009, 1792(5): 444-453.

[39] Sabri O, Hellwig D, Schreckenberger M, et al. Influence of diabetes mellitus on regional cerebral glucose metabolism and regional cerebral blood flow[J]. Nucl Med Commun, 2000, 21(1): 19-29.

[40] Yuen N, Anderson S E, Glaser N, et al. Cerebral blood flow and cerebral edema in rats with diabetic ketoacidosis[J]. Diabetes, 2008, 57(10): 2 588-2 594.

[41] Sarac K, Akinci A, Alkan A, et al. Brain metabolite changes on proton magnetic resonance spectroscopy in children with poorly controlled type 1 diabetes mellitus[J]. Neuroradiology, 2005, 47(7): 562-565.

[42] Heikkila O, Lundbom N, Timonen M, et al. Hyperglycaemia is associated with changes in the regional concentrations of glucose and myo-inositol within the brain[J]. Diabetologia, 2009, 52(3): 534-540.

[43] Makimattila S, Malmberg-Ceder K, Hakkinen A M, et al. Brain metabolic alterations in patients with type 1 diabetes-hyperglycemiainduced injury[J]. J Cereb Blood Flow Metab, 2004, 24(12): 1 393-1 399.

[44] Lyoo I K, Yoon S J, Musen G, et al. Altered prefrontal glutamate-glutamine-gamma-aminobutyric acid levels and relation to low cognitive performance and depressive symptoms in type 1 diabetes mellitus[J]. Arch Gen Psychiatry, 2009, 66(8): 878-887.

[45] Biessels G J, Braun K P, De Graaf R A, et al. Cerebral metabolism in streptozotocin-diabetic rats: an in vivo magnetic resonance spectroscopy study[J]. Diabetologia, 2001, 44(3): 346-353.

[46] Duarte J M, Carvalho R A, Cunha R A, et al. Caffeine consumption attenuates neurochemical modifications in the hippocampus of streptozotocin-induced diabetic rats[J]. J Neurochem, 2009, 111(2): 368-379.

[47] Pasquier F, Boulogne A, Leys D, et al. Diabetes mellitus and dementia[J]. Diabetes Metab, 2006, 32(5 Pt 1): 403-414.

[48] Van Der Flier W M, Van Straaten E C, Barkhof F, et al. Medial temporal lobe atrophy and white matter hyperintensities are associated with mild cognitive deficits in nondisabled elderly people: the LADIS study[J]. J Neurol Neurosurg Psychiatry, 2005, 76(11): 1 497-1 500.

[49] Verdelho A, Madureira S, Ferro J M, et al. Differential impact of cerebral white matter changes, diabetes, hypertension and stroke on cognitive performance among non-disabled elderly. The LADIS study[J]. J Neurol Neurosurg Psychiatry, 2007, 78(12): 1 325-1 330.

[50] Verdelho A, Madureira S, Moleiro C, et al. White matter changes and diabetes predict cognitive decline in the elderly: the LADIS study[J]. Neurology, 2010, 75(2): 160-167.

[51] Li Z G, Mang W, Sima a A. Alzheimer-like changes in rat models of spontaneous diabetes[J]. Diabetes, 2007, 56(10): 2 650-2 650.

[52] John I M, Suzan H, Samuel S, et al. Hyperglycemia not hypoglycemia alters neuronal dendrites and impairs spatial memory[J]. Pediatric Diabetes, 2008, 9(6): 531-539.

[53] Martinez-Tellez R, Gomez-Villalobos Mde J, Flores G. Alteration in dendritic morphology of cortical neurons in rats with diabetes mellitus induced by streptozotocin[J]. Brain Res, 2005, 1 048(1-2): 108-115.

[54] Ohi T, Saita K, Furukawa S, et al.Therapeutic effects of aldose reductase inhibitor on experimental diabetic neuropathy through synthesis/secretion of nerve growth factor[J]. Exp Neurol, 1998, 151(2): 215-220.

[55] Lai P H, Tien R D, Chang M H, et al. Chorea-ballismus with nonketotic hyperglycemia in primary diabetes mellitus[J]. Am J Neuroradiol, 1996, 17(6): 1 057-1 064.

[56] Tung C S, Guo Y C, Lai C L, et al. Irreversible striatal neuroimaging abnormalities secondary to prolonged, uncontrolled diabetes mellitus in the setting of progressive focal neurological symptoms[J]. Neurol Sci, 2010, 31(1): 57-60.

[57] Lin J J, Lin G Y, Shih C, et al. Presentation of striatal hyperintensity on T_1-weighted MRI in patients with hemiballism-hemichorea caused by non-ketotic hyperglycemia: report of seven new cases and a review of literature[J]. J Neurol, 2001, 248(9): 750-755.

[58] Lai P H, Chen P C, Chang M H, et al. In vivo proton MR spectroscopy of chorea-ballismus in diabetes mellitus[J]. Neuroradiology, 2001, 43(7): 525-531.

[59] Altafullah I, Pascual-Leone A, Duvall K, et al. Putaminal hemorrhage accompanied by hemichorea-hemiballism[J]. Stroke, 1990, 21(7): 1 093-1 094.

[60] Abe Y, Yamamoto T, Soeda T, et al. Diabetic striatal disease: clinical presentation, neuroimaging, and pathology[J]. Intern Med, 2009, 48(13): 1 135-1 141.

[61] Dong Ji-yang(董继扬), Xu Le(徐乐), Cao Hong-ting(曹红婷), et al.A new data processing method for metabonomic and its application in a study of diabetes(代谢组学数据分析方法及在糖尿病研究中的应用)[J]. Chinese J Magn Reson(波谱学杂志), 2007, 24(4): 381-393.

[62] Mao Xuan(毛璇), Zhang Dong-juan(张冬娟), Guan You-fei(管又飞), et al. A metabonomic study of aqueous kidney extract in the mouse model of type Ⅱ diabetic nephropathy(Ⅱ型糖尿病肾病小鼠肾水提物代谢组学研究)[J]. Chinese J Magn Reson(波谱学杂志), 2010, 27(4): 532-539.