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Erschienen in: Diabetologia 10/2006

01.10.2006 | Article

Voxel-based morphometry demonstrates reduced grey matter density on brain MRI in patients with diabetic retinopathy

verfasst von: A. M. Wessels, S. Simsek, P. L. Remijnse, D. J. Veltman, G. J. Biessels, F. Barkhof, P. Scheltens, F. J. Snoek, R. J. Heine, S. A. R. B. Rombouts

Erschienen in: Diabetologia | Ausgabe 10/2006

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Abstract

Aims/hypothesis

In addition to nephropathy, retinopathy and peripheral neuropathy, a microvascular complication of type 1 diabetes that may be tentatively referred to as ‘diabetic encephalopathy’ has gained increasing attention. There is growing evidence that lowered cognitive performance in patients with type 1 diabetes is related to chronic hyperglycaemia rather than recurrent episodes of severe hypoglycaemia, as previously speculated. The aim of our study was to use magnetic resonance imaging (MRI) to establish whether long-term hyperglycaemia, resulting in advanced retinopathy, contributes to structural changes in the brain (reduced grey matter).

Subjects, materials and methods

We applied voxel-based morphometry on magnetic resonance images to compare grey matter density (GMD) between three groups of participants. GMD is used as a marker of cortical atrophy. We compared 13 type 1 diabetic patients with a microvascular complication (i.e. proliferative retinopathy) with 18 type 1 diabetic patients who did not have retinopathy in order to assess the effects of microvascular changes on GMD. Both patient groups were compared with 21 healthy control subjects to assess the effect of diabetes in itself.

Results

Patients with diabetic retinopathy showed reduced GMD in the right inferior frontal gyrus and right occipital lobe compared both with patients without retinopathy and with healthy controls (p<0.05).

Conclusions/interpretation

Our data show that patients with type 1 diabetes, who, as a consequence of chronic hyperglycaemia, had developed advanced retinopathy, also showed increased focal cortical atrophy on brain MRI.
Literatur
1.
Zurück zum Zitat Reske-Nielsen E, Lundbaek K, Rafaelsen OJ (1965) Pathological changes in the central and peripheral nervous system of young longterm diabetics. Diabetologia 1:233–241CrossRef Reske-Nielsen E, Lundbaek K, Rafaelsen OJ (1965) Pathological changes in the central and peripheral nervous system of young longterm diabetics. Diabetologia 1:233–241CrossRef
2.
Zurück zum Zitat Brands AM, Biessels GJ, de Haan EH, Kappelle LJ, Kessels RP (2005) The effects of type 1 diabetes on cognitive performance: a meta-analysis. Diabetes Care 28:726–735PubMedCrossRef Brands AM, Biessels GJ, de Haan EH, Kappelle LJ, Kessels RP (2005) The effects of type 1 diabetes on cognitive performance: a meta-analysis. Diabetes Care 28:726–735PubMedCrossRef
3.
Zurück zum Zitat Ryan CM, Geckle MO, Orchard TJ (2003) Cognitive efficiency declines over time in adults with Type 1 diabetes: effects of micro- and macrovascular complications. Diabetologia 46:940–948PubMedCrossRef Ryan CM, Geckle MO, Orchard TJ (2003) Cognitive efficiency declines over time in adults with Type 1 diabetes: effects of micro- and macrovascular complications. Diabetologia 46:940–948PubMedCrossRef
4.
Zurück zum Zitat Ferguson SC, Blane A, Perros P et al (2003) Cognitive ability and brain structure in type 1 diabetes: relation to microangiopathy and preceding severe hypoglycemia. Diabetes 52:149–156PubMedCrossRef Ferguson SC, Blane A, Perros P et al (2003) Cognitive ability and brain structure in type 1 diabetes: relation to microangiopathy and preceding severe hypoglycemia. Diabetes 52:149–156PubMedCrossRef
5.
Zurück zum Zitat Dejgaard A, Gade A, Larsson H, Balle V, Parving A, Parving HH (1991) Evidence for diabetic encephalopathy. Diabet Med 8:162–167PubMedCrossRef Dejgaard A, Gade A, Larsson H, Balle V, Parving A, Parving HH (1991) Evidence for diabetic encephalopathy. Diabet Med 8:162–167PubMedCrossRef
6.
Zurück zum Zitat Yousem DM, Tasman WS, Grossman RI (1991) Proliferative retinopathy: absence of white matter lesions at MR imaging. Radiology 179:229–230PubMed Yousem DM, Tasman WS, Grossman RI (1991) Proliferative retinopathy: absence of white matter lesions at MR imaging. Radiology 179:229–230PubMed
7.
Zurück zum Zitat Araki Y, Nomura M, Tanaka H et al (1994) MRI of the brain in diabetes mellitus. Neuroradiology 36:101–103PubMedCrossRef Araki Y, Nomura M, Tanaka H et al (1994) MRI of the brain in diabetes mellitus. Neuroradiology 36:101–103PubMedCrossRef
8.
Zurück zum Zitat Lunetta M, Damanti AR, Fabbri G, Lombardo M, Di Mauro M, Mughini L (1994) Evidence by magnetic resonance imaging of cerebral alterations of atrophy type in young insulin-dependent diabetic patients. J Endocrinol Invest 17:241–245PubMed Lunetta M, Damanti AR, Fabbri G, Lombardo M, Di Mauro M, Mughini L (1994) Evidence by magnetic resonance imaging of cerebral alterations of atrophy type in young insulin-dependent diabetic patients. J Endocrinol Invest 17:241–245PubMed
9.
Zurück zum Zitat Ashburner J, Friston KJ (2000) Voxel-based morphometry – the methods. Neuroimage 11:805–821PubMedCrossRef Ashburner J, Friston KJ (2000) Voxel-based morphometry – the methods. Neuroimage 11:805–821PubMedCrossRef
10.
Zurück zum Zitat Wong TY, Klein R, Klein BE, Tielsch JM, Hubbard L, Nieto FJ (2001) Retinal microvascular abnormalities and their relationship with hypertension, cardiovascular disease, and mortality. Surv Ophthalmol 46:59–80PubMedCrossRef Wong TY, Klein R, Klein BE, Tielsch JM, Hubbard L, Nieto FJ (2001) Retinal microvascular abnormalities and their relationship with hypertension, cardiovascular disease, and mortality. Surv Ophthalmol 46:59–80PubMedCrossRef
11.
Zurück zum Zitat Patton N, Aslam T, Macgillivray T, Pattie A, Deary IJ, Dhillon B (2005) Retinal vascular image analysis as a potential screening tool for cerebrovascular disease: a rationale based on homology between cerebral and retinal microvasculatures. J Anat 206:319–348PubMedCrossRef Patton N, Aslam T, Macgillivray T, Pattie A, Deary IJ, Dhillon B (2005) Retinal vascular image analysis as a potential screening tool for cerebrovascular disease: a rationale based on homology between cerebral and retinal microvasculatures. J Anat 206:319–348PubMedCrossRef
12.
Zurück zum Zitat Kwa VI, van der Sande JJ, Stam J, Tijmes N, Vrooland JL (2002) Retinal arterial changes correlate with cerebral small-vessel disease. Neurology 59:1536–1540PubMed Kwa VI, van der Sande JJ, Stam J, Tijmes N, Vrooland JL (2002) Retinal arterial changes correlate with cerebral small-vessel disease. Neurology 59:1536–1540PubMed
13.
Zurück zum Zitat Aldington SJ, Kohner EM, Meuer S, Klein R, Sjolie AK (1995) Methodology for retinal photography and assessment of diabetic retinopathy: the EURODIAB IDDM complications study. Diabetologia 38:437–444PubMed Aldington SJ, Kohner EM, Meuer S, Klein R, Sjolie AK (1995) Methodology for retinal photography and assessment of diabetic retinopathy: the EURODIAB IDDM complications study. Diabetologia 38:437–444PubMed
14.
Zurück zum Zitat No authors listed (1997) Hypoglycemia in the Diabetes Control and Complications Trial. The Diabetes Control and Complications Trial Research Group. Diabetes 46:271–286 No authors listed (1997) Hypoglycemia in the Diabetes Control and Complications Trial. The Diabetes Control and Complications Trial Research Group. Diabetes 46:271–286
15.
Zurück zum Zitat Good CD, Johnsrude IS, Ashburner J, Henson RN, Friston KJ, Frackowiak RS (2001) A voxel-based morphometric study of ageing in 465 normal adult human brains. Neuroimage 14:21–36PubMedCrossRef Good CD, Johnsrude IS, Ashburner J, Henson RN, Friston KJ, Frackowiak RS (2001) A voxel-based morphometric study of ageing in 465 normal adult human brains. Neuroimage 14:21–36PubMedCrossRef
16.
Zurück zum Zitat Senjem ML, Gunter JL, Shiung MM, Petersen RC, Jack CR Jr (2005) Comparison of different methodological implementations of voxel-based morphometry in neurodegenerative disease. Neuroimage 26:600–608PubMedCrossRef Senjem ML, Gunter JL, Shiung MM, Petersen RC, Jack CR Jr (2005) Comparison of different methodological implementations of voxel-based morphometry in neurodegenerative disease. Neuroimage 26:600–608PubMedCrossRef
17.
Zurück zum Zitat Friston K, Holmes AP, Worsley KJ, Poline JB (1995) Statistical parametric maps in functional imaging: a general linear approach. Hum Brain Mapp 2:189–210CrossRef Friston K, Holmes AP, Worsley KJ, Poline JB (1995) Statistical parametric maps in functional imaging: a general linear approach. Hum Brain Mapp 2:189–210CrossRef
18.
Zurück zum Zitat Perros P, Deary IJ, Sellar RJ, Best JJ, Frier BM (1997) Brain abnormalities demonstrated by magnetic resonance imaging in adult IDDM patients with and without a history of recurrent severe hypoglycemia. Diabetes Care 20:1013–1018PubMedCrossRef Perros P, Deary IJ, Sellar RJ, Best JJ, Frier BM (1997) Brain abnormalities demonstrated by magnetic resonance imaging in adult IDDM patients with and without a history of recurrent severe hypoglycemia. Diabetes Care 20:1013–1018PubMedCrossRef
19.
Zurück zum Zitat Musen G, Lyoo IK, Sparks CR et al (2006) Effects of type 1 diabetes on gray matter density as measured by voxel-based morphometry. Diabetes 55:326–333PubMedCrossRef Musen G, Lyoo IK, Sparks CR et al (2006) Effects of type 1 diabetes on gray matter density as measured by voxel-based morphometry. Diabetes 55:326–333PubMedCrossRef
20.
Zurück zum Zitat Brownlee M (2005) The pathobiology of diabetic complications: a unifying mechanism. Diabetes 54:1615–1625PubMedCrossRef Brownlee M (2005) The pathobiology of diabetic complications: a unifying mechanism. Diabetes 54:1615–1625PubMedCrossRef
21.
Zurück zum Zitat Johnson PC, Brendel K, Meezan E (1982) Thickened cerebral cortical capillary basement membranes in diabetics. Arch Pathol Lab Med 106:214–217PubMed Johnson PC, Brendel K, Meezan E (1982) Thickened cerebral cortical capillary basement membranes in diabetics. Arch Pathol Lab Med 106:214–217PubMed
22.
Zurück zum Zitat de la Torre JC, Mussivand T (1993) Can disturbed brain microcirculation cause Alzheimer’s disease? Neurol Res 15:146–153PubMed de la Torre JC, Mussivand T (1993) Can disturbed brain microcirculation cause Alzheimer’s disease? Neurol Res 15:146–153PubMed
23.
Zurück zum Zitat Kalaria RN, Hedera P (1995) Differential degeneration of the cerebral microvasculature in Alzheimer’s disease. Neuroreport 6:477–480PubMedCrossRef Kalaria RN, Hedera P (1995) Differential degeneration of the cerebral microvasculature in Alzheimer’s disease. Neuroreport 6:477–480PubMedCrossRef
24.
Zurück zum Zitat Pfefferbaum A, Mathalon DH, Sullivan EV, Rawles JM, Zipursky RB, Lim KO (1994) A quantitative magnetic resonance imaging study of changes in brain morphology from infancy to late adulthood. Arch Neurol 51:874–887PubMed Pfefferbaum A, Mathalon DH, Sullivan EV, Rawles JM, Zipursky RB, Lim KO (1994) A quantitative magnetic resonance imaging study of changes in brain morphology from infancy to late adulthood. Arch Neurol 51:874–887PubMed
25.
Zurück zum Zitat Tomlinson BE, Blessed G, Roth M (1970) Observations on the brains of demented old people. J Neurol Sci 11:205–242PubMedCrossRef Tomlinson BE, Blessed G, Roth M (1970) Observations on the brains of demented old people. J Neurol Sci 11:205–242PubMedCrossRef
26.
Zurück zum Zitat Kaplan JG, Katzman R, Horoupian DS, Fuld PA, Mayeux R, Hays AP (1985) Progressive dementia, visual deficits, amyotrophy, and microinfarcts. Neurology 35:789–796PubMed Kaplan JG, Katzman R, Horoupian DS, Fuld PA, Mayeux R, Hays AP (1985) Progressive dementia, visual deficits, amyotrophy, and microinfarcts. Neurology 35:789–796PubMed
27.
Zurück zum Zitat Munoz DG (1991) The pathological basis of multi-infarct dementia. Alzheimer Dis Assoc Disord 5:77–90PubMedCrossRef Munoz DG (1991) The pathological basis of multi-infarct dementia. Alzheimer Dis Assoc Disord 5:77–90PubMedCrossRef
28.
Zurück zum Zitat Kovari E, Gold G, Herrmann FR et al (2004) Cortical microinfarcts and demyelination significantly affect cognition in brain aging. Stroke 35:410–414PubMedCrossRef Kovari E, Gold G, Herrmann FR et al (2004) Cortical microinfarcts and demyelination significantly affect cognition in brain aging. Stroke 35:410–414PubMedCrossRef
29.
Zurück zum Zitat Snowdon DA, Greiner LH, Mortimer JA, Riley KP, Greiner PA, Markesbery WR (1997) Brain infarction and the clinical expression of Alzheimer disease. The Nun Study. JAMA 277:813–817PubMedCrossRef Snowdon DA, Greiner LH, Mortimer JA, Riley KP, Greiner PA, Markesbery WR (1997) Brain infarction and the clinical expression of Alzheimer disease. The Nun Study. JAMA 277:813–817PubMedCrossRef
30.
Zurück zum Zitat Esiri MM, Wilcock GK, Morris JH (1997) Neuropathological assessment of the lesions of significance in vascular dementia. J Neurol Neurosurg Psychiatry 63:749–753PubMedCrossRef Esiri MM, Wilcock GK, Morris JH (1997) Neuropathological assessment of the lesions of significance in vascular dementia. J Neurol Neurosurg Psychiatry 63:749–753PubMedCrossRef
31.
Zurück zum Zitat del Ser T, Bermejo F, Portera A, Arredondo JM, Bouras C, Constantinidis J (1990) Vascular dementia. A clinicopathological study. J Neurol Sci 96:1–17PubMedCrossRef del Ser T, Bermejo F, Portera A, Arredondo JM, Bouras C, Constantinidis J (1990) Vascular dementia. A clinicopathological study. J Neurol Sci 96:1–17PubMedCrossRef
32.
Zurück zum Zitat Vinters HV, Ellis WG, Zarow C et al (2000) Neuropathologic substrates of ischemic vascular dementia. J Neuropathol Exp Neurol 59:931–945PubMed Vinters HV, Ellis WG, Zarow C et al (2000) Neuropathologic substrates of ischemic vascular dementia. J Neuropathol Exp Neurol 59:931–945PubMed
33.
Zurück zum Zitat Esiri MM (2000) Which vascular lesions are of importance in vascular dementia? Ann N Y Acad Sci 903:239–243PubMedCrossRef Esiri MM (2000) Which vascular lesions are of importance in vascular dementia? Ann N Y Acad Sci 903:239–243PubMedCrossRef
34.
Zurück zum Zitat Lee JH, Olichney JM, Hansen LA, Hofstetter CR, Thal LJ (2000) Small concomitant vascular lesions do not influence rates of cognitive decline in patients with Alzheimer disease. Arch Neurol 57:1474–1479PubMedCrossRef Lee JH, Olichney JM, Hansen LA, Hofstetter CR, Thal LJ (2000) Small concomitant vascular lesions do not influence rates of cognitive decline in patients with Alzheimer disease. Arch Neurol 57:1474–1479PubMedCrossRef
35.
Zurück zum Zitat Schofield PW, Logroscino G, Andrews HF, Albert S, Stern Y (1997) An association between head circumference and Alzheimer’s disease in a population-based study of aging and dementia. Neurology 49:30–37PubMed Schofield PW, Logroscino G, Andrews HF, Albert S, Stern Y (1997) An association between head circumference and Alzheimer’s disease in a population-based study of aging and dementia. Neurology 49:30–37PubMed
36.
Zurück zum Zitat Obara K, Meyer JS, Mortel KF, Muramatsu K (1994) Cognitive declines correlate with decreased cortical volume and perfusion in dementia of Alzheimer type. J Neurol Sci 127:96–102PubMedCrossRef Obara K, Meyer JS, Mortel KF, Muramatsu K (1994) Cognitive declines correlate with decreased cortical volume and perfusion in dementia of Alzheimer type. J Neurol Sci 127:96–102PubMedCrossRef
37.
Zurück zum Zitat Meyer JS, Rauch GM, Crawford K et al (1999) Risk factors accelerating cerebral degenerative changes, cognitive decline and dementia. Int J Geriatr Psychiatry 14:1050–1061PubMedCrossRef Meyer JS, Rauch GM, Crawford K et al (1999) Risk factors accelerating cerebral degenerative changes, cognitive decline and dementia. Int J Geriatr Psychiatry 14:1050–1061PubMedCrossRef
38.
Zurück zum Zitat de Leon MJ, George AE, Reisberg B et al (1989) Alzheimer’s disease: longitudinal CT studies of ventricular change. AJR Am J Roentgenol 152:1257–1262PubMed de Leon MJ, George AE, Reisberg B et al (1989) Alzheimer’s disease: longitudinal CT studies of ventricular change. AJR Am J Roentgenol 152:1257–1262PubMed
39.
Zurück zum Zitat DeCarli C, Haxby JV, Gillette JA, Teichberg D, Rapoport SI, Schapiro MB (1992) Longitudinal changes in lateral ventricular volume in patients with dementia of the Alzheimer type. Neurology 42:2029–2036PubMed DeCarli C, Haxby JV, Gillette JA, Teichberg D, Rapoport SI, Schapiro MB (1992) Longitudinal changes in lateral ventricular volume in patients with dementia of the Alzheimer type. Neurology 42:2029–2036PubMed
40.
Zurück zum Zitat Salerno JA, Murphy DG, Horwitz B et al (1992) Brain atrophy in hypertension. A volumetric magnetic resonance imaging study. Hypertension 20:340–348PubMed Salerno JA, Murphy DG, Horwitz B et al (1992) Brain atrophy in hypertension. A volumetric magnetic resonance imaging study. Hypertension 20:340–348PubMed
41.
Zurück zum Zitat Strassburger TL, Lee HC, Daly EM et al (1997) Interactive effects of age and hypertension on volumes of brain structures. Stroke 28:1410–1417PubMed Strassburger TL, Lee HC, Daly EM et al (1997) Interactive effects of age and hypertension on volumes of brain structures. Stroke 28:1410–1417PubMed
42.
Zurück zum Zitat Yamano S, Sawai F, Yamamoto Y et al (1999) Relationship between brain atrophy estimated by a longitudinal computed tomography study and blood pressure control in patients with essential hypertension. Jpn Circ J 63:79–84PubMedCrossRef Yamano S, Sawai F, Yamamoto Y et al (1999) Relationship between brain atrophy estimated by a longitudinal computed tomography study and blood pressure control in patients with essential hypertension. Jpn Circ J 63:79–84PubMedCrossRef
43.
Zurück zum Zitat Taki Y, Goto R, Evans A et al (2004) Voxel-based morphometry of human brain with age and cerebrovascular risk factors. Neurobiol Aging 25:455–463PubMedCrossRef Taki Y, Goto R, Evans A et al (2004) Voxel-based morphometry of human brain with age and cerebrovascular risk factors. Neurobiol Aging 25:455–463PubMedCrossRef
44.
Zurück zum Zitat Meyer JS, Rauch G, Rauch RA, Haque A (2000) Risk factors for cerebral hypoperfusion, mild cognitive impairment, and dementia. Neurobiol Aging 21:161–169PubMedCrossRef Meyer JS, Rauch G, Rauch RA, Haque A (2000) Risk factors for cerebral hypoperfusion, mild cognitive impairment, and dementia. Neurobiol Aging 21:161–169PubMedCrossRef
45.
Zurück zum Zitat Jennings JR, Muldoon MF, Ryan C et al (2005) Reduced cerebral blood flow response and compensation among patients with untreated hypertension. Neurology 64:1358–1365PubMed Jennings JR, Muldoon MF, Ryan C et al (2005) Reduced cerebral blood flow response and compensation among patients with untreated hypertension. Neurology 64:1358–1365PubMed
Metadaten
Titel
Voxel-based morphometry demonstrates reduced grey matter density on brain MRI in patients with diabetic retinopathy
verfasst von
A. M. Wessels
S. Simsek
P. L. Remijnse
D. J. Veltman
G. J. Biessels
F. Barkhof
P. Scheltens
F. J. Snoek
R. J. Heine
S. A. R. B. Rombouts
Publikationsdatum
01.10.2006
Verlag
Springer-Verlag
Erschienen in
Diabetologia / Ausgabe 10/2006
Print ISSN: 0012-186X
Elektronische ISSN: 1432-0428
DOI
https://doi.org/10.1007/s00125-006-0283-7

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