The corpus callosum in Binswanger's disease: A quantitative fractional anisotropy analysis

Engelhardt, Eliasz; Moreira, Denise Madeira; Alves, Gilberto Oliveira; Lanna, Maria Elisa Oliveira; Alves, Carlos Eduardo de Oliveira; Ericeira-Valente, Letice; Sudo, Felipe Kenji; Laks, Jerson

doi:10.1590/S1980-57642009DN20400008

Abstract

To study the integrity of the corpus callosum in Binswanger's disease (BD) patients using quantitative fractional anisotropy (DTI-FA). Methods: Controls (12) and patients with BD (12) were included. MR [GE Signa Horizon-1.5T] scans were performed. BD patients presented Fazekas's score=6 and leukoaraiosis extension ³75%, as assessed on FLAIR sequence. Standard parameters for DTI-FA acquisition were used. Functool was employed for post-processing, and ROIs placed on the genu and splenium of the corpus callosum on one axial plane at the basal ganglia level. Statistics [ANOVA] for genu and splenium comparison were analyzed. Results: DTI-FA showed reduction of anisotropy in both regions of the corpus callosum, more prominently in anterior (genu) than posterior (splenium) in BD patients versus controls. Conclusion: The reduction of anisotropy reflects loss of integrity of fibers of the studied regions of the corpus callosum. This finding indicates an interruption of the most important inter-hemispheric commissure, and component of neural networks that underlies cognitive, behavioral, motor and sensory integration. The affected genu and splenium, together with damage to other fiber systems that connect the prefrontal and parietal-occipital regions, may manifest clinically as dysfunction of high-level integrative regions linked to the domains of executive and sensory functions, respectively, that can occur in Binswanger's disease.

Key words:
Binswanger's disease; corpus callosum; genu; splenium; diffusion tensor; fractional anisotropy.

Resumo

Estudar a integridade do corpo caloso em pacientes com doença de Binswanger (DB) com anisotropia fracionada quantitativa (DTI-FA). Métodos: Foram incluídos controles (12) e pacientes com DB (12). Imagens de RM [GE Signa Horizon-1,5T] foram obtidas. Os pacientes com DB apresentavam escore=6 de Fazekas e leucoaraiose com extensão ³75% como avaliado na seqüência em FLAIR. Foram utilizados parâmetros padrão para DTI-FA e utilizado Functool para pós-processamento. ROIs localizados no joelho e no esplênio do corpo caloso em um plano axial no nível dos gânglios da base. Estatística [ANOVA] feita para comparar joelho e esplênio. Resultados: DTI-FA mostrou redução da anisotropia em ambas as regiões do corpo caloso, com predomínio na anterior (joelho) em relação à posterior (esplênio), nos pacientes com DB em comparação aos controles. Conclusões: A redução da anisotropia reflete perda da integridade de fibras das regiões estudadas do corpo caloso. Esses achados indicam interrupção da mais importante comissura inter-hemisférica e componente de redes neurais subjacentes à integração cognitiva, comportamental e de funções motora e sensorial. O comprometimento do joelho e do esplênio, juntamente com a lesão de outros sistemas de fibras, que conectam regiões pré-frontais e parieto-occipitais, podem ser expressas clinicamente por disfunção de regiões de alto nível de integração, relacionadas aos domínios das funções executiva e sensorial, respectivamente, que pode ocorrer na doença de Binswanger.

Palavras-chave:
doença de Binswanger; corpo caloso; joelho; esplênio; tensor de difusão; anisotropia fracionada.

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References

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Dejerine J. Anatomie des Centres Nerveux. Paris: J Rueff Ed; 1895:338-344.
²
Doron KW, Gazzaniga MS. Neuroimaging techniques offer new perspectives on callosal transfer and interhemispheric communication. Cortex 2008;44:1023-1029.
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Tomimoto H, Lin J-X, Matsuo M et al. Different mechanisms of corpus callosum atrophy in Alzheimer's disease and vascular dementia. J Neurol 2004;251:398-406.
⁴
Türe U, Yasargil MG, Krisht AF. The arteries of the corpus callosum: a microsurgical anatomic study. Neurosurgery 1996;39:1075-1084.
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Funnell MG, Corballis PM, Gazzaniga MS. Insights into the functional specificity of the human corpus callosum. Brain 2000;123:920-926.
⁶
Gazzaniga MS. Cerebral specialization and interhemispheric communication. Does the corpus callosum enable the human condition? Brain 2000;123:1293-1326.
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Putnam MC, Wig GS, Grafton ST et al. Structural Organization of the Corpus Callosum Predicts the Extent and Impact of Cortical Activity in the Nondominant Hemisphere. J Neurosci 2008;28:2912-2918.
⁸
Stephan KE, Marshall JC, Penny WD et al. Interhemispheric Integration of Visual Processing during Task-Driven Lateralization. J Neurosci 2007; 27:3512-3522.
⁹
Wahl M, Lauterbach-Soon B, Hattingen E et al. Human Motor Corpus Callosum: Topography, Somatotopy, and Link between Microstructure and Function. J Neurosci 2007;27: 12132-12138.
¹⁰
Furuta A, Ishii N, Nishihara Y et al. Medullary Arteries in Aging and Dementia. Stroke 1991;22:442-446.
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Kahilogullari G, Comert A, Arslan M et al. Callosal branches of the anterior cerebral artery: an anatomical report. Clin Anat 2008;21:383-388.
¹²
Moody DM, Bell MA, Challa VR. The corpus callosum, a unique white-matter tract: anatomic features that may explain sparing in Binswanger disease and resistance to flow of fluid masses. Am J Neuroradiol 1988;9:1051-1059.
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Uchino A, Takase Y, Nomiyama K et al. Acquired lesions of the corpus callosum: MR imaging. Eur Radiol 2006;16:905-914.
¹⁴
Engelhardt E, Laks J, Cavalcanti J, et al. Demência vascular. Rev Bras Neurol 2004;40:5-25.
¹⁵
Erkinjuntti T. Subcortical Ischemic Vascular Disease and Dementia. Int Psychogeriat 2003;15(Suppl 1):23-26.
¹⁶
Caplan LR and Schoene WC. Clinical features of subcortical arteriosclerotic encephalopathy (Binswanger disease). Neurology 1978;28:1206-1215.
¹⁷
Babikian V and Ropper AH. Binswanger's Disease: A Review. Stroke 1987;18:2-12.
¹⁸
Jones DK, Lythgoe D, Horsfield MA et al. Characterization of white matter damage in ischemic leukoaraiosis with diffusion tensor MRI. Stroke 1999;30:393-397.
¹⁹
Román GC. Senile dementia of the Binswanger type. A vascular form of dementia in the elderly. JAMA 1987;258:1782-1788.
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Yamanouchi H, Sugiura S, Tomonaga M. Decrease in nerve fibres in cerebral white matter in progressive subcortical vascular encephalopathy of Binswanger type. An electron microscopic study. J Neurol 1989;236:382-387.
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Brown WR, Moody DM, Thore CR et al. Vascular dementia in leukoaraiosis may be a consequence of capillary loss not only in the lesions, but in normal-appearing white matter and cortex as well. J Neurol Sci 2007;257:62-66.
²²
Moody DM, Thore CR, Anstrom JA, et al. Quantification of Afferent Vessels Shows Reduced Brain Vascular Density in Subjects with Leukoaraiosis. Radiology 2004;233:883-890.
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Smid J, Nitrini R, Bahia VS, Caramelli P. Clinical characterization of vascular dementia: retrospective evaluation of an outpatient sample [Caracterização clínica da demência vascular]. Arq Neuropsiquiatr 2001;59:390-393.
²⁴
Young VG, Halliday GM, Kril JJ. Neuropathologic correlates of white matter hyperintensities. Neurology 2008;71:804-811.
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Awad IA, Johnson PC, Spetzler RF, Hodak JA. Incidental subcortical lesions identified on magnetic resonance imaging in the elderly. II. Postmortem pathological correlations. Stroke. 1986;17:1090-1097.
²⁶
Hachinski VC, Potter P, Merskey H. Leuko-araiosis: an ancient term for a new problem. Can J Neurol Sci 1986;13(Suppl 4):533-534.
²⁷
O'Sullivan M. Leukoaraiosis. Pract Neurol 2008;8:26-38.
²⁸
Rosenberg GA, Kornfeld M, Stovring J and Bicknell JM. Subcortical arteriosclerotic encephalopathy (Binswanger): Computerized tomography. Neurology 1979;29:1102-1106.
²⁹
Román GC. Binswanger disease: the history of a silent epidemic. Ann N Y Acad Sci 2000;903:19-23.
³⁰
Alexander AL, Lee JE, Lazar M, Field AS. Diffusion tensor imaging of the brain. Neurotherapeutics 2007;4:316-329.
³¹
Mori S and Zhang J. Principles of diffusion tensor imaging and its applications to basic neuroscience research. Neuron 2006;51:527-539.
³²
O'Sullivan M, Summers PE, Jones DK, et al. Normal-appearing white matter in ischemic leukoaraiosis: A diffusion tensor MRI study. Neurology 2001;57:2307-2310.
³³
Román GC, Tatemichi TK, Erkinjuntti T, et al. Vascular dementia: diagnostic criteria for research studies: report of the NINDS-AIREN international workshop. Neurology 1993;43: 250-260.
³⁴
Folstein MF, Folstein SE and McHugh PR. "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 1975;12:189-198.
³⁵
Hughes CP, Berg L, Danziger WL, et al. A new clinical scale for the staging of dementia. Br J Psychiatry 1982;140:566-572.
³⁶
Hachinski VC, Iliff LD, Zilhka E, et al. Cerebral blood flow in dementia. Arch Neurol 1975;32:632-637.
³⁷
Fazekas F, Chawluk JB, Alavi A, et al. MR signal abnormalities at 1.5 T in Alzheimer's dementia and normal aging. Am J Neuroradiol 1987;8:421-426.
³⁸
Pantoni P, Simoni M, Pracucci G, et al. Visual Rating Scales for Age-Related White Matter Changes (Leukoaraiosis). Can the Heterogeneity Be Reduced? Stroke. 2002;33:2827-2833.
³⁹
VassarStats: Statistical Computation Web Site. http://faculty.vassar.edu/lowry/VassarStats.html (acessado em junho de 2008).
» http://faculty.vassar.edu/lowry/VassarStats.html
⁴⁰
Yamauchi H, Fukuyama H and Shio H. Corpus callosum atrophy in patients with leukoaraiosis may indicate global cognitive impairment. Stroke 2000;31:1515-1520.
⁴¹
O'Sullivan M, Morris RG, Huckstep B, et al. Diffusion tensor MRI correlates with executive dysfunction in patients with ischaemic leukoaraiosis. J Neurol Neurosurg Psychiatry 2004;75:441-447.
⁴²
Hanyu H, Imon Y, Sakurai H, et al. Regional differences in diffusion abnormality in cerebral white matter lesions in patients with vascular dementia of the Binswanger type and Alzheimer's disease. Eur J Neurol 1999;6:195-203.
⁴³
Sugihara S, Kinoshita T, Matsusue E, Fujii S, Ogawa T. Usefulness of Diffusion Tensor Imaging of White Matter in Alzheimer Disease and Vascular Dementia. Acta Radiol 2004;45: 658-663.
⁴⁴
Ota M, Obata T, Akine Y, et al. Age-related degeneration of corpus callosum measured with diffusion tensor imaging. Neuroimage. 2006;31:1445-1452.
⁴⁵
Taylor WD, Bae JN, MacFall JR, et al. Widespread Effects of Hyperintense Lesions on Cerebral White Matter Structure. Am J Roentgenol 2007;188:1695-1704.
⁴⁶
Masterman DL, Cummings JL. Frontal-subcortical circuits: the anatomic basis of executive, social and motivated behaviors. J Psychopharmacol 2007;11:107-114.
⁴⁷
Schmahmanna JD, Pandya DN. Disconnection syndromes of basal ganglia, thalamus, and cerebrocerebellar systems. Cortex 2008;44:1037-1066.
⁴⁸
Catani M, Ffytche DH. The rises and falls of disconnection syndromes. Brain 2005;128:2224-2239
⁴⁹
Catani M, Mesulam M. What is a disconnection syndrome? Cortex 2008; 44:911-913.
⁵⁰
Jokinen H, Ryberg C, Kalska H, et al. Corpus callosum atrophy is associated with mental slowing and executive deficits in subjects with age-related white matter hyperintensities: the LADIS Study. J Neurol Neurosurg Psychiatry 2007;78:491-496.

Publication Dates

Publication in this collection
Oct-Dec 2008

History

Received
24 Sept 2008
Accepted
12 Nov 2008

This is an open-access article distributed under the terms of the Creative Commons Attribution License

[1] ¹
Dejerine J. Anatomie des Centres Nerveux. Paris: J Rueff Ed; 1895:338-344.

[2] ²
Doron KW, Gazzaniga MS. Neuroimaging techniques offer new perspectives on callosal transfer and interhemispheric communication. Cortex 2008;44:1023-1029.

[3] ³
Tomimoto H, Lin J-X, Matsuo M et al. Different mechanisms of corpus callosum atrophy in Alzheimer's disease and vascular dementia. J Neurol 2004;251:398-406.

[4] ⁴
Türe U, Yasargil MG, Krisht AF. The arteries of the corpus callosum: a microsurgical anatomic study. Neurosurgery 1996;39:1075-1084.

[5] ⁵
Funnell MG, Corballis PM, Gazzaniga MS. Insights into the functional specificity of the human corpus callosum. Brain 2000;123:920-926.

[6] ⁶
Gazzaniga MS. Cerebral specialization and interhemispheric communication. Does the corpus callosum enable the human condition? Brain 2000;123:1293-1326.

[7] ⁷
Putnam MC, Wig GS, Grafton ST et al. Structural Organization of the Corpus Callosum Predicts the Extent and Impact of Cortical Activity in the Nondominant Hemisphere. J Neurosci 2008;28:2912-2918.

[8] ⁸
Stephan KE, Marshall JC, Penny WD et al. Interhemispheric Integration of Visual Processing during Task-Driven Lateralization. J Neurosci 2007; 27:3512-3522.

[9] ⁹
Wahl M, Lauterbach-Soon B, Hattingen E et al. Human Motor Corpus Callosum: Topography, Somatotopy, and Link between Microstructure and Function. J Neurosci 2007;27: 12132-12138.

[10] ¹⁰
Furuta A, Ishii N, Nishihara Y et al. Medullary Arteries in Aging and Dementia. Stroke 1991;22:442-446.

[11] ¹¹
Kahilogullari G, Comert A, Arslan M et al. Callosal branches of the anterior cerebral artery: an anatomical report. Clin Anat 2008;21:383-388.

[12] ¹²
Moody DM, Bell MA, Challa VR. The corpus callosum, a unique white-matter tract: anatomic features that may explain sparing in Binswanger disease and resistance to flow of fluid masses. Am J Neuroradiol 1988;9:1051-1059.

[13] ¹³
Uchino A, Takase Y, Nomiyama K et al. Acquired lesions of the corpus callosum: MR imaging. Eur Radiol 2006;16:905-914.

[14] ¹⁴
Engelhardt E, Laks J, Cavalcanti J, et al. Demência vascular. Rev Bras Neurol 2004;40:5-25.

[15] ¹⁵
Erkinjuntti T. Subcortical Ischemic Vascular Disease and Dementia. Int Psychogeriat 2003;15(Suppl 1):23-26.

[16] ¹⁶
Caplan LR and Schoene WC. Clinical features of subcortical arteriosclerotic encephalopathy (Binswanger disease). Neurology 1978;28:1206-1215.

[17] ¹⁷
Babikian V and Ropper AH. Binswanger's Disease: A Review. Stroke 1987;18:2-12.

[18] ¹⁸
Jones DK, Lythgoe D, Horsfield MA et al. Characterization of white matter damage in ischemic leukoaraiosis with diffusion tensor MRI. Stroke 1999;30:393-397.

[19] ¹⁹
Román GC. Senile dementia of the Binswanger type. A vascular form of dementia in the elderly. JAMA 1987;258:1782-1788.

[20] ²⁰
Yamanouchi H, Sugiura S, Tomonaga M. Decrease in nerve fibres in cerebral white matter in progressive subcortical vascular encephalopathy of Binswanger type. An electron microscopic study. J Neurol 1989;236:382-387.

[21] ²¹
Brown WR, Moody DM, Thore CR et al. Vascular dementia in leukoaraiosis may be a consequence of capillary loss not only in the lesions, but in normal-appearing white matter and cortex as well. J Neurol Sci 2007;257:62-66.

[22] ²²
Moody DM, Thore CR, Anstrom JA, et al. Quantification of Afferent Vessels Shows Reduced Brain Vascular Density in Subjects with Leukoaraiosis. Radiology 2004;233:883-890.

[23] ²³
Smid J, Nitrini R, Bahia VS, Caramelli P. Clinical characterization of vascular dementia: retrospective evaluation of an outpatient sample [Caracterização clínica da demência vascular]. Arq Neuropsiquiatr 2001;59:390-393.

[24] ²⁴
Young VG, Halliday GM, Kril JJ. Neuropathologic correlates of white matter hyperintensities. Neurology 2008;71:804-811.

[25] ²⁵
Awad IA, Johnson PC, Spetzler RF, Hodak JA. Incidental subcortical lesions identified on magnetic resonance imaging in the elderly. II. Postmortem pathological correlations. Stroke. 1986;17:1090-1097.

[26] ²⁶
Hachinski VC, Potter P, Merskey H. Leuko-araiosis: an ancient term for a new problem. Can J Neurol Sci 1986;13(Suppl 4):533-534.

[27] ²⁷
O'Sullivan M. Leukoaraiosis. Pract Neurol 2008;8:26-38.

[28] ²⁸
Rosenberg GA, Kornfeld M, Stovring J and Bicknell JM. Subcortical arteriosclerotic encephalopathy (Binswanger): Computerized tomography. Neurology 1979;29:1102-1106.

[29] ²⁹
Román GC. Binswanger disease: the history of a silent epidemic. Ann N Y Acad Sci 2000;903:19-23.

[30] ³⁰
Alexander AL, Lee JE, Lazar M, Field AS. Diffusion tensor imaging of the brain. Neurotherapeutics 2007;4:316-329.

[31] ³¹
Mori S and Zhang J. Principles of diffusion tensor imaging and its applications to basic neuroscience research. Neuron 2006;51:527-539.

[32] ³²
O'Sullivan M, Summers PE, Jones DK, et al. Normal-appearing white matter in ischemic leukoaraiosis: A diffusion tensor MRI study. Neurology 2001;57:2307-2310.

[33] ³³
Román GC, Tatemichi TK, Erkinjuntti T, et al. Vascular dementia: diagnostic criteria for research studies: report of the NINDS-AIREN international workshop. Neurology 1993;43: 250-260.

[34] ³⁴
Folstein MF, Folstein SE and McHugh PR. "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 1975;12:189-198.

[35] ³⁵
Hughes CP, Berg L, Danziger WL, et al. A new clinical scale for the staging of dementia. Br J Psychiatry 1982;140:566-572.

[36] ³⁶
Hachinski VC, Iliff LD, Zilhka E, et al. Cerebral blood flow in dementia. Arch Neurol 1975;32:632-637.

[37] ³⁷
Fazekas F, Chawluk JB, Alavi A, et al. MR signal abnormalities at 1.5 T in Alzheimer's dementia and normal aging. Am J Neuroradiol 1987;8:421-426.

[38] ³⁸
Pantoni P, Simoni M, Pracucci G, et al. Visual Rating Scales for Age-Related White Matter Changes (Leukoaraiosis). Can the Heterogeneity Be Reduced? Stroke. 2002;33:2827-2833.

[39] ³⁹
VassarStats: Statistical Computation Web Site. http://faculty.vassar.edu/lowry/VassarStats.html (acessado em junho de 2008).
» http://faculty.vassar.edu/lowry/VassarStats.html

[40] ⁴⁰
Yamauchi H, Fukuyama H and Shio H. Corpus callosum atrophy in patients with leukoaraiosis may indicate global cognitive impairment. Stroke 2000;31:1515-1520.

[41] ⁴¹
O'Sullivan M, Morris RG, Huckstep B, et al. Diffusion tensor MRI correlates with executive dysfunction in patients with ischaemic leukoaraiosis. J Neurol Neurosurg Psychiatry 2004;75:441-447.

[42] ⁴²
Hanyu H, Imon Y, Sakurai H, et al. Regional differences in diffusion abnormality in cerebral white matter lesions in patients with vascular dementia of the Binswanger type and Alzheimer's disease. Eur J Neurol 1999;6:195-203.

[43] ⁴³
Sugihara S, Kinoshita T, Matsusue E, Fujii S, Ogawa T. Usefulness of Diffusion Tensor Imaging of White Matter in Alzheimer Disease and Vascular Dementia. Acta Radiol 2004;45: 658-663.

[44] ⁴⁴
Ota M, Obata T, Akine Y, et al. Age-related degeneration of corpus callosum measured with diffusion tensor imaging. Neuroimage. 2006;31:1445-1452.

[45] ⁴⁵
Taylor WD, Bae JN, MacFall JR, et al. Widespread Effects of Hyperintense Lesions on Cerebral White Matter Structure. Am J Roentgenol 2007;188:1695-1704.

[46] ⁴⁶
Masterman DL, Cummings JL. Frontal-subcortical circuits: the anatomic basis of executive, social and motivated behaviors. J Psychopharmacol 2007;11:107-114.

[47] ⁴⁷
Schmahmanna JD, Pandya DN. Disconnection syndromes of basal ganglia, thalamus, and cerebrocerebellar systems. Cortex 2008;44:1037-1066.

[48] ⁴⁸
Catani M, Ffytche DH. The rises and falls of disconnection syndromes. Brain 2005;128:2224-2239

[49] ⁴⁹
Catani M, Mesulam M. What is a disconnection syndrome? Cortex 2008; 44:911-913.

[50] ⁵⁰
Jokinen H, Ryberg C, Kalska H, et al. Corpus callosum atrophy is associated with mental slowing and executive deficits in subjects with age-related white matter hyperintensities: the LADIS Study. J Neurol Neurosurg Psychiatry 2007;78:491-496.

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