The role of diffusion magnetic resonance imaging in Parkinson's disease and in the differential diagnosis with atypical parkinsonism

Oliveira, Romulo Varella de; Pereira, João Santos

doi:10.1590/0100-3984.2016-0073

Romulo Varella de Oliveira Mailing address: Dr. Romulo Varela de Oliveira. Hospital Universitário Pedro Ernesto – Serviço de Imagem. Boulevard 28 de Setembro, 77, Vila Isabel. Rio de Janeiro, RJ, Brazil, 20551-030. E-mail: romulovarella@hotmail.com.

Full Member of the Colégio Brasileiro de Radiologia e Diagnóstico por Imagem (CBR), Masters Student in the Graduate Program in Medical Sciences at the Faculdade de Ciências Médicas da Universidade do Estado do Rio de Janeiro (FCM-UERJ), MD, Radiologist at the Hospital Universitário Pedro Ernesto (HUPE) and at the Clínica Alta Excelência Diagnóstica (DASA), Rio de Janeiro, RJ, Brazil

Universidade do Estado do Rio de Janeiro, Faculdade de Ciências Médicas, Program in Medical Sciences , Universidade do Estado do Rio de Janeiro, Rio de Janeiro, RJ, Brazil

Hospital Universitário Pedro Ernesto, Clínica Alta Excelência Diagnóstica, Rio de Janeiro, RJ, Brazil

João Santos Pereira

PhD, Full Member of the Academia Brasileira de Neurologia (ABN), Associate Professor, Coordinator of the Movement Disorders Sector of the Neurology Department of the Hospital Universitário Pedro Ernesto da Universidade do Estado do Rio de Janeiro (HUPE-UERJ), Rio de Janeiro, RJ, Brazil

Universidade do Estado do Rio de Janeiro, Hospital Universitário Pedro Ernesto, Neurology Department, Universidade do Estado do Rio de Janeiro, Rio de Janeiro, RJ, Brazil

Mailing address: Dr. Romulo Varela de Oliveira. Hospital Universitário Pedro Ernesto – Serviço de Imagem. Boulevard 28 de Setembro, 77, Vila Isabel. Rio de Janeiro, RJ, Brazil, 20551-030. E-mail: romulovarella@hotmail.com.

Full Member of the Colégio Brasileiro de Radiologia e Diagnóstico por Imagem (CBR), Masters Student in the Graduate Program in Medical Sciences at the Faculdade de Ciências Médicas da Universidade do Estado do Rio de Janeiro (FCM-UERJ), MD, Radiologist at the Hospital Universitário Pedro Ernesto (HUPE) and at the Clínica Alta Excelência Diagnóstica (DASA), Rio de Janeiro, RJ, Brazil

Universidade do Estado do Rio de Janeiro, Faculdade de Ciências Médicas, Program in Medical Sciences , Universidade do Estado do Rio de Janeiro, Rio de Janeiro, RJ, Brazil

Hospital Universitário Pedro Ernesto, Clínica Alta Excelência Diagnóstica, Rio de Janeiro, RJ, Brazil

PhD, Full Member of the Academia Brasileira de Neurologia (ABN), Associate Professor, Coordinator of the Movement Disorders Sector of the Neurology Department of the Hospital Universitário Pedro Ernesto da Universidade do Estado do Rio de Janeiro (HUPE-UERJ), Rio de Janeiro, RJ, Brazil

Universidade do Estado do Rio de Janeiro, Hospital Universitário Pedro Ernesto, Neurology Department, Universidade do Estado do Rio de Janeiro, Rio de Janeiro, RJ, Brazil

Figures (3)
Tables (1)

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Figure 1
Findings on conventional MRI and DTI in Parkinson's disease. On T2-weighted sequences and susceptibility-weighted imaging, the normal substantia nigra presents as a band of hypointensity between the cerebral peduncle and the mesencephalic tegmentum. In a 66-year-old patient without Parkinson's disease (A), an axial slice of the midbrain on susceptibility-weighted imaging shows a well-delineated substantia nigra (black circle), of normal thickness, showing well-defined cleavage with the red nucleus (white circle). In a 68-year-old patient with Parkinson's disease (B), an axial slice of the midbrain on susceptibility-weighted imaging shows a poorly delineated, thin substantia nigra and poorly defined cleavage of the substantia nigra with the red nucleus. The reduced volume of the substantia nigra in the patient with Parkinson's disease is attributable to iron deposition. The regions of interest in the substantia nigra in patients A and B (black circles) were copied and pasted onto the FA map (C and D, respectively), which shows that the FA value was lower in the patient with Parkinson's disease than in the patient without (0.425 vs. 0.581), indicating a loss of neuronal integrity. The contralateral findings were comparable between the two patients (images not shown).

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Figure 2
Conventional MRI findings in progressive supranuclear palsy. In a sagittal T1-weighted sequence, the hummingbird sign can be seen (A), due to the volumetric reduction of the midbrain (asterisk) in relation to the pons (black asterisk), unlike what is seen in the normal brainstem (B). In the axial plane, the Mickey Mouse sign (C) occurs due to widening of the interpeduncular cistern (white arrow) and retraction of the dorsolateral regions of the midbrain, none of which were observed in the control patient (D).

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Figure 3
Morphological and signal changes on a conventional MRI scan of a patient with multiple system atrophy. The hot cross bun sign appears as two perpendicular lines in the pons, which present a hyperintense signal in an axial T2-weighted sequence, together with accentuation of the basal cisterns, cerebellar sulci, and fourth ventricle (A). A sagittal T1-weighted sequence (B) shows the volume reduction of the pons relative to the midbrain (compare with the normal brainstem shown in ).

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Table 1
Findings on conventional and diffusion MRI in Parkinson's disease and atypical parkinsonism.

	Conventional MRI		Diffusion-weighted MRI
	Findings	Considerations	Findings	Considerations
PD	- Thinning of the substantia nigra pars compacta, best visualized in axial T2-weighted sequences and susceptibility-weighted imaging⁽¹²12 Meijer FJ, Goraj B. Brain MRI in Parkinson's disease. Front Biosci (Elite Ed). 2014;6:360-9.⁾	- Quite high specificity, although quite low sensitivity, found only in the more advanced stages⁽¹²12 Meijer FJ, Goraj B. Brain MRI in Parkinson's disease. Front Biosci (Elite Ed). 2014;6:360-9.⁾	- Reduced FA in the substantia nigra, more evident in the caudal portion⁽⁸8 Cochrane CJ, Ebmeier KP. Diffusion tensor imaging in parkinsonian syndromes: a systematic review and meta-analysis. Neurology. 2013;80:857-64.^,¹⁰10 Modrego PJ, Fayed N, Artal J, et al. Correlation of findings in advanced MRI techniques with global severity scales in patients with Parkinson disease. Acad Radiol. 2011;18:235-41.^,¹¹11 Jiang MF, Shi F, Niu GM, et al. A novel method for evaluating brain function and microstructural changes in Parkinson's disease. Neural Regen Res. 2015;10:2025-32.^,²¹21 Zhan W, Kang GA, Glass GA, et al. Regional alterations of brain microstructure in Parkinson's disease using diffusion tensor imaging. Mov Disord. 2012;27:90-7. 22 Vaillancourt DE, Spraker MB, Prodoehl J, et al. High-resolution diffusion tensor imaging in the substantia nigra of de novo Parkinson disease. Neurology. 2009;72:1378-84. 23 Lenfeldt N, Larsson A, Nyberg L, et al. Fractional anisotropy in the substantia nigra in Parkinson's disease: a complex picture. Eur J Neurol. 2015;22:1408-14. 24 Zhang K, Yu C, Zhang Y, et al. Voxel-based analysis of diffusion tensor indices in the brain in patients with Parkinson's disease. Eur J Radiol. 2011;77:269-73.^-²⁵25 Schwarz ST, Abaei M, Gontu V, et al. Diffusion tensor imaging of nigral degeneration in Parkinson's disease: a region-of-interest and voxel-based study at 3 T and systematic review with meta-analysis. Neuroimage Clin. 2013;3:481-8.⁾	- High specificity and sensitivity, even in the early stages of the disease, data more established in the literature⁽⁸8 Cochrane CJ, Ebmeier KP. Diffusion tensor imaging in parkinsonian syndromes: a systematic review and meta-analysis. Neurology. 2013;80:857-64.^,¹⁰10 Modrego PJ, Fayed N, Artal J, et al. Correlation of findings in advanced MRI techniques with global severity scales in patients with Parkinson disease. Acad Radiol. 2011;18:235-41.^,¹¹11 Jiang MF, Shi F, Niu GM, et al. A novel method for evaluating brain function and microstructural changes in Parkinson's disease. Neural Regen Res. 2015;10:2025-32.^,²¹21 Zhan W, Kang GA, Glass GA, et al. Regional alterations of brain microstructure in Parkinson's disease using diffusion tensor imaging. Mov Disord. 2012;27:90-7. 22 Vaillancourt DE, Spraker MB, Prodoehl J, et al. High-resolution diffusion tensor imaging in the substantia nigra of de novo Parkinson disease. Neurology. 2009;72:1378-84. 23 Lenfeldt N, Larsson A, Nyberg L, et al. Fractional anisotropy in the substantia nigra in Parkinson's disease: a complex picture. Eur J Neurol. 2015;22:1408-14. 24 Zhang K, Yu C, Zhang Y, et al. Voxel-based analysis of diffusion tensor indices in the brain in patients with Parkinson's disease. Eur J Radiol. 2011;77:269-73.^-²⁵25 Schwarz ST, Abaei M, Gontu V, et al. Diffusion tensor imaging of nigral degeneration in Parkinson's disease: a region-of-interest and voxel-based study at 3 T and systematic review with meta-analysis. Neuroimage Clin. 2013;3:481-8.⁾
			- Reduced FA in the frontal lobes (motor, premotor and supplemental motor cortices)⁽¹⁸18 Gattellaro G, Minati L, Grisoli M, et al. White matter involvement in idiopathic Parkinson disease: a diffusion tensor imaging study. AJNR Am J Neuroradiol. 2009;30:1222-6.^,²¹21 Zhan W, Kang GA, Glass GA, et al. Regional alterations of brain microstructure in Parkinson's disease using diffusion tensor imaging. Mov Disord. 2012;27:90-7.^,²⁷27 Kendi ATK, Lehericy S, Luciana M, et al. Altered diffusion in the frontal lobe in Parkinson disease. AJNR Am J Neuroradiol. 2008;29:501-5.⁾	- Low specificity and sensitivity⁽¹⁸18 Gattellaro G, Minati L, Grisoli M, et al. White matter involvement in idiopathic Parkinson disease: a diffusion tensor imaging study. AJNR Am J Neuroradiol. 2009;30:1222-6.^,²¹21 Zhan W, Kang GA, Glass GA, et al. Regional alterations of brain microstructure in Parkinson's disease using diffusion tensor imaging. Mov Disord. 2012;27:90-7.^,²⁷27 Kendi ATK, Lehericy S, Luciana M, et al. Altered diffusion in the frontal lobe in Parkinson disease. AJNR Am J Neuroradiol. 2008;29:501-5.⁾
			- Reduced FA in the striatum and cerebellar hemispheres⁽²⁸28 Péran P, Cherubini A, Assogna F, et al. Magnetic resonance imaging markers of Parkinson's disease nigrostriatal signature. Brain. 2010;133:3423-33.^,²⁹29 Mormina E, Arrigo A, Calamuneri A, et al. Diffusion tensor imaging parameters' changes of cerebellar hemispheres in Parkinson's disease. Neuroradiology. 2015;57:327-34.⁾	- Rarely studied but could be associated with specific signs of the disease⁽²⁸28 Péran P, Cherubini A, Assogna F, et al. Magnetic resonance imaging markers of Parkinson's disease nigrostriatal signature. Brain. 2010;133:3423-33.^,²⁹29 Mormina E, Arrigo A, Calamuneri A, et al. Diffusion tensor imaging parameters' changes of cerebellar hemispheres in Parkinson's disease. Neuroradiology. 2015;57:327-34.⁾
	- Diffuse cortical atrophy, mainly in the frontal lobes⁽¹²12 Meijer FJ, Goraj B. Brain MRI in Parkinson's disease. Front Biosci (Elite Ed). 2014;6:360-9.⁾	- Low sensitivity and specificity, occurs in the terminal phase⁽¹²12 Meijer FJ, Goraj B. Brain MRI in Parkinson's disease. Front Biosci (Elite Ed). 2014;6:360-9.⁾	- Reduced FA in the genu of the corpus callosum, cingulate gyrus, hip-pocampus, superior/inferior longitudinal fasciculi and inferior/uncinate fronto-occipital fasciculi⁽³⁰30 Kamagata K, Motoi Y, Abe O, et al. White matter alteration of the cingulum in Parkinson disease with and without dementia: evaluation by diffusion tensor tract-specific analysis. AJNR Am J Neuroradiol. 2012;33:890-5. 31 Matsui H, Nishinaka K, Oda M, et al. Dementia in Parkinson's disease: diffusion tensor imaging. Acta Neurol Scand. 2007;116:177-81. 32 Zheng Z, Shemmassian S, Wijekoon C, et al. DTI correlates of distinct cognitive impairments in Parkinson's disease. Hum Brain Mapp. 2014;35:1325-33. 33 Duncan GW, Firbank MJ, Yarnall AJ, et al. Gray and white matter imaging: a biomarker for cognitive impairment in early Parkinson's disease? Mov Disord. 2016;31:103-10. 34 Wiltshire K, Concha L, Gee M, et al. Corpus callosum and cingulum tractography in Parkinson's disease. Can J Neurol Sci. 2010;37:595-600. 35 Hattori T, Orimo S, Aoki S, et al. Cognitive status correlates with white matter alteration in Parkinson's disease. Hum Brain Mapp. 2012;33:727-39.^-³⁶36 Carlesimo GA, Piras F, Assogna F, et al. Hippocampal abnormalities and memory deficits in Parkinson disease: a multimodal imaging study. Neurology. 2012;78:1939-45.⁾	- Appears to be related to dementia in PD but warrants further study⁽³⁰30 Kamagata K, Motoi Y, Abe O, et al. White matter alteration of the cingulum in Parkinson disease with and without dementia: evaluation by diffusion tensor tract-specific analysis. AJNR Am J Neuroradiol. 2012;33:890-5. 31 Matsui H, Nishinaka K, Oda M, et al. Dementia in Parkinson's disease: diffusion tensor imaging. Acta Neurol Scand. 2007;116:177-81. 32 Zheng Z, Shemmassian S, Wijekoon C, et al. DTI correlates of distinct cognitive impairments in Parkinson's disease. Hum Brain Mapp. 2014;35:1325-33. 33 Duncan GW, Firbank MJ, Yarnall AJ, et al. Gray and white matter imaging: a biomarker for cognitive impairment in early Parkinson's disease? Mov Disord. 2016;31:103-10. 34 Wiltshire K, Concha L, Gee M, et al. Corpus callosum and cingulum tractography in Parkinson's disease. Can J Neurol Sci. 2010;37:595-600. 35 Hattori T, Orimo S, Aoki S, et al. Cognitive status correlates with white matter alteration in Parkinson's disease. Hum Brain Mapp. 2012;33:727-39.^-³⁶36 Carlesimo GA, Piras F, Assogna F, et al. Hippocampal abnormalities and memory deficits in Parkinson disease: a multimodal imaging study. Neurology. 2012;78:1939-45.⁾
			- Reduced FA in the dorsomedial thalamus and anterior cingulate gyrus⁽¹¹11 Jiang MF, Shi F, Niu GM, et al. A novel method for evaluating brain function and microstructural changes in Parkinson's disease. Neural Regen Res. 2015;10:2025-32.^,³¹31 Matsui H, Nishinaka K, Oda M, et al. Dementia in Parkinson's disease: diffusion tensor imaging. Acta Neurol Scand. 2007;116:177-81.^,³⁷37 Li W, Liu J, Skidmore F, et al. White matter microstructure changes in the thalamus in Parkinson disease with depression: a diffusion tensor MR imaging study. AJNR Am J Neuroradiol. 2010;31:1861-6.⁾	- Could be related to depression, although it has not been extensively studied⁽¹¹11 Jiang MF, Shi F, Niu GM, et al. A novel method for evaluating brain function and microstructural changes in Parkinson's disease. Neural Regen Res. 2015;10:2025-32.^,³¹31 Matsui H, Nishinaka K, Oda M, et al. Dementia in Parkinson's disease: diffusion tensor imaging. Acta Neurol Scand. 2007;116:177-81.^,³⁷37 Li W, Liu J, Skidmore F, et al. White matter microstructure changes in the thalamus in Parkinson disease with depression: a diffusion tensor MR imaging study. AJNR Am J Neuroradiol. 2010;31:1861-6.⁾
			- Reduced FA in the olfactory bulbs, white matter adjacent to the primary olfactory cortex, and gyrus rectus⁽³⁸38 Skorpil M, Söderlund V, Sundin A, et al. MRI diffusion in Parkinson's disease: using the technique's inherent directional information to study the olfactory bulb and substantia nigra. J Parkinsons Dis. 2012;2:171-80.^,⁴⁰40 Rolheiser TM, Fulton HG, Good KP, et al. Diffusion tensor imaging and olfactory identification testing in early-stage Parkinson's disease. J Neurol. 2011;258:1254-60.^,⁴¹41 Ibarretxe-Bilbao N, Junque C, Marti MJ, et al. Olfactory impairment in Parkinson's disease and white matter abnormalities in central olfactory areas: a voxel-based diffusion tensor imaging study. Mov Disord. 2010;25:1888-94.⁾	- Can be present in individuals with altered olfactory tests, with the potential to identify patients in the premotor phase of PD⁽³⁸38 Skorpil M, Söderlund V, Sundin A, et al. MRI diffusion in Parkinson's disease: using the technique's inherent directional information to study the olfactory bulb and substantia nigra. J Parkinsons Dis. 2012;2:171-80.^,⁴⁰40 Rolheiser TM, Fulton HG, Good KP, et al. Diffusion tensor imaging and olfactory identification testing in early-stage Parkinson's disease. J Neurol. 2011;258:1254-60.^,⁴¹41 Ibarretxe-Bilbao N, Junque C, Marti MJ, et al. Olfactory impairment in Parkinson's disease and white matter abnormalities in central olfactory areas: a voxel-based diffusion tensor imaging study. Mov Disord. 2010;25:1888-94.⁾
MSA	- Hot cross bun sign in axial T2-weighted sequences, with atrophy of the pons⁽¹³13 Massey LA, Micallef C, Paviour DC, et al. Conventional magnetic resonance imaging in confirmed progressive supranuclear palsy and multiple system atrophy. Mov Disord. 2012;27:1754-62. 14 Quattrone A, Nicoletti G, Messina D, et al. MR imaging index for differentiation of progressive supranuclear palsy from Parkinson disease and the Parkinson variant of multiple system atrophy. Radiology. 2008;246:214-21.^-¹⁵15 Paviour DC, Price SL, Jahanshahi M, et al. Regional brain volumes distinguish PSP, MSA-P, and PD: MRI-based clinico-radiological correlations. Mov Disord. 2006;21:989-96.⁾	- All have good specificity but can be seen in other conditions⁽¹³13 Massey LA, Micallef C, Paviour DC, et al. Conventional magnetic resonance imaging in confirmed progressive supranuclear palsy and multiple system atrophy. Mov Disord. 2012;27:1754-62. 14 Quattrone A, Nicoletti G, Messina D, et al. MR imaging index for differentiation of progressive supranuclear palsy from Parkinson disease and the Parkinson variant of multiple system atrophy. Radiology. 2008;246:214-21.^-¹⁵15 Paviour DC, Price SL, Jahanshahi M, et al. Regional brain volumes distinguish PSP, MSA-P, and PD: MRI-based clinico-radiological correlations. Mov Disord. 2006;21:989-96.⁾	- Reduced FA and increased ADC in the putamen⁽⁴³43 Ito M, Watanabe H, Kawai Y, et al. Usefulness of combined fractional anisotropy and apparent diffusion coefficient values for detection of involvement in multiple system atrophy. J Neurol Neurosurg Psychiatry. 2007;78:722-8. 44 Köllensperger M, Seppi K, Liener C, et al. Diffusion weighted imaging best discriminates PD from MSA-P: a comparison with tilt table testing and heart MIBG scintigraphy. Mov Disord. 2007;22:1771-6. 45 Pellecchia MT, Barone P, Mollica C, et al. Diffusion-weighted imaging in multiple system atrophy: a comparison between clinical subtypes. Mov Disord. 2009;24:689-96. 46 Seppi K, Schocke MFH, Prennschuetz-Schuetzenau K, et al. Topography of putaminal degeneration in multiple system atrophy: a diffusion magnetic resonance study. Mov Disord. 2006;21:847-52. 47 Tsukamoto K, Matsusue E, Kanasaki Y, et al. Significance of apparent diffusion coefficient measurement for the differential diagnosis of multiple system atrophy, progressive supranuclear palsy, and Parkinson's disease: evaluation by 3.0-T MR imaging. Neuroradiology. 2012;54:947-55.^-⁴⁸48 Barbagallo G, Sierra-Peña M, Nemmi F, et al. Multimodal MRI assessment of nigro-striatal pathway in multiple system atrophy and Parkinson disease. Mov Disord. 2016;31:325-34.⁾	- High sensitivity and specificity, especially in MSA-P, but can also occur in PSP⁽⁴³43 Ito M, Watanabe H, Kawai Y, et al. Usefulness of combined fractional anisotropy and apparent diffusion coefficient values for detection of involvement in multiple system atrophy. J Neurol Neurosurg Psychiatry. 2007;78:722-8. 44 Köllensperger M, Seppi K, Liener C, et al. Diffusion weighted imaging best discriminates PD from MSA-P: a comparison with tilt table testing and heart MIBG scintigraphy. Mov Disord. 2007;22:1771-6. 45 Pellecchia MT, Barone P, Mollica C, et al. Diffusion-weighted imaging in multiple system atrophy: a comparison between clinical subtypes. Mov Disord. 2009;24:689-96. 46 Seppi K, Schocke MFH, Prennschuetz-Schuetzenau K, et al. Topography of putaminal degeneration in multiple system atrophy: a diffusion magnetic resonance study. Mov Disord. 2006;21:847-52. 47 Tsukamoto K, Matsusue E, Kanasaki Y, et al. Significance of apparent diffusion coefficient measurement for the differential diagnosis of multiple system atrophy, progressive supranuclear palsy, and Parkinson's disease: evaluation by 3.0-T MR imaging. Neuroradiology. 2012;54:947-55.^-⁴⁸48 Barbagallo G, Sierra-Peña M, Nemmi F, et al. Multimodal MRI assessment of nigro-striatal pathway in multiple system atrophy and Parkinson disease. Mov Disord. 2016;31:325-34.⁾
	- Hyperintense signal in axial T2-weighted sequences, with atrophy of the putamen⁽¹³13 Massey LA, Micallef C, Paviour DC, et al. Conventional magnetic resonance imaging in confirmed progressive supranuclear palsy and multiple system atrophy. Mov Disord. 2012;27:1754-62. 14 Quattrone A, Nicoletti G, Messina D, et al. MR imaging index for differentiation of progressive supranuclear palsy from Parkinson disease and the Parkinson variant of multiple system atrophy. Radiology. 2008;246:214-21.^-¹⁵15 Paviour DC, Price SL, Jahanshahi M, et al. Regional brain volumes distinguish PSP, MSA-P, and PD: MRI-based clinico-radiological correlations. Mov Disord. 2006;21:989-96.⁾	- Moderate sensitivity, because they are not normally seen in the early stages of the disease⁽¹³13 Massey LA, Micallef C, Paviour DC, et al. Conventional magnetic resonance imaging in confirmed progressive supranuclear palsy and multiple system atrophy. Mov Disord. 2012;27:1754-62. 14 Quattrone A, Nicoletti G, Messina D, et al. MR imaging index for differentiation of progressive supranuclear palsy from Parkinson disease and the Parkinson variant of multiple system atrophy. Radiology. 2008;246:214-21.^-¹⁵15 Paviour DC, Price SL, Jahanshahi M, et al. Regional brain volumes distinguish PSP, MSA-P, and PD: MRI-based clinico-radiological correlations. Mov Disord. 2006;21:989-96.⁾	- Reduced FA and increased ADC in the pons, cerebellum, and middle cerebellar peduncles⁽⁴³43 Ito M, Watanabe H, Kawai Y, et al. Usefulness of combined fractional anisotropy and apparent diffusion coefficient values for detection of involvement in multiple system atrophy. J Neurol Neurosurg Psychiatry. 2007;78:722-8.^,⁵⁰50 Paviour DC, Thornton JS, Lees AJ, et al. Diffusion-weighted magnetic resonance imaging differentiates Parkinsonian variant of multiple-system atrophy from progressive supranuclear palsy. Mov Disord. 2007;22:68-74. 51 Yang H, Wang X, Liao W, et al. Application of diffusion tensor imaging in multiple system atrophy: the involvement of pontine transverse and longitudinal fibers. Int J Neurosci. 2015;125:18-24.^-⁵²52 Blain CRV, Barker GJ, Jarosz JM, et al. Measuring brain stem and cerebellar damage in parkinsonian syndromes using diffusion tensor MRI. Neurology. 2006;67:2199-205.⁾	- High sensitivity and specificity, especially in MSA-C. In conjunction with changes in the putamen, they increase the specificity consider-ably⁴³43 Ito M, Watanabe H, Kawai Y, et al. Usefulness of combined fractional anisotropy and apparent diffusion coefficient values for detection of involvement in multiple system atrophy. J Neurol Neurosurg Psychiatry. 2007;78:722-8.^,⁵⁰50 Paviour DC, Thornton JS, Lees AJ, et al. Diffusion-weighted magnetic resonance imaging differentiates Parkinsonian variant of multiple-system atrophy from progressive supranuclear palsy. Mov Disord. 2007;22:68-74. 51 Yang H, Wang X, Liao W, et al. Application of diffusion tensor imaging in multiple system atrophy: the involvement of pontine transverse and longitudinal fibers. Int J Neurosci. 2015;125:18-24.^-⁵²52 Blain CRV, Barker GJ, Jarosz JM, et al. Measuring brain stem and cerebellar damage in parkinsonian syndromes using diffusion tensor MRI. Neurology. 2006;67:2199-205.⁾
	- Atrophy of the cerebellar hemispheres and the middle cerebellar peduncles⁽¹³13 Massey LA, Micallef C, Paviour DC, et al. Conventional magnetic resonance imaging in confirmed progressive supranuclear palsy and multiple system atrophy. Mov Disord. 2012;27:1754-62. 14 Quattrone A, Nicoletti G, Messina D, et al. MR imaging index for differentiation of progressive supranuclear palsy from Parkinson disease and the Parkinson variant of multiple system atrophy. Radiology. 2008;246:214-21.^-¹⁵15 Paviour DC, Price SL, Jahanshahi M, et al. Regional brain volumes distinguish PSP, MSA-P, and PD: MRI-based clinico-radiological correlations. Mov Disord. 2006;21:989-96.⁾			- Diffusion measures, taken together with conventional MRI measures, present high accuracy in the differential diagnosis with PD⁽⁵³53 Nair SR, Tan LK, Mohd Ramli N, et al. A decision tree for differentiating multiple system atrophy from Parkinson's disease using 3-T MR imaging. Eur Radiol. 2013;23:1459-66.⁾
PSP	- Hummingbird or penguin sign in the sagittal plane⁽¹³13 Massey LA, Micallef C, Paviour DC, et al. Conventional magnetic resonance imaging in confirmed progressive supranuclear palsy and multiple system atrophy. Mov Disord. 2012;27:1754-62. 14 Quattrone A, Nicoletti G, Messina D, et al. MR imaging index for differentiation of progressive supranuclear palsy from Parkinson disease and the Parkinson variant of multiple system atrophy. Radiology. 2008;246:214-21.^-¹⁵15 Paviour DC, Price SL, Jahanshahi M, et al. Regional brain volumes distinguish PSP, MSA-P, and PD: MRI-based clinico-radiological correlations. Mov Disord. 2006;21:989-96.⁾	- All have very high specificity, al-though they might not be seen in the early stages⁽¹³13 Massey LA, Micallef C, Paviour DC, et al. Conventional magnetic resonance imaging in confirmed progressive supranuclear palsy and multiple system atrophy. Mov Disord. 2012;27:1754-62. 14 Quattrone A, Nicoletti G, Messina D, et al. MR imaging index for differentiation of progressive supranuclear palsy from Parkinson disease and the Parkinson variant of multiple system atrophy. Radiology. 2008;246:214-21.^-¹⁵15 Paviour DC, Price SL, Jahanshahi M, et al. Regional brain volumes distinguish PSP, MSA-P, and PD: MRI-based clinico-radiological correlations. Mov Disord. 2006;21:989-96.⁾	- Reduced FA in the midbrain and superior cerebellar peduncles⁽¹⁶16 Rizzo G, Martinelli P, Manners D, et al. Diffusion-weighted brain imaging study of patients with clinical diagnosis of corticobasal degeneration, progressive supranuclear palsy and Parkinson's disease. Brain. 2008;131(Pt 10):2690-700.^,⁴⁹49 Nicoletti G, Tonon C, Lodi R, et al. Apparent diffusion coefficient of the superior cerebellar peduncle differentiates progressive supranuclear palsy from Parkinson's disease. Mov Disord. 2008;23:2370-6.^,⁵²52 Blain CRV, Barker GJ, Jarosz JM, et al. Measuring brain stem and cerebellar damage in parkinsonian syndromes using diffusion tensor MRI. Neurology. 2006;67:2199-205.⁾	- High sensitivity and specificity⁽¹⁶16 Rizzo G, Martinelli P, Manners D, et al. Diffusion-weighted brain imaging study of patients with clinical diagnosis of corticobasal degeneration, progressive supranuclear palsy and Parkinson's disease. Brain. 2008;131(Pt 10):2690-700.^,⁴⁹49 Nicoletti G, Tonon C, Lodi R, et al. Apparent diffusion coefficient of the superior cerebellar peduncle differentiates progressive supranuclear palsy from Parkinson's disease. Mov Disord. 2008;23:2370-6.^,⁵²52 Blain CRV, Barker GJ, Jarosz JM, et al. Measuring brain stem and cerebellar damage in parkinsonian syndromes using diffusion tensor MRI. Neurology. 2006;67:2199-205.⁾
	- Mickey Mouse sign in the axial plane⁽¹³13 Massey LA, Micallef C, Paviour DC, et al. Conventional magnetic resonance imaging in confirmed progressive supranuclear palsy and multiple system atrophy. Mov Disord. 2012;27:1754-62. 14 Quattrone A, Nicoletti G, Messina D, et al. MR imaging index for differentiation of progressive supranuclear palsy from Parkinson disease and the Parkinson variant of multiple system atrophy. Radiology. 2008;246:214-21.^-¹⁵15 Paviour DC, Price SL, Jahanshahi M, et al. Regional brain volumes distinguish PSP, MSA-P, and PD: MRI-based clinico-radiological correlations. Mov Disord. 2006;21:989-96.⁾		- Reduced FA in the globus pallidus and caudate nucleus⁽⁴⁷47 Tsukamoto K, Matsusue E, Kanasaki Y, et al. Significance of apparent diffusion coefficient measurement for the differential diagnosis of multiple system atrophy, progressive supranuclear palsy, and Parkinson's disease: evaluation by 3.0-T MR imaging. Neuroradiology. 2012;54:947-55.^,⁴⁹49 Nicoletti G, Tonon C, Lodi R, et al. Apparent diffusion coefficient of the superior cerebellar peduncle differentiates progressive supranuclear palsy from Parkinson's disease. Mov Disord. 2008;23:2370-6.^,⁵⁰50 Paviour DC, Thornton JS, Lees AJ, et al. Diffusion-weighted magnetic resonance imaging differentiates Parkinsonian variant of multiple-system atrophy from progressive supranuclear palsy. Mov Disord. 2007;22:68-74.^,⁵⁴54 Focke NK, Helms G, Pantel PM, et al. Differentiation of typical and atypical Parkinson syndromes by quantitative MR imaging. AJNR Am J Neuroradiol. 2011;32:2087-92.⁾	- Can facilitate the differential diag-nosis but have not been widely studied⁽⁴⁷47 Tsukamoto K, Matsusue E, Kanasaki Y, et al. Significance of apparent diffusion coefficient measurement for the differential diagnosis of multiple system atrophy, progressive supranuclear palsy, and Parkinson's disease: evaluation by 3.0-T MR imaging. Neuroradiology. 2012;54:947-55.^,⁴⁹49 Nicoletti G, Tonon C, Lodi R, et al. Apparent diffusion coefficient of the superior cerebellar peduncle differentiates progressive supranuclear palsy from Parkinson's disease. Mov Disord. 2008;23:2370-6.^,⁵⁰50 Paviour DC, Thornton JS, Lees AJ, et al. Diffusion-weighted magnetic resonance imaging differentiates Parkinsonian variant of multiple-system atrophy from progressive supranuclear palsy. Mov Disord. 2007;22:68-74.^,⁵⁴54 Focke NK, Helms G, Pantel PM, et al. Differentiation of typical and atypical Parkinson syndromes by quantitative MR imaging. AJNR Am J Neuroradiol. 2011;32:2087-92.⁾
	- Atrophy of midbrain and superior cerebellar peduncles⁽¹³13 Massey LA, Micallef C, Paviour DC, et al. Conventional magnetic resonance imaging in confirmed progressive supranuclear palsy and multiple system atrophy. Mov Disord. 2012;27:1754-62. 14 Quattrone A, Nicoletti G, Messina D, et al. MR imaging index for differentiation of progressive supranuclear palsy from Parkinson disease and the Parkinson variant of multiple system atrophy. Radiology. 2008;246:214-21.^-¹⁵15 Paviour DC, Price SL, Jahanshahi M, et al. Regional brain volumes distinguish PSP, MSA-P, and PD: MRI-based clinico-radiological correlations. Mov Disord. 2006;21:989-96.⁾
CBD	- Asymmetric atrophy of the parietal lobes⁽¹⁶16 Rizzo G, Martinelli P, Manners D, et al. Diffusion-weighted brain imaging study of patients with clinical diagnosis of corticobasal degeneration, progressive supranuclear palsy and Parkinson's disease. Brain. 2008;131(Pt 10):2690-700.⁾	- Low specificity and sensitivity⁽¹⁶16 Rizzo G, Martinelli P, Manners D, et al. Diffusion-weighted brain imaging study of patients with clinical diagnosis of corticobasal degeneration, progressive supranuclear palsy and Parkinson's disease. Brain. 2008;131(Pt 10):2690-700.⁾	- Reduced FA and increased ADC in the corpus callosum and frontal lobes, mainly in the corticospinal tract contralateral to the symptomatic side⁽¹⁶16 Rizzo G, Martinelli P, Manners D, et al. Diffusion-weighted brain imaging study of patients with clinical diagnosis of corticobasal degeneration, progressive supranuclear palsy and Parkinson's disease. Brain. 2008;131(Pt 10):2690-700.^,⁵⁵55 Boelmans K, Kaufmann J, Bodammer N, et al. Involvement of motor pathways in corticobasal syndrome detected by diffusion tensor tractography. Mov Disord. 2009;24:168-75.⁾	- Low sensitivity and specificity but can be seen in the early stages, even in the absence of atrophy⁽¹⁶16 Rizzo G, Martinelli P, Manners D, et al. Diffusion-weighted brain imaging study of patients with clinical diagnosis of corticobasal degeneration, progressive supranuclear palsy and Parkinson's disease. Brain. 2008;131(Pt 10):2690-700.^,⁵⁵55 Boelmans K, Kaufmann J, Bodammer N, et al. Involvement of motor pathways in corticobasal syndrome detected by diffusion tensor tractography. Mov Disord. 2009;24:168-75.⁾
CBD	- Thinning of the corpus callosum⁽¹⁶16 Rizzo G, Martinelli P, Manners D, et al. Diffusion-weighted brain imaging study of patients with clinical diagnosis of corticobasal degeneration, progressive supranuclear palsy and Parkinson's disease. Brain. 2008;131(Pt 10):2690-700.⁾		- Increased ADC in the motor thala-mus, precentral gyrus, and postcentral gyrus⁽⁵⁶56 Erbetta A, Mandelli ML, Savoiardo M, et al. Diffusion tensor imaging shows different topographic involvement of the thalamus in progressive supranuclear palsy and corticobasal degeneration. AJNR Am J Neuroradiol. 2009;30:1482-7.⁾	- Rarely studied but can facilitate the differential diagnosis with PSP, especially if asymmetric⁽⁵⁶56 Erbetta A, Mandelli ML, Savoiardo M, et al. Diffusion tensor imaging shows different topographic involvement of the thalamus in progressive supranuclear palsy and corticobasal degeneration. AJNR Am J Neuroradiol. 2009;30:1482-7.⁾

[1] Mailing address: Dr. Romulo Varela de Oliveira. Hospital Universitário Pedro Ernesto – Serviço de Imagem. Boulevard 28 de Setembro, 77, Vila Isabel. Rio de Janeiro, RJ, Brazil, 20551-030. E-mail: romulovarella@hotmail.com.

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The role of diffusion magnetic resonance imaging in Parkinson's disease and in the differential diagnosis with atypical parkinsonism

Abstract