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

person Romulo Varella de Oliveira

schoolFull 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, BrazilschoolUniversidade 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, BrazilschoolHospital Universitário Pedro Ernesto, Clínica Alta Excelência Diagnóstica, Rio de Janeiro, RJ, Brazil

person João Santos Pereira

schoolPhD, 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, BrazilschoolUniversidade 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⁽¹²⁾	- Quite high specificity, although quite low sensitivity, found only in the more advanced stages⁽¹²⁾	- Reduced FA in the substantia nigra, more evident in the caudal portion⁽⁸^,¹⁰^,¹¹^,²¹^-²⁵⁾	- High specificity and sensitivity, even in the early stages of the disease, data more established in the literature⁽⁸^,¹⁰^,¹¹^,²¹^-²⁵⁾
			- Reduced FA in the frontal lobes (motor, premotor and supplemental motor cortices)⁽¹⁸^,²¹^,²⁷⁾	- Low specificity and sensitivity⁽¹⁸^,²¹^,²⁷⁾
			- Reduced FA in the striatum and cerebellar hemispheres⁽²⁸^,²⁹⁾	- Rarely studied but could be associated with specific signs of the disease⁽²⁸^,²⁹⁾
	- Diffuse cortical atrophy, mainly in the frontal lobes⁽¹²⁾	- Low sensitivity and specificity, occurs in the terminal phase⁽¹²⁾	- Reduced FA in the genu of the corpus callosum, cingulate gyrus, hip-pocampus, superior/inferior longitudinal fasciculi and inferior/uncinate fronto-occipital fasciculi⁽³⁰^-³⁶⁾	- Appears to be related to dementia in PD but warrants further study⁽³⁰^-³⁶⁾
			- Reduced FA in the dorsomedial thalamus and anterior cingulate gyrus⁽¹¹^,³¹^,³⁷⁾	- Could be related to depression, although it has not been extensively studied⁽¹¹^,³¹^,³⁷⁾
			- Reduced FA in the olfactory bulbs, white matter adjacent to the primary olfactory cortex, and gyrus rectus⁽³⁸^,⁴⁰^,⁴¹⁾	- Can be present in individuals with altered olfactory tests, with the potential to identify patients in the premotor phase of PD⁽³⁸^,⁴⁰^,⁴¹⁾
MSA	- Hot cross bun sign in axial T2-weighted sequences, with atrophy of the pons⁽¹³^-¹⁵⁾	- All have good specificity but can be seen in other conditions⁽¹³^-¹⁵⁾	- Reduced FA and increased ADC in the putamen⁽⁴³^-⁴⁸⁾	- High sensitivity and specificity, especially in MSA-P, but can also occur in PSP⁽⁴³^-⁴⁸⁾
	- Hyperintense signal in axial T2-weighted sequences, with atrophy of the putamen⁽¹³^-¹⁵⁾	- Moderate sensitivity, because they are not normally seen in the early stages of the disease⁽¹³^-¹⁵⁾	- Reduced FA and increased ADC in the pons, cerebellum, and middle cerebellar peduncles⁽⁴³^,⁵⁰^-⁵²⁾	- High sensitivity and specificity, especially in MSA-C. In conjunction with changes in the putamen, they increase the specificity consider-ably⁴³^,⁵⁰^-⁵²⁾
	- Atrophy of the cerebellar hemispheres and the middle cerebellar peduncles⁽¹³^-¹⁵⁾			- Diffusion measures, taken together with conventional MRI measures, present high accuracy in the differential diagnosis with PD⁽⁵³⁾
PSP	- Hummingbird or penguin sign in the sagittal plane⁽¹³^-¹⁵⁾	- All have very high specificity, al-though they might not be seen in the early stages⁽¹³^-¹⁵⁾	- Reduced FA in the midbrain and superior cerebellar peduncles⁽¹⁶^,⁴⁹^,⁵²⁾	- High sensitivity and specificity⁽¹⁶^,⁴⁹^,⁵²⁾
	- Mickey Mouse sign in the axial plane⁽¹³^-¹⁵⁾		- Reduced FA in the globus pallidus and caudate nucleus⁽⁴⁷^,⁴⁹^,⁵⁰^,⁵⁴⁾	- Can facilitate the differential diag-nosis but have not been widely studied⁽⁴⁷^,⁴⁹^,⁵⁰^,⁵⁴⁾
	- Atrophy of midbrain and superior cerebellar peduncles⁽¹³^-¹⁵⁾
CBD	- Asymmetric atrophy of the parietal lobes⁽¹⁶⁾	- Low specificity and sensitivity⁽¹⁶⁾	- Reduced FA and increased ADC in the corpus callosum and frontal lobes, mainly in the corticospinal tract contralateral to the symptomatic side⁽¹⁶^,⁵⁵⁾	- Low sensitivity and specificity but can be seen in the early stages, even in the absence of atrophy⁽¹⁶^,⁵⁵⁾
CBD	- Thinning of the corpus callosum⁽¹⁶⁾	- Low specificity and sensitivity⁽¹⁶⁾	- Increased ADC in the motor thala-mus, precentral gyrus, and postcentral gyrus⁽⁵⁶⁾	- Rarely studied but can facilitate the differential diagnosis with PSP, especially if asymmetric⁽⁵⁶⁾

[TFN1] PD, Parkinson's disease; MSA, multiple system atrophy; PSP, progressive supranuclear palsy; CBD, corticobasal degeneration; FA, fractional anisotropy; ADC, apparent diffusion coefficient; MSA-P, MSA with a predominance of parkinsonian symptoms; MSA-C, MSA with a predominance of cerebellar symptoms.