Eur Radiol DOI 10.1007/s00330-015-3678-3

NEURO

Investigation of Apparent Diffusion Coefficient from Ultra-high b-Values in Parkinson’s Disease Ling Xueying & Zhang Zhongping & Zhao Zhoushe & Guo Li & Tang Yongjin & Shi Changzheng & Zhou Zhifeng & Chen Peihao & Xu Hao & Huang Li

Received: 26 November 2014 / Revised: 9 February 2015 / Accepted: 17 February 2015 # European Society of Radiology 2015

Abstract Objectives To assess brain damage in Parkinson’s disease (PD) based on apparent diffusion coefficient (ADC) data obtained from ultra-high b-values. Methods Eighteen PD patients and 18 controls received diffusion-weighted imaging (DWI) with standard b-values (0, 1,000 s/mm2) and 15 b-values (0–5,000 s/mm2). Standard ADC (ADCst) maps were calculated from standard b-values, while maps of pure diffusion coefficients (D), pseudodiffusion coefficients (D*), and ultra-high ADCs (ADCuh) were calculated from the 15 b-values using a tri-component model. In this model, D and D* values were quantified with a bi-exponential equation using b-values less than 2,000 s/mm2, while ADCuh was quantified by fitting the signals at ultra-high b-values (2,000–5,000 s/mm2) to the mono-exponential equation. ADCst, ADCuh, D, and D* of the globus pallidus (GP), putamen (P), and substantia nigra (SN) were compared between PD patients and normal control subjects. Results ADCuh of the GP, P, and SN was significantly lower in PD patients than those in control subjects (P0.05).

L. Xueying : T. Yongjin : S. Changzheng : Z. Zhifeng : C. Peihao : X. Hao : H. Li (*) Department of Medical Imaging Center, the First Affiliated Hospital, Jinan University, Huangpu West Road, Guangzhou, China e-mail: [email protected] Z. Zhongping : Z. Zhoushe General Electric Healthcare, Shanghai, China G. Li Department of Neurology, the First Affiliated Hospital, Jinan University, Guangzhou, China

Conclusions ADCuh may be a useful measurement for evaluating brain damage in PD patients. Key Points • DWI with ultra-high b-values may provide new insight into Parkinson’s disease pathology • ADC calculated using ultra-high b-values is different between PD and controls • ADCuh may be associated with water transportation by aquaporins Keywords Diffusion . Parkinson’s disease . Globus pallidus . Putamen . Substantia nigra

Abbreviations and acronyms 3D BRAVO three-dimensional brain volume imaging ADC apparent diffusion coefficient ADCst ADC calculated using standard b-values ADCuh ADC calculated using ultra-high b-values BA Bland–Altman D pure diffusion coefficient * D pseudo-diffusion coefficient DWI diffusion weighted imaging ECS extracellular compartment space FOV field of view FSE axial fast spin-echo HY Hoehn and Yahr staging scale ICC intraclass correlation LOA limits of agreement MD mean diffusivity MSA multiple system atrophy MSA-C MSA with predominant cerebellar dysfunction MSA-P MSA with predominant Parkinsonism PD Parkinson’s disease ROI region of interest

Eur Radiol

TE TR T2FLAIR T2WI UPDRS SD

echo time repetition time T2 fluid attenuation inversion recovery T2-weighted imaging Unified Parkinson’s Disease Rating Scale standard deviation

Introduction Diffusion-weighted imaging (DWI) has been widely used to measure the random motion of water molecules in biological tissues, and the apparent diffusion coefficient (ADC) is the major parameter for quantifying water diffusion [1, 2]. ADC values are often estimated by fitting a series of images acquired with different diffusion weightings (b-values) using a mono-exponential model [3, 4]. However, other physiological changes in vivo, such as vascular flow and tubular flow, can impact ADC estimates. Therefore, the ADC does not represent pure water diffusion (D) in biological tissues. Intra-voxel incoherent motion (IVIM) DWI has been shown to distinguish pure water diffusion (D) from pseudodiffusion or blood perfusion (D*) in different lesions [5–7]. IVIM imaging is based on a bi-component model with a slow diffusion component (true water diffusion) and a fast diffusion component (blood perfusion) in each voxel [5]. Unlike the two standard b-values used in the mono-exponential model, multiple b-values, including low b-values (200 s/mm2), are required in IVIM-based DWI for distinguishing the fast and slow diffusion components [5]. This is owing to the fact that the signal from blood perfusion with a rapid flow disappears with b-values greater than 200 s/ mm2, while true water diffusion with a slower flow mainly contributes to the signal acquired with b-values larger than 200 s/mm2 [8]. The high b-values for measuring true water diffusion usually range from 200–1,000 s/mm2, and can vary in different tissues [9, 10]. However, the exchange effects between the fast and slow diffusion pools and membrane permeability are not taken into account in this bi-component model [11]. There is also evidence that ADC may be related to expression of aquaporin-4 (AQP4) in the membrane, which is located mainly in astrocytic foot processes, particularly at the borders between the brain parenchyma and major fluid compartments [12, 13]. Recently, ultra-high b-values were reported to improve the diagnostic performance of DWI in the detection of prostate cancer and high grade gliomas [2, 14]. Furthermore, the ADC of meningiomas at a b-value of 2,000 s/mm2 was reported to be lower than those at a b-value of 1,000 s/mm2. Although the reason for this difference is unknown, the fraction of the slower diffusion component may be larger in brain tumours and surrounding oedema than in normal contralateral brain

tissue [15]. Therefore, we hypothesize that D and D* calculated by IVIM, and ADC calculated from ultra-high b-values, might be useful in evaluating brain damage in Parkinson’s disease (PD) patients. As ADC data calculated from standard b-values (0, 1,000 s/mm2) do not consistently differentiate between PD and controls [16–18], we used a tri-component model to calculate D, D*, and an ultra-high ADC (ADCuh). In this model, we presumed that b-values (0–5,000 s/mm2) may exhibit three diffusion components in each voxel, being mostly influenced by blood perfusion, true water diffusion, and the permeability of AQPs in the cell membrane.

Methods This prospective study was approved by the institutional review board at the First Affiliated Hospital of Jinan University, and was in compliance with national legislation and the Declaration of Helsinki guidelines. Informed consent was obtained from all participants. Study population Twenty PD patients and 18 control subjects who underwent conventional MRI and DWI at our hospital between March 2013 and January 2014 were included in this study. Inclusion criteria for PD patients were as follows: (i) fulfilment of the PD diagnostic criteria from the UK Parkinson’s Disease Society Brain Bank [19]; (ii) no history of other neurological or psychiatric diseases, and no MRI evidence of focal brain lesions; (iii) absence of diabetes mellitus; and (iv) no history of ocular disease. The severity of PD was assessed by using the Unified PD Rating Scale-III (UPDRS-III) motor score and modified Hoehn and Yahr staging scale (HY) [20, 21]. All clinical examinations were performed by a neurologist who specialized in movement disorders. Inclusion criteria for control subjects were as follows: (i) absence of diabetes mellitus; (ii) no history of neurological or psychiatric diseases; (iii) no MRI evidence of focal brain lesions; and (iv) no history of ocular disease. Exclusion criteria for both groups were as follows: (i) aged

Investigation of Apparent Diffusion Coefficient from Ultra-high b-Values in Parkinson's Disease.

To assess brain damage in Parkinson's disease (PD) based on apparent diffusion coefficient (ADC) data obtained from ultra-high b-values...
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