Abstract
This study focused on the substantia nigra (SN) in Parkinson’s disease (PD). We measured its area and volume, mean diffusivity (MD), fractional anisotropy (FA) and iron concentration in early and late PD and correlated the values with clinical scores. Twenty-two early PD (EPD), 20 late PD (LPD) and 20 healthy subjects (age 64.7 ± 4.9, 60.5 ± 6.1, and 61 ± 7.2 years, respectively) underwent 1.5 T MR imaging with double-TI-IR T1-weighted, T2*-weighted and diffusion tensor imaging scans. Relative SN area, MD, FA and R2* were measured in ROIs traced on SN. Correlation with Unified Parkinson Disease Rating Scale (UPDRS) scores was assessed. In LPD, the SN area was significantly reduced with respect to EPD (p = 0.04) and control subjects (p < 0.001). In EPD, the SN area was also significantly smaller than in controls (p = 0.006). Similarly, the SN volume significantly differed between LPD and controls (p = 0.001) and between EPD and LPD (p = 0.049), while no significant differences were found between controls and EPD. Both SN area (r = 0.47, p = 0.004) and volume (r = 0.46, p = 0.005) correlated with UPDRS scores. At 1.5 T, SN morphological measurements were sensitive to early PD changes and able to track the disease progression, while MD and FA measures and relaxometry did not provide significant results.
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References
Halliday G, Lees A, Stern M (2011) Milestones in Parkinson’s disease—clinical and pathologic features. Mov Disord 26:1015–1021
Seppi K, Poewe W (2010) Brain magnetic resonance imaging techniques in the diagnosis of parkinsonian syndromes. Neuroimaging Clin N Am 20:29–55
Dickson DW, Braak H, Duda JE et al (2009) Neuropathological assessment of Parkinson’s disease: refining the diagnostic criteria. Lancet Neurol 8:1150–1157
Chahine LM, Stern MB (2011) Diagnostic markers for Parkinson’s disease. Curr Opin Neurol 24:309–317
Wilson JM, Levey AI, Rajput A et al (1996) Differential changes in neurochemical markers of striatal dopamine nerve terminals in idiopathic Parkinson’s disease. Neurology 47:718–726
Innis RB, Seibyl JP, Scanley BE et al (1993) Single photon emission computed tomographic imaging demonstrates loss of striatal dopamine transporters in Parkinson disease. Proc Natl Acad Sci USA 90:11965–11969
Leenders KL, Oertel WH (2001) Parkinson’s disease: clinical signs and symptoms, neural mechanisms, positron emission tomography, and therapeutic interventions. Neural Plast 8:99–110
Thobois S, Jahanshahi M, Pinto S, Frackowiak R, Limousin-Dowsey P (2004) PET and SPECT functional imaging studies in Parkinsonian syndromes: from the lesion to its consequences. Neuroimage 23:1–16
Hutchinson M, Raff U (2008) Detection of Parkinson’s disease by MRI: spin–lattice distribution imaging. Mov Disord 23:1991–1997
Minati L, Grisoli M, Carella F, De Simone T, Bruzzone MG, Savoiardo M (2007) Imaging degeneration of the substantia nigra in Parkinson disease with inversion-recovery MR imaging. AJNR Am J Neuroradiol 28:309–313
Vaillancourt DE, Spraker MB, Prodoehl J et al (2009) High-resolution diffusion tensor imaging in the substantia nigra of de novo Parkinson disease. Neurology 72:1378–1384
Sian-Hülsmann J, Mandel S, Youdim MB, Riederer P (2011) The relevance of iron in the pathogenesis of Parkinson’s disease. J Neurochem 118(6):939–957
Carroll CB, Zeissler ML, Chadborn N et al (2011) Changes in iron-regulatory gene expression occur in human cell culture models of Parkinson’s disease. Neurochem Int 59:73–80
Martin WR, Wieler M, Gee M (2008) Midbrain iron content in early Parkinson disease: a potential biomarker of disease status. Neurology 70:1411–1417
Péran P, Cherubini A, Assogna F et al (2010) Magnetic resonance imaging markers of Parkinson’s disease nigrostriatal signature. Brain 133:3423–3433
Cherubini A, Péran P, Caltagirone C, Sabatini U, Spalletta G (2009) Aging of subcortical nuclei: microstructural, mineralization and atrophy modifications measured in vivo using MRI. Neuroimage 48:29–36
Hutchinson M, Raff U (1999) Parkinson’s disease: a novel MRI method for determining structural changes in the substantia nigra. J Neurol Neurosurg Psychiatry 69:815–818
Hughes AJ, Daniel SE, Kilford L, Lees AJ (1992) Accuracy of clinical diagnosis of idiopathic Parkinson’s disease: a clinico-pathological study of 100 cases. J Neurol Neurosurg Psychiatry 55:181–184
Hoehn MM, Yahr MD (1967) Parkinsonism: onset, progression and mortality. Neurology 17:427–442
Brazzelli M, Capitani E, Della Sala S, Spinnler H, Zuffi M (1994) A neuropsychological instrument adding to the description of patients with suspected cortical dementia: the Milan overall dementia assessment. J Neurol Neurosurg Psychiatry 57:1510–1517
Romito LM, Contarino MF, Vanacore N, Bentivoglio AR, Scerrati M, Albanese A (2009) Replacement of dopaminergic medication with subthalamic nucleus stimulation in Parkinson’s disease: long-term observation. Mov Disord 24:557–563
Fahn S, Elton RL (1987) Members of the UPDRS Development Committee. Unified Parkinsons disease rating scale. In: Fahn S, Marsden CD, Calne D, Goldstein M (eds) Recent developments in Parkinsons disease, 2nd edn. Macmillan Healthcare Information, Florham Park, pp 153–163
Raff U, Hutchinson M, Rojas GM, Huete I (2006) Inversion recovery MRI in idiopathic Parkinson disease is a very sensitive tool to assess neurodegeneration in the substantia nigra: preliminary investigation. Acad Radiol 13:721–727
Basser PJ, Pierpaoli C (1996) Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. J Magn Reson B 111:209–219
Hallgren B, Sourander P (1958) The effect of age on the non-haemin iron in the human brain. J Neurochem 3:41–51
Aquino D, Bizzi A, Grisoli M, Garavaglia B, Bruzzone MG, Nardocci N (2009) Age-related iron deposition in the basal ganglia: quantitative analysis in healthy subjects. Radiology 252:165–172
Gattellaro G, Minati L, Grisoli M, Mariani C, Carella F, Bruzzone MG (2009) White matter involvement in idiopathic Parkinson disease: a diffusion tensor imaging study. AJNR Am J Neuroradiol 30:1222–1226
Du G, Lewis MM, Styner M, Shaffer ML, Sen S, Yang QX, Huang X (2011) Combined R2* and diffusion tensor imaging changes in the substantia nigra in Parkinson’s disease. Mov Disord 26:1627–1632
Meijer FJA, Bloem RB, Mahlknecht P, Seppi K, Goraj B (2013) Update on diffusion MRI in Parkinson’s disease and atypical parkinsonism. J Neurol Sci 332(2013):21–29
Chan LL, Rumpel H, Yap K, Lee E, Loo HV, Ho GL et al (2007) Case control study of diffusion tensor imaging in Parkinson’s disease. J Neurol Neurosurg Psychiatry 78(12):1383–1386
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This work was funded by the Italian Ministry of Health, RF 110 (ex art 56), year 2010.
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Aquino, D., Contarino, V., Albanese, A. et al. Substantia nigra in Parkinson’s disease: a multimodal MRI comparison between early and advanced stages of the disease. Neurol Sci 35, 753–758 (2014). https://doi.org/10.1007/s10072-013-1595-2
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DOI: https://doi.org/10.1007/s10072-013-1595-2