Skip to main content
Erschienen in: Neuroradiology 12/2017

06.10.2017 | Functional Neuroradiology

Pool size ratio of the substantia nigra in Parkinson’s disease derived from two different quantitative magnetization transfer approaches

verfasst von: Paula Trujillo, Paul E. Summers, Alex K. Smith, Seth A. Smith, Luca T. Mainardi, Sergio Cerutti, Daniel O. Claassen, Antonella Costa

Erschienen in: Neuroradiology | Ausgabe 12/2017

Einloggen, um Zugang zu erhalten

Abstract

Purpose

We sought to measure quantitative magnetization transfer (qMT) properties of the substantia nigra pars compacta (SNc) in patients with Parkinson’s disease (PD) and healthy controls (HCs) using a full qMT analysis and determine whether a rapid single-point measurement yields equivalent results for pool size ratio (PSR).

Methods

Sixteen different MT-prepared MRI scans were obtained at 3 T from 16 PD patients and eight HCs, along with B1, B0, and relaxation time maps. Maps of PSR, free and macromolecular pool transverse relaxation times (\( {T}_2^f \), \( {T}_2^m \)) and rate of MT exchange between pools (k mf ) were generated using a full qMT model. PSR maps were also generated using a single-point qMT model requiring just two MT-prepared images. qMT parameter values of the SNc, red nucleus, cerebral crus, and gray matter were compared between groups and methods.

Results

PSR of the SNc was the only qMT parameter to differ significantly between groups (p < 0.05). PSR measured via single-point analysis was less variable than with the full MT model, provided slightly better differentiation of PD patients from HCs (area under curve 0.77 vs. 0.75) with sensitivity of 0.75 and specificity of 0.87, and was better than transverse relaxation time in distinguishing PD patients from HCs (area under curve 0.71, sensitivity 0.87, and specificity 0.50).

Conclusion

The increased PSR observed in the SNc of PD patients may provide a novel biomarker of PD, possibly associated with an increased macromolecular content. Single-point PSR mapping with reduced variability and shorter scan times relative to the full qMT model appears clinically feasible.
Anhänge
Nur mit Berechtigung zugänglich
Literatur
1.
Zurück zum Zitat Zecca L, Fariello R, Riederer P, Sulzer D, Gatti A, Tampellini D (2002) The absolute concentration of nigral neuromelanin, assayed by a new sensitive method, increases throughout the life and is dramatically decreased in Parkinson’s disease. FEBS Lett 510:216–220CrossRefPubMed Zecca L, Fariello R, Riederer P, Sulzer D, Gatti A, Tampellini D (2002) The absolute concentration of nigral neuromelanin, assayed by a new sensitive method, increases throughout the life and is dramatically decreased in Parkinson’s disease. FEBS Lett 510:216–220CrossRefPubMed
2.
Zurück zum Zitat Fearnley J, Lees A (1991) Ageing and Parkinson’s disease: substantia nigra regional selectivity. Brain 114:2283–2301CrossRefPubMed Fearnley J, Lees A (1991) Ageing and Parkinson’s disease: substantia nigra regional selectivity. Brain 114:2283–2301CrossRefPubMed
4.
Zurück zum Zitat Dauer W, Przedborski S (2003) Parkinson’s disease: mechanisms and models. Neuron 39:889–909CrossRefPubMed Dauer W, Przedborski S (2003) Parkinson’s disease: mechanisms and models. Neuron 39:889–909CrossRefPubMed
8.
Zurück zum Zitat Miyoshi F, Ogawa T, Kitao S, Kitayama M, Shinohara Y, Takasugi M, Fujii S, Kaminou T (2013) Evaluation of Parkinson disease and Alzheimer disease with the use of neuromelanin MR imaging and 123I-metaiodobenzylguanidine scintigraphy. AJNR Am J Neuroradiol 34:2113–2118. https://doi.org/10.3174/ajnr.A3567 CrossRefPubMed Miyoshi F, Ogawa T, Kitao S, Kitayama M, Shinohara Y, Takasugi M, Fujii S, Kaminou T (2013) Evaluation of Parkinson disease and Alzheimer disease with the use of neuromelanin MR imaging and 123I-metaiodobenzylguanidine scintigraphy. AJNR Am J Neuroradiol 34:2113–2118. https://​doi.​org/​10.​3174/​ajnr.​A3567 CrossRefPubMed
10.
Zurück zum Zitat Reimão S, Pita Lobo P, Neutel D, Correia Guedes L, Coelho M, Rosa M, Ferreira J, Abreu D, Gonçalves N, Morgado C, Nunes RG, Campos J, Ferreira JJ (2015) Substantia nigra neuromelanin magnetic resonance imaging in de novo Parkinson’s disease patients. Eur J Neurol 22:540–546. https://doi.org/10.1111/ene.12613 CrossRefPubMed Reimão S, Pita Lobo P, Neutel D, Correia Guedes L, Coelho M, Rosa M, Ferreira J, Abreu D, Gonçalves N, Morgado C, Nunes RG, Campos J, Ferreira JJ (2015) Substantia nigra neuromelanin magnetic resonance imaging in de novo Parkinson’s disease patients. Eur J Neurol 22:540–546. https://​doi.​org/​10.​1111/​ene.​12613 CrossRefPubMed
17.
Zurück zum Zitat Dixon WT, Engels H, Castillo M, Sardashti M (1990) Incidental magnetization transfer contrast in standard multislice imaging. Magn Reson Imaging 8:417–422CrossRefPubMed Dixon WT, Engels H, Castillo M, Sardashti M (1990) Incidental magnetization transfer contrast in standard multislice imaging. Magn Reson Imaging 8:417–422CrossRefPubMed
18.
Zurück zum Zitat Nakane T, Nihashi T, Kawai H, Naganawa S (2008) Visualization of neuromelanin in the substantia nigra and locus ceruleus at 1.5T using a 3D-gradient echo sequence with magnetization transfer contrast. Magn Reson Med Sci 7:205–210CrossRefPubMed Nakane T, Nihashi T, Kawai H, Naganawa S (2008) Visualization of neuromelanin in the substantia nigra and locus ceruleus at 1.5T using a 3D-gradient echo sequence with magnetization transfer contrast. Magn Reson Med Sci 7:205–210CrossRefPubMed
19.
Zurück zum Zitat Schwarz ST, Bajaj N, Morgan PS, Reid S, Gowland P, Auer DP (2013) Magnetisation transfer contrast to enhance detection of neuromelanin loss at 3T in Parkinson’s disease. In: Proc. Intl. Soc. Mag. Reson. Med. p 2848 Schwarz ST, Bajaj N, Morgan PS, Reid S, Gowland P, Auer DP (2013) Magnetisation transfer contrast to enhance detection of neuromelanin loss at 3T in Parkinson’s disease. In: Proc. Intl. Soc. Mag. Reson. Med. p 2848
20.
Zurück zum Zitat Ogisu K, Kudo K, Sasaki M, Sakushima K, Yabe I, Sasaki H, Terae S, Nakanishi M, Shirato H (2013) 3D neuromelanin-sensitive magnetic resonance imaging with semi-automated volume measurement of the substantia nigra pars compacta for diagnosis of Parkinson’s disease. Neuroradiology 55:719–724. https://doi.org/10.1007/s00234-013-1171-8 CrossRefPubMed Ogisu K, Kudo K, Sasaki M, Sakushima K, Yabe I, Sasaki H, Terae S, Nakanishi M, Shirato H (2013) 3D neuromelanin-sensitive magnetic resonance imaging with semi-automated volume measurement of the substantia nigra pars compacta for diagnosis of Parkinson’s disease. Neuroradiology 55:719–724. https://​doi.​org/​10.​1007/​s00234-013-1171-8 CrossRefPubMed
24.
Zurück zum Zitat Thomas SD, Al-Kwifi O, Emery DJ, Wilman AH (2002) Application of magnetization transfer at 3.0 T in three-dimensional time-of-flight magnetic resonance angiography of the intracranial arteries. J Magn Reson Imaging 15:479–483CrossRefPubMed Thomas SD, Al-Kwifi O, Emery DJ, Wilman AH (2002) Application of magnetization transfer at 3.0 T in three-dimensional time-of-flight magnetic resonance angiography of the intracranial arteries. J Magn Reson Imaging 15:479–483CrossRefPubMed
25.
Zurück zum Zitat van Buchem MA (1999) Magnetization transfer: applications in neuroradiology. J Comput Assist Tomogr 23(Suppl 1):S9–18CrossRefPubMed van Buchem MA (1999) Magnetization transfer: applications in neuroradiology. J Comput Assist Tomogr 23(Suppl 1):S9–18CrossRefPubMed
29.
Zurück zum Zitat Eckert T, Sailer M, Kaufmann J, Schrader C, Peschel T, Bodammer N, Heinze HJ, Schoenfeld MA (2004) Differentiation of idiopathic Parkinson’s disease, multiple system atrophy, progressive supranuclear palsy, and healthy controls using magnetization transfer imaging. NeuroImage 21:229–235CrossRefPubMed Eckert T, Sailer M, Kaufmann J, Schrader C, Peschel T, Bodammer N, Heinze HJ, Schoenfeld MA (2004) Differentiation of idiopathic Parkinson’s disease, multiple system atrophy, progressive supranuclear palsy, and healthy controls using magnetization transfer imaging. NeuroImage 21:229–235CrossRefPubMed
32.
Zurück zum Zitat Sled JG, Pike GB (2001) Quantitative imaging of magnetization transfer exchange and relaxation properties in vivo using MRI. Magn Reson Med 46:923–931CrossRefPubMed Sled JG, Pike GB (2001) Quantitative imaging of magnetization transfer exchange and relaxation properties in vivo using MRI. Magn Reson Med 46:923–931CrossRefPubMed
42.
Zurück zum Zitat Skinner T, Glover G (1997) An extended two-point Dixon algorithm for calculating separate water, fat, and B0 images. Magn Reson Med 37:628–630CrossRefPubMed Skinner T, Glover G (1997) An extended two-point Dixon algorithm for calculating separate water, fat, and B0 images. Magn Reson Med 37:628–630CrossRefPubMed
43.
Zurück zum Zitat Yarnykh V (2007) Actual flip-angle imaging in the pulsed steady state: a method for rapid three-dimensional mapping of the transmitted radiofrequency field. Magn Reson Med 57:192–200CrossRefPubMed Yarnykh V (2007) Actual flip-angle imaging in the pulsed steady state: a method for rapid three-dimensional mapping of the transmitted radiofrequency field. Magn Reson Med 57:192–200CrossRefPubMed
44.
Zurück zum Zitat Fram EK, Herfkens RJ, Johnson GA, Glover GH, Karis JP, Shimakawa A, Perkins TG, Pelc NJ (1987) Rapid calculation of T1 using variable flip angle gradient refocused imaging. Magn Reson Imaging 5:201–208CrossRefPubMed Fram EK, Herfkens RJ, Johnson GA, Glover GH, Karis JP, Shimakawa A, Perkins TG, Pelc NJ (1987) Rapid calculation of T1 using variable flip angle gradient refocused imaging. Magn Reson Imaging 5:201–208CrossRefPubMed
45.
Zurück zum Zitat Jenkinson M, Smith S (2001) A global optimisation method for robust affine registration of brain images. Med Image Anal 5:143–156CrossRefPubMed Jenkinson M, Smith S (2001) A global optimisation method for robust affine registration of brain images. Med Image Anal 5:143–156CrossRefPubMed
46.
Zurück zum Zitat Henkelman RM, Huang X, Xiang QS, Stanisz GJ, Swanson SD, Bronskill MJ (1993) Quantitative interpretation of magnetization transfer. Magn Reson Med 29:759–766CrossRefPubMed Henkelman RM, Huang X, Xiang QS, Stanisz GJ, Swanson SD, Bronskill MJ (1993) Quantitative interpretation of magnetization transfer. Magn Reson Med 29:759–766CrossRefPubMed
49.
Zurück zum Zitat Vymazal J, Righini A, Brooks RA, Canesi M, Mariani C, Leonardi M, Pezzoli G (1999) T1 and T2 in the brain of healthy subjects, patients with Parkinson disease, and patients with multiple system atrophy: relation to iron content. Radiology 211:489–495CrossRefPubMed Vymazal J, Righini A, Brooks RA, Canesi M, Mariani C, Leonardi M, Pezzoli G (1999) T1 and T2 in the brain of healthy subjects, patients with Parkinson disease, and patients with multiple system atrophy: relation to iron content. Radiology 211:489–495CrossRefPubMed
50.
Zurück zum Zitat 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. Am J 309–313 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. Am J 309–313
51.
Zurück zum Zitat Dexter DT, Wells FR, Agid F, Agid Y, Lees AJ, Jenner P, Marsden CD (1987) Increased nigral iron content in postmortem parkinsonian brain. Lancet 2:1219–1220CrossRefPubMed Dexter DT, Wells FR, Agid F, Agid Y, Lees AJ, Jenner P, Marsden CD (1987) Increased nigral iron content in postmortem parkinsonian brain. Lancet 2:1219–1220CrossRefPubMed
52.
Zurück zum Zitat Dexter D, Wells F, Lees A, Agid F, Agid Y, Jenner P, Marsden C (1989) Increased nigral iron content and alterations in other metal ions occurring in brain in Parkinson’s disease. J Neurochem 52:1830–1836CrossRefPubMed Dexter D, Wells F, Lees A, Agid F, Agid Y, Jenner P, Marsden C (1989) Increased nigral iron content and alterations in other metal ions occurring in brain in Parkinson’s disease. J Neurochem 52:1830–1836CrossRefPubMed
53.
Zurück zum Zitat Faucheux B, Martin M, Hauw J, Agid Y, Hirsch E, Beaumont C, Hauw J, Agid Y, Hirsch E (2003) Neuromelanin associated redox-active iron is increased in the substantia nigra of patients with Parkinson’s disease. J Neurochem 86:1142–1148CrossRefPubMed Faucheux B, Martin M, Hauw J, Agid Y, Hirsch E, Beaumont C, Hauw J, Agid Y, Hirsch E (2003) Neuromelanin associated redox-active iron is increased in the substantia nigra of patients with Parkinson’s disease. J Neurochem 86:1142–1148CrossRefPubMed
54.
Zurück zum Zitat Morgen K, Sammer G, Weber L, Aslan B, Mu C, Sandmann D, Oechsner M, Vaitl D (2011) Structural brain abnormalities in patients with Parkinson disease: a comparative voxel-based analysis using T1-weighted MR imaging and magnetization transfer imaging. AJNR Am J Neuroradiol 32:2080–2086CrossRefPubMed Morgen K, Sammer G, Weber L, Aslan B, Mu C, Sandmann D, Oechsner M, Vaitl D (2011) Structural brain abnormalities in patients with Parkinson disease: a comparative voxel-based analysis using T1-weighted MR imaging and magnetization transfer imaging. AJNR Am J Neuroradiol 32:2080–2086CrossRefPubMed
58.
Zurück zum Zitat Zecca L, Pietra R, Goj C, Mecacci C, Radice D, Sabbioni E (1994) Iron and other metals in neuromelanin, substantia nigra, and putamen of human brain. J Neurochem 62:1097–1101CrossRefPubMed Zecca L, Pietra R, Goj C, Mecacci C, Radice D, Sabbioni E (1994) Iron and other metals in neuromelanin, substantia nigra, and putamen of human brain. J Neurochem 62:1097–1101CrossRefPubMed
59.
Zurück zum Zitat Zecca L, Bellei C, Costi P, Albertini A, Monzani E, Casella L, Gallorini M, Bergamaschi L, Moscatelli A, Turro N, Eisner M, Crippa PR, Ito S, Wakamatsu K, Bush WD, Ward WC, Simon JD, Zucca FA (2008) New melanic pigments in the human brain that accumulate in aging and block environmental toxic metals. Proc Natl Acad Sci U S A 105:17567–17572. https://doi.org/10.1073/pnas.0808768105 CrossRefPubMedPubMedCentral Zecca L, Bellei C, Costi P, Albertini A, Monzani E, Casella L, Gallorini M, Bergamaschi L, Moscatelli A, Turro N, Eisner M, Crippa PR, Ito S, Wakamatsu K, Bush WD, Ward WC, Simon JD, Zucca FA (2008) New melanic pigments in the human brain that accumulate in aging and block environmental toxic metals. Proc Natl Acad Sci U S A 105:17567–17572. https://​doi.​org/​10.​1073/​pnas.​0808768105 CrossRefPubMedPubMedCentral
60.
Zurück zum Zitat Zhang W, Phillips K, Wielgus A, Liu J, Albertini A, Zucca F, Faust R, Qian S, Miller D, Chignell C, Wilson B, Jackson-Lew V, Przedborski S, Joset D, Loike J, Hong J, Sulzer D, Zecca L (2011) Neuromelanin activates microglia and induces degeneration of dopaminergic neurons: implications for progression of Parkinson’s disease. Neurotox Res 19:63–72. https://doi.org/10.1016/j.bbi.2011.09.016.Mast CrossRefPubMed Zhang W, Phillips K, Wielgus A, Liu J, Albertini A, Zucca F, Faust R, Qian S, Miller D, Chignell C, Wilson B, Jackson-Lew V, Przedborski S, Joset D, Loike J, Hong J, Sulzer D, Zecca L (2011) Neuromelanin activates microglia and induces degeneration of dopaminergic neurons: implications for progression of Parkinson’s disease. Neurotox Res 19:63–72. https://​doi.​org/​10.​1016/​j.​bbi.​2011.​09.​016.​Mast CrossRefPubMed
63.
Zurück zum Zitat Promteangtrong C, Kolber M, Ramchandra P, Moghbel M, Houshmand S, Schöll M, Bai H, Werner T, Alavi A, Buchpiguel C (2015) Multimodality imaging approach in Alzheimer disease. Part I: structural MRI, functional MRI, diffusion tensor imaging and magnetization transfer imaging. Dement Neuropsychol 9:318–329. https://doi.org/10.1590/1980-57642015DN94000318 CrossRef Promteangtrong C, Kolber M, Ramchandra P, Moghbel M, Houshmand S, Schöll M, Bai H, Werner T, Alavi A, Buchpiguel C (2015) Multimodality imaging approach in Alzheimer disease. Part I: structural MRI, functional MRI, diffusion tensor imaging and magnetization transfer imaging. Dement Neuropsychol 9:318–329. https://​doi.​org/​10.​1590/​1980-57642015DN940003​18 CrossRef
66.
Zurück zum Zitat Mitchell DG, Cohen M (2004) MRI principles, 2nd ed. Saunders (W.B.) Co Ltd, Elsevier health sciences Mitchell DG, Cohen M (2004) MRI principles, 2nd ed. Saunders (W.B.) Co Ltd, Elsevier health sciences
69.
Zurück zum Zitat Castellanos G, Fernández-Seara M, Lorenzo-Betancor O, Ortega-Cubero S, Puigvert M, Uranga J, Vidorreta M, Irigoyen J, Lorenzo E, Muñoz-Barrutia A, Ortiz-de-Solorzano C, Pastor P, Pastor MA (2015) Automated neuromelanin imaging as a diagnostic biomarker for Parkinson’s disease. Mov Disord 30:945–952. https://doi.org/10.1002/mds.26201 CrossRefPubMed Castellanos G, Fernández-Seara M, Lorenzo-Betancor O, Ortega-Cubero S, Puigvert M, Uranga J, Vidorreta M, Irigoyen J, Lorenzo E, Muñoz-Barrutia A, Ortiz-de-Solorzano C, Pastor P, Pastor MA (2015) Automated neuromelanin imaging as a diagnostic biomarker for Parkinson’s disease. Mov Disord 30:945–952. https://​doi.​org/​10.​1002/​mds.​26201 CrossRefPubMed
Metadaten
Titel
Pool size ratio of the substantia nigra in Parkinson’s disease derived from two different quantitative magnetization transfer approaches
verfasst von
Paula Trujillo
Paul E. Summers
Alex K. Smith
Seth A. Smith
Luca T. Mainardi
Sergio Cerutti
Daniel O. Claassen
Antonella Costa
Publikationsdatum
06.10.2017
Verlag
Springer Berlin Heidelberg
Erschienen in
Neuroradiology / Ausgabe 12/2017
Print ISSN: 0028-3940
Elektronische ISSN: 1432-1920
DOI
https://doi.org/10.1007/s00234-017-1911-2

Weitere Artikel der Ausgabe 12/2017

Neuroradiology 12/2017 Zur Ausgabe

Leitlinien kompakt für die Neurologie

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Update Neurologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.