Journal of the Korean Society of Radiology (대한영상의학회지)

The Korean Society of Radiology (대한영상의학회)
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MRI Findings in Parkinson's Disease: Radiologic Assessment of Nigrostriatal Degeneration

파킨슨병의 자기공명영상 소견: 흑질선조체 변성의 영상학적 평가

  • Yun Jung Bae (Department of Radiology, Seoul National University Bundang Hospital, Seoul National University College of Medicine) ;
  • Jong-Min Kim (Department of Neurology, Seoul National University Bundang Hospital, Seoul National University College of Medicine) ;
  • Byung Se Choi (Department of Radiology, Seoul National University Bundang Hospital, Seoul National University College of Medicine) ;
  • Yoo Sung Song (Department of Nuclear Medicine, Seoul National University Bundang Hospital, Seoul National University College of Medicine) ;
  • Yoonho Nam (Division of Biomedical Engineering, Hankuk University of Foreign Studies) ;
  • Se Jin Cho (Department of Radiology, Seoul National University Bundang Hospital, Seoul National University College of Medicine) ;
  • Jae Hyoung Kim (Department of Radiology, Seoul National University Bundang Hospital, Seoul National University College of Medicine) ;
  • Sang Eun Kim (Department of Nuclear Medicine, Seoul National University Bundang Hospital, Seoul National University College of Medicine)
  • 배윤정 (서울대학교 의과대학 분당서울대학교병원 영상의학과) ;
  • 김종민 (서울대학교 의과대학 분당서울대학교병원 신경과) ;
  • 최병세 (서울대학교 의과대학 분당서울대학교병원 영상의학과) ;
  • 송요성 (서울대학교 의과대학 분당서울대학교병원 핵의학과) ;
  • 남윤호 (한국외국어대학교 바이오메디컬공학부) ;
  • 조세진 (서울대학교 의과대학 분당서울대학교병원 영상의학과) ;
  • 김재형 (서울대학교 의과대학 분당서울대학교병원 영상의학과) ;
  • 김상은 (서울대학교 의과대학 분당서울대학교병원 핵의학과)
  • Received : 2022.04.06
  • Accepted : 2022.05.12
  • Published : 2022.05.01
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Abstract

Parkinson's disease (PD) is a movement disorder that develops due to degenerative loss of dopaminergic cells in the substantia nigra of the midbrain. Recent advances in MRI techniques have demonstrated various imaging findings that can reflect the underlying pathophysiological processes occurring in Parkinson's disease. Many imaging studies have shown that such findings can assist in the diagnosis of Parkinson's disease and its differentiation from atypical parkinsonism. In this review, we present MRI techniques that can be used in clinical assessment, such as nigrosome imaging and neuromelanin imaging, and we provide the detailed imaging features of Parkinson's disease reflecting nigrostriatal degeneration.

파킨슨병은 중뇌 흑질에 위치한 도파민성 신경세포의 퇴행성 소실로 인해 발생하는 이상운동질환이다. 최근 다양한 자기공명영상기법의 발전으로 파킨슨병에서 일어나는 병리생태학적인 변화를 반영하는 여러 영상 소견들이 보고되었다. 여러 연구에서 이러한 영상 소견들은 파킨슨병의 진단 및 비정형 파킨슨증과의 감별 등에 유의미한 도움을 줄 수 있는 것이 밝혀졌다. 본 종설에서는, 파킨슨병에서 일어나는 흑질선조체 변성의 병태생리를 나타낼 수 있는 나이그로좀 영상 및 뉴로멜라닌 영상 등을 포함한 자기공명영상기법들과 각 영상에서 나타나는 소견에 대하여 자세히 다루었다.

Keywords

Acknowledgement

This study was supported by grant No. 02-2021-0015 from the Seoul National University Bundang Hospital Research Fund.

References

  1. Damier P, Hirsch EC, Agid Y, Graybiel AM. The substantia nigra of the human brain. I. Nigrosomes and the nigral matrix, a compartmental organization based on calbindin D(28K) immunohistochemistry. Brain 1999;122(Pt 8):1421-1436  https://doi.org/10.1093/brain/122.8.1421
  2. Damier P, Hirsch EC, Agid Y, Graybiel AM. The substantia nigra of the human brain. II. Patterns of loss of dopamine-containing neurons in Parkinson's disease. Brain 1999;122(Pt 8):1437-1448  https://doi.org/10.1093/brain/122.8.1437
  3. Rispoli V, Schreglmann SR, Bhatia KP. Neuroimaging advances in Parkinson's disease. Curr Opin Neurol 2018;31:415-424  https://doi.org/10.1097/WCO.0000000000000584
  4. Schwarz ST, Xing Y, Tomar P, Bajaj N, Auer DP. In vivo assessment of brainstem depigmentation in Parkinson disease: potential as a severity marker for multicenter studies. Radiology 2017;283:789-798  https://doi.org/10.1148/radiol.2016160662
  5. Langkammer C, Krebs N, Goessler W, Scheurer E, Ebner F, Yen K, et al. Quantitative MR imaging of brain iron: a postmortem validation study. Radiology 2010;257:455-462  https://doi.org/10.1148/radiol.10100495
  6. Guan X, Xu X, Zhang M. Region-specific iron measured by MRI as a biomarker for Parkinson's disease. Neurosci Bull 2017;33:561-567  https://doi.org/10.1007/s12264-017-0138-x
  7. Foo H, Mak E, Yong TT, Wen MC, Chander RJ, Au WL, et al. Progression of small vessel disease correlates with cortical thinning in Parkinson's disease. Parkinsonism Relat Disord 2016;31:34-40  https://doi.org/10.1016/j.parkreldis.2016.06.019
  8. Sang T, He J, Wang J, Zhang C, Zhou W, Zeng Q, et al. Alterations in white matter fiber in Parkinson disease across different cognitive stages. Neurosci Lett 2022;769:136424 
  9. Blazejewska AI, Schwarz ST, Pitiot A, Stephenson MC, Lowe J, Bajaj N, et al. Visualization of nigrosome 1 and its loss in PD: pathoanatomical correlation and in vivo 7 T MRI. Neurology 2013;81:534-540  https://doi.org/10.1212/WNL.0b013e31829e6fd2
  10. Schwarz ST, Afzal M, Morgan PS, Bajaj N, Gowland PA, Auer DP. The 'swallow tail' appearance of the healthy nigrosome-a new accurate test of Parkinson's disease: a case-control and retrospective cross-sectional MRI study at 3T. PLoS One 2014;9:e93814 
  11. Cosottini M, Frosini D, Pesaresi I, Donatelli G, Cecchi P, Costagli M, et al. Comparison of 3T and 7T susceptibility-weighted angiography of the substantia nigra in diagnosing Parkinson disease. AJNR Am J Neuroradiol 2015;36:461-466  https://doi.org/10.3174/ajnr.A4158
  12. Noh Y, Sung YH, Lee J, Kim EY. Nigrosome 1 detection at 3T MRI for the diagnosis of early-stage idiopathic Parkinson disease: assessment of diagnostic accuracy and agreement on imaging asymmetry and clinical laterality. AJNR Am J Neuroradiol 2015;36:2010-2016  https://doi.org/10.3174/ajnr.A4412
  13. Reiter E, Mueller C, Pinter B, Krismer F, Scherfler C, Esterhammer R, et al. Dorsolateral nigral hyperintensity on 3.0T susceptibility-weighted imaging in neurodegenerative Parkinsonism. Mov Disord 2015;30:1068-1076  https://doi.org/10.1002/mds.26171
  14. Bae YJ, Kim JM, Kim E, Lee KM, Kang SY, Park HS, et al. Loss of nigral hyperintensity on 3 tesla MRI of parkinsonism: comparison with (123) I-FP-CIT SPECT. Mov Disord 2016;31:684-692  https://doi.org/10.1002/mds.26584
  15. Gao P, Zhou PY, Wang PQ, Zhang GB, Liu JZ, Xu F, et al. Universality analysis of the existence of substantia nigra "swallow tail" appearance of non-Parkinson patients in 3T SWI. Eur Rev Med Pharmacol Sci 2016;20:1307-1314 
  16. Kim JM, Jeong HJ, Bae YJ, Park SY, Kim E, Kang SY, et al. Loss of substantia nigra hyperintensity on 7 Tesla MRI of Parkinson's disease, multiple system atrophy, and progressive supranuclear palsy. Parkinsonism Relat Disord 2016;26:47-54  https://doi.org/10.1016/j.parkreldis.2016.01.023
  17. Acosta-Cabronero J, Cardenas-Blanco A, Betts MJ, Butryn M, Valdes-Herrera JP, Galazky I, et al. The whole-brain pattern of magnetic susceptibility perturbations in Parkinson's disease. Brain 2017;140:118-131  https://doi.org/10.1093/brain/aww278
  18. Langley J, Huddleston DE, Sedlacik J, Boelmans K, Hu XP. Parkinson's disease-related increase of T2*-weighted hypointensity in substantia nigra pars compacta. Mov Disord 2017;32:441-449  https://doi.org/10.1002/mds.26883
  19. Sung YH, Lee J, Nam Y, Shin HG, Noh Y, Shin DH, et al. Differential involvement of nigral subregions in idiopathic Parkinson's disease. Hum Brain Mapp 2018;39:542-553  https://doi.org/10.1002/hbm.23863
  20. Cho SJ, Bae YJ, Kim JM, Kim HJ, Baik SH, Sunwoo L, et al. Iron-sensitive magnetic resonance imaging in Parkinson's disease: a systematic review and meta-analysis. J Neurol 2021;268:4721-4736  https://doi.org/10.1007/s00415-021-10582-x
  21. Tatsch K, Poepperl G. Nigrostriatal dopamine terminal imaging with dopamine transporter SPECT: an update. J Nucl Med 2013;54:1331-1338  https://doi.org/10.2967/jnumed.112.105379
  22. Sung YH, Noh Y, Lee J, Kim EY. Drug-induced Parkinsonism versus idiopathic Parkinson disease: utility of nigrosome 1 with 3-T imaging. Radiology 2016;279:849-858  https://doi.org/10.1148/radiol.2015151466
  23. Oustwani CS, Korutz AW, Lester MS, Kianirad Y, Simuni T, Hijaz TA. Can loss of the swallow tail sign help distinguish between Parkinson disease and the Parkinson-plus syndromes? Clin Imaging 2017;44:66-69  https://doi.org/10.1016/j.clinimag.2017.04.005
  24. Perez Akly MS, Stefani CV, Ciancaglini L, Bestoso JS, Funes JA, Bauso DJ, et al. Accuracy of nigrosome-1 detection to discriminate patients with Parkinson's disease and essential tremor. Neuroradiol J 2019;32:395-400  https://doi.org/10.1177/1971400919853787
  25. De Marzi R, Seppi K, Hogl B, Muller C, Scherfler C, Stefani A, et al. Loss of dorsolateral nigral hyperintensity on 3.0 tesla susceptibility-weighted imaging in idiopathic rapid eye movement sleep behavior disorder. Ann Neurol 2016;79:1026-1030  https://doi.org/10.1002/ana.24646
  26. Bae YJ, Kim JM, Kim KJ, Kim E, Park HS, Kang SY, et al. Loss of substantia nigra hyperintensity at 3.0-T MR imaging in idiopathic REM sleep behavior disorder: comparison with 123I-FP-CIT SPECT. Radiology 2018;287:285-293  https://doi.org/10.1148/radiol.2017162486
  27. van der Pluijm M, Cassidy C, Zandstra M, Wallert E, de Bruin K, Booij J, et al. Reliability and reproducibility of neuromelanin-sensitive imaging of the substantia nigra: a comparison of three different sequences. J Magn Reson Imaging 2021;53:712-721  https://doi.org/10.1002/jmri.27384
  28. Kashihara K, Shinya T, Higaki F. Neuromelanin magnetic resonance imaging of nigral volume loss in patients with Parkinson's disease. J Clin Neurosci 2011;18:1093-1096  https://doi.org/10.1016/j.jocn.2010.08.043
  29. Wang J, Li Y, Huang Z, Wan W, Zhang Y, Wang C, et al. Neuromelanin-sensitive magnetic resonance imaging features of the substantia nigra and locus coeruleus in de novo Parkinson's disease and its phenotypes. Eur J Neurol 2018;25:949-e73 
  30. Cho SJ, Bae YJ, Kim JM, Kim D, Baik SH, Sunwoo L, et al. Diagnostic performance of neuromelanin-sensitive magnetic resonance imaging for patients with Parkinson's disease and factor analysis for its heterogeneity: a systematic review and meta-analysis. Eur Radiol 2021;31:1268-1280  https://doi.org/10.1007/s00330-020-07240-7
  31. Schwarz ST, Rittman T, Gontu V, Morgan PS, Bajaj N, Auer DP. T1-weighted MRI shows stage-dependent substantia nigra signal loss in Parkinson's disease. Mov Disord 2011;26:1633-1638  https://doi.org/10.1002/mds.23722
  32. Fabbri M, Reimao S, Carvalho M, Nunes RG, Abreu D, Guedes LC, et al. Substantia nigra neuromelanin as an imaging biomarker of disease progression in Parkinson's disease. J Parkinsons Dis 2017;7:491-501  https://doi.org/10.3233/JPD-171135
  33. Kuya K, Ogawa T, Shinohara Y, Ishibashi M, Fujii S, Mukuda N, et al. Evaluation of Parkinson's disease by neuromelanin-sensitive magnetic resonance imaging and 123I-FP-CIT SPECT. Acta Radiol 2018;59:593-598  https://doi.org/10.1177/0284185117722812
  34. Okuzumi A, Hatano T, Kamagata K, Hori M, Mori A, Oji Y, et al. Neuromelanin or DaT-SPECT: which is the better marker for discriminating advanced Parkinson's disease? Eur J Neurol 2019;26:1408-1416  https://doi.org/10.1111/ene.14009
  35. Kashihara K, Shinya T, Higaki F. Reduction of neuromelanin-positive nigral volume in patients with MSA, PSP and CBD. Intern Med 2011;50:1683-1687  https://doi.org/10.2169/internalmedicine.50.5101
  36. Matsuura K, Maeda M, Yata K, Ichiba Y, Yamaguchi T, Kanamaru K, et al. Neuromelanin magnetic resonance imaging in Parkinson's disease and multiple system atrophy. Eur Neurol 2013;70:70-77  https://doi.org/10.1159/000350291
  37. Wang J, Huang Z, Li Y, Ye F, Wang C, Zhang Y, et al. Neuromelanin-sensitive MRI of the substantia nigra: an imaging biomarker to differentiate essential tremor from tremor-dominant Parkinson's disease. Parkinsonism Relat Disord 2019;58:3-8  https://doi.org/10.1016/j.parkreldis.2018.07.007
  38. Gaurav R, Pyatigorskaya N, Biondetti E, Valabregue R, Yahia-Cherif L, Mangone G, et al. Deep learning-based neuromelanin MRI changes of isolated REM sleep behavior disorder. Mov Disord 2022;37:1064-1069  https://doi.org/10.1002/mds.28933
  39. de Rochefort L, Liu T, Kressler B, Liu J, Spincemaille P, Lebon V, et al. Quantitative susceptibility map reconstruction from MR phase data using bayesian regularization: validation and application to brain imaging. Magn Reson Med 2010;63:194-206  https://doi.org/10.1002/mrm.22187
  40. Pyatigorskaya N, Sanz-Morere CB, Gaurav R, Biondetti E, Valabregue R, Santin M, et al. Iron imaging as a diagnostic tool for Parkinson's disease: a systematic review and meta-analysis. Front Neurol 2020;11:366 
  41. Ulla M, Bonny JM, Ouchchane L, Rieu I, Claise B, Durif F. Is R2* a new MRI biomarker for the progression of Parkinson's disease? A longitudinal follow-up. PLoS One 2013;8:e57904 
  42. Wieler M, Gee M, Camicioli R, Martin WR. Freezing of gait in early Parkinson's disease: nigral iron content estimated from magnetic resonance imaging. J Neurol Sci 2016;361:87-91  https://doi.org/10.1016/j.jns.2015.12.008
  43. Du G, Liu T, Lewis MM, Kong L, Wang Y, Connor J, et al. Quantitative susceptibility mapping of the midbrain in Parkinson's disease. Mov Disord 2016;31:317-324  https://doi.org/10.1002/mds.26417
  44. He N, Ling H, Ding B, Huang J, Zhang Y, Zhang Z, et al. Region-specific disturbed iron distribution in early idiopathic Parkinson's disease measured by quantitative susceptibility mapping. Hum Brain Mapp 2015;36: 4407-4420  https://doi.org/10.1002/hbm.22928
  45. Langkammer C, Pirpamer L, Seiler S, Deistung A, Schweser F, Franthal S, et al. Quantitative susceptibility mapping in Parkinson's disease. PLoS One 2016;11:e0162460 
  46. Uchida Y, Kan H, Sakurai K, Inui S, Kobayashi S, Akagawa Y, et al. Magnetic susceptibility associates with dopaminergic deficits and cognition in Parkinson's disease. Mov Disord 2020;35:1396-1405  https://doi.org/10.1002/mds.28077
  47. Lee JH, Lee MS. Brain iron accumulation in atypical Parkinsonian syndromes: in vivo MRI evidences for distinctive patterns. Front Neurol 2019;10:74 
  48. Azuma M, Hirai T, Nakaura T, Kitajima M, Yamashita S, Hashimoto M, et al. Combining quantitative susceptibility mapping to the morphometric index in differentiating between progressive supranuclear palsy and Parkinson's disease. J Neurol Sci 2019;406:116443 
  49. Mazzucchi S, Frosini D, Costagli M, Del Prete E, Donatelli G, Cecchi P, et al. Quantitative susceptibility mapping in atypical Parkinsonisms. Neuroimage Clin 2019;24:101999 
  50. Novellino F, Cherubini A, Chiriaco C, Morelli M, Salsone M, Arabia G, et al. Brain iron deposition in essential tremor: a quantitative 3-Tesla magnetic resonance imaging study. Mov Disord 2013;28:196-200  https://doi.org/10.1002/mds.25263
  51. Sun J, Lai Z, Ma J, Gao L, Chen M, Chen J, et al. Quantitative evaluation of iron content in idiopathic rapid eye movement sleep behavior disorder. Mov Disord 2020;35:478-485  https://doi.org/10.1002/mds.27929
  52. Basser PJ, Pierpaoli C. Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. J Magn Reson B 1996;111:209-219  https://doi.org/10.1006/jmrb.1996.0086
  53. Prodoehl J, Li H, Planetta PJ, Goetz CG, Shannon KM, Tangonan R, et al. Diffusion tensor imaging of Parkinson's disease, atypical parkinsonism, and essential tremor. Mov Disord 2013;28:1816-1822  https://doi.org/10.1002/mds.25491
  54. Atkinson-Clement C, Pinto S, Eusebio A, Coulon O. Diffusion tensor imaging in Parkinson's disease: review and meta-analysis. Neuroimage Clin 2017;16:98-110  https://doi.org/10.1016/j.nicl.2017.07.011
  55. Vaillancourt DE, Spraker MB, Prodoehl J, Abraham I, Corcos DM, Zhou XJ, et al. High-resolution diffusion tensor imaging in the substantia nigra of de novo Parkinson disease. Neurology 2009;72:1378-1384  https://doi.org/10.1212/01.wnl.0000340982.01727.6e
  56. Ofori E, Pasternak O, Planetta PJ, Li H, Burciu RG, Snyder AF, et al. Longitudinal changes in free-water within the substantia nigra of Parkinson's disease. Brain 2015;138(Pt 8):2322-2331  https://doi.org/10.1093/brain/awv136
  57. Chen F, Wu T, Luo Y, Li Z, Guan Q, Meng X, et al. Amnestic mild cognitive impairment in Parkinson's disease: white matter structural changes and mechanisms. PLoS One 2019;14:e0226175 
  58. Pasternak O, Sochen N, Gur Y, Intrator N, Assaf Y. Free water elimination and mapping from diffusion MRI. Magn Reson Med 2009;62:717-730  https://doi.org/10.1002/mrm.22055
  59. Hoy AR, Koay CG, Kecskemeti SR, Alexander AL. Optimization of a free water elimination two-compartment model for diffusion tensor imaging. Neuroimage 2014;103:323-333  https://doi.org/10.1016/j.neuroimage.2014.09.053
  60. Guttuso T Jr, Bergsland N, Hagemeier J, Lichter DG, Pasternak O, Zivadinov R. Substantia nigra free water increases longitudinally in Parkinson disease. AJNR Am J Neuroradiol 2018;39:479-484  https://doi.org/10.3174/ajnr.A5545
  61. Ofori E, Krismer F, Burciu RG, Pasternak O, McCracken JL, Lewis MM, et al. Free water improves detection of changes in the substantia nigra in parkinsonism: a multisite study. Mov Disord 2017;32:1457-1464  https://doi.org/10.1002/mds.27100
  62. Burciu RG, Ofori E, Archer DB, Wu SS, Pasternak O, McFarland NR, et al. Progression marker of Parkinson's disease: a 4-year multi-site imaging study. Brain 2017;140:2183-2192  https://doi.org/10.1093/brain/awx146
  63. Yang J, Archer DB, Burciu RG, Muller MLTM, Roy A, Ofori E, et al. Multimodal dopaminergic and free-water imaging in Parkinson's disease. Parkinsonism Relat Disord 2019;62:10-15  https://doi.org/10.1016/j.parkreldis.2019.01.007
  64. Zhang Y, Wu IW, Buckley S, Coffey CS, Foster E, Mendick S, et al. Diffusion tensor imaging of the nigrostriatal fibers in Parkinson's disease. Mov Disord 2015;30:1229-1236  https://doi.org/10.1002/mds.26251
  65. Planetta PJ, Ofori E, Pasternak O, Burciu RG, Shukla P, DeSimone JC, et al. Free-water imaging in Parkinson's disease and atypical parkinsonism. Brain 2016;139(Pt 2):495-508  https://doi.org/10.1093/brain/awv361
  66. Mitchell T, Archer DB, Chu WT, Coombes SA, Lai S, Wilkes BJ, et al. Neurite orientation dispersion and density imaging (NODDI) and free-water imaging in Parkinsonism. Hum Brain Mapp 2019;40:5094-5107  https://doi.org/10.1002/hbm.24760
  67. Pyatigorskaya N, Gaurav R, Arnaldi D, Leu-Semenescu S, Yahia-Cherif L, Valabregue R, et al. Magnetic resonance imaging biomarkers to assess substantia nigra damage in idiopathic rapid eye movement sleep behavior disorder. Sleep 2017;40:zsx149 
  68. Zhou L, Li G, Zhang Y, Zhang M, Chen Z, Zhang L, et al. Increased free water in the substantia nigra in idiopathic REM sleep behaviour disorder. Brain 2021;144:1488-1497 https://doi.org/10.1093/brain/awab039