Abstract
Introduction
The characteristics of dementia with Lewy bodies (DLB), Alzheimer’s disease (AD) and amnestic mild cognitive impairment (a-MCI) overlap but require different treatments; therefore, it is important to differentiate these pathologies. Assessment of dopamine uptake in the striatum using dopamine transporter (DaT) single-photon emission computed tomography (SPECT) is the gold standard for diagnosing DLB; however, this modality is expensive, time consuming and involves radiation exposure. Degeneration of the substantia nigra nigrosome-1, which occurs in DLB, but not in AD/a-MCI, can be identified by 3T susceptibility-weighted imaging (SWI). Therefore, the aim of this retrospective observational study was to compare SWI with DaT-SPECT for differentiation of DLB from AD/a-MCI.
Methods
SWI data were acquired for patients with clinically diagnosed DLB (n = 29), AD (n = 18), a-MCI (n = 13) and healthy controls (n = 26). Images were analysed for nigrosome-1 degeneration. Diagnostic accuracy was evaluated for DLB, AD and a-MCI compared with striatal dopamine uptake using DaT-SPECT.
Results
SWI achieved 90% diagnostic accuracy (93% sensitivity, 87% specificity) for the detection of nigrosome-1 degeneration in DLB and not in AD/a-MCI as compared with 88.3% accuracy (93% sensitivity, 84% specificity) using DaT-SPECT.
Conclusions
SWI nigrosome-1 evaluation was useful in differentiating DLB from AD/a-MCI, with high accuracy. This less invasive and less expensive method is a potential alternative to DaT-SPECT for the diagnosis of DLB.
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Abbreviations
- AD:
-
Alzheimer’s disease
- a-MCI:
-
Amnestic mild cognitive impairment
- DLB:
-
Dementia with Lewy bodies
- DaT:
-
Dopamine transporter
- MMSE:
-
Mini-mental state examination
- MRI:
-
Magnetic resonance imaging
- NINCDS–ADRDA:
-
National Institute of Neurological and Communicative Disorders and Stroke–Alzheimer’s Disease and Related Disorders Association
- PD:
-
Parkinson’s disease
- PDD:
-
Parkinson’s disease with dementia
- SBR:
-
Specific binding ratio
- SPECT:
-
Single-photon emission computed tomography
- SWI:
-
Susceptibility-weighted imaging
- 123I-FP-CIT:
-
[123I]-2β-carbomethoxy-3β-(4-iodophenyl)-N-(3-fluoropropyl) nortropane
References
McKeith IG, Dickson DW, Lowe J, Emre M, O’Brien JT, Feldman H, Cummings J, Duda JE, Lippa C, Perry EK, Aarsland D, Arai H, Ballard CG, Boeve B, Burn DJ, Costa D, Del Ser T, Dubois B, Galasko D, Gauthier S, Goetz CG, Gomez-Tortosa E, Halliday G, Hansen LA, Hardy J, Iwatsubo T, Kalaria RN, Kaufer D, Kenny RA, Korczyn A, Kosaka K, Lee VM, Lees A, Litvan I, Londos E, Lopez OL, Minoshima S, Mizuno Y, Molina JA, Mukaetova-Ladinska EB, Pasquier F, Perry RH, Schulz JB, Trojanowski JQ, Yamada M (2005) Diagnosis and management of dementia with Lewy bodies: third report of the DLB Consortium. Neurology 65(12):1863–1872. doi:10.1212/01.wnl.0000187889.17253.b1
McKeith I, Mintzer J, Aarsland D, Burn D, Chiu H, Cohen-Mansfield J, Dickson D, Dubois B, Duda JE, Feldman H, Gauthier S, Halliday G, Lawlor B, Lippa C, Lopez OL, Carlos Machado J, O'Brien J, Playfer J, Reid W, International Psychogeriatric Association Expert Meeting on DLB (2004) Dementia with Lewy bodies. The Lancet Neurology 3(1):19–28
McKeith I (2007) Dementia with Lewy bodies and Parkinson’s disease with dementia: where two worlds collide. Pract Neurol 7(6):374–382. doi:10.1136/jnnp.2007.134163
Bajaj N, Hauser RA, Grachev ID (2013) Clinical utility of dopamine transporter single photon emission CT (DaT-SPECT) with (123I) ioflupane in diagnosis of parkinsonian syndromes. J Neurol Neurosurg Psychiatry 84(11):1288–1295. doi:10.1136/jnnp-2012-304436
Damier P, Hirsch EC, Agid Y, Graybiel AM (1999) The substantia nigra of the human brain. II. Patterns of loss of dopamine-containing neurons in Parkinson’s disease. Brain 122(Pt 8):1437–1448
Blazejewska AI, Schwarz ST, Pitiot A, Stephenson MC, Lowe J, Bajaj N, Bowtell RW, Auer DP, Gowland PA (2013) Visualization of nigrosome 1 and its loss in PD: pathoanatomical correlation and in vivo 7 T MRI. Neurology 81(6):534–540. doi:10.1212/WNL.0b013e31829e6fd2
Cosottini M, Frosini D, Pesaresi I, Costagli M, Biagi L, Ceravolo R, Bonuccelli U, Tosetti M (2014) MR imaging of the substantia nigra at 7 T enables diagnosis of Parkinson disease. Radiology 271(3):831–838. doi:10.1148/radiol.14131448
Kwon DH, Kim JM, SH O, Jeong HJ, Park SY, ES O, Chi JG, Kim YB, Jeon BS, Cho ZH (2012) Seven-Tesla magnetic resonance images of the substantia nigra in Parkinson disease. Ann Neurol 71(2):267–277. doi:10.1002/ana.22592
Lotfipour AK, Wharton S, Schwarz ST, Gontu V, Schafer A, Peters AM, Bowtell RW, Auer DP, Gowland PA, Bajaj NP (2012) High resolution magnetic susceptibility mapping of the substantia nigra in Parkinson’s disease. Journal of Magnetic Resonance Imaging: JMRI 35(1):48–55. doi:10.1002/jmri.22752
Cosottini M, Frosini D, Pesaresi I, Donatelli G, Cecchi P, Costagli M, Biagi L, Ceravolo R, Bonuccelli U, Tosetti M (2015) Comparison of 3T and 7T susceptibility-weighted angiography of the substantia nigra in diagnosing Parkinson disease. AJNR Am J Neuroradiol 36(3):461–466. doi:10.3174/ajnr.A4158
Mueller C, Pinter B, Reiter E, Schocke M, Scherfler C, Poewe W, Seppi K, Blazejewska AI, Schwarz ST, Bajaj N, Auer DP, Gowland PA (2014) Visualization of nigrosome 1 and its loss in PD: pathoanatomical correlation and in vivo 7T MRI. Neurology 82(19):1752. doi:10.1212/WNL.0000000000000398
Noh Y, Sung YH, Lee J, Kim EY (2015) 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 36(11):2010–2016. doi:10.3174/ajnr.A4412
Schwarz ST, Afzal M, Morgan PS, Bajaj N, Gowland PA, Auer DP (2014) 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 9(4):e93814. doi:10.1371/journal.pone.0093814
Haller S, Fallmar D, Larsson EM (2015) Susceptibility weighted imaging in dementia with Lewy bodies: will it resolve the blind spot of MRI? Neuroradiology. doi:10.1007/s00234-015-1605-6
Petersen RC, Doody R, Kurz A, Mohs RC, Morris JC, Rabins PV, Ritchie K, Rossor M, Thal L, Winblad B (2001) Current concepts in mild cognitive impairment. Arch Neurol 58(12):1985–1992
McKhann G, Drachman D, Folstein M, Katzman R, Price D, Stadlan EM (1984) Clinical diagnosis of Alzheimer’s disease: report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer’s disease. Neurology 34(7):939–944
Tossici-Bolt L, Hoffmann SM, Kemp PM, Mehta RL, Fleming JS (2006) Quantification of [123I]FP-CIT SPECT brain images: an accurate technique for measurement of the specific binding ratio. Eur J Nucl Med Mol Imaging 33(12):1491–1499. doi:10.1007/s00259-006-0155-x
Badiavas K, Molyvda E, Iakovou I, Tsolaki M, Psarrakos K, Karatzas N (2011) SPECT imaging evaluation in movement disorders: far beyond visual assessment. Eur J Nucl Med Mol Imaging 38(4):764–773. doi:10.1007/s00259-010-1664-1
Wang Y, Butros SR, Shuai X, Dai Y, Chen C, Liu M, Haacke EM, Hu J, Xu H (2012) Different iron-deposition patterns of multiple system atrophy with predominant parkinsonism and idiopathetic Parkinson diseases demonstrated by phase-corrected susceptibility-weighted imaging. AJNR Am J Neuroradiol 33(2):266–273. doi:10.3174/ajnr.A2765
Haller S, Badoud S, Nguyen D, Barnaure I, Montandon ML, Lovblad KO, Burkhard PR (2013) Differentiation between Parkinson disease and other forms of parkinsonism using support vector machine analysis of susceptibility-weighted imaging (SWI): initial results. Eur Radiol 23(1):12–19. doi:10.1007/s00330-012-2579-y
Walker Z, Jaros E, Walker RW, Lee L, Costa DC, Livingston G, Ince PG, Perry R, McKeith I, Katona CL (2007) Dementia with Lewy bodies: a comparison of clinical diagnosis, FP-CIT single photon emission computed tomography imaging and autopsy. J Neurol Neurosurg Psychiatry 78(11):1176–1181. doi:10.1136/jnnp.2006.110122
McKeith I, O'Brien J, Walker Z, Tatsch K, Booij J, Darcourt J, Padovani A, Giubbini R, Bonuccelli U, Volterrani D, Holmes C, Kemp P, Tabet N, Meyer I, Reininger C, Group DLBS (2007) Sensitivity and specificity of dopamine transporter imaging with 123I-FP-CIT SPECT in dementia with Lewy bodies: a phase III, multicentre study. The Lancet Neurology 6(4):305–313. doi:10.1016/S1474-4422(07)70057-1
Antonini A (2007) The role of I-ioflupane SPECT dopamine transporter imaging in the diagnosis and treatment of patients with dementia with Lewy bodies. Neuropsychiatr Dis Treat 3(3):287–292
Roselli F, Pisciotta NM, Perneczky R, Pennelli M, Aniello MS, De Caro MF, Ferrannini E, Tartaglione B, Defazio G, Rubini G, Livrea P (2009) Severity of neuropsychiatric symptoms and dopamine transporter levels in dementia with Lewy bodies: a 123I-FP-CIT SPECT study. Movement Disorders: Official Journal of the Movement Disorder Society 24(14):2097–2103. doi:10.1002/mds.22702
Siepel FJ, Dalen I, Gruner R, Booij J, Bronnick KS, Buter TC, Aarsland D (2016) Loss of dopamine transporter binding and clinical symptoms in dementia with Lewy bodies. Movement Disorders: Official Journal of the Movement Disorder Society 31(1):118–125. doi:10.1002/mds.26327
Weintraub D, Newberg AB, Cary MS, Siderowf AD, Moberg PJ, Kleiner-Fisman G, Duda JE, Stern MB, Mozley D, Katz IR (2005) Striatal dopamine transporter imaging correlates with anxiety and depression symptoms in Parkinson’s disease. J Nucl Med 46(2):227–232
Ziebell M, Andersen BB, Pinborg LH, Knudsen GM, Stokholm J, Thomsen G, Karlsborg M, Hogh P, Mork ML, Hasselbalch SG (2013) Striatal dopamine transporter binding does not correlate with clinical severity in dementia with Lewy bodies. J Nucl Med 54(7):1072–1076. doi:10.2967/jnumed.112.114025
Piggott MA, Marshall EF, Thomas N, Lloyd S, Court JA, Jaros E, Burn D, Johnson M, Perry RH, McKeith IG, Ballard C, Perry EK (1999) Striatal dopaminergic markers in dementia with Lewy bodies, Alzheimer’s and Parkinson’s diseases: rostrocaudal distribution. Brain 122(Pt 8):1449–1468
Perry RH, Irving D, Blessed G, Perry EK, Smith CJ, Fairbairn AF (1990) Dementia in old age: identification of a clinically and pathologically distinct disease category. Adv Neurol 51:41–46
Zecca L, Casella L, Albertini A, Bellei C, Zucca FA, Engelen M, Zadlo A, Szewczyk G, Zareba M, Sarna T (2008) Neuromelanin can protect against iron-mediated oxidative damage in system modeling iron overload of brain aging and Parkinson's disease. J Neurochem 106(4):1866–1875. doi:10.1111/j.1471-4159.2008.05541.x
Gomez-Tortosa E, Newell K, Irizarry MC, Albert M, Growdon JH, Hyman BT (1999) Clinical and quantitative pathologic correlates of dementia with Lewy bodies. Neurology 53(6):1284–1291
McKeith IG, Galasko D, Kosaka K, Perry EK, Dickson DW, Hansen LA, Salmon DP, Lowe J, Mirra SS, Byrne EJ, Lennox G, Quinn NP, Edwardson JA, Ince PG, Bergeron C, Burns A, Miller BL, Lovestone S, Collerton D, Jansen EN, Ballard C, de Vos RA, Wilcock GK, Jellinger KA, Perry RH (1996) Consensus guidelines for the clinical and pathologic diagnosis of dementia with Lewy bodies (DLB): report of the consortium on DLB international workshop. Neurology 47(5):1113–1124
Yamamoto R, Iseki E, Marui W, Togo T, Katsuse O, Kato M, Isojima D, Akatsu H, Kosaka K, Arai H (2005) Non-uniformity in the regional pattern of Lewy pathology in brains of dementia with Lewy bodies. Neuropathology 25(3):188–194
Lindboe CF, Hansen HB (1998) The frequency of Lewy bodies in a consecutive autopsy series. Clin Neuropathol 17(4):204–209
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We declare that all human studies have been approved by the ethics committee of Toho University and have therefore been performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments. We declare that due to the retrospective nature of the observational study design, informed consent was waived.
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An erratum to this article is available at http://dx.doi.org/10.1007/s00234-017-1814-2.
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Kamagata, K., Nakatsuka, T., Sakakibara, R. et al. Diagnostic imaging of dementia with Lewy bodies by susceptibility-weighted imaging of nigrosomes versus striatal dopamine transporter single-photon emission computed tomography: a retrospective observational study. Neuroradiology 59, 89–98 (2017). https://doi.org/10.1007/s00234-016-1773-z
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DOI: https://doi.org/10.1007/s00234-016-1773-z