Abstract
Background
Transcranial duplex scanning (TCD) of the substantia nigra (SN) is increasingly used to diagnose Idiopathic Parkinson’s Disease (IPD). Up until now 70 diagnostic studies have been published, not only on investigation of the SN, but also of the lenticular nucleus (LN) and the Raphe nuclei (RN).
Method
We systematically reviewed all diagnostic TCD studies in parkinsonian patients up to June 2008.
Results
We found 35 eligible studies. Of the 1534 IPD patients investigated in the 35 studies 200 (13 %) had an inconclusive SN-TCD. An increased echo-intensity of the SN was seen in 1167 (87 %) of the 1334 IPD patients, 276 (12 %) of the 2340 healthy controls and in 41 (30 %) of the 138 patients with an atypical parkinsonian syndrome (APS). On the contrary, a pathological LNTCD was found more often in APS patients (79 %) than in IPD patients (23 %) and healthy controls (6 %). A decreased echo-intensity of the RN was found more often in depressed (46 %) than in non-depressed IPD patients (16 %).
Conclusions
SN-TCD accurately differentiates between patients with IPD and healthy controls, but not between patients with IPD and APS. LN-TCD is only moderate accurate to delineate IPD from APS, but combinations of SN- and LN-TCD may be more promising. RN-TCD has only marginal diagnostic accuracy in diagnosing depression in IPD and non-IPD patients. Before TCD can be implicated, more research is needed to standardize the TCD technique, to investigate the TCD in non-research settings and to determine the additional value of TCD compared with currently used clinical techniques like SPECT imaging.
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Abbreviations
- APS:
-
Atypical Parkinsonian Syndromes
- DIP:
-
Drug Induced Parkinsonism
- ET:
-
Essential Tremor
- IPD:
-
Idiopathic Parkinson’s Disease
- LN:
-
Lenticular Nucleus
- MSA:
-
Multiple System Atrophy
- PET:
-
Positron Emission Tomography
- PSP:
-
Progressive Supranuclear Palsy
- RN:
-
Raphe Nuclei
- SN:
-
Substantia Nigra
- SPECT:
-
Single Photon Emission Computer Tomography
- TCD:
-
Transcranial Duplex Scanning
- VP:
-
Vascular Parkinsonism
References
Litvan I, Agid Y, Jankovic J, Goetz C, Brandel JP, Lai EC, et al. (1996) Accuracy of clinical criteria for the diagnosis of progressive supranuclear palsy (Steele-Richardson-Olszewski syndrome). Neurology 46(4):922–930
Gilman S, Low PA, Quinn N, Albanese A, Ben-Shlomo Y, Fowler CJ, et al. (1999) Consensus statement on the diagnosis of multiple system atrophy. J Neurol Sci 163(1):94–98
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(3):181–184
Bain P, Brin M, Deuschl G, Elble R, Jankovic J, Findley L, et al. (2000) Criteria for the diagnosis of essential tremor. Neurology 54(11 Suppl 4):S7
Zijlmans JC, Daniel SE, Hughes AJ, Revesz T, Lees AJ (2004) Clinicopathological investigation of vascular parkinsonism, including clinical criteria for diagnosis. Mov Disord 19(6):630–640
Watanabe H, Saito Y, Terao S, Ando T, Kachi T, Mukai E, et al. (2002) Progression and prognosis in multiple system atrophy: an analysis of 230 Japanese patients. Brain 125(Pt 5):1070–1083
Rajput AH, Rozdilsky B, Rajput A (1991) Accuracy of clinical diagnosis in parkinsonism — a prospective study. Can J Neurol Sci 18(3):275–278
Dujardin K, Duhamel A, Becquet E, Grunberg C, Defebvre L, Destee A (1999) Neuropsychological abnormalities in first degree relatives of patients with familial Parkinson’s disease. J Neurol Neurosurg Psychiatry 67(3):323–328
Ponsen MM, Stoffers D, Booij J, van Eck-Smit BLF, Wolters EC, Berendse HW (2004) Idiopathic hyposmia as a preclinical sign of Parkinson’s disease. Ann Neurol 56:173–181
Storch A, Hofer A, Kruger R, Schulz JB, Winkler J, Gerlach M (2004) New developments in diagnosis and treatment of Parkinson’s disease — from basic science to clinical applications. J Neurol 251(Suppl 6):VI/33–8
Lee PH, Yeo SH, Kim HJ, Youm HY (2006) Correlation between cardiac 123I-MIBG and odor identification in patients with Parkinson’s disease and multiple system atrophy. Mov Disord 21(11):1975–1977
Spiegel J, Mollers MO, Jost WH, Fuss G, Samnick S, Dillmann U, et al. (2005) FP-CIT and MIBG scintigraphy in early Parkinson’s disease. Mov Disord 20(5):552–561
Vlaar AM, van Kroonenburgh MJ, Kessels AG, Weber WE (2007) Metaanalysis of the literature on diagnostic accuracy of SPECT in parkinsonian syndromes. BMC Neurol 7:27
Becker G, Seufert J, Bogdahn U, Reichmann H, Reiners K (1995) Degeneration of substantia nigra in chronic Parkinson’s disease visualized by transcranial color-coded real-time sonography. Neurology 45(1):182–184
Walter U, Niehaus L, Probst T, Benecke R, Meyer BU, Dressler D (2003) Brain parenchyma sonography discriminates Parkinson’s disease and atypical parkinsonian syndromes. Neurology 60(1):74–77
Berg D, Siefker C, Becker G (2001) Echogenicity of the substantia nigra in Parkinson’s disease and its relation to clinical findings. J Neurol 248(8):684–689
Berg D, Roggendorf W, Schroder U, Klein R, Tatschner T, Benz P, et al. (2002) Echogenicity of the substantia nigra: association with increased iron content and marker for susceptibility to nigrostriatal injury. Arch Neurol 59(6):999–1005
Berg D, Becker G, Zeiler B, Tucha O, Hofmann E, Preier M, et al. (1999) Vulnerability of the nigrostriatal system as detected by transcranial ultrasound. Neurology 53(5):1026–1031
Berg D (2007) Disturbance of iron metabolism as a contributing factor to SN hyperechogenicity in Parkinson’s disease: implications for idiopathic and monogenetic forms. Neurochem Res 32(10):1646–1654
Walter U, Behnke S, Eyding J, Niehaus L, Postert T, Seidel G, et al. (2007) Transcranial brain parenchyma sonogrpahy in movement disorders: state of the art. Ultrasound Med Biol 33(1):15–25
Hennerici MG, Meairs SP (2001) Cerebrovascular Ultrasound: Theory, Practice and Future Developments. First edition ed. Cambridge, U.K.: Cambridge University Press
Schoning M, Grunert D, Stier B (1989) Transcranial duplex sonography through intact bone: a new diagnostic procedure. Ultraschall Med 10(2):66–71
Walter U, Behnke S, Eyding J, Niehaus L, Postert T, Seidel G, et al. (2007) Transcranial brain parenchyma sonography in movement disorders: state of the art. Ultrasound Med Biol 33(1):15–25
Walter U, Wittstock M, Benecke R, Dressler D (2002) Substantia nigra echogenicity is normal in nonextrapyramidal cerebral disorders but increased in Parkinson’s disease. J Neural Transm 109(2):191–196
Behnke S, Berg D, Naumann M, Becker G (2005) Differentiation of Parkinson’s disease and atypical parkinsonian syndromes by transcranial ultrasound. J Neurol Neurosurg Psychiatry 76(3):423–425
Becker G, Becker T, Struck M, Lindner A, Burzer K, Retz W, et al. (1995) Reduced echogenicity of brainstem raphe specific to unipolar depression: a transcranial color-coded real-time sonography study. Biol Psychiatry 38(3):180–184
Glaser M, Weber U, Hinrichs H, Niehaus L (2006) Neuroimaging of midbrain structures with different phased array ultrasound systems. Klin Neurophysiol 37:165–168
Budisic M, Trkanjec Z, Bosnjak J, Lovrencic-Huzjan A, Vukovic V, Demarin V (2009) Distinguishing Parkinson’s disease and essential tremor with transcranial sonography. Acta Neurol Scand 119(1):17–21
Schweitzer KJ, Hilker R, Walter U, Burghaus L, Berg D (2006) Substantia nigra hyperechogenicity as a marker of predisposition and slower progression in Parkinson’s disease. Mov Disord 21(1):94–98
Huang YW, Jeng JS, Tsai CF, Chen LL, Wu RM (2007) Transcranial imaging of substantia nigra hyperechogenicity in a Taiwanese cohort of Parkinson’s disease. Mov Disord 22(4):550–555
Godau J, Schweitzer KJ, Liepelt I, Gerloff C, Berg D (2007) Substantia nigra hypoechogenicity: definition and findings in restless legs syndrome. Mov Disord 22(2):187–192
Godau J, Wevers AK, Gaenslen A, Di Santo A, Liepelt I, Gasser T, et al. (2008) Sonographic abnormalities of brainstem structures in restless legs syndrome. Sleep Med 9(7):782–789
Kim JY, Kim ST, Jeon SH, Lee WY (2007) Midbrain transcranial sonography in Korean patients with Parkinson’s disease. Mov Disord 22(13): 1922–1926
Walter U, Dressler D, Wolters A, Wittstock M, Greim B, Benecke R (2006) Sonographic discrimination of dementia with Lewy bodies and Parkinson’s disease with dementia. J Neurol 253(4):448–454
Tromp SC, Vlaar AMM, Kroonenburgh MJPG, Mess WH, Nijs de T, Winogrodzka A, et al. (2007) The diagnostic value of transcranial duplex scanning and SPECT imaging versus clinical diagnosis (clinical prospective study). Movement Disorders 22(Suppl 16):S220
Tsai CF, Wu RM, Huang YW, Chen LL, Yip PK, Jeng JS (2007) Transcranial color-coded sonography helps differentiation between idiopathic Parkinson’s disease and vascular parkinsonism. J Neurol 254(4):501–507
Stockner H, Seppi K, Kiechl S, Schmidauer C, Sojer M, Schwaiger M, et al. (2006) Midbrain transcranial sonography finding in a population based study. Movement Disorders 21(Suppl 15):S634
Okawa M, Miwa H, Kajimoto Y, Hama K, Morita S, Nakanishi I, et al. (2007) Transcranial sonography of the substantia nigra in Japanese patients with Parkinson’s disease or atypical parkinsonism: clinical potential and limitations. Intern Med 46(18):1527–1531
Walter U, Dressler D, Wolters A, Probst T, Grossmann A, Benecke R (2004) Sonographic discrimination of corticobasal degeneration vs progressive supranuclear palsy. Neurology 63(3):504–509
Walter U, Dressler D, Probst T, Wolters A, Abu-Mugheisib M, Wittstock M, et al. (2007) Transcranial brain sonography findings in discriminating between parkinsonism and idiopathic Parkinson disease. Arch Neurol 64(11):1635–1640
Berg D, Siefker C, Ruprecht-Dorfler P, Becker G (2001) Relationship of substantia nigra echogenicity and motor function in elderly subjects. Neurology 56(1):13–17
Ruprecht-Dorfler P, Berg D, Tucha O, Benz P, Meier-Meitinger M, Alders GL, et al. (2003) Echogenicity of the substantia nigra in relatives of patients with sporadic Parkinson’s disease. Neuroimage 18(2):416–422
Walter U, Klein C, Hilker R, Benecke R, Pramstaller PP, Dressler D (2004) Brain parenchyma sonography detects preclinical parkinsonism. Mov Disord 19(12):1445–1449
Sommer U, Hummel T, Cormann K, Mueller A, Frasnelli J, Kropp J, et al. (2004) Detection of presymptomatic Parkinson’s disease: combining smell tests, transcranial sonography, and SPECT. Mov Disord 19(10):1196–202
Shahed J, Jankovic J (2007) Exploring the relationship between essential tremor and Parkinson’s disease. Parkinsonism Relat Disord 13:67–76
Walter U, Hoeppner J, Prudente- Morrissey L, Horowski S, Herpertz SC, Benecke R (2007) Parkinson’s diseaselike midbrain sonography abnormalities are frequent in depressive disorders. Brain 130(7):1799–1807
Walter U, Dressler D, Wolters A, Wittstock M, Benecke R (2007) Transcranial brain sonography findings in clinical subgroups of idiopathic Parkinson’s disease. Mov Disord 22(1):48–54
Becker T, Becker G, Seufert J, Hofmann E, Lange KW, Naumann M, et al. (1997) Parkinson’s disease and depression: evidence for an alteration of the basal limbic system detected by transcranial sonography. J Neurol Neurosurg Psychiatry 63(5):590–596
Spiegel J, Hellwig D, Mollers MO, Behnke S, Jost W, Fassbender K, et al. (2006) Transcranial sonography and [123I]FP-CIT SPECT disclose complementary aspects of Parkinson’s disease. Brain 129(Pt 5):1188–1193
Doepp F, Plotkin M, Siegel L, Kivi A, Gruber D, Lobsien E, et al. (2008) Brain parenchyma sonography and 123I-FPCIT SPECT in Parkinson’s disease and essential tremor. Mov Disord 23(3):405–410
Mijajlovic M, Dragasevic N, Stefanova E, Petrovic I, Svetel M, Kostic VS (2008) Transcranial sonography in spinocerebellar ataxia type 2. J Neurol 255(8):1164–1167
Postert T, Lack B, Kuhn W, Jergas M, Andrich J, Braun B, et al. (1999) Basal ganglia alterations and brain atrophy in Huntington’s disease depicted by transcranial real time sonography. J Neurol Neurosurg Psychiatry 67(4):457–462
Prestel J, Schweitzer KJ, Hofer A, Gasser T, Berg D (2006) Predictive value of transcranial sonography in the diagnosis of Parkinson’s disease. Mov Disord 21(10):1763–1765
Ressner P, Skoloudik D, Hlustik P, Kanovsky P (2007) Hyperechogenicity of the substantia nigra in Parkinson’s disease. J Neuroimaging 17(2):164–167
Schmidauer C, Sojer M, Seppi K, Stockner H, Hogl B, Biedermann B, et al. (2005) Transcranial ultrasound shows nigral hypoechogenicity in restless legs syndrome. Ann Neurol 58(4):630–634
Schweitzer KJ, Behnke S, Liepelt I, Wolf B, Grosser C, Godau J, et al. (2007) Cross-sectional study discloses a positive family history for Parkinson’s disease and male gender as epidemiological risk factors for substantia nigra hyperechogenicity. J Neural Transm 114(9):1167–1171
Stockner H, Sojer M, Seppi K, Mueller J, Wenning GK, Schmidauer C, et al. (2007) Midbrain sonography in patients with essential tremor. Mov Disord 22(3):414–417
Gaenslen A, Unmuth B, Godau J, Liepelt I, Di Santo A, Schweitzer KJ, et al. (2008) The specificity and sensitivity of transcranial ultrasound in the differential diagnosis of Parkinson’s disease: a prospective blinded study. Lancet Neurol 7(5):417–424
Becker G, Struck M, Bogdahn U, Becker T (1994) Echogenicity of the brainstem raphe in patients with major depression. Psychiatry Res 55(2):75–84
Berg D, Supprian T, Hofmann E, Zeiler B, Jager A, Lange KW, et al. (1999) Depression in Parkinson’s disease: brainstem midline alteration on transcranial sonography and magnetic resonance imaging. J Neurol 246(12):1186–1193
Doepp F, Plotkin M, Siegel L, Kivi A, Gruber D, Lobsien E, et al. (2008) Brain parenchyma sonography and (123)I-FP-CIT SPECT in Parkinson’s disease and essential tremor. Mov Disord 23(3):405–410
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Vlaar, A.M.M., Bouwmans, A., Mess, W.H. et al. Transcranial duplex in the differential diagnosis of parkinsonian syndromes. J Neurol 256, 530–538 (2009). https://doi.org/10.1007/s00415-009-0143-8
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DOI: https://doi.org/10.1007/s00415-009-0143-8