Transcranial Sonography (TCS) of Brain Parenchyma in Movement Disorders: Quality Standards, Diagnostic Applications and Novel Technologies

Abstract

Transcranial B-mode sonography (TCS) of brain parenchyma is being increasingly used as a diagnostic tool in movement disorders. Compared to other neuroimaging modalities such as magnetic resonance imaging (MRI) and computed tomography, TCS can be performed today with portable machines and has the advantages of noninvasiveness and high resistance to movement artifacts. In distinct brain disorders TCS detects abnormalities that cannot be visualized or can only be visualized with significant effort with other imaging methods. In the field of movement disorders, TCS has been established mainly as a tool for the early and differential diagnosis of Parkinson’s disease. The postoperative position control of deep brain stimulation electrodes, especially in the subthalamic nucleus, can reliably and safely be performed with TCS. The present update review summarizes the current methodological standards and defines quality criteria of adequate TCS imaging and assessment of diagnostically relevant deep brain structures such as substantia nigra, brainstem raphe, basal ganglia and ventricles. Finally, an overview is given on recent technological advances including TCS-MRI fusion imaging and upcoming technologies of digitized image analysis aiming at a more investigator-independent assessment of deep brain structures on TCS.

Zusammenfassung

Die transkranielle B-Bild-Sonografie (TCS) tiefer Hirnstrukturen wird zunehmend als diagnostisches Instrument bei Bewegungsstörungen eingesetzt. Im Vergleich zu anderen Bildgebungsverfahren wie Magnetresonanztomografie (MRT) und Computertomografie liegen die Vorteile der TCS in der hohen Mobilität bis hin zum heute möglichen Einsatz tragbarer Geräte, der gesundheitlichen Unbedenklichkeit und der geringen Störbarkeit durch Patientenbewegungen. Bei bestimmten Hirnerkrankungen detektiert die TCS abnorme Befunde, die mit anderen Verfahren nicht oder nur mit hohem Aufwand darstellbar sind. Im Bereich der Bewegungsstörungen hat sich die TCS hauptsächlich als Instrument zur Früh- und Differenzialdiagnose des idiopathischen Parkinson-Syndroms etabliert. Die postoperative Positionskontrolle von Tiefenhirnstimulations-Sonden, insbesondere im Nucleus subthalamicus, kann zuverlässig und unschädlich mittels TCS durchgeführt werden. Die vorliegende aktuelle Übersicht fasst die gegenwärtigen methodischen Standards zusammen und definiert Qualitätskriterien für eine adäquate Bildgebung und Befundung diagnostisch relevanter tiefer Hirnstrukturen wie Substantia nigra, Hirnstamm-Raphe, Basalganglien und Hirnventrikel. Schließlich wird ein Überblick über aktuelle technologische Entwicklungen inklusive der TCS-MRT-Fusions-Bildgebung und aufkommender Technologien zur digitalen Bildanalyse gegeben, die das Ziel einer geringeren Untersucher-Abhängigkeit bei der Beurteilung tiefer Hirnstrukturen mittels TCS verfolgen.

Key words

basal ganglia - brain - ultrasound - movement disorders - TCS

• References

• 1 Berg D, Godau J, Walter U. Transcranial sonography in movement disorders. Lancet Neurol 2008; 7: 1044-1055
• 2 Walter U, Behnke S, Eyding J et al. Transcranial brain parenchyma sonography in movement disorders: state of the art. Ultrasound Med Biol 2007; 33: 15-25
• 3 Go CL, Frenzel A, Rosales RL et al. Assessment of substantia nigra echogenicity in German and Filipino populations using a portable ultrasound system. J Ultrasound Med 2012; 31: 191-196
• 4 Walter U, Kanowski M, Kaufmann J et al. Contemporary ultrasound systems allow high-resolution transcranial imaging of small echogenic deep intracranial structures similarly as MRI: a phantom study. Neuroimage 2008; 40: 551-558
• 5 Kern R, Perren F, Kreisel S et al. Multiplanar transcranial ultrasound imaging: standards, landmarks and correlation with magnetic resonance imaging. Ultrasound Med Biol 2005; 31: 311-315
• 6 Skoloudík D, Walter U. Method and validity of transcranial sonography in movement disorders. Int Rev Neurobiol 2010; 90: 7-34
• 7 Walter U, Kirsch M, Wittstock M et al. Transcranial sonographic localization of deep brain stimulation electrodes is safe, reliable and predicts clinical outcome. Ultrasound Med Biol 2011; 37: 1382-1391
• 8 Walter U. How to measure substantia nigra hyperechogenicity in Parkinson’s disease: detailed guide with video. J Ultrasound Med 2013; 32: 1837-1843
• 9 Školoudík D, Fadrná T, Bártová P et al. Reproducibility of sonographic measurement of the substantia nigra. Ultrasound Med Biol 2007; 33: 1347-1352
• 10 van de Loo S, Walter U, Behnke S et al. Reproducibility and diagnostic accuracy of substantia nigra sonography for the diagnosis of Parkinson's disease. J Neurol Neurosurg Psychiatry 2010; 81: 1087-1092
• 11 Plate A, Ahmadi SA, Pauly O et al. Three-dimensional sonographic examination of the midbrain for computer-aided diagnosis of movement disorders. Ultrasound Med Biol 2012; 38: 2041-2050
• 12 Blahuta J, Soukup T, Čermák P et al. Ultrasound medical image recognition with artificial intelligence for Parkinson’s disease classification. In: Biljanovic P, Butkovic Z, Skala K, et al. (eds.) Proceedings of 35th International Convention on Information and Communication Technology, Electronics and Microelectronics. Rijeka: Croatian Society for Information and Communication Technology, Electronics and Microelectronics – MIPRO; 2012: 958-962
• 13 Chen L, Hagenah J, Mertins A. Feature analysis for Parkinson's disease detection based on transcranial sonography image. Med Image Comput Comput Assist Interv 2012; 15: 272-279
• 14 Walter U. Transcranial sonography in brain disorders with trace metal accumulation. Int Rev Neurobiol 2010; 90: 166-178
• 15 Berg D, Godau J, Riederer P et al. Microglia activation is related to substantia nigra echogenicity. J Neural Transm 2010; 117: 1287-1292
• 16 Berg D, Becker G, Zeiler B et al. Vulnerability of the nigrostriatal system as detected by transcranial ultrasound. Neurology 1999; 53: 1026-1031
• 17 Mehnert S, Reuter I, Schepp K et al. Transcranial sonography for diagnosis of Parkinson's disease. BMC Neurol 2010; 10: 9
• 18 Hagenah J, König IR, Sperner J et al. Life-long increase of substantia nigra hyperechogenicity in transcranial sonography. Neuroimage 2010; 51: 28-32
• 19 Behnke S, Double KL, Duma S et al. Substantia nigra echomorphology in the healthy very old: Correlation with motor slowing. Neuroimage 2007; 34: 1054-1059
• 20 Mijajlović M, Dragasević N, Stefanova E et al. Transcranial sonography in spinocerebellar ataxia type 2. J Neurol 2008; 255: 1164-1167
• 21 Stockner H, Sojer M, Seppi K et al. Midbrain sonography in patients with essential tremor. Mov Disord 2007; 22: 414-417
• 22 Fedotova EIu, Chechetkin AO, Shadrina MI et al. Transcranial sonography in Parkinson's disease. Zh Nevrol Psikhiatr Im S S Korsakova 2011; 111: 49-55
• 23 Kim JY, Kim ST, Jeon SH et al. Midbrain transcranial sonography in Korean patients with Parkinson's disease. Mov Disord 2007; 22: 1922-1926
• 24 Glaser M, Weber U, Hinrichs H et al. Transkranielle Sonographie des Mittelhirns mit verschiedenen Ultraschallsystemen. Klin Neurophysiol 2006; 37:  165-168
• 25 Vivo-Orti MN, Tembl JI, Sastre-Bataller I et al. Evaluación de la sustancia negra mediante ultrasonografía transcraneal. Rev Neurol 2013; 56: 268-274
• 26 Becker G, Becker T, Struck M et al. Reduced echogenicity of brainstem raphe specific to unipolar depression: a transcranial color-coded real-time sonography study. Biol Psychiatry 1995; 38: 180-184
• 27 Berg D, Behnke S, Seppi K et al. Enlarged hyperechogenic substantia nigra as a risk marker for Parkinson's disease. Mov Disord 2013; 28: 216-219
• 28 Walter U. Substantia nigra hyperechogenicity is a risk marker of Parkinson's disease: no. J Neural Transm 2011; 118: 607-612
• 29 Doepp F, Plotkin M, Siegel L et al. Brain parenchyma sonography and 123I-FP-CIT SPECT in Parkinson's disease and essential tremor. Mov Disord 2008; 23: 405-410
• 30 Behnke S, Berg D, Naumann M et al. Differentiation of Parkinson's disease and atypical parkinsonian syndromes by transcranial ultrasound. J Neurol Neurosurg Psychiatry 2005; 76: 423-425
• 31 Walter U, Dressler D, Probst T et al. Transcranial brain sonography findings in discriminating between parkinsonism and idiopathic Parkinson disease. Arch Neurol 2007; 64: 1635-1640
• 32 Busse K, Heilmann R, Kleinschmidt S et al. Value of combined midbrain sonography, olfactory and motor function assessment in the differential diagnosis of early Parkinson's disease. J Neurol Neurosurg Psychiatry 2012; 83: 441-447
• 33 Berardelli A, Wenning GK, Antonini A et al. EFNS/MDS-ES recommendations for the diagnosis of Parkinson's disease. Eur J Neurol 2013; 20: 16-34
• 34 Schmidauer C, Sojer M, Seppi K et al. Transcranial ultrasound shows nigral hypoechogenicity in restless legs syndrome. Ann Neurol 2005; 58: 630-634
• 35 Godau J, Schweitzer KJ, Liepelt I et al. Substantia nigra hypoechogenicity: definition and findings in restless legs syndrome. Mov Disord 2007; 22: 187-192
• 36 Walter U, Hoeppner J, Prudente-Morrissey L et al. Parkinson's disease-like midbrain sonography abnormalities are frequent in depressive disorders. Brain 2007; 130: 1799-1807
• 37 Berg D, Supprian T, Hofmann E et al. Depression in Parkinson's disease: brainstem midline alteration on transcranial sonography and magnetic resonance imaging. J Neurol 1999; 246: 1186-1193
• 38 Krogias C, Strassburger K, Eyding J et al. Depression in patients with Huntington disease correlates with alterations of the brain stem raphe depicted by transcranial sonography. J Psychiatry Neurosci 2011; 36: 187-194
• 39 Postert T, Eyding J, Berg D et al. Transcranial sonography in spinocerebellar ataxia type 3. J Neural Transm Suppl 2004; 68: 123-133
• 40 Synofzik M, Godau J, Lindig T et al. Transcranial sonography reveals cerebellar, nigral, and forebrain abnormalities in Friedreich's ataxia. Neurodegener Dis 2011; 8: 470-475
• 41 Naumann M, Becker G, Toyka KV et al. Lenticular nucleus lesion in idiopathic dystonia detected by transcranial sonography. Neurology 1996; 47: 1284-1290
• 42 Walter U, Blitzer A, Benecke R et al. Sonographic detection of basal ganglia abnormalities in spasmodic dysphonia. Eur J Neurol 2014; 21: 349-352
• 43 Wollenweber FA, Schomburg R, Probst M et al. Width of the third ventricle assessed by transcranial sonography can monitor brain atrophy in a time- and cost-effective manner – results from a longitudinal study on 500 subjects. Psychiatry Res 2011; 191: 212-216
• 44 Hagenah J, König IR, Kötter C et al. Basal ganglia hyperechogenicity does not distinguish between patients with primary dystonia and healthy individuals. J Neurol 2011; 258: 590-595
• 45 Brüggemann N, Schneider SA, Sander T et al. Distinct basal ganglia hyperechogenicity in idiopathic basal ganglia calcification. Mov Disord 2010; 25: 2661-2664
• 46 Blahuta J, Soukup T, Čermák P. The image recognition of brain-stem ultrasound images with neural network based on PCA. In: Savino M, Andria G, (eds.) 2011 IEEE International Symposium on Medical Measurements and Applications (MeMeA 2011) Proceedings. Bari: IEEE; 2011: 134-142
• 47 Sakalauskas A, Lukoševičius A, Laučkaitė K et al. Automated segmentation of transcranial sonographic images in the diagnostics of Parkinson's disease. Ultrasonics 2013; 53: 111-121
• 48 Pauly O, Ahmadi SA, Plate A et al. Detection of substantia nigra echogenicities in 3D transcranial ultrasound for early diagnosis of Parkinson disease. Med Image Comput Comput Assist Interv 2012; 15: 443-450
• 49 Skoloudik D, Herzig R, Blahuta J et al. Comparison of automatic and manual transcranial sonographic morphometric measurement of the substantia nigra. Neurology 2013; 80 (Meeting Abstracts 1): S39.006
• 50 Forzoni L, D'Onofrio S, De Beni S et al. Virtual Navigator Registration Procedure for Transcranial Application. In: Hellmich C, Hamza MH, Simsik D, (eds.) Proceedings of the IASTED International Conference Biomedical Engineering (BioMed 2012). February 15-17, 2012 Innsbruck Austria Calgary: ACTA Press; 2012: 496-503
• 51 Berg D, Behnke S, Walter U. Application of transcranial sonography in extrapyramidal disorders: updated recommendations. Ultraschall in Med 2006; 27: 12-19