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Neurological Sciences

, Volume 39, Issue 11, pp 1887–1894 | Cite as

The predictive power of transcranial sonography in movement disorders: a longitudinal cohort study

  • Daniela Monaco
  • Daniela Berg
  • Astrid Thomas
  • Vincenzo Di Stefano
  • Filomena Barbone
  • Michela Vitale
  • Camilla Ferrante
  • Laura Bonanni
  • Marta Di Nicola
  • Tonia Garzarella
  • Luciano Paolo Marchionno
  • Giovanni Malferrari
  • Rocco Di Mascio
  • Marco Onofrj
  • Raffaella Franciotti
Original Article
  • 81 Downloads

Abstract

Transcranial sonography (TCS) is a noninvasive, easily performed, and commonly available neuroimaging technique useful for the study of brain parenchyma in movement disorders. This tool has been increasingly used in the diagnosis of Parkinson’s disease and atypical parkinsonism. The aim of the study was to evaluate the applicability of this technique as supportive tool in the early diagnosis of movement disorders. We performed TCS on 315 individuals which were diagnosed as healthy controls or affected by idiopathic Parkinson’s disease, monogenetic subtypes of Parkinson’s disease, atypical parkinsonism, and Dementia with Lewy bodies. Five TCS diagnostic patterns were defined on the basis of substantia nigra’s and lenticular nuclei’s echogenicity. TCS evaluations were performed by two blinded neuro-sonographers. Clinical diagnosis on all individuals was performed at baseline and at 4-year follow-up. The concordance rate between TCS patterns and clinical diagnosis and the specificity of TCS pattern to discriminate each group of individuals were compared at baseline and at follow-up. The concordance rate between TCS patterns and clinical diagnosis of all individuals was 84% at baseline and increased at follow-up (91%) significantly (p = 0.01). The specificity of TCS pattern in the comparison between patients diagnosed as affected by idiopathic Parkinson’s disease and atypical parkinsonism showed a significant increase at follow-up (p = 0.03). Our study strongly confirms the role of TCS as a noninvasive and cost-effective tool in early diagnosis of movement disorders.

Keywords

Transcranial sonography Substantia nigra Lenticular nuclei Idiopathic Parkinson’s disease Atypical parkinsonism Dementia with Lewy bodies 

Notes

Compliance with ethical standards

Statement of informed consent

The study was approved by the ethics committee. Written informed consent was obtained from each participant before the inclusion in the study.

References

  1. 1.
    Rizzo G, Copetti M, Arcuti S, Martino D, Fontana A, Logroscino G (2016) Accuracy of clinical diagnosis of Parkinson disease: a systematic review and meta-analysis. Neurology 86(6):566–576CrossRefGoogle Scholar
  2. 2.
    Pilotto A, Yilmaz R, Berg D (2015) Developments in the role of transcranial sonography for the differential diagnosis of parkinsonism. Curr Neurol Neurosci Rep 15(7):43CrossRefGoogle Scholar
  3. 3.
    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 45:182–184CrossRefGoogle Scholar
  4. 4.
    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):448–454CrossRefGoogle Scholar
  5. 5.
    Schweitzer KJ, Brüssel T, Leitner P, Krüger R, Bauer P, Woitalla D, Tomiuk J, Gasser T, Berg D (2007) Transcranial ultrasound in different monogenetic subtypes of Parkinson’s disease. J Neurol 254(5):613–616CrossRefGoogle Scholar
  6. 6.
    Venegas-Francke P (2010) Transcranial sonography in the discrimination of Parkinson’s disease versus vascular parkinsonism. Int Rev Neurobiol 90:147–156CrossRefGoogle Scholar
  7. 7.
    Bouwmans AE, Vlaar AM, Srulijes K, Mess WH, Weber WE (2010) Transcranial sonography for the discrimination of idiopathic Parkinson’s disease from the atypical parkinsonian syndromes. Int Rev Neurobiol 90:121–146CrossRefGoogle Scholar
  8. 8.
    Iranzo A, Lomeña F, Stockner H, Valldeoriola F, Vilaseca I, Salamero M, Molinuevo JL, Serradell M, Duch J, Pavía J, Gallego J, Seppi K, Högl B, Tolosa E, Poewe W, Santamaria J (2010) Sleep Innsbruck Barcelona (SINBAR) pattern. Decreased striatal dopamine transporter uptake and substantia nigra hyperechogenicity as risk markers of synucleinopathy in patients with idiopathic rapid-eye-movement sleep behavior disorder: a prospective study. Lancet Neurol 9(11):1070–1077CrossRefGoogle Scholar
  9. 9.
    Berg D, Seppi K, Behnke S, Liepelt I, Schweitzer K, Stockner H, Wollenweber F, Gaenslen A, Mahlknecht P, Spiegel J, Godau J, Huber H, Srulijes K, Kiechl S, Bentele M, Gasperi A, Schubert T, Hiry T, Probst M, Schneider V, Klenk J, Sawires M, Willeit J, Maetzler W, Fassbender K, Gasser T, Poewe W (2011) Enlarged substantia nigra hyperechogenicity and risk for Parkinson disease: a 37-month 3-center study of 1847 older persons. Arch Neurol 68(7):932–937CrossRefGoogle Scholar
  10. 10.
    Berg D, Merz B, Reiners K, Naumann M, Becker G (2005) Five-year follow-up study of hyperechogenicity of the substantia nigra in Parkinson’s disease. Mov Disord 20(3):383–385CrossRefGoogle Scholar
  11. 11.
    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):181–184CrossRefGoogle Scholar
  12. 12.
    McKeith IG, Dickson DW, Lowe J, Emre M, O’Brien JT, Feldman H et al (2005) Diagnosis and management of dementia with Lewy bodies: third report of the DLB consortium. Neurology 65:1863–1872CrossRefGoogle Scholar
  13. 13.
    Litvan I, Agid Y, Calne D, Campbell G, Dubois B, Duvoisin RC, Goetz CG, Golbe LI, Grafman J, Growdon JH, Hallett M, Jankovic J, Quinn NP, Tolosa E, Zee DS (1996) Clinical research criteria for the diagnosis of progressive supranuclear palsy (Steele-Richardson-Olszewski syndrome): report of the NINDS-SPSP international workshop. Neurology 47(1):1–9CrossRefGoogle Scholar
  14. 14.
    Gilman S, Wenning GK, Low PA, Brooks DJ, Mathias CJ, Trojanowski JQ, Wood NW, Colosimo C, Durr A, Fowler CJ, Kaufmann H, Klockgether T, Lees A, Poewe W, Quinn N, Revesz T, Robertson D, Sandroni P, Seppi K, Vidailhet M (2008) Second consensus statement on the diagnosis of multiple system atrophy. Neurology 71(9):670–676CrossRefGoogle Scholar
  15. 15.
    Mathew R, Bak TH, Hodges JR (2012) Diagnostic criteria for corticobasal syndrome: a comparative study. J Neurol Neurosurg Psychiatry 83(4):405–410CrossRefGoogle Scholar
  16. 16.
    Berg D, Godau J, Walter U (2008) Transcranial sonography in movement disorders. Lancet Neurol 7:1044–1055CrossRefGoogle Scholar
  17. 17.
    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 60:74–77CrossRefGoogle Scholar
  18. 18.
    Walter U, Dressler D, Wolters A, Probst T, Grossmann A, Benecke R (2004) Sonographic discrimination of corticobasal degeneration vs progressive supranuclear palsy. Neurology 63:504–509CrossRefGoogle Scholar
  19. 19.
    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 22:48–54CrossRefGoogle Scholar
  20. 20.
    Bartova P, Skoloudik D, Bar M, Ressner P, Hlustik P, Herzig R, Kanovsky P (2008) Transcranial sonography in movement disorders. Biomed Pap Med FacUnivPalacky Olomouc Czech Repub 152(2):251–258CrossRefGoogle Scholar
  21. 21.
    Gaenslen A, Unmuth B, Godau J, Liepelt I, Di Santo A, Johanna Schweitzer K, Gasser T, Machulla HJ, Reimold M, Marek K, Berg D (2008) The specificity and sensitivity of transcranial ultrasound in the differential diagnosis of Parkinson’s disease: a prospective blinded study. Lancet Neurol 7:417–424CrossRefGoogle Scholar
  22. 22.
    Schrag A, Good CD, Miszkiel K, Morris HR, Mathias CJ, Lees AJ, Quinn NP (2000) Differentiation of atypical parkinsonian syndromes with routine MRI. Neurology 54(3):697–702CrossRefGoogle Scholar
  23. 23.
    Dickson DW, Anderton B, Morris H et al (2001) International medical workshop covering progressive supranuclear palsy, multiple system atrophy and corticobasal degeneration. Mov Disord 16:382–395CrossRefGoogle Scholar
  24. 24.
    Berardelli A, Wenning GK, Antonini A, Berg D, Bloem BR, Bonifati V, Brooks D, Burn DJ, Colosimo C, Fanciulli A, Ferreira J, Gasser T, Grandas F, Kanovsky P, Kostic V, Kulisevsky J, Oertel W, Poewe W, Reese JP, Relja M, Ruzicka E, Schrag A, Seppi K, Taba P, Vidailhet M (2013) EFNS/MDS-ES/ENS [corrected] recommendations for the diagnosis of Parkinson’s disease. New European guidelines for the diagnosis of Parkinson’s disease. TCS evaluation has a level a of evidence in early and differential diagnosis of PD. Eur J Neurol 20:16–34CrossRefGoogle Scholar
  25. 25.
    Li X, Xue S, Jia S, Zhou Z, Qiao Y, Hou C, Wei K, Zheng W, Rong P, Jiao J (2017) Transcranial sonography in idiopathic REM sleep behavior disorder and multiple system atrophy. Psychiatry Clin Neurosci 71(4):238–246CrossRefGoogle Scholar
  26. 26.
    Sanzaro E, Iemolo F (2016) Transcranial sonography in movement disorders: an interesting tool for diagnostic perspectives. Neurol Sci 37(3):373–376CrossRefGoogle Scholar
  27. 27.
    Li DH, He YC, Liu J, Chen SD (2016) Diagnostic accuracy of transcranial sonography of the substantia nigra in Parkinson’s disease: a systematic review and meta-analysis. Sci Rep 6:20863CrossRefGoogle Scholar
  28. 28.
    Berg D, Becker G, Zeiler B, Tucha O, Hofmann E, Preier M, Benz P, Jost W, Reiners K, Lange KW (1999) Vulnerability of the nigrostriatal system as detected by transcranial ultrasound. Neurology 53:1026–1031CrossRefGoogle Scholar
  29. 29.
    Berg D, Roggendorf W, Schroder U et al (2002) Echogenicity of the substantia nigra: association with increased iron content and marker for susceptibility to nigrostriatal injury. Arch Neurol 59:999–1005CrossRefGoogle Scholar
  30. 30.
    Berg D, Behnke S, Seppi K, Godau J, Lerche S, Mahlknecht P, Liepelt-Scarfone I, Pausch C, Schneider N, Gaenslen A, Brockmann K, Srulijes K, Huber H, Wurster I, Stockner H, Kiechl S, Willeit J, Gasperi A, Fassbender K, Gasser T, Poewe W (2013) Enlarged hyperechogenic substantia nigra as a risk marker for Parkinson’s disease. Mov Disord 28(2):216–219CrossRefGoogle Scholar
  31. 31.
    deRijk MC, Tzourio C, Breteler MM et al (1997) Prevalence of parkinsonism and Parkinson’s disease in Europe: the EUROPARKINSON collaborative study. European Community Concerted Action on the Epidemiology of Parkinson’s disease. J Neurol Neurosurg Psychiatry 62:10–15CrossRefGoogle Scholar
  32. 32.
    Zecca L, Swartz HM (1993) Total and paramagnetic metals in human substantia nigra and its neuromelanin. J Neural Transm Park Dis Dement 3:203–213CrossRefGoogle Scholar
  33. 33.
    Berg D, Godau J, Riederer P, Gerlach M, Arzberger T (2010) Microglia activation is related to substantia nigra echogenicity. J Neural Transm 117:1287–1292CrossRefGoogle Scholar
  34. 34.
    Li DH, Zhang LY, Hu YY, Jiang XF, Zhou HY, Yang Q, Kang WY, Liu J, Chen SD (2015) Transcranial sonography of the substantia nigra and its correlation with DAT-SPECT in the diagnosis of Parkinson’s disease. Parkinsonism Relat Disord 21:923–928CrossRefGoogle Scholar
  35. 35.
    Fengler S, Liepelt-Scarfone I, Brockmann K, Schäffer E, Berg D, Kalbe E (2017) Cognitive changes in prodromal Parkinson’s disease: a review. Mov Disord 32(12):1655–1666CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Italia S.r.l., part of Springer Nature 2018

Authors and Affiliations

  • Daniela Monaco
    • 1
  • Daniela Berg
    • 2
  • Astrid Thomas
    • 3
  • Vincenzo Di Stefano
    • 3
  • Filomena Barbone
    • 3
  • Michela Vitale
    • 3
  • Camilla Ferrante
    • 3
  • Laura Bonanni
    • 3
  • Marta Di Nicola
    • 4
  • Tonia Garzarella
    • 5
  • Luciano Paolo Marchionno
    • 6
  • Giovanni Malferrari
    • 7
  • Rocco Di Mascio
    • 8
  • Marco Onofrj
    • 3
  • Raffaella Franciotti
    • 3
  1. 1.Stroke Unit, Department of Urgency and EmergencyS. Spirito HospitalPescaraItaly
  2. 2.Department of NeurologyChristian-Albrechts-University of KielKielGermany
  3. 3.Department of Neuroscience, Imaging and Clinical Sciences“G. d’Annunzio” UniversityChietiItaly
  4. 4.Laboratory of Biostatistics, Department of Medical, Oral and Biotechnological Sciences“G. d’Annunzio” UniversityChietiItaly
  5. 5.Division of Hygiene, Epidemiology and Public Health, Department of Medicine and Science of Aging“G. d’Annunzio” UniversityChietiItaly
  6. 6.Department of NeurologySS Annunziata HospitalChietiItaly
  7. 7.Stroke Unit, Neurology UnitIRCCS Reggio EmiliaItaly
  8. 8.INPSChietiItaly

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