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Pisa syndrome in Parkinson’s disease: an electrophysiological and imaging study

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Abstract

The pathophysiology of postural abnormalities in patients with Parkinson’s disease is poorly understood. In the present study, 13 patients with Pisa syndrome (PS) underwent EMG study of paraspinal lumbar (L2–L4) and thoracic (T8–T10) muscles, and of non-paraspinal muscles. Patients also underwent a whole spine X-ray and an MRI assessment of paraspinal muscles (L1–S1). The EMG evaluation disclosed two main patterns: patients with pattern I (n = 6, hyperactivity of lumbar paraspinals ipsilateral to the trunk leaning side) or pattern II (n = 7: hyperactivity of lumbar paraspinals contralateral to the trunk leaning side. In pattern I, half the patients also had ipsilateral hyperactivity of the thoracic paraspinals, the other half had contralateral thoracic hyperactivity; in pattern II, thoracic paraspinal hyperactivity was contralateral in all patients (like the lumbar paraspinal hyperactivity). Non-paraspinal muscles were hyperactive ipsilaterally in four of six patients with pattern I and in all patients with pattern II. The MRI showed mild muscular atrophy with fatty degeneration in patients with pattern I, whereas in pattern II patients this was greater and prevalent on paraspinal lumbar muscles ipsilateral to the leaning side. The present data support the hypothesis that two main patterns of muscular activation are associated with PS. In both patterns, hyperactivity of contralateral paraspinal muscles is probably compensatory for the trunk leaning.

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References

  1. Doherty KM, van de Warrenburg BP, Peralta MC, Silveira-Moriyama L, Azulay JP, Gershanik OS, Bloem BR (2011) Postural deformities in Parkinson’s disease. Lancet Neurol 10(6):538–549. doi:10.1016/S1474-4422(11)70067-9

    Article  PubMed  Google Scholar 

  2. Yokochi F (2006) Lateral flexion in Parkinson’s disease and Pisa syndrome. J Neurol 253(Suppl 7):17–20. doi:10.1007/s00415-006-7005-4

    Google Scholar 

  3. Di Matteo A, Fasano A, Squintani G, Ricciardi L, Bovi T, Fiaschi A, Barone P, Tinazzi M (2011) Lateral trunk flexion in Parkinson’s disease: EMG features disclose two different underlying pathophysiological mechanisms. J Neurol 258(5):740–745. doi:10.1007/s00415-010-5822-y

    Article  PubMed  Google Scholar 

  4. Ekbom K, Lindholm H, Ljungberg L (1972) New dystonic syndrome associated with butyrophenone therapy. Z Neurol 202(2):94–103

    Article  PubMed  CAS  Google Scholar 

  5. Colosimo C (1998) Pisa syndrome in a patient with multiple system atrophy. Mov Disord 13(3):607–609. doi:10.1002/mds.870130342

    Article  PubMed  CAS  Google Scholar 

  6. Cannas A, Solla P, Floris G, Borghero G, Tacconi P, Spissu A (2005) Reversible Pisa syndrome in Parkinson’s disease during treatment with pergolide: a case report. Clin Neuropharmacol 28(5):252 00002826-200509000-00012 [pii]

    Article  PubMed  Google Scholar 

  7. Gambarin M, Antonini A, Moretto G, Bovi P, Romito S, Fiaschi A, Tinazzi M (2006) Pisa syndrome without neuroleptic exposure in a patient with Parkinson’s disease: case report. Mov Disord 21(2):270–273. doi:10.1002/mds.20711

    Article  PubMed  Google Scholar 

  8. Harada K (2006) Pisa syndrome without neuroleptic exposure in a patient with Parkinson’s disease: a case report. Mov Disord 21(12):2264. doi:10.1002/mds.21168 author reply 2264–2265

    Article  PubMed  Google Scholar 

  9. Solla P, Cannas A, Congia S, Floris G, Aste R, Tacconi P, Marrosu MG (2008) Levodopa/carbidopa/entacapone-induced acute Pisa syndrome in a Parkinson’s disease patient. J Neurol Sci 275(1–2):154–156. doi:10.1016/j.jns.2008.07.017

    Article  PubMed  CAS  Google Scholar 

  10. Cannas A, Solla P, Floris G, Tacconi P, Serra A, Piga M, Marrosu F, Marrosu MG (2009) Reversible Pisa syndrome in patients with Parkinson’s disease on dopaminergic therapy. J Neurol 256(3):390–395. doi:10.1007/s00415-009-0072-6

    Article  PubMed  Google Scholar 

  11. Bonanni L, Thomas A, Varanese S, Scorrano V, Onofrj M (2007) Botulinum toxin treatment of lateral axial dystonia in Parkinsonism. Mov Disord 22(14):2097–2103. doi:10.1002/mds.21694

    Article  PubMed  Google Scholar 

  12. Tassorelli C, Furnari A, Buscone S, Alfonsi E, Pacchetti C, Zangaglia R, Pichiecchio A, Bastianello S, Lozza A, Allena M, Bolla M, Sandrini G, Nappi G, Martignoni E (2012) Pisa syndrome in Parkinson’s disease: clinical, electromyographic, and radiological characterization. Mov Disord 27(2):227–235. doi:10.1002/mds.23930

    Article  PubMed  Google Scholar 

  13. Susan Standring (2008) Gray’s Anatomy. 40th edn. Elsevier, Amsterdam

  14. Netter F (2000) Atlas der Anatomie des Menschen. 2nd edn. Novartis Thieme, Verlag

  15. Gelb DJ, Oliver E, Gilman S (1999) Diagnostic criteria for Parkinson disease. Arch Neurol 56(1):33–39

    Article  PubMed  CAS  Google Scholar 

  16. Mercuri E, Counsell S, Allsop J, Jungbluth H, Kinali M, Bonne G, Schwartz K, Bydder G, Dubowitz V, Muntoni F (2002) Selective muscle involvement on magnetic resonance imaging in autosomal dominant Emery–Dreifuss muscular dystrophy. Neuropediatrics 33(1):10–14. doi:10.1055/s-2002-23593

    Article  PubMed  CAS  Google Scholar 

  17. Fasano A, Di Matteo A, Vitale C, Squintani G, Ferigo L, Bombieri F, Santangelo G, Amboni M, Barone P, Tinazzi M (2011) Reversible Pisa syndrome in patients with Parkinson’s disease on rasagiline therapy. Mov Disord 26(14):2578–2580. doi:10.1002/mds.23918

    Article  PubMed  Google Scholar 

  18. Floyd WF, Silver PH (1955) The function of the erectores spinae muscles in certain movements and postures in man. J Physiol 129(1):184–203

    PubMed  CAS  Google Scholar 

  19. Quirk JA, Sheean GL, Marsden CD, Lees AJ (1996) Treatment of nonoccupational limb and trunk dystonia with botulinum toxin. Mov Disord 11(4):377–383. doi:10.1002/mds.870110405

    Article  PubMed  CAS  Google Scholar 

  20. Comella CL, Shannon KM, Jaglin J (1998) Extensor truncal dystonia: successful treatment with botulinum toxin injections. Mov Disord 13(3):552–555. doi:10.1002/mds.870130330

    Article  PubMed  CAS  Google Scholar 

  21. Wunderlich S, Csoti I, Reiners K, Gunthner-Lengsfeld T, Schneider C, Becker G, Naumann M (2002) Camptocormia in Parkinson’s disease mimicked by focal myositis of the paraspinal muscles. Mov Disord 17(3):598–600. doi:10.1002/mds.10110

    Article  PubMed  Google Scholar 

  22. Gomez-Puerta JA, Peris P, Grau JM, Martinez MA, Guanabens N (2007) Camptocormia as a clinical manifestation of mitochondrial myopathy. Clin Rheumatol 26(6):1017–1019. doi:10.1007/s10067-006-0259-5

    Article  PubMed  Google Scholar 

  23. Ozer F, Ozturk O, Meral H, Serdaroglu P, Yayla V (2007) Camptocormia in a patient with Parkinson disease and a myopathy with nemaline rods. Am J Phys Med Rehabil 86(1):3–6

    Article  PubMed  Google Scholar 

  24. Margraf NG, Wrede A, Rohr A, Schulz-Schaeffer WJ, Raethjen J, Eymess A, Volkmann J, Mehdorn MH, Jansen O, Deuschl G (2010) Camptocormia in idiopathic Parkinson’s disease: a focal myopathy of the paravertebral muscles. Mov Disord 25(5):542–551. doi:10.1002/mds.22780

    Article  PubMed  Google Scholar 

  25. Spuler S, Krug H, Klein C, Medialdea IC, Jakob W, Ebersbach G, Gruber D, Hoffmann KT, Trottenberg T, Kupsch A (2010) Myopathy causing camptocormia in idiopathic Parkinson’s disease: a multidisciplinary approach. Mov Disord 25(5):552–559. doi:10.1002/mds.22913

    Article  PubMed  Google Scholar 

  26. Wrede A, Margraf NG, Goebel HH, Deuschl G, Schulz-Schaeffer WJ (2012) Myofibrillar disorganization characterizes myopathy of camptocormia in Parkinson’s disease. Acta Neuropathol 123(3):419–432. doi:10.1007/s00401-011-0927-7

    Article  PubMed  CAS  Google Scholar 

  27. Ng JK, Richardson CA (1996) Reliability of electromyographic power spectral analysis of back muscle endurance in healthy subjects. Arch Phys Med Rehabil 77(3):259–264 S0003-9993(96)90108-2 [pii]

    Article  PubMed  CAS  Google Scholar 

  28. Danneels LA, Cagnie BJ, Cools AM, Vanderstraeten GG, Cambier DC, Witvrouw EE, De Cuyper HJ (2001) Intra-operator and inter-operator reliability of surface electromyography in the clinical evaluation of back muscles. Man Ther 6(3):145–153. doi:10.1054/math.2001.0396

    Article  PubMed  CAS  Google Scholar 

  29. Schwerthoffer D, Fatke B, Bauml J, Forstl H (2012) Senile anorexia: three cases with complicated treatment and two occurrences of a Pisa syndrome. Int J Geriatr Psychiatry 27(7):765–768. doi:10.1002/gps.2778

    Article  PubMed  Google Scholar 

  30. Vitale C, Marcelli V, Furia T, Santangelo G, Cozzolino A, Longo K, Allocca R, Amboni M, Marciano E, Barone P (2011) Vestibular impairment and adaptive postural imbalance in parkinsonian patients with lateral trunk flexion. Mov Disord 26(8):1458–1463. doi:10.1002/mds.23657

    Article  PubMed  Google Scholar 

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Conflicts of interest

The authors declare that they have no conflict of interest.

Ethical standard

This study has been approved by the appropriate ethics committee and has therefore been performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki.

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Authors and Affiliations

  1. Dipartimento di Scienze Neurologiche, Psicologiche, Morfologiche e Motorie, Università di Verona, Verona, Italy

    Michele Tinazzi, Ina Juergenson, Giovanna Squintani, Gaetano Vattemi & Tommaso Bovi

  2. Istituto di Radiologia, Azienda Ospedaliera-Universitaria Integrata di Verona, Verona, Italy

    Stefania Montemezzi & Daniela Censi

  3. Dipartimento di Neuroscienze, Università di Salerno, Salerno, Italy

    Paolo Barone

  4. Division of Neurology, Movement Disorders Center, TWH, UHN, University of Toronto, 399 Bathurst St, 7 MC412, Toronto, ON, M5T 2S8, Canada

    Alfonso Fasano

Authors
  1. Michele Tinazzi
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  2. Ina Juergenson
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  3. Giovanna Squintani
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  4. Gaetano Vattemi
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  5. Stefania Montemezzi
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  6. Daniela Censi
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  7. Paolo Barone
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  8. Tommaso Bovi
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  9. Alfonso Fasano
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Correspondence to Alfonso Fasano.

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Tinazzi, M., Juergenson, I., Squintani, G. et al. Pisa syndrome in Parkinson’s disease: an electrophysiological and imaging study. J Neurol 260, 2138–2148 (2013). https://doi.org/10.1007/s00415-013-6945-8

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  • DOI: https://doi.org/10.1007/s00415-013-6945-8

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