Abstract
Background
Detailed information about the epidemiological and phenomenological differences among the aetiological subtypes of oromandibular dystonia (OMD) is lacking. Moreover, the OMD tendency to spread to other body sites has never been investigated.
Aim
To compare the main demographic and clinical features of OMD in different aetiological groups and assess the risk of spread.
Materials and methods
We retrospectively analysed data from patients contained in the Italian Dystonia Registry. The risk of spread was assessed by Kaplan Meyer curves and Cox regression analysis.
Results
The study included 273 patients (175 women) aged 55.7 years (SD 12.7) at OMD onset. Female predominance was observed. Idiopathic dystonia was diagnosed in 241 patients, acquired dystonia in 22. In 50/273 patients, dystonia started in the oromandibular region (focal OMD onset); in 96/273 patients the onset involved the oromandibular region and a neighbouring body site (segmental/multifocal OMD onset); and in 127/273 patients OMD was a site of spread from another body region. Sensory trick (ST) and positive family history predominated in the idiopathic group. No dystonia spread was detected in the acquired group, whereas spread mostly occurred within the first five years of history in 34% of the focal OMD onset idiopathic patients. Cox regression analysis revealed ST as a significant predictor of spread (HR, 12.1; 95% CI, 2.5 – 18.8; P = 0.002).
Conclusion
This large study provides novel information about the clinical phenomenology of idiopathic and acquired OMD. We pointed out a possible role of oestrogens in favouring dystonia development. Moreover, we described for the first time the association between ST and dystonia spread, revealing possible common pathophysiological mechanisms. Our findings may be suggested as a referral point for future pathophysiological and therapeutic studies on OMD.
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Data Availability
The data that support the findings of this study are available on request from the corresponding author, [A.T.]. The data are not publicly available due to restrictions [information that could compromise the privacy of research participants].
References
Marsden CD (1976) The problem of adult-onset idiopathic torsion dystonia and other isolated dyskinesias in adult life (including blepharospasm, oromandibular dystonia, dystonic writer’s cramp, and torticollis, or axial dystonia). Adv Neurol 14:259–276
Marsden CD (1976) Blepharospasm-oromandibular dystonia syndrome (Brueghel’s syndrome). A variant of adult-onset torsion dystonia? J Neurol Neurosurg Psychiatry 39(12):1204–92
Termsarasab P, Tanenbaum DR, Frucht SJ (2014) The phenomenology and natural history of idiopathic lower cranial dystonia. J Clin Mov Disord 1:3
Yoshida K (2020) Development and validation of a disease-specific oromandibular dystonia rating scale (OMDRS). Front Neurol 11:583177
Albanese A, Bhatia K, Bressman SB et al (2013) Phenomenology and classification of dystonia: a consensus update. Mov Disord 28:863–873
Manzo N, Ginatempo F, Belvisi D, Defazio G, Conte A, Deriu F, Berardelli A (2022) Pathophysiological mechanisms of oromandibular dystonia. Clin Neurophysiol 134:73–80
Scorr LM, Cho HJ, Kilic-Berkmen G, McKay JL et al (2022) Clinical features and evolution of blepharospasm: A multicenter international cohort and systematic literature review. Dystonia 1:10359
Ray S, Kutty B, Pal PK, Yadav R (2021) Sleep and other non-motor symptoms in patients with idiopathic oromandibular dystonia and meige syndrome: A questionnaire-based study. Ann Indian Acad Neurol 24(3):351–355
Balal M, Demirkiran M (2023) Oromandibular Dystonia: Clinical and Demographic Data from Eight-Two Patients. Tremor Other Hyperkinet Mov (N Y) 30(13):3
Tan EK, Jankovic J (1999) Botulinum toxin A in patients with oromandibular dystonia: long-term follow-up. Neurology 53:2102–2107
Yoshida K (2021) Prevalence and incidence of oromandibular dystonia: an oral and maxillofacial surgery service-based study. Clin Oral Investig 25(10):5755–5764
Slaim L, Cohen M, Klap P, Vidailhet M, Perrin A, Brasnu D et al (2018) Oromandibular dystonia: demographics and clinical data from 240 patients. J Mov Disord 11:78–81
Defazio G, Esposito M, Abbruzzese G et al (2017) The Italian Dystonia Registry: rationale, design, and preliminary findings. Neurol Sci 38:819–825
Saraf U, Chandarana M, Divya KP, Krishnan S (2022) Oromandibular dystonia - a systematic review. Ann Indian Acad Neurol 25(1):26–34. https://doi.org/10.4103/aian.aian_242_21
Khooshnoodi MA, Factor SA, Jinnah HA (2013) Secondary blepharospasm associated with structural lesions of the brain. J Neurol Sci 331(1–2):98–101. https://doi.org/10.1016/j.jns.2013.05.022
Liuzzi D, Gigante AF, Leo A, Defazio G (2016) The anatomical basis of upper limb dystonia: lesson from secondary cases. Neurol Sci 37(9):1393–1398
Dressler D, Altenmüller E, Giess R, Krauss JK, Adib SF (2022) The epidemiology of dystonia:the Hannover epidemiology study. J Neurol 269:6483–6493
Jinnah HA, Berardelli A, Comella C, Defazio G, Delong MR, Factor S, Galpern WR, Hallett M, Ludlow CL, Perlmutter JS, Rosen AR, Dystonia Coalition Investigators (2013) The focal dystonias: current views and challenges for future research. Mov Disord 28(7):926–43. https://doi.org/10.1002/mds.25567
Sciamanna G, El Atiallah I, Montanari M et al (2022) Plasticity, genetics and epigenetics in dystonia: an update. Handb Clin Neurol 184:199–206
Reizel Y, Spiro A, Sabag O, Skversky Y, Hecht M, Keshet I, Berman BP, Cedar H (2015) Gender-specific postnatal demethylation and establishment of epigenetic memory. Genes Dev 29(9):923–933. https://doi.org/10.1101/gad.259309.115
Klein C, Lohmann K, Marras C et al (2017) Hereditary dystonia overview. In: Adam MP, Feldman J, Mirzaa GM et al (eds) GeneReviews® [Internet]. University of Washington, Seattle, Seattle (WA), pp 1993–2024. Available from: https://www.ncbi.nlm.nih.gov/books/NBK1155/
Martino D (2023) What can Epidemiological studies teach on the pathophysiology of adultonset isolated dystonia. Int Rev Neurobiol 169:21–60
Velucci V, Idrissi S, Pellicciari R, Esposito M, Trinchillo A, Belvisi D, Fabbrini G, Ferrazzano G, Terranova C, Girlanda P, Majorana G, Rizzo V, Bono F, Idone G, Laterza V, Avanzino L, Di Biasio F, Marchese R, Castagna A, Ramella M, Lettieri C, Rinaldo S, Altavista MC, Polidori L, Bertolasi L, Tozzi MC, Erro R, Barone P, Barbero P, Ceravolo R, Mascia MM, Ercoli T, Muroni A, Artusi CA, Zibetti M, Scaglione CLM, Bentivoglio AR, Cotelli MS, Magistrelli L, Cossu G, Albanese A, Squintani GM, Schirinzi T, Gigante AF, Maderna L, Eleopra R, Pisani A, Cassano D, Romano M, Rizzo M, Berardelli A, Defazio G (2024) Italian Dystonia registry participants. Does sex influence the natural history of idiopathic adult-onset dystonia? J Neurol Neurosurg Psychiatry. https://doi.org/10.1136/jnnp-2023-332927
Latorre A, Cocco A, Bhatia KP, Erro R, Antelmi E, Conte A, Rothwell JC, Rocchi L (2021) Defective somatosensory inhibition and plasticity are not required to develop dystonia. Mov Disord 36(4):1015–1021. https://doi.org/10.1002/mds.28427
Berman BD, Groth CL, Sillau SH et al (2020) Risk of spread in adult-onset isolated focal dystonia: a prospective international cohort study. J Neurol Neurosurg Psychiatry 91:314–320
Martino D, Berardelli A, Abbruzzese G, Bentivoglio AR, Esposito M, Fabbrini G, Guidubaldi A, Girlanda P, Liguori R, Marinelli L, Morgante F, Santoro L, Defazio G (2012) Age at onset and symptom spread in primary adult-onset blepharospasm and cervical dystonia. Mov Disord 27(11):1447–1450. https://doi.org/10.1002/mds.25088
Esposito M, Fabbrini G, Ferrazzano G et al (2018) Spread of dystonia in patients with idiopathic adult-onset laryngeal dystonia. Eur J Neurol 25(11):1341–1344
Ercoli T, Erro R, Fabbrini G, Pellicciari R, Girlanda P, Terranova C, Avanzino L, Di Biasio F, Barone P, Esposito M, De Joanna G, Eleopra R, Bono F, Manzo L, Bentivoglio AR, Petracca M, Mascia MM, Albanese A, Castagna A, Ceravolo R, Altavista MC, Scaglione C, Magistrelli L, Zibetti M, Bertolasi L, Coletti Moja M, Cotelli MS, Cossu G, Minafra B, Pisani A, Misceo S, Modugno N, Romano M, Cassano D, Berardelli A, Defazio G (2021) Italian dystonia registry participants. Spread of segmental/multifocal idiopathic adult-onset dystonia to a third body site. Parkinsonism Relat Disord 87:70–74. https://doi.org/10.1016/j.parkreldis.2021.04.022
Sarasso E, Agosta F, Piramide N, Bianchi F, Butera C, Gatti R, Amadio S, Del Carro U, Filippi M (2020) Sensory trick phenomenon in cervical dystonia: a functional MRI study. J Neurol 267(4):1103–1115. https://doi.org/10.1007/s00415-019-09683-5
Amadio S, Houdayer E, Bianchi F et al (2014) Sensory tricks and brain excitability in cervical dystonia: a transcranial magnetic stimulation study. Mov Disord 29:1185–1188
Manzo N, Leodori G, Ruocco G et al (2023) Cortical mechanisms of sensory trick in cervical dystonia. Neuroimage Clin 37:103348
Abbruzzese G, Berardelli A, Girlanda P et al (2008) Long-term assessment of the risk of spread in primary late-onset focal dystonia. J Neurol Neurosurg Psychiatry 79(4):392–6
Acknowledgements
Italian dystonia Registry Study Group:
Maria Russo, MD (5); Vincenzo Laterza, MD (6); Denise Cerne, MD (16); Michela Fanzecco, PhD (13); Francesca Valentino, MD (14,15); Roberto Eleopra, MD, PhD (17,18); Roberto Ceravolo, MD (19); Maria Sofia Cotelli, MD (20), Salvatore Misceo, MD (21); Anna Castagna MD, PhD (22); Marta Bianchi, MD (23); Giovanni Cossu, MD, PhD (24); Nicola Modugno, MD, PhD (25); Luca Magistrelli, MD, PhD (26); Simone Simoni, MD (27); Maurizio Zibetti, MD, PhD (28,29), Giovanna Squintani, MD (30); Laura Bertolasi, MD, PhD (31).
17—IRCCS Institute of Neurology “Carlo Besta” Foundation, Milan, Italy.
18 – Clinical Neurology Unit – Parkinson’s disease and Movement disorders center, Milan, Italy.
19 – Clinical Unit of Neurology – Parkinson’s disease center, University Hospital of Pisa, Italy.
20—Neurology Unit Asst. Valcamonica, Esine, Brescia, Italy.
21 – Clinical Neurophysiology Unit, “S. Paolo Hospital”, Bari, Italy.
22—IRCCS Don Carlo Gnocchi Foundation, ONLUS, Milan, Italy.
23 – Clinical Unit of Neurology, ASST Val Camonica, Italy.
24—Clinical Unit of Neurology, Hospital “Brotzu”—Parkinson’s disease center, Italy.
25—IRCCS Neuromed, Pozzilli (IS).
26—Department of Translational Medicine, Section of Neurology, University of Piemonte Orientale and "Maggiore della Carità" University Hospital, Novara,
27 – Clinical Unit of Neurology, University Hospital “S. Maria della Misericordia”, Perugia, Italy.
28—Department of Neuroscience “Rita Levi Montalcini”, University of Torino, Via Cherasco 15, 10126 Torino, Italy.
29—Neurology 2 Unit, AOU Città della Salute e della Scienza, Corso Bramante 88, 10126 Torino, Italy.
30 – Department of Neuroscience, Biomedicine and Movement, University of Verona, Italy.
31 – Clinical Unit of Neurology, Univeristy Hospital "Ospedale Policlinico Borgo Roma", Verona, Italy.
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AT and ME: conception, design, execution, analysis, writing of the first draft, editing the draft. GD: design, analysis, editing the draft, review and critique. AB: editing the draft, review and critique. All authors contributed to data collection, reviewed and approved the final version of the manuscript.
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M.Z. received speaking honoraria from AbbVie, Bial, and Medtronic.
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Trinchillo, A., Esposito, M., Terranova, C. et al. Oromandibular dystonia: from onset to spread a multicenter italian study. Neurol Sci (2024). https://doi.org/10.1007/s10072-024-07488-7
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DOI: https://doi.org/10.1007/s10072-024-07488-7