Oromandibular dystonia: from onset to spread a multicenter italian study.

Adult-Onset Dystonia Movement disorders Oromandibular dystonia Sensory Trick Spread of dystonia

Journal

Neurological sciences : official journal of the Italian Neurological Society and of the Italian Society of Clinical Neurophysiology
ISSN: 1590-3478
Titre abrégé: Neurol Sci
Pays: Italy
ID NLM: 100959175

Informations de publication

Date de publication:
27 Mar 2024
Historique:
received: 07 11 2023
accepted: 19 03 2024
medline: 27 3 2024
pubmed: 27 3 2024
entrez: 27 3 2024
Statut: aheadofprint

Résumé

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. To compare the main demographic and clinical features of OMD in different aetiological groups and assess the risk of spread. 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. 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). 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.

Sections du résumé

BACKGROUND 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 OBJECTIVE
To compare the main demographic and clinical features of OMD in different aetiological groups and assess the risk of spread.
MATERIALS AND METHODS 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 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 CONCLUSIONS
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.

Identifiants

pubmed: 38536550
doi: 10.1007/s10072-024-07488-7
pii: 10.1007/s10072-024-07488-7
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2024. Fondazione Società Italiana di Neurologia.

Références

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
pubmed: 941774
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
doi: 10.1136/jnnp.39.12.1204 pubmed: 1011031 pmcid: 492566
Termsarasab P, Tanenbaum DR, Frucht SJ (2014) The phenomenology and natural history of idiopathic lower cranial dystonia. J Clin Mov Disord 1:3
doi: 10.1186/2054-7072-1-3 pubmed: 26788329 pmcid: 4676493
Yoshida K (2020) Development and validation of a disease-specific oromandibular dystonia rating scale (OMDRS). Front Neurol 11:583177
doi: 10.3389/fneur.2020.583177 pubmed: 33224096 pmcid: 7669987
Albanese A, Bhatia K, Bressman SB et al (2013) Phenomenology and classification of dystonia: a consensus update. Mov Disord 28:863–873
doi: 10.1002/mds.25475 pubmed: 23649720 pmcid: 3729880
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
doi: 10.1016/j.clinph.2021.11.075 pubmed: 34979293
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
doi: 10.3389/dyst.2022.10359 pubmed: 36248010 pmcid: 9557246
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
doi: 10.4103/aian.AIAN_906_20 pubmed: 34446996 pmcid: 8370173
Balal M, Demirkiran M (2023) Oromandibular Dystonia: Clinical and Demographic Data from Eight-Two Patients. Tremor Other Hyperkinet Mov (N Y) 30(13):3
doi: 10.5334/tohm.730
Tan EK, Jankovic J (1999) Botulinum toxin A in patients with oromandibular dystonia: long-term follow-up. Neurology 53:2102–2107
doi: 10.1212/WNL.53.9.2102 pubmed: 10599789
Yoshida K (2021) Prevalence and incidence of oromandibular dystonia: an oral and maxillofacial surgery service-based study. Clin Oral Investig 25(10):5755–5764
doi: 10.1007/s00784-021-03878-9 pubmed: 33956216
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
doi: 10.14802/jmd.17065 pubmed: 29860784 pmcid: 5990905
Defazio G, Esposito M, Abbruzzese G et al (2017) The Italian Dystonia Registry: rationale, design, and preliminary findings. Neurol Sci 38:819–825
doi: 10.1007/s10072-017-2839-3 pubmed: 28215037
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
doi: 10.4103/aian.aian_242_21 pubmed: 35342238
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
doi: 10.1016/j.jns.2013.05.022 pubmed: 23747003 pmcid: 3732185
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
doi: 10.1007/s10072-016-2598-6 pubmed: 27173653
Dressler D, Altenmüller E, Giess R, Krauss JK, Adib SF (2022) The epidemiology of dystonia:the Hannover epidemiology study. J Neurol 269:6483–6493
doi: 10.1007/s00415-022-11310-9 pubmed: 35948800 pmcid: 9618521
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
doi: 10.1002/mds.25567 pubmed: 23893450 pmcid: 3733486
Sciamanna G, El Atiallah I, Montanari M et al (2022) Plasticity, genetics and epigenetics in dystonia: an update. Handb Clin Neurol 184:199–206
doi: 10.1016/B978-0-12-819410-2.00011-4 pubmed: 35034734
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
doi: 10.1101/gad.259309.115 pubmed: 25934504 pmcid: 4421981
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
doi: 10.1016/bs.irn.2023.05.015 pubmed: 37482393
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
doi: 10.1002/mds.28427 pubmed: 33332649
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
doi: 10.1136/jnnp-2019-321794 pubmed: 31848221
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
doi: 10.1002/mds.25088 pubmed: 22890501
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
doi: 10.1111/ene.13731 pubmed: 29935029
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
doi: 10.1007/s00415-019-09683-5 pubmed: 31897600
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
doi: 10.1002/mds.25888 pubmed: 24753013
Manzo N, Leodori G, Ruocco G et al (2023) Cortical mechanisms of sensory trick in cervical dystonia. Neuroimage Clin 37:103348
doi: 10.1016/j.nicl.2023.103348 pubmed: 36791488 pmcid: 9950946
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
doi: 10.1136/jnnp.2007.124594 pubmed: 17635969

Auteurs

Assunta Trinchillo (A)

Department of Neurosciences, Reproductive Sciences and Odontostomatology, "Federico II" University, Naples, Italy. assuntatrinchillo94@gmail.com.

Marcello Esposito (M)

Clinical Neurophysiology Unit, Cardarelli Hospital, Naples, Italy.

Carmen Terranova (C)

Department of Clinical and Experimental Medicine, University of Messina, Messina, Italy.

Vincenzo Rizzo (V)

Department of Clinical and Experimental Medicine, University of Messina, Messina, Italy.

Giovanni Fabbrini (G)

Department of Human Neurosciences, Sapienza University of Roma, Rome, Italy.

Gina Ferrazzano (G)

Department of Human Neurosciences, Sapienza University of Roma, Rome, Italy.

Daniele Belvisi (D)

Department of Human Neurosciences, Sapienza University of Roma, Rome, Italy.

Roberto Erro (R)

Department of Medicine, Surgery and Dentistry "Scuola Medica Salernitana" University of Salerno, Baronissi, SA, Italy.

Paolo Barone (P)

Department of Medicine, Surgery and Dentistry "Scuola Medica Salernitana" University of Salerno, Baronissi, SA, Italy.

Francesco Bono (F)

Academic Hospital - A.O.U. "R. Dulbecco", Catanzaro, Italy.

Francesca Di Biasio (F)

IRCCS Ospedale Policlinico San Martino, Genoa, Italy.

Anna Rita Bentivoglio (AR)

Clinical Neurology Unit - Movement Disorders, University of Rome "Università Cattolica del Sacro Cuore", Hospital of Rome "Agostino Gemelli", Rome, Italy.

Christian Lettieri (C)

Clinical Neurology Unit "S. Maria Della Misericordia" University, Hospital of Udine, Udine, Italy.

Maria Concetta Altavista (MC)

Clinical Neurology Unit "San Filippo Neri"; Hospital in Rome, Rome, Italy.

Cesa Lorella Maria Scaglione (CLM)

Clinical Neurology Unit, Bologna, Italy.

Alberto Albanese (A)

Clinical Institute, Department of Neurology, "Humanitas", Milan, Italy.

Marcello Mario Mascia (MM)

Neurology Unit, University Hospital of Cagliari, Cagliari, Italy.

Antonella Muroni (A)

Neurology Unit, University Hospital of Cagliari, Cagliari, Italy.

Antonio Pisani (A)

Department of Brain and Behavioral Sciences, University of Pavia, Pavia, Italy.
IRCCS Mondino Foundation, Pavia, Italy.

Alfredo Berardelli (A)

Department of Human Neurosciences, Sapienza University of Roma, Rome, Italy.

Giovanni Defazio (G)

Department of Translational Biomedicine and Neuroscience, University of Bari, Bari, Italy.

Classifications MeSH