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April 2022; 8 (2) Research ArticleOpen Access

Clinical-Genetic Features Influencing Disability in Spastic Paraplegia Type 4

A Cross-sectional Study by the Italian DAISY Network

Salvatore Rossi, Anna Rubegni, Vittorio Riso, Melissa Barghigiani, Maria Teresa Bassi, Roberta Battini, View ORCID ProfileEnrico Bertini, View ORCID ProfileCristina Cereda, View ORCID ProfileEttore Cioffi, Chiara Criscuolo, Beatrice Dal Fabbro, Clemente Dato, Maria Grazia D'Angelo, Antonio Di Muzio, Luca Diamanti, Maria Teresa Dotti, Alessandro Filla, Valeria Gioiosa, Rocco Liguori, Andrea Martinuzzi, Roberto Massa, Andrea Mignarri, View ORCID ProfileRossana Moroni, Olimpia Musumeci, View ORCID ProfileFrancesco Nicita, Ilaria Orologio, Laura Orsi, Elena Pegoraro, Antonio Petrucci, Massimo Plumari, Ivana Ricca, Giovanni Rizzo, View ORCID ProfileSilvia Romano, Roberto Rumore, Simone Sampaolo, Marina Scarlato, Marco Seri, Cristina Stefan, Giulia Straccia, Alessandra Tessa, Lorena Travaglini, Rosanna Trovato, Lucia Ulgheri, Giovanni Vazza, View ORCID ProfileAntonio Orlacchio, Gabriella Silvestri, Filippo Maria Santorelli, Mariarosa Anna Beatrice Melone, Carlo Casali
First published March 30, 2022, DOI: https://doi.org/10.1212/NXG.0000000000000664
Salvatore Rossi
From the Dipartimento di Neuroscienze Università Cattolica del Sacro Cuore, Facoltà di Medicina e Chirurgia, and Dipartimento di Scienze dell'Invecchiamento, Neurologiche, Ortopediche e della Testa-Collo, UOC Neurologia, Fondazione Policlinico Universitario A. Gemelli IRCCS, Rome (Salvatore Rossi, V.R., Gabriella Silvestri); IRCCS Fondazione Stella Maris (A.R., M.B., R.B., I.R., A.T., R.T., F.M.S.), Calambrone, Pisa; Laboratorio di Biologia Molecolare (M.T.B.), IRCCS E. Medea, Bosisio Parini, Lecco; Dipartimento di Medicina Clinica e Sperimentale (R.B.), Università di Pisa; Unità di Malattie Neuromuscolari e Neurodegenerative (E.B., F.N., L.T.), Laboratorio di Medicina Molecolare, Dipartimento di Neuroscienze, IRCCS Ospedale Pediatrico Bambino Gesù, Rome; Dipartimento della Donna (Cristina Cereda), della Mamma, del Neonato, ASST Fatebenefratelli Sacco, Ospedale dei Bambini “V. Buzzi,” Milano; Dipartimento di Scienze e Biotecnologie medico-chirurgiche (E.C., V.G., Carlo Casali), Sapienza Università di Roma; Dipartimento di Neuroscienze (Chiara Criscuolo, A.F.), Scienze Riproduttive e Odontostomatologiche, Università Federico II, Napoli; Department of Advanced Medical and Surgical Sciences (I.O., S.S., M.A.B.M.), 2nd Division of Neurology, Center for Rare Diseases and InterUniversity Center for Research in Neurosciences, University of Campania “Luigi Vanvitelli,” Naples, Italy; Dipartimento di Scienze del Sistema Nervoso e del Comportamento (B.D.F.), Fondazione Istituto Neurologico C. Mondino IRCCS, Pavia; U.O. Neurologia (C.D.), IRCCS Policlinico San Donato, Milano; Unità Operativa Patologie Neuromuscolari (M.G.D.A.), IRCCS E. Medea, Bosisio Parini, Lecco; Ospedale Clinicizzato “SS Annunziata” (A.D.M.), Università di Chieti; U.O. Neuro-Oncologia (L.D.), IRCCS Mondino Foundation, Pavia; Unit of Neurology and Neurometabolic Disorders (M.T.D., Andrea Mignarri), Department of Medicine, Surgery and Neurosciences, University of Siena, Siena; IRCCS Istituto delle Scienze Neurologiche di Bologna (R.L., G.R.); Dipartimento di Scienze Biomediche e Neuromotorie (R.L.), Università di Bologna; Dipartimento di Neuroriabilitazione, IRCCS Medea, Polo di Conegliano-Pieve di Soligo (Andrea Martinuzzi), Conegliano, Treviso; Unit Malattie Neuromuscolari (Roberto Massa), Policlinico and Università di Roma Tor Vergata; Direzione Scientifica (Rossana Moroni), Fondazione Policlinico A. Gemelli IRCCS, Rome; Dipartimento di Medicina Clinica e Sperimentale (O.M.) Università di Messina; Dipartimento di Neuroscienze e Salute Mentale (L.O.), SC Neurologia 1, A.O.U Città della Salute e della Scienza di Torino; Clinica Neurologica (E.P.), Dipartimento di Neuroscienze, Azienda Ospedale Università Padova; Centro Malattie Neuromuscolari e Neurologiche Rare (A.P.), A.O. San Camillo–Forlanini, Rome; Laboratorio di Genetica Molecolare e Citogenetica (M.P.), Fondazione Istituto Neurologico C. Mondino IRCCS, Pavia; Department of Neurosciences (Silvia Romano), Mental Health and Sensory Organs, Sapienza University of Rome; Laboratorio di Neurogenetica (R.R., A.O.), Centro Europeo di Ricerca Sul Cervello, IRCCS Fondazione Santa Lucia, Rome; Dipartimento di Neurologia (Marina Scarlato), IRCCS Ospedale San Raffaele; Dipartimento di Scienze Mediche e Chirurgiche, Università di Bologna, and IRCCS Azienda Ospedaliero-Universitaria di Bologna (Marco Seri), Servizio di Genetica Medica, Bologna; IRCCS E. Medea, Pieve di Soligo, Treviso; Fondazione IRCCS Istituto Neurologico Carlo Besta (Giulia Straccia), Department of Clinical Neurosciences, Parkinson and Movement Disorders Unit, Milan, Italy; Dipartimento Salute Donna e Bambino (L.U.), S.S.D. di Genetica Clinica e Biologia dello Sviluppo, Azienda ospedaliero-universitaria di Sassari; Dipartimento di Biologia (G.V.), Università degli Studi di Padova; Dipartimento di Medicina e Chirurgia (A.O.), Università di Perugia; Dipartimento di Scienze dell'Invecchiamento (Gabriella Silvestri), Neurologiche, Ortopediche e della Testa-Collo, UOC Neurologia, Fondazione Policlinico Universitario A. Gemelli IRCCS, Rome; and Sbarro Institute for Cancer Research and Molecular Medicine (M.A.B.M.), Center for Biotechnology, Temple University, Philadelphia, PA.
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Anna Rubegni
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Citation
Clinical-Genetic Features Influencing Disability in Spastic Paraplegia Type 4
A Cross-sectional Study by the Italian DAISY Network
Salvatore Rossi, Anna Rubegni, Vittorio Riso, Melissa Barghigiani, Maria Teresa Bassi, Roberta Battini, Enrico Bertini, Cristina Cereda, Ettore Cioffi, Chiara Criscuolo, Beatrice Dal Fabbro, Clemente Dato, Maria Grazia D'Angelo, Antonio Di Muzio, Luca Diamanti, Maria Teresa Dotti, Alessandro Filla, Valeria Gioiosa, Rocco Liguori, Andrea Martinuzzi, Roberto Massa, Andrea Mignarri, Rossana Moroni, Olimpia Musumeci, Francesco Nicita, Ilaria Orologio, Laura Orsi, Elena Pegoraro, Antonio Petrucci, Massimo Plumari, Ivana Ricca, Giovanni Rizzo, Silvia Romano, Roberto Rumore, Simone Sampaolo, Marina Scarlato, Marco Seri, Cristina Stefan, Giulia Straccia, Alessandra Tessa, Lorena Travaglini, Rosanna Trovato, Lucia Ulgheri, Giovanni Vazza, Antonio Orlacchio, Gabriella Silvestri, Filippo Maria Santorelli, Mariarosa Anna Beatrice Melone, Carlo Casali
Neurol Genet Apr 2022, 8 (2) e664; DOI: 10.1212/NXG.0000000000000664

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Abstract

Background and Objectives Hereditary spastic paraplegias (HSPs) are a group of inherited rare neurologic disorders characterized by length-dependent degeneration of the corticospinal tracts and dorsal columns, whose prominent clinical feature is represented by spastic gait. Spastic paraplegia type 4 (SPG4, SPAST-HSP) is the most common form. We present both clinical and molecular findings of a large cohort of patients, with the aim of (1) defining the clinical spectrum of SPAST-HSP in Italy; (2) describing their molecular features; and (3) assessing genotype-phenotype correlations to identify features associated with worse disability.

Methods A cross-sectional retrospective study with molecular and clinical data collected in an anonymized database was performed.

Results A total of 723 Italian patients with SPAST-HSP (58% men) from 316 families, with a median age at onset of 35 years, were included. Penetrance was 97.8%, with men showing higher Spastic Paraplegia Rating Scale (SPRS) scores (19.67 ± 12.58 vs 16.15 ± 12.61, p = 0.009). In 26.6% of patients with SPAST-HSP, we observed a complicated phenotype, mainly including intellectual disability (8%), polyneuropathy (6.7%), and cognitive decline (6.5%). Late-onset cases seemed to progress more rapidly, and patients with a longer disease course displayed a more severe neurologic disability, with higher SPATAX (3.61 ± 1.46 vs 2.71 ± 1.20, p < 0.001) and SPRS scores (22.63 ± 11.81 vs 12.40 ± 8.83, p < 0.001). Overall, 186 different variants in the SPAST gene were recorded, of which 48 were novel. Patients with SPAST-HSP harboring missense variants displayed intellectual disability (14.5% vs 4.4%, p < 0.001) more frequently, whereas patients with truncating variants presented more commonly cognitive decline (9.7% vs 2.6%, p = 0.001), cerebral atrophy (11.2% vs 3.4%, p = 0.003), lower limb spasticity (61.5% vs 44.5%), urinary symptoms (50.0% vs 31.3%, p < 0.001), and sensorimotor polyneuropathy (11.1% vs 1.1%, p < 0.001). Increasing disease duration (DD) and abnormal motor evoked potentials (MEPs) were also associated with increased likelihood of worse disability (SPATAX score>3).

Discussion The SPAST-HSP phenotypic spectrum in Italian patients confirms a predominantly pure form of HSP with mild-to-moderate disability in 75% of cases, and slight prevalence of men, who appeared more severely affected. Early-onset cases with intellectual disability were more frequent among patients carrying missense SPAST variants, whereas patients with truncating variants showed a more complicated disease. Both longer DD and altered MEPs are associated with worse disability.

Glossary

AAA=
ATPases Associated with diverse cellular Activities;
AAE=
age at the last available examination;
AAO=
age at onset;
AD=
autosomal dominant;
DD=
disease duration;
HSP=
hereditary spastic paraplegia;
MEP=
motor evoked potential;
SPG=
spastic paraplegia gene;
SPG4=
SPG type 4;
SPRS=
Spastic Paraplegia Rating Scale;
SSEP=
somatosensory evoked potential;
TCC=
thin corpus callosum;
UL=
upper limb

Footnotes

  • Go to Neurology.org/NG for full disclosures. Full information is provided at the end of the article.

  • ↵* These authors contributed equally to this work.

  • The Article Processing Charge was funded by the Fondazione Policlinico A. Gemelli IRCCS.

  • Received October 13, 2021.
  • Accepted in final form January 31, 2022.
  • Copyright © 2022 The Author(s). Published by Wolters Kluwer Health, Inc. on behalf of the American Academy of Neurology.

This is an open access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND), which permits downloading and sharing the work provided it is properly cited. The work cannot be changed in any way or used commercially without permission from the journal.

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